Arch oralBiol. Vol. 35,No. 2,pp. 109-I12, 1990 Printed in Great Britain. All rights reserved
0003-9969/90 $3.00+ 0.00
Copyright 0 1990Pergamon Press plc
ROOT MORPHOLOGY OF MANDIBULAR PREMOLARS IN HUMAN 45,X FEMALES J. VARRELA Institute of Dentistry, University of Turku, Lemminkaisenkatu
2, SF-20520 Turku, Finland
(Accepted 30 August 1989) Summary-The
teeth of 87 Finnish 45,X females, 60 of their first-degree relatives and 87 normal females were examined. The presence of separate mesial and distal root canals and separate root apices was noted from orthopantomograms. Of the 45,X females, 40 (or 46%) had lower premolars with separate root canals; 30 individuals in first and 28 in second premolars. The number of first and second premolars with separate mesial and distal root canals was 40 and 43, and of those also showing separate apices, 28 and 21 respectively. Three of the female relatives and two of the normal females had premolars with separate mesial and distal root canals. The differences between the 45,X females and the two control samples were highly significant (p -C0.001; Fisher exact test). The findings indicate increased molarization of the premolars in 45,X females; this contrasts with the earlier observation of a tendency to reduced crown morphology. The present outcome supports the hypothesis that the X chromosome has gene(s) involved in the regulation of root morphology. Key words: root morphology, genetics, anthropology
INTRODUCTION The 45,X female has smaller teeth than the normal female (Filipson, Lindsten and Almquist, 1965; Kari, Alvesalo and Manninen, 1980; Townsend, Jensen and
Alvesalo, 1984); the (difference varies depending on the tooth type. In general, the effect is more pronounced in the permanent than in the deciduous dentition (Townsend et al., 1984). The observations of Alvesalo and Tammisalo (1981) indicate that the reduction in crown size in 45,X females is mainly due to thinner enamel. In addition, Kirveskari and Alvesalo (1982), who studied the expression of certain non-metric traits, have demonstrated a tendency towards simplified tooth crown morphology in 45,X females. The common oclcurrence of taurodont lower molars in individua’ls with extra X chromosomes indicates that the X chromosome is involved in the regulation of root development (Varrela and Alvesalo, 1988, 1989). These findings are compatible with the hypothesis that morphogenesis of the molar roots is influenced by gene(s) on the X chromosome (Varrela and Alvesalo, 1988). I have now studied the morphology of the roots of the mandibular premolars in a sample of 87 45,X females, with special reference to the occurrence of separate mesial and distal roots. My aim was to investigate further the role of the X chromosome in dental development. MATERIALS AND
METHODS
The group studied comprised 87 Finnish 45,X females, 60 of their first-degree female relatives, and a control sample of E;7normal females. No individuals with mosaicism were included in the sample of 45,X females. The individuals in the control popula-
tion sample were relatives of people with other sex-chromosome anomalies. The mean age of the 45,X females was 19.6 yr and that of their female relatives 28.4 yr. The mean age of the sample of normal females was 29.9 yr. The morphology of the root canals and the presence of separate apices in the roots were studied from orthopantomograms. Premolars were considered as two-rooted if separate mesial and distal root canals were at least partially visible (see Fig. 1). Rotated premolars showing division of buccal and lingual roots or separate root canals were classified as singlerooted. From the orthopantomograms, it was not always possible to determine whether the roots actually were divided (see Fig. 1). Therefore, only the presence of separate apices was recorded. For the same reason, no distinction was made between division of roots along a mesio-lingual groove and along a buccal groove. As shown by Goh (1957) both types may show separate root canals and total or partial division of the roots. Furthermore, the level where the root division occurred varied considerably: in some premolars it was near the cementum-enamel junction while in others a more apical location was noted. No attempt was made to study any variation in the site of the division. For statistical comparisons, the Fisher exact test was used. RESULTS Of the 87 45,X females, 40 (46%) had first or second premolars (or both) with separate root canals. Thirty individuals (34%) had two-rooted first premolars, 20 unilaterally and 10 bilaterally. A two-rooted second premolar was found in 28 individuals (32%); 13 cases were unilateral and 15 bilateral. Six 45,X females had all 4 lower premolars with separate root 109
