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Continuous tooth eruption in Australian aboriginal skulls.

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Continuous Tooth Eruption in Australian Aboriginal Skulls
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
Attrition, Facial growth, Periodontitis
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,
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
Received December 18,1989; accepted January 29,1991.
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.,
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-
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.
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.
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-
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).
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.
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
1 1 N
In this study, significantly lar er CEJ-AC
distances were measured in teet with more
advanced attrition. All teeth studied were
N 0 In
0 e N
TABLE 2. Statistical analysis for each tooth studied'
Maxillary right
PM 1
Maxillary left
Mandibular right
PM 1
Mandibular left
1 <2<3
Site of CEJ-AC measurement
m vs. d
b vs. li
b < li
b < li
b > li
b < li
b < li
b < li
b > li
b < li
b < li
b > li
b < li
< li
'An entry indicates the presence a n d direction of a statistically significant effect. Abbreviations used: m, mesial; d, distal; b, buccal; li,
"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
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
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.
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
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
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
f 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. The exact relationship between
age, attrition, and continuous eru tion may
only be revealed by well-controlled ongitudinal studies, but the results of this study
indicate the significance of continuous eruption in maintaining the normal function of
the masticatory system.
The South Australian Museum is acknowledged for granting access to the collection of pre-white-contact Australian aboriginal skulls, which has been used as a resource
for this study and which provided the figures
for the paper.
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