Professional Documents
Culture Documents
mtWi
Identification
of Pathological Conditions
in H u m a n Skeletal Remains
^
s
DONALD J. ORTNER
and
WALTER G. J. PUTSC:
'<Jf'\
SMITHSONIAN CONTlfeUTIONS TO ANTHROPOLOGY "^^
s
T ^^^
SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION
S. Dillon Ripley
Secretary
Smithsonian Institution
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY NUMBER 28
Identification
of Pathological Conditions
in H u m a n Skeletal Remains
Donald J. Ortner
and Walter G. J. Putschar
Page
Scalping "^
Pathology ^^
Paleopathology "*^
Mutilation 94
Trephination "^
History "^
Paleopathology ""
Types of Trephination "'
Complications of Trephination 97
Traumatic Problems Arising from Pregnancy 100
Pathology 100
Paleopathology 101
Sincipital-T Mutilation 102
INFECTIOUS DISEASES 104
The Inflammatory Response 104
The Biology of Infection 104
Osteomyelitis 105
Pathology 105
Hematogenous Osteomyelitis 109
Changes in Individual Bones 116
Paleopathology 121
The Skull 123
Postcranial Bones 123
Periostitis 129
Pathology 129
Paleopathology 131
Brucellosis 138
Pathology 138
Paleopathology 139
Glanders 141
Pathology 141
Tuberculosis of Bones and Joints 141
Pathology 141
Statistical Data 142
General Pattern of Bone and Joint Tuberculosis 144
The Spine 145
The Pelvis 149
The Hip 150
The Trochanter 153
The Knee 154
The Ankle and Tarsal Bones 154
The Tubular Bones of the Hands and Feet (Spina Ventosa) . . 156
The Shoulder 157
The Elbow 157
The Wrist and Carpal Bones 159
The Shaft of Long Bones 159
NUMBER 28
se
T h e Thoracic Cage l^'^
T h e Skull 162
Paleopathology 1""
Leprosy 1'"
Pathology 1^6
Paleopathology 1''
Treponemal Infections 10
Pathology 180
Yaws 180
Endemic Syphilis (Treponarid) 181
Venereal Syphilis 182
Congenital Syphilis 198
Paleopathology 201
Congenital Syphilis 207
Adult Treponemal Disease 210
Actinomycosis and Nocardiosis 218
Pathology 218
Mycetoma (Maduromycosis) "^"^^
Pathology ^^^
Fungal Infections ^
Pathology 224
North American Blastomycosis 224
994
Cryptococcosis
924
Paracoccidioidomycosis
994
Coccidioidomycosis
Histoplasmosis 995
Sporotrichosis
. 99fi
Aspergillosis
Mucormycosis (Phycomycosis) 227
Paleopathology
Viral Infections
Pathology 227
Smallpox
Rubella 229
Parasitic Infections (Echinococcosis) 229
Pathology 229
Paleopathology ^^
Sarcoidosis
Pathology
CIRCULATORY DISTURBANCES '^^^
Blood Supply of Bones 235
235
Ischemia and Infarction
Pathology ^;^^
Necrosis of Femoral Head 236
Pathology 236
Paleopathology
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
VI
Page
Perthes' Disease and Slipped Femoral Capital Epiphysis 238
Pathology 238
OQQ
Paleopathology "^"^^
Other Vascular Disturbances of Epiphyses and Apophyses 242
Kohler's Disease of the Tarsal Navicular Bone 242
Pathology 242
942
Osteochondritis Dissecans ^^^
Pathology 242
Paleopathology '^ ^
Osffood-Schlatter's Disease of the Tibial Tubercle 243
Pathology ^^^
Paleopathology 243
Freiberg's Disease of a Metatarsal Head 244
Pathology 244
Kienbock's Disease of the Carpal Lunate Bone 244
Pathology 244
Pulmonary Osteoarthropathy 245
Pathology 245
Aneurysmal Erosion 246
Pathology 246
RETICULOENDOTHELIAL AND HEMOPOIETIC DISORDERS 248
Lipid Storage Diseases 248
Pathology 248
Gaucher's Disease 248
Niemann-Pick's Disease 249
Other Lipidoses 249
Histiocytosis X 249
Pathology 249
Anemias 251
Pathology 251
Thalassemia 251
Sickle Cell Anemia and Its Genetic Variants 254
Hereditary Spherocytosis (Congenital Hemolytic Anemia) ... 257
Iron-deficiency Anemia 257
Erythroblastosis Fetalis 258
Paleopathology 258
Leukemia 263
Pathology 263
Myeloma 264
Pathology 264
Paleopathology 265
METABOLIC DISORDERS 270
Vitamin C Deficiency 270
Pathology 270
Infantile Scurvy (Moller-Barlow's Disease) 270
Adult Scurvy 272
NUMBER 28 vii
Page
Paleopathology 272
Vitamin D Deficiency 273
Pathology 273
Rickets 273
Rachitic and Postrachitic Changes in Individual Bones 274
Late Rickets 280
Osteomalacia 280
Skeletal Changes Resembling Rickets and Osteomalacia 283
Paleopathology 283
Hypophosphatasia 287
Pathology 287
Starvation 287
Pathology 287
Fluorosis 288
Pathology 288
Osteoporosis 289
Pathology 289
Paleopathology 291
Localized Hyperostosis 294
Pathology 294
Pregnancy Osteophyte 294
Internal Frontal Hyperostosis 294
Leontiasis Ossea 294
Infantile Cortical Hyperostosis (Caffey's Disease) 294
Generalized Hyperostosis with Pachydermia 294
Pathology 294
Paleopathology 297
ENDOCRINE DISTURBANCES 298
Pituitary Disturbances 298
Pathology 298
Pituitary Gigantism 298
Acromegaly 298
Hypopituitarism 300
Pituitary Dwarfism 300
Paleopathology 300
Acromegaly 300
Pituitary Dwarfism 302
Other Endocrine Disturbances 304
Pathology 304
Hypothyroidism 304
Hyperthyroidism 305
Cushing's Syndrome 305
Hypogonadism 306
Hypergonadism 306
Hypoparathyroidism 306
Hyperparathyroidism 307
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Page
SKELETAL MALFORMATIONS 346
Skull 346
Pathology 346
Paleopathology 346
Spine 355
Pathology 355
Paleopathology 356
Ribs 359
Pathology 359
Pelvis 359
Pathology 359
Paleopathology 360
Extremities 362
Pathology 362
Paleopathology 363
TUMORS 365
General Discussion 365
Pathology 365
Paleopathology 365
Primary Benign Tumors 366
Pathology 366
Cysts 366
Osteoblastic Tumors 368
Chondroblastic Tumors 370
Fibroblastic Tumors 374
Giant Cell Tumor 375
Hemangioma 376
Meningioma 378
Paleopathology 378
Osteoblastic Tumors 378
Chondroblastic Tumors 380
Meningioma 382
Primary Malignant Bone Tumors 384
Pathology 384
Osteosarcoma 384
Chondrosarcoma 385
Ewing's Sarcoma 387
Chordoma 388
Paleopathology 389
Metastatic Tumors 391
Pathology 391
Paleopathology 395
LESIONS OF THE JOINTS 399
Septic Arthritis 399
Pathology 399
Paleopathology 401
SMITHSONIAN CONTRIBUTIONS TO A N T H R O P O L O G Y
Page
Page
Pathology 444
Abnormal Quality of Teeth 444
Abnormal Quantity of Teeth 446
Abnormal Size and Shape of Teeth 447
Dental Anomalies 447
Dental Crowding 447
Paleopathology 447
Abnormal Quality of Teeth 447
Abnormal Quantity of Teeth 448
Abnormal Size and Shape of Teeth 451
Dental Anomalies 451
Dental Crowding 452
Dental T r a u m a 452
Pathology 452
Paleopathology 453
Dental Attrition 454
Pathology 454
Paleopathology 454
Dental Discoloration 456
Pathology 456
Paleopathology 456
LITERATURE CITED 457
This book is dedicated
to the memory of
ERWIN UEHLINGER
Emeritus Professor of Pathology
of the University of Zurich (Switzerland)
the dean of European bone pathologists
whose continued interest and advice
from the inception of this book
was a great inspiration
Erwin Uehlinger
8 August 1 8 9 9 - 1 8 April 1980
Identification
of Pathological Conditions
in H u m a n Skeletal Remains
Donald J. Ortner
and Walter G. J. Putschar
Introduction
H u m a n biological history involves the inter- ate. Genetics and its influence on several biolog-
action of countless individuals and their environ- ical factors, including the immune response, must
ment. This dynamic condition includes extraor- be significant. To the extent that heritable factors
dinarily complex interrelationships, not only play a role in resistance to disease, morbid con-
among peoples but between individuals and a ditions influence the continuing process of human
host of physical and biological factors that affect biological adaptation. Similarly the existence of
their well-being. One of the major objectives of cultural mechanisms that minimize the effect of
the biologist is to discover and record this history. disease may be of considerable biological impor-
However, any attempt to write even a partial tance. Thus, our understanding of man's cultural
biological history of man depends ultimately on and biological response to disease through time
our knowledge of the factors that influence it. becomes an important dimension of our under-
Even the most superficial review of the history standing of human history.
of disease reveals its enormous significance in
human biological history. The terrifying plagues Objectives of this Book
recorded in European history prematurely ended
the lives of millions of people. The influenza The genesis of this book began in 1970, at
epidemic after World War I resulted in the death which time plans were developed for the first
of over twenty million peoplefar more than Paleopathology Seminar Series to be held in 1971.
died as a direct result of that most devastating This seminar series brought several leading au-
and bloody war. thorities on skeletal disease, paleopathology, and
Why do some people survive a morbid condi- related subjects to the Smithsonian Institution to
tion and others die? Clearly chance factors oper- present lectures to a select group of scholars in-
terested in skeletal paleopathology.
Donald J. Ortner, Department of Anthropology, National Museum of The seminar series was held yearly through
Natural History, Smithsonian Institution, Washington, D. C. 20560.
Walter G. J. Putschar, Department of Pathology, Massachusetts
1974. By that time the logistics of obtaining funds
General Hospital, Boston, Massachusetts 02114. to offer the series, arranging for students to come
1
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
from many universities, including foreign ones, It is against the background of the substantial
and assembling an outstanding faculty for the literature in paleopathology (exceeding 3000 ci-
ten-week series became almost overwhelming. Dr. tations) and the scholarly needs revealed by this
Donald J. Ortner, physical anthropologist and literature that we have formulated the objectives
director of the series, and Dr. Walter G. J. Put- of this book. The most fundamental objective is
schar, pathologist and the principal lecturer on to provide an integrated detailed discussion of the
skeletal pathology, decided that many more gross pathology of the human skeleton, emphasiz-
scholars interested in skeletal paleopathology ing those conditions that can be seen in dry
would have access to the substance of the seminar specimens regardless of whether or not they have
series if the information were incorporated into a so far been identified in archeological material.
In order to provide reliable standard specimens
book. This book would reflect the content of the
for dry bone diagnosis, we had to concentrate on
seminar series, which had included lectures on
the period from about AD 1750 to 1930. Earlier,
calcified tissue biology, methodology, pathology,
the medical data are too ambiguous and, later,
and radiology, and laboratory sessions on paleo-
the pathologic manifestations are too altered by
pathology, all emphasizing the human skeleton.
surgery, chemotherapy, radiation therapy and,
There are many sources of information on the above all, by the use of antibiotics. For this
history of disease including ancient medical doc- purpose we had to turn to the great medical
uments, historical records, art, and the physical museums of Great Britain and of continental
remains of ancient people, both soft tissues and Europe. The British collections proved in many
skeletons. Undoubtedly human skeletons repre- ways the most useful, because they were made by
sent the most ubiquitous source of information on physicians and surgeons, who were at all times
ancient diseases. Unfortunately this fact must be interested in documenting clinical and historical
tempered with the knowledge that relatively few data. We realize that even this material, which
morbid conditions affect the skeleton in a way represents as closely as possible the natural history
that leaves visible changes in the dry bones. In of the affections at that period in time and which
spite of this limitation, the study of skeletal pa- are not modified by significant therapeutic pro-
thology in archeological materials can provide cedures, is not necessarily identical with previous
time depth to our understanding of disease and manifestations seen in archeological specimens.
contribute to our understanding of the role of However, it is the only documented material
disease in human adaptation. In addition, skeletal available for comparison.
paleopathology may also broaden our under- This book is mainly intended to serve as a text
standing of disease as it affects bone at the present and atlas of dry bone pathology, regardless of
time. The paleopathologist generally has access whether or not each entity has been identified in
to all portions of the skeleton, a situation rarely paleopathology. For that reason, as many aspects
realized in modern pathology. This means that as possible of documented, dry bone pathology
the gross pattern and distribution of the morbid have been illustrated, especially because the orig-
condition in all areas of the skeleton can be inal skeletal collections can never be duplicated
studied in detail. A good example of such a study and may ultimately disappear. In the paleopath-
is the work by M0ller-Christensen (1967) on the ological discussions, emphasis is laid on careful
medieval human skeletons from a leper cemetery and critical study of published reports and of
in Denmark, which revealed hitherto not fully actual specimens, bringing all types of evidence
appreciated skeletal manifestations of the disease. to bear on arriving at a reasonable diagnostic
Undoubtedly more careful analysis of paleopath- assumption. It hardly needs to be emphasized
ological skeletons will reveal additional informa- that, even so, multiple possibilities and uncertain-
tion on the biology of other bone diseases. ties often remain. Not the least of these problems
NUMBER 28
pathological specimens jointly studied. For some ing, preparing the bibliography, editing, and
cases we were able to obtain X-ray films as well. otherwise making her remarkable abilities avail-
W. G. J. Putschar described the specimens in able to the project. Mrs. Joyce Ortner has also
detail on tape and included original autopsy and assisted in obtaining illustrative material and
clinical data where available. This collection of skeletal specimens used in the book.
photographs. X-rays, and the transcripts of case
Abbreviations
descriptions is available for study at the Depart-
ment of Anthropology, National Museum of Nat- T h e illustrations in this book are of specimens
ural History, Smithsonian Institution, Washing- from many institutions. T h e following abbrevia-
ton, D.C. Many of them are used as illustrations tions are used in the legends to avoid repetition
in this book. of lengthy institutional names and locations.
A number of people have made significant
AFIP Armed Forces Institute of Pathology
contributions in the preparation of the manu- Washington, D. C. USA
script. Mrs. Paula Cardwell, Mrs. Eleanor Haley
AIAC Australian Institute of Anatomy
and particularly Mrs. Katharine Holland typed Canberra, Australia
initial drafts. Mrs. Marguerite Brigida and Mrs.
AIUZ Anthropological Institute
Elizabeth Beard typed the final draft. Mrs. Mar- University of Zurich
cia Bakry prepared some of the drawings. To Ms. Zurich, Switzerland
Jacqui Schulz goes a special note of appreciation ANM National Museum of Anthropology
for the many unpaid hours spent in preparing the Prague, Czechoslovakia
remaining drawings and getting the photographic BMNH British Museum (Natural History)
illustrations ready for publication. Photographic London, England
enlargements were prepared by Mr. H. E. Daugh- CGH Department of Pathology
erty and Mrs. Agnes Stix. Mrs. Stix also assisted Charleston General Hospital
in editing and typing the manuscript. Mr. David Charleston, West Virginia
Yong, Mr. Edward Garner and Mr. Dwight DPUS Department of Pathology
Schmidt provided valuable technical assistance. University of Strasbourg
The staff of the library of the Smithsonian Insti- Strasbourg, France
tution, particularly Mrs. Janette Saquet, was FM Field Museum of Natural History
most helpful. Drs. J. Lawrence Angel, T. Dale Chicago, Illinois, USA
Stewart, and Douglas H. Ubelaker, Department FPAM Federal Pathologic-Anatomy Museum
of Anthropology, Smithsonian Institution, have Vienna, Austria
made valuable suggestions, as have Dr. Saul Jar- GHPM Gordon Pathology Museum
cho, New York City, USA, and Dr. George Ar- Guy's Hospital Medical School
melagos, University of Massachusetts, Amherst, London, England
Massachusetts, USA. The staff of the Smithson- HM Hunterian Museum
ian Institution Press, particularly Mr. Albert L. T h e Royal College of Surgeons of England
Ruffin, Jr., Managing Editor, Series Publications, London, England
and Ms. Joan B. Horn, senior editor, deserve HMCS Historical Museum
special recognition for their assistance from the Chur, Switzerland
with a broad range of new papers on numerous human paleopathology, which addressed this
subjects related to the study of ancient disease. problem among others. T h e participants called
Morse's report (1969) on skeletal pathology in for the establishment of a paleopathology registry
human archeological material from the midwest- and improved diagnostic methodology to par-
ern United States provides excellent descriptive tially correct these problems. Steinbeck's recent
details on many types of skeletal diseases. textbook (1976) on diagnosis of ancient bone
Throughout the development of human skele- disease represents the first integrated attempt to
tal paleopathology as a scholarly discipline, there establish diagnostic criteria for the paleopathol-
have been recurring problems in both theory and ogist. As such it represents an important step in
methodology. In the early stages of this develop- improving the knowledge regarding the types of
ment most of the research was conducted by diseases that affect bone and the morphological
physicians who had little knowledge of archeol- features associated with the disease.
ogy. In more recent times most of the studies of
pathological skeletal specimens have been con-
The Paleopathology Program at the
ducted by anthropologists whose background in
Smithsonian Institution
gross bone pathology may have been inadequate.
This has led to problems in which lesions of bone Ortner (1976) has reported the development of
were incorrectly attributed to the pre-Columbian a program at the Smithsonian Institution, which
time period by those unfamiliar with the com- addresses the need for a registry and includes
plexities of archeological dating and in which additional reference materials. This Paleopath-
bone lesions were incorrectly diagnosed through ology Program has as its major objective the
ignorance of anatomy and the total range of identification and classification of all pathological
diseases that affect bone (see Stewart's comments specimens in the vast human skeletal collections
on this problem in Jarcho, 1966:43). of the National Museum of Natural History.
Much of the emphasis in paleopathology until Significant progress has been made toward this
recently has been on descriptions of pathological objective. Another objective is to build a reference
specimens, and there has been little effort to relate collection of clinically documented cases of skel-
the evidence of disease to the broader problems etal disease including gross specimens, photo-
of human adaptation. Hints of such an emphasis graphs, and roentgen films.
exist in Hooton's Pecos Pueblo monograph (1930) In the United States, Drs. George Huntington,
and more recently in the consideration of epide- College of Physicians and Surgeons in New York
miological factors in evaluating the data on pre- City, T. Wingate Todd, Western Reserve Uni-
Columbian tuberculosis in the New World versity in Cleveland, Ohio, and Robert Terry in
(Morse, 1969) and in discussions on the origin of collaboration with Mildred Trotter, Washington
treponemal diseases (Hackett, 1963; Hudson, University in St. Louis, Missouri, developed ma-
1965). The trend toward population studies of jor anatomical skeletal collections from anatomi-
ancient disease undoubtedly will become increas- cal, dissecting-room cadavers. Each of these col-
ingly important as descriptive data accumulate lections contained about 2000 skeletons, among
and the diagnostic criteria for skeletal disease are which were pathological specimens. Ales
clarified. Hrdlicka, the founder of physical anthropology
Much of the descriptive literature in skeletal at the Smithsonian Institution and one of the
paleopathology depends on the scholar's knowl- pioneers of American paleopathology, obtained
edge of gross bone pathology. Unfortunately, the Huntington skeletal collection for the Na-
where this knowledge is inadequate there have tional Museum of Natural History. This collec-
been few reference sources that could be of assist- tion was accessioned in 1921, partially in the hope
ance. Jarcho (1966) organized a symposium on that it would become the nucleus of a reference
NUMBER 28
collection on pathology of the skeleton (Hrdlicka cheological skeletons is awkward at best. Careful
letter to J. H. Kellogg, 31 January 1921). More photographs and roentgen films of such materials
recently the Terry collection has also been trans- are the most realistic vehicle for comparative
ferred to the Smithsonian. T h e Todd collection is studies.
currently housed at the Cleveland Museum of The final objective in the Smithsonian Paleo-
Natural History, Cleveland, Ohio, USA. pathology Program is to gather together biblio-
It is clear that collections of documented bone graphic source materials from the literature on
pathology will need to be added to these fine bone and joint pathology and on paleopathology.
skeletal collections to supply adequate compara- Much of this material is in older, rather inacces-
tive material for the needs of the paleopathologist. sible sources, and considerable effort has been
In the United States, there are a few skeletal expended to obtain originals or copies of much of
collections specifically devoted to pathological the relevant literature. This bibliographic mate-
conditions including those of the Armed Forces rial, as well as the photographs and detailed
Institute of Pathology in Washington, D. C , The descriptions of the cases studied in our joint Eu-
Warren Anatomical Museum at Harvard Uni- ropean museum survey, are available for study at
versity and the Mutter Museum of the College of the Department of Anthropology at the National
Physicians of Philadelphia. However, direct com- Museum of Natural History of the Smithsonian
parison of material in these collections with ar- Institution in Washington, D. C , USA.
T h e Biology of Skeletal Tissues
8
NUMBER 28
FIGURE 2.Fiber bone formation (FB) on calcified cartilage cores (CC). Osteoblasts (OB) are
active in the left of the field. An osteoclast (OC) is destroying calcified cartilage near the right
edge of the field. T h e section is from the femur of a 5-month h u m a n fetus. (Approximately
X 1000.)
10 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
fetus, it is apparent that mineralized cartilage is in diameter. Growth in diameter occurs by ap-
a very temporary tissue. Within 10 to 15 milli- position as the result of intramembranous ossifi-
meters distance of the zone where the cartilage is cation. However, early in embryonic life most of
mineralizing, most of such tissue has been re- the centers of ossification in the skull are of the
placed by the combined activity of osteoclasts intramembranous type. T h e development of the
and osteoblasts. bones of the skull is complex and the reader
The initial site of penetration by the blood should consult a standard reference on h u m a n
vessels into the cartilage model of a long bone embryology (e.g., Hamilton and Mossman, 1972)
becomes the nutrient foramen of the mature for a detailed discussion. For the purposes of this
bone. Bone growth takes place centrifugally from book, it is sufficient to note that the centers of
this site, although not necessarily in equal endochondral ossification in the skull are primar-
amounts in all directions. As the zone of miner- ily associated with the skull base including the
alizing cartilage moves away from the initial sphenoid and part of the occipital (Figure 3).
center of ossification, the sleeve bone is also grow- It might be well at this point to emphasize that
ing in both directions and forms the initial com- the distinction between endochondral cartilage
pact tissue or shaft of the developing bone. Be- and membrane-formed bone is more than an
cause the shaft flares near the ends, the process of academic exercise. As will be emphasized subse-
growth also involves a process of remodeling in quently, some diseases focus on skeletal tissue
which the flared end is reduced to the appropriate formed in a cartilage model (e.g., achondropla-
dimensions for the shaft. sia). Other diseases also affect the process of
Toward the end of fetal life some of the long membrane bone formation (e.g., osteogenesis im-
bones such as the femur establish secondary cen- perfecta) .
ters of ossification in the epiphyses. In these cen- T h e embryological development of vertebrae is
ters the process of cartilage mineralization, fol- also complex. There are, however, congenital de-
lowed by vascular invasion and the addition of
bone, in turn followed by the removal of trabec-
ulae containing mineralized cartilage, is essen-
tially the same as the growth of the diaphysis.
In intramembranous ossification, mesenchymal
cells differentiate (probably through one or more
intermediate steps) into bone forming cells (oste-
oblasts). This process occurs within the mesen-
chymal cell condensation. As cell differentiation
takes place, the cells become organized and form
smooth, membranous sheets. Continuing devel-
opment involves the synthesis of organic bone
matrix by osteoblasts. This organic matrix is in
close proximity to the cell and consists primarily
of collagen but contains noncollagenous, organic
materials as well. In its unmineralized state the
organic matrix of bone is called osteoid. Normally
the mineralization of osteoid proceeds rapidly (in
a matter of hours) although full mineralization of
bone matrix, particularly in the adult, may take FiGURE 3.Midsagittal drawing of the skull of a 4-month
h u m a n fetus. Stippled areas indicate approximate region of
months or years.
intramembranous ossification, horizontal lines indicate ap-
As the long bones lengthen they also increase proximate regions of endochondral ossification.
NUMBER 28 11
FIGURE 5.Fiber bone in a 5-month human fetus. Note the FIGURE 6.Calcified cartilage (arrow) surrounded by devel-
irregular orientation of most of the fiber bundles. (Approxi- oping bone in a 5-month h u m a n fetus. T h e light is partially
mately X 100.) polarized. Note that the calcified cartilage has optical prop-
erties similar to the background in contrast with bone, which
is generally much brighter. This brightness is due to the
anisotropic properties of bone. (Approximately X 1000.)
tures are easily seen in histological preparations
using a polarizing microscope. The collagen of
the protein matrix of bone has crystalline prop- Cartilage
erties because of the periodic arrangement of the
molecules of tropocoUagen, which make up the With this background on the early develop-
major component of the matrix. This arrange- ment of skeletal tissue let me review in greater
ment results in an optical property called aniso- detail the role of cartilage and bone in the func-
tropy (birefringence), in which the axis of light tion of skeletal tissue. Three types of cartilage
passing through the fibers is rotated. tissue occur in human organisms: (1) hyaline, (2)
If two polarizing filters are adjusted so that the fibrous, and (3) elastic. Of these three, hyaline
filter axes are perpendicular to each other, light cartilage is germane to our discussion of skeletal
cannot pass through the filters. If a histological tissue because of its importance in bone growth.
specimen is placed between such filters, birefrin- I have already discussed the role of cartilage in
gent areas in the tissue will rotate the light per- endochondral bone formation in which hyaline
mitting some of the rays to pass through the filter cartilage provides a temporary mineralized scaf-
farthest away from the light source and be seen fold for bone formation. These endochondral os-
as a light area of tissue. Portions of the tissue that sification centers or zones persist throughout the
are not birefringent will not rotate light and this growth period and are obliterated at varying ages
will appear dark in polarized light. In this context in different bones; the last fusion occurs by about
it may be well to emphasize that both fiber bone the age of 25 years with the fusion of the two
and lamellar bone have anisotropic properties in growth centers of the iliac crest.
contrast with calcified cartilage, which does not In addition to its involvement in growth, hya-
rotate light and thus appears dark in a polarizing line cartilage provides the gliding surface of all
microscope (Figure 6). true joints such as those between the long tubular
NUMBER 28 13
bones. Hyaline cartilage, like bone, has two basic ing a number of abnormal conditions seen in the
components, cells and intercellular matrix. How- joint surfaces of bone, particularly in the arthri-
ever, there are many features of hyaline cartilage tides.
that are in distinct contrast to bone. Although
The Cells of Bone
chondrocytes and chondroblasts are derived from
mesenchymal cells, as are bone cells, the cartilage Two cells of bone (osteoblasts and osteoclasts)
matrix secreted by chondroblasts contains less are directly responsible for its gross appearance.
collagen (about 10 percent) but cartilage contains The third bone cell, the osteocyte, is very much
much more water and a higher concentration of part of the histological appearance of bone and
chondroitin sulfate, a type of noncollagenous pro- plays an important role in mineralization, bone
tein, than is found in bone. During the growth tissue maintenance, and mineral physiology. The
phase, chondroblasts are in direct contact with activity of all three bone cells may be divided
the enlarging cartilage and are contributing to into five functions: (1) protein matrix synthesis,
the growth process by secreting protein matrix, (2) mineralization of protein matrix, (3) bone
which occasionally surrounds some chondro- tissue maintenance, (4) resorption of mineralized
blasts. T h e chondroblasts that become sur- tissue, and (5) involvement in general mineral
rounded by matrix differentiate into chondro- physiology.
cytes but retain many of the chondroblastic prop- The osteoblast itself contains the normal basic
erties (Ham, 1974:372), such as the ability to ingredients of a cell, a nucleus and cytoplasm
divide, to produce new cells, and the ability to containing organelles (mitochondria, endoplas-
secrete matrix. Bone cells (osteocytes) do not di- mic reticulum, ribosomes, and Golgi bodies) in-
vide and have only very limited ability to produce volved particularly in the synthesis of protein
matrix. matrix. The fluid phase of cytoplasm includes
Cartilage tissue is similar to bone tissue in that water, glycogen, and fat vacuoles. The cytoplasm
it has the capacity to grow by adding cells and is surrounded by a thin membrane, which has
matrix to existing surfaces (appositional growth). long, fine extensions filled with cytoplasmic fluid.
However, unlike bone, cartilage can expand (in- These cytoplasmic extensions form an intercon-
terstitial growth) by multiplication of cells and necting network, with adjacent cells forming the
interstitial secretion of matrix by its chondrocytes main component of the germinative layer of the
(Ham, 1974:372-374). Cartilage cells, both chon- bone forming tissue (Figure 7).
droblasts and chondrocytes, retain optimal ability As the osteoblast sheets, applied to an existing
to divide and secrete matrix only during the surface of bone or calcified cartilage, begin to
growth phase of the individual (Ham, 1974:374). secrete osteoid, a matrix is formed, which becomes
Another contrast between hyaline cartilage and interposed between them and the bone surface
bone is that cartilage is poorly vascularized. The (Figure 8). However, some of the osteoblasts be-
nutrients that are needed for chondrocyte func- come surrounded by the matrix in spaces called
tion and the metabolites that result from cell lacunae (Figure 9). The cytoplasmic extensions
activity must arrive and be removed while rela- are maintained with other nearby osteoblasts,
tively isolated from vascular supply by the gel- which are also being surrounded by osteoid, and
like matrix that surrounds the cell. The minimal with the osteoblasts, which remain at the protein
vascularization and the reduced ability of car- secreting front. Surrounded osteoblasts are now
tilage cells to multiply after the end of longitu- osteocytes. The interconnections between osteo-
dinal growth appear to be related factors in cytes surrounded by matrix are maintained after
greatly limiting the capacity of cartilage to repair mineralization and form the little canals (canalic-
itself if damaged by injury or disease after ma- uli), which are a prominent part of bone histol-
turity. This fact becomes important in interpret- ogy. The interconnections between the osteoid
14 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Bone Growth
DIAPHYSIS i
METAPHYSIS
GROWTH ^
PLATE \
EPIPHYSIS FIGURE 12.Remodeling dynamics at the end of a growing
bone. T h e conical end represents the metaphysis and growth
plate. Hatching indicates the earlier stage in growth. T h e
cross hatching indicates bone that must be removed as the
FIGURE 11.Diagrammatic representation of the major com- bone grows in length. Arrows indicate the direction of bone
ponents of a growing long bone. addition during the growth process.
18 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
endosteal surface and posterolateral periosteal about a relatively large histological structure. The
surface. Histologically what is apparent is that length of an osteon is problematical since osteons
surface parallel lamellar bone characterizes those are not discrete units but divide, rejoin and inter-
areas where bone is being added, while internally connect with other osteons to form a complex
(osteon) remodeled bone and partially resorbed network. The order of magnitude for the length
osteons characterize areas of bone removal. The of an osteon segment from where it splits off and
process of drift is a response to continuing changes forms a discrete unit to the point where it joins
in the load axis of the tibia during and to a lesser another similar structure or terminates is from 2
extent after the cessation of growth. As such it is to 5 millimeters. While osteons are most often
analogous to the remodeling of bone in fracture viewed in two dimensions it is important to be
healing (p.61), where alignment of the broken aware of the three dimensional aspect of their
ends is poor. morphology.
Structurally, an osteon in cross-section has a
Osteon Remodeling histologically discrete, round boundary. Within
this boundary are circular layers of bone tissue
During the growth phase, and to a greatly whose collagen fibers are aligned in alternating
reduced extent throughout the remainder of life, directions like the layers in circumferential la-
compact bone is added to existing external sur- mellar bone. Osteocytes are distributed through-
faces of bone by apposition. Appositional bone is out these layers and are interconnected by cana-
deposited in layers, which give rise to the char- liculi in the bone, which contain the cytoplasmic
acteristic histological appearance of circumfer- extensions of the osteocytes. All viable osteons
ential lamellar bone. However, like most other contain a central (Haversian) canal averaging
tissues of the body, bone needs to be renewed. about 50 microns in diameter, which includes a
T h e process of renewal is called internal or osteon
remodeling (Figure 14). All bone remodeling re-
flects an obvious but important biological prop-
erty of bone, namely, it is hard. This means that
it cannot grow by interstitial expansion as carti-
lage can, and it cannot be removed without de-
struction by cellular activity. Because of the hard-
ness of bone this renewal process involves the
removal of existing tissue and its replacement
with newly formed tissue. Throughout the skele-
ton much of the lamellar bone formed during
growth and remodeling remains at least through
early adulthood. However, in compact bone, par-
ticularly in the diaphysis of long bones, the sur-
face parallel lamellar bone is replaced by the
osteons.
T h e classic appearance of the osteon is seen in
cross-sections of compact bone (Figures 15, 16).
T h e basic structure of an osteon in such a prep-
FIGURE 14.Photomicrographic field of osteons in adult
aration is circular, having a diameter that varies
human compact bone. The elongated white structures within
in size but averages approximately 300 microns. an osteon are lacunae. The fine filament-like structure ra-
T h e thickness of this page of paper is about 100 diating out from the central canal are canaliculi. (Darkfield
microns, so it is apparent that we are talking illumination, approximately X 100.)
20 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 15, 16.Microscopic field showing osteons in various stages of development: 15, A
resorption space (RS) is seen in the lower right corner. A forming osteon (FO) is in the lower
left corner. Most of the remaining osteons in the field have completed protein matrix synthesis
as indicated by the small size of the central canals. (Approximately X 45.) 16, Microradiograph
of field in Figure 15 showing variation in osteon density. Less mineralized osteons are darker.
minimum of one blood vessel. At least some filling front varies, but classically it is thought to
osteons contain a nerve. Some of the canaliculi be rather small. Therefore, both resorption and
containing cytoplasmic processes of the osteocytes formation take place at the same time, although
open into the central canal thus providing a in different parts of the tunnel. T h e refill of the
pathway for nutrients and for mineral ions
needed for continuing mineralization or ion re-
moval in mineral physiology. The canaliculi usu-
ally do not communicate between adjacent os-
teons.
The process of osteon remodeling begins with
the removal of bone, creating a circular tunnel
(Haversian resorption space). The actual process
is best visualized in its longitudinal axis (Figure
17). As an advancing wedge of osteoclasts forms
the tunnel, the osteoblasts generally begin the FIGURE 17.Diagrammatic representation of osteon remod-
eling in longitudinal section. Osteoclastic resorption is seen
refill process. The initial layer of bone matrix
to the left, with large multinucleated osteoclasts associated
deposited on the walls of the resorption space with the scalloped edge of bone. Osteoclastic activity is
tends to be somewhat different histologically. It associated with active hyperemia represented by the inter-
is more highly mineralized and the proportion of connected network of capillaries adjacent to the osteoclasts.
noncollagenous protein is somewhat greater. The In the center and right portions of the illustration osteopro-
term "reversal line" is used to distinguish this genitor cells (spindle-shaped cells adjacent to the blood
vessels) are differentiating into osteoblasts. Bone matrix syn-
layer from the remaining layers of bone in the
thesis and mineralization fill in the resorption space leaving
osteon. The space and time sequence between the an interconnected network of osteocytes seen as stellate cells
osteoclast resorbing front and the osteoblast re- in the layered matrix.
NUMBER 28 21
tunnel involves a process essentially identical to source of food. The two American Indian groups
that described earlier for circumferential lamellar and particularly the Pueblo Indians depended
bone formation: (1) layers of protein matrix are heavily on maize. Meat contains much more
secreted by osteoblasts; (2) cells and their cyto- protein than maize and would thus be more likely
plasmic processes are incorporated in the protein to provide the amino acids needed for synthesis
matrix; (3) primary mineralization occurs; (4) the of organic bone matrix. Stout and Simmons
process is repeated in a centripetal direction leav- (1979) review the application of histomorpho-
ing a central canal; and (5) osteocytes mediate metrical analysis in archeological bone specimens.
continuing secondary mineralization. During os- During the growth phase appositional devel-
teonal refill of resorption spaces there may be opment of circumferential bone tends to be rela-
temporary pauses in the refill process. This results tively rapid. Woven bone may be deposited on
in an arrest line, which is histologically similar to the cortex as fine, cancellous bone. Subsequently,
the reversal line. With the resumption of matrix the spaces in such woven, cancellous bone are
synthesis and mineralization, these arrest lines are filled in by lamellar bone, creating primary os-
retained. The physiological factors in the tempo- teons (Enlow, 1963:63). Although similar in ap-
rary arrested development of osteons are not pearance to secondary osteons, such structures do
known, but could prove to be a valuable source not represent a remodeling event. Histologically
of information on physiological conditions in ar- they differ from secondary osteons, tending to be
cheological skeletons. The time needed for resorp- smaller in cross-section. Also, primary osteons do
tion and refill are important. Bone formation not have a clearly defined reversal line marking
takes at least ten times as long as the destruction the termination of bone resorption (Figure 18).
of an equal amount of bone (Johnson, 1966:127). Primary osteons are generally replaced by sec-
This means that for formation-resorption to be in
balance, there needs to be ten times as many sites
of active bone formation as there are sites of
active bone destruction. In osteon remodeling the
theoretical equilibrium ratio in normal tissue re-
modeling is about ten osteons in the forming stage
for each resorption space.
In fact some studies have shown that in com-
pact bone of present day populations the observed
ratio is very close to the theoretical ratio (Blum-
berg and Kerley, 1966:159; Ortner, 1970:65).
Deviation from this ratio may be indicative of
inadequate nutrition or other morbid conditions.
A study by Richman and Ortner (1978) of osteon
remodeling in Eskimos, Arikara (Plains Indians),
and Pueblo Indians (Southwest U.S.) indicated
that the Eskimo sample has a formation-resorp-
tion ratio of 10 to 1. However, the two American
Indian samples have a ratio of approximately 6
to 1, indicating a substantial reduction in bone FIGURE 18.Primary osteon (arrow) in the long bone of an
replacement after resorption. The meaning of this infant about 6 months of age. This structure results from the
fill-in of spaces in newly formed bone. In human bone it is
finding needs further clarification; however, nu-
primarily associated with the very rapid growth occurring
tritional factors seem a rather obvious possibility. during fetal and infant development. (Approximately
Among the Eskimos meat constitutes the major X 100.)
22 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 20, 21.Cross-section of a compact bone from a young adult: 20, The right half of the
field is primarily circumferential lamellar bone containing several primary vascular canals. T h e
left portion of the field contains remnants of circumferential bone, but much of this bone has
been replaced by secondary osteons. (Polarized light, approximately X 70.) 21, Microradiograph
of field seen in Figure 20. Note that the circumferential lamellar bone is denser than that in the
osteons.
(Posner, 1969). The precise relationship between crystal. Given the small crystal size found in bone
the two types of mineral is not known. However, mineral, a few hundred angstroms in length and
the proportion of amorphous mineral decreases breadth and about fifty angstroms thick (Neu-
with increasing mineralization. This suggests that man and Neuman, 1958:55), there is an enormous
the amorphous calcium-phosphate might be a amount of bone crystal surface and a high like-
transitional phase existing predominantly during lihood of considerable exchange of ions between
the early stages of mineralization, There is some bone and body fluids. This offers the potential for
evidence that there may be localized concentra- bone to contain a considerable variety of chemical
tions of amorphous mineral in discrete histologi- elements. It has also been noted that bone mineral
cal zones within bone tissue (Ortner and Von may be present in an amorphous phase, which
Endt, 1971). These zones may be important in may have particular significance in bone physi-
mineral physiology by providing a more reactive ology.
or labile source of mineral ions. Johnson (1966:67-68) suggests that mineral
A detailed review of hypotheses regarding the ions are almost instantly available from the labile
chemical and structural relationship of bone pro- mineral lining the canalicular system. The next
tein and mineral is not pertinent here. However, most accessible source of mineral would be from
bone protein precedes bone mineral and is in- the osteocyte lacunae. Neither of these sources
volved in the mineralization process possibly by necessarily involves the dissolution of bone ma-
providing the initial site for mineralization. Two trix. The surfaces of bone including trabeculae
mechanisms have been proposed for this process. provide a second source of mineral ions, with the
In one hypothesis collagen provides a template or Haversian canals providing the least accessible
pattern to which mineral ions are attracted and source of mineral. Johnson appears to assume
arranged in the appropriate spacial relationship that ions from the last two sources must be re-
for mineral crystallization. The second hypothesis leased by osteoclastic activity. However, radio-
involves chemical binding of one of the mineral active tracer studies suggest that exchange (in-
components, such as phosphate to a reactive cluding both uptake and loss of radioactive ions)
group of some of the amino acids of collagen. can occur without matrix destruction by osteo-
Lees (1979) has proposed a model with both inter- clasts in the tissue surrounding the Haversian
and intrafibril mineralization of collagen. canal (Rowland, 1966:243).
Another view of initial bone mineralization Regardless of the actual mechanisms involved,
implicates the noncollagenous protein. However, it is clear that bone acts as a mineral bank.
Hancox (1972:87) notes that much of the research Removal of mineral components from bone tissue
supporting this hypothesis is based on mineraliza- is controlled systemically by parathyroid hor-
tion in cartilage. He is of the opinion that bone mone. J a n d e (1972) has shown that increases in
mineralization is different from that occurring in serum parathyroid hormone levels results in loss
cartilage and questions the validity of such re- of mineral around the osteocyte. Parathyroid hor-
search in explaining mineralization in bone. mone also increases the activity of the osteoclasts
The mineral phase of bone includes calcium in destroying bone. The hormone calcitonin is
and phosphate. However, the crystal structure of thought to act antagonistically to parathyroid
bone mineral is such that substitutions by some hormone, although its action is less well under-
elements (e.g., strontium, radium, and lead for stood and less obvious than parathyroid hormone.
calcium; fluorine for the hydroxyl group) can The major factor that affects the secretion of
take place for elements and ions in the crystal parathyroid hormone is the serum calcium level.
lattice. Furthermore, many elements may be at- The normal range for calcium in blood serum is
tracted to the surface of bone crystallites (adsorp- from 8.5 to 10.5 milligrams percent (or 8.5 to 10.5
tion) and the hydration shell surrounding the milligrams per 100 cubic centimeters of serum).
26 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
T h e mature tooth consists of three components the dental lamina. Subsequently the dental lam-
(Figure 23). The first of these is the very hard, ina forms individual enamel organs with a lining
exposed surface called enamel. Enamel has no of epithelial (ectodermal) cells called ameloblasts.
vascular supply and no cells. Dentine is the sec-
ond component and provides support for the
enamel in the tooth crown and forms the hard
tissue portion of the tooth root. Dentine is avas-
cular but has cells (odontoblasts) lining its inner
surface. Tubules extend from the odontoblasts to
the outer surface of the dentine. The third com-
ponent of a mature tooth is the pulp cavity and
root canal, which contain the nerve, vascular
supply, and pulp mesenchyme, which is the
source of the odontoblasts.
The following review of tooth development is
based largely on the figures and text of Hamilton
and Mossman (1972:572-575, figs. 549-554) and
Sicher and Bhaskar (1972). About the sixth week
of embryonic development, ectoderm begins to
FIGURE 24.Schematic representation of a developing hu-
invade mesoderm in the region of the upper and
man fetal incisor with a crown-rump length of 100 m m ,
lower jaw. This invasion consists of an outer arch, approximately 2V2 months fetal-life (Reprinted, with per-
which will result in the gum and inner arch called mission, from Hamilton and Mossman, 1972:574, fig. 552.).
NUMBER 28 27
This lining develops cup-like structures, which ectodermal cells (epithelium), (2) an intermediate
will form the enamel of each deciduous tooth. A zone of stellate reticulum, (3) an inner layer of
branch of the lamina will similarly form the ectodermal cells, (4) highly vascularized mesoder-
enamel for the permanent teeth. Filling the cup- mal cells (mesenchyme) associated with the inner
like indentation in an enamel organ are prolifer- layer of ectodermal cells, (5) a capillary network
ating mesenchymal (mesodermal) cells known as surrounding both the enamel organ and the den-
the dental papilla, which will produce the dentin tal papilla, and (6) a connective tissue sheath
(Figure 24). around the capillary network.
With the establishment of a connective tissue Later in the development of the embryo the
sheath around both the enamel organ and the inner layer of ectodermal cells (ameloblasts) will
dental papilla the two structures are called a secrete the enamel of the tooth and is called the
tooth germ or bud. At this stage of development, ameloblastic layer. Some of the mesodermal cells
the tooth bud consists of (1) an outer layer of in the dental papilla become arranged along the
FIGURES 25, 26.Tooth bud in a 5-month human fetus: 25, Low magnification, the enamel is
the dark layer of the apex of the tooth. (Partially polarized, approximately X 85.) 26, Higher
magnification showing detail of dentin and enamel in tooth bud. Boundary between dentin
and enamel is indicated by the arrow. Odontoblasts (OD) are seen with long processes extending
into dentinal tubules. Ameloblasts (AM) line the outer surface of the tooth bud and are actively
forming the enamel. (Approximately X 400.)
28 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
ameloblastic layer. The cells in this layer are provides attachment for connective tissue (the
odontoblasts and will produce the dentin. The periodontal membrane), which in turn attaches
two layers of cells are separated by a membrane to bone. The sequence of tooth formation and
(membrana praeformativa) the shape of which eruption provides a useful index of age through
directly defines the ultimate shape of the tooth. the adolescent years. For the present discussion it
The formation of both dentin and enamel pro- is sufficient to emphasize that the timing of erup-
ceeds by addition (apposition) away from this tion varies with the developmental age of the
membranedentin in a centripetal direction, individual and the tooth type.
enamel in a centrifugal direction (Figures 25, 26). During development, teeth require adequate
The ameloblasts ultimately disappear after nutritional input including protein, calcium,
enamel formation is completed, leaving behind, phosphate, trace elements, and vitamins A, C,
on the enamel surface, a thin covering or dental and D. Inadequacies in these components may
cuticle. The odontoblasts persist throughout the result in grossly abnormal teeth or in teeth more
life of the tooth as an inner lining of the dentin. susceptible to wear and microbial invasion (car-
The remainder of the mesodermal cells in the ies). Abnormalities of teeth may also be the result
dental papilla become richly vascularized and of diseases occurring during development, such as
form the dental pulp. The tooth root begins to rubella and syphilis, as well as of genetic prob-
form before eruption but is not completely formed lems. Various components, such as the enamel or
until some time after eruption. The root surface dentin, may be differently affected by a morbid
consists of a specialized tissue (cementum), which condition.
Methods Used in the Analysis of Skeletal Lesions
Today's physicians have at their disposal a vast anemia, thalassemia, is found in peoples from the
array of data to assist them in diagnosing a Mediterranean area and in southeast Asia. While
morbid condition in a living patient. Most of there is generally an association between racial
these data are not available to the paleopatholo- distribution and geography, the factors affecting
gist trying to diagnose a lesion in an archeological the individual in a specific geographic location
skeleton. In spite of the obvious limitations facing may not be genetic as is the case in sickle cell
paleopathologists, it is well to remember that they anemia and thalassemia. For example, coccidioi-
have at least one significant advantage over a domycosis is endemic mainly in dry, dusty regions
present day pathologist. If an archeological skel- of southwestern United States. This disease affects
eton is recovered in a good state of preservation, members of any human population living in this
the paleopathologist can examine an abnormal area although the incidence may vary (Miller
skeleton in its entirety and to a degree that would and Birsner, 1949).
be quite impossible in a current patient, living or Time should rarely be a crucial factor in the
dead. In paleopathology the fundamental objec- diagnosis of a skeletal lesion. However, it cannot
tive should be to obtain as much background be ignored. The significance of the time factor
information on the skeleton as possible and take will be more apparent in the discussion of trepo-
maximum advantage of one's ability to evaluate nemal conditions (p. 180). The problem can be
the skeletal lesion itself by direct observation. I stated briefly for illustrating its importance. The
shall review the methods for obtaining back- question is whether syphilis was introduced by
ground information on skeletal specimens first people from the Old World into the New World
and then review the methods for analyzing a or vice versa. This is a very complex problem but
morbid condition in the skeleton. the unambiguous identification of a case of syph-
Basic to any evaluation of pathology in arche- ilis in a specimen dated before 1492 in either the
ological specimens is the following data: (1) age, Old or New World would obviously be a signifi-
(2) race or human population, (3) sex, (4) geo- cant bit of information.
graphic location, and (5) time period or archeo- In evaluating all of the above factors with
logical horizon. A knowledge of these factors can respect to a diseased archeological skeleton it is
have a substantial influence on the probabilities important to be open minded before eliminating
of various types of morbid conditions. For exam- a possible disease on the basis of any one element.
ple, if we are able to determine that a specimen For example, it would be unwise to eliminate the
was a young adult at the time of death, this fact diagnosis of syphilis for a pre-Columbian New
would greatly reduce the probability that a dis- World skeleton simply because some scholars feel
eased skeleton was affected by carcinoma, since that syphilis originated in the Old World. While
this is primarily a problem of the aged. Likewise this is a rather obvious situation the principle
the knowledge that a skeleton, with multiple, applies to other variables as well, particularly
disseminated, destructive lesions, was male would since there is always a margin of error in deter-
tend to rule out metastasis from breast cancer. mining any of these variables in an archeological
It is clear that some diseases are associated with skeleton.
specific human populations. Sickle cell anemia Many of the criteria for determining the above
primarily affects black populations while another variables are available in published sources and
29
30 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
need not be discussed in detail here. The follow- conditions, particularly the latter, frequently are
ing review is derived largely from published not met. In such situations one hopes that the
sources and will provide a general summary of approximation is close.
methods for obtaining background data on ar- There is evidence that different methods of
cheological specimens. However, the emphasis determining age may reflect different statistical
will be on those aspects of the variables that are populations. Merchant and Ubelaker (1977) com-
significant for research in paleopathology. pared two different techniques of determining
age in subadult material, both of which were
based on the sequence of dental development.
Age Determination
When both techniques were applied to a single
The estimation of biological age in an archeo- archeological sample, they found considerable
logical specimen is related to several biological difference in the age as determined by each tech-
processes, such as growth and skeletal remodeling, nique. With this and other limitations in mind
which result in age related changes in the mor- let us review the various methods for estir. iting
phology of skeletal components. These changes biological age in archeological samples.
are seen at the gross, as well as at the microscopic Fetal material in archeological skeletal series is
level. All of the methods for age determination relatively rare but may be very significant, as in
attempt to establish the relationship between a situation where the mother died and was buried
morphological changes in the skeleton and the with the fetus. Estimation of age in such material
age of the individual at the time of death. Fur- may be a factor in inferring whether problems in
thermore, the methods involve the establishment birth might have been a factor in the mother's
of procedures for estimating age on the basis of death. Stewart (1968:132) provides a regression
these changes. Methods for determining age vary formula based on femur length for estimating age
significantly in terms of research design, statistical from the fifth fetal month through birth. At birth
methodology, appropriate age range, etc. the bony femur is about 80 mm in length, which
Through the age of 18 (subadult) three meth- provides a convenient criterion for distinguishing
ods of aging are used. These are based on age- fetal from postfetal material.
related variations in (1) bone length, (2) dental Other criteria may be inferred, if the preser-
eruption and root development, and (3) the ap- vation and excavation has been very careful, by
pearance and fusion of secondary centers of bone determining the presence or absence of centers of
development (epiphyses and apophyses). Excel- ossification. Standards for these features are pub-
lent and readily available reviews of these meth- lished in Stewart (1979a) and Krogman (1962:
ods are found in Krogman (1962) and Stewart 56-68). However, these standards are for birth
(1968, 1979a). It is important to emphasize that onward. T h e absence of bones, such as the cal-
estimates of age based on these methods reflect caneous, talus, cuboid, and the epiphyses of the
the usual problems in standardizing such proce- distal femur, proximal tibia, and proximal hu-
dures. One must assume that the research design merus, would be indicative of death before birth.
of the original study was adequate, particularly In archeological material identification of such
with respect to sampling the entire age distribu- ossification centers may be difficult or impossible
tion and population and that the morphological since they may bear little if any resemblance to
features can be assessed objectively. Furthermore, the shape of the bone later in development and
in applying any method of aging to an archeolog- may not be preserved. Careful excavation may
ical skeletal sample one assumes that the sample permit recovery of ossification centers in associa-
used to establish the prediction procedure and tion with an identifiable bone.
the unknown archeological sample are from the From birth through the growth phase, the cri-
same statistical population of individuals. These teria for estimating age are based on long bone
NUMBER 28 31
length (particularly femur), the appearance of part of the process of biological aging, such as the
ossification centers, the sequence of dental erup- coarseness of the diet and the physical activity of
tion and root development, and, during the late the individual.
growth period, the fusion of secondary ossification A recently developed method for age estima-
centers. T h e methods of age estimation based on tion is based on the process of microscopic bone
these variables are summarized by Krogman tissue renewal (osteon remodeling), which contin-
(1962), Stewart (1968, 1979a), and Ubelaker ues throughout life. Early studies by Amprino
(1978:46-53). By the age of 18 years (earlier in and Bairati (1936) and by Jowsey (1960) sug-
females), significant growth has stopped in most gested the existence of age dependent changes in
individuals although some epiphyses will con- osteon remodeling. Kerley (1965) was the first to
tinue to fuse through about age 25 years. apply adequate statistical samples and proce-
From 18 years onward, other aging criteria dures to this problem. In his research he used four
become more significant. These include the con- histological features: (1) osteons, (2) fragments of
tinuing metamorphosis of the pubic symphysis former osteons, (3) the amount of unremodeled
(Todd, 1920, 1921; McKern and Stewart, 1957; bone, and (4) the number of nonosteonal vascular
Gilbert and McKern, 1973), which provides age canals. The first two of these criteria increase with
estimates to the age of 50 years. The fusion of age, while the last two decrease with age. The
skull sutures has been a traditional criterion for statistical association between age and frequency
age determination. In their study of Americans of these features is the basis for estimating the age
killed in the Korean War, McKern and Stewart of an unknown specimen. Kerley determined this
(1957:37) found that suture closure was poorly relationship for three major bones: femur, tibia,
correlated with age and of little use in age esti- and fibula.
mation. Krogman (1962:89) supports this conclu- The error in estimating age using this method
sion but notes that the skull may be the only part compares favorably with estimates based on
of the skeleton present and thus the only source changes in the pubic symphysis. However, micro-
for estimating age in an unknown specimen. scopic aging methods can be applied to ages in
While Krogman's observations are addressed to excess of 50 years and thus, extends our ability to
forensic modern specimens they are also appro- estimate age into the older age categories. Because
priate for archeological skeletal collections. At the there is an increasing discrepancy between bio-
National Museum of Natural History, for exam- logical and chronological age as one gets older,
ple, more than half of the collection of about the factor of error is higher in the 50-plus age
25,000 skeletal specimens consists of the skull range. Regardless, this is the only method cur-
alone. Another problem in archeological material rently available that allows age estimation for
is that the pubic symphysis and other age criteria skeletons over 50 years of age. Kerley and Ube-
are particularly vulnerable to destruction in the laker (1978) have published revised regression
soil and may not be useable. Thus, age estimation formulae for Kerley's earlier study.
based on suture closure may be the only criterion As with any method there are problems in
available, but its limitations should be recog- using Kerley's method. Preparation of bone sec-
nized. tions is a time consuming and delicate procedure
Other aging methods have been developed in- and even more so in archeological specimens,
cluding those based on tooth wear (Brothwell where the bone may have to be strengthened with
1965a:67-70) and the degree of arthritic degen- plastic to prevent crumbling during processing.
eration (Stewart, 1958a). Without doubt these Soil erosion and organisms may destroy micro-
methods provide helpful corroboration for age scopic features needed for such an analysis. The
estimates from other sources. However, they are procedure also assumes a fairly sophisticated
limited by the influence of factors that are not knowledge of compact bone microstructure. One
32 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
modification of Kerley's method appears to offer unambiguous evidence of racial affiliation. Stew-
a simpler procedure (Ahlqvist and Damsten, art (1962) has reported that the femora of Negroes
1969) but does not appear to be as accurate in tend to be straighter than those of other races.
the lower age ranges (Bouvier and Ubelaker, However, there is considerable overlap in the
1977; Ubelaker, 1978:66). distribution of the data, making prediction of
race difficult. Furthermore, the postcranial skel-
Race Determination eton is greatly affected by nongenetic factors such
as diet, making it unlikely that racial differences
Race (here used in the sense of a discrete can be resolved on this basis alone, at least to the
human population) determination in archeologi- extent of being useful in paleopathology.
cal skeletons is rarely a significant problem for
the paleopathologist, since the archeological Sex Determination
provenience usually provides a reliable indication
of at least the broad racial background. Occasion- Sex differences in skeletal specimens are prob-
ally, however, members of more than one human ably the least ambiguous of all the factors basic
population will be buried in the same cemetery, to the paleopathologist. In the skeleton the best
and identification of this fact can provide relevant criteria for determining sex are in the pelvic
background data for the interpretation of skeletal bones. These bones reflect the fundamental dif-
lesions. Methods for distinguishing between ferences in functions associated with reproduc-
broad racial categories (e.g.. White, Negro, Mon- tion, particularly childbearing, in the female. In
goloid) are well known and have been summa- the female pelvis the major factor influencing its
rized in Krogman (1962) and Stewart (1968, shape is the necessity for the infant to pass
1979a). through the pelvic canal during birth. Both the
The major differences between human popu- dimensions and the shape of the pelvic inlet and
lations are best seen in the skull. Traditionally, outlet reflect this function (Figure 27). Thus, the
physical anthropologists have characterized these female inlet and outlet are relatively and usually
differences in terms of various complexes of the absolutely larger and rounder than in the male.
skull such as skull vault shape (long headed, A more detailed review of the specifics of these
round headed), relative projection of the jaws differences is given in Krogman (1962) and Stew-
(prognathism), shape of the nose (long and nar-
row in Whites, short and broad in Negroes), and
relative position of the cheek bones (prominent in
Mongoloids).
In the traditional approach to racial character-
ization, measurement of skull dimensions is im-
portant, but each measurement tends to be
treated as a discrete feature. A more recent de-
velopment has applied multivariate statistical
procedures to broad racial classification (Giles
and Elliot, 1962) and to more subtle skull varia-
tions within broad racial categories (e.g., Howells,
1973, Ortner and Corruccini, 1976). A multivar- FIGURE 27.Comparative views of the male a n d female
iate statistical approach to racial variation pro- pelves. Although the male pelvis is larger overall, the female
pelvic inlet is larger. T h e female sacrum is wider and the
vides greater objectivity and a measure of racial
pubic bone is longer. T h e female subpubic angle is larger
distance, which is based on many measurements. than the male. (Male, left, N M N H 320026; female, right,
The remainder of the skeleton does not provide N M N H 320001.)
NUMBER 28 33
it. Much can be learned by the analysis of mor- oping a life table for skeletal material. However,
tality and the demographic aspects associated it is important that one be generally aware of the
with it. Bogue (1969:549) notes that mortality assumptions and hazards in applying such tech-
exerts a varying force on different human popu- niques to archeological populations. T h e most
lations. Clearly a major factor in this variation is obvious problem arises from the fact that modern
the condition of health in these populations. life tables are based on events (deaths) occurring
Bogue (1969:549) also emphasized that "mortal- in a living population, whereas archeological re-
ity has a very unequal impact on various age constructions of life tables are based on a popu-
groups." The overall pattern of death rate in lation of individuals all of whom are dead. The
various age categories will also vary in different characteristics of the two types of populations are
populations. This is clearly demonstrated in the not necessarily the same, although this must be
marked reduction of infant deaths in highly de- assumed in such applications. Another problem
veloped societies as contrasted with developing is the extent to which skeletons recovered from a
societies (Bogue, 1969:556-557). Estimates of cemetery represent all the individuals who died
mortality in an American Indian skeletal popu- in a given population. Cultural practices regard-
lation reveals high infant mortality but, in addi- ing formal interment in cemeteries vary and may
tion, another peak in mortality is present around not include burial of infants. Furthermore smaller
adolescence (Ubelaker, 1974:60). Other estimates skeletons may not be preserved as well as larger
of mortality in ancient skeletal populations from ones. This would, for example, adversely affect
the eastern Mediterranean have indicated higher the proportion of infants recovered from the cem-
mortality in females of childbearing age than etery during excavation. Swedlund and Armela-
males of the same age, which probably reflects gos (1976:47) note that the validity of developing
the hazards associated with pregnancy and child- life tables for archeological populations depends
birth (Angel, 1969a; 1971:71). on the degree to which the population is (1)
Of several statistical methods treating mortal- sedentary and (2) large, and (3) provides a large
ity, one of the most useful is the life table (e.g., number of recoverable skeletons. When these
Bogue, 1969:551-552; Swedlund and Armelagos, three conditions prevail, or are at least approxi-
1976:47). In general, the life table summarizes mated, life table data provide a significant sup-
the frequency of events and the probability of plement to analysis of bone disease.
events happening within discrete intervals of time
throughout the entire range of life within a pop-
Archeological Documentation
ulation. Basically these events include (1) the
number of deaths occurring per unit of popula- I cannot overstress the importance of good
tion within specific age intervals and (2) the archeological documentation of all skeletal spec-
probable average number of years of remaining imens. Resolution of interesting and significant
life for individuals in each category. Variations epidemiological problems may hinge on such
in these factors reflect many conditions, such as data. For example, one archeological skeleton
diet, disease, warfare, and other problems. As from Arkansas in the collection of the National
such, data in life tables may provide nonspecific Museum of Natural History, Washington, D . C ,
but useful information on the relative health of a USA, probably represents one of the most con-
human population. vincing examples of treponemal infection that
A discussion of the methods and limitations of exists. This specimen ( N M N H 258778) was ex-
constructing life tables is given in several sources cavated in the late nineteenth century using
(e.g., Bogue, 1969:551-555; Swedlund and Ar- methods that make accurate archeological dating
melagos 1976:63-64; Ubelaker, 1978:91-97). impossible without considerable destruction of
Such sources should be consulted before devel- the specimen (Figures 329-332). This skeleton, if
NUMBER 28 35
dated before Columbus, would provide valuable pendable skeletal material exists for such a pur-
information toward resolving the problem of the pose, there are many problems encountered in
origin of syphilis. Thus, the usual elements of assuring that the ^'^C was part of the tissue at the
archeological provenience, geographical location, time of death and not added later.
archeological horizon or date, and cultural asso- Some of the carbon in bone is associated with
ciation, are important variables in paleopathol- the mineral phase of bone as carbonate. Hassan
ogy- and Ortner (1977) have noted that carbonate
In most cases, data obtained during excavation exchange may occur after death and burial. Fur-
of an archeological specimen will supply detailed thermore they point out that physical contami-
information on provenience. Although it is con- nation with carbonaceous material also occurs.
ceivable that the geographical location of a spec- Thus, the mineral phase of bone is a poor source
imen could be lost due to a mistake in museum of ^^C because of contamination and recrystalli-
cataloging, we assume that data or geographical zation.
location will almost always be readily available. The protein phase in bone also contains car-
Very often the archeolgist can determine the date bon, but it is much more stable than bone mineral
or archeological horizon of the specimen on the after death and burial. Thus, bone protein is
basis of associated artifacts. In many areas of the probably the best source of radioactive carbon. It
world the evolution of artifacts has been carefully is, however, essential to remove all contaminants.
documented and associated with time. These time In the case of bone protein, it is very much
sequences of artifact series frequently provide the simpler to do this than for bone mineral, since
most accurate dating of associated skeletal mate- bone protein is more highly resistant to deminer-
rial. Dates based on association of artifacts may alizing agents. Such agents would tend to remove
be checked with dates obtained by absolute dat- soil contaminants and leave behind the insoluble
ing methods such as ^^C analysis, where appro- protein containing carbon incorporated in bone
priate material such as charcoal exists. Bone itself tissue during the life of the individual.
can be analyzed, but the methods currently avail- In theory, at least, the protein matrix of bone
able on a routine basis involve the destruction of should provide an accurate source for C analy-
a considerable amount of bone. sis. However, keep in mind that varying soil
Various methods of dating have been applied conditions affect the stability of bone protein.
directly to bone including ^'*C, nitrogen, fluorine, Acid soils will hydrolyze bone protein over the
and amino acid dating. However, all these meth- years, destroying the protein, and breaking down
ods may produce spurious results because of any the tissue in general. This results in the loss of
one of several variables that can affect the anal- nitrogen and this loss has been used as an index
ysis. There are several sources that review the of time (Oakley, 1950, 1963a, 1963b; Cook, 1960;
methods of dating and their inherent problems Doberenz and Matter, 1965). The effect of pro-
(e.g., Zuener, 1958; Brothwell and Higgs, 1970; tein degradation on ^"^C analysis is unknown but
Ortner, Von Endt, and Robinson, 1972; Michels, cannot be ignored.
1973; Hare, 1974; Von Endt, 1979). However, in Nitrogen analysis does provide supporting evi-
view of the importance of dating in paleopathol- dence of age. However, the degradation of bone
ogy it seems appropriate to provide a brief review protein, on which this method depends, is affected
of the problems with particular reference to the by several factors including soil pH, temperature,
biology of bone as it affects dating methods. and water (Ortner, Von Endt, and Robinson,
In ^"^C analysis of bone, the fundamental prob- 1972), which have not yet been fully clarified.
lem is bone's low carbon content, which requires Another dating method that is based on bone
the destruction of substantial quantities of bone protein utilizes the ratio between natural amino
for obtaining analytical data. Assuming that ex- acids (L form) and D amino acids, which gener-
36 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
ally do not occur in biological tissue. Through of the morphology of the abnormal bone. T h e
time racemization occurs, in which L amino acids remainder of this chapter focuses on the descrip-
convert to D forms. This process is correlated tive system for paleopathological skeletal speci-
with time (Hare, 1974) and has the advantage mens.
over nitrogen analysis of being affected by fewer The most fundamental concept relating to the
variables. Regrettably, as of this writing, much interpretation of abnormal bone conditions is
remains to be done before amino acid dating that the abnormal morphology that results from
provides a reliable method for dating archeolog- pathological processes in bone is always the result
ical skeletons. of disturbances in the osteoblast and osteoclast
cell populations (Schinz, Baensch, Friedl, and
Uehlinger, 1951-1952:191). Shifts in the relative
Gross Study of Skeletal Lesions
and absolute activity of these cells may be asso-
With this background on data basic to an ciated with abnormal activity by the osteocytes,
analysis of a pathological specimen, we can focus but this is a minor component of any disease
on methods for analyzing specific morbid condi- process in bone. Not only can there be shifts in
tons in a skeleton. Fundamentally, there are four the relative and absolute proportions of these
sources of information that may be relevant in cells, but, at least in the case of osteoblasts, the
paleopathology: (1) gross analysis of the skeleton speed or metabolic rate of the cells may change.
itself, (2) analysis of X-ray images, (3) chemical Thus, it is variation in the cell population balance
analysis of bone, and (4) microscopic examination and in cell activity that accounts for all the
of bone. variation in the morphology of abnormal bone.
The gross appearance and X-ray images of an In this sense then, one of the basic objectives of a
abnormal bone represent overlapping features of descriptive analysis of abnormal bone is to deter-
a disease process, and both should be part of any mine the actions of the cells that produced the
descriptive analysis of the morbid condition (see abnormal tissue. T h e importance of this perspec-
p. 45 ff). The ultimate goal of a descriptive tive cannot be overemphasized.
analysis is the identification of the disease process. Both systemic and local factors can stimulate
It is important to recognize that the specific cause or inhibit the activity of osteoblasts and osteo-
or etiology of an abnormal bone condition cannot clasts. Pathogenic organisms, including fungi,
always be derived from even the most careful bacteria, viruses, and parasites, act on bone ar-
analysis of the paleopathological specimen. How- chitecture by creating conditions that stimulate
ever, even when the specific disease cannot be or inhibit the bone cells. While it is rather re-
identified, the description of the abnormal con- markable that the activity of only two types of
dition may, in itself, provide important data in cell can produce such a large variety of abnormal
paleopathological research by providing infor- conditions in bone, it is important to remember
mation on the frequencies of cases in the descrip- that many distinctly different diseases produce
tive categories. I cannot overemphasize the im- very similar types of lesions.
portance of careful descriptive analysis of all As we begin to think about the description of
paleopathological specimens. This is basic to the morbid conditions in the skeleton, it is important
identification of disease, but it also represents to be aware of the fundamental ways bone cells
significant data in and of itself can respond to the stimulus of disease. Schinz,
In a descriptive system for abnormal bone con- Baensch, Friedl, and Uehhnger (1951-1952:194-
ditions, there are several essential elements. These 220) provide an excellent summary of these re-
include (1) an unambiguous terminology, (2) pre- sponses, and their description has been used in
cise identification of the location and distribution the following review of bone cell reactions to
of abnormal bone, and (3) a descriptive summary disease. All abnormal conditions of bone can be
NUMBER 28 37
placed in one of the following general categories bone. The following outline can serve as a guide
reflecting bone cell activity: (1) abnormal bone to the degree of precision that should be at-
loss, (2) abnormal bone gain, (3) a combination tempted. In the discussion of particular diseases
of abnormal bone loss and abnormal bone gain, in subsequent chapters we will identify, wherever
and (4) normal quality of bone but abnormal possible, the sites in the skeleton affected prefer-
shape or contour. entially by a disease.
T h e first step in a descriptive analysis of a
pathological specimen is to determine whether A. Location of abnormal bone(s) in skeleton
the abnormality consists of (1) a solitary lesion in 1. Axial skeleton
which there is a single focus for the disease pro- a. Skull
(1) Vault
cess, (2) multiple lesions in which there is more
(2) Face
than one focus for the disease process, (3) diffuse (a) alveolar
abnormal bone in which there is no specific focus (b) nonalveolar
for the disease but a general change in bone (3) Base (including entire sphenoid and temporal
quality, and (4) a local or generalized disturbance bones)
b. Mandible
of normal size or shape in which the quality of
(1) Body
the bone tissue is normal. If the abnormality is a (a) alveolar
solitary lesion one should identify the bone in- (b) nonalveolar
volved and its position on the bone, and then (2) Ramus
describe the lesion itself However, if the abnor- (a) articular
(b) nonarticular
mality involves one of the other three categories
c. Vertebral column (except sacrum and coccyx)
the descriptive process is somewhat more compli- (1) Cervical
cated, largely because the distribution of abnor- (a) body
mal bone in the skeleton is more complex. It is (b) arch, transverse processes, and spinous
also important to remember that multiple lesions process
may not represent the same morbid process. (c) joint surfaces
(2) Thoracic
Regardless of which of the above categories is (a) body
appropriate for a specific abnormal specimen, the (b) arch, transverse processes, and spinous
location of the abnormal bone in the skeleton is process
a crucial descriptive parameter. Various disease (c) joint surfaces
processes often affect preferentially groups of (3) Lumbar
(a) body
bones, specific bones, and specific locations in (b) arch, transverse processes, and spinous
bones. Indeed, predilection, or lack of it, is an process
important aspect in itself (c) joint surfaces
Functionally the skeleton may be divided into d. Ribs
two groups of bones. T h e first group is the axial (1) Near vertebrae (proximal)
(2) Near sternum (distal)
skeleton and consists of the skull, mandible, ver- (3) Intermediate
tebral column, ribs, manubrium, and sternum. e. Sternum
The second broad group is the appendicular skel- (1) Manubrium
eton, which includes the pectoral girdle, the arms (2) Corpus
and hands, the pelvic girdle, and the legs and (3) Xiphoid process
2. Appendicular skeleton
feet. Within the bones of the axial and appendic-
a. Pectoral girdle
ular skeleton specific disease processes vary in (1) Scapula
their distribution. A descriptive analysis of an (2) Clavicle
abnormal skeleton should be specific regarding b. Arm and forearm
the bones involved and the location within the (1) Humerus
38 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
(2) Radius ify the activity of bone cells with respect to the
(3) Ulna abnormal morphology. In the chapter on the
c. H a n d
biology of skeletal tissue (p. 13) I note that bone
(1) Carpals
(2) Metacarpals cell populations can destroy bone or form bone
(3) Phalanges and may do both in fairly close proximity in some
d. Pelvic girdle disease processes. Let me review the morphologi-
(1) Innominate cal manifestations associated with each of these
(a) Ilium possibilities.
