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Malocclusion Comparison Essay

Abstract

The aim of this study was to assess the prevalence of malocclusion and its association with socio-demographic characteristics, caries experience, and level of oral hygiene in 12- to 14-year-old schoolchildren residing in two socio-economically different districts of Tanzania. A total of 1601 children (mean age 13 years, 60.5 per cent girls) attending 16 primary schools in Kinondoni and Temeke districts participated in a clinical examination and were interviewed in school settings. Chi-square and multiple logistic regression models were used to test for statistically significant differences between different groups.

The results showed that 63.8 per cent (62.6 per cent in Kinondoni and 66.0 per cent in Temeke) of the subjects had at least one type of anomaly, with a midline shift (22.5 per cent), spacing of at least 2 mm (21.9 per cent), and an open bite (16.1 per cent) being the most frequently recorded. The majority (93.6 per cent) of the children showed a Class I molar relationship. Class II and Class III malocclusions were registered in 4.4 and 2.0 per cent, respectively. Multiple logistic regression analyses, controlling for socio-demographic factors, showed that the odds ratio for having an open bite was 1.8 if residing in a less socio-economically privileged district. Subjects with decayed, missing, and filled teeth (DNFT) (>0) were 1.7, 2.1, 2.4, and 1.7, respectively, more likely to be diagnosed with a malocclusion, a midline shift, Angle Class II and III, and an open bite. Schoolchildren with fair/poor oral hygiene were less likely than their counterparts with good oral hygiene to be diagnosed with a midline shift.

Malocclusions were prevalent in the Tanzanian children investigated and were associated with environmental factors in terms of caries experience and residing in a less affluent district. Preventive programmes to combat the prevalence of malocclusion are recommended.

Introduction

Planning orthodontic treatment within a public health system requires information on the prevalence and distribution of malocclusions (Foster and Menezes, 1976). A malocclusion is defined as an irregularity of the teeth or a malrelationship of the dental arches beyond the range of what is accepted as normal (Walther et al., 1994). Malocclusion is one of the most common dental problems in mankind, together with dental caries, gingival disease, and dental fluorosis (Dhar et al., 2007). Maloccluded teeth can cause psychosocial problems related to impaired dentofacial aesthetics (Kenealy et al., 1989), disturbances of oral function, such as mastication, swallowing, and speech (Proffit and Fields, 2000), and greater susceptibility to trauma (Grimm et al., 2004) and periodontal disease (Greiger, 2001).

Numerous studies have been published regarding the prevalence of malocclusion in various populations. The results have shown wide variations, with the reported prevalence ranging from 39 to 98 per cent (Table 1). Differences in the age ranges of the populations studied, ethnicity, and the number of subjects examined could explain some of the variations (Abu Alhaija et al., 2005). Moreover, differences in the registration methods are probably the most important factors explaining these variations.

Table 1

Percentage distribution of malocclusions in children and adolescents in different ethnic groups.

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In Tanzania, a number of epidemiological studies have provided evidence of the prevalence of malocclusion in the child population. Kerosuo et al. (1988) examined schoolchildren aged 11–18 years in the city of Dar es Salaam and found that 96 per cent of the 642 children had a Class I molar occlusion, whereas 3, 1, and 16 per cent had a distal occlusion, mesial occlusion, and crowding, respectively. The overall prevalence of malocclusion was reported to be 45 per cent (Kerosuo et al., 1991). In a sample of 353 12-year olds from Bukoba and Moshi (townships in the northern parts of Tanzania), a Class I occlusion was observed in 90 per cent while a large overjet (>3.5 mm), deep bite (≥3.5 mm), and spacing were found in 35, 35 and, 50 per cent, respectively (Mugonzibwa et al., 1990). Another study in Dar es Salaam examined 698 schoolchildren aged 6–18 years. In all, 93–96 per cent of the children showed a Class I molar occlusion, 9–13 per cent an anterior open bite (AOB), and more than 33 per cent spacing (Mugonzibwa, 1992). In a further study (Mugonzibwa et al., 2004) considering 869 schoolchildren (3–16 years) in Dar es Salaam, found an overall prevalence of malocclusion of up to 51 per cent. Recently, the overall prevalence of malocclusion among 289 schoolchildren (12–15 years) in Moshi was reported to be 97.6 per cent (Rwakatema et al., 2006). Thus, earlier reports indicate a wide variation in the prevalence of malocclusion among Tanzanian children.

