close

Вход

Забыли?

вход по аккаунту

?

Associations between Carabelli trait and cusp areas in human permanent maxillary first molars.

код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 129:196–203 (2006)
Associations Between Carabelli Trait and Cusp Areas
in Human Permanent Maxillary First Molars
Shintaro Kondo1,2* and Grant C. Townsend2
1
Department of Oral Anatomy and Developmental Biology, Showa University School of Dentistry,
Tokyo 142-8555, Japan
2
Dental School, University of Adelaide, Adelaide 5005, Australia
KEY WORDS
odontometry; sexual differences; tooth size; crown morphology
ABSTRACT
Few dental anthropological studies have
investigated the associations between tooth crown size
and crown traits in humans using quantitative methods.
We tested several hypotheses about overall crown size,
individual cusp areas, and expression of Carabelli cusps
in human permanent first molars by obtaining data from
standardized occlusal photographs of 308 Australians of
European descent (171 males and 137 females). Specifically, we aimed to calculate the areas of the four main
molar cusps, and also Carabelli cusp, and to compare the
relative variability of cusp areas in relation to timing of
development. We also aimed to compare cusp areas
between males and females and to describe how Carabelli cusp interacted with other molar cusps. Measurements included maximum crown diameters (mesiodistal
and buccolingual crown diameters), the areas of the four
main cusps, and the area of Carabelli cusp. The pattern
of relative variability in absolute areas of molar cusps
corresponded with their order of formation, the firstforming paracone displaying the least variation, and the
last-forming Carabelli cusp showing the greatest. Overall crown size and areas of individual cusps all showed
sexual dimorphism, with values in males exceeding
those in females. Sexual dimorphism was smallest for
paracone area and greatest for Carabelli cusp area.
Overall crown size and cusp areas were larger in individuals displaying a Carabelli cusp, especially the hypocone
area. Although the combined area of the protocone and a
Carabelli cusp was greater in cuspal forms than noncuspal forms, protocone area alone was significantly smaller
in the former. Our findings lead us to propose that, in
individuals with the genotype for Carabelli trait expression, larger molar crowns are more likely to display Carabelli cusps, whereas molars with smaller crowns are
more likely to display reduced forms of expression of the
trait. We suggest that the pattern of folding of the internal enamel epithelium in developing molar crowns, particularly in the protocone region, can be modified by a
developing Carabelli cusp. Am J Phys Anthropol
129:196–203, 2006. V 2005 Wiley-Liss, Inc.
Metric and nonmetric analyses of the human dentition
have formed a central focus in the field of dental anthropology for over a century (Keiser, 1990; Hillson, 1996;
Scott and Turner, 1997). Many metric studies involved
measurement of the maximum mesiodistal and buccolingual dimensions of dental crowns with calipers (e.g.,
Moorrees et al., 1957; Garn et al., 1967; Townsend and
Brown, 1979) or more recently from standardized photographs (e.g., Reid et al., 1991, 1992; Townsend et al.,
2003). Investigations of so-called nonmetric dental crown
traits, including the Carabelli cusp, were usually based
on scoring features with reference to standard plaques
(e.g., Dahlberg, 1949; Turner et al., 1991), leading to calculations of their frequency of occurrence and degree of
expression. Metric approaches confirmed that sexual
dimorphism exists in overall crown size, with values for
males exceeding those for females on average. Sexual
dimorphism was also reported for Carabelli trait occurrence and expression, but there seems to be no consistent pattern across different ethnic groups (Townsend
and Brown, 1981; Hsu et al., 1997).
Some studies included both metric and nonmetric data
to make comparisons within and between populations,
and some looked at the interactions or associations
between these variables (Garn et al., 1966; Keene, 1968;
Sasaki, 1968; Bang and Hasund, 1972; Lombardi, 1975;
Noss et al., 1983; Reid et al., 1991, 1992; Hsu et al.,
1997). More recently, researchers began analyzing intra-
coronal components, e.g., cusp areas and intercuspal distances, which are thought to provide a better biological
basis for describing tooth size variation (e.g., Biggerstaff,
1969; Corruccini, 1979; Townsend et al., 2003). These
studies aimed to clarify the ontogenetic basis of crown
size and shape, especially the role of enamel knots in
influencing folding of the internal enamel epithelium,
leading to the development of cusps (Jernvall and Jung,
2000). Each enamel knot represents the site of a future
cusp tip, and it was suggested that evolutionary change
in molar morphology is constrained to some extent by
the relationship between when enamel knots start to
form and when intercuspal growth ceases during odontogenesis (Polly, 1998).
C
V
2005 WILEY-LISS, INC.
C
Grant sponsor: National Health and Medical Research Council of
Australia.
*Correspondence to: Shintaro Kondo, Department of Oral Anatomy and Developmental Biology, Showa University School of Dentistry, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo142-8555, Japan.
E-mail: kondos@dent.showa-u.ac.jp
Received 26 October 2004; accepted 6 January 2005
DOI 10.1002/ajpa.20271
Published online 1 December 2005 in Wiley InterScience
(www.interscience.wiley.com).
CARABELLI TRAIT AND MOLAR CUSP AREAS
Although the relationship between lower molar crown
size, cusp number, and groove pattern was first addressed
by Dahlberg (1961), very few studies since then have
looked at associations between overall crown size, intracoronal components, and dental crown traits, with quantitative methods being used to describe observed variation (Reid et al., 1991, 1992).
