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Twins and the paradox of dental-age estimations: A caution for researchers and clinicians
Accepted Manuscript Title: Twins and the paradox of dental-age estimations: a caution for researchers and clinicians Author: M. Pechn´ıkov´a D. De Angelis D. Gibelli V. Vecchio R. Cameriere B. Zeqiri C. Cattaneo PII: DOI: Reference:
S0018-442X(14)00057-2 http://dx.doi.org/doi:10.1016/j.jchb.2014.05.003 JCHB 25348
To appear in: Received date: Accepted date:
23-1-2012 30-1-2014
Please cite this article as: Pechn´ikov´a, M., De Angelis, D., Gibelli, D., Vecchio, V., Cameriere, R., Zeqiri, B., Cattaneo, C.,Twins and the paradox of dental-age estimations: a caution for researchers and clinicians., Journal of Comparative Human Biology (2014), http://dx.doi.org/10.1016/j.jchb.2014.05.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Twins and the paradox of dental-age estimations: a caution for researchers and clinicians. M. Pechníkováa, b, D. De Angelisb, D. Gibellia, V. Vecchiob, R. Camerierec, B. Zeqirid†, C.
a
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Cattaneoa*
LABANOF – Laboratorio di Antropologia ed Odontologia Forense, Sezione di Medicina
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Legale, Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, b
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Via Mangiagalli 37 - 20133 Milano, Italy
Institute of Anatomy, Department of Anatomy, Histology and Embryology, Faculty of
Medicine, University of Ostrava, 70103 Ostrava, Czech Republic
Institute of Legal Medicine, University of Macerata, 62100 Macerata, Italy
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University Dental Clinical Center of Kosovo
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c
Received 23 January 2012, accepted 30 January 2014
*Corresponding author. Tel.: +39 0250315678, fax: +39 02-50315724. E-mail address: [email protected] (Cristina Cattaneo)
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Abstract The biological age difference among twins is frequently an issue in studies of genetic influence on various dental features, particularly dental development. The timing of dental development is a crucial issue also for many clinicians and researchers. The aim of this study was therefore to verify within groups of twins how dental development differs, by applying Demirjian’s method, Mincer’s charts of development of third molars and two of Cameriere’s
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methods for dental age estimation, which are among the most popular methods both in the
clinical and the forensic scenario. The sample consisted of 64 twin pairs: 21 monozygotic, 30
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dizygotic same-sex and 13 dizygotic opposite-sex with an age range between 5.8 and 22.6
years. Dental age was determined from radiographs using the mentioned methods. Results
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showed that dental age of monozygotic twins is not identical even if they share all their genes. The mean intra-pair difference of monozygotic pairs was low and similar to the difference in
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dizygotic same-sex twins; the maximum difference between monozygotic twins, however, was surprisingly large (nearly two years). This should lead to some circumspection in the
Introduction
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scenario.
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interpretation of systematic estimations of dental age both in the clinical and forensic
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The special nature of the twinning process provides an opportunity to learn more about human development. Because monozygotic twins result from the same fertilized ovum, they share all their genes. Dizygotic twins, on the other hand, originate from two different ova that are separately fertilized and share, on average, only one half of their genes. By comparing monozygotic and dizygotic twins raised together, and thus subjected to similar environmental factors, the genetic contribution to a specific phenotypic characteristic can be assessed (Martin et al., 1997; Pelsmaekers et al., 1997). The first use of twins for the study of the relative roles of genes and environment is frequently attributed to Galton, but it was Siemens who in 1924 first used the classical twin study comparing similarities of monozygotic and dizygotic twins (Rende et al., 1990). Since then, plenty of twin studies were performed on a wide variety of physical and mental traits. The twin model is very often applied to various dental features. It was suggested by many research groups that genetic factors influence the manifestation of many dental disorders, anomalies and illnesses such as dental malformation, hypodontia (Liu et al., 1998, 1999; Townsend et al., 2005), supernumerary teeth (Łangowska-Adamczyk and Karmańska, 2001),
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agenesis (Zengina et al., 2008), transposition (Peck et al., 1997), periodontitis (Michalowicz et al., 1991a; Potter, 1990) or dental caries (Boraas et al., 1988; Bretz et al., 2005a, 2005b; Townsend et al., 1998). However, much more attention has been given to genetic and environmental determinants of dental variation, especially to tooth size and morphology (Kabban et al., 2001; Townsend et al., 2009a), to the heritability of arch size and tooth size (Liu et al., 1998; Sharma et al.,
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1985) or to the variation in crown size of deciduous and permanent teeth (Dempsey et al., 1995; Hughes et al., 2000). Differences in dental diameters have been observed between
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monozygotic twins (Townsend et al., 2009a, 2009b) and also between twins and singletons
(Boklage, 1987). Research on occlusal morphology and its variations has been performed by
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two research groups (Corruccini et al., 1990; Su et al., 2008) and genetic variance for alveolar bone height has been estimated by Michalowicz et al. (1991b).
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Although the classical twin model has already been used for the study of genetic influence on dental eruption (Garn et al., 1960; Green and Aszkler, 1970; Hatton, 1955), the rate of genetic influence is still a question. In the study of Hughes et al. (2007) the authors quantified
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the contribution of genetic and environmental factors to variation in timing of the eruption of human deciduous incisors; the eruption disturbance of second and third molars was examined
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by Oikarinen et al. (1990). Eruption asymmetry was studied many times with different, sometimes opposite, results (Green and Aszkler, 1970; Garn and Smith, 1980; Mihailidis et
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al., 2009; Pelsmaekers et al., 1997). Genetic influence of the rate of tooth mineralization has also been assessed in the research of Merwin and Harris (1998). The timing of dental development is a crucial topic for anthropologists, dentists and forensic scientists; but the most commonly used methods in forensic anthropology and odontology in the living, namely Demirjian’s and Cameriere’s method, as well as applications of Demirjian’s charts to the third molar (Mincer et al., 1993) have never been assessed in this perspective.
