International Journal of Osteoarchaeology

Int. J. Osteoarchaeol. (2012)

Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/oa.2282

SHORT REPORT

Vascular Grooves on Human Femora and Tibiae as a Potential Activity-related Trait

A. SOTYSIAKa*
Department of Bioarchaeology, Institute of Archaeology, University of Warsaw, Warszawa, Poland

ABSTRACT

The presence of vascular grooves on the shafts of femora and tibiae was scored for a sample of human remains from a mass burial at Tell Majnuna, Syria, dated to the early fourth millennium BCE. In the sample of 140 femora and 64 tibiae, many of which were damaged or fragmented, the grooves were most common on the femoral midshaft (31/108 = 28.7%) and on the proximal and middle shaft of the tibia (10/45 = 22.2 and 14/54 = 26.0%, respectively). For femoral midshafts, the difference in mean cross-sectional size and shape indices between bones with and without vascular grooves was checked with multivariate analysis of variance for a sample of 51 bones. The presence of grooves appeared to correspond signicantly with higher mean values of both indices. As the shape index is interpreted as an indicator of the level of terrestrial mobility and the size index may be used for sex assessment, it is possible that vascular grooves occur more frequently at the femoral midshafts of men and more active individuals, and thus they may be cautiously interpreted as another activity-related trait. Copyright 2012 John Wiley & Sons, Ltd. Key words: biomechanics; blood vessels; lower limb; terrestrial mobility

Vascular grooves are always present on the inner table of the neurocranium, although they may also appear on the external table, for example, the frontal bone (Padget, 1956). They also occur quite frequently on the shafts of long bones, especially of the femur and tibia (Hughes, 1963; Wells, 1963), and some radiographic studies note their potential for confusion with fractures (e.g. Cerezal et al., 2002; Brogdon, 2005; Dwek, 2011). However, there is a lack of medical publications dealing with their development and variability. In the bioarchaeological literature, the presence of vascular grooves is noted chiey in the context of the differential diagnosis of cut marks or tooth marks on human and animal bones (Morlan, 1984; Shipman & Rose, 1984; DErrico & Villa, 1997; DErrico et al., 1998; Haverkort & Lubell, 1999), and only a few papers discussing their variability in past human populations have been published (cf. Mller-Christensen, 1952; Wells, 1963). In human lower limbs, vascular grooves may be expected chiey on the proximal and middle shaft of
*Correspondence to: Arkadiusz Sotysiak, Department of Bioarchaeology, Institute of Archaeology, University of Warsaw, Krakowskie Przedmiecie 26/28, 00-927 Warszawa, Poland. e-mail: a.soltysiak@uw.edu.pl

the tibia where muscular branches of the anterior tibial artery are present (Keen, 1961) and on the entire shaft of the femur where three perforating arteries supply blood for thigh muscles (Massoud & Fletcher, 1997). Formation of the vascular grooves in human long bones has not been researched in detail, but it is likely that they appear during periods of accelerated growth, especially during puberty, when higher growth rates and higher bone plasticity are possible because of subperiosteal brolamellar bone expansion at that stage of ontogeny (Goldman et al., 2009). It is then possible that muscular tension together with blood pressure, where a blood vessel is adjacent to the periosteum, locally inhibits bone growth and leaves a more or less clear vascular groove on the surface of the modelled bone. If this hypothesis of vascular groove formation on long bone shafts is valid, their expression should be correlated with the intensity of muscular tension, especially during the period of puberty. It may then be expected that vascular grooves occur more frequently in individuals with higher muscle size, men and those with higher activity levels when compared with individuals of lower muscle size, women or less active people. To test this hypothesis, the presence, location and morphology of vascular grooves were noted
Received 16 June 2012 Accepted 9 August 2012

Copyright 2012 John Wiley & Sons, Ltd.