J. VARRELA
110 Table
1. Mandibular first premolars in 45,X females, in their first-degree female relatives and in the sample of normal females 45.x females (N = 87) .-_____
First premolar Missing Single root canal Separate root canals
Female relatives (N = 60)
N
(X)
N
(%)
0 134 40*
(0) (77) (23)
1 116 3
(1) (97) (3)
Population females (N = 87) N
(%)
1
(1)
171 2
(98) (1)
*p < 0.001. Table
2. Mandibular
second
premolars
in 45.X females,
m their first-
degree female relatives and in the sample of normal females 45,x females (N = 87) Second
premolar
Missing Single root canal Separate root canals
Female relatives (N = 60)
Populatron females (N = 87)
N
(%)
N
(X)
N
(X)
5 126 43’
(3) (72) (25)
11 109 0
(9) (91) (0)
9 165 0
(5) (95) (0)
*p < 0.001
canals (7%). Of the 40 first premolars with separate root canals, in 28 the apices of the roots also seemed to be separated; in the second premolars, the respective numbers were 43 and 21. Tables 1 and 2 show the number and frequency of missing, single-rooted and two-rooted first premolars and second premolars, respectively. Three of the female relatives (5%) and two of the population females (2%) had premolars with separate root canals. In the two control samples, all affected teeth were first premolars and all cases were unilateral. Only one premolar with separate root canals and separate apices was found (in a population control female). With regard to the occurrence of two-rooted first and second premolars, the differences between 45,X females and their female relatives, and between 45,X females and population control females, were statistically highly significant (p < 0.001, the Fisher exact test). No statistical difference was found between the sample of female relatives and the sample of population control females. DISCUSSION
As shown by Pedersen (1949) the frequency of multirooted premolars varies considerably in different populations. The occurrence of two-rooted first premolars in my two control samples is consistent with the findings of Hjelmman (1928). He found that division of roots occurs in 4.7% of the lower first premolars of Finns, but in none of the lower second premolars. This is in sharp contrast with my finding that almost half of the 45,X females had one or more lower premolars with separate root canals and that
Plate
the majority of these premolars showed at least partial division of the roots. The occurrence of multirooted mandibular premolars in Turner’s syndrome was mentioned by Dixon and Stewart (1976) but the source of their information was not given. A high frequency of both taurodont molars and multirooted lower premolars has been reported in the Bantu (Shaw, 1928. 1931). This may suggest a common causative factor for these traits. The mechanism by which the location of the furcation is determined is related to the growth of the transverse processes of the Hertwig’s root sheath (Orban and Mueller, 1929) and is common for both traits. However, the growth of the transverse processes seems to be delayed in taurodont molars, whereas development of extra processes must take place in multirooted premolars. This indicates a difference in the regulation of the growth of the root sheath. In individuals with extra X chromosomes, taurodont molars are found frequently (Varrela and Alvesalo, 1988, 1989) but there are no reports on the root morphology of their premolars. Nevertheless, my findings suggest that quantitative variation in the X chromosome is associated with changes in root morphology, not only in molars but also in premolars. Jaspers (1981) demonstrated a high frequency of taurodontism in Down’s syndrome and suggested that the low mitotic activity of the cells with trisomy 21 could disturb root development and promote the formation of taurodont molars. It is therefore of interest that 45,X cells also seem to have a longer cycle and grow more slowly than normal cells (Cure, BouC and Boue, 1974; Simpson and Lebeau, 1981; Varrela et al., 1989). My findings indicate that a
1
Fig. 1. Radiograph of first and second mandibular premolars in a 45,X female (patient S.A.). Both show separate mesial and distal root canals, but only in the second premolar is the division of roots clearly visible.
Mandibular premolars in 45,X females
111
112
J. VARRELA
prolonged cell cycle does not necessarily interfere with the development of the transverse processes of the Hertwig’s root sheath. A possible differentiating factor might be the rate of dental development, which in Down’s syndrome is delayed and in 45,X females advanced (Filinson et al.. 1965: Barden. 1983).