Demirjian’s method (Demirjian et al., 1973) is based on morphological stages of seven developing teeth and determines age in individuals up to16 years. The method is widely used and accepted, thanks to an easy and universal maturity scoring system. The same stages (from A to H) can be applied also to the third molars, in order to obtain information concerning age in individuals older than 16 years: this allowed several authors (i.e. Mincer et al., 1993), to provide sheets reporting age of development of third molars according to Demirjian’s classifications (hence our denomination from now on as “Mincer’s” method).
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Cameriere’s methods, on the other hand, are based on metric analyses: on the measurement of open apices for age estimation in children (Cameriere et al., 2006) and on the measurement of pulp/tooth ratio for adults (Cameriere et al., 2004, 2007, 2009). For the sake of simplicity, we will from now on, however, refer to the Demirjian’s method, Mincer’s method and Cameriere’s methods. The methods of Demirjian and of Mincer have been designated as the most reliable among
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others (Cunha et al., 2009) and they are generally applied in the forensic field and frequently used by practical dentists. It is surprising that none of these methods has ever been applied to
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a twin model with the intention of determining whether the characters observed in these
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methods vary in genetically related individuals living in the same conditions.
Material and methods
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Dental orthopantograms performed for clinical purposes at the University Dental Clinical Centre of Kosovo were used for this study. The radiological examinations were performed between 1993 and 2003. The sample included 77 pairs of twins (154 individuals, 84 boys and
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70 girls of European origin and all from Kosovo from middle class families). After examination, low quality radiographs and those with dental abnormalities were excluded. The
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final sample consisted of 64 twin pairs: 21 of monozygotic twins, 30 dizygotic same-sex and
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13 dizygotic opposite-sexed (Table 1). The age range was 5.8 – 22.6 years with a mean age of 14.4 years. Distinction between monozygotic and dizygotic was performed according to the similarity method introduced by Siemens in 1924 and adapted by Essen-Moller in 1941 which takes into consideration the resemblance between morphological characteristics (Dencker et al., 1961).
INSERT Table 1 ABOUT HERE
Dental age of all suitable sets aged between 5.8 and 15.9 years was determined by the method of Demirjian, based on seven left mandibular teeth. Intra-pair age differences were estimated and the values compared within the twin groups and between them. Next, the developmental stages of third molars (preferably from the left side) were observed in pairs between 13.6 and 22.6 years of age by the Mincer’s method. The intra-pair variation was assessed separately for maxillary and mandibular molars. Cameriere’s method based on the measurement of open apices was applied to monozygotic twin pairs previously aged by the
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Demirjian method (less than 16 years old) whereas the method which focuses on the pulp/tooth area ratio was used for monozygotic pairs above 13.5 years of age, previously scored according to Mincer; the intra-pair differences of observed dental age were then counted once again. The statistical significance of intra-pair age differences was determined using a paired T-test. Cameriere’s methods were performed by one observer - the author of the method. The
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Demirjian’s and Mincer’s methods were applied by two observers each, independently, and
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the inter-observer error was evaluated.
Results
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Demirjian’s method
The difference in dental age within each pair was compared. The percentages of
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dis/agreement, mean intra-pair differences and maximum values are listed in Table 2. The lowest mean intra-pair difference was found in monozygotic pairs (0.56 years), immediately followed by dizygotic same-sex group (0.69 years) while the dizygotic opposite-sex pairs had
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INSERT Table 2 ABOUT HERE
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one-time greater mean difference (1.24 years).
The greatest percentage of agreement (number of pairs where both sibs reach the same maturity score) was found within pairs in the identical group (64%), followed again by dizygotic same-sex group with 40% of agreement whereas dizygotic opposite-sex pairs had no agreement (0%).
The maximum difference within monozygotic pairs was 1.85 years and mean observed difference of age within monozygotic pairs was statistically significant (t14 = 3.049, p < 0.01). Significant difference between co-twins was found also in both dizygotic groups (same-sex: t19 = 3.931, opposite-sex: t8 = 4.827; p < 0.01). Intra-observer error was calculated at 86% within a one year variation.
Mincer’s method The evaluation of third molar development was limited by the small number of teeth present in the sample so the values have a merely informative character. Table 3 shows mean intra-pair differences in dental age of maxillary third molars. The lowest value was
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unexpectedly found in the dizygotic opposite-sex group (0.08 years) whereas the monozygotic and dizygotic same-sex group had greater differences (0.43 years and 0.54 years respectively). Exact agreement of dental age (the same value of maturity score) within the co-twins varied from 33% to 75%.
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INSERT Table 3 ABOUT HERE The results of the intra-pair differences from mandibular third molars are listed in Table 4.
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Monozygotic pairs showed the lowest mean variance (0.32 years) which was less than that of the maxilla. The values of both dizygotic twin groups were quite similar (0.74 years for same-
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sex and 0.73 years for opposite-sex) and greater than in the maxilla. The percentage of exact agreement in dental age within the pairs was again variable: 60% in monozygotic twins, 50%
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in dizygotic same-sex and 0% in dizygotic opposite-sex.
The concordance between two observations by the same operator using the Mincer’s al., 2006).
