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Archives of Oral Biology 97 (2019) 97–101

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Archives of Oral Biology


journal homepage: www.elsevier.com/locate/archoralbio

A 3000 year old case of an unusual dental lesion: Pre-eruptive intracoronal T


resorption

Uri Zilbermana, , Ianir Milevskib,c, Dimitry Yegorovd,e, Patricia Smithf
a
Head of Pediatric Dental Clinic, Barzilai Medical University Center, Ashkelon, Israel
b
Head of the Prehistoric Branch, Israel Antiquities Authority Jerusalem, Israel
c
Program “Raíces”, Ministry of Science and Technology, Argentina
d
Israel Antiquities Authority, Southern District, Omer, Israel
e
Ben-Gurion University of the Negev, Beer Sheva, Israel
f
Laboratory of Bioarchaeology and Ancient DNA, Faculties of Medicine and Dental Medicine, The Hebrew University of Jerusalem, Israel

A R T I C LE I N FO A B S T R A C T

Keywords: Objective: To determine the cause of a large dental lesion, tentatively identified as a case of pre-eruptive intra-
PEIR coronal resorption (PEIR), in the permanent second mandibular molar of a young individual from an Iron Age
Tel Erani cemetery at Tel Erani (Israel), dated to ca. 3000 years B.P. The provisional diagnosis was based on the massive
Caries size of the lesion in a young individual in whom the adjacent teeth were caries-free and showed no visible
Dentine resorption
enamel defects.
Iron age
Design: The lower molars of Tel Erani on the affected side were radiographed and compared to radiographs of a
Dental disease
modern clinical case of PEIR treated by one of us (U.Z) and the internal structure and mineral content of the
lesion examined in detail using energy-dispersive X-ray spectroscopy (EDS).
Results: The Tel Erani specimen closely resembled the modern clinical case of PEIR. Moreover, both cases oc-
curred in young individuals in whom the adjacent teeth were caries-free. Examination with SEM revealed ab-
sence of dentine in the affected tooth from Tel Erani, together with changes in structure and mineral content
characteristic of resorption.
Conclusions: Our study shows that the changes found in the lower second molar of the 3000 year old mandible
from Tel Erani are characteristic of PEIR and demonstrate the antiquity of this condition.

1. Introduction but crumbles soon after eruption exposing a large cavity lacking of
dentine. The condition has been described in deciduous as well as
Dental caries is one of the most common diseases affecting hu- permanent teeth with no apparent gender or population differences
mankind at the present and is attributed primarily to the consumption (Skillen 1941, Seow & Hackley 1996; Seow et al., 1999; Seow 2000,
of fermentable carbohydrates, with sugars and soft drinks considered 2003; Moskovitz & Holan, 2004; Al-Batayneh et al., 2014; Omar et al.,
the main cariogenic agents (Kassebaum et al., 2015). The cavities that 2015; Schwimmer et al., 2017), although Al-Tuwirqi and Seow (2017)
characterize caries are caused by acid-fermenting bacteria that destroy found that PEIR was significantly more frequent in children with de-
the enamel and dentine (Aas et al., 2008; Takahashi & Nyvad, 2011) layed dental development of at least six months.
facilitating the spread of pathogens via the pulp cavity and root canals The factor or factors that trigger the activity of the clastic cells that
to the periapical bone. Numerous genetic and developmental insults resorb the dentine and its replacement by soft tissue are still unknown,
that result in hypoplastic or hypomineralized enamel are known to but Counihan and O’Connel (2012) identified them as osteoclast-like
facilitate the onset and progress of carious lesions (Seow, 2014, 2003). giant cells on the pulpal surface of the dentine, while Seow (2003)
Such defects can usually be easily identified on visual examination and suggested that they may originate from undifferentiated cells of the
normally affect many teeth. These considerations, however, do not developing dental follicle. Serial radiographs of developing teeth have
apply to the condition known as pre-eruptive intra-coronal resorption shown that the process begins soon after crown formation is completed
(PEIR), also known as hidden caries or occult caries. In this condition (Seow, 2003), as the dentine underlying the enamel is progressively
only one tooth is usually affected and the enamel appears to be intact, resorbed and replaced by soft granulation tissue. This leaves the