(b) Ischium
(c) Pubis Abnormal bone loss can be the result of four
(2) Sacrum types of cellular disturbances: (1) an abnormal
(3) Coccyx increase in osteoclast activity with normal osteo-
e. Thigh and leg blast activity, (2) an abnormal decrease in osteo-
(1) Femur blast activity with normal osteoclast function, (3)
(2) Patella
a combination of increased osteoclast activity and
(3) Tibia
(4) Fibula decreased osteoblast activity, and (4) normal os-
f Foot teoclast function with normal osteoblast matrix
(1) Tarsals synthesis but an inability to mineralize the ma-
(2) Metatarsals trix. Since unmineralized protein matrix will
(3) Phalanges
rarely survive in archeological material the last
B. Distribution of abnormal lesions within affected bones
1. Long bones
category will probably appear as increased osteo-
a. Longitudinal axis clast activity.
(1) Proximal joint surface Abnormal bone loss is seen macroscopically as
(2) Proximal epiphysis bone atrophy. Schinz, Baensch, Friedl, and Ueh-
(3) Proximal apophyses
linger (1951-1952:197-200) divide bone atrophy
(4) Proximal metaphysis
(5) Diaphysis
into two general categories: osteoporosis and os-
(6) Medullary teolysis. Osteoporosis involves a loss of bone in
(7) Distal metaphysis which much of the spongy bone is resorbed,
(8) Distal epiphysis leaving behind a few, sometimes thickened, tra-
(9) Distal apophyses beculae and an increased porosity of compact
(10) Distal joint surface
bone. There may be a thinning of the compact
b. Cross-sectional axis
(1) Extracortical bone as well. Osteolysis is localized bone destruc-
(2) Periosteal (Parosteal) tion, which results in a specific defect in the
(3) Cortical morphology of bone. When osteolysis occurs in a
(4) Endosteal limited area on the outer surface of bone it is
(5) Medullary
called erosion; if erosion is more extensive the
2. Skull/Mandible
a. Outer table (Outer cortex)
term "caries" is more appropriate. Osteolysis
b. Diploe (Medullary) within compact bone or marrow may result in a
c. Inner table (Inner cortex) bone cyst or cavity.
While osteoporosis will usually involve more
The above outline provides a systematic no- than one bone, osteolysis may be solitary or mul-
menclature for identifying the location of abnor- tiple, and, if multiple, it may be seen in one bone
mal bone tissue. With the spatial parameters of or several. Furthermore, the osteolytic lesions may
the disease clearly identified, the next step is a be discrete or coalescent. At this stage of the
careful description of the abnormal bone tissue discussion it is appropriate to introduce the con-
itself. Keep in mind that the objective of any cept of time in the development of an osteolytic
description of the abnormal conditions is to clar- lesion (Figure 28). If the lytic disease process is
NUMBER 28 39
FIGURE 31.Bone hypertrophy producing spicules or plates FIGURE 32.Bone hypertrophy in which the new bone has
of bone that are perpendicular to the bone surface. Specimen the appearance of cauliflower. T h e lesion is attributed to
is the right femur of a child about 7 years of age. Osteosar- osteosarcoma, but periosteal chondrosarcoma should also be
coma, Ewing's sarcoma, and metastatic neuroblastoma are considered. (Distal right femur, 31-year-old male, W M
possible morbid conditions stimulating this bony reaction. S72 a.2.)
(7-year-old child, W M S72 a.3.)
FIGURES 33, 34.Endostosis and periostosis of the midshaft of a left tibia: 33, Internal view.
T h e arrow indicates the original cortex. 34, External view of periostosis in the diaphysis; note
the porous nature of the thickened diaphysis. ( P M W H W0721.)
(bone hypertrophy) but with the compact bone in the compact bone. In general, more bone tissue
becoming quite porous (bone atrophy) and have cannot be incorporated within existing compact
periostosis, endostosis, and spongiosclerosis in the bone since the only place for such addition would
same bone. Here, I have introduced one, new, be vascular spaces. The increase in radiologic
descriptive element and that is the quality of the compact bone density is a function of new bone
compact bone. added to existing surfaces. Thus, the only abnor-
Changes in periosteal, endosteal, or cancellous mal development that can occur within previ-
areas of bone are often associated with changes ously normal, compact bone is rarefaction or
NUMBER 28 43
pearance if this cannot be determined by the X- Damage by careless excavation can easily be
ray film. The attempt should always be made to confused with antemortem trauma. Indeed, the
determine if the bone abnormality is the result of distinction between injury immediately before
abnormal osteoblast or osteoclast activity or an death and that occurring after death, including
abnormal combination of both. It is also impor- that occurring at the time of excavation, cannot
tant to indicate whether the disease process is always be made. In general, trauma will result in
accomodating some other body function, as is inflammation, within a few days, followed by
true in some cases where the development of bone remodeling, which is frequently apparent in
abnormal bone tends not to affect areas of muscle archeological specimens. Depressed fractures oc-
attachment. curring during life will generally have less sharply
In archeological skeletal material one is also defined borders than those resulting from post-
confronted with abnormal-appearing bone tissue mortem damage. There may be bone fragments
that is not the result of antemortem biological still attached at the edge of the defect. This is
processes. Such conditions have been called pseu- almost certainly indicative of an antemortem le-
dopathologies and considerable experience with sion.
pathological conditions may be necessary to make Careless handling of a shovel can remove a slab
a distinction. However, an understanding of gen- of bone from a skull, the cut surface of which will
eral principles of bone biology will help to resolve resemble a sword wound. However, with suffi-
many such problems. cient experience with pathological specimens and
Pseudopathologies are the result of postmortem the knowledge of how bone reacts to disease, the
destruction of bone tissue and result from two paleopathologist should be better able to identify
basic conditons: (1) the immediate burial envi- pseudopathology in specimens.
ronment and (2) careless excavation techniques. Assuming that paleopathological conditions
While the identification of pseudopathology as can be described and classified in most cases, the
pathology is to be guarded against, it is important information from such classifications needs to be
to remember that many pathological conditions integrated with the broader biological frame-
will result in weakened bone tissue that may work. In this context human group dynamics
deteriorate more rapidly after burial than adja- become the focus rather than individual cases of
cent normal bone. Thus, destruction of bone tis- disease. Having determined the frequency of dif-
sue by components of the soil does not always ferent types of disease in a group, such frequencies
mean that such abnormal bones represent only can be compared between groups. Inferences
pseudopathologies. about demographic or environmental effects may
The preservation of bone tissue is generally a be possible, as in Angel's research on malaria in
function of soil p H , temperature, and ground the eastern Mediterranean areas (Angel, 1964,
water volume. However, local conditions imme- 1966).
diately adjacent to a specific bone may produce In the broader paleopathological context of
marked changes in bone preservation. Copper group responses to disease, we need to be careful
containing ornaments buried with the individual in making inferences about the relative health of
will greatly enhance the preservation of bones a population on the basis of the incidence of
located next to the ornament. In contrast, bone skeletal disease. Skeletal manifestations of morbid
resting on wood, as in a wooden coffin, deterio- conditions tend to be associated with chronic
rates more rapidly than parts of the skeleton not responses to disease. Skeletal paleopathology, par-
in direct contact with wood. Earlier I have noted ticularly infections, tend to be viewed as evidence
changes at the microscopic level, produced by of high morbidity and, indeed, this may be the
fungi, which could be confused with osteoclastic case. T h e converse, however, is also possible. Skel-
activity. etal paleopathology may indicate a better host
NUMBER 28 45
response to a disease since the host lived through (6) the density of the specimen. In actual practice
the acute stage when other afflicted individuals most of the above variables are standardized,
may have died. Thus, absence of skeletal disease making the preparation of most X-ray films rou-
implies death due to acute conditions, while evi- tine. Current, energy, and time are variables that
dence of skeletal disease indicates a sufficiently are limited by the X-ray machine. In general,
adequate immune response to insure survival to varying either current or time will produce the
the chronic stage. same result. Thus, if, as is often the case, the
A final cautionary note is that skeletal diseases, current is fixed on a particular machine, time is
particularly those caused by infectious agents, adjusted to meet the requirements of different
may not be the same today as they were in exposures. The energy of the X-rays affects their
ancient times. Selection and adaptation undoubt- potential to penetrate dense materials. The
edly improve the immune response to disease. At greater the energy the greater the penetrating
the same time infectious agents tend to become potential.
less virulent since the organism typically dies with One tries to select a voltage that will penetrate
the host making reduced virulence selectively ad- the thickest or densest part of the specimen
vantageous. This means, of course, that an in- enough to expose the film somewhat, but not so
crease in the frequency of skeletal manifestations high that it is not partially absorbed by the
of disease after mutation of an existing disease thinner or less dense areas of a specimen. For
organism or the introduction of a new infectious most archeological specimens the energy used to
disease may mean only that the disease is becom- generate X-rays is between 60 and 80 kilovolts.
ing more chronic in nature and thus, is more However, if the specimen is fossilized, higher
likely to affect the skeleton. kilovoitages may be necessary. For delicate or
small bones (e.g., hands, feet, ribs, or fetal bone)
lower voltages may be needed.
X-ray Film Study of Skeletal Lesions
Radiology shares with photography many of
Analysis of X-ray films of gross pathological the problems inherent in projecting the image of
bone specimens is one of the most important tools a three dimensional object onto a two dimen-
for the paleopathologist and should be part of sional plane. Like photography, it is possible to
almost all descriptions of such material. The prep- minimize the effect of inevitable distortion by
aration of X-ray films has the advantage over keeping in mind certain principles. The first of
many other methods in being completely nonde- these is primarily inherent in the X-ray equip-
structive and thus, should always be used before ment and is a function of the area of the target
chemical or histological methods are applied. In which produces X-rays (the focal spot). X-rays
view of the importance of X-ray films in paleo- are generated from the entire surface of the focal
pathological studies I will review, in considerable spot and radiate out in a cone from each discrete
detail, the methods involved in producing good point in the spot. For illustrative purposes I have
X-ray films as well as the principles in interpret- taken the extreme edge of the focal spot, which,
ing such films after they are prepared. in effect, produces overlapping but slightly differ-
T h e correct exposure of an X-ray film depends ent images and results in reduced sharpness of the
on several factors including (1) electrical current X-ray image (Figure 36). In selecting X-ray
flow measured in milliamperes, (2) energy of equipment it is important to obtain one with a
current measured in kilovolts, (3) time of exposure small focal spot. Most manufacturers produce
usually measured in seconds, (4) the distance equipment with a focal spot of 0.5 millimeters or
between the source of X-rays and the film, (5) the smaller.
speed of the film emulsion which may be en- The effect of distortion produced by the ge-
hanced by the use of phosphorescent screens, and ometry of the focal spot can be minimized by
46 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
\^o'^-^
FIGURE 37.Variation in parallax distortion (D2) of X-ray
images due to differences in focal spot to film plane distances
(Di).
circumscribed by dense bone. In these and other centimeters. In my experience, this size will ac-
related situations one positions the specimen so commodate the largest skulls, including the man-
that these factors can best be visualized. In gen- dible, where this is desired. For the bones of the
eral one should have lateral and front views of a postcranial skeleton, film 35 X 43 centimeters is
lesion on diseased bone, so that can at least the largest standard size available from Kodak
partially reconstruct the three dimensional ap- and is satisfactory for most applications. This size
pearance of the lesion. It is important to try to film is frequently not long enough to contain an
avoid the superimposition of other parts of the entire femur on its long axis. In such a situation
bone on the diseased part if possible. In some the diagonal position may be adequate. However,
bones, such as the skull, this may be very difficult, there will be femora for which even this orienta-
but an effort should be made to minimize the tion will be inadequate. In such situations one
effect of superimposition. This can be done by eliminates the least important end or exposes two
careful positioning. films. Longer films are available commercially
There are several advantages in producing X- but create problems in processing and storage.
ray films of archeological specimens in contrast In choosing a film one needs to keep in mind
with those of a living patient. Obviously, we are the method which will be used for processing. In
not concerned with radiation hazard to a skele- most clinical laboratories. X-ray films are devel-
ton, so long exposures and film speeds are not a oped in high speed processors, which produce a
critical consideration. Furthermore, if carefully dry film in one to two minutes. Special films have
positioned and supported, the bone specimen will been created to accommodate this rapid process-
not move. In addition, there are no soft tissue ing. Such equipment has high initial and main-
features to interfere with the image of the skeletal tenance costs and will generally not be appropri-
tissue. So many of the variables of concern to the ate for the intermittent use needed by most pa-
clinical radiologist need not concern the paleo- leopathologists. It may be possible to have film
pathologist. processed by a clinical facility, but frequently the
These advantages need to be considered in more conventional and slower manual processing
selecting a film. Film speed is, in general, inversely procedures will be used. Film not adapted for
related to film resolution. Thus, the faster the high speed processing must be processed by hand.
film the poorer the quality of the image. Since However, the Kodak X-Omat G film can be
high film speed is not an advantage with paleo- processed manually or in a high speed processor.
pathological specimens, image quality and con- A decision on the method for processing should
venience of processing become important factors be made before X-ray film is purchased.
in selecting a film. In my experience I have found While film can be purchased in a light proof
Kodak Royal Blue Medical and Kodak X-Omat envelope, it is considerably more expensive than
G film, to be satisfactory. I have evaluated some film packed for loading in a film holder or cas-
slower, high resolution industrial films, such as sette. For most applications in paleopathology a
Kodak Industrex M film, and found them to simple cardboard film holder, such as the Kodak
produce excellent image quality. These should be X-ray Exposure Holder, is adequate. These hold-
considered in situations where fine detail is ers are reasonable in cost. The purchase of several
needed to bring out all the radiographic features for each of the film sizes to be used will be a
of a lesion. convenience. Film cassettes are much more ex-
X-ray film is available in many sizes. Many of pensive but last longer. Recent developments in
these sizes are appropriate to specific applications cassette design, such as the Kodak X-Omatic
in modern clinical radiology and only two are cassette make loading very simple and offer the
needed for general radiography in paleopathol- option of using phosphorescent screens to shorten
ogy. T h e most useful size for skulls is 24 X 30 exposure times. These screens are placed in close
48 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
contact with the X-ray film and are excited when anatomical position and relationships. It is fre-
exposed to X-rays. Those areas of screen that are quently possible to group the bones of the arm
excited by X-rays give off light (fluoresce), and and entire pectoral girdle (scapula and clavicle)
since the film is sensitive to both X-rays and light on a single 35 X 43 centimeter film. T h e proximal
the effect of the screen is to enhance the effect of end of the long bones should be positioned at the
the X-rays and decrease the exposure time. While top of the film, bones from the right grouped
shortened exposure times are not a crucial factor together and, likewise, for bones from the left
in paleopathology, they do have two advantages: side.
(1) they lessen the effect of vibration on the X- The vertebrae pose special problems for the
ray image, and (2) they lessen the risk of exposure paleoradiologist because of their irregular shape.
to X-rays for persons exposing the X-ray film. One solution is to obtain some soft, flexible, poly-
Recently, I have begun the routine use of the urethane foam and cut it into strips about 2 X 2
Kodak X-Omatic cassette with fine, intensifying X 35 centimeters long. After assembling the ver-
screens. There is a slight loss of resolution when tebrae in their correct anatomical relationship the
these screens are used. However, the contrast may foam can be threaded through the neural canal
be enhanced and the overall X-ray film appear- of the individual vertebrae. The vertebrae can be
ance of a lesion may be as good, or better, than adjusted by sliding or twisting on the foam to
the same film exposed without a screen. achieve correct anatomical relationship. The
Basically, two types of situations exist in the foam will hold the vertebrae in the correct rela-
radiology of paleopathological specimens. In the tionship and will have negligible effect on the X-
first of these we may have some external evidence ray image. Since a complete vertebral column is
of disease and want to clarify the nature of the usually too long for a single 35 X 43 centimeter
lesion or see if there is any additional evidence of film, I divide the vertebrae into anatomical
disease not apparent externally. To accomplish groups: cervical, thoracic, and lumbar vertebrae.
the latter objective we will need X-ray films of In the standard radiography of all bones it is
the bones of the entire skeleton. A second objec- important to orient the bones in the anteropos-
tive of radiology in paleopathology would be to terior (A-P) axis or mediolateral (M-L) axis. To
conduct a general survey of nonspecific bone facilitate this, it is very helpful to have several
responses to disease (such as Harris' lines) in an wedge-shaped pieces of polyurethane foam. For
archeological skeletal sample. In both these ap- most purposes these need not be large, the longest
plications it is important to prepare a standard edge being about 5-8 centimeters long. A few
set of films for the entire skeleton with views that pieces two or three times this size are useful for
can be compared with X-ray films of normal skull radiography.
skeletons. T h e skull poses the most difficult problems in
In doing this, attention to a few details will the radiography of skeletal material. Because of
make comparison and interpretation much sim- the globular nature of the bone, it is impossible
pler. It is very important to include some type of to avoid superimposition of images of one part of
identification number (museum catalog number the skull on other parts. For this reason the
or field number) on the film and to indicate from positioning of the skull is more critical than that
which side of the skeleton the bones are taken. of other bones and should be done carefully. In a
Lead letters and numbers are available from complete skull, the most useful landmarks for
distributors of X-ray supplies and should be part orienting the skull are the mastoid processes. In
of an X-ray facility. If they are not available, a lateral view the tips of the mastoid processes
process each film separately and write the infor- should be perpendicular to the film plane (Figure
mation on the film when processed and dry. 38). In an anteroposterior view the tips of the
Common sense dictates that the orientation of mastoid processes should be parallel to the film
the bones conform as much as possible to the plane (Figure 39). The skull should be rotated on
NUMBER 28 49
first English edition of Roentgen-Diagnostics ing and storage. A detailed review of these pro-
(Schinz, Baensch, Friedl, and Uehlinger 1951- cedures is available from X-ray film suppliers
1952:3-72) and the first chapter in Anatomy Basic (e.g., Eastman Kodak publication, Radiography in
to Radiology (Meschan, 1975:1-23) are excellent Modern Industry, 1969).
examples of such sources. In my brief discussion of film selection I have
After exposure of the X-ray film, it must be already noted that a decision regarding automatic
processed to make the image visible. The princi- versus hand processing needs to be made before
ples involved are very similar to processing pho- the purchase of film. Using the automatic pro-
tographic film and involve immersing the film in cessing facility of a local clinical X-ray laboratory
(1) a developer solution that darkens the exposed is a great convenience and saves a considerable
silver halide crystals on the film and (2) a fixing amount of time. For most paleopathologists the
solution that removes the unexposed crystals (Fig- number of X-ray films processed simply does not
ure 40). The film must be washed to remove the justify the establishment of a special laboratory,
processing solutions and then dried before view- and arrangements to take and process films
should be made with a clinical facility. Often this
will be done as a professional courtesy, but even
if charges are made for this service it is probably
very much cheaper than establishing one's own
laboratory.
In the event that the volume of X-ray film
DEVELOPER preparation justifies the establishment of an X-
ray laboratory the major expenses will be (1) the
construction of a special room to protect the
WASH technical staff from radiation during exposure,
(2) the purchase of an X-ray machine, (3) the
(C ONSTANT TEMPERATUR E
construction of a dark room, and (4) the purchase
BATH) of film processing tanks. Many educational or
research institutions have regulations regarding
FIXER the safety of such a facility, and the official
responsible for implementing these regulations
should be consulted in the planning stage. The
operator of X-ray generating equipment must
minimize personal exposure to X-rays and insure
that others in the vicinity are protected as well.
FINAL Given the existence of an adequate facility for
preparing X-ray films, one should consult stan-
WASH dard sources for the specific details on taking and
processing such films. I have already indicated
the approximate parameters for exposing X-ray
film. H a n d processing the exposed film involves
FIGURE 40.The processing sequence in the preparation of attention to the processing specifications that are
X-ray films. T h e first solution is developer, which darkens appropriate for a given film. T h e most critical
the silver halide crystals in the exposed portions of the film
emulsion. T h e developed film is washed for about two
stage in processing is development, where time
minutes before immersion in the fixer solution, which re- and temperature are the most important factors.
moves the unexposed silver halide crystals. A final wash In general, the temperature of the developer
removes all the processing solutions. should be between 60 and 75F. Exceeding this
NUMBER 28 51
temperature range on either end will result in standard X-ray envelopes, available through any
poor image quality and should be avoided. In X-ray supply dealer. These envelopes have special
view of the importance of temperature the pro- areas for recording the specimen number and
cessing tanks should be in a water bath in which additional information that cannot be put on the
the temperature can be controlled. Cold tap wa- film itself X-ray films are much more useful
ter can be mixed with hot water to produce the when this information is part of the record. Con-
optimum temperature by using a temperature siderable care should be taken in handling the
control valve. This valve is generally part of a dry X-ray film. The image is part of a thin
commercial hand processing tank system. Unfor- emulsion and is easily scratched. As with any
tunately, tap water temperature during the sum- photographic film. X-ray film should be handled
mer months may exceed the upper limit for de- by the edges both before and after processing. As
velopment. If you anticipate processing film dur- the number of X-ray films accumulate, a wise
ing such periods you will need to install a water investment is a film storage file that will keep the
cooling system as part of a processing system. films in order and make them more accessible.
Such equipment should be compatible with the
water flow through the tank and can generally
be purchased as part of the system. The temper-
Chemical Analysis of Pathological Bone
ature of the fixative is less critical, but since both
developing and fixing tanks are usually in the In modern medical practice, tests of biological
same water bath, correct temperature for the functions and products have become a routine
developer automatically results in appropriate part of diagnostic procedures. However, most of
temperature for the fixer. Films such as Kodak these tests utilize materials, such as blood or
X-Omat G are adapted for high temperature urine, which are not available in archeological
automatic processing and have greater tempera- material. Diseases that affect protein synthesis,
ture latitude when hand processed. such as osteogenesis imperfecta, may result in
In hand processing, the exposed film is at- abnormal bone proteins. Eastoe, Martens, and
tached to special, stainless steel wire, developing Thomas (1973) have determined the amino acids
frames and immersed in the developing tank. A in biopsy specimens from recent cases of this
typical developing tank contains 5 gallons of disease and found a relative increase in the neu-
reagent and can develop 5 X-ray films at one tral amino acids compared to normal bone pro-
time. Practical experience has shown that the risk tein. In research conducted in my laboratory
of scratching the film surface greatly increases if (unpublished), I have found abnormal amino
this number is exceeded. It is also important not acid residues in a rare bone disease, known as
to process different sizes of film at the same time. fibrogenesis imperfecta ossium.
T h e almost inevitable result is scratches on some In archeological skeletons the application of
of the film surfaces. After development for the chemistry in the diagnosis of disease is very lim-
appropriate time (usually about 5 minutes) the ited but should not be overlooked where appro-
film is washed for about 2 minutes. The film is priate. Such analyses will be limited to situations
then immersed in the fixer solution for about 5 where bone preservation is very good, since deg-
minutes, then washed for 30 to 45 minutes in radation of bone protein by the soil introduces an
running water and hung up to dry. Most X-ray uncontrolled variable making interpretation of
films are made to be insensitive to a fairly bright data difficult, if not impossible. Von Endt and
amber light so that the work in the dark room is Ortner (1977) have applied amino acid analysis
done in relatively light conditions. However, safe- of bone to a suspected case of iron deficiency
light specifications should be followed carefully. anemia in a prehistoric child's skeleton from the
Once the film is dry, it should be stored in American Southwest. In this study, samples from
52 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
two prehistoric skeletons were analyzed. One Microscopic Study of Skeletal Lesions
specimen (NMNH 308697) had no evidence of
disease affecting the skeleton. The other specimen Microscopic study of bone, like chemical anal-
(NMNH 327107) had marked, gross, porotic hy- ysis, is limited in its application. As a general rule,
perostosis of the skull and in the postcranial in archeological skeletal material, microscopic
skeleton, thinned compact bone and expanded data add little to what can be seen grossly or on
marrow spaces. This combination of lesions is X-ray films. Because microscopic examination
strongly suggestive of anemia. The amino acid does involve destruction of some of the bone, it
residues from the abnormal skeleton were differ- should only be applied when diagnosis is likely to
ent from the normal skeleton and from bone of a be aided. It should not be considered a routine
modern child. These results are discussed in procedure.
greater detail in the chapter on reticuloendothe- If, after careful analysis of gross and X-ray film
lial and hemopoietic disorders (p. 248) and sug- data, it seems likely that microscopic data would
gest the potential for the study of protein chem- be valuable, several factors need to be considered.
istry in archeological specimens. The first step in any analysis is the removal of a
The mineral phase of bone may also be affected sample of the abnormal bone. Every effort should
by disease. In rickets, the protein matrix does not be made to minimize the amount of tissue taken
mineralize. In fluorosis, abnormally high levels of for microscopic study. Very thin, dental saw-
fluorine can result in gross and microscopically blades are available, which destroy only a minute
abnormal bone. It may also increase the concen- amount of bone in the cutting process. Further-
tration of fluorine in bone mineral. I have used more, there is usually no need to remove a sample
the electron probe microanalyzer to investigate more than Vi centimeter thick since the sample
the toxic effects of fluorine on bone (unpublished will usually be reduced to a thinness that will
data). This research demonstrated almost twice permit transmission of light.
the normal concentration of fluorine in affected In removing a specimen of tissue for micro-
bone mineral. Analysis of strontium levels in bone scopic analysis, include in the section some of the
have been used in dietary studies of archeological normal bone adjacent to the morbid tissue and
specimens (Schoeninger, 1979). Strontium levels enough of the abnormal tissue to insure that
in bone are lower with greater emphasis on meat different aspects of the pathological process will
in the diet and higher if plant sources account for be included. For example in some disease proc-
more of the caloric intake. esses the edge of a lesion may reveal bone resorp-
While chemical analysis of archeological skel- tion while the more central part of the lesion may
etons may provide valuable data on a disease show bone formation. A clear understanding of
condition, considerable caution is needed in in- the lesion requires that tissue from both areas be
terpreting such an analysis. The process involves examined.
at least a small amount of destruction of valuable Once an appropriate thin slab of bone has been
bone. Furthermore, one must insure that data removed for study it can be viewed in reflected or
from chemical analysis reflect conditions during incident light using either a dissecting microscope
the life of the individual and not one or more or incident light optics on a research microscope.
variable changes of bone in the soil. Data ob- However, one of the cut surfaces of the specimen
tained by comparison of normal and abnormal should be prepared to insure reasonable resolu-
tissue from the same site may not be reliable, tion. On most cut surfaces, microscopic detail is
since soil conditions may vary within a cemetery obscured by the irregular groves from the cutting
site. Indeed, a complete understanding of the action. If the bone is fragile it should first be
chemical composition of normal and abnormal infiltrated with or imbedded in some plastic ma-
modern bone tissue remains an unachieved goal. terial before cutting to strengthen it. Ubelaker
NUMBER 28 53
(1978:99-101) provides a brief review of this pro- laboratories doing such work would be appropri-
cedure. ate.
After strengthening, one surface can be ground Having obtained a bone section and perhaps a
on fine, water-resistant, carborundum paper to microradiograph, the next step is to evaluate the
remove the rough scratches. It can then be pol- findings. One should be familiar with the micro-
ished slightly by rubbing the surface on good scopic appearance of normal bone at different
quality bond paper. Repeated microscopic in- ages, for it is against this background that an
spection during processing will indicate when understanding of the abnormal condition must
grinding and polishing is adequate but the order be obtained. Given this background there are
of magnitude is a few minutes. several aspects of disease that should be consid-
In most cases a bone section (75-100 microns) ered. However, with the exception of slight
is the most satisfactory preparation for micro- changes produced by osteocytes, all the abnormal
scopic study. Elaborate equipment and proce- changes seen in bone microstructure are the result
dures exist for making such preparations (e.g., of abnormal osteoclastic or osteoblastic activity.
Jowsey 1955; Moreland, 1968; Ortner and Yong, Microscopically, one can, in theory, see de-
1975); however, a few inexpensive supplies will creased, normal, or increased osteoblast activity
make it possible to produce a satisfactory thin in combination with either decreased, normal, or
section in most cases (Frost, 1958). increased osteoclast activity. Within a single le-
In general the preparation is an extension of sion there may be one or more combinations of
the procedure for polishing a single surface except cell activity, and multiple lesions may vary in
that the grinding stage continues until the speci- their expression.
men is very thin (about 100 microns) before the In compact bone, disease is expressed as an
polishing begins. Usually it is important to grind abnormal quantity of resorption spaces and/or
both cut surfaces and polish at least one surface, forming osteons. The latter can be identified by
although the latter may not be needed if the the presence of osteoid seams or, if these are
section is mounted on a glass slide and cover- missing in archeological bone, as low density
slipped. If the specimen is large (2 cm or more) it osteons (in a microradiograph) with large central,
may be difficult to grind the surface uniformly. or Haversian, canals. Let me illustrate these prin-
Mounting one ground and polished surface on ciples with a few concrete examples. I have al-
the glass slide and then grinding down the free ready noted that Paget's disease involves an in-
surface to the appropriate thinness may help, but crease in the activity of both osteoclasts and
specially designed cutting and grinding equip- osteoblasts with an increase in the internal or
ment will produce the best results. Such equip- osteon remodeling of compact bone. This results
ment is available at many universities in the in a microscopic appearance of many resorption
departments of geology or mineral sciences. spaces and many forming osteons and many os-
Additional data may be obtained from a con- teon fragments. In hyperparathyroidism, there is
tact microradiograph of a bone section. Tech- a marked increase in osteoclast activity but little
niques for preparation of microradiographs are or no effect on osteoblasts. Here the microscopic
well-known (Amprino and Engstrom, 1952; Sis- picture is one of abnormal resorption occurring
sons, Jowsey, and Stewart, 1960; Ortner, 1975). within existing bone. In compact bone there is a
In essence the technique involves placing a bone dramatic increase in the number of resorption
section on a high resolution X-ray film or plate spaces. The trabeculae of spongy bone will fre-
and exposing the plate to low energy (10-15 Kv quently be tunneled out by osteoclastic activity.
primary voltage) X-rays for a relatively long time This contrasts with severe osteoporosis, in which
(up to iy2 hours). Special equipment is necessary there is increased osteoclastic activity and/or pos-
for this, and consultation with one of several sibly decreased osteoblastic activity in which the
54 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
overall cortex becomes thinned (involution) in There is an additional problem to keep in mind
addition to the increase in resorption spaces. in archeological specimens. Microorganisms in
Another aspect of the overall bone cell response the soil have the ability to cause local destructions
to disease is the speed of the activity, particularly of bone and may give at least a superficial ap-
pearance of osteoclastic activity (Hamperl, 1966:
with respect to bone formation. If the process
82-83). Marchiafava, Bunocci, and Ascenzi
driving osteoblasts to produce bone is very rapid,
(1974) report that fungi are one type of organism
the result will be poorly organized fiber bone
responsible for such activity. In general the spaces
rather than lamellar bone. Such bone will also produced by destruction of bone microorganisms
tend to be poorly mineralized, a feature that are much smaller than those produced by osteo-
would be apparent in a microradiograph. clasts.
Trauma
55
56 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 44, 45.Healed fracture of the twelfth thoracic vertebra (second vertebra from the
top): 44, Lateral view. The vertebral body has collapsed because of compression; however, the
spinous process has separated from tension produced during the compression of the anterior
portion of the body; the fracture resulted in angular deformity. 45, Anterior view. (24-year-old
male, F P A M 5085.)
direction of the force. In long bones excessive Because the stress occurs in a spiral direction the
compression may produce a fracture in which the fracture line also spirals. Torsion fractures can be
cortex buckles and bulges outward. Pure com- confused with compression fractures in long
pression fractures are best illustrated in the spine bones, which follow a natural spiral cleavage
where most fractures of the vertebral body are plane in the bone. Torsion fractures always in-
the result of compression (Figures 43-46). One volve abnormal rotation of the bone.
also sees compression fractures resulting from a Bending fractures are the most common type
blow to the skull (Figures 47, 48). Many of the of bone separation and are often complicated by
fractures of joint surfaces are the result of com- other types of stress. Abnormal stress can result
pression. when the bone is bent as the result of a fall or in
In torsion fractures the force is directed in a response to a blow, as in the "parrying" fractures
spiral or twisting direction as when one end of a of the forearm. In either case the maximum stress
limb is fixed and the other rotates. In modern often occurs at a discrete spot in the bone and
times this type of fracture is frequently associated may result in a simple transverse separation of
with skiing accidents, in which the lower leg is the bone. The force can also radiate from the
rigidly fixed and the body twists during a fall. impact point in a conical shape with the fracture
58 SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
fracture in which the distal end of the radius is populations unusual and continued stress over a
sheared off and displaced backward. Schinz, period of weeks may result in a fatigue fracture.
Baensch, Friedl, and Uehlinger (1951-1952:276) In fatigue fractures the stress applied to bone does
note that in Colles' fracture the shearing stress not immediately result in fracture. In all cases
rapidly changes to bending stress, and it may be such fractures are associated with the onset of
impossible to distinguish the effects of the two intense physical activity of a type not engaged in
types of stress in the resulting fracture. previously. Fatigue fractures are often seen in
A fracture varies not only in terms of the type military recruits during their initial training pe-
of stress but also with respect to its severity, which riod (Schinz, Baensch, Friedl, and Uehlinger
is related to the extent of the fracture. A simple 1951-1952:285). In fatigue fracture of the tibia,
fracture is one in which there is only one separa- for example, the predilected site is the proximal,
tion of the bone. This contrasts with a more severe medial metaphysis, particularly in the region of
fracture with many broken fragments, which is active cutback, where cancellous support is poor.
called a comminuted fracture. In either of these Such fractures are often incomplete, involving
types of fracture the traumatic event may result only a portion of the cross-sectional plane of a
in the broken bone being exposed through the bone. They are also associated with unosteonized
skin. This is called a compound fracture and can circumferential lamellar bone (Johnson, 1964:
greatly complicate healing because of the possi- 607). The physical activity triggers an attempt by
bility of infection (Collins, 1966:50). the bone to increase its mechanical strength by
While fractures brought about by sudden over- osteon remodeling. However, the first step in
whelming stress are the most frequent of trau-
matic problems, other types of fracture occur in
which other patterns of stress or pathological
conditions are contributing factors. In modern
FIGURE 49.Schematic representation of bending fracture FIGURE 50.Schematic representation of bending fracture,
a n d the triangular fragment that may occur in such frac- which produces ix green stick separation of part of a bone.
tures. Both transverse and longitudinal breakage may occur.
60 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
TABLE 1.Distribution and types of fractures in cases pathology in part because of these cultural vari-
reported by Hamilton (1853:33) ations and the inferences that can be made re-
garding the characteristic hazards encountered
Total by different groups.
Bone(s) affected Compound & Com- Sim- no. of
comminuted pourul ple cases
Nose and face 6 6 12 24
Fracture Healing
Clavicle 0 4 37 41
The process of fracture healing in some respects
Scapula 0 0 3 3
Humerus 2 1 36 39 recapitulates events associated with growth.
Radius 0 2 25 27 There are, however, significant differences in
Ulna 0 2 20 22 which the conditions associated with the fracture
Radius and ulna 0 2 31 33 event itself are significant. Traumatic, fatigue,
Femur 3 1 67 71 and pathological fractures will also vary in the
Patella 0 0 7 7
healing process. In the following review of frac-
Tibia 0 6 13 19
Fibula 1 4 11 16 ture healing the major emphasis is on the biology
Tibia and fibula 13 19 40 72 of traumatic fracture repair.
Bones of the hand 1 2 2 5 Several events occur with the fracture of a
Ribs 0 0 4 4 bone. Blood vessels are ruptured both in the
Vertebral column 0 0 3 3
cortex (in Haversian canals) and also in the per-
Pelvis 0 0 1 1
Total number 26 49 312 387 iosteum and marrow. Blood vessels in overlying
of cases muscle may also be torn. With the rupture of the
blood vessels, blood flows into the fracture region
plasms. Collins also reports that pathological frac- forming a hematoma, which coagulates. There is
tures from different diseases are associated with some debate regarding the value of the hematoma
rather specific age categories. To this list should in the healing process. Collins (1966:50) suggests
be added aging, which is generally associated that the clot interferes with healing. More recent
with gradual bone loss and which can contribute research (Schenk, 1973:xv) suggests that hema-
to pathological fracture (Schinz, Baensch, Friedl, toma is not essential to fracture healing and
and Uehlinger, 1951-1952:256). indirectly supports Collins' opinion. Regardless
Previous studies have shown that the location of its value in fracture repair a hematoma is an
of fractures in the skeleton varies with the age almost inevitable result of fracture. The broken
and sex of the individual (e.g., Buhr and Cooke, ends of the blood vessels contract and the open
1959). Furthermore, there are differences in the ends are sealed by clotted blood. However, the
frequencies of fracture in various locations in the traumatic event stimulates an inflammatory re-
skeleton (Table 1), which may be associated with action in which intact blood vessels and the un-
cultural differences (Hamilton, 1853; Schinz, damaged portions of broken vessels dilate and
release a plasma exudate, which adds to the fluid
Baensch, Friedl, and Uehlinger, 1951-1952:249;
at the fracture site (Collins, 1966:44).
De Souza, 1973; Iqbal, 1974). It is apparent that
different cultural and environmental conditions The periosteum will usually be broken during
create different fracture hazards. The potential fracture, although this is not inevitable, particu-
fracture hazard of someone negotiating an icy larly in young individuals. The stress that breaks
sidewalk is quite different from a person living in the periosteum also tends to strip it from the
the tropics. Similarly, the fracture hazard of the surface of the bone for a few millimeters adjacent
ancient hunter is likely to be different from that to the fracture site. This appears to activate the
of the ancient city dweller. Differences in fracture bone-forming potential of the osteogenic layer in
pattern have considerable significance for paleo- the periosteum and initiates the formation of
62 SMITHSONIAIN CONTRIBUTIONS TO ANTHROPOLOGY
callus (Schinz, Baensch, Friedl, and Uehlinger, age. This bone will ultimately have to be removed
1951-1952:378). and replaced.
Breakage of the blood vessels at the fracture In classic fracture healing, the formation of a
site also results in the death of tissue and cells blood clot is followed by the second step in frac-
including the osteocytes supplied by such vessels ture repair, in which the blood clot is permeated
and any bone fragments resulting from the break- by fibrous connective (granulation) tissue. Collins
FIGURES 53, 54.Healed fracture with slight angulation in an adult right femur: 53, Anterior
view, arrow indicates callus. 54, Posterior view. (IPAZ 1780/62.)
NUMBER 28 63
(1966:50) notes that the hematoma, if not exten- It is important to remember that bone forma-
sive, can assist in initial union by providing a tion requires an adequate blood supply. Intense
matrix for the advance of granulation tissue. vascular proliferation begins with the formation
However, granulation tissue can penetrate he- of granulation tissue and is associated with callus
matoma only to a limited depth; thus, extensive formation. The blood vessels supplying the for-
hematoma between broken ends seems to delay mation of callus also create conditions in which
the healing process. resorption of bone fragments and dead bone ends
Schinz, Baensch, Friedl, and Uehlinger (1951- at the fracture site can occur.
1952:378) indicate that the fibrous callus that The fifth stage in fracture healing involves the
unites the ends of the fragments is derived from conversion of the fiber bone callus to lamellar
the granulation tissue. This fibrous union of the bone. This includes the apposition of lamellar
broken ends is the third stage of fracture healing. bone to existing fiber bone surfaces, the removal
While the fibrous callus is unmineralized, it pro- of fiber bone by osteoclasts, and internal osteon
vides the matrix for the formation of fiber bone remodeling. The result is a much stronger union
and the primary bony callus, which is the fourth of the broken ends. This in turn means that less
stage in fracture healing. As I have indicated bone is needed for optimal mechanical strength.
previously (p. 11), fiber bone is associated with In the final, sixth stage of fracture healing the
rapid bone formation. In normal conditions it callus is reduced to a minimum (Figures 53, 54).
occurs only during the growth phase. Fiber bone If the orientation of the broken ends is good, the
is a temporary tissue, replaced by lamellar bone, callus may no longer be apparent. If angulation
which has much greater mechanical strength. has occurred there is compensatory remodeling
Collins (1966:47) notes that primary callus for- (Figure 55).
mation generally begins about one week after The time for fracture healing varies based on
fracture in human bone. Initially, primary callus several variables including (1) the bone involved,
consists of coarse, fibrillar trabeculae within the (2) the severity of the fracture, (3) the apposition
fibrous callus. Primary callus is associated with of the ends, (4) the stability of the fractured ends,
different areas of the fracture site and three basic (5) the nutritional state of the individual, and (6)
types have been defined for conceptual purposes the age of the individual. Collins (1966:52) indi-
(Schinz, Baensch, Friedl, and Uehlinger, 1951- cates that in a typical bone under ideal conditions
1952:378). The intermediate or sealing callus the primary callus takes about six weeks to de-
joins the broken ends of the bone. The endosteal velop. The secondary callus becomes significant
callus unites the opened marrow spaces forming after this time but bony union and return of
a plug between the two ends, while the periosteal adequate function is too variable to predict.
or bridging callus arches over the fracture site. Cruess and Dumont (1975:97), rather than
The bridging callus provides the externally visible assigning a specific timetable, indicate the ap-
evidence of healed fracture in an archeological proximate percentage of the total healing time
specimen. One other component of primary callus spent in the three major phases of fracture heal-
is the occasional occurrence of cartilage in the ing. These phases include the inflammatory phase
region of the callus. Collins (1966:48) expresses (10 percent), the reparative phase (40 percent)
the opinion that cartilage is incidental to the and, the remodeling phase (70 percent). The
overall process of fracture healing. In support of phases do not total 100 percent because of the
this conclusion, he cites the work of Ham (1930), overlap in time between the phases. In any case
who suggested that cartilage formation is associ- the time of reduced mechanical function is cer-
ated with poor vascular supply. Aegerter and tainly a matter of weeks even in an ideal situation.
Kirkpatrick (1975:237) challenge this concept but The significance of this period of reduced ac-
offer no alternative. tivity is difficult to assess. Schultz (1939:978)
64 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
period, in which the estimated mortality from be exuberant bony response to unrelieved trauma
open fractures in German hospitals was 40 to the joint (Figures 56, 57).
percent. T h e data reported in Table 1 indicate In some cases the distribution of dynamic forces
that compound fractures (compound-commi- immediately after trauma may not break the
nuted and compound only) occur in about 19 bone but will disrupt the blood supply, lead to
percent of all fracture cases. ischemia, and may result in tissue necrosis. Three
Another complication of local infection at the such cases may be seen in the Hunterian Collec-
fracture site is disruption of the blood supply to tion in London (Figures 58-60). All three cases
bone leading to death of the tissue (necrosis). At are attributed to a blow on the head. If the blood
the boundaries of the dead tissue osteoclasts may supply in the immediate region of the blow is
isolate the dead bone through osteoclastic resorp- disrupted, the tissue becomes ischemic or necrotic,
tion. Such an isolated segment of dead bone is and there is an inflammatory response adjacent
known as a sequestrum. Often, if the blood supply to the affected bone.
to the bone itself is cut off, the periosteum remains Traumatic interruption of blood supply in a
intact and produces a new sheath of bone called growing bone can produce abnormal shortening
involucrum around the necrotic tissue. A more of bone. The growth plate in such bones is partic-
detailed review of infection in bone is presented ularly vulnerable to trauma because of the rela-
in the chapter on infectious diseases (p. 104). tive weakness of calcified cartilage. Trauma to
With respect to fracture the significant point is the ends of growing bone cannot only break the
that infection, certainly in pre-antibiotic times, is cortex but, also, can shear the epiphysis (Schinz,
a most serious complication, having a significant Baensch, Friedl, and Uehlinger, 1951-1952:422).
risk of mortality. However, in archeological skel- In both cases, the blood supply is disrupted and
etons it will require very careful and observant growth is retarded. Such injuries to the epiphysis
excavation technique to distinguish an unhealed may also result in premature fusion of the growth
fracture resulting in or associated with death from plate. The result of any of these complications is
that of postmortem damage from soil movement a shortened bone. If only one of the two bones of
or careless excavation. the forearm or lower leg is involved, abnormal
I have already noted that rupture of some angulation of the hand or foot ensues. If both the
blood vessels is an inevitable result of all fractures radius and ulna or the tibia and fibula are af-
(p. 61). Damage to major blood vessels and nerves fected the entire forearm or lower leg will be
is not inevitable because of the flexible and rela- shortened. Similarly, fracture at the growth zone
tively tough nature of these structures. Hazard to of other long bones can produce reduced length
major blood vessels and nerves is greatest in of the bone.
crushing injuries resulting in fracture. However, Serious disruption of nervous supply to other
even in simple fractures, the displacement of bone parts of the body may be associated with fracture
ends can compress or twist blood vessels or nerves of the vertebral column, depending on the verte-
(Bohler, 1935:73) and lead to ischemia and loss brae involved, since either the spinal cord or
of nervous stimulation. Loss of blood supply will spinal nerves can be affected. Bohler (1935:109-
lead to delayed fracture healing and, if uncor- 145) reviews these fractures and their complica-
rected, can result in bone necrosis. Loss of nerve tions. The most serious complication occurs in
supply does not appear to be as serious. However, complete severance of the spinal cord. The per-
if sensory nerve supply is lost to the fracture site, manent paralysis below the level of the injury,
the lack of pain may allow continued use of the which inevitably results, affects various parts of
broken bone and prevent healing or, in the case the body depending on where the break occurs.
of a fracture of an articular surface, lead to a The comminuted fragments can put pressure
neuropathic or Charcot joint, in which there will on the spinal cord or spinal nerves producing
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
66
^^H^^^3| '^1
^^H^p-v. ^^i^P,,^^H
^^^^B9v ~ '^ ^A^^^^^^^^H
FIGURES 56, 57.Charcot joint resulting from traumatic fracture of the left femoral neck: 56,
Anterior view of innominate and femur; note the large mass of bone over the acetabulum
creating a new joint, which comes in contact with the greater trochanter. 57, Inferior-lateral
view. (ANM 2243.)
paralysis, which probably will not heal sponta- or incomplete. This condition is almost always
neously. Since medical procedures are not likely the result of inadequate immobilization of the
to have been available in archeological popula- fracture during the healing phase. Two compli-
tions, evidence of a partially occluded neural cations can arise. In the first of these there is
canal above the second lumbar vertebra should inadequate mineralization of the callus allowing
be suggestive of paralysis. Evidence of this should the fractured ends continued movement. Such a
be sought in the limbs likely to have been affected condition is called pseudarthrosis. T h e second
(e.g., Figure 46). In general, paralysis prevents condition is called nearthrosis and differs from
effective use of the paralyzed limb and will result pseudarthrosis in that an actual joint space is
in bone atrophy (p. 325). formed (Schinz, Baensch, Friedl, and Uehlinger,
A less serious result of spinal fracture is a blood 1951-1952:425-430). In the American literature
clot or callus producing pressure on the spinal both these terms are frequently used synony-
cord or nerve root. The blood clot will disappear mously and with the term "nonunion." However,
in time if the individual is kept quiet and the each condition produces a slightly different result
callus may be partially remodeled away after the in bone and thus, should have distinguishing
break is healed. Dysfunction in the form of pa- terms.
ralysis in such cases may be temporary. T h e factors that produce nonunion remain
In some fractures the healing process is delayed somewhat obscure. Schinz, Baensch, Friedl, and
NUMBER 28 67
FIGURE 58.Central bone necrosis surrounded by a zone of FIGURE 59.A large area of bone necrosis (arrows) sur-
hypervascularity (arrows) following a blow to the head. rounded by a zone of hypervascularity following a blow to
(Portion of the left frontal bone, H M P626.) the head. (Frontal bone, H M P627.)
FIGURES 61, 62.Healed diagonal fracture of the distal, left femur with marked mediolateral
and longitudinal displacement of the broken ends: 61, Medial view. 62, Posterior view. T h e
displaced ends are joined by abundant callus. There has been considerable cortical remodeling
of the broken ends, which have been sealed off with compact bone. ( W M S32.7.)
of the limb. However, in the case of the forearm misalignment is high. In modern clinical practice
or lower leg, nonunion in one bone may be com- initial management of fracture involves minimiz-
pensated by extensive hyperplasia of the other ing muscle contraction and careful realignment
bone and adequate function can result (Schinz, of the broken ends so that the bone approximates,
Baensch, Friedl, and Uehlinger, 1951-1952:428). as near as possible, its original shape.
Problems in mechanical function can also be Even when this procedure is attempted, how-
caused by misalignment of the broken ends. Two ever, misalignment can occur as is illustrated in
factors contribute to this. The stress producing a modern case (Figure 55). T h e effects of poor
the fracture may produce misalignment. At least alignment vary with the bone involved and the
equally significant, however, is the fact that the severity of the fracture. Rarely, if ever, does it
sensory stimuli triggered by the fracture produce produce a direct threat to life. However, it can
a virtually instantaneous and powerful contrac- lead to premature and severe degeneration of a
tion of the muscles in the fracture area. Subse- joint because of the abnormal stress on the joint
quent movement of the limb will repeat this brought about by misalignment. In the long
stimulus if pain results (Bohler, 1935:58-59). bones this can result in reduced locomotion and
With such muscle contraction the likelihood of manipulative ability. Misalignment of a vertebral
NUMBER 28 69
fracture can result in varying degrees of angula- ment of spine, perhaps associated with angula-
tion in the spine since the vertebrae are all closely tion, resulting in little overall loss of spinal move-
linked to each other in mechanical function. ment. Fusion of fractured joints can easily be
Fracture can, directly or indirectly, produce confused with fusion following infection of the
premature osteoarthritic degeneration of joints. If joint (p. 113). In some cases a distinction may not
the joint surface is broken, the cartilage and be possible; however, traumatic fusion may retain
subchondral bone are disrupted. Because of the evidence of the fracture line.
absence of blood supply, the repair of cartilage The treatment of many fractures can be accom-
depends on nutrients from the joint capsule, and plished on the basis of intuitive knowledge and
any repair is a slow process. A break of the common sense. The frequent occurrence of well-
subchondral plate will usually result in perma- healed fractures in archeological skeletons testifies
nent discontinuity of the bony joint surface. This eloquently to this fact. Bohler (1935:566) lists
complicates the healing process of the articular three fundamental laws for fracture treatment.
cartilage, since it results in poor contact between They are (1) reposition and realignment of the
the gliding surfaces of the joint. This creates broken ends (reduction of the fracture), (2) im-
serious problems in dissipating the stress applied mobilization (fixation) of the broken bone, and
to the joint and results in premature deterioration (3) maintenance of circulation and muscle tone
of the articular cartilage. through careful exercise of the affected limb.
T h e fracture need not involve the joint itself to Obviously, in comminuted fractures, com-
produce premature degenerative changes in the pound fractures, or simple fractures where
joint. As I have already noted (p. 68), a change marked displacement has taken place, proper
in the axis of a long bone can shift the major reduction and restoration may be difficult, if not
focus of mechanical stress to a portion of the joint impossible, without modern techniques, includ-
less well adapted for such stress. Similarly, abnor- ing traction and surgical intervention. However,
mal shortening of a long bone after fracture it is also apparent in archeological specimens that
(Figures 61, 62) can produce uneven locomotion, badly misaligned bones do heal and, judging
which results in unusual stress to the joint and from the lack of disuse atrophy, provide at least
premature degenerative change (Schinz, Baensch, limited use of the limb. Perhaps such fractures
Friedl, and Uehlinger, 1951-1952:430). In trying heal spontaneously with the pain associated with
to distinguish between premature degenerative movement being the immobilizing force.
change resulting from fracture and degenerative I have noted earlier (p. 61) that trauma to bone
change from aging, it is helpful to make a com- can also damage the overlying muscle. Johnson
parison with the joint of the corresponding limb. (1964:610) notes that muscle tissue can provide
Fracture of the joint surfaces can also result in cells that contribute to callus formation around
destruction and fusion of the joint. This problem the fracture site. As with bone, the trauma to
is associated with comminuted fractures of the muscle tends to produce hematoma. With time
joint where more than one joint surface is in- the hematoma is usually dissolved. Occasionally,
volved and callus formation joins two or more however, the muscle tissue will respond to the
bones. In the limbs this means loss of movement trauma by producing bone directly in the muscle
for the joint. In the vertebral column such a tissue itself, often in association with the hema-
fusion is seen in Figure 46 and is a common toma. This condition is known as traumatic myo-
sequela of compression fractures of one or more sitis ossificans. This excessive formation of bone
vertebral bodies (Bohler, 1935:142-143). In such by muscle can be entirely separate from the bone
cases, the mechanism is activation of the perios- (Figure 63) or it can become part of existing bone
teum of the body with callus formation extending tissue (Figures 64, 65). The most common areas
to adjacent vertebrae. The effect is a rigid seg- are the extensors and adductors of the thigh, the
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
70
FIGURES 66, 67.Saber wounds of the left parietal: 66, There is a large, displaced fragment on
the lateral portion of the left parietal; the wound healed with the fragment in the displaced
position leaving an opening in the skull; the second healed saber wound is seen superior to the
large defect. Only the outer table was affected. 67, Internal view. (Adult male, A N M 2069.)
Museum of Anthropology, Prague, the edges of improvement took a q u a n t u m leap forward with
the wound are well remodeled, indicating consid- the development of antibiotics, which have
erable time after the injury before death occurred greatly reduced the possibility of infection com-
due to an unrelated cause. In this specimen the plicating the traumatic event.
glancing nature of the sword wound may have These introductory comments serve to high-
prevented any damage to the brain. Another case light the importance of a reference point for the
of severe trauma to the skull is seen in a specimen paleopathology of trauma, in which modern med-
(FPAM 5719) from the Federal Pathologic-Anat- ical concepts and treatment, to a large extent, did
omy Museum in Vienna (Figure 68). This speci- not exist. It is important to add that, in the
men shows massive fracturing of the left parietal treatment of fracture, ancient populations often
and occipital bones with fracture lines radiating did a remarkably good j o b (e.g., Elliot-Smith,
from the major fracture site. T h e size of the gap 1908:734).
is suggestive of a wound from a saber or axe. T h e Fracture and the complications arising from
edges of the break are well remodeled indicating fracture most often provide the paleopathologist
a long-standing recovery. with easily interpretable lesions in archeological
Surgical intervention in pathological condi- skeletons. However, there are some problems in
tions that affect the skull or its contents is a the interpretation of this type of trauma of which
common practice today. Such a procedure carries the paleopathologist should be aware. First, evi-
with it the risk of infection and damage to the dence of healed fractures occurring in children
brain seen in traumatic injury of the skull. In can be completely obliterated by the skeletal
view of the risk, evidence of surgical treatment of remodeling that occurs with growth. Second, it is
the skull (trephination) in antiquity is a remark- difficult and often impossible to make a distinc-
able phenomenon and will be discussed as part of tion between fractures occurring at the time of
the review of the paleopathology of trauma. death and those that occur subsequent to death
and burial. Wood-Jones (1908b: 736) indicates
that in Egyptian skeletons, fractures occurring at
PALEOPATHOLOGY the time of death produced blood staining adja-
cent to the fracture site. However, such staining
History and Examples
may survive only under conditions of minimal
In the following review of fracture in archeo- rainfall and soil water content, so that this crite-
logical skeletal material I use published source rion may be of little value in most geographical
materials but emphasize skeletal specimens from areas.
the collections of the National Museum of Natu- In fracture occurring while the periosteum and
ral History, Smithsonian Institution, Washing- other soft tissues are still intact, small bone frag-
ton, D. C , USA, and my own experience and ments in the fracture site may still be adherent to
observations on paleopathology. It is important adjacent bone (Figure 69). This condition is very
to emphasize, at the outset, that the advent and helpful in distinguishing between fracture at the
expansion of civilization has not eliminated time of death and damage to the skeleton after
trauma, either of the accidental or intentional interment resulting from shifting soil or damage
type. What has happened is the introduction of during excavation. Also surfaces of bone tend to
new factors producing trauma, such as the sub- be stained a somewhat different color from bone
stitution of the automobile for the horse in trans- not in direct contact with the soil. Thus, breaks
portation, and the use of guns and bombs instead occurring during excavation or in subsequent
of clubs, axes, swords, arrows, and spears in war- processing may have a surface coloration quite
fare. distinct from surfaces in contact with the soil for
While the human species is still subject to a long period of time.
trauma, treatment has greatly improved. This A third factor of significance to the paleopath-
NUMBER 28 73
early twentieth-century. Western city popula- Anglo-Saxon England (ca. eighth century A.D.).
tions. Other comparisons indicate fewer fractures While recognizing that fracture treatment may
of the lower leg in the ancient Nubian material have been fairly sophisticated in regions of an-
in contrast with modern city dwellers. Wood- cient high civilization, it is equally apparent that
Jones attributes this difference to modern foot- many fractures, even in these areas, received little,
wear, which increases slipping and which was not if any, helpful treatment (Wood-Jones, 1910c:
worn by the Nubians (1910c: 296). Another 294). The large number of badly deformed,
marked contrast with modern populations is the healed fractures from many archeological skele-
incidence of hand fractures, which is about 10 tons testifies to this (Figures 75-77). The fact that
times greater in modern city populations. Injuries fractures heal spontaneously, allowing at least
from machinery appear to be a major factor in some continued function of the affected bone, is
this difference (Wood-Jones, 1910c:297). In the not surprising in view of the reports of healed
New World, Hooton (1930:312) found a rate of fractures in wild shot primates (Duckworth, 1912;
3.96 percent fractures of long bones or pelvis in a Schultz, 1939, 1956) where, obviously, there was
skeletal series of 503 pre- and post-Columbian no treatment.
skeletons from the Pecos site in the North Amer- Evidence on the methods for treating fractures
ican southwest. When fractures of the skull are in archeological populations is scanty. However,
added, the total percentage increases to 7.23. among primitive and peasant groups living in
Angel's findings (1974a: 13) in skeletal material historic times, there are records of fairly sophisti-
of various time periods from the Eastern Medi- cated techniques to reduce fractures (bring about
terranean suggest an inverse relationship between optimal realignment of the broken ends) and
cultural level and fracture incidence. However, immobilize the broken bone until healing can
this trend does not occur in modern populations take place (Elliot-Smith, 1908:734; Daland, 1935:
in the United States, where the fracture incidence 550). There is convincing evidence for the use of
is almost twice that of ancient Eastern Mediter- splints, pads to absorb blood in compound frac-
ranean peoples. Like Wood-Jones, Angel finds tures, and linen bandaging by the Fifth Dynasty
that the most common site of fracture is the (2730-2625 B.C.) in ancient Egypt (Elliot-Smith,
forearm, which he also attributes to an effort to 1908:732-733). Freeman (1918:445) reports that
parry a blow. This suggests that intentional vio- manipulation and splinting of fractures occurs
lence is a major causative factor of fracture in the among the indigenous peoples of North America
Eastern Mediterranean, as well as in Nubia. as well. Elliot-Smith (1908:733) notes one case
Courville (1967:621) reaches a similar conclusion where the splinting did little to stabilize the frac-
with respect to cranial injuries in antiquity, not- ture. This is not a serious indictment of their skill
ing that most wounds and fractures of the skull since, without X-ray examination and in the
are the result of "blows of malicious intent." presence of considerable pain, it could be very
Earlier (p. 69), I have indicated that the basic difficult to identify the location of the fracture.
concepts of fracture treatment do not require With or without effective reduction and immo-
sophisticated knowledge and indeed reflect com- bilization, most often the healing of fracture was
mon sense procedures. It is not surprising then to uneventful. Elliot-Smith (1908:733) notes evi-
find that immobilization of fractured bones with dence of infection in only one case out of 100
a splint was practiced at least as early as the Fifth fractures in ancient Egyptian material.
Dynasty in Egypt (Elliot-Smith, 1908). Although Injuries to the skull are rather common in
much later in time, there is evidence of similar archeological specimens. One type of skull injury
sophistication in treating fracture among the In- is trephination, but because of its importance
cas of Peru (Daland, 1935:550). Wells (1974a) in antiquity this topic will be treated as a sepa-
finds evidence for both reduction and splinting in rate category of the paleopathology of trauma
78 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 88, 89.Early stages of fracture healing and callus formation in the midshaft of an
isolated left humerus from an Eskimo cemetery on St. Lawrence Island, Alaska, USA: 88, Note
the porous nature of the recently formed callus. 89, X-ray film; note the radiolucent line (arrow)
indicating the fracture line. ( N M N H 364816-32)
of the right parietal, superior to the squamous the rock tombs at Lisht in Upper Egypt exhibits
portion of the right temporal bone. This lesion is a circular lesion suggestive of a healed, glancing,
deeper and more extensive than the first lesion, sword wound (Figure 80). This specimen is dated
but it does not exhibit the long, radiating fracture to the Twelfth Dynasty. The outer boundary of
lines. Both lesions are completely healed, indicat- the lesion is pitted, perhaps indicative of an in-
ing long survival after the injury. flammatory response. T h e sword wound appar-
A right parietal bone (NMNH 256414a) from ently removed the outer portion of the parietal in
NUMBER 28 !1
the region of the parietal boss, exposing the diploe 85, 86). The fracture involves only a portion of
in the central portion of the lesion and creating the posterior segment and was in the early stages
the porous appearance, which was partially filled of healing at the time of death. Evidence of early
in by subsequent remodeling. callus formation can be seen in Figure 86. The
Another specimen from the rock tombs at Lisht third example of vertebral fracture is from the
and dated between the Twentieth and Twenty- Saxon period at an archeological site in Winches-
fifth Dynasty (NMNH 256384) illustrates a lesion ter, England (BMNH CG66, XXIII, layer IV).
resulting from a sword or axe wound, which The first lumbar vertebra is wedge-shaped on the
occurred at the time of death. The wound pene- left portion of the body (Figure 87). There is bony
trated the left parietal bone near vertex (Figure bridging between the right sides of the first and
81). The blow removed a portion of the right second lumbar bodies and considerable rotation
parietal bone (Figure 82). No postcranial bones of the axis of LI. The fracture is well healed
are associated with this adult male skull. indicating survival after the trauma.
An adult female skull from Pachacamac, Peru Fracture in the remaining postcranial bones is
(NMNH 266584) has an extensive unhealed frac- common in archeological specimens and should
ture of the left parietal bone (Figure 83). The offer few problems in correct diagnosis. Evidence
archeological age of this skull is unknown. The of a fracture line seen in an X-ray film will
focus of the trauma is the anterior portion of the confirm such a diagnosis. This line will often be
left parietal, which exhibits a crushing injury seen as a rather sharply defined radiodense line
with fracture lines radiating down the left parietal in the fracture callus. However, in some cases,
along the coronal suture. A fracture of the left particularly if the individual died within a few
zygoma could have occurred at the time of the months following the trauma, the line may be
skull fracture. Another fracture line proceeds pos- radiolucent. An example of the latter is seen in
terolaterally across the sagittal suture and into an isolated left humerus from an Eskimo burial
the right parietal. There is no evidence of healing, on St. Lawrence Island off the coast of Alaska
indicating that the blow came at the time of (NMNH 364816-32). The archeological age of
death. this specimen is uncertain. The fracture is located
Three examples of fracture of the vertebral near midshaft with evidence for the fracture seen,
column serve to illustrate the essential features of externally, as a porous bony callus (Figure 88).
such trauma in archeological specimens. The first The X-ray film appearance shows a general in-
of these is seen in the second lumbar of an adult crease in radiodensity resulting from the callus
male from the Hawikuh site in New Mexico, added to the cortical bone. However, the radio-
USA. This is a multicomponent site dating from lucent fracture line is apparent in Figure 89.
the late prehistoric to early historic period. The
anterior portion of the second lumbar vertebral Complications of Fracture
body is crushed (Figure 84). There is fusion with
the left lateral and central portions of the inferior Severe pain undoubtedly accompanies any at-
border of the first lumbar vertebra and contact tempt to reduce a fracture. Thus, even in those
between large, bony projections from the inferior time periods and areas where fractures could be
L2 and superior L3 vertebral bodies. The second treated, it is not surprising to find numerous
example of fracture of the vertebral column is a examples of malaligned, but healed, fractures in
male sacrum from Lisht in Egypt dated between archeological skeletons. Wood-Jones (1910c) re-
the Eighteenth and Twenty-first Dynasty ports many such examples in his review of frac-
(NMNH 252874). The fracture occurs in the third tures in ancient Nubian skeletons. Wells (1974a)
sacral segment and radiates laterally from the finds similar evidence in Anglo-Saxon England.
superior portion of the spinous process (Figures Perhaps the important point to be made regard-
82 SMITHSONIAN CONTRIBUTIONS TO A N T H R O P O L O G Y
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' ^' ^^\__^^^^
'^^- -^ V ^ j ^ ^ ^ R ^^^^^ <^B^D . > ' 'isi^H
, % ' ' ' '
^E >v^
I ^^^^^^^m BL '''JifK-^'''-^'-1m
'^^^B^^ ^^H
VV "i WF ."I^KI
m^m
ijA ^ K - > ^ ^ ^ ^ m
Z ''^^
,,} ' '^^H
^^B' >fl
^^^^a^^^ ^ ^ ^ B ^ ^ j
C*i
FIGURE 93.Fracture and nonunion of the left femoral neck FIGURE 94.Healed compound fracture complicated by in-
in an adult male skeleton from Lisht in Upper Egypt dated fection in the right femur from a young adult female skeleton
from the Twelfth Dynasty. T h e fragmentary remains of the excavated from an archeological site near Akron, New York,
femoral head and neck are seen to the left. Note the extensive USA. Note the deviated axis of the distal shaft at the fracture
development of callus and the sclerotic remodeling in the site. There is a large cloaca and reactive bone (arrow)
cavity of the proximal femur. ( N M N H 256580.) probably associated with a fistula. ( N M N H 326853.)
333453 and 256580) the fracture and nonunion dial half of the femoral head. The latter is sugges-
occurred in the neck of the femur. In both cases tive of impaired circulation. There has been con-
there is evidence of continued use of the limb siderable remodeling activity on both sides of the
with the fractured end of the femoral head and fracture site (Figure 92). The second specimen
neck becoming embedded in the marrow space of (NMNH 256580) is from the site of Lisht in Egypt
the greater trochanter and proximal shaft (Figure and is dated to the Twelfth Dynasty. The fracture
91). One of these two examples (NMNH 333453) occurred in the femoral neck of the left femur.
is from an Eskimo site in Golovin Bay, Alaska. There is exuberant callus formation around the
The skeleton is that of an adult male between 20 fracture site (Figure 93) with extensive remodel-
and 25 years of age. The archeological age is ing in the bone adjacent to the fracture. The
uncertain. The fracture occurred through the individual was an old male and exhibits excessive
neck of the left femur. The X-ray film of both osteoporosis of the fractured femur. The nonun-
femora reveals considerable osteoporosis of the ited femoral head is damaged by postmortem
left femur shaft and diminished density of the breakage. In these examples of nonunion the
nonunited femoral head, particularly in the me- weight of the body tends to force the broken end
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
84
although he does not indicate whether this is due its sequelae could have affected locomotion.
to death occurring shortly after fracture or to However, the long-standing callus and extensive
nonunion. Hooton also indicates that some frac- remodeling indicate long survival and an active
tures seem to have suppurated, indicating that life after trauma.
they were complicated by infection. In the collec- The last factor complicating fracture to be
tions of the National Museum of Natural History, discussed in this review is myositis ossificans. Per-
Smithsonian Institution, USA, there are several haps the most famous example of this condition
examples of fracture complicated by infection. is the bone excrescence on the fossil left femur
These cases tend to show marked deformation from Java (Figure 96) associated with Homo erectus
suggesting considerable traumatic force, possibly (Pithecanthropus). In this specimen there is an
indicating penetration of the skin by the fractured exuberant growth of bone on the posterior aspect
bone. One example of this complication of a of the femur extending from the insertion of the
compound fracture is seen in the skeleton of a adductor muscles. Wood-Jones (1910c:317) has
young adult female from an archeological site published a line drawing of a right femur from
near Akron, New York, USA (NMNH 326853). Nubia with fracture of the femoral neck. There is
The archeological age is uncertain. The fracture an extensive, bony spur projecting medially,
is located in the distal shaft of the right femur. which Wood-Jones attributes to extensive callus.
There is considerable axial deviation, as well as The extent and shape of the bony mass suggests
some rotation. The callus is massive with consid- ossification in muscle tissue rather than exhub-
erable porosity. O n the posterior portion of the erant callus formation. However, the distinction
callus there is a large, oblong cloaca measuring between the two may be academic. While the
15 by 25 millimeters (Figure 94). There is bony Java and the Nubian specimens have the bony
evidence of a fistula, which would have extended growth attached, the paleopathologist should be
to the skin surface. T h e tibia of the same leg was aware that ectopic bone can develop in muscle
also fractured but with good alignment and no tissue and be completely unattached to any bone.
evidence of infection.
In archeological populations one finds arthritic
deterioration occasionally associated with frac- Dislocation
ture. Although not specifically addressing this PATHOLOGY
problem, Wood-Jones (1910c:308, 312, 315, 317,
318, 322) cites several examples of fracture con- The second major category of trauma involving
tributing to the development of arthritis. Morse the skeleton includes luxation, in which the joint
(1969:100, 104) cites similar conditions in arche- constituents are out of contact and the joint
ological specimens from the midwestern United capsule is disrupted. Subluxation is a less severe
States. Making the distinction between traumat- condition characterized by partial loss of the
ically induced arthritis and degenerative arthritis contact between joint components, but no disrup-
depends on two factors: (1) demonstration of tion of the capsule. Both these conditions can be
fracture in the affected bone and (2) lack of associated with fracture but often occur without
bilateral symmetry in the pattern and degree of fracture. Luxation and subluxation can occur in
arthritis (Morse, 1969:13). most joints. However, to be detected in an arche-
T r a u m a to adjacent bones may also result in ological specimen there must be permanent
ankylosis. An example of this condition is found change in the skeleton. This means that sublux-
in an historic period archeological specimen from ation will rarely be identified and luxation will
South Dakota, USA (NMNH 383010), in which be seen most often in joints where the anatomy
the distal tibia and fibula are fused in the area of makes spontaneous correction of the problem dif-
a fracture (Figure 95). Clearly such an injury and ficult. The two joints particularly prone to
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
86
cent of dislocations were traumatic in origin, 4 to make this distinction. The mechanism for trau-
percent are nontraumatic. Congenital defects in matic hip dislocation varies, depending on the
the bony structure or supporting ligaments and position of the leg and the direction of the force.
muscles appear to play a minor role in traumatic Depending on these factors, dislocation of the
and nontraumatic dislocations. femoral head may occur in an anterior or poste-
Because of the anatomy of the glenohumeral rior direction with the latter being the most com-
joint, spontaneous reduction of the dislocation mon in modern orthopedic practice (H. Epstein,
often will not occur. Rockwood (1975:625-627) 1973:116). Reduction of hip dislocations is more
notes that the methods for reducing shoulder difficult than reduction of the shoulder. The fail-
dislocations go back at least to the time of Hip- ure to reduce the dislocation will result in the
pocrates (ca. 430 B.C.). Thus, it seems possible formation of a secondary articular surface on the
that the treatment of dislocations could have innominate (Figure 98). Since spontaneous reduc-
existed in many archeological populations. How- tion is less likely, identification of this type of
ever, it is also clear that unreduced dislocations trauma to the hip in archeological material
do occur in archeological populations. In such should be fairly easy and should more accurately
situations a new joint surface is created where the reflect the actual incidence of dislocations in the
humeral head comes in contact with the scapula archeological population than evidence of shoul-
and provides clear evidence of dislocation. der dislocation.