Our general aim in this study was therefore to quantify overall crown size and cusp areas of a sample of
human maxillary first molars, as well as expression of
Carabelli cusps, by calculating areas from standardized
occlusal photographs of dental casts. Specifically, we
aimed to calculate the areas of the four main molar
cusps, and also Carabelli cusp, and to compare relative
variability of cusp areas in relation to timing of development. Further objectives included making comparisons
between males and females and describing how Carabelli
cusp interacted with other molar cusps. We then aimed
to explain our findings in the light of current knowledge
about crown morphogenesis, including the folding of the
internal enamel epithelium in response to the formation
of enamel knots.
The specific hypotheses we sought to test were:
That the pattern of relative variation of cusp areas
reflects the ontogeny of maxillary first molar crown
development, with earlier-forming cusps showing less
variation than later-forming cusps;
That molar cusp areas, and the areas of Carabelli
cusps, are larger in males on average than in females;
That teeth with a Carabelli cusp have larger crowns
on average than those without a Carabelli cusp;
That the size of the protocone is reduced in teeth
with a Carabelli cusp compared with those without
a Carabelli cusp, reflecting an interaction between
adjacent growth regions of the developing crown;
and
That the hypocone is larger in molars with a Carabelli
cusp, reflecting a general increase in cusp expression
on the lingual aspect of these teeth.
MATERIALS AND METHODS
In total, 308 dental casts of South Australian twins
aged 8–29 years, with the majority being teenagers,
were selected from a collection of over 600 pairs of dental casts housed in the Dental School at the University
of Adelaide. The twins were all of European ancestry.
Previous studies considered genetic aspects of tooth size
and Carabelli trait expression (Pinkerton et al., 1999;
Dempsey and Townsend, 2001), but in this study we concentrated on phenotypic associations, so only one member from each twin pair was included in the analysis.
Only subjects with little or no evidence of wear on their
maxillary first molars, either occlusally or interproximally, were included in the study. Only molars with four
main cusps were included.
Our ongoing study of teeth and faces of Australian
twins was approved by the Committee on the Ethics of
Human Experimentation, University of Adelaide (approval no. H/07/84A), and all participants provided informed
consent.
Initially, Carabelli trait was scored according to the
nine grades described by Reid et al. (1991, 1992), but
these grades were then combined into four categories:
grade 0, representing absence of the trait, formed cate-
197
gory 0; grades 1–4, including pits and furrows, became
category 1; grade 5, defined as a mesial and distal furrow, was grouped with teeth showing minor lingual
prominences that could not be measured from photographs to form category 2; and grades 6–8, including
examples with free apices and those forms of expression
that could be measured on occlusal photographs, were
combined to form category 3.
Standardized photographs of the occlusal surfaces of
maxillary first molars were obtained from dental casts
using a Nikon CoolPix 950 digital camera. The molar
crowns were oriented so that the plane produced by the
cusp tips of the three major cusps, excluding the hypocone, was perpendicular to the optical axis of the camera. The tooth was positioned in the center of the image,
and a millimeter scale was placed next to the tooth in
the same horizontal plane as the occlusal surface. Measurements on photographs were performed with manual
image measurement software (Visual Measure 32, Version 1.2, Rise Co.) on a personal computer. The method
described by Wood and Engleman (1988) was followed
when measuring basal cusp areas, using the primary
occlusal grooves to define the four main cusps, and the
grooving associated with a Carabelli cusp to determine
its area. Measurements were obtained normally of first
molars on the right side, but if a tooth on the right could
not be measured because of absence, abnormality, heavy
wear, or other reasons, the corresponding tooth on the
left side of the arch was measured.
Maximum mesiodistal and buccolingual crown diameters, and the areas of the four main cusps, i.e., the paracone (mesiobuccal), protocone (mesiolingual), metacone
(distobuccal), and hypocone (distolingual), were measured to the nearest 1 mm2 (Fig. 1). Only those forms of
Carabelli trait that appeared as distinct lingual prominences (category 3), and that could be distinguished
clearly from the protocone, were measured separately.
Total crown area was calculated by summing the areas
of individual cusps.
Previous studies to assess the replicability of the photographic procedure based on linear measurements of
scanned images compared with those obtained directly
from dental casts showed no systematic methodological
errors (Townsend et al., 2003). Furthermore, Bailey
et al. (2004) showed that the levels of interobserver error
for cusp area measurements obtained from digitized
images are similar to those for intraobserver comparisons. In the present study, measurement errors of the
method were analyzed by a procedure in which double
determination measurements were made on separate
occasions for 40 subjects selected at random for whom
the entire photographic and digitizing process was
repeated. Differences between first and second determinations were analyzed by computing the standard deviation of a single determination, or so-called technical
error of measurement, using the following formula
(Dahlberg, 1940):
sffiffiffiffiffiffiffiffiffi
Rd2
Error ¼
2N
In this formula, d ¼ difference between double determinations, and N ¼ number of double determinations.
Paired t-tests were also used to detect systematic errors.
To assess the observation error in classifying Carabelli
198
S. KONDO AND G.C. TOWNSEND
Fig. 1. Measurement of overall crown dimensions and cusp
areas of maxillary right molar. Individual cusps were distinguished by locating major occlusal grooves. Carabelli cusp area
was only measured when it could be discerned clearly from protocone. MD, mesiodistal crown diameter; BL, buccolingual crown
diameter; Pa, paracone area; Pr, protocone area; Me, metacone
area; Hy, hypocone area; Ca, Carabelli cusp area.
trait, the concordance rate in the double determination
observations was calculated for 50 subjects selected at
random.