Corresponding author: Head of the Pediatric Dental Unit, Barzilai Medical University Center, 2nd Hahistadrut st., 7830604, Ashkelon, Israel.
E-mail address: ori@barzi.health.gov.il (U. Zilberman).

https://doi.org/10.1016/j.archoralbio.2018.10.015
Received 15 July 2018; Received in revised form 14 October 2018; Accepted 15 October 2018
0003-9969/ © 2018 Elsevier Ltd. All rights reserved.
U. Zilberman et al. Archives of Oral Biology 97 (2019) 97–101

occlusal layer of enamel unsupported so that it fractures soon after The site, located near the modern town of Kiriat Gat, was traditionally
eruption exposing the pulp chamber and root canals to the oral flora. known during the Iron Age as Gat of the Philistines, described in the
The prevalence of PEIR at the present time has been determined as bible (Killebrew & Lehman, 2013). However, it is now known that Tel
2–8% by subject and 0.6–2% by tooth, primarily affecting the man- Erani was settled at least 5000 years ago by the early Canaanites
dibular first premolar and second and third molars (Seow & Hackley, (Kempinski & Gilead, 1991; Yeivin, 1961; Milewski et al., 2016) The
1996; Savage, Gentner, & Symons, 1998; Nik & Rahman, 2003; Al- specimen in question was found in the remains of an Iron Age cemetery
Batayneh et al., 2014; Demirtas et al., 2016). dug into Early Bronze Age deposits at the foot of the Tel (Yegorov &
To the best of our knowledge the condition has not previously been Milevski, 2017; Milevski, Yegorov, Aladjem, & Pasternak, 2016) and
described in skeletal remains from archaeological contexts. In the case contained some 50 skeletons as well as numerous grave goods. The
described here, an extremely large lesion was identified in the lower grave goods included pottery vessels and other offerings that date to the
right second molar of a young individual in an otherwise caries-free end of the Iron Age IB (11th century) and are characteristic of the local
mouth. The provisional diagnosis of PEIR was based on the character- Canaanite culture.
istics of such lesions described by Seow (2003) who wrote “the dis- The specimen studied here comprises part of the right mandibular
proportionate size of the cavity relative to the short time the tooth has corpus with all three permanent molars erupted and in good alignment.
been in the mouth should alert the clinician to the fact that the lesion is Enamel wear facets were present on the first molar cusps, with pinpoint
unlikely to be caries”. He continues by describing the lesion that is exposure of dentine on the tips of the buccal cusps and only small en-
uncovered after collapse of the occlusal enamel as a large carious cavity amel facets on the mesial cusps of the third molars, attesting to the
that rapidly becomes attacked by oral microbial flora. All these criteria young age of this individual. No deposits of calculus were present
apply to the specimen from Tel Erani that is examined here, where we around the teeth and the bony margins around the teeth showed no
have evaluated the diagnosis of PEIR through (a) comparison with a signs of resorption. The first and third molars were caries-free, but in
recent clinical case treated by one of us (U.Z) in which the diagnosis of the second permanent molar there was an extensive cup-shaped carious
PEIR was based on pre-eruption radiographs and subsequent treatment lesion exposing the floor of the pulp chamber and openings of the root
and (b) detailed examination of the structure and chemical composition canals (Fig. 2). The partial mandible with the lesion was radiographed
of the lesion and intact enamel of adjacent teeth in the Tel Erani spe- and compared to a clinical case of PEIR identified from radiographs
cimen to examine the extent to which the lesion may have been mod- taken prior to eruption and treated by one of us (UZ).
ified by other factors. We used an energy-dispersive X-ray spectroscopy (EDAX EDS
System) SEM (FEI Quanta 200 microscope operating at 25 keV) to
compare the mineral content of the surface enamel in a recently ex-
2. Materials and methods
tracted first molar and first permanent molar from the Tel Erani spe-
cimen, the internal surface of the lesion from the Tel Erani second
The specimen containing the affected tooth was found in the course
molar and five samples of the soil from the soil in contact with the bone.
of salvage excavations carried out in 2015–2016 on the lower terrace of
The structure of the internal surface of the lesion was then examined at
Tel Erani on behalf of the Israel Antiquities Authority (IAA) (Fig. 1).

