at SciVerse ScienceDirect

Quaternary International 295 (2013) 83e93

Contents lists available

Quaternary International

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

Orofacial pathology in Homo heidelbergensis: The case of Skull 5 from the Sima delos Huesos site (Atapuerca, Spain)

Ana Gracia-Téllez a,b,*, Juan-Luis Arsuaga b,c, Ignacio Martínez a,b, Laura Martín-Francés d,María Martinón-Torres d, José-María Bermúdez de Castro d, Alejandro Bonmatí b,c, Jaime Lira b

aÁrea de Paleontología, Departamento de Geología, Universidad de Alcalá de Henares, Edificio de Ciencias, Campus Universitario, 28871 Alcalá de Henares, SpainbCentro Mixto UCM-ISCIII de Evolución y Comportamiento Humanos, C/Monforte de Lemos, 5, 28029 Madrid, SpaincDepartamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, C/José Antonio Novais s/n, 28040 Madrid, SpaindCentro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca s/n, 09002 Burgos, Spain

a r t i c l e i n f o

Article history:Available online 8 February 2012

* Corresponding author.E-mail address: ana.graciat@uah.es (A. Gracia-Téll

1040-6182/$ e see front matter � 2012 Elsevier Ltd adoi:10.1016/j.quaint.2012.02.005

a b s t r a c t

This paper presents a detailed palaeopathological study of the orofacial lesions present in Skull 5 fromthe Sima de los Huesos Middle Pleistocene site. Besides testing a previous diagnosis of periodontaldisease, tooth wear, left P3 fracture and two periapical abscesses, unreported lesions are identified: the I1abscess and the M3 fracture. The timing of the pathological events that have produced the conspicuousbone growth of the maxilla was determined with the aid of computer tomography techniques. This isparticularly important to assess the duration/chronicity of the lesions and the cause/s of them. Somephysiological particularities of the region affected could account for the maxillary osteitis andconcomitant infection as a probable cause of death.

� 2012 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction

Since the discovery in 1992 of Cranium 5 from Atapuerca-Simade los Huesos (SH) site (Skull 5 since 1993, after its mandible wasrecovered; dental individual number XXI) it was noticed that ananomalous bone growth was present on the left maxillary bone.This lesion was preliminarily described in a first publication as an“extensive osteitis on the left maxilla” (Fig.1 in Arsuaga et al., 1993).Pérez et al. (1997) made a larger description of this facial pathology,referring also to other dental pathologies that were present in thisindividual (Fig. 1). Those signs were: a) a fistulation process presentin the osteitis; b) a dental apical abscess in the left I2; c) the pres-ence of anomalous inter-proximal tooth wear facets; d) calculusdeposition; and e) alveolar bone resorption, suggesting that anongoing serious infection might had been present in this individualat the time of death and that it was very likely the cause of death bymeans of generalized septicaemia.

Skull 5 display other minor pathological signs previouslydescribed, including a bilateral mild expression of tempor-omadibular joint arthropathy, thirteen slight cranial lesions withsigns of healing and a worm-like pattern on the orbital roof prob-ably related to cribra orbitaria (Pérez et al., 1997). The teeth of Skull

ez).

nd INQUA. All rights reserved.

5 are extensively worn, so it was not possible to analyze if thisindividual suffered from dental hypoplasia and therefore, devel-opmental stress (Cunha et al., 2004).

There are other specimens from Sima de los Huesos site dis-playing pathologies (see Pérez et al., 1997; Gracia, 2007; Graciaet al., 2010; Martín-Francés et al., 2011). Although most of themare presumably non-severe, two very remarkable ones wererecorded. The first consists of an immature cranium displayinga rare cranial deformation, a lambdoid unilateral craniosynostosis(Gracia et al., 2009), that represents a crucial case to study socialbehaviour in past populations, as a very probable case of con-specific social care (Gracia et al., 2009; Hublin, 2009). The secondcase deals with the pathological condition displayed by the Pelvis 1and its associated lumbar spine (Bonmatí et al., 2010), and couldrepresent another example of social care among this population.Given the valuable information that palaeopathological studies canprovide regarding behaviour and adaptation of an extinct humangroup, it is important to contribute to the knowledge of thepathologies of the SH collection. Furthermore, SH is a unique casewhere the remains of at least 28 individuals belonging to the samebiological population (Arsuaga et al., 1993, 1997a, 1997b; Bermúdezde Castro et al., 2004) have been recovered, an unparallelledopportunity to study a Middle Pleistocene population.

The aim of this study is to describe and analyze exhaustively allthe above-mentioned pathological signs in Skull 5, as well as some

Fig. 1. Pathological signs present in Skull 5. Pathologies that have been previously described and studied extensively in this work, (1) Heavy tooth wear; (2) Dental calculus; (3) I2dental abscess; (4) Alveolar crest lesions and root exposure; (5) Anomalous inter-proximal wear facets; (6) Broken P3; (7) Fistula at the P3. Unreported lesions included in this study(8) I1 dental abscess; (9) Dental chipping at M3; Previously reported but studied with new evidence here (10) Maxillary osteitis. Scale bar 2 cm (Right etching credit: AlmudenaAlcázar de Velasco).

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e9384

lesions that have not been previously described. The diagnosis willbe approached under a general orofacial pathological framework, inorder to establish the possible etiological factors that were involvedand whether they could be the cause of death of this individual(Fig. 1).

2. Materials and methods

Skull 5 (AT-700 þ AT-888) from Sima de los Huesos, Atapuercasite was recovered during the 1992/93/99/2001 field seasons(Arsuaga et al., 1993, 1997a, 1997b), and represents one of the mostcomplete and best preserved skulls of the hominid fossil record(Fig. 1). At present, the Sima de los Huesos hominid sampleconstitutes the largest one among the Middle Pleistocene hominidfossil record. This collection comprises more than 6500 fossils,belonging to at least 28 individuals, of different ages at death (from5 years old to >45 years old) and both sexes equally represented(e.g., Arsuaga et al., 1991, 1997b; Bermúdez de Castro et al., 2004;Bonmatí et al., 2010; Martinón-Torres et al., 2012), and almost allthe skeletal elements are represented (e.g., Carretero et al., 1997;Arsuaga et al., 1997b; Martínez et al., 2004, 2008; Bonmatí andArsuaga, 2005; Gómez-Olivencia et al., 2007; Arsuaga, 2010;Pablos et al., 2011; Quam et al., 2011). Skull 5 individual also has itsassociated cervical vertebrae (Gómez-Olivencia et al., 2011;Martínez et al., 2013).