While the anatomy of the hip permits consid- I have reviewed dislocation of only two of the
erable movement, its structure is influenced by its major joints for illustrative purposes. The student
major weight-bearing function. In contrast with of paleopathology interested in this subject should
the glenohumeral joint, the hip is a classic ball consult the orthopaedic source materials for a
and socket joint with the head of the femur deeply more comprehensive treatment. However, these
extended into the hip socket or acetabulum. two examples of dislocation reveal several prin-
While the ball and socket arrangement of the ciples that are associated with all dislocations: (1)
bony components suggests a more stable arrange- Although there may be congenital factors in-
ment than is found in the glenohumeral joint, it volved, trauma is by far the most common cause
is important to remember that the ligaments and of dislocation; (2) dislocation may be associated
muscles associated with the hip joint provide with fracture; (3) unreduced dislocation creates a
relatively less support than analogous structures secondary joint surface; (4) the evidence for dis-
in the shoulder. location in archeological samples reflects only a
Unlike the glenohumeral joint, the hip joint portion of the actual incidence of this type of
components are joined directly by a ligament trauma; (5) the blood supply to the bony part of
(ligamentum teres), which also contains the vas- the joint may be disrupted by dislocation, result-
cular supply for that portion of the femoral head ing in tissue death (aseptic necrosis); and (6) the
adjacent to the ligament. Dislocation of the fem- trauma associated with dislocation may also tear
oral head thus threatens the vascular supply of the ligaments and muscles associated with the
part of the femoral head. joint.
In congenital hip dysplasia, the acetabulum is
abnormally shallow, creating a tendency for the
femoral head to slip out of the socket in response P A L E O P A T H O LOGY
to slight trauma or even walking. Such a condi-
tion may be recognizable in skeletal material due Dislocation of the shoulder and hip should
to the abnormally shallow acetabulum, although come to the attention of the paleopathologist
the tendency for the acetabulum to be remodeled more often than other types of dislocation, be-
after traumatic dislocation may make it difficult cause of high frequency and problems in reduc-
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
88
(NMNH 363615). The archeological dating is changes associated with hip dislocation. The skel-
uncertain. T h e dislocation in this specimen also eton is from Kodiak Island, Alaska, USA
involves the left shoulder. However, the luxation (NMNH 372897), its archeological age is uncer-
was not as severe, having stimulated a secondary tain. Figure 103 shows the effects of the disloca-
joint on the anterior portion of the glenoid fossa tion on the right innominate, comparing it with
(Figure 101). There is considerable arthritic de- the normal left innominate. In both innominates
generation on the humeral head. One example of the acetabulum is somewhat shallower than nor-
posterior dislocation of the shoulder was found in mal, suggesting a possible congenital predilection
a disturbed burial from an Early Bronze Age for dislocation. Figure 104 provides a detailed
cemetery associated with the town site of Bab view of the secondary joint on the innominate
edh-Dhra in Jordan (Figure 102). A secondary
joint was created on the posterior half of the
glenoid fossa. There is evidence of arthritic de-
generation and eburnation on the secondary
joint. The humerus was not recovered.
Figures 103 and 104 illustrate fairly typical
rsMic.i'-':S",.L*CdHr?is;^.i:^iaiiff_ii:'^"':^* ^
and the degenerative changes on the femoral In modern skulls one occasionally finds the
head. skull vault to be asymmetrical or the occipital
bone flattened; such deformation may be inten-
Deformation tional. In the modern skulls, however, there is no
evidence of intentional pressure on the skull.
PATHOLOGY Probably this deformity is the result of the indi-
vidual sleeping in the identical position on a
Thus far, I have largely focused on the effects relatively hard surface during infancy and child-
of sudden trauma on the skeleton. However, hood. Such deformation illustrates the fact that
chronic, low-grade trauma over an extended pe- slight, intermittant pressure over a long time is
riod of time can also modify the normal shape of adequate to produce a gross deformity in a bone.
bone. Such deformities are often, but not always,
intentional. The basic principal to be emphasized
is that any long-term, deforming pressure brought PALEOPATHOLOGY
to bear on a bone or group of bones can result in
permanent deformity, particularly if it occurs Dingwall's review (1931) of cranial deforma-
during the growth period. tion indicates that artificial modifications of the
In relatively recent times perhaps the best skull was one of the most ubiquitous cultural
known intentional deformity was the foot-binding practices in antiquity, being found on every con-
practice of upper class Chinese women. In this tinent except Australia. A comprehensive review
practice the feet of female children were bound of cranial deformation and other forms of artifi-
in such a way that the metatarsals were bent cial modification of bony structure is beyond the
downward and compressed toward the heel of the scope of this book. It is important, however, that
foot. This created abnormal angulation of the cultural deformation not be confused with patho-
tarsal bones and abnormal relationships between logical processes, such as osteomalacia, which also
all the bones and joints of the foot (Figure 105). can result in bones of abnormal shape.
While several methods of producing cranial
deformation exist, most modifications of skull
shape are the result of applying pressure to var-
ious areas of the skull, namely: (1) the occipital
region, (2) the frontal region, (3) both frontal and
occipital regions (Figure 106), and (4) along a
transverse axis, approximately passing through
vertex, the mastoid region, and the region just
above the insertion of the nuchal ligament on the
occipital bone. This last type of pressure, utilizing
circular bands, produces the circular or Aymara
type of deformity (Stewart 1941:343) and pro-
portionately lengthens the skull (Figures 107,
108).
T h e reason for the practice of cranial defor-
mation is universally cosmetic and is frequently
associated with physical manifestations of high
social status. The origins of such practices are
FIGURE 105.Lateral view of artificially deformed, right
foot in an adult, Chinese female resulting from foot-binding.
buried in the unknown past of the people who
T h e arch of the foot is greatly exaggerated with major induced the deformation. Snorrason (1946) hy-
changes occurring in the metatarsals. (WM SI7.1.) pothesizes that abnormal, artistic representations
NUMBER 28 91
FIGURES 107, 108.Circular or Aymara type of artificial skull deformation, which results from
circular constricting bands wrapped around the posterior half of the skull during the early
growth phase of the individual: 107, Lateral view. 108, T o p view showing somewhat elongated
aspect of the deformed skull. (Specimen from Ancon, Peru, archeological age unknown, N M N H
242844.)
92 SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
Scalping
PATHOLOGY
the lesion is compatible with a diagnosis of scalp- bone. In this section we shall only review muti-
ing. lations of bone. Dental mutilations will be dis-
Regardless of the origin of scalping, it is well cussed, but soft tissue mutilations are beyond the
documented for many of the Indian tribes in scope of this book.
various geographical regions of North America in Mutilation affecting bone may be voluntary,
early Colonial times. Catlin (1844:239-240) re- in which the victim either performs the mutila-
ports that the Colonists would pay for scalps of tion on himself or willingly allows it to be per-
enemies both White and Indian. Indeed, he notes formed by someone else. Involuntary mutilations
that a knife commonly used for scalping was are usually associated with punitive action
made in Sheffield, England, and traded to the against a criminal or a captive. Moodie (1920:
Indians for horses (Catlin, 1844:236). 1300) has published Aurignacian (ca. 20,000 B.P.)
The scalp was removed to provide evidence of cave art from Gargas, Spain, suggesting finger
having killed an enemy. Nadean (1941:181-182) amputations in that period. He further reports
indicates that some tribal variation existed re- (1920:1303) the existence of finger mutilation
garding the amount of scalp taken. Catlin (1844: throughout the world. In the Old World, the
30-31, 238) indicates that the scalp taken from most commonly reported reason for finger muti-
"the place where the hair radiates from a point" lation is as a symbol of mourning. Among the
was most important but that scalp from other North American Indians it was part of initiation
areas would be used to decorate clothing in some rites.
tribes (e.g., Blackfoot). In removing the scalp, the Major portions of one or more limbs have also
skin would be cut around the desired area and been removed. Brothwell and M0ller-Christensen
pealed off The initial cutting may have left (1963b) report a case of amputation with subse-
marks on the skull whether or not the victim was quent healing of the stump of the distal right
dead (Owsley, Berryman, and Bass, 1977). forearm from Egypt dated 2000 B.C. They offer
Catlin (1844:239), Reese (1940:16), and Na- three possibilities for the cause of the mutilation:
dean (1941:193) report that survival after scalp- (1) injury during warfare, (2) punitive action
ing did occur. Reese (1940:18-19) included in his against a criminal or captive, and (3) surgical
paper a report by a physician who treated a case amputation for therapeutic reasons. While pun-
of scalping by Cheyenne Indians in 1867. The ishment for criminal behavior remains a possibil-
report indicates that the scalp was removed, the ity, Aldred (1964:56) challenges the likelihood
periosteum covering the skull cut and badly dam- that the Egyptians would have cut off the hand
aged. The outer table was exfoliated (shed), after of a captive. He notes that to do so would have
which the wound healed. Hamperl and Laughlin deprived the captors of a valuable spoil of war:
(1959:88), in commenting on this case, suggest the slave labor. He further notes that amputation
that the destruction of the periosteum deprived of the hand was limited to the dead and dying
the outer table of its superficial blood supply. victims of warfare and was used as a method of
This resulted in necrosis with granulation tissue recording the dead from the field of battle. In
in the diploe eventually separating the necrotic another report Brothwell and M0ller-Christensen
tissue from the skull. An archeological specimen (1963a) described an amputation of the distal left
showing a lesion probably reflecting this same forearm in a skeleton from Sicily dated to the
process is reported by Hamperl and Laughlin seventh century A.D. The ends of the radius and
(1959). ulna have fused, indicating healing. They con-
clude that the amputation was punishment for a
Mutilation criminal acta practice common also in that
age. Stewart (1950:43) reports the existence of
Among historical preliterate groups mutilation bones showing amputations from Peru but does
of the body involves the soft tissues, teeth, and not indicate which bones are involved.
NUMBER 28 95
While there seems to be convincing evidence have been found in Egypt in view of the contact
that both voluntary and involuntary mutilation with Greece where it was practiced in antiquity.
of bony parts of the skeleton did occur in antiq- Ruffer (1918a:95) published a photograph of a
uity, a word of caution is appropriate regarding purported trephination from Egypt. Moodie
unequivocal interpretation. With respect to miss- (1919:485) has expressed reservations regarding
ing fingers or toes in an archeological specimen, Ruffer's case and further states (p. 494) that
at least two other conditions could be implicated. trephining did not occur among Greeks, Romans,
These are infectious disease (particularly leprosy) Phoenicians, Babylonians, or Egyptians. More
and frostbite. Amputation of the distal forearm recently Oakley, Brooke, Akester, and Brothwell
or distal leg should also be reported with caution. (1959:95) report a case of trephination from Tark-
Stewart (1974:889-890) calls attention to the han, Egypt, dated to early dynastic times. Clearly
morphological similarity between the skeletal the Greeks of the Periclean Age performed tre-
manifestation of pseudarthrosis and what might phination (Withington, 1927:3) and the strong
be expected in an amputation. He suggests that evidence of trephination in Palestine suggests that
bony fusion of the distal radius and ulna in the the practice occurred in Middle East countries.
case reported by Brothwell and M0ller-Christen- Mallin and Rathbun (1976) have reported a case
sen (1963b) might be more reasonably explained of trephination in ancient Iran. In any case, the
by fracture and nonunion. Diagnosis in this case practice in the Middle East appears to be rela-
is complicated by the fact that the fused radius tively rare, certainly by comparison with South
and ulna are isolated bones, raising the possibility America, where over 1000 cases of trephining
that the distal portion of the specimen, if it was have been found (Stewart, 1958b:474).
a case of nonunion, had not been recovered. There is debate regarding the practice of tre-
phination in pre-Columbian North America.
Stewart (1958b:476-479) surveyed 17 purported
Trephination cases and concluded that evidence for trephina-
tion in North America had not been demon-
HISTORY
strated. One of the factors contributing to the
Perhaps the most remarkable trauma seen by controversy is the difficulty of conclusively iden-
the paleopathologist is trephination or the surgi- tifying a trephination in an archeological speci-
cal removal of a portion of the skull. The earliest men. Given a partial or complete hole in a skull
written accounts of trephination are found in the there are several possibilities for the cause. Gold-
Hippocratic writings (460-377 B.C.). However, smith (1945:348) suggests that some of the so-
the evidence of trephining goes back at least to called examples of trephination are, in reality,
the Neolithic period (Moodie, 1919:484; Guiard, cases of congenital, bilateral openings of the pa-
1930; Parry, 1931; Hrdlicka, 1939; Stewart, rietal bones (p. 352). This condition is a heredi-
1958b:470; Oakley, Brooke, Akester, and Broth- tary enlargement of the parietal foramina (Gold-
well, 1959:93). It continues to be practiced among smith, 1945:350). Other congenital conditions
many recent, primitive peoples (Ruffer, 1918a: such as dysraphism (p. 351) can be confused with
99-102; Freeman, 1918:445; Moodie, 1919:485; trephination. Both infection and neoplasm can
Hrdlicka, 1939; Oakley, Brooke, Akester, and produce holes in the skull, which might be con-
Brothwell, 1959). The geographical distribution fused with trephination. Injury such as a glancing
of the practice is extensive, including Europe, the sword or axe wound can remove a portion of the
Pacific, North Africa, the Middle East, and South skull and produce a healed lesion similar to tre-
America (Stewart, 1958b:470-480). Wood-Jones phination. Furthermore, a trephine-like wound
(1910c:299) states that trephining has not been may not have been part of a surgical procedure
on the living. Some groups apparently practiced
reported in ancient Egyptian skulls. However, he
postmortem removal of circular pieces of skull
saw no reason why trephined skulls should not
96 SMITHSONIAN CONTRIBUTIONS T O ANTHROPOLOGY
(Ruffer, 1918a:91, Parry, 1931:1388-1389; Stew- of repair to the surgically induced defect. If there
art, 1958b:475). Obviously, no healing would is no healing, as evidenced by the lack of remod-
have occurred, but polishing of the edges by eling of the cut edges or fill in of exposed, diploic
intentional or unintentional rubbing can create spaces, the reasonable assumption is that death
a superficial appearance of healing (Stewart, occurred at the time of, or shortly after, surgery.
1958b:477). A zone of porous, reactive bone surrounding the
It is clear that the identification of the cause of surgical area suggests survival for some time after
holes in the skull cannot always be made. How- surgery, but with the possibility of infection com-
ever, there are some criteria that will be impor- plicating the healing process and causing death.
tant in any analysis. T h e first question to be Partial to complete refill of the surgical defect is
resolved is whether the hole is the result of me- indicative of recovery and long-term survival
chanical intervention. Evidence for cutting or after surgery.
scraping may still exist even if healing has taken
place. T h e next problem to be clarified is if the PALEOPATHOLOGY
cutting was done before or after death. T h e sig- Freeman (1918:445) remarks, somewhat whim-
nificant question here is whether we are seeing sically, that trephination in ancient populations
the product of a surgical procedure or the result was probably no worse "than the torture occa-
of some postmortem ritual. Any evidence of heal- sionally inflicted on us by our dentist." Neverthe-
ing or inflammatory reaction to the cutting is less, the pain involved, as well as the threat to life
indicative of trephination. However, it is possible inherent in the procedure, raise inevitable ques-
that a patient can die during the trephination or tions regarding the biological or cultural reasons
so soon after it that no reaction takes place. Such for trephination. Broca (1876:572) suggested that
a situation in an archeological example of tre- trephination was performed as a cure for mental
phination may be indistinguishable from post- disorders. Ruffer (1918a:91) states that in Europe
mortem ritual removal. In such situations the until the Middle Ages, powdered cranial bone
demonstration of unambiguous trephination in was thought to possess curative properties. He
the same geographical area would certainly be also states that roundels (circular pieces of human
significant in interpreting the equivocal cases. skull) were worn as ornaments as late as Gallic
Another important criterion is the presence of times. Parry (1931:1388) asserts that Neolithic
fracture in association with evidence of cutting. man performed trephination "as a religious rite
Many, if not most, trephinations occur in associ- ridding an affected individual of some demon or
ation with skull fracture. As with most other demons " H e also indicates (1931:1388-1389)
problems in paleopathology careful observation that amulets were made from the trephined skulls
combined with a comprehensive knowledge of of deceased individuals, which included healed
the options is the most important prerequisite in edges of the trephination. Stewart (1958b:481)
determining the presence of trephination. suggests that this practice is limited mainly to
In trephination, four basic responses can occur. Europe. More recently Oakley, Brooke, Akester,
First, in those cases where trauma preceded the and Brothwell (1959:93) have supported the con-
trephination procedure, death may be due to the cept of the ritual significance of trephination,
initial trauma. Second, the surgical procedure citing Albert Schweitzer's observation in modern
itself may cause death. Third, the surgical pro- African tribes that trephination is used to obtain
cedure may not directly cause death but may a powerful fetish object.
introduce disease organisms that cause infection While the evidence for religious implications in
and possibly death. Fourth, there may be no trephination appears convincing, it is equally
complications resulting from surgery, in which clear that trephination was also a surgical proce-
case the individual survives with varying degrees dure done to correct a serious medical problem.
NUMBER 28 97
The Hippocratic writings (Withington, 1927:3, with a sharp implement to the desired depth
35) indicate that trephination was well known (Figures 112-114). This method undoubtedly in-
and practiced in the Golden Age of Greece (ca. volved the lowest risk of damaging the brain and
500 B.C.) for relief of the effects of skull fracture. is found in all geographical areas where trephin-
The expertise of the technique revealed in the ation occurs. Other methods included drilling a
discussion suggests even greater antiquity for tre- circle of small holes and breaking or cutting the
phination as a treatment of skull trauma. intervening bone and sawing or cutting directly
It should not be surprising to find trephination into the bone (Figures 115, 116). Both these meth-
practiced for therapeutic treatment of skull frac- ods involved considerable risk to the brain. Elo-
ture in other geographical areas and time periods. quent testimony to this risk is seen in unhealed
Moodie (1919:484) suggests that this is the reason trephination of this type indicating that death
for trephination in primitive societies. Hrdlicka occurred during, or shortly after, surgery (Figure
(1939:175) notes that "a very large proportion of 117). Initially the direct cutting type of trephin-
aboriginal trephinings in America were true sur- ation was thought to occur only in the New
gical or curative operations for the relief of the World; however. Parry (1936:170-171) reports
effects of head wounds or for that of actual or this type of trephination in Palestine.
supposed pathological conditions within the The surgical approach for trephination re-
skull." Stewart (1958b:481) concludes that relief quired that the overlying skin be cut, unless it
of pressure from skull fracture was the most fre- was already cut by injury. Stewart (1958b:483)
quent reason for trephination in Peru and Mela- suggests that in some cases a portion of the scalp
nesia. Oakley, Brooke, Akester, and Brothwell would be removed entirely. In modern cases from
(1959:93) indicate a similar rationale for trephin- Melanesia the skin is reflected back, the bone
ation practiced by medicine men in Bolivia in the removed and the skin replaced over the trephine.
1950's. He notes that the incision into the scalp may
produce scratches on the underlying bone and
can occasionally be seen peripherally to the tre-
Types of Trephination
phine indicating the extent of scalp removal.
Trephinations vary in terms of the extent of
bone removed, the depth to which bone is re-
Complications of Trephination
moved, and methods used. The extent or area of
bone removal varies with the size of the injury There are two major potential problems arising
and the judgment of the surgeon. The depth of from trephination: (1) direct injury to the brain
bone removal appears to reflect two possibilities: resulting from improper method or poor tech-
(1) the surgeon can remove the outer table of nique, and (2) infection. Either of these compli-
bone and diploe or (2) he can remove both tables cations can cause death. Moodie (1919:481-485)
of bone, exposing the dura. In ancient Greece, estimates the total mortality rate from trephina-
surgeons were conscious of the dangers of pene- tion at 50-75 percent as compared with a rate of
trating into the dura (Toole, 1964:91-92), and it 15-18 percent in civilized modern populations in
is likely that such knowledge would quickly be the early 1900's. Hrdlicka (1939:175) is much
acquired and disseminated. more optimistic regarding the outcome of tre-
The methods of trephination have been re- phination, expressing the opinion that complica-
viewed by several scholars (e.g.. Parry, 1931, tions, including infection, were rare. Piggott
1936; Hrdlicka, 1939; Stewart, 1958b; Oakley, (1940:122) and Stewart (1958b:486) support this
Brooke, Akester, and Brothwell, 1959). From opinion. Stewart reports that of 214 operations he
these reports it is clear that the most widely used studied, 55.6 percent show healing, 16.4 percent
method was careful scraping through the bone show slight healing, and only 28 percent show no
98 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
sequestration of bone near the point of impact Although death during pregnancy may occur
and a marked, inflammatory reaction to the due to any number of reasons, including ob-
trauma in the surrounding tissue. This process structed labor, infection, or hemorrhage, it is
may have been complicated by infection. Surgical difficult to estimate how these hazards relate to
intervention was not completed, perhaps because ancient populations. Indeed, it is likely that the
of the poor condition or death of the patient. knowledge and experience needed to minimize
mortality varied significantly in ancient societies.
In obstructed labor the problem may be the
Traumatic Problems Arising from Pregnancy result of the pelvic outlet being too small for the
infant or an abnormal presentation of the infant
PATHOLOGY
during delivery. In modern clinical practice the
Pregnancy and particularly traumatic compli- physician has several options available to alle-
cation of pregnancy that threatens the life of a viate this problem and complications arising from
mother is difficult to document in skeletal re- it, including surgical intervention and forceps
mains. Evidence for pregnancy, or at least par- delivery. These options were not generally avail-
turition, is thought to be seen in the pitting and able in populations whose skeletons are studied
erosion of the pubic bones adjacent to the pubic by the paleopathologist. Therefore, obstructed
symphysis (Putschar, 1931, 1976b; Angel, 1969a; labor would have been a serious threat to life,
Stewart, 1970; Gilbert and McKern, 1973). Even although midwives or their analogue in modern
demographic data suggesting increased female primitive and peasant societies, show rather re-
mortality (e.g., Acsadi and Nemeskeri, 1970:251) markable skill in successfully assisting a compli-
does not provide unequivocal evidence of in- cated delivery.
creased death directly due to pregnancy and Implantation and development of the fetus in
childbirth. Wells (1975) argues that death due to any place other than the uterus is known as
pregnancy may have been high in Europe from ectopic pregnancy. Willson, Beecham, and Car-
the seventeenth to the early twentieth century rington (1971:180) indicate population differ-
when widespread rickets produced unusually ences in frequency. However, in the general U.S.
high mortality from obstructed parturition. He population incidence is one in about 80 normal
states that rickets was not widespread before the intrauterine pregnancies. Termination generally
seventeenth century and that complication from occurs in 6 to 16 weeks and is accompanied by a
pregnancy may have been too rare to account for rupture of the fallopian tube, where the fetus is
the high female mortality. Wells attributes differ- most often implanted in ectopic pregnancy. The
ential female mortality to the cultural practice of rupture is associated with profuse bleeding which,
males having nutritional needs met first, with without surgery, almost always will cause death.
females getting less and poorer quality food, par- In the early 20th century, the mortality was
ticularly during periods of famine. between 10 and 15 percent for such pregnancies
In contemporary developing countries, death (Willson, Beecham, and Carrington, 1971:188).
due to complications of pregnancy accounts for However, much higher mortality would be ex-
about 10 percent of female deaths during the pected in more primitive societies. If the fetus
childbearing period from 15 to 44 years of age continues to full term there is a serious problem
(World Health Organization, 1976). Thus, while in delivery which must be done by surgical re-
it may be inappropriate to attribute all the dif- moval of the infant, an option not available in
ference between male and female life expectancy most ancient societies.
to the hazards of pregnancy, it does constitute a Pregnancy increases the risk of infection, which
significant threat to life today and probably did represents a serious hazard to both mother and
so in antiquity. the developing fetus. There are, for example.
NUMBER 28
101
some urinary tract infections that seem to be similar cases from Hungary, although Wells
exacerbated by pregnancy (Willson, Beecham, (1975:1238) challenges their interpretation and
and Carrington, 1971:272). The childbed fever suggests that only two of these cases were deaths
scourge, with its high mortality in the obstetric resulting from childbirth itself Wells, however,
hospitals of the eighteenth and nineteenth cen- does not rule out other complications of preg-
turies, may not have caused significant mortality nancy, such as erysipelas or meningitis as a cause
in ancient populations (Wells, 1975:1240). How- of death. Sj0vold, Swedborg, and Diener (1974)
ever, women are particularly prone to infection report a case of death due to childbirth in a
through the genital area immediately following woman having multiple exostoses blocking the
childbirth. birth canal. Hawkes and Wells (1975) report a
Hemorrhage during pregnancy or childbirth case of a female burial with a baby's skeleton still
can be caused by several conditions. I have al- partially in the pelvis. They conclude that death
ready noted this problem in association with ec- took place during childbirth.
topic pregnancy. Postpartum hemorrhage occurs Unambiguous archeological examples leave lit-
in about 5 percent of normal deliveries. It is also tle doubt that awareness of this problem and
associated with improper implantation of the pla- attention to careful excavating technique make it
centa in the lower region of the uterus (Willson, possible to reconstruct a traumatic event. How-
Beecham, and Carrington, 1971:318). ever, Wells correctly cautions against the assump-
Willson, Beecham, and Carrington (1971:306) tion that all examples of infants buried with a
report that 7 to 10 percent of all pregnancies in female skeleton or fetal bone lying inside the
the United States are complicated by toxemias. abdominal region are indicative of death due to
One-half of these is due to high blood pressure, pregnancy and childbirth. A pregnant woman
the other half is due to a poorly understood can die of infectious diseases and several other
condition called preeclampsia and its more seri- conditions not necessarily related to pregnancy.
ous form eclampsia. Eclampsia is characterized One should also keep in mind that labor and
by convulsions or coma. Mortality in the United childbirth may be traumatic to the infant even
States for advanced stages of preeclampsia and when delivery is completed. Evidence for such
eclampsia is 10 percent, making it a fairly serious trauma will probably be uncommon in archeo-
threat to pregnant women. Presumably the mor- logical materials, since severe trauma would result
tality would be even higher in populations that in the immediate death of the infant. In modern
do not have access to modern therapeutic means. clinical practice difficult labor may be assisted by
instrument delivery, in which the infant is phys-
ically drawn out of the mother with large forceps.
PALEOPATHOLOGY
Such intervention may injure the tissues of the
The conditions that cause death during preg- infant and produce hematoma. When this occurs
nancy rarely leave any evidence in the skeleton. on the skull, the outer portion of the hematoma
However, this brief summary of the more serious may ossify, creating a thin shell of bone. While
complications of pregnancy should alert the pa- the events leading to this specific problem are
leopathologist to these conditions when there is unlikely to occur in archeological popiilations,
evidence of fetal or newborn skeletal materials in the morphological features seen in such problems
association with an adult female burial. serve to illustrate what might be seen if an infant
Elliot-Smith and Wood-Jones (1910:260) re- were injured in some other way during delivery.
port from ancient Nubia five cases of female Two cases from recent times provide examples
skeletons with deformed pelves, in which death of ossifying hematoma in infant skulls. Figure 119
occurred during pregnancy and possibly labor. shows a large hematoma on the left parietal in a
Acsadi and Nemeskeri (1970:253) report twelve case from the Federal Pathologic-Anatomy Mu-
102 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Sincipital-T Mutilation
In Europe, skulls with these lesions were found one specimen exists in which the sincipital-T
in skeletons of the Neolithic period (Manouvrier, defect in part penetrated through both tables of
1895). Zaborowski (1897) reports similar findings the skull.
in central Asia. Moodie (1921) and Weiss (1955) There is also a possibility that senile atrophy
report the sincipital-T pattern in ancient Peru- can occur in the sagittal and lambdoid sutures.
vian skulls. However, Stewart (1958b: 480) cau- Atrophy in this location would produce a depres-
tions against interpreting any large bone scar as sion very similar to the changes reported for
the result of cautery. sincipital-T mutilation. One skull from a prehis-
Virchow (cited in MacCurdy, 1905:20) sug- toric site (Irene Mound) in Georgia, USA
gested that a tartar-emetic ointment smeared on (NMNH unumbered) exhibits a depression in the
the scalp could produce scarring and affect the posterior sagittal suture and much of the lamb-
bone. However, weight is lent to the hypothesis doid suture (Figure 121). The inner table is nor-
of cautery being the cause of the lesion by Avi- mal. The skull appears to be that of a female over
cenna's medieval prescription of melancholia in 50 years of age with considerable antemortem
which "the head is to be cauterized in the form tooth loss. There is evidence of senile atrophy
of a cross" (MacCurdy, 1905:23). Most often the medial to both temporal lines suggesting that
lesion resulting from cautery did not expose the senile atrophy is a likely explanation for the
dura (MacCurdy, 1905:17-18), although at least atrophy of the sutural areas.
Infectious Diseases
The Inflammatory Response blasts laying down collagen, which is the main
constituent of scar tissue. In infections that have
The inflammatory response to infection begins
a component of allergic reactivity, as, particu-
as a vascular phenomenon. The capillaries dilate
larly, in parasitic diseases, eosinophilic leucocytes
and their walls begin to allow the escape of large
may be prominent in the immediate inflamma-
molecular proteins and cells normally retained in
tory response. In viral infections, where the or-
the circulation. Albumins, globulins, and fibrin-
ganisms propagate intracellularly and offer no
ogen enter the tissue where fibrinogen is con-
opportunity for phagocytosis, the initial leucocy-
verted into fibrin. This is followed by active
tic response as well as the formation of pus is
emigration of neutrophilic leucocytes, which are
usually lacking. Lymphocytes, plasma cells, and
capable of amoeboid motion and thereby can
macrophages dominate the picture even in the
squeeze through moderately enlarged pores in the
acute phase, mainly in response to the breakdown
vascular wall. In the tissue they migrate, by
of infected tissue cells.
chemotactic attraction, to the bacterial focus. It
is these leucocytes, in connection with proteins Organisms that are difficult or impossible to
and fibrin, which make up the pus of acute control by the ordinary cellular defense mecha-
infections. Many leucocytes ingest bacteria by nisms discussed above produce the so-called gran-
phagocytosis and may inactivate or destroy them; ulomatous response to infection. Such organisms
others succumb to bacterial toxins and disinte- are the acid-fast mycobacteria of tuberculosis and
grate. The severity of inflammatory response is leprosy, many of the fungi, and treponemal infec-
proportional to the number and virulence of in- tions. In these infections histiocytic proliferation
fecting organisms. If the capillary leakage be- around organisms form nodular foci. Multinucle-
comes gross, erythrocytes, which have no active ated giant cells phagocytose organisms but often
mobility, may also enter the tissue in large num- are not able to kill them. Thus, the center of the
bers. Thus, it is customary to classify the inflam- granuloma may undergo necrosis but harbor con-
matory response by the type of exudate as serous, fined, viable organisms for a long time. Lympho-
fibrinous, hemorrhagic, or purulent, reflecting the cytes and plasma cells border the granulomas,
increasing severity of the infection. After the indicating the continued response to the infection.
acute phase other cells, from the blood and from
the tissue, participate in the inflammatory re-
The Biology of Infection
sponse. Lymphocytes and plasma cells particu-
larly, involved in the cellular and humoral im- In human populations of antiquity, generally
mune responses, appear in increasing numbers in about half the individuals born died during in-
and around the lesion in the subacute and chronic fancy or childhood. T h e major cause of this mor-
phases of infections. tality was infectious disease, the single greatest
Histiocytes and macrophages of the tissue are threat to life. Of those living to adulthood, many
mobilized and serve in cleaning up infected areas died of the direct or indirect effects of infectious
by means of phagocytosis of debris and of orga- disease, but trauma becomes increasingly signifi-
nisms. Multinucleated symplasts, so-called giant cant. Even among hunters and gatherers living
cells, may appear in this phase. The healing is today, infection of the digestive system results in
mainly accomplished by proliferation of fibro- the death of many of the infants and children.
104
NUMBER 28 105
Osteomyelitis
PATHOLOGY
Hematogenous Osteomyelitis
FIGURES 142, 143.Chronic sclerosing osteomyelitis of both femora; notice the similarity of the
periosteal bone pattern to tertiary syphilis: 142, Anterior view. 143, Interior a n d medial view.
(23-year-old male with periosteal abscess and skin fistula over both femora; died from amyloi-
dosis; P M U G 1712 a and b, autopsy 3260 from 1869.)
skull participate least in hematogenous osteomye- of large, often circumferential (Figures 122, 123)
litis (Wilensky, 1934:276, 277). and sometimes total necrosis of the diaphysis
The acute hematogenous osteomyelitis begins (Figures 124, 125). T h e dead bone becomes the
with one or several purulent foci in a metaphysis, sequestrum, which can only be resorbed or re-
leading to lytic destruction of the newly formed modeled if small. Large sequestra remain and
spongiosa: The exudate spreads through the mar- maintain the infection if they are not extruded
row cavity, increasing the pressure within the through fistulae or removed by surgical interven-
rigid confinement of the diaphysis and resulting tion. The elevated periosteum continues to pro-
in more or less extensive necrosis of the cortex by duce bone, forming a shell of hypervascular bone
means of vascular compression. In the metaphy- surrounding the sequestrum (Figure 126). This
sis, near the growth plate, the thin remodeling enveloping reactive bone formation is called in-
cortex permits easy extension of the exudate un- volucrum and serves as a scaffolding in ultimate
der the periosteum. The active osteogenic perios- repair. The metaphysial bone usually does not
teum of the child readily strips from the cortex, undergo total necrosis because of the easy escape
permitting the formation of a subperiosteal ab- of the exudate through the thin, porous cortex.
scess and depriving the diaphysial cortex of its The separation of living bone and sequestrum
external blood supply. This results in formation takes place in this area by means of osteoclastic
NUMBER 28 113
FIGURES 150, 151.Acute osteomyelitis of left tibia: 150, Tibial diaphysial sequestrum, extracted
from the fistula. 151, X-ray one year later, showing complete regeneration of the tibia.
(2-month-old African negro, W M S44.6, from 1963.)
separation. The mortality of this disease used to it healed temporarily to recur after years; others
be at least 20 percent. In many instances the healed permanently. Other cases showed a less
disease remained active for a long time; in others severe course with fewer or no sequestrations and
more sclerotic response (Figure 139) (Garre, 1893:
257-263). In the absence of sequestra and of
FIGURES 146, 147.Chronic recurring osteomyelitis of right
cloacal openings entering the medullary canal,
tibia with involvement of the proximal epiphysis and elon- differentiation from tertiary syphilis is difficult or
gation. Notice the low position of the proximal end of the impossible (Figure 140-143). Some cases result
fibula. Reactive periostitis of fibula: 146, Anterior view. 147, only in a local abscess formation (Brodie's abscess)
Cut surface; notice abscess cavities with perifocal sclerosis. (Figures 144-147), usually near the growth plate,
(FPAM 4921, autopsy 86827 from 1888.)
in the metaphysis, surrounded by sclerotic bone.
FIGURE 148.Both lower legs. Chronic osteomyelitis of right The collateral hyperemia, not uncommonly, re-
tibia with elongation and with ankylosis of ankle joint,
sults in excessive, longitudinal growth of the af-
periostitis of fibula. (53-year-old female, FPAM 5217, au-
topsy 91835 from 1892.)
fected bone if the growth plate (Figure 148) is not
destroyed. In rare cases of chronic osteomyelitis,
FIGURE 149.Squamous cell carcinoma of left tibia second-
carcinoma may develop from the epithelium of
ary to chronic osteomyelitis. Notice the extensive destruction
and pathological fracture of the tibia and periostitis of fibula. the fistulous tract (Figure 149).
(45-year-old male with osteomyelitis since childhood, P M E S INFANTILE OSTEOMYELITIS.This disease ex-
IVNa 16(4).) hibits some differences from juvenile osteomyeli-
116 SMITHSONIAN CONTRIBUTIONS TO A N T H R O P O L O G Y
tis. It used to be uncommon in the preantibiotic Multiple bones are affected in about two-thirds
period, because most infants succumbed to the of these cases. Long bones are predilected, but
septicemia before osteomyelitis was established about 25 percent of the patients show involve-
(Green and Shannon, 1936). In infantile osteo- ment of bones of hands a n d feet. There are usu-
myelitis massive sequestration is unusual because ally no major sequestra and the periosteal reactive
the thin, loosely structured cortex permits escape bone is sparse (Putschar, 1976a:49).
of pus without raising the intramedullary pressure
to critical levels. Involvement of the epiphysis
Changes in Individual Bones
and concomittant septic arthritis are common
because, in this age group, the epiphysial blood T h e overall description of hematogenous osteo-
supply is not yet separated from that of the myelitis given above mainly focuses on the
metaphysis (Trueta, 1957:360-366). If the osteo- changes in long bones of the extremities. A dis-
myelitis heals, rapid remodeling removes much of cussion of the pecularities of osteomyelitis in dif-
the evidence of the disease, for, in the rapidly ferent other parts of the skeleton is therefore
enlarging bone, the entire old cortex is removed indicated.
as the bone grows in diameter. This is true even SHORT TUBULAR BONES.Phalanges, metacar-
after elimination of a large sequestrum (Figures pals, and metatarsals are uncommon sites of os-
150, 151). teomyelitis. In young children hematogenous in-
ADULT OSTEOMYELITIS.Adult hematogenous fections in these rapidly growing bones do occur
osteomyelitis is rare and may often represent and lead to rapid destruction of the thin cortex
continued or recurrent juvenile osteomyelitis. and formation of a massive expanded involu-
New infections also predilect the metaphysial crum, resembling the spina ventosa in tubercu-
areas of long bones, especially femur and tibia. losis and similar changes in congenital syphilis
The inflammation is less acute and less extensive. (Figure 152). In adults phalanges, especially of
Sequestra tend to be small. T h e firm attachment toes, are more often involved in cases of peripheral
of the periosteum prevents extensive stripping but vascular disease secondary to skin ulcerations.
local subperiosteal abscesses and fistulae are com- These cases resemble the features of chronic adult
mon. Since, after closure of the growth plate, osteomyelitis in other bones (Figure 153).
communications of metaphysial and epiphysial T H E SPINE.Vertebral osteomyelitis is uncom-
blood vessels are reestablished to some extent, mon, amounting to about 2 percent of all cases
involvement of the epiphysis and of the adjacent (Schmorl and Junghanns, 1971:389). It occurs
joint is not unusual. more often in adults than in children (Kulowski,
Hematogenous osteomyelitis caused by bacte- 1936:343-344). In contrast to tuberculosis, only
ria other than Staphylococcus and Streptococcus one vertebra is affected in 75 percent of the cases
should be briefly discussed. About one percent of (Donati, 1906:1132-1133). T h e frequency of lo-
patients with typhoid fever, regardless of age, cation in the spine increases distally. Lauche
develop osteomyelitis (Murphy, 1916). T h e main (1939:39) estimates that of cervical, dorsal, and
locations are ribs, tibia, and spine. T h e tibial lumbar involvement at a ratio of 1:2:3. T h e first
lesion often is a diaphysial subperiosteal abscess and second cervical segments are very rarely af-
involving the underlying cortex. T h e spinal lesion fected. As far as the location within the vertebra
predilects the lumbar segment and often involves is concerned, in contrast to tuberculosis, the spi-
two adjacent vertebrae and the intervertebral disc nous process and neural arch often participate in
between them. In various hemoglobinopathies, the lesion. T h e infection may even be limited to
especially in sickle cell anemia, complicating sal- the neural arch a n d / o r spinous process (66 per-
monella osteomyelitis is not uncommon (Hook, cent (Donati, 1906:1133) 58 percent (Volkmann,
Campbell, Weens, and Cooper, 1957:403-407; 1915:485)). T h e transverse process is rarely af-
Golding, Maclver, and Went, 1959:711-718). fected. In destructive spinal osteomyelitis, col-
NUMBER 28 117
FIGURE 152.X-ray of hematogenous staphylococcic osteo- FIGURE 153.Osteomyelitis of basal phalanx of right big toe
myelitis of first metatarsal, massive involucrum of diaphysis. with involucrum and sequestrum, periostitis of terminal
(3-year-old male, surgical specimen 7637-1970, MGH.) phalanx, secondary to infected wound. (Adult, P M E S 1 EB
18 (100).)
this skeleton is the right and left tibia, both of which is a localized periosteal reaction. T h e distal
which are in an excellent state of preservation. metaphysis has a cloaca on the medial aspect,
The estimated age, based on the length of the which is continuous with the opening in the
normal, right tibia, is 9 years. Unfortunately, the growth plate mentioned above.
archeological provenience is poorly documented. The diseased shaft contains a sequestrum,
However, it seems likely that the specimen is pre- which projects through a large cloaca on the
Columbian. anterior shaft (Figure 170). There is a smaller (5
Grossly the two tibiae differ dramatically in mm diameter) cloaca inferior to the large cloaca.
size (Figures 169-175). The measurements in Ta- Both of these openings are part of a single channel
ble 2 indicate the marked increase in size of the that contains the sequestrum. There is a small,
pathological left tibia in contrast with the normal lytic pit near the sequestrum and a cloaca in the
right tibia. Osteomyelitis results in hyperemia, posterior portion of the distal shaft.
which may stimulate excessive growth in the The roentgen-film appearance of the diseased
affected bone. This effect of the disease is clearly left tibia shows a greatly thickened, but porous,
seen in the two tibiae of this case. The excessive involucrum. The old sequestrated shaft is still
growth of periosteal involucrum is the result of apparent, although the cortex of the metaphyses
pathological stimulation in response to the death has been removed by remodeling. T h e diameter
of the cortex. This problem does not exist at the of the shaft is compatible with an age of a 4- to
growth plate where excessive, longitudinal 5-year-old child. Since sequestration would most
growth is stimulated by the general hyperemia. likely have occurred shortly after the onset of the
disease, this suggests that the child suffered from
TABLE 2.Metric comparisons of the right (normal) and left osteomyelitis for about 5 years before death.
(pathological) tibia in osteomyelitis from a 9-year-old child In the lateral roentgen view of the osteomyelitic
from an archeological site near La Oroya, Peru ( N M N H tibia, there appears to be another, much smaller,
378243)
sequestrum in the distal anterior cortex (Figure
Measurement
Left Right 175). Grossly, there is a bulge in this area but no
(mm) (mm) cloaca. There are other roentgen features also
Maximum length 219 196 suggesting sequestra; however, their identifica-
Maximum midshaft diameter 34 17 tion on the X-ray film is less clear cut.
Mediolateral diameter of 50 45
proximal growth plate
A comparison of Harris' lines also offers some
insight into the disease process. In the normal
(right) tibia there are four distinct lines in the
While the proximal growth plate of the patho- distal and three in the proximal ends. The osteo-
logical, left tibia is enlarged, the surface appears myelitic tibia contains two distinct Harris' lines
normal, although there is a postmortem break in and two much less distinct lines in the distal tibia,
the surface. There is a cloaca one centimeter which may correspond to the four distal lines seen
below the growth plate, but it does not penetrate in the normal tibia. There is no evidence of
it. The distal medial cortex of this bone has a Harris' lines in the proximal end of the patholog-
large, cloacal opening with a channel penetrating ical tibia. If they existed the disease has obliter-
the distal growth plate. There is also some post- ated the roentgen evidence.
mortem damage. The cloacal openings penetrate Table 3 shows the distances between the Har-
into the marrow space and are lined with smooth ris' lines in both distal tibiae. Since the distances
compact bone indicating a long-standing chronic between all Harris' lines are greater in the osteo-
condition. myelitic tibia it would appear that accelerated
The proximal metaphysis of the left tibia con- growth has characterized all stages of the disease
tains a cloaca in the anterior cortex. There is a process. Table 4 shows the distances between the
small, bony spur on the lateral anterior cortex, distal Harris' lines and the growth plate. In every
NUMBER 28 125
TABLE 3.Distance (in millimeters) between the Harris' TABLE 4.Distance (in millimeters) between the distal
lines for the right (normal) and left (pathological) tibia of Harris' lines and the distal growth plate of the right (normal)
N M N H 378243 (lines 1 and 4 are indistinct in the left tibia, and left (pathological) tibiae of N M N H 378243 (lines 1 and
making the associated measurement somewhat speculative 4 are indistinct in the left tibia, making the associated
as emphasized by the question marks) measurement somewhat speculative as emphasized by the
question marks)
Left Right
Harris' line
(mm) (mm) Left Right
Hams' line
First to second 20(?) 18 (mm) (mm)
Second to third 27 21 First to growth plate 63(?) 50
Third to fourth 6(?) 3 Second to growth plate 42 32
Total 53 42 Third to growth plate 15 10
Fourth to growth plate 8(?) 3
case the distance is greater in the pathological long bones both suggest a muscular, robust indi-
tibia. vidual.
If we assume that growth in the distal tibia There are two pathological conditions in this
accounts for approximately two-thirds of total specimen. Undoubtedly, the immediate cause of
tibial growth, we can get an estimate of the age death was a bullet injury to the skull, in which
of the individual when the first Harris' line was the bullet entered the occipital region and exited,
formed. Doing this for the normal tibia only we with a typical fracturing pattern, through the left
find that there is 50 millimeters from the first parietal (Figure 176). The other pathological con-
Harris' line to the growth plate. This translates dition is a largely destructive process limited to
to about 75 millimeters total growth for the tibia the lumbar vertebrae and sacrum (Figures 177,
from the first arrested growth line. Extrapolating 178).
from Stewart (1968:133) the tibia grows about 17 The first lumbar vertebra is only slightly af-
millimeters per year between the ages of 4 and 9 fected by the disease process with barely visible,
years. At this rate, it would take approximately lytic foci on the lateral parts of the vertebral
4^2 years to add 75 millimeters to the total length body. The second lumbar vertebra has large,
of the tibia. Since the child was about 9 years old lytic, scalloped lesions in the posterior part of the
at the time of death, this suggests that the first vertebral body. These lesions are continuous with
Harris' line was formed between the ages of 4 and the spinal canal and on the right side extend into
5 years. Because this age is in agreement with the the transverse process. The proximal and distal
age estimated on the basis of the midshaft diam- endplates of the vertebral body and the true joints
eter of the sequestrated tibial shaft, this first of the superior and inferior processes are unaf-
Harris' line may coincide with the time of onset fected in the first two lumbar vertebrae. There
of the osteomyelitis. are three lytic depressions approximately one cen-
The second case I shall review in considerable timeter wide on the left lateral and anterior cortex
detail is an Eskimo specimen from Shishmaref, of the second lumbar vertebra. In all of the lytic
Alaska (NMNH 332611). This case is illustrative depressions there is a varying amount of bone
of the problems encountered in identifying the remodeling in the spaces of the spongy bone in
specific cause of an infectious condition. The the vertebral body adjacent to the disease process.
archeological age is uncertain, but a bullet wound This is a typical response by bone, particularly
in the skull indicates a date in the postcontact spongy bone, to a destructive disease process. In
period. slowly developing, chronic, destructive condi-
The specimen is clearly male with an age at tions, there may be a continuous wall of bone
death estimated to be about 23 years on the basis adjacent to the disease focus. There has been a
of pubic symphysis morphology. The skull and limited, but incomplete, osteoblastic response to
NUMBER 28 127
the disease suggesting a somewhat chronic con- sive involvement in the lumbosacral vertebrae.
dition. In the third lumbar vertebra, the entire Both osteomyelitis and tuberculosis are strong
vertebral body, the left transverse process, and possibilities and neither can be ruled out. There
the left superior articular process have been en- are several factors, however, that more strongly
tirely destroyed. There is a slight amount of indicate osteomyelitis.
reactive bone adjacent to the lytic areas. The It has been noted that vertebral arches, joints,
spinous process is normal. Like the third lumbar, and spinous processes are almost never destroyed
the vertebral body of the fourth lumbar vertebra in tuberculosis (p. 145). In this specimen there is
has been completely destroyed. However, all ar- destruction of transverse processes, diarthrodial
ticular processes are present, although the left intervertebral joints and portions of the arch.
articular facets have been partially destroyed. Furthermore, the extent of osteoblastic response
There are long spurs coming off the transverse at this stage in the lytic process would be less
processes with the most prominent one found on likely in tuberculosis than in osteomyelitis.
the right side. The anterosuperior plate of the
body of the fifth lumbar vertebra is destroyed.
However, the articular surface of the inferior Periostitis
body is largely intact. There is a large depression
PATHOLOGY
on each of the sides of the vertebral body and
evidence of cavitation, mostly destroyed postmor- Periostitis, as a disease by itself, is uncommon.
tem, on the anterior vertebral body. There has It usually represents part of, or a reaction to,
been some osteoblastic activity, which had begun pathologic changes of the underlying bone. The
to fill in spongy bone forming a new cortex. The inner layer of the periosteum retains osteoblastic
vertebral processes are generally intact although capacity throughout life, even after termination
the left superior articular facet is porous with fine of growth. It is, therefore, not surprising that the
reactive bone around the porous joint area. There periosteum reacts to many different insults with
is some periosteal reaction on the left dorsal lam- formation of woven bone, which later may be-
ina. In the first segment of the sacrum the antero- come incorporated into the underlying cortex and
superior portion of the body is destroyed as is remodeled into lamellar bone. This periosteal
the inferior body of the same segment. There are bone formation is not always an expression of
large, well-circumscribed cavities in the body. inflammation and certainly not restricted to in-
Both alae of the first segment have a lytic cavity fection. In most of the infections discussed in this
extending into them. However, the articular sur- chapter, periosteal bone formation is one of the
face with the innominate bone is normal. The significant changes. Of these changes, first and
articular facets, sacral canal, as well as spinous foremost, inflammatory periostitis plays a role in
and articular tubercles, are unaffected. The sec- the infections of bone, specific and nonspecific.
ond segment is affected only on the superior Obviously, transitory periosteal reaction, which
portion of the body. There are lytic lesions 1 to 2 neither leaves permanent bone deposition nor
centimeters in diameter, some of which appear to resorptive pitting of the underlying cortex, cannot
be continuous with lesions in the body of the first be recognized on dry bone. This brings up the
segment. question: What are the characteristics of inflam-
In this case the lesions are predominately lytic, matory periosteal bone? There are no unequivo-
but with some time for an osteoblastic response cal characteristics. Generally, inflammatory peri-
to the disease process before the individual died. osteal bone deposited over a long period of time
The skeletal remains suggest a disease process tends to be unevenly distributed, not involving
with an initial, acute, destructive phase followed the entire bone. The surface tends to be irregular
by a short but more chronic phase with an exclu- and the thickness often variable. The marked.
130 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
PALEOPATHOLOGY
FIGURE 182.Ossifying periostitis of right tibia beneath leg While periostitis, as an isolated disease process,
ulcer, synostosis of tibia and fibula. (Adult, W M S 47.1 is uncommon in modern medical literature and
before 1831.) clinical practice, undifferentiated, nonspecific,
periosteal lesions of long bones are rather com-
mon in archeological skeletons. The main reason
bone. Large chronic ulcers on the skin, especially for this difference between clinical and paleo-
those due to venous stasis, not uncommonly pro- pathology is that many of the periosteal reactions
duce a reactive, local, ossifying periostitis on the may be part of the expression of a specific disease
tibia (Figure 179). This may represent a plaque- process, which can be identified in a living pa-
like deposition of periosteal bone of considerable tient, whereas in archeological specimens the
thickness, roughly copying the outline of the ul- pathological characteristics necessary to make a
cer. Occasionally such deposits may separate as specific diagnosis are not available. This would
shallow sequestra (Figures 180, 181). In other have the effect of increasing the frequency of
cases, rough exostosis-like osteophytes, which flat- nonspecific periostitis in archeological skeletal se-
ten out below the ulcer, may occur. This is ob- ries.
served particularly in tropical ulcer, a skin ulcer It is important to emphasize that periostitis (as
over the shin, characterized by presence of fusi- is also the case with osteomyelitis) has both a
form bacilli and saprophytic spirochetes (Brown general descriptive usage as a term and a discrete
and Middlemiss, 1956). Occasionally, such reac- usage. Thus, periostitis is part of a disease syn-
tive bone deposits may bridge the gap between drome such as syphilis, but it is also a specific
tibia and fibula (Figure 182). Massive reactive disease itself This varied usage of the term is well
periosteal bone formation of the mandible used illustrated in Brothwell and Sandison's book. Dis-
to be observed in the nineteenth century in per- eases in Antiquity (1967). The index to their work
132 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
lists six references to periostitis. Of these six, the syphilis forms on bones that tend to be near the
term is used five times in the context of a syn- skin surface, such as the tibia and skull vault.
drome associated with a specific disease, such as Such bones may be somewhat cooler than bones
syphilis. Only once is the term applied to primary like the femur, which are enclosed in a heavy
periostitis. Since we discuss secondary periostitis mass of muscle and fat. It is also true that bones
in the context of specific disease entities, the near the skin are more exposed to direct trauma
following discussion on the paleopathology of than bones protected by overlying muscle. Per-
periostitis will focus on the primary type. How- haps both these factors are significant in locali-
ever, the designation of primary periostitis in zation of periostitis.
paleopathological skeletons may mean only that The distinction between osteomyelitis and per-
a more specific diagnosis is impossible and does iostitis cannot always be made in dry bone spec-
not eliminate the possibility that the periosteal imens. However, in periostitis there will be no
reaction is secondary to a specific disease process. cloacae, involucrum, or changes in the marrow
Primary periostitis is most often the result of cavity. Furthermore, periosteal bone tends to be
two pathological conditions, trauma and infec- superficial to the normal cortex, at least in early
tion (Senn, 1886:5-6). Putschar (1966:60) notes stages of the disease condition. The superficial
that it is often impossible to determine which of nature of periosteal lesions can be seen in a
these two conditions gave rise to a given lesion in skeletal specimen from Ossuary II at the Juhle
an archeological skeleton. While the periosteum site near Nanjemoy, Maryland, USA (NMNH
will always be activated in fracture, periosteal 384380). The specimen is dated to the sixteenth
reactive bone can also be stimulated by injury century A.D. There is no evidence of European
that does not produce fracture. The latter may contact. T h e secondary nature of the burials
resemble periosteal reactions stimulated by local- makes it virtually impossible to obtain complete
ized infectious foci. skeletons. However, the two long bones in ques-
Traumatic periostitis is brought on by sudden tion, the left ulna and tibia, exhibit similar peri-
or chronic insult to bone. Wood-Jones (1910b: osteal lesions and both are from an individual
285-286) has described a periostitis of the skull between 14 and 18 years of age. Thus, the prob-
common in Nubian archeological specimens. The ability is high that the two bones came from the
initial lesion is characterized by hypervascularity same individual. The periosteal, reactive bone is
either on or near the vertex of the skull. However, superficial to the intact cortex (Figure 184) and
there are also small spicules of bone formed, and is porous fiber bone rather than compact bone.
later stages may be characterized by hypervas- There is no evidence of a cloaca or marrow
cularity and, in extreme cases, exfoliation of por- involvement. Thus, a diagnosis of primary per-
tions of the skull. Wood-Jones attributes this per- iostitis is justified.
iostitis to chronic insult produced by women In his study of pre- and post-Columbian Pecos
carrying water jars on their heads. This observa- Pueblo skeletal material, Hooton (1930:308-309)
tion is supported by the fact that the lesion occurs distinguished between periostitis and osteomyeli-
much more often in female skulls. Periosteal re- tis. Although he does not indicate the criteria by
actions of the skull are occasionally associated which this distinction is made, Hooton diagnosed
with trephination; however, here the periostitis is periostitis in 13 of 503 skeletons, an incidence of
probably due to complication of the surgical pro- 2.6 percent. There were four cases of osteomyelitis
cedure by infection. found in 503 skeletons indicating that periosteal
Periostitis of long bones is often seen in the reactions were more common. Morse (1969:17,
tibiae of archeological skeletons. The reasons for 106-111) presents four prehistoric cases of perios-
this localization remain obscure. It is, however, titis in his monograph on paleopathology in ar-
instructive to note that periosteal reaction in cheological skeletons from the midwestern United
FIGURE 184.Periosteal reactive bone on the left ulna of an
individual between 14 and 18 years of age. Some of the
periosteal reactive bone was broken away postmortem re-
vealing the underlying cortex (arrow), which exhibits mini-
mal changes. Specimen from an archeological site in Mary-
land, USA. ( N M N H 384380; scale in cm.)
of the hands and feet. The skull is normal except scessed teeth. The postcranial skeleton is incom-
for a slight amount of occipital flattening, dental plete. With the exception of severe arthritic de-
caries, and the loss of the lower left second molar generation of the right elbow, there is no evidence
antemortem. There is a supernumerary premolar of pathology except for a lesion on the shaft of
in the left mandible. The postcranial skeleton is the right tibia (Figures 187-189). This lesion
also normal except for a bilateral, diaphysial, begins at midshaft and extends distally 10 centi-
cortical thickening of the tibiae (Figures 185, meters. It involves both the medial and lateral
186). Grossly, the thickening takes place circum- sides of the shaft and encompasses most, but not
ferentially. The lesions of both tibiae are remark- all, of the circumference. On the medial side, the
ably similar. T h e bone surface of both lesions is lesion consists of fine porous bone with a longi-
smooth except for a medial focus, which has a tudinally striated appearance at the boundary
slightly raised plaque adjacent to a region of with normal bone. Laterally the lesion has a more
longitudinal striations. The overall appearance of irregular surface but is still composed of fine
the lesions is one of a well-contained chronic porous bone. Posteriorly there are two small iso-
process. There are no cloacae and no evidence of lated plaques of fine periosteal bone located dis-
fracture. tally to the main lesion. The overall appearance
The original cortex of both tibiae has been of the lesion suggests an active, but chronic,
partially remodeled near the main focus of the inflammation limited to a single bone of the
lesion. A somewhat greater amount of periosteal skeleton. The location, morphology, and circum-
bone has been added on the lateral side, and it is scribed nature of the lesion is suggestive of the
on this side that the maximum cortical remodel- bony reaction to an overlying skin ulcer. The X-
ing has taken place. The predominant lesion is ray picture of the two tibiae is of poor quality due
periosteal and thus it is appropriately classified to soil infiltration into the cortex and medullary
as periostitis. However, there is evidence of en- cavity. There has been a slight degree of remod-
croachment by bone reacting to the disease in the eling of the original cortex beneath the lesion, in
which the lytic process predominates. There may
marrow cavity. This means that the focus of the
have been slight encroachment into the medul-
lesion could have been the marrow cavity with
lary cavity by reactive bone, although the pre-
secondary activation of the periosteum, as does
dominant disease process is periosteal.
occur in osteomyelitis. However, the superficial
nature of the lesion and minimal medullary Another case from the same site in Canaveral,
change make a periosteal origin somewhat more Florida (NMNH 377516) illustrates a periosteal
probable. reaction apparently resulting from a penetrating
Another example of periostitis is seen in an wound into the medial tibia just proximal to the
archeological skeleton from the Canaveral Pen- midshaft. The main focus of the pathology on the
insula of Florida, USA (NMNH 377457). The tibia is a central, elongated, sharply outlined,
skeleton is an adult male approximately 30 years traumatic defect (Figures 190-191), surrounded
of age as estimated by pubic symphysis morphol- by a thickened periosteal lesion. There is a second
ogy. Arthritic degeneration elsewhere in the skel- periosteal lesion just inferior to the tuberosity.
eton is suggestive of a somewhat older age. The This lesion does not contain a central cavity. The
presence of trade beads indicates a post-Colum- skeleton is an adult male with an age estimated
bian date for the site. The skull vault is normal, to be 24 to 30 years on the basis of pubic sym-
although the temporal portion of the temporo- physis morphology. There is a hint of reactive
mandibular joint exhibits considerable arthritic periostitis on the skull near vertex and a small
degeneration. The mandibular portion of the depression on the right frontal bone. The right
joint is much less severely affected. The dentition humerus has a thickened periosteal lesion in the
is considerably worn, as is typical of this popula- distal medial region. Adjacent to this lesion is a
lytic focus. The left ulna has a slight swelling of
tion, and there is evidence of at least two ab-
SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
136
the distal diaphysis with an irregular surface.
There is no corresponding pathological involve-
ment on the radius. A comparison of the lateral
roentgen images of the two tibiae suggests a slight
reactive remodeling in the marrow cavity of the
pathological right bone. However, the predomi-
nant lesion is periosteal. There is no apparent
sclerotic reaction surrounding the central cavity
in the most distal lesion.
If the tibial lesion was the only lesion in the
skeleton, a periosteal reaction to a local trauma
(perhaps a sharp penetrating object embedded in
the bone) would be the most probable diagnosis
and, indeed, this remains a strong probability.
However, the complications introduced because
of the other bone lesions raises the possibility of
a systemic disease affecting many parts of the
skeleton, but producing a more pronounced lesion
in a bone traumatized by a penetrating wound.
In any case, we do have a lesion on the tibia,
which is not bilateral and seems to be associated
with a localized trauma. As such, it provides an
example of what one might expect to find in
periostitis resulting from injury to bone.
There are several examples of periosteal reac-
tions to skin ulcers in the h u m a n skeletal collec-
tions of the National Museum of Natural History,
Washington, D. C. One of these illustrates the
distinctive external morphology associated with
this condition. This specimen is a right tibia
excavated from Ossuary II at the Juhle site near
Nanjemoy, Maryland, USA ( N M N H 384299).
This site is dated to the sixteenth century A.D.
There is no evidence of European trade contact.
There is a large area of reactive thickening on the
medial part of the bone just below the midshaft.
This lesion measures 65 by 40 millimeters (Figure
FIGURES 192, 193.Right adult tibia from the J u h l e site in Maryland, USA. This site is dated
to the sixteenth century. There is no evidence of European contact. 192, Anterior view; note the
large area of reactive bone on the medial side just distal to midshaft (scale in cm). 193, A
detailed view of the bony reaction to an overlying skin ulcer. Distal to this lesion is an additional
periosteal reaction, which is not as well organized (arrow). ( N M N H 384299.)
192). There is a nodular thickening superior to involves the external surface of the skull and
this lesion and another area of reactive bone on includes the contiguous portions of the frontal
the distal metaphysis (Figure 193). The sharply and both parietal bones (Figure 194). Less exten-
demarcated, thickened nature of the central le- sive lesions can be seen on the supraorbital region
sion is characteristic of a bony response to a skin of the left frontal, lateral left parietal, and left
ulcer. This case appears to have been complicated temporal bones. These last two lesions may have
by disseminated infection giving rise to the two been bilateral, although postmortem damage pre-
other foci of periostitis. vents confirmation on the right side. Porous le-
Periosteal skull lesions are also seen in archeo- sions are also seen in the left orbital roof. A
logical materials and present a challenge to the diffuse, porous lesion appears on the posterior
paleopathologist because of their resemblance to part of the skull, primarily on the parietals near
the expansive, porous bone seen in the anemias. the lambdoid suture. The maxilla, both facial
An example of skull periostitis is seen in a skull of and palatine portions, is also affected, as is the
a young child ( N M N H 377545). The dental age anterior portion of the mandible. In the temporal
of the specimen is about 3 years. T h e presence of bone, the maxilla, and the mandible, the lesions
trade beads indicates a post-Columbian date for appear to involve the spongiosa. The other le-
the site, located on the Canaveral Peninsula in sions, including the large lesion on the vault, are
Florida, USA. T h e major lesion on the skull superficial. A cut section from the left parietal
138 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Brucellosis
PATHOLOGY
METR IC
mil
1 SYST EM
n. n more than one vertebra (Lowbeer, 1948, 1949).
The lesion is a lytic cavitation. Grossly and on X-
ray, it frequently can be seen penetrating the
195 vertebral end-plate and extending through the
nucleus pulposus of the disc into the next verte-
FIGURES 194, 195.An extensive periosteal lesion concen-
trated in the anterior region of the skull vault: 194, T o p view
bral body (Figure 196). T h e cancellous bone
of skull. 195, Detailed view of cut section of bone including within the focus is destroyed without formation
areas of the lesion and normal bone. Note that the periosteal of significant sequestra. The cortex also may be
bone has been layed down on the intact cortex (arrow) and perforated, leading to parosteal abscesses. There
that there is no expansion of the diploe. (3-year-old child is usually very little, if any, reactive bone forma-
from a post-Columbian site on the Canaveral Peninsula,
tion except in the healing phase (Glasgow, 1976).
Florida, USA, N M N H 377545.)
In contrast to tuberculosis, which it resembles in
several ways, complete collapse of vertebrae with
gibbus formation is usually not observed (Keenan
shows the outer cortex to be intact with abnormal
and Metz, 1972) and paravertebral abscess is rare
bone, added in layers, superficially over the outer
(Kelly, Martin, Schirger, and Weed, 1960; Glas-
cortex (Figure 195). Unfortunately there are no
gow, 1976). Lesions in the pelvis likewise show,
postcranial bones associated with the skull.
NUMBER 28 139
endplates of the ninth and tenth thoracic verte- to some lesions seen in leprosy. Joint involvement
brae. T h e total bilobed appearance of the two in glanders is not rare, occurring mostly by exten-
cavities suggests an initial focus for the disease in sion from adjacent soft tissue lesions, and only
the intervertebral disk. This is an unlikely focus occasionally secondary to an epiphysial bone fo-
for tuberculosis, osteomyelitis, or mycotic infec- cus. In 27 cases gathered from the literature,
tions, but is typical for brucellosis (Glasgow, 1976: Beitzke (1934c) found distribution as follows:
286). The fact that the vertebral bodies have not Knee 16, elbow 4, ankle 4, toes 2, fingers 1, tarsus 1.
collapsed argues against tuberculosis. The roent-
gen appearance of the humerus has at least a
Tuberculosis of Bones and Joints
superficial resemblance to patterns seen in mul-
tiple myeloma (plasmacytoma), although the ir-
PATHOLOGY
regular distribution of the lytic process argues
against this disease. Tuberculosis is a chronic infectious disease
caused by Mycobacterium tuberculosis of the human
Glanders or bovine type. The route of infection is usually
through the respiratory tract, leading to the for-
PATHOLOGY
mation of a primary focus in the lung, followed
by single or multiple foci in the regional hilar
Glanders is an infectious disease of horses and lymph nodes. Both lesions together form the pri-
donkeys, caused by the gram negative bacterium mary complex. Much less common is the intes-
Malleomyces mallei. The disease is transmissible tinal pathway with formation of a primary com-
from animal to man and from man to man. In plex in the intestinal wall and mesenteric lymph
animals and man the nasal mucosa is frequently nodes. The later course of the disease depends on
involved and often the portal of entry. Bone the size of the inoculum, the virulence of the
lesions in glanders are rare. The organism may organisms, and the resistance of the host. In most
affect the periosteum from adjacent soft tissue instances (at least in Western populations of the
abscesses and skin ulcers. There can be marked nineteenth century), the primary complex heals
periosteal reactive bone formation. Hematoge- without leading to a progressive disease. If the
nous osteomyelitis in glanders is very rare and primary complex fails to heal, the lung lesion
inconspicuous (Beitzke, 1934c). The part of the progresses and tubercle bacilli may be early dis-
skeleton most often affected is the skull, secondary seminated through the bloodstream to other or-
to nasal and oral mucosal lesions. Involvement gans and tissues. Again, the number of organisms
with defects of nasal bones, nasal septum, eth- and the immunological capacity of the patient
moid, and sphenoid have been observed. Destruc- determine whether this early hematogenous dis-
tion of turbinates with perforation into the max- semination will lead to fatal miliary tuberculosis
illary sinus and perforations of the hard palate and/or tuberculous meningitis or to isolated or-
occur. Cranial vault lesions, secondary to ulcer- gan tuberculosis. Organ tuberculosis may not
ating glanders of the scalp, have been seen. Other make its appearance until years after the early
bone lesions in glanders are almost exclusively dissemination of organisms, and is precipitated
limited to the lower extremities, particularly the by lowered host resistence due to malnutrition,
tibia. The lesion may present as periostitis or other disease, or possibly local trauma. Since
osteomyelitis, occasionally with secondary infec- dormant primary pulmonary foci may harbor
tion by staphylococci, which modify the picture viable organisms for many years, late hematoge-
towards the appearance of ordinary osteomyelitis. nous dissemination also may become the source
The bone lesions in glanders are not diagnostic of organ tuberculosis. Skeletal tuberculosis is,
in dry bone. T h e main reason to mention them is with rare exceptions, the result of limited hema-
to point out the similarity to tertiary syphilis and togenous dissemination.
142 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
TABLE 6.Age distribution of skeletal tuberculosis in bones and joints listed in order of
decreasing frequency (after Alfer, 1892)
^ears old*
Location m in m in o in o o
-20
-30
-50
-45
-40
in
o CM en in
LD 1 1 1 1 1 1 1 1 00
1 1 o m in m o in in o in
o i n1
in o o o n t5
o CM
CM
CO CO
in
BONES
Spine 89 59 32 23 9 10 3 6 3 1 4 _ _ _
Tarsals and 9 20 26 38 14 10 10 7 6 8 11 9 9 5 2 1
metatarsals
Carpals and 16 12 16 23 12 5 1 5 3 6 2 2 4 2 _
metacarpals
Ribs - 4 9 8 5 9 5 5 10 - 7 2 2 1 -
Tibia a n d fibula 12 5 7 8 3 1 7 _ 1 1 _ 1 2 1
Radius and ulna 6 9 6 8 4 2 5 1 2 _ 2 1 2 _ _
Phalanges of fingers 15 7 4 4 1 2 2 - - - 1 1 1 - -
Temporal bone 6 4 2 3 7 5 2 3 1 - - - -
Phalanges of toes 2 6 5 7 1 1 2 1 2 - 1 1 - 2 - -
Pelvis 1 1 3 7 5 2 3 3 - - - 1 1
Sternum - 1 - 3 1 1 1 3 2 3 2 3 1 _
Femur 2 2 1 3 2 1 2 - - - - -
Humerus 1 2 1 1 - 1 1 1 1 - - - -
Scapula - 2 2 3 - - - - - - - -
Orbital margin 1 2 - 1 2 - - - - - -
Frontal bone - 2 1 1 - - - - - - - _
Maxilla - - 1 1 1 - _ 2 - - - -
Mandible 2 - - 1 3 - 1 1 - - 1 - _ -
Parietal bone - 2 1 1 - 1 _ _ - - - - - -
Sacrum - - - 1 - 1 - 1 - - _ - -
Patella - - - - - - - - 1 - 1 - - -
Clavicle - - - - - 1 - - - 1 - - -
Zygoma - 1 - - - 1 - - - - - - -
Occipital bone - - - - - - 1 - - - -
Coccyx - - - - - - - 1 - - -
JOINTS
Knee 47 52 47 37 20 11 23 11 11 3 2 8 6 3 -
Hip 58 59 43 46 9 11 6 - 4 1 1 3 - -
Elbow 7 14 14 21 12 9 6 5 9 8 5 2 2 -
Ankle 5 9 10 5 2 1 1 3 2 - 3 - 2 - -
Shoulder - 2 2 6 3 5 3 1 1 2 2 1 - -
Wrist 1 - 1 5 - 3 1 3 2 1 3 - -
Metacarpal phalan- - - 1 1 - 1 1 1 - -
geal joints
Metatarsal phalan- - 1 3 - - - - - - -
geal joints
Sternoclavicular - - 1 - I 1 - 1 - - - -
joint
Acromioclavicular - - - 1 - - - - -
joint
Multiple foci | 19 13 14 11 6 5 4 3 2 1 5 4 3 1 -
* Overlap in age categories is from Alfer and is not resolved here.
