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New Paleopathological Evidence of Tuberculosis in Child Skeletal Remains from Tell Aswad (8,730-8,290 cal. BC, southern Syria)

Joseph Oussama Baker, Bérénice Chamel et Olivier Dutour
p. 97-108

Résumés

Résumé. En paléopathologie, en plus des lésions osseuses typiques, l’étude des lésions secondaires ou mineures augmente le niveau de détection des pathologies dans les populations humaines du passé. Dans cette perspective, nous avons examiné les vestiges osseux du site néolithique de Tell Aswad, situé dans le Levant central (Syrie du Sud) afin de détecter des lésions attribuables à une infection tuberculeuse. Des lésions osseuses, vertébrales et endocrâniennes, ont été observées chez un jeune enfant daté du début de l’horizon PPNB. Ces lésions endocrâniennes présentent le schéma de Serpens Endocrania Symmetrica (SES) qui est attribué à la leptoméningite (méningite tuberculeuse chronique). Sur la face antérieure de quatre vertèbres thoraciques, un remodelage et un élargissement des foramens vasculaires ont également été observés, suggérant une infection tuberculeuse. Ce cas inédit constitue un nouvel indice en faveur de la présence au Levant de la tuberculose humaine dès le Néolithique dans le contexte de l’adoption de l’agriculture et de la domestication animale.

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Texte intégral

We would like to express our thanks to Danielle Stordeur, Emeritus Researcher at CNRS-Archéorient and Henri de Contenson (CNRS) for giving us the opportunity to work on the Tell Aswad material. We would like to also thank Professor Henry de Lumley director of the IPH in Paris and Amélie Vialet for providing access to the skeletal material curated in the collections.

1For a long time tuberculosis was considered as an infection originated from animals and transmitted to humans during the Neolithic, due to cattle domestication. This dogma was later challenged by phylogenetic analyses of the Mycobacterium tuberculosis complex (Brosch et al. 2002). According to this new evolutionary model, tuberculosis existed as a human infection long before the Neolithic and animal domestication and was therefore more ancient than animal tuberculosis (Gutteriez et al. 2005). A more recent alternative model proposes that animal tuberculosis is as old as human ancestry, but that the human TB pathogen postdated cattle domestication and did not emerge until 6,000 BP (Bos et al. 2014).

2The Levant has provided the earliest evidence of human tuberculosis (TB): the sites of Dja’de el-Mughara, Tell Aswad, Abu Hureyra and Tell Ain el-Kerkh in Syria (Chamel 2014; Baker et al. 2015, 2017), Atlit Yam in Israel (Hershkovitz et al. 2008) and Ain Ghazal in Jordan (El-Najjar et al. 1996), are all dated from the Pre-Pottery Neolithic B and C periods, and correspond to pre- and early animal domestication phases. The skeletal remains of a young adult from the Early PPNB/ Middle PPNB period of Tell Aswad (Syria) provided paleopathological evidence of Hypertrophic Pulmonary Osteopathy (HPO) attributed to TB, confirmed by lipid biomarkers analysis and paleoimaging study (Baker et al. 2015; Coqueugniot et al. 2015; Baker et al. 2017). The purpose of this paper is to investigate clues of tuberculosis among skeletons from the ancient phase of Tell Aswad, dating from the Early PPNB Horizon. The human remains from this period were excavated by Henri de Contenson in the early 1970s (Contenson 1972, 1992, 1995), and were not studied in our previous analyses.

Archaeological Context

3The site of Tell Aswad, located about 30 km from East-Southeast Damascus (fig. 1), was first excavated between 1971 and 1972 by Henri de Contenson. The study of lithic industry and the absolute dating by C-14 allowed archaeologists to define an ancient occupation divided into three chronological phases: phase IA, PPNA “Aswadian”; phase IB, Early PPNB; phase II, Middle PPNB (Contenson 1972).

Fig. 1 – Location map showing Tell Aswad and other Neolithic sites of Middle East with evidence of TB.

Fig. 1 – Location map showing Tell Aswad and other Neolithic sites of Middle East with evidence of TB.