The finding in 1999 of the left upper third premolar (AT-2719) ofthis individual was especially relevant to this study, as will bedescribed below.

The state of preservation of Skull 5 is exceptional, and preservesalmost in total the cranial and mandibular bone structures andteeth, without any distortion or deformation. All the fragmentsrecovered in subsequent excavation seasons were consolidated(Primal and/or Paraloid B-72) and later refitted with cellulosenitrate (Imedio� glue) and Paraloid B-72.

According to the dental evidence (Bermúdez de Castro et al.,2004), Skull 5 belongs to an adult male, older than 35 years

although not senile, as there are no signs of suture closure, neitherexocranial nor endocranially. It preserves the complete upper andlower premolar and molar series, as well as both upper centralincisors.

This study employed visual inspection and microscopic tech-niques including a scan with a YXLON Y.CT Compact housed at theUniversidad de Burgos (Spain) (CT e scans parameters: Sliceincrement ¼ 0.3 mm; Image size ¼ 1024 � 1024 & 512 � 512; Greylevels ¼ 16 bits; Pixel size ¼ 0.161e0.217 mm). The images wereimported to Mimics� 13.0 software (Materialise, Leuven) forvirtual reconstruction.

3. Results and discussion

3.1. Dental calculus, alveolar crest lesions, root exposure and tooth-pick facets

3.1.1. Dental calculusThere is presence of dental calculus in almost all postcanine

teeth of Skull 5 (Fig. 2). The presence of an asymmetric pattern ofcalculus between left and right mandibular dentitions suggestssome kind of post-mortem loss. In those teeth where calculus iswell preserved, it is adhered to the upper third of the exposedbuccal roots and lower half of the crown. According to Brothwell(1981), the score of those teeth displaying remaining patches ofdental calculus can be attributed to the medium category, and arepresented in Table 1.

3.1.2. Periodontal diseaseGiven the extraordinary state of preservation, the alveolar crest

of both the maxilla and mandible of Skull 5 can be analyzed. Thereis a root exposure of at least one third of the root in all of thepreserved teeth (see, for example, Fig. 2). There are signs ofmarginal lipping along the buccal margin of the crest of the alveolarprocess, particularly pronounced in the region of the posteriorteeth in both maxillae (Fig. 2). The superior rim of the entire

Fig. 2. Right side dental calculus on mandibular dentition. All the preserved post-canine teeth display a moderate expression of dental calculus.

Fig. 3. Occlusal view of the Skull 5 mandible, the left side. Left P3eM2 mandibularteeth are in place, showing alveolar recession, root denudation and periodontalpockets (see text).

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e93 85

preserved crest is thickened in both the buccal and the lingualsides. The lingual crest is particularly altered in the mandible. Thealveolar crest shows extensive porosity and signs of recession andremodelling (Figs. 2e4). The margin is rounded and irregular, andthere is a periodontal pocket from 1 to 2 mm depth between thetooth and the alveolus (Fig. 3, arrows).

The changes in the alveolar crest would result in the resorptionof the alveolar bone and the formation of an abnormally largedistance between bone and the cement-enamel junction (Ortnerand Putschar, 1981), with the presence of calculus probablyrelated to it. Changes in the architecture and texture of the alveolarcrest have been cited as more diagnostic of periodontal diseasethan the extent of root exposed, as the latter can be also a conse-quence of compensatory eruption processes (Ogden, 2008a, 2008b;Martinón-Torres et al., 2011a, 2011b). The association of the rootexposure and the pathological changes assessed in the alveolarcrest suggest that this individual suffered at least moderate peri-odontal disease (Ogden, 2008a, 2008b).

Table 1Dental calculus and anomalous inter-proximal grooves in Skull 5.

Element Side Calculus Tooth-pick

Maxillar P3 Right e e

Left Eroded e

P4 Right e MLeft e M & D

M1 Right Medium M & DLeft Medium M & D

M2 Right Medium MLeft Medium e

M3 Right Medium e

Left Medium e

Mandibular P3 Right Medium e

Left Eroded e

P4 Right Medium MLeft Eroded e

M1 Right Medium M & DLeft Eroded M & D

M2 Right Medium MLeft Eroded M

M3 Right Medium MLeft Small patch e

Dental calculus has been scored following Brothwell (1981) and not other moreacurated methods, as there is very probable an important post-mortem calculus’loss in almost all the teeth. Tooth-pick grooves presence is recorded on the mesial(M) and/or distal (D) inter-proximal surfaces.

Marginal lipping has been identified in the superior rim of thealveolar margin at the level of the lower molars in Skull 5. Marginallipping is more likely to be related to moderate periodontal diseaseand calculus. Simple compensatory eruption classically producesa knife-edged profile to the alveolar margin, if there is no peri-odontal disease to further complicate the picture (Hillson, 2008;Ogden, 2008a). These alveolar changes, together with a high degreeof occlusal wear (see below) suggest heavy and intense masticatoryhabits for this individual (following also Newman and Levers, 1979;Clarke and Hirsch, 1991).

3.1.3. Anomalous inter-proximal tooth wear pattern (Fig. 4)According to Lukacs and Pastor (1988), an inter-proximal groove

is a transverse furrow of variable shape worn into the mesial ordistal surface of a tooth at or near the cement-enamel junction. Theearliest documented case was reported by Siffre (1911), and in thehominid fossil record by Weidenreich (1937). The first publicationof an inter-proximal groove in the SH dental collection was thatfrom Bermúdez de Castro et al. (1997). Since that publication, other

Fig. 4. Tooth-pick groove on the distal inter-proximal surface of the right M1. Close-upof the Skull 5 mandible, right side. Arrow points to the inter-proximal anomalousgroove.

