Root lengths in the permanent teeth of Klinefelter (47,XXY)men
Raija Lahdesmaki *, Lassi Alvesalo
Department of Oral Development and Orthodontics, Institute of Dentistry, University of Oulu and University Hospital of Oulu, Finland
a r c h i v e s o f o r a l b i o l o g y 5 2 ( 2 0 0 7 ) 8 2 2 – 8 2 7
a r t i c l e i n f o
Article history:
Accepted 5 February 2007
Keywords:
Klinefelter man
X chromosome
Y chromosome
Humans
Aneuploidy
Tooth root
Growth and development
a b s t r a c t
Earlier studies on human teeth have provided proof of an expression of the X and Y
chromosome genes in tooth crown growth. The Y chromosome promotes the growth of
permanent tooth crown enamel and dentin, whereas the effect of the X chromosome seems
to be restricted mainly on enamel formation. Also, there are evidences that both of the sex
chromosomes are expressed in tooth root growth. The permanent tooth crowns in 47,XXY
males or individuals with an extra X or Y chromosome show increased size compared to
normal men, which is mainly due to increased enamel thickness, the dentin thickness is
somewhat reduced. There is some evidence of increased mesio-distal tooth crown size also
in their primary dentition. The aim of the present study was to determine their complete
permanent tooth root lengths. The study groups consisted of 49 47,XXY males, 22 relative
males, 8 relative females, 35 population control males and 46 population control females
from the Kvantti research project. Root length measurements were made from panoramic
radiographs on both sides of the jaw using a digital sliding calliper. The results showed
growth increase in the final tooth root sizes in 47,XXY males which conceivably become
evident beginning 8 years after birth up to the age of 14 years, at least. The present results
and earlier ones on 45,X and 45,X/46,XX females, normal females and males indicate that
the promoting effect of the Y chromosome on tooth root growth is greater than that of the X
chromosome. These differential effects are conceivably causative factors in the develop-
ment of the sexual dimorphism in tooth root size.
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1. Introduction
Men with Klinefelter syndrome have two X chromosomes in
addition to one Y chromosome (47,XXY), or in rare cases three
or four X chromosomes. This is in fact the most common sex
chromosome abnormality, with an incidence of 1 in 576
newborn boys,1 and 1 in 769 has also been suggested.2 The
incidence of 47,XXY boys increases with maternal age finding
an explanation in maternal meiosis. Prenatal testosterone
level of 47,XXY boys does not differ significantly from normal
men. Later the production of testosterone is insufficient and
needs to be substituted already from the age of 11 until 50
* Corresponding author. Tel.: +358 8 3153934; fax: +358 8 5375560.E-mail address: [email protected] (R. Lahdesmaki).
0003–9969/$ – see front matter # 2007 Elsevier Ltd. All rights reservedoi:10.1016/j.archoralbio.2007.02.002
years of age. The head circumference, body weight and length
have been found to be relatively reduced among 47,XXY boys
at birth.3 They show somewhat greater height growth
acceleration than normal boys between 5 and 8 years of age
owing to relatively greater leg growth. The magnitude and
timing of the pubertal growth spurt is like in normal boys.
47,XXY men grow taller than normal men, with a mean adult
height of 186 and 180 cm correspondingly, but remain 8–10 cm
shorter than 47,XYY men or males with an extra Y chromo-
some.2 In a Finnish study the final height in 47,XXY men was
182 cm.4 The somewhat greater growth acceleration in adult
height is due to relatively increased leg length and the
d.
a r c h i v e s o f o r a l b i o l o g y 5 2 ( 2 0 0 7 ) 8 2 2 – 8 2 7 823
feminine trunk proportions in 47,XXY males are caused by a
decrease in shoulder width, possibly affected by the double
dose of X chromosomes. Their adult head circumference is
under normal men, but above normal women,4 also, their
facial dimensions are smaller than those in normal men.4,5
Interestingly enough, 47,XXX females or females with an extra
X chromosome also show reduced head and skull size,6 and
they are tall because of relatively increased leg length.
The total permanent tooth crown size increase in 47,XXY
males is caused by thicker enamel layer relative to normal
men or women, the dentin thickness is less than in men, but
above that of women.7 Larger tooth crown size in normal men
relative to women is due to the thicker dentin layer in men,8–10
and men also show longer roots than women.11,12 A case
report of increased mesio-distal tooth crown size in the
primary dentition13 of a 47,XXY male is parallel with the
results of the permanent dentition.7 After the crown growth is
completed the epithelial cells in the tooth root sheath
determine the size, shape and number of the roots.14 Root
dentin is formed later than crown dentin and requires a
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.14 Excluding third molars, in terms of population
developmental standards, permanent tooth roots complete
their growth on average between the ages of 8 and 14 years.
