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Representing children in excavated cemeteries: the intrinsic preservation factors.



The analysis of excavated human remains offers major rewards for archaeology and anthropology, bur is significantly affected by the preservation of the bone. Poor bone preservation inhibits the determination of age, sex, morbidity and mortality and distorts demographic profiles (Walker et al. 1988; Mays 1992; Guy & Masset 1997; Guy et al. 1997; Kamp 2001; Hopa & Vaupel 2002; Bello et al. 2002a & b, 2006; Bello 2005; Bello & Andrews 2006; Shea 2006). Poor preservation particularly affects the visibility of children in a community, even perhaps lessening the interest of anthropologists in their study (Kamp 2001; Shea 2006; Lewis 2007).

The degree of preservation depends both on extrinsic factors (the character of the terrain and type of burial) and intrinsic factors (the character of the bone). Extrinsic factors include the geological environment of a site, the nature of the local flora and fauna and human activities (Gordon & Buikstra 1981; Lambert et al. 1985; Henderson 1987; Garland & Janaway 1989; Klein 1989; Haglund & Sorg 1997, 2002; Karkanas et al. 1999; Nielsen-Marsh & Hedges 2000; Stiner et al. 2001; Tuller & Duric 2006; Smith et al. 2007; Lee-Thorp & Sealy 2008). Soil chemistry is believed to be the most influential extrinsic factor in bone diagenesis (Garland & Janaway 1989), in particular the acidity (pH value) of the local soil (Gordon & Buikstra 1981). In addition, preservation may be dependent on the burial rite (Henderson 1987; Klein 1989; Lewis 2007), and the subsequent processes of archaeological excavation, cleaning and curation (Henderson 1987; Klein 1989; Galloway et al. 1997; Tuller & Duric 2006; Lewis 2007).

Intrinsic factors have attracted less attention in preservation studies (Bouchud 1977; Von Endt & Ortner 1984; Lyman 1996; Willey et al. 1997; Bello et al. 2002, 2006; Duric et al. 2004). Authors often suggest that small size, high porosity, lower mineralisation and high organic content of children's bones make them more susceptible to taphonomic decay (Buckberry 2000; Bello et al. 2006; Lewis 2007). However, so far there has been no comprehensive study that addresses the influence of intrinsic factors on the preservation of skeletal remains of children.

In this paper we focus on how intrinsic factors influence bone survival. We use a case study to show what archaeologists can expect when excavating skeletons of children, and how to appreciate what may have been lost, given a similar terrain to that we encountered at Stara Torina.


Stara Torina is located in the lowlands of northern Serbia, near the city of Subotica. The late medieval cemetery excavated there provides our case study. The cemetery was associated with the ruins of a church dated to the period between the second half of the ninth and the eleventh century AI). Both were identified during the preparations for the building of highway E-75, and full excavation was carried out in advance of construction. In prehistoric times the area was swampy, given the vicinity of Ludosko Lake. Nowadays, although no longer waterlogged, the soil is relatively wet even during the summer and even at relatively shallow depth. In the excavation, the soil was sandy, loose, uniform and rich in humus, and there were no significant differences in soil composition across the site that could differentially affect the bones. Stratigraphically, all the burials belong to the same horizontal layer and were encountered at about the same depth below the modern day surface, generally between 0.4 and 0.8m. In the graves, skeletons were laid out horizontally, and there was direct contact with the soil (continuous infilling: Roksandic 2002). In the case of multiple graves, individuals were laid side by side, i.e. they were not in direct physical contact with other individuals in the grave. There were no coffins or grave goods.


All excavated banes were cleaned in water and dried naturally. The banes were placed in paper boxes and transported to the Laboratory for Anthropology, Institute of Anatomy, School of Medicine University of Belgrade where they have been kept ever since. The minimum number of excavated individuals estimated by the number of left proximal femora was 951. Of these, 543 were adults, 81 were adolescents and 327 were younger than 14 years of age. Age-at-death estimation followed standard osteological procedures based on the epiphyseal union method (Brothwell 1981), diaphyseal length measurement (Maresh 1955, 1970; Scheuer & Black 2000) and dental age estimation (Ubdaker 1978).

Our study focused on the immature group for which we selected only individuals with secure contexts and uneventful excavation and curation histories. There were 155 of these, 95 from individual graves, and 60 from multiple graves (minimum two individuals out of which at least one is non-adult). We classified the sample into three age-categories: the first category comprising individuals less than three years (49 individuals), the second with an age range of four to seven years (43 individuals), and the third between eight and fourteen years (44 individuals). In addition, due to their poor preservation, 19 skeletons remained un-aged.

