Root Lengths in 47,XYY Males Permanent Teeth

Transcription

1 RESEARCH REPORTS Clinical R. Lähdesmäki 1 * and L. Alvesalo 1,2 1 Department of Oral Development and Orthodontics, Institute of Dentistry, University of Oulu, PL 5281, FIN OULUN YLIOPISTO, Finland; and 2 University Hospital of Oulu, Finland; *corresponding author, rlahdesm@mail.student.oulu.fi Root Lengths in 47,XYY Males Permanent Teeth J Dent Res 83(10): , 2004 ABSTRACT Studies on individuals with sex chromosome anomalies have demonstrated the promoting effect of the Y chromosome on tooth crown enamel and dentin growth. The present research investigated permanent tooth root lengths in 47,XYY males. The measurements were made from panoramic radiographs. The results indicate longer tooth roots in 47,XYY males compared with those in control males and females. The promoting effect of the Y chromosome on dental growth thus continues in the form of root dentin after the completion of crown growth. The results, together with those on tooth crown sizes in 47,XYY males, suggest that growth excesses are evident and final, beginning a few months after birth and continuing up to the age of 14 years, at least. The excess root dentin growth in 47,XYY males, as well as sexual dimorphism in the growth of crown and root dentin, might be caused by the same factor on the Y chromosome. KEY WORDS: 47,XYY males, Y chromosome, dental growth, tooth root, sexual dimorphism. Received August 26, 2003; Last revision July 8, 2004; Accepted July 19, 2004 A supplemental appendix to this article is published electronically only at INTRODUCTION 47,XYY males, or males with an extra Y chromosome, do not differ from normal males in terms of birth weight, height, or head circumference, but the velocity of height growth increases significantly from two years of age and continues to be high throughout childhood. This effect is still evident during the growth spurt in puberty, which occurs a few months later than in controls (Ratcliffe et al., 1992). The sex difference in the adult height of normal individuals is achieved through pubertal growth, but the growth excess in 47,XYY males is due both to growth during childhood and to pubertal growth. Relative to normal males, the extra Y chromosome in these males increases adult height to an extent that is equal to the difference between normal males and females that is, 47,XYY males are about 13 centimeters taller than normal males (Ratcliffe et al., 1992). Not only height but also virtually all adult body, head, and cephalometric dimensions of 47,XYY males are larger than those in normal males with similar body proportions (Varrela and Alvesalo, 1985; Grön et al., 1997). The hormone levels of 47,XYY males are generally normal and similar to those of the normal male population, although they seem to show greater variability in plasma testosterone levels (BeneZech and Noel, 1985). Previous studies on deciduous and permanent tooth crown dimensions in 47,XYY boys and men (Alvesalo et al., 1975; Alvesalo and Kari, 1977) have shown increased tooth crown growth. For example, the mesiodistal dimension of the upper permanent central incisor is about 5% larger than in normal males. Sexual dimorphism in permanent tooth crown sizes is from 2 to 4%, with males having larger teeth than females (Selmer-Olsen, 1949; Garn et al., 1964; Alvesalo, 1971). This is due to the thicker dentin layer in males (Alvesalo and Tammisalo, 1981; Harris and Hicks, 1998), while the increase in tooth crown size in 47,XYY males is due to both thicker dentin and thicker enamel (Alvesalo et al., 1985). All the deciduous and permanent tooth crowns, except for those of the third permanent molars, reach their final size and shape, on average, between the ages of 2 mos and 8 yrs. By comparison, in 45,X females that is, females with one X chromosome both deciduous and permanent tooth crowns are reduced in size (Filipsson et al., 1965; Kari et al., 1980; Alvesalo and Tammisalo, 1981; Townsend