Fig. 1. Map of Middle East showing location of Israel with insert showing location of Tel Erani and other Iron Age sites.

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U. Zilberman et al. Archives of Oral Biology 97 (2019) 97–101

Fig. 2. Tel Erani mandibular fragment, Locus 2151.


A. Buccal view- Note the intact first and third erupted permanent molars and the large lesion in the second molar. Note: attrition of the cusps on the occlusal surface
of first molar. B. Lingual view.

X6000 with the SEM in backscattered electron mode. Radiographs of the three molars in the partial mandible from Tel
Erani confirmed that the lower first and third permanent molars were
3. Results caries-free and in good alignment with no obvious structural abnorm-
alities. The large lesion in the second molar (Fig. 3d) was associated
In the clinical case used as a standard for evaluating the lesion in the with small periapical lesions indicative of abscess formation while the
Tel Erani mandible, the condition of PEIR was initially diagnosed from apices of the third molar roots were patent, indicative of a mean age of
panoramic radiographs taken as part of a routine dental examination 18–20 years for this individual. (AlQahtani, Hector, & Liversidge, 2010;
(Fig. 3a). It showed a large radiolucent lesion in the crown of the un- Gunst, Mesotten, Carbonez, & Willems, 2003; Liversidge & Marsden,
erupted second molar, while all other teeth in this individual were 2010; Solari & Abramovitch, 2002). As can be seen from Figs. 2 and 3,
caries-free. The tooth was treated by surgical exposure of the crown and the lesion in the Tel Erani molar closely resembles that seen in the
removal of the occlusal enamel (Fig. 3b). This exposed a layer of soft clinical case of PEIR described above. In both individuals, the affected
granular tissue that was removed and found to be composed of myo- tooth was the lower second permanent molar, and the adjacent teeth
fibroblastic cells (spindle shaped actin positive), macrophages (oval were caries-free, while the location and extent of dentine loss appears
shaped CD68 and CD163 positive) and lymphocytes. The cavity was similar.
filled with glass-ionomer (EQUIA FORTE FIL by GC co. Japan) re- Table 1 shows the mineral content of the teeth examined with EDS
storative material (Fig. 3c). Follow-up of 18 months showed normal program of SEM. The intact enamel surface of the first molar from Tel
eruption of the crown with no signs of further resorption, pulpal sen- Erani was similar to that of the recent first molar, but showed some
sitivity, or pathologies. The parents gave their consent for publication evidence of diagenesis, expressed in the loss of carbon and phosphate
of the images. and its replacement with silica and alumina from the burial context.

Fig. 3. PEIR in modern mandibular second


permanent molar and in Tel Erani.
A.Panoramic view-No dentin on the mesial as-
pect of the crown. B. Clinical view of the PEIR
lesion in the dentin of the exposed second
molar- Note the large cavity. C. Radiograph
showing follow-up of 18 months after restora-
tion with glass-ionomer cement. D. Radiograph
of Tel Erani the mandible. Note the normal
enamel on first and third molars and the large
coronal lesion and periapical radiolucency in
the second molar.

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et al., 2000). No dentine tubules were identified.