Fig. 5. Occlusal views of upper and lower dentitions of Skull 5. (A) Upper dentition; (B) Lower dentition. All the teeth show heavy tooth wear, with dentine exposure in all cusps.Scale bar 2 cm.

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e9386

cases have been recorded in the SH sample (Gracia et al., 2011).Skull 5 is one of the individuals that display a higher presence ofthis trait in his dentition.

The gross size, shape and orientation of the marks together withan assessment of the microstriae on their surface are employed inthe interpretation of activity-induced marks. As stated before (e.g.Bermúdez de Castro et al., 1997; Gracia et al., 2011), these anoma-lous abrasive facets are consequence of a continuous and reiterativeprocess of insertion and retraction of a probe as a tooth-pick.

There are eleven postcanine teeth out of 20 of Skull 5 that showclear tooth-pick grooves, all at the cement-enamel junction level.Table 1 lists the teeth surfaces displaying this type of anomalouswear. All the Skull 5 teeth that show tooth-pick grooves alsopresent a denudation of the roots larger than 3.2 mm. The roughporosity that characterizes the alveolar crest at the level ofpremolars and molars is compatible with an inflammatory condi-tion that probably affected the overlying soft tissues and justifiedthe continuous introduction of a hard probe to alleviate pain ordislodge impacted food particles.

All the pathological signs of Skull 5 imply some kind of inflam-matory response to one or more irritants and would be typical ofperiodontal disease (Ortner and Putschar, 1981). Although chronicperiodontitis is usually painless, it can cause discomfort, swellingand halitosis. It also favours dental drift and potential tooth lossduring the life of the individual (Dowsett et al., 2001).

Fig. 6. Upper central incisors tooth wear. Heavy tooth wear has worn almost the completeright I1 occlusal view (red arrow). White arrows indicate the presence and direction of the buin this figure legend, the reader is referred to the web version of this article.)

3.2. Tooth wear

All the preserved teeth show a severe occlusal and inter-proximal wear (Fig. 5), that had concomitant forward displace-ment of the whole postcanine teeth-row by means of mesial drift.Dental attrition is based on Molnar’s (1971) classification, with thedistinction between attrition (¼ a form of wear caused by tooth totooth friction), and abrasion (¼ a form of wear caused by frictionbetween a tooth and an exogenous agent), sensu Grippo et al.(2004).

All the maxillary teeth, except the premolars (category 5) andthe left M2 (category 6), show category 7 of tooth wear. Regardingthe lower dentition, all of the reserved teeth, excepting for the leftP3, right M2 and right M3 (category 6) display category 7 of occlusalwear (Molnar, 1971). This severe attrition is also reflected in theinter-proximal contact facets, which in some cases presenta complete wear of the enamel crown on its mesial and distalsurfaces (Fig. 5). The obtained Molnar scores suggest heavy andprolongedmasticatory habits, but no abrasion signs were observed.

The upper central incisors crowns are almost worn away in a flatwear pattern (Fig. 6A). On their occlusal surfaces, it is possible todistinguish a bucco-lingual macro-striation. These bucco-lingualcrests (Fig. 6B) of the occlusal areas of the upper central incisors,seems to match the inter-proximal spaces of the flatly worn lowercentral and lateral incisors (not yet found). The pulp cavity of these

crown (A) and exposed the pulp cavity (B). Secondary dentine can be observed on thecco-lingual crests left by dental attrition. (For interpretation of the references to colour

Fig. 7. Fracture of the left P3. (A) The breakage occupies almost half of the crown, and has exposed the pulp cavity. (B) Occlusal view of the broken P3, showing the smoothing of thecrown’s fracture edges.

Fig. 8. Fractured left M3. The chipping of this tooth comprises almost the completeprotoconid, both on the mesio-buccal and occlusal surfaces. The fracture edges appearsmooth and rounded.

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e93 87

teeth was exposed and there are signs of secondary dentinedeposition (Fig. 6B). There is post-mortem erosion at the apicalroots level of these incisors, simulating abscesses (as shown inBrothwell, 1981, Fig. 6.15b).

As noticed by Kaifu et al. (2003, Fig. 2 caption, p.48), “publisheddescription and photographs of various human populations inheavy-wear environments indicate that individuals with moderateor extensive tooth wear in such populations show several commonocclusal features”. Such features include flatly worn occlusalsurfaces of teeth, development of a reversed Monson curve inposterior teeth (occlusal plane that inclines downward to buccal),extensive inter-proximal wear, and anterior edge-to-edge occlu-sion. More upright positioning of anterior teeth and a nearly flatocclusal plane in lateral view may be added to this list. The samecharacteristics are also ubiquitous among fossil hominids. Well-preserved fossils of Neandertals and fragmentary fossils ofvarious other fossil human taxa suggest that this type of occlusionhas been normal in human lineage. In other words, Skull 5 presentsthis kind of attritional heavy toothwear, but does not show any signof occlusal bevelling abrasion of the anterior dentition as is presentin some Neandertal specimens, such as La Ferrassie 1 and Shanidar1 (e.g. Trinkaus, 1983). Although in Skull 5 the heavy tooth wear ofthe central upper incisors does not allow study of labial wear striae,they are present in a large number of SH specimens, always cor-responding to right-handed individuals (Bermúdez de Castro et al.,1988; Lozano et al., 2004) and relating this pattern to non-masticatory uses of the anterior teeth.

Thus, the heavy attrition in Skull 5 is interpreted as caused by themasticatory process and cannot be the consequence of the use ofdentition as a tool in the same way was documented for Inuit (e.g.De Poncins, 1941 in Hylander, 1977) and suggested for Neandertals(e.g. Brace, 1962; Trinkaus, 1983, 1989; Spencer and Demes, 1993).

3.3. Teeth fractures

There are two cases of tooth breakage in Skull 5 individual (seebelow), that are especially relevant because there are signs showingthat they occurred during the individual’s life. There are other teethfractures on this individual, but their edges are sharp, suggestinga peri/post-mortem origin.

3.3.1. Left upper third premolarThe first time the pathological condition of Skull 5 was pub-

lished, Pérez et al. (1997) noticed a pathological bone aperture onthe top of the osteitis. This sign was described as the aperture ofa drainage canal of an apical abscess of the left P3 (see below). In the1999 field season, this tooth was recovered and it was broken(Fig. 7).