Previous attempts to investigate a possible association of malocclusion and dental caries have shown conflicting or inconclusive results (Helm and Petersen, 1989a; Stahl and Grabowski, 2004). While some authors reported a positive association between malocclusion and dental caries (Gábris et al., 2006; Nobile et al., 2007), others could not establish any significant relationship (Helm and Petersen, 1989a; Stahl and Grabowski, 2004). Moreover, conflicting results have been obtained in studies considering a possible relationship between malocclusion and various oral hygiene measures (Ramfjord, 1987). The presence of a positive association between malocclusion and periodontal health has been described by Helm and Petersen (1989b) and Gábris et al. (2006), yet, other studies found no association when the amount of plaque, calculus, gingivitis, or pocketing was related to various indices of malocclusion (Katz, 1978; Buckley, 1980).

The relationship between dental caries, oral hygiene, and malocclusion has not yet been investigated in Tanzania. Since the Tanzanian oral health policy gives priority to children as a target group for oral health care services (Ministry of Health, 2002), such information is worthy of consideration. Knowledge concerning the distribution of malocclusion in the child population and the identification of predisposing factors and associated conditions might help in understanding its occurrence and assist public health policy makers improve interventions (Frazão and Narvai, 2006). Considering the varying prevalence of malocclusion that has been reported among Tanzanian children, the wide age ranges and mixed ethnicity of the investigated groups, the relatively small sample sizes employed, and the fact that many studies have been confined to only one district, a large-scale epidemiological study was, therefore, conducted focusing on schoolchildren aged 12–14 years residing in two socio-economically different districts of Tanzania. This study aimed to assess the prevalence of malocclusion and its distribution by socio-demographic characteristics, dental caries experience, and oral hygiene status.

Subjects and methods

Subjects

The study was carried out in Kinondoni and Temeke districts of the Dar es Salaam region in Tanzania (Fig. 1). These two districts differ in that Kinondoni (with a higher employment rate, literacy rate, and proportions of the population using electricity) is more affluent than Temeke (National Bureau of Statistics, 2004). A stratified proportionate two-stage cluster sampling design with public primary schools as the primary sampling unit was utilized. One thousand six hundred and one (632 boys, 969 girls) primary schoolchildren aged 12–14 years were randomly selected from 16 schools from a total of 220 public schools. The schools were selected from urban and rural areas of the two districts covering different socio-economic background. Lists of all schoolchildren in the 16 selected schools with information on age and gender were collected from the schools. Selected children fulfilled the inclusion criteria of being in the defined age range of 12–14 years and in the permanent dentition. Only consenting subjects were included in the study and none of the pupils invited for participation had a history of orthodontic treatment (either interceptive or elective). A detailed description of the sampling procedure has been published previously (Mtaya et al., 2008). Ethical approval was obtained from all relevant persons, authorities, and committees in Tanzania. These included written permission from the Research and Publication Committee of the Muhimbili University of Health and Allied Sciences. Permission to work with school children was obtained from Kinondoni and Temeke municipalities, their respective educational authorities, school administrations, parents, and the children.

Interview

Before being clinically examined, the participants completed a questionnaire in a face-to-face interview undertaken by two trained research assistants. The content and performance of the interview has been described in detail previously (Mtaya et al., 2007).

Clinical examination

One trained and calibrated examiner (MM) conducted all clinical examinations in a classroom setting with natural daylight as the source of illumination and with an assistant recording the observations. Participants identified with problems that needed treatment were referred or advised to seek treatment at the two municipal hospitals of Kinondoni and Temeke districts. Oral health education sessions were provided for all participants. Before commencing the present investigation, a pilot study on 63 children was performed. Caries experience was assessed in accordance with the criteria by the World Health Organization (1997). Oral hygiene was assessed using the simplified oral hygiene index (OHI-S) (Greene and Vermillion, 1964). This index was developed to assess oral hygiene status, by combining the average individual or group debris and calculus scores (Greene and Vermillion, 1964). Occlusion was registered according to Björk et al. (1964), with some modifications by al-Emran et al. (1990).

Sagittal molar occlusion.