et al., 1984), mainly because of thin enamel, at least in the permanent teeth (Alvesalo and Tammisalo, 1981; Zilberman et al., 2000). Their permanent tooth roots are reduced in length (Midtbø and Halse, 1994), and premolars (Varrela, 1990; Midtbø and Halse, 1994) and lower first molars (Midtbø and Halse, 1994) tend to show increased numbers of root components in dissimilar variants. Taurodontism is an extension of the pulp chamber in which the furcation of the roots takes place later than in a normal molar. The prevalence of taurodontism increases with additional X chromosomes (Jaspers and Witkop, 1980), but it appears to occur in 45,X females and 47,XYY males as in a normal population (Alvesalo and Varrela, 1991). 771

2 772 Lähdesmäki & Alvesalo J Dent Res 83(10) 2004 The average difference between males and females in permanent tooth root lengths is about 6% in the mandibular canines, premolars, and molars (Garn et al., 1978). Tooth roots of incisors, canines, and premolars are more sexually stamped than the molars; the upper first molars in particular show practically no real sexual difference (Selmer-Olsen, 1949). There also seems to be a clear sexual difference in extreme root lengths, with extremely short roots to be found most often in girls and extremely long roots in boys (Jakobsson and Lind, 1973). The lower face, which is connected to the chewing apparatus, shows greater difference between sexes than other craniofacial dimensions. There seems to be some connection between root length and facial height, focused on upper first incisors and canines (Selmer-Olsen, 1949). Excluding third molars, permanent tooth roots complete their growth, on average, between the ages of 8 and 14 yrs. The growth of root dentin occurs after the completion of crown development. Here, we set out to investigate permanent tooth root lengths in 47,XYY males to gain additional information on the nature of the effect of the Y chromosome on dental growth. SUBJECTS & METHODS Population The patients, their relatives, and population controls comprised participants in Lassi Alvesalo's large Kvantti dental research project on individuals with sex-chromosome abnormalities. The subjects were from different parts of Finland, and all of their cytogenetic diagnoses had been made for medical reasons. The Institutional Review Board of the Medical Faculty, the University of Turku, Finland, reviewed and approved the protocol, of which the patients and their relatives were informed. Either the protection of human subjects was secured or they were not at risk. The subjects consisted of 15 47,XYY males (mean age, 18.6 yrs; SD, 7.38 yrs), and the relative controls were four fathers and five brothers of the 47,XYY males (mean age, 27.9 yrs; SD, yrs). Population controls were 22 males (mean age, 23.7 yrs; SD, yrs) and 26 females (mean age, 26.4 yrs; SD, yrs), who were relatives of patients other than those of 47,XYY males in the Kvantti project. Measurements Tooth root lengths in the maxilla and mandible were measured from dental panoramic radiographs, and crown heights were measured at the same time for further studies. One person had radiographs taken at the Institute of Dentistry, University of Turku, following a standardized procedure and with the same machine (Orthopantomograph 3, Palomex Corporation, Helsinki, Finland). The magnification ranged between 1.28 and 1.31 on the image layer of the panoramic radiograph. We used a magnifying lens (2x) to determine the outlines of the tooth from the radiograph on a light table, after which the outlines were marked in a special pencil for plaster (Schwan All Stabilo 8008, Schwanhäußer GmbH & Co. KG, Heroldsberg, Germany), and the measurements were made in the same manner with a sliding digital caliper (Mitutoyo, digimatic U, CD- 15B, Andover, England) to an accuracy of 0.01 mm. All drawings and measurements were made by one of the authors (RL). The measurements of root lengths were made on a perpendicular