The left P3 fracture comprises almost the complete half of thecrown, a large area of the root and the pulp cavity is exposed. Thevertical length of the fracture, including the crown and part of theroot, is 8.7 mm. If this fracture was produced antemortem, it couldexplain the infection found at the apex of the P3 socket. Accordingto Ortner and Putschar (1981, p.603), “one possible criterion formaking the distinction between ante- and post-mortem fracture isthe smoothing of the fractured edges of the tooth, which wouldoccur in antemortem fracture if sufficient time had elapsedbetween the fracture and death” The fracture edges of the brokenleft P3 that affected the crown have been smoothed (Fig. 7A, B)while the fracture edges of the tooth root remain sharp, Thedifferential wearing on both surfaces of the same fracture is verylikely due to a fairly long attrition of the broken crown tooth surfaceafter the fracture.

3.3.2. Left lower third molarOn the mesio-buccal surface of the protoconid of the lower left

thirdmolar of themandible of Skull 5, there is a large loss of enameland dentine (Fig. 8). The fracture affects more than half of the cusp,including both the mesio-buccal and occlusal surfaces of the tooth(see Figs. 5 and 8). This chipped tooth was broken during Skull 5individual’s life, as can be interpreted from the conspicuoussmoothing of the fractured edges, observable at the enamel anddentine tissues (see Ortner and Putschar, 1981, p.603).

Fig. 9. Fistular canal from the apex of the left broken P3. (A) Frontal view of the left maxilla of Skull 5. (B) CT scan segmentation of Skull 5 showing the fistular canal path (orange)from the apex of the broken P3 (blue) to the external aperture. Arrows point to the aperture of the fistula on the maxillary bone. (For interpretation of the references to colour in thisfigure legend, the reader is referred to the web version of this article.)

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e9388

3.4. Periapical lesions

The most common type of cysts in archaeological remains areperiapical cysts (e.g. Ripamonti, 1988; Lebel and Trinkaus, 2002;Gracia, 2007). The origin of periapical cysts is an inflammatoryprocess that develops from death of the pulp due to trauma orinfection by oral bacteria (Dias and Tayles, 1997; Dias et al., 2007).The infection starts in the pulp cavity and, consequently, it willaffect all the pulp chambers and canals (Ogden, 2008b). The accu-mulation of the breakdown products resulting from the necrosiswill create the apical lesion. The infectionmay eventually dischargethrough the least resistant zone of the bone, normally the buccalrather than the lingual plate.

The mandibular and maxillary alveolar bones of Skull 5 exhibitthree osteoclastic lesions at the level of left I1, I2 and the left P3, thatcan be well defined as chronic abscesses, sensu Ogden (2008a), asthey all three display different smooth-walled sinus trackingthrough the cortical bone.

Fig. 10. Alveolar cysts on the mandible of Skull 5. (A) Frontal view. (B) Enlarged image of theScale bar 2 cm. (For interpretation of the references to colour in this figure legend, the rea

3.4.1. Periapical abscess at the level of left P3

An oval lytic lesion was observed in the left side of maxillarybone of Skull 5, at the top of a very extensive remodelled area. Itclearly represents the external aperture of a drainage canal,resulted from a fistulation process at the level of the apex of theP3 socket (Fig. 9). The shape of the lytic void is funnel shaped,measuring 2.25 mm (vertical dimension) � 2.56 mm (horizontaldimension). The surrounding bone presents a large area ofpathological alteration, abnormal bone density in the form ofporotic and periosteal remodelling, and significant bone deposi-tion that alters the morphology of the face at this point (seebelow).

It is important to bear in mind that the associated tooth, the leftP3, was broken during life (see above), and that the pulp chamberwas exposed. It is suggested that a chronic infection of this toothwas coursing when this individual died, after the development ofthe extensive maxillary bone remodelling, as the fistula crosses thecomplete bone mass to drain out the pus.

blue area shown in (A). Left I1 (left arrow) and I2 (right arrow) apical cysts are indicated.der is referred to the web version of this article.)

Fig. 11. Maxillary osteitis of Skull 5. The new bone formation and the remodelled areaoccupy a large area of the left maxilla (see text). Scale bar 2 cm.

Fig. 12. CT scan images of Skull 5. (A) Sagittal CT scan slice showing the new bone formatimaximum expression of the new bone formation of the osteitis. Differential thickness of theanterior; (P) posterior; (R) right; (L) left. Scale bar 2 cm.

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e93 89

3.4.2. Periapical cyst at the level of left I2In themandible, themost outstanding lytic bone lesion is located

inferiorly to the alveolar socket of the left I2, and its maximummeasurements are 5.25 mm (vertical dimension) � 4.62 mm (hori-zontal dimension) (Fig. 10). Morphologically, the void is character-ized bywell-defined roundmargins, and signs of bone remodelling,with porosity and bone deposition around it. In fact, this lytic lesiondisplays “a rolled and thickened rimwhere it penetrates the corticalplate of the alveolus, and the opening is often surrounded by a ‘halo’of new bone formation”, exactly as is characterized as a ‘chronicabscess’ in Ogden (2008a, Fig. 13.10).

Although the associated tooth, the left I2, has not been recoveredyet, its alveolar floor does not display any sign of bone resorption, orloss of alveolar height in its anterior aspect, indicating that thetooth loss was likely peri/post-mortem. There are no signs ofalveolar crest recession beyond a slight thickening and porositypossibly related to the concomitant periodontal disease. This wouldsupport the hypothesis of a peri/post-mortem tooth loss. It can bereasonably concluded that this tooth was also functional to thedemise of this individual. Finally, the heavy occlusal attrition (seeupper incisors) is compatible with the exposure of the pulp cavityto infective agents and the frequent development of apicalabscesses in this situation.

on caused by the osteitis. (B) This coronal CT scan slice was selected attending to thecortical bone on the left (pathological) and right (normal) are shown in figure (B). (A)

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e9390

3.4.3. Periapical cyst at the level of the left I1 (Fig. 10)The mandibular buccal wall of the first lower incisor’s sockets is

not preserved, and it cannot be determined if it was a post-mortemloss, as it shows eroded borders that could be either the result oftaphonomical erosion or remodelling. Nevertheless, it is possible toobserve at the apex of the left I1 socket a clear enlargement on thebottom (Fig. 10). It corresponds to a small lytic lesion (maximumbreadth ¼ 2.9 mm). A small, short and shallow canal runs out anddownwards from the most apical margin (see Fig. 10), probablycorresponding to a drainage groove. Moreover, the margins of theaperture are rounded and polished. Although the tooth has notbeen recovered, it is very likely that it had a heavy tooth wear, andthe pulp cavity was exposed, as it is the case for the upper incisors,indicating a possible way of infection. Taking into account all thesedata, this apical abscess was coursing at the time of death of thisindividual.