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INSERT Table 4 ABOUT HERE
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method is known to be between 74 % and 81% according to previous publications (Dhanjal et
Cameriere’s methods
Dental age of monozygotic twins was scored and values were confronted with results found by Demirjian’s method (Table 5). The mean intra-pair difference between pairs observed with the Cameriere’s method was notably lower (0.18 years) than Demirjian’s (0.56 years). When age was assessed from the third molar, Mincer’s method gave the smaller difference when the mandibular molar was used (mean intra-pair difference 0.32 years) but maxillary third molars gave similar low values (mean difference 0.43 years). Apparently a greater disagreement between twins (mean difference 2.12 years) was obtained when the method of Cameriere was applied (Table 5). The intra-observer error for both Cameriere’s methods as performed by the author is not statistically significant (p>0.05) (De Luca et al., 2012).
INSERT Table 5 ABOUT HERE
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Inter-observer errors The mean inter-observer error for Demirjian’s method was 0.29 years and the difference between the observers was never more than one stage. The concordance rate was high also for the Mincer’s method applied to third molars. Even if the observers’ disagreement a few times reached two stages, the total mean difference was low (for maxilla: 0.33 years, for mandible:
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0.28 years) and very similar to Demirjian’s.
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Discussion
The rate of dental development and tooth eruption is dependent on many factors. Genetics
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as well environment play an important role. Genetic control of tooth eruption and growth rate has already been confirmed by many research groups (Garn et al., 1960; Green and Aszkler,
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1970; Hatton, 1955; Merwin and Harris, 1998).
The aim of this study was primarily to verify in monozygotic and dizygotic twins how biological age.
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dental age assessment methods would perform and up to what extent genetics would influence The comparison of mean intra-pair differences found by the Demirjian’s method disclosed
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low values in both monozygotic and dizygotic same-sex group against dizygotic opposite-sex
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group (Table 2). Low values within pairs of the dizygotic same-sex group with respect to monozygotic pairs could point to environmental factors largely influencing the rate of dental development. The higher disagreement between dizygotic opposite-sex co-twins could be explained by biological dissimilarities and different timing of growth processes in boys and girls.
Results for the maxilla are greatly affected by the small sample size (Table 3). Differences in mandibular third molar development were lower in monozygotic twins than in dizygotic groups which showed quite similar mean intra-pair variation (Table 4). This finding could point to a genetic influence on the rate of third molar development, but the sample is too small for a significant statement. When we compare percentage of absolute agreement in co-twins among all three twin groups, we can find similar results for Demirjian’s and Mincer’s methods applied to the mandibular third molar: the greatest percentage of agreement is in the monozygotic group (60 % - 64%), the lower value in dizygotic same-sex group (40% - 50%) and no agreement in the dizygotic opposite-sex group (0%).
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The inter-pair differences ascertained by Cameriere’s method (based on the measurement of open apices) were notably lower than when we applied Demirjian’s method whereas the absolute agreement between co-twins was of the same frequency for both methods. When the age of adolescents and young adults was assessed by the third molar, lower intra-pair differences were found using Mincer’s method whereas very large differences were observed when applying Cameriere’s method focused on the pulp/tooth area ratio measurement. Using
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Mincer’s method, full agreement in maturity score was observed in mandibular molars whereas for the maxilla no agreement was observed using this method as well as using
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Cameriere’s method on pairs older than 16 years (Table 6).
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INSERT Table 6 ABOUT HERE
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Such disagreements found by each method in the same twin pairs may be due to the nature of the methods: Demirjian’s and Mincer’s methods are based on an atlas/scoring system which divides the process of tooth development into eight stages (so it is more probable that
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two teeth will belong to the same stage) whereas Cameriere’s method refers to a linear regression function of a continuous developmental process and finding a difference between
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two persons is much easier.
A comparison of our results with those of previously performed studies is complicated
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because the Mincer method and Cameriere’s method were never applied on a twin set. There is only one study where the dental age of twins was determined by Demirjian’s method, performed by Pelsmaeker et al. (1997) who aimed to determine the genetic and environmental influence of dental maturation: correlation coefficients for the mean maturation score of the mandibular teeth were presented. The intra-pair correlation was significantly greater in the monozygotic pairs than in same-sex dizygotic pairs. These results are in agreement with ours: the difference of monozygotic pairs was the lowest, they were more similar than pairs of dizygotic twin groups.
Regardless of the methods used and their different performance, the results of our research confirmed that the rate of tooth development is an individual matter and as indicated before, it is not completely concordant even in monozygotic twins. The mean intra-pair difference of monozygotic pairs observed by three applied methods was never greater than six months in children as well as in young adults. On the other hand, the difference in dental age between co-twins was found by all applied methods and the maximum difference in dental age between monozygotic twins was surprisingly large. According to our results, the difference
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within monozygotic pairs could be nearly two years (in children under 16 years of age) and in adolescents and young adults even four years. Although monozygotic twins are much more similar than dizygotic twins and singletons in timing of dental development, the maximum discordance among monozygotic twins illustrates that environmental factors are extremely important. This study proves once again the great variability of growth even among twins and this
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should be food for thought; in other words this study seems to indicate using 3 samples of
twins distinguished by zygosity and sex that mean intrasample differences were greater than
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intersample differences and especially when comparing maximum intrasample differences. dental age both in the clinical and forensic scenario.
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References
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This should lead to some circumspection in the interpretation of systematic estimations of
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Table 1. Numbers of individuals involved in the study Total obtained
Suitable for research
Twins Pairs
Pairs
Pairs ≤ 16
Pairs > 16
Age interval
Mean age
24
21
14
7
8.0 – 22.6
15.4
Male
14
11
7
4
8.0 – 22.6
15.6
Female
10
10
7
3
9.9 – 22.1
15.2
DZ same-sex
39
30
20
10
8.4 – 21.9
14.7
Male
21
16
11
Female
18
14
9
DZ opposite-sex
14
13
12
TOTAL
77
64
46
cr 8.4 – 21.9
14.6
5
9.7 – 19.9
14.8
1
5.8 – 16.4
13.1
18
5.8 – 22.6
14.4
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5
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DZ – dizygotic
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Monozygotic
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Table 2. Intra-pair difference found by method of Demirjian, in years.