Sex differences were compared by calculating the percentage of sexual dimorphism (Garn et al., 1967), defined
as [(M F)/F] 3 100, where M and F are the mean values of males and females, respectively.
Descriptive statistics, including distribution parameters, were calculated with JMP statistical software (SAS
Institute, Version 4.02) on a personal computer. Differences
in cusp area measurements between different categories
of Carabelli trait were analyzed with one-way ANOVA
followed by Dunnett’s test, with statistical significance
set at P < 0.05.
RESULTS
There was no indication of systematic methodological
errors in the calculation of crown dimensions or areas
between first and second determinations, based on
paired t-tests. Mean differences between first and second
determinations for mesiodistal and buccolingual diameters were 0.02 and 0.03 mm, and for each cusp area
including Carabelli cusp area, values ranged from 0.07
to 0.07 mm2. Percentage errors for the areas of the four
main cusps were less than 0.5%, while that for Carabelli
cusp area was 1.5%. These percentage values for intraobserver errors were smaller than those of interobserver
errors for molar cusp area in Pan reported by Bailey
et al. (2004). The technical errors of measurement were
0.17 and 0.18 mm, respectively, for mesiodistal and buccolingual dimensions, and ranged from 0.22–0.29 mm2
for cusp areas. Error variances, calculated as the square
of the Dahlberg statistic, were all less than 10% of total
observed variation, confirming that errors of the method
were small and unlikely to bias the results.
The concordance rate for scoring the Carabelli trait on
two separate observations was 92% in the sample of 50
individuals, and all discordances between first and second determinations were between categories 1 and 2.
Thus, errors in scoring were small.
Table 1 shows basic descriptive statistics for molar
crown measurements. All mean values were significantly
larger in males than in females (P < 0.01). Dimorphism
percentage values for absolute crown areas exceeded
those for overall crown diameters, but no statistical tests
were applied to compare these values, and care is needed
in drawing any conclusions based on comparisons of this
measure of sexual dimorphism. Carabelli trait area
showed the largest dimorphism value, and the smallest
value was for the paracone area.
The hypocone was the most variable in absolute area
of the four main molar cusps, whereas the least variable
cusp in absolute area was the paracone. Carabelli cusp
area showed the most variation in size of all molar
cusps. To take account of overall tooth size, comparisons
of relative crown size were also made between males and
females. With the exception of the Carabelli cusp, sexual
differences in the relative cusp areas were fairly small.
Carabelli cusps still showed the largest sexual difference
in the relative cusp area (P < 0.01).
Table 2 shows crown measurements for each category
of Carabelli trait. Around 70–80% of all subjects showed
evidence of the trait in varying forms, with 19–25%
exhibiting cusps (category 3). Approximately 13–19% of
subjects showed category 2, and 35–38% showed category 1. These percentages are similar to those reported
in our earlier studies of Australian twins (Townsend and
Martin, 1992; Pinkerton et al., 1999). Although there
was no statistically significant sex difference in frequencies for each of the categories (v2 ¼ 6.126, P ¼ 0.106),
the cuspal forms of Carabelli trait tended to be more
common in males than in females (25.7% compared with
19.0%). Overall crown measurements were larger in cuspal forms than in noncuspal forms. For example, the
mean mesiodistal diameter of first molars without
Carabelli trait was 10.1 mm in males and 9.9 mm in
females, compared with 10.5 mm and 10.3 mm, respectively, in molars displaying category 3 expression of the
Carabelli trait. Furthermore, the lingual cusps, i.e., protocone and hypocone, showed larger differences between
cuspal forms and noncuspal forms than the buccal cusps,
i.e., paracone and metacone. In males, lingual cusps
showed significant differences between cuspal forms and
noncuspal forms (P < 0.05), but buccal cusps did not.
For example, the mean area of the hypocone in molars
without Carabelli trait was 17.4 mm2, compared with
19.5 mm2 in molars showing category 3 expression. Similar trends were also shown in females, but the results of
statistical tests were not significant. The combined area
of the protocone and Carabelli trait was significantly
larger in cuspal forms (30.9 mm2 in males and 28.8 mm2
in females) than in noncuspal forms, where the areas
averaged 28.1 mm2 and 27.1 mm2, respectively (P <
0.05). However, the protocone area alone was smaller in
cuspal forms than in noncuspal forms (25.8 mm2 compared with 28.1 mm2 in males, and 25.4 mm2 compared
with 27.1 mm2 in females), the difference in males being
significant at P < 0.05.
Table 3 shows a correlation matrix of molar crown
measurements, with values for males above the diagonal
and values for females below. Correlation coefficients calculated between crown diameters and total crown areas
were all moderately high. However, values of correlation
coefficients between cusp areas were low to moderate in
magnitude, especially between the hypocone area and
other cusp areas. These findings are consistent with our
previous results for intercuspal distances in molar teeth,
199
CARABELLI TRAIT AND MOLAR CUSP AREAS
1
TABLE 1. Basic statistics of maxillary first molar crown diameters, and absolute and relative cusp areas
Males
N
Mean
Sexual
difference
Females
SD
Crown diameters (mm)
MD
171
10.3
0.54
BL
171
11.3
0.52
2
Absolute cusp areas and total crown area (mm )
Pa
171
23.6
2.61
Pr þ Ca
171
29.6
3.62
Ca
44
5.1
2.79
Me
171
22.5
2.89
Hy
171
19.0
3.46
Total crown area
171
94.7
8.45
Relative cusp area to total crown area (%)2
Pa
171
25.0
2.20
Pr þ Ca
171
31.3
2.97
Ca
44
5.2
2.78
Me
171
23.7
2.04
Hy
171
20.0
2.78
CV3
N
Mean
SD
CV3
t-test
5.3
4.6
137
137
10.1
11.0
0.51
0.59
5.0
5.4
**
**
2.6
3.1
11.1
12.2
55.1
12.9
18.2
8.9
137
137
26
137
137
137
22.6
27.8
3.4
21.2
17.9
89.6
2.61
3.49
1.40
2.82
3.40
8.74
11.6
12.5
40.9
13.3
19.0
9.8
**
**
**
**
**
**
4.4
6.6
48.3
5.8
6.1
5.8
8.8
9.5
53.5
8.6
13.9
137
137
26
137
137
25.3
31.1
3.7
23.7
20.0
2.19
2.64
1.49
2.00
2.89
8.7
8.5
40.0
8.4
14.5
NS
NS
**
NS
NS
1.3
0.8
39.0
0.0
0.3
%
1
Abbreviations of crown dimensions are summarized in Figure 1. NS, not significant.
