Anemia and Childhood Mortality: Latitudinal Patterning

Along the Coast of Pre-Columbian Peru

Deborah E. Blom,
1
* Jane E. Buikstra,
2
Linda Keng,
3
Paula D. Tomczak,
4
Eleanor Shoreman,
5
and Debbie Stevens-Tuttle
6
1
Department of Anthropology, University of Vermont, Burlington, Vermont 05405
2
Department of Anthropology, University of New Mexico, Albuquerque, New Mexico 87131
3
Department of Anthropology, University of Houston, Houston, Texas 77204
4
Department of Anthropology, University of New Mexico, Albuquerque, New Mexico 87131
5
Department of Anthropology, Vanderbilt University, Nashville, Tennessee 37235
6
Department of Neurology, University of Vermont, Burlington, Vermont 05405
KEY WORDS paleopathology; porotic hyperostosis; skeletal biology; Andes; parasites
ABSTRACT Hrdlicka ([1914] Smithson. Inst. Misc.
Collect. 61:169) reported that pre-Columbian skeletal
material from the coastal lowland Andean region exhib-
ited a high frequency of porotic hyperostosis, a patholog-
ical condition of bone that generally is thought to indicate
childhood anemia. While subsequent studies tended to
reinforce this conclusion, factors implicated in the condi-
tion have yet to be fully explored in the region as a whole.
This study explores regional and intravalley variation as
one step in establishing biocultural variables that in-
crease the apparent risk of childhood anemia. The study
sample includes 1,465 individuals: 512 from Peruvian col-
lections housed at the Field Museum of Natural History,
and 953 from systematically excavated contexts from Mo-
quegua, Peru. Environmental stressors, such as parasites
and disease, rather than specic dietary practices were
found to be more likely associated with childhood anemia
in these coastal Andean samples. The study supports cri-
bra orbitalia as an earlier expression of porotic hyperos-
tosis and suggests that porotic hyperostosis, as recorded
here, cannot be easily dismissed as a result of cranial
shape modication. No clear temporal patterns were ob-
served. Finally, the study establishes that comparing data
for children and adults can reveal the relative association
between childhood anemia and mortality. Childhood mor-
tality associated with anemia was elevated where the
presence of tuberculosis or tuberculosis-like conditions
was more common and the presence of water-borne patho-
gens was negligible. In contrast, those buried at lower
altitudes, closer to the coast, and consuming mainly ma-
rine resources were less likely to die in childhood with
anemia than in the other contexts studied. Am J Phys
Anthropol 127:152169, 2005. 2004 Wiley-Liss, Inc.
The archaeological record of coastal Peru is excep-
tionally rich. Human remains, organic artifacts, and
diverse remnants of human subsistence are well-
preserved due to extreme aridity in archaeological
sites that date back at least 10,00011,000 years.
Consequently, archaeologists and collaborative sci-
entists have been unlocking various aspects of the
rich pre-Columbian archaeological record in Peru
and the broader Andean region for more than 100
years. Working with an extensive human osteologi-
cal sample of 3,400 individuals from Andean sites
such as Chan Chan and Pachacamac, Hrdlicka
(1914) rst noted that pre-Columbian Andean skel-
etal material from the coast exhibits a high fre-
quency of porotic hyperostosis, a pathological condi-
tion of bone generally thought to indicate childhood
anemia. More recent work reafrmed the presence
of porotic hyperostosis in additional Andean con-
texts (e.g., El-Najjar, 1976; Allison, 1984; Fouant,
1984; Benfer, 1990; Williams, 1990; Ubelaker, 1992;
Verano, 1992, 1997; Burgess, 1999; Tung, 2003; Far-
num, 2002). The present study extends this research
by incorporating a large sample of human remains
fromcoastal archaeological sites to examine regional
patterning in ancient Peruvian porotic hyperostosis.
Porotic hyperostosis (also termed cribra cranii ex-
terna, symmetrical osteoporosis, osteoporotic pit-
ting, and spongy hyperostosis) is an increase in the
cranial diploe at the expense of the outer table,
resulting in a thinning and porosity of the cortex
(Moseley, 1966; Steinbock, 1978; Ortner and Put-
schar, 1985; Stuart-Macadam, 1985; Walker, 1985;
Hershkovitz et al., 1997). It is characterized on ra-
diographs by a hair-on-end appearance, and can
also take the form of cribra orbitalia, i.e., orbital roof
*Correspondence to: Deborah E. Blom, Department of Anthropol-
ogy, University of Vermont, Williams Hall 508, Burlington, VT 05405-
0168. E-mail: Deborah.Blom@uvm.edu
Received 17 December 2002; accepted 16 September 2003.
DOI 10.1002/ajpa.10431
Published online 19 November 2004 in Wiley InterScience (www.
interscience.wiley.com).
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 127:152169 (2005)
2004 WILEY-LISS, INC.
lesions that are widely recognized as an early ex-
pression of porotic hyperostosis (Hengen, 1971; Cy-
bulski, 1977; Lallo et al., 1977; Stuart-Macadam,
1985, 1989; Walker, 1985). Numerous causal factors
have been suggested for porotic hyperostosis, includ-
ing syphilis, rickets, scurvy, anemia, toxins, and
pressure from binding or carrying (Williams, 1929;
Angel, 1966; Moseley, 1966; El-Najjar, 1976; Stein-
bock, 1978; Ortner and Putschar, 1985; Stuart-Mac-
adam, 1985; Walker, 1985; Hill and Armelagos,
1990; Hill, 2001). However, most researchers cur-
rently agree that porotic hyperostosis is the osseous
evidence of marrow hyperplasia (references
throughout; but see Ortner et al., 1999, 2001;
Schultz, 2001).
Marrow hyperplasia is a response to several pos-
sible conditions, including acquired and genetic ane-
mia, as well as other rare conditions that ultimately
result in hypoxia (low oxygen saturation of arterial
hemoglobin; Moseley, 1966; Hengen, 1971; Cybul-
ski, 1977; Lallo et al., 1977; Mensforth et al., 1978;
Steinbock, 1978; Ortner and Putschar, 1985; Stuart-
Macadam, 1985, 1989; Walker, 1985; Hill and
Armelagos, 1990). In these situations, the body re-
sponds to decreased oxygen levels by increasing its
production of red blood cells (erythropoiesis) and
large immature cell precursors. When the increase
in production is marked, marrow cavity expansion
occurs in order to accommodate diploe proliferation.
Children under 4 years of age produce red blood cells
in all available marrow and have greater bone plas-
ticity, so the pressure produced by red marrow hy-
perplasia in these cases may result in erosion of the
cranial vault cortex, causing porotic hyperostosis.
Therefore, in the case of children, marrow hyperpla-
sia can manifest itself in bone, while bony evidence
is less common in adults. The presence of porotic
hyperostosis in adults is almost always in a healed
state and indicates that the individual experienced
marrow hyperplasia in childhood.
Marrow hyperplasia and its potential skeletal
manifestation, porotic hyperostosis, result from var-
ious disease processes. In rare cases, cyanotic con-
genital heart disease, renal osteodystrophy, heredi-
tary spherocytosis, or dystrophic myotonia are
possible causes (Angel, 1966; Moseley, 1966; Stein-
bock, 1978; Ortner and Putschar, 1985; Stuart-Mac-
adam, 1989). More commonly, genetically inherited
forms of anemia, such as thalassemia and sickle-cell
anemia, are implicated. These often present sepa-
rate and distinctive bony changes that involve the
face and/or long bones (Diggs et al., 1937; Moseley,
1966; Steinbock, 1978; Ortner and Putschar, 1985;
Hershkovitz et al., 1997). However, congenital ane-
mia probably did not occur in the New World until
after contact with the malaria-adapted populations
of the Old World (Rucknagel, 1966; but see Zaino,
1967), and skeletal cases generally do not show the
facial and postcranial involvement characteristic of
the congenital conditions (e.g., for Peru, Hrdlicka,
1911, 1914; see also Moseley, 1966). Therefore, pre-
contact cases of porotic hyperostosis in the New
World probably do not result from genetically inher-
ited anemia, but are more likely the result of ac-
quired iron-deciency anemia (but see Schultz,
2001). To further support this, Benfer (1990) showed
the relation expected between iron content in bone
and the presence or absence of anemia in children
and adults.
The effect of iron-deciency anemia on life can be
dramatic. Maternal anemia is associated with ele-
vated pre- and postnatal infant mortality (Walker,
1985; Bharati and Basu, 1990). After infancy, grow-
ing children are also very susceptible to anemia
(Saddi and Schapira, 1970; Canadian Department of
National Health and Welfare, 1973; Dallman et al.,
1980; Ryan, 1997). For those children who survive
with anemia, social engagement and productivity
may be quite limited. A carefully controlled study of
modern American children showed that children
who have anemia are less alert, active, responsive,
and goal-directed; they have shorter attention spans
and speak less (Lozoff, 1988). Cognitive and motor
functions may also be altered in adolescents and
adults. Minimally, work productivity is reduced.
Potential causes of iron deciency are numerous.