144 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Table 6. It indicates the great preponderance of little, if any, perifocal reactive bone formation is
skeletal tuberculosis affecting infants and chil- elicited, and often the involved bone shows peri-
dren. focal or general osteoporosis. The process in long
bones tends to remain localized, mostly to the
metaphysial or epiphysial portion. In contrast to
General Pattern of Bone and Joint Tuberculosis
purulent osteomyelitis, massive sequestra, espe-
Tubercle bacilli circulating in the bloodstream cially of cortical bone, are very uncommon. Peri-
locate within the skeleton, particularly in areas of osteal reactive bone is very limited or absent with
hemopoietic (red) marrow, which has a high cir- the exception of tuberculosis of small tubular
culatory and metabolic rate. These are, essen- bones in infants and children, characterized by
tially, the areas of cancellous bone rather than destruction or sequestration of the cortex and
the cortex or medullary cavity. As far as long formation of an expanded shell of periosteal re-
bones are concerned, this especially means meta- active bone (spina ventosa). Similar changes af-
physes and epiphyses in adults. In infants and fecting part of an involved long bone are observed
young children, the distribution of hemopoietic also in the young age group. Perforation of the
marrow is much wider so that tuberculous foci cortex with formation of an extraosseous abscess,
often occur in tubular bones of hands and feet with or without fistulous perforation of the skin,
and in ossification centers of tarsal and carpal is common. Traces of such an abscess can some-
bones in addition to occasional diaphysial lesions times be seen in the presence of reactive periosteal
in long bones. At all ages, vertebrae, ribs, and bone in the vicinity of the opening and, occasion-
sternum have hemopoietic marrow, which ex- ally, ossification of portions of the abscess wall.
plains the frequent tuberculosis of the spine at all In joints, destruction of the articular surface
ages. The flat bones, particularly the cranial may be minimal if the process is limited to the
vault, are more frequently involved in infants and synovium. Undermining and resorptive grooving
children than in adults. Joint tuberculosis is inti- of the articulating bones frequently occurs along
mately linked to involvement of the adjacent the line of synovial or ligamentous attachments.
bones and for that reason discussed here rather If the process started in the bone or involves bone
than separately. The process may begin in the extensively, destruction of the articular surface
synovial membrane or in the bone or simultane- and of the epiphyses with formation of cancellous
ously, in both. This is explained by the joint sequestra a n d / o r cavitation often occurs. Skeletal
blood supply to the epiphysis and the joint cap- tuberculosis can heal without specific or surgical
sule. In an advanced stage, the original focus therapy. Small foci, particularly in infants and
often cannot be ascertained. small children, may leave no trace, because the
The morphology of tuberculous lesions in dry area is removed in the process of subsequent
bones is not specific and overlaps considerably in growth and remodeling. Foci destroying a growth
appearance with manifestations of other bone plate will leave a growth deficit a n d / o r deformity
infections. However, there are some general char- of the involved bone in the young age group. Foci
acteristics of diagnostic value, in addition to the in the vicinity of a growth plate may lead to
age-modified distribution of the lesions in the excessive growth. This is not different from the
skeleton. effect of osteomyelitis. Joint tuberculosis may heal
The tuberculous process, in its exudative phase, with obliteration of the joint cavity, often termi-
permeates the marrow spaces, devitalizing areas nating in bony ankylosis with varying degrees of
of cancellous bone, thus leading to formation of volume loss of the constituent bones. After heal-
centrally located sequestra of cancellous bone ing, the spongiosa undergoes remodeling along
(caries). In its proliferative granulomatous phase, altered stress lines but never reaches the original
the process leads to local destruction and cavita- density of cancellous bone (Kastert and Uehlin-
tion in the cancellous bone. In either case very ger, 1964:467).
NUMBER 28 145
The Pelvis
ities with or without a central sequestrum, per- only to acetabular and femoral epiphysial foci
foration of the cortex, or fistula (Konschegg, 1934: but also to metaphysial foci of the femoral neck.
409-410). Extension of a psoas abscess into the In the Kastert series, one-third of the cases
ilium does occur (Figure 207). started from an extra-articular focus (Kastert and
PUBIS AND SYMPHYSIS.The pubis is rarely af- Uehlinger, 1964:508). In addition to the usual
fected by tuberculosis. Both sexes participate hematogenous route, direct extension to the hip
about equally and most instances concern older joint can also occur by contact with long-standing
children and young adults. T h e largest series abscesses from vertebral or pelvic tuberculosis. In
published are 27 cases of Fares and Pagani (1966), advanced stages of the disease, the point of origin
of which about half showed other adjacent or can no longer be determined. A series of 416 cases
remote tuberculous skeletal focj. There is appar- of tuberculous coxitis reported by Vacchelli in
ently no relationship to trauma or parturition. 1922 (in Kremer and Wiese, 1930:202) gives the
T h e lesion in adults is usually close to the sym- following breakdown: total destruction of femoral
physis, which may be involved. In that case, both head and acetabulum 22, diffuse involvement of
pubic bones may be affected (Kremer and Wiese, femoral head and acetabulum 220, diffuse syno-
1930:195). T h e lesion is lytic and destructive, vial tuberculosis 52, isolated osseous tuberculous
occasionally with formation of small sequestra. foci 122. T h e isolated foci were distributed as
Abscess formation and fistula are common. In follows: femoral head 60, femoral neck 24, ace-
children, the lesion may be medial to the hip joint tabulum 30, greater trochanter 8. T h e foci in the
because of the incomplete ossification of the pubic femoral head or neck may be small cavitating
area. lesions or larger triangular foci with a spongiosa
ISCHIUM.Similar lesions occur in the ischial sequestrum in the center. These foci may repre-
ramus (14 ischial compared to 20 pubic lesions in sent territories of terminal arteries. Acetabular
the series of Sorrel and Sorrel-Dejerine, 1932:76). foci predilect the posterior superior rim and the
In addition, occasionally an isolated lesion can cartilage-free center around the origin of the
occur in the tuber ischii, similar to the more round ligament (Figures 208, 209). Foci in the
common lesion in the greater trochanter (Blan- neck of the femur are often adjacent to the medial
koff, 1927). inferior cortex (Girdlestone, 1965:44,45). Exten-
sion of primarily synovial tuberculosis into the
bone occurs along the synovial attachment on the
The Hip neck of the femur. T h e weight-bearing articular
Tuberculosis of the hip joint is the second most surfaces are longest preserved. Ultimately, de-
frequent skeletal lesion after tuberculous spon- struction of the bones may be very extensive with
dylitis. All statistical series agree that the majority sloping upward extension of the acetabulum,
of cases start in childhood and that onset of the leading to upward partial or complete dislocation
disease after 25 years of age is rare (Johansson, of the remnant of the femoral head a n d / o r neck
1926:159; Sorrel and Sorrel-Dejerine, 1932:309). (Figures 210, 211). If the dislocation is complete,
In the series of Sorrel and Sorrel-Dejerine, com- a neo-acetabulum is formed on the lateral surface
of the iliac wing. In contrast to the appearance in
prising 995 cases, the maximal incidence of onset
congenital dislocation of the hip, the head of the
is at 4 to 6 years of age with a second smaller
femur is more eroded and there is no groove for
peak around puberty. There were only 28 cases
the round ligament, which is destroyed by the
in the fourth, 11 cases in the fifth decade, and 4
infection before the dislocation occurs. T h e old
cases beginning after 50 years of age. In the
acetabulum is not rudimentary and the neo-ace-
majority, the lesion starts with an osseous focus
tabulum shows evidence of infection. If there is
(Konschegg, 1934:461-462). T h e anatomy of the
extensive necrosis and destruction of the acetab-
hip joint allows early access to the joint space, not
NUMBER 28 151
FIGURES 212, 213.Tuberculosis of the left hip: 212, Anterior view. 213, Medial view. Notice
destruction of femoral head with exposure of porotic spongiosa a n d perforations of the involved
acetabulum. (Adult, I P M I K M 352.)
NUMBER 28 153
FIGURES 214, 215.Tuberculous arthritis of right hip with FIGURE 216.Chronic tuberculosis of right greater trochan-
complete destruction of the acetabulum and central dislo- ter with fistulating abscess, hip joint free. Notice scalloped
cation of the remnant of the femoral head; notice sparsity of destruction of greater trochanter exposing porotic cancellous
reactive bone: 214, Lateral view. 215, Medial view. (Male bone. (54-year-old female with pulmonary tuberculous focus,
about 30 years old, IPAZ 1940, old no. 2167.) FPAM, Jubilaumspital 857, autopsy from 1924.)
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
154
The Knee
shows a cavity with a central spongiosa seques- pals 68 times, metatarsals 32 times, and toes 11
trum and often some perifocal osteosclerosis. After times.
termination of growth in the adult, tuberculous In infancy and early childhood these short
foci of the calcaneus readily breaks through or tubular bones still have hemopoietic marrow
around the articular cartilage into the talocalca- throughout the shaft. In these small bones a focus
neal joint and from there spread to the tibiotalar will readily occupy the whole diaphysis, leading
joint (Sorrel and Sorrel-Dejerine, 1932:59-60). to ischemic necrosis a n d / o r penetration of the
The cuboid is much less often involved and thin cortex. The cortex may be rapidly resorbed
most of the patients are children (11 children, 2 or form a sequestrum. The elevated periosteum
adults). The ossification of the cuboid begins at forms a new bony shell, which accounts for the
3 months of age and terminates at 9 to 10 years. ballooned appearance of the involved bone (Fig-
Occasionally the navicular also is involved in ure 219). These lesions often accompany other
older children (6 cases in children, 1 adult). The skeletal manifestations of tuberculosis. If the child
ossification of the navicular begins at 2V2 to 5 does not die from tuberculosis located elsewhere,
years of age and terminates between 10 and 12 the lesion usually heals. Destruction of the growth
years. The cuneiformes are rarely involved; if plate in metacarpals and metatarsals, and, less
destroyed, medial deflection of the foot may oc- commonly, of phalanges, may lead to marked
cur. Foci like these may remain isolated in chil- shortening of the digit after healing. If this is not
dren and may heal without joint involvement.
All these data are taken from the discussions of
Sorrel and Sorrel-Dejerine (1932:63-65). In
adults, tarsal bones not uncommonly participate
in extensive tuberculosis of the ankle. The differ-
ential diagnosis between tuberculosis and sub-
acute osteomyelitis on isolated tarsal lesions may
be impossible on dry bone.
The Elbow
The Wrist and Carpal Bones uration of the constituent bones. In children be-
low 4 years of age, the carpus is mainly a block of
The wrist consists of three partly separated cartilage with minimal focal ossification. At this
joints: the radiocarpal joint, the intercarpal joints, stage carpal tuberculosis is not observed. From 4
and the carpometacarpal joint. Any one or all of to 12 years of age, carpal ossification centers
them may be involved in tuberculosis. The follow- become larger and more numerous. At this time,
ing discussion is mainly based on the detailed localized carpometacarpal involvement is ob-
study of Sorrel and Sorrel-Dejerine (1932:91- served, since adjacent bones are still protected by
120). They observed 63 instances in children and thick layers of unossified cartilage. The carpo-
51 in adults. The location and manifestation of metacarpal joint is uncommonly involved by ex-
the lesions vary greatly in different age groups. tension of a spina ventosa of an adjacent meta-
In children, the carpometacarpal joint is mainly carpal. In general, an active growth plate serves
involved and the radiocarpal joint is spared. In as a barrier for spread to the adjacent joint. The
adults, the process usually begins in the radiocar- metacarpals two to five are devoid of a proximal
pal joint and spreads rapidly throughout the joint growth plate. These localized joint lesions may
compartments of the wrist (Figure 224). The heal along with the healing of the accompanying
difference is explained by the anatomy and mat- spina ventosa, leading to bony fusion between
individual carpals and metacarpals. With increas-
ing age, the cartilage cover diminishes and exten-
sive joint involvement becomes the rule. In chil-
dren and adults, the joint lesion may originate
directly in the synovium or by contact with tu-
berculous tenosynovitis. In the adult, osseous de-
structive foci are not infrequently present in the
distal radial epiphysis and/or metaphysis. The
disease rapidly spreads through the entire wrist
and, in contrast to the infantile type, the proximal
row of carpal bones is more severely involved. In
healing, with various degrees of bone loss, the
entire carpus becomes a solid bone block, fused
to the radius and often to the base of the meta-
carpals as well.
The Thoracic Cage are more often affected than the upper or lower
ones and secondary involvement of adjacent ribs
RIBS.Tuberculous involvement of one or sev- can occur (Konschegg, 1934:407). Differentiation
eral ribs is not rare. Sorrel and Sorrel-Dejerine from osteomyelitis, fibrous dysplasia, and eosino-
(1932:84-88) observed 93 instances, of which 56 philic granuloma may be very difficult on dry
concerned children and 37 adults. The infection bone.
is usually hematogenous, but direct extension STERNUM.The sternum is much less fre-
from paravertebral abscesses and other adjacent quently involved than the ribs. Konig (1906:155)
tuberculous foci can occur (Kremer and Wiese, observed that ribs are five times as often affected
1930:283). The hematogenous foci predilect the as the sternum. T h e most frequent location is in
area near the osteocartilaginous border and may the manubrium (Figure 231). These lesions may
involve the cartilage secondarily (Kastert and extend into the sternoclavicular joint and involve
Uehlinger, 1964:515). The process creates a lytic the medial portion of the clavicle. The sternal
lesion with fusiform enlargement of the involved lesion is mostly lytic and may perforate the an-
area and often perforations of the cortex lead to terior or posterior cortex or both. In the differ-
chest wall abscesses. Periosteal reactive bone for- ential diagnosis, erosion of the manubrium by an
mation is usually rather meager. The middle ribs aortic aneurysm must be considered.
SCAPULA.The scapula is very rarely involved
except by extension of tuberculosis of the shoulder
joint into the glenoid fossa or the acromion. In
hematogenous tuberculosis of the scapula, the
vertebral margin is predilected (Kremer and
Wiese, 1930:301).
The Skull
''I^^^W -k T
1 r^^oer^''
234 w.
ear tuberculosis (Krause, 1899:54) (Figures 239, 242). Most of these cases show multiple skeletal
240). Occasionally the base of the occipital bone tuberculosis elsewhere. T h e lesions are superficial,
in the vicinity of the foramen magnum may leading to small sequester formation eliminated
participate in suboccipital tuberculosis of the at- through a fistula (Krause, 1899:54-55; Kremer
las and axis (malum suboccipitale) (Figure 241). and Wiese, 1930:153-155).
FACIAL BONES.In small children focal tuber- The bony walls of the nasal cavity may be
culosis of the inferior lateral orbital margin is not secondarily affected by extension of mucosal tu-
uncommon, involving the maxilla, especially at berculosis (Figures 243-246). T h e facial bones
the junction with the zygoma. Involvement of the also can be secondarily involved by long-standing
zygoma itself also is seen frequently. Chronic tuberculosis of the facial skin and soft tissues
tuberculosis of the zygomatic arch may lead to (lupus vulgaris), which often leads to destruction
an abscess, which typically ascends on the tem- of the nasal bones, as in leprosy (Figures 247-
poral squama along the temporal muscle (Figure 249).
NUMBER 28 165
^ ^-^ ^^
V
'. ^ l " "
^^^^^K^sip^^^^^. .
t
-S^r-jJ***^''""'")'''?.'!'''"
^^^^^^^^^^^k ^-
^'^T^^'^'^ <
2 H & -^
Columbian kyphotic Indian spines from New sive regeneration is a great rarity; even sponta-
York state. In this study he submitted photo- neous fusion of affected vertebrae is uncommon.
graphs and roentgen filrns of the three specimens In addition to these criteria, Morse argues that
to 17 specialists. The majority opinion of the the rarity of lesions in pre-Columbian skeletal
medical specialists was that in all three abnormal material argues against the disease being present.
cases the lesions were the result of tuberculosis, He bases this conclusion on the following argu-
although there were some dissenting opinions. ment. In his survey of American Indian groups
Lichtor and Lichtor (1957) published their ob- living in the American Southwest around the
servations on a pre-Columbian kyphotic spine turn of the twentieth century, Hrdlicka (1909)
from Tennessee. The tenth thoracic through the found the incidence of bone tuberculosis to be 7
fourth lumbar were involved with vertebral body cases in every 100 cases of tuberculosis. Since one
destruction followed by collapse, angulation, and of every 3 deaths among the Indians was due to
fusion. The authors conclude that the lesion is this disease, Morse (1961:493) suggests that about
characteristic of spinal tuberculosis. Roney (1966: 22 of every 1000 burial specimens should show
103) reports a case of thoracic vertebrae destruc- some evidence of tuberculosis. Morse (1961:493)
tion followed by kyphosis in a spine from an concludes that if tuberculosis was endemic among
archeological site in California. the prehistoric Indians, we should see more evi-
Morse (1961, 1967) reviews the evidence for dence of it than we do. Since lesions that might
prehistoric tuberculosis in America. He bases his be attributed to tuberculosis are rare, paleopath-
review on artistic representations of abnormal ological cases of such lesions are more likely to be
human figures suggestive of tuberculosis and on one of the several other pathological conditions
a critical evaluation of 15 cases of Indian skeletons that can produce similar lesions. One problem
that have vertebral lesions, possibly attributable with this argument is that social and environmen-
to tuberculosis. Nine cases were from published tal conditions in the post-Columbian period were
reports and six were based on original observa- very much worse for the American Indians. Both
tions by Morse. Of these 15 cases, Morse consid- these factors adversely affect the incidence and
ered only four to be sufficiently typical to allow course of tuberculosis. Thus the incidence re-
a strong presumption of spinal tuberculosis. One ported by Hrdlicka (1909) may not be indicative
of these four cases could not be dated to the pre- of the incidence in pre-Columbian times.
Columbian period with certainty. Despite the In his review of the 15 purported cases from
strong evidence of pre-Columbian tuberculosis in the Western Hemisphere, Morse (1961) most of-
the other three, Morse concluded that the exist- ten argues against the diagnosis of tuberculosis
ence of the disease among the prehistoric Ameri- on the basis of two criteria: (1) destructive lesions
can Indians had not been demonstrated. extending to more than four vertebrae and (2)
It would seem appropriate to review critically significant amounts of bone regeneration. How-
the criteria on which Morse bases his judgment. ever, Morse (1961:489) himself, notes that the
The following are the characteristics that he at- skeletal response to the tubercle bacilli is depen-
tributes to classic vertebral tuberculosis: (1) One dent on the virulence of the organism and the
to four vertebrae are usually involved, rarely host response. If the host had little ability to
more. (2) Bone destruction occurs with little or defend himself, then tuberculosis could cause a
no bone regeneration. (3) Angular kyphosis of the rapidly progressive type of acute osteomyelitis
affected spine is a frequent sequela. (4) Neural and early death. "If the host's resistance was
arches, transverse and spinous processes are rarely considerable, it is presumed that the disease then
involved. (5) Cold abscesses drain mostly along would be extra-chronic with the possibility of
the anterior surface of the vertebrae; they almost extensive healing and bone regeneration."
never drain posteriorly through the skin. (6) Mas- It is significant to note that in only one of the
168 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
' "f^K^'ff'--:'^:'--^\^>:
244
FIGURES 243-246.Tuberculosis of cranium with right fron-
tal and basal lesion: 243, External view showing small sieve-
like perforation of outer table. 244, Endocranial view show-
ing large dura-based lesion crossing the coronal suture. 245,
Destructive lesion of sphenoid-ethmoid area, endocranial
view. 246, Exterior view of skull base. (10-year-old female,
ANM 2439 from 1870.)
nine cases does Morse indicate age and it is that evidence regarding the presence of tuberculosis in
of a child. Furthermore, it is this case that pro- the Western Hemisphere during pre-Columbian
vides the most typical expression of vertebral times.
tuberculosis, implying that the acute or subacute T h e existence of valid evidence for tuberculosis
cases do not survive to adulthood. As a result in the New World in the prehistoric period has
acute or subacute cases show the primarily lytic, considerable significance for the diagnosis of le-
bony response typical of spinal tuberculosis. As sions in skeletal remains that could be attributed
has been stated, vertebral tuberculosis begins to tuberculosis. Morse (1961:491) lists 13 diseases
most often in early childhood (p. 145). This means that produce lesions that can be confused with
that the vertebral tuberculosis occurring in the tuberculosis. The most serious problems in differ-
adult probably reflects a chronic condition in ential diagnosis arises in distinguishing between
which the host response is at least sufficiently pyogenic osteomyelitis, perhaps the mycotic in-
adequate to insure survival through childhood fections, and tuberculosis. Brucellosis should be
and adolescence. In such long-term, chronic, added to this list. Assuming that all of these
adult cases the criteria of no more than four infectious conditions are endemic, tuberculosis,
vertebrae being involved with little bone regen- because it is the most frequent morbid condition,
eration may be less applicable. becomes the most likely diagnosis on the basis of
Morse's (1961:489) caution about attributing probability. Thus, the unequivocal demonstra-
a specific bone lesion in an archeological speci- tion of tuberculosis in the pre-Columbian New
men to tuberculosis is understandable and, in- World means that the disease was endemic and
deed, commendable, particularly at a time when acceptance of this diagnosis in more questionable
unequivocal evidence for tuberculosis in the cases becomes a more acceptable conclusion.
Western Hemisphere during pre-Columbian Three cases of possible bone tuberculosis in
times does not exist. Allison, Mendoza, and Pez- archeological specimens are presented to illustrate
zia (1973) have published a report of a case of the morphology of bone lesions associated with
tuberculosis in a naturally preserved body of a this disease. T h e first of these cases is a child's
child from southern Peru. The case appears to be skeleton from Pueblo Bonito, New Mexico
well-dated to about A.D. 700, clearly long before ( N M N H 327127). T h e archeological date for cul-
European contact. The child was a male between tural materials from this site is A.D. 828-1130.
8 and 10 years of age. The roentgen and gross T h e right femur of this specimen measures 265
appearance of the lumbar spine indicates partial millimeters (without the epiphyses) which indi-
destruction of the first three lumbar vertebrae. cates an age at death of about 9 years. This
The authors indicate that the burial position was estimate is in good agreement with age based on
unusual and suggest that the position of the legs dental eruption. Determination of sex in a child's
of the burial is commonly seen in living individ- skeleton of this age is not reliable.
uals with paralysis of the lower limbs. While some of the bones are damaged or miss-
At autopsy, the mummy had a psoas abscess ing, the majority are present including some of
overlying the lumbar vertebrae and nodules re- the hands and feet. There is no grossly observable
sembling tubercles in the right lung. By rehy- evidence of disease in any of the bones except the
drating some of the recovered tissues it was pos- vertebrae. The first through the fifth cervical
sible to prepare stained histological sections, vertebrae are missing, although the sixth and
which revealed acid-fast bacilli in the tubercles. seventh are normal. T h e first through the tenth
The evidence from the roentgen, gross, and his- thoracic vertebrae are normal. T h e pathological
tological sources leave little doubt that the child process begins with the eleventh thoracic (Figures
suffered and probably died from tuberculosis. 250, 251). T h e superior surface of the body of this
This study would seem to provide unambiguous vertebra is normal, as are the transverse, spinous.
NUMBER 28 171
FIGURES 250, 251.Slight to pronounced destruction of the vertebral bodies of the eleventh
thoracic through first lumbar vertebrae probably due to tuberculosis: 250, Destruction of the
thoracic and lumbar (arrow) vertebrae has resulted in kyphosis; there has been a limited
amount of healing. 251, T h e right lateral view of the lower vertebrae; note the large cavity
(arrow) on the remnant of the body of T12. (9-year-old child from the pre-Columbian site of
Pueblo Bonito in New Mexico, USA, N M N H 327127; scale in cm.)
and articular processes. Cavitation is seen on the normal; however, there is slight deformation ap-
anterior and left portion of the vertebral body. parent in the lamina. This suggests the possibility
An enlarged canal resembling a cloaca occurs in of compensatory remodeling after the destruction
the left sector of the body. The inferior surface of of the vertebral body.
the body is eroded from the central to the left The superior surface of the body of L2 is eroded
side. All vertebral processes are normal. and fused with the remnant of L l . The inferior
The anterior body of the twelfth thoracic ver- body is intact but has slight exostoses on the left
tebra is destroyed leaving a scalloped spongy side. All processes are normal. The third through
surface in the remaining bone. There is no bony the fifth lumbar vertebrae are all normal except
fusion and the spinous, transverse, and articular for slight evidence of deformity on L5, which, like
processes are normal. the deformation seen in the lamina of L l , may be
The first lumbar vertebra is the most exten- a reaction to the kyphosis produced by the col-
sively affected bone with almost complete de- lapse and fusion of Ll and L2.
struction of the body. The left pedicle is fused X-ray films of the vertebrae demonstrate the
with the body of L2. All vertebral processes are anterior angulation (kyphosis) of the normal axis
NUMBER 28 173
of the spine. T h e collapse of the vertebrae pro- although the left ilium is visibly less flared than
duced an angle of about 110 degrees (170-180 the right.
normal). T h e film also shows evidence of bony In the lower extremities, the left tibia is missing,
response to the deformity in the form of reinforced although the right is normal, as are both fibulae.
trabecular bone in the affected vertebrae. X-ray Comparative measurements of the two femora
films of the femur suggest two, and possibly three, are presented in Table 8 and suggest significant
Harris' lines indicative of acute disease episodes differences.
at various times before death. The skull is badly
broken and deformed by actions subsequent to TABLE 8.Comparative measurements of the left and right
death and burial. However, there is no evidence femur in possible case of skeletal tuberculosis of archeological
of disease on the skull. The erupted teeth are specimen from Illinois, USA ( N M N H 381853)
normal. The age of the individual and the mor-
Measurement Left Right
phology of the lesion are compatible with a di-
(mm) (mm)
agnosis of tuberculosis, although other diseases
Maximum length 428 421
are possible. Morse (1961:500) provides a brief
Maximum midshaft diameter 27 29
descriptive summary of this case (his No. 10) and Minimum midshaft diameter 18 21
concludes that it is "quite typical of tuberculosis Neck-shaft angle 152 136
with destruction of vertebral bodies, angular de-
formity, and very little bone regeneration."
The left femur is grossly more gracile than the
The second case (Figures 252-255) is a skeleton
right. The neck and head of the left femur are
from Illinois, USA (NMNH 381853), whose ar-
more nearly in line with the long axis of the shaft
cheological provenience cannot be accurately de-
than the right (Figure 253). This condition (coxa
termined. In his brief report of this specimen,
valga) is typical when partial to complete paral-
however, Morse (1961:502) indicates that it was
ysis of the limb occurs during the growth phase.
probably late Hopewell or post-Hopewell Wood-
The abnormally large neck-shaft angle of the left
land (A.D. 200-1000). The age at death of this
femur, the reduced size of the shaft diameters,
individual was about 22 years and the sex is male.
and the diminished flare of the left ilium suggest
Only a few of the bones of the hands and feet
partial paralysis of the left limb perhaps caused
are present. None of these bones show any evi- by the collapse of the vertebrae.
dence of disease. The bones of the upper extrem-
In the vertebral column (Figure 252) the first
ity are normal. In the pelvis the sacrum is missing.
cervical is missing. The remaining cervical verte-
There are no gross lesions of the innominates.
brae are normal, as are the first three thoracic
vertebrae. On T4 there is a lytic lesion on the
FIGURES 252-255.Probable spinal tuberculosis in an ar- anterior inferior surface of the vertebral body,
cheological specimen from Illinois, USA: 252, T h e right with a similar but smaller lesion on the right
lateral view of the vertebral column. T h e entire vertebral portion of the body. T 5 - T 7 have a slight perios-
body of T 8 is destroyed and the posterior remnant is fused teal bony reaction on both sides of the posterior
with T 9 (arrow). 253, Anteroposterior X-ray film of the right
portion of the body. The inferior articular surface
and left femora, the fibulae, and the right tibia. Compare
the left femur with the right, noticing the diminished di-
of the body of T7 is eroded but shows evidence of
ameter of the midshaft and the increased neck-shaft angle of circumscription, although there is no exuberant
the left femur. 254, Detailed view of the major lytic and bone formation. The body of T8 is destroyed with
kyphotic focus in the vertebrae. T h e body of T 8 is completely the posterior remnant fused with T9 (Figures 254,
missing and the partially eroded body of T7 is resting on the 255). Both inferior articular facets are fused with
partially destroyed body of T 9 (arrow). 255, Lateral X-ray
their corresponding facets on T9 producing an
film of the area of angulation of the spine. Osteosclerosis is
apparent in the partially destroyed remains of the T 9 body
anterior angulation. The superior plate of the
(arrow) and in the body of TIO. ( N M N H 381853.) body of T9 is destroyed. There is some peripheral
174 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
reactive bone formation with a large, bony spur T h e upper extremities are normal although
on the right lateral portion of the vertebral body. small and suggest robust muscle activity. The
In TIO the articular surface of the vertebral body bones of the hands are small but appear normal.
is intact. There are bilateral bony spurs on the There is no evidence of disease in the vertebrae
vertebral body with slight cavitation on the an- either grossly or on the X-ray film.
terior surface. T I 1 and T12 are missing. T h e sacrum is normal, although small. The
The first lumbar vertebra has slight erosion of right innominate is small and somewhat de-
the superior articular surface of the body and formed in response to the pathological condition
lateral bony spurs with anterior cavitation. The in the left hip. T h e left innominate is grossly
inferior articular surface of the vertebral body is deformed, but the major focus of the infection is
normal. Both L2 and L3 show evidence of de- the acetabulum. The acetabulum is very shallow,
structive lesions on the anterior part of the body. an effect created by the destruction of the aceta-
There is a reactive spur joining L2 and L3 on the bular rim and articular surface with subsequent
right portion of their respective bodies with a remodeling and healing. There are large, well-
draining sinus affecting primarily the body of L3. organized osteophytes in the posterior rim area
L4, L5, and the sacrum are normal. The skull and a pronounced cavity in the inferior rim area.
and mandible were badly crushed and not avail- A well-developed bony ridge on the anterior-su-
able for study. perior margin of the acetabulum is suggestive of
In his review of this case Morse (1961:502) upward migration and subluxation of the joint.
expresses the opinion that such an extensive, de- There is a large hole through the acetabulum in
structive process would have resulted in rapid the region of the fovea. T h e overall gracility of
death and that the bony fusion of T 8 and T 9 the innominate is exemplified by the very delicate
must have occurred early in the disease process. ischial ramus.
Initially he suggests a type of acute osteomyelitis The left femoral head is destroyed with subse-
of short duration as the cause of the lesion. How- quent cavitation. Apparently this destruction
ever, he did not rule out tuberculosis and later took place in late childhood with diminished
(1967:257-258) included this case as one of four growth of the bone following the acute phase of
cases "considered typical enough to give a strong the disease. The measurements of the two femora
presumption of spinal tuberculosis." An alterna- highlight the differences in growth occurring after
tive opinion is that the destruction is suggestive the onset of the disease (Table 9).
of an acute initial condition. However, the bony
spurs, fusion, and draining sinuses are all sugges-
TABLE 9.Comparative measurements of the left and right
tive of limited recovery and a more chronic re- femur and tibia in a possible case of tuberculosis of the hip
sponse with life prolonged for some time (a year ( N M N H 345394)
or two) beyond the acute stage. The abnormality
of the left femur suggests a longer time. Left Right
Measurement
(mm) (mm)
The third case (Figures 256-258) is a skeleton
of an Eskimo from the Yukon River in Alaska FEMUR
( N M N H 345394). The archeological age of the Length from medial condyle 332 340
specimen is uncertain. The estimated age on the to greater trochanter
basis of epiphysial union and pubic symphysis M a x i m u m midshaft diameter 20 22
morphology is 20 years. The sex appears to be M i n i m u m midshaft diameter 15 20
male, although the small size for the long bones TIBIA
and the abnormal shape of the pelvis make sex Length from lateral condyle 299 290
determination difficult. The skull, which does not to medial maleolus
exhibit any gross pathology, is male in appear- M a x i m u m midshaft diameter 18 20
M i n i m u m midshaft diameter 13 15
ance.
NUMBER 28 175
257
The measurements of femora length do not shorter due to the destroyed femoral head and
include the diseased femoral heads and thus re- the pathological superior subluxation of the hip
flect the diminished growth of the pathological joint. The resulting abnormal gait undoubtedly
left femur. Notice that the left tibia has under- contributed to the deformity of both innominates.
gone accelerated growth, perhaps in an attempt In addition to diminished growth in length (en-
to compensate for the shortened left femur. In- dochondral ossification) there is reduced apposi-
deed, the total lengths of the femur plus the tibia tional growth (intramembranous ossification) of
for the two sides are virtually identical. This, the shaft diameter. While the left tibia has un-
however, would have left the left leg somewhat dergone compensating growth in length exceed-
176 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
ing that of the right side, its development in ing occurs, the early death of this individual
midshaft diameter is relatively deficient, suggest- would have precluded this effect. Furthermore,
ing only limited use of the limb in locomotion. subluxation is not typical in septic arthritis. While
The powerful development of the arms may be other diseases obviously cannot be ruled out, this
the result of using some type of crutch to assist in case does provide an example of what tuberculosis
locomotion. of the hip could look like in an archeological
The developmental difference between the legs specimen.
is also seen in the bones of the feet. The left
Leprosy
metatarsals have attained the same length as the
right, but have visibly narrower shafts. Curiously, PATHOLOGY
there is a lytic lesion in the right talocalcaneal
joint, which has affected the medial articular Leprosy is a very chronic granulomatous infec-
surface of both bones. The lesion is somewhat tion of man caused by Mycobacterium leprae, which
circumscribed, indicating containment of the dis- is acid-fast and Gram-positive. There is no known
ease process. The relationship of this lesion to the animal reservoir for the organism. Leprosy used
disease process in the left leg remains problemat- to be worldwide in distribution with the arctic
ical. regions the only exception. Presently, the most
It has been noted that differential diagnosis of affected areas are the tropical and subtropical
distinctive lesions in major joints is difficult (p. regions of Asia (India, Thailand, Indonesia, Phil-
144). Morse (1961:489) indicates that bone lesions ippines), Africa, and of the Americas. There is a
from tuberculosis in locations other than the spine predominance of male over female in a ratio 2:1
are indistinguishable from many other diseases. (Faget and Mayoral, 1944). T h e infection mainly
In view of the obvious problems in differential involves skin, mucous membranes, soft tissues,
diagnosis it is, of course, appropriate to avoid and nerves. The disease manifests itself either as
dogmatic assertions. However, with this caution lepromatous, with abundant bacteria in the le-
in mind, let us review the evidence presented thus sions, or as tuberculoid, with scanty organisms, or
far and seen in the illustrations of this case. an intermediate type. Peripheral, especially sen-
In addition to tuberculosis, osteomyelitis and sory, nerves of the extremities are often involved
septic arthritis are important entities in the dif- (neural leprosy) leading to loss of sensory percep-
ferential diagnosis. In tuberculosis, it has been tion in affected areas. T h e development and pro-
noted that the active phase leads to destruction gression of the disease extends over decades. Var-
and cavitation in the cancellous bone with little ious skeletal changes can be observed, based on
perifocal reactive bone. This description certainly three different pathogenetic mechanisms: (1) lep-
applies to the destructive process in the femoral romatous osteomyelitis and periostitis, (2) neuro-
head of this case. There is no evidence of seques- trophic bone and joint lesions, in neural leprosy,
tration or involucrum as would tend to occur in and (3) ordinary osteomyelitis and septic arthritis
osteomyelitis, nor is there fusion of the joint, due to secondary infection. In a series of 483
which is a common sequela in both septic arthritis lepers, 306 showed bone lesions radiologically
and tuberculosis of the hip. (Esguerra-Gomez and Acosta, 1948).
Furthermore, tuberculosis of the hip is second Lepromatous osteomyelitis is an uncommon
in frequency to the involvement of the spine in and frequently insignificant lesion, which may
bone tuberculosis and is the most common de- take decades to develop and involves only a small
structive lesion of the hip. Dislocation and per- portion of a bone. Only 5.6 percent of the lep-
foration of the acetabulum in the region of the romatous type showed specific lepromatous bone
fovea are also associated with hip tuberculosis. disease (Faget and Mayoral, 1944). Small bones
Although ankylosis is a common sequela if heal- of the extremities (fingers and metatarsals) are
NUMBER 28 177
predilected, mostly the epiphysis (Beitzke, 1934d: foot, the concentric resorption starts in the prox-
595). These lesions appear as lytic destructive imal phalanges and distal metatarsals, often spar-
foci, which may extend into the adjacent joint. ing the subluxed distal toes. The difference is
There is no periosteal reaction on the phalanges, probably due to the effect of local trauma (Faget
and no sclerosis is observed in the healing phase and Mayoral, 1944). At all times, one observes a
(Paterson and J o b , 1964:430). The bone may be complete cortex on these tapered pointed rem-
infected by the hematogenous route or, more nants of involved bones. Similar changes, with a
commonly, by direct extension from adjacent skin similar pathogenic mechanism, are seen in ad-
or mucosal lepromas. On the skull, destruction of vanced cases of rheumatoid arthritis, but in lep-
nasal bones, nasal septum, turbinates, and of the rosy no primary arthritic changes are seen. Severe
hard palate does occur (Job, Karat, and Karat, degenerative arthritis and even neuropathic ar-
1966). Erosions of the cranial vault, secondary to thropathy, similar to Charcot's joint, can be seen
lepromatous scalp lesions, can be observed. in weight-bearing joints of ankles and feet in
M0ller-Christensen (1953) has described the so- advanced cases of leprosy. In addition, the exist-
called facies leprosa, which he observed on skele- ing anesthesia facilitates traumatic mutilations
tons with neurotrophic lesions from a medieval and secondary infections.
Danish cemetery of a leprosarium. The charac- Osteomyelitis and septic arthritis may modify
teristic features frequently found were the disap- the appearance of the skeletal lesions of leprosy
pearance of the anterior nasal spine, the rounding in the terminal phase. In mutilating leprosy,
and widening of the nasal aperture, and the hands or feet may be almost completely de-
partial resorption of the premaxillary alveolar stroyed. Even secondary tuberculous arthritis is
process with or without loss of the upper incisors. not uncommon (Beitzke, 1934d:611). In seven of
He usually found the bony nasal septum and, in eight autopsied lepers, active pulmonary tuber-
most cases, the hard palate intact. Similar lesions culosis was found (Brutzer, 1898). The specific
occur in tertiary syphilis and in lupus vulgaris. granulomatous bone lesions, especially in the pha-
Periostitis with subperiosteal new bone depo- langes of hands and feet, resemble very closely
sition is not uncommon (de la Camp, 1900; Rior- those observed in sarcoidosis (Paterson and J o b ,
dan, 1960). M0ller-Christensen (1953) frequently 1964:432). Mutilations also occur in both dis-
found finely, longitudinally striated, subperios- eases. Differentiation of these lesions on dry bone
teal bone deposits on the tibia and/or fibula on alone may be impossible (see also page 233).
skeletons of medieval Danish lepers.
Neurotrophic changes in advanced leprosy are
PALEOPATHOLOGY
the most common bone and joint lesions observed
in this disease. Faget and Mayoral (1944) found Leprosy is one of the diseases in which features
such lesions in 66 percent of neural and 33 percent identified in archeological specimens have been
of mixed cases. Destruction of the sensory nerves of value in modern diagnosis (M0ller-Christensen,
with ensuing anesthesia, circulatory alterations, 1965:603). It has been noted in the discussion of
and local pressure (Coony and Crosby, 1944) lead the clinical aspects of leprosy that its distribution
to slowly progressive concentric atrophy of ter- was virtually worldwide until recently. However,
minal phalanges of fingers, metatarsals, and toes. while the evidence of leprosy in the ancient Old
Anesthesia often begins in the distribution of the World is convincing, its presence in pre-Colum-
ulnar nerve and, therefore, the terminal phalanx bian New World populations is doubtful (Coch-
of the fifth finger is usually involved first (Hop- rane, 1964:10).
kins, 1928). In the hands, the resorption begins in The earliest purported evidence of leprosy is
the distal phalanges and progresses proximally, from a Canaanite jar from Beth-Shan in Palestine
occasionally including the metacarpals. In the (Yoeli, 1955:331). The vessel is dated between
178 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
1411 and 1314 B.C. and shows features of the face M0ller-Christensen and Hughes (1966:243) con-
that resemble those associated with leprosy. Coch- cluded that this destructive process was probably
rane (1964:2) questions Yoeli's interpretation but the result of leprosy. They also found an addi-
indicates that there are references to a disease like tional Nubian skull from the same series, in which
leprosy in China dating to 600 B.C. The disease is leprosy was a probable diagnosis. Gladykowska-
first reported in Europe around A.D. 150, increas- Rzeczycka (1976) attributes to leprosy the lesions
ing to its most serious intensity between A.D. 1000 seen in an adult male skeleton (her No. 20) from
and 1400. By 1798, the disease had died out in a medieval cemetery located in Suraz, Lapy
Great Britain, although it continued to be a County, Poland. There is atrophy of the anterior
minor problem in continental Europe (Cochrane, nasal spine, evidence of truncated metatarsals,
1964:7). It was present in Norway through the and extensive periostitis of the long bones.
nineteenth century. Andersen (1969:123) suggests If, as seems probable, leprosy was introduced
that the disease may have been introduced into into the New World during the colonial period,
the Western World by the soldiers of Alexander archeological examples of leprosy should be rare
the Great on their return from the campaign in and limited to the post-contact period. I know of
India in 327-326 B.C. no reports suggesting the presence of leprosy in
One of the problems in using historical docu- the New World before Columbus. Indeed, leprosy
ments in studying the history of leprosy is the remains a condition rarely mentioned in the New
vagueness of the descriptions and imprecision of World paleopathology in the post-contact period
terms. MacArthur (1953:8) suggests that the term as well. This is not too surprising, since leprosy is
"leprosy" was used for nonspecific skin diseases, one of the least contagious of transmissible infec-
elephantiasis, small pox, bubonic plague, mange, tious diseases (Browne, 1970:640). Thus, its intro-
etc. He further suggests that many of the people duction into the New World would not have had
relegated to lazar houses in medieval times may nearly the impact of other infectious diseases,
have been suffering from diseases other than lep- such as small pox, malaria, and measles. M0ller-
rosy. However, Chapman Binford (1965), re- Christensen and Inkster (1965:12) have a refer-
sponding to a scientific paper read by M0ller- ence to an Indian skull from Vancouver Island,
Christensen (1965), emphasized that the work by off the coast of Canada, found in 1866, which
M0ller-Christensen on the cemeteries of leper they suggest had the facies leprosa syndrome
houses or hospitals in Denmark showed that most associated with leprosy.
if not all of the people buried there could have M0ller-Christensen's experience with many
had leprosy. This suggests greater precision in the skeletons from leper cemeteries having lesions
diagnosis of leprosy than MacArthur (1953) pro- presumably produced by leprosy provides signifi-
poses. cant insight regarding the bone changes to be
M0ller-Christensen's research (1952, 1953, expected from this disease (M0ller-Christensen,
1961, 1965, 1967, 1978) has provided empirical 1961). The major foci for the disease are the face
evidence for the presence of leprosy in Denmark and the small bones of the hands and feet, al-
during the Middle Ages. Wells (1962a) reports a though other bones may be affected. The skull
probable case of leprosy in a sixth-century A.D. lesions include the destruction of the nasal bones,
Saxon burial in Great Britain. Brothwell (1958: particularly the anterior nasal spine and hard
287) found lesions in a post-Conquest skull from palate. He also found a high incidence of cribra
Scarborough in England, which he attributes to orbitalia (usura orbitae) in leprous specimens
leprosy. Wood-Jones (1910b:283) describes an an- (1953:134-135; 1961:29). Henschen (1961:729)
cient Nubian skull in which the nasal bones, observed that cribra orbitalia may result from
including the turbinates and nasal septum, were insufficient nutrition and chronic inflammation.
destroyed. In the same specimen the major por- This suggests that cribra orbitalia may not be a
tions of the hard palate were also destroyed. primary lesion of leprosy but arise from the poor
NUMBER 28
179
able for study. However, M0ller-Christensen all three treponematoses affecting bone, the or-
(1953) does provide descriptions of bone lesions ganisms are disseminated throughout the body
in the extremities of other skeletons from the and reach the skeleton by the bloodstream.
Naestved cemetery, which resemble those dis-
Yaws
cussed earlier (p. 176). One possibly significant
diagnostic feature is that the metacarpals are not Bone lesions in yaws occur in about one percent
as severely affected in leprosy as the metatarsals of the patients (Wilson and Mathis, 1930). The
(M0ller-Christensen, 1953:141). location of such lesions in 101 cases observed by
Goldmann and Smith (1943) was as follows: tibia
46, fibula 20 (19 times with tibia), femur 13, ulna
Treponemal Infections 10, humerus 9, radius 7 (6 times with ulna), spine
5, clavicle 4, hand 4, foot 4, skull 3, ribs 3, pelvis 2.
PATHOLOGY
Since yaws is mostly acquired in childhood, the
Treponemal infections occur in four clinically most active lesions are seen in children and in
different diseases having a worldwide distribution adolescents. Many are similar to those seen in
through the tropical and temperate zones of all congenital syphilis. This is particularly true of the
continents. They are venereal syphilis, endemic often symmetrical dactylitis of the spina ventosa
syphilis (treponarid), yaws, and pinta, of which type and of the periostitis (Hackett, 1957:14-15).
only the first three may affect the skeleton. However, since it is not a disease of the newborn,
Whether they are caused by four different species osteochondritis is not seen in yaws. T h e early
of treponema or by variants of the same species bone lesions of yaws may completely heal without
is still unresolved and does not concern us here. leaving permanent bone changes. Another find-
The important feature is that bone lesions of ing frequently observed in yaws is bending of the
venereal syphilis, endemic syphilis, and yaws are tibia (boomerang leg) (Figure 261), which is very
so similar that diagnostic differences of individual similar to the saber tibia of congenital syphilis
lesions cannot be elicited with certainty (Hackett, and usually begins before 15 years of age (Wilson
1976). However, there is no evidence that yaws and Mathis, 1930). Hackett (1936:54-56) de-
produces the "worm-eaten" appearance of the scribes disseminated radiologic lucencies in the
outer table of the skull that is seen in syphilis anterior cortex in the early stages followed by
(Williams 1935:613). The geographic distribution anterior cortical thickening and bending. In the
before antibiotic eradication was very character- late stage, the posterior concave cortex is thick-
istic. Yaws was a worldwide disease of tropical ened and the anterior cortex thinned, as in late
indigenous populations. Pinta was restricted to rachitic deformities. Rarely, the fibula partici-
tropical America. Endemic syphilis was wide- pates in the deformity and occasionally radius
spread among indigenous populations of subtrop- and ulna show similar bending (Hackett, 1936:
ical North Africa, the Near East, and temperate 52-54). These changes are indistinguishable from
Asia, but not found in the Americas. Venereal postrachitic deformities and may not be due to
syphilis is a sporadic disease following the habi- yaws alone.
tations and colonizations of urbanized white Late yaws show destructive dactylitis of single
races. In all treponematoses, the infecting orga- phalanges. The long bones, especially the tibia
nisms enter the body through the skin or mucous and bones of the forearm, show gummatous per-
membrane near the skin surfaces. In venereal iostitis and osteomyelitis, very similar to tertiary
syphilis, Treponema pallidum enters mostly in areas syphilis. In contrast to early yaws, the overlying
of sexual contact, especially the genitals. In en- soft tissues frequently ulcerate and thus open the
demic syphilis and yaws, the infection may locate way for secondary pyogenic infections (Hackett,
anywhere on the body surface by intimate con- 1957:16).
tact, mostly already occurring in childhood. In
Skull changes mainly consist of destruction
NUMBER 28 181
essentially based on cases of venereal syphilis, which means, approximately before 1910. It is
with the understanding that similar or identical estimated that at that period about 10 percent of
lesions can occur in yaws and in endemic syphilis inhabitants of European cities gave positive se-
(treponarid). rological reactions for syphilis, which is not iden-
tical with active disease (McElligott, 1960). In a
Venereal Syphilis survey of 2000 cases of syphilis in Norway cover-
Venereal syphilis is transmitted through sexual ing the three decades from 1890 to 1920, Gjest-
contact. This type is called "acquired syphilis." land (1955) found that approximately one per-
However, the actively infected female can pass cent of the patients showed bone lesions. The
the organisms transplacentally to a fetus, so that combination of these figures would result in the
the infant is born with the disease. This type is frequency of syphilitic bone lesions in about one
called "congenital syphilis" and will be discussed in 1000 Europeans in the time period before
separately (p. 198). In view of the mode of trans- effective treatment was discovered (Hackett,
mission, it is obvious that, as a rule, acquired 1976:114).
syphilis commences beyond the age of puberty. The tertiary syphilitic bone lesions usually de-
After an incubation period of several weeks fol- velop between 2 and 10 years after the infection,
lowing the infective contact, a distinct primary but may occasionally occur earlier or much later.
lesion (chancre) usually develops at the point of Often more than one bone is affected. Although
entry. The ensuing long lasting disease is custom- any bone can be occasionally the seat of a syphi-
arily divided into three stages. litic lesion, there are a few areas that are greatly
The primary stage begins with the appearance predilected: the tibia, the bones surrounding the
of the chancre and ends with the involvement of nasal cavity and the cranial vault. These three
the regional lymph nodes, to which the organisms locations combined represent about 70 percent of
migrate. The secondary stage begins with dissem- all tertiary syphilitic bone lesions. These are fol-
ination of the organisms through the blood lowed in decreasing frequency by the cancellous
stream, characterized by transitory skin rash and bone, rich in hemopoietic marrow (ribs, sternum),
mucous membrane lesions. The borderline be- and the long bones of the extremities. A survey of
tween the secondary and the tertiary stage is not frequency from the greatest series of Fournier
as clearly defined. However, the tertiary stage is (1906, as cited in Beitzke 1934a:471) is given in
mostly characterized by progressive syphilitic in- Table 10. T h e spine is an exception to the behav-
volvement of different organs, as, for instance, the ior of other cancellous bones, rarely being in-
skeleton. It is in this stage that the tissue reaction volved by syphilis.
may assume a distinct granulomatous appearance Tertiary syphilitic bone changes are the result
of nodular foci with central liquifying necrosis of either chronic nongranulomatous inflamma-
(gumma). The character of the inflammation at tion or granulomatous (gummatous) processes. In
all stages is more chronic, with lymphocytes and many cases a combination of the two is present.
plasma cells predominating. Neutrophilic leuco- Either one of these changes can affect only a
cytes are not prominent and there is no significant localized area of the bone or the entire bone. The
formation of pus. Hypervascularity is usually inflammation may begin on the periosteum or in
marked. In the secondary stage periostitis is not the bone. Ultimately, however, periosteum and
uncommon, producing some periosteal bone. cortex, more rarely the medullary cavity, are
These changes are usually transitory and leave no involved. All tertiary syphilitic bone lesions are
characteristic permanent alterations on the bone. characterized by an excessive osteosclerotic re-
Our main interest centers on the bone lesions sponse to the infection. In many instances adja-
of the tertiary period. For the study of these one cent mucosal surfaces, as in the nasopharyngeal
has to go back to specimens collected before the area, and overlying skin, as on the scalp or shin,
advent of effective chemotherapy and antibiotics. or soft tissue are involved and ulcerated. The
FIGURE 262.Tertiary syphilis of cranial vault, outside view.
These are relatively early lesions with central destruction
and peripheral reactive bone. T h e inner table shows only
minimal diffuse reactive bone deposition. (Adult, A N M FIGURE 264.Syphilis of cranial vault with considerable
2232.) healing; top view. (HM P717.)
Bone No.
Tibia 248
Nose and palate 238
Skull 179
Ulna 37
Ribs 35
Sternum 29
Clavicle 27
Metacarpals 21
Humerus 20
Radius 17
Femur 16
Mandible 14
Fibula 12
Spine 9
Nasal bone 9
Fingers 7
Pelvis 5
Metatarsals 4
Scapula 4
Ribs and sternum 3
Tarsals 3 FIGURES 270, 271.Tertiary syphilis of cranial vault: 270,
Toes 3 Surface view, wet preparation, showing multiple scalp ulcer-
Maxilla 3 ations exposing the affected bone. 271, Endocranial view,
Patella 1 wet preparation, showing multiple perforations of the dura
Carpals 1 over the affected bone. ( G H P M 3914 from 1914.)
186 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
the nose results in the syphilitic saddle nose (Fig- Gummatous osteoperiostitis is a much more
ure 280). Major sequestration may be the result characteristic lesion. In its localized form it may
of secondary infection (Figure 281). result in tumor-like enlargement of the affected
The skull base is rarely involved, but extension bone area (Axhausen, 1913). In dry bone, the
of the nasopharyngeal process into the sphenoid marked hypervascular periosteal bony buildup
does occur, resulting in marked sclerosis of the surrounds a scooped-out defect, extending into
area (Schinz, Baensch, Friedl, and Uehlinger, the cortex. This corresponds to the location of a
1951-1952:627)(Figure 282). destructive gumma in the fresh specimen. At
T H E LONG BONES.The tibia is approximately times the scooped-out lesions are smaller and
10 times more often the site of syphilitic lesions grouped, resembling the picture of cranial caries
than any other long bone of the extremities (Fig- sicca, but individual gummatous defects tend to
ures 283, 284). The syphilitic lesions of long bones be larger than on the skull. The underlying cortex
can be separated into nongummatous and gum- is hyperostotic and endosteal bone formation may
matous osteoperiostitis. The nongummatous le- encroach upon the medullary canal (Figures 290,
sions are suggestive but probably not diagnostic 291). Diffuse gummatous osteoperiostitis resem-
of treponemal infection (Figure 285). Hackett bles closely the surface appearance of cranial
(1976:87-90) puts them into his "on trial" cate- caries sicca (Figures 292, 293). In some cases
gory of diagnoses. T h e localized form of nongum- larger defects are seen in the mantle of hypervas-
matous syphilitic periostitis may leave elevated, cular periosteal bone, exposing to view deep cor-
placque-like exostoses on the cortex of bones with tex (Figures 294-296) and sometimes small se-
a large muscle mantle (as the femur or questra. These lesions must not be confused with
humerus) (Figures 286-289), or circumscribed cloacal openings of hematogenous osteomyelitis.
buildup of surface parallel lamellar bone of vary- In contrast to that condition, major sequestra are
ing thickness and density on bones immediately missing, and the margins of the defects are rough
beneath the subcutis (as the anterior surface of and thin, and not smooth and sclerotic as on the
the tibia). Extensive periosteal thickening is often cloacas of pyogenic osteomyelitis. Hackett (1976:
combined with cortical thickening, including the 82, 93-97) accepts this form of osteoperiostitis as
endosteal surface. Diffuse nongummatous osteo- diagnostic of treponemal infection. Central gum-
periostitis tends to leave the bone thick and mas of the medullary cavity occur in the form of
heavy. The entire surface, with exception of the larger lytic lesions surrounded by a marked peri-
cartilage-covered articular facets, may be in- focal reactive sclerosis. This lesion may not be
volved. The periosteal bony buildup may be thick differentiated with assurance from a Brodie's ab-
and becomes firmly fused with the old cortex. scess, although the sclerosis is more marked than
The outer surface is rough and markedly hyper- in the latter. Pathologic fractures in bones weak-
vascular. In late stages of nongummatous osteo- ened by syphilitic osteoperiostitis are not uncom-
periostitis, the medullary canal may be com- mon.
pletely obliterated by sclerotic trabeculae, while T H E SPINE.Syphilitic osteomyelitis of the
the old cortex may be loosened up by Haversian spine is rare (Whitney and Baldwin, 1915) and
resorption so that, on cross-section, the bone ap- the changes in dry bone would not be diagnostic
pears uniformly coarsely cancellous with loss of in themselves. The outcome may be gibbus, after
the distinction of cortex and medulla. Differential destruction of adjacent vertebrae, similar to tu-
diagnoses from Paget's disease can be made mi- berculosis. In contrast to tuberculosis, a paraver-
croscopically by the absence of the typical Paget tebral abscess is missing; however, this may not
mosaic patterns in syphilis, in which bone depo- be obvious on dry bone. Also, in contrast to
sition is not interrupted by many phases of active tuberculous spondylitis, the cervical spine is af-
resorption. fected three times as often as any other segment
198 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
(Beitzke, 1934a:510). This may suggest extension livery of a living infected infant. If the infection
from nasopharyngeal mucosal lesions rather than is mild it may not manifest itself for several years
hematogenous origin. (syphilis congenita tarda). In massive infections,
T H E JOINTS.Syphilitic arthritis occasionally all organs and tissues of the fetus are permeated
occurs in the large joints (knee, shoulder, elbow) with numerous treponemal organisms. Since the
during the secondary stage (Glutton's joint). This immune capacity to mount an inflammatory re-
affection is transitory and leaves no changes visi- sponse is not yet developed in the first half of
ble on dry bone. Occasionally an epiphysial pregnancy, such aborted fetuses show no tissue
gumma may perforate into a joint and lead to changes. Furthermore, such fetuses are obviously
gummatous arthritis (Axhausen, 1913). The per- subject to rapid disintegration and, therefore, do
foration into the joint predominantly occurs near not concern us here. In premature and full-term
the margin of the articular cartilage (Freund, stillborns, as well as in actively infected newborn
1933). Subsequent bone changes, if present, are living infants, characteristic skeletal changes are
not significantly different from other forms of almost always present in form of syphilitic osteo-
arthritis, particularly degenerative arthritis. Only chondritis. This is the result of hematogenous
the presence of the gummatous bone lesion may dissemination of Treponema pallidum throughout
be a clue to the treponemal etiology. the fetus in utero. It affects all areas of enchondral
Indirect suspicion of syphilitic infection may growth in the entire skeleton but is most marked
be aroused by observation of pressure erosions of in the fastest growing metaphyses (distal femur
sternum, ribs, or thoracic vertebrae or from find- and proximal tibia). T h e lesions are symmetrical.
ings of a Charcot joint. However, it should be They consist of accumulation of calcified carti-
realized that not all aneurysms of the thoracic lage adjacent to an area of lucency due to poor
aorta are syphilitic and not all neuropathic ar- bone formation (Figure 305). This may represent
thropathies are the result of tabes dorsalis (nerve merely a toxic effect on the enchondral ossifica-
degeneration associated with syphilis). tion ("passive osteochondritis" of Schneider,
The multiplicity and complexity of tertiary 1923-1924:205) or be the result of formation of
syphilitic bone lesions is illustrated in selected syphilitic granulation tissue in this area ("active
views from two complete skeletons of the Pathol- osteochondritis" of Schneider, 1923-1924:205).
ogy Museum of the University of Strasbourg, Similar disturbances of enchondral growth are
France (Figures 297-304). seen in a variety of conditions and are not diag-
nostic of syphilis (Caffey, 1939). It is appreciated
Congenital Syphilis that these fetal and neonatal alterations will have
very little chance of recognition in archeological
Congenital syphilis was a common disease with material. In the surviving infants, transverse met-
high mortality before the possibility of effective aphysial pathologic fractures through this weak-
treatment of the infected mother during preg- ened area of the metaphysis not uncommonly
nancy. Among 4500 consecutive autopsies at occur (Parrot's pseudoparalysis). Since, in the
Johns Hopkins Hospital before 1933, there were infant, before walking, the arms are more me-
189 fatal cases of congenital syphilis, only two of chanically stressed than the legs, the distal hu-
which were older than 4 years of age (Smith, merus is the predilected site of such fractures.
1933). In congenital syphilis the treponemal in- This osteochondritis heals in the infant even if
fection is transmitted transplacentally from the untreated. Syphilitic periostitis often develops
actively infected mother to the fetus. T h e result during infancy, mostly following the osteochon-
is fetal death followed by abortion in the first half dritis. Occasionally it has already begun in intra-
of pregnancy, fetal death with delivery of a pre- uterine life and is present at birth. It consists of
mature or mature diseased stillborn fetus, or de- multiosseous, usually symmetrical, circumferen-
NUMBER 28 199
FIGURES 312, 313.Congenital syphilis with destructive lesion of right frontal bone involving
both tables: 312, Outside view. 313, Endocranial view. (8-month-old female, A N M 2233 from
1865.)
Columbus and may have been introduced into his subsequent conclusions. T h e problem, of
the New World by Columbus. A third point of course, is that so far there is no source that can
view is that treponemal diseases existed in both provide overwhelmingly convincing evidence for
the Old and New World before Columbus. any of the three hypotheses.
These different and conflicting opinions are While a comprehensive review of the basic
based on three distinct, but not necessarily mu- literature on the subject of the history of trepo-
tually exclusive, sources of information: (1) his- nemal diseases is beyond the scope of this work,
torical documents, (2) pathological remains, and a brief summary of the major concepts is essential
(3) speculation based on evolutionary theory. The to our subsequent presentation of paleopatho-
relative dependence of a scholar on one of these logical specimens. It also serves to highlight the
sources appears to have considerable influence on pitfalls of uncritical reliance on published sources.
FIGURE 314.Tertiary cranial syphilis (congenital?). Notice
active and healing lesions in frontonasal area, widened nasal
aperture, loss of nasal septum and inferior nasal spine, and
perforation of palate. (16-year-old male, A N M 2009 from
1870.)
European skeletons on which this conclusion was major integrating concept. In essence this concept
based. Undoubtedly, Bloch's reference to unnum- of treponemal diseases suggests that they have
bered thousands of skeletons of pre-Columbian evolved with man and migrated with him
age refers primarily to the work of Elliot-Smith throughout the world and thus were endemic in
and Wood-Jones on Egyptian material, where both the Old and New World long before Colum-
other epidemiological considerations need to be bus (Hudson, 1968; Cockburn, 1961; Hackett,
considered before one eliminates the possibility of 1963). Although not phrased in evolutionary
syphilis in that population. terms, the concept of treponemal diseases being
In discussing evidence for pre-Columbian syph- endemic in both Europe and the Americas goes
ilis in the New World we are primarily limited to back to an early report by Krumbhaar. He states
human remains and most of the evidence is from (1936:232): "Personally, I regard as most con-
the skeleton. With skeletal material there are vincing the theory of the existence of syphilis in
two fundamental requirements: (1) unambiguous both continents as far back as prehistoric times."
identification of treponemal disease and (2) un- Similarly, Stewart and Spoehr (1952) speculate
ambiguous determination of pre-Columbian ar- that treponemal diseases existed in the Old and
cheological age. Several purported cases of pre- New World but had developed different strains
Columbian syphilis have foundered on one or while isolated from each other. When contact
both of these factors. between the European explorers and indigenous
The earliest reference to syphilitic lesions in Americans occurred, they traded strains of tre-
New World skeletons is Jones' (1876:66) report ponemal organisms to which neither had devel-
on archeological skeletons from Tennessee. In- oped any immunity. This they suggest is the
deed, this early report appears to have been the reason for the syphilis epidemic in Europe after
basis for subsequent reports in which the authors Columbus and the increase in bony lesions pos-
concluded that syphilis was in the New World sibly attributable to syphilis in post-Columbian
before Columbus (e.g.. Lamb 1898). Morgan Indian skeletons in the New World. Stewart and
(1894) challenges Jones' conclusions calling into Spoehr's (1952) observations on the increase in
question both the diagnosis of syphilis and the syphilitic type lesions in post-Columbian indige-
pre-Columbian date. nous American skeletons is significant, because of
Many other purported cases of skeletal syphilis Stewart's extensive experience with New World
have been reported in New World specimens. skeletal material.
One of the most respected scholars studying this Hudson, in several papers, has attempted to
material was H. U. Williams, a pathologist, who reconstruct the evolutionary history of the trepo-
concluded on the basis of a critical review of nemal organism. In one of his earlier papers
published material and his own observations that (1958:23) he suggests that the treponeme evolved
the case for pre-Columbian syphilis was probable from a saprophyte (a microorganism that is
beyond reasonable doubt (Williams, 1932:978). closely related to the treponemal organism) early
He found the evidence for Old World skeletal in man's evolutionary history through the intro-
syphilis before 1490 to be much less convincing. duction of such an organism into a break in the
After a careful study of Eskimo and Aleut skulls, skin. He further speculates that this event may
Holcomb (1940:189) concluded that syphilis have taken place in Central Africa in an environ-
probably did not exist in these northern regions ment similar to the rain forest of today (Hudson,
of the New World until after contact with Russian 1965:890-891). Such an early disease would prob-
sailors and traders. ably have been similar to yaws of today, in which
The third source of speculation on the history the organism survives on the moist skin.
of treponemal diseases is based on theoretical Crucial to an understanding of Hudson's evo-
reconstructions with evolutionary theory as the lutionary history of treponemal diseases is the
206 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
concept that treponemal organisms represent a landmass as a mutant of the pinta treponeme and
"biological gradient" rather than separate spe- spread throughout the Old World. Endemic syph-
cies. In this scheme the various treponemal dis- ilis evolved from yaws during the drying trend
eases reflect adaptations by the same microorgan- following the last Pleistocene glacial period. As in
ism to varying epidemiological conditions. Thus, Hudson's reconstruction, Hackett associates the
when man moved to more temperate regions the development of venereal syphilis with the emer-
organism migrated to the more moist regions of gence of cities. However, he suggests that the
the body (the mouth, axillae, and the crotch), disease was mild until a virulent mutation toward
creating a new disease syndrome called endemic the end of the fifteenth century A.D. gave rise to
syphilis by Hudson (1965:891). the European epidemic attributed to the return
Hudson (1965:895) argues that the develop- of Columbus from the New World. Subsequent
ment of venereal syphilis was the result of devel- to this event venereal syphilis was spread through-
opment of the cities with the improved hygiene out the world during the European colonial ex-
associated with city life. Also the increased use of pansion in the sixteenth and seventeenth centu-
clothing prevented the frequent skin contact in ries (Hackett, 1963:38). Like Hudson, Hackett
children necessary for transmission of endemic does find a likely association between the evolu-
syphilis. After man's migration to the New World, tion of treponemal diseases and environment,
the development of the South American trepo- particularly climate. However, these two scholars
nemal disease, pinta, was, in Hudson's reconstruc- differ in the evolutionary mechanism. Hudson
tion, the result of a local adaptation, in which the supports the concept of a pluripotential organism;
treponeme was again introduced to environmen- Hackett evokes multiple mutations and different
tal conditions similar to those found in Central organisms.
Africa (Hudson, 1965:892). While these arguments may seem rather ar-
Hudson recognizes the inherent question in his cane, scholarly debates that are probably unre-
theory which is, why did venereal syphilis not solvable, it is important to stress that these spec-
develop sooner in the evolutionary process if all ulations do have a bearing on the interpretation
treponemal diseases are the result of adaptations of skeletal lesions or the lack of skeletal lesions.
in a single species? In response to this question he T h e historical and contemporary expression of
notes that immunity to the treponeme would be treponemal diseases suggests some variation in
acquired during childhood as the result of expo- the organ systems affected (Hackett, 1963:8-9)
sure to nonvenereal syphilis so that venereal and the virulence of the disease. These basic
transmission after sexual maturity was not possi- principles apply to the effect of treponemal dis-
ble until children no longer contracted the disease ease on the skeleton. Thus, the absence of skeletal
(Hudson, 1965:892). evidence of treponemal disease is necessary but
Hackett (1963) takes a somewhat different ap- not sufficient support for the absence of the dis-
proach in reviewing the origin and history of ease in an archeological population. Indeed, the
treponemal diseases. While recognizing that the arguments presented, particularly by Hudson
organisms associated with the four contemporary and Hackett, should make one cautious about
treponemal diseases are indistinguishable micro- assumptions of the absence of treponemal diseases
scopically, he continues to distinguish the diseases on any continent at any point in man's history of
as clinical entities (Hackett, 1963:9). In Hacketts's the last 10,000 years.
evolutionary scheme, treponemal diseases began Crosby's observation (1969:219) that the typi-
in the Afro-Asian landmass about 15,000 B.C. The cal evolutionary development of some infectious
syndrome was pinta, which spread throughout diseases is characterized by decreasing virulence
the world, subsequently becoming isolated in is a well-known epidemiological principle and is
America. Yaws, also, developed in the Afro-Asian based on the fact that those organisms that kill
NUMBER 28 207
the host generally die as a result, while organisms ness of the body on the left side. The maxillary
that are less virulent or infect individuals with a deciduous incisors are missing on the left. How-
more effective immune response tend to survive. ever, both right maxillary incisors have marked
Where a disease has been endemic for centuries, hypoplastic enamel defects (Figure 322). Indeed,
as Hudson and Hackett suggest was the case for the defect was so severe that the lower portion of
treponemal diseases, milder forms of the disease the right lateral incisor appears to have broken
and improved host-response could have devel- off antemortem. There is a less severe hypoplastic
oped in which the skeleton was not affected, as is defect on the left deciduous maxillary canine.
the case with pinta today. The enamel of the right canine has been damaged
postmortem, although there is a slight vestige of
a defect on this tooth as well. The deciduous and
Congenital Syphilis
first permanent molars are normal, as is the
Because of the problems in differentiating var- emerging permanent left central incisor.
ious expressions of treponemal disease in paleo- The dentition of the mandible is less severely
pathological specimens, most of the following case affected. The central incisors are hypoplastic with
descriptions will not be attributed to a specific antemortem loss of the superior portions of the
syndrome. An exception to this is an archeological crown. The lateral incisors have a very slight
example of probable treponemal disease in a 6- enamel defect. The remaining teeth appear to be
to 7-year-old American Indian child from Vir- normal, although the severe caries of both decid-
ginia (NMNH 379177). The sex of the child is uous second molars suggests weakened enamel.
unknown. There were no European trade goods Caries of the lower left first deciduous molar has
found at the site. Both the pottery types and the resulted in an abscess on the left side.
presence of stone pipes suggest a date before 1400. All of the major bones of the postcranial skel-
While a later date cannot be ruled out, the evi- eton exhibit porous periosteal lesions. The sever-
dence points to the pre-Columbian period. ity and thickness of these lesions varies and is
Lesions on the skull appear to be confined to significant in reaching a preferred diagnosis. Both
the face and forehead (Figure 320). There is some scapulae are normal, as is the manubrium. Both
postmortem damage to the skull, which compli- clavicles have periosteal bone deposits on the
cates the picture somewhat. The lesion on the anterior medial aspect of the diaphysis; the me-
forehead is located near the midline and measures taphyses are normal. Both humeri have patchy,
about 35 millimeters by 45 millimeters. It may periosteal bone deposits, which are limited to the
extend to the left of the frontal bone, but post- diaphysis. Involvement is slight and there is no
mortem damage precludes confirmation. The le- appreciable expansion of the cortex. The radii are
sion itself consists of periosteal bone, which shows somewhat damaged but clearly indicate a general
only slight evidence of porosity (Figure 321). The deposition of periosteal bone on the diaphysis,
most markedly abnormal bone tissue occurs which is more severe distally. There is a slight
around the nose. The nasal bones and the max- expansion of the diaphysis, and the metaphysis is
illary bone adjacent to the nasal bones and nasal normal. A similar distribution of periosteal bone
aperture have thickened, porous, periosteal bone occurs on the ulnae, but the diaphysial expansion
on their external surfaces (Figure 323). The re- is more marked. This expansion occurs through
maining portions of the maxilla appear to be the apposition of periosteal bone, but this is also
normal. There is a slight degree of porosity of the associated with an expansion of the marrow
orbital roof (cribra orbitalia). There are plaques space, although there appears to be a net increase
of porous periosteal bone on the inferior and in the thickness of the cortex.
anterior portions of the mandibular body. This is Many of the smaller bones of the hands were
accompanied by a slight expansion in the thick- not recovered during excavation, although all the
208 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
/I i,'.VJ
mr
210 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 329-332.Probable acquired syphilis in an adult female Indian from Arkansas, USA:
329, Right lateral view of skull; note that the reactive bone is minimal below the area of the
temporalis muscle. 330, Detailed view of the irregular, lumpy outer table of the right parietal.