A. Sotysiak
systematically for a sample of human femora and tibiae retrieved from a mass burial of commingled human remains at Tell Majnuna in northeast Syria, dated to the rst half of the fourth millennium BCE. In the case of femora, the sample size was large enough to check the correlation between the presence of a vascular groove at midshaft and the midshaft size and shape cross-sectional indices, which are used here as proxies for sex and the level of mobility. one was selected for further analysis. However, most bones were separated. As only a small part of the site was excavated, it may be assumed that the contralateral counterparts of most bones were not retrieved. For that reason, the statistical analyses were done for all single right and left bones except those for which likely counterparts were identied. The criteria for identifying probable counterparts (separately for each deposit) were the following: (1) a difference in antero-posterior and medio-lateral diameters of 1 mm or less; (2) morphological similarity, especially in expression of the linea aspera, gluteal tuberosity and lateral fossa; and (3) a similar degree of degenerative joint disease, if observed. If two bones were identied as probably belonging to the same individual, the less complete one was rejected. If both were complete, the right one was selected for further analysis. This procedure was applied to avoid bias in case the presence/absence of vascular grooves is symmetrical, which cannot be properly veried in the sample from Tell Majnuna. As lower limb bones exhibit no clear directional symmetry (Auerbach & Ruff, 2006) and after the selection procedure each individual was likely represented by only one bone or bone fragment, bones from the right and left side were pooled together for further analyses. All of the remains present represented adult individuals. Age assessment was based on epiphyseal union andif the metaphyses were completely damaged by scavening or other taphonomic agentson morphology of the linea aspera for the femur and of the popliteal line for the tibia (Scheuer & Black, 2000). Because of the rescue-oriented nature of the excavation and restrictions in exportation of archaeological material from Syria, all human remains had to be studied in the dig house at the site and completed during the excavation season. Because the mass deposits of human remains at Tell Majnuna were heavily damaged as a result of scavenging and trampling (Sotysiak, 2010), during the rst two seasons of excavations (20062007),

Material and methods

During the 3 years (20062008) of archaeological excavations at Tell Majnuna, a small satellite mound near Tell Brak, several deposits of human remains were unearthed in a large midden dated to the Late Chalcolithic 3, c. 38003600. A contemporary cemetery was also found on top of the site. In total, the assemblages contained the remains of at least 228 individuals (Sotysiak & Chiliska-Drapella, 2009; Sotysiak, 2010; McMahon et al., 2011). The human remains dated to the period when Tell Brak emerged as a major urban centre in Northern Mesopotamia, covering more than 130 ha. As the site was located in a marginal dry farming zone, with high risk of drought, such a large urban population must have been relatively mobile to transport food from distant elds and search for alternative resources in case of insufcient crops (Sotysiak, 2010). Sometimes, it did not sufce, and it is likely that the mass deposits of human remains found at Tell Majnuna reect episodes of increased mortality because of natural or social factors. A majority of the human remains found at Tell Majnuna were commingled and disarticulated, although occasionally large portions of a single skeleton (e.g. two legs articulated with the pelvis) were also found. If both a right and left bone of one individual were found in anatomical relation, the more complete

Table 1. General distribution of vascular grooves in femora and tibiae from Tell Majnuna Position (n) Element Femur, proximal shaft Femur, midshaft Femur, distal shaft Tibia, proximal shaft Tibia, midshaft Tibia, distal shaft MNE 93 108 65 45 54 32 % 4.3 28.7 3.1 22.2 26.0 6.3 M 17 2 L 1 4 8 9 A/P/? 3 10 2 5 2 1 3 18 2 6 10 2 N-partite (n) 2 2 2 1 3 1 11 2 3

Minimum Number of Elements (MNE) counted with no side differentiation. Percent frequencies counted for each MNE separately, for example, four vascular grooves were observed on the proximal shaft of the femur for 93 elements = 4.3%. M, medial; L, lateral; A, anterior; P, posterior; ?, unknown.

Copyright 2012 John Wiley & Sons, Ltd.