They consist of maternal anemia affecting infant
iron stores, increased iron needs during growth, low
dietary intake, inhibited iron absorption, infectious
disease processes, and parasite load. Although many
researchers argued for a multifactorial approach
(Hengen, 1971; Cybulski, 1977; Mensforth et al.,
1978; Goodman, 1994; Holland and OBrien, 1997;
Buckley, 2000), there is disagreement over the im-
portance of the role of each of these factors (e.g.,
Stuart-Macadam, 1985, 1989; Walker, 1986; Stuart-
Macadam and Kent, 1992). Broad comparative stud-
ies of regions with diverse environments and corre-
spondingly different human diets and disease will
aid in our evaluation of these assertions. The An-
dean coast provides an excellent setting for such
initiatives because of its extreme aridity and docu-
mented variation in marine- and maize-based diets
over space and time.
The Peruvian coast is best characterized as desert
dissected by approximately 50 small rivers carrying
runoff from Andean mountain ranges. These water-
ways form narrow oasis zones and provide water for
irrigation agriculture. Their ow varies seasonally,
based on volume of highland Andean rainfall. The
most striking latitudinal differences seen as one
moves from north to south along the coast toward
the Atacama Desert of northern Chile are reduced
water availability and increased ruggedness, with
rivers etched more deeply into landscapes to the
south. While some southern areas, such as the Ica
Valley, have large plains abutting the rivers, scar-
city of water limits agricultural intensication. Al-
though water is less scarce in central Peru, coastal
shelves are not as expansive. Northern areas are
less arid with the broadest valleys, and are therefore
more agriculturally productive than those in the
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 153
south. Additionally, along the entire coast, altitude
increases with distance from the shoreline. Varia-
tions in environment have implications for blood
iron levels because of differential support of para-
sites and other disease vectors, as well as amount of
arable land.
Varying dietary patterns along the coast have im-
portant implications for the study of anemia. An-
cient coastal agriculture consisted of peppers,
squash, beans, and fruits, as well as maize, which
was often a prominent dietary staple during the
time periods represented in this study (Wilson,
1999). In addition, the Peruvian coast contains the
richest aquatic biomass in the Pacic Ocean (Mose-
ley, 1992, p. 47) and provides easily accessible ma-
rine resources year-round, including sh, algae,
shellsh, sea animals, shore birds, and salt (Mose-
ley, 1975). While the food supply is generally pre-
dictable and abundant, el Nin o events can cause
destruction of some marine plants and animals as
well as terrestrial resources (Wilson, 1981). Such
natural catastrophes render lifeways fragile and
leave people more susceptible to anemia due to pro-
tein-calorie malnutrition (Walker, 1986). El Nin o
events have also been associated with ancient evi-
dence of porotic hyperostosis in the Andes (Farnum,
2002).
Because an association between anemia and ma-
rine- and/or maize-based diets has been demon-
strated in other areas (see below), the degree to
which diets are based on these resources has impor-
tant implications for the prevalence of iron de-
ciency. Although environmental variables suggest
less dependence on maize and more emphasis on
marine resources toward the south, socioeconomic
factors can often be more signicant in determining
diet in any particular temporal and spatial context.
Therefore, the relationship between diet and anemia
can be best explored through Ba/Sr ratios or stable
isotope analyses. These analyses can provide a mea-
sure of food consumption far more precise than other
forms of ecological or archaeological data (Sandness,
1992). By offering a broad-based regional survey of
anemia in the western lowland area of Peru, our
study furthers the understanding of porotic hyper-
ostosis and its etiology in the Americas during pre-
Columbian times, thus illuminating the types of con-
texts (both environmental and social) that are
associated with elevated or decreased rates of po-
rotic hyperostosis and, by inference, childhood ane-
mia.
MATERIALS
The study sample includes 1,465 individuals: 512
from Peruvian collections housed at the Field Mu-
seum of Natural History (FMNH) in Chicago, and
953 from systematically excavated contexts from
Moquegua, Peru. The FMNH sample, which was
amassed during late 19th and early 20th century
museum-supported excavations in Peru, is sizeable
and covers a broad geographical area across western
Peru (Dorsey, 1894; Kroeber and ONeale, 1926
1937; Kroeber and Collier, 1998; Schreiber, 1998)
(Table 1). A previous study of anemia in a portion of
this collection (El-Najjar, 1976) was part of a grand
synthesis of the presence of anemia in the New
World. The present subdivides the collection accord-
ing to provenience data.
The FMNH collection is well-documented spa-
tially, so it can be used to anchor regional analyses
of anemia in the Andes. The sample includes re-
mains interred in 29 sites spanning 11 valleys along
the coast of Peru, from Lambayeque in the north to
Nasca in the south. Because the samples by site are
relatively small, data are analyzed by valley here. In
order to explore latitudinal variation more fully,
valley localities are grouped into broader north/
south geographical areas, following the traditional
categories of North (including North and Far
North), Central (including North Central, Cen-
tral, and South Central), and South (including
South and Far South) (Bennett and Bird, 1949;
Willey, 1971; Lumbreras, 1974), as illustrated in
Figure 1.
Chronological control is currently available for a
portion of the FMNH collection, and time periods
represented include the Early Intermediate Period
(ca. 200 BCAD 600), Middle Horizon (ca. AD 600
1000), and Late Intermediate Period (ca. AD 1000
1476). Temporal contexts were derived from notes
on le at FMNH. Although some individuals could
be dated more accurately (e.g., early or late Early
Intermediate Period), sample sizes required that
these broader categories be used. Furthermore,
some temporal contexts overlapped broad catego-
ries, and hybrid categories were created where nec-
essary (e.g., Early Intermediate Period/Middle Ho-
rizon).
Demographic data on le at the FMNH (Konigs-
berg, no date) indicate a bias toward adult males in
this collection. Of the identiable specimens, there
are almost twice as many males as females. This
imbalance is likely the result of collection practices
or biases in pre-Columbian burial practices rather
than from osteological assessments. Additionally,
the majority (86.9%, N 513) of individuals in the
FMNH collection were 10 years old at time of
death, and some juvenile remains were reportedly
abandoned in the eld without any reason stated
(Kroeber, no date).
Little chemical dietary information is available for
the FMNH collection. Stable isotope studies are
available from the Nasca Valley, which is in the
South coast region (Kennedy and Carmichael, 1991,
as cited in Kroeber and Collier, 1998, p. 2223).
Analyses reveal that Nasca Valley diets were largely
comprised of maize, and marine resources played
no special role. Therefore, the Nasca Valley sample
will allow us to explore the effects of a heavily
maize-based diet.
Recognizing the limitations of the FMNH skeletal
sample and the need for extended regional coverage,
154 D.E. BLOM ET AL.
this study also includes recent data collected from
systematically excavated contexts from the Osmore
drainage of Moquegua, Peru. The Osmore drainage
includes the Ilo and Moquegua Valleys and is lo-
cated in the Far South region of coastal Peru. Site
locations are illustrated in Figure 2. D.E.B. collected
data on 361 individuals from the Chen Chen site,
which dates to the Middle Horizon Tiwanaku Period
(ca. AD 5001150). In addition, recent studies pro-
vide data for temporal and ne-scale spatial compar-
isons. Burgess (1999) studied three Chiribaya Mid-
dle Horizon/Late Intermediate Period (ca. AD 600
1300, Lozada Cerna and Buikstra, 2003) samples
from San Geronimo, Chiribaya Alta, and El Yaral
(N 444), and Williams (1990) conducted investi-
gations at the Late Intermediate Period site of Es-
tuquin a (N 138) (see also Buikstra, 1995). A study
by Tung (2003) of a Middle Horizon Majes Valley
site, La Real, just north of the Osmore drainage and
60 km inland, provides additional data. Interob-
server error studies are not available, so the Chen
Chen data are emphasized in comparisons with the
FMNH sample.
The sites in the Osmore drainage range from sea-
coast to mid-altitude portions of the Moquegua Val-
ley, and extensive isotopic studies undertaken by
Tomczak (2001) indicate that the diets of inhabit-
ants varied from almost entirely marine-based to
heavily maize-based (see also Sandness, 1992). The
Chiribaya site closest to the Pacic Ocean is San
Geronimo. The site is located directly on the coast,
200 m from the ocean. Those buried at San
Geronimo were identied as sher people (pescado-
res) through artifactual and other analyses (Lozada
Cerna and Buikstra, 2003). Dietary protein was pri-
marily derived from marine sources.
Chiribaya Alta is a complex, multicemetery site,
with little residential area, located 6.5 km from the
Pacic Ocean. Diets varied through time and across
cemeteries. Overall, the food base consisted of a
signicant amount of marine foods, but slightly less
than that from San Geronimo. Some individuals
supplemented their diets with C
4
plants, likely
maize. Artifactual and isotopic analyses indicate
that those buried at Chiribaya Alta were both sh-
ermen and agriculturalists, and some cemeteries
were conned to economic specialists of one type or
another. Although the data by Burgess (1999) on
childhood anemia did not report separately on these
cemeteries, future studies might explore intrasite
analyses.