This is a typical bony reaction to gummatous lesions. 331, Anterior view of the femora and
tibiae. 332, Detailed view of medial side of right femur near midshaft; note the bony bridging
that took place over blood vessels (white arrows) and the undercut periosteal bone (black
arrow). Such lesions are typical of bony reactions in treponemal disease. ( N M N H 258778.)
212 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
extensive. Broken sections of the frontal and the exhibits a slight labyrinthian periostitis, which
parietals reveal a thickening of the skull with may or may not be associated with the disease
almost complete fill-in of the diploe by compact process affecting the rest of the skeleton.
bone. The lesions of the external table are typical The proximal left ulna is the only long bone of
gummatous lesions characterized by a mixture of the upper extremity that exhibits a morbid con-
bone formation and destruction, creating an ir- dition. The lesion consists of an expansion of the
regular lumpy appearance. In this case, the proximal metaphysial cortex with slight porosity.
smoothed surfaces of the lesions indicate a long- Because of the rotation of the biceps tendon and
term chronic condition. The left orbital roof was the biceps tubercle of the radius, the superior
not recovered; however, the right orbital roof lateral portion of the metaphysis could not par-
NUMBER 28 213
338 'i
ticipate in this expansion, creating a depression the joint. However, the joints of the affected bones
in this region of the ulna. The insertion of the of the lower extremity are normal.
brachialis muscle is markedly rough with spicules The abnormal bone of the left femur is re-
occurring on the periphery of the insertion area. stricted to the proximal shaft and metaphysis
The joint surface itself shows a slight degree of (Figure 331). The lesion does not extend to the
breakdown on the coronoid portion, which may trochanters or the femoral neck. The disease pro-
reflect an expansion of the disease process into cess has resulted in concentric thickening of the
214 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
skull, sparing only part of the outer table under- larly in association with the most extensive lesions
lying the temporalis muscle, the alveolar portion on the outer table. There is very little evidence of
of the maxilla, the base of the skull, and most of healing and this is largely restricted to a slight
the occipital bone (Figures 333, 334). In general, remodeling (smoothing) of remaining bone pro-
the lesions are almost purely lytic, coalescing foci, jections. The penetrating damage on both parie-
which leave more or less intact projections of tals and the frontal appears to be postmortem.
bone between the foci. This creates the very The lesions in this specimen have a distribution
irregular surface seen on the frontal bone and on and morphology compatible with treponemal dis-
the posterior portion of both parietals. The de- ease, although the predominantly active nature
structive process was sufficiently severe to expose of the lesions is less commonly seen in such skel-
the frontal sinuses. The bones of the face are etons. The young age of the specimen, along with
affected as well, including the nasal spine, which the active nature of the lesions, suggests that the
has been destroyed. At the edges of the large individual died during the active phase of the
coalescing lytic lesions one sees fine, porous, peri- disease.
osteal, reactive bone (Figure 335). The lesions are The above specimen contrasts with another
largely confined to the outer table, although slight Eskimo skull (Figures 336-338), St. Lawrence
porosity is apparent on the inner table, particu- Island, Alaska (NMNH 280095). The mandible
216 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
there is a slight development of reactive bone at T h e third case of probable treponemal disease
the margins of the more active lesions. is also the skull of an Australian aborigine (Fig-
The general picture in this case is that of a ures 344-346) currently located in T h e Royal
more chronic course of the disease process with College of Surgeons of England Wellcome Mu-
considerable healing in the frontal region but seum (WM H S 50a.4). T h e date in the catalog is
with active lesions elsewhere. The more active 1811; thus the skull dates to before that year. In
lesions on the younger specimen from M u d Bay, contrast to previously described specimens, this
Alaska, may reflect a more aggressive course of shows much more extensive destruction, particu-
the disease, an earlier infection by the disease, or larly in the posterior portion of the parietals and
death occurring during the active phase of the the superior occipital bone (Figure 346). On the
disease and before any healing could occur. The frontal bone there are large carious defects with
specimen from St. Lawrence Island may have porous reactive bone on the boundary with nor-
acquired the disease later in life or the disease mal bone and evidence of some healing (Figure
may have taken a less aggressive course. 344). However, the occipital bone exhibits an
The pattern of healing lesions on the frontal active destructive process, which could be active
bone with more active lesions in the posterior syphilis or possible secondary pyogenic osteomye-
portion of the skull is also seen in three specimens litis (Figure 345). Again, the lesions exhibit a
located in the European pathology collections. pattern of increasing activity toward the posterior
The first of these is a specimen now located in portion of the skull.
the Wellcome Museum in London, but found on Hackett (1978) describes several cases of bone
Atui in the Cook Islands (WM S 50 A5). The lesions in pre-European skeletons from Australia.
skull probably dates to before 1850. Age and sex He attributes these lesions to yaws or treponarid
are unknown, but the condition of the teeth (endemic syphilis), since venereal syphilis is not
suggests fully adult age and the skull morphology thought to have been present until European
is female. There is considerable destruction of the contact. The long bone lesions of one of these
nasal bones and the hard palate (Figure 339). cases is shown in Figures 347 and 348. The lytic
The frontal bone shows extensive confluent lytic lesions in this case are quite different from bony
foci, which have been remodeled and healed. reaction seen in the femur of the specimen from
More active lesions are seen in the right parietal Arkansas, USA (Figures 331, 332).
bone (Figure 340).
The second specimen is the skull of an adult
Actinomycosis and Nocardiosis
aboriginal Australian. The skull appears to be
female and judging from toothwear was over 30
PATHOLOGY
years of age. It dates to before 1920 and probably
is much older. Currently the specimen is in the Actinomyces israelii is a higher bacterium, rather
Pathology Museum of The Royal College of Su- than a true fungus, and is a common saprophyte
geons of Edinburgh (PMES 1GD1(116)). The of the human oral cavity. Infections with this
frontal bone exhibits extensive, but mostly organism are uncommon and occur mainly in
healed, lesions (Figure 341). However, the lesions three areas of the body: cervicofacial, thoracic,
become more active in appearance toward the and abdominal. T h e organism enters through the
occipital region (Figures 342, 343). The most oral mucosa in the first area, by aspiration into
active lesions are seen in the occipital bone but the lungs in the second, and by the gastrointes-
extend up into the left parietal (Figure 342). The tinal route in the third. T h e cervicofacial location
skull has been sectioned and reveals a sclerotic is the most common (Nathan, R a d m a n , and Bar-
diploe similar to that seen in the archeological ton, 1962). Of 60 clinical cases reported by Baracz
specimen from Arkansas described earlier. (1902), 55 involved head and neck, 3 thoracic.
NUMBER 28 219
and 2 abdominal lesions. The distribution of the reported 73 incidents of skeletal involvement (15
disease is worldwide. The great majority of the percent). The bone or bones are usually affected
human infections is restricted to the soft tissue by direct extension of the infection from an ad-
and organs (lungs, liver, intestines). It consists of jacent soft tissue focus. This means that, in most
a protracted purulent infection with great tend- instances, the bone infection starts on the perios-
ency for local invasion and extension and fre- teal surface and frequently remains limited to it.
quent fistula formation. Bone involvement is un- Hematogenous dissemination, especially to the
common. In a study including statistics of 486 long bones of the extremities, rarely occurs. The
cases of human actinomycosis, Grassner (1929) frequency of actinomycotic lesions in the different
FIGURES 352, 353.Actinomycosis of lumbar spine and left pelvis, showing mainly periosteal
reactive bone deposition and hypervascularity with focal erosion of cortex: 352, Interior view.
353, Exterior view. (18-year-old male, FPAM 5686, autopsy 130155-1353 from 1909.)
spinous processes are usually spared. The inter- leading to cavitation and expansion of the bone,
vertebral discs are usually preserved. Lumbosac- is very rare in the human. By contrast, this is the
ral actinomycosis may spread to the pelvic bones most frequent type observed in bovines and
(Figures 352, 353). equines infected with Actinomyces bovis, which is
The mandibular lesions are mostly limited to usually not pathogenic for humans. In the rare
periosteal reactive bone formation of moderate actinomycosis of the maxilla, adjacent paranasal
extent with occasional destruction and focal ne- sinuses, facial bones (zygoma), and middle and
crosis of the underlying bone, especially of the inner ear may become involved. Destruction of
alveolar process. A central involvement of the mastoid process and petrous bone have been ob-
mandible, possibly through a dental alveolus. served.
222 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
In small and flat bones (ribs, sternum, pelvis), lytic cavitation, often complicated by fistula (Fig-
the destruction may be more extensive, creating ure 354). There is little, if any, reactive bone
a "worm-eaten" appearance and large cortical formed.
perforations. Actinomycosis of long bones is
rather rare and probably mostly the result of
hematogenous dissemination from a pulmonary Mycetoma (Maduromycosis)
focus. The area most frequently affected is the
metaphysis. Extensive destruction of the cortex PATHOLOGY
with reactive periosteal bone formation may be
Mycetoma or maduromycosis is a clinicopath-
observed, but large cortical sequestra, as in coccal
ological entity, caused by a variety of different
osteomyelitis, do not occur. Focal cavitation may
closely resemble a Brodies's abscess, but perifocal higher bacteria {Actinomyces, Nocardia, Streptomyces)
osteosclerosis is usually slight or wanting. and different true fungi of various genera that
occur in the soil (Winslow, 1971:591). The infec-
Joint involvement may occur, secondarily, to
tion almost always is located in the foot (Madura
lesions in adjacent bones. This is most often the
foot), much less commonly in the upper extremity
case in costovertebral and less commonly in in-
(Oyston, 1961)(Figures 355, 356). T h e disease is
tervertebral joints (Beitzke, 1934b:563). Pelvic
practically limited to tropical and subtropical
actinomycosis can extend to the hip joint and
areas. The geographic distribution illustrates this
proximal femur. Periosteal reactive bone is seen
point. In Asia, the disease is common in India,
in such areas. If actinomycotic arthritis heals,
particularly in the south, in Ceylon, and in the
bony ankylosis results.
Philippines. In Africa, the affected areas are Mad-
Nocardia asteroides is a bacterium of the actino-
agascar, Zanzibar, East Africa, Senegal, Tunis,
mycetales group which, in contrast to actino-
Algiers, Morocco, and southwestern Africa. In the
myces, grows aerobically and stains acid-fast. In-
Americas, the disease is not uncommon in Cuba,
fections occur through the pulmonary route and
Nicaragua, Costa Rica, Guyana, Brazil, Argen-
mostly are confined to the lung and pleural cavity
tina, and Chile. In the United States, 30 cases
(Pizzolato, 1971:1064-1066). In rare instances
had been observed before 1921, mostly in the
hematogenous spread to bones occurs. The lesions
southwestern states. In Oceania, cases were re-
predilect cancellous areas and mainly consist of
ported from Yap (Carolines). In Europe, myce-
toma was observed in Sardinia, southern Italy,
and Greece (Plehn, 1928). The infection occurs
through skin lacerations in barefoot-going popu-
lations, producing long-lasting, progressive, soft
tissue lesions with formation of multiple fistulae.
The bones become secondarily infected through
the periosteum. T h e tarsal and metatarsal bones
usually show multiple lytic foci and progressive
osteoporosis (Figure 357). T h e tarsal and ankle
joints frequently participate in the process. The
distal tibia and fibula as well as the metatarsals
are involved in advanced cases, showing multiple
cortical perforations and destructions with very
FIGURE 354.X-ray of nocardia osteomyelitis of pubis with little reactive bone formation. If the process heals,
fistula, proven by culture. (27-year-old female with pulmo-
bony ankylosis of the affected joints is to be
nary cavity, M G H 1293348.)
expected (Figure 358).
FIGURES 355, 356.Actinomycosis (maduromycosis) of left hand: 355, Volar view; notice
extensive periosteal involvement of carpals, metacarpals and phalanges. 356, X-ray; notice
subcortical involvement and cloacal openings on some bones. (Adult Iranian male, AFIP
859604.)
Paracoccidio idomycosis
North American Blastomycosis
Paracoccidioidomycosis is due to infection with
North American blastomycosis is caused by Paracoccidioides brasiliensis. This American fungus
Blastomyces dermatitidis, which usually enters the disease mainly occurs in Brazil, Venezuela, and
body through the respiratory tract. It can mani- Colombia but is found from Mexico to Argentina
fest itself as a skin infection, but frequently pre- with the exception of Chile, San Salvador, and
sents as a systemic disease (Witorsch and Utz, Panama. The disease mainly affects middle-aged
1968:169-171). Its main distribution is in North persons with a male:female ratio of at least 12: 1.
America, especially in the Mississippi and Ohio About half of the patients are farmers. Whites are
valleys and North Carolina, but presently it has most often involved and Negroes least (Angulo
worldwide distribution to some extent. In Can- and Pollak, 1971:511-513). Bone involvement is
ada, Ontario and Quebec have a significant num- not rare in disseminated cases. The lesions are
ber of cases. The male:female ratio in dissemi- round and lytic, single or multiple, or may mimic
nated cases is at least 5 : 1 . There is no distinct ordinary osteomyelitis (Emmons, Binford, and
racial predilection. The highest incidence is be- Utz, 1970:336). T h e predilected locations are
tween 30 and 50 years of age (Chick, 1971:466- clavicles, ribs, vertebrae, and extremities (Angulo
468). Two-thirds of the disseminated cases show and Pollak, 1971:555-556).
bone involvement. The predilected areas are ver-
tebrae and ribs (often multiple), skull, tibia, and
Coccidioidomycosis
tarsus. The lesions are usually purely lytic with
sharp borders (Boswell, 1959). In contrast to tu- Coccidioidomycosis is the result of inhalation
berculosis, vertebral collapse is rare. Paraverte- of spores of Coccidioides immitis. This disease is
bral abscesses occur. In long bones the focus can heavily concentrated in parts of Southern Cali-
mimic an infarct. The foci in long bones predilect fornia (San Joaquin Valley) but occurs in the dry
subarticular epiphysial and metaphysial areas. areas of adjacent southwestern states and Mexico
Periosteal reactive bone can be found (data from with additional foci in Central America, Vene-
Chick, 1971:485-486). zuela, Bolivia, and Argentina (Huntington, 1971:
NUMBER 28
225
Histoplasmosis
Aspergillosis
orbit or anterior cranial fossa can be observed. There are, however, no published cases of bone
Hematogenous dissemination is rare but may lesions in paleopathological specimens attributed
involve ribs or vertebrae. In vertebral aspergil- to fungal infections. Clearly in geographical re-
losis, collapse and gibbus occurs, which may gions where such diseases are known to have been
mimic tuberculous lesions (Pena, 1971:807-812). endemic in the historic period, it is probable that
they existed in ancient times as well. Lesions in
Mucormycosis (Phycomycosis) skeletal material recovered from such areas, such
as the American Southwest, should be studied
Several genera of Mucoraceae {Rhizopus, Mucor, with an awareness that fungal diseases represent
and Absidia) can occasionally become invasive a significant cause of conditions that can produce
opportunistic pathogens. Most of the patients skeletal lesions.
affected are diabetics in the acidotic state
(Straatsma, Zimmerman, and Gass, 1962). Exten- Viral Infections
sion into bone is seen in the cranial form of
PATHOLOGY
mucormycosis, starting from the nasal cavity with
involvement of the paranasal sinuses and their Of the viral infections involving the skeleton,
walls. The main reason for discussing this lesion only smallpox and rubella need to be discussed.
here is that perforation of the hard palate, with In chickenpox, bone and joint participation is
or without sequestrum, occurs, which may be extremely rare, and vaccinia osteomyelitis, rep-
confused with a tertiary syphilitic lesion. Since resenting a rare complication of prophylactic vac-
only one maxillary sinus is usually affected by cination, does not fall within the scope of this
mucormycosis, the perforation of the hard palate book.
is more often unilateral (Baker, 1971:835-860).
Smallpox
PALEOPATHOLOGY
Smallpox was a worldwide common viral in-
Fungal infections and their effect on human fection, especially in infants and children, before
bone have received little attention in the litera- the use of vaccination. Until recently, large areas
ture on paleopathology. Poswall (1976) has called of Africa had a high incidence of smallpox. As
attention to the presence of both coccidioidomy- late as 1958, Cockshott and MacGregor reported
cosis and blastomycosis in North America. She a series of 2500 cases observed in 18 months in
suggests that skeletal lesions from these fungal Nigeria, and Davidson and Palmer (1963) report
diseases may be distinguishable from other infec- 400 cases from southern Rhodesia. During my
tious diseases of bone and may be a more proba- w^ork in India and Indonesia in the 1960's I had
ble diagnosis for bone lesions seen in skeletal ample opportunity to study the radiological
remains of some American Indian groups. Morse changes of smallpox osteomyelitis and arthritis.
(1969:45) had included both blastomycosis and The skeletal involvement varies in different series
coccidioidomycosis as diseases that must be con- from 2 to 5 percent (Cockshott and MacGregor,
sidered in the diagnosis of destructive lesions of 1958:377, 1959:57; Middlemiss, 1962:11-13) to
the spine. Similarly, Buikstra (1976) has called about 20 percent (Davidson and Palmer, 1963:
attention to the need to differentiate fungal infec- 687). The skeletal infection starts between one
tions from other infectious conditions that affect and four weeks after onset of the disease; 80
bone. She indicates the importance of epidemio- percent of the patients in the series of Davidson
logical factors, as well as the morphology and and Palmer (1963) were less than 5 years of age.
location of the lesions in the skeleton, as helpful Skeletal involvement is not seen in the adult.
diagnostic features. Variola osteomyelitis, in contrast to most other
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
228
ondary to destruction or slipping of the growth stage causes echinococcosis in humans and do-
plate (Figure 363). Dactylitis may lead to short mestic animals (sheep, cattle, and pigs), which
stubby digits for the same reason. Joint involve- serve as intermediate hosts. This circumstance
ment may terminate in bony ankylosis. gives this disease a special paleopathological in-
terest, since human involvement would depend
Rubella on the domestication of the dog and the herding
of domestic animals. The present and recently
Rubella is a relatively harmless viral infection past geographic distribution of the disease is
of children and adults which, however, often has closely tied to the use of dogs in cattle and sheep
serious effects on the fetus, if acquired by the herding by people living under primitive hygienic
mother during the first trimester of pregnancy. In conditions. The disease occurs in two different
addition to the triad of congenital cataract, heart manifestations, probably caused by two different
defects, and mental retardation, frequent skeletal but closely related parasites. The common man-
changes have been appreciated only recently. In ifestation is the hydatid cyst, which has world-
a series of 81 infants with a history of maternal wide distribution. The European areas presently
rubella during pregnancy, 34 showed skeletal in- or previously involved are Iceland (with the great-
volvement (Singleton, Rudolph, Rosenberg, and est frequency in the past), Mecklenburg, Pomer-
Singer, 1966). The most characteristic lesions are ania, Friesland, Spain, Sardinia, Sicily, Yugo-
seen on X-ray in the metaphysial areas of the slavia, Hungary, Bulgaria, Rumania, Greece,
long bones of upper and lower extremities of the Russia, parts of France and Switzerland, and
newborn. The changes affect all metaphysial England. Outside of Europe, the areas of highest
areas but are most obvious on the distal femoral incidence are Australia and Argentina, followed
and proximal tibial metaphysis, reflecting the by New Zealand, South Africa, Uruguay and
greatest growth rate in these areas. These changes Chile. In my own experience, even presently,
consist of poor mineralization adjacent to the cystic echinococcosis is a common disease in Iran.
growth plate and coarsening of the reduced tra- The alveolar type of echinococcosis is much rarer
becular pattern. The diaphyses are not involved. and occurs in a more limited area: in Europe,
The lesion is similar to that of congenital syphilis, particularly in the Alps and their forelands (Ba-
but in contrast to syphilis, ossifying periostitis is varia, Austria, eastern France, Switzerland,
not observed in rubella (Highman, 1967). There northern Italy) and, to some extent, the Balkans
is general retardation of growth, and the skull and southern Russia. I have seen one case in
may show enlargement of the anterior fontanel northern Iran. In the areas where the alveolar
and poor mineralization. If the infant survives, form occurs, the hydatid form is rare (Posselt,
the bone changes disappear at about 3 months of 1900:238, 314).
age without leaving residual irregularities of ar-
In the heavily infested areas, echinococcosis is
chitecture; but the mortality rate in this group
a major health problem and a significant cause
with skeletal involvement was 32 percent (Single-
of death. As recently as 1935, Racic reported that
ton, Rudolph, Rosenberg, and Singer, 1966).
in Split (Yugoslavia) 70 to 100 percent of the
animals coming to the slaughterhouse were in-
fected with hydatid cysts and that he, alone, in
Parasitic Infections (Echinococcosis) 20 years operated on 269 cases of human echin-
ococcosis, including five involving the skeleton.
PATHOLOGY
Ivanissevich (1934) surveyed the problem in Ar-
The only parasitic infestation of the human gentina and found that 1 percent of all hospital
causing significant bone changes is the Echinococ- patients and 3 percent of all operated patients in
cus. Echinococcus granulosus is a tapeworm, which a large hospital in Buenos Aires suffered from
inhabits the small intestine of canines. The larval hydatid cysts. Similar figures are reported from
230 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Australia. In Concepcion (Chile), hydatid cysts cosis involving bone, the microcysts may not be
were found in about 1 percent of all autopsies recognizable grossly but, as in other tissue, the
and over 0.5 percent of all surgicals (Behn, 1938). parasite shows a more aggressive growth and
Slightly lower autopsy figures were reported from produces extensive necrosis and inflammatory re-
Virchow's Institute in Berlin (Boecker, 1868). In sponse (Klages, 1930:141). T h e main difference
this series of 33 cases, none were found in individ- between the two types is that the hydatid form
uals below 15 or above 70 years of age. resumes its macrocystic patterns when it escapes
The infection occurs either by direct contact from the confines of the bone into the soft tissue,
with dogs or by contamination of pasture, crops while the alveolar form always maintains its mi-
and drinking water with dog feces containing the crocystic destructive growth. There are very few
ova of the parasite. Domestic animals form the cases of alveolar echinococcosis of bone on record
reservoir, reinfecting dogs through their eating of and this type of bone lesion has never been found
or contact with the offal of slaughter. The embry- in Africa, Australia, or America.
onated ova, ingested, lose their shells by digestive The frequency of skeletal involvement in echin-
action of the stomach and penetrate with their ococcosis of the hydatid type is about 2 percent
six hooks the intestinal blood capillaries of the in the statistics of Ivanissevich (1934:17) from
portal system. Through the portal blood they
most commonly infect the liver but may, with
varying frequency, settle in any part of the body.
In the organ or tissue involved, the larva forms a
cyst, which consists of laminated chitin and is
usually surrounded, by the host, by a fibrous
capsule. The inner layer of a fertile cyst forms
many little tapeworm heads (scolices), each with
a crown of hooks. If such a cyst ruptures, each
scolex can form a new cyst. Hydatid cysts are
usually well tolerated by the affected tissue. In
contrast, the rare alveolar Echinococcus continues
to invade and destroy the infected tissue in the
form of a microcystic invasion, producing exten-
sive necrosis of the tissue and giving the gross
appearance of a malignant neoplasm. It was Vir-
chow (1856) who first recognized the parasitic
origin of this lesion.
The behavior of the hydatid type of echinococ-
cosis in the skeleton is different from that in
organs and soft tissues. Usually, no major cysts
are formed, but small cysts rupture and dissemi-
nate between the bone trabeculae, causing osteo-
clastic resorption. There is often foreign body
giant cell reaction around ruptured cysts but no
inflammatory reaction or fibrous encapsulation
(Ivanissevich, 1934). Extensive permeation of the FIGURE 364.Echinococcus granulosus cyst of left scapula
showing ballooning of the inferior angle and the lateral
marrow spaces may cause local ischemic necrosis
margin with sparse reticulated new cortex. (Adult, specimen
of the bone with formation of sequestra. By con- provided by Lord Joseph Lister's collection, before 1912,
trast, in the few instances of alveolar echinococ- W M S 54.1.)
NUMBER 28 231
Argentina and other series give similar data. Ac- means predilection, in the long bones, of the
cording to collective worldwide statistics of 406 metaphysis and, in the spine, of the vertebral
cases of skeletal echinococcosis published by Pas- bodies. The infection progresses very slowly over
quali (1930:369), the distribution through the decades and may remain asymptomatic for a long
skeleton is as follows: vertebrae 41.6 percent, hip time. The changes in different bones are different.
bone 22.1 percent, humerus 9.4 percent, tibia and In the spine, progressive destruction of one or
fibula 8.9 percent, femur 8.1 percent, skull 5.2 several vertebral bodies may lead to angular ky-
percent, sternum and ribs 2.2 percent, scapula 1.5 phosis, similar to a tuberculous gibbus. Trans-
percent, phalanges 0.7 percent. All bones are verse processes and posterior elements are more
occasionally involved, with the exception of the often involved in echinococcosis than in tuber-
carpal and tarsal bones and the ulna (Ivanissev- culosis. In flat bones, the outer contour is often
ich, 1934:21). The vertebral lesions form close to expanded by slow destruction of the old cortex
one-half of all cases, followed in frequency by the and formation of a new bony shell (Figure 364).
pelvic bones. The segments of the spine most The progressive destruction, especially of pelvic
often affected are the middorsal and sacral region bones (Doebbelin, 1898), may be extreme, leading
(Ivanissevich, 1934:21). to multiple large cystic cavities separated by re-
The parasites most often settle in areas of can- sidual bony septa (Figures 365, 366). The large
cellous bone with hemopoietic marrow. This cavities do not contain large parasitic cysts but
FIGURES 365, 366.Echinococcus granulosus cysts of left pelvis with secondary infection and
destruction of acetabulum, 18 years duration: 365, Lateral view. 366, Medial view. (Adult male,
G H P M 4196.)
232 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
numerous small cysts and tube-like membranes. and early Romano-British farmstead. In the left
Destruction of the floor of the acetabulum with side of the thoracic cavity, the excavators found
central dislocation of the head of the femur has a mineralized shell approximately ellipsoid in
been observed (Racic, 1935). On X-ray, the shape measuring 47 X 35 millimeters. T h e object
polycystic transformation and great reduction of was not attached to bone. Wells and Dallas con-
bony density is apparent. In the differential di- clude that the specimen is the mineralized shell
agnosis on dry bone, fibrous dysplasia has to be of a hydatid cyst produced in response to infes-
excluded. In this latter condition, the destruction tation by the tapeworm Echinococcus granulosus.
of the bony structure between the fibrous foci is Similar cyst-like structures are associated with
much less pronounced. The cystic form of hyper- an adult female skeleton from Jones Point, Ko-
parathyroidism can give a similar picture but diak Island, Alaska, USA ( N M N H 374623). The
would not be limited to one area. The rest of the skeleton is associated with what Hrdlicka called
skeleton would show other evidence of hyperpara-
thyroidism.
In long bones, the parasitic small cysts starting
in the cancellous bone of the metaphysis may
ultimately occupy the entire marrow cavity. Ar-
ticular or epiphysial cartilage forms a barrier,
which is not penetrated by the parasite. This
explains the absence of joint involvement. The
outer contour of the involved bone may not be
altered, but scalloping of the endosteal cortical
surface may be apparent on X-ray. Pathological
fractures occur frequently in the late stage of the
disease. Gangolphe (1894:675) observed in 25
cases of long bone involvement 14 pathological
fractures (humerus 5, femur 5, tibia 4). Ulti-
mately, even long bones may be extensively de-
stroyed if the cortex is transgressed and the par-
asites extend into the soft tissue. Reactive osteo-
sclerosis and periosteal new bone formation is
uncommon except in cases complicated by super-
imposed bacterial osteomyelitis.
PALEOPATHOLOGY
the intermediate, pre-Koniag period, which ges, the lesions predilect the distal epiphysis but
would have been before Russian contact. The do not break through into the interphalangeal
skeleton is incomplete and fragmentary, but the joints. The granulomas cause purely lytic, round,
skull and postcranial bones exhibit no external or slightly lobulated defects in the spongiosa,
evidence of disease. X-ray films of the major long varying from one millimeter to one centimeter or
bones, vertebrae, and innominates do not reveal more. If the granuloma is located in the diaphysis,
any cystic changes with the exception of a partial the cortex is markedly thinned and the shaft may
cyst-like structure in the cancellous bone of the be slightly widened, with loss of the dumbbell
right iliac crest. The postmortem damage of this shape of the bone. There is usually no significant
bone makes firm identification impossible. There perifocal sclerosis. There is no sequestra forma-
are, however, three fragmentary, ovoid structures tion. Perforations of the thin diaphysial cortex by
associated with the skeleton but not attached to the granulomas are not uncommon and create
any bones (Figures 367, 368). These fragmentary round defects. There is usually only minimal or
structures appear to represent three different mi- no reactive periosteal bone formation. Occasion-
neralized cysts. The external surfaces of the cysts ally phalanges, especially terminal, may be com-
are irregular with calcified spurs and holes in the pletely destroyed. Destruction of nasal bones oc-
surface, indicating that the external shell of the curs secondary to granulomas of the skin of the
cyst was not completely mineralized. Internally bridge of the nose (Holt and Owens, 1949).
there is no evidence of bony divisions in the cyst. Lesions of similar lytic character have occasion-
Wells and Dallas (1976) note that hydatid cysts ally been described in other bones, such as skull,
of Echinococcus typically are unilocular and may pelvis, long tubular bones, especially in the meta-
range in size from a pigeon's egg to as large as a epiphysial spongiosa, and vertebrae. The verte-
human skull. The mineralized cysts from this bral lesions are located in the vertebral bodies
specimen are very similar to the cyst illustrated and usually spare the intervertebral discs and the
by Wells and Dallas (1976, pi. 6). I would agree pedicles. Vertebral collapse may occur. Lesions
that the most likely diagnosis is that they repre- usually involve multiple, sometimes widely sepa-
sent the mineralized partial outer shell of a hy- rated, vertebrae and may show sclerotic rimming.
datid cyst resulting from Echinococcus infestation. In differential diagnosis, the hand and foot
lesions have to be differentiated from leprosy,
spina ventosa, and from osteochondromatosis
Sarcoidosis (Ollier's disease). In tuberculous and syphilitic
spina ventosa the widening of the affected bone
PATHOLOGY
is more pronounced; there is marked periosteal
Sarcoidosis is a granulomatous disease of un- new bone formation and a central sequestrum is
known etiology affecting mainly lymph nodes, often present. In Ollier's disease the enlargement
lungs, and skin. The disease is more often ob- and distension of the involved phalanges is much
served in adolescents and young adults than in more marked. There is also usually similar in-
children and is even rarer in infants. There is a volvement of large tubular bones of the same
marked racial predilection for Negroes. About 14 extremity while bilaterality is uncommon. The
percent of the cases show bone involvement greatest similarity exists between the bone lesions
(Mayock, Bertrand, Morrison, and Scott, 1963: of sarcoidosis and those of lepromatous leprosy
76). The bone lesions are usually multiple and (Paterson and Job, 1964:432). Both show the
often bilateral. same predilection of the phalanges of fingers and
The bone lesions are most commonly located toes, the lytic character of the lesions, and absence
in the fingers and toes, less often in metacarpals of reactive bone formation. A differentiation of
and metatarsals. The second and third phalanges individual lesions may be impossible on dry bone
are most frequently involved. Within the phalan- alone. The cranial lesion may be more character-
234 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
istic, since sarcoidosis mainly affects the nasal the intervertebral space, and, therefore, often in-
bones but not particularly the inferior nasal spine volves two adjacent vertebrae, while discontin-
and maxilla. The mutilating lesions have to be uous involvement of vertebral bodies is less com-
differentiated from leprosy, which would not usu- mon. The sarcoid lesions also have to be distin-
ally show simultaneously lytic lesions in other guished from metastatic lytic neoplastic lesions
phalanges. The vertebral lesions have to be dif- which, by contrast, usually involve the pedicles
ferentiated from those of tuberculosis and of os- and spinous processes multifocally.
teomyelitis. Osteomyelitis usually does not spare
Circulatory Disturbances
Blood Supply of Bones row, wide. They collect into a large, thin-walled
vein, running lengthwise in the medullary canal.
For the present purpose we are mainly inter-
The venous return in part follows the nutrient
ested in the arterial supply of the long bones of
artery, in part exits through multiple, circumfer-
the extremities. There is a separate arterial supply
entially located, venous outlets in the metaphysial
for the diaphyses, for the metaphyses, and for the
area. The epiphysial venous return drains into
epiphyses. The one or several larger nutrient ar-
that of the adjacent joint capsule. On smaller and
teries enter the bone through a grossly visible
cancellous bones the blood supply is less compli-
nutrient canal on the posterior aspect and branch
cated, except for those with growth plates, which
into an ascending and descending ramus in the
always lead to separate epiphysial and apophysial
medullary cavity. The metaphyses have several
vascular territories, at least during the growing
smaller nutrient vessels entering through the cor-
period. The vertebral bodies show a radiant ar-
tex around the circumference. The epiphyses re-
rangement of larger veins, which converge medi-
ceive several smaller arteries, which branch from
ally and emit on the posterior surface of the
a vessel that also supplies the joint capsule and
vertebral body through two foramina, close to the
synovium. During the growing period, the growth
midline. These segmental veins join the longitu-
plate completely separates the vascular territories
dinal vertebral plexus in the spinal canal, which
of the metaphysis and the epiphysis. After closure
is of some significance in the dissemination of
of the growth plate, some connections between
infection or malignancy. The diploe of the cranial
the two systems are reestablished, but the circu-
vault likewise shows large interconnecting venous
lation, to a large extent, remains separate. The
channels, which drain through the parietal and
intraosseous arteries, being enclosed in a rigid
mastoid emissary foramina but also have some
compartment shielded from external pressure, are
connection with the large intracranial venous
usually thin-walled. This is particularly true of
sinuses through small openings in the inner table.
the arterioles. The diaphysial cortex is, in part,
supplied by ramifications of the nutrient vessels,
in part by the periosteal vessels. The relative Ischemia and Infarction
contribution of these two systems varies in differ-
ent portions of the same bone. The epiphysial PATHOLOGY
vessels, which form a system of arcades beneath Continued cortical remodeling during adult
the articular cartilage, contribute to the nutrition life leads to formation of more osteon fragments
of the cartilage during the growing period, before and interstitial lamellae, which are devoid of vas-
formation of a more or less solid subchondral cular channels. With increasing age more and
bony plate. The cortical bone has vascular supply more of these fragments become necrotic (Miiller,
through the Haversian and the Volkmann canals, 1926). In arteriosclerotic peripheral vascular dis-
which connect Haversian canals and also enter
ease, extensive portions, especially of the cortex,
directly from the periosteum. Cancellous bone
can become necrotic (Jaffe and Pomeranz, 1934;
trabeculae are usually avascular, depending on
Sherman and Selakovich, 1957). Although micro-
the vasculature of the marrow spaces for nutri-
scopic study of the intact fresh specimen will
tion. The sinusoidal veins of the marrow are
reveal these changes, they are demonstrable on
.numerous, thin-walled, and, in hemopoietic mar-
X-ray and on dry bone only if reaction in the
235
236 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
adjacent living bone, in the form of bone resorp- necrosis of part or all of the femoral head (Figures
tion or bone formation, has occurred. In many 369, 370). This is due to the peculiarity of the
instances, such reactions to cortical necrosis do blood supply to the femoral head, which consists
not occur and therefore will not be recognizable of three groups of vessels: (1) the artery of the
in an archeological specimen. ligamentum teres, supplying a portion of the
In infarction, larger areas of the fatty bone upper part around the fovea; (2) the inferior
marrow and the intervening bone trabeculae un- metaphysial vessels coursing beneath the synov-
dergo necrosis, presumably due to interruption of ium on the inferior aspect of the femoral neck
the circulation. The lesion is almost exclusively
observed in the long bones of the extremities,
mostly in adults. The areas involved are princi-
pally the diaphysial and metaphysial marrow of
the femur, tibia, or humerus. The epiphyses, par-
ticularly the head of the femur or, less commonly,
of the humerus are also the sites of avascular
necrosis.
An infarction in the shaft of a long bone un-
dergoes calcification, particularly at the interface
between living and dead marrow, due to conver-
sion of the liberated fat into calcium soaps. In
fact, it is this change that makes the lesion visible
on X-ray as a circumscribed lesion, often of up to
10 centimeters in length, showing a radiodense
shell around the whole lesion and between its
individual components. There is little or no
change in the overlying cortex. It is questionable
whether calcium deposits could be preserved in
archeological material. Also, the sifting in of min-
eral particles into the marrow cavities of interred
bones may mimic infarction on X-ray.
In the majority of present cases a definite cause
for the infarction cannot be stated. Some known
causes of circulatory impairment are blood sludg-
ing in hemoglobinopathies, nitrogen gas emboli-
zation in decompression disease, and arteritis in
systemic lupus erythematosus. Circulating lipase,
a fat splitting enzyme, in extensive pancreatic fat
necrosis may also cause necrosis of medullary fat
tissue (Scarpelli, 1956).
FIGURES 369, 370.Aseptic necrosis of femoral head: 369,
Proximal right femur, anterior view, showing collapse and
cavitation of femoral head with sequestrum of necrotic bone
Necrosis of Femoral Head (arrow). 370, X-ray, showing reactive osteosclerosis on the
border of living and dead bone. (69-year-old male with
PATHOLOGY bilateral aseptic necrosis of femoral head for several years;
U S P H S surgical specimen 2427 of 1975, courtesy of Dr. B.
Subcapital or transcervical fracture of the neck Ragsdale, Armed Forces Institute of Pathology, Washington,
of the femur frequently is complicated by aseptic D. C., U.S.A.)
NUMBER 28 237
and supplying the inferior portion of the head; ing area of the femoral head, beneath the artic-
and (3) the lateral epiphysial vessels, which enter ular cartilage. Its further development and gross
the head within one centimeter distal to the and radiologic appearances are not different from
margin of the articular cartilage, supplying most those of known etiology, such as sickle cell anemia
of the femoral head and communicating espe- or Gaucher's disease. In systemic lupus erythe-
cially with the vessels of the ligamentum teres matosus, a disease of the connective tissue of the
(Trueta and Harrison, 1953). These are, appar- body, unilateral or bilateral necrosis of the fem-
ently the most important vessels. If they are sev- oral head is not uncommon (Dubois and Cozen,
ered by the fracture, aseptic necrosis always de- 1960).
velops, whereas the common severance of the
inferior metaphysial vessels bears no consistant
PALEOPATHOLOGY
relationship to necrosis (Claffey, 1960). The area
around the fovea is often spared if the ligamen- In the paleopathological literature, circulatory
tum teres is intact. disturbances have received little attention. Gray
If the fracture is survived for a long time, (1968) describes two possible cases of bone infarc-
inactivity osteoporosis characteristically will be tion in Egyptian archeological material. The first
present in any surviving part of the femoral head of these is a mummy (his No. 6) dated to the
and in the femoral neck, while the necrotic por- Greek period (ca. 330 B.C.). The mummy is cur-
tion maintains the trabecular pattern as of the rently located in the Horniman Museum in Lon-
time of fracture, if no revascularization and new don. Gray found radiodensities in the distal fem-
bone deposition has occurred. The necrotic por- ora and proximal and distal tibia, all of which he
tion appears dense on X-ray for several reasons: attributes to bone infarction. The figures of the
(1) the above-mentioned inactivity atrophy and X-ray films show radiodense lines circumscribing
osteoporosis in the adjacent surviving bone, (2) normal or radiolucent areas. The remainder of
the deposition of calcium into the necrotic tissue the skeleton is normal. The second case is a
of the fatty marrow, (3) the compression of dead mummy (his No. 7) dated to the Roman period
bone trabeculae into a smaller area during col- (first to second century A.D.). The distal portion
lapse, and (4) the deposition of new bone on dead- of the femur has a large, oblong radiodensity
bone in the process of repair. aligned with the long axis of the bone. Gray
Traumatic dislocation of the hip also can be attributes this condition to a solitary bone infarct
followed by aseptic necrosis. This is seen more or enchondroma. While these may very well be
frequently in posterior dislocations, especially if examples of bone infarction, all of the lesions
they are complicated by acetabular fractures. In illustrated in the published figures are suspicious.
traumatic dislocations the ligamentum teres is All the changes seen on the X-ray film could be
usually torn, and it is particularly an area on the due to dried overlying soft tissues or, depending
top of the femoral head that may become necrotic on burial conditions, to infiltration of the tissue
and demarcated as a sequestrum surrounded by by soil constituents. Final judgment on these cases
a sclerotic rim on its base, resembling a focus of should be postponed until these possibilities are
osteochondritis dissecans. eliminated.
The so-called idiopathic aseptic necrosis of the A possible case of necrosis of the femoral head
femoral head is not common. About 50 percent is seen in a proximal fragment of a left femur
of the cases are bilateral. Approximately 80 per- (Figures 371-374) excavated in an American In-
cent of the cases occur between 30 and 60 years dian site ih Arkansas, USA (NMNH 255142).
of age, and approximately 80 percent are in males The archeological age is uncertain. Most of the
(Jaffe, 1972:634). superior portion of the femoral head was de-
The necrosis usually begins in the weight-bear- stroyed antemortem creating two large confluent
238 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
I
^k. ^'fWt^ mtSjie.^
''>
'*
FIGURES 371-374.Necrosis of the femoral head of left femur fragment: 371, Anterior view.
372, X-ray of anteroposterior view; note the radio-dense sclerosis inferior to the necrotic defect.
373, Anterosuperior view of reactive bone. 374, Detailed view of reactive bone showing the
thickened trabeculae. ( N M N H 255142.)
depressions. The smallest of these is superior, oral head. However, periosteal reaction to an
lateral, and continuous with the femoral neck. aseptic inflammation arising from trauma is also
T h e largest depression involves about one-half of possible.
the area of the femoral head. There has been
considerable bony reaction in the depressions, in
which the exposed trabeculae have become Perthes' Disease and Slipped Femoral
greatly thickened indicating a long-standing con- Capital Epiphysis
dition. On the anteroinferior margin of the artic-
PATHOLOGY
ular surface there is a bony projection about one
centimeter square extending inferiorly. There is Perthes' disease is represented by extensive
noticeable periosteal bone deposition on the fem- aseptic necrosis of the epiphysis of the femoral
oral neck, suggestive of a low grade inflammatory head. It is an uncommon disease occurring uni-
condition. This raises the possibility of a septic laterally in 90 percent of the cases. It usually
condition contributing to the necrosis of the fem- begins between 5 and 9 years of age and involves
NUMBER 28 239
boys four times as often as girls (Jaffe, 1972:566). healed stage, the head, united with the neck in
The condition has been found in different races the slipped position, shows some dislocation of
but is rare in Negroes. the center of the head towards the axis of the
In the course of the disease the necrotic epi- neck. The neck is always short and thick, reflect-
physis increases in radiodensity, contrasted with ing both the attrition in the fracture area and the
focal radiolucency of the area of the femoral neck loss of enchondral growth for several years. As in
bordering the growth plate. Later the head flat- Perthes' disease, early and severe degenerative
tens, due to a combination of compression frac- arthritis complicates the picture. Occasionally,
ture and lack of enchondral growth. The basal upward dislocation of the femur is observed, cre-
bulge of the flattened head leads to subperiosteal ating a new "acetabulum" on the lateral aspect
and enchondral bone formation, thickening the of the ilium, while the slipped head is held in the
neck of the femur. The end result, after revascu- anatomical acetabulum by the ligamentum teres
larization, is a mushroom shaped femoral head (Schinz, Baensch, Friedl, and Uehlinger, 1951-
with overhanging margin but without significant 1952 (l):450-454).
dislocation of the center of the femoral head from
the axis of the shortened femoral neck. Early
PALEOPATHOLOGY
severe degenerative arthritis modifies the appear-
ance and can make the differentiation from the A right femur from the Valley of Chicama in
endstage of slipped femoral epiphysis difficult or Peru provides a possible example of Perthes' dis-
impossible. In the acute stage, the differentiation ease. This case is from a miscellaneous group of
from tuberculous coxitis and from aseptic necrosis femora all accessioned as N M N H 265331 at the
in Gaucher's disease may be uncertain in dry National Museum of Natural History, Washing-
bone. ton, D. C. The archeological age is unknown. The
Although slipped femoral capital epiphysis is epiphyses of the femur are fully fused indicating
not primarily an aseptic necrosis, it is best to full adulthood. The femur is 383 millimeters in
discuss it in this connection. The primary pathol- length and gracile, suggesting female sex. The
ogy of this lesion is a stress fracture between the diaphysis, distal metaphysis, and the joint surface
metaphysial side of the growth plate and the neck are normal. The maximum diameter of the fem-
of the femur. This allows medial posterior and oral head is 60 millimeters, much larger than
downward displacement of the head of the femur expected for a female. Part of the femoral head
and, not uncommonly, leads to some degree of was damaged postmortem, although enough re-
aseptic necrosis in the epiphysial bone. The dis- mains to indicate the nature of the pathology.
ease is uncommon and occurs more frequently in There is a large circumscribed porous lesion
boys than in girls. The age of manifestation covering more than half of the remaining joint
ranges from 10 to 16 years in boys, 9 to 14 years surface of the femoral head (Figures 375-377).
in girls (Jaffe, 1972:577). Kelsey, Keggi, and This porosity has completely obliterated the de-
Southwick (1970) found Negroes almost twice as pression for the ligamentum teres. There is a
often affected as Whites. depressed groove at the boundary with normal
Since the growth plate remains with the epi- bone. The margins of the joint surface are char-
physis, the bone of the epiphysis is little altered, acterized by exuberent bony overgrowth creating
except in cases with extensive aseptic necrosis. a mushroom-like appearance. This overgrowth
The proximal end of the femoral neck, however, extends well over the femoral neck. There are
shows irregularities due to the fracture with sub- some bony outgrowths on the superior portion of
sequent abrasion and resorption. In dry bone, the neck, but otherwise the neck appears normal.
since the joint capsule and the cartilage are miss- The X-ray film shows considerable thickening
ing, the appearance of the proximal surface of the of the trabeculae under the porous lesion. This is
femoral neck would be the main clue. In the indicated by a radiodense zone on the medial
240 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 380, 381.Slipped femoral capital epiphysis in a left femur: 380, Anterior view; note
that the superior articular surface is below the level of the greater trochanter. 381, Posterior
view. ( H M C S GR 1582.)
242 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
defective femoral head. T h e femoral head is dis- growing child, leading to aseptic necrosis, usually
placed inferiorly (Figures 378, 379) so that the with flattening of the bony center and increased
superior margin is about 15 millimeters lower density on X-ray. This flattening may be due in
than the greater trochanter. There is no evidence part to compression of the necrotic bone, in part
of porosity. Indeed the joint surface is smooth and merely an effect of arrested enchondral ossifica-
intact. The depression for the ligamentum teres tion in the necrotic area. Over the years more or
is well defined, unlike that of the head in Perthes' less complete repair can be observed, secondary
disease. Its position relative to the joint surface is to revascularization. T h e disease is uncommon
much nearer the inferior, posterior margin of the and occurs four to five times as often in males as
joint surface than normal. The ligament attach- in females. T h e onset of the disease is around 3
ment was maintained after the epiphysis slipped. years of age, usually several months earlier in
Growth continued in the epiphysis but predomi- females in whom this ossification center develops
nantly on the anterior and superior aspects. Ul- correspondingly earlier (Jaffe, 1972:606).
timately, the head reunited with the neck. The
femoral neck is abnormally short and thick re- Osteochondritis Dissecans
sulting from the loss of the growth plate activity PATHOLOGY.Osteochondritis dissecans is a
when the epiphysis slipped. type of aseptic necrosis characterized by the for-
The X-ray film shows an even, well-organized, mation of a small, in profile triangular, seques-
trabecular structure with no unusual radiologic trum consisting of articular cartilage on one sur-
abnormalities. It is possible to identify the growth face and necrotic subchondral cancellus bone.
plate of the femoral head in the film and see that T h e disease occurs in the adolescent and young
the mediolateral diameter of the head is relatively adult and is much more common in males than
normal. In marked contrast with Perthes' disease, in females. Familial occurrence has been observed
the femoral neck is almost nonexistent on the (Stougaard, 1964). The knee is the affected joint
superior aspect and greatly shortened inferiorly. in 90 percent of the cases, and the most frequent
Another example of slipped epiphysis is seen in location is the lateral portion of the articular
a left femur of a specimen from the Historical surface of the medial femoral condyle. Other
Museum in Chur, Switzerland (HMCS GR large joints are only rarely involved.
1582). The specimen is from the archeological site In the course of the disease, the necrotic frag-
at Bonaduz in Canton Grissons, Switzerland. The ment is extruded into the joint cavity and be-
epiphysis has slipped inferiorly and the femoral comes a loose osteocartilaginous body, which of-
neck is shortened (Figures 380, 381). ten enlarges due to circumferential growth of the
surviving cartilage. The cartilage may calcify, but
Other Vascular Disturbances of Epiphyses the bone fragment remains dead and unaltered
and Apophyses in size and shape. The subchondral osseous defect
of the condyle closes over with a thin layer of
There are a number of skeletal areas that are
bone but always remains a depression on the
subjected to severe mechanical stress, which may
lead to vascular disturbances of chronic trauma bony articular surface.
or a combination of both. This is particularly true PALEOPATHOLOGY.Wells (1961) describes an
of the skeletons of growing children and adoles- archeological skeleton from a Bronze Age ceme-
cents. tery (1600 B.C.) at Long Crickel, Dorset, England.
T h e skeleton is that of a young female about 16
Kohler's Disease of the Tarsal Navicular Bone years of age. T h e abnormality consists of deficient
bone on the anterosuperior margins of the third
PATHOLOGY.This bone is in such a key posi- and fourth lumbar vertebral bodies. About one-
tion in the vault of the foot that its blood supply third of the affected body is missing. Wells attri-
to the ossification center may be impaired in the butes this condition to adolescent osteochondritis.
NUMBER 28 243
i^i
-
^4
W,m^^
^
''*C^j
SliiS^feja^
v , . i ^ Q | t / - j ^ s^K^jPaQV^'^iS^iML.
v't'
*i^^HL. P/--'>f
HXg. ^ H L j y i i f .$r ,' <N'
cess but the powerful pull of the quadriceps may
lead to partial avulsion of the tendon insertion
with fragmentation of the apophysial center and
ultimate marked nodular irregularity of the tibial
3eui^Bil^E^''W i.' ] tubercle after fusion with the metaphysis. This
^ ^ ^
# . ^^ - r**"
condition is essentially of traumatic origin and
, ^ 1 ^ .<L&USVHi^flB aseptic necrosis plays a minor, secondary part, if
N;^^S.^^ any. It is more common in boys than in girls. It
k.^^^^^^^^ does not occur before 8 years of age in girls and
10 years of age in boys and does not commence
FIGURE 382.Osteochondritis dissecans of the medial right in either sex after 14 years of age (Jaffe, 1972:
femoral condyle with severe arthritic degeneration of the 599). More than 20 percent of the cases involve
joint. Specimen is a Late Saxon period burial from Thorpe both knees.
St. Catherine, Great Britain. (Photograph reproduced from
PALEOPATHOLOGY.Wells (1968) reports a pos-
Wells 1974b, fig. 4, with permission from Mrs. Calvin Wells.)
sible case of Osgood-Schlatter's disease in a Late
Saxon (ninth or tenth century A.D.) burial in
However, a congenital malformation of the Mor- Norwich, England (Norwich Castle Museum No.
quio or Hurler type should be considered, as 15, 953 [9]). The affected bone is a left tibia from
should trauma. a male skeleton containing a defect of the tibial
Wells (1962b) reports a case of osteochondritis tuberosity. The defect consists of an oblong de-
dissecans in a Late Saxon burial excavated near pression 30 millimeters long, 20 millimeters wide,
Norwich, England. The specimen is male and the and 10 millimeters deep.
abnormality occurs on the medial condyle of the Another possible case of Osgood-Schlatter's dis-
left femur. The defect is a large circumscribed ease is found in the miscellaneous long bones
depression in the joint surface about one centi- from Chicama, Peru (NMNH 265330-661). This
meter in depth. Additional evidence of osteochon- specimen is a right tibia (Figures 383, 384) of a
dritis dissecans is reported in skeletons of Ro- fairly small adult, probably a female. The arche-
mano-British date from the leklingham cemetery ological age is unknown. The diaphysis, distal
in England (Wells, 1976). Several additional pur- metaphysis, and distal joint surface are normal.
ported cases of osteochondritis dissecans in an- In the region of the tibial tubercle there is a large
cient British skeletal material are described by irregular spur, which projects toward the knee
Wells (1974b). Figure 4 of his report shows a joint. Both medial and lateral to the spur are
fairly certain example of osteochondritis dissecans zones of periosteal reactive bone. These are well
of the distal femoral joint surface (Figure 382). In healed indicating that the condition was not ac-
this report Wells expresses the opinion that osteo- tive at the time of death. The proximal joint
chondritis dissecans is more common in Romano- surface of the tibia is abnormal. The bony surface
British and Anglo-Saxon skeletons than skeletons for the attachments of the cruciate ligaments is
of Bronze Age people in the British Isles. poorly defined. The lateral and medial joint sur-
faces are poorly delimited. The medial joint sur-
face extends posteriorly creating an irregular sur-
Osgood-Schlatter's Disease of the Tibial Tubercle face. There is a sharply defined narrow depression
PATHOLOGY.The tibial tubercle is the site of 11 millimeters long by 3 millimeters wide and 4
the insertion of the patellar tendon. It develops millimeters deep on the anterior lateral edge of
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
244
the lateral joint surface. Grossly this defect ap- the head broadened transversally, and the distal
pears to have resulted from a crushing injury to portion of the diaphysis thickened, with disap-
this portion of the joint. Reactive bony spurs in pearance of the usual necklike constriction (Koh-
the region of the tibial tubercle and reactive bone ler, 1923). There is a corresponding change in the
deposition are compatible with Osgood-Schlat- configuration of the articular surface of the ad-
ter's disease. jacent basal phalanx.
Freiberg's Disease of a Metatarsal Head Kienbock's Disease of the Carpal Lunate Bone
PATHOLOGY.This lesion involves the head of PATHOLOGY.The carpal lunate forming the
the second, less commonly the third, metatarsal. center of the proximal carpal chain bears the
The lesion consists of subchondral necrosis and brunt of the mechanical impact transmitted to
infarction of the metatarsal head, which may the radius. T h e disease consists of necrosis and
separate from the shaft, similar to the fragment fragmentation of this bone, mainly on a basis of
in osteochondritis dissecans. The second metatar- chronic trauma. T h e condition is not rare, more
sal is usually the longest and bears the burden of common in males, occurring between 20 and 40
pressure against the ground, especially when the years of age, with predilection of the right hand.
heel is unduly elevated. Radiologically, areas of increased density and
T h e lesion usually occurs in adolescents but lucency alternate, and in the dry state bone areas
may be observed in adults. Bilateral involvement may actually be fragmented after disappearance
occurs. There is a concave defect in the articular of interposed fibrous and cartilaginous tissue.
bony surface of the metatarsal head with a scle- More rarely the carpal navicular bone may be
rotic base. The metatarsal is somewhat shortened. similarly affected (Preiser's disease).
NUMBER 28 245
FIGURES 385, 386.Pulmonary osteoarthropathy: 385, Right radius and ulna showing marked,
diffuse periosteal hyperostosis with pronounced vascular grooving. 386, Right foot, dorsal view;
note periosteal hyperostosis of metatarsals and phalanges. (58-year-old female with large,
solitary metastasis of breast cancer in lung; IPAZ 6649, autopsy 1259 of 1961.)
246 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Aneurysmal Erosion
PATHOLOGY
248
NUMBER 28
249
may show lamination and thinning, secondary to a Mendelian dominant. The condition is charac-
invasion of the Haversian canals by Gaucher cells terized by elevated blood cholesterol levels and
(Pick, 1927:23). If this process is severe, a minimal often leads to tumor-like deposits of cholesterol in
amount of subperiosteal bone deposit can be subcutaneous and periarticular connective tissues
observed, but usually the external cortical lamel- or tendons (xanthoma tuberosum). There is no
lae, although thin, remain smooth. Similar predilection of sex or race.
changes may be observed on the proximal tibial There seems to be no deposit of cholesterol in
metaphysis or on the humerus, albeit less often. the bone marrow. Observed bone changes mainly
In long-standing cases, severe destruction of the consist of pressure erosions of phalanges of fingers
proximal humerus with varus deformity is not and toes by adjacent xanthoma nodes (Merrill,
uncommon. In these late cases, lytic skull and 1920). This is apparently caused by the tightness
mandibular lesions and focal reactive sclerosis of space in the subcutaneous compartments of
may occur (Rourke and Heslin, 1965). Bone mar- digits, whereas much larger xanthomatous depos-
row infarcts have been observed in various long its in the vicinity of larger bones and joints do
bones (Arkin and Schein, 1948). not usually indent the bones. The scooped-out
cortical erosions may cross interphalangeal joints
Niemann-Pick's Disease and simulate defects caused by gouty tophi (Gaal,
1933).
Niemann-Pick's disease is a rare, congenital,
familial disorder of the phospholipid metabolism, Lipid (cholesterol) granulomatosis (Erdheim-
leading to progressive storage of phospholipids Chester's disease) is a rare disorder characterized
(mainly sphingomyelin) in the reticuloendothelial by massive cholesterol deposition in the bone
cells of the liver, spleen, lymph nodes, and bone marrow and occasionally in other organs, but
marrow. There is no sex predilection and the sparing the spleen. The condition remains asymp-
inheritance seems to be recessive. About 50 per- tomatic into adult life. The reason for mentioning
cent of the affected individuals are Jews. The it here is that distinct bone changes have been
majority of the individuals die in infancy but demonstrated radiologically and anatomically
survival to young adult age has been observed (Chester, 1930-1931:577-592; Jaffe, 1972:537-
(Crocker and Farber, 1958:2-4). 541). The most marked lesions were found in the
long bones of the forearms and lower legs, sym-
Bone changes are mostly limited to reduction
metrically. The changes consist of spotty and
of number and size of trabeculae and cortical
diffuse osteosclerosis, most pronounced in the
thinning of long bones. Occasionally, moderate
metaphysial area but often also involving the
widening of the distal femoral metaphysis is ob-
epiphysis. The shaft cortex may be thickened but
served, not reaching the extent often seen in
shows widened Haversian canals. The changes
Gaucher's disease (Crocker and Farber, 1958:82).
extend into the bones of hands and feet, most
The generally poor health of affected infants may
markedly so in the talus and calcaneus. Femur
manifest itself in delayed appearance of second-
and humerus are less affected and the skull is
ary ossification centers. Superimposed deficiency
normal. The sclerosis observed is due to both
in Vitamins D and C may add features of rickets
trabecular thickening and ossification of medul-
and scurvy to the picture. In contrast to Gaucher's
lary cholesterol granulomas.
disease, collapse of the femoral head and focal
lytic lesions do not occur (Gildenhorn and Am-
romin, 1961). Histiocytosis X
bone formation does occur. Rib lesions may cir- or Negro genes. A detailed discussion of the
cumferentially erode the old cortex and expand geographic, ethnic, and genetic problems of this
the diameter, eliciting some sclerotic response in disease complex has been given by Rucknagel
the new cortex. Pathological fractures can occur (1966). Although extremely interesting, it is of
in long bones and ribs. little significance to the present problem since,
regardless of genetic background, the clinical and
Anemias skeletal changes are the same. A geographic dis-
tribution in different populations is given in Ta-
PATHOLOGY
ble 11 from Rucknagel (1966). The percentages
In various, mostly hemolytic, anemias bone
changes occur secondary to the need for expan- TABLE 11.World distribution of alpha and beta thalasse-
sion of the spaces occupied by hemopoietic mar- mia in indigenous populations (from Rucknagel, 1966) (dash
row (Caffey, 1937:293, 294). = no data; ? = questionable data)
Alpha Beta
Geographic area
{%) {%)
Thalassemia
SOUTHERN EUROPE
Thalassemia is a hemolytic anemia caused by 0-20
Italy 0.2
a genetic defect in the hemoglobin structure. The Sicily - 3-13
severe manifestations of thalassemia major are Sardinia 1 4-38
usually restricted to homozygotes as regards the Greece 4-7 6-14
abnormal gene. Heterozygotes show thalassemia Portugal - 0.6
Turkey >
?
minor with little or no clinical, and certainly
without skeletal, manifestations. Moderately se- AFRICA
quoted include homozygotes and heterozygotes, tire skeleton of the child is affected, more or less
and it is understood that there is more than one uniformly, while, in the adult, characteristic bone
genetic type of beta-thalassemia. changes remain only in areas of permanent hemo-
Thalassemia major results in a very high mor- poietic activity.
tality in infancy and childhood and a limited T h e most severe changes are in the skull. In
adult life span in the few survivors. The hetero- children, the diploe of the cranial vault expands,
zygote without anemia presumably has a selective leading to marked thickening of the cranial vault,
advantage in malaria-infested areas, which would usually beginning in the upper portion of the
explain the geographic distribution. However, the frontal bone (Figures ,392-394). T h e trabeculae
evidence is more circumstantial and less clear-cut of the diploe are reduced in number with thick-
than in sickle cell anemia (Rucknagel, 1966). In ening and later radial rearrangement of the re-
thalassemia major, bone changes always develop maining trabeculae. The external table is pro-
and become radiologically obvious after the first gressively eroded and later completely destroyed.
year of life. Intermediate thalassemia may show This is accompanied by honeycombed compart-
skeletal lesions; thalassemia minor does not. T h e ments of subperiosteal new bone, harboring hy-
bone lesions in thalassemia are entirely due to perplastic marrow. T h e destruction of the inner
increased spatial demands for the hyperplastic table comes much later and is always much more
erythropoietic marrow. In keeping with the gen- limited than that of the outer table. O n X-ray, in
eral distribution of hemopoietic marrow, the en- these severe cases, the honeycombed compart-
NUMBER 28 253
by thinning of the cortex, most pronounced in ital spherocytic anemia, and iron deficiency ane-
the femur. In the metaphysial area, the cortex mia have to be considered. T h e skull changes of
may assume a reticulated appearance with mark- thalassemia occasionally resemble those in sickle
edly enlarged vascular foramina, harboring hy- cell anemia but the extensive lesions of the rest of
perplastic marrow. There is often inhibited re- the skeleton do not. Cyanotic congenital heart
modeling of the distal femoral metaphysis, lead- disease (Ascenzi and Marinozzi, 1958) and,
ing to a widened contour without the usual con- rarely, polycythemia (Dykstra and Halbertsma,
cave flare, closely resembling the so-called Erlen- 1940) can mimic the skull changes in thalassemia.
meyer flask deformity seen in Gaucher's disease. Congenital hemolytic anemia and iron deficiency
Multiple "lines of arrested growth" are frequently anemia never show bone changes of such severity.
present, in keeping with the usual inhibited
growth and delayed epiphysial closure observed
Sickle Cell Anemia and Its Genetic Variants
in this disease. In a smaller percentage, premature
and irregular fusion of the growth plate occurs, A variety of normal and abnormal hemoglo-
especially of the proximal humerus, leading to bins can be identified by electrophoresis. At birth,
significant medial tilting of the humeral head. In fetal hemoglobin F amounts to about 60-80 per-
the series published by Currarino and Erlandson cent of the total and remains in significant
(1964), 12 of 79 thalassemia patients showed pre- amounts until about 6 months of age. It is rapidly
mature fusion of growth plates beginning after 10 replaced by adult hemoglobin A to a level below
years of age and producing shortening and de- one percent, but there exists genetic abnormal
formity. Of these, nine concerned the proximal persistence of hemoglobin F. Hemoglobin S is an
humerus (three bilateral), three the distal femur abnormal hemoglobin, responsible for the sickling
(one bilateral). The general reduction of growth phenomenon. Another abnormal hemoglobin is
may lead to an infantilistic, dwarfed skeleton C. A further abnormality of hemoglobin is caused
(Caffey, 1972 (2): 1284). by the thalassemia genes (Thai). All these genetic
In adults, the tubular bones of hands and feet factors are realized in the various genotypic com-
resume normal contours and may develop some binations of any two of them.
osteosclerosis subsequent to the replacement of Sickle cell anemia patients have a genotype SS
erythropoietic by fatty marrow (Caffey, 1972 (2): while individuals with sickle cell trait have gen-
1284). The widening and reticulation of the ribs otype SA. The gene for hemoglobin S is almost
remains mostly in the posterior portions and exclusively limited to the Negro race with a slight
rarely may lead to a tumor-like expansion of scattering in adjacent Mediterranean populations
erythropoietic marrow covered by a thin, ex- (southern Italy, Greece, Armenia). Other genetic
panded, cortical shell, projecting into the thoracic combinations (SC, and SThal) represent the ge-
cavity. Changes in the vertebrae and, to a lesser netic variants of sickle cell anemia. In persons
extent, in the cranium remain. Pathological frac- with two abnormal hemoglobin genes, hemolytic
tures, especially of the femur, occur in adults anemia will develop in intermittent crises, and
more frequently than in children. the erythrocytes will assume sickle shape under
Double heterozygous combinations with other hypoxemic stress, due to crystallization of the
hemoglobin abnormalities occur, but only in thal- abnormal hemoglobin within the cell. T h e result
assemia-hemoglobin S combinations are bone in- is constantly increased demand for red cell pro-
farctions observed (Middlemiss and Raper, 1966: duction to compensate for the cell loss in hemo-
698). Pure thalassemia creates no circulatory ob- lysis. During crises, the misshapen red cells con-
structions and does not have an increased rate of glutinate and cause vascular obstructions, leading
osteomyelitis. In the differential diagnosis of dry to areas of ischemic necrosis. Although the genetic
skeletal parts, other hemoglobinopathies, congen- abnormality is present at birth, the clinical man-
NUMBER 28 255
ifestation is prevented before 6 months of age due mon nor obvious nor specific. The most careful
to the protective effect of the high concentration and detailed study of bone changes in this disease
of fetal hemoglobin F before that age. The mor- has been published by Diggs, Pullian, and King
tality of infants and children with sickle cell (1937) in a series of their own cases. Their series
anemia is high. comprised 39 Negro patients with active severe
In persons with sickle cell trait (SA), only ex- sickle cell anemia, ranging from 1 to 51 years of
treme hypoxemic stress can produce hemolysis age. This includes eight autopsies at which special
and infarctions. Persons with the genetic combi- attention was paid to bone changes. The fre-
nation of sickle cell trait and persistent fetal quency and degree of bone involvement increased
hemoglobin (SF) are usually free of anemia. Of with age beginning in children past 5 years of
considerable interest is the fact that hemoglobin age. The bones most likely to reveal alterations
S is more resistant to attack by malaria parasites. are the skull, vertebrae, tibia, and fibula, with the
This offers survival advantage to carriers of he- skull changes appearing the earliest. They found
moglobin S, which in turn leads to increasing in their series that the majority of patients showed
frequency of hemoglobin S in inhabitants of the no alteration in size, shape, and density of their
malaria infested areas of tropical Africa. The bones on X-ray. There is general agreement
frequency of hemoglobin S varies in different among all observers that bone changes are not
Negro populations. In North American Negroes, related to the severity of the disease.
7.5 percent show the sickling trait but only 1 in The first and most conspicuous changes are
40 (2.5 percent) of these suffers from sickle cell observed in the skull. The diploe may be thick-
anemia (Lewis, 1942:234-235). Of course the ened, and there may be diminished definition of
American Negroes are a dislocated group of the outer table on X-ray. The radiation density
mixed genetic background. In Panama, Tomlin- is diminished, sometimes with coarsened trabec-
son (1945) found at autopsy that 9 percent of ulation arranged perpendicular to the inner table.
individuals with sickling trait actually showed Complete destruction of the outer table with so-
clinical sickle cell anemia. The sex distribution called "hair on end" arrangement of bony septa
rate of the sickling trait in 3000 determinations is uncommon. It was present in only 1 of 39 cases
in Panama (representing autopsies, hospital pa- in the series of Diggs, Pullian, and King (1937).
tients and village populations), was 7.2 percent They found the thickening of the diploe to be
in males and 11.4 percent in females. In spite of bilateral, symmetrical, and usually limited to the
a high frequency of hemoglobin S in African parietal bones, less often involving the frontal
Negroes, clinical sickle cell anemia is uncommon. and occipital bones. The maximal thickness oc-
A survey of over 2000 Yorubas in Ibadan (Ni- curs in the vertex, tapering to normal towards the
geria) showed the following distribution of he- temporal area. Skull changes are most often ob-
moglobin genes: normal 70.9 percent, carriers of served in older children and in young adults.
AS 23.9 percent, AC 4.3 percent, SC 0.7 percent, Occasionally the osteoporosis may lead to small
and CC 0.2 percent (from Cockshott, 1958). focal lytic lesions resembling myeloma. The facial
The skeleton may be involved in sickle cell bones showed normal appearance on X-ray in
disease in three different ways: (1) changes sec- their cases. Sarjeant (1974:166) states that the
ondary to increased demand of space for hemo- zygoma may be enlarged and the orbital roof
poietic marrow; (2) sequelae of vascular obstruc- tlTickened, but the frontal sinuses develop nor-
tion of smaller and larger blood vessels; and (3) mally, although the other sinuses may be delayed
secondary infections superimposed on ischemic and hypoplastic. In the mandible, reduction and
areas. Although a variety of bone changes have coarsening of trabeculae is observed, accompa-
been described in sickle cell anemia, it should be nied by prominence of the lamina dura of the
emphasized that, as a rule, they are neither com- alveoli and thinning of the cortex. The vertebrae
256 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
show rarefaction of the spongiosa in the vertebral calcium salts around the necrotic focus, which is
bodies. In adults, depression of the central portion readily visible on X-ray. T h e metaphysial foci
of the end-plate with intact peripheral portion is may appear as focal increased densities alternat-
observed, which is somewhat different from the ing with spotty lucencies of hyperplastic marrow.
"fish vertebra" appearance in postmenopausal In fact, some of the bony plugging of the medul-
osteoporosis. Widening and flattening of vertebral lary cavity, as described by Diggs, Pullian, and
bodies, especially in the lumbar area, is seen in King (1937), may well represent healed infarc-
about 30 percent of adult patients (Jaffe, 1972: tions. T h e cortical infarcts may reveal a lytic
700). The ratio of height to width of vertebral intracortical separation on X-ray. Infarctions of
bodies in anterior-posterior views on X-ray the cortex of short tubular bones of hands and
ranged from 1:1.4 to 1:2.8 with a normal of 1:1.4 feet are not uncommon in infants and small
for Negroes of comparable age (Diggs, Pullian, children. These may elicit moderate periosteal
and King, 1937). reactive bone formation and spotty densities and
The scapula, sternum, pelvic bones, and ribs lucencies in the course of repair (Jaffe, 1972:697-
(flat bones) may show increased lucency and 703). However, Diggs, Pullian, and King (1937)
coarsening of the trabeculation. However, in the found no bone changes in hands and feet in their
series reported by Diggs, Pullian, and King cases, but in some instances epiphysial necrosis
(1937), only slight osteoporosis without widening may lead to shortening of individual fingers (Sar-
of the bones was observed. jeant, 1974:175-177).