The basic Angle classification was used. The intermaxillary relationship of the first permanent molars was registered as Class I (normal/neutral) when the mesiobuccal cusp of the maxillary first permanent molar occluded with the mesiobuccal groove of the mandibular first permanent molar. A Class II (distal) or Class III (mesial) molar occlusion was recorded when there was deviation of at least one-half cusp width distally or mesially to Class I, respectively. It was recorded as Class I (CL I = 1), II (CL II = 2), and III (CL III = 3) and dichotomized into 0 (CL I) and 1(CL II and III) for use in cross-tabulation and logistic regression analysis. No registration was made when the first permanent molars were missing.

Overjet.

Overjet is the distance from the most labial point of the incisal edge of maxillary right central incisor to the most labial surface of the corresponding mandibular incisor measured to the nearest half millimetre, using a metal ruler parallel to the occlusal plane. A positive value (maxillary overjet) was recorded if the upper incisor was ahead of the lower incisor and a negative value (mandibular overjet) when the upper incisor was behind the lower incisor.

Maxillary overjet was categorized as 1, 1–4.9 mm (grade 1); 2, 5–8.9 mm (grade 2); and 3, ≥9 mm (grade 3). It was considered increased when the value exceeded 5 mm and dichotomized into 0 < 5 and 1 ≥ 5 mm for use in cross-tabulation and logistic regression analyses.

Mandibular overjet was coded as 0, absent; 1, <0 to −1.9 mm (grade 1); and 2, ≤−2 mm (grade 2) and recoded into 0 = absent and 1 = present (1 and 2).

Overbite.

Overbite is the vertical overlap of incisors, measured to the nearest half millimetre vertically from the incisal edge of the maxillary right central incisor to the incisal edge of the corresponding mandibular right incisor. If the right central incisor was missing or fractured, it was substituted by the left central incisor. It was coded as 1, 0.1–2.9 mm (grade 1); 2, 3–4.9 mm (grade 2); and 3, ≥5 mm (grade 3) and then recoded into 0 = absent (<5 mm) and 1 = present (≥5 mm). It was considered as a deep bite when the value exceeded 5 mm.

Open bite.

An AOB was recorded when there was no vertical overlap of the incisors, measured to the nearest half millimetre. A visible space between antagonistic fully erupted canines, premolars, or molars was registered as a lateral open bite. An open bite was coded as 0, absent; 1, 0–1.9 mm (AOB grade 1); 2, ≥2 mm (AOB grade 2); and 3, lateral open bite and recoded into 0 = absent and 1 = present (1, 2, and 3).

Lateral crossbite.

A lateral crossbite was registered when one or more buccal cusps of the mandibular canines, premolars, and/or molars occluded bucally to the buccal cusps of the maxillary antagonists, recorded as 1, absent; 2, present unilaterally; or 3, present bilaterally. It was then dichotomized into 0 = absent (1) and 1 = present (2 and 3).

Scissor bite.

A scissor bite was registered when any of the maxillary premolars and/or molars totally occluded to the buccal surface of the opposing mandibular teeth, recorded as 1, absent; 2, present unilaterally; or 3, present bilaterally. It was then dichotomized into 0 = absent (1) and 1 = present (2 and 3).

Midline shift.

A midline shift was defined as non-coincident upper and lower midlines when the posterior teeth were in maximum intercuspation. It was coded as 1, absent and 2, present when the displacement was at least 2 mm or more. It was then recoded into 0 = absent (1) and 1 = present (2).

Crowding.

Crowding was recorded when the total sum of slipped contacts measured in the segment was at least 2 mm. It was coded as 1, absent; 2, present upper jaw; 3, present lower jaw; and 4, present both jaws. It was then recoded into 0 = absent (1) and 1 = present (2, 3, and 4).

Spacing.

Spacing was recorded when the total spacing was at least 2 mm in a segment. It was coded as 1, absent; 2, present upper jaw; 3, present lower jaw; and 4, present both jaws. It was then recoded into 0 = absent (1) and 1 = present (2, 3, and 4).

A sum score of malocclusions was constructed for use in cross-tabulation and logistic regression, based on the diagnosis of the absence (0)/presence (1) of the following recordings: maxillary overjet, mandibular overjet, Class II and Class III molar occlusions, open bite, deep bite, lateral crossbite, scissor bite, midline shift, crowding, and spacing.