Int. J. Osteoarchaeol. (2012)

Vascular Grooves on Human Femora and Tibiae

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

Figure 1. Differential diagnosis of vascular grooves: (a) vascular groove on a frontal bone, MTW 4 loc. 63, bone 21; (b) single vascular groove connected with the nutrient foramen on a right femur, MTW 4 loc. 65, bone 2.35; (c) tripartite vascular grooves on a right tibia, EM loc. 53, layer 5, bone 20; (d) carnivore tooth marks on a left tibia, MTW 4, loc. 65, bone 3.32; (e) rodent tooth marks on a right femur, EM loc. 53, layer 4, bone 46; (f) insect tunnelling on a rib, EME loc. 8, body D; (g) root etching on a left femur, EM loc. 29, layer 1, bone 18; (h) trampling, femoral fragment, EM 53, layer 2, bone 10. Scale bar 1 cm. This gure is available in colour online at wileyonlinelibrary.com/journal/oa.

Copyright 2012 John Wiley & Sons, Ltd.

Int. J. Osteoarchaeol. (2012)

A. Sotysiak
vascular grooves in femora and tibiae were noted in a non-systematic way as a differential diagnosis of taphonomic agents. Only in the last season, when it became evident that the vascular grooves were quite common, especially on larger bones, was their presence on femoral and tibial shafts systematically scored in six major deposits located in the western part of the site, namely MTW1, MTW4, EM loc. 25, 29, 32 and 53. The vascular notches were scored separately for the proximal, middle and distal portions of the shaft because most bones were damaged and fragmented, and in several cases, only one or two parts of the shaft were available for examination. The minimum number of elements for each part of the femoral and tibial shafts is presented in Table 1 and ranges from 32 (distal tibia) to 108 (femoral midshaft). The total number of examined fragments is 140 for femora (78 men and 58 women) and 64 for tibiae (24 men and 17 women). Sex was assessed using the available metric measurements for the femora and tibae, and their discriminant functions were calibrated for Mesopotamian populations (Sotysiak, 2010). Because of the limitations imposed by the rescue-oriented nature of the project, the estimation of inter-observer and intra-observer error was not possible. All of the studied deposits contained commingled human remains with many tooth marks from scavenging animals, extensive root etching and insect tunnelling as well as evidence of trampling (Sotysiak, 2010), so differentiation between vascular grooves and various taphonomic effects was crucial (Figure 1). The differential diagnosis was based on ve criteria: position and direction, linearity, margin shape, end expression and the absence of microstriations. Vascular grooves are roughly perpendicular to the shaft axis, but their slope may vary to some extent. Their length and depth are highly variable, and they are not perfectly straight like cut marks, but roughly linear, unlike root etching. Vascular grooves are U-shaped in cross section. Margins are rounded, with no signs of erosion or microfractures which are typical for cut or tooth marks and damage because of trampling. Both ends are difcult to notice, especially if the groove is shallow. Only features which met all ve criteria were scored as vascular grooves, although there is still a small possibility that some trampling-related lines mimic vascular grooves based on the criteria, especially in the case of eroded bones (cf. Olsen & Shipman, 1988; Fiorillo, 1989; Domnguez-Rodrigo et al., 2009). For each observation of a vascular groove, position of the feature (proximal, middle, distal part of the shaft; medial, anterior, lateral, posterior aspect of the shaft) was noted together with basic information about the
Copyright 2012 John Wiley & Sons, Ltd.

morphology of the groove (i.e., whether it was single, double or tripartite) (Figures 2 and 3). In the case of femora, the sample size enabled statistical analysis of correspondence between the presence or absence of vascular grooves at midshaft and the size and shape indices of the midshaft cross section. The size index was counted as the sum of antero-posterior and medio-lateral diameters and the shape index as a quotient of antero-posterior by medio-lateral diameter. The former reects the general size of the body and may be used as an effective method of sex assessment (Wescott, 2006; cf. Sotysiak, 2010), and the latter is interpreted as a proxy indicator of the level of terrestrial mobility (Holt, 2003; Wescott, 2006; Ruff, 2008). Correlation between size and shape indices was expected (cf. Wescott, 2006), so differences in their means between subsets of bones with and without vascular grooves were tested using the multivariate analysis of variance (MANOVA) with Wilks test of signicance. Homogeneity of variance was checked with the Cochran C test, and the homogeneity of covariance matrices was checked with the Box M test. Distribution patterns of vascular grooves were checked with the w2 test. All statistics were calculated using STATISTICA, version 9.0 (StatSoft, Inc, 2010).

