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https://doi.org/10.15644/asc53/2/2

Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka

Christopher Maier ; Eckerd College, Department of Anthropology, 4200 54th Ave. S. St. Petersburg, FL 33711, USA
Jelena Dumančić   ORCID icon orcid.org/0000-0002-6444-3041 ; Zavod za dentalnu antropologiju Stomatološkog fakulteta Sveučilišta u Zagrebu, Hrvatska; Klinika za stomatologiju Kliničkoga bolničkog centra Zagreb, Hrvatska
Hrvoje Brkić ; Zavod za dentalnu antropologiju Stomatološkog fakulteta Sveučilišta u Zagrebu, Hrvatska
Zvonimir Kaić   ORCID icon orcid.org/0000-0003-2213-9946 ; Hrvatska komora dentalne medicine, Zagreb, Hrvatska; Akademija medicinskih znanosti Hrvatske, Zagreb, Hrvatska
Ivana Savić Pavičin ; Zavod za dentalnu antropologiju Stomatološkog fakulteta Sveučilišta u Zagrebu, Hrvatska
Zvonko Poje ; Hrvatska komora dentalne medicine, Zagreb, Hrvatska
G. Richard Scott ; Zavod za antropologiju Sveučilišta u Nevadi, Reno, Nevada, SAD

Puni tekst: hrvatski, pdf (297 KB) str. 106-118 preuzimanja: 33* citiraj
APA 6th Edition
Maier, C., Dumančić, J., Brkić, H., Kaić, Z., Savić Pavičin, I., Poje, Z. i Scott, G.R. (2019). Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka. Acta stomatologica Croatica, 53 (2), 106-118. https://doi.org/10.15644/asc53/2/2
MLA 8th Edition
Maier, Christopher, et al. "Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka." Acta stomatologica Croatica, vol. 53, br. 2, 2019, str. 106-118. https://doi.org/10.15644/asc53/2/2. Citirano 19.11.2019.
Chicago 17th Edition
Maier, Christopher, Jelena Dumančić, Hrvoje Brkić, Zvonimir Kaić, Ivana Savić Pavičin, Zvonko Poje i G. Richard Scott. "Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka." Acta stomatologica Croatica 53, br. 2 (2019): 106-118. https://doi.org/10.15644/asc53/2/2
Harvard
Maier, C., et al. (2019). 'Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka', Acta stomatologica Croatica, 53(2), str. 106-118. https://doi.org/10.15644/asc53/2/2
Vancouver
Maier C, Dumančić J, Brkić H, Kaić Z, Savić Pavičin I, Poje Z i sur. Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka. Acta stomatologica Croatica [Internet]. 2019 [pristupljeno 19.11.2019.];53(2):106-118. https://doi.org/10.15644/asc53/2/2
IEEE
C. Maier, et al., "Morfologija krune zuba u osoba s Turnerovim i Klinefelterovim sindromom iz hrvatskog uzorka", Acta stomatologica Croatica, vol.53, br. 2, str. 106-118, 2019. [Online]. https://doi.org/10.15644/asc53/2/2
Puni tekst: engleski, pdf (297 KB) str. 106-118 preuzimanja: 40* citiraj
APA 6th Edition
Maier, C., Dumančić, J., Brkić, H., Kaić, Z., Savić Pavičin, I., Poje, Z. i Scott, G.R. (2019). Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample. Acta stomatologica Croatica, 53 (2), 106-118. https://doi.org/10.15644/asc53/2/2
MLA 8th Edition
Maier, Christopher, et al. "Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample." Acta stomatologica Croatica, vol. 53, br. 2, 2019, str. 106-118. https://doi.org/10.15644/asc53/2/2. Citirano 19.11.2019.
Chicago 17th Edition
Maier, Christopher, Jelena Dumančić, Hrvoje Brkić, Zvonimir Kaić, Ivana Savić Pavičin, Zvonko Poje i G. Richard Scott. "Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample." Acta stomatologica Croatica 53, br. 2 (2019): 106-118. https://doi.org/10.15644/asc53/2/2
Harvard
Maier, C., et al. (2019). 'Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample', Acta stomatologica Croatica, 53(2), str. 106-118. https://doi.org/10.15644/asc53/2/2
Vancouver
Maier C, Dumančić J, Brkić H, Kaić Z, Savić Pavičin I, Poje Z i sur. Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample. Acta stomatologica Croatica [Internet]. 2019 [pristupljeno 19.11.2019.];53(2):106-118. https://doi.org/10.15644/asc53/2/2
IEEE
C. Maier, et al., "Tooth Crown Morphology in Turner and Klinefelter Syndrome Individuals from a Croatian Sample", Acta stomatologica Croatica, vol.53, br. 2, str. 106-118, 2019. [Online]. https://doi.org/10.15644/asc53/2/2