The third Chiribaya site, El Yaral, is located 50
km from ocean at 1,000 m above sea level, and was
composed of domestic and administrative contexts
and two cemeteries. On the basis of artifactual and
other analyses, Lozada Cerna and Buikstra (2003)
TABLE 1. FMNH study sample (total N 512)
1
Coastal area Valley
Site (sample size; N per sector/cemetery,
noted where available)
Temporal
context
North Coast, N 12, MH/LIP La Leche Tu cume (N 1; Purgatorio) LIP
Lambayeque Huaca Chotuna (N 1)
Viru Huaca Santa Clara (N 3) LIP
Purpur (N 1) LIP
Taitacaltin (N 6) MH/LIP
Central Coast, N 325, MH/LIP Ancon Ancon (N 156) MH/LIP
Near Ancon Sierra Gorda (N 10)
Chancay Chancay (N 10) LIP
Chillon Ma rquez (N 42)
Lima/Rimac Aramburu (N 107)
South Central Coast, N 64, EIPLIP Can ete Cerro Azul (N 10; 3-Pyramid H; 6,
Quebrada 2)
EIP/LIP
Cerro del Oro (N 52; 25- A; 2, B; 1- C;
1- C-D; 6-near C; 6- F; 5- above F; 3-
NE; 1- east of walled cemetery)
MH/LIP
San Beni (N 2)
South Coast, N 111, EIPLIP Pisco Cabeza Larga (N 8)
Cerro South of Puntilla (N 2)
Nazca Agua Santa (N 4) EIP/MH
Aja (7- A; 1- B) (N 8) EIP
Cahuachi (N 20; 7- A; 1- G; 2, O) EIP/MH
Cahuachi South (N 5)
Cantayo (N 15; 2- Ca; 3- Cax; 3- Cb;
2- D; 1- L; 1- M)
EIP/MH/LIP
La Estaqueria (N 1) MH
La Huayrona (N 3) MH
Las Trancas (N 2)
Majoro Chico (N 17; 10- A; 4- B) EIP/MH
Nazca (N 2)
Ocongalla (N 8; 2- west; 4- zero) EIP
Pangaravi East (N 1)
Paredones (N 2) MH
Soisongo (N 13; 1- A; 3- B; 6- C; 1- D) EIP/MH/LIP
1
EIP, Early Intermediate Period; MH, Middle Horizon; LIP, Late Intermediate Period.
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 155
Fig. 1. Study area.
Fig. 2. Osmore drainage sites (Moquegua/Ilo Valley).
156 D.E. BLOM ET AL.
argued that those buried in this site were agricul-
turalists. Supporting this, the diet at El Yaral was
primarily terrestrial. Artifactual and isotopic anal-
yses indicate evidence of exchange between these
three Chiribaya sites. Further, studies of DNA (Hay-
don, 1992) and epigenetic traits (Lozada Cerna,
1998; Tomczak, 2001; Lozada Cerna and Buikstra,
2003) indicate no signicant biological distance be-
tween the Chiribaya burial samples.
The Chen Chen site is located in the middle Mo-
quegua Valley at 1,4741,530 m above sea level
(Vargas, 1988; Blom, 1999). Approximately 300 km
southwest of the capital of Tiwanaku, which is near
Lake Titicaca in Bolivia, the Moquegua middle val-
ley is the region of most extensive and intensive
Tiwanaku inuence outside of the altiplano high-
lands (Goldstein, 2000). Carbohydrates in the Chen
Chen diet are predominately maize, while protein is
overwhelmingly from terrestrial resources (likely
camelid and guinea pig; Sandness, 1992; Tomczak,
2001). The presence of manos and metates through-
out the site indicates that maize was being ground
there, but the absence of signicant dental attrition
suggests that the inhabitants were preparing it for
export (Blom et al., 2003). Altiplano, lacustrine, and
coastal resources were virtually absent in the diet.
However, based on diet, a very small number of
individuals may have been altiplano in origin (Tom-
czak, 2001). Additionally, biodistance analyses by
Blom (1999) and Lozada Cerna (1998) revealed that
individuals from Chen Chen are more closely related
to altiplano residents than to people from the
Chiribaya sites or earlier Moquegua occupations.
Estuquin a is an inaccessible, fortied site, located
just up valley from the site of Chen Chen, and is
associated with the Late Intermediate Period Estu-
quin a culture (Stanish and Rice, 1989; Williams,
1990; Buikstra, 1995). Those buried at Estuquin a
were found to be genetically distinct from Chiribaya
populations (Tomczak, 2001). Isotopic values for the
site of Estuquin a were intermediate between the
Chiribaya sites and Chen Chen, and reected a sig-
nicant portion of terrestrial resources. These ter-
restrial resources are generally varied compared to
the Chen Chen sample, and unlike Chen Chen, some
lacustrine and marine resources were present in the
diet. Thus, the data presented here can be used to
compare anemia prevalence with maize- vs. marine-
based diets, both of which have been implicated in
the etiology of childhood anemia.
The most extensive archaeoparasitological studies
to date have been carried out on Far South Chirib-
aya sites and have established that terrestrial and
marine-borne parasites were affecting Chiribaya in-
dividuals to some degree (Martinson et al., 2003;
Santoro et al., 2003). Specically, Diphyllobothrium
pacicum was found to be quite high at San
Geronimo and rare at Chiribaya Alta (Martinson
et al., 2003). Additionally, Trichuris trichiura was
found in human coprolites at San Geronimo. The
other Far South sites could not be included in the
study because human coprolites were not available.
The researchers argue that the parasite load of San
Geronimo individuals was likely due to the fact that
the site was directly on the shore, and fresh water
supplies were susceptible to being contaminated by
occupations upstream.
Although direct information about parasite load is
not available for the majority of the study sample, it
is likely that terrestrial parasites are better sup-
ported in less arid areas to the north or where irri-
gation systems are well-developed. This is supported
by the fact that extensive analysis of many copro-
lites and mummies from southern Peru revealed
only two helminth species, Diphyllobothrium paci-
cum and Trichuris trichiura. In contrast, a limited
study of a small number of coprolites from the north-
ern areas revealed these two species plus Ascaris
lumbricoides and Enterobius vermicularis (Patrucco
et al., 1983). In the Osmore drainage, irrigation was
most extensive in the middle valley where Chen
Chen and El Yaral are located, because the valley is
at its widest (approximately 25 km) there. Irrigation
systems were especially elaborate during the Middle
Horizon, when Chen Chen was occupied (Williams,
1997). Estuquin a is located slightly farther up the
valley on a relatively inaccessible ridge. Irrigation
was required in this area, but the water owed from
upstream, above the relatively moist midvalley. It
should be noted that we are using cemetery samples
in this study, so we cannot be certain that individ-
uals lived where they were buried. This is especially
true of Chiribaya Alta, which seems to have been
primarily a mortuary site; however, we can use this
information along with dietary data to approximate
environmental conditions.
Acute and chronic respiratory diseases, such as
pneumonia and tuberculosis, and gastrointestinal
infections, precisely those conditions that are often
linked to the presence of other diseases (Buikstra,
1981; Buikstra and Cook, 1981), are commonly ob-
served in the Far South (Allison et al., 1981; Allison,
1984; Williams, 1990; Buikstra and Williams, 1991;
Salo et al., 1994; Burgess, 1999; Buikstra, 1999).
Buikstra and Williams (1991) argued that certain
lesions in the Estuquin a sample were very likely due
to tuberculosis, but they did not rule out the pres-
ence of an environmental mycobacterium. The sub-
sequent identication of Mycobacterium tuberculo-
sis DNA in Chiribaya remains further supports the
identication of tuberculosis within the Osmore Val-
ley (Salo et al., 1994). Similar lesions to those found
at Estuquin a were also found at each of the other
Far South sites (Burgess, 1999; unpublished obser-
vations by D.E.B.). Variable reporting practices pre-
vent comparisons between the Chiribaya, Tiwan-
aku, and Estuquin a studies. However, tuberculosis-
like lesions were signicantly more common in the
El Yaral sample than those from the two other
Chiribaya sites (Burgess, 1999, p. 146147). Bur-
gess (1999, p. 136) provided additional insight into
general health in Chiribaya society through data on
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 157
periostosis. Frequencies of periostosis were signi-
cantly different among Chiribaya sites, with per-
centages of elements affected decreasing with alti-
tude (San Geronimo, 8.45%; Chiribaya Alta, 7.97%;
El Yaral, 4.5%), a pattern similar to that found in
the archaeoparasitological data. The information
presented here has clear implications for the study
of childhood anemia in coastal Peru, and will be
discussed in more detail following the presentation
of the studys results.
METHODS
After isolating individuals from geographic local-
ities with sample sizes of 10 or more, D.E.B. exam-
ined each cranium for gross evidence of pathology.
Instances of cribra orbitalia were recorded for all
individuals with intact and visible orbits.
1
Lesions
were coded for severity, location, and state of heal-
ing. Severity was determined to be slight, moder-
ate, or severe, following methods described by
Stuart-Macadam (1985). Because some researchers
suggest that pressure from binding might result in
porotic hyperostotic lesions of the vault, orbital and
vault lesions are reported separately, since cranial
shape modication is present in many individuals
and may be linked to vault lesions (Guillen, 1991;
Farnum, 2002; Verano, 2003).