4. Discussion

The changes observed in the elemental composition of the lesion in


the Tel Erani individual resemble those reported (Robinson et al., 2000)
for carious lesions in recent teeth where some degree of remineraliza-
tion occurs, although in the archaeological specimen the external en-
vironment is soil and not saliva. They reported that the extent of mi-
neral exchange with the oral environment changes through the various
zones of decalcification and remineralisation characteristic of caries.
These changes differ from those seen in chemical erosion where the
surface zone is most affected with 62–64% mineral loss and increased
porosity, since much of the organic matrix is unaffected (Eisenburger,
2009). This was obviously not the case in the specimens studied here,
where oral pathogens have broken down the organic matrix. Moreover,
in the case in question we are dealing with a localised condition af-
fecting one tooth, whereas erosion during life usually affects many teeth
surfaces, rather than one tooth (Ganss, Klimek, & Borowski, 2002;
Coupal & Sołtysiak, 2017). The same applies to factors affecting the
Fig. 4. Occlusal surface of Tel Erani first permanent molar.
11a marks the intact enamel examined by EDS. 11b shows the region with integrity of the mineralized tissues after death as far as erosion from the
cupping of dentine due to attrition. pH of the burial context is concerned. Attack by biological agents in the
soil to produce the localized lesions seen in bones and occasionally in
exposed cementum rarely attack the more highly mineralized dental
Table 1
enamel (Kendall, Høier Eriksen, Kontopoulos, Collins, & Turner-Walker,
Mineral content of intact enamel from modern M1, the intact occlusal surface of
2018). The only account of such a lesion we have seen, is that shown in
Tel Erani M1, internal surface from Tel Erani M2 (PEIR lesion) and soil samples.
the crown of a fossilized rat and has shallow sloping margins
Elements Modern M1 Tel Erani Tel Erani Tel Erani Soil samples (Fernandez-Jalvo & Andrews, 2016: Fig. A423) that are very different
Enamel M1 Enamel PEIR-M2 PEIR-M2
to the steep undercut enamel margins in the Tel Erani specimen.
Fig. 4 Fig. 5A Fig. 5A
Loc1A Loc 1B The size and shape of the lesion is therefore in our opinion unlikely
to be attributable to diagenesis, while it differs from that typical of diet
C 12.75 8.70 0.23 0.28 4.85 related caries. This, since the time of onset and progress are primarily
O 41.74 37.08 57.73 56.14 36.3
correlated with diet and age so that the frequency of caries is usually
P 14.53 10.77 1.07 0.82
Ca 30.99 39.85 31.74 28.34 9.5 higher in the early erupting first molar than in the second molar
Si 2.48 5.59 9.41 29.5 (Nordblad & Larmas, 1975) as well as in older individuals (Hopcraft &
Al 1.11 1.46 2.31 7.95 Morgan, 2006). The latter reported that the first molar was the tooth
Mg 0.55 0.53 1.04 most frequently affected in all age groups they examined, even though
Fe 1.95 1.76 6.95
the mean score for DMTS (Decayed, Missing, Treated Surfaces) teeth
Note: C = Carbon, O = Oxygen, P = Phosphate, Ca = Calcium, Si = Silica, was far greater in those aged 31–35 years, than in those aged 17–21
Al = Alumina, Mg = Magnesium, Fe = Iron. (13.04 and 3.21 respectively). Thus there is only a low possibility that
the extremely large carious lesion in the second molar of the otherwise
More extensive changes were seen in the partially decalcified internal caries-free mandible from Tel Erani is not associated with PEIR, since it
surface of the PEIR lesion in respect to carbon and phosphate together fits all the criteria described by Seow, Wan & McCallen (1999), and
with an increased content of silica, alumina and iron. At the same time Seow (2003).
the calcium content of the internal surface was high and this was as- In both the Tel Erani specimen and the modern clinical case of PEIR
sociated with the presence of large recrystallized apatite crystals, a used for comparison described here the cavities in the second molars
phenomenon commonly seen at the base of carious lesions (Robinson resembled one another in size and shape and were associated with
caries-free first molars and were lacking dentine.

Fig. 5. Internal surface of the PEIR lesion in


Tel Erani second molar.
A. Labels 6a and 6b on the figure denote the
locations of ESD analyses. B. Enlargement
X6000 of region 6b. Note: absence of dentin,
different sized enamel crystals. A. Labels 1A
and 1B on the figure denote the location of EDS
analyses. B. enlargement X6000 of region 1B.
Note: absence of dentin, different sized enamel
crystals.