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Sažetak
Svrha: Turnerov sindrom (TS) i Klinefelterov sindrom (KS) dvije su najčešće aneuploidije kromosoma X i svaka je povezana sa sustavnim poremećajima u rastu i razvoju. Istraživan je utjecaj tih sindroma na morfologiju krune zuba na uzorku osoba iz Hrvatske. Ispitanici i postupci: Uzorak je sadržavao 57 osoba s TS-om, 37 s KS-om i 88 u kontrolnom uzorku. Morfologija kruna zuba vrjednovana je prema Turner-Scottovu dentoantropološkom sustavu. Rezultati: Lopatasti sjekutići i hipokonus bili su značajno drukčiji u osoba s TS-om u odnosu prema kontroli i osobama s KS-om. Osobe s TS-om pokazuju niže stupnjeve ekspresije negoli one u drugim skupinama. Nadalje, značajno je različit bio broj lingvalnih kvržica na mandibularnim pretkutnjacima, hipokonulid na mandibularnom drugom kutnjaku i kvržica 7 na mandibularnom prvom kutnjaku, premda uparena usporedba nije rasvijetlila te razlike. Tuberculum dentale, distalni akcesorni greben očnjaka i Carabellijevo obilježje , bili su izraženi slično kao u kontroli. Osobe s KS-om nisu se značajno razlikovale od kontrolnog uzorka ni u jednom obilježju, što je možda povezano s veličinom uzorka. Zaključak: U dosadašnjim istraživanjimaautori pretpostavljaju da gubitak kromosoma X reducirajuće utječe na morfologiju krune zuba, što je
potvrđeno u ovom istraživanju. Osobe s TS-om pokazuju opće pojednostavljenu morfologiju zuba u usporedbi s kontrolnim uzorkom, premda su neka obilježja izražena podjednako kao u kontrolnom uzorku. Učinci KS-a manje su jasni. Premda se u dosadašnjim istraživanjima sugerira da prekobrojni kromosom X povećava dimenzije zubne krune, u ovom istraživanju nije nađen značajan učinak na morfologiju krune zuba.

Ključne riječi
morfologija krune zuba, Turnerov sindrom, Klinefelterov sindrom, kromosom X

Hrčak ID: 220894

URI
https://hrcak.srce.hr/220894

▼ Article Information



Introduction

Turner syndrome (TS) and Klinefelter syndrome (KS) represent the two most common disorders due to aneuploidy of the sex chromosomes. TS occurs in females with complete or partial absence of the second X chromosome, while KS affects males with an extra X chromosome(s). The leading symptom in both syndromes is gonadal dysgenesis. General growth and development are affected with the most consistent feature being short stature in TS and tall stature in KS (1, 2). Numerous, but mild, stigmata manifest in the craniofacial region including distinctive cephalometric features (3-10).

Pronounced effects on dental development have also been noted for TS and KS individuals (11-14). Dental researchers predominantly focus on the effects of these syndromes on tooth crown size, as compared to individuals with a normal chromosomal complement (15-25). Comparatively little research has explored the effects of these aneuploidies on tooth crown morphology (21, 26-28). Roots seem to be more affected than the crowns, demonstrating shortening and increased complexity in TS individuals (29-32) and an increase in root length and taurodontism among those with KS (26, 32, 33). Both syndromes are characterized by a higher incidence of malocclusion (24, 32, 34, 35).

With respect to crown morphology, TS individuals have been characterized by simplification (15, 17, 21, 32, 36-38). Distinctive patterns with respect to control populations are related to an overall reduction in tooth size and/or the thinning of enamel in TS individuals (15, 39). Most often these differences manifest as lower grades of expression of traits already present in the population. For example, incisor shoveling is found at lower grades, or is more commonly absent than in control groups (21), the size and number of lingual cusps on mandibular premolars may be reduced (15), the hypocone and/or the hypoconulid of the first molar is typically reduced or absent (21, 27, 28), and there is a tendency toward absence of Carabelli’s trait (21, 28). KS individuals show fewer differences in crown morphology, but the presence of additional X chromosomes has been linked to increased expression of Carabelli’s trait (32).