Although some studies recognize osteoporotic pit-
ting (Walker, 1985) or scattered ne foramina
(Stuart-Macadam, 1989) as porotic hyperostosis,
there is considerable disagreement about its etiol-
ogy, and this is especially the case in adults (e.g.,
Williams, 1929; Zaino, 1967; Walker, 1985). Pitting
in the absence of diploic expansion (an observation
that is not uncommon; Carlson et al., 1974; Stuart-
Macadam, 1989) cannot be considered rm evidence
of marrow hyperplasia, according to the widely ac-
cepted mechanism for the development of porotic
hyperostosis. Normal variation or other disease pro-
cesses such as scurvy or rickets (Ortner et al., 1999,
2001; Schultz, 2001) are possible explanations for
the etiology of these lesions. Since it was not possible
to use radiographic or cross-sectional studies on the
FMNH specimens, we did not collect evidence of
vault lesions on adult remains. Following proce-
dures outlined by El-Najjar et al. (1976), the demo-
graphic categories were labeled children (010
years of age at time of death) and adults (10
years of age at time of death). The comparison data
from Estuquin a and Chiribaya sites are recast,
where possible, by age category to permit compari-
son between studies.
Some researchers suggest that only juvenile ma-
terial be considered (e.g., Stuart-Macadam, 1985),
but this study includes individuals from all age cat-
egories for better estimation of the overall preva-
lence of anemia in living populations. A correlation
often exists between anemia and childhood mortal-
ity (Walker, 1986), and this correlation can vary
between populations (Wright and Chew, 1999). If
childhood anemia (or associated causes) and child-
hood mortality are correlated, the prevalence of po-
rotic hyperostosis in a juvenile mortality sample will
usually overestimate the prevalence in the living
sample. Likewise, an adult sample will be biased
toward individuals who differentially survived ane-
mia and other childhood illnesses. Inclusion of indi-
viduals from all ages is especially important in com-
parative studies, because each sample may differ in
the association between factors resulting in anemia
and the causes of childhood death, or simply in the
number of juveniles vs. adults present in the sam-
ple. Certainly it must be recognized that an acute
illness resulting in death likely will not leave bony
evidence of any accompanying acute anemia. There-
fore, through the analysis of porotic hyperostosis we
are examining more chronic childhood anemia. If
adult material and juvenile data are compared, we
can calculate the morbidity, as well as mortality,
associated with chronic childhood anemia.
RESULTS
FMNH sample
In the FMNH sample, 30.1% of the individuals
(N 465) exhibit orbital lesions. Adults demon-
strate cribra orbitalia in 23.1% of the observable
cases (N 402), all of which are in the healed form.
In contrast, 81.8% of the children (N 66) exhibit
evidence of anemia. These results are comparable to
those reported in the broad study by El-Najjar
(1976) of anemia in the Americas, which docu-
mented a 29.3% frequency of porotic hyperostosis
(77.2% of children; 22.8% of adults). Overall, there
was no signicant difference between males and
females for cribra orbitalia in the FMNH sample
(Table 2). Only 1 of 25 sites, Cerro del Oro in the
South Central coastal valley of Can ete, displayed
signicantly more lesions in females than males
(66.7% vs. 8.3%; N 12). The lack of signicance at
the other sites in the FMNH sample could certainly
be due to small sample sizes. Males and females
were combined in subsequent analyses.
The distribution of lesions by location in the
FMNH sample is similar to those reported by other
researchers. Vault lesions were most commonly ob-
served in the region adjacent to the lambdoidal su-
ture and on the center of the occipital squamous
(88.8%), with the remaining lesions recorded on the
parietal and frontal bones. None of the individuals
with porotic hyperostosis exhibited lesions exclu-
sively on the greater wing of the sphenoid, an indi-
cation of scurvy (Ortner et al., 1999). Orbital lesions
are commonly bilateral (85.8% of cases; right vs. left
cribra orbitalia: Fishers exact test, P 0.001) and
conned to the anterior orbit (83.9%). However,
1
In addition to more typical problems of preservation, the FMNH
Peruvian collection includes individuals who could not be studied due
to burial treatment, such as cotton stufng the orbits, or the presence
of soft tissue obstructing the observation.
158 D.E. BLOM ET AL.
some children have extensive lesions that affect the
entire superior half of the orbital area, sometimes
extending toward the region near the pterion.
A strong relationship is demonstrated between
the presence of orbital and vault lesions (Fishers
exact test, P 0.001). If we partition our sample by
severity, nearly two-thirds of the cribra orbitalia
was classied as slight (62%; 26%, moderate; 12%,
severe). However, when vault lesions are also
present, the severity of cribra orbitalia is twice as
likely to fall into the severe category (45.8%, slight;
30.6%, moderate; 23.6%, severe), thus supporting
the hypothesis that cribra orbitalia is an earlier
expression of porotic hyperostosis (Hengen, 1971;
Stuart-Macadam, 1989), and suggesting that porotic
hyperostosis as recorded here cannot be easily dis-
missed as being caused by cranial shape modica-
tion.
Age-stratied analyses reveal that the presence of
porotic hyperostosis or cribra orbitalia is highest in
children (see above) and signicantly different from
that in adults (Fishers exact test, P 0.001). How-
ever, when children are grouped by age, as sug-
gested by Mensforth et al. (1978), the distributions
are not signicantly different (Table 3). The lack of
signicance might be explained by the small sample
size in some categories (e.g., only one individual less
than 6 months of age).
When the FMNH data are partitioned by valley,
signicant differences are seen in the presence of
cribra orbitalia and lesions in children (Table 4).
Because the number of cells with missing data was
high, the sample was grouped by coastal areas
(North, Central, South Central, and South; Table 5).
Since the low prevalence of lesions noted in the
North (9.1%, N 11) cannot be considered signi-
cant until a larger sample, including children, is
studied, statistical analyses excluded the small
North coastal sample. Analyses demonstrate signif-
icant differences between coastal areas for all lesion
types in adults and children. Individuals from the
South coast had signicantly fewer lesions than
those from the Central and South Central coast.
Differences in the association between childhood
mortality and anemia in each of the geographical
areas also vary. This relationship can be seen by
calculating the ratio of lesion frequencies between
adults and children. Statistically, these can also be
seen by calculating Fishers exact test for the asso-
ciation between the expression of cribra orbitalia
and age at death for each region. For the Central
coast inhabitants, the difference between cribra or-
bitalia lesion frequencies in those who died in child-
hood vs. adulthood is 3.5:1 (80.9%:23.1%; Fishers
exact P 0.001). This is much higher than the 1.4:1
(50%:37%) ratio reported for the earlier (ca. 5800
2700 BC) Central coast site of Paloma (Benfer, 1990;
Farnum, 2002, and personal communication). Com-
parable data from the North coast also reveal a
relatively low 1.8:1 (23%:13%) ratio from the Late
Intermediate Period (ca. AD 1100) Sica n cemetery
associated with Huaca Cao Viejo at the El Brujo
complex in the Chicama valley (Farnum, 2002, and
personal communication), but the effect of interob-
server differences between this and the present
study is unknown. In the FMNH South Central and
South samples, the ratios between children and
adults with lesions are 2.1:1 (75%:35.2%; Fishers
exact P 0.052) and 2.2:1 (37.5%:16.7%; Fishers
exact P 0.162), respectively. Therefore, data from
the FMNH sample indicate that Central coast chil-
dren with chronic anemia had a lower chance of
surviving until adulthood. Children living in the
South and South Central coast areas were almost
twice as likely to survive with anemia.
In an attempt to explore the association between
temporal context and childhood anemia, the data
were partitioned by time. Table 6 presents the
FMNH sample by area for which temporal data are
available. Unfortunately, temporal and spatial data
are greatly confounded because of collection biases,
TABLE 2. Cribra orbitalia by sex by site (FMNH
individuals of known sex)
1
Site Female Male
Huaca Santa Clara 0% (N 2) 0% (N 1)
Purpur 0% (N 1) (N 0)
Taitacaltin 0% (N 1) (N 0)
Ancon 8.9% (N 45) 15.5% (N 58)
Sierra Gorda (N 0) 14.3% (N 7)
Chancay 0% (N 2) 60.0% (N 5)
Ma rquez 20.0% (N 5) 22.2% (N 9)
Aramburu 23.1% (N 13) 25.6% (N 39)
Cerro Azul 33.3% (N 3) (N 0)
Cerro del Oro* 66.7% (N 12) 8.3% (N 12)
Cabeza Larga (N 0) 20.0% (N 5)
Agua Santa 0% (N 2) (N 0)
Aja 100% (N 1) 25.0% (N 4)
Cahuachi 0% (N 2) 16.7% (N 6)
Cahuachi South (N 0) 0% (N 3)
Cantayo 0% (N 1) 25.0% (N 4)
La Estaquer a (N 0) 0% (N 1)
La Huayrona 0% (N 2) 0% (N 1)
Las Trancas (N 0) 0% (N 1)
Majoro Chico 33.3% (N 3) 25.0% (N 4)
Nazca 0% (N 1) (N 0)
Ocogalla 0% (N 1) 0% (N 1)
Pangaravi East 0% (N 1) (N 0)
Paredones (N 0) 0% (N 1)
Soisongo 0% (N 2) 0% (N 2)
Total** 19.0% (N 100) 18.9% (N 164)
1
Statistics only reported for sites in which there was a signicant
difference and for sample as a whole.