Figure 2. Two single vascular grooves located on the midshaft of a femur. Note the evidence of root etching (black lines) between them. MTW4 loc. 65, bone 2.24. Scale bar 1 cm. This gure is available in colour online at wileyonlinelibrary.com/journal/oa.

Figure 3. Tripartite vascular groove on the midshaft of a femur. EM loc. 53.1, bone 2.19. Scale bar 1 cm. This gure is available in colour online at wileyonlinelibrary.com/journal/oa.

Int. J. Osteoarchaeol. (2012)

Vascular Grooves on Human Femora and Tibiae

Results
In total, 37 vascular grooves were observed in femora and 26 in tibiae. Their distribution in the studied sample of human remains from Tell Majnuna is shown in Table 1. In tibiae, vascular grooves were observed chiey on the lateral side of the bone, both on the proximal and middle parts of the shaft. In contrast, femoral vascular grooves were most frequent at midshaft, often close to the nutrient foramen and on the medial side of the bone. Differences in the proportion of lines per shaft region are very clear for femora (w2 = 33.5, df = 2, p near 0) and insignicant for tibiae (w2 = 5.13, df = 2, p = 0.077). Single and tripartite grooves were noted both in femora and in tibiae; double lines were much less frequent. There were no differences between the two studied lower limb bones in the proportion of single and multiple lines (w2 = 0.34, df = 1, NS). The sample size was too small to check for sex differences in the vascular groove distribution and morphology. In the studied sample, 51 femoral midshafts were preserved well enough to take medio-lateral and antero-posterior diameters. A scatterplot showing the distribution of bones with and without vascular grooves is shown in Figure 4. Because size and shape indices in the sample of human remains from Tell Majnuna as a whole demonstrated a moderate positive correlation with each other (Pearson r = 0.42, n = 102, p < 0.0001), MANOVA was used to check the relation between the presence/absence of vascular grooves and two
1.4

indices. Both the mean size and the shape indices signicantly differ between subsets of bones with and without grooves (Table 2), and in the former the difference is more signicant. The Wilks test was signicant at p < 0.01, and the Box M test value as well as the Cochran C result was insignicant for both indices, which validated the MANOVA results.

Discussion and conclusion

In the sample of human femora and tibiae from Tell Majnuna, vascular grooves are quite common although not so frequent as in the Anglo-Saxon sample studied by Wells (1963), which may just reect a different scoring method (Wells did not describe his protocol). Grooves are not randomly distributed, with an obviously higher rate on the medial side of the femur at midshaft and on the lateral side of the tibia on the proximal and middle parts of the shaft. Such a distribution is consistent with the assumption that they reect the position of the muscular branches of the anterior tibial artery, and in the case of femur, it may be specied that the second perforating artery leaves many more grooves than the rst and the third. Both in the tibia and femur, vascular grooves were single or tripartite, with many fewer cases of double grooves and no grooves with more than three notches. The sample size was only enough to check whether the presence/absence of vascular grooves is a good

1.3

1.2

Shape Index

1.1

1.0

0.9

0.8 44

46

48

50

52

54

56

58

60

62

64

66

68

70

Size Index

VG absent VG present

Figure 4. Scatterplot diagram showing relation between size index, shape index and presence/absence of vascular grooves (VG). This gure is available in colour online at wileyonlinelibrary.com/journal/oa.

Copyright 2012 John Wiley & Sons, Ltd.