3.5. Maxillary osteitis

The most conspicuous pathological sign of Skull 5 is a boneproliferation on the left maxillary bone above the canine-molarroots (Fig. 11). After visual inspection, these lesions correspond toa chronic maxillary osteitis present for months before death, whichextends up to the orbit, medially to the lower left nasal border andlaterally to the distal M1 level, affecting the complete alveolar bonein that region.

The use of CT scanning established the incidence of concomitantanatomic variations and accurate recording the extent of thelesions (Fig. 12). The cortical bone of the left maxilla is considerablythickened (Fig. 12) reaching the thickest point at the anteriorinsertion of the inferior turbinate (3.9 mm). The thickness at thesame point on the right side is 3.7 mm. The alveolar region is also

Fig. 13. Details of Skull 5 maxillary bone remodelling. (A) General view of the left side. (B) Crthe lacrimal canal. (C) Smooth and concave remodelled area on the left inferior nasal rim, sugnew bone formation. Scale bar 2 cm.

thickened, reaching the alveolar border. At the inferior orbitalmargin, the bone is not thickened.

As described (see above) a fistular drainage canal goesthroughout the new maxillary bone formation (Fig. 9). Otheranomalous drainage patterns towards the nasal and orbital cavitiescan be deduced from the two remodelled external surfaces thatappear on the maxilla of Skull 5 (Fig. 13A). The first remodelledgroove-like surface crosses the upper part of the maxillary bone,ending some 12mm below the infero-medial lacrimal corner of theorbital socket (Fig. 13B). The new bone formation shapes a craneo-caudal groove with some collateral bony spiculae along its lateralborder.

The second anomalous groove, wider than the first one, affectsthe complete left lower nasal rim. It shows a smooth and pol-ished concave remodelled aspect (Fig. 13C). The morphology ofthis region, as well as the one previously described, fit witha drainage canal towards the nasal aperture and the nasal cavity,respectively.

The proliferative bone thickening appears localized, as well asthe remodelled regions. All the lesions seem to be developed fromor nearby the apical abscess of the left P3. Moreover, there is a boneovergrowth displaying a radial disposition (Fig. 13C). The mostconspicuous remodelling affects the area of the left inferior leftnasal rim, where the lesser alar cartilages and some of the facialmuscles insertions are placed, being the original normalmorphology completely altered (Fig. 14).

The outline of the bone thickening points to an inflammatoryreaction to the pathological process either started on the maxillarybone and/or on the concomitant soft tissues. The purpose of thisbone reaction is to aid the repair process by increasing the bloodsupply to the affected area. This can be assessed by the dilatation ofall the tiny capillaries that penetrate the bone, evident in the porouscancellous bone texture that can be observed laterally (Fig. 15).

anio-caudal groove running from the highest point of the new bone formation towardsgesting the presence of drainage via towards the nasal aperture. (D) Radial aspect of the

Fig. 14. Remodelled nasal rim of Skull 5 (A). In red, the normal (outlined) and modified(solid) anatomies of the lower nasal rim (B). (For interpretation of the references tocolour in this figure legend, the reader is referred to the web version of this article.)

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e93 91

The authors have not found a similar case than the Skull 5 in allthe available literature. For the differential diagnosis of the maxil-lary osteitis, several etiological factors were considered.

The contours of the lesion are continuous (Fig. 12), elimi-nating signs of osteoclastic activity, which would be typical of

Fig. 15. Lateral viewof themaxillary osteitis of Skull 5. (A)General viewof the left side. (B) Closthat suggests active inflammation at the time of death. (For interpretation of the references t

a neoplastic formation (see Ortner and Putschar, 1981). This,together with all the inflammatory signs mentioned above, arecompatible with an associated infectious process, as describedfor other facial regions, such as for the maxillary sinuses;resulting in a buttressing increase of bone (e.g. Wright andKellman, 2002). Their description referred only to the interiorwalls of the maxillary sinuses, but the CT scan images of theaffected cortical periostitic bone of Skull 5 reveal a similar bonedensity.

As reported in a previous study (Pérez et al., 1997), “thismaxillary osteitis could resemble a late lesion of a non-veneraltreponematosis”. However, none of the postcranial elements thathave been found so far in the SH site display any sign compatiblewith this diagnosis.

A focalized osteomyelitis cannot be discarded, as in somecases this kind of bone infection can be found localized in onlyone type of bone tissue (Douglass and Trowbridge, 1993). In thiscase, the bone infection should be present only on the periostiumand the cortical bone. Nevertheless, the density of the new boneformation, as well as the absence of disorganized structures,sequestra and osteolysis, makes the osteomyelitis diagnosis lessprobable.

Having only the bony evidence, an associated infection of therelated soft tissues cannot be discarded. If the adjacent musculartissue has a severe and chronic infection, it is possible that theinfection spread towards and through the periostium and thecortex of the subjacent bony tissue. This was a likely possibility inthe case of Skull 5’s osteitis, as it is focused in a small area, but alsoremodelled the floor of the left nasal cavity. Whether this intenseosteitis could have been the cause of death of this individual or notis difficult to prove. However, it is important to note that the entireregion affected corresponds to the so-called “maxillofacial deathpyramid”, where the nature of the blood supply makes this areasusceptible for retrograde infections from the nasal area to thebrain (e.g., Binder et al., 2010; Zhang and Stringer, 2010). Thevenous communication between the facial veins and the cavernoussinus inside the cranial vault potentially allows the direct spreadinto the brain of infections located in the “triangle” that covers fromthe corners of the mouth to the bridge of the nose (Zhang andStringer, 2010). A single heavy blow on the left side of the face(breaking the left P3) could have triggered themaxillary osteitis andthe abscess at the left P3 apex, both active at the moment of theSkull 5 individual’s death (and probably associated with a serioussoft tissue injury).

e-upof the blue area in (A), showing theporous surface on the lateral borderof the osteitiso colour in this figure legend, the reader is referred to the web version of this article.)