No. of pairs
Monozygotic 12
DZ Same-sex
DZ opposite-sex
20
9
Mean
0.56
0.69
1.24
Max
1.85
2.95
2.40
63.6
40.0
0.00
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% agreement
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Demirjian
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DZ – dizygotic
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Table 3. Intra-pair difference of maxillary third molar development, in years. Monozygotic
DZ same-sex
DZ opposite-sex
No. of pairs
4
Mean
0.43
0.54
0.08
Max
0.8
1.9
0.3
33.3
63.6
4
75
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% agreement
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Mincer
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DZ – dizygotic
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Table 4. Intra-pair difference of mandibular third molar development, in years. Monozygotic
DZ same-sex
DZ opposite-sex
No. of pairs
9
Mean
0.32
0.74
0.73
Max
0.8
2.2
1.3
60
3
50
0
cr
% agreement
12
ip t
Mincer
Ac ce pt e
d
M
an
us
DZ – dizygotic
16
Page 16 of 18
Cameriere
No. of pairs Average Max
pairs of age > 16 years 6 2.12 4.1 0
Ac ce pt e
d
M
an
us
cr
% agreement
pairs of age ≤ 16 years 15 0.18 1.5 40
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Table 5. Intra pair difference found by two of Cameriere’s methods in monozygotic pairs, in years.
17
Page 17 of 18
Table 6. Intra-pair difference in monozygotic twins found by different methods, in years Inter-pair diff. ≤ 16 years
No. of pairs
Demirjian
12
Cameriere
Mincer MX
Mincer MN
Cameriere
4
9
6 2.12
15
Average
0.56
0.18
0.43
0.32
Max
1.85
1.5
0.8
0.8
40
0
60
cr
40
4.1
0
us
% agreement
ip t
Method
Inter-pair dif. > 16 years
MX – maxillary third molars
Ac ce pt e
d
M
an
MN – mandibular third molars
18
Page 18 of 18
S0018-442X(14)00057-2 http://dx.doi.org/doi:10.1016/j.jchb.2014.05.003 JCHB 25348
To appear in: Received date: Accepted date:
23-1-2012 30-1-2014
Please cite this article as: Pechn´ikov´a, M., De Angelis, D., Gibelli, D., Vecchio, V., Cameriere, R., Zeqiri, B., Cattaneo, C.,Twins and the paradox of dental-age estimations: a caution for researchers and clinicians., Journal of Comparative Human Biology (2014), http://dx.doi.org/10.1016/j.jchb.2014.05.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Twins and the paradox of dental-age estimations: a caution for researchers and clinicians. M. Pechníkováa, b, D. De Angelisb, D. Gibellia, V. Vecchiob, R. Camerierec, B. Zeqirid†, C.
a
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Cattaneoa*
LABANOF – Laboratorio di Antropologia ed Odontologia Forense, Sezione di Medicina
cr
Legale, Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, b
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Via Mangiagalli 37 - 20133 Milano, Italy
Institute of Anatomy, Department of Anatomy, Histology and Embryology, Faculty of
Medicine, University of Ostrava, 70103 Ostrava, Czech Republic
Institute of Legal Medicine, University of Macerata, 62100 Macerata, Italy
d
University Dental Clinical Center of Kosovo
Ac ce pt e
d
M
an
c
Received 23 January 2012, accepted 30 January 2014
*Corresponding author. Tel.: +39 0250315678, fax: +39 02-50315724. E-mail address: [email protected] (Cristina Cattaneo)
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Page 1 of 18
Abstract The biological age difference among twins is frequently an issue in studies of genetic influence on various dental features, particularly dental development. The timing of dental development is a crucial issue also for many clinicians and researchers. The aim of this study was therefore to verify within groups of twins how dental development differs, by applying Demirjian’s method, Mincer’s charts of development of third molars and two of Cameriere’s
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methods for dental age estimation, which are among the most popular methods both in the
clinical and the forensic scenario. The sample consisted of 64 twin pairs: 21 monozygotic, 30
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dizygotic same-sex and 13 dizygotic opposite-sex with an age range between 5.8 and 22.6
years. Dental age was determined from radiographs using the mentioned methods. Results
us
showed that dental age of monozygotic twins is not identical even if they share all their genes. The mean intra-pair difference of monozygotic pairs was low and similar to the difference in
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dizygotic same-sex twins; the maximum difference between monozygotic twins, however, was surprisingly large (nearly two years). This should lead to some circumspection in the
Introduction
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scenario.