Since tooth crown traits are not simply discrete presence/absence of variables but exhibit a wide range of expression from slight to pronounced, researchers use ranked standards for scoring non-metrical variation of dental traits. The most widely used scheme and recommended standard is the Turner-Scott Dental Anthropology System, formerly ASUDAS (40, 41).

Data indicate that sex chromosome aberrations influence dental morphology in a variety of ways. To the knowledge of authors, despite numerous studies, a systematic analysis of morphological variants of all tooth classes in TS and KS individuals has not been published. To get a comprehensive and objective picture of the influence of X-chromosome aberration on the crown morphology of a complete dentition, a sample of Croatian individuals with TS and KS was evaluated using the Turner-Scott Dental Anthropology System.

Materials and Methods

In August 2014, GRS observed nonmetric crown traits on a sample of dental casts of TS and KS individuals and a control group of unrelated individuals at the University of Zagreb School of Dental Medicine (n=182) (Table 1). TS and KS individuals were part of a larger sample of individuals with various sex chromosome anomalies examined in the course of the research project ‘‘Characteristics of the Craniofacial Complex in Gonadal Dysgenesis’’ between 1981 and 1998 (Croatian Ministry of Science and Technology, Project 3-02-383). All individuals underwent dental exams, impressions, and radiographs at the Departments of Dental Anthropology and Orthodontics, School of Dental Medicine, University of Zagreb, Croatia. Karyotypes were determined by chromosome analysis of peripheral lymphocytes and skin fibroblasts. Informed consent was obtained from all participants and legal guardians.

Table 1 Sample composition
Karyotype n
Control 88
Turner Syndrome Total 57
45,X 33
45,X/46,XX 6
45,X/46X,r(X) 5
45,X/46,X,i(Xq) 5
45,X/46,X,frX 1
45,X/46,X,del(Xp) 1
46,X,i(Xq) 6
Klinefelter Syndrome Total 37
47,XXY 35
47,XXY/46,XY 2
Total 182

Dental morphological variants were scored following the guidelines of the Turner-Scott Dental Anthropology System, formerly ASUDAS (40, 41). The system consists of a set of plaques for permanent teeth, accompanied by trait descriptions and scoring standards. The Croatian population belongs to the Western Eurasian dental complex, which is characterized by relatively simple crown morphology (42, 43). As such, many traits of the Turner-Scott System are rare in European populations, and an insufficient amount of data were collected to present the findings of qualitative research in a coherent and meaningful way.. Additionally, factors like occlusal wear and ante mortem tooth loss precluded observations of some traits. The resulting dataset contains traits regularly observed in the three samples (Table 2).

Table 2 ASUDAS (Turner et al. 1991) traits observed, teeth recorded, and breakpoints used for analysis.
Trait Tooth Breakpoints
Shoveling UI1 0/1/2+
UI2 0/1/2+
Tuberculum dentale UI1 0-1/2-3/4+
UI2 0-1/2-3/4+
UC 0-1/2-3/4+
Hypocone UM1 <5/5
UM2 0-1/2-3/4+
Carabelli’s UM1 0-1/2-4/5+
UM2 0-1/2-4/5+
Cusp 5 UM1 0/1+
UM2 0/1+
Distal accessory ridge LC 0/1+
Multiple lingual cusps LP1 0/1/2+
LP2 0/1/2+
Hypoconulid LM1 0-1/2-3/4+
LM2 0/1+
Cusp 6 LM1 0/1+
LM2 0/1+
Cusp 7 LM1 0/1+
LM2 0/1+

U - upper dentition

L - lower dentition

I - incisor

C - canine

P - premolar

M – molar

For these analyses, dental morphological data were recorded following the individual count method (64). The underlying premise of the individual count method is that dental traits are threshold traits; consequently, the higher expression of the trait, regardless of side, is most indicative of the individual’s genotype. This method reduces redundancy in the data, and streamlines data collection for subsequent analysis.