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e9392

4. Conclusions

A detailed palaeopathological study was presented of the oro-facial lesions present in Skull 5 from Sima de los Huesos site. Apartfrom testing previous diagnosis and identifying unreported lesions(the I1 abscess and the M3 fracture), the timing of the pathologicalevents was determined, producing the conspicuous bone growth ofthe maxilla with the aids of CT images. This is particularly impor-tant to assess the duration/chronicity of the lesions and the cause/sof them. Some physiological particularities of the region affectedcould point to the maxillary osteitis and concomitant infection asa probable cause of death.

This study reveals several dental lesions in Skull 5, such asremodelling and recession of the alveolar crest, calculus deposits,several apical abscesses and root exposure. These pathological signsare compatible with at least moderate periodontal disease that,together with the severe dental attrition and teeth fractures wouldpoint to an intense and heavy use of dentition. In addition, anom-alous wear facets are compatible with the use of toothpicks,probably associated with the denudation of the roots. All apicalabscesses were active at the time of death of Skull 5.

Apart from these dentognathic lesions, the left maxilla presentsan anomalous growth that alters the external morphology of theface. Taking into account all the pathological signs in this region,the differential diagnosis allows discarding neoplastic formationand other infectious diseases such as non-venereal treponematosisfor the maxillary osteitis of Skull 5. Thus, the pathological bonyevidence present in Skull 5 is only a slight reflection of a hardtrauma suffered by the bone itself and the broken P3, provoking thelocalized spread of the infection to the associated soft tissues, andeventually evolving into a chronic infection, probably with pain andfunctional masticatory disability, apart from obvious externaldeformation of the face. The maxillary infection coursed duringa long time, and the broken premolar became infected afterwards,as the fistula crosses the new bone formation.

This individual could have suffered a heavy impact, developingan important chronic infection. Whether that could have resultedin a septicaemia and be a possible cause of death is difficult toprove. However, the described lesions affect the so-called “maxil-lofacial death pyramid”, whose particular vascular anatomy wouldallow the spread of facial infections directly to the brain.

Acknowledgements

We wish to thank the Atapuerca Research and Excavation Teamfor their work in the field, especially at the Sima de los Huesos site.This research was supported with funding from the DirecciónGeneral de Investigación of the Spanish Ministerio de Ciencia eInnovación (MICINN), Project N� CGL2009-12703-C03-03 and 01.Excavations at the Atapuerca sites are funded by the Junta deCastilla y León, Project N� BU005A09 and Fundación Atapuerca. AnaGracia-Téllez has a Contract e Grant from the Ramón y CajalProgram, RYC-2010-06152. Laura Martín-Francés is beneficiary ofa predoctoral grant of the Fundación Atapuerca. Alejandro Bonmatíreceived a predoctoral grant from the Fundación Atapuerca/Duquesde Soria. To Almudena Alcázar de Velasco, for her etching of Skull 5used to compose Fig. 1 and for her help and assistance; to JavierTrueba and the Centro Mixto UCM-ISCIII investigation team forsome of the photographs; to Francisco Gracia, Richard Téllez andRolf Quam for help with the English; to Dr. Anthony Bartziokas, forfruitful discussions and some photographs; to Laura Rodríguez,Rebeca García, Elena Santos and José Miguel Carretero, for theirtechnical assistance with the CT scan and Mari Cruz Ortega for herhelp with restoration of the specimen.We also thank the FundaciónAncestros, for technical support. Special thanks are given to the

reviewers Drs. Alan R. Ogden and Eugenia Cunha, who have showntheir strong interest in this work by carefully examining it andproviding very helpful comments.

References

Arsuaga, J.L., Carretero, J.M., Martínez, I., Gracia, A., 1991. Cranial remains and longbones from Atapuerca/Ibeas (Spain). Journal of Human Evolution 20, 191e230.

Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Carbonell, E., 1993. Three newhuman skulls from the Sima de los Huesos Middle Pleistocene site in Sierra deAtapuerca, Spain. Nature 362, 534e537.

Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Lorenzo, C., García, N.,Ortega, A.I., 1997a. Sima de los Huesos (Sierra de Atapuerca, Spain): the site.Journal of Human Evolution 33, 109e127.

Arsuaga, J.L., Martínez, I., Gracia, A., Lorenzo, C., 1997b. The Sima de los Huesoscrania (Sierra de Atapuerca, Spain): a comparative study. Journal of HumanEvolution 33, 219e281.

Arsuaga, J.L., 2010. Terrestrial apes and phylogenetic trees. Proceedings of theNational Academy of Sciences 107, 8910e8917.

Bermúdez de Castro, J.M., Bromage, T.G., Fernández-Jalvo, Y., 1988. Buccal striationson fossil human anterior teeth: evidence of handedness in the middle and earlyUpper Pleistocene. Journal of Human Evolution 17, 403e412.

Bermúdez de Castro, J.M., Arsuaga, J.L., Pérez, P.-J., 1997. Interproximal grooving inthe Atapuerca-SH hominid dentitions. American Journal of Physical Anthro-pology 102, 369e376.

Bermúdez de Castro, J.M., Martinón-Torres, M., Lozano, M., Sarmiento, S., Muela, A.,2004. Paleodemography of the Atapuerca-Sima de los Huesos hominin sample:a revision and new approaches to the paleodemography of the EuropeanMiddle Pleistocene population. Journal of Anthropological Research 60, 5e26.

Binder, D.K., Sonne, D.C., Fischbein, N.J., 2010. Cranial Nerves: Anatomy, Pathology,Imaging. Thieme Medical Publishers, New York.