In long bones, the most marked changes occur Of special significance is the occurrence of
in the tibia and fibula. Hemopoietic marrow may aseptic necrosis in the head of the femur in sickle
occupy Haversian resorption spaces in the cortex, cell anemia and its genetic variants. This is the
especially near the medullary canal (Diggs, Pul- most common site of infarction. Apparently, it is
lian, and King, 1937). In adults with advanced even more common in the variants, particularly
disease, endosteal reactive lamellar bone and oc- in SC patients, than in classical SS anemia (Cock-
casional bony plugging of segments of the marrow shott, 1958). Golding, Maclver, and Went (1959)
cavity can occur (Diggs, Pullian, and King, 1937). reported from Jamaica only 5 instances in 51 SS
In these cases neither the medullary cavity nor patients, but 13 in 19 SC and in 1 of 2 SThal
the diameter of the shaft is widened. On the patients. Chung and Ralston (1969:38) quote the
contrary Diggs, Pullian, and King (1937) found incidence of aseptic necrosis of the femoral head
the cortex thickened and the medullary cavity from a literature survey as 0-12 percent in SS but
actually narrowed. In their series they found 11 20-60 percent in SC disease. The lesion occurs
cases, mostly adults, with marked changes of long mostly in adolescents near the time of fusion of
bones. The hyperplastic marrow also may pro- the proximal growth plate. It resembles Perthes'
duce multifocal spotty radiolucency in the meta- disease, however with two differences: The lesion
physial areas. The medullary cavities of metacar- occurs several years later and it lacks metaphy-
pals may be widened and vascular foramina en- sial changes adjacent to the growth plate. Fur-
larged (Cockshott, 1958). The changes produced thermore, Perthes' disease is uncommon in Ne-
by sickling and blocking of blood vessels are groes (Chung and Ralston, 1969:51). If the ne-
essentially ischemic infarctions, which may be crotic focus is small, hugging the base of the
large and located in the medullary cavity, small articular cartilage, it may simulate an unusually
and spotty in the metaphysis, or involving por- large osteochondritis dissecans or Perthes' disease
tions of shaft cortex due to blockage of Haversian (Middlemiss and Raper, 1966:695). In a series of
vessels. Generally, the large medullary infarcts 13 cases reported by Chung and Ralston (1969:
are indistinguishable from those produced by 38), four showed bilateral hip lesions and six of
other causes. As in those, they also tend to collect these patients also showed aseptic necrosis of the
NUMBER 28 257
Hereditary Spherocytosis
(Congenital Hemolytic Anemia)
Iron-deficiency Anemia
FIGURE 397.X-ray of right humerus, of sickle-cell anemia Bone changes in iron-deficiency anemia are
with Salmonella osteomyelitis. (Nigerian negro, courtesy Dr. uncommon. If such changes occur, they are usu-
Stanley Bohrer, Ibadan, Nigeria.)
ally limited to the skull vault, showing expansion
of the diploe, vertical striation and occasional
humeral head; others had infarcts in long bones. "hair on end" appearance on X-ray (Moseley,
These additional necrotic foci mostly concerned 1961, 1963, 1966; Lanzkowsky, 1968). The pa-
older patients with classical (SS) sickle cell ane- tients reported as showing the bone changes men-
mia rather than genetic variants. Occasional un- tioned have been Indonesian (Eng, 1958), Ne-
usual locations of aseptic necrosis, such as elbow, groes (Burko, Mellins, and Watson, 1961), or
knee, sacroiliac joint, and ankle, have been ob- prematures and twins (Shahidi and Diamond,
served in SS disease (Chung and Ralston, 1969: 1960). The facial bones and long bones are usu-
40). Secondary infections are not uncommonly ally spared and pneumatization of the paranasal
258 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
sinuses is not delayed (Moseley, 1963:5). How- and possibly thalassemia tend to be influenced by
ever, in some Turkish patients, enlargement of the distribution of malaria, since the abnormal
the facial bones, delayed pneumatization, and hemoglobin in such anemias reduces the severity
coarse porotic trabeculation around elbows, of the symptoms of malaria. Acquired anemia is
hands, and feet have been observed (Aksoy, a response to one or more of several variables
^ a m l i , and Erdem, 1966). including nutrition and debilitating diseases and
In other conditions, such as cyanotic congenital thus occurs in any human population irrespective
heart disease with secondary polycythemia (As- of the presence of malaria.
cenzi and Marinozzi, 1958) or in polycythemia Most of the inferences made about the presence
vera (Dykstra and Halbertsma, 1940), expansion of anemia in paleopathological specimens are
of the cranial diploe due to hyperplasia of the based on lesions of the skull thought to be asso-
hemopoietic marrow has been described. ciated with this disease. T h e lesions are found on
the skull vault, primarily the outer surface of the
Erythroblastosis Fetalis parietal bones, and on the orbital roof (Figure
398). They consist of porous periosteal bone dep-
In some infants with this disorder, usually osition in these areas of the skull. Henschen (1961:
based on R H incompatibility between the R H 724) attributes the earliest awareness of these
negative sensitized mother and the R H positive lesions in clinical cases to Rokitansky (1844) and
fetus, bone changes have been described. They Virchow (1848). Several descriptive terms have
consist of alternating band-like areas of increased been used for this condition including cribra
and decreased radiodensity, especially in the me- crania, symmetrical osteoporosis, and spongy hy-
taphysis of the most rapidly growing bones (distal perostosis. I shall use the term "porotic hyperos-
femur and proximal tibia). These changes were tosis" introduced by Angel (1966).
present in 20 of 110 cases (Brenner and Allen, The relationship between the calvarial and or-
1963) but are not specific. They reflect distur- bital lesions has never been clear. Virchow (1874:
bances of the late fetal enchondral ossification 61-62) believed that both lesions are part of the
with delayed resorption of calcified cartilage cores
in primary trabeculae (Follis, Jackson, and
Carnes, 1942). The only reason to mention this
finding is that similar changes can be seen in the
newborn in congenital syphilis.
PALEOPATHOLOGY
same disease process. Hrdlicka (1914) indicated some type of hemolytic anemia, probably thal-
that the calvarial lesions begin in the orbit. M0ller- assemia, in the pre-Columbian New World. The
Christensen and Sandison (1963:180) note the problem in inferring the presence of thalassemia
possibility of lacrimal gland involvement in or- in the ancient New World from skeletal lesions
bital lesions and suggest mumps as a possible is that there is no evidence of this gene in
cause. Local inflammation of the orbital roof post-Columbian unmixed .American indigenous
from such a cause probably would not affect the -populations.
cranial vault. The implication of this opinion is Moore (1929) summarizes the modern clinical
that orbital lesions are not necessarily associated findings in sickle cell anemia, which include the
with calvarial lesions. My own experience is that thickened hair-on-end appearance in roentgen
one often finds both types of lesion in a single films. He briefly describes a modern skull with
skull, but one also finds each type of lesion occur- similar lesions. He attributes this example of po-
ring by itself and occasionally in association with rotic hyperostosis to sickle cell anemia and offers
morbid conditions other than anemia. the opinion that the morbid condition was wide-
Several morbid conditions other than anemia spread. As with thalassemia, however, there is no
have been proposed as the cause of porotic hy- evidence of this genetic blood abnormality in
perostosis. Williams (1929:854-855) suggested modern unmixed indigenous populations in the
rickets as the most likely cause but also suggested New World.
that abnormal conditions created by artificial In the Old World, Angel (1964, 1966) has
deformation of the skull could produce similar proposed that porotic hyperostosis found in an-
lesions. Earlier, Hrdlicka (1914:58) expressed the cient Greek skulls is evidence for the presence of
opinion that the condition was not rachitic but thalassemia in antiquity. Here, however, the evi-
more likely a "toxic" rather than a nutritive or dence for the genetic variant in modern ethnic
degenerative disorder. Henschen (1961:724, 729) groups is unquestioned, making such an inference
examined 2000 modern skulls from Sweden and much more plausible.
found no evidence of porotic hyperostosis. How- Moseley (1965) added acquired anemia to the
ever, he did find four such lesions in some mid- list of possible morbid conditions producing po-
nineteenth century Swedish skulls. He suggests rotic hyperostosis. On the basis of his clinical
that the lesions may have been caused by nutri- experience as a radiologist he proposed to differ-
tional conditions or chronic infection. entiate thalassemia major from other genetic and
While infectious and metabolic disease may be acquired anemias because of its involvement of
implicated in porotic hyperostosis of the skull, the face and long bones. He expressed the opinion
anemia has received much more attention in the (1965:141) that porotic hyperostosis seen in skulls
paleopathological literature as a possible cause of from Peru and Yucatan is due to iron-deficiency
this condition. Vyhnanek, Kolar, and Stloukal anemia. This diagnosis was also applied to a
(1963) describe two medieval skulls of children Bronze Age (1650-1550 B.C.) skull of a 6-year-old
from central Europe with porotic hyperostosis. child from Wales with porotic hyperostosis, de-
The authors conclude that they are examples of scribed by Cule and Evans (1968). Sir Arthur
hemolytic anemia but are not more specific. Keith, who also saw the skull, attributed the
Zaino (1964:403) proposes that the porotic hy- lesions to rickets (in Wheeler, 1923:21). The pub-
perostosis, which is common in pre-Columbian lished photographs, as well as Keith's description,
skulls from Peru, is due to thalassemia. also suggest congential syphilis as a possibility.
Jarcho, Simon, and Jaffe (1965) report a case The presence of hypoplastic enamel defects in the
of porotic hyperostosis from a Pueblo Indian site teeth is also compatible with a diagnosis of con-
in the American Southwest. The authors con- genital syphilis but could also occur in anemia,
clude that bone changes suggest the presence of particularly if related to poor nutrition.
260 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
El-Najjar, Lozoff, and Ryan (1975) studied the enlarged diploe with the virtual elimination of
expression of porotic hyperostosis in archeological the outer table.
skeletal samples from the southwestern United An X-ray film was prepared of the extant long
States. In their study they found an association bones including major portions of both femora,
between presumed dietary factors and the fre- right tibia, both humeri, and ulnae. This film
quency of skeletons having porotic hyperostosis. reveals a relatively enlarged marrow cavity and
The authors conclude that acquired anemia due greatly diminished thickness of the cortex in all
to inadequate iron absorption is the most likely long bones.
causative factor for porotic hyperostosis in skele- The second specimen ( N M N H 327107) has a
tons from the southwestern United States. Mens- dental age of about 2 years. The state of preser-
forth, Lovejoy, Lallo, and Armelagos (1978:38) vation is not as good. Like the previous specimen
report an association between evidence of infec- the most severely affected region is the external
tious disease and the occurrence of porotic hyper- table of the parietals (Figures 403, 404). The
ostosis in prehistoric skeletons from Ohio, USA. lesion does not cross the sagittal suture. The left
They suggest that illness and nutritional stress frontal bone is also affected, with the disease
are important factors stimulating iron-deficiency process continuous across the coronal suture.
anemia. Only portions of the right orbit are present. They
Two specimens from the National Museum of reveal no evidence of porotic hyperostosis. The
Natural History, USA, provide useful insight into left temporal bone is abnormal with an irregular
the expression of porotic hyperostosis. The two surface, which is thickened and slightly porous.
cases are both from the American Southwest Two features distinguish this specimen from
(NMNH 327074 and 327107) and are skeletons the preceding one. First, the lesion does occur in
of young children from the Pueblo Bonito ruin, the region of deformation. This may be related to
Chaco Canyon, New Mexico. This site is associ- the fact that the occipital deformation is not as
ated with the Pueblo III cultural period and severe. Second, unlike the preceding specimen,
dated between A.D. 919 and 1130 (Seltzer, 1944: there appears to be slight deposition of reactive
25), thus making it clearly precontact. During bone on the inner table. T h e abnormal bone is
this period skulls show marked artificial defor- concentrated in the region of the anterior fontanel
mation characterized by occipital flattening. The with reactive tissue apparent at its sutural bor-
dental age of the first specimen (NMNH 327074) ders. There is a solitary lesion on the left parietal
is about iy2 years (Figures 399-402). The lesions boss. A lateral X-ray film of the skull reveals the
in this specimen are primarily porous but with vertical striations in the area where porotic hy-
some labyrinth-like lesions as well. The affected perostosis is most pronounced.
area involves the frontals including the orbital Also apparent in the film is the absence of the
roofs but predominantly involves the outer table outer cortex in the porous area. T h e lesion itself
of the parietal bones. The inner table is not is slightly different from the first specimen in
affected. The specimen is characterized by severe being more variable in appearance. Beginning on
occipital flattening and the lesion encroaches only either side of the sagittal suture, the parietal
slightly on the deformed part of the skull. The lesion has a narrow zone of finely porous bone.
facial bones and mandible are not markedly af- This quickly merges with bone that is labyrin-
fected, although the region surrounding the zy- thian in gross appearance. Continuing in a lateral
gomaticofacial foramen on the zygomatic bone direction the lesion is characterized by a circular
suggests an inflammatory reaction. The lateral porosity, which becomes finer and less pro-
X-ray film shows the perpendicular striations nounced in the area below the temporal muscle.
found in many examples of porotic hyperostosis. Here the bone takes on the lumpy quality like
A postmortem break through the lesion in the that seen in the left temporal bone.
right parietal reveals an intact inner table, greatly Like the first specimen, the long bones are
NUMBER 28
261
affected by the disease process. An X-ray film of 1 millimeter for the abnormal specimen, while
the complete right femur and the partially com- the normal femora are between 2 and 3 millime-
plete tibiae, left femur, and humerus reveals a ters.
generalized enlargement of the medullary cavity As El-Najjar, Lozoff, and Ryan (1975) argue,
with the cortex much thinner than normal. Com- if some porotic hyperostosis is caused by nutri-
parison of the abnormal femur with normal fem- tional anemia in which iron is deficient, one
ora (Figure 405) of similar size from the same might find evidence of other metabolic problems
population reveals a cortical thickness of less than resulting from iron deficiency. Von Endt and
262 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Leukemia
PATHOLOGY
In the growing bone of children, the replace- T h e initial lesion usually arises in that part of
ment of the normal marrow cells by tumor cells the skeleton that contains hemopoietic marrow
and their subsequent proliferation lead, not which, in the older adult individual, is the trunk
rarely, to recognizable alterations of the bone skeleton and the proximal metaphyses, especially
structure. The most frequent lesion is a narrow of the femur and the humerus. Single tumor cells
radiolucent line on the metaphysial side of the disseminated through the blood colonize mostly
growth plate. This change is not specific and in the areas of hemopoietic marrow. In the cranial
resembles, to some extent, the lucent metaphysial vault and in portions of the long bones of the
zone in scurvy. Another alteration seen in acute extremities, reactivated hemopoietic marrow ap-
childhood leukemias concerns the cortical surface pears, secondary to massive marrow involvement
of the metaphyses. Normally, in these areas, os- in the trunk. The facial bones and the small bones
teoclastic resportion of the modelling process cre- of the extremities are usually spared.
ates a rough and somewhat grooved or porous T h e initial lesion may remain localized and
cortical surface. In acute leukemia, these areas of solitary for months or years, but ultimately dis-
the periosteum may be colonized by tumor cells semination to other parts of the skeleton almost
emanating through the vascular foramina. This always occurs. A typical location for this type of
leads to widening of the vascular foramina and lesion is the proximal metaphysis of the femur
exaggerated grooving and porosity of the meta- and humerus (Schinz, Baensch, Friedl, and Ueh-
physial cortical surface (Figure 406). This may be linger, 1951-1952:1947). T h e solitary lesion is
the most characteristic bone lesion of acute leu- slow-growing, creating an osteolytic defect, ulti-
kemia. Occasionally, widespread nonspecific sub- mately eroding the cortex but permitting the new
periosteal bone deposits are observed over formation of an expanded bony shell with ridge-
thinned cortices of long bones and ribs. Bone like internal reinforcements, giving the so-called
changes in adult leukemias are too uncommon soap bubble pattern on X-ray. Pathological frac-
and uncharacteristic to warrant discussion in this tures through the lesion are not uncommon. The
context. lesion usually does not extend into the head of
In malignant lymphoma, bone lesions, if pre- the femur. This distinguishes it from giant cell
sent, resemble lytic or sclerotic metastases of car- tumor and chondroblastoma. In dry bone, the
cinoma. Occasionally diffuse subperiosteal in- solitary lesion could not be differentiated with
volvement with cortical erosion occurs (Figure certainty from unicameral bone cyst, chondro-
407). myxoid fibroma or nonossifying fibroma, except
for the fact that these would usually occur in a
younger age group. T h e differentiation of the
Myeloma lesion from solitary lytic metastasis of renal or
thyroid carcinoma may be impossible. The most
PATHOLOGY
frequently observed and most characteristic man-
Myeloma is a highly malignant tumor of ifestation is the disseminated form (multiple mye-
plasma cells, usually arising in an area of hemo- loma). The lesions start within bone marrow but
poietic bone marrow and, after varying time in- ultimately scallop and destroy cortex. In most
tervals, involving extensive portions of the skele- affected bones (vertebrae, ribs, sternum, clavicles,
ton. scapulae, pelvis, calvarium, and long bones) the
The disease is relatively rare. There is a great individual lesions create punched out, purely lytic
prevalence of males over females affected. The defects without reactive bony margins (Figure
tumor rarely occurs below 40 years of age with a 408). Most are round, 3 to 10 millimeters in
maximal frequency between 50 and 70 years of diameter. Individual large lesions are rare, with
age. There is no known racial or geographic exception of the original ones; but small lesions
prevalence. can become confluent, often showing scalloped
NUMBER 28 265
State, USA. The skeleton is that of an old male. could be the cause. T h e large size of some lesions
The roentgen films show multiple lytic lesions of and the possibility of bony reaction would, in my
the skull, which vary from a few to 25 millimeters opinion, tilt the scale in favor of a diagnosis of
in diameter. Other postcranial bones show similar metastatic carcinoma rather than myeloma. In-
lesions, with the long bones less affected then the deed, Brothwell (1967a: 337), in commenting on
axial skeleton. They suggest that prostate carci- this and other similar cases, offers the opinion
noma is a possible cause but indicate that multi- that skeletons with multiple lytic lesions should
ple myeloma is more likely, citing the opinions of be considered cancer metastases, until more con-
H. U. Williams and R. M. Moodie in support of vincing evidence can be provided for a diagnosis
this diagnosis. The age and sex of the individual of multiple myeloma.
is compatible with a diagnosis of multiple mye- Wells (1964b) reported on two medieval skulls
loma. However, the large variation in the size of with multiple lytic lesions. T h e skulls were from
the lytic foci is more compatible with metastatic Kent and Suffolk, England, and both were adults
carcinoma. of unknown age. Wells was reluctant to offer a
Williams, Ritchie, and Titterington (1941) re- firm diagnosis but suggested metastatic carci-
port a case of multiple lytic lesions in the skeleton noma and multiple myeloma as likely, with mye-
of a 10-year-old pre-Columbian child excavated loma the more probable.
near Rochester, New York, USA. The lesions vary Brooks and Melbye (1967) describe a pre-Co-
between 3 and 10 millimeters in diameter in lumbian skeleton from Missouri, USA, with mul-
almost every bone recovered. The authors suggest tiple lytic lesions. The skeleton is that of a female
multiple myeloma as a probable cause, but this over 40 years of age. Photographs of skull and
is unlikely because of the young age. A more femora reveal considerable variation in the size
likely cause would be one of the histiocytoses, of the lesions. Some on the femora are at least
such as Schiiller-Christian's disease. half the diameter of the femur (about 15 mm).
Fuste (1955) describes a neolithic human skull They attribute the probable cause of the lesions
from the Pyrenees that had multiple, lytic lesions. to multiple myeloma. T h e age and sex of this
The lesions were roughly circular with irregular specimen is more compatible with a diagnosis of
borders associated with reactive bone. Either mul- metastatic carcinoma, such as breast cancer, but
tiple myeloma or metastatic carcinoma is possi- certainly multiple myeloma is a strong possibility
ble, although the presence of reactive bone is as well.
more likely in metastatic carcinoma. Morse (1969:25, 144) briefly discusses a possible
Nemeskeri and Harsanyi (1959) describe the case of multiple myeloma from a site on Santa
skeletal remains, from the tenth to eleventh cen- Cruz Island, California, dated between A.D. 300
tury site of Kerpuszta, of a male about 50 years and 1450. T h e specimen is in the Lowie Museum
of age (burial no. 38, catalog no. 5293) which (No. 12-4356), University of California, Berkeley,
contain multiple lytic lesions. Their figures 9 - USA. There are multiple, coalescing, lytic lesions
12 show longitudinal sections of humerus, femur, on the skull and postcranial bones, features that
and innominate bones, all of which have lesions are compatible with multiple myeloma. T h e skel-
including a fairly large lytic lesion in the innom- eton is reported to be a female with an estimated
inate. Although a scale is not provided, this lesion age of 45.
appears to be in excess of 2 centimeters in largest Morse, Dailey, and Bunn (1974) published a
diameter. Roentgen films of the skull show mul- report on four paleopathological specimens from
tiple lytic lesions of fairly uniform size, none Florida and Mississippi, USA, with lesions that
appearing to be in excess of one centimeter. There they attribute to multiple myeloma. All were
seems to be evidence.of bony reaction surround- dated to the pre-Columbian period. The first of
ing some lytic foci, although sand infiltration these is a skull (their specimen number 1) from
NUMBER 28 267
the Sowell Mound thought to be a male about 45 to be associated with the postcranial bones shows
years of age. A photograph shows a large circular a normal outer cortex (Morse, Dailey, and Bunn,
lytic lesion 24 millimeters in diameter on the 1974, fig. 6). The roentgen film reveals lytic le-
occipital bone. There are other lytic lesions in the sions in the diploic space sometimes penetrating
skull ranging from 2 to 8 millimeters in diameter. through the inner table. There is a large eroded
The age and sex of this case are compatible with surface on the inner table, which the authors feel
a diagnosis of multiple myeloma; however, met- is antemortem. They suggest a large myelomatous
astatic carcinoma is equally possible and is more area could have destroyed the inner table. How-
compatible with the large variation in the size of ever, they indicate that this large lesion is not
the lesions. typical of myeloma. The long bones are unusually
Burials 1 and 2 from the Calico Hills mounds light suggesting osteoporosis.
in Jefferson County, Florida, USA, both show Three paleopathological specimens from the
multiple lytic lesions of the skeleton. Burial 1 is National Museum of Natural History, Washing-
reported to be a female about 25 years of age. ton, D . C , provide further insight into the prob-
The lytic lesions range in size from 1 to 13 milli- lems of differentiating between multiple myeloma
meters. The published roentgen picture reveals and osteolytic metastatic carcinoma. The first of
some lesions on the skull, but major involvement these is a female skeleton (NMNH 290064) from
is on the innominates and the distal femur. The the Indian Knoll site in Kentucky, USA. Most of
latter in particular shows multiple coalescing lytic the artifacts from this site are dated in the Late
lesions with some evidence of bony circumscrip- Archaic period (ca. 3000-1000 B . C ) ; however,
tion, although sand infiltration could be creating some components date to the Late Woodland
the appearance of reactive bone around the le- period (ca A.D. 800-1700). Thus the archeological
sion. The age and sex of the individual, as well as age of this specimen remains obscure but with a
the possibility of bony reaction to the disease strong probability of being Archaic. The age of
process, argue more for metastatic carcinoma the individual cannot be determined precisely.
rather than multiple myeloma in this case. The skull sutures had just begun to fuse on the
Burial 2 from the Calico Hills site consists of endocranial side, there is little evidence of arthri-
several postcranial bones and fragments of the tis, and tooth v^ear is marked. However, in this
skull. The authors report that the skull appears population tooth wear typically is marked in
to be female and 25 years of age or less. A adults. These criteria suggest an age in the 30- to
roentgen film of the skull shows multiple lytic 40-year range. The disease process consists of
lesions with no evidence of bony reaction. How- multifocal, mostly lytic lesions distributed in the
ever, a photograph of the skull (Morse, Dailey, skull, mandible, axial skeleton, and the proximal
and Bunn 1974, fig. 4) shows considerable porous left femur (the right femur is missing). The bones
bony reaction of the external skull surface in areas of the hands and feet are unaffected except for a
surrounding lytic foci. In this case the lytic lesions slight, superficial osteoporosis of the superior sur-
are compatible with multiple myeloma, but the face of the calcanei. The gross lesions vary in size
age and sex favor a diagnosis of metastatic car- from being barely detectable to about 15 milli-
cinoma. Infectious disease should be considered meters in diameter. Most of the cranial lesions
as well. (Figure 410) penetrate both tables, with no clear
The fourth case of purported multiple mye- pattern regarding which table is most extensively
loma is from the Magnum Mound in Clarbourne affected. The lytic process is more extensive in the
County, Mississippi, USA. Burial 4 from this site diploe, suggesting that the marrow was the focal
is a female postcranial skeleton of about 35 years point for the disease process. The roentgen films
of age. The vertebrae, ribs, pelvis, and right scap- of the skull and long bones reveal additional lytic
ula show multiple lytic foci. T h e skull (4) thought foci that are not visible from the outside. The
268 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
scapulae are present and both show multiple lytic of the other lytic lesions in the skeleton. This
foci (Figure 411), although the glenoid fossa is suggests a rather acute disease process. Steinbock
normal. However, unlike lesions elsewhere in the (1976:381-384) has reported on this case and
skeleton, there is a slight osteoblastic response concludes that "the size, location, and appearance
adjacent to several of the lytic foci. With this of the destructive lesions in this Archiac Indian
exception, there is no osteoblastic reaction to any are highly indicative of multiple myeloma rather
than metastatic carcinoma." While conceding
that multiple myeloma is a strong possibility
based on some aspects of the gross and roentgen
film morphology of the lesions, I feel that an even
stronger case can be made for metastatic carci-
noma. T h e lesions are somewhat more variable
in size than typical for multiple myeloma. Pe-
ripheral bone reaction on the scapulae is more
characteristic of metastatic carcinoma as is the
age and sex of the skeleton.
Another possible case of multiple myeloma is
a female skull from Peru ( N M N H 242559). This
specimen is fully adult and probably in the 30- to
40-year age range. T h e archeological age is un-
known. The external gross aspect of the entire
skull, except the face, is characterized by several
scalloped, lytic lesions (Figure 412), which vary
in size from pin holes to 15 millimeters in diam-
eter. There is no evidence of bony circumsciption
(Figure 413) either by inspection or on roentgen
films. The lesions are characteristic of both mye-
loma and metastatic carcinoma and, again to the
extent that age and sex are useful variables in
differential diagnosis, metastatic carcinoma
would appear slightly more probable.
The third case from the National Museum of
Natural History, Washington, D . C , USA, is also
a female skull from Peru ( N M N H 242578). Age
at death is, like the two previous cases, in the
range of 30 to 40 years. The archeological age is
unknown. Unlike the lesions in the preceding two
cases, the external appearance of the lesions is
much less obvious. T h e lytic lesions, which do
penetrate the surface, are small holes typically 1-
2 millimeters in diameter. O n the internal table
the lesions are somewhat more pronounced. All
FIGURES 410, 411.Multiple lytic lesions of the skull and
bones of the skull are affected, but the facial
postcranial skeleton: 410, Left lateral view of the skull and
mandible. 411, Posterior view of left scapula with lytic lesions
bones and occipital bone show much less involve-
and porous bone hypertrophy (arrow) adjacent to lytic focus. ment. T h e greater wings of the sphenoid and the
(Adult female from Indian Knoll, Kentucky, USA, N M N H body of the sphenoid are markedly affected with
290064.) much of the latter totally destroyed. In the X-ray
NUMBER 28 269
FIGURES 412, 413.Multiple scalloped lesions of the skull: 412, Left lateral view of the skull
with lytic lesions of varying size. 413, Detail of lytic lesion demonstrating the presence of spongy
bone which indicates a lack of circumscription. (Adult female from Caudivilla, Peru, N M N H
242559; scale in cm.)
270
NUMBER 28 271
supports his conclusion by citing sources that 580). In a subsequent publication Follis (1948:
indicate that the amount of vitamin C in contem- 140) states that "subperiosteal hemorrhages de-
porary Maya Indian diet is deficient and in the velop as a result of trauma and normal stress and
past many Indians died from scurvy. strain." Whether the normal stresses and strains
The lesions in Saul's figures are nonspecific and to which the head is subjected in the infant or
are more compatible with a diagnosis of infectious young child is sufficient to trigger bleeding, which
disease or trauma. The antemortem tooth loss could give rise to a large porous lesion, must
seen in Saul's figures 40 and 41 is from a specimen remain an open question. Although Fraenkel did
whose age he estimates to be 60+ years. The not note skull vault lesions in his report of scor-
pattern of alveolar resorption is more typical of butic autopsied cases, he did note the develop-
tooth loss due to caries and abscess. The anterior ment of porotic, hypertrophic bone in the orbital
teeth of the mandible are present as well, a con- roof (Fraenkel, 1929:228-229). The association of
dition that would be unlikely if the molar tooth both these features with scurvy needs further
loss was due to scurvy. confirmation. However, it would seem prudent to
Hooton (1930:317) suggested that porotic hy- consider scurx^^ as a possibility when such a lesion
perostosis found in the Pecos skeletal material is encountered in archeological specimens.
from the American Southwest is due to scurvy or
rickets. Cranial involvement in scurvy is not as Vitamin D Deficiency
common as that found in the long bones. Barlow
PATHOLOGY
(1883:169) however, noted porous lesions of the
external skull vault in association with at least
Rickets
one case of scurvy and reported (1883:168) ab-
normal conditions in the crania of 8 cases in a Rickets is a systemic disease of early childhood
sample of 31 scorbutic infants and children. extensively affecting the skeleton, but without
There remains a problem in ascribing porous direct mortality. It is caused by inadequate avail-
lesions of the skull to scurvy. It is a well-docu- ability of effective vitamin D, which is essential
mented fact that scurvy and rickets frequently in the mineralization process of the organic ma-
occur in the same case (Follis, Jackson, and Park, trix of bone (osteoid). Dietary vitamin D is trans-
1940:745). The presence of one disease does seem formed in the liver into the active compound.
to have an inhibiting effect on the expression of Precursors of vitamin D taken with the food
the other disease. The question of which disease are transformed in the skin under the influence
is dominant is unresolved. Based on histological of the ultraviolet fraction of sunlight. This ex-
evidence, Follis, Jackson, and Park (1940:746) plains the prevalence of rickets in populations
suggest that "vitamin D deficiency certainly in- climatically (high latitudes) or mechanically
hibits vitamin C deficiency from expressing it- (crowded cities, occlusive clothing) deprived of
self . . . " I n contrast Park, Guild, Jackson, and sunlight. However, it should be appreciated that
Bond (1935:286) offer the opinion that, since the darkly pigmented races are not fully benefited
vitamin C deficiency inhibits osteoid formation, by tropical sunshine, because most of the ultra-
the expression of rickets would be inhibited by violet rays are absorbed by the skin melanin
scurvy. It is also possible that scurvy could be pigment. The main causative factor remains the
found in association with anemia (Goldberg, inadequate intake of vitamin D and its precur-
1963:51) and that porous lesions of the skull are sors.
caused by anemia rather than scurvy. Rickets was not well documented by written
The experimental evidence suggests that hem- descriptions until the sixteenth or seventeenth
orrhage from scurvy with the associated bone century. From then on, increasing attention has
formation is seen only following trauma (Park, been paid to this common disease of early child-
Guild, Jackson, and Bond, 1935:276; Follis, 1943: hood, especially in northern Europe and North
274 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
America. There was a marked increase of fre- direct effects of the metabolic disturbance, de-
quency with industrialization and metropolitan formities secondary to the vulnerability a n d pli-
crowding. Figures for autopsy material in Dres- ability of the poorly mineralized skeleton, and
den, Germany, show that 89 percent of all chil- retardation of growth.
dren between 2 months and 4 years of age ex-
hibited evidence of active or healed rickets Rachitic and Postrachitic Changes
(Schmorl, 1909:437). Clinically, 97 percent of
in Individual Bones
young children had evidence of rickets in Vienna
(Escherich, 1899, cited in Hess, 1929:48) and, as SKULL.In active infantile rickets the cranial
late as 1921, Hess found 75 percent of the children vault may develop thin and soft areas, especially
in New York City affected by rickets (Hess, 1921: in the posterior lateral portions of the parietal
697). T h e disease occurs worldwide with varying bones and of the occipital squama (craniotabes).
frequency. This is due to the rapid remodeling of the infant
Rickets rarely begins before 4 months of age skull to accommodate the growing brain, replac-
because vitamin D passes from the mother to the ing mineralized bone with osteoid. This is not to
fetus through the placenta and is stored in the be confused with the incomplete ossification of
liver of the infant. T h e highest frequency is ob- the entire cranial vault in premature infants or
served between 6 months of age and 2 years in with the congenital lacunar skull often compli-
the sunless winter months. Only a few new cases cating spina bifida, in which sharply marginated
develop after 4 years of age. T h e manifestations multiple defects in various areas of the cranial
are earliest seen and most marked on the rapidly vault are present. Craniotabes may lead to per-
growing areas of the skeleton: osteocartilaginous manent posterior flattening or lateral and asym-
junctions of ribs, distal metaphysis of femur, ra- metrical deformities of the skull, due to pressure
dius and ulna, and proximal humerus (Wimber- of the head against the supporting surface in the
ger, 1925:269-288). T h e changes at the growth lying position. T h e closure of the fontanels is
plate consist of lack of preparatory calcification delayed in rickets. In cases where long-standing
of the columnar cartilage and of the newly de- thickening of the cranial vault is seen, especially
posited bone matrix (osteoid). Since the prolifer- in older children, mainly due to external (occa-
ation of cartilage and the formation of bone sionally also internal), subperiosteal bone depo-
matrix by osteoblasts continues at close to normal sition, the external deposition often spares the
levels, both uncalcified cartilage, which cannot center of the parietal and frontal tubera
be resorbed, and unmineralized osteoid pile up (Schmidt, 1929:32) (Figures 417-420). In this pro-
next to the growth plate. In the ribs this results in cess of remodeling, the outer and often the inner
a rounded nodular swelling of the osteocartilagi- table as well disappears, so that the entire thick-
nous junction, the "rachitic rosary," and, in long ness of the cranial vault has the porous appear-
bones, in a broadening and cup-shaped depres- ance of diploe (Figures 421-423). T h e weight of
sion of the metaphysial areas. Since the intra- the head may cause the bone surrounding the
membranous bone formation is affected equally foramen magnum of the softened skull base to be
to the enchondral one, the rapidly growing and pushed upward, diminishing or effacing the angle
expanding cranial vault of the infant becomes of the clivus (Schmidt, 1929:60). Similar subper-
increasingly replaced by nonmineralized osteoid iosteal deposits can occur on the facial bones
giving rise to areas of thinning and softening (Figures 424-426).
(craniotabes). This actually precedes recognition LONG BONES.The frequent combination of
of the changes in the long bones in acute rickets hypovitaminosis D and general malnutrition
(Hess, 1929:208). leads to a combination of rickets and osteoporosis,
T h e changes observed in rickets are threefold: resulting in the so-called porotic form of rickets,
NUMBER 28 275
FIGURE 421.Rachitic calvarium showing subperiosteal FIGURE 423.Rachitic calvarium, cut surface, showing po-
bone deposition with pronounced vascular pattern on right rous hyperostosis with obliteration of outer a n d partial ob-
parietal boss. T h e dried periosteum appears dark. (7-month- literation of inner table. (2-year-old male, F P A M 2694 from
old female with rickets and scarlet fever, D P U S 5212 from 1858.)
1904.)
NUMBER 28
277
FIGURES 428, 429.Severe malacic rickets with very light, porous bones: 428, Both arms and
shoulder girdle with bending deformities and healing stress fractures of all bones. 429, Close-up
of left hand. (About 2 years of age, A N M 3334 and 3335.)
long bones and sternal ends of the ribs would drain on the mother of bone mineral and vitamin
have the best chance of being preserved. How- D. This loss to the fetal skeleton and, through the
ever, postrachitic deformities of the various bones milk, to the infant is a significant factor in the
of the skeleton would be readily recognizable. pathogenesis of puerperal osteomalacia.
The disease used to be common in Europe in
Late Rickets crowded cities and under poor economic condi-
tions. Numerous cases have been reported from
Rickets developing or recurring in later child- China and I have seen, even recently, many cases
hood and adolescence, at a time when bone in India. There, skin pigmentation, shrouding
growth has slowed down greatly, is more charac- clothing, and seclusion of women indoors (pur-
terized by severe mechanical deformities than by dah) still contribute to the prevalence of the
changes at the growth plate resulting in deficient disease, in addition to the other factors enumer-
or altered growth. These deformities are essen- ated above.
tially identical with those of adult osteomalacia.
Although the deficiencies affect the entire skel-
eton, the most marked changes are observed in
Osteomalacia
the bones that contain mostly cancellous bone
The etiology of osteomalacia is identical with and, therefore, have the highest remodeling rate.
that of ricketsvitamin D deficiency. The differ- These are the ribs, sternum, vertebrae, and pelvis
ence in the manifestations is due to the fact that (Figures 434, 435). The skull and the solid cortices
in the adult the skeleton is no longer growing; of the long bones of the extremities have a low
therefore, various changes on the cartilage and remodeling rate. Therefore, deformities of osteo-
bones of the growth plate, which dominate the malacia rarely occur in these bones except in
picture of rickets, are no longer present. As in young, still growing individuals (late rickets and
rickets, the bone matrix formed during the disease juvenile osteomalacia).
remains uncalcified (osteoid). The first radiolog- The specific change of osteomalacia is the dep-
ical changes are a diffuse diminished density of osition of unmineralized osteoid on the trabeculae
the otherwise normal-appearing skeleton, not dis- of old bone and the replacement of resorbed old
tinguishable from osteoporosis. In dry bone the bone with osteoid. However, in contrast to rickets,
light weight and cardboard-like consistency is subperiosteal deposits do not occur.
noted (Figure 431). Depending on the remodeling Looser-Milkman zones of great radiolucency,
rate, it takes considerable time before the skeleton often followed by stress fractures only transecting
is sufficiently weakened to show radiolucent zones the overburdened cortex, occur in characteristic
in mechanically stressed areas, due to replace- locations and often symmetrically. The predi-
ment of the mineralized bone with osteoid lected areas are the ribs, the medial cortex of the
(Looser, 1920; Milkman, 1930). In severe and neck of the femur and of the humerus, the pubic
protracted cases, mechanical deformation of the rami, and the lateral margin of the scapula. In
skeleton, due to fractures and pliability, dominate many instances multiple such stress fractures oc-
the picture (Figures 432, 433). cur in each area. In healing, internal and external
In the causation of osteomalacia, in addition callus is formed, which ultimately mineralizes.
to vitamin D deficiency, general malnutrition, The osteomalacic deformities are usually re-
especially deficiency of protein and fat, and low stricted to the trunk skeleton. T h e vertebrae are
intake or loss of calcium and phosphorus, play an flattened with accentuated cupping of the end-
important role. This explains the great prevalence plates and dense trabeculae. There is angular
of the disease in the female, particularly between kyphosis in severe cases, often at the level of the
20 and 40 years of age. Numerous closely spaced eighth or ninth dorsal vertebra, occasionally com-
pregnancies and protracted lactation are a heavy bined with a scoliotic curve (Jaffe, 1972:401). The
NUMBER 28 281
spinal deformity alters the shape of the thorax, 1939:535-540). Deformities of the long bones of
which becomes deep and laterally narrowed. The the extremities are much less common. They
ribs show a decreased curvature and the sternum consist most often of downward bending of the
is angulated and pushed forward. In very severe neck of the femur (coxa vara) or of the humerus.
cases the ribs may, in addition, show inward Deformities of the shafts of these bones are rare
bending, laterally, due to the pressure of the arms and due more to fractures than to pliability.
(Figure 436).
The most marked and most characteristic de-
formation is observed on the pelvis in puerperal
osteomalacia (Figure 436). The fourth or fifth
lumbar vertebral bodies descend and protrude
into the pelvic canal. The iliac wings are rolled
and folded inward. The pubic rami are pushed
together with the symphysis pubis projecting,
beak-like, forward. The ischial tubera are bent
medially and the acetabular floors protrude in-
ward. The sacrum is bent angularly forward in
the lower portion (Figure 437). All these deform-
ities narrow and partly obliterate the pelvic canal,
reducing it to a cloverleaf-shaped space (Breus
and Kolisko, 1900-1911(2) :50-62; Putschar,
Although the osteoid of the active phase would Hrdlicka (1907:540) stated that in North
not survive burial, the characteristic deformities America rickets did not occur in prehistoric in-
that remain, even after healing and restored min- digenous groups. Snow (1948:508) describes a
eralization, will be readily recognizable. possible case of rickets in an 8-month-old infant
(Burial 633, Indian Knoll site, Kentucky, USA).
Skeletal Changes Resembling Rickets and Osteomalacia However, the description of features that lead to
this conclusion is not convincing. Snow does not
Excessive loss of dietary vitamin D due to report any evidence of deformity in the long
inability of resorption from the intestines will lead bones. He bases his conclusion on the presence of
to the changes of rickets or osteomalacia, depend- "swollen spongy extremities" in the smaller long
ing on the age of the patient. Such conditions are bones and abnormal sternal ends of ribs. Since
celiac disease and nontropical sprue, chronic bil- these are areas of active growth and consequent
iary stasis and biliary fistula. In the first, the fat- remodeling, they would normally appear some-
soluble vitamin D is eliminated with the fatty what spongy. In view of the lack of evidence of
diarrheic stools; in the others, the bile salts nec- rickets in other North American skeletal series,
essary for the resorption of vitamin D are not this case should be reevaluated.
present in the gut. In the Old World, Wood-Jones (1910b:263)
A group of syndromes characterized by various found no evidence of rickets in ancient Egyptian
congenital defects in the renal tubules concerning skeletal material. Virchow (cited in Pales, 1930:
excretion and reabsorption of different substances 40) thought that the distinctive features of Euro-
also, ultimately, affect the metabolic integrity of pean Neanderthal skulls were due to rickets. This
the skeleton (refractory or vitamin D-resistant possibility has not, however, received serious con-
rickets). The changes, when they occur, are essen- sideration by subsequent scholars who have stud-
tially identical with rickets or osteomalacia, the ied the Neanderthal skeletons. In the Winchester
only difference being that they do not develop Saxon collection of paleopathological specimens
until later childhood or adulthood. In those con- (BMNH CG 1966, no number) is a case of me-
ditions in which various amino acids are lost dieval healed rickets in a child about 6 years of
through faulty renal excretion on a genetic basis, age. The specimen consists of the right femur,
in addition to and preceding the manifestation of tibia, and fibula. Anterior bowing is most pro-
rickets or osteomalacia, one may observe severely nounced on the femur and tibia (Figure 438).
inhibited growth (dwarfism) and severe osteopo- Another example of healed rickets is from the
rosis leading to pathological fractures because of Royal College of Surgeons of England pathology
the inability to produce adequate amounts of collection at the British Museum (Natural His-
organic bone matrix. tory). The case is from the Ludgate Hill site in
England (No. 1961, 5, 12, 5). The specimen is a
right femur from an adult. There is marked an-
terolateral bowing with anteroposterior flattening
PALEOPATHOLOGY
and a buildup of bone along the linea aspera
Wells (1964a: 116-117) expresses the opinion (Figure 439).
that medieval European towns and the "perpet- An example of rickets is found in the skeletal
ual twilight of dark tenements," in the city slums, collections of the Historical Museum in Chur,
which were a prominent feature of cities during Switzerland. The specimen is from the medieval
the Industrial Revolution, were the major factors archeological site of Bonaduz in canton Grissons,
in the marked increase of rickets associated with Switzerland. The skeleton in question is a male,
this phase of human history. Evidence of rickets probably over 50 years of age. The only evidence
in other geographical areas and other time pe- of deformity is seen in the tibiae. Both the right
riods is not common. and left tibiae show bowing with an increased
284 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURE 438.Healed rickets in the right leg of a child about FIGURE 439.Healed rickets in an adult femur. (BMNH,
6 years of age. Note that the interosseous line of the tibia is Ludgate Hill No. 1961, 5, 12, 5.)
curved. (BMNH CG 1966, no number; scale in cm.)
anteroposterior diameter of the midshaft and a geons of England pathology collection, which is
very prominent anterior edge (Figure 440). stored at the British Museum (Natural History)
Osteomalacia must certainly have occurred in (BMNH 178A). The specimen is from a predyn-
ancient times although the evidence for it is astic Nubian and consists of the major bones of
scarce. A probable example of osteomalacia is the arms and legs, the pelvis, and three lower
seen in an isolated sacrum from the Twelfth lumbar vertebrae. The most striking feature of
Dynasty, rock tombs at Lisht, Upper Egypt the specimen is the very extensive hypertrophic
(NMNH 256470 PI). The sacrum is small in size bone development on the femora. Rowling attri-
and unusually light in weight. It appears to be butes this development to paraplegia with possi-
from an adult female skeleton. There is a 90 ble complications of rickets.
degree angle between the lower and upper por- T h e authors have also studied this specimen
tion of the sacrum (Figure 441) with the angula- during our survey of pathological specimens in
tion primarily at the third sacral segment (cf 1974. In addition to the extensive hypertrophic
Figure 437). bone associated with the femora, these bones
Rowling (1967:275-278) describes a remark- show anterolateral bowing (Figures 442, 443). On
able specimen from the Royal College of Sur- the right femur, bowing is complicated by a
NUMBER 28 285
Hypophosphatasia
PATHOLOGY
Starvation
PATHOLOGY
Fluorosis
PATHOLOGY
are affected. Such teeth show spotted enamel and showed the greatest female prevalence in
consisting of small, round, discolored and pitted Sweden and the least in the Bantus (Chalmers
areas in the otherwise shiny and white enamel and Ho, 1970).
surface. Bone changes are only observed in long- Osteoporosis does not affect the entire skeleton
standing and severe cases (Flemming M0ller and evenly. Since the greatest physiological turnover
Gudjonsson, 1932; Sankaran and Gadekar, 1964). of bone occurs in cancellous bone, the bones rich
Fluorine stimulates periosteal and endosteal bone in spongiosa are most involved in osteoporosis.
formation, but the bone produced is microscopi- The bones of the trunk, such as the spine, ribs,
cally and mechanically abnormal. Externally, ex- sternum, and pelvis, are most severely affected by
aggeration of insertions of muscles and ligaments osteoporosis. Of the large bones, the heavily bur-
are noted by addition of bone-forming irregular dened femoral neck, which also mainly depends
excrescences (Figure 445). There is marked accen- for its integrity on the trabecular architecture,
tuation of the linea aspera of the forearm and shows the most characteristic changes. The skull,
lower leg (Figure 446). T h e ribs and vertebrae especially the calvarium, participates very little
show ridges and icicle-like, bony excrescences into in senile osteoporosis. This may be, at least in
the intercostal muscles and paraspinal ligaments. part, due to the continued mechanical stresses of
There is considerable subperiosteal and endosteal chewing.
bony accretion, often accompanied by increased T H E CANCELLOUS BONES.The vertebral bod-
resorption in the old cortex on long bones (Figure ies usually show osteoporosis first and most se-
447). The fluorosis bone is mechanically inferior verely. The normal dense vertical and transverse
and pathological fractures occur. trabecular system becomes reduced. In this pro-
cess the transverse trabeculae are more affected
Osteoporosis than the vertical ones. The trabeculae are not
only diminished in number but also in size. In
PATHOLOGY late stages of osteoporosis the few remaining ver-
Senile osteoporosis represents a condition of tical trabeculae may become reinforced (sclerotic
significantly diminished bone mass due to long- atrophy). Although the bone is normal in matrix
standing imbalance between bone resorption and structure and mineralization, the diminished
bone formation. With increasing age, bone for- quantity creates mechanical instability. If the
mation lags more and more behind bone resorp- intervertebral discs retain their normal turgor,
tion thus diminishing the entire bone mass. This they will bulge the thinned vertebral, bony end-
leads imperceptibly into osteoporosis, which most plates, creating the picture of so-called "fish ver-
observers arbitrarily define as a loss of 30 percent tebrae" (Figure 448). If the intervertebral discs
of bone mass or more. Osteoporosis usually does are degenerated, this deformity of the vertebral
not manifest itself before the fifth decade and is body does not occur in spite of severe osteoporosis.
more frequent and more severe in the female than Compression fractures resulting in flattened or
in the male. This, at least in part, reflects the wedged vertebrae are common, the latter result-
sharp drop in estrogens at menopause as com- ing in secondary kyphosis. The other cancellous
pared with the slow steady decrease of testoster- bones show similar changes characterized by rar-
one in the aging male. However, comparative efaction of the spongiosa and pronounced cortical
statistical studies between affluent industrialized thinning. The ribs also often exhibit multiple
populations and primitive populations requiring osteoporotic fractures which, however, heal with
strenuous physical activity from both sexes, indi- good callus response.
cate that the mechanical forces play a great role T H E LONG BONES.Since the physiological
in the development of senile osteoporosis. Severe turnover in cortical bone is much slower and less
osteoporosis, as measured by the incidence of than in cancellous bone, the long bones, with
fractures of the femoral neck, was highest overall predominantly cortical bone, are later and less
290 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 449, 450.Extreme osteoporosis of right femur due to disuse and malnutrition. 449,
External posterior view; notice reticulated perforations of metaphysial cortex. 450, Cut surface;
notice paper-thin cortex and sparse trabeculae. (28-year-old female with tuberculosis of hip
died in extreme cachexia, F P A M 4433, autopsy 81477 from 1884.)
suggests that the atrophic condition involves the male. The oblong atrophic lesions are located in
outer table and diploe with, in extreme cases such the posterior region of the parietals (Figures 452-
as this one, some thinning of the inner table. 454). The depressions are smooth but show re-
There is no evidence of abnormal loss of bone modeled spongy bone. The lesions are even larger
thickness or density in other parts of the skull. than those in the skull from Peru. The morphol-
The second example is a skull from the Twelfth ogy of the atrophic depressions suggests a process
Dynasty site near Lisht in Upper Egypt (NMNH that primarily involves the outer cortex and the
256186). The skull appears to be from an old diploe. The remainder of the skull is normal.
294 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
This is a rare condition in which long-contin- This is a rare familial disorder characterized by
ued excessive bone formation on the cranial and excessive formation of dermal collagen and of
facial bones leads to marked distortions of the periosteal bone. T h e disease usually begins
NUMBER 28 295
around puberty and progresses through adult life. bones may be transformed into solid bony blocks.
The outstanding feature in advanced cases is the (For a detailed discussion see Uehlinger, 1941.)
markedly increased diameter of long bones, with-
out alteration of the joint ends (Figure 458). The PALEOPATHOLOGY
surface of the bones shows a rough irregular Allison, Gerszten, Sotil, and Pezzia (1976) have
texture. On cross-section the new bone blends described an archeological case of generalized
into the old cortex, which may show considerable hyperostosis with pachydermia in an adult female
porosis. The medullary canal is not obliterated. skeleton. The case is from a Huari-culture ceme-
The skull usually shows only sclerosis of the skull tery, which is dated about A.D. 1000 and is located
base and of the diploe. The cancellous bones are in the Ingenio Valley, lea, Peru. The bones of the
less thickened and their trabecular architecture skeleton are thickened and have greatly dimin-
becomes coarse and exaggerated (Figure 459). ished marrow spaces. This has resulted in the
The pelvis shows rough osteophytes and exostoses. bones being as much as '2}h times heavier than
In late stages spinal ligaments and interosseous normal. Histologically the bone tissue, while
membranes may be ossified. Large and small thicker than normal, has good lamellar bone with
joints may become ankylotic. Carpal and tarsal normal osteon remodeling.
Endocrine Disturbances
The skeletal growth and maturation is results in an open communication between the
mainly controlled by an intricate interrelation- sella and the cavum sphenoidale in the dry skull.
ship between pituitary and thyroid. This interre- In pituitary hyperplasia the contour of the sella
lationship can be separated only in the animal may not be significantly altered. Continued hy-
experiment, revealing that the pituitary mainly perpituitarism beyond the growing period leads
controls growth and the thyroid maturation to a superposition of acromegalic features onto
(Asling and Evans, 1956). Estrogens and andro- the giant skeleton (Figure 460).
gens of testicular or adrenal origin stimulate lon-
gitudinal growth but hasten epiphysial closure. Acromegaly
(For a general discussion of endocrine-skeletal
relations see Putschar, 1960:405-414.) This condition is much more common than
pituitary gigantism and is usually the result of an
acidophilic adenoma of the pituitary occurring in
Pituitary Disturbances an adult (Figures 461-464). After closure of the
PATHOLOGY
Pituitary Gigantism
298
^ ^ **
FIGURES 461-464.Acromegaly: 461, Skull, lateral view, showing prominent chin, malocclu-
sion of teeth and prominence of inferior and superior nasal spine. 462, Skull base, showing
enlarged frontal sinuses, enlarged sella (arrow) with resorption of anterior and posterior clinoid
processes. 463, Right hand, showing extreme arrowhead tufting of terminal phalanges, and
periosteal hyperostosis. 464, L u m b a r vertebrae, showing marked subperiosteal apposition. (39-
year-old male with pituitary adenoma, FPAM, Jubilaumspital 610.)
300 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
an apparent overgrowth leading to prognathism Morse (1969:26, pi. 22b) provides a brief sum-
and malocclusion. Brothwell's diagnosis of acro- mary of features associated with acromegaly ac-
megaly is almost certainly correct. companied by a lateral photograph and roentgen
film of the skull and mandible of a Late Wood-
land (ca. A.D. 900) burial from Dick's mound in
Illinois, USA. He describes the long bones as
elongated and thickened and the lower jaw as
lengthened. The photograph of the roentgen film
and description of the long bones support a di-
agnosis of acromegaly.
The almost complete skeleton of an indigenous
North American from the Midwest, USA
(NMNH 227508) provides another possible ex-
ample of acromegaly. The skeleton is from the
historic period and is remarkable because of the
massive size of both skull and postcranial bones.
The maximum length of the skull is 201 milli-
meters, maximum breadth is 144 millimeters. The
cranial capacity is estimated to be 1865 cubic
centimeters, which is well within the normal hu-
man range but about 400 cubic centimeters
greater than average. The gross morphology of
the skull is rugged (Figures 465, 466) with pro-
nounced and unusually high markings (near the
sagittal suture) for the origin of the temporalis
muscle. The mandible has slightly overgrown the
development of the maxilla and has prominent
bony projections on the anteroinferior border of
the chin. The roentgen film demonstrates clearly
the additional growth of the mandibular condyles
and the increased angle between the ramus and
mandibular body. The roentgen film (Figure 467)
reveals a large but not abnormal pituitary fossa;
thus the presence of a pituitary tumor is proble-
matical.
The long bones are long and heavy. The right
femur, for example, is somewhat damaged post-
mortem, but the estimated length is 545 milli-
meters. Stature estimates based on this length are
189.75 centimeters (ca. 75 inches). This is cer- have fused, indicating an age in excess of 12 years.
tainly at the upper end of the normal range The ischiopubic ramus is unfused. T h e distal
among American Indians but not abnormal. This epiphysis of the humerus has fused. These features
suggests somewhat greater pituitary function dur- added to the dental eruption clearly indicate an
ing growth but with major morphological age in excess of 12 years in a normal individual.
changes, as in the skull, occurring after the nor- Because of the delayed development and fusion
mal growth period had ended. of epiphyses in pituitary dwarfism, a minimal age
The skeleton appears to be fully adult and in the twenties would seem more likely for this
male with estimated age, based on the morphol- case.
ogy of the fragmentary pubic symphysis, about The skull is somewhat deformed postmortem
35 to 45 years of age. The ends of the ribs show but is obviously much smaller than normal (Fig-
evidence of secondary growth as would be ex- ures 468, 469). Maximum length is 145 millime-
pected in acromegaly. The bones of the hands ters, maximum width is 108 millimeters. Typical
and feet are large but of normal proportions, skull measurements for a 12-year-old child from
although the phalanges, particularly the terminal the same site would be maximum length 160
phalanges, show evidence of secondary growth millimeters and maximum width 127 millimeters.
and remodeling on the distal ends (tufting). The The relative proportions of the skull are normal
abnormal features of this skeleton are compatible although more typical of a child than a 20 year
with a diagnosis of acromegaly. However, the old. Unfortunately, the base of the skull has been
disease process does not appear to be as severe as damaged and lost, making observations on the
cases encountered in the European pathology pituitary fossa impossible.
collections. The postcranial long bones are very slender
and shorter than normal (Figures 470,471). Stew-
Pituitary Dwarfism art (1968:133) indicates that the approximate
femoral length (without epiphyses) of a 12 year
I know of no references on pituitary dwarfs in old is 310 millimeters. T h e femoral length of the
the literature on paleopathology; however, there dwarf is about 280 millimeters or 90 percent of
is a probable case of this condition in the collec- the expected length of a 12 year old. If, as I think
tions of the National Museum of Natural History, likely, the dwarf was fully grown the expected
Washington, D . C , USA (NMNH 314306). This femur length would be about 370 millimeters and
remarkable case is from the Hawikuh site in New thus would have been only three-fourths as tall
Mexico, USA, which includes late precontact and as normal. T h e torsion angle of the left femur is
early historical components. The skeleton is frag- unusually large and probably would be associated
ile and damaged but includes most of the bones. with an abnormal gait during life.
The features of dental and skeletal maturation The vertebrae are small but of normal propor-
used in estimating age are affected by a deficiency tions, although the bodies of thoracic vertebrae
of pituitary hormone. Therefore, the age of the T 5 - T 1 1 show a slight eccentric development to
skeleton cannot be determined with certainty. the right, which might be associated with a slight
However, the second permanent molars have scoliosis. T h e sacrum and innominates are small
erupted. There is no evidence of a third molar in but of fairly normal proportions, although the
the left mandibular fragment; however, this ab- anteroposterior dimension of the pelvis is longer
sence might be due to agenesis rather than young than would be expected. T h e pubic symphysis is
age. All the teeth that are present are normal in poorly formed lacking the normal features of the
size, which has created severe crowding in the symphysial face and the ridge formation. The
small jaws. bones of the hands and feet are of normal shape
In the postcranial skeleton most epiphyses are although very small.
unfused. The primary elements of the innominate T h e overall appearance of the skeleton conveys
NUMBER 28 303
FIGURES 468-471.Pituitary dwarf: 468, Comparative facial views of normal (left) and dwarf
(right) skulls: normal skeleton selected on basis of comparable dental and epiphyseal develop-
ment and closure. 469, Right lateral view of skulls; note the prognathism of the dwarf skull.
470, Compartive anterior views of a right normal and abnormal femur and tibia. 471, X-ray of
same long bones. (Normal bones, N M N H 308611; dwarf, N M N H 314306.)
304 SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
ultimately close, albeit beyond middle age. The Excessive amounts of thyroxin, as observed in
last to close is the spheno-occipital growth plate, Graves' disease or toxic goiter, mostly occur in
resulting in a brachycephalic configuration. The adults. Skeletal changes in this condition may be
cranial sutures also remain open longer than nor- absent or limited to increased bone resorption,
mal. Continued growth at the mandibular con- producing osteoporosis. Occasionally, these
dyle may ultimately result in some degree of changes may mimic those in mild hyperparathy-
prognathism. The marginal ossification centers of roidism and result in stress fractures (Askanazy
the scapula and the ilium may form only incom- and Rutishauser, 1933; Uehlinger, 1957). These
pletely and remain open (Looser, 1929). findings would not be diagnostic of hyperthyroid-
Most epiphyses show multifocal irregular ossi- ism in dry bones.
fication centers, which later fuse (for details see
Wilkins, 1941) (Figure 473). These abnormalities Cushing's Syndrome
of the ossification centers are specific. The devel-
opment of the ossification center of the head of Of the different hormones produced by the
the femur is not only delayed but often abnormal. adrenal cortex under stimulation of pituitary
The lack of bony support of the femoral head adrenocorticotropic hormone (ACTH), only the
leads to deformation of the cartilage model, sec- glucocorticoid cortisone needs to be discussed
ondary to static and dynamic stresses. The end briefly in regard to its skeletal effects.
result is a misshapen flattened head with a mush- Cushing's syndrome may be caused by any of
306 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
the following: hyperplasia, adenoma, carcinoma surface appears normal. Although this osteopo-
of the adrenal cortex, or, less commonly, adenoma rosis is not specific, severe changes of this kind
of the basophilic pituitary cells. The excessive and severity, particularly in a child or young
secretion of cortisone leads to suppression of pro- individual, are very suggestive of Cushing's syn-
tein synthesis, including production of collagen. drome.
T h e ensuing osteoblastic suppression and scarcity
of bone matrix production results in severe osteo-
Hypogonadism
porosis. The osteoclastic resorption is not in-
creased, but it is not balanced by a corresponding Estrogen and testosterone both stimulate en-
amount of bone formation. The condition may chondral growth and skeletal maturation. In both
be observed at any age. The severe osteoporosis is sexes subnormal production of gonadal hormones
most marked in bones rich in trabeculae where will delay the appearance of secondary ossifica-
the normal turnover is rapid. The vertebral col- tion centers and postpone the closure of epiphys-
umn and ribs are most severely affected. The ial discs and sutures. Periosteal bone formation is
vertebral bodies show marked cortical thinning also inhibited, resulting in a gracile skeleton with
and severe reduction in the number and size of thin cortices. Since the period of enchondral
the trabeculae (Figure 475). The end-plates bulge growth is markedly lengthened, the normal skel-
inward due to the pressure exerted by the resilient etal proportions are altered due to disproportional
intervertebral discs, creating the picture of bicon- length of the upper and lower extremities
cave, so-called "codfish" vertebrae. The vertebral (eunuchoid stature) and elogation of the mandi-
bodies lose height and compression fractures are ble, producing some degree of prognatism. Since
common. Anterior wedging with kyphotic de- castration of the male was practiced in various
formity on the vertebral column occurs. The ribs cultures, it is worth mentioning that in the early
become severely osteoporotic and may exhibit castrate (eunuch) the above-mentioned changes
multiple pathological fractures (Sissons, 1956). are present in a most marked degree, resulting in
The long tubular bones also show trabecular a tall, long-legged, gracile skeleton. Cessation of
osteoporosis and endosteal cortical resorption, but production of gonadal hormones in the adult,
the changes are less obvious and the outer cortical either by involution (menopause) or pathologic
destruction of the gonads will often ultimately,
over a period of about one decade, result in trunk
osteoporosis in either sex (Nowakowski, 1955).
Hypergonadism
Hypopara thyroidism
FIGURE 475.Cushing's syndrome. Vertebra with extreme The parathyroids control the level of ionized
osteoporosis after 10 years of cortisone therapy. (51-year-old calcium in the blood plasma. This is accom-
female, M G H autopsy 20884.) plished by increased secretion of parathormone
NUMBER 28 307
Hyperparathyroidism
309
FIGURE 480.Mosaic pattern with numerous cement lines
in Paget's disease, femoral cortex. Ground polished section
of undecalcified bone. Polarized light, approximately XlOO.
(Specimen courtesy Prof E. Uehlinger.)
"^ ^^'k
'1 1
t'.'i'. - M
I. * Jl1 ^ if. j
but does not cross the synchondrosis. Ribs are not tibiae was sent for study to Dr. Lent C. Johnson
uncommonly affected and may become markedly at the Armed Forces Institute of Pathology in
thickened. Washington, D.C. Johnson found no histological
PAGET SARCOMA.In longstanding active Pa- evidence of Paget's disease in the bone.
get, especially of the long bones and calvarium, Wells and Woodhouse (1975) report a case of
a sarcoma may arise in one or several areas Paget's disease in a skeleton from an Anglo-Saxon
(Figure 494). burial ground (A.D. 950) in Durham, England.
The skeleton is male with an estimated age of 65
PALEOPATHOLOGY years. The authors indicate that the skull is unu-
sually thick. The surface of most bones is rough
The earliest reference to Paget's disease in ar- and pitted. T h e spine exhibited kyphoscoliosis
cheological human remains is a report by Pales with evidence of osteoarthritis. The pelvis has the
(1929:263-267), which includes a brief discussion appearance of a slight osteomalacic deformity.
of a femur from the Neolithic site at Lozere in The major bones of all the extremities are bowed.
France. The specimen is part of the collections of The left femur was fractured antemortem with
the Museum of Natural History of Paris. There poor alignment and considerable deformity with
has been some postmortem damage to the joint healing. The poor quality of the bone prevented
surfaces, but otherwise they appear normal. the preparation of microscopic sections; thus the
There is considerable anterior curvature of the presence of the mosaic histological pattern could
diaphysis with a marked expansion of the cortex. not be determined. However, the generalized dis-
The X-ray film indicates that the cortical bone tribution of abnormal bone, the long bone de-
in the diaphysis is reduced in density. T h e line formity, and the roentgen film appearance of the
drawings, published in Pales (1929) as figures 1 femora and vertebrae are compatible with a di-
and 2, portray a gross morphology compatible agnosis of Paget's disease. T h e vertebrae show
with a diagnosis of Paget's disease. No histology coarse vertical striations and discontinuity of af-
was reported, making this diagnosis probable but fected vertebrae.
not certain. The antiquity of this specimen would
certainly make restudy with appropriate histol-
ogy desirable. Fibrous Dysplasia
Five purported cases of Paget's disease in pre- PATHOLOGY
historic skeletons from the Illinois River Valley
in the United States were published by Denninger Fibrous dysplasia is a bone disease of unknown
(1933). In all cases the long bones have a thick- etiology characterized by faulty differentiation of
ened cortex. In some of the cases the skulls were portions of the osteogenic mesenchyme into fibro-
thickened. In no case was there any report of the osseous tissue. It manifests itself in a single or in
histology. In view of the many disease conditions multiple bones, often limited to one limb or one
that can produce the lesions described by Den- side of the body (Lichtenstein and Jaffe, 1942:
ninger, including periostitis and osteomyelitis, 814). The entire skeleton is never involved even
these specimens would need to be restudied before in widespread manifestations, and there is no
the diagnosis of Paget's disease can be accepted. basic metabolic disorder (Figures 495, 496). T h e
Fisher (1935) reports a purported case of Pa- disease, especially the polyostotic form with wide-
get's disease in a skeleton from a prehistoric spread manifestations, usually begins in child-
mound in Crawford County, Wisconsin, USA. hood and often stops progressing at the termina-
The specimen consists of portions of both tibiae tion of the growth period (Uehlinger, 1960:283).
and a part of the lower jaw. Morse (1969:57-58) Females are more often affected than males and
also discusses this case noting that the jaw frag- may exhibit endocrine disturbances leading to
ment is normal. He also notes that one of the precocious puberty and premature termination of
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
316
FIGURES 495, 496.Polyostotic fibrous dysplasia showing "shepherd crook" deformity of both
proximal femora and deforming involvement of many bones: 495, Anterior view. 496, Posterior
view. (40-year-old female, D P U S 4016, French catalog 323a from before 1891.)
growth (Albright's disease) (Albright, Butler, cyst-like lesion confined by a ridged, thin, bony
Hampton, and Smith, 1937) (Figures 497-499). shell, particularly in small and flat bones, such as
The bone lesion consists of dysplastic prolifer- ribs and pelvis. The weakened bony structure
ation of endosteal fibrous tissue, in which fine permits mechanical deformities with or without
trabeculae of woven bone arise by direct fibro- major pathological fractures (Figure 497). The
osseous metaplasia, without differentiation of os- recognition of the lesion in dry bone would de-
teoblasts. Depending on the amount of bone and pend on at least partial preservation of the fine
the degree of mineralization, the lesion may ap- or coarse woven bone trabeculae (Figure 500).
pear purely lytic, ground-glass, or dense on X- Admittedly such preservation may be unlikely
ray. It may ultimately involve most parts of a and differentiation from various other lesions,
bone, sparing some portions and practically al- especially giant cell tumor, unicameral cyst, and
ways sparing the epiphyses. In small bones, tu- nonossifying fibroma may be impossible in a
mor-like expansion is observed after pressure re- single lesion. Hyperparathyroidism should be pos-
sorption of the old cortex. However, at least a sible to rule out on the basis of absence of meta-
thin shell of newly formed periosteal bone sur- bolic bone disease in uninvolved parts of the
rounds the lesion at all times. This results in a skeleton.
NUMBER 28 317
This condition occurs most frequently in a rib, Denninger (1931) provides a description of a
the proximal femoral metaphysis, the jaws, or the probable case of polyostotic fibrous dysplasia in
tibia. Other bones are less frequently involved an adult male skeleton from a pre-Columbian site
(Schlumberger, 1946a, 1946b). In dry bone, dif in Illinois, USA. The disease affected the bones
ferentiation from eosinophilic granuloma and en- of the left side of the body. The left side of the
chondroma may be impossible, especially in the skull was deformed and there was the character-
rib. In the mandible, or less often in the maxilla, istic shepherd's crook deformity of the left femur.
giant cell reparative granuloma or eosinophilic The cortex of the bowed upper end of the left
granuloma may give a similar picture. Probably femur is thin. This region has multiple cyst-like
the most characteristic solitary lesion is that of lesions revealed in the roentgen film. Postmortem
the proximal femoral metaphysis. The dysplastic breakage reveals the poorly organized bone par-
focus often weakens the subtrochanteric area re- tially filling the marrow space. The right femur
sulting in the typical "shepherd crook" deformity, is not deformed but exhibits some pathological
while the head and neck of the femur are more changes on the proximal end. In the region of the
nearly normal. greater trochanter, there are perforations of the
cortex with poorly organized, spongy bone ap-
parent through the perforations. Similar lesions
are found on both tibiae and fibulae. The bones
Polyostotic Fibrous Dysplasia
of the left foot show increased porosity of the
In involved limbs the disease affects the proxi- cortical surface with cortical perforations and
mal bones earlier and more severely than the spongy bone apparent in the first and second
distal ones. The proximal femoral metaphysis is metatarsals. Perforations and spongy bone devel-
the most frequent location (Figures 501-503). In opment are also seen in the bones of the pelvis
36 cases of polyostotic fibrous dysplasia, the in- primarily on the left side. The ribs of the left side
volvement of different bones was as follows: femur are similarly affected as is the seventh cervical
36, tibia 24, fibula 10, metatarsals 10, toes 8, vertebra and many of the thoracic vertebrae.
humerus 12, radius 9, metacarpals 8, fingers 6, Denninger's description of this case leaves little
pelvis 15, skull base 6 (Schinz, Baensch, Friedl, doubt that this pre-Columbian Indian skeleton is
and Uehlinger, 1951-1952(2): 1199). an example of polyostotic fibrous dysplasia.