Trait frequencies among TS individuals, KS individuals, and the control group were assessed for significant differences using the Pearson’s chi-square test. Trait frequencies for which a difference was found among groups were then analyzed using the Fischer’s exact test with the Bonferroni correction for multiple comparisons. The Fischer’s exact test was used to identify between which specific groups (e.g. TS/KS, TS/control, KS/control) differences in dental morphology occurred. Sexes were pooled for analyses. Both the TS and KS samples comprise a single sex, and most of the traits examined exhibit negligible sexual dimorphism (42).

Results

The frequencies for all traits recorded are presented in an appendix to facilitate future comparisons to other populations. Frequencies of the following traits showed no significant differences among groups: tuberculum dentale, Carabelli’s trait, cusp 5, canine distal accessory ridge, and cusp 6.

Individuals in the TS sample showed a variety of expression in dental crown traits, including both simple and pronounced grades (Figures 1 and 2). Of the traits examined, only incisor shoveling and the hypocone were significantly different (p=0.05) between individuals with TS and both control and KS individuals (Tables 3-4{ label needed for table-wrap[@id='t4'] }). Shoveling among TS individuals is significantly different from the control sample and individuals with KS on both the central and lateral incisors (p<0.05). Inspection of the relative frequencies of each shoveling score indicates that individuals with TS more often exhibit the absence of shoveling than both the control and KS samples, and that when present, it is expressed to a lesser degree (Table 3).

Table 3 Frequency of incisor shoveling. Frequencies among Turner syndrome individuals differ from both the control and Klinefelter syndrome groups (p=0.05).
Grade Control Turner syndrome Klinefelter syndrome
UI1 UI2 UI1 UI2 UI1 UI2
0 0.51 (43/84) 0.53 (46/86) 0.77 (44/57) 0.85 (44/52) 0.48 (11/23) 0.41 (9/22)
1 0.43 (36/84) 0.37 (32/86) 0.21 (12/57) 0.15 (8/52) 0.35 (8/23) 0.50 (11/22)
2+ 0.06 (5/84) 0.09 (8/86) 0.02 (1/57) 0.00 (0/52) 0.17 (4/23) 0.09 (2/22)

U - upper dentition

I - incisor

{ label needed for table-wrap[@id='t4'] }
Table 4 Frequency of the hypocone on maxillary first and second molars. Frequencies on the first molar are significantly different in Turner syndrome individuals than in both the control group and Klinefelter syndrome individuals (p=0.05). On the second molar, Turner syndrome individuals differ only from the control group (p=0.05)
Grade Control Turner syndrome Klinefelter syndrome
UM1 UM2 UM1 UM2 UM1 UM2
<5 (UM1)
0-1 (UM2)
0.56 (49/87) 0.39 (23/59) 0.96 (47/49) 0.52 (22/42) 0.59 (13/22) 0.26 (8/31)
5 (UM1)
2-3 (UM2)
0.44 (38/87) 0.59 (35/59) 0.04 (2/49) 0.31 (13/42) 0.41 (9/22) 0.52 (16/31)
4+ (UM2) NA 0.02 (1/59) NA 0.17 (7/42) NA 0.23 (7/31)

U - upper dentition

M – molar

The hypocone is significantly different in TS individuals compared to KS and control individuals, on the maxillary first molar, but only from control individuals on the second molar (p<0.01). As with shoveling, TS individuals are more likely to exhibit the absence of the hypocone than other groups, and instances in which the hypocone is present, it is minimally expressed (Table 4).

Additionally, significant differences were found among groups for lingual cusps on the mandibular premolars, the hypoconulid on the mandibular second molar, and cusp 7 on the mandibular first molar. Although the chi-square test identified that significant differences exist, the Bonferroni correction applied to the Fisher’s test did not identify any significant pair-wise comparisons. This difference is likely due to the conservative nature of the Bonferroni correction, which is designed to combat Type I error, or false positives, at the cost of a reduction in statistical power, or an increase in false negatives.

The frequencies of lingual premolar cusps and the hypoconulid on the second molar follow similar patterns to shoveling and the hypocone; that is, individuals with TS more frequently exhibit trait absence than either the control or KS samples (Appendix 1). TS individuals, for example, fail to exhibit a lingual cusp on the lower first premolar 21.4% of the time (Figure 1A, Figure 1B{ label needed for fig[@id='f1B'] }). This simplified phenotype is far less common in control (5.9%) and KS (2.9%) individuals. In cases where TS individuals express multiple lingual cusps or the hypoconulid, it is typically of a lesser degree than in the other groups. The frequency distribution for cusp 7 is different. TS individuals do not seem to have a marked increase in absence of the trait compared to other groups. However, the control sample is the only one of the three groups to have non-zero frequencies for expression above grade 2, which may contribute to this difference.