To assess the variation of preservation through the sample, we recorded whether each bane was complete, fragmented at missing, focusing on long banes and cranial banes. We also measured the bane mineral density (BMD) using a HOLOGIC QDR 1000W bane densitometer. In order to evaluate the contribution of bane shape to the preservation, we first conducted a study to select different banes of approximately the same bane volume (measured by gauge glass), but of different shape. This was evaluated in the same individual, and was repeated in the individuals of different age to exclude the possibility of age influence.

The role of bane structure was assessed by cross-sectional analysis of un-decalcified bane samples from three different diaphyseal regions: proximal, midshaft and distal region (Figure 1). The samples were embedded in epoxy resins (Mecaprex KM-U) and were cut in transversal 100[micro]m thick bane sections using a diamond-saw microtome (Leica SP1600). In order to analyse mechanical stress (Jenkins & Khanna 2005) and locate the part of the bane most susceptible to breakage, we calculated maximum bending stress in three different transversal sections (at the middle of the diaphysis, at the proximal diaphyseal end and at the distal diaphyseal end of the bane) using the models of a simple beam and cantilever beam loaded by uniform continuous load.

The results of these tests were then analysed by age group.

Results (Tables 1-8)

Complete femurs were more common than other long banes, while there were no significant differences between the preservation of other banes (Table 1). Within the age groups, the femur and humerus were better preserved than other long banes for the youngest, while in the third age category tibia was the best preserved bane (Table 2). In the second age group, no significant difference existed in the preservation of various long banes. There was some variation between groups; for the youngest, radius, tibia and fibula were significantly less well preserved than in older age groups.


Among fragmented long bones, midshafts survived the best (Table 3), and midshaft combined with the proximal diaphyseal end had the highest percentage of preservation in the case of the ulna (44.85%), followed by the tibia (33%) and radius (30.7%). The midshaft combined with the distal diaphyseal end was the best preserved zone in the case of the fibula (42.86%).

Based on the analysis of long bone fragments (portions), we identified the position of fracture lines in particular bones (Table 4, Figure 2). It was shown that all long bones were rarely broken at the middle of the diaphysis, while the proximal diaphyseal region was the most common place of fracture in humerus, femur and fibula. On the other hand, the distal diaphyseal portion was the most common breakage point in radius, ulna and tibia.


Among cranial bones, the mandible was the most frequently completely preserved bone (23.87%) (Table 5). Although the zygomatic bone was often missing (74.19%), when present, it was the least fragmented cranial bone (8.71%). When unfused, the frontal bone was rarely preserved; when fused, our results show that it was the second best preserved cranial bone (19.35%) and was not commonly fragmented. The temporal bone was significantly less preserved than maxilla, zygomatic bone or parietal bone. Furthermore, it was less well preserved than the mandible or frontal bone, while there were no differences between other bones. However, the petrous part of the temporal bone was completely preserved in nearly one third of the cases.

Among flat postcranial bones, the ilium was the best preserved, easily reaching statistical significance over scapula, manubrium of the sternum and ischium, and over pubis (Table 6). The scapula was poorly preserved, significantly less than ischium and ilium. Sternebrae were significantly less preserved than all other flat bones (vs ilium, ischium, pubis, scapula, manubrium). The manubrium was less well preserved than ischium and ilium.

Within the majority of long bones, the midshafts were the best preserved parts. This can be attributed to the fact that the midshaft, compared to the bone ends, has a thicker cortex, and a higher amount of dense compact bone (Figure 3), resulting in higher BMD of the section (Galloway et al. 1997; Willey et al. 1997; Bello et al. 2002; Stojanowski et al. 2002). For humerus and fibula, the highest bending stress was observed for the proximal section, followed by the distal section, while in the middle of diaphysis it showed the minimum value (Table 7). Similarly, in the case of ulna and tibia, maximum bending stress was determined in the distal part, followed by the proximal part, and with minimum values at the midshaft. This indicates that a long bone in a horizontal position in the ground is most likely to break at either end.

Different shaped diaphyseal ends displayed different preservation. The proximal end of the ulna showed much better preservation than the proximal end of the humerus. This could be related to the difference in size of the surface area of the growth plate, i.e. in the ulna this surface is very small and situated only on the upper surface of the olecranon, while in the humerus, the same surface is broader and located between the humeral head and anatomical neck (Figure 4). As a consequence, the proximal end of the ulna is completely lined with compact bone except on the small surface on olecranon, while on the humerus, the large surface of epiphyseo-diaphyseal junction is not covered with compact cortical bone, which makes this largely trabecular surface more susceptible to taphonomic deterioration.