4Three decades later, new excavations were conducted from 2001 to 2007 by a Franco-Syrian archaeological mission co-directed by Danielle Stordeur and Bassam Jammous (Stordeur et al. 2010). This fieldwork led to a reinterpretation of the previous chronological frame defined by Henri de Contenson. The “Aswadian culture” was discarded and three PPNB phases were proposed: the first one (phase I or “Phase ancienne”, ca. 8,650-8,300 cal. BC) representing levels B12-B9, corresponds to the Early PPNB horizon. The following period (phase II or “Phase moyenne”, ca. 8,450-8,250 cal. BC) corresponding to levels B8-B1 is also dated from the Early PPNB horizon; finally, phase III or “Phase récente” is dated from the end of Early PPNB horizon and the Middle PPNB (ca. 8,300-7,800 cal. BC) and corresponds to occupation levels B0-B5 (Stordeur et al.2010).

  • 1 J. Sánchez Priego, personal communication.

5The chronological attributions made by Henri de Contenson were reviewed, following the AMS dates obtained from emmer wheat grains of Triticum dicoccoides from the 1972 excavations at Aswad (Willcox 2005; Stordeur et al. 2010), as well as the unpublished dates of Sánchez Priego and colleagues.1 The phases are defined as follows:

  • Phase IA (ca. 8,730-8,290 cal. BC): Early PPNB horizon, corresponding to phases I, II and III of the new chronology proposed by Danielle Stordeur and colleagues.
  • Phase IB (ca. 8,550-7,950 cal. BC): Early PPNB horizon/Middle PPNB corresponding to phases I, II and III of the new chronology.
  • Phase II (ca. 8,240-7,760 cal. BC): end of Early PPNB horizon/Middle PPNB corresponding to new phase III.

6The study of the faunal assemblages indicated the presence of domesticated animals (goats, sheep and pigs) at the end of the Early PPNB horizon (Helmer and Gourichon 2008; Stordeur et al. 2010). Whereas cattle were mostly domesticated in the Middle PPNB, their domestic status is still not conclusive for the Early PPNB, due to the lack of data (Helmer and Gourichon 2008, 2017). The presence of Triticum dicoccoides remains (domestic form) attests to the domestication of plants from the earliest phases of the Tell’s occupation (Willcox 2000, 2005; Stordeur et al. 2010).

7More than ninety burial deposits have been unearthed at Tell Aswad, both during ancient and recent excavations (Contenson 1972, 1992, 1995; Stordeur 2003; Stordeur et al. 2006, 2010; Stordeur and Khawam 2007; Chamel 2014; Khawam 2014; Khawam et al. 2016). Excavations carried out by Henri de Contenson uncovered two deposits: a double burial located in the Eastern survey and dated to the Early PPNB, and a collective burial in the Western survey, from the end of Early PPNB or Middle PPNB.

8The Aswad East survey burial is a rectangular shaped pit that appears to have been dug into the virgin soil. It contains the skeleton of a mature or elderly individual, buried in a contracted position, lying on its right side. The upper limbs are flexed in front of the thorax, and the lower limbs are in a hypercontracted position against the rib cage. Skeletal remains of an immature individual were found against the right forearm of the adult individual, but it is not known if the skeleton was complete at the time of excavation (Contenson 1995). The type of deposition is primary: it would appear that we are dealing with an intentional double burial, possibly simultaneous, as the vertebrae and hand bones of the immature individual are located in front of the adult upper limbs, whereas the femur, on the other hand, is underneath the adult’s knee. It is therefore likely that the two individuals were buried together (Chamel 2014).

9The Western survey burial is dated from the end of Early or Middle PPNB. All publications mention a “collective burial” comprising both primary and secondary deposits (Contenson 1992, 1995). The human remains were found about 1.5 m deep in pit 1, which had been dug into virgin soil. Following the original description, the skeleton of an adult individual was found at about 50 cm from the top of the pit in a contracted position and lying on its left side (Contenson 1972, 1995; Chamel 2014). As all the bones were in anatomical connection, the burial can be considered as primary. Henri de Contenson (1992, 1995) mentions the discovery of a child skeleton in anatomical connection at the same level of 2.90 m, but this was not precisely recorded, and other human remains are also described at the same level, consisting in four skulls, as well as infracranial skeletal bones of two adults and two immature individuals (Contenson 1972; Chamel 2014). This pattern suggests a secondary deposit.

10In this pit, a child’s skeleton is also described as being “disarticulated” (Contenson 1992) and “scattered” (Contenson 1995). This might be either a disturbed primary deposit or a secondary deposit. Finally, Pit 1 also yielded an adult skull with a mandible at 2.55 m, which could result from a secondary deposit (Chamel 2014).