The develodment of additional roots indicates a tendency to molarization of the lower premolars of 45,X females and suggests a change in the morphodifferentiation of these teeth. This, together with the earlier findings (Kirveskari and Alvesalo, 1982; Varrela and Alvesalo, 1988, 1989), seems to suggest that tooth morphology in general is under the regulative influence of sex chromosome gene(s). However, as suggested by Kirveskari and Alvesalo (1982), part of the morphological reduction may be due to a size factor. It therefore seems possible that the X chromosome may exert independent and partly counteracting effects on size on the one hand, and on morphology on the other. Acknowledgements-1 thank Professor Lassi Alvesalo permission to use his material. This study was supported the Academy of Finland.
for by
REFERENCES Alvesalo L. and Tammisalo E. (1981) Enamel thickness in 45,X females’ permanent teeth. Am. J. hum. Genet. 33, 464469. Barden H. S. (1983) Growth and develonment of selected hard tissues in Down syndrome: a review. Hum. Biol. 55, 539-576. Cure S., Bout and Bout: A. (1974) Growth characteristics of human embryonic cell lines with chromosomal anomalies. Biomedicine 21, 2333236. Dixon G. H. and Steward R. E. (1976) Oral Facial Genetics (Edited by Stewart R. E. and Prescott G. H.) Chap. 6, p. 133. Mosby, St Louis, MO. Fihpson R., Lindsten J. and Almquist S. (1965) Time of eruption of the permanent teeth, cephalometric and tooth measurements and sulphation factor activity in 45
with Turner’s syndrome with different types of aberration. Acra endocr. 48, 91-I 13. Goh S. W. (1957) Variations m the morphology of mandibular premolar roots. Br. denf. J. 102, 31 I-314. Hjelmman G. (1928) Morphologishe Beobachtungen an den Zahnen der Finnen. Acta sot. med. “Duodecim” 11, * *1-s patients
X-chromosome
Jaspers M. T. (198 1) Taurodontism in the Down syndrome. Oral Stag. 51, 632636. Kari M., Alvesalo L. and Manninen K. (1980) Sizes of deciduous teeth in 45,X females. J. dent. Res. 59, 1382-1385. Kirveskari P. and Alvesalo L. (1982) Dental morphology in Turner’s syndrome (45,X females). In. Teeth: Form, Function, and Evolution (Edited by Kurten B.) pp. 2988303. Columbia University Press, New York. Pedersen P. 0. (1949) The Easl Greenland Eskimo Denwon. Numerical Variations and Anatomy. Bianco Lunos Bogtrykkeri, Copenhagen. Orban B. and Mueller E. (1929) The development of the bifurcation of multirooted teeth. J. Am. dent. Ass. 16, 297-319. Shaw J. C. M. (1928) Taurodont teeth in South African races. J. Anat. 62, 476498. Shaw J. C. M. (1931) The Teeth, the Bony Palate and the Mandible m Banm Races of South Africa. Bale, Sons, Danielsson, London. Simpson J. L. and Lebeau M. M. (1981) Gonadal and statural determinants on the X chromosome and their relationship to in vitro studies showing prolonged cell cycles in 45,X; 46,X,del(X)(pll); 46,X,del(X)(q13); and 46,X,del(X)(q22) libroblasts. Am. J. Obstet. Gynec. 141, 93&940. Townsend G., Jensen B. L. and Alvesalo L. (1984) Reduced tooth size in 45.X (Turner svndrome) females. Am. J phys. Anthrop. 65, 3677371. . ’ Varrela J. and Alvesalo L. (1988) Taurodontism in 47,XXY males: an effect of the extra X chromosome on root development. J. denf. Res. 67, 5OlL502. Varrela J. and Alvesalo L. (1989) Taurodontism m females with extra X chromosomes. J. craniofac. Genet. devl. B~ol. In press. Varrela J., LarJava H., Jlrvelainen H., Penttinen R., Eerola E. and Alvesalo L. (1989) Effect of sex chromosome aneuploidy on growth of human skin fibroblasts in cell culture. Ann. hum. Biol. 16, 9-13.