between two parallel lines, a line touching the outermost part of the root and a line joining the mesial and distal cervical margins of the enamel (EL). Root length refers to the longest root on the radiograph in the case of premolars and the longest mesial root in the case of molars. The aim was to measure all teeth, except third molars, with complete root formation on both sides of the jaws. Teeth that were partly outside the plane-in-focus in the panoramic radiograph or showed obvious distortion, because of location on the inner or outer surface of the image layer (Tammisalo, 1964), were excluded. Teeth with root resorption or incomplete root formation were also excluded, but teeth with large restorations or large caries lesions with pronounced loss of crown structure were measured when possible. The dilacerated, or crooked, roots were measured as a perpendicular length explained above. Some impacted canine teeth with closed apices were measured. Acellular cementum is formed on the root surface until the tooth reaches occlusion, at which time the proliferation of the epithelial root sheath is reduced and may become entrapped within the forming matrix of cellular cementum (Thomas, 1995). Cellular cementum formation continues after the root form is complete. In the present root length determinations, the apical cement layer was excluded. We examined the reliability of the measurements by performing double determinations on a total of 45 dental radiographs from the 'Kvantti' research material, representing adult 45,X females and their female and male relatives, with 15 persons in each group. The measurements were made by the same person (RL) at an interval of 2 wks, the marked line joining the mesial and distal cervical margins of the enamel on each tooth (EL) being rubbed out after the first measurement and determined again and re-drawn for the second measurement. The reproducibility of the double determinations of root length was expressed with the method error statistic (S) ( 1 = original measurement value, 2 = repeated-measurement value, n = number of patients). ( 1-2 ) 2 S = ( ) (Dahlberg, 1948) 2n The error values of root length measurement ranged from 0.35 mm to 0.75 mm, with corresponding percentages of 1.95 and 5.11, respectively. The values were considered acceptable for further measurements. Statistical Analysis The SPSS package 10.0 (Statistical Package for the Social Sciences, The Apache Software, Chicago, IL, USA) was used for the statistical analysis. The mean values for root length were calculated and compared among the 47,XYY males, male relatives, and population control males and females, with the t test for equality of means to indicate the significance of differences between/among the groups. Results were considered statistically significant when p was 0.05 or less. RESULTS The results showed that the means of the measurements of permanent tooth root lengths in the 47,XYY males were generally larger than those for the population control males, the only exception being the right lateral incisor in the maxilla (Table 1). The differences were significant in 4 out of 14 comparisons in the maxilla and 7 in the mandible. The actual relative metric differences in the mandible exceeded those in the maxilla, in most instances.

3 J Dent Res 83(10) 2004 Root Lengths in 47,XYY Males 773 Table 1. Mean Maxillary and Mandibular Permanent Tooth Root Lengths in 47,XYY Males, Population Control Males, and Females a 47,XYY Males Population Control Males Population Control Females Tooth Mean (mm) SD N p < b,c Mean (mm) SD N p < Mean (mm) SD N Maxillary Right second molar 16.4 (± 2.0) 9 * 14.8 (± 1.7) (± 1.9) 20 First molar 16.4 (± 2.5) (± 1.7) (± 1.7) 20 Second premolar 20.2 (± 3.0) 11 ** 16.7 (± 1.7) (± 1.2) 18 First premolar 18.6 (± 2.2) (± 2.0) (± 1.8) 18 Canine 24.6 (± 2.8) (± 2.3) 19 * 22.0 (± 2.2) 21 Lateral incisor 19.2 (± 1.9) (± 1.6) 19 * 18.3 (± 1.4) 20 Central incisor 20.7 (± 2.0) (± 1.9) 21 ** 18.8 (± 1.2) 21 