Among pairs of bones of similar size (volume) but different shape, ischium and ulna showed no significant difference in preservation, but the radius was better preserved than the similarly-sized scapula. In this context, it is likely that the significance of shape on preservation mainly depends upon the presence of some critical geometrical trait (e.g. in the case of scapula very low thickness of the subscapular fossa) much more than upon general bone shape.

The bone mineral density (BMD) of the femur was higher than that of the fibula in ali age groups (Table 8). However, the high values of BMD that we found in the femur are not exclusively the indicator of true bone tissue density (as a material property) but also of bone geometry (i.e. cross-section area and cortical thickness).


Given that the total number of preserved complete long bones in the first age group (0-3 years) was significantly lower than in the second and the third age categories, it is likely that the difference was due to small bone size. This is consistent with previous studies that showed that the bones of the youngest children were less preserved (Walker et al. 1988; Guy & Masset 1997; Guy et al. 1997; Bello et al. 2002, 2006). The bone size affects the accessibility of the bone to chemical reagents in the soil. The rate of chemical breakdown in bone is related to the proximity of a given unit of tissue to the bone surface, which causes the small bones to be less well preserved than the large (Von Endt & Ormer 1984). Archaeozoologists have suggested that the remains of young mammals are rare in the archaeological sites owing to their low bone density (Lyman 1996; Bello et al. 2002, 2006). Immature individuals have brittle bones, with low tensile and compressive strength, and in the ground they are poorly mineralised, with higher porosity and smaller crystals, presenting a large surface of attack per unit volume (Guy et al. 1997). BMD in a normal infant skeleton decreases in the first year of life and then increases through childhood and adolescence (Rauch & Schoenau 2001), so it is plausible that low BMD in the youngest age category contributed to their poor preservation in our sample. An overall trend of good preservation of dense bones with a higher ratio of cortical to cancellous bone, over small, less dense and fragile bones has been already recognised in the literature (Henderson 1987; Waldron 1987; Garland & Janaway 1989; Buckberry 2000; Stojanowski et al. 2002; Bello et al. 2006).



In our material, the mandible was the most frequently preserved complete cranial bone. Since it is a bone with a predominant compact component and a very rigid and nondeformable structure (Percac & Nikolic 1992; Van Eijden 2000), it is recognised in the archaeological literature as the most resistant bone, not only in humans (Bello et al. 2002), but also in faunal skeletal remains (Leroi-Gourhan 1964). The 'cult of the mandible' is a nice example of how previous ignorance of the intrinsic factors (as well as inexperience in interpreting their significance for bone recovery) has led to a wrong conclusion. Instead of cultural factors, the intrinsic characteristics of the mandible (its density and structure) were actually responsible for its good preservation (Leroi-Gourhan 1964). Other cranial bones of compact structure, such as the zygomatic and the pyramid of the temporal bone, were also preserved intact more often than other bones, which is in agreement with Rewekant (2001) and Ingvarsson-Sundstrom (2003).

The differential preservation of bones can sometimes hide important pathology, because the bones affected by the disease may be missing. The fact that some bones (e.g. of the skull vault) are frequently missing (or fragmented) can hamper the revelation of the pathological conditions that are usually or exclusively encountered on these specific bones. Such an example would be porotic hyperostosis or cribra orbitalia (bone signs of anaemia). Similarly, poor preservation of some bones (compared to the other bones) blurs the picture of the prevalence of bone trauma. Therefore, palaeopathological evidence will need to be subject to correction by the intrinsic bone preservation factors.

Our results may help to resolve whether observed bone fractures occurred at the time of death (perimortem) or under the ground (postmortem). Long bone fractures caused by the pressure of soil were usually recorded near either of the bone ends, which we explained by biomechanical analysis. Therefore, the finding of a fracture line in mid-diaphysis on sub-adult bones could raise the possibility of perimortem trauma.

Consideration of intrinsic variations can also qualify observed differences within a community. Assuming the whole of a cemetery population lies in the same terrain, any differences observed should be tested for intrinsic factors in the first instance. In a Christian cemetery, funeral treatments are less likely to vary (Bello et al. 2002), so that sociological causes will probably be less influential than the peculiar behaviour of infants' bones in the burial (Guy et al. 1997).