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As with many other diseases affecting modern societies, technical Al-Tuwirqi, A., & Seow, W. K. (2017). A controlled study of pre-eruptive intracoronal
advances in diagnosis, combined with the greater availability of med- resorption and dental development. The Journal of Clinical Pediatric Dentistry, 41,
374–380.
ical care, have led to improved diagnosis of PEIR, a condition, which Counihan, K. P., & O’Connel, A. C. (2012). Case report: Pre-eruptive intracoronal radi-
untreated results in rapid loss of the affected tooth once it erupts. While olucencies revisited. European Archives of Paediatric Dentistry, 13, 221–226.
the clinical diagnosis is now primarily based on diagnosis from radio- Coupal, I., & Sołtysiak, A. (2017). Dental erosion in archaeological human remains: A
critical review of literature and proposal of a diff ;erential diagnosis protocol. Archives
graphy of the developing jaws, this is not usually carried out during of Oral Biology, 84, 50–57.
routine dental examination of skeletal remains. However, we propose Demirtas, O., Ertas, E. T., Dane, E. A., Fahrettin, A., Kalabalik, F., & Sozen, E. (2016).
that it is another factor to consider in evaluating the cause of an ex- Evaluation of pre-eruptive intracoronal resorption on cone-beam computed tomo-
graphy: A retrospective study. Scanning, 38, 442–447.
tremely large carious cavity in a recently erupted tooth in an otherwise Eisenburger, M. (2009). Degree of mineral loss in softened human enamel after acid
caries-free mouth in the skeletal remains of young individuals. erosion measured by chemical analysis. Journal of Dentistry, 37, 491–494.
Moreover, since the untreated tooth is lost soon after eruption because Fernandez-Jalvo, Y., & Andrews, P. (Eds.). (2016). Atlas of taphonomic identifications.
Dordrecht Heidelberg, New-York, London: Springer.
of the rapid destruction of the tooth and resultant resorption of the
Ganss, C., Klimek, J., & Borowski, N. (2002). Characteristics of tooth wear in relation to
supporting bone, it may account for the early loss of a single tooth in an different nutritional patterns including contemporary and medieval subjects.
otherwise healthy dentition. As with other pathologies where the ae- European Journal of Oral Sciences, 110, 54–60.
tiology is still unknown, identifying when and where PEIR occurred in Gunst, K., Mesotten, K., Carbonez, A., & Willems, G. (2003). Third molar root develop-
ment in relation to chronological age: A large sample sized retrospective study.
the past may contribute to a better understanding of the factors in- Forensic Science International, 136, 52–57.
volved. Certainly the fact that the condition was present some Hopcraft, M. S., & Morgan, M. V. (2006). Pattern of dental caries experience on tooth
3000 years ago means that it long predated the on-going deterioration surfaces in an adult population. Community Dentistry and Oral Epidemiology, 34,
174–183.
in environment and increased stress of modern lifestyles. Kassebaum, N. J., Bernebe, E., Dahiya, M., Bhandari, B., Murray, C. J. L., & Marcenes, W.
(2015). Global burden of untreated caries. A systematic review and metaregression.
5. Conclusions Journal of Dental Research, 94, 650–658.
Kempinski, A., & Gilead, I. (1991). New excavations at Tel Erani: A preliminary report of
the 1985-1988 seasons. Tel Aviv, 18, 164–191.
This study demonstrates that PEIR is not a disease of recent origin, Kendall, C., Høier Eriksen, A. M., Kontopoulos, I., Collins, M. J., & Turner-Walker, G.
but was present at least 3000 years ago. We propose that the criteria (2018). Diagenesis of archaeological bone and tooth. Palaeogeography,
Palaeoclimatology, Palaeoecology, 491, 21–37.
used in the clinical diagnosis of this condition, are adequate for its di- Killebrew, A., & Lehman, G. (Eds.). (2013). Sea peoples. Atlanta: Society of Biblical
agnosis in skeletal remains and should be taken into consideration in Literature.
evaluating the pathogenesis of unusual dental lesions in recently Liversidge, H. M., & Marsden, P. H. (2010). Estimating age and the likelihood of having
attained 18 years of age using mandibular third molars. British Dental Journal, 209(8),
erupted teeth, or early ante- mortem loss in skeletal remains.
E13.
Milewski, I., Yegorov, D., Aladjem, E., & Pasternak, M. D. (2016). Salvage excavation at