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interpretation of systematic estimations of dental age both in the clinical and forensic
Ac ce pt e
The special nature of the twinning process provides an opportunity to learn more about human development. Because monozygotic twins result from the same fertilized ovum, they share all their genes. Dizygotic twins, on the other hand, originate from two different ova that are separately fertilized and share, on average, only one half of their genes. By comparing monozygotic and dizygotic twins raised together, and thus subjected to similar environmental factors, the genetic contribution to a specific phenotypic characteristic can be assessed (Martin et al., 1997; Pelsmaekers et al., 1997). The first use of twins for the study of the relative roles of genes and environment is frequently attributed to Galton, but it was Siemens who in 1924 first used the classical twin study comparing similarities of monozygotic and dizygotic twins (Rende et al., 1990). Since then, plenty of twin studies were performed on a wide variety of physical and mental traits. The twin model is very often applied to various dental features. It was suggested by many research groups that genetic factors influence the manifestation of many dental disorders, anomalies and illnesses such as dental malformation, hypodontia (Liu et al., 1998, 1999; Townsend et al., 2005), supernumerary teeth (Łangowska-Adamczyk and Karmańska, 2001),
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Page 2 of 18
agenesis (Zengina et al., 2008), transposition (Peck et al., 1997), periodontitis (Michalowicz et al., 1991a; Potter, 1990) or dental caries (Boraas et al., 1988; Bretz et al., 2005a, 2005b; Townsend et al., 1998). However, much more attention has been given to genetic and environmental determinants of dental variation, especially to tooth size and morphology (Kabban et al., 2001; Townsend et al., 2009a), to the heritability of arch size and tooth size (Liu et al., 1998; Sharma et al.,
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1985) or to the variation in crown size of deciduous and permanent teeth (Dempsey et al., 1995; Hughes et al., 2000). Differences in dental diameters have been observed between
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monozygotic twins (Townsend et al., 2009a, 2009b) and also between twins and singletons
(Boklage, 1987). Research on occlusal morphology and its variations has been performed by
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two research groups (Corruccini et al., 1990; Su et al., 2008) and genetic variance for alveolar bone height has been estimated by Michalowicz et al. (1991b).
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Although the classical twin model has already been used for the study of genetic influence on dental eruption (Garn et al., 1960; Green and Aszkler, 1970; Hatton, 1955), the rate of genetic influence is still a question. In the study of Hughes et al. (2007) the authors quantified
M
the contribution of genetic and environmental factors to variation in timing of the eruption of human deciduous incisors; the eruption disturbance of second and third molars was examined
d
by Oikarinen et al. (1990). Eruption asymmetry was studied many times with different, sometimes opposite, results (Green and Aszkler, 1970; Garn and Smith, 1980; Mihailidis et
Ac ce pt e
al., 2009; Pelsmaekers et al., 1997). Genetic influence of the rate of tooth mineralization has also been assessed in the research of Merwin and Harris (1998). The timing of dental development is a crucial topic for anthropologists, dentists and forensic scientists; but the most commonly used methods in forensic anthropology and odontology in the living, namely Demirjian’s and Cameriere’s method, as well as applications of Demirjian’s charts to the third molar (Mincer et al., 1993) have never been assessed in this perspective.
Demirjian’s method (Demirjian et al., 1973) is based on morphological stages of seven developing teeth and determines age in individuals up to16 years. The method is widely used and accepted, thanks to an easy and universal maturity scoring system. The same stages (from A to H) can be applied also to the third molars, in order to obtain information concerning age in individuals older than 16 years: this allowed several authors (i.e. Mincer et al., 1993), to provide sheets reporting age of development of third molars according to Demirjian’s classifications (hence our denomination from now on as “Mincer’s” method).
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Page 3 of 18
Cameriere’s methods, on the other hand, are based on metric analyses: on the measurement of open apices for age estimation in children (Cameriere et al., 2006) and on the measurement of pulp/tooth ratio for adults (Cameriere et al., 2004, 2007, 2009). For the sake of simplicity, we will from now on, however, refer to the Demirjian’s method, Mincer’s method and Cameriere’s methods. The methods of Demirjian and of Mincer have been designated as the most reliable among
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others (Cunha et al., 2009) and they are generally applied in the forensic field and frequently used by practical dentists. It is surprising that none of these methods has ever been applied to
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a twin model with the intention of determining whether the characters observed in these
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methods vary in genetically related individuals living in the same conditions.
Material and methods
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Dental orthopantograms performed for clinical purposes at the University Dental Clinical Centre of Kosovo were used for this study. The radiological examinations were performed between 1993 and 2003. The sample included 77 pairs of twins (154 individuals, 84 boys and
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70 girls of European origin and all from Kosovo from middle class families). After examination, low quality radiographs and those with dental abnormalities were excluded. The
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final sample consisted of 64 twin pairs: 21 of monozygotic twins, 30 dizygotic same-sex and
Ac ce pt e
13 dizygotic opposite-sexed (Table 1). The age range was 5.8 – 22.6 years with a mean age of 14.4 years. Distinction between monozygotic and dizygotic was performed according to the similarity method introduced by Siemens in 1924 and adapted by Essen-Moller in 1941 which takes into consideration the resemblance between morphological characteristics (Dencker et al., 1961).
INSERT Table 1 ABOUT HERE
Dental age of all suitable sets aged between 5.8 and 15.9 years was determined by the method of Demirjian, based on seven left mandibular teeth. Intra-pair age differences were estimated and the values compared within the twin groups and between them. Next, the developmental stages of third molars (preferably from the left side) were observed in pairs between 13.6 and 22.6 years of age by the Mincer’s method. The intra-pair variation was assessed separately for maxillary and mandibular molars. Cameriere’s method based on the measurement of open apices was applied to monozygotic twin pairs previously aged by the
4
Page 4 of 18
Demirjian method (less than 16 years old) whereas the method which focuses on the pulp/tooth area ratio was used for monozygotic pairs above 13.5 years of age, previously scored according to Mincer; the intra-pair differences of observed dental age were then counted once again. The statistical significance of intra-pair age differences was determined using a paired T-test. Cameriere’s methods were performed by one observer - the author of the method. The
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Demirjian’s and Mincer’s methods were applied by two observers each, independently, and
cr
the inter-observer error was evaluated.
Results
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Demirjian’s method
The difference in dental age within each pair was compared. The percentages of
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dis/agreement, mean intra-pair differences and maximum values are listed in Table 2. The lowest mean intra-pair difference was found in monozygotic pairs (0.56 years), immediately followed by dizygotic same-sex group (0.69 years) while the dizygotic opposite-sex pairs had
Ac ce pt e
INSERT Table 2 ABOUT HERE
d
M
one-time greater mean difference (1.24 years).