In the present study, complete permanent tooth root
lengths in Klinefelter men (47,XXY males) or individuals with
extra X or Y chromosome are determined to gain additional
information about their dental growth and the role of the X
and Y chromosomes in this process. It has been suggested
earlier that the genes on the X and Y chromosome that affect
tooth crown growth are also expressed in the following root
growth.15
Fig. 1 – Root lengths were measured by reference to lines
marked on the tomographic radiographs (a) as described
in the text and shown in the picture (b).
2. Subjects and methods
2.1. Subjects
The patients, their relatives and population controls were all
participants in Alvesalo’s Kvantti dental research project on
individuals with sex chromosome abnormalities. The subjects
were from different parts of Finland and consisted of 49
47,XXY males (mean age 30.7 years, S.D. 11.71, minimum
10.16, maximum 57.61), 22 relative men (16 fathers and 6
brothers) (mean age 41.0 years, S.D. 15.53, minimum 13.52,
maximum 67.50), 8 relative women (mothers) (mean age 39.7
years, S.D. 5.64, minimum 31.17, maximum 50.55), 35 popula-
tion control men (mean age 25.5 years, S.D. 12.41, minimum
11.60, maximum 45.64) and 46 population control women
(mean age 27.6 years, S.D. 10.66, minimum 9.74, maximum
55.63), who were relatives of patients other than 47,XXY men
in the Kvantti research project. The diagnoses of the patients
were based on clinical and karyotypic evidence. All their
cytogenetic diagnosis had been carried out for medical
reasons. For comparisons the relatives were chosen on a
paired basis, one relative of the same phenotypic sex for each
patient and comparisons were also extended to opposite sex if
possible. The other criteria were age, generation and the
number of the teeth available. The Institutional Review Board
of the Medical Faculty, University of Turku, Finland, had
reviewed and approved the protocol, of which the patients and
their relatives were informed. All examinations were carried
out with the individuals’ consent, and the subjects were not at
risk in any way.
2.2. Measurements
Permanent tooth root lengths in maxilla and mandible were
measured from dental panoramic radiographs and crown
heights were measured at the same time for further study. All
the radiographs had been taken by the same person at the
Institute of Dentistry, University of Turku, following a
standardized procedure and with the same machine, an
Orthopantomograph 3, Palomex Corporation, Helsinki, Fin-
land. The magnification was in the range 1.28–1.31 throughout
the image layer of the panoramic radiograph. A magnifying
lens (2�) was used to determine the outlines of the tooth from
the radiograph on a light table, after which the outlines were
marked with a special pencil for plaster (Schwan All Stabilo
8008, Schwanhauber GmbH & CO, KG Heroldsberg, Germany)
and the measurements made in the same manner with a
sliding digital calliper (Mitutoyo, digimatic 500-123U, CD-15B,
Andover, England) to an accuracy of 0.01 mm. The outlines of
the roots were hard to determine in places and the drawings
had to be made straight on the radiograph. All the drawings
and measurements were made by one of the authors (RL)
(Fig. 1a). The measurements of root lengths were made
perpendicular to two parallel lines, one touching the outer-
most part of the root and the other joining the mesial and
distal cervical margins of the enamel (Fig. 1b). 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 the teeth with complete root
formation on both sides of the jaws except for the third
molars. Teeth that were partly outside the plane-in-focus in
a r c h i v e s o f o r a l b i o l o g y 5 2 ( 2 0 0 7 ) 8 2 2 – 8 2 7824
the panoramic radiograph or showed obvious distortion
because of being on the inner or outer surface of the image
layer16 were excluded. Teeth with root resorption or incom-
plete root formation were also excluded, but teeth with large
restorations or large caries lesions with pronounced loss of
crown structure were measured whenever possible. Dilacer-
ated or crooked roots were measured in terms of perpendi-
cular length as explained above. Some impacted canine teeth
with a closed apex were measured. Acellular cementum is
formed on the root surface until the tooth reaches the
occlusion, at which time the proliferation of the epithelial
root sheath is reduced and it may become entrapped within
the forming matrix of cellular cementum.17 Cellular cemen-
tum formation continues after the root form is complete. The
line between apical cementum and dentin was evaluated
while marking the outlines of the roots and the apical
cementum layer was excluded from the present root length
determinations.
Permanent tooth root lengths may be affected by several
external factors, which could bias the results. Orthodontic
treatment, especially with fixed appliances, may cause root
resorption, as also can traumatic occlusion, bruxism, nail-
biting, trauma, apical infection or root treatment, for instance.
According to anamnestic information, the patients or their
relatives had not had any orthodontic treatment, at least with
fixed appliances, before the examination procedures. Simi-
larly, anamnestic information on the population controls
suggested that they had not undergone orthodontic therapy.
This is supported by the fact that at the time in question there
were only very few dental offices in Finland where fixed
appliance orthodontics, or orthodontics in general, were
carried out. Regarding the possible effects of other external
factors, an assumption was made of an even distribution
between the groups.