Statistical analyses

Data were analysed using the Statistical Package for Social Sciences version 14.0 (SPSS Inc., Chicago, Illinois, USA). Test–retest reliability for the clinical parameters was assessed using Cohen's weighted kappa statistics. Cross-tabulation and chi-square statistics were used to assess bivariate relationships. Multivariate analysis was conducted using multiple logistic regression analysis. The P value for statistical significance was set at 0.05.

Test–retest reliability

Duplicate clinical examinations were carried out by the same examiner (MM) on a randomly selected subsample of 71 participants considered to be representative of the study subjects, after a time interval of 3 weeks. Analyses performed on the duplicate examination recordings gave Kappa values of 0.78, 0.79, 0.82, 0.93, and 0.97 for midline shift, deep bite, mandibular overjet, maxillary overjet, and spacing, respectively. The Kappa values for open bite, sagittal molar relationship, crossbite, scissor bite, and crowding were 1. Intraexaminer consistencies for decayed, missing, and filled teeth (DMFT) and OHI-S scores gave Kappa values of 0.93 and 0.74, respectively. These figures indicate very good intraexaminer reliability (World Health Organization, 1997).

Results

Sample profile

A total of 1003 children from Kinondoni (63.5 per cent urban, 58.9 per cent girls, mean age 13.1 years) and 598 children from Temeke (82.3 per cent urban, 63.2 per cent girls, mean age 13.0 years) completed an extensive personal interview and underwent a full-mouth clinical examination. The mean DMFT scores were 0.37 [standard deviation (SD) = 0.86] and 0.39 (SD = 0.84) in Kinondoni and Temeke, respectively. Corresponding OHI-S scores were 1.0 (SD = 0.53, range 0.0–3.3) and 1.2 (SD = 0.54, range 0.0–4.2). Finger sucking was reported by 12.1 per cent of the total sample. The percentage distribution of participants’ socio-demographic characteristics, DMFT scores, OHI-S score, and sucking habits according to the district of residence are shown in Table 2.

Table 2

Distribution of socio-demographic characteristics, decayed, missing, and filled teeth (DMFT), simplified oral hygiene index (OHI-S) status, and sucking habits in Kinondoni and Temeke districts.

Variables Categories Kinondoni % (nTemeke % (nP value 
Gender Male 41.1 (412) 36.8 (220) 0.050 
Female 58.9 (591) 63.2 (378) 
Age 12 years 26.1 (262) 23.9 (143) 0.033 
13 years 41.9 (420) 48.5 (290) 
14 years 32.0 (321) 27.6 (165) 
Parental education Both low 38.5 (210) 53.8 (149) <0.001 
One low/one  high 24.2 (132) 20.9 (58) 
Both high 37.2 (203) 25.3 (70) 
Place of residence Urban 63.5 (637) 82.3 (492) <0.001 
Rural 36.5 (366) 17.7 (106) 
DMFT 78.3 (785) 77.6 (464) 0.399 
≥1 21.7 (218) 22.4 (134) 
OHI-S score Good 68.0 (682) 61.9 (370) 0.007 
Fair/poor 32.0 (321) 38.1 (228) 
Sucking habit No 88.5 (888) 86.8 (519) 0.301 
Yes 11.5 (115) 13.2 (79) 
Variables Categories Kinondoni % (nTemeke % (nP value 
Gender Male 41.1 (412) 36.8 (220) 0.050 
Female 58.9 (591) 63.2 (378) 
Age 12 years 26.1 (262) 23.9 (143) 0.033 

Citation: Sarig R, Slon V, Abbas J, May H, Shpack N, Vardimon AD, et al. (2013) Malocclusion in Early Anatomically Modern Human: A Reflection on the Etiology of Modern Dental Misalignment. PLoS ONE 8(11): e80771. https://doi.org/10.1371/journal.pone.0080771

Editor: David Frayer, University of Kansas, United States of America

Received: August 4, 2013; Accepted: October 15, 2013; Published: November 20, 2013