In summary, children's bones have a specific pattern of intrinsic characteristics (size, BMD, structure) quite different from that of adults'. Therefore, even when they are exposed to the same external factors as adult bones, their preservation is usually weaker (Bello et al. 2002). This commonly leads to the under-representation of children's bones (Walker et al. 1988; Guy & Masset 1997; Guy et al. 1997; Shea 2006), which distorts the demographic picture. Not only does the difference exist in intrinsic factors between the children and adults, but children themselves also show different bone preservation according to their age, so that the youngest children (under the age of 3) are less well preserved (Walker et al. 1988; Guy et al. 1997; Bello et al. 2002, 2006). The relative absence of children's bones has forced some archaeologists to practically neglect sub-adults in their work (see: Lewis 2007); however, there are others who have appreciated the significance of the problem of the 'missing children' (Walker et al. 1988; Buckberry 2000; Kamp 2001; Bello et al. 2002, 2006; Shea 2006).


The study of intrinsic factors teaches us that excavators need to be more careful during bone retrieval and should make more effort to find small bones. Bones with some particularly unfavourable intrinsic characteristic, such as small size or low density, are very susceptible to going unnoticed. Therefore, the excavation process has to be adjusted to take account of this unequal visibility.

Understanding the intrinsic factors will assist the interpretation of the skeletal assemblages in analysis. Making the necessary corrections to allow for differential survival could improve estimates of past human population profiles and redress the balance in favour of the role of children in society.


This study was supported by the Ministry of Science of the Republic of Serbia--Project 45005. Some results of the study were presented at the Fifteenth Congress of the European Anthropological Association: 'Man and Environment: Trends and Challenges in Anthropology', Budapest, Hungary, 31 August-3 September 2006. We would like to thank medical students Maria Martin Lopez from Spain and Szu-Hsuan Chen from Taiwan for their contribution during data analysis, as well as Dusan Milovanovic, mechanical engineer and professor of technical science for contributing to the analysis of bone mechanical properties. The authors are very thankful to Martin Carver for his valuable suggestions, reducing and editing the manuscript thoroughly, as well as to the reviewers of this paper (Silvia Bello and an anonymous reviewer) for very helpful suggestions which also led to significant improvement of the manuscript.

Received: 21 August 2009; Revised: 5 January 2010; Accepted: 24 February 2010


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Marija Djuric ([double dagger]), Ksenija Djukic, Petar Milovanovic, Aleksa Janovic & Petar Milenkovic *

* Laboratory for Anthropology, Institute of Anatomy, School of Medicine, University of Belgrade, 4/2 Dr Subotica, 11000 Belgrade, Serbia

([double dagger]) Author for correspondence (Email:
Table 1. Preservation of long bones (left + right)' in the whole

 Complete bone Fragmented bonne (1)
 Missing bones (2) present

Bone N % N % N %

Humerus 191 61.61 85 27.42 34 10.97
Radius 189 60.97 90 29.03 31 10
Ulna 203 65.48 74 23.87 33 10.65
Femur 172 55.48 109 35.16 29 9.35
Tibia 181 58.39 98 31.61 31 10
Fibula 207 66.77 70 22.58 33 10.65

(4) Expected number of paired bones for 155 investigated individuals
was 310.

(2) Complete bone means entire bone without epiphyses--they can be
measured for age assessment; fragmented bone means that the bone is
broken regardless of whether all fragments are present.

Table 2. Frequency of complete long bones in different age groups.

 0-3 years 4-7 years 8-14 years

Bone N % N % N %

Humerus 33 33.67 32 37.21 20 22.73
Radius 19 19.39 36 41.86 35 39.77
Ulna 24 24.49 29 33.72 21 23.86
Femur 40 40.82 37 43.02 32 36.36
Tibia 23 23.47 36 41.86 39 44.32
Fibula 14 14.29 28 32.56 28 31.82
Total 153 26.02 198 38.37 175 33.14

Table 3. Frequency of long one fragments in the whole sample.

 Humerus Radius Ulna

Bone section N % N % N %

Prox. diaphyseal end 2 7.14 0 0 2 6.89
Prox. 1/2 1 3.57 2 7.69 2 6.89
Midshaft with prox. end 2 7.14 8 30.77 13 44.85
Dist. diaphyseal end 0 0 0 0 1 3.45
Dist. 1/2 2 7.14 2 7.69 2 6.89
Midshaft with dist. end 9 32.15 6 23.08 3 10.34
Midshaft 12 42.86 8 30.77 6 20.69
Total 28 100 26 100 29 100

 Femur Tibia Fibula

Bone section N % N % N %

Prox. diaphyseal end 3 13.04 1 4.17 0 0
Prox. 1/2 3 13.04 0 0 2 7.14
Midshaft with prox. end 2 8.69 8 33.30 4 14.28
Dist. diaphyseal end 1 4.35 3 12.50 0 0
Dist. 1/2 4 17.39 0 0 1 3.57
Midshaft with dist. end 3 13.04 1 4.17 12 42.86
Midshaft 7 30.45 11 45.86 9 32.15
Total 23 100 24 100 28 100

Table 4. Position of fracture lines on the long bones.