* P 0.0094, Fishers exact test.
** P 1.000, Fishers exact test.
TABLE 3. Porotic hyperostosis and cribra orbitalia
lesions by age range (FMNH sample)
1
Age range Present
0.5 years 0% (N 1)
0.51.0 years 100% (N 2)
1.02.0 years 66.7% (N 6)
2.03.0 years 100% (N 13)
3.05.0 years 77.8% (N 9)
5.010 years 80.0% (N 35)
Total 81.8% (N 66)
1
Kruskal-Wallis test exact P 0.1166.
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 159
as shown by Fishers exact tests indicating a high
association between area and time periods repre-
sented in the collection. When the presence of ane-
mia was viewed by time period, a clear trend of
increasing frequencies of lesions over time can be
seen, as shown in Table 7. However, the only signif-
icant difference between temporal context and evi-
dence of childhood anemia was present in adults
with (healed) cribra orbitalia. Because multiple
analyses were run and the temporal and spatial
TABLE 4. Porotic hyperostosis and cribra orbitalia by valley (FMNH sample)
1
Coastal area Valley
Cribra
orbitalia
(010 years)*
Cribra
orbitalia
(10 years)**
Porotic
hyperostosis
(010 years)***
Any lesions
(010 years)****
North coast La Leche N 0 0% N 0 N 0
N 1
Lambayeque N 0 0% N 0 N 0
N 1
Viru N 0 11.1% N 0 N 0
N 9
Central Coast Ancon 81% 16.1% 75% 90.5%
N 21 N 118 N 20 N 21
Near Ancon N 0 20% N 0 N 0
N 10
Chancay N 0 40% N 0 N 0
N 10
Chillon 100% 23.1% 83.3% 100%
N 12 N 26 N 12 N 13
Lima/Rimac 64.3% 31.5% 71.4% 78.6%
N 14 N 89 N 14 N 14
South Central Coast Can ete 75% 35.2% 87.5% 88.9%
N 8 N 54 N 8 N 9
South Coast Pisco N 0 20% N 0 N 0
N 10
Nazca 37.5% 16.2% 33.3% 33.3%
N 8 N 74 N 9 N 9
1
Fishers exact tests for all data.
* P 0.0182.
** P 0.0721.
*** P 0.1095.
**** P 0.0015.
TABLE 5. Porotic hyperostosis and cribra orbitalia by coastal area (FMNH sample)
1
Lesion (age) North Coast Central Coast South Central Coast South Coast
Cribra orbitalia (010 years)* N 0 80.9% 75% 37.5%
N 47 N 8 N 8
Cribra orbitalia (10 years)** 9.1% 23.1% 35.2% 16.7%
N 11 N 253 N 54 N 84
Porotic hyperostosis (010 years)*** N 0 76.1% 87.5% 33.3%
N 46 N 8 N 9
Any lesions (010 years)**** N 0 89.6% 88.9% 33.3%
N 48 N 9 N 9
1
Fishers exact tests for all data.
* P 0.0369.
** P 0.0451.
*** P 0.0210.
**** P 0.0014.
TABLE 6. Individuals available in for each area by time (FMNH sample)
1
Time period North Central South Central South Total
Early Intermediate Period N 0 N 0 2.0% 52.9% 12.8%
N 1 N 37 N 38
EIP/MH N 0 N 0 N 0 8.6% 2.0%
N 6 N 6
Middle Horizon N 0 N 0 58.8% 32.9% 17.8%
N 30 N 23 N 53
MH/LIP 54.5% 94.0% N 0 1.4% 54.7%
N 6 N 156 N 1 N 163
Late Intermediate Period 45.5% 6.0% 39.2% 4.3% 12.8%
N 5 N 10 N 20 N 3 N 38
1
Fishers exact test, P 0.0001. EIP, Early Intermediate Period; MH, Middle Horizon; LIP, Late Intermediate Period.
160 D.E. BLOM ET AL.
contexts are so confounded, the validity of this ob-
servation cannot be certain. Furthermore, multivar-
iate analyses will not provide additional insight into
these data, due to strong area and time interactions
along with empty cells and missing data.
Overall, in the FMNH samples, latitudinal pat-
terning displays higher frequencies of childhood
anemia in the Central and South Central samples.
However, childhood anemia is associated with child-
hood mortality almost twice as often in the Central
coast sample as compared to the South and South
Central collections. Because of the nature of the
data, the signicance of the observed trend of in-
creasing lesion frequency over time cannot be as-
sured.
Far South sample
Table 8 depicts the summary data for Far South
samples. At Chen Chen, 57.4% (N 115) of children
(010 years) displayed cribra orbitalia, while 71.6%
(N 155) had porotic hyperostosis. The percentage
of adults with cribra orbitalia lesions was 39.2%
(N 181). These values are distinct from those
reported by Tung (2003) at the Middle Horizon
Majes Valley site, La Real, where 21.8% of adults
(N 64) displayed cribra orbitalia. Among La Real
subadults, 64% (N 25) displayed cribra orbitalia,
and 50% (N 12) showed porotic hyperostosis. Val-
ues for the Chen Chen sample are higher than the
FMNH South coast sample for lesions in children,
but lower than those reported for the Central and
South Central samples. However, cribra orbitalia in
those dying in adulthood is lower than in the South
Central samples but higher than in the Central and
South coast collections.
Lesions are also signicantly more common in
children vs. adults in the Chen Chen sample (Fish-
ers exact test, P 0.003). However, like the FMNH
sample, no signicant difference existed between
ner age distributions of children (Kruskal-Wallis
TABLE 7. Porotic hyperostosis and cribra orbitalia by time (FMNH sample)
1
Time period
Cribra
orbitalia
(010 years)*
Cribra
orbitalia
(10 years)**
Porotic
hyperostosis
(010 years)***
Any lesions
(010 years)****
Early Intermediate Period 50.0% 16.0% 50.0% 50.0%
N 4 N 25 N 4 N 4
EIP/MH N 0 16.7% N 0 N 0
N 6
Middle Horizon 60.0% 23.8% 50.0% 50.0%
N 5 N 42 N 6 N 6
MH/LIP 81.0% 16.1% 75.0% 90.5%
N 21 N 124 N 20 N 21
Late Intermediate Period 100% 42.9% 100% 100%
N 3 N 35 N 2 N 3
1
Fishers exact tests for all data. EIP, Early Intermediate Period; MH, Middle Horizon; LIP, Late Intermediate Period.
* P 0.3504.
** P 0.0216.
*** P 0.4156.
**** P 0.0497.
TABLE 8. Porotic hyperostosis and cribra orbitalia (Far South sample)
1
Lesion/sample Age ranges Chiribaya
2
Estuquin a
3
Chen Chen Far South total
Cribra orbitalia 010 years N 0 40.0% 57.4% 51.8%
N 55 N 115 N 170
018 years* 60.5% 44.4% 58.8% 56.6%
N 152 N 72 N 131 N 355
10 years N 0 12.0% 39.2% 30.7%
N 83 N 181 N 264
18 years** 43.2% 4.5% 36.4% 36.1%
N 292 N 67 N 165 N 524
All ages 49.1% 23.2% 46.3% 44.1%
N 444 N 138 N 296 N 878
Porotic hyperostosis 010 years N 0 40.5% 61.5% 56.8%
N 42 N 148 N 190
018 years*** 51.6% 45% 63.7% 56.0%
N 153 N 60 N 171 N 384
Any lesions 010 years N 0 56.4% 71.6% 68.6%
N 39 N 155 N 194
1
Fishers Exact tests for all data.
2
Burgess (1999).
3
Williams (1990).
* P 0.0652.
** P 0.0001.
*** P 0.0154.
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 161
test exact P 0.5179). The ratio for individuals
dying with lesions in childhood vs. adulthood in the
Chen Chen sample is approximately 1.5:1 (57.4%:
39.2%). The presence of childhood anemia does not
seem to be as associated with increased childhood
mortality in the Chen Chen sample as it is in the
regions to the north represented by FMNH samples.
Also similar to the majority of FMNH results, no
signicant difference exists between females (39.4%;
N 99) and males (34%; N 53) in the presence of
cribra orbitalia at Chen Chen (Fishers exact test,
P 0.599). This is also true of the Estuquin a (Wil-
liams, 1990) and La Real (Tung, 2003) collections.
The Chiribaya results were not reported in a format
that permits sex differences in lesion frequencies to
be assessed.