Bonmatí, A., Arsuaga, J.L., 2005. Inventory and preliminary description of MiddlePleistocene pelvis remains from the site of Sima de los Huesos, Atapuerca(Spain). American Journal of Physical Anthropology S40, 76.

Bonmatí, A., Gómez-Olivencia, A., Arsuaga, J.L., Carretero, J.M., Gracia, A., Martínez, I.,Lorenzo, C., Bermúdez de Castro, J.M., Carbonell, E., 2010. Middle Pleistocenelower back and pelvis froman agedhuman individual from the Simade losHuesossite, Spain. Proceedings of the National Academy of Sciences 107, 18386e18391.

Brace, C.L., 1962. Refocusing on the Neanderthal problem. American Anthropologist64, 729e741.

Brothwell, D.R., 1981. Digging up Bones. Oxford University Press, Oxford.Carretero, J.M., Arsuaga, J.L., Lorenzo, C., 1997. Clavicles, scapulae and humeri from

the Sima de los Huesos site (Sierra de Atapuerca, Spain). Journal of HumanEvolution 33, 357e408.

Clarke, N.G., Hirsch, R.S., 1991. Tooth dislocation: the relationship with tooth wearand dental abscesses. American Journal of Physical Anthropology 85, 293e298.

Cunha, E., Ramirez Rozzi, F., Bermúdez de Castro, J.M., Martinón-Torres, M.,Wasterlain, S.N., Sarmiento, S., 2004. Enamel hypoplasias and physiologicalstress in the Sima de los Huesos Middle Pleistocene hominins. American Journalof Physical Anthropology 125, 20e231.

De Poncins, G., 1941. Kablooma. Reynal, New York.Dias, G., Tayles, N., 1997. “Abscess cavity” e a misnomer. International Journal of

Osteoarchaeology 7, 548e554.Dias, G.J., Prasad, K., Santos, A.L., 2007. Pathogenesis of apical periodontal cysts:

guidelines for diagnosis in palaeopathology. International Journal of Osteo-archaeology 17, 619e626.

Douglass, G.D., Trowbridge, H.O., 1993. Chronic focal sclerosing osteomyelitisassociated with a cracked tooth: report of a case. Oral Surgery, Oral Medicine,Oral Pathology 76, 351e355.

Dowsett, S.A., Archila, L., Segreto, V.A., Eckert, G.J., Kowolik, M.J., 2001. Periodontaldisease status of an indigenous population of Guatemala, Central America.Journal of Clinical Periodontology 28, 663e671.

Gómez-Olivencia, A., Carretero, J.M., Arsuaga, J.L., Rodríguez-García, L., García-González, R., Martínez, I., 2007. Metric and morphological study of the uppercervical spine from the Sima de los Huesos site (Sierra de Atapuerca, Burgos,Spain). Journal of Human Evolution 53, 6e25.

Gómez-Olivencia, A., Arsuaga, J.L., Carretero, J.M., Gracia, A., Martínez, I., 2011.A Complete Neck From Sima de los Huesos and the Evolution of the CervicalSpine in Neandertal Lineage. Proceedings of the Inaugural Meeting of EuropeanSociety for the Study of Human Evolution, Leipzig, Germany, 41 p.

Gracia, A., Arsuaga, J.L., Martínez, I., Lorenzo, C., Carretero, J.M., Bermúdez deCastro, J.M., Carbonell, E., 2009. Craniosynostosis in the Middle Pleistocenehuman Cranium 14 from the Sima de los Huesos, Atapuerca, Spain. Proceedingsof the National Academy of Sciences 106, 6573e6578.

Gracia, A., Martínez-Lage, J.F., Arsuaga, J.L., Martínez, I., Lorenzo, C., Pérez-Espejo,M.Á.,2010. The earliest evidence of true lambdoid craniosynostosis: the case of “Ben-jamina”, a Homo heidelbergensis child. Child’s Nervous System 26, 723e727.

Gracia, A., Martín-Francés, L., Martinón-Torres, M., Martínez, I., Bermúdez deCastro, J.M., Arsuaga, J.L., 2011. Anomalous Wear Facets in the Sima de los HuesosDental Sample (Atapuerca, Spain). Paleopathology Newsletter Supplement, 9.

Gracia, A., 2007. Investigaciones paleobiológicas sobre los restos craneales de loshomínidos de Atapuerca con especial referencia a los fósiles de la Sima de losHuesos. Ph.D. Thesis, Universidad Complutense de Madrid, Spain.

A. Gracia-Téllez et al. / Quaternary International 295 (2013) 83e93 93

Grippo, J.O., Simring, M., Schreiner, S., 2004. Attrition, abrasion, corrosion andabfraction revisited: a new perspective on tooth surface lesions. The Journal ofthe American Dental Association 135, 1109e1118.

Hillson, S., 2008. Dental pathology. In: Katzenberg, M.A., Saunders, S.R. (Eds.),Biological Anthropology of the Human Skeleton. John Wiley & Sons, Inc., NewJersey, pp. 301e340.

Hublin, J.J., 2009. The prehistory of compassion. Proceedings of the NationalAcademy of Sciences 106, 6429e6430.

Hylander, W.L., 1977. The adaptive significance of Eskimo craniofacial morphology.In: Dahlberg, A.A., Graber, T.M. (Eds.), Orofacial Growth and Development.Mouton, The Hague, pp. 129e169.

Kaifu, Y., Kasai, K., Townsend, G.C., Richards, L.C., 2003. Tooth wear and the “design”of the human dentition: a perspective from evolutionary medicine. Yearbook ofPhysical Anthropology 46, 47e61.

Lebel, S., Trinkaus, E., 2002. Middle Pleistocene human remains from the Bau del’Aubesier. Journal of Human Evolution 43, 659e685.

Lozano, M., Bermúdez de Castro, J.M., Martinón-Torres, M., Sarmiento, S., 2004.Cutmarks on fossil human anterior teeth of the Sima de lo Huesos site (Ata-puerca, Spain). Journal of Archaeological Science 31, 1127e1135.