 Bone region

 Proximal diaphyseal region
Bone (total
number) Min N (1) NO (2) Unknown (3)

Humerus (34) 21 30 10
Radius (31) 14 10 7
Ulna (33) 9 15 9
Femur (29) 10 5 14
Tibia (31) 12 8 11
Fibula (33) 21 6 6

 Bone region

 Distal diaphyseal region
Bone (total
number) Min N NO Unknown

Humerus (34) 14 11 9
Radius (31) 16 8 7
Ulna (33) 19 5 9
Femur (29) 9 7 13
Tibia (31) 19 1 11
Fibula (33) 13 13 7

 Bone region

 Middle of the diaphysis
Bone (total
number) Min N NO Unknown

Humerus (34) 2 23 9
Radius (31) 2 22 7
Ulna (33) 2 22 9
Femur (29) 4 12 13
Tibia (31) 0 20 11
Fibula (33) 2 25 6

(1) Min N--minimum number of cases with fracture at this bone region.

(2) NO--number of cases with no fractures at this bone region.

(3) Unknown--number of cases where fragments are missing and we are
not able to conclude whether a break line was present at a particular
bone region.

Table 5. Preservation of cranial bones (expected number of unpaired
cranial bones was 155, and for paired 310).

 Complete bone Fragmented
 Missing bones present bones
 N % N % N

Frontal Non fused 193 62.26 4 1.29 17 5.48
 Fused 30 19.35 18 11.61
Parietal 192 61.94 53 17.10 65 20.97
Temporal 208 67.10 33 10.65 69 22.26 (1)
Occipital 97 62.58 24 15.48 34 21.94
Zygomatic 230 74.19 53 17.10 27 8.71
Maxilla 215 69.35 54 17.42 41 13.23
Mandible 89 57.42 37 23.87 29 18.71

(1) Complete pyramid with some fragment of the squamous part.

Table 6. Frequency of flat postcranial bones (expected number of
paired bones for 155 investigated individuals was 310).

 Complete bone Fragmented
 Missing bones present bones

Bone N % N % N

Sternum Manubrium 133 85.81 19 12.26 3 1.94
 Primary sternal 562 94.30 30 5.03 4 0.67
Scapula segments (1) 191 61.61 42 13.55 77 24.84
Os coxae Ilium 181 58.39 102 32.90 27 8.71
 Ischium 228 73.55 72 23.23 10 3.23
 Pubis 237 76.45 61 19.68 12 3.87

(1) We noted a completely fused sternal body in only two cases while
in the remaining cases the body was composed of primary sternal

Table 7. Calculated values of maximum bending stresses at given long
one sections.

 Maximum bending stress
Bone Section level [N/[mm.sup.2]] (1)

Humerus Proximal diaphyseal region 86
 Mid-diaphysis 31
 Distal diaphyseal region 85

Ulna Proximal diaphyseal region 77
 Mid-diaphysis 67
 Distal diaphyseal region 353

Tibia Proximal diaphyseal region 26
 Mid-diaphysis 16
 Distal diaphyseal region 51

Fibula Proximal diaphyseal region 751
 Mid-diaphysis 103
 Distal diaphyseal region 467

Maximum bending stress for a given section was calculated for
continual load q = 1 [N/[mm.sup.2], in order to determine the level
of critical section.

Table 8. Bone mineral density (BMD) of the best and the worst preserved
long bones.

Estimated Femur Global BMD adjusted Fibula Global BMD
age (years) for bone size (g/ adjusted for bone size (g/
 [cm.sup.2]) [cm.sup.2])

2 0.268605 0.134091
3 0.33445 0.177019
4 0.278855 0.177401
5 0.322222 0.163636
G 0.314615 0.187317
7 0.339286 0.212385
8 0.286408 0.182906
9 0.274608 0.1625
10 0.297421 0.191729
11 0.267204 0.155782
12 0.287047 0.145806
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Title Annotation:Method
Author:Djuric, Marija; Djukic, Ksenija; Milovanovic, Petar; Janovic, Aleksa; Milenkovic, Petar
Article Type:Report
Date:Mar 1, 2011
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