0003-9969/90 $3.00+ 0.00
Copyright 0 1990Pergamon Press plc
ROOT MORPHOLOGY OF MANDIBULAR PREMOLARS IN HUMAN 45,X FEMALES J. VARRELA Institute of Dentistry, University of Turku, Lemminkaisenkatu
2, SF-20520 Turku, Finland
(Accepted 30 August 1989) Summary-The
teeth of 87 Finnish 45,X females, 60 of their first-degree relatives and 87 normal females were examined. The presence of separate mesial and distal root canals and separate root apices was noted from orthopantomograms. Of the 45,X females, 40 (or 46%) had lower premolars with separate root canals; 30 individuals in first and 28 in second premolars. The number of first and second premolars with separate mesial and distal root canals was 40 and 43, and of those also showing separate apices, 28 and 21 respectively. Three of the female relatives and two of the normal females had premolars with separate mesial and distal root canals. The differences between the 45,X females and the two control samples were highly significant (p -C0.001; Fisher exact test). The findings indicate increased molarization of the premolars in 45,X females; this contrasts with the earlier observation of a tendency to reduced crown morphology. The present outcome supports the hypothesis that the X chromosome has gene(s) involved in the regulation of root morphology. Key words: root morphology, genetics, anthropology
INTRODUCTION The 45,X female has smaller teeth than the normal female (Filipson, Lindsten and Almquist, 1965; Kari, Alvesalo and Manninen, 1980; Townsend, Jensen and
Alvesalo, 1984); the (difference varies depending on the tooth type. In general, the effect is more pronounced in the permanent than in the deciduous dentition (Townsend et al., 1984). The observations of Alvesalo and Tammisalo (1981) indicate that the reduction in crown size in 45,X females is mainly due to thinner enamel. In addition, Kirveskari and Alvesalo (1982), who studied the expression of certain non-metric traits, have demonstrated a tendency towards simplified tooth crown morphology in 45,X females. The common oclcurrence of taurodont lower molars in individua’ls with extra X chromosomes indicates that the X chromosome is involved in the regulation of root development (Varrela and Alvesalo, 1988, 1989). These findings are compatible with the hypothesis that morphogenesis of the molar roots is influenced by gene(s) on the X chromosome (Varrela and Alvesalo, 1988). I have now studied the morphology of the roots of the mandibular premolars in a sample of 87 45,X females, with special reference to the occurrence of separate mesial and distal roots. My aim was to investigate further the role of the X chromosome in dental development. MATERIALS AND
METHODS
The group studied comprised 87 Finnish 45,X females, 60 of their first-degree female relatives, and a control sample of E;7normal females. No individuals with mosaicism were included in the sample of 45,X females. The individuals in the control popula-
tion sample were relatives of people with other sex-chromosome anomalies. The mean age of the 45,X females was 19.6 yr and that of their female relatives 28.4 yr. The mean age of the sample of normal females was 29.9 yr. The morphology of the root canals and the presence of separate apices in the roots were studied from orthopantomograms. Premolars were considered as two-rooted if separate mesial and distal root canals were at least partially visible (see Fig. 1). Rotated premolars showing division of buccal and lingual roots or separate root canals were classified as singlerooted. From the orthopantomograms, it was not always possible to determine whether the roots actually were divided (see Fig. 1). Therefore, only the presence of separate apices was recorded. For the same reason, no distinction was made between division of roots along a mesio-lingual groove and along a buccal groove. As shown by Goh (1957) both types may show separate root canals and total or partial division of the roots. Furthermore, the level where the root division occurred varied considerably: in some premolars it was near the cementum-enamel junction while in others a more apical location was noted. No attempt was made to study any variation in the site of the division. For statistical comparisons, the Fisher exact test was used. RESULTS Of the 87 45,X females, 40 (46%) had first or second premolars (or both) with separate root canals. Thirty individuals (34%) had two-rooted first premolars, 20 unilaterally and 10 bilaterally. A two-rooted second premolar was found in 28 individuals (32%); 13 cases were unilateral and 15 bilateral. Six 45,X females had all 4 lower premolars with separate root 109