Relative cusp area ¼ (Cusp area)/(Total crown area) 3 100.
3
CV ¼ (SD/Mean) 3 100.
**P < 0.01.
2
which showed that the values of correlation coefficients
between intercuspal dimensions were consistently lower
than those between overall crown measurements, suggesting that much of the intracoronal covariation in cusp
position and area is unexplained (Townsend et al., 2003).
DISCUSSION
The pattern of relative variation in absolute areas of
the four main molar cusps mirrored the known ontogenetic sequence of cusp development, with earlier-forming
cusps being more stable than later-forming cusps. This
finding is consistent with the results of previous studies
(Gingerich, 1974; Corruccini, 1979; Kondo et al., 2005).
Relative cusp areas were more stable than absolute cusp
areas, especially for the metacone (Table 1). Absolute
cusp areas were also associated with greater sexual
dimorphism percentage values than mesiodistal and buccolingual crown diameters, a result consistent with a
previous finding based on molar cusp diameters (Kondo
et al., 2005).
However, because most researchers used categorical
systems to classify the expression of Carabelli trait, little
information has been available about its relative variation in size. Our method enabled accurate quantification
of the area of Carabelli cusps, and showed that it displays greater relative variation in its area than any of
the main molar cusps, consistent with being the last
cusp to appear during crown development (Kraus and
Jordan, 1965).
This quantitative approach also provided support for a
previous finding in our sample of Australian twins: the
cuspal form of Carabelli trait displays significant sexual
dimorphism in its expression. Some workers found significant sexual differences in the expression of Carabelli
trait (e.g., Townsend and Brown, 1981; Mizoguchi, 1985),
but others reported no sex differences in this trait (Garn
et al, 1966). Mizoguchi (1985) highlighted the inconsistencies one can encounter when assessing sex differences
in crown trait expression. He presented frequency distributions for 12 different crown traits observed in two Japanese samples, and found that only Carabelli trait
showed a significant sex difference in both samples. Our
earlier studies of Australian twins based on scoring the
Carabelli trait showed differences in frequency of occurrence and degrees of expression between the sexes
(Townsend and Martin, 1992; Pinkerton et al., 1999),
whereas this quantitative study showed that the average
area of a Carabelli cusp is significantly greater in males
than females. It seems that the extent of sexual dimorphism for Carabelli trait varies between different ethnic
groups, so care is needed when making comparisons
between groups using standardized scoring systems (e.g.,
Turner et al., 1991), especially if sex is unknown.
We found that the mesiodistal and buccolingual crown
diameters of first molars were larger on average in those
individuals who displayed Carabelli trait than in those
who did not, a result consistent with many former studies (De Terra, 1905; Broekman, 1938; Keene, 1968;
Sasaki, 1968; Lombardi, 1975; Noss et al., 1983; Hsu
et al., 1997). Furthermore, cusp areas were larger in cuspal forms than in noncuspal forms, a trend that was particularly evident in the hypocone. Reid et al. (1991,
1992) also used a quantitative approach to show that
molars with a Carabelli cusp were larger than those
without, so it seems that this is a common positive association. Our finding that the hypocone area displayed
the biggest difference between molars with and without
a Carabelli cusp supports an earlier report by Mizoguchi
(1985), and is also consistent with the trait being less
common in three-cusped molars (Keene, 1968; Suzuki
and Sakai, 1973; Scott, 1979).
