AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 85:305-312 (1991) Continuous Tooth Eruption in Australian Aboriginal Skulls P.J. DANENBERG, R.S. HIRSCH, N.G. CLARKE, P.I. LEPPARD, AND L.C. RICHARDS Department of Dentistry (P. J.D., R.S.H., N.G.C., L.C.R.) and De artment of Statistics (P.I.L.), University of Adelaide, ALlaide, South Australia 5001 KEY WORDS Attrition, Facial growth, Periodontitis ABSTRACT Increases in the distance from the cemento-enamel junction to the alveolar crest (CEJ-AC)have often been attributed to senile atrophy of the bone or to the effects of periodontitis, without reference to the condition of the alveolar crest. This study investigated the relationship between CEJ-AC distance, tooth wear, gender, site ofthe CEJ-AC measurements, and age in 161 pre-white-contact Australian aboriginal skulls. Individual teeth were included in the study when there was no evidence of dehiscence, periodontitis, or abscess cavity formation in the supporting alveolar bone. The CEJ-AC distances increased as the severity of attrition increased; in male skulls, CEJ-AC distances were greater than in female skulls for all categories of tooth wear. In general, CEJ-AC distances measured on the mesial aspects of teeth were greater than those recorded distally; lingual distances generally exceeded buccal recordings. The best explanation of these findings and similar reports in the anthropological literature is that continuous tooth eruption occurred without the concomitant coronal movement of alveolar bone. This conclusion has significant ramifications for anthropological, epidemiological,and clinical studies which use the CEJ and AC as reference points when measuring periodontal attachment loss (periodontitis). In periodontology, the normal distance from the cemento-enamel junction (CEJ) to alveolar crest (AC) is assumed to be approximately 2 mm (Davies and Picton, 19691, allowing for the attachment of the ginpval fibre network to the tooth. Increases in this distance, other than those related to dehiscent bone, enamel pearls, spurs, or grooves have been ascribed to either senile atrophy or periodontitis, even when there were no obvious signs of pathological changes at the alveolar crest. Comprehensive reviews of the different concepts of the CEJ-AC relationship have been made by Barker (1975) and Whittaker et al. (1985,1990). A gradual recession of the alveolar crest from the enamel margin between childhood and senility was observed by Lei h (19281, who noted this to be a physiologica condition rather than a athological process. Begg (1938)considerei that denudation of the root of the tooth was not necessarily a pathological process, but was the result of continuous eruption; a definite relationship was noted between attrition and eruption. However, B @ 1991 WILEY-LISS, INC root exposure was attributed to atrophy or progressive recession of the investing tissues that accompanied eruption. In skeletal remains of the primitive Eskimo, severe attrition of the anterior teeth resulted in a considerable degree of tooth eruption, which left only the root apices suported by bone (Baarregaard, 1949). In morars, severe occlusal wear resulted in separation of the roots, which continued to function. Periodontitis was absent. Baarregaard concluded that lower face height was undiminished by the severe wear and that continuous eruption resulted in maintenance of both the clinical crown and face height at the expense of tooth sup ort. In Australian aboriginal skulls, Murp y (1959)found that continuous tooth eruption and generalized alveolar bone growth were compensatory mechanisms for attrition; it was the first study to give continuous eruption quantitative support. Where severe attrition had occurred in R Received December 18,1989; accepted January 29,1991. 306 P.J. DANENBERG ET AL Maori skulls, the loss of tooth structure was compensated for by extrusion of the tooth in its socket. The worn surface was maintained in the occlusal plane but the CEJ was more coronal to that of ad’acent but less worn teeth(Taylor, 1963). easurements made on skulls using the up er border of the inferior dental canal (ID ) as a fixed marker (Newman and Levers, 1979)showed that the distance between the IDC and the occlusal surface increased in skulls (aged between 20 and 50 years). These authors also found that the distance from the IDC to the alveolar crest was constant, indicating that, despite the loss of tooth structure on the occlusal surface from attrition, continuous eruption more than compensated for loss of clinical crown height without the concomitant deposition of alveolar bone. Continuous tooth eru tion has also been observed in skulls wit minimal tooth wear (Whittaker et al., 1990). There is no evidence available to the authors to support the contention that alveolar atrophy occurs as a result of aging. Alexandersen (19671, who reviewed the relevant material available, concluded that further studies were necessary to clarify