Left central incisor 20.9 (± 1.9) (± 2.0) 21 ** 18.9 (± 0.9) 21 Lateral incisor 20.2 (± 1.8) (± 2.2) 21 * 18.4 (± 1.3) 19 Canine 25.4 (± 1.2) (± 1.8) 20 *** 22.0 (± 1.9) 20 First premolar 18.1 (± 3.7) (± 1.4) (± 1.7) 20 Second premolar 18.9 (± 2.7) 12 ** 16.3 (± 2.0) (± 1.7) 19 First molar 16.0 (± 2.0) 13 * 14.6 (± 1.3) (± 1.8) 19 Second molar 15.6 (± 1.3) (± 2.5) (± 1.6) 19 Mandibular Right second molar 19.5 (± 2.8) 9 ** 16.7 (± 1.6) (± 1.5) 18 First molar 20.2 (± 2.2) 11 * 18.5 (± 1.0) (± 1.2) 18 Second premolar 20.9 (± 1.9) (± 2.3) (± 1.7) 20 First premolar 19.8 (± 1.8) 13 * 18.3 (± 2.2) (± 1.9) 23 Canine 23.8 (± 2.5) 12 * 21.1 (± 2.9) (± 2.0) 24 Lateral incisor 18.8 (± 1.9) (± 2.5) 19 * 15.7 (± 1.7) 26 Central incisor 17.8 (± 1.8) 13 *** 15.0 (± 2.3) (± 1.8) 26 Left central incisor 16.8 (± 2.4) (± 2.1) (± 1.8) 25 Lateral incisor 18.9 (± 2.1) 14 * 17.2 (± 2.2) 22 * 16.0 (± 1.8) 25 Canine 24.0 (± 2.4) (± 1.9) 21 *** 19.8 (± 1.8) 22 First premolar 20.0 (± 1.5) (± 2.3) (± 1.3) 23 Second premolar 21.7 (± 2.7) 9 * 19.2 (± 2.4) (± 1.7) 20 First molar 20.3 (± 1.8) (± 2.1) (± 1.3) 17 Second molar 18.5 (± 1.9) (± 1.3) (± 1.3) 19 a The results indicate increased root lengths in 47,XYY males. b Statistical testing by two-tailed t test. 47,XYY males vs. control males, control males vs. control females. c Significances: = p < 0.1, * = p < 0.05, ** = p < 0.01, *** = p < Comparisons of mean tooth root lengths between nine 47,XYY males and their brothers or fathers showed that the measurements for the 47,XYY males were, with one exception, larger than those for the male relatives (Table 2). The differences were significant in half of the comparisons, and the values for the male relatives were closer to the male population control values than those for 47,XYY males. The root lengths of the population control males were, in most cases, larger than those of females. The excess root growth in the 47,XYY males compared with normal males was, in most cases, greater than the difference between normal males and females, except in upper incisors. The mean percentage difference of all root lengths between the sexes was 4%, and between 47,XYY males and normal males, 9%. The fact that the mean root lengths of antimeric teeth differed to some extent may also be due to sample sizes, the various numbers of measurements available, and technical reasons. Accordingly, the measurements of natural tooth roots also differed from the means of antimeric tooth roots (Selmer- Olsen, 1949). Visual inspection of root morphology on panoramic radiographs of 47,XYY males did not reveal any major deviations from normality. DISCUSSION The results showed that the roots of the teeth in 47,XYY males were markedly larger than those in control males or females, and males showed longer roots than females. Selmer-Olsen's (1949) findings on tooth root lengths measured from natural teeth showed the same trend of sexual dimorphism. In comparison with their tooth crown growth, e.g., root length difference of the right permanent upper central incisor was 3% between the 47,XYY males and normal males and 5% between the normal males and females. The difference in the mesiodistal dimension of the crown of the same tooth was 5% between 47,XYY males and normal males and 2% between the

4 774 Lähdesmäki & Alvesalo J Dent Res 83(10) 2004 Table 2. Mean Maxillary and Mandibular Permanent Tooth Root Lengths in 47,XYY Males and Their Fathers and Brothers a Tooth 47,XYY Males Male Relatives Mean (mm) SD N p < b,c Mean (mm) SD N Maxillary Right second molar 16.5 (± 1.6) (± 2.3) 8 First molar 15.5 (± 2.6) (± 1.2) 6 Second premolar 19.0 (± 3.0) 6 ** 16.2 (± 2.8) 8 First premolar 19.1 (± 2.1) (± 1.4) 6 Canine 25.1 (± 2.9) (± 0.9) 5 Lateral incisor 20.0 (± 1.3) (± 2.0) 5 Central incisor 20.9 (± 1.7) 9 * 19.3 (± 3.1) 7 Left central incisor 21.3 (± 1.7) (± 2.5) 7 Lateral incisor 20.5 (± 1.9) 8 *** 18.1 (± 1.4) 7 Canine 25.3 (± 1.3) 6 * 23.8 (± 1.8) 6 First premolar 17.1 (± 4.3) (± 2.2) 6 Second