Dahlberg (1949) and Korenhof (1960) reported that
protocone size tends to be reduced when Carabelli trait
is strongly developed. Reid et al. (1991, 1992) contradicted these findings, but they included protocone area
within their measurement of Carabelli trait, and so they
were unable to separate the contributions of the two
cusps. We measured Carabelli cusp and protocone areas
independently, and found that combined protocone and
Carabelli cusp area was significantly larger in cuspal
forms than in noncuspal forms. However, protocone area
alone was significantly smaller in cuspal forms than in
noncuspal forms. Thus, it seems that protocone area is
200
S. KONDO AND G.C. TOWNSEND
TABLE 2. Maxillary first molar crown diameters (mm) and cusp areas (mm2) for various categories of Carabelli trait1
Category of Carabelli trait
Males
N (%)
MD
BL
Pa
Pr þ Ca
Pr
Ca
Me
Hy
Total crown area
Females
N (%)
MD
BL
Pa
Pr þ Ca
Pr
Ca
Me
Hy
Total crown area
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Mean
SD
0
1
2
3
33 (19.3%)
10.1
0.55
11.1
0.61
23.0
2.88
28.1
3.47
28.1
3.47
61 (35.7%)
10.4***
0.57
11.3
0.50
23.5
2.89
29.7
3.29
33 (19.3%)
10.4
0.48
11.3
0.51
23.5
2.07
29.4
2.92
44 (25.7%)
10.5****
0.50
11.5****
0.45
24.3
2.29
30.9****
4.23
25.8*****
4.08
5.1
2.79
22.7
2.50
19.5***
3.55
97.3****
7.97
22.2
2.90
17.4
3.20
90.8
9.27
40 (29.2%)
9.9
0.53
10.7
0.63
22.3
2.80
27.1
3.76
27.1
3.76
20.2
2.50
16.8
3.74
86.5
9.27
22.4
2.95
19.2***
3.50
94.7
8.07
52 (38.0%)
10.1
0.43
11.0
0.48
22.6
2.31
27.6
3.21
21.5
2.16
18.2
3.38
90.0
7.49
22.6
3.30
19.7***
3.15
95.1
7.76
19 (13.9%)
10.2
0.54
11.1
0.67
22.9
3.41
28.3
3.58
22.0
2.84
18.5
3.24
91.6
9.36
26 (19.0%)
10.3****
0.52
11.2****
0.55
22.8
2.30
28.8
3.44
25.4
3.33
3.4
1.40
21.6
3.98
18.7
2.69
92.0***
8.85
ANOVA
F-ratio
P value
F-ratio
P value
F-ratio
P value
F-ratio
P value
3.503
0.017*
3.619
0.014*
1.664
0.177
3.902
0.010**
F-ratio
P value
F-ratio
P value
F-ratio
P value
0.184
0.907
3.286
0.022*
4.029
0.008**
F-ratio
P value
F-ratio
P value
F-ratio
P value
F-ratio
P value
3.496
0.017*
3.735
0.013*
0.290
0.832
1.505
0.216
F-ratio
P value
F-ratio
P value
F-ratio
P value
2.567
0.057
2.241
0.086
2.857
0.040*
1
Abbreviations of crown dimensions are summarized in Figure 1.
*P < 0.05.
**P < 0.01 (ANOVA).
***P < 0.05.
****P < 0.01 (Dunnett’s test between category 0 and others for this and P < 0.05).
*****Significant difference between mean areas for category 0 and 3 at P < 0.05 level by t-test.
reduced when the Carabelli trait is well-developed, and
we believe that this can be explained by interactions
between adjacent folding regions of the internal enamel
epithelium during odontogenesis. Figure 2 gives an
example of a molar with a well-developed Carabelli cusp
and with the protocone displaced buccally and distally.
The Carabelli trait originates from the lingual cingulum region of maxillary molar crowns, being evident particularly on the first molar (Korenhof, 1960; Sakai and
Hanamura, 1967). Kraus and Jordan (1965) noted that a
Carabelli cusp is created by an extension of the calcification process from the protocone during tooth development, and that it appears after the other cusps have
begun to calcify. It is evident, at least in its cuspal form,
at the dentino-enamel junction of fully-formed teeth in
modern humans (Sakai and Hanamura, 1971; Sasaki,
1997). Schwartz et al. (1998) also noted some correspondence between expression of Carabelli cusp on the
tooth crown surface and the topography of the dentino-
enamel junction in early hominid specimens, even
though the nature of the relationship was variable. So
even though the expression of the trait on the surface of
the tooth and at the dentino-enamel junction may not
coincide precisely, it appears that expression of Carabelli
trait on molar crowns is related to folding of the internal
enamel epithelium during odontogenesis, and is not produced merely by deposition of enamel.
The Carabelli trait appears to be under strong genetic
control, and there were suggestions of major gene
involvement for its expression (Kolakowski et al., 1980;
Nichol, 1989; Townsend and Martin, 1992). Some
researchers reported low estimates of heritability (Biggerstaff, 1973; Alvesalo et al., 1975; Mizoguchi, 1977),
but these results may reflect differences in methodologies between studies. In fact, Alvesalo et al. (1975) noted
that the dichotomy of having a Carabelli cusp or not
may have a genetic basis, but that there appeared to be
large variation in the expression of the ‘‘cusp-genotype.’’
CARABELLI TRAIT AND MOLAR CUSP AREAS
TABLE 3. Matrix of correlations between molar crown
diameters and cusp areas1
MD
BL
Pa
MD
0.81** 0.61**
BL
0.84**
0.59**
Pa
0.64** 0.68**
Pr þ Ca 0.60** 0.72** 0.43**
Me
0.71** 0.68** 0.44**
Hy
0.63** 0.60** 0.18*
TCA
0.91** 0.94** 0.68**
Pr þ Ca
Me
Hy
TCA
0.56**
0.58**
0.29**
0.63**
0.68**
0.42**
0.17*
0.64**
0.61**
0.12
0.15*
0.48**
0.91**
0.92**
0.63**
0.64**
0.74**
0.68**
0.39**
0.22**
0.74**
0.37**
0.76** 0.65**
1
Abbreviations of crown dimensions are summarized in Figure 1.
TCA, total crown area. Upper right, males (N ¼ 171); lower left,
females (N ¼ 137).
*P < 0.05.
**P < 0.01.
Fig. 2. Example of permanent first molar with well-developed Carabelli cusp. Protocone is displaced buccally and distally,
and its size is reduced. Mesial marginal ridge is very well-developed. D, distal; L, lingual; Pa, paracone; Pr, protocone; Me,
metacone; Hy, hypocone; Ca, Carabelli cusp.