Statistical analyses were undertaken to compare
the Osmore sites. Because Burgess (1999) only re-
ported lesion frequency for 018-year-olds and those
over 18 years, analyses are necessarily carried out
comparing these groups. Fishers exact tests indi-
cate that the three Far South cultures (Estuquin a,
Tiwanaku [Chen Chen], and Chiribaya) are signi-
cantly different in the presence of cribra orbitalia in
adults and porotic hyperostosis in children. Differ-
ences for cribra orbitalia in individuals who died
before 18 years of age approach statistical signi-
cance (P 0.0652). Table 9 presents the lesion fre-
quency separately for each of the three Chiribaya
sites studied by Burgess (1999).
Although a trend in the Chiribaya sites of increasing
percentages of cribra orbitalia (56.7% to 64.5%) and
porotic hyperostosis (41.9% to 58.1%) with altitude
and distance from the coast can be seen in those dying
in childhood, Burgess (1999) reported that these dif-
ferences are not statistically signicant. The percent-
age of those dying in adulthood with healed orbital
lesions is remarkably similar from site to site (42.5
45.2%). We also observe a slight increase in childhood
mortality associated with childhood anemia with alti-
tude and distance from the coast in the Chiribaya
samples (San Geronimo, 1.3:1; Chiribaya Alta, 1.4:1;
El Yaral, 1.5:1).
The collection from the Late Intermediate Period
site of Estuquin a had consistently lower frequencies
of lesions than the other Osmore samples. However,
age at death (childhood vs. adulthood) and the pres-
ence of orbital lesions are highly associated, with a
ratio of 9.9:1 (44.4%:4.5%). The same ratio calcu-
lated for Chen Chen is 1.6:1 (58.8%:36.4%). These
data demonstrate a clear increase with distance
from the coastline and altitude in childhood mortal-
ity associated with bony evidence of childhood ane-
mia. The Osmore data do not demonstrate the tem-
poral trend observed in the FMNH collection.
For comparisons, Table 10 illustrates trends in
TABLE 10. Sample comparisons
Cribra orbitalia frequency for children (010 years)
Central

South
Central

Far
South
1

South
80.9% 75% 57.4% 37.5%
Ratio of childhood mortality associated with cribra orbitalia (010 vs. 10 years)
Central

South

South
Central

Far
South
1
3.5:1 2.2:1 2.1:1 1.5:1
Cribra orbitalia frequency for children (018 years)
El Yaral Chiribaya Alta Chen Chen San Geronimo Estuquin a Nasca Valley
2
64.5% 60.4% 58.8% 56.7% 44.4% 37.5%
Ratio of childhood mortality associated with cribra orbitalia (018 vs. 18 years)
Estuquin a Nasca Valley
2
ChenChen El Yaral Chiribaya Alta San Geronimo
9.9:1 2.1:1 1.6:1 1.5:1 1.4:1 1.3:1
1
Here, Far South indicates Chen Chen sample.
2
Nasca valley data are calculated with children of ages 010 years.
TABLE 9. Porotic hyperostosis and cribra orbitalia (Chiribaya sample)
1
Lesion/sample Age ranges San Geronimo Chiribaya Alta El Yaral
Cribra orbitalia 018 years* 56.7% 60.4% 64.5%
N 30 N 91 N 31
18 years** 45.2% 42.5% 42.4%
N 73 N 160 N 59
All ages 48.5% 49.0% 50.0%
N 103 N 251 N 90
Porotic hyperostosis 018 years*** 41.9% 52.7% 58.1%
N 31 N 91 N 31
1
Chi-square analyses as reported by Burgess (1999, p. 83).
* P 0.9201.
** P 0.9195.
*** No signicant difference at 0.05 level.
162 D.E. BLOM ET AL.
the relevant Osmore and FMNH data. Data pre-
sented include cribra orbitalia frequencies for chil-
dren and the ratio of lesions in children vs. adults.
The frequencies for those with lesions dying in
adulthood are used in the calculation of ratio data.
Frequencies overall for each site are not included
because of varying numbers of children and adults
in the samples. Once again, interobserver error po-
tentially confounds comparisons between datasets.
DISCUSSION
Iron-deciency anemia is the most likely cause of
marrow hyperplasia in ancient coastal Peru, since
congenital anemias are not thought to have been
present in the New World at this time (Rucknagel,
1966). Rare causes for the condition such as cyanotic
congenital heart disease, renal osteodystrophy, and
dystrophic myotonia can be ruled out because the
frequency of porotic hyperostosis in the sample is
relatively high (Moseley, 1966; Steinbock, 1978; Ort-
ner and Putschar, 1985; Stuart-Macadam, 1989).
Polycythemia due to high-altitude hypoxia is cer-
tainly a potential problem in highland populations
of the Andes (Salzano and Callegari-Jacques, 1988).
Since this sample was collected in the coastal low-
lands, hypoxic anemia could have occurred in indi-
viduals who lived in the highlands but were buried
in the lowlands. Although evidence of such popula-
tion movement exists (e.g., Knudson et al., 2001;
Tomczak et al., 2002), the likelihood of this happen-
ing among a signicant number of children is negli-
gible. More probable causes have been posited.
A multifactorial etiology for marrow hyperplasia
in response to iron-deciency anemia is most appro-
priate (Hengen, 1971; Cybulski, 1977; Mensforth et
al., 1978; Goodman, 1994; Holland and OBrien,
1997; Buckley, 2000). In general, factors implicated
in marrow hyperplasia include physiological
changes during the life cycle, low dietary intake or
uptake, disease, infection, and parasite load. The
present study examines the following archaeologi-
cally recoverable variables independently, recogniz-
ing that interactive effects may also have been
present: sex- or gender-related differences in access
to resources and exposure to risks, diet, parasite
load, and infectious disease.
Sex- or gender-based differences
Although everyone is susceptible to iron de-
ciency, not all sectors of a population are at equal
risk. Increased stress on females during menstrua-
tion, pregnancy, and lactation increases their risk of
anemia (Bharati and Basu, 1990; Ryan, 1997). How-
ever, because porotic hyperostosis generally only
manifests itself actively in the bones of children, it is
indicative of childhood anemia. Furthermore, osteo-
logical evidence typically cannot reveal whether
anemia was overcome in childhood or persisted into
adulthood. Likewise, cases in which children with
anemia died before bony evidence was manifested or
never developed lesions cannot be differentiated
from children who never experienced anemia. How-
ever, differences in observations of lesions between
male and female adults can be informative about the
treatment of boys and girls.
Except for the site of Cerro del Oro on the South
Central coast, the data presented here indicate no
signicant difference in the frequency of lesions in
males and females dying in adulthood. No signi-
cant differentiation by sex was reported in many
other studies (e.g., El-Najjar et al., 1976; Walker,
1985, 1986; Stuart-Macadam, 1989, 1991; Williams,
1990; Tung, 2003). Since porotic hyperostosis is in-
dicative of a childhood condition, these data indicate
that there was likely no difference in exposure to
factors that resulted in anemia among boys and girls
or that, if a difference existed, differential mortality
in childhood obscured any evidence. For example,
osteological data could not be informative in situa-
tions where girls were more commonly aficted with
anemia and were more likely to die in childhood.
Likewise, the presence of higher frequencies of le-
sions in adult males could indicate either that boys
were more at risk for anemia or that they were more
likely to survive than girls were. As the results for
Cerro del Oro indicate (see also Farnum and Petch-
enkina, 1999), sex- or gender-related patterns
should be explored in each case.
Diet
Several interrelated factors determine the bodys
dietary need for iron, since nutrient uptake is never
equivalent to intake. For example, humans can more
readily access heme and ferrous iron such as that
from meat, while ferric iron derived from plants is
not as easily absorbed (Ryan, 1997). Other dietary
nutrients such as amino acids, protein, and ascorbic
acid can increase iron absorption (Wadsworth, 1975;
Mensforth et al., 1978; Steinbock, 1978; Arthur and
Isbister, 1987; Calvo and Gnazzo, 1990). Conse-
quently, diets decient in protein or certain vita-
mins (e.g., vitamin C) can limit the bodys access to
iron; thus dietary iron deciency commonly accom-
panies other types of malnutrition. Some food prep-
aration techniques increase the amount of available
iron, such as by adding ash or grinding (Walker,
1985), but the practice of adding calcium, phospho-
rous, or alkali solutions during food preparation
(e.g., soaking maize in lime) will lessen absorption
by rendering iron insoluble (Cravioto et al., 1940;
Bressani and Scrimshaw, 1958; Stahl, 1989).
In healthy situations, children are born with a
46-month supply of iron, so infants are usually
temporarily buffered from anemia (Dallman et al.,
1980; Stini, 1985; Oski, 1993). A common cause of
iron-deciency anemia in young children is a diet
lacking a sufcient amount of bioavailable iron after
initial iron stores are depleted (Ryan, 1997;
Mitchem, 1998; Ortner et al., 2001). Human milk
has a low iron concentration, and if breast-feeding is
prolonged or weaning foods are iron poor, iron de-
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 163
ciency may result (Mensforth et al., 1978; Saarinen,
1978; Siimes et al., 1984; Weismantel, 1988; Calvo
and Gnazzo, 1990). This is especially problematic
because growing children have a much greater need
for iron (Dawson and Desforges, 1958; Dallman et
al., 1980; Dallman, 1986; Ryan, 1997).