Figure 1A Turner syndrome, Case 1. TS individuals often show simplified crown morphology. A. Complete absence of shoveling and lingual tubercles on the six upper anterior teeth. B. No expression of Carabelli’s trait. C. A compressed upper second molar, also referred to as a ‘potato tooth.’ D. Upper third molar reduced in size.
ASC_53(2)_106-118-f1A
{ label needed for fig[@id='f1B'] }
Figure 1B Turner syndrome, Case 1. Morphological simplification in lower dentition. A. Lower canine with no marginal or accessory ridges. B. Lower first premolars have greatly reduced lingual cusps with no free apex. C. Significantly reduced hypoconulid on lower first molar. D. Pronounced reduction of entoconid (distolingual cusp) on lower second molar.
ASC_53(2)_106-118-f1B

Individuals with KS were not significantly different from the control individuals for any trait, though this may be a product of the small number of individuals observed with KS.

Discussion

The present research investigated nonmetric crown traits in TS and KS individuals, who express clinical manifestations of X chromosome aneuploidy. One benefit of this research is the systematic analysis of complete dentitions using a standard established for that purpose, thus giving an insight on the influence of the X chromosome on tooth crown morphology of a variety of tooth classes. Secondly, an assessment of nonmetric crown traits can be difficult and training is required to confidently distinguish between grades of individual traits. Since evaluation was performed by an experienced researcher (GRS), who is one of the authors of the standard, these distinctions were made with confidence, which is another benefit to this study. The syndrome groups, TS and KS, are well represented, both in the presence of common karyotypes and in their relative distributions (Table 1).

Ten traits in total were present both in syndromic groups and in the control group (Table 2). TS individuals showed a great variety including both simple and pronounced grades of expression. While some traits (shoveling, hypocone, lingual premolar cusps, hypoconulid on the second molar and cusp 7 on the first molar) were reduced in the TS group, the others showed frequencies and expressions comparable to those in the control sample (tuberculum dentale, canine distal accessory ridge, Carabelli’s trait, cusp 5, and cusp 6). This finding is new, as in the literature tooth crown morphology in TS is described as simplified (15, 17, 21, 28, 32, 36-39).

As KS manifest the opposite findings to TS regarding body stature, craniofacial patterning, mandibular growth, and tooth size, one would expect the same for tooth crown morphology. However, this study did not reveal any significant differences between KS and the control group. This result may be influenced by the small number of individuals in KS group, which is a potential limitation of this study.

Aneuploidies of the X chromosome, including KS and TS, affect tooth crown size (15-25). TS and KS influence tooth size due to differences in the number of X chromosomes, and consequently differences in amelogenin secretion and enamel formation (24, 32). The X chromosome has been linked to enamel thickness as well as the rate of dental development (2, 16, 32, 39, 44-46). Consequently, males affected by KS have larger teeth than males with a normal chromosomal complement (19, 32, 36, 44, 47-49). The importance of the X chromosome to tooth size is directly related to the number of extra X chromosomes, and its effect on general growth patterns and enamel thickness (50). Similarly, females affected by monosomatic (45,X), structural aberrations, and mosaic forms of TS have smaller teeth due to the absence of all or part of an X chromosome (13, 15, 17, 20, 23, 36, 37, 51, 52). Interestingly, because TS is an aneuploidy specifically of the X chromosome, it is only enamel formation that is affected; dentine does not appear to be affected by TS (17). Odontometric investigations on the effect of chromosomal aneuploidies on the dentition have identified an inverse relationship between the degree of size reduction and the length of time a given tooth requires for development. Teeth that take longer to develop, such as the canines, have less reduced crown diameters, whereas quickly developing teeth, like the molars, are more reduced (23, 36).

The discussion of the effect on tooth size is an important consideration with respect to dental crown morphology. There is a positive association between crown size and crown complexity, meaning that larger teeth exhibit crown traits more frequently and to a more pronounced degree (53-66). The size and degree of expression of Carabelli’s trait is reduced with small tooth size (21, 26, 28). Additionally, minimal expression of Carabelli’s trait and hypocone reduction have also been linked to one another (57, 65, 67, 68). Although crown size and complexity are correlated, there is not necessarily a causal link.