Hlusko and Mahaney (2003) found that cusp-like structures which derived from the lingual cingula of maxillary molars in baboons, similar to features referred to as
Carabelli trait in humans, were significantly heritable.
However, several studies mentioned that Carabelli trait
may be present on the deciduous second molar but not
on the permanent first molar of the same individual
(Townsend and Brown, 1981; Saunders and Mayhall,
1982; Smith et al., 1987; Pinkerton et al., 1999). Interestingly, the reverse relationship is very rare. It was
suggested that reduced expression in the permanent first
molar may result from environmental influences operating during its longer period of development. In other
words, the Carabelli phenotype of deciduous second
molars may represent a more faithful representation of
the underlying genotype than its phenotypic expression
in the permanent dentition. We plan to extend our study
201
of cusp areas and Carabelli trait expression to the deciduous dentition, but believe that analyses taking account
of the timing and sequence of crown formation of the
permanent first molar crown can also provide valuable
insights into the nature of variation in expression of the
Carabelli trait.
Developments in molecular biology are now providing
a much clearer picture of the processes involved in odontogenesis, including the development of dental crown
shape (Sperber, 2004). Reciprocal interactions between
oral epithelium and neural crest-derived mesenchyme
influence how the internal enamel epithelium, which
represents the future dentino-enamel junction and provides a blueprint for completed crown structure, will
fold. This folding is associated with the appearance of
groups of nondividing cells, referred to as enamel knots,
that act as signaling centers. The primary enamel knot
is one such transient signaling center that seems to be
an important regulator of overall tooth shape during the
cap stage of odontogenesis (Jernvall and Jung, 2000).
Secondary enamel knots form subsequently at the sites
of future cusp tips, providing the first signs of speciesspecific cusp patterns. Control of secondary enamel knot
spacing must exist during morphogenesis, as this process
determines correct cusp position and size, leading to a
functional tooth shape (Jernvall and Thesleff, 2000).
Although the spacing between enamel knots needs to be
accurately controlled to produce the patterns of cusp
position that distinguish different species, the results of
our correlation analysis in this study, together with findings from previous analyses of intercuspal distances,
suggest that the stochastic nature of the local epigenetic
events involved in crown formation may contribute to
variation in cuspal arrangements within human tooth
classes (Townsend, 1985; Townsend et al., 2003). The
recent findings of Hlusko et al. (2004) of genetic independence of mesial and distal loph variation in baboon
molar crowns also support the view that minor variations in cusp position within species are determined
intrinsically.
No cusp-specific differences in homeobox gene expression have been reported within species (Zhao et al.,
2000), and the development of individual cusps appears
to use repeatedly the same set of developmental genes,
forming a ‘‘developmental module.’’ In fact, the repeated
activation of these developmental modules may explain
the cumulative variation in later-developing cusps
(Jernvall and Jung, 2000). It was proposed that the
wave-like expression of signaling factors produced within
developing teeth, reflecting dynamic interactions
between molecules, may be responsible for crown patterns (Weiss, 1990; Weiss et al., 1998). Furthermore, a
patterning cascade mode of cusp spacing may promote
the evolution of new cusps (Polly, 1998; Jernvall, 2000).
If a simple patterning cascade is applied to human
molars, a larger Carabelli cusp would be expected to be
present when the height of the protocone, relative to the
paracone, is large. As the differences would be cumulative, only a very small increase in size of the protocone
would be needed to have a large effect on the size of a
Carabelli cusp.
Putting together the various aspects of molar morphogenesis described above, and drawing on the morphogenetic triangle concept of Keene (1991), we propose the
following explanation for observed relationships between
overall molar crown size, cusp areas, and Carabelli trait
(Fig. 3). In those individuals who have the genetic con-
202
S. KONDO AND G.C. TOWNSEND
crown formation in males leading to larger teeth on
average. Furthermore, the tendency for teeth with Carabelli cusps to have larger hypocones may also relate to
an extended period of crown development, enabling
stronger expression of this later-formed cusp. The reduction in area of the protocone in those molars with welldeveloped Carabelli cusps is thought to reflect the interaction occurring between closely developing cusp regions,
as the inner enamel epithelium folds at the site of each
of the five enamel knots.
CONCLUSIONS
We propose that molars with larger crowns will be
more likely to display Carabelli cusps in genetically predisposed individuals, because the fifth enamel knot that
appears late during crown development will be more
likely to be fully expressed. In contrast, smaller molars
will tend to be associated with less developed forms of
Carabelli trait. Furthermore, we suggest that the pattern of folding of the internal enamel epithelium in the
protocone region can be modified by the presence of a
fifth enamel knot for Carabelli cusps, leading to displacement of the protocone on the fully calcified crown.
ACKNOWLEDGMENTS
Fig. 3. Proposed relationship between maxillary molar
crown size and shape, and Carabelli trait expression. G and E
represent genetic and environmental factors.
The assistance of the Australian Twin Registry is
greatly appreciated, and we also thank the twins and their
families for their enthusiastic participation. Sandy Pinkerton and Wendy Schwerdt assisted in data collection.
LITERATURE CITED
stitution for Carabelli trait expression, we suggest that
molars with larger crowns are more likely to display
Carabelli cusps. In these individuals, a fifth enamel knot
will tend to develop near to the protocone during the
later stages of molar crown development. This genotypic
potential will only be expressed to its full extent phenotypically if the period of crown growth is extended for a
sufficient time to enable an additional late folding of the
inner enamel epithelium to occur in the protocone region.