Material and Methods

11This research was carried out at the Institut de Paléontologie Humaine (IPH) in Paris, France where the skeletal remains from the Neolithic site of Tell Aswad resulting from ancient excavations are currently stored. This osteoarcheological material was studied in the framework of the second author’s PhD (Chamel 2014). The material is comprised of the remains of ten individuals coming from two burials, resulting from the two archaeological surveys (West and East) performed by Henri de Contenson, and previously dated from the end of PPNB to Middle PPNB.

12The collective burial of the West survey “Aswad Ouest” (level II, Layer II1 3, 4-1,9 m) yielded a minimum number of 8 individuals(Chamel 2014; table 1), corresponding to the end of Early or Middle PPNB. The subject of the present work came from the East survey “Aswad Est” (level IA, Layer IA1 4,45-4,20 m) that provided the skeletal remains of two individuals, one adult and one immature, attributed to the Early PPNB.

Table 1 – Inventory of the human skeletal remains from the site of Tell Aswad studied in this paper. HC: Henri de Contenson; DS: Danielle Stordeur.

Table 1 – Inventory of the human skeletal remains from the site of Tell Aswad studied in this paper. HC: Henri de Contenson; DS: Danielle Stordeur.

13Age-at-death estimation and observation of paleopathological alterations were carried out using the conventional methods of macroscopic and morphological examinations (Moorrees et al. 1963a, 1963b; Steinbock 1976; Ubelaker 1978; Aufderheide and Rodriguez-Martin 1998; Baker 1999; Scheuer and Black 2000; Hershkovitz et al. 2002; Ortner 2003; Dutour 2008, 2011). Different skeletal expressions were considered for the paleopathological diagnosis of TB, according to our previous records (Baker 2014; Baker et al. 2015, 2017). Sex cannot be reliably determined due to the poorly preserved state of the coxal bone.

Results

14Ten skeletons from Tell Aswad were examined for paleopathological analyses. Two adults from the Eastern and Western surveys showed typical morphological lesions of cribra orbitalia, porotic hyperostosis and signs of vertebral osteoarthritis.

15The paleopathological changes of interest in favor of TB were observed on the remains of the immature individual buried in the Eastern archaeological survey.

16The age at death of this individual can be estimated around 2-3 years according to its dental maturation stages (Moorees et al. 1963a, 1963b; Ubelaker 1978). The skeleton is incomplete, mainly represented by skull fragments (frontal, occipital, parietal, and facial bones); four unfused thoracic vertebrae; fragmented right femur and fibula; incomplete metatarsal; right talus and six phalanges of right hand (fig. 2).

Fig. 2 Osteological conservation of Aswad East immature (2-3 years old at death).

Fig. 2        – Osteological conservation of Aswad East immature (2-3 years old at death).

17Endocranial lesions were observed on the occipital and on the right parietal bones. On the occipital, the new bone formation is located on the cerebral fossa, sagittal and transverse sulci, the cerebellar fossa and the internal occipital crest. The internal table, in those areas, is slightly discolored, presenting sinuous superficial changes, with labyrinth-like features characterized by convoluted superficial interconnected channels (fig. 3).

Fig. 3 Two parts of occipital from the Aswad East immature show the characteristic changes of SES (Tell Aswad, end of Early PPNB horizon).

Fig. 3        – Two parts of occipital from the Aswad East immature show the characteristic changes of SES (Tell Aswad, end of Early PPNB horizon).

18On the right parietal, two types of endocranial changes are observed: scattered lesions with labyrinth-like pattern are localized in the postero-superior portion, and micro-porosity associated with periosteal reaction on the surface of the postero-inferior area (fig. 4: 2). We also observe micro-porosities on the external face of the postero-superior portion, without any associated thickening of the diploe (fig. 4: 1).

Fig. 4 Elements of the right parietal from the same immature individual. 1. Posterior view of the parietal exocranial surface showing porotic hyperostosis; 2. The endocranial surface with SES-like pattern (Serpens Endocrania Symmetrica), micro-porosity and periosteal reaction.

Fig. 4        – Elements of the right parietal from the same immature individual. 1. Posterior view of the parietal exocranial surface showing porotic hyperostosis; 2. The endocranial surface with SES-like pattern (Serpens Endocrania Symmetrica), micro-porosity and periosteal reaction.

19The postcranial skeleton is poorly preserved; however, the few isolated thoracic vertebrae show signs of periosteal reaction and hypervascularization demarcated on the anterior part of the vertebral bodies, around an enlarged vascular foramen (fig. 5).

Fig. 5 Isolated and unfused vertebrae of Aswad East immature showing hypervascularization of vertebral bodies.

Fig. 5        – Isolated and unfused vertebrae of Aswad East immature showing hypervascularization of vertebral bodies.