the pathogenesis of this form of “resorption” of the alveolus. It is more likely that the large CEJ-AC distances seen in older skulls were misinterpreted by early workers as senile resorption rather than continuous eru tion of the teeth. The earlier workers did, owever, recognise that the intact bone indicated an absence of periodontitis. We were unable to find an histologcal study of skeletal, autopsy, or ot er materials to support the hypothesis that senile atrophy occurs. On the contrary, a small increase in alveolar height occurs into late adulthood (Behrents 1985). Whittaker et al. (1985) found that the position of the alveolar crest remained almost constant throughout life relative to the inferior alveolar canal. In ound sections of the older skulls examined, 0th active resor tion and de osition occurred concurrent y at the alveo ar crest. In a radiographic and morphological study of skulls from a late medieval European population with no evidence of periodontitis, alveolar growth had not accompanied continuing tooth eruption (Varrela et al., 1989). However, the ‘tooth gain” resulting from continuous eruption was greater than the “bone gain” from continuing facial growth, resulting in increasing CEJ-AC distances. Clinically, measurements from the fixed muco- Id 8 K K K f P P gingival ‘unction (Ainamo, 1978) show that the attac ed gingiva increases in width from age 23 to 65 years (Ainamo et al., 19811, also indicating bone deposition rather than involution. The discrimination between physiolo ’cal and athological causes of increased FEJAC istances is difficult in the clinical setting. The widespread presence of plaque and gingivitis, and the assumption that ngiviP tis frequently progresses to perioC ontitis, confounds clinical assessments of the condition of alveolar bone. The absence of plaque and soft tissues in dry skulls sim lifies and clarifies the interpretation o alveolar changes. An intact alveolar crest with normal morphological appearance signifies the absence of periodontitis. Where continuous eruption has occurred, it is erroneous to assume that CEJ-AC measurements greater than 2 mm are due to periodontitis, particularly when the alveolar crests show no evidence of pathological changes. However, this assumption is made in contemporar periodontology. Continuous eru tion o f t e teeth in response to attrition an continuing facial growth occurring ee of growth of alveolar bone is the explanation for that have been previously reported. The aim of this stud was to correlate the degree of attrition wit the CEJ-AC distance in teeth supported by intact, non-diseased alveolar bone. h b! P t $ l MATERIALS AND METHODS The collection of pre-white-contact Australian abori ’nal skulls held by the South Australian useum was used as the resource for this study. The collection comrises skulls from diverse tribes, which inabited different locations. Skulls were included in this study if they had minimal post-mortem damage. a R Selection of Teeth Individual teeth were studied only when intact alveolar margins were present around all tooth surfaces-that is, when there was no evidence of periodontitis (as defined by the exposure of cancellous bone or alteration in its morphology),abscess cavities, or dehiscences (Fi s. 1 , 2 ) . The tee& studied were 11, PM1, M1, and M3 in each quadrant. The degree of tooth attrition was measured using the Lavelle (1973) modification of the method intro- 307 CONTINUOUS TOOTH ERUPTION Fig. 1. Anterior maxillary and mandibular teeth of an Australian aboriginal skull showing intact alveolar bone and CEJ-AC distances of approximatel 6 mm a s a result of continuous tooth eruption. (Graiuations on periodontal probe = 1,2, 3, 5, 7, 8, 9, 10mm from tip). Fig. 2. Buccal view of mandibular M1 and M2; the anatomical crowns have been almost completely removed by attrition. Continuous tooth eru tion, resulting in a CEJ-AC distance of a proximatefy 6 mm, now provides the clinical crown. &is is an example of physiological periodontal attachment loss which is not due to periodontitis; the alveolar bone is intact. duced by Davies and Pedersen (1955). Each tooth was assigned to one of four categories of tooth wear: It was modified to provide an appropriate section point for this population (Townsend et al., 1982). The ages of the skulls were estimated by the method ofRichards and Brown (1981)for Australian aborigines, which is based on the extent of attrition. Colour transparencies of the occlusal surfaces of M1 (maxillary or mandibular) were taken and orthogonally pro'ected. The outlines of the tooth crowns an exposed dentine were traced and the crown areas and areas of exposed dentine were measured from the tracings with a Hewlett Packard 9874A digitizer programmed for use as a planimeter. The data were anlayzed on the Universit of Adelaide's Vax computer using the BMD extended repeated measures program 5V (BMDP statistical software, Los Angeles, California, USA). Data obtained for each tooth