Copyright: © 2013 Sarig et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The study was supported by Dan David Foundation and the Tassia and Dr. Joseph Meychan Chair for the History and Philosophy of Medicine. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Malocclusion in general, and dental crowding in particular, are very rare findings among human fossils [1]. Several intrinsic and extrinsic factors (e.g., better adjustment between teeth and jaw size, different type and rate of dental attrition) have been proposed to explain the scarcity of these phenomena among our ancestors [2-4]. Nevertheless, since malocclusions can be examined only in well preserved skulls that have most of their teeth intact (to explore both the intra and inter-arch conditions) [5], evaluation of occlusal state is limited to very few fossils. It is therefore essential, when such an opportunity exists, to carry out a detailed orthodontic study in order to better understand our ancestors' masticatory system, by which we will be able to shed light on present day malocclusions. The Qafzeh 9 skull presents a well-preserved dentition of both the upper and lower jaws, allowing the exploration not only of the intra-arch condition, but also of inter-arch occlusion.

Malocclusions are common in modern populations [6]. The most common condition is the anterior cross bite, found in 4-5% of the population, which usually develops at the early mixed-dentition stage [7-9]. In this condition, one or more primary or permanent mandibular incisors occlude labially against their antagonists, or one or more maxillary incisors are lingual to their antagonists [10]. Crowding is often ‘blamed’ for anterior cross bite [11], although other factors have been mentioned.

The etiology of cross bites (and Class I malocclusions in general) usually involves the initial position of the tooth buds and the environmental pressure that guides the eruption sequence [11]. Naturally, this pathology can occur only if the pressure lasts long enough to affect the displacement of the tooth buccally or palatally. Several factors have been suggested as the cause for anterior cross bite, including a lingual eruption path in the maxillary anterior incisors; trauma to the primary incisor resulting in lingual displacement of the permanent tooth germ; supernumerary anterior teeth; an over-retained necrotic or pulpless deciduous tooth or root; odontomas; crowding in the incisor region; inadequate arch length; and a habit of biting the upper lip [12-14].

There is a general agreement that anterior cross bite is often caused by modification in the masticatory function together with genetic or developmental components [11]. Abnormal occlusal interference (e.g. early tooth contact) caused by a constricted upper arch or a local factor such as a malposed tooth can result in mandibular displacement in centric occlusion. A mandible pushed laterally or anterior-posteriorly due to occlusal interferences can cause functional asymmetries, which in turn can prevent proper intercuspation in the centric relation [15].

The purpose of this study is to examine the occlusal condition in the Qafzeh 9 specimen in light of modern knowledge regarding the etiology of malocclusion.

Materials and Methods

The Qafzeh 9 specimen

The Qafzeh Cave is located in the slope of Har Qedumim (Jebel Qafzeh) Lower Galilee, on the eastern bank of the Nahal Mizra (Wadi el-Haj) creek, in the Jezreel Valley, Israel. The dates for the site range between 94 ka to 115 ka [16-18].

The first excavations were conducted by R. Neuville and M. Stekelis in 1933-1935, during which the remains of seven individuals were uncovered in the Middle and Upper Palaeolithic layers. Excavations were renewed between 1965 and 1979 by B. Vandermeersch. During the excavations, the skeletal remains of several additional individuals, adults and immatures, were discovered in the Middle Palaeolithic layers [19,20].

The hominids found at Qafzeh were recognized as anatomically modern humans even though some primitive archaic features were present [19,21]. The occurrence of purposeful human burials, hearths, ochre and non-edible marine shells in the cave has been interpreted as evidence for the existence of a symbolic culture (see, among others, [19,22,23].

The skeleton and skull of Qafzeh 9, the subject of this paper (Figure 1), was found buried with the child Qafzeh 10, in the Mousterian layer XVII. Qafzeh 9 dental estimation exhibits open root apex of the third molar therefore, age of death was estimated to be between late adolescence and adulthood probably 16 and 21 years [24]. Two gender determinations were proposed based on pelvic study [19,25]. Recent analysis enhanced the assumption of female determination [24,26].

Qafzeh 9 was found lying on its right side, in a semi-flexed position. The Qafzeh 9 skeleton is the most complete specimen found to date at the site [19].

A detailed osteological analysis of Qafzeh 9, with an emphasis on the cranium, was conducted by Vandermeersch [19]. Later studies on Qafzeh 9’s skeleton include, among others, analysis of the pelvis [25], femur [27], patella [28], hands [29], feet [30], mandible [31-33] and teeth [34,35].