The most likely explanation for the relationship between tooth size and crown complexity is that both size and cusp number and pattern are regulated by the same or related processes (59). The role of enamel knots in tooth development may be critical. Enamel knots are regions of non-dividing cells on the inner enamel epithelium present during tooth formation. Signaling factors released by these regions promote cell growth in adjacent regions that ultimately form the cusps of the tooth (69-72). Additionally, several studies suggest that substances released by the enamel knots are involved in the regulation of crown size and cusp pattern (73-77). Nakayama and colleagues (28) argue that the complement of X chromosomes affects the development of enamel knots. If Nakayama and colleagues are correct in their hypothesized relationship between the X chromosome and the formation of enamel knots, then individuals missing an X chromosome, or part of one, would be expected to exhibit smaller teeth with fewer cusps, which is supported both by odontometric data (13, 15, 17, 20, 23, 36, 37, 51, 52) and the frequencies of morphological traits observed in this sample as well as in previous work (21, 26-28).

In this sample, individuals with TS exhibit significantly different frequencies for incisor shoveling and the hypocone, compared to control individuals and individuals with KS. Similar patterns were observed in Finnish and Norwegian samples (21, 26, 28, 68). Individuals with TS exhibit multiple lingual premolar cusps less frequently than the control group and the KS group. Although rarely examined, previous work has found that TS can result in fewer lingual cusps on the mandibular premolars (15). Furthermore, work on Carabelli’s trait and hypocone reduction (21, 26, 28, 68) has linked TS to a general reduction in cusp number, in some cases independent of the reduction in crown size. The generalized relationship between TS and cusp reduction may also explain the potential differences seen in expression of the hypoconulid and cusp 7, though to our knowledge, these patterns have not been previously described.

Several studies on the influence of different TS karyotypes on tooth size and morphology demonstrated that the isochromosome karyotype 46,X,i(Xq) (lack of the short arm Xp with duplication of the long arms Xq) is the most divergent showing the most reduced crown dimensions, the mosaic 45,X/46,XX karyotype (having both normal XX and one X sex chromosome cell lines) exhibits the largest crown dimensions, close to those of normal females, and the 45,X karyotype is intermediate to these extremes (13, 17, 25, 37, 68). In a recent study by Nakayama et al., the difference between karyotypes in distribution of Carabelli's cusp was not significant (68). Surprisingly, the same study found the absence of the hypocone to be most frequent in 45, X/46, XX individuals and the least frequent in the 45, X karyotype (68). Smaller crown size was associated with a reduced distolingual cusp but not with a reduction in Carabelli’s cusp. The hypothesized explanation of these findings is that the candidate genes (promoters) for controlling tooth crown size are located in the region PAR1 in Xp, whereas their inhibitor is located in the region PAR2 of Xq. Therefore, phenotypic variation is a result of an interactive equilibrium between the promoters and inhibitors. The process of unilateral X chromosome inactivation should also be considered. The comparison of TS karyotypes was not the aim of the present investigation; however, it is interesting that the two TS cases showing the largest grades of Carabelli's trait on M1 and a distinctive Carabelli's trait on M2 (Figures 2A and 2B{ label needed for fig[@id='f2B'] }) were both of 45, X karyotype. Where crown morphology is concerned, it is possible that 45, X karyotype is phenotypically closest to normal females.

Figure 2A Turner syndrome, Case 2. Not all TS individuals show simplification of crown morphology. A. Moderate to pronounced lingual tubercles on all six upper anterior teeth. B. A large grade 7 Carabelli’s trait on upper first molar (second molar also has a distinctive Carabelli’s trait). C. The upper second molar has a pronounced hypocone (distolingual cusp).
ASC_53(2)_106-118-f2A
{ label needed for fig[@id='f2B'] }
Figure 2B Turner syndrome, Case 2. In the lower dentition of the same individual, some morphology is evident although crown simplification is a hallmark of the Western Eurasian dentition. A. Two distinct lingual cusps with free apices on the lower first premolar. B. Distinct lingual cusp on lower second premolar. C. Distinct hypoconulid on lower first molar.
ASC_53(2)_106-118-f2B

If the size of the crown is correlated with morphological complexity, e.g. (53-55, 57, 58, 60, 63-66), it might be expected that individuals with KS would exhibit more complex dental morphology. Although the presence of an additional X chromosome does correlate with an increase in crown size in KS males (32, 36, 44, 47-49), it does not appear to have any effect on crown morphology in the Croatian sample. Mayhall and Alvesalo (78) also did not find differences between KS and normal males in Carabelli's trait expression. In the light of the hypothesis by Nakayama et al. (68), it is possible that two copies of the X chromosome in KS individuals contribute to a dosage of promoter and inhibitor genes that result in the suppression of the development of complex dental morphology.