were anal zed separately because each skull had a di erent complement of teeth suitable for study. The statistical model included sex and tooth wear category as between-skull factors, with site of CEJ-AC measurement as a within-skull factor. Age was included as a covariate. A fully parameterized error structure was used and statistical significance was taken at the 5% level. TW l-attrition of enamel only; TW 2-attrition into dentin; TW 3-attrition into reparative dentin; TW &attrition ex osing the pul chamber (althou h include in the researc protocol, no teet with TW 4 were recorded). a B K The CEJ-AC distance was measured at four locations per tooth at the mesio-buccal, mesio-lingual, disto-buccal, and disto-lingual corners of the teeth. Measurements were made with a dial caliper (Mitutoyo,Japan) t o an accuracy of 0.1 mm. One examiner (P.J.D.) recorded all the information; repeated measurements on a series of five skulls prior to commencement of the study indicated a low measurement error. The sex of individual skulls was assigned after examining the dimorphic features. Characteristic male features included the presence of brow rid ing, everted gonial angle, development o f t e mastoid process, and greater overall size. In ambiguous cases, the method of discriminant function analysis described by Giles and Elliot (1963)was used. fl d H x 308 P.J. DANENBERG ET AL. RESULTS A total of 98 male and 63 female skulls were examined. The number of teeth studied for each tooth t pe and the average CEJ-AC distance in ma es and females is shown in Table 1. This table uses average CEJ-AC measurements (four er tooth in each wear category)to present t e large amount of data in an easily interpreted form. The repeated measures analysis of variance used individual CEJ-AC measurements for each tooth and each tooth surface. Results are summarized for each tooth type in Table 2. Each column of this table corresponds to a term in the statistical analysis, and an entry in a column for a articular tooth indicates that a statistical significant effect was detected. Converse y, no entry implies that a significant effect was not found. Moreover, by examinin the values of the estimated arameters oftfle underlying statistical mogl, the direction of the effect could be determined. For example, for the maxillary right PM1, the gender column entry of "m > f" indicates the presence of a significant gender effect on CEJ-AC distance, with males having (on average) larger values than females. Similarly, for the same tooth, the attrition column has an entry "1 < 2 < 3" denoting both an attrition effect and its direction. In all cases where a sex effect occurs, the CEJ-AC distance is greater in males than in females. For teeth other than the RI1, RM1, and RPM1, there is a significant relationship between CEJ-AC distances and attrition; larger CEJ-AC distances are associated with more advanced wear. In addition, there is a significant positive relationship between age and CEJ-AC distance for first premolars (except mandibular left) and for first molars. The significance of the location of the CEJAC measurement varies between tooth t pes. In general, measurements made on t e mesial aspects of teeth (i.e., either mesiolingual or mesio-buccal) are greater than those recorded for distal tooth locations. For most teeth, recordings made on the lingual aspects (i.e.,mesio-lingual and disto-lingual) are greater than those recorded on the buccal aspects. T K ommN-3mommm1ocn33 N 0 ww 1 1 N 1 3 N ! i DISCUSSION a In this study, significantly lar er CEJ-AC distances were measured in teet with more advanced attrition. All teeth studied were 3 N 0 mw N 0 In N 3 m 0 e N 1 O 309 CONTINUOUS TOOTH ERUPTION TABLE 2. Statistical analysis for each tooth studied' Gender Maxillary right I1 PM 1 MI M3 I1 PMI MI M3 Maxillary left Mandibular right Attrition m>f m>f m>f 1<2<3 1<2<3 1<2<3 1<2<3 1<2<3 1<2<3 1<2<3 m>f m>f m>f I1 PM 1 MI M3 I1 PM1 Mandibular left m>f m>f M1- 1<2<3 1<2<3 1<2<3 1<2<3 1<2<3 M.? 1 <2<3 m>f Site of CEJ-AC measurement Interaction m vs. d b vs. li present m<d m>d m>d m>d m<d m>d m>d m>d m>d m<d m>d b < li b < li yes b > li b < li b < li b < li b > li yes h 0.013 0.023 yes 0.013 0.018 yes 0.024 0.017 b < li b < li b > li b < li m>d Age2 < li ves 0.019 'An entry indicates the presence a n d direction of a statistically significant effect. Abbreviations used: m, mesial; d, distal; b, buccal; li, lingual. "egression slope, if significant. supported by intact alveolar bone, indicating that the increased CEJ-AC distances resulted from continuous tooth eruption and not from senile atrophy of the alveolar bone (see Alexandersen, 1967)or from eriodontitis which has been assumed to e present when CEJ-AC distances were greater than 2 mm (Davies and Picton, 1969).Periodontitis is an unusual consequence of gingivitis in both pre-modern (Clarke et al., 1986) and modern populations (Burt, 1988). Consequently, the prevalence of eriodontitis has been overestimated