The Qafzeh 9 specimen is housed in the Anthropological Collection at Tel-Aviv University. All necessary permits were obtained for the described study, which complied with all relevant regulations.

Dental evaluation

The Qafzeh 9 skull was scanned using high resolution CT scans (iCT256, Philips Medical Systems, Cleveland, Ohio; slice thickness 0.67mm, voltage 120kV, current 298mA) taken at the Carmel Medical Center, Haifa, Israel. The scans were reviewed and analyzed using an “Extended Brilliance Workspace” portal (v2.6.0.27) (Philips Medical Systems, Cleveland, Ohio). 

The following aspects of the jaws were evaluated: teeth alignment, crowding, arch symmetry, occlusal attrition, non-occlusal attrition, occlusion and roots position.

Teeth alignment was evaluated using Andrews' definition [36].

Dental crowding was evaluated on CT scans following Proffit method [11]: arch circumference (not including the molars) was measured along the contact points and subtracted from the mesial-distal size of the teeth (premolars, canines, and incisors) (Figure 2).

Figure 2. Evaluation of crowding.

First, arch circumference (not including the molars) was measured along the contact points (a), then the sum of the mesial-distal sizes of the same teeth was measured (b). Crowding was calculated by subtracting arch circumference from the sum of all mesial-distal sizes of the teeth.

https://doi.org/10.1371/journal.pone.0080771.g002

Arch symmetry was measured relatively to the mid-palatal suture (MPS) in the upper arch, and relatively to a midline drawn perpendicular to the central incisors in the lower arch (Figure 3).

Figure 3. Occlusal view of the arches; crowding and asymmetry.

(a) Occlusal view of the upper arch; (b) and of the lower arch. Note that upper arch symmetry and upper dental midline (UML) was evaluated relative to the palatal midline suture (MPS).

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Occlusal attrition rate was based on the Molnar scale [37]. Malocclusion was recognized following Andrews' definition [36]. Evaluation of occlusion status was problematic since the mandible could not be fitted to the maxilla properly, i.e., it was not possible to occlude the mandible in a manner that allows the condyles to seat in the fossa while matching the attrition facets. This could be due to post mortem changes or reconstruction difficulties both in the mandible and the skull. Therefore, a setup was used to evaluate occlusion in this skull. An impression of the lower arch was taken using a two-stage polyvinyl-siloxane (PVS) impression (Coltene Whaledent Germany). The cast was then created using dental stone material (orthodontic plaster type II, WhipMix, USA). The setup was carried out only for areas of the jaw where a previous reconstruction was carried out. The setup teeth were separated along the contact points and re-aligned to allow maximal intercuspation. The teeth of the setup were placed in maximal intercuspation.

Roots examination was carried out in order to appreciate the possibility of trauma. The roots of the upper incisors were examined (using CT scans) for the presence of fractures and root resorption. The position of the upper lateral incisors roots was measured as the distance from the midpoint marked on the buccal surface of the root to the line connecting the buccal midpoints of the canines and central incisors (Figure 4). This procedure was carried out for both the apical and the gingival segments.

Results

Dental alignment and crowding

From an occlusal view, the upper arch appears oval (Figure 3). The right central incisor is in mesio-buccal rotation. The upper left lateral incisor is palatally positioned (Figure 3). The left second premolar (PM) tilts palatally more than the adjacent molar. As a result, the contact point on the crown of the second PM is more buccally situated, whereas the one on the molar is positioned more palatally. The lower jaw arch corresponds to the oval shape of the upper jaw, its teeth are properly aligned. The left canine is slightly tilted buccally.

The upper jaw's arch circumference is 86.2 mm, whereas the accumulated teeth's mesiodistal size is 92 mm, resulting in 5.8 mm of crowding (Figure 2). The mesiodistal diameter of the right central incisor (11.9 mm) is wider than the left (9.4 mm). The lack of interproximal attrition in the right central incisor left it with undisturbed morphology: a round distal margin with pronounced height of contour.

Arch symmetry

The breadth of the left half of the hard palate (measured at the second PM's level) was narrower than the right (Figure 3). The upper midline (UML) deviates (from the MPS) to the left by 2 mm (Figure 3). From a frontal view, the central incisors tilt towards the left (Figure 5).