The greatest percentage of agreement (number of pairs where both sibs reach the same maturity score) was found within pairs in the identical group (64%), followed again by dizygotic same-sex group with 40% of agreement whereas dizygotic opposite-sex pairs had no agreement (0%).
The maximum difference within monozygotic pairs was 1.85 years and mean observed difference of age within monozygotic pairs was statistically significant (t14 = 3.049, p < 0.01). Significant difference between co-twins was found also in both dizygotic groups (same-sex: t19 = 3.931, opposite-sex: t8 = 4.827; p < 0.01). Intra-observer error was calculated at 86% within a one year variation.
Mincer’s method The evaluation of third molar development was limited by the small number of teeth present in the sample so the values have a merely informative character. Table 3 shows mean intra-pair differences in dental age of maxillary third molars. The lowest value was
5
Page 5 of 18
unexpectedly found in the dizygotic opposite-sex group (0.08 years) whereas the monozygotic and dizygotic same-sex group had greater differences (0.43 years and 0.54 years respectively). Exact agreement of dental age (the same value of maturity score) within the co-twins varied from 33% to 75%.
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INSERT Table 3 ABOUT HERE The results of the intra-pair differences from mandibular third molars are listed in Table 4.
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Monozygotic pairs showed the lowest mean variance (0.32 years) which was less than that of the maxilla. The values of both dizygotic twin groups were quite similar (0.74 years for same-
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sex and 0.73 years for opposite-sex) and greater than in the maxilla. The percentage of exact agreement in dental age within the pairs was again variable: 60% in monozygotic twins, 50%
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in dizygotic same-sex and 0% in dizygotic opposite-sex.
The concordance between two observations by the same operator using the Mincer’s al., 2006).
Ac ce pt e
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INSERT Table 4 ABOUT HERE
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method is known to be between 74 % and 81% according to previous publications (Dhanjal et
Cameriere’s methods
Dental age of monozygotic twins was scored and values were confronted with results found by Demirjian’s method (Table 5). The mean intra-pair difference between pairs observed with the Cameriere’s method was notably lower (0.18 years) than Demirjian’s (0.56 years). When age was assessed from the third molar, Mincer’s method gave the smaller difference when the mandibular molar was used (mean intra-pair difference 0.32 years) but maxillary third molars gave similar low values (mean difference 0.43 years). Apparently a greater disagreement between twins (mean difference 2.12 years) was obtained when the method of Cameriere was applied (Table 5). The intra-observer error for both Cameriere’s methods as performed by the author is not statistically significant (p>0.05) (De Luca et al., 2012).
INSERT Table 5 ABOUT HERE
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Page 6 of 18
Inter-observer errors The mean inter-observer error for Demirjian’s method was 0.29 years and the difference between the observers was never more than one stage. The concordance rate was high also for the Mincer’s method applied to third molars. Even if the observers’ disagreement a few times reached two stages, the total mean difference was low (for maxilla: 0.33 years, for mandible:
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0.28 years) and very similar to Demirjian’s.
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Discussion
The rate of dental development and tooth eruption is dependent on many factors. Genetics
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as well environment play an important role. Genetic control of tooth eruption and growth rate has already been confirmed by many research groups (Garn et al., 1960; Green and Aszkler,
an
1970; Hatton, 1955; Merwin and Harris, 1998).
The aim of this study was primarily to verify in monozygotic and dizygotic twins how biological age.
M
dental age assessment methods would perform and up to what extent genetics would influence The comparison of mean intra-pair differences found by the Demirjian’s method disclosed
d
low values in both monozygotic and dizygotic same-sex group against dizygotic opposite-sex
Ac ce pt e
group (Table 2). Low values within pairs of the dizygotic same-sex group with respect to monozygotic pairs could point to environmental factors largely influencing the rate of dental development. The higher disagreement between dizygotic opposite-sex co-twins could be explained by biological dissimilarities and different timing of growth processes in boys and girls.
Results for the maxilla are greatly affected by the small sample size (Table 3). Differences in mandibular third molar development were lower in monozygotic twins than in dizygotic groups which showed quite similar mean intra-pair variation (Table 4). This finding could point to a genetic influence on the rate of third molar development, but the sample is too small for a significant statement. When we compare percentage of absolute agreement in co-twins among all three twin groups, we can find similar results for Demirjian’s and Mincer’s methods applied to the mandibular third molar: the greatest percentage of agreement is in the monozygotic group (60 % - 64%), the lower value in dizygotic same-sex group (40% - 50%) and no agreement in the dizygotic opposite-sex group (0%).
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Page 7 of 18
The inter-pair differences ascertained by Cameriere’s method (based on the measurement of open apices) were notably lower than when we applied Demirjian’s method whereas the absolute agreement between co-twins was of the same frequency for both methods. When the age of adolescents and young adults was assessed by the third molar, lower intra-pair differences were found using Mincer’s method whereas very large differences were observed when applying Cameriere’s method focused on the pulp/tooth area ratio measurement. Using
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Mincer’s method, full agreement in maturity score was observed in mandibular molars whereas for the maxilla no agreement was observed using this method as well as using
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Cameriere’s method on pairs older than 16 years (Table 6).
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INSERT Table 6 ABOUT HERE
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Such disagreements found by each method in the same twin pairs may be due to the nature of the methods: Demirjian’s and Mincer’s methods are based on an atlas/scoring system which divides the process of tooth development into eight stages (so it is more probable that
M
two teeth will belong to the same stage) whereas Cameriere’s method refers to a linear regression function of a continuous developmental process and finding a difference between
d
two persons is much easier.