J. VARRELA
110 Table
1. Mandibular first premolars in 45,X females, in their first-degree female relatives and in the sample of normal females 45.x females (N = 87) .-_____
First premolar Missing Single root canal Separate root canals
Female relatives (N = 60)
N
(X)
N
(%)
0 134 40*
(0) (77) (23)
1 116 3
(1) (97) (3)
Population females (N = 87) N
(%)
1
(1)
171 2
(98) (1)
*p < 0.001. Table
2. Mandibular
second
premolars
in 45.X females,
m their first-
degree female relatives and in the sample of normal females 45,x females (N = 87) Second
premolar
Missing Single root canal Separate root canals
Female relatives (N = 60)
Populatron females (N = 87)
N
(%)
N
(X)
N
(X)
5 126 43’
(3) (72) (25)
11 109 0
(9) (91) (0)
9 165 0
(5) (95) (0)
*p < 0.001
canals (7%). Of the 40 first premolars with separate root canals, in 28 the apices of the roots also seemed to be separated; in the second premolars, the respective numbers were 43 and 21. Tables 1 and 2 show the number and frequency of missing, single-rooted and two-rooted first premolars and second premolars, respectively. Three of the female relatives (5%) and two of the population females (2%) had premolars with separate root canals. In the two control samples, all affected teeth were first premolars and all cases were unilateral. Only one premolar with separate root canals and separate apices was found (in a population control female). With regard to the occurrence of two-rooted first and second premolars, the differences between 45,X females and their female relatives, and between 45,X females and population control females, were statistically highly significant (p < 0.001, the Fisher exact test). No statistical difference was found between the sample of female relatives and the sample of population control females. DISCUSSION
As shown by Pedersen (1949) the frequency of multirooted premolars varies considerably in different populations. The occurrence of two-rooted first premolars in my two control samples is consistent with the findings of Hjelmman (1928). He found that division of roots occurs in 4.7% of the lower first premolars of Finns, but in none of the lower second premolars. This is in sharp contrast with my finding that almost half of the 45,X females had one or more lower premolars with separate root canals and that
Plate
the majority of these premolars showed at least partial division of the roots. The occurrence of multirooted mandibular premolars in Turner’s syndrome was mentioned by Dixon and Stewart (1976) but the source of their information was not given. A high frequency of both taurodont molars and multirooted lower premolars has been reported in the Bantu (Shaw, 1928. 1931). This may suggest a common causative factor for these traits. The mechanism by which the location of the furcation is determined is related to the growth of the transverse processes of the Hertwig’s root sheath (Orban and Mueller, 1929) and is common for both traits. However, the growth of the transverse processes seems to be delayed in taurodont molars, whereas development of extra processes must take place in multirooted premolars. This indicates a difference in the regulation of the growth of the root sheath. In individuals with extra X chromosomes, taurodont molars are found frequently (Varrela and Alvesalo, 1988, 1989) but there are no reports on the root morphology of their premolars. Nevertheless, my findings suggest that quantitative variation in the X chromosome is associated with changes in root morphology, not only in molars but also in premolars. Jaspers (1981) demonstrated a high frequency of taurodontism in Down’s syndrome and suggested that the low mitotic activity of the cells with trisomy 21 could disturb root development and promote the formation of taurodont molars. It is therefore of interest that 45,X cells also seem to have a longer cycle and grow more slowly than normal cells (Cure, BouC and Boue, 1974; Simpson and Lebeau, 1981; Varrela et al., 1989). My findings indicate that a
1
Fig. 1. Radiograph of first and second mandibular premolars in a 45,X female (patient S.A.). Both show separate mesial and distal root canals, but only in the second premolar is the division of roots clearly visible.
Mandibular premolars in 45,X females
111
112
J. VARRELA
prolonged cell cycle does not necessarily interfere with the development of the transverse processes of the Hertwig’s root sheath. A possible differentiating factor might be the rate of dental development, which in Down’s syndrome is delayed and in 45,X females advanced (Filinson et al.. 1965: Barden. 1983).