The data on this Croatian sample are consistent with other studies on the effects of chromosomal aneuploidies on dental morphology, supporting the role of the X chromosome both in the production of enamel, and the development and pattern of tooth cusps. Though most traits exhibit the simplification expected in TS individuals, it is important to note that for some traits (tuberculum dentale, canine distal accessory ridge, Carabelli’s trait, cusp 5, and cusp 6), TS individuals have frequencies and expressions comparable to those seen in the control sample. Considering the findings of this research, classifying the effect of TS on dental crown morphology as ‘simplification’ may be an overly simplistic categorization. The available literature focuses on individuals from European samples. The Western Eurasian dental complex is already characterized by simplified crown morphology (42, 43, 79); therefore, the effects of these aneuploidies on populations with more complex morphology remain unknown.

Conclusions

Aneuploidies of the X chromosome affect dental development. The effect on tooth size is well-documented, but comparatively little research has focused on its effects on dental crown morphology. Previous studies suggest that the loss of X chromosome material has a reducing effect on dental crown morphology, which has been largely confirmed in this research. Although a typical Western Eurasian dentition is characterized by simplification, individuals with TS generally exhibit simpler morphology, particularly in expressions of incisor shoveling and the reduction of the hypocone. However, not all crown traits seem to be equally affected by the absent X chromosome; tuberculum dentale, canine distal accessory ridge, and Carabelli’s trait are in particular expressed similarly to the control sample. The effects of KS are less clear and may be elucidated through the study of populations with a more complex dental morphology. Though the presence of an extra X chromosome increases dental crown dimensions, there was no notable effect on crown morphology in this study.

Appendices

Appendix 1

Frequencies for all traits recorded in control individuals, individuals with Turner syndrome and individuals with Klinefelter syndrome.