A comparison of our results with those of previously performed studies is complicated
Ac ce pt e
because the Mincer method and Cameriere’s method were never applied on a twin set. There is only one study where the dental age of twins was determined by Demirjian’s method, performed by Pelsmaeker et al. (1997) who aimed to determine the genetic and environmental influence of dental maturation: correlation coefficients for the mean maturation score of the mandibular teeth were presented. The intra-pair correlation was significantly greater in the monozygotic pairs than in same-sex dizygotic pairs. These results are in agreement with ours: the difference of monozygotic pairs was the lowest, they were more similar than pairs of dizygotic twin groups.
Regardless of the methods used and their different performance, the results of our research confirmed that the rate of tooth development is an individual matter and as indicated before, it is not completely concordant even in monozygotic twins. The mean intra-pair difference of monozygotic pairs observed by three applied methods was never greater than six months in children as well as in young adults. On the other hand, the difference in dental age between co-twins was found by all applied methods and the maximum difference in dental age between monozygotic twins was surprisingly large. According to our results, the difference
8
Page 8 of 18
within monozygotic pairs could be nearly two years (in children under 16 years of age) and in adolescents and young adults even four years. Although monozygotic twins are much more similar than dizygotic twins and singletons in timing of dental development, the maximum discordance among monozygotic twins illustrates that environmental factors are extremely important. This study proves once again the great variability of growth even among twins and this
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should be food for thought; in other words this study seems to indicate using 3 samples of
twins distinguished by zygosity and sex that mean intrasample differences were greater than
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intersample differences and especially when comparing maximum intrasample differences. dental age both in the clinical and forensic scenario.
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References
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This should lead to some circumspection in the interpretation of systematic estimations of
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Boraas, J.C., Messer, L.B., Till, M.J., 1988. A genetic contribution to dental caries, occlusion, and morphology as demonstrated by twins reared apart. J. Dent. Res. 67, 1150-1155.
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Bretz, W.A., Corby, P.M., Hart, T.C., Costa, S., Coelho, M.Q., Weyant, R.J., Robinson, M.,
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Schork, N.J., 2005a. Dental caries and microbial acid production in twins. Caries Res. 39, 168-172.
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Corruccini, R.S., Townsend, G.C., Richards, L.C., Brown, T., 1990. Genetic and environmental determinants of dental occlusal variation in twins of different nationalities. Hum. Biol. 62, 353-367. Cunha, E., Baccino, E., Martrille, L., Ramsthaler, F., Prieto, J., Schuliar, Y., Lynnerup, N., Cattaneo, C., 2009. The problem of aging human remains and living individuals: a review. Forensic Sci. Int. 15, 1-13.
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De Luca, S., De Giorgio, S., Butti. A.C., Biagi, R., Cingolani, M., Cameriere, R., 2012. Age estimation in children by measurement of open apices in tooth roots: study of a Mexican
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Demirjian, A., Goldstein, H., Tanner, J.M., 1973. A new system of dental age assessment.
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Hum. Biol. 45, 211-227.
Dempsey, P.J., Townsend, G.C., Martin, N.G., Neale, M.C., 1995. Genetic covariance
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structure of incisor crown size in twins. J. Dent. Res. 74, 1389-1398.
Dencker, S.J., Hauge, M., Kaij, L., Nielsen, A., 1961. The use of anthropological traits and blood groups in the determination of the zygosity of twins. Acta Genet. 11, 265-285.
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Dhanjal, K.S., Bhardwaj, M.K., Liversidge, H.M., 2006. Reproducibility of radiographic stage assessment of third molars, Forensic Sci. Int. 159S, S74-77. Dent. Res. 39, 170-175.
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Garn, S.M., Lewis, A.B., Polacheck, D.L., 1960. Sibling similarities in dental development. J.
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Garn, S.M., Smith, B.H., 1980. Patterned asymmetry in tooth emergence timing. J. Dent. Res. 59, 1526-1527.
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Hatton, M.E., 1955. A measure of the effects of heredity and environment on eruption of the deciduous teeth. J. Dent. Res. 34, 397-401. Hughes, T., Dempsey, P., Richards, L., Townsend, G., 2000. Genetic analysis of deciduous tooth size in Australian twins. Arch. Oral Biol. 45, 997-1004. Hughes, T.E., Bockmann, M.R., Seow, K., Gotjamanos, T., Gully, N., Richards, L.C., Townsend, G.C., 2007. Strong genetic control of emergence of human primary incisors. J. Dent. Res. 86, 1160-1165. Kabban, M., Fearne, J., Jovanovski, V., Zou, L., 2001. Tooth size and morphology in twins. Int. J. Paediatr. Dent. 11, 333-339. Liu, H., Deng, H., Cao, C.F., Ono, H., 1998. Genetic analysis of dental traits in 82 pairs of female-female twins. Chin. J. Dent. Res. 1, 6-12.
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Liu, H., Deng, H., Cao, C., 1999. Genetic analysis of tooth developement and eruption in 82 pairs of female-female twins. Zhonghua Kou Qiang Yi Xue Za Zhi 34, 159-161. Łangowska-Adamczyk, H., Karmańska, B., 2001. Similar locations of impacted and supernumerary teeth in monozygotic twins: A report of 2 cases. Am. J. Orthod. Dentofacial. Orthop. 119, 67-70. Martin, N., Boomsma, D., Machin, G., 1997. A twin-pronged attack on complex trails. Nat.
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Genet. 17, 387-392.
Merwin, D.R., Harris, E.F., 1998. Sibling similarities in the tempo of human tooth
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Bouchard, T.J. Jr, Pihlstrom, B.L., 1991a. Periodontal findings in adult twins. J. Periodontol. 62, 293-299.