Many studies concluded that porotic hyperostosis
is much more frequent and severe in populations
that depend on maize agriculture (Williams, 1929;
El-Najjar, 1976; El-Najjar et al., 1976; Lallo et al.,
1977; Mensforth et al., 1978; Cassidy, 1980; Cohen
and Armelagos, 1984; Holland and OBrien, 1997),
since maize is low in iron and lacks phytase, the
enzyme needed to break down phytic acid (an iron-
chelating agent). Additionally, populations that rely
on both marine and agricultural resources may also
have a greater prevalence of diet-related anemia,
because the high phosphoric content of marine foods
might further reduce iron uptake (e.g., Cybulski,
1977; Lallo et al., 1977; Walker, 1986).
If anemia in a sample is principally caused by
dietary factors, there should be a correlation be-
tween frequency of anemia and reliance on a partic-
ular dietary source, as measured by stable isotope
analyses. Table 11 illustrates expectations for the
variables considered. If childhood anemia resulted
from a marine-based diet, we expect to see the high-
est percentage of individuals affected at San
Geronimo, with Chiribaya Alta and El Yaral follow-
ing in that order. Evidence of anemia in the Estu-
quin a, Chen Chen, and Nasca samples should be
negligible. On the other hand, if a maize-based diet
resulted in the anemia, samples from Chen Chen
and the Nasca Valley would have the highest repre-
sentation, with frequencies decreasing through Es-
tuquin a and El Yaral, Chiribaya Alta, and San
Geronimo. Finally, if consuming both marine foods
and maize simultaneously resulted in the highest
risk for iron deciency, sites with a mixed-resource
base such as Chiribaya Alta and El Yaral would
exhibit the greatest number of cases.
The distribution of cribra orbitalia does not sup-
port hypotheses that marine- or maize-based diets
are associated with childhood anemia. In fact, the
data indicate that in this sample, a mixed marine-
and maize-based diet is more predictive of childhood
anemia. The data comparing the ratios for individ-
uals dying with lesions in childhood vs. adulthood
can also provide insights. Those consuming more
marine resources (or buried at lower altitudes,
closer to the coastline) were most likely to survive
with childhood anemia or died very early, before any
bony evidence formed. This indicates that those bur-
ied higher in altitude and farther from the coast are
more likely to die in childhood vs. adulthood with
cribra orbitalia. It also supports suggestions by some
researchers that sher peoples invested more paren-
tal care in their offspring (Robert Benfer, personal
communication; Julie Farnum, personal communi-
cation; Benfer and Petchenkina, 1998). Differences
could also be due to differential adaptation, knowl-
edge, or access to resources that could be used to
treat childhood anemia or related causes. In order to
interpret the data further, it is necessary to explore
other factors thought to be associated with anemia.
Parasites
Bioarchaeological studies of marine-dependent
populations indicate that contaminated water
sources and sh- and sea mammal-borne parasites
can also explain the prevalence of anemia in popu-
lations that focus on marine resources (Walker,
1986; Reinhard et al., no date). Individuals with
chronic gastrointestinal conditions, causing abdom-
inal bleeding and diarrhea, are especially prone to
anemia because of blood loss and gastric mobility too
rapid for sufcient iron absorption (Gerritsen et al.,
1954; Mensforth et al., 1978; Dallman, 1986; Arthur
and Isbister, 1987). Because equivalent frequencies
of porotic hyperostosis were observed in maize- and
marine-dependent populations, parasites caused by
inadequate sanitation in agricultural settlements
may be more signicant in causing anemia than the
nutritional deciencies of a maize-based diet
(Walker, 1986; Reinhard et al., 2002).
Goncalves et al. (2003) provided a summary of
available archaeoparasitological data for the Amer-
icas. Although studies on ancient Andean parasites
are relatively rare, small numbers of pinworm (En-
terobius vermicularis), whip worm (Trichuris tri-
chiura), hookworm (Ancylostoma duodenale), and a
sh-borne parasite (Diphyllobothrium sp.) were
found in coastal Peruvian samples to the north
(Callen and Cameron, 1960; Ubelaker, 1992) and
south (Allison et al., 1974; Fouant, 1981; Martinson
et al., 2003; Santoro et al., 2003; Patrucco et al.,
1983). Fouant (1981) suggested that the reason for
the small number may be due to arid desert cli-
mates, small human population, a lack of interme-
TABLE 11. Predictions for factors related to childhood anemia
Anemia associated with diet
Marine-based: San Geronimo Chiribaya Alta El Yaral
[Estuquin a and Chen Chen]
Maize-based: [Chen Chen and Nasca] [Estuquin a and El
Yaral] Chiribaya Alta San Geronimo
Mixed maize/marine-based: [Chiribaya Alta and El Yaral]
[San Geronimo, Estuquin a, Nasca, and Chen Chen]
Anemia associated with endoparasitism
Altitude: San Geronimo Chiribaya Alta El Yaral Chen
Chen Estuquin a
Irrigation: [Chen Chen and El Yaral] [San Geronimo and
Chiribaya Alta] Estuquin a
Latitude: Central Coast South Central Coast South
Coast Far South [Chen Chen]
Anemia associated with generalized infectious disease
San Geronimo Chiribaya Alta El Yaral
See also endoparasitism predictions
Anemia associated with tuberculosis
El Yaral [Chiribaya Alta and San Geronimo]
Estuquin a ? Chen Chen
164 D.E. BLOM ET AL.
diate hosts, or an absence of archaeologically pre-
served ova. In some cases, excessively arid coastal
climates certainly can support the full life cycle of
some terrestrial parasites (e.g., Ubelaker, 1992), but
the degree to which this happens is not known. In
addition to terrestrial parasites, those who subsist
on marine resources are at risk of exposure to ma-
rine-borne parasites, especially if food is consumed
raw (i.e., ceviche) or poorly cooked.
If childhood anemia on the Andean coast is in part
due to parasites, we expect an association between
the documented presence of endoparasites and/or
risk factors and the presence of porotic hyperostosis.
Two potential expectations exist for the Osmore
drainage (Table 11). Based on the archaeoparasito-
logical data, lesion frequencies should increase with
decreasing altitude and distance from the coast, due
to marine-borne parasites and parasites carried
downstream from higher-altitude population cen-
ters. However, the fact that irrigation was well-
developed in the middle valley might also result in
elevated frequencies at the sites of Chen Chen and
El Yaral. Estuquin a would have been buffered from
both of these risks because of its location. It is dif-
cult to weigh the importance of these two con-
founded variables for the Osmore samples without
actual parasitological data for sites other than San
Geronimo and Chiribaya Alta. In the latitudinal
comparisons, if parasites were a major factor in
childhood anemia, we expect lesions to be roughly
more prevalent toward the north, since the climate
becomes less arid.
In the sample, both social and physical environ-
ments were involved if parasites were a factor in
childhood anemia. To some extent we see an in-
crease in cribra orbitalia with lower altitude in the
Osmore drainage sample, just as we see a rough
increase latitudinally toward the less arid environ-
ments to the north. However, the degree to which
irrigation systems were, or could be, developed is
also signicant. In general, the moister, irrigated
Osmore sites in the midvalley also had greater le-
sion frequencies. The sample from Estuquin a, which
is upstream, had the lowest frequencies. Conversely,
childhood mortality associated with cribra orbitalia
is more common in the Estuquin a sample, and lati-
tudinally in the least arid environments. Therefore,
where anemia was generally less common, children
with cribra orbitalia were more likely to die. The
data on childhood mortality associated with lesions
can best be explained by the last factor considered,
infectious disease.
Infectious disease
Infectious disease processes are often implicated
in the etiology of iron-deciency anemia (Lallo et al.,
1977; Mensforth et al., 1978; Dallman, 1986; Stuart-
Macadam, 1992; Stuart-Macadam and Kent, 1992;
Ryan, 1997; Buckley, 2000). During infectious bouts,
humans can become anemic for three main reasons.
First, gastrointestinal infections increase ones sus-
ceptibility to anemia in the same ways in which
macroparasites cause problems. Second, because
bacteria need iron to survive and reproduce, the
invading bacteria often temporarily decrease the
iron content of the blood. Therefore, bacterial infec-
tion can reduce individuals with barely sufcient
iron levels to an even lower, now decient state.
Third, anemia and infection are related through
anemia of chronic disease.
Some researchers argue that mild anemia may be
an adaptive response to infection, and that the hu-
man body responds adaptively to a high pathogen
load by lowering blood iron levels (Wadsworth, 1975;
Weinberg, 1984; Arthur and Isbister, 1987). Cer-
tainly, individuals who are chronically and severely
anemic are more susceptible to infection (Weinberg,
1984), but Stuart-Macadam (1991, p. 3738, 1992;
see also Stuart-Macadam and Kent, 1992) called for
a perspective that recognizes porotic hyperostosis as
an adaptation to high disease load and not necessar-
ily associated with an iron-decient diet. However,
critics of this perspective note that even mild ane-
mia cannot be described as benecial or adaptive,
especially for a growing child, and at best anemia
reects the bodys adjustment to a hostile situation
(Goodman, 1994; for a detailed discussion of the
relationship between anemia and infection, see
Ryan, 1997; Walter et al., 1997). Others state that
the evidence for the connection between anemia and
chronic disease is not sufcient to remove diet en-
tirely from the etiology of porotic hyperostosis, espe-
cially since this alternative interpretation relies
largely on studies from industrialized societies (Hol-
land and OBrien, 1997).