in stu ies that have ignored the condition of the alveolar crest. In this study, a fixed reference oint (for example, the inferior alveolar cana )was not used to quantify the CEJ-AC distances partly for practical reasons (lack of radioaphic facilities in the museum) and partly Kr the followin theoretical reasons. The lower border o the mandible, although readily measured, is not necessaril stable over time (Whittaker et al., 1985). rn addition, the same measurement oint on the inferior aspect of the mandib e cannot be used in both youn and old skulls due to mesial driftin o f t e teeth over a lifetime. The fact that ahittaker et al. (1985) showed that the osition of the alveolar crest remained a most constant throughout life reinforced the validity of the approach taken in this study. Furthermore, our measurement method enabled data to be gathered from g B f H a f f maxillary as well as mandibular teeth. Stable reference points in the maxilla are difficult to find. Mandibular reference points cannot be used for the maxilla when quantifying CEJ-AC distances because the amount of tooth crown lost by attrition can only be estimated. Facial growth, attrition, and continuous eruption lay a si ificant role in determination o the CE -AC relationship (for a review, see Clarke and Hirsch, 1991).Dental com ensation for facial growth can occur as a resu t of the maxillary incisors moving slowly to upright over time, effectively resultingin an increase in CEJ-ACdistance. In response to continuing facial growth, maxillary first molars in the male tend to upright, whereas in females they tend to a more distal inclination (Behrents, 1985).Because of continuing facial growth, the tooth-bone relationshi is d namic, and has an influence on the CgJ-A? relationshi . In the present study, it was not possib e to measure the effects of continuing facial growth or to estimate the magnitude of its effects on the CEJ-AC distances measured. Continuous tooth eru tion may also occur in response to attrition ?Barker, 1975) or anticipated attrition (Murphy, 1959; Ainamo and Amamo, 1984).A combination of genetic and physiological factors is probably involved with the maintenance of lower face hei ht and dental articulation in compensation or attrition. P Y 'I P H 310 P.J. DANENBERG ET AL Evidence for continuous tooth eruption In addition to the present and revious anthropological studies, there are ot er lines of evidence which indicate that the active rocess never completely stops. eruption deciduous teeth have been obAnkylose served to apparently “submerge” with time, as the adjacent ermanent teeth continue to erupt. In a stu of 108 submerged deciduous molars, Darfing and Levers (1973) concluded that, although the teeth had originally erupted and reached occlusion, there was no evidence that these teeth moved apically. Rather, the apparent submergence was due to occlusal movement of the adjacent teeth and the amount of eruption of the neighbouring teeth was expressed by the degree of submergence. The greatest degrees of submergence were observed in the older patients. Many previous workers had incorrectly interpreted this phenomenon as being due to apical movement, local failure of eruption, or some fault in the bone. Submerging deciduous teeth offer unique fixed reference oints from which continuous tooth eruption as been observed and quantified. Epithelial remnants of the root sheath, which are normally found only in the periodontal ligament, have been detected below tooth apices. Since the epithelial structures cannot change their position, it is evident that they are left behind as the tooth continued to erupt. Deeper bony areas have been observed to contain isolated islands of bundle bone that were once alveolar bone, which did not move coronally with the tooth (Grant et al., 1988a). Attrition and the CEJ-AC relationship Cultural practices, the composition of the diet, and personal habits are several important factors that determine the rate of tooth wear. In the present sample of Australian aboriginal skulls, the severe attrition which occurred with increasing age often resulted in almost complete destruction of the anatomical crowns; continuous tooth eruption provided part of the mechanism for maintenance of face hei ht and continuing tooth function (Fig. 2). is process results in loss of periodontal attachment because less root surface is embedded within the bone. In Eskimos, the same physiological rocess was reported to have caused the teet to become very mobile and even to exfoliate (Baaregaard, 1949). Ainamo and Ainamo (1984) considered K cp cp R A K that continuous eruption was not strict1 a compensatory mechanism for attrition, i u t rather was a genetic function intended to compensate for anticipated wear. In populations with minor degrees of attrition, the observed increase in lower face height occurs as a result of continuing facial growth and continuous eruption. In opulations with excessive wear, lower face eight