Lukacs, J.R., Pastor, R.F., 1988. Activity-induced patterns of dental abrasion inprehistoric Pakistan: evidence from Mehrgarh and Harappa. American Journalof Physical Anthropology 76, 377e398.

Martínez, I., Rosa, M., Arsuaga, J.L., Jarabo, P., Quam, R., Lorenzo, C., Gracia, A.,Carretero, J.M., Bermúdez de Castro, J.M., Carbonell, E., 2004. Auditory capac-ities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain.Proceedings of the National Academy of Sciences 101, 9976e9981.

Martínez, I., Arsuaga, J.L., Quam, R., Carretero, J.M., Gracia, A., Rodríguez, L., 2008.Human hyoid bones from the middle Pleistocene site of the Sima de los Huesos(Sierra de Atapuerca, Spain). Journal of Human Evolution 54, 118e124.

Martínez, I., Rosa,M., Quam, R., Jarabo, P., Lorenzo, C., Bonmatí, A., Gómez-Olivencia, A.,Gracia, A., Arsuaga, J.L., 2013. Communicative capacities in Middle Pleistocenehumans from the Sierra de Atapuerca in Spain. Quaternary International 295,94e101.

Martín-Francés, L., Gracia, A., Martinón-Torres, M., Martínez, I., Bermúdez deCastro, J.M., Arsuaga, J.L., 2011. Root Hypercementosis in the Atapuerca-Sima delos Huesos Hominin Sample: Incidence and Implications. PaleopathologyNewsletter Supplement, 13-14.

Martinón-Torres, M., Gracia, A., Martín-Francés, L., Arsuaga, J.L., Carbonell, E., Ber-múdez de Castro, J.M., 2011a. Severe Dental Lesions in the First Hominin inEurope: a Case of Strong Compensatory Eruption in the Sima del ElefanteMandible (Atapuerca, Spain). Paleopathology Newsletter Supplement, 14.

Martinón-Torres, M., Martín-Francés, L., Gracia, A., Olejniczak, A., Prado-Simón, L.,Gómez-Robles, A., Lapresa, M., Carbonell, E., Arsuaga, J.L., Bermúdez deCastro, J.M., 2011b. Early Pleistocene human mandible from Sima del Elefante(TE) cave site in Sierra de Atapuerca (Spain): a palaeopathological study. Journalof Human Evolution 61, 1e11.

Martinón-Torres, M., Bermúdez de Castro, J.M., Gómez-Robles, A., Prado-Simón, L.,Arsuaga, J.L., 2012. Morphological description and comparison of the dental

remains from Atapuerca-Sima de los Huesos site. Journal of Human Evolution62, 7e68.

Molnar, S., 1971. Human tooth wear, tooth function and cultural variability. Amer-ican Journal of Physical Anthropology 34, 175e189.

Newman, H.N., Levers, B.G.H., 1979. Tooth eruption and function in an early Anglo-Saxon population. Journal of the Royal Society of Medicine 72, 341e350.

Ogden, A.R., 2008a. Advances in the paleopathology of teeth and jaws. In: Mays, S.,Pinhasi, R. (Eds.), Advances in Human Paleopathology. John Wiley & Sons,Chichester, pp. 283e307.

Ogden, A.R., 2008b. Periapical voids in human jaw bones. In: Smith, M., Brickley, M.(Eds.), Proceedings of the 8th Annual Meeting of the British Association forBiological Anthropology & Osteoarchaeology. British Archaeological ReportsInternational Series, 1743. Archaeopress, Oxford, pp. 51e56.

Ortner, D.J., Putschar, W.G., 1981. Identification of Pathological Conditions in HumanSkeletal Remains. Smithsonian Institution Press, Washington.

Pablos, A., Martínez, I., Lorenzo, C., Gracia, A., Carretero, J.M., Arsuaga, J.L., 2011.Ankle Bones of Homo heidelbergensis From the Middle Pleistocene Site of Simade los Huesos (Atapuerca, Burgos, Spain). Proceedings of the InauguralMeeting of European Society for the Study of Human Evolution. Leipzig,Germany, 83 p.

Pérez, P.J., Gracia, A., Martínez, I., Arsuaga, J.L., 1997. Paleopathological evidence ofthe cranial remains from the Sima de los Huesos Middle Pleistocene site (Sierrade Atapuerca, Spain). Description and preliminary inferences. Journal of HumanEvolution 33, 409e421.

Quam, R., Martínez, I., Rak, Y., Hylander, W., Gracia, A., Arsuaga, J.L., 2011. NewMiddlePleistocene mandibles from the Sima de los Huesos (Sierra de Atapuerca,Spain). American Journal of Physical Anthropology 144, 244.

Ripamonti, U., 1988. Paleopathology in Australopithecus africanus: a suggested caseof a 3-million-year-old prepubertal periodontitis. American Journal of PhysicalAnthropology 76, 197e210.

Siffre, A., 1911. Note sur une usure spéciale des molaires du squelette de la Quina.Bulletin de la Société Préhistorique Française 8, 741e743.

Spencer, M.A., Demes, B., 1993. Biomechanical analysis of masticatory systemconfiguration in Neandertals and Inuits. American Journal of Physical Anthro-pology 91, 1e20.

Trinkaus, E., 1983. The Shanidar Neanderthals. Academic Press, New York.Trinkaus, E., 1989. The Upper Pleistocene transition. In: Trinkaus, E. (Ed.), The

Emergence of Modern Humans: Biocultural Adaptations in the Later Pleisto-cene. Cambridge University Press, Cambridge, pp. 42e66.

Weidenreich, F., 1937. The dentition of Sinanthropus pekinensis: a comparativeodontography of the hominids. Palaeontologia Sinica 101, 1e180.

Wright, D.L., Kellman, R.M., 2002. Craniomaxillofacial bone infections: etiologies,distributions, and associated defects. In: Greenberg, A.M., Prein, J. (Eds.), Cra-niomaxillofacial Reconstructive and Corrective Bone Surgery: Principles ofInternal Fixation Using the AO/ASIF Technique. Springer-Verlag, New York,pp. 76e89.

Zhang, J., Stringer, M.D., 2010. Ophthalmic and facial veins are not valveless. Clinical& Experimental Ophthalmology 38, 502e510.