Int. J. Osteoarchaeol. (2012)

A. Sotysiak
Table 2. Results of MANOVA for mean size and shape femoral indices in bones with and without vascular grooves at midshaft. VG present Index Size (AP + ML) Shape (AP/ML) n 18 18 Mean 56.3 1.10 SD 5.5 0.11 n 33 33 VG absent Mean 52.4 1.02 SD 4.2 0.10 Multiple R 0.384 0.321 F 8.46 5.62 p 0.006 0.022

MANOVA, multivariate analysis of variance; VG, vascular grooves; AP, antero-posterior; ML, medio-lateral.

predictor of cross-sectional size and shape indices for the femoral midshaft. The results are quite promising as both the mean size and the mean shape index were signicantly higher in the subsample of bones with vascular grooves. Moreover, these two effects are mutually independent. It suggests that vascular grooves are more likely to be present in larger individuals (implicitly in men) and in individuals who were more mobile on average (as reected by a higher average cross-sectional shape index). As a result, the frequency of vascular groovesat least on the femoral midshaftmay potentially be used as another proxy indicator of mobility in past human populations, especially for research on highly fragmented samples. Of course, corrections for sex, body size and other types of physical activity are necessary (Weiss, 2007; Klaus et al., 2009), and the possibility of age-related variation must be considered (Cardoso & Henderson, 2010; Milella et al., 2012). The preliminary results presented here are promising, but the potential of vascular grooves as indicators of activity-related traits needs further conrmation on larger skeletal samples with better control for sex, body size and age at death. At the present stage of research, a scoring method for further studies can be proposed. Most vascular grooves are present near the nutrient foramina of the tibia and femur, so it would be sufcient to score them only in the lateral part of the tibial shaft 4 cm above and below the nutrient foramen and in the medial part of the femoral shaft 4 cm above and below the nutrient foramen. Also, morphological observations such as the distinction between single and tripartite grooves and the metric measurements of groove length and breadth may be useful in research related to the relationship between these anatomical features and the activity patterns in past human populations. In the present paper, the differential diagnosis was based on macroscopic criteria, which in some cases can lead to inconclusive or erroneous results, especially in the differentiation between vascular grooves and trampling-related damage of eroded bones. It therefore seems appropriate to develop also a set of microscopic criteria for the differential diagnosis of vascular grooves.
Copyright 2012 John Wiley & Sons, Ltd.

The present paper reports an unexpected discovery, which was the by-product of detailed eld documentation of taphonomic effects in a peculiar sample of commingled and scavenged human remains. The sample is too homogenous, too fragmented and too small to draw any conclusions on inter-population variability or temporal changes in the number, position and/or morphology of vascular grooves. However, even if the scope of the present paper is very limited because it was based on data gathered during archaeological excavations and not in an anatomical laboratory, the observed correspondence between the presence of vascular grooves and the size and shape of the femoral midshaft cross section introduces the potential for a new perspective in the research on activity-related traits of the human skeleton.

References
Auerbach BM, Ruff CB. 2006. Limb bone bilateral asymmetry: variability and commonality among modern humans. Journal of Human Evolution 50: 203218. Brogdon BG. 2005. Radiology of the lower extremity. In Forensic Medicine of the Lower Extremity. Rich J, Dean DE, Powers RH (eds). Humana Press: New York; 113237. Cardoso FA, Henderson CY. 2010. Enthesopathy formation in the humerus: data from known age-at-death and known occupation skeletal collections. American Journal of Physical Anthropology 141: 550560. Cerezal L, del Pial F, Abascal F, Garcia-Valtuille R, Pereda T, Canga A. 2002. Imaging ndings in ulnar-sided wrist impaction syndromes. RadioGraphics 22: 105121. DErrico F, Villa P. 1997. Holes and grooves: the contribution of microscopy and taphonomy to the problem of art origins. Journal of Human Evolution 33: 131. DErrico F, Villa P, Pinto Llona AC, Ruiz Idarraga R. 1998. A Middle Palaeolithic origin of music? Using cave-bear bone accumulations to assess the Divje Babe I bone ute. Antiquity 72: 6579. Domnguez-Rodrigo S, de Juana S, Galn AB, Rodrguez M. 2009. A new protocol to differentiate trampling marks from butchery cut marks. Journal of Archaeological Science 36: 26432654. Int. J. Osteoarchaeol. (2012)