In truth, it may be that certain pathogens benet
from high levels of iron, at least in the case of sup-
plementation, while other pathogens likely thrive in
anemic individuals (Dallman et al., 1980; Walter et
al., 1997). However, anemia as an adaptive response
to chronic disease does not supply a satisfactory
explanation for porotic hyperostosis. Anemia as a
response to chronic infection is characterized by re-
duced erythropoiesis (Arthur and Isbister, 1987;
Walter et al., 1997). Porotic hyperostosis is not a
likely result of a case of adaptive, self-induced ane-
mia, because porotic hyperostosis is not direct evi-
dence of anemia per se, but an indicator of the bodys
attempt to overcome anemia through marrow hyper-
plasia. It indicates that the body was attempting to
correct the deciency through erythropoiesis.
Although relatively few paleopathological studies
are available for Andean South America (for an
overview, see Verano, 1997), researchers usually re-
port trends of increased pathological conditions with
sedentism (e.g., for Northern Chile, Allison, 1984;
for Ecuador, Ubelaker, 1992). At the preceramic,
preagricultural site of La Paloma on the Central
coast, health improved over time with increased
population density (Benfer, 1984, 1990). However;
overall health worsened in the terminal preceramic
and more so in the formative time period (Benfer,
ANEMIA AND CHILDHOOD MORTALITY IN ANCIENT PERU 165
personal communication; Vradenburg, 2001). In gen-
eral, we see an association between disease, sedent-
ism, and population density, especially after the pre-
ceramic period (Verano, 1992; Benfer and Farnum,
personal communication). This may be due to in-
creased social stratication and differential access to
resources accompanying sedentism (Verano, 1992).
Reinhard (1992) and Reinhard et al. (no date)
argued that the presence of parasites can be an
indirect measure for exposure to infectious disease,
because vectors are often the same. The prevalence
of infectious diseases and parasites is often affected
by the same conditions, e.g., sedentism, high popu-
lation density, and poor sanitation. Children ex-
posed to parasitic infestation may have an even
lower resistance to other pathogens, such as those
causing weanling diarrhea (Walker, 1985; Lallo et
al., 1977; Salvadei et al., 2001). Given this, we might
expect the distribution of childhood anemia to be
similar to that expected for the effects of parasitism.
Certainly, generalized infection, as measured by
periostosis, was more common with decreasing alti-
tude in the Chiribaya sites (Burgess, 1999). Because
population density and sedentism generally corre-
late positively with the availability of arable land,
we might also expect the same distribution as that
presented for parasites associated with irrigation
water. Therefore, the factors supporting high para-
site loads cannot be readily separated from those
likely to result in many other diseases. However, the
data on tuberculosis complicate the predictions.
If childhood anemia is related to tuberculosis in-
fection, we expect a different distribution from that
presented for parasitism and generalized disease. In
this case, it is expected that all the Osmore drainage
sites will have relatively high frequencies of child-
hood anemia, and that the frequency for El Yaral
would exceed those of the other Chiribaya sites.
Although we cannot make a direct comparison be-
tween the other sites for bony evidence of the dis-
ease, we might expect that tuberculosis was more
common at Estuquin a, because of the circumscribed
nature of the site. The distribution of cribra orbitalia
in Chiribaya children is similar to our predictions if
tuberculosis were a major factor in childhood ane-
mia or associated mortality. While the lesion fre-
quency at Estuquin a is the lowest, the childhood
mortality associated with anemia is highest. Addi-
tionally, the Chiribaya mortality ratios, while rela-
tively similar, also follow the expectations. So while
cribra orbitalia is less common at Estuquin a, the
children with anemia were much more likely to die.
Future research on the impact of tuberculosis on
Chen Chen populations will be helpful in further
testing this observation.
Another pattern expected in the case of any form
of infectious disease would be the presence of porotic
hyperostosis in infants under 6 months of age, when
they should be buffered by iron stores from birth
(Buikstra and Cook, 1981), although premature
birth, low birth weight, or severe maternal anemia
are other possible explanations (Dawson and Des-
forges, 1958; Dallman, 1986; Palkovich, 1987). In
the present sample, little evidence exists for anemia
in children under 6 months of age. However, the
sample size of very young individuals is exceedingly
small, especially since affected infants can easily die
before lesions are visible osteologically. A larger
sample will be needed to explore this further.
CONCLUSIONS
For the inhabitants of the Andean coastal region,
childhood anemia added an extra burden in an al-
ready harsh and demanding environment. Bioar-
chaeological analyses presented here indicate that a
majority of individuals in the mortality sample pre-
sented evidence of childhood anemia in the form of
porotic hyperostosis or cribra orbitalia. A strong as-
sociation between childhood mortality and childhood
anemia is present throughout, but no signicant
difference exists between ner age distributions
within the subadult sample. Likewise, little signi-
cant difference exists between adult females and
males in the presence of cribra orbitalia. However,
differences are established between contexts in the
overall frequency of lesions, as well as the associa-
tion between childhood mortality and anemia. In
order to help explain the patterns observed, ar-
chaeologically recoverable variables, including diet,
parasite load, and infectious disease, were studied
independently, with the knowledge that interactive
effects were probable.
Environmental stressors, such as parasites and
disease, rather than specic dietary practices were
more likely to be associated with childhood anemia
in these coastal Andean samples. Reliance on a ma-
rine- or maize-based diet was not associated with
the presence of childhood anemia. However, a mixed
marine- and maize-based diet was more predictive.
Overall, childhood anemia was more common in in-
dividuals buried in less arid environments, whether
those environments were due to natural variation in
aridity or landscapes modied through irrigation.
These factors are associated with high parasite
loads, as well as many other diseases. Water-borne
contamination from neighboring groups likely
played a part in the overall pathogen load. Addition-
ally, the distribution of cribra orbitalia in children
indicates that tuberculosis, and/or a tuberculosis-
like pathogen, was a major factor in childhood ane-
mia and/or associated mortality.
This study establishes that if data on porotic hy-
perostosis and cribra orbitalia for both children and
adults are presented separately, they reveal the rel-
ative association between childhood anemia and
childhood mortality, and allow comparisons to be
made between mortuary samples in which the pro-
portions of children and adults vary. When the data
on childhood mortality and childhood anemia were
examined, it was found that in some populations
childhood anemia was generally less common, but
individuals were more likely to die in childhood if
166 D.E. BLOM ET AL.
they had porotic hyperostosis, as compared to other
samples. This was found to be the case in areas
where tuberculosis was common and the presence of
water-borne pathogens was negligible. Those buried
at lower altitudes, closer to the coast, and consum-
ing mainly marine resources were less likely to die
in childhood with anemia. This supports suggestions
by others that sher peoples may have invested
more parental care in their offspring. Alternatively,
differences could be due to differential adaptations,
knowledge, or access to resources that could be used
to treat childhood anemia or related causes.
The study also supports the hypothesis that cribra
orbitalia is an earlier expression of porotic hyperos-
tosis, and suggests that porotic hyperostosis, as re-
corded here, cannot be easily dismissed as a result of
cranial shape modication. The presence of lesions
generally increased over time (from the Early Inter-
mediate Period to the Late Intermediate Period) in
the FMNH sample. However, the signicance of this
trend cannot be assured, due to the nature of the
data. No temporal patterns were revealed in the
Osmore data. Additional studies will be needed to
further test the hypotheses presented here. It is
hoped that this article provides regional porotic hy-
perostosis patterning in coastal Peru in such a way
that it can be used to inform these future studies.
ACKNOWLEDGMENTS
We express our extreme gratitude to Donna Nash
at the Field Museum of Natural History for collect-
ing the temporal contexts for the FMNH sample,
with assistance by Amber Stucke. Glenn Cole and
Chris Gross kindly provided access to the materials
at FMNH. Bertha Vargas excavated the remains
from the site of Chen Chen and provided contextual
information, and Antonio Oquiche and the Museo
Contisuyo staff were very supportive during the
analysis of these remains. This study would not
have been possible without the thorough disserta-
tions written by Sloan Williams and Shelly Burgess.
Likewise, Karl Reinhard was generous in providing
manuscripts that were still in press. Karl Rein-
hard, Bob Benfer, Jim Pokines, Jim Petersen, Julie
Farnum, Tifny Tung, and Christina Torres-Rouff
were extremely helpful in discussions of content and
style throughout the writing process, and Alan
Howard of the University of Vermonts Academic
Computing Services kindly provided consultation on
statistical analyses. This paper could not have been
completed without the generous help and support of
Cindy Longwell, along with the assistance of John
Anderson and Jennifer Gagnon. Finally, we thank
three anonymous reviewers and the editor of the
AJPA, Clark Spencer Larsen, who made several
helpful suggestions. Any errors are the responsibil-
ity of the authors.
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