Although part of the lower arch asymmetry (Figure 3) is due to mal-reconstruction, a high degree of asymmetry is preserved on the setup. The deviation from the central line is more marked on the right side (Figure 3). This finding corresponds with the finding on the upper jaw.

Occlusal and non-occlusal attrition

Occlusal attrition was slight (stage 1-2 on the Molnar scale), except for the upper and lower incisors where a patch of dentin was exposed (matching stage 3 on the Molnar scale). Beside the occlusal attrition facets, two other unique non-occlusal facets were observed: a buccal facet on the upper left lateral incisor and a lingual facet on the lower left lateral incisor (Figure 6). Interproximal attrition facets are evident in all teeth along the dental arch except for the distal surface of the upper left central incisor and mesial aspect of the upper left lateral incisor.

Occlusion

An anterior cross bite, caused by malposition of the upper left lateral incisor, is clearly seen (Figure 7). At the buccal segments (the area of molars and premolars), a shallow overbite and overjet, creating an edge-to-edge contact with a tendency for a posterior cross bite, was noticed. The palatal tipping of the left lateral incisor and the lack of contact with the antagonist lower incisor allowed the over eruption of the upper left lateral incisor.

Figure 7. Anterior cross-bite in Qafzeh 9.

An anterior cross bite caused by the malposed left lateral incisor (a). Following the setup, edge-to-edge contact with a tendency for a posterior cross bite in the buccal segments is clearly seen (b).

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Roots examination

The root of the upper left lateral incisor is palatally positioned (Figure 4); the apical area of the root is located 2.2 mm palatally to the buccal margin of the arch, while on the right, it is only 0.9 mm (Figure 4). The gingival segment of the left tooth is distanced by 3.6 mm from the buccal margin, whereas on the right side, it reaches the buccal margin of the arch (Figure 4).

Discussion

Studying occlusion in fossils is a frustrating task, not only because of the rarity of appropriate material (complete maxilla and mandible), but also since even when the two jaws are present and all teeth are intact, in many cases the jaws are distorted. When articulating the Qafzeh 9 jaws, the incompatibility between the two is evident. This is due to a noticeable deformation in the lower jaw as a consequence of inadequate reconstruction as well as post-mortem taphonomical factors (see also 33). The use of a cast setup allowed us to fix areas that were inadequately reconstructed in the past and restore the original shape of the lower dental arch. Once this was done, the teeth were placed in maximal intercuspation with attrition facets taken into account, which allowed the evaluation of the occlusion condition [38].

The most noticeable deviation from normal occlusion was the malposition of the upper left lateral incisor. It is difficult to evaluate what was the direct cause of the malposed upper left lateral incisor, as many factors might cause malposition of a single tooth. Nevertheless, trauma can be excluded since following trauma, we would expect the crown to tip palatally while the root keeps its position (or even tilts buccally). In our case, however, the root of the upper left lateral incisor is located palatally to the dental arch, indicating that the tooth position had already been established during early life (development and eruption stages). The absence of an interproximal facet on the distal surface of the upper central incisor and on the mesial surface of the lateral incisor indicates that the two teeth were never in contact. This lends additional support to our suggestion that this malocclusion did not result from a traumatic event, but rather is of developmental origin.

Relative to central incisors, lateral incisor buds are formed in a more palatal position (Figure 8a). During eruption, the lateral incisors move buccally (Figure 8b) to align with the central incisors (Figure 8c). However, early loss of deciduous tooth or crowding in the upper jaw may interfere with the normal developmental process described above and cause malposition of teeth similar to that seen in Qafzeh 9. Once this occurs, the entire biomechanical force transmission, both in the intra and inter-arch, is affected, with noticeable morphological consequences.

Figure 8. Development of the anterior dental arch.

Lateral incisors buds are formed more palatally compared to the central incisors (a) and erupt more anteriorly (b) to finally align with the central incisors (c).

https://doi.org/10.1371/journal.pone.0080771.g008

Regarding the intra-arch effect, physiologically, contact between teeth lessen the masticatory forces along the dental arch [39-41], thus preventing mesial migration of teeth [42], protecting arch integrity and avoiding food impaction [43]. The occlusal forces applied to the arch are also transformed into interproximal forces and interproximal attrition. When arch integrity is preserved, arch symmetry is kept allowing similar dissipation of force on both sides (Figure 9a). When arch continuity is interrupted, force transmission is not equal on both sides (Figure 9b). The anterior component of the force caused by the occlusal forces may result in mesialization of the teeth, midline deviation, rotations and the aggravation of crowding [44]. All these potential outcomes are evident in the Qafzeh 9 skull: the midline deviates to the left; the incisors rotate mesio-buccally; the left segment is constricted; the left first molar is buccally positioned and the left premolars palatally tilted.