Discussion

20The morphological pattern observed on the skull has been described as Serpens Endocrania Symmetrica (SES) by Hershkovitz et al. (2002) and considered as resulting from a slowly developing and well remodeled endocranial periosteal reaction most probably due to a chronic meningitis, attributable to TB leptomeningitis.

21Several etiologies should be considered in the differential diagnosis of SES: metabolic disorders due to vitamin deficiencies (rickets, scurvy), marrow hyperplasia due to hematopoietic disorders (anemia) and subdural hematoma (mainly due to trauma; Mensforth el al. 1978; Roland et al. 1987; Hershkovitz et al. 2002). The SES pattern is very different from other bone changes, both in terms of morphology and location. According to Hershkovitz et al. (2002), it is due to changes in the primary and secondary anastomotic arteries crossing the dura mater, with the possibility that its typical sinuous pattern is related to increased blood flow linked to localized inflammation of the dura mater secondary to an infectious process.

22When looking at the records of anatomical collections of individuals presenting endocranial changes, studies on the Hamann-Todd and Terry skeletal documented collections revealed a significant association with intrathoracic or respiratory infections, death by tuberculosis being at the top of the list (Hershkovitz et al. 2002; Pálfi 2012). Among the TB cases documented in the Coimbra Collection, endocranial lesions were observed on one individual with pulmonary TB. However, juvenile individuals who died from meningeal tuberculosis displayed only periosteal reaction on the long bones (Santos and Roberts 2001) corresponding to a so-called secondary syndrome (non hereditary), Hypertrophic Pulmonary Osteopathy (HPO). This syndrome may be associated with various pulmonary chronic diseases including cancer, sarcoidosis, sarcoidosis, fibrosis and tuberculosis (Kumari et al. 2018). However, HPO is mainly attributed to tuberculosis in paleopathology due to its frequency and association with other changes attributed to TB (Hershkovitz et al. 2002; Pálfi 2002; Maczel 2003; Pálfi et al. 2012; Masson et al. 2013).

23Regarding external porosities on the cranial vault, they can be related to the so-called “porotic hyperostosis” (PH) or hyperostosis spongiosa cranii (HSC) or cribra cranii (CC) as cranial porosities can be observed without any thickening of the vault, that discard hyperostotic changes at the origin of these cranial porosities. This pattern is classically attributed to iron-deficiency anemia (Goodman et al. 1984; Stuart-Macadam 1987; Oxenham and Cavill 2010), but tuberculosis is also mentioned (Masson et al. 2015; Teschler-Nicola et al. 2015). A recent study (O’Donnell et al. 2020) suggested that porous cranial lesions should be considered as potential indicators of respiratory infections in bioarchaeological contexts. Even if tuberculosis was a major cause of pulmonary infections and fatal meningitis in the past, the paleopathological link between SES and PH/ HSC/CC is not yet evidenced (Hershkovitz et al. 2002).

24Unlike cranial porosities, HPO is commonly associated with SES (Hershkovitz et al. 2002). In our case, no alterations in favor of HPO are found, whereas it should be noted that a case of HPO attributed to tuberculosis has been previously described in the same site (Baker 2014; Baker et al. 2015, 2017; Coqueugniot et al. 2015).

25If the observed spinal changes may be of physiological nature and related to normal pattern of vertebral growth in children (anterior external vertebral venous plexuses or extraspinal veins), they may also be due to tuberculosis. Indeed, the enlargement of foramina of the anterior aspect of vertebra associated with periosteal changes has been reported over a century ago by Ménard (1888) as being the expression of spinal TB distinct from classic Pott’s disease, characterized by a hypervascularized aspect of bone tissue of the vertebrae’s anterior surface (development of TB fongosities enlarging the orifices of the venous plexuses), involving five to twelve vertebrae in total. The vertebral changes were later described by Baker (1999) as lytic lesions with rounded walls called “smooth walled resorptive lesions” or “severe circumferential pitting” and attributed to an early stage of tuberculosis infection. Some cases were reported on immature individuals from skeletal collections, and attributed to TB (Pálfi et al. 2002, 2012). These lesions have been identified in osteoarchaeological samples and diagnosis of TB was supported by biomolecular analysis (Mays et al. 2002; Maczel 2003; Baker 1999; Baker et al. 2015, 2017; Coqueugniot et al. 2015).