This may occur if the duration of mitotic activity of the
developing tooth germ is extended and/or the coalescence
of calcification between cusp tips is delayed. In either
case, it is likely that the Carabelli trait will be expressed
in its cuspal form, and also that the crown will tend to be
larger overall. In contrast, smaller molars, in which the
period of crown growth is shorter, will be less likely to
express the more developed forms of Carabelli trait,
because the extent of folding related to formation of the
fifth enamel knot will be reduced. Thus the positive association between crown size and presence of Carabelli cusp
may not relate to the Carabelli cusp ‘‘causing’’ the crown
to be bigger, but rather may occur because individuals
whose first molars tend to be bigger will consequently be
more likely to display the Carabelli trait.
This proposal is strengthened by the finding that not
only does the buccolingual diameter of molar crowns
tend to be larger in individuals with the Carabelli trait,
as one might expect, but that the mesiodistal diameter is
also larger, even though the Carabelli trait does not contribute directly to this dimension. The greater area of
Carabelli cusps in males compared with females may be
a further reflection of the more extended period of dental
Alvesalo L, Nuutila M, Portin P. 1975. The cusp of Carabelli.
Occurrence in first upper molars and evaluation of its heritability. Acta Odontol Scand 33:191–197.
Bailey SE, Pilbrow VC, Wood BA. 2004. Interobserver eror
involved in independent attempts to measure cusp base areas
of Pan M1s. J Anat 205:323–331.
Bang G, Hasund A. 1972. Morphologic characteristics of the
Alaskan Eskimo dentition II. Carabelli’s cusp. Am J Phys
Anthropol 37:35–40.
Biggerstaff RH. 1969. The basal area of posterior tooth crown
components: the assessment of within tooth variations of premolars and molars. Am J Phys Anthropol 31:163–170.
Biggerstaff RH. 1973. Heritability of the Carabelli cusp in
twins. J Dent Res 52:40–44.
Broekman RW. 1938. Anthrologische Besonderheiten des Menschenschädels. Zahnärztl Rundschau 47:336–342,465–468.
Corruccini RS. 1979. Molar cusp-size variability in relation to
odontogenesis in hominoid primates. Arch Oral Biol 24:
633–634.
Dahlberg AA. 1949. The dentition of the American Indians. In:
Laughlin WS, editor. Papers of the physical anthropology of
the American Indians. New York: Viking Fund. p 138–176.
Dahlberg AA. 1961. Relationship of tooth size to cusp number
and groove conformation of occlusal surface patterns of lower
molar teeth. J Dent Res 40:34–38.
Dahlberg G. 1940. Statistical methods for medical and biological
students. London: George Allen and Unwin, Ltd.
Dempsey PJ, Townsend GC. 2001. Genetic and environmental
contributions to variation in human tooth size. Heredity 86:
685–693.
De Terra M. 1905. Beitrage zu einer Odontographie der Menschenrassen. Inaugural dissertation, University of Zurich.
Garn SM, Lewis AB, Kerewsky RS. 1966. Genetic independence
of Carabelli’s trait from tooth size or crown morphology. Arch
Oral Biol 11:745–747.
CARABELLI TRAIT AND MOLAR CUSP AREAS
Garn SM, Lewis AB, Swindler DR, Kerewsky RS. 1967. Genetic
control of sexual dimorphism in tooth size. J Dent Res 46:
963–972.
Gingerich PD. 1974. Size variability of the teeth in living mammals and the diagnosis of closely related sympatric fossil species. J Paleontol 48:895–903.
Hillson S. 1996. Dental anthropology. Cambridge: Cambridge
University Press.
Hlusko LJ, Mahaney MC. 2003. Genetic contributions to expression of the baboon cingular remnant. Arch Oral Biol 48:663–672.
Hlusko LJ, Maas ML, Mahaney MC. 2004. Statistical genetics
of molar cusp patterning in pedigreed baboons: implications
for primate dental development and evolution. J Exp Zool
(Mol Dev Evol) 302:268–283.
Hsu JW, Tsai PL, Hsiao TH, Chang HP, Lin LM, Liu KM, Yu
HS, Ferguson D. 1997. The effect of shovel trait on Carabelli’s
trait in Taiwan Chinese and Aboriginal populations. J Forensic Sci 42:802–806.
Jernvall J. 2000. Linking development with generation of novelty in mammalian teeth. Proc Natl Acad Sci USA 97:2641–
2645.
Jernvall J, Jung HS. 2000. Genotype, phenotype, and developmental biology of molar tooth characters. Yrbk Phys Anthropol 43:171–190.
Jernvall J, Thesleff I. 2000. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev
92:19–29.
Keene HJ. 1968. The relationship between Carabelli’s trait and
the size, number and morphology of the maxillary molars.
Arch Oral Biol 13:1023–1025.
Keene HJ. 1991. On heterochrony in heterodonty: a review of
some problems in tooth morphogenesis and evolution. Yrbk
Phys Anthropol 34:251–282.
Keiser JA. 1990. Human adult odontometrics. Cambridge: Cambridge University Press.
Kolakowski D, Harris EF, Bailit HL. 1980. Complex segregation
analysis of Carabelli’s trait in a Melanesian population. Am J
Phys Anthropol 53:301–308.
Kondo S, Townsend GC, Yamada H. 2005. Sexual dimorphism
of cusp dimensions in human maxillary molars. Am J Phys
Anthropol 126: in press.
Korenhof CAW. 1960. Morphogenetical aspects of the human
upper molar. Thesis, University of Utrecht.
Kraus BS, Jordan RJ. 1965. The human dentition before birth.
Philadelphia: Lea & Febiger.