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Michalowicz, B.S., Aeppli, D., Kuba, R.K., Bereuter, J.E., Conry, J.P., Segal, N.L., Bouchard, T.J., Jr., Pihlstrom, B.L., 1991b. A twin study of genetic variation in proportional radiographic alveolar bone height. J. Dent. Res. 70, 1431-1435.
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Mihailidis, S., Woodroffe, S.N., Hughes, T.E., Bockmann, M.R., Townsend, G.C., 2009. Patterns of asymmetry in primary tooth emergence of Australian twins. Front. Oral. Biol.
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Mincer, H.H., Harris, E.F., Berryman, H.E., 1993. The A.B.F.O. study of third molar
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Peck, S., Peck, L., Hirsh, G., 1997. Mandibular lateral incisor-canine transposition in monozygotic twins. ASDC J. Dent. Child 64, 409-413. Pelsmaekers, B., Loos, R., Carels, C., Derom, C., Vlietinck, R., 1997. The Genetic Contribution to Dental Maturation. J. Dent. Res. 76, 1337-1340. Potter, R.H., 1990. Twin half-sibs: a research design for genetic epidemiology of common dental disorders. J. Dent. Res. 69, 1527-1530. Rende, D., Plomin, R., Vandenberg, .SG., 1990. Who discovered the twin method? Behav. Genet. 20, 277-285. Sharma, K., Corruccini, R.S., Henderson, A.M., 1985. Genetic variance in dental dimensions of Punjabi twins. J. Dent. Res. 64, 1389-1391.
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Su, C.Y., Corby, P.M., Elliot, M.A., Studen-Pavlovich, D.A., Ranalli, D.N., Rosa, B., Wessel, J., Schork, N.J., Hart, T.C., Bretz, W.A., 2008. Inheritance of occlusal topography: a twin study. Eur. Arch. Paediatr. Dent. 9, 19-24. Townsend, G.C., Aldred, M.J., Bartold, P.M., 1998. Genetic aspects of dental disorders. Aust. Dent. J. 43, 269-286. Townsend, G.C., Richards, L., Hughes, T., Pinkerton, S., Schwerdt, W., 2005. Epigenetic
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influences may explain dental differences in monozygotic twin pairs. Aust. Dent. J. 50, 95100.
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Townsend, G., Hughes, T., Luciano, M., Bockmann, M., Brook, A., 2009a. Genetic and environmental influences on human dental variation: A critical evaluation of studies
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involving twins. Arch. Oral Biol. 54, 45-51.
Townsend, G., Hughes, T., Bockmann, M., Smith, R., Brook, A., 2009b. How studies of twins
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can inform our understanding of dental morphology. Front. Oral. Biol. 13, 136-141. Zengin, A.Z., Sumer, A.P., Karaarslan, E., 2008. Impacted primary tooth and tooth agenesis: a
Ac ce pt e
d
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case report of monozygotic twins. Eur. J. Dent. 2, 299-302.
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Table 1. Numbers of individuals involved in the study Total obtained
Suitable for research
Twins Pairs
Pairs
Pairs ≤ 16
Pairs > 16
Age interval
Mean age
24
21
14
7
8.0 – 22.6
15.4
Male
14
11
7
4
8.0 – 22.6
15.6
Female
10
10
7
3
9.9 – 22.1
15.2
DZ same-sex
39
30
20
10
8.4 – 21.9
14.7
Male
21
16
11
Female
18
14
9
DZ opposite-sex
14
13
12
TOTAL
77
64
46
cr 8.4 – 21.9
14.6
5
9.7 – 19.9
14.8
1
5.8 – 16.4
13.1
18
5.8 – 22.6
14.4
an
us
5
Ac ce pt e
d
M
DZ – dizygotic
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Monozygotic
13
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Table 2. Intra-pair difference found by method of Demirjian, in years.
No. of pairs
Monozygotic 12
DZ Same-sex
DZ opposite-sex
20
9
Mean
0.56
0.69
1.24
Max
1.85
2.95
2.40
63.6
40.0
0.00
cr
% agreement
ip t
Demirjian
Ac ce pt e
d
M
an
us
DZ – dizygotic
14
Page 14 of 18
Table 3. Intra-pair difference of maxillary third molar development, in years. Monozygotic
DZ same-sex
DZ opposite-sex
No. of pairs
4
Mean
0.43
0.54
0.08
Max
0.8
1.9
0.3
33.3
63.6
4
75
cr
% agreement
11
ip t
Mincer
Ac ce pt e
d
M
an
us
DZ – dizygotic
15
Page 15 of 18
Table 4. Intra-pair difference of mandibular third molar development, in years. Monozygotic
DZ same-sex
DZ opposite-sex
No. of pairs
9
Mean
0.32
0.74
0.73
Max
0.8
2.2
1.3
60
3
50
0
cr
% agreement
12
ip t
Mincer
Ac ce pt e
d
M
an
us
DZ – dizygotic
16
Page 16 of 18
Cameriere
No. of pairs Average Max
pairs of age > 16 years 6 2.12 4.1 0
Ac ce pt e
d
M
an
us
cr
% agreement
pairs of age ≤ 16 years 15 0.18 1.5 40
ip t
Table 5. Intra pair difference found by two of Cameriere’s methods in monozygotic pairs, in years.
17
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Table 6. Intra-pair difference in monozygotic twins found by different methods, in years Inter-pair diff. ≤ 16 years
No. of pairs
Demirjian
12
Cameriere
Mincer MX
Mincer MN
Cameriere
4
9
6 2.12
15
Average
0.56
0.18
0.43
0.32
Max
1.85
1.5
0.8
0.8
40
0
60
cr
40
4.1
0
us
% agreement
ip t
Method
Inter-pair dif. > 16 years
MX – maxillary third molars
Ac ce pt e
d
M
an
MN – mandibular third molars
18
Page 18 of 18