Funding Tel Erani, areas P to U. Preliminary report. In K. M. Ciałowicz, Y. Yekutieli, & M.
Czarnowicz (Eds.). Tel Erani I. preliminary report of the 2013–2015 excavations (pp. 45–
57). Kraków: Jagiellonian University in Kraków.
This research did not receive any specific grant from funding Moskovitz, M., & Holan, G. (2004). Pre-eruptive intracoronal radiolucent defect: A case of
agencies in the public, commercial, or non-for-profit sectors. a non-progressive lesion. Journal of Dentistry for Children, 71, 175–178.
Nik, N. N., & Rahman, R. A. (2003). Pre-eruptive intracoronal dentin defects of permanent
teeth. The Journal of Clinical Pediatric Dentistry, 27, 371–375.
Acknowledgments Nordblad, A., & Larmas, M. (1975). The pattern of dental health in relation to age at a
Finnish dental school. Proceedings of the Finnish Dental Society, 71, 103–110.
We want to thank the Department of Publications of the IAA (Israel Omar, S., Choi, J., Nelson, B., Shin, M., & Chen, J. W. (2015). Pre-eruptive intracoronal
resorption: Literature review and case report. Journal of the California Dental
Antiquities Authority) for the permit granted to publish data from the Association, 43, 255–260.
salvage excavations at Tel Erani (Permit A-7524/2015). We also want Robinson, C., Shore, R. C., Brookes, S. J., Strafford, S., Wood, S. R., & Kirkham, J. (2000).
to thank the staff and workers at Tel Erani; special thanks to Yossi The chemistry of enamel caries. Critical Reviews in Oral Biology and Medicine, 1,
481–495.
Nagar (physical anthropologist at the field), Svetlana Talis (Iron Age
Savage, N. W., Gentner, M., & Symons, A. L. (1998). Pre-eruptive intracoronal radi-
pottery), Emil Aladjem and Martin Pasternak (field supervisors), and olucencies: Review and report of case. Journal of Dentistry for Children, 65, 36–40.
Daniel Varga (Southern District of the IAA). Schwimmer, Y., Zeltser, R., & Moskowitz, M. (2017). Deep caries due to pre-eruprive
intracoronal resorption in a newly erupted primary molar. International Journal of
We want to thank Roxana Golan from the Isle Katz Institute for
Paediatric Dentistry, 27, 313–315.
Nanoscale Science and Technology, Ben Gurion University of the Seow, W. K., & Hackley, D. (1996). Pre-eruptive resorption of dentin in the primary and
Negev, Beer-Sheva for the work on the SEM and the EDS analysis of the permanent dentitions: Case reports and literature review. Pediatric Dentistry, 18,
ions content. 67–71.
Seow, W. K., Wan, A., & McCallen, L. H. (1999). The prevalence of pre-eruptive dentin
radiolucencies in the permanent dentition. Pediatric Dentistry, 21, 26–33.
Conflict of Interest Seow, W. K. (2000). Pre-eruptive intracoronal resorption as an entity of occult caries.
Pediatric Dentistry, 22, 370–376.
Seow, W. K. (2003). Diagnosis and management of unusual dental abscesses in children.
None. Australian Dental Journal, 48, 156–168.
Seow, W. K. (2014). Developmental defects of enamel and dentine: Challenges for basic
References science research and clinical management. Australian Dental Journal, 59(Suppl. 1),
143–154.
Skillen, W. G. (1941). Intra-follicular caries. Dental Journal, 10, 307–308.
Aas, J. A., Griffen, A. L., Dardis, S. R., Lee, A. M., Olsen, I., Dewhirst, F. E., et al. (2008). Solari, A. C., & Abramovitch, K. (2002). The accuracy and precision of third molar de-
Bacteria of dental caries in primary and permanent teeth in children and young velopment as an indicator of chronological age in Hispanics. Journal of Forensic
adults. Journal of Clinical Microbiology, 46, 1407–1414. Sciences, 47, 531–535.
Al-Batayneh, O. B., Al-Jamal, G. A., & Al-Tawashi, E. K. (2014). Pre-eruptive intracoronal Takahashi, N., & Nyvad, B. (2011). The role of bacteria in the caries process: Ecological
dentine radiolucencies in the permanent dentition of Jordanian children. European perspectives. Journal of Dental Research, 90, 294–303.
Archives of Paediatric Dentistry, 15, 229–236. Yegorov, D., & Milevski, I. (2017). Tel ‘Erani. Hadashot Arkheologiyot129.
AlQahtani, S. J., Hector, M. P., & Liversidge, H. M. (2010). Brief communication: The Yeivin, S. (1961). First preliminary report of the excavations at “Tel Gat”(Tell Sheykh `Ahmed
London atlas of human tooth development and eruption. American Journal of Physical el-`Areyny): Seasons 1956-1958)Jerusalem: The Gat Expedition.
Anthropology, 142, 481–490.

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