Lombardi AV. 1975. Tooth size associations of three morphologic
dental traits in a Melanesian population. J Dent Res 54:239–
243.
Mizoguchi Y. 1977. Genetic variability in tooth crown characters: analysis by the tetrachoric correlation method. Bull Nat
Sci Mus Tokyo Ser D 3:37–62.
Mizoguchi Y. 1985. Shovelling: a statistical analysis of its morphology. Univ Mus Univ Tokyo Bull 26:1–176.
Moorrees CFA, Thomsen SO, Jensen E, Yen PKJ. 1957. Mesiodistal crown diameters of the deciduous and permanent teeth
in individuals. J Dent Res 36:39–47.
Nichol CR. 1989. Complex segregation analysis of dental morphological variants. Am J Phys Anthropol 78:37–59.
Noss JF, Scott GR, Potter RHY, Dahlberg AA, Dahlberg T. 1983.
The influence of crown size dimorphism on sex differences in
the Carabelli trait and the canine distal accessory ridge in
man. Arch Oral Biol 28:527–530.
Pinkerton S, Townsend GC, Richards L, Schwerdt W, Dempsey
P. 1999. Expression of Carabelli trait in both dentitions of
Australian twins. Perspect Hum Biol 4:19–28.
Polly PD. 1998. Variability, selection, and constraints: development and evolution in viverravid (Carnivora, Mammalia)
molar morphology. Paleobiology 24:409–429.
203
Reid C, Van Reenan JF, Groeneveld HT. 1991. Tooth size and
the Carabelli trait. Am J Phys Anthropol 84:427–432.
Reid C, Van Reenan JF, Groeneveld HT. 1992. The Carabelli trait
and maxillary molar cusp and crown base areas. In: Smith P,
Tchernov E, editors. Structure, function and evolution of teeth.
London: Freund Publishing House, Ltd. p 451–466.
Sakai T, Hanamura H. 1967. A morphological analysis of Carabelli’s cusp. Aichi Gakuin J Dent Sci 5:60–72 [in Japanese
with English summary].
Sakai T, Hanamura H. 1971. A morphological study of enameldentine border on the Japanese dentition. Part V. Maxillary
molar. J Anthropol Soc Nippon 79:297–222 [in Japanese with
English summary].
Sasaki I. 1968. Relationship of tooth size to its features in man.
Aichi Gakuin J Dent Sci 6:126–173 [in Japanese with English
summary].
Sasaki K. 1997. Morphological study on dentino-enamel junction
of the upper second deciduous molar. J Anthropol Soc Nippon
105:273–291 [in Japanese with English summary].
Saunders SR, Mayhall JT. 1982. Developmental patterns of
human dental morphological traits. Arch Oral Biol 27:45–49.
Schwartz GT, Thackeray JF, Reid C, Van Reenan JF.
1998. Enamel thickness and the topography of the enameldentine junction in South African Plio-Pleistocene hominids
with special reference to the Carabelli trait. J Hum Evol 35:
523–542.
Scott GR. 1979. Association between the hypocone and Carabelli’s trait of the maxillary molars. J Dent Res 58:1403–1404.
Scott GR, Turner CG II. 1997. The anthropology of modern
human teeth. Cambridge: Cambridge University Press.
Smith P, Koyoumdjisky-Kaye E, Kalderon W, Stern D. 1987.
Directionality of dental trait frequency between human second deciduous and first permanent molars. Arch Oral Biol
32:5–9.
Sperber GH. 2004. The genetics of odontogenesis: implications
in dental anthropology and paleo-odontology. Dent Anthropol
17:1–7.
Suzuki M, Sakai T. 1973. The Japanese dentition. Matsumoto:
Shinshu University School of Medicine.
Townsend GC. 1985. Intercuspal distances of maxillary premolar teeth in Australian Aboriginals. J Dent Res 64:443–
446.
Townsend GC, Brown T. 1979. Tooth size characteristics of Australian Aborigines. Occas Pap Hum Biol 1:17–38.
Townsend GC, Brown T. 1981. The Carabelli trait in Australian
Aboriginal dentition. Arch Oral Biol 26:809–814.
Townsend GC, Martin NG. 1992. Fitting genetic models to Carabelli trait data in South Australian twins. J Dent Res 71:403–
409.
Townsend GC, Richards L, Hughes T. 2003. Molar intercuspal
dimensions: genetic input to phenotypic variation. J Dent Res
82:350–355.
Turner CG II, Nichol CR, Scott GR. 1991. Scoring procedures
for key morphological traits of the permanent dentition: the
Arizona State University Dental Anthropology System. In:
Kelley MA, Larsen CS, editors. Advances in dental anthropology. New York: Wiley-Liss. p 13–31.
Weiss KM. 1990. Duplication with variation: matameric logic in evolution from genes to morphology. Yrbk Phys Anthropol 33:1–23.
Weiss KM, Stock DW, Zhao Z. 1998. Dynamic interactions and
the evolutionary genetics of dental patterning. Crit Rev Oral
Biol Med 9:369–398.
Wood BA, Engleman CA. 1988. Analysis of the dental morphology of Plio-Pleistocene hominids. V. Maxillary postcanine
tooth morphology. J Anat 161:1–35.
Zhao Z, Stock DW, Buchanan AV, Weiss KM. 2000. Expression
of Dlx genes during the development of the murine dentition.
Dev Genes Evol 210:270–275.
Документ
Категория
Без категории
Просмотров
0
Размер файла
146 Кб
Теги
cusp, associations, first, molar, area, maxillary, human, traits, carabelli, permanent
1/--страниц
Пожаловаться на содержимое документа