26Mariotti and colleagues (2015) studied the link of vertebral foramina observed on late adolescent and adults from the documented skeletal collection of Bologna with TB as cause of death. They found that cavities of various shapes (named foramina, other than vascular enlarged foramina) are present on one-fourth of adult individuals who died from pulmonary TB, that is almost five times more frequent than the frequency observed in the non-TB group. However, they studied mainly adults and their description and pictures do not match exactly the descriptions made by Ménard (1888) or Baker (1999).

27Therefore, the associated skeletal changes we observed allow us to raise the issue of their tuberculosis origin.

Conclusion

28We present here a new possible case of tubercular infection from the Early PPNB level of the Neolithic site of Tell Aswad. A young child (2-3 years old) from a burial in the Aswad East survey presents consistent associated changes: Serpens Endocrania Symmetrica, porotic hyperostosis, and vertebral changes (periosteal reaction and hypervascularization of the anterior aspect of vertebral bodies). Further studies (such as paleomicrobiological and paleoimaging analyses) will help in confirming this diagnosis. However, as the skeletal remains are part of a museum’s collection, we were yet not allowed to perform any destructive sampling for paleomicrobiological investigation.

29This study adds a new possible TB case, to the list of paleopathological cases of TB previously identified at Tell Aswad.

30The paleopathological evidence from two Pre-Pottery Neolithic sites discovered in Syria, Dja’de el-Mughara and Tell Aswad (Baker 2014; Baker et al. 2015, 2017; Coqueugniot et al. 2015), demonstrated that tuberculosis already existed as a human infection at least as early as 10,000 years ago.

31The number of paleopathological cases of TB dating from before or during the early phase of the Neolithization process in the Fertile Crescent (fig. 1), is now increasing. All these observations converge on the evolutionary model supporting the antiquity of human tuberculosis (Brosch et al. 2002; Gutierrez et al. 2005; Wirth et al. 2008; Comas et al. 2013).

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Notes

1 J. Sánchez Priego, personal communication.

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Table des illustrations

Titre Fig. 1 – Location map showing Tell Aswad and other Neolithic sites of Middle East with evidence of TB.
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-1.jpg
Fichier image/jpeg, 159k
Titre Table 1 – Inventory of the human skeletal remains from the site of Tell Aswad studied in this paper. HC: Henri de Contenson; DS: Danielle Stordeur.
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-2.jpg
Fichier image/jpeg, 93k
Titre Fig. 2 Osteological conservation of Aswad East immature (2-3 years old at death).
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-3.jpg
Fichier image/jpeg, 481k
Titre Fig. 3 Two parts of occipital from the Aswad East immature show the characteristic changes of SES (Tell Aswad, end of Early PPNB horizon).
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-4.jpg
Fichier image/jpeg, 244k
Titre Fig. 4 Elements of the right parietal from the same immature individual. 1. Posterior view of the parietal exocranial surface showing porotic hyperostosis; 2. The endocranial surface with SES-like pattern (Serpens Endocrania Symmetrica), micro-porosity and periosteal reaction.
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-5.jpg
Fichier image/jpeg, 148k
Titre Fig. 5 Isolated and unfused vertebrae of Aswad East immature showing hypervascularization of vertebral bodies.
URL http://journals.openedition.org/paleorient/docannexe/image/926/img-6.jpg
Fichier image/jpeg, 495k
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Pour citer cet article

Référence papier

Joseph Oussama Baker, Bérénice Chamel et Olivier Dutour, « New Paleopathological Evidence of Tuberculosis in Child Skeletal Remains from Tell Aswad (8,730-8,290 cal. BC, southern Syria) »Paléorient, 47-1 | 2021, 97-108.

Référence électronique

Joseph Oussama Baker, Bérénice Chamel et Olivier Dutour, « New Paleopathological Evidence of Tuberculosis in Child Skeletal Remains from Tell Aswad (8,730-8,290 cal. BC, southern Syria) »Paléorient [En ligne], 47-1 | 2021, mis en ligne le 01 décembre 2021, consulté le 13 juin 2025. URL : http://journals.openedition.org/paleorient/926 ; DOI : https://doi.org/10.4000/paleorient.926

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Auteurs

Joseph Oussama Baker

PACEA, UMR 519, École Pratique des Hautes Études, PSL Research University, Université de Bordeaux, Pessac – France

Bérénice Chamel

Archéorient, UMR 5133, Maison de l’Orient et de la Méditerranée, Université Lyon 2, Lyon – France

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Olivier Dutour

PACEA, UMR 519, École Pratique des Hautes Études, PSL Research University, Université de Bordeaux, Pessac – France

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