The develodment of additional roots indicates a tendency to molarization of the lower premolars of 45,X females and suggests a change in the morphodifferentiation of these teeth. This, together with the earlier findings (Kirveskari and Alvesalo, 1982; Varrela and Alvesalo, 1988, 1989), seems to suggest that tooth morphology in general is under the regulative influence of sex chromosome gene(s). However, as suggested by Kirveskari and Alvesalo (1982), part of the morphological reduction may be due to a size factor. It therefore seems possible that the X chromosome may exert independent and partly counteracting effects on size on the one hand, and on morphology on the other. Acknowledgements-1 thank Professor Lassi Alvesalo permission to use his material. This study was supported the Academy of Finland.
for by
REFERENCES Alvesalo L. and Tammisalo E. (1981) Enamel thickness in 45,X females’ permanent teeth. Am. J. hum. Genet. 33, 464469. Barden H. S. (1983) Growth and develonment of selected hard tissues in Down syndrome: a review. Hum. Biol. 55, 539-576. Cure S., Bout and Bout: A. (1974) Growth characteristics of human embryonic cell lines with chromosomal anomalies. Biomedicine 21, 2333236. Dixon G. H. and Steward R. E. (1976) Oral Facial Genetics (Edited by Stewart R. E. and Prescott G. H.) Chap. 6, p. 133. Mosby, St Louis, MO. Fihpson R., Lindsten J. and Almquist S. (1965) Time of eruption of the permanent teeth, cephalometric and tooth measurements and sulphation factor activity in 45
with Turner’s syndrome with different types of aberration. Acra endocr. 48, 91-I 13. Goh S. W. (1957) Variations m the morphology of mandibular premolar roots. Br. denf. J. 102, 31 I-314. Hjelmman G. (1928) Morphologishe Beobachtungen an den Zahnen der Finnen. Acta sot. med. “Duodecim” 11, * *1-s patients
X-chromosome
Jaspers M. T. (198 1) Taurodontism in the Down syndrome. Oral Stag. 51, 632636. Kari M., Alvesalo L. and Manninen K. (1980) Sizes of deciduous teeth in 45,X females. J. dent. Res. 59, 1382-1385. Kirveskari P. and Alvesalo L. (1982) Dental morphology in Turner’s syndrome (45,X females). In. Teeth: Form, Function, and Evolution (Edited by Kurten B.) pp. 2988303. Columbia University Press, New York. Pedersen P. 0. (1949) The Easl Greenland Eskimo Denwon. Numerical Variations and Anatomy. Bianco Lunos Bogtrykkeri, Copenhagen. Orban B. and Mueller E. (1929) The development of the bifurcation of multirooted teeth. J. Am. dent. Ass. 16, 297-319. Shaw J. C. M. (1928) Taurodont teeth in South African races. J. Anat. 62, 476498. Shaw J. C. M. (1931) The Teeth, the Bony Palate and the Mandible m Banm Races of South Africa. Bale, Sons, Danielsson, London. Simpson J. L. and Lebeau M. M. (1981) Gonadal and statural determinants on the X chromosome and their relationship to in vitro studies showing prolonged cell cycles in 45,X; 46,X,del(X)(pll); 46,X,del(X)(q13); and 46,X,del(X)(q22) libroblasts. Am. J. Obstet. Gynec. 141, 93&940. Townsend G., Jensen B. L. and Alvesalo L. (1984) Reduced tooth size in 45.X (Turner svndrome) females. Am. J phys. Anthrop. 65, 3677371. . ’ Varrela J. and Alvesalo L. (1988) Taurodontism in 47,XXY males: an effect of the extra X chromosome on root development. J. denf. Res. 67, 5OlL502. Varrela J. and Alvesalo L. (1989) Taurodontism m females with extra X chromosomes. J. craniofac. Genet. devl. B~ol. In press. Varrela J., LarJava H., Jlrvelainen H., Penttinen R., Eerola E. and Alvesalo L. (1989) Effect of sex chromosome aneuploidy on growth of human skin fibroblasts in cell culture. Ann. hum. Biol. 16, 9-13.