Shoveling UI1 n 0 1 2 3 4 5 6 7
Control 84 0.512 0.429 0.060 0.000 0.000 0.000 0.000 0.000
TS 57 0.772 0.211 0.018 0.000 0.000 0.000 0.000 0.000
KS 23 0.478 0.348 0.174 0.000 0.000 0.000 0.000 0.000
Shoveling UI2 n 0 1 2 3 4 5 6 7
Control 86 0.535 0.372 0.093 0.000 0.000 0.000 0.000 0.000
TS 52 0.846 0.154 0.000 0.000 0.000 0.000 0.000 0.000
KS 22 0.409 0.500 0.091 0.000 0.000 0.000 0.000 0.000
Tuberculum dentale UI1 n 0 1 2 3 4 5
Control 85 0.376 0.224 0.224 0.118 0.059 0.000
TS 56 0.357 0.339 0.143 0.089 0.071 0.000
KS 24 0.417 0.292 0.167 0.083 0.042 0.000
Tuberculum dentale UI2 n 0 1 2 3 4 5
Control 81 0.346 0.309 0.235 0.086 0.012 0.012
TS 50 0.200 0.320 0.220 0.200 0.040 0.020
KS 19 0.526 0.263 0.211 0.000 0.000 0.000
Tuberculum dentale UC n 0 1 2 3 4 5
Control 85 0.235 0.353 0.271 0.118 0.024 0.000
TS 53 0.302 0.321 0.245 0.075 0.057 0.000
KS 26 0.269 0.346 0.192 0.154 0.038 0.000
Hypocone UM1 n 0 1 2 3 4 5
Control 87 0.000 0.000 0.000 0.023 0.540 0.437
TS 53 0.000 0.075 0.000 0.340 0.547 0.038
KS 22 0.000 0.000 0.000 0.136 0.455 0.409
Hypocone UM2 n 0 1 2 3 4 5
Control 78 0.077 0.218 0.077 0.372 0.244 0.013
TS 42 0.333 0.190 0.048 0.262 0.167 0.000
KS 28 0.143 0.143 0.143 0.429 0.143 0.000
Carabelli's UM1 n 0 1 2 3 4 5 6 7
Control 88 0.250 0.250 0.159 0.068 0.080 0.148 0.034 0.011
TS 54 0.519 0.130 0.130 0.074 0.037 0.056 0.019 0.037
KS 22 0.364 0.227 0.091 0.091 0.136 0.045 0.045 0.000
Carabelli's UM2 n 0 1 2 3 4 5 6 7
Control 74 0.838 0.083 0.012 0.012 0.012 0.024 0.000 0.000
TS 38 0.868 0.053 0.000 0.000 0.026 0.026 0.000 0.026
KS 27 0.889 0.037 0.000 0.037 0.037 0.000 0.000 0.000
Cusp 5 UM1 n 0 1 2 3 4 5
Control 76 0.908 0.066 0.026 0.000 0.000 0.000
TS 49 0.857 0.122 0.000 0.000 0.020 0.000
KS 18 0.722 0.278 0.000 0.000 0.000 0.000
Cusp 5 UM2 n 0 1 2 3 4 5
Control 57 0.737 0.193 0.070 0.000 0.000 0.000
TS 21 0.905 0.048 0.000 0.000 0.048 0.000
KS 19 0.842 0.053 0.053 0.053 0.000 0.000
Distal accessory ridge LC n 0 1 2 3 4 5
Control 83 0.723 0.181 0.084 0.000 0.012 0.000
TS 56 0.732 0.143 0.107 0.000 0.018 0.000
KS 26 0.885 0.115 0.000 0.000 0.000 0.000
Lingual cusp no. LP1 n 0 1 2 3 4 5 6 7
Control 85 0.059 0.729 0.188 0.024 0.000 0.000 0.000 0.000
TS 56 0.214 0.643 0.107 0.036 0.000 0.000 0.000 0.000
KS 34 0.029 0.676 0.118 0.147 0.029 0.000 0.000 0.000
Lingual cusp no. LP2 n 0 1 2 3 4 5 6 7
Control 87 0.000 0.356 0.437 0.138 0.057 0.000 0.011 0.000
TS 54 0.019 0.463 0.407 0.093 0.019 0.000 0.000 0.000
KS 24 0.000 0.542 0.292 0.083 0.083 0.000 0.000 0.000
Hypoconulid LM1 n 0 1 2 3 4 5
Control 83 0.084 0.000 0.036 0.241 0.494 0.145
TS 37 0.243 0.000 0.054 0.351 0.351 0.000
KS 7 0.143 0.143 0.000 0.143 0.571 0.000
Hypoconulid LM2 n 0 1 2 3 4 5
Control 80 0.863 0.038 0.013 0.038 0.050 0.000
TS 46 0.957 0.022 0.000 0.022 0.000 0.000
KS 19 0.789 0.105 0.053 0.000 0.053 0.000
Cusp 6 LM1 n 0 1 2 3 4 5
Control 78 0.885 0.038 0.077 0.000 0.000 0.000
TS 37 0.919 0.054 0.027 0.000 0.000 0.000
KS 7 1.000 0.000 0.000 0.000 0.000 0.000
Cusp 6 LM2 n 0 1 2 3 4 5
Control 79 1.000 0.000 0.000 0.000 0.000 0.000
TS 45 1.000 0.000 0.000 0.000 0.000 0.000
KS 17 0.941 0.000 0.059 0.000 0.000 0.000
Cusp 7 LM1 n 0 1 1A 2 3 4 5
Control 84 0.810 0.000 0.095 0.012 0.024 0.012 0.048
TS 32 0.844 0.031 0.063 0.063 0.000 0.000 0.000
KS 7 0.857 0.000 0.000 0.143 0.000 0.000 0.000
Cusp 7 LM2 n 0 1 1A 2 3 4 5
Control 75 0.933 0.000 0.067 0.000 0.000 0.000 0.000
TS 36 0.944 0.000 0.056 0.000 0.000 0.000 0.000
KS 16 0.938 0.000 0.063 0.000 0.000 0.000 0.000

U - upper dentition

L - lower dentition

I - incisor

C - canine

P - premolar

M – molar

Acknowledgements

The research project ‘‘Characteristics of the Craniofacial Complex in Gonadal Dysgenesis’’ was supported by the Croatian Ministry of Science and Technology, grant 3-02-383.

Notes

[1] Conflicts of interest The authors have declared that no competing interests exist.

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