Figure 9. Force transmission in the dental arch.

When arch integrity is preserved, there is similar dissipation of force on both sides maintaining arch symmetry (a). When arch continuity is interrupted (like in the Qafzeh 9 skull), force transmission is not equal on both sides (b), resulting in asymmetry, crowding, midline deviation and rotations.

https://doi.org/10.1371/journal.pone.0080771.g009

As to the inter-arch effect, when the jaws are in occlusion, the palatal position of the left lateral incisor causes the mandible to occlude in a more anterior and lateral position, resulting in a cross bite with a functional shift. This is evidenced by the buccal facet found on the maxillary left lateral incisor and the lingual facet found on the mandibular left lateral incisor of Qafzeh 9. This type of occlusion may lock the mandible in a position that does not coincide with the centric occlusion expected in this individual.

Cross bite might cause asymmetrical muscle function during chewing or clenching, as the temporalis muscle is more active and the masseter muscle less active on the cross bite side than on the non-cross bite side [45,46]. Moreover, the asymmetry in muscle activity that is associated with the cross bite might reduce the bite force [47,48].

The notion that ancient populations had better aligned dentitions than modern ones is well rooted in the anthropological and dental literature (e.g., 2,3,11,49,50). Most of the evidence was obtained from orthodontic studies carried on historical (mainly Medieval populations) or modern pre-industrial populations demonstrating low prevalence of malocclusion compared to modern populations (e.g.,[51-55]). Yet, not just that the prevalence was lower, but the severity was smaller and there was a significant sex-biased towards females [56]. It is of note worthy, however, that the above described trends have been shown for specific populations (mainly Europeans), that the time depth is limited (several hundred years), that modern populations varies in regard to malocclusion prevalence [57], and that the relative contributions of heredity and environment to the etiology of malocclusion varies among its different entities [51]. As the great obstacle in studying trends in malocclusion remained the small sample size of prehistoric skulls suitable for such studies, Vodanović and colleagues [5] have recently suggested to move from orthodontic features requiring presence of both jaws and almost all teeth to orthodontic anomalies affecting only one tooth or group of teeth. Finally, it was suggested (e.g., 58,59) that dental crowding is a result of an evolutionary trend towards a reduced jaw size, without a corresponding reduction in tooth dimension a process usually attributed to reduction in masticatory requirements due to nutritional change, i.e., softer food [60]. However, the study of the Qafzeh 9 jaws together with previous findings from Neanderthals and Upper Paleolithic skulls [61] may suggest a more complex etiology for malocclusion (for further discussion see 52,62).

In sum, the well-preserved dentition in the Qafzeh 9 skull allowed us also to orthodontically evaluate its inter and intra-arch relationships. The presence of a clear malocclusion of developmental origin in this specimen is the oldest recorded in the hominid lineage. The upper crowding and the malposed teeth affect not only the inter-arch dental alignment, but also the intra-arch association, causing an anterior cross bite with functional shift, all of which may affect the bite force and the force transmission along the dental arch.

Conclusions

The analysis of the Qafzeh 9 jaws and teeth clearly show that crowding and malocclusion are present in early anatomically modern humans. These findings challenge the notion that early anatomically modern humans had a better adjustment between teeth and jaw, and question the common theories for crowding, suggesting an increase in jaw-teeth size discrepancy towards modern times. It also questions the role of soft diet and may indirectly indicate that genetic may prevails over environment.

Acknowledgments

We thank Prof. Nathan Peled and Mati Shnapp for the CT scans. We would also like to thank Anna Behar for the graphics; and Ze'ev Stein and Ilan James for their photographs.

Author Contributions

Conceived and designed the experiments: RS ADV IH. Performed the experiments: RS VS. Analyzed the data: RS NS ADV IH. Contributed reagents/materials/analysis tools: HM JA NS. Wrote the manuscript: RS VS IH.

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