may be maintained, or decrease in s ite of continuous eruption. Maintenance o the dental articulation in a relatively stable position in the presence of continuing facial growth reuires eruption of the teeth in compensation ?or the degree of growth of the lower face Anthropological investigations also indicate that continuous eruption occurs in the presence or absence of attrition. In a study of 500 Romano-British skulls with heavy attrition, Whittaker et al. (1985)found that tooth wear was compensated by continuing movement of the teeth in an occlusal direction. The position of the alveolar crest remained constant relative to the inferior alveolar canal. In an 18th-century opulation from East London, in which perio ontitis was minimal or absent and which had little attrition, continuous eruption had occurred at a rate of 0.07 m d y e a r (Whittaker et al. 1990). The total movement of the teeth towards the occlusal plane was estimated to be 5 mm over a 40 year period. The physiological response to attrition robably occurs as a result of the biological ink that exists between the tooth cementum, periodontal ligament, and bone. Changes in dental occlusion result in remodelling of bone, dental cementum, and the collagen bundles that connect the two hard structures. It may be postulated that where attrition is mild and compensatory tooth eruption is slow, little or no tension is established within the periodontal ligament. Minor tooth movement could be accommodated by remodelling of the periodontal apparatus allowing asynchronous tooth movement relative to the alveolar bone, resulting in a significant increase in the CEJ-AC distance over a lifetime. When tooth wear is rapid, the rate of eruptive movement of the tooth is such that tension in the periodontal ligament is transmitted to bone, resulting in a combined movement of tooth and bone, as occurs in tooth eruption. Similarly, the rapid extrusive movement of teeth in clinical orthodontics maintains the concordance of the CEJ-AC relationship. Rapid coronal tooth R P ts F 311 CONTINUOUS TOOTH ERUPTION movement is accom anied by coronal movement of the alveo ar crest (Grant et al., 1988b).Whether crestal bone moves with the tooth as it continues to erupt would appear to depend on the rate of attrition. In the present study, the increasing CEJ-AC distances indicate that the continuous tooth eruption was not sufficiently rapid to stimulate an e uivalent growth rate of alveolar bone (Jigs. 1,2). Attrition is common lace in modern opulations, although stuiies of its reva ence are rare. In industrialized popu ations, an abrasive diet is replaced by parafunction (bruxism), digestive disturbances, and salivary and dietary variables (acidity).Whereas severe attrition in the molars is uncommon and found only in subjects aged 60 or older, incisors ex erienced increasing severit of wear in su jects aged between 20 an 30 (Hugoson et al., 1988). Other findings of the present study An occasional effect of age was detected by the repeated measures analysis of variance; this was particularly evident for all M1 teeth (Table 2). This is not surprising since in most cases, age estimates were based on attrition scores for these teeth. However, the method may not have been applicable to the diverse tribes from which the study population was drawn, because of differences in diet, food pre aration, and dental mor hology. d e consistent gender di ferences in the CEJ-AC distances for all degrees of attrition (males > females) are in agreement with the findings of Murphy (19591, whose study included part of the same material. With a more powerful masticatory apparatus, the male probably experienced a greater degree of attrition at the same age (Helkimo et al., 1977), resulting in more continuous tooth eruption. Males also experienced more tooth wear than females in contemporary populations (Hugoson et al. 1988). The greater CEJ-AC distances measured on the mesio-buccal/mesio-lingual tooth surfaces than disto-buccaUdisto-lingual surfaces for both males and females and all degrees of occlusal tooth wear may reflect the effects of mesial drift which compensates for roximal tooth wear. T\e CEJ-AC distances in male mandibular M3 with TW 3 were considerably less than in the M1; in the maxilla, this difference was less pronounced. M3 is usually subjected to less attrition than M1 because it P f P B P comes into function approximately 12 years later and ma be subjected to less use than the other mo ars. In addition, the pattern of M3 wear is extremely variable. Continuous tooth eru tion remains a confounding factor in mo ern epidemiological studies which use the CEJ as one reference point in measuring loss of periodontal attachment. This is particularly the case in older populations where the physiological effects of attrition and continuing facial owth on the CEJ position relative to the C and inferior dental canal are the most pronounced. 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