premolar 18.7 (± 2.8) (± 3.0) 7 First molar 15.3 (± 1.3) 9 * 13.7 (± 1.9) 6 Second molar 15.6 (± 1.2) (± 2.4) 7 Mandibular Right second molar 19.3 (± 3.3) (± 1.1) 4 First molar 19.8 (± 2.3) (± 2.1) 5 Second premolar 20.4 (± 1.7) (± 1.8) 8 First premolar 19.5 (± 1.7) (± 2.3) 9 Canine 23.9 (± 2.9) 6 * 21.9 (± 3.0) 9 Lateral incisor 19.0 (± 1.9) (± 2.9) 9 Central incisor 18.3 (± 1.8) 8 * 16.2 (± 2.1) 9 Left central incisor 17.3 (± 2.6) (± 2.0) 9 Lateral incisor 19.3 (± 2.1) 9 * 17.4 (± 2.1) 9 Canine 24.2 (± 2.9) (± 2.7) 8 First premolar 20.3 (± 1.3) (± 2.2) 8 Second premolar 20.8 (± 2.9) 6 * 18.9 (± 2.8) 7 First molar 20.0 (± 1.7) (± 2.1) 6 Second molar 18.8 (± 1.9) (± 1.7) 4 a The results indicate increased root lengths in 47,XYY males. b Statistical testing by two-tailed t test. 47,XYY males vs. male relatives. c Significances = p < 0.1, * = p < 0.05, ** = p < 0.01, *** = p < sexes (Alvesalo, 1971; Alvesalo et al., 1975). When all teeth are considered, the results suggest that the growth increase in 47,XYY males' tooth roots is at least of the same magnitude as that in tooth crowns. It is known that the dividing epithelial cells in the tooth root sheath determine the size, shape, and number of tooth roots. Root dentin is formed later than crown dentin and requires the proliferation of epithelial cells from the cervical loop of the dental organ around the growing dental papilla to initiate the differentiation of root odontoblasts. The formation of primary physiological dentin continues until the external root form is completed (Ten Cate, 1994). Morphological and phenotypic differences between crown and root odontoblasts may result from differences in the inductive mechanisms operating between the crown and the root (Thomas, 1995). It has been suggested that the expression of the difference between the sexes in various dental features results from the differential effects of the X and Y chromosomes on growth. The Y chromosome promotes both dentin and enamel growth, whereas the effect of the X chromosome on tooth crown growth seems to be restricted to enamel formation. The effect of the Y chromosome on dental development in particular explains the expression of sexual dimorphism in the size, shape, and number of the teeth e.g., supernumerary permanent teeth are approximately twice as common in normal males as in normal females, while permanent ordinary teeth are more frequently missing in females than in males (Alvesalo, 1985, 1997). If one assumes genetic pleiotropy, the differences between the sexes in the expression of the torus mandibularis, skeletal maturation, statural growth, and sex ratio (the ratio of the number of males to that of females) at birth and in the earlier stages of development are explained by these differential effects of the X and Y chromosomes on growth (Alvesalo, 1985, 1997). It is of great interest that molecular studies have shown that loci for human amelogenin, the main component of the organic matrix of enamel, are on both X and Y chromosomes (Lau et al., 1989; Salido et al., 1992). The amino acid sequences of X and Y chromosome genes seem to differ to some extent, however. The present results show that the permanent tooth roots are longer in 47,XYY males than in normal males or females. Earlier results have shown increased deciduous and permanent tooth crown growth in 47,XYY males. Present results indicate that the effect of the extra Y chromosome on the promotion of dental growth continues in the form of root dentin after the completion of crown growth. Together, these results indicate that growth excesses in 47,XYY males are evident and final, beginning a few months after birth and continuing up to the age of 14 yrs, at least. Excess root dentin growth and sexual dimorphism in the growth of crown and root dentin might be caused by the same factor on the Y chromosome. ACKNOWLEDGMENTS The Kvantti research project has been supported by the

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