Vascular Grooves on Human Femora and Tibiae

Dwek JR. 2011. The radiographic approach to child abuse. Clinical Orthopaedics and Related Research 469: 776789. Fiorillo A. 1989. An experimental study of trampling: implications for the fossil record. In Bone Modication. Bonnichsen R, Sorg H (eds). Center for the Study of the First Americans: Orono; 6171. Goldman H, Mcfarlin S, Cooper D, Thomas C, Clement J. 2009. Ontogenetic patterning of cortical bone microstructure and geometry at the human mid-shaft femur. The Anatomical Records 292: 4864. Haverkort CM, Lubell D. 1999. Cutmarks on Capsian human remains: implications for Maghreb Holocene social organization and palaeoeconomy. International Journal of Osteoarchaeology 9: 147169. Holt BM. 2003. Mobility in Upper Paleolithic and Mesolithic Europe: evidence from the lower limb. American Journal of Physical Anthropology 122: 200215. Hughes DR. 1963. Cortical grooves on the tibia. Man 63: 149. Keen JA. 1961. A study of the arterial variations in the limbs, with special reference to symmetry of vascular patterns. Americal Journal of Anatomy 108: 245261. Klaus HD, Larsen CS, Tam ME. 2009. Economic intensication and degenerative joint disease: life and labor on the postcontact north coast of Peru. American Journal of Physical Anthropology 139: 204221. Massoud TF, Fletcher EWL. 1997. Anatomical variants of the profunda femoris artery: an angiographic study. Surgical and Radiologic Anatomy 19: 99103. McMahon A, Sotysiak A, Weber J. 2011. Late Chalcolithic mass graves at Tell Brak, Syria, and violent conict during the growth of early city-states. Journal of Field Archaeology 36: 201220. Milella M, Belcastro MG, Zollikofer CPE, Mariotti V. 2012. The effect of age, sex, and physical activity on entheseal morphology in a contemporary Italian skeletal collection. American Journal of Physical Anthropology 148: 379388. Mller-Christensen V. 1952. Case of leprosy from the Middle Ages of Denmark. Acta Medica Scandinavica 142: 101108. Morlan RE. 1984. Toward the denition of criteria for the recognition of articial bone alterations. Quaternary Research 22: 160171. Olsen SL, Shipman P. 1988. Surface modication on bone: trampling versus butchery. Journal of Archaeological Science 15: 535553. Padget DH. 1956. The cranial venous system in man in reference to development, adult conguration, and relation to the arteries. The American Journal of Anatomy 98: 307355. Ruff CB. 2008. Biomechanical analyses of archeological human skeletons. In Biological Anthropology of the Human Skeleton, Katzenberg MA, Saunders SR (eds). 2nd edn. Wiley: New York; 183206. Scheuer L, Black S. 2000. Developmental Juvenile Osteology. Elsevier: San Diego and London. Shipman P, Rose JJ. 1984. Cutmark mimics on modern and fossil bovid bones. Current Anthropology 25: 116117. Sotysiak A. 2010. Death and Decay at the Dawn of the City. Institute of Archaeology, University of Warsaw: Warsaw. Sotysiak A, Chiliska-Drapella A. 2009. Short eldwork report. Tell Majnuna (Syria), seasons 20072008. Bioarchaeology of the Near East 3: 5358. StatSoft, Inc. 2010. STATISTICA (data analysis software system), version 9.1, www.statsoft.com. Weiss E. 2007. Muscle markers revisited: activity pattern reconstruction with controls in a Central California Amerind population. American Journal of Physical Anthropology 133: 931940. Wells C. 1963. Cortical grooves on the tibia. Man 63: 112114, 180. Wescott DJ. 2006. Effect of mobility on femur midshaft external shape and robusticity. American Journal of Physical Anthropology 130: 201213.

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