The lesions in the cranial vault and face are Wells' (1963b) report of an adult skeleton from
asymmetrical and often unilateral (Figure 498). an Anglo-Saxon site in Britain, dated in the
Rounded masses of woven bone can be found in seventh century A.D., provides another example
the diploe, similar to those seen more frequently of probable fibrous dysplasia. Of the bones re-
in advanced Paget's disease. Lesions of the skull covered, only the left humerus shows evidence of
base tend to be sclerotic and inhibit pneumati- the disease. The normal axis of the bone has been
zation of the paranasal sinuses (Figure 499). deformed producing anterior bowing. The cortex
The skeletal distribution of the lesions, espe- of the diaphysis is enlarged with the focus being
cially in the limbs, is similar to that of Ollier's near midshaft. The longitudinal cut section re-
enchondromatosis; but, in the latter the distal veals extensive development of fine spongy bone
tubular bones of the extremities (metacarpals, in this region with cystic cavities between the
metatarsals, and phalanges) are most frequently spongy bone and the cortex.
and more severely involved. The presence of the A possible case of fibrous dysplasia in a young
cranial changes discussed above would also rule adult female skull from Egypt (NMNH 256360)
out enchondromatosis. was brought to my attention by Dr. Eugen Strou-
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
318
NUMBER 28 319
hal during his research on the Egyptian skeletal The gross morphology of the lesions is compat-
collection in the National Museum of Natural ible with a diagnosis of either Paget's disease or
History, USA. The skull is from the rock-tombs fibrous dysplasia. The young adult age estimate
at Lisht, a Twelfth Dynasty site near Matanieh would, however, make Paget's disease unlikely. A
in Upper Egypt. The skull is fragmentary but ground section through one of the circular nod-
includes much of the vault and face. The abnor- ules of bone reveals a mixture of well-organized
mality is limited to the frontal bone in the region lamellar bone and poorly organized woven bone.
of the frontal sinus. Indeed it was a postmortem There is no evidence of the characteristic mosaic
break in the skull in this region that revealed the pattern associated with Paget's disease. The com-
presence of dense round nodules of bone near the bination of fiber bone proliferation, the lack of
frontal sinus and coarse bony spicules covering mosaic pattern in the histology, and the young
the internal bony surface of the sinus cavity (Fig- age of the specimen support a diagnosis of fibrous
ure 504). dysplasia, although a very mild expression of this
^^^^^H^^H
H^-I
B /^
B^ll
st^ JBi\^^
piv ^^B
3l ^
^BiL **
1^
FIGURES 505, 506.Myositis ossificans progressiva: 505,
Thorax, lateral view, showing bony bridging along fascial
planes. 506, Pelvis and right thigh, anterior view, showing
extensive fascial ossification. (48-year-old female, IPAZ au-
topsy 2406 from 1968.)
322 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
disease. Greenfield (1975, fig. 3:106) has pub- alies. These are shortness, usually bilateral, of the
lished a documented case of fibrous dysplasia first metatarsal a n d / o r the first metacarpal. At
showing similar nodular proliferation of bone in times the second phalanx of the fifth finger is
the frontal sinus revealed by the roentgen films. missing. T h e disease usually begins to manifest
itself in the neck-shoulder area and progresses
distally. It begins as fibroblastic proliferation fol-
Myositis Ossificans Progressiva
lowed by metaplastic ossification of the fibrous
PATHOLOGY
tissue. The end result is formation of bony prongs
and spicules following the outline of muscles from
This is a rare hereditary and familial disease origin to insertion and immobilizing intervening
(Uehlinger, 1936). The name is really misleading joints. The ossification of spinal ligaments may
because it is not an inflammatory disease and it be followed by ankylosis of spinal and costover-
does not primarily affect the muscles but the tebral joints. T h e disease progresses into adult-
fascias, tendons, and ligaments. Although the hood, resulting in almost complete skeletal im-
disease may not manifest itself until a child is mobility (Figures 505, 506). T h e limitation of
several years of age, its congenital nature is at- respiratory motion and the bridging of the tem-
tested by frequent concomitant congenital anom- poromandibular joint may contribute to death.
Neuromechanical Deformities
323
324 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
tebral disc may be replaced by continuous bone and ligaments, accounts for the bone changes by
trabeculae and the lipping may be completely means of modified growth a n d modeling. Since,
smoothed down by modeling resorption. in the dry skeleton, the continuity ofthe vertebral
SECONDARY KYPHOSIS.This deformity is sec- column is not maintained, alterations of individ-
ondary to lowered mechanical resistance of the ual vertebrae are important for the recognition of
vertebrae. A variety of conditions, especially os- the deformity. T h e transverse processes of the
teoporosis (Figure 507, right), osteomalacia, hy- thoracic vertebrae are deflected backwards on the
perparathyroidism, and Paget's disease, may pre- convex and forwards on the concave side. The
sent this complication. In this condition wedge transverse processes of the lumbar spine are short
vertebrae, due to compression fractures, are com- and plump on the convex side and long, slender,
mon. T h e intrinsic changes of the underlying and pointed on the concave side. T h e spinous
bone disease would help in recognition of the processes usually are deflected towards the con-
deformity as secondary. This is especially true of cavity in the lumbar spine. The vertebral bodies
kyphosis due to a congenital anomaly ofthe spine, show lateral wedging at the apex of the curvature
such as dorsal hemivertebra. in addition to rotation and torsion. The latter is
reflected in a diagonal pattern of the vertebral
cortex, secondary to the altered course of the
Scoliosis
fibers of the anterior spinal ligament. The spon-
The vertical position of the spinal column in giosa architecture of the laterally wedged verte-
the human depends on a precarious balance of brae usually shows sclerotic reinforcement on the
neuromuscular control and fibrous supportive overburdened concave side and reduction in
structures. Scoliosis is the term used for lateral number and size of trabeculae on the unburdened
deviations of the spinal column from the midsa- convex side. T h e areas of the neural arch and of
gittal plane. The factors leading to this deformity the diarthrodial intervertebral joints show the
are various and usually not obvious. An exception least degree of deformation. In long-standing
to this is scoliosis due to congenital maldevelop- severe scoliosis, additional bone changes may oc-
ment of one or several spinal segments, especially cur secondary to degenerative processes in the
lateral hemivertebra or segmental disarrange- eccentrically stressed intervertebral discs. These
ment. However, the pathogenesis need not con- changes are most marked laterally on the concave
cern us here since the observable bone changes, side of the wedged vertebrae and follow the same
which develop secondary to the deformity, are all pattern as described in senile kyphosis. Bony fu-
essentially the same. Scoliosis, with or without a sion across the narrowed intervertebral space oc-
significant kyphotic component, often starts in curs in the apex of the curvature. The overexpan-
childhood and progresses throughout the growing sion of the disc on the convex side may lead to
age and early adult life. This factor is of impor- bony replacement of the disc itself Ossification
tance because the bone changes are, to a large of various spinal ligaments and, occasionally, an-
extent, the result of altered growth and modeling kylosis across the diarthrodial joints can occur,
under abnormally directed static and dynamic especially on the concave side of the apex of the
stresses (Putschar, 1937:649-675). curvature.
The deformity usually shows a double curva- T h e ribs, which are firmly attached to the spine
ture, which permits the position of the head close by two joints and to the sternum through the rib
to the midsagittal plane despite the lateral devia- cartilage, must adapt their shape and curvature
tion of the spinal column. These deviations are to the spinal deformity. Generally, they are
not purely lateral but include a considerable ele- spread on the convexity a n d pressed together on
ment of rotation toward the convexity (Figure the concavity of the spinal deformity. These
508). This, as well as abnormal pull of tendons changes include alterations of the size and loca-
NUMBER 28 325
Postparalytic Deformities
References to spinal deformities in the litera- Another problem is that kyphosis and scoliosis
ture on paleopathology are rare. This is due, in are most noticeable in an articulated spine and
part, to the fact that vertebrae are not as well thus would tend to be overlooked in archeological
preserved as many other parts of the skeleton. specimens unless the defect was noticed during
NUMBER 28 327
excavation. (For some examples of kyphosis in- and a Franciscan mission was established there in
duced by infectious destruction of vertebral bod- 1630 (Smith, Woodbury, and Woodbury, 1966:
ies, see pages 125, 145, 166). 1). The site, including the cemetery, was exca-
Brothwell (1961:327-328) reviewed five pub- vated between 1917 and 1923. Skeletal material
lished and unpublished cases of scoliosis in British from both the pre- and post-contact period was
skeletons. One of these is from the Beaker period recovered from the cemetery.
(ca. 2000 B.C.). Brothwell attributes the scoliosis The skeleton in question (NMNH 314297) is
in this specimen to congenital problems in which from that portion of the cemetery associated with
additional centers of ossification developed as the historic period. However, the skull is morpho-
semi vertebrae. The anterior view shown on logically different from the Indian Christian bur-
Brothwell's plate 8d clearly shows the lateral ials. J. Lawrence Angel (personal communica-
deviation that resulted from this abnormal devel- tion) suggests that the ethnic affinity of the skull
opment. is Spanish and that this skeleton may be the
An interesting case of scoliosis comes from the remains of one of the priests massacred during
archeological site of Hawikuh located near the the Pueblo Revolt of 1680.
modern village of Zuni in New Mexico, USA. The estimated age of the skeleton is between
The site includes pre-Columbian and historic 25 and 35 years. The sex is clearly male. There is
components. During the early historic period the no evidence of deformity on the skull although
site was used as a base of operations for the there is considerable antemortem tooth loss, in-
Spanish explorer Francisco Vasquez de Coronado cluding all incisors. The upper right canine was
lost shortly before death as evidenced by the the distal tibiae and fibulae. T h e combination of
reactive bone still in evidence in this part of the scoliosis and slight deformity ofthe limbs suggests
maxilla. Caries is well advanced in the upper left the possibility of rickets in early childhood as the
first molar although the corresponding molar on cause of scoliosis.
the right is worn but not decayed. Only the lower
right third molar is present in the mandible, with
Postparalytic Deformities
clear evidence that most of the molars were lost
antemortem. Wells (1964a:92) reports the presence of a left
The upper extremities have a slight lateral humerus and radius, which is shorter and lighter
deviation of the distal humeri and considerable than the right humerus and radius in a Neolithic
bowing of both radii and ulnae. The major ab- skeleton from Sussex, England. He notes a similar
normality is seen in the vertebrae, which exhibit deformity in a Bronze Age skeleton from Norfolk,
an S-shaped scoliosis (Figure 513). The ribs (Fig- England. Both of these cases are probable exam-
ure 514) and manubrium are also abnormal re- ples of postparalytic deformity.
flecting the conditions on the vertebrae. The cer- Mitchell (1900) has described a predynastic
vical vertebrae and first two thoracic vertebrae Egyptian skeleton in which the left femur is
are normal. The first lateral deviation to the right shorter than the right. He attributes this condi-
begins at T-3 and continues to T-8 where the tion to poliomyelitis. Elliot-Smith (1912) noted
lateral deviation begins to be oriented toward the the existence of a deformity of the left foot in the
left, continuing until L-2 when the lateral ori- Nineteenth Dynasty Egyptian m u m m y of Phar-
entation shifts back toward the right. The sacrum aoh Siptah. Initially he attributed the deformity
shows minimal evidence of abnormality and the to poliomyelitis but in a subsequent publication
pelvis appears normal. The major long bones of (Elliot-Smith and Dawson, 1924:100, 157) he re-
the lower limbs have a slight lateral bowing of fers to this specimen as an example of clubfoot.
Skeletal Dysplasias
The skeletal dysplasias can be grouped into shortened. Thus, the trunk, although shortened,
two categories: (1) those affecting the prolifera- is least affected because of the great number of
tion and biology of cartilage and (2) those affect- growth plates in the spine. The extremities are
ing the formation a n d / o r resorption of bone. much more severely shortened and, in the extrem-
As far as the group of cartilage dysplasias is ities, the fast growing long bones, which have
concerned, a great number of syndromes have only two growth plates, are most markedly af-
been described. Most of them are very rare and fected. The femur is more shortened than any
terminate fatally during infancy or early child- other bone, followed by the humerus, and the
hood. Others are survived but fail to show diag- bones of the lower legs and forearms. The fingers
nostic features in the macerated skeleton that and toes with their numerous growth plates are
would permit classification beyond the term "dys- less affected. The body disproportions in the
plasia." For these reasons only classical achondro- achondroplastic newborn are about the same as
plasia, with typical disproportional dwarfism and in the adult. The discrepancy between longitu-
some mucopolysaccharidoses will be discussed dinal growth, controlled by cartilage prolifera-
here in some detail. The dysplasias of bone for- tion, and circumferential growth, controlled by
mation and resorption, however, are better char- periosteal bone formation, results in changes in
acterized and, in most instances, due to the tissue the shape ofthe bones (Figure 516). The diameter
involved, exhibit identifiable skeletal changes. of the diaphyses and the cortical thickness are
For this reason, even rare entities have been close to normal. The epiphyses and metaphyses
included in this discussion. are usually disproportionately wide as compared
to the length of the bones (Figure 517). The
Achondroplasia degree of penetration varies from case to case and
milder forms are observed. For details the reader
PATHOLOGY
is referred to the monograph of M0rch (1941),
Achondroplasia is a familial or sporadic con- who studied more than 100 achondroplastic in-
genital disorder of cartilage growth. This condi- dividuals. The skull typically is brachycephalic
tion is the cause of the most common form of but large and bulbous. This is due to the discrep-
dwarfism. In many cases, affected persons can ancy of the short skull base, which depends on
reach adult age. The basic defect is a severe enchondral growth at the intersphenoidal and
inhibition of cartilage proliferation, thereby lim- spheno-occipital synchondroses, and the normal
iting the enchondral growth in all areas of the sized cranial vault, which is intramembranous in
body. The enchondral ossification of the limited its development. The more normally large cranial
amount of proliferated cartilage proceeds nor- vault over the short skull base exhibits an in-
mally and so does the intramembranous and creased curvature, which is responsible for the
periosteal bone formation. Adult achondroplastic bulging forehead. On the other hand, the short-
dwarfs usually reach a height of 130 centimeters ness of the skull base is responsible for the mark-
or less (M0rch, 1941:118). The dwarfism is dis- edly depressed bridge ofthe nose. M0rch (1941:
proportionate (Figure 515). This is due to the fact 118) found this typical skull deformity in 80
that the bones with the fastest growth and the percent of his cases. However, the characteristic
least number of growth plates are most severely shortness of all four limbs was present in all cases.
329
330 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
523
is less affected than the long bones. The bones of mound (Figure 522). The reported stature ofthe
all limbs are short but robust. male dwarf is about 150 centimeters, but this
The second skeleton is a male dwarf excavated estimate is probably too large. The skull (Figure
five years later but from the same area of the 523) is virtually complete and exhibits abnormal
334 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
features similar to the female dwarf The cranium but had lost many teeth to decay antemortem.
is large (Snow estimates cranial capacity to be T h e long bones are short but robust. T h e humeral
2011 cc), but the skull base is short, creating a and femoral heads are abnormally displaced dis-
midfacial depression. The individual was an adult tally. In the femora, the greater trochanter is at
the same level as the femoral head. T h e morpho-
logical features of both dwarf skeletons are com-
patible with a diagnosis of achondroplasia.
Hoffman (1976) provides a description of an
archeological achondroplastic skeleton from Sac-
ramento County, California, USA. T h e specimen
is dated between A.D. 1500 and 1800. The skeleton
is nearly complete and is currently part of the
Lowie Museum of Anthropology skeletal collec-
tion (University of California, Berkeley, Califor-
nia, USA). The cranium is large and bulbous.
The midfacial region is depressed and the cranial
base shortened. The vertebrae are small and
kyphotic at T i l and T12. Vertebral bodies of
T l O - L l have projecting osteophytes creating a
beak-like lateral appearance. T h e long bones are
very short but robust exhibiting an external mor-
phology common in achondroplasia. The ky-
phosis associated with the lower thoracic and
upper lumbar vertebrae is also suggestive of
Hunter's disease.
An isolated skull from ossuary IV at the Fer-
guson Farm, Accokeek, Maryland, USA, is prob-
ably another New World example of achondro-
plasia. T h e site is Late Woodland with no evi-
dence of European trade goods associated with
the ossuary. This suggests a pre-contact date. The
skull vault is of normal size. T h e face is fragmen-
tary, although there is little doubt that the region
of the nasal bones was depressed (Figure 524).
The base of the skull exhibits an abnormal fora-
men magnum and an abnormally short basi-
occipital (Figure 525).
Mucopolysaccharidoses
PATHOLOGY
saccharides are, in part, accumulated in these hand shows marked widening of the metaphyses
cells, interfering with their normal function. Since of metacarpals and phalanges adjacent to the
mucopolysaccharides form a large part of carti- growth plate, with tapered narrowing on the
lage matrix, cartilage proliferation and, therefore, other end. Thus, the enlarged metacarpals taper
skeletal growth and development are variously proximally, the phalanges distally. As usual, the
affected in these conditions. The base of these first metacarpal behaves like a phalanx. The
conditions is an inborn, genetically controlled, distal phalanges are hypoplastic. The changes are
biochemical abnormality, which often manifests less marked in the corresponding bones of the
itself in several members of one family. Presently, feet.
six different mucopolysaccharidoses have been Early in the disease, the long bones show peri-
recognized (McKusick, 1972:521-686), of which osteal bone deposition followed by increased en-
only three are sufficiently well characterized in dosteal cortical resorption, leading to widening of
their skeletal manifestations to warrant a brief the marrow space and cortical thinning (Caffey,
discussion here: Hurler's syndrome (gargoylism), 1951, 1952). The humeri often show varus de-
Hunter's syndrome, and Morquio-Brailsford's formities of the head. Other deformities are coxa
syndrome. valga with plump femoral necks, shallow aceta-
HURLER'S SYNDROME (mucopolysaccharidosis bula and genu valgum due to lateral tilting ofthe
type I).This syndrome is transmitted as an maldeveloped distal femoral epiphysis (Jaffe,
autosomal recessive trait affecting children of 1972:542-552).
either sex. The time and degree of its manifesta- The skull frequently shows premature closure
tions vary. Often it becomes apparent in infancy ofthe sagittal suture, giving a laterally narrowed,
or early childhood and few individuals live be- anteroposteriorly elongated, configuration. The
yond 10 years. Skeletal changes have even been skull base in the area ofthe sella is elongated; the
observed in the newborn (Caffey, 1951, 1952). mandibular condyles are flattened or even con-
The main substance accumulated in fibroblasts cave (Aegerter and Kirkpatrick, 1968:138-152).
and cartilage cells is chondroitin sulphate B. The The skull bones are thick and dense. The scapulae
abnormality involves many tissues and organs of are often broad and thick, as are the ribs, with
the body, but we are here only concerned with exception of their misshapen necks and their nar-
the bone changes. In typical cases the affected row osteocartilaginous junctions.
growth cartilages lead to markedly stunted HUNTER'S SYNDROME (mucopolysaccharidosis
growth or dwarfism. Also, the development of type II).In this syndrome, which was only re-
secondary ossification centers is delayed and mor- cently differentiated from Hurler's syndrome, the
phologically abnormal (Jaffe, 1972:545). Among skeletal changes are practically identical with
the many deviations from the normal size and those of Hurler's syndrome. The inheritance is
shape of bones observed, the changes ofthe spine sex-linked so that only males are affected. Sur-
and of the hands are the most typical. The spine vival into adult age occurs.
shows a characteristic ossification defect at the MORQUIO-BRAILSFORD SYNDROME (mucopoly-
dorsolumbar junction. This may affect the twelfth saccharidosis type IV).This syndrome is trans-
thoracic but usually involves the first and often, mitted as an autosomal recessive trait. Both sexes
to a lesser degree, the second lumbar vertebral are involved equally and there are usually mul-
body. The cartilage model of any involved ver- tiple siblings affected in one family. The syn-
tebra is ossified only in the posterior and inferior drome is not apparent at birth but begins to
portions, giving the impression of a beak-like manifest itself in early childhood. The progressive
inferior projection on the lateral view of the X- accumulation of a mucopolysaccharide, probably
ray or of the dry bone. This lack of anterior mostly keratan sulfate, leads to skeletal changes
ossification at the dorsolumbar junction leads to and growth disturbances. The outstanding bone
a sharply angulated kyphosis at this level. The change is the flattening of all vertebrae with
336 SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
widening of the transverse and anteroposterior may be significantly shortened and often show
diameter. There is anterior wedging, especially at flaring of the metaphyses with lipping at the
the dorsolumbar junction, leading to severe ky- junction with the epiphysis. Similar spike-like
phosis. Subsequent to this deformity, the ribs projections occur on tarsal bones (Jaffe, 1972:
show an altered configuration and the thorax is 220). Hip deformities are common, consisting of
enlarged in its anteroposterior diameter. The ster- large deep acetabula with irregular contour and
num is angulated at the junction of the manu- delayed ossification of the femoral head (Jaffe,
brium and corpus and protrudes forward. Growth 1972:219).
is generally stunted, resulting in dwarfed stature.
There is disproportionate shortening of the neck PALEOPATHOLOGY
and trunk due to general flattening of the verte-
bral bodies (platyspondylia). The skull is normal In the Maclvor collection stored in the British
and, therefore, relatively too large. The primary Museum (Natural History), there is a pair of
dentition is usually normal, but the permanent deformed humeri (BMNH AF.l 1.3/75). There
teeth are abnormal in shape and position (Ae- are no other bones associated with this specimen
gerter and Kirkpatrick, 1968:141). which is from early dynastic Egypt. Both humeri
Secondary ossification centers are delayed and are abnormally short (Figure 526). T h e diaphysis
show abnormal configuration. The long bones is normal in diameter with a well-developed del-
FIGURES 526, 527.Possible mucopolysaccharidoses in the isolated right and left humeri of an
early dynastic Egyptian specimen: 526, Anterior view, showing the shortened ,'ength and
abnormal development ofthe humeral heads. 527, Medial view, showing porosity and abnormal
development of humeral heads. ( B M N H AF. 11.3/75; scales in cm.)
NUMBER 28 337
toid tuberosity. This combination of features is fatal at birth or in early childhood. Already in
suggestive of achondroplasia. However, the hu- the uterus the fetus suffers numerous fractures,
meral heads exhibit severe malformation of the which show various stages of callus formation at
articular surface with pitting of the subchondral birth. The newborn reveals markedly shortened
plate particularly on the right (Figure 527). The extremities because of the accordion pleating of
left humerus is about 2 centimeters shorter than numerous transverse fractures of the long bones.
the right. Brothwell (1965a: 164) includes an il- The trunk is also shortened because of compres-
lustration of the right humerus in his discussion sion fractures of the vertebral bodies. Numerous
of congenital defects but does not attempt a transverse rib fractures exhibit multiple knobby
specific diagnosis. The general appearance of the swellings of fracture callus. The skull is soft and
humeri is undoubtedly indicative of a chondro- may show only very rudimentary ossification cen-
dysplasia, although the extreme abnormality of ters in the cranial vault. If the condition is sur-
the humeral heads is not typical of achondropla- vived for a longer time, multiple ossification cen-
sia. The external morphology of the humeral ters may form, giving rise to Wormian bones. The
heads suggests an almost complete failure in the bones show an extremely thin cortex and very
development of the epiphysis. This aspect is more sparse and thin cancellous trabeculae. Recogni-
compatible with conditions seen in the muco- tion of this type in skeletal remains would depend
polysaccharidoses. While the age cannot be de- on ideal conditions of preservation. However,
termined, the fusion of the distal humeral epiph- since the condition affects the entire skeleton, it
yses and apophyses indicate a minimum age of could be surmised even from single bones.
about 14 with a good probability of at least being OSTEOGENESIS IMPERFECTA TARDA.This con-
a young adult. The age of the individual makes dition is not manifest at birth but reveals itself
Hurler's syndrome a less likely possibility than during childhood and adolescence. The contin-
either Hunter's syndrome or Morquio-Brailsford's ued deficiency of bone formation results in fre-
syndrome. quent fractures, particularly of the long bones.
Although normal bone formation is inhibited,
trauma can overcome the osteoblastic inhibition
Osteogenesis Imperfecta and fractures heal. In some instances callus for-
mation can be so excessive that it may be mis-
PATHOLOGY
taken for an osteosarcoma. In these individuals,
Osteogenesis imperfecta is based on an inborn enchondral growth is normal, but periosteal bone
deficiency of the mesenchymal cells in the pro- formation is very limited. This results in bones of
duction of mature collagen fibrils. It is often a normal length but subnormal diameter of the
familial disorder but also occurs as a spontaneous shafts. The cortex is very thin and the cancellous
mutation. In severe manifestations of this disorder bone sparse. The inhibited osteoblastic activity is
the collagenous fibrous tissue throughout the also reflected in the delay of cortical remodeling.
body is poorly developed. However, since the This can be demonstrated microscopically in un-
organic bone matrix almost entirely consists of decalcified ground sections, revealing persistence
collagen, skeletal changes dominate the picture. of surface parallel lamellar bone and scarce os-
The disease expresses itself in two forms: osteo- teonization. Multiple fractures may lead to severe
genesis imperfecta fetalis (Vrolik type) and osteo- deformities, especially of the weight-bearing
genesis imperfecta tarda (Lobstein type). bones of the lower extremities and the pelvis.
OSTEOGENESIS IMPERFECTA FETALIS.In this However, some of the severe deformities are also
condition the disease fully manifests itself in in- due to bending by muscle pull and static forces,
trauterine life. Osteoblastic inhibition results in which the defective skeleton cannot resist (Figure
great reduction of enchondral and intramembra- 528). Any bone except the skull may be deformed.
neous bone formation. The condition is often The tendency to develop new fractures usually
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
338
^^^^^HP^^
^^HFr'
Tf 1
Si K^
^ "1
nft*'!'^|31
^ J
k )l V
Osteopetrosis is a congenital disorder of the a jumbled, solid mass of bone and calcified car-
skeleton characterized by severe inhibition of os- tilage, filling the bone marrow spaces and ulti-
teoclastic activity. The disease often is familial, mately causing fatal anemia. All remodeling has
occurring in several generations and in multiple to be initiated by osteoclastic resorption, but it is
siblings. There is no sex predilection. Parental generally inhibited in this disease. This condition
consanguinity is common. The disease occurs in first becomes noticeable on the metaphysial side
an infantile severe form leading to death in in- of the fast growing plates, such as the distal femur
fancy or early childhood, and a mild form, start- and proximal tibia; however, ultimately all bones
ing in later childhood or adolescence and com- show abnormal density. Since there is some fluc-
patible with adult survival. tuation in the degree of osteoclastic suppression,
INFANTILE OSTEOPETROSIS.This condition be- parallel banding of denser and more lucent areas
gins in fetal life. The basic defect is severe inhi- occur in the metaphyses. Corresponding to this
bition of osteoclastic activity without suppression are concentric layers of alternating degrees of
of osteoblastic activity. This leads to preservation density in ossification centers (Figures 533, 534).
of primary trabeculae of enchondral growth con- Ultimately, the whole medullary space is filled
taining cores of calcified cartilage. Continued with the abnormal bone containing calcified car-
deposition of bone on such trabeculae results in tilage (Figure 535). O n the long bones the physi-
NUMBER 28 341
Pyknodysostosis
PATHOLOGY
PATHOLOGY
PALEOPATHOLOGY
FIGURES 538, 539.Melorheostosis: 538, Left leg, lateral view, showing nodular and plaque-like
periosteal hyperostosis. 539, Distal left femur, longitudinally cut section, showing medullary
endosteal sclerosis and spotty epiphysial spongiosclerosis. (24-year-oId male, IPAZ M B 6672
from 1964.)
344 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
Diaphysial Sclerosis
(Camurati-Engelmann's Disease)
PATHOLOGY
PATHOLOGY
Osteopoikilosis PATHOLOGY
PATHOLOGY
This anomaly is similar to osteopoikilosis and
likewise is not visible by external inspection ofthe
This is a familial hereditary anomaly of the bones. The lesion consists of parallel, streak-like
skeleton, which may manifest itself in several condensations of cancellous bone, involving
siblings. It has been found in the newborn. Since epiphyses and metaphyses of long bones. The
the anomaly is not visible on external inspection skeletal distribution is similar to that in osteo-
and is asymptomatic, only a chance X-ray will poikilosis and mixtures of both anomalies have
reveal its presence. The anomaly consists of mul- been observed.
Skeletal Malformations
Malformations ofthe entire skeleton are mostly PALEOPATHOLOGY
related to incomplete twinning and usually are
C L E F T L I P AND C L E F T PALATE.These abnor-
not compatible with prolonged postfetal life (Fig-
malities are uncommon in archeological skele-
ure 542). T h e various forms of these malforma-
tons. However, this does not mean that cleft lip
tions will not be discussed here. Less serious mal-
and palate were rare in antiquity. Tretsven (1965:
formations ofthe skeleton are often due to failure
229) found the incidence of cleft abnormalities
of closure of fetal clefts or suppression of a portion
among living American Indians in Montana to
of the skeletogenic mesenchyme. Many of these
be higher than non-Indian people. H e further
are compatible with life and maturity. Of these
notes (p. 236) that many American Indian groups
the most frequent and characteristic will be dis-
have descriptive terms for cleft abnormalities in
cussed here in their regional occurrence.
their native language. Mortality of infants with
cleft lip a n d / o r palate would have been high in
Skull antiquity. T h e defect inhibits effective nursing
which would have contributed to early death.
PATHOLOGY
Also many infants with grossly observable de-
The most frequent fatal malformation of the formities would have been killed.
skull is anencephaly, a condition in which the Berndorfer (1962) has described a female skull
cranial vault never developed and the rudimen- about 25-30 years of age excavated in southern
tary brain is directly exposed. This condition is Hungary and dated to the fifteenth century A.D.
not infrequently combined with partial or com- T h e only abnormality of the skull is a poorly
plete failure of closure of the neural canal (cran- developed premaxilla and a small defect of the
iorachischisis). T h e skull base shows marked de- inferior aspect ofthe right pyriform aperture. The
formities of its constituent bones. T h e skull vault anterior alveolar region ofthe maxilla has a slight
is absent and the orbits may be rudimentary. indentation suggestive of a cleft lip. T h e incisors
A common malformation compatible with life are missing antemortem and the sockets for their
is the uni- or bilateral lack of fusion of the glob- roots are not present. Berndorfer rules out gingi-
ular and maxillary processes resulting in various val atrophy following antemortem loss of the
degrees of hare-lip and cleft palate. T h e defect is incisors, because the remaining teeth are normal.
located between the lateral incisor and the canine He does not consider cultural artificial extraction
tooth. of the teeth as a possible cause of the slight defect
Congenital herniations of meninges and brain in the alveolar bone. However, the abnormality
will present on the skull bones as round, midline of the pyriform aperture and subnormal devel-
defects above the bridge of the nose or in the opment of the premaxilla would support a diag-
occipital area (Figures 543, 544). nosis of slight cleft lip.
Premature synostoses of one or several cranial Brooks and Hohenthal (1963) report the pres-
sutures result in various characteristic skull de- ence of cleft abnormalities in three indigenous
formities distinctly different from cultural, artifi- skulls from two archeological cemeteries in Cali-
cial deformations (Figure 545). T h e increasing fornia, USA. Two of the skulls are from the
pressure of the growing brain leads to separation Newark site on the southeastern shore of San
of open sutures (Figure 546) and deep cerebral Francisco Bay. T h e skulls come from the Late
impressions on the inner table (Figure 547), Middle Horizon level dated by carbon-14 to 2340
346
FIGURE 542.Dicephalic infant with duplication of the
spine. (Newborn, F P A M 1576.)
flg^*^ - ^ ^ ^
K;,--/'V ^% * ^
. ^I^'HBP' ' .^^^I^B
V^^4^^^^^^^^>v,
kl^^^l
uous with the cleft of the left hard palate. The 243208). The archeological age is unknown. The
maxillary defect is continuous with the pyriform alveolar portion ofthe left maxilla may have been
aperture. affected as is suggested by the antemortem loss of
Three specimens from the National Museum the central and lateral incisors (Figures 555, 556).
of Natural History collections at the Smithsonian However the major defect is a large oval opening
Institution, Washington, D . C , USA, provide ad- in the palate. The vomer and conchae are missing
ditional evidence for the presence of cleft abnor- as well.
malities in New World indigenous populations. The above-published and original examples
The first of these two specimens is a complete serve to document the presence of the cleft lip
cranium of a young adult female about 18 to 20 and palate in both New and Old World indige-
years of age from southwestern Colorado, USA nous ancient populations. They also serve to il-
(NMNH 316482). The archeological age of the lustrate the point that other conditions such as
skull is unknown. T h e skull exhibits some occipi- trauma and infection need to be considered in
tal flattening, which is unrelated to the abnor- differential diagnosis.
mality of the maxilla. Both maxillary central CONGENITAL HERNIATION.Stewart (1975) has
incisors and the right lateral incisor are absent called attention to the misinterpretation of con-
antemortem. The sockets are absent and the al- genital herniations (dysraphism) ofthe skull. The
veolar bone is thin. Dental alveolei are present for defects in the bone produced by such herniations
the remaining teeth although the socket for the have been attributed to the practice of trephina-
upper right canine is poorly formed with the tion (Powell, 1965; Sublett and Wray, 1970).
anterior portion missing. There is a small cleft in Both examples, published by Stewart (1975), ex-
the central portion of the intermaxillary suture hibit herniation very close to bregma. They have
(Figure 551). The nasal bones are depressed about a sharply defined anterior border but a more
15 millimeters below nasion, as if the result of a gradual slope to the depression posteriorly.
healed blow in childhood. The palate is cleft Another example of this abnormality was
primarily to the right of the midline with slight brought to my attention by T. D. Stewart. The
abnormality to the left (Figure 552). Both the skull is from the skeletal collections of the Field
palatine process of the maxilla and the palatine Museum of Natural History (FM 40208) and is
bone are involved although the defect is less from a child 6 to 8 years of age from Ancon, Peru.
severe in the posterior portion of the palate. The The archeological age is thought to be between
mandible is normal. A.D. 1000 and 1200. The large abnormality is
The second specimen is from an 8- to 10-year- located on the frontal bone anterior to bregma
old child from the Nasca region in Peru (NMNH (Figures 557, 558). The defect extends completely
293252). The archeological age is not known. through both tables of the frontal bone. The
Only the anterior portion of the skull is present margin is most sharply defined on the posterior
including the frontal, sphenoid, zygomatic, nasal, edge with a gradual elongated depression extend-
palatine bones, and the maxilla. The cleft defect ing anteriorly about midway toward nasion. Lat-
is primarily on the left side (Figure 553, 554) and eral to the defect are two areas of porous reactive
involves the alveolar and palatine process of the bone. The defect itself is well circumscribed, ex-
maxilla, as well as the palatine bone and the hibiting smooth compact bone throughout.
internal bones ofthe nasal cavity. The cleft ofthe The nature of the soft tissue lesion, of course,
alveolus and palate are continuous with each is not known. Stewart (1975:437) notes that the
other and with the nasal cavity. There has been prognosis in a living patient depends on the type
a lateral deviation of the intermaxillary suture of herniated tissue and the amount of herniation.
toward the right side of the face. The prognosis for survival to adulthood would be
The final example of cleft palate is from an poor in a case where the herniation was as exten-
archeological site in Kentucky, USA (NMNH sive as evidenced by the size of the skull defect.
352 SMITHSONIAN C O N T R I B U T I O N S T O ANTHROPOLOGY
Thus, it appears that this abnormality may have (e.g., Davis, 1865; Eiseley and Asling, 1944; Hoh-
led to the premature death of the child. enthal and Brooks, 1960; Comas, 1965; Bennett,
BIPARIETAL PERFORATIONS.Broca (1875) has 1967; Stewart, 1972).
described another congenital defect of the skull Of the many examples of craniostenosis in the
vault in which there are unusually large perfora- collections of the National Museum of Natural
tions of the parietal bones often occurring as an History, Washington, D . C , USA, I have chosen
enlargement of the parietal foramina. An exam-
ple of this condition is seen in a skull from Cali- ^^I^R^^m^^H
fornia, USA (NMNH 276981). The skull is that ^ - *-^v' " ^ 5 ^ B
of an adult male with bilateral perforations ofthe
parietals exceeding one centimeter in diameter
(Figure 559). The perforations are located on the
^^H^
^
posterior portion of both parietals near the sag-
# "
ittal suture. 4^^H
PREMATURE FUSION OF SUTURES OF THE SKULL
(Craniostenosis).This abnormality can change
the normal shape of the skull. The changes in
shape will depend on which sutures are involved
and the age of onset of the fusion. For example,
fusion of the sagittal suture in early childhood
produces an elongated skull with a prominent
forehead. Fusion of the coronal suture in early
S3liilfc.-*' '^.i^^^MSi
childhood results in a shorter skull but prominent
development of the frontal region with a very :f^^'7ai.; ^
high forehead. Several reports on craniostenosis FIGURE 559.Biparietal perforations in an adult skull from
in archeological skeletons have been published an archeological site in California, USA. ( N M N H 276981.)
NUMBER 28 353
deviation of the skull suggestive of excessive the sagittal and lambdoid have begun to fuse.
growth on the right side ofthe skull vault. Except for 2 centimeters on either side of the
Premature fusion of the coronal suture is seen midline, the coronal suture is completely fused
in a female Eskimo skull from Wales, Alaska, ectocranially with obliteration of the sutural lines
USA (NMNH 333470). The skull is from an (Figures 562, 563). T h e sphenoparietal suture is
individual about 25 to 30 years of age at the time also fused and obliterated. In profile the skull
of death. Endocranially the coronal, sagittal, and vault exhibits a saddle-like depression just poste-
lambdoid sutures are fused. Ectocranially both rior to bregma. Otherwise, the shape of the skull
NUMBER 28 355
is normal indicating that the premature fusion of neural arches pointing laterally (complete spina
the coronal and sphenoparietal suture occurred bifida). Incomplete bony fusion of one or several
after significant growth ofthe brain and skull had spinous processes (spina bifida occulta) is com-
ceased. mon, especially in the sacral area (Figure 567).
Another example of craniostenosis in an adult Lateral or dorsal hemivertebrae occur, causing
skull illustrates the morphological features that abnormal curvature of the spine (congenital sco-
occur when premature fusion occurs early in liosis and kyphosis) (Figures 568, 569). Segmental
childhood or infancy. T h e skull is from Cinco disarrangement of vertebral ossification centers
Cerros, Peru, and is from an adult male (NMNH may result in fusion of vertebral segments, partic-
293841). The archeological age is not known with ularly in the cervical area (Klippel-Feil syn-
certainty but is thought to be pre-Columbian. drome). Symmetrical or asymmetrical sacraliza-
The skull is long and very narrow (markedly tion of the fifth lumbar vertebra is common.
dolichocephalic) with the elongation primarily in Lumbarization of the first sacral vertebra is more
the posterior portion of the skull (Figures 564- rare. The sacrum and coccyx may completely fail
566). The sagittal suture is completely fused both to develop, resulting in close approximation of
endo- and ectocranially. The coronal and lamb- the posterior iliac spines.
doid sutures are completely fused endocranially
and partially fused ectocranially.
HYDROCEPHALUS.Although this condition is
rarely a congenital abnormality, it does produce
malformation of the skull that could be observed
in archeological specimens; for this reason brief
mention of this condition is included below. Derry
(1913) provides a detailed report on an abnor-
mally large skull and postcranial bones from the
Roman period in Egypt. The bones are those of
a fully adult male. Derry reports that the cranial
capacity is at least 2900 cubic centimeters, which
exceeds the normal range of cranial capacity by
several hundred cubic centimeters. The lateral
drawing of the skull exhibits relatively normal
proportions for the face so that the skull abnor-
mality is limited to the brain case. The postcran-
ial bones exhibit abnormalities that Derry attri-
butes to partial paralysis of the left side. Grim
and Plathner (1952) describe a hydrocephalic
skull from central Europe dated to the Stone Age.
Armelagos (1969) reports the presence of a hydro-
cephalic skull of a child in Nubian skeletal ma-
terial dated between A.D. 350 and 550.
Spine
PATHOLOGY
Complete lack of closure of the neural canal FIGURE 567.Spina bifida of sacrum. (Young adult female,
shows the two halves of the spinous processes and FPAM 2381.)
356 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 568, 569.Supernumerary wedge vertebra between first and second lumbar with
secondary scoliosis and right sacralization of fifth lumbar vertebra: 568, Anterior view. 569,
Lateral view. (60-year-old male, F P A M autopsy 61729.)
vertebrae of this skeleton are fused. Fusion oc- pubis is absent and, although the pubic and
curred at the spines, diarthrodial joints, and the ischial rami are properly fused, there is a gap of
lateral portions of the vertebral bodies. The disc several centimeters between the two halves of the
space is preserved and the cause of the fusion is pelvis anteriorly (cleft pelvis) (Figure 573). Fail-
not apparent. ure of development of the massa lateralis of the
first sacral vertebra results in marked pelvic asym-
Ribs metry (Figure 574).
PATHOLOGY
Pelvis
PATHOLOGY
PALEOPATHOLOGY
sharply defined and the base of the lesion is The curvature of the anterior defect corresponds
porous but well remodeled. The posterior defect to the curvature of the anterior margin of the
is a narrow deep groove beginning with the pit acetabulum. There is little doubt that chronic
for the ligamentum teres and continuing poste- and abnormal abrasion of the femoral head dur-
riorly through the boundary of the joint surface. ing repeated episodes of partial, anterosuperior
subluxation produced this defect. The posterior
defect is due to abnormal pressure on the joint
surface by the ligamentum teres perhaps during
dislocation. Another possibility is that part of an
abnormally elongated ligamentum teres might
have lain across the joint surface when the head
was in the normal anatomical position. In view
ofthe lack of a secondary joint and any evidence
of fracture, congenital dislocation would appear
to be the most appropriate diagnosis.
An example of hip dislocation with secondary
joint formation is seen in an adult female from
the ancient Pueblo site of Kwasteyerkiva in New
Mexico, USA (NMNH 271828). The specimen
consists of the right innominate and femur, al-
though only the innominate was available for
study. The most noticeable feature is the presence
of a large secondary joint projecting well above
the acetabular rim (Figure 579). The articular
surface is rough with many pores penetrating the pression results in peromelia. At times, only the
surface. Considerable remodeling has taken place proximal portions of the limb are rudimentary,
in the acetabulum. The original surface is very while hands or feet are developed (phocomelia).
coarse and is almost completely covered over by As far as individual simple long bone defects are
a concave layer of bone, which may have been a concerned, the radius and the tibia (Figure 580)
temporary shallow joint before the femur slipped are more often missing than the ulna or the fibula.
again and stimulated the formation of the final Congenital bony ankylosis between the proximal
joint. T r a u m a cannot be ruled out, in part due to radius and ulna (Figure 581) and between the
postmortem damage. The acetabulum appears to distal tibia and fibula are typical anomalies, pre-
be abnormally shallow, which would support a venting, in the former, pronation of the forearm
diagnosis of congenital hip malformation leading but not affecting the function of the ankle sig-
to dislocation and secondary development of an- nificantly in the latter. There are many, fre-
other joint. quently hereditary and familial, syndromes con-
cerning the number, length, and position of digits
Extremities of fingers and toes (polydactyly, brachydactyly,
clinodactyly). T h e number may be more or less
PATHOLOGY
than normal (Figure 582). Single rays may be
Complete failure of development of one or fused through their entire length or only distally
several limb buds results in amelia; partial sup- (various forms of syndactyly). Clubfoot deformity
(pes equino-varus), often bilateral, can also occur
FIGURE 580.Congenital absence of left tibia with hyper- FIGURE 581.Proximal congenital radioulnar synostosis
trophic fibula and equinovarus deformity of foot. (18-year- (left) in pronation, radial head hypoplastic. (Adult W M S
old female, W M S 16.2 from 1892.) 8.1.)
NUMBER 28 363
FIGURES 585, 586.Synostosis of the proximal right radius and ulna: 585, Near-term fetus or
young infant from the late prehistoric J u h l e site at Nanjemoy, Maryland, U S A ( N M N H
384347). 586, Adolescent skeleton from the historic period, Mobridge site in South Dakota,
USA ( N M N H 382993).
date is Late Woodland and thus could be post- lights the problems in distinguishing between
Columbian. Even at the young age of this speci- congenital clubfoot and postparalytic deformities,
men, the radioulnar fusion is well established. such as those produced by poliomyelitis. Broth-
The second example of radioulnar synostosis is well (1967b:424) has reviewed one reported case
from an adolescent skeleton from the Mobridge of clubfoot in a Twelfth Dynasty Egyptian
site in South Dakota, USA (NMNH 382993). m u m m y and finds the evidence inadequate to
This site contained trade goods and is thought to support this diagnosis. Brothwell (1967b:425-
date around A.D. 1750. The right ulna and radius 428) describes a fragmentary Neolithic skeleton
are fused in a slightly pronated position (Figure from Gloustershire, England, with foot deformi-
586). The fusion has taken place in the radial ties attributable to clubfoot. Johnson and Kerley
tuberosity and the supinator fossa of the ulna. (1974) found evidence of clubfoot deformity in
The radial head is not involved. There is no four skeletons from the pre-European site at
evidence of trauma and the young age of the Mokapu in Hawaii, USA. They also note the
specimen, as well as the nature of the fusion, problem in distinguishing between congenital
make congenital radioulnar synostosis the appro- and postparalytic deformities. Johnson and Ker-
priate diagnosis. ley make the useful conceptual distinction be-
Deformities attributed to clubfoot have been tween malformation, which could be associated
described in the literature on paleopathology. with congenital abnormalities, and deformation,
Pales (1930:36-38) reviews some of the earlier which would be more likely in postparalytic
reports on this condition. His discussion high- changes.
Tumors
365
366 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
during the growth period, their frequency in an- growth plate (Figure 587). Its location is central
cient skeletons might be expected to be similar to in regard to the axis of the involved bone. It
modern skeletal samples. However, secondary tu- always spares the epiphysis. In the course of
mors of bone are associated with the older age longitudinal growth of the individual, it usually
categories and are thus less likely to be found in seems to move away, towards the diaphysis, by
archeological skeletons. Individuals who lived in interposition of newly grown bone between it and
antiquity usually died of other causes before sec- the growth plate. T h e most frequent locations are
ondary tumors could become a serious factor in proximal humerus, proximal and distal femur,
morbidity and mortality. proximal and distal tibia, and proximal fibula.
Another factor is the well known environmen- All other locations are unusual, especially in small
tal effect on the type and incidence of cancer. tubular and in flat bones. In Jaffe's (1958:63)
Carcinoma of the lung, for example, is associated material of 75 cases, the male-female sex ratio
with smoking and air pollution. Metastases to the was 2:1.
skeleton from this type of cancer may be minimal T h e enlargement of the cyst leads to smooth,
where such environmental problems did not exist. tapering resorption of the overlying cortex, due
It is important to emphasize, however, that ex- to increasing fluid pressure. Ultimately the cortex
posure to other conditions, such as smoke from a may be replaced with a newly formed shell of
wood fire, may be carcinogenic. Wells (1964b: cortical bone, which may show reinforcing ridges
1611) has noted the relatively high incidence of on the inner surface. Usually the actively enlarg-
nasopharyngeal tumors of bone in paleopathol- ing cyst shows osteoclastic resorption on the inside
ogical specimens. Today, this condition is rare in and osteoblastic bone deposition on the outside
the Western world but rather common in Africa. of the shell. Pathological fractures, crushing the
The condition is also rather common among the thin wall, are common and often heal readily.
Chinese. ANEURYSMAL BONE CYST.This is a much less
common lesion of older children and adolescents.
Primary Benign Tumors It is always eccentric in location as regards the
axis of the involved bone. It shows a distinct
bulge, consisting of a thin newly formed shell
PATHOLOGY
over the eroded cortex, which accounts for its
Cysts name (Figures 588, 589). T h e contralateral cortex
of the involved bone and the adjacent cancellous
A cyst, in the anatomical sense, is a lesion bone are usually spared. T h e lesion occurs with
characterized by a fluid-filled cavity surrounded equal frequency in long bones and in the spine.
by a distinct wall. Several types of lesions fulfilling In long bones, the location is usually the metaph-
these criteria occur in bone in different charac- ysis, seldom the diaphysis. The epiphysis is
teristic locations. spared. In the spine, vertebral bodies, transverse
UNICAMERAL BONE CYST.This tumor-like le- processes and neural arches may be involved. If
sion occurs about as frequently as giant cell tu- the lesion is large, pressure defects on adjacent
mor. It consists, in the fully developed state, of a vertebrae can occur. In 35 cases studied by Jaffe
round or oval fluid-filled single cavity of several (1958:56), the lesion was more common in fe-
centimeters in diameter that is lined by a thin males.
membrane of poorly vascularized osteogenic mes- T h e aneurysmal bone cyst is usually multi-
enchyme. The lesion occurs most often in young locular, but the different compartments are sep-
children or adolescents but may be carried into arated only by soft tissue septa, which are devoid
adult age. It is most common in long bones and of bone. T h e wall consists of highly vascular
starts in the metaphysis in close proximity to the connective tissue with numerous giant cells. The
NUMBER 28 367
derived from the growth plate, numerous smaller tendon insertions) in the affected area. Thus, the
chondromas are formed by faulty differentiation common exostoses around the knee area become
ofthe inner layer ofthe periosteum. In the process elongated polypoid structures with bulbous tips
of growth some of these assume an elongated, pointed away from the joint; upward on the
streak-like, radiolucent appearance. The presence femur and downward on the tibia. This is an
of large cartilage masses during the growing pe- effect of secondary remodeling. Fractures of slen-
riod results in alteration of the normal process der, elongated exostosis in this area are not un-
consisting of diminished growth, bowing deform- common. The flaring remodeling of the metaph-
ities due to uneven growth, and widening of the ysis is often inhibited on the side of the bone
metaphyses of involved bones due to delayed and bearing the osteochondroma. On the proximal
incomplete remodeling. humerus, osteochondromas tend to remain broad-
CARTILAGINOUS EXOSTOSIS (Osteochondro- based and rather bulky without pedunculation.
ma).Cartilaginous exostosis, appearing as a sol- Osteochondromas of the pelvis appear as cauli-
itary lesion, is one of the most common benign flower-like osteochondrous masses projecting out-
bone tumors. Its initiation is limited to the grow- ward or toward the pelvic canal (Figure 595).
ing period of the skeleton beginning most often In dry bone and on X-ray, the tumor shows
in childhood. There is no sex predilection. The easily recognized diagnostic characteristics. If
lesion may occur on any bone that develops by transsected, the continuity ofthe cancellous mar-
enchondral ossification, but the cranial base and row spaces of the lesion and of the involved bone
the facial bones are rarely involved. The tumor are readily apparent as is the reflection of the
most commonly occurs in proximity to the growth cortex onto the lesion. The inner structure consists
plate on the metaphysial surface of long bones. of more or less regular cancellous bony trabeculae
The distal metaphysis of the femur and the prox-
imal metaphysis of the tibia are the site of the
majority of the lesions. Other long bones of the
extremities, including small tubular bones of
hands and feet, ribs, pelvis, and scapula are less
commonly involved. The spine and sternum are
usually spared.
The lesion begins close to the growth cartilage
with a faulty differentiation of the inner layer of
the periosteum into cartilage. This cartilage un-
dergoes enchondral ossification from the under-
lying osteogenic mesenchyme, mimicking to a
great extent the enchondral growth of the growth
plate. Since, in the involved area, the periosteum
produces cartilage instead of bone, there is never
a cortex separating the medullary spaces of the
exostosis from those of the affected bone. Thus,
the exostosis enlarges continuously due to the
growth of the basal layer of the cartilage cap.
Usually the growth of the exostosis stops when
the nearby growth plate terminates its growth.
The lesion begins as a rounded outgrowth on
the periosteal surface. The final shape is greatly FIGURE 595.Osteochondroma of left ilium. (59-year-old
modified by mechanical stresses (muscle pull and female, IPAZ autopsy 1776 from 1962.)
372 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 596, 597.Multiple cartilaginous exostoses: 596, Right femur; notice lack of meta-
physial remodeling in area of exostoses. 597, Left tibia and fibula with multiple exostoses. (54-
year-old male, IPAZ S.1201 from 1965.)
NUMBER 28 373
mingled with areas of densely calcified cartilage sionally shows a lesion on the endocranial aspect.
or sclerotic bone. The number of lesions may vary from a few to
HEREDITARY MULTIPLE EXOSTOSES (Diaphysial several hundred in different cases.
Aclasia).This dominant hereditary condition, If numerous lesions are present in a metaphys-
which affects multiple bones of the skeleton, is ial area, remodeling of the metaphysis is lacking,
rare. It usually manifests itself in several siblings leaving a broad metaphysis without flare (Figure
and several generations of one family. There is a 596). Growth is retarded and, at times, irregular,
marked predominance in the male sex. Basically, leading to shortening and axial deviation of the
the individual lesion is identical with that of affected bone. If the distal ulnar metaphysis is
solitary cartilaginous exostosis. The predominant severely involved, the ulna is shortened and the
location is again the knee area, often involved radius, due to its intimate attachment to the ulna,
symmetrically (Figures 596, 597). In addition, the is abnormally curved, giving the appearance of a
proximal humeral metaphysis, the distal tibial Madelung's deformity of the forearm. In a mod-
metaphysis, and the small tubular bones of the erate number of cases in the older age group, a
hands are frequently involved. Other locations in chondrosarcoma develops from the residual car-
decreasing order of frequency are: proximal fib- tilage cap in one or several of the lesions (Figure
ula, iliac bone, metatarsals and toes, radius, ulna, 598).
ribs, and scapula. The spine is rarely affected; CHONDROBLASTOMA.This fairly rare benign
neither are the facial bones. The skull base occa- tumor is made up of primitive chondroblasts and
giant cells. It occurs mainly in adolescents and
young adults, with a marked preponderance of
males over females. The tumor occurs most com-
monly in the epiphyses of long bones (Figure
599). In fact, this is the only bone tumor that
bone the lesion would present as a streak-like or rated by a distinct, frequently scalloped, bony
multiloculated defect beneath the cortex, bor- shell from the medullary tissue. Only in a thin
dered by smooth surfaced sclerotic bone in the long bone, like the fibula, may the tumor ulti-
depth. These lesions may reach several centime- mately transect the entire diameter, but even
ters in length but usually not more than one then the contralateral cortex is usually less in-
centimeter in diameter. They may fill in sponta- volved. However, since large portions of cancel-
neously or remain stationary. In few instances lous bone and cortex are progressively destroyed,
they behave agressively and become truly neo- pathological, usually diagonal, fracture occurs
plastic (nonossifying fibroma). commonly, especially in weight-bearing bones.
In Caffey's (1955) series of 1000 healthy chil- The tumors may reach up to 10 centimeters in
dren examined radiologically, the most common length.
location of the defect was found on the distal CORTICAL DESMOID.A lesion, similar to fi-
femur and with equal frequency as a unilateral brous cortical defect, is occasionally seen on long
or bilateral symmetrical lesion. The solitary uni- and short tubular bones in which a similarly
lateral lesions were, in both sexes, twice as often scalloped cortical defect is filled with tough ma-
located in the right than in the left femur. Of 254 ture collagen. There is also a separating cortical
femoral defects, 224 were present on the medial shell at the deep margin of the lesion. The indi-
cortex of the metaphysis and only 30 on the viduals affected are often adult. On the dry bone,
lateral cortex. T h e anterior cortex was involved the defect would appear very similar to that of a
only once. Multiple defects within a single femur fibrous cortical defect.
were found only 19 times. No defects were dem-
onstrated in the first two years of life, but in the
Giant Cell Tumor
third, almost 8 percent of the children showed
defects. In the fourth year, the number of affected One ofthe most common primary bone tumors
children rose sharply to 15 percent, maintaining is the giant cell tumor (osteoclastoma), a border-
a frequency of 14 to 17 percent through the line-benign neoplasm made up of stromal cells
twelfth year. In the thirteenth year, the frequency and multinucleated giant cells similar to osteo-
of cortical defects dropped sharply to 10 percent clasts. The lesion most commonly occurs in ado-
and reached 8 percent in the fourteenth year. The lescents and young adults, mostly less than 40
defects in the distal femoral metaphysis were 25 years of age. The tumor is eccentric, epimetaphy-
times more frequently encountered than those in sial in location, and most often found in long
the proximal tibial metaphysis and 60 times more bones. The predilected areas are distal femur,
common than those in the proximal fibular me- proximal tibia, distal radius, and proximal hu-
taphysis. Cortical defects in the proximal femoral merus. All other locations are rare, but it can
metaphysis were rare. occur in vertebrae, pelvis, cranial vault, or small
NONOSSIFYING FIBROMA.As already indicated bones of the extremities.
(p. 374), this neoplastic lesion derives from a The most characteristic lesion, and the only
fibrous cortical defect that behaves aggressively one that could be identified with a reasonable
and continues to grow. The location is the same degree of certainty in dry bone, is the epime-
as that of the latter. T h e age of the individuals taphysial lesion of long bones. The tumor usually
affected is older (later childhood and adoles- completely destroys the preexisting spongiosa and
cence). The occurrence is much less common than the original cortex, allowing the formation of a
the fibrous cortical defect and is usually unifocal. thin, new, periosteal cortical shell in an expanded
The lesion always starts eccentrically in the me- position, which often has small rounded perfora-
taphysis of long bones and, even after penetration tions and reinforcing ridges on the inner surface
into the medullary portion of the bone, is sepa- (Figures 601, 602). This accounts for the radiolog-
376 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
ical "soap bubble" appearance of the cortical into the intact cortex on the diaphysial end ofthe
shell. The lesion often excavates the epiphysis and lesion is usually sharp and narrow. Pathological
closely approaches the articular surface, without fractures through advanced lesions, especially in
penetrating into the joint. The zone of transition weight-bearing bones, are not uncommon. The
normal consistency and appearance of the rest of
the bone and of other bones of the same skeleton
should permit differentiation from reactive giant
cell tumors (brown tumors) in severe hyperpara-
thyroidism.
Hemangioma
Meningioma
^ < "3
FIGURE 610.Button osteoma ofthe frontal bone in an adult
FIGURE 611.Large osteoma ofthe right parietal in an adult
female skull from Pachacamac, Peru. ( N M N H 267377.)
skull from a site near Lima, Peru. ( N M N H 242462.)
almost 4 millimeters above the plane of normal report of racial variation suggests a genetic com-
bone at the center ofthe lesion (Figure 611). ponent but environmental or cultural conditions
Another common type of tumor seen in arche- cannot be ruled out. Hrdlicka (1935:80) did find
ological specimens is the small bony growth, that the incidence increased with the age of the
which may partially to completely fill the external individual. Other scholars, including Adis-Castro
auditory meatus. Hrdlicka (1935) was unable to and Neumann (1948) and Gregg and McGrew
reach any firm conclusion regarding the cause of (1970), have described cases in archeological pop-
these ear exostoses. He did not feel that they were ulations. Stewart (1979b: 268) has called attention
the result of infectious or malignant diseases and to lytic lesions of the bony external auditory
suggested chemical or mechanical irritation as a canal, which he suggests may be the bony re-
possibility. Hrdlicka (1935:80) observed that sponse to a soft-tissue tumor (ear cholesteatoma).
males are far more subject to the disease. His The circumscribed enlargement of the canal does
FIGURE 612.Bony tumor o f t h e left external auditory mea- FIGURE 613.Large bony tumor ofthe left external auditory
tus of an adolescent skull from Chicama, Peru. ( N M N H meatus of an adult male from an archeological site in Illinois,
264344.) USA. ( N M N H 243180.)
380 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
not exceed the size of an acorn. The condition measures 25 by 33 millimeters and extends 18
appears to be fairly common among the Eskimos millimeters above the plane of the normal adja-
and Aleuts of Alaska, USA. cent surface. T h e surface ofthe tumor is irregular
There are numerous examples of ear exostoses and has a rounded, lumpy appearance. T h e joint
in the collections of the National Museum of surface of the acetabulum is normal; however,
Natural History, USA. Only two will be described
here. The first of these is an adolescent skull from
Chicama, Peru (NMNH 264344) illustrating
what appears to be the incipient stage of this
condition (Figure 612). All secondary teeth have
erupted. The basioccipital synchondrosis is not
fused indicating an age of around 18 years at the
time of death. Sex is thought to be female. Both
auditory canals exhibit narrowing; the right au-
ditory meatus has a slight, hypertrophic ridge
that may represent the early stage of tumor de-
velopment.
The second skull is from Illinois, USA (NMNH
243180). It is from a fully adult male. The man-
dible is missing and the maxilla has a slight
development of bony tumors in the buccal region
of both sides. Like the previous specimen the
auditory canals are abnormally narrow. In addi-
tion there are large bony tumors in both external
meatus with the most pronounced development
on the left side (Figure 613). Both tumors arise
from the posterior portion of the canal.
Beraud, Morel and Boyer (1961) describe an
osteoma of the ethmofrontal region in a skull
from France. The specimen is from the medieval
cemetery of St. Hermentaire and is dated to the
11th century A.D. The authors estimate the age at
death to be 22-25. The tumor encroaches on the
endocranium.
Chondroblastic Tumors
the tumor bone has extended the anterosuperior interesting burial from a cemetery on the island
margin of the acetabulum. The X-ray film of the of Gotland off the southeastern coast ofthe Swed-
tumor reveals that the medullary space of the ish mainland. T h e burial is dated to about A.D.
exostosis is continuous with the innominate. 1250 and includes the skeleton of a young female
HEREDITARY MULTIPLE EXOSTOSES (Diaphysial between 17 and 20 years of age and a near-term
Aclasia).Singer (1962) describes a case of dia- fetus. Both skeletons exhibit multiple exostoses.
physial aclasia in a young adult female skeleton T h e authors suggest that exostoses protruding
from a cave in South Africa. The archeological from the pelvis prevented the birth of the infant
age is reported to be post-European. There are and led to the death of both the mother and fetus.
multiple exostoses on all the major long bones. Another archeological example of multiple car-
Gladykowska-Rzeczycka and Urbanowicz (1970) tilaginous exostoses is located in the Winchester
report a case of this condition in a skeleton of an Saxon skeletal-pathology collections of the British
adolescent from a cemetery in Pruszcy Gdanski, Museum (Natural History) in London. This spec-
Poland. The site is dated to between the first imen (BMNH G932, CG69, T R X L 1085) in-
century B.C. and the fourth century A.D. There cludes most of the major postcranial bones. The
are multiple bony projections primarily of the age estimate based on femur length is around 4
metaphysial areas of the major long bones. Sj0v- years, sex is unknown. Prominent bony projec-
old, Swedborg, and Diener (1974) describe a most tions can be seen on the distal metaphyses of the
left humerus and of both femora (Figure 616).
The left scapula and both iliac bones are affected
as well. Other bones, including the ribs, vertebrae,
and tarsals, are normal. Since this tumor is usu-
ally benign, it is unlikely to have been the cause
of death.
A New World example of multiple cartilagi-
nous exostoses is seen in a right femur of an adult
from Chicama, Peru ( N M N H , uncataloged).
There are no other bones associated with the
specimen and the archeological age is unknown.
There is a large bony exostosis, which developed
between the greater trochanter and the superior
surface ofthe femoral neck. T h e remaining lesions
are in the distal metaphysial region (Figure 617)
and consist of multiple bony projections.
Meningioma
^^^^^^^^^^^^^^
>i^B
.-'.. - *
Snil
t a ML
1
^
^
*
'/ t . - i .1 /C
FIGURES 618, 619.Multiple lytic lesions ofthe skull possibly due to meningioma. Specimen an
adult male from an archeological site on St. Lawrence Island, Alaska, USA: 618, Posterolateral
view, showing large lesion on the left parietal. 619, Detailed view of large, parietal lesion; note
the partial bony fill-in o f t h e exposed diploe in the larger lesion. ( N M N H 280091.)
from San Nicolas Island off the coast of southern ably the same Peruvian skull described later by
California. The lesion is similar to the Peruvian Abbot and Courville (1939)). The coalescing os-
specimen. Meningiomas are known to produce teophytes extend outward from the skull about
lytic lesions in early stages of the tumor develop- 4.5 centimeters. The tables ofthe skull have been
ment (Schinz, Baensch, Friedl, and Uehlinger, destroyed beneath the tumor. MacCurdy attri-
1951-1952:1628), but blastic lesions are common butes this tumor to osteosarcoma, but a menin-
(Gushing, 1922:150). gioma would seem to be more likely.
Rogers (1949) briefly describes two skulls from An Eskimo skull from St. Lawrence Island,
Egypt having lesions, which he attributes to me- Alaska, USA (NMNH 280091) exhibits lesions
ningiomas. The first of these is from the First that can be attributed to meningioma ofthe lytic
Dynasty and shows a hyperostotic lesion of the type. The archeological provenience is obscure.
right parietal involving both the inner and outer The skull is male and fully adult, probably in the
table. The second specimen is from the Twentieth 45 to 65 year age range. The mandible is missing
Dynasty and exhibits a large honeycomb lesion as are all the postcranial bones. On the external
with a focus in the right parietal but involving table of the vault, there is a diffuse porosity,
the left parietal and the frontal bone. The lesion which is also seen to a more limited degree on the
is large including most of the right parietal. It is nasal bones and maxilla. There has been some
not clear whether the inner table was involved. postmortem erosion that obscures the surface tex-
The first of these two cases differs from the two ture somewhat, but the remaining surface has a
cases of Abbot and Courville (1939) in involving pumice-like quality. On the posterior portion of
both tables of the skull. the left parietal the most dramatic feature is a
MacCurdy (1923:264, pi. 39) describes an adult large lytic lesion, which is confluent with a
male skull from Paucarcancha, Peru, with a large smaller lytic lesion encroaching on the right pa-
tumor of the left parietal and frontal bones (prob- rietal (Figures 618, 619). The larger of the two
384 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
lytic lesions has a maximal diameter of 4 centi- in frequency by the proximal tibial metaphysis
meters and a slightly scalloped but well-circum- and proximal humeral metaphysis. T h e epiphyses
scribed appearance, with the inner table some- are practically never the primary site and often
what more affected than the outer. The smaller remain uninvolved, being protected by the open
lytic lesion is similar in appearance but less well growth plate. T h e tumor predilects the long bones
circumscribed, suggesting lytic activity at the ofthe extremities, rarely involving the cancellous
time of death. Other smaller lesions occur pri- bones, the small tubular bones of the extremities,
marily on the left side of the skull with only one or the skull. Of the skull bones, the mandible is
moderately large lesion, which measures 1.5 cen- most often involved. Osteosarcomas arising past
timeters in diameter in the right temporal bone, middle age may develop in abnormal bone, par-
and which also involves the sphenoid. The skull ticularly in Paget's disease of bone.
is somewhat thicker than normal, measuring 13 Osteosarcoma arises within the bone at or near
millimeters near the edge ofthe major lytic focus. the metaphysial side of the growth plate. The
There are several conditions that could give tumor destroys varying amounts of the normal
rise to the pattern seen in the skull. Eosinophilic bone and extends through the cortex into the
granuloma produces lesions similar to that seen surrounding soft tissue. T h e appearance of the
in this skull. Metastatic carcinoma and angiosar- tumor, especially in dry bone, depends on the
coma are also possibilities. amount of mineralized bone formation. This
ranges from almost purely lytic forms (Figure
620) to those with massive production of sclerotic
Primary Malignant Bone Tumors tumor bone (Figures 621, 622). T h e bone pro-
duced by the tumor is woven bone, occurring in
PATHOLOGY
sheets and masses without architectural arrange-
Primary malignant bone tumors are compara- ment of trabeculae. T h e extracortical portion of
tively rare lesions that, in contrast to other malig- the tumor may exhibit a radiant alignment of
nant lesions, most frequently occur during the tumor bone, so-called sunburst (Figure 623). The
growing period. These sarcomas arise from osteo- elevation of the periosteum at the margin of the
genic mesenchyme and are classified according to cortical breakthrough leads to some reactive, non-
their matrix production as osteosarcomas, chon- neoplastic bone formation decreasing in thickness
drosarcomas, fibrosarcomas, reticulum cell sar- away from the tumor. In profile, this area appears
comas, and angiosarcomas. The most common triangular on X-ray (Codman's triangle) (Figures
primary malignant bone tumor is the osteosar- 624, 625). T h e epiphysis adjacent to the tumor
coma followed by chondrosarcoma and Ewing's may ultimately become involved, but the joint
sarcoma in decreasing frequency. All other types surface usually remains intact. The tumor extends
are rare. through the medullary cavity but practically
never involves the epiphysis on the end remote
from the tumor. Occasionally osteosarcoma me-
Osteosarcoma
tastasizes to other bones (Figures 626, 627).
This tumor occurs most often in adolescents Parosteal osteosarcoma arises on the outside of
and young adults. Males are about twice as often the bone in or near the periosteum. This tumor is
affected as females. The appearance of this tumor less frequent than endosteal osteosarcoma and
is closely related to the areas and periods of shows no particular sex predilection. Its occur-
greatest enchondral growth. The most active rence is more evenly spread throughout adult age.
growth plates in the skeleton are those of the It, too, occurs most commonly on the distal me-
distal femur, the proximal tibia, and the proximal taphysis of the femur (Figure 628). This tumor is
humerus. The most common location of this tu- slow growing and may produce large extraosseous
mor is in the distal femoral metaphysis, followed masses of dense bone (Figure 629). Penetration
NUMBER 28 385
Chondrosarcoma
FIGURES 624, 625.Sclerosing osteosarcoma of distal left femur: 624, Surface. 625, Cut surface.
Notice extensions of tumor bone through the cortex into soft tissue and shelf of reactive bone
at proximal tumor margin (Codman's triangle). (12-year-old male, M G H surgical specimen
11078 from 1972.)
NUMBER 28 387
Ewing's Sarcoma
FIGURES 629, 630.Parosteal osteosarcoma of proximal right tibial metaphysis: 629, External
view, showing layer of reactive bone at junction of cortex and tumor. 630, Cut surface, showing
dense radiating tumor bone. Notice slight involvement of underlying cortex. (Young adult,
FPAM 3639 from 1878; scales in cm.)
is a long bone of an extremity or a pelvic bone. differentiation between Ewing's and osteosar-
T h e structure of the tumor, consisting of loose coma impossible on dry bone. T h e absence of
round cells not held together by matrix, is respon- massive destruction and the long axial involve-
sible for the permeative pattern of this lesion. The ment, together with permeative intracortical re-
tumor cells can easily push through intertra- sorption, would arouse suspicion that the lesion
becular marrow spaces and invade Haversian may have been a Ewing's sarcoma or a reticulum
canals of the cortex. The result of this is that a cell sarcoma, which usually affects adults, espe-
large segment of the bone, including the dia- cially past 50 years of age.
physis, is involved. T h e destruction of trabecular
bone may be less marked, but resorption along Chordoma
Haversian canals leads to lamination of the cor-
tex. T h e tumor spreads into and through the Chordoma is a rare tumor arising from noto-
periosteum, eliciting some reactive bone forma- chordal rests. T h e tumor mostly affects individ-
tion of surface parallel ("onion skin") or radiant uals above 40 years of age and somewhat predi-
("sunburst") type. Of all the bone tumors, this is lects males. During embryonic development the
the one most often metastasizing to other bones. notochord extends from the skull base to the tip
T h e presence of reactive bone may make the of the coccyx, through the entire spine. In the
NUMBER 28 389
FIGURES 631, 632.Parosteal chondrosarcoma of distal right femur: 631, Outside view; notice
the nodular character of the mineralized portion of the tumor. 632, Cut surface; notice the
mature trabecular pattern of the bone replacing the core of the tumor. (31-year-old male, 10
years duration, W M S.72a.2 from 1894.)
process of vertebral development the notochordal or the sacrococcygeal area centered on the mid-
tissue is extruded into the nucleus pulposus of the line. Since no mineralized matrix is formed, noth-
intervertebral disc. In the movable part of the ing ofthe tumor itself could remain in dry bone.
spine, it is mostly destroyed by mechanical attri-
tion. Only in mechanically sheltered areas of the PALEOPATHOLOGY
axis do notochordal remnants survive into later
life. These areas are the skull base, the sacrum, Primary malignant tumors of bone are rare in
and the second cervical vertebra, where the odon- modern medical practice and are equally rare in
toid process is united with the body of C2 by archeological specimens. Ruffer and Willmore
fusion of an intervening disc. These facts explain (1914) report a tumor of the pelvis from Egypt
the localizations of chordomas: 55 percent sacral, dated about A.D. 250. The tumor affects the right
35 percent skull base, and only 10 percent verte- innominate, particularly the ischium and inferior
bral, especially cervical. ilium. It appears to have started in the cancellous
Small notochordal rests are common in the tissue of the pelvis and is slightly expansive in
clivus of the skull base and may show a small, nature, producing a deformation ofthe obdurator
pitted defect in dry bone in this area. The tumor foramen and encroaching on the acetabulum.
is purely destructive producing large, lytic defects The authors rule out carcinoma and infection
in the spheno-occipital portion of the skull base and suggest osteosarcoma adding that they can-
M Iff: 1m
J
not determine if the tumor was primary or sec- An unambiguous example of a primary malig-
ondary. The illustration of the lesion is of little nant tumor of bone is found in the skeletal col-
value but does not show the active irregular lections of the Natural History Museum in Bern,
growth of bone usually seen in osteoblastic osteo- Switzerland. This specimen (NHMB A95) is the
sarcoma. The lesion appears to be chronic rather left humerus from a Celtic warrior tomb dated to
than acute, which would tend to rule out osteo- approximately 800-600 B.C. and found near the
sarcoma. However, a tumor of some type is pos- town of Muensingen in Canton Bern. Brothwell
sible as is infection. (1967a:331) provides a brief description of the
Dastugue (1965) describes a tumor ofthe right specimen. Although damaged by postmortem
maxilla and zygomatic bone on a skull from a erosion, the humerus is complete except for the
Middle Age site associated with the town of Caen distal epiphysis, which was lost postmortem. The
in France. The tumor measures 60 millimeters lesion extends completely around the proximal
wide by 40 millimeters high and encroaches both humerus but is least developed on the medial
on the nasal passage and the right orbit. The aspect. The bone associated with the lesion is
surface of the tumor is very irregular with rela- approximately 7 centimeters in maximum diam-
tively large coalescing spicules. There are three eter and abnormal tissue extends slightly more
inferior projections. Curiously, there is antemor- than one-third the length ofthe humerus (Figures
tem damage to the right zygomatic bone adjacent 633, 634). Tumor bone overlies the insertion of
to the tumor and Dastugue suggests the possibil- the joint capsule but does not involve the joint
ity of surgical intervention to explain this defect. surface itself. The gross morphology of the tumor
The tumor appeared malignant to Dastugue and consists of large coalescing bony projections,
he expresses the opinion that it caused the death which have a coarse coral-like appearance. While
of the individual. The morphology of the lesion the age at death of the individual cannot be
is compatible with a primary malignant tumor of determined, the humeral head appears to be fused
bone. However, other possibilities, such as callus indicating an age in excess of 15 years.
following trauma to the face, seem more proba- X-ray films of this specimen were provided
ble. In my opinion, particularly in view of the through the courtesy of Dr. Walter Huber, the
injury to the zygomatic bone, trauma rather than Director ofthe Natural History Museum in Bern.
surgical intervention is more probable. The films reveal a lytic process extending 2 to 3
A tumor of the mandible was found in an centimeters into the externally normal cortex dis-
American Indian skeleton excavated in the state tal to the lesion (Figure 635). The location ofthe
of West Virginia (Kelln, McMichael, and Zim- tumor, as well as its gross and X-ray film appear-
mermann, 1967). The authors date the specimen ance, is compatible with the diagnosis of primary
to the mid-seventeenth century. The lesion is osteosarcoma or chondrosarcoma.
rather large, measuring about 24 millimeters in
diameter and 19 millimeters in depth. The man-
Metastatic Tumors
dible is probably from a female of about 20 years
of age. The authors suggest several possible neo- PATHOLOGY
plastic conditions including osteoma and osteo-
sarcoma as the cause of the lesion. T h e position Tumors metastatic to the skeleton are a com-
of the tumor near the symphysis and the young mon occurrence in carcinoma but rare in sar-
age of the individual are compatible with a di- coma. The tumor cells reach the skeleton, usually
agnosis of primary malignant tumor. However, the bone marrow, by the blood stream. The fre-
the chin is prone to trauma and infection and quency of skeletal metastases of different tumors
bony reaction to these morbid conditions is more depends, to a considerable extent, on the location
likely. of the primary tumor. Larger tumor particles
392 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
^^^^^^^^^^^^^^^^
^HB(^^^^Bi^^^^^S^w3w^^^^^^^^
^ M pi . '
'^^k
/^ ^'^ i
^
y " amk
^^^1
The tumor cells reaching the bone marrow mainly osteolytic, while slow growing ones elicit
grow and first replace the marrow without change an osteoblastic response.
of the bone architecture. The majority of meta- Carcinoma of the breast mostly shows osteoly-
static deposits discovered at autopsy are not dem- tic metastases, while carcinoma of the prostate
onstrated by external inspection or radiography. usually shows osteoblastic deposits. The great
In the Zurich series, only 36 percent ofthe skeletal majority of metastatic bone tumors are multiple
metastases were discovered during life (Walther, and involve more than one bone. Solitary and
1948:189). Continued growth o f t h e tumor cells relatively slow growing metastases are most often
usually leads to destruction and osteoclastic re- caused by renal cortical or thyroid carcinomas.
sorption of cancellous bone and internal scallop- These solitary lesions occur with predilection in
ing or complete destruction of cortical bone (os- the shaft of femur or humerus, less commonly in
teolytic metastases). At least microscopically, the cranial vault. They may appear on X-ray as
however, some reactive bone formation is often a cystic lesion, with an expanded shell of new
seen in some ofthe lesions a n d / o r in their vicinity. cortex showing soap bubble appearance. They
In other cases, a strong osteoblastic response to may mimic benign lesions, except for the fact that
the presence of the tumor cells is observed, con- diaphysial benign lesions are very uncommon.
sisting of new bone deposits replacing old trabec- Lytic metastases progressively destroy cancel-
ulae or coating remaining old trabeculae. This lous bone and erode the cortex of long bones from
results in blotchy or diffuse densities on X-ray. It within. Disseminated lytic metastases may be
IS not entirely clear what causes this difference. indistinguishable from multiple myeloma in dry
In general, however, fast growing tumors are bone. In the spine, the most frequently involved
394 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
vertebrae are the lower thoracic, followed in de- cinoma o f t h e stomach 14 percent, carcinoma of
creasing frequency by the lumbar, sacral, and the prostate 0.2 percent and no pathological frac-
cervical vertebrae. The metastases are prevail- tures in cancers of other primary sites.
ingly located in the vertebral bodies, but neural Subperiosteal metastases are uncommon. If
arches and spinous processes may also be affected present they are usually lytic, causing deep scal-
(Figure 636). Compression fractures are common, loping of the underlying cortex. This is seen most
secondary to lytic metastases. In the cranial vault, commonly in renal cortical carcinoma (Schinz,
the most marked destruction is in the diploe, Baensch, Friedl, and Uehlinger, 1951-1952(2):
while the outer and inner tables are long spared. 1008). Osteoblastic metastases are most com-
Metastases in the long bones predilect the inter- monly observed in carcinoma ofthe prostate. The
trochanteric area of the femur or proximal por- distinct lesions may become confluent and ex-
tion of the humerus. Pathological fractures sec- tremely sclerotic. There is usually little if any
ondary to lytic deposits in long bones are com- bone destruction, and the outer contours of the
mon. The frequency in Copeland's (1931) radio- involved bones are not significantly altered except
logical series is as follows: renal cortical carci- for those advanced cases where massive subper-
noma 45 percent, thyroid carcinoma 33 percent, iosteal bone is deposited in the form of mossy
malignant melanoma 33 percent, carcinoma of osteophytes (Figure 637). T h e distribution of met-
the colon 33 percent, carcinoma of the lung 25 astatic prostate carcinoma is different from that
percent, carcinoma of the breast 15 percent, car- of the usual hematogenous metastases. T h e ear-
NUMBER 28 395
liest and most massive involvement is in the much more common then primary malignant
pelvis, sacrum, and lumbar vertebrae. This is tumors of bone. Thus, even though they are
probably due to the fact that the pelvis and associated with the older age categories, they
vertebral venous plexuses freely communicate might be more common in archeological skele-
and thus permit direct colonization of the adja- tons. However, like primary malignant tumors,
cent bones without passage through the pulmo- they pose problems in differential diagnosis in
nary filter (Batson, 1940). In most instances blas- dry bone specimens, particularly from infectious
tic or lytic pelvic metastases begin in the floor of diseases.
the acetabulum, spread into the pubic rami, and A skeletal specimen from a cemetery near Du-
lastly involve the iliac wings (Schinz, Baensch, bendorf. Canton Zurich, Switzerland, dated be-
Friedl, and Uehlinger, 1951-1952(2): 1007). The tween the eleventh and fifteenth centuries ex-
differentiation from Paget's disease can be diffi- hibits a diffuse osteoblastic reaction. The speci-
cult on gross inspection or X-ray. However, mi- men is an adult male probably in excess of 50
croscopic sections should reveal the typical mosaic years of age at death and is currently stored in
structure if the lesion is Paget's. the Anthropological Institute ofthe University of
Special mention should be made of the ap- Zurich, Switzerland (AIUZ 7757). The right in-
pearance of skeletal metastasis in neuroblastoma, nominate contains a lesion largely limited to the
a malignant tumor of the adrenal or of the sym- periosteal surfaces ofthe ilium (Figure 643). The
pathetic chain in infants and children, usually lesion consists of extensive fine porous bony
under 3 years of age. This tumor, a round cell buildup. There is no obvious destruction of un-
lesion, freely seeds to the bone marrow in wide derlying bone nor evidence of abscess or cloacas.
distribution, including trunk, skull, and extremi- There is a similar bony reaction on the right
ties. The lesions often elicit osteoblastic reaction anterior proximal femur. Two of the ribs in this
leading to "hair-on-end" appearance in areas of specimen also show periosteal lesions (Figure
the cranial vault and periosteal layered-bone for- 644). The disseminated nature ofthe disease and
mation of varying thickness on the long bone the morphology ofthe lesions are compatible with
shafts of the actively growing childhood skeleton metastatic tumor. The extensive involvement of
(Figures 638-640). The periosteal deposis differ- the innominate and the sex of the case suggest
entiate it from similar skull lesions in severe ane- prostate cancer.
mias. Osteolytic metastatic cancer of the skeleton is
Craniofacial involvement may occur by direct probably the most common type of malignant
extension of paranasal carcinomas. Craniophar- lesion seen in archeological specimens. The major
yngeal carcinoma may erode the cranial base problem in diagnosis is to distinguish between
from without. Carcinoma of the ethmoid may metastatic carcinoma and multiple myeloma. In
destroy the adjacent frontal bone and the orbital the skeleton these two types of cancer reflect a
wall (Figure 641). Carcinoma ofthe nasal cavity morphological gradient making differential di-
may destroy part of the maxilla and of the hard agnosis impossible in many cases. A presentation
palate (Figure 642). In these cases the absence of of three problem cases is provided in the discus-
reactive bone and the strictly localized area of sion on reticuloendothelial and hemopoietic dis-
destruction usually permits, in dry bone, differ- orders (pp. 267-269).
entiation from lesions of tertiary syphilis, leprosy, Bony responses to neoplasms may produce
and lupus vulgaris. mixed blastic and lytic lesions. An archeological
example of this condition is seen in a skeleton
from Kachemak Bay, Alaska, USA (FM SEL30
PALEOPATHOLOGY
A M U 3 Burial 11). The skeleton was excavated in
Secondary tumors of bone are by definition 1974 and dated circa A.D. 350 by carbon-14 anal-
malignant. These types of tumors are presently ysis. The skeleton was shown to me through the
396 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
courtesy of John Lobdell, currently with the De- coarse fiber bone in the more central portions of
partment of Anthropology at the University of the lesion. T h e central osteoblastic activity pro-
Alaska, Anchorage, Alaska, USA. The specimen duces bone that rises above the plane of the
consists of the skull and the incomplete portions normal bone. The lesions in this skull are similar
ofthe postcranial skeleton. The sex is female and to lesions occurring in the skull of a modern case
the pitting on the posterior portion of the pubic of metastasis from lung carcinoma. T h e latter
symphysis suggests multiple pregnancies. Skeletal case is from the Institute of Pathological Anatomy
age is in the 50-year-plus range. at the University of Zurich, Switzerland (IPAZ
The disease process is multifocal with lesions autopsy 1850/67). In the skull lesions there is a
on the skull, ribs, vertebrae, left humerus, both lytic front adjacent to normal bone with fiber
innominates, the right femur and both tibiae. bone formation in the more central portion ofthe
The skull lesions are circular and fairly large lesion (Figure 648).
(Figures 645-647), the smallest is about 25 milli- T h e postcranial lesions in the Alaskan speci-
meters in diameter and the largest about 45 men appear to be more variable morphologically
millimeters in diameter. One lesion is on the than those of the skull, although the picture is
frontal, two are entirely on the left parietal, and complicated by considerable postmortem break-
a third is partially on the left parietal but crosses age. T h e cervical vertebrae are missing postmor-
the sagittal suture into the right parietal. T h e tem. T h e upper thoracic vertebrae are somewhat
lesions show an active lytic front at the boundary osteoporotic but are normal, except for slight
with normal bone. The lytic process results in the degenerative-arthritic changes. However, TIO
bone having the appearance of a fine sponge. and T12 both have lytic lesions of the lamina.
There is no osteoblastic circumscription of the Similar destructive lesions occur on the laminae
lytic process. The residual porous, spongy bone of the first two lumbar vertebrae. T h e vertebral
provides the scaffolding for the formation of bodies of L l , L2, L3, and L5 show evidence of
NUMBER 28 397
FIGURES 645-648.Mixed blastic and lytic lesions ofthe skull: 645, Left lateral view of a skull
showing two large porous lesions on the parietal bone. Specimen from an archeological site
dated about A.D 350 located near Kachemak Bay, Alaska, USA. 646, Detailed view of parietal
lesion adjacent to the sagittal suture. 647, Frontal view, showing lesion of right portion of
frontal bone. (FM SEL 30 A M U 3 Burial 11.) 648, Metastatic skull lesions from lung carcinoma
in a modern case. (IPAZ autopsy 1850/67.)
398 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
erosion and disk herniation (Figure 649). The first lytic and blastic processes (Figure 650). The prox-
through the third vertebral bodies are wedged imal ends of both tibiae have large, purely lytic
due to partial collapse. The wedging defect ofthe defects in the metaphysial cortex (Figure 651).
vertebrae is well consolidated, suggesting a long- Both lesions are oblong, the left measuring about
standing condition that does not appear to be 40 by 20 millimeters on the X-ray film. Postmor-
related to the active lytic process in the vertebrae. tem damage has destroyed part of the lesion on
The few rib fragments show active lytic involve- the right tibia. What remains suggests a lytic
ment. lesion that is even larger than the one seen on the
On both innominates there is a large lytic area left.
in the region of the acetabulum in which the T h e morphological similarity of the skull le-
bone is entirely destroyed. Both these lesions ap- sions to those seen in known metastatic carcinoma
pear active. The left femur appears to be normal, of bone make carcinoma a probable cause of the
although the distal end is missing postmortem. lesions. T h e lesions of the long bones would be
Only the diaphysis ofthe right femur is preserved. compatible with this diagnosis. Another possible
It shows multiple lesions, all of which combine consideration is a mycotic infection.
Lesions of the Joints
In order to avoid duplication, the joint mani- Stream, extension of infection from the bone (os-
festation of the specific infections have been dis- teomyelitis) or soft tissue, or by direct introduc-
cussed in connection with the respective bone tion through a wound. Occasionally any joint
lesions in the discussion on infectious disease (pp. may be involved, but about one-third ofthe cases
141, 198). involve the knee and one-third the hip joint,
leaving one-third for all other locations. About 10
Septic Arthritis percent show osteomyelitis. The causative orga-
nisms identified are staphylococci in about one-
PATHOLOGY third and streptococci in about one-fourth of the
Septic arthritis is caused by bacteria entering cases (Heberling, 1941). Other organisms causing
the synovium and the joint cavity by the blood septic arthritis are gonococci, pneumococci, men-
ingococci, and various Gram-negative rods from
enteric infections {Salmonella, Shigella). Gonococ-
cal arthritis is more often multiarticular than
other septic joint infections. Harkness (1942) ob-
served multiarticular involvement in over 80 per-
cent of instances of gonococcal arthritis.
The acute phase of septic arthritis is limited to
the synovial membrane and the articular carti-
lage and will not be recognizable in dry bone
399
400 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
unless the subchondral bone has become involved shortening in septic arthritis than in tuberculosis.
and eroded. Unrelieved septic arthritis will often In infants, before separation of the blood sup-
terminate in bony ankylosis (Figure 652). The ply of the femoral head from that of the proximal
acute and final stages are very similar to tuber- metaphysis, direct extension of osteomyelitis to
culous arthritis in dry bone, although there is the hip joint is common. In such cases, destruction
usually less bone destruction and concomitant of the femoral head and of the growth cartilage
NUMBER 28 401
FIGURES 658, 659.Septic arthritis of the knee resulting in fusion of the left femur and tibia:
658, Medial view; note the periosteal reactive bone on the distal femur. 659, X-ray of
mediolateral view. (Adult, surface find from Chancay, Peru, N M N H uncataloged.)
deformed. Two isolated pieces of bone appear to was used throughout the life of the individual
be sequestra from the head of the femur. The (Figure 659, 661). The knee has fused in the
specimen is from the Klunk site in Illinois, USA, extended position with some rotation of the axis
and is probably pre-Columbian (Hopewell Cul- of the tibia relative to the femoral condyles. Be-
ture). Morse attributes the arthritic changes to cause of this rotation the medial condyle of the
infection. tibia projects posteriorly. There is extensive peri-
Clear evidence of septic arthritis is seen in the osteal bone reaction on the distal diaphysis and
fused left femur and tibia from an isolated surface metaphysis of the femur. Periosteal reactive bone
find near Chancay, Peru (Figures 658-661). on the tibia is minimal and limited to the bone
There are no data on cultural association or date. adjacent to the proximal articular surface. There
The specimen is part of the skeletal collections of is a cloaca in the posterior cortex of the distal
the National Museum of Natural History, Wash- femur just superior to the lateral condyle (Figure
ington, D . C , USA ( N M N H , uncataloged). Al- 660). T h e X-ray film reveals considerable sclerosis
though the bones are somewhat short, they are in the distal femur. T h e periosteal reactive bone,
robust. Arthritic change is limited to the knee. sclerosis, and cloaca are indicative of infection
The X-ray film indicates normal cortical bone and inflammation, making a diagnosis of septic
thickness and density indicating that the limb arthritis highly probable.
NUMBER 28 403
FIGURES 660, 661.Septic arthritis o f t h e knee resulting in fusion o f t h e left femur and tibia:
660, Posterior view; note the cloaca (arrow) in the femur. 661, X-ray of anteroposterior view.
(Adult, surface find from Chancay, Peru, N M N H uncataloged.)
Rheumatoid Arthritis tion I am here only concerned with the late stages
exhibiting significant bone changes.
PATHOLOGY
Rheumatoid arthritis is a generalized connec-
Adult Rheumatoid Arthritis
tive tissue disease of unknown etiology with most
significant involvement of joints. Genetic factors This disease usually commences in the fourth
and climatic conditions are thought to be impor- and fifth decades and continues through the life-
tant. Generally, the disease is thought to be more time of the patient. There is a great predilection
common in cold than in hot climates. However, of females over males with a ratio of about 3:1.
a statistical study carried out on the Blackfoot The disease is not rare. In northern Europe, about
Indians of northern Montana and the Pima In- 4 percent of the males and 16 percent of the
dians of southern Arizona confirmed neither of females over 65 years of age showed some pre-
these viewpoints (Bunim, Burch, and O'Brien, sumptive or definite evidence of this disease (Law-
1964). The disease manifests itself in the adult rence, Laine, and de Graaff, 1961).
and in the juvenile forms. Although the pathology Rheumatoid arthritis usually involves multiple
in both conditions is essentially the same, the joints and is frequently symmetrical. Joints ofthe
areas of involvement are sufficiently different to hands are most frequently, most characteristi-
necessitate a separate discussion. In either situa- cally, and often first involved. In the hands, the
404 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
predilected locations are the metacarpophalan- nied by marked osteoporosis in the adjacent
geal joints and the proximal interphalangeal bones. If joint mobility is maintained, degenera-
joints. The second interphalangeal joints are usu- tive arthritis is superimposed on the rheumatoid
ally spared. The knee is the most frequently lesion. However, in contrast to primary degener-
involved large joint. The temporomandibular ative arthritis, osteoporosis still prevails and mar-
joint is affected in about 25 percent of the cases ginal lipping is less prominent.
(Garrod, 1890:250). Other commonly involved The bone changes on large joints consist of
joints are wrist, carpal joints, shoulder, and elbow. osteoporosis of the articular ends, thinning and
Tarsal, tarsometatarsal, metatarsophalangeal resorption of the subchondral bone plate, sub-
joints, and toe joints are less often involved than chondral bone resorption, and lytic foci due to
the corresponding joints of the hands. The hip subchondral cysts (Figure 663). The contour of
joint is the least often affected ofthe large joints. the articular surface is deformed and irregular.
The joints of the trunk are much less commonly Subluxation is most commonly observed on
involved. If the spine is affected, the changes are metacarpophalangeal joints with axial deviation
usually most marked in the diarthrodial joints of towards the ulnar side. O n dry bone, evidence of
the cervical spine, including the joint between subluxation would consist of extension of the
axis and atlas. convex articular surface on the side of deviation.
The disease process consists of an inflammatory Corresponding unilateral marginal lipping may
infiltration and proliferation of the synovium, be present on the concave articular facet.
which is slowly progressive over many years and Ankylosis may fuse carpals and tarsals into
ultimately destroys and disfigures the joint. The solid blocks of extremely porotic bone showing
process in untreated cases often terminates in sparse trabeculae. Carpometacarpal and tarso-
either loosening of the joint with subluxation or metatarsal joints may also be found ankylosed.
ankylosis (Figure 662) with bony continuity. In
the active phase the joint changes are accompa-
FIGURES 672, 673.Probable rheumatoid arthritis: 672, Posterior view of spine. 673, Detail of
joint fusion of ribs and thoracic vertebrae. (Adult male skeleton from Golovnin Bay, Alaska,
USA, N M N H 346117.)
ditions in dry bone specimens, there are very few and feet compatible with a diagnosis of rheuma-
case descriptions of this type of arthritis in the toid arthritis.
literature on paleopathology. Indeed the evidence Hormell (1940) attributes arthritic changes in
for rheumatoid arthritis in antiquity is so limited a skeleton from Lower Egypt, dated about 1300
that Short (1974) suggests that this disease did B.C., to rheumatoid arthritis. Morse (1969:15, pis.
not occur until fairly recent times with no con- 6E, 11 A) reports a case of possible rheumatoid
vincing evidence before A.D. 1676. arthritis from the Dickson Mound in Illinois,
May (1897) describes a skeleton excavated by USA. The skeleton is from an old male whose
Sir Flinders Petrie from a tomb at Deshasheb, knees were buried in a partly flexed position.
Egypt, dated to the Fifth Dynasty. The skeleton Although evidence of arthritic change in the skel-
is from a male probably 50 to 60 years of age. eton is minimal, Morse argues that the flexed
There is considerable arthritic degeneration of knee is the only example of this burial position at
the spine. The arthritic change affects with de- the site and that this may be evidence of rheu-
creasing severity the cervical, thoracic, and lum- matoid deformity without marked bone changes.
bar vertebrae. The vertebral bodies are flattened, A possible case of rheumatoid arthritis is found
but the anterior margins bulge out with irregular in the skeletal material excavated in Cathedral
lip-like projections. The plate published as part Green at Winchester, England (BMNH XXIII,
of May's report shows a deformity of the hands Burial 2). This specimen is medieval in date and
NUMBER 28 409
FIGURES 674-677.Probable rheumatoid arthritis: 674, Anterior view of pelvis; note the
marginal osteophyte development and erosion in the region of the pubic symphysis. 675,
Erosion and porosity of the distal joint of the femur. 676, Erosion and porosity of the distal
joint of the second and third, right metacarpal bones. 677, X-ray of first, second, and third
right metacarpals; note the subchondral joint sclerosis of the distal, second and third metacar-
pals (arrows). (Adult male skeleton from Golovnin Bay, Alaska, USA, N M N H 346117.)
consists of most of the bones of both feet. There (Figures 668-677) from Golovnin Bay, Alaska,
is bilateral ankylosis of most tarsometatarsal USA (NMNH 346117). The specimen consists of
joints accompanied by marked osteoporosis (Fig- most of the bones from the postcranial skeleton.
ures 665-666). The porosity associated with the The skull and mandible were not recovered. The
joints is indicative of a chronic inflammatory archeological age is not known. The articular
condition. The interphalangeal joint of the right surfaces of the shoulder joints are intact. How-
great toe is fused as well (Figure 667). ever, there has been some arthritic lipping and
Another possible case of rheumatoid arthritis is marginal erosion and porosity. There is some
a male Eskimo skeleton about 34 years of age degenerative change on the articular surfaces of
410 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
addition to rheumatoid arthritis, ankylosing arthritis anatomically. The disease usually begins
spondylitis and degenerative arthritis. The fusion in the lumbar spine and in the sacroiliac joints
of the diarthrodial joints of the spine would be and progressively ascends until the entire spine
very unlikely for degenerative arthritis. Differen- and all costovertebral joints are affected (Figure
tiation from ankylosing spondylitis is much less 679).
certain. Favoring a diagnosis of rheumatoid ar- The disease develops as an inflammatory ar-
thritis would be peripheral joint involvement, thritis of the diarthrodial joints of the spine,
lack of fusion of the sacroiliac joint, and the which leads to early bony ankylosis, either limited
absence of any squaring off of the vertebral bod- to the periphery of the joints or across the entire
ies. The distribution of arthritic change in the facet. In the same type of process, the joints
spine with minimal arthritis of the cervical ver- between the necks of the ribs and the transverse
tebrae is more typical of ankylosing spondylitis. processes and those between the heads of the ribs
However, the overall pattern of arthritic change and the vertebral bodies become ankylosed. In
favors a diagnosis of rheumatoid arthritis. addition, the peripheral portion of the annulus
From a Pueblo Indian site dated around A.D. fibrosus becomes ossified, bridging the inner por-
1559-1672 Steinbock (1976:305-309) describes a tions of the intervertebral discs, which at first are
skeleton, which has partial ankylosis of the spine not affected, but later bony replacement of the
and many other joints, including some bones of nucleus pulposus does occur. The vertebral bodies
the hands and fingers (Figure 678). Steinbock lose their concave flare on the outer circumfer-
attributes this condition to ankylosing spon- ence, resulting in the so-called squaring of their
dylitis, and this is certainly a possible diagnosis. contour in lateral view. This process of fusion of
However, the involvement of peripheral joints, the spinal segments is accompanied by pro-
including severe flexion contractures ofthe hands, nounced osteoporosis ofthe vertebral bodies (Fig-
is more typical of rheumatoid arthritis. ure 680). The result of this ankylosing process is
the rigid, so-called bamboo spine with loss of its
Ankylosing Spondylitis physiological curvatures. In late stages, also, the
(Marie-Striimpell's Disease) various ligaments attached to the spine ossify.
PATHOLOGY
The changes at the sacroiliac joints are usually
bilateral and are never absent if the lumbar spine
Ankylosing spondylitis is a progressive inflam- is involved. They commence with irregular ero-
matory disease of unknown etiology primarily sion of the articular surfaces accompanied by
affecting the diarthrodial joints of the spine, the sclerotic condensation of the subchondral bone
costovertebral joints, and the sacroiliac joints. on both the sacral and the iliac sides of the joint.
The pathologic changes in the active phase are This process ultimately establishes trabecular
practically identical with those of rheumatoid continuity between ilium and sacrum and com-
arthritis. The question of the relationship of the pletely effaces the joint. After establishment of
two diseases is still open but does not concern us complete ankylosis the subchondral sclerosis dis-
here. The manifestations are sufficiently different appears (Schinz, Baensch, Friedl, and Uehlinger,
to justify a separate discussion. 1951-1952(2): 1514). Erosive changes also occur
Ankylosing spondylitis prevailingly involves on the symphysial facet ofthe pubis, but ankylosis
males, in contrast to rheumatoid arthritis. The of the symphysis pubis is uncommon. If periph-
male to female ratio is about 9:1. The disease eral joints are involved in this disease, early bony
usually begins in the second or third decade of ankylosis without marked bone destruction com-
life. In about half of the cases other joints, partic- monly occurs (Rutishauser and Jacqueline, 1959:
ularly hips or shoulders, are affected (Policy and 10-11). The atlantoaxial, the atlantooccipital,
Slocumb, 1947). Involvement of peripheral joints, and occasionally the temporomandibular joint
if present, is indistinguishable from rheumatoid can also be ankylosed.
412 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
FIGURES 679, 680.Ankylosing spondylitis: 679, Frontal view, showing smooth ankylosis of left
sacroiliac joint and "bamboo spine.'' 680, Cut surface, showing ankylosis o f t h e diarthrodial
joints, ossification of interspinal ligaments and the anulus fibrosus, and severe osteoporosis of
vertebral bodies. (67-year-old male, IPAZ autopsy 572 from 1963.)
FIGURES 681, 682.Ankylosing spondylitis of spine: 681, Anterior view of spine. 682, X-ray of
anteroposterior view of fused vertebrae and ribs. (Adult male skeleton from Kuskokwim River,
Alaska, USA, N M N H 351296.)
but currently stored at the British Museum (Nat- male Eskimo from Alaska, USA (NMNH
ural History). Both the diarthrodial joints and 351296). On the skull there is some arthritic
amphiarthrodial joints were fused. Kidd (1954) degeneration of the occipital condyles with mar-
reports the presence of ankylosing spondylitis in ginal lipping and porosity of the left surface. The
two skeletons from a post-Columbian, Huron temporomandibular joints are normal. The sixth
cemetery in Ontario, Canada. Morse (1969, pi. 2 cervical vertebra is missing. The diarthrodial
B, C) briefly describes two possible cases of an- joints of the second and third cervical are fused.
kylosing spondylitis from archeological sites in There is some erosive degeneration of the atlan-
Illinois, USA. Bass, Gregg, and Provost (1974) tooccipital joint surface and some marginal lip-
report one case of ankylosing spondylitis in 2600 ping of all the cervical diarthrodial joint surfaces,
skeletons of Plains Indians from North and South but this is minimal. The first thoracic vertebra
Dakota, USA. Steinbock (1976:304-309) attrib- (TI) is unfused. T2 through T4 are fused and
uted the fusion of the spine in a Zuni skeleton may have been fused to T5 although postmortem
from New Mexico, USA (NMNH 239208) to damage makes this uncertain. T5 through the
ankylosing spondylitis. fourth lumbar vertebrae were fused during life.
A probable example of ankylosing spondylitis Interlocking osteophytes between L4 and L5
is seen in the postcranial skeleton of an adult would have limited the movement of L5. The
k'JI^^^^^^I
s^ipv
^ 4 /-^
^: V ~'^
^^H^
^^^1
^^^H l ^ ^ t ^^
FIGURES 687, 688.Anklylosing spondylitis of spine: 687, Detail of rib and vertebral body
fusion; note smooth anterior surface of vertebral bodies. 688, X-ray of lateral view of fused
vertebrae; note the "squaring off" ofthe vertebral bodies. (Adult male skeleton from Kuskokwim
River, Alaska, USA, N M N H 351296.)
Ochronosis (Alkaptonuria)
Hemophilic Arthropathy
chondral cysts are often present, especially in the More recently Wells (1973) has described a
distal femur and proximal tibia. Femoral con- male skeleton from a R o m a n cemetery (A.D. 150)
dyles and corresponding portions of the tibial at Gloucester, England. There were lytic lesions
plateau can be extensively destroyed. Large pres- in the bone adjacent to the joints of the ankles
sure erosions through the cortex can occur near and feet, suggestive of the type of bone reaction
the capsular attachment. Severe grooving and that could occur in long-standing chronic gout.
eburnation of secondary osteoarthritis is often
absent due to limited motion in the severely Ochronosis (Alkaptonuria)
altered joint. For the same reason the irregulari-
Simon and Zorab (1961) examined one young
ties in the level of the joint surface are more
female Egyptian m u m m y from the Roman Pe-
marked than in ordinary degenerative arthritis.
riod before 30 B.C. T h e X-ray films ofthe mummy
In some cases limited mobility leads to bony
show radiodensities ofthe intervertebral discs and
ankylosis, especially between patella and femur
end-plate cartilage between all vertebrae. Corre-
and between femur and tibia. Early changes may
sponding X-ray films of other mummies did not
be indistinguishable from tuberculous arthritis in
show this feature. O n the basis of similar radio-
dry bone because of the undermining marginal
logic findings in known cases of ochronosis, the
erosion common to both.
authors suggest that the m u m m y may have had
ochronosis during life.
Hemophilic Pseudotumor Wells and Maxwell (1962) describe a possible
case of ochronosis in another female Egyptian
In some cases of hemophilia, massive subper-
mummy. This specimen is dated to the Twenty-
iosteal or medullary hemorrhages occur. These
sixth Dynasty and exhibits dense shadows in the
subperiosteal or intraosseous hematomas may cre-
region of the lumbar discs with narrow, translu-
ate large pressure defects and reactive bony shells
cent zones adjacent to the dense zones. These
simulating neoplasm. Such pseudotumors may be
roentgen features are seen in modern clinical cases
found on the diaphysis or near the joint. Patho-
of ochronosis, and the authors conclude that this
logical fractures through such lesions do occur
disease was present in the mummy specimen.
(Ghormley and Clegg, 1948). Medullary hema-
They also prepared histological sections of af-
tomas may also result in formation of large
fected tissue but found no satisfactory micro-
metaphysial and diaphysial cysts (Stiris, 1958).
scopic support for their conclusion.
T h e major unresolved problem in these reports
PALEOPATHOLOGY
is that shrinkage of cartilage occurs during desic-
cation of the mummy, and as -cartilage discs
Gouty Arthritis
shrink they become more radiodense. T h e varia-
A possible case of gout has been reported by tion in radiodensity between mummies reported
Elliot-Smith and Dawson (1924:157-158) in an by Simon and Zorab (1961) may reflect different
old male mummy from a Christian cemetery near conditions of desiccation and preservation.
the temple of Philae, Egypt. Many of the joints Stenn, Milgram, Lee, Weigand, and Veis
of the extremities have white concretions. T h e (1977) report another possible case of ochronosis
most noticeable of these is seen on the metatarsal in Egyptian m u m m y material. T h e radiologic
bones of the great toe. O n e of these concretions appearance of the spine suggests mineralization
measured 23 by 10 by 5 millimeters. T h e upper of the intervertebral discs. Furthermore, samples
extremity was less affected than the lower. Anal- ofthe discs had zones of black pigment suggestive
ysis ofthe concretion produced a reaction typical of local concentrations of homogentisic acid.
of uric acid. Rowling (1961:414) has reconfirmed Chemical analysis of this dark substance supports
this analysis. this suggestion.
NUMBER 28 419
Cartilage in naturally desiccated human mum- 1000 autopsies of individuals above the age of 15
mies is typically very dark or black. This indicates years. This does not mean that other joints not
that chemical changes in cartilage through time accessible at autopsy or not included in this study
naturally produce dark-pigmented substances. do not also considerably contribute to the total
Whether such cartilage would produce an ana- picture of degenerative arthritis. Heine's data
lytical pattern similar to cartilage containing indicate that a significant degree of degenerative
homogentisic acid has not been demonstrated. arthritis, which may be accompanied by bone
Until this type of experiment has been conducted changes, does not appear before the fourth decade
and the effect of other variables on mummy tissue and increases with age after that time. Since, for
considered, it would appear prudent to defer final our purpose here, only the advanced lesions show-
judgment on the presence of ochronosis in antiq- ing significant bone changes are of interest, the
uity. life span of an archeological population will
greatly influence the recognition and frequency
Degenerative Arthritis of this condition in skeletal material.
ostoses. It is realized that marginal lipping can lytic cavities are not uncommon in the head.
represent a feature of joint remodeling without Acetabular changes mostly consist of marginal
degenerative cartilage changes. However, for our lipping and deepening, leading occasionally to
purpose in the study of dry bone, it has to be protrusion into the pelvis. T h e acetabular roof is
included in the manifestations of degenerative often sclerosed and may also contain cystic cavi-
joint disease. Admittedly there is no sharp line of ties. Degenerative arthritis of the hip often is
separation between aging changes and degener- preceded by other disease processes in this joint,
ative joint disease, but severe and irregular mar- particularly Perthes' disease and slipped epi-
ginal lipping definitely represents a manifestation physis.
of the latter. SHOULDER.The changes are similar to those
Focal or complete attrition of articular carti- in the hip but usually less severe because of lack
lage leads to a sclerotic osteoblastic response in of weight-bearing.
the subchondral bone and to mechanical attrition K N E E . T h e dominant feature is marginal lip-
and polishing of the exposed bony articular sur- ping, often most pronounced on the patella. Ebur-
face (eburnation). These polished areas are ab- nation is usually less extensive than in the hip.
solutely diagnostic of severe degenerative arthri- Exaggerated medial condylar lipping is seen in
tis. Within and around eburnated areas smaller genu varum deformity and on the lateral condyle
and larger pits occur on the joint surface leading in genu valgum. T h e tibial surface is usually less
into subchondral bone. In part, such defects con- affected because of the protective effect of the
nect with smaller and larger cystic spaces, which menisci.
may be sizeable in the articulating bone ends. In ELBOW.Eburnation occurs on all joint sur-
ball and socket joints, such as the hip and shoul- faces. Excavation is observed on the trochlea of
der, these processes lead to enlargement, altered the ulna. T h e radial head shows more overhang-
curvature, and deformation, especially ofthe con- ing lipping.
vex joint surface. The eburnation in these joints BIG T O E . T h e frequent severe involvement of
has a smoothly polished appearance resembling the first metatarsophalangeal joint in Heine's
porcelain. In joints with a hinge-like action, such (1926) series may, in part, reflect the effect of
as the knee and elbow, eburnated areas may heeled shoes, particularly in women. However,
exhibit deep parallel grooves. In joints with little even in a barefoot population the pressure trans-
mobility, such as the diarthrodial joints of the mission through the first metatarsal is great, re-
spine, eburnation may be minimal or absent, sulting in eburnation and sclerosis, especially of
while marginal lipping dominates the picture. the metatarsal head. Lateral deviation of the big
In addition to changes on and around the toe (hallux valgus) leads to formation of a new
articular surface, subsynovial osteophytes, as on joint facet of the lateral slope of the metatarsal
the neck of the femur or humerus, and osteo- head.
phytes at the insertion of capsule and ligaments FINGERS.Degenerative arthritis usually in-
occur in advanced cases. Regardless of the sever- volves the distal interphalangeal joints, charac-
ity of changes, ankylosis does not occur in degen- terized by marked marginal osteophytes (Heber-
erative arthritis. A brief discussion of the local den's nodes). This condition is usually multiarti-
pecularities of degenerative arthritis in different cular and bilateral. It is much more common in
joints follows. females than in males.
H I P . T h e most severe changes are found on
the femoral head. Eburnation and erosion are
Spondylitis Deformans (Spinal Osteophytosis)
most marked on the upper surface. Marginal
exostoses may completely overhang the femoral Degenerative changes leading to bony spur
neck (mushroom deformity). Osteophytes occur formations in the vicinity of intervertebral discs
on the intracapsular portion of the neck. Large are exceedingly common in skeletal material past
NUMBER 28 421
dry bone they appear as round or oval defects in TABLE 13.Frequency of degenerative arthritis in major
long bones of adult archeological skeletons from the Chicama
the bony end-plate bordered by a basket-like
Valley, Peru (from Hrdlicka, 1914:62-69)
arrangement of reactive bone within the vertebral
body. Corresponding lesions in two adjacent ver-
Bones No. examined No. arthritic % of total
tebrae bordering the same disc are common.
Humeri 593
Proximal 1 0.2
P A LEOPATHO LOGY Distal 12 2.0
Ulnae 301
The expression of degenerative arthritis in ar- Proximal 16 5.3
cheological material affects both joint surfaces Distal 0 0
and the articular margins of bone. Degenerative Radii 255
arthritis of joint surfaces may result in bone de- Proximal 6 2.4
Distal 1 0.4
struction a n d / o r bony hypertrophy. Arthritic de-
Femora 1210
struction is expressed as porosity, often with ebur- Proximal 16 1.3
nation (polishing) of the disturbed bone surface. Distal 36 3.0
Arthritic hypertrophy is less common and is seen Tibiae 781
as an irregular thickening of the joint surface, Proximal 12 1.5
which may be somewhat porous. Marginal degen- Distal 0 0
Fibulae 266
erative arthritis is also expressed as a destructive
Proximal 1 0.4
a n d / o r hypertrophic process although the latter, Distal 2 0.8
in contrast with joint-surface degenerative arthri-
tis, is more common. In diarthrodial joints, hy-
pertrophic, marginal, degenerative arthritis is affected by degenerative arthritis. He concludes
usually seen as a fairly smooth extension of the that their vigorous life style is the major causative
joint surface. In amphiarthrodial joints of the factor in this difference. In an earlier study, Stew-
vertebral bodies, hypertrophic arthritic change art (1947) found differences in the degree and
gives rise to osteophytes or finger-like projections location of vertebral degenerative arthritis be-
from the bony periphery of the joint. tween Eskimo, Pueblo Indian, and modern White
While several factors may contribute to the skeletons. He suggested that cultural differences
development of degenerative arthritis, stress un- were important, but he also noted that racial
doubtedly is the most significant of these factors. variation in the structure ofthe vertebral column
Thus, as Ortner (1968:146) suggested, the distri- may affect patterns of movement ofthe vertebrae
bution and severity of degenerative arthritis in and thus affect the expression of spinal degener-
the skeleton are likely to vary between societies ative arthritis.
and with different roles (e.g., male-female) within Although stress is a major factor in degenera-
a society. Hrdlicka's data (1914:62-69) indicates tive arthritis, it is likely that different types of
that the elbow joint was the most frequent site stress will affect the development of arthritis in
for degenerative arthritis in ancient Peruvian different ways. It is here that the paleopathologist
skeletal remains. The knee was next in severity with access to the entire skeleton and joint sur-
(Table 13). This finding differs from modern faces, could contribute to the understanding of
populations where the knee is most frequently degenerative arthritis. For example, what is the
affected. effect of relatively continuous but moderate stress
In a study comparing modern American on a joint, as contrasted with intermittant but
Whites, Blacks, pre-Columbian Indians from high stress? In such a problem comparisons of
New Mexico, and protohistoric Eskimos, J u r m a i n degenerative arthritis in joints of the left and
(1977) found the Eskimos to be most severely right side and male versus female joints or skele-
FIGURES 693, 694.Degenerative arthritis of the shoulder
and hip: 693, Lateral view of the left scapula showing
porosity of the glenoid cavity. 694, Porous degeneration of
the right hip joint. (Adult female Eskimo skeleton from
Hooper Bay, Alaska, USA, N M N H 339115.)
r.ti.UimMitii'.
gairvfii!lj^<
FIGURES 695, 696.Subchondral bone in a section through the capitulum: 695, Normal joint
surface and subchondral trabeculae. 696, Sclerosis of trabeculae underlying porous degenerative
change of the capitular joint surface. ( N M N H , unidentified humeri from the Huntington
collection.)
424 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
The left scapula has considerable porosity on the aspects of arthritic change in the elbow. Briefly,
anteroinferior surface of the glenoid fossa with a of the three related but distinct changes that
small area of porosity on the posterior margin occur, the first is a degenerative change of the
(Figure 693). Marginal lipping is minimal. joint surface, which is most common between the
In archeological skeletal remains the elbow is head of the radius and the capitulum. This is
a common site of degenerative arthritis. Ortner probably related to the fact that both flexion-
(1968) discussed the anatomical and functional extension and rotation are movements associated
FIGURES 697-700.Degenerative arthritis of the elbow and wrist: 697, Anterior view of the
distal humerus; note the porosity of the capitular surface and the bone hypertrophy of the
capitular and trochlear fossae. 698, Marginal lipping adjacent to the trochlear joint surface.
699, Hypertrophic bone filling in the olecranon fossa. 700, Degenerative arthritis of the distal
joints of the radius and ulna. (Adult male Eskimo skeleton from Golovnin Bay, Alaska, USA,
N M N H 279209.)
NUMBER 28 425
with this joint surface. Porous degeneration ofthe arthritis (Figure 700). The joint between the ulna
joint stimulates sclerosis of subchondral trabec- and radius exhibits marked marginal lipping as
ulae (Figures 695, 696). Second, there is marginal does the joint surface ofthe wrist. There is coarse
Upping primarily adjacent to the trochlear joint porous degeneration, particularly on the ulnar
surface. Third, there is bony fill-in of the three surface, with some evidence of eburnation. It is
fossae of the humeral component of the elbow. possible that fracture may have stimulated some
An adult male Eskimo from a site on Golovnin of the arthritic degeneration in the wrist. The
Bay, Alaska, USA (NMNH 279209) exhibits the bones of the hands are often lost in archeological
major features associated with degenerative ar- skeletons. However, a common site for arthritic
thritis ofthe humerus. Nearly the entire capitular change in Eskimo skeletal specimens is the joint
joint surface is porous with slight traces of ebur- between the trapezium and the first metacarpal
nation (Figure 697). Marginal lipping is most bone.
pronounced on the margins of the trochlear sur- Arthritic degeneration of the hip is a fairly
face (Figure 698). There is considerable fill-in of common condition in archeological specimens.
both the capitular and trochlear fossae (Figure Wells (1963a) and Pitt-Rivers (1965) are among
697). This condition is more severe on the right many who have described typical cases. An ex-
side. Similarly the olecranon fossa has a large bar ample of moderate arthritic change is seen in the
of hypertrophic bone filling in most of the de- Eskimo skeleton also discussed below in the con-
pression (Figure 699). The hypertrophic bone in text of spinal degenerative arthritis (NMNH
the fossae would have limited the amount of 339115). The right hip joint of this specimen
flexion and extension of the elbow. exhibits marked porosity on the superior joint
The distal joint of the radius and ulna of the surface ofthe acetabulum with a trace of porosity
same specimen also shows marked degenerative on the peripheral margin of the remaining joint
FIGURES 708-711.Degenerative arthritis o f t h e third through fifth lumbar vertebrae and left
and right first metatarsals: 708, Osteophyte development of vertebral bodies. 709, Superior
aspect of the fourth (left) and fifth (right) lumbar vertebrae; note the erosive lesion suggestive
of the presence of Schmorl's node in the fifth vertebral body (arrow). 710, Inferior view o f t h e
fifth lumbar vertebra; note the marked porosity o f t h e vertebral body surface. 711, T h e distal
articular surface of the right and left first metatarsal bones; note the porosity and eburnation
associated with the central ridge of the joint surface. (Adult male Eskimo skeleton from an
archeological site in Pastolik, Alaska, USA, N M N H 332556.)
NUMBER 28 429
Alaska, USA (NMNH 333467). Both knees are The Axial Skeleton
affected. T h e right knee exhibits erosion, porosity,
and eburnation of the lateral condylar surfaces. SKULL AND MANDIBLE.In the adult the skull
The medial posterior portion of the femoral por- has only two jointsthe temporomandibular and
tion of the knee has a lytic porous focus with a atlantooccipital. The latter is most appropriately
small area of hypertrophic bone adjacent to the considered with the vertebral column. Degener-
porosity. There is some marginal lipping. The left ative arthritis of the temporomandibular joint
knee exhibits degenerative changes, which are has received little attention in the literature on
somewhat different from those described earlier paleopathology (see reviews of by Pales, 1930:
(p. 427). O n the medial condyle ofthe femur, the 165-173, and Alexandersen, 1967:586-590).
arthritic change is characterized by a large area Given the hard use of the jaw often thought to be
of irregular hypertrophic bone on the posterior associated with archeological skeletal populations
portion (Figures 706, 707). There is some porosity, it is surprising that the frequency of arthritic
eburnation, and marginal lipping. The lateral change in the temporomandibular joint is not
condyle has a small area of irregular hypertrophic greater. As with other joints, degenerative change
bone on the posterior portion. Marginal lipping in this joint may involve porosity, eburnation,
is minimal. There is a defect between the condylar and hypertrophy of the joint surface. Marginal
surfaces suggestive of an old well-healed fracture. lipping is not common.
On the tibia the medial condyle is eroded, porous, A fairly typical expression of temporoman-
and eburnated with slight marginal lipping. On dibular degenerative arthritis is seen in an adult
the lateral condyle, arthritic change is primarily female skull from the Nushagak Region in Alaska,
a focus of irregular hypertrophic bone rising USA (NMNH 363530). Both the glenoid fossa
above the joint surface. O n both condyles there and the mandibular condyles are involved (Fig-
is slight marginal lipping. The tibial portions of ure 712) but the most severe change is on the
the ankle joints of this specimen also exhibit glenoid fossa. There the porous lesions are re-
slight, porous degeneration of the joint surface. stricted to the anterior edge of the fossa and are
There is minimal marginal lipping. Arthritic de-
generation of the ankle is uncommon in archeo-
logical specimens, even when there is marked
degenerative change in other joints.
Bones of the feet commonly exhibit degenera-
tive arthritis. The bones most often affected are
those of the great toe. An example of this condi-
tion is seen on the distal joint surface of the right
and left first metatarsal (Figure 711) from an
Eskimo burial from Pastolik, Alaska, USA
(NMNH 332556). The left metatarsal exhibits
considerable porous erosion on the central ridge
of the joint surface. There is minimal marginal
lipping, although there is an erosive depression
on the medial margin of the joint extending onto
the adjacent cortex. O n the right first metatarsal
there is some porosity, but the major degenerative
FIGURE 712.Degenerative arthritis of the left temporoman-
change is eburnation of the central ridge. There
dibular joint. (Adult female Eskimo skull from an archeolog-
is also an erosive depression on the medial margin. ical site in the Nushagak Region, Alaska, USA, N M N H
The other metatarsals are normal. 363530.)
430 SMITHSONIAN CONTRIBUTIONS TO A N T H R O P O L O G Y
characterized by erosion and porosity of the sur- The second example is from an archeological
face. site on the Seward Peninsula, Alaska, USA
VERTEBRAL COLUMN.Wood-Jones (1910b: ( N M N H 342482). T h e specimen is from an adult
277) observed that virtually all adult ancient male Eskimo of uncertain archeological age. Diar-
Nubian skeletons showed some evidence of degen- throdial joints between the vertebrae exhibit min-
erative arthritis of the spine. A similar generali- imal evidence of abnormality except for the fusion
zation would apply to virtually any archeological of C2 and C3 and degenerative arthritis of the
skeletal sample. However, the frequency, age of joints from the seventh cervical through the sixth
onset, severity, and distribution within the spine thoracic (Figures 717-719). T h e spine of T I was
varies in different populations (Snorrason, 1942; broken off (Figure 716) and the degenerative
Stewart, 1947; Zorab, 1961; Chapman, 1965). change ofthe diarthrodial joints may be a sequela
All vertebrae have diarthrodial joints, which of the trauma. This conclusion is supported by
permit movement of adjacent joint surfaces. the relative lack of degeneration in the remaining
These joints are between the facets ofthe articular vertebrae.
processes of adjacent vertebrae. In addition the Degenerative arthritis of the amphiarthrodial
vertebral bodies are connected by cartilage discs vertebral joints is more easily noticed and has
in which gliding does not occur. All movement is received greater attention in the literature on
due to the compression and expansion of the disc. paleopathology. Two degenerative conditions are
T h e thoracic vertebrae have additional joints for associated with these joints. In the first of these,
the articulation of the ribs on the bodies and degeneration of the disc may result in herniation
transverse processes. Porosity, eburnation, and of the disc and pressure erosion of one or more
marginal lipping are associated with degenerative foci on the bony articular surface (Schmorl's
arthritis of the diarthrodial joints. Erosion and nodes) of the vertebral body. With disc degener-
marginal osteophyte development are associated ation there may also be a generalized porosity of
with degenerative change ofthe vertebral bodies; virtually the entire surface of the vertebral body.
porosity and eburnation occur rarely. The joints The second type of degenerative arthritis involves
between ribs and vertebrae (costovertebral joints) marginal development of osteophytes. In some
exhibit marginal lipping and porosity but rarely cases the antecedent cause of osteophyte devel-
eburnation. opment appears to be anterior herniation of the
Two cases serve to illustrate degenerative ar- disc. This condition is suggested in a specimen
thritis of diarthrodial joints ofthe vertebrae. The from an Eskimo skeleton from Pastolik, Alaska,
first of these is an adult female skeleton from USA ( N M N H 332553). T h e specimen is from a
Hooper Bay, Alaska, USA (NMNH 339115). The young adult male of uncertain archeological age.
archeological age is uncertain. The diarthrodial The vertebral column is incomplete but the de-
joints between the vertebrae all exhibit arthritic generative change is limited to the joint between
degeneration (Figures 713, 714). However, the the fourth and fifth vertebral bodies (Figures 720,
cervicals have the most extensive involvement 721). The lesion consists of anterior periarticular
including porosity, eburnation, and marginal lip- lipping with adjacent periosteal reactive bone on
ping (Figure 713). The lumbar vertebrae are the anterior cortex of the bodies with rather
somewhat less affected and the thoracic vertebrae marked erosion o f t h e anterior joint surfaces par-
least affected. The vertebral bodies of the lower ticularly on the fifth vertebral body. T h e lesions
thoracic and lumbar vertebrae exhibit the great- of the two bodies are suggestive of an anterior
est osteophyte development. The inferior surface herniation of the disc resulting in focal pressure
of the tenth vertebral body shows the typical erosion and peripheral periosteal reactive bone.
bony erosion associated with Schmorl's nodes Another example of degenerative arthritis of
(Figure 715). the vertebral bodies is seen in the spinal column
NUMBER 28 431
" .
..M^^^ ""f^^ltBfS^^ymM
B^4 ^ B ailr .^
mi^i^^KBSr^Wk
S F "^^r^'*''^H
Wm''' ^^^/- &UHk^^Pyfe^'^* -^H
^^^HB^^RM^^,.' . J ^ H
of another specimen from Pastolik, Alaska, USA (Figures 708-710). The superior joint surfaces of
(NMNH 332556). The skeleton is an adult male L l , L2, and L5 exhibit slight to moderate lytic
of uncertain archeological age. The vertebral col- activity suggestive of pressure erosion from a
umn is complete, although there is some post- Schmorl's node. The inferior surface of L5 (Figure
mortem damage. All of the vertebral joints, both 710) and the corresponding surface of the first
diarthrodial and amphiarthrodial, show evidence sacral body are porous. There is extensive devel-
of degenerative arthritis. However, the most se- opment of marginal osteophytes, some of which
vere changes are seen in association with the were in contact with osteophytes of adjacent ver-
amphiarthrodial joints of the lumbar vertebrae tebral bodies. Within the periarticular lipping
432 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
there is a concave depression, often with cyst-like ticular lipping increases toward the fifth lumbar
cavities, between the outer edge of the original body. These vertebrae exhibit a typical, although
body and the outer edge of the degenerative rather severe, pattern of degenerative arthritis of
lipping (Figure 709). The severity o f t h e periar- the spine.
NUMBER 28 433
PATHOLOGY
The Jaws but remains, forming a cyst into the base of which
the incomplete tooth projects. Again it is the area
PATHOLOGY of the third molar that is predilected. This type
of cyst usually develops from a tooth bud of the
T h e jaws participate in a great variety of le-
second dentition or from a supernumerary dental
sions, which also may affect other parts of the
follicle. In dry bone it would be similar to the
skeleton. Here I will discuss only the lesions that
primordial cyst except for the presence of an
are found exclusively in the jaws, because of their
incomplete tooth projecting into the cavity if it
intimate relationship to' the teeth and to the
were preserved intact.
complicated development of the facial skeleton.
RADICULAR CYST.This third type of odonto-
These lesions fall into two groups: odontogenic
genic cyst is the most common of all. It is not the
and nonodontogenic.
result of maldevelopment but of infection of the
pulp cavity and the root canal of an erupted
tooth. It starts as an apical abscess or granuloma
Odontogenic Cysts
and secondarily acquires an epithelial lining from
remnants of the epithelial sheath of the dental
The complicated dental development resulting root. It may be located on any erupted tooth of
from the coordinated interplay of the ectodermal the mandible or maxilla and is always intimately
enamel epithelium and of the mesodermal tooth associated to the root of an erupted tooth. This
bud lends itself to a variety of malformations. tooth may have fallen out but its alveolus would
Since the third molar is regressing in the human still connect with the cyst cavity. In contrast to
and may be not developed, or at least not erupted, the dentigerous cyst, where the tooth is below the
anomalies affecting its development are not too cyst, in the radicular cyst the tooth is above.
uncommon.
PRIMORDIAL CYST.This cyst is the result of an
abortive development of a dental follicle without Odontogenic Tumors
formation of a tooth. The cyst has a fibrous wall
and is lined by odontogenic epithelium. It predi-
lects the area of the third molar, more often in A variety of tumors can arise from epithelial or
the mandible than in the maxilla. As the cyst mesenchymal components ofthe dental bud. The
enlarges it may occupy part of the ascending most important of these is the ameloblastoma
mandibular ramus. In dry bone it would appear arising from enamel epithelium. This lesion is
as a cystic cavity that may bulge the overlying more common in the mandible than in the max-
cortex but is not intimately associated with a illa, predilecting the area of the third molar.
dental root and does not contain a tooth. Males are more often affected than females. The
DENTIGEROUS CYST.This type of cyst is the lesion is unusually frequent in certain populations
product of a later stage of deranged dental devel- of African Negroes, but it can occur in all races.
opment. After the crown of a tooth is already The lesion begins in childhood or adolescence
developed the enamel epithelium fails to involute and slowly progresses. It is basically a benign
436
NUMBER 28 437
lesion. The fully developed tumor presents as a between the lateral upper incisor and the canine
cystic mass, often multiloculated, which expands tooth in the alveolar process.
the bone but maintains a thin, ridged, bony shell. The nasoalveolar cyst is due to epithelial rem-
Enamel is not formed by the tumor tissue and a nants between the lateral nasal and the maxillary
tooth is not included in the lesion. process. It is not located between the teeth and
All the other odontogenic tumors are of mes- tends to bulge into the nasal cavity when it
enchymal origin. The odontoma is a tumor pre- enlarges.
vailingly consisting of dentin, but cementum and The nasopalatine cyst is based on persistence
enamel can be intermixed. This tumor may be a and continued secretion ofthe epithelial lining of
shapeless mass of tissue of increased radiodensity, the vestigial nasopalatine duct. It may form uni-
but in its most mature form it may show a laterally or bilaterally in the incisive canal and
conglomeration of fairly well-developed teeth. destroy or partly destroy the anterior portion of
Thin, polished, undecalcified sections should the hard palate.
readily reveal the finely tubular structure of den- Unicameral bone cysts occur in the jaws as in
tin microscopically. The cementoma is usually a other bones. In the mandible they tend to be
tumor of moderate size, intimately attached to located below the nerve canal rather than pri-
one or several adjacent erupted teeth. Cementum marily in the alveolar process. In the maxilla they
is a mineralized tissue resembling bone, which tend to bulge the cortex forward and towards the
covers the dental root in a thin layer and serves antrum.
as attachment of the alveolar ligament. Tumor-
like proliferations of cementum are not uncom- Nonodontogenic Tumors
mon in the jaws of persons with Paget's disease.
The myxoid mesenchyme normally forming Various fibro-osseous tumors occur in the jaws,
the tooth pulp may give rise to an odontogenic more often in the maxilla than in the mandible.
fibroma. This would appear in the dry bone They are characterized by production of finely or
merely as a smooth-walled, more or less ex- coarsely trabecular, mostly woven, bone. The
panded, lytic defect without any identifiable relationship of such lesions to fibrous dysplasia is
characteristics. open to question. Bilateral disfiguring fibro-os-
seous maxillary tumors are seen in young individ-
uals (cherubism). Recognition of such lesions in
Nonodontogenic Cysts
dry bone would depend on perfect preservation
These cysts are related to the closure of various of frail trabecular bone.
fissures in the development of the facial skeleton A variety of lytic lesions, such as eosinophilic
or remnants of the nasopalatine duct. Most of granuloma, "brown tumor" of hyperparathyroid-
them are located in the maxilla, and all but the ism, giant cell reparative granuloma or metastatic
unicameral bone cyst arise on the basis of minor carcinoma, occur with some frequency in the
developmental disturbances. jaws. In dry bone such lesions are devoid of
The median cysts occur between the central identifying characteristics in themselves but may
incisors of the maxilla or of the mandible, due to be interpretable in the context of findings else-
trapping of epithelium between the two halves of where in the skeleton.
the maxilla or mandible. This is the only non- Carcinoma of the oral or nasal cavity, the
odontogenic epithelial cyst found in the mandi- paranasal sinuses, and even the facial skin may
ble. cause extensive destruction of a jaw or other facial
The globomaxillary cyst results from epithelial bone by direct invasion. As a rule the lesion would
inclusions between the maxillary and globular show a frayed margination in dry bone with little,
processes of the maxilla. It is always located if any, osteosclerotic reaction.
438 SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
These distances are more than twice the normal conditions depends on good medical histories, soft
distance between alveolar bone and the cemento- tissue pathology, and bacteriology. It is thus un-
enamel junction and are indicative of consider- likely that all the specific factors that induce
able alveolar resorption, which exposed the root periodontal disease will be identifiable in dry
to caries. bone specimens. For this reason I shall limit my
SECONDARY EFFECTS OF DENTAL CARIES.If discussion to the more common causative factors
tooth destruction from dental caries penetrates and those which may be identifiable in archeo-
the pulp cavity, infection of the support tissues is logical specimens.
an almost inevitable result. Bone tissue reaction As a general principle, periodontal disease in-
to infection initially involves bone destruction volves an inflammatory response to one or more
providing a drain for pus. Chronic infection leads irritants. This inflammation often results in re-
to at least partial bony circumscription around sorption of alveolar bone creating an abnormally
the infectious focus. Tooth exfoliation and hem- large distance between bone and the cemento-
atogenous dissemination of the infection are ad- enamel junction. A common irritant is calculus
ditional potential secondary effects. and its precursor, bacterial plaque, which consists
Most of these morbid processes, secondary to of a sticky coating including protein, food parti-
dental caries, are demonstrated in the maxillary cles, living and dead microorganisms. When
dentition of an adult male skull from the pre- plaque mineralizes, it becomes calculus and in
Columbian site of Puye, New Mexico, USA this form can be found on archeological skeletal
(NMNH 262948). The left central incisor is miss- specimens as relatively hard additions to the tooth
ing postmortem. The right second premolar and surface. The role of calculus in periodontal disease
right third molar are missing antemortem. In the is not clear. Ruben, Goldman, and Schulman
case of the premolar there is evidence of abscess (1970:397) express the opinion that mechanical
at the base of alveolus. The alveolus of the third irritation from calculus is secondary to inflam-
molar is shallow with evidence of remodeling mation directly induced by bacterial activity. In
suggestive of infection. However, there is no evi- any case the presence of calculus on dental tissues
dence of a draining sinus through the alveolar is an important consideration in evaluating the
bone. The major periapical lesions are associated cause of periodontal disease in archeological skel-
with the first molars. Both teeth have large cavi- etal material.
ties in the crown, which have penetrated the pulp Metabolic problems may result in inflamma-
cavity (Figure 732). The resulting infection has tory conditions that affect the periodontal tissues.
resulted in lytic lesions of the maxilla, which In scurvy, for example, the quality of the connec-
penetrate the external cortex of the maxilla on tive tissue associated with teeth is weakened.
both sides and the inner cortex on the left (Figure Bleeding results from weakened blood vessel walls
733). Whether this condition led to disseminated being traumatized by chewing. T h e inflamma-
infection elsewhere in the body cannot be deter- tory response in scurvy may lead to exfoliation of
mined. Indeed evidence for such a complication teeth, particularly those with single roots. Simi-
would be rare in dry skeletal material. larly, protein deficiency may lead to diminished
quality of supporting tissue and periodontal dis-
ease.
Periodontal Disease
Peridontal abscess may result in relatively lo-
PATHOLOGY calized periodontal disease. T h e effect on sup-
porting tissue may be similar to that produced by
Ruben, Goldman, and Schulman (1970:394) periapical abscess. However, the focus of infection
note that several morbid conditions result in peri- in periodontal abscess is outside the pulp cavity
odontal disease. Identification of many of these and often between the roots of multirooted teeth
NUMBER 28 443
(Ruben, Goldman, and Schulman, 1970:423). alveolar resorption. The distinction will need to
Abscess of alveolar bone without evidence of car- be made between alveolar resorption from peri-
ies involvement of the pulp cavity would be odontal disease and resorption associated with
suggestive of periodontal abscess. periapical abscess and tooth loss. Clearly if there
is alveolar resorption but little or no evidence of
PALEOPATHOLOGY caries or tooth loss, a diagnosis of periodontal
disease is appropriate. An example of this condi-
In archeological skulls the major manifestation tion is seen in the mandible of a skeleton from an
of periodontal disease will be local or general archeological site on Horr's Island, Florida, USA
(NMNH 352156). The maxilla was broken post-
mortem and only fragments recovered. On the
mandibular teeth there is considerable root ex-
posure, which is indicative of alveolar resorption
(Figures 734, 735). Dental calculus is adherent on
the exposed buccal root surfaces of the incisors
and canines. Alveolar resorption is particularly
noticeable in the bone supporting the first molars.
Although there is considerable wear, there is no
evidence of pulp-cavity exposure or caries. The
presence of calculus in association with alveolar
resorption and lack of dental caries supports a
diagnosis of periodontal disease.
Another example of marked tooth root expo-
sure with no evidence of dental caries is found in
the mandible of a skeleton from an archeological
site at Canaveral, Florida, USA ( N M N H the formation of dental tissue. Fairly typical mul-
377439). T h e maxilla was broken postmortem tiple hypoplastic lines are seen in the dentition of
and only fragmentary portions were recovered. a 26-year-old male from the Pathology Museum
These fragments exhibit considerable root expo- of the University of Graz in Austria (PMUG
sure of the right incisors, canine, and first pre- 3421, autopsy 9497 from 1879). Autopsy records
molar. These teeth were extensively worn with state that the individual was a syphilitic. Trans-
evidence of secondary dentin formation in the verse hypoplastic lines are most pronounced on
incisors. The mandibular incisors appear to have the maxillary dentition, particularly the central
been lost antemortem as was the left first pre- incisors (Figure 737). In addition to the defective
molar. The right canine, premolars, left second lines, there are numerous fine pores in the enamel.
premolar and first molar were probably lost post- Congenital syphilis may result in defective first
mortem. However, in the case of the left first molars (mulberry molars). The crown size is
molar, alveolar resorption had resulted in very smaller than normal, tending to be smaller than
poor support for the tooth roots. There is consid- that of the second molar; normally the crown of
erable root exposure of the second and third the first molar is the larger. T h e occlusal surface
molars and marked build up of calculus on the is very irregular. A skull from a modern female
crown and exposed root (Figure 736). Rough about 30 years of age exhibits dental defects fairly
porosity characterizes the bone associated with typical of congenital syphilis (NMNH 219398).
the left molar roots. This is indicative of an The upper right central, lower right central, and
inflammatory condition, probably including the lower left lateral incisor crowns have hypoplastic
overlying soft tissues. The pattern of alveolar defects o f t h e incisal edge (Figure 738). The first
exposure and lack of caries supports a diagnosis molars are smaller than the second and have a
of periodontal disease. pitted, poorly formed, occlusal surface (Figure
739).
Disturbances in Dental Development Dental hypoplasia is also thought to be associ-
ated with rickets. Figures 424 and 426 show hy-
PATHOLOGY
i
so that the diagnosis of tuberculosis cannot be
evaluated. T h e lytic lesion on the mandible is not
typical of tuberculosis. T h e disease processes
would have had to begun in late fetal life or early
infancy to have produced these effects on the
incisors.
An undoubted case of tuberculosis with multi-
ple hypoplastic lines is associated with the skull
of a 17-year-old boy, which is part of the Federal
Pathologic-Anatomy Museum in Vienna, Austria
(FPAM 2016, autopsy 16648 and 1842). There
are multiple lytic lesions ofthe skull. T h e incisors,
canines, and premolars that remain in the jaws
show hypoplastic lines (Figure 743).
FIGURE 744.Enamel hypoplasia expressed as hypoplastic FIGURE 745.Multiple hypoplastic transverse defects of the
transverse lines of the buccal crown surface of all teeth canine teeth. (Adult male from Fort Concho, Texas, USA,
except the molars. Anterior tooth wear is marked with N M N H 243490.)
secondary dentin apparent on the occlusal surfaces. (Adult
female from Mobridge site. South Dakota, USA, N M N H
325416.
erotopic). T h e first of these is the facial portion of
a child's skull from Chicama, Peru (NMNH
Abnormal Quantity of Teeth
293595). T h e mandible was not recovered. The
Supernumerary teeth (hyperodontia) are archeological age is unknown. Both second per-
rather common in archeological specimens (e.g., manent molars have erupted, although the third
Brothwell, 1965a: 114, 115). Two cases serve to permanent molar is still deep in the maxilla. Most
illustrate the development of supernumerary of the teeth have been lost postmortem. The
teeth outside the alveolar region of the jaws (het- alveoli indicate that the normal number of teeth
FIGURE 746.Heterotopic supernumerary canine projecting FIGURE 747.Heterotopic supernumerary canine projecting
through the left maxilla. (Child's skull about 12 years of age through the left palate (Adult skull from Pachacamac, Peru,
from Chicama, Peru, N M N H 293595.) N M N H 267104.)
NUMBER 28
449
Dental Anomalies
PALEOPATHOLOGY
Romero, 1958, 1970). Tooth filing, associated of secondary dentin, the pulp cavity will be ex-
with blackening with burnt oil, is common in posed creating the potential for infection of the
Sumatra and probably throughout much of the pulp and supporting alveolar bone.
Pacific. Attrition also takes place on the opposing sur-
T h e variation in the practice of dental muti- faces of adjacent teeth (interproximal attrition).
lation is remarkable, although beyond the objec- This type of wear is due to the contact between
tives of this book. O n e previously unpublished teeth and the slight movement of the teeth that
case will serve to illustrate this type of dental accompanies chewing. This type of attrition is
trauma. T h e specimen is from Saint Croix in the relatively slight, rarely if ever exposing the dentin.
Virgin Islands and was discovered when it was
washed out by a storm (NMNH 382048). T h e
morphology ofthe skull is distinctively Negro and PALEOPATHOLOGY
Hjt'
^ $^ ^ f
^^^^^^^^^^^^^^^^r^^
^HHI k ^
^^^^^^^^^^^^^HM^ ''
^^^^^^F^
^\
# -
i^
^ . .^
.^1
JGH
Dental Discoloration
PATHOLOGY
457
SMITHSONIAN CONTRIBUTIONS TO ANTHROPOLOGY
458
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