The reliability of the measurements was examined by
performing double determinations on a total of 45 dental
radiographs from the Kvantti research material representing
adult 45,X females and their relative men and women, with 15
persons in each group. The measurements were made by the
same person (RL) at an interval of 2 weeks, the line joining the
mesial and distal cervical margins of the enamel marked on
each tooth being rubbed out after the first measurement and
determined again and re-drawn for the second. The reprodu-
cibility of the double determinations of root length was
expressed with the method error statistic (S) (x1 = original
measurement value, x2 = repeated measurement value,
n = number of patients) S ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiPðx1 � x2Þ2=2n
q.18
The absolute error values for the root length measure-
ments ranged from 0.35 to 0.75 mm, the corresponding
percentages being 1.95 and 5.11. The largest differences in
the double determinations of root lengths were in the upper
second premolars and molars and mandibular incisors and
canines. The values were considered acceptable for further
measurements.
2.3. Statistical analysis
The Statistical Package for the Social Sciences 10.0 (SPSS, CA,
USA) was used for the statistical analysis. Mean values for root
length were calculated and compared between the 47,XXY
males, relative men (47,XXY male versus father or brother),
population control men and women using the t-test for
equality of means to indicate the significance of differences
between the groups. Results were considered statistically
significant when p was 0.05 or less.
3. Results
The results show that mean permanent tooth root lengths in
47,XXY males are generally longer than those in normal
control men (Table 1). In the mandible, the differences are
significant in 12 out of 14 comparisons and in the maxilla in
premolars and molars. The root lengths of lower and upper
canines in 47,XXY males are close to the corresponding values
of control men. Relative to control women, the 47,XXY males
have significantly longer roots except in maxillary canines
(Table 1), and control men also show longer roots than control
women. Comparison with their relative men the 47,XXY males
show numerically larger values in root length in 22 measure-
ments out of 28 (Table 2), and the roots of relative men are
generally longer than those of relative women. It is notable
that the differences of root lengths between 47,XXY males and
control women are larger with one exception than those
between 47,XXY males and control men. Visual inspection of
the root morphology on the radiographs of 47,XXY males did
not reveal any major deviations from normality. However,
minor deviation in the form of taurodontic teeth was present
in mild expression in 30% of the cases. Taurodontism is an
extension of the pulp chamber in which the furcation of the
roots takes place more apically in multirooted teeth. The fact
that the mean root lengths of antimeric teeth differed to some
extent may be due to the sample sizes, the varying numbers of
measurements available and general technical reasons.
Certainly, the measurements of natural tooth roots also show
differences between the mean lengths for antimeric teeth.11
4. Discussion
Studies on families19,20 and individuals with sex chromosome
abnormalities,8,21–23 and molecular research,24–26 have pro-
vided proof of an expression of the X and Y chromosome genes
in tooth crown growth. The Y chromosome promotes growth
of permanent tooth crown enamel and dentin, whereas the
effect of the X chromosome in tooth crown growth seems to be
restricted mainly on enamel formation.22,23 Enamel growth is
decisively influenced by cell secretory function and that of
dentin by cell proliferations.27 The promoting effect of the Y
chromosome genes on tooth crown development, particularly
on dentin, can explain the expression of somatic sexual
dimorphism in the crown size, shape, maturation and in the
number of the teeth, e.g. supernumerary permanent teeth are
approximately twice as common in normal men than in
women, and ordinary teeth are more frequently missing in
women than in men.20,22,23 Also, assuming genetic pleiotropy,
sexual dimorphism in root size,12 in the expression of torus
mandibularis, the timing of skeletal maturation, statural
growth and sex ratio (the ratio of the number of boys to that
Table 1 – Mean maxillary and mandibular permanent tooth root lengths in 47,XXY males, population control men andwomen
Tooth 47,XXY males Population control men Population control women
Mean (mm) S.D. N Mean (mm) S.D. N pa Mean (mm) S.D. N pb
Maxillary
Right central incisor 21.0 2.4 33 20.1 2.2 31 ns 18.8 1.5 39 ***
Lateral incisor 19.8 1.9 28 19.3 2.0 26 ns 18.1 1.6 36 ***
Canine 23.3 2.9 30 23.8 2.2 27 ns 21.5 2.2 39 *
First premolar 19.9 2.2 29 18.1 1.8 22 ** 17.3 1.9 33 ***
Second premolar 19.5 2.6 18 16.8 1.9 29 *** 17.1 1.4 32 ***
First molar 17.4 1.8 23 14.8 1.6 26 *** 14.5 1.8 32 ***
Second molar 17.1 2.2 24 15.0 1.8 29 *** 14.3 1.9 37 ***
Maxillary
Left central incisor 21.1 2.4 32 20.1 2.1 31 $ 19.0 1.2 39 ***
Lateral incisor 20.0 2.0 28 19.2 2.1 31 ns 18.2 1.7 36 ***
Canine 23.4 2.7 25 24.1 1.7 29 ns 21.7 1.9 38 *
First premolar 19.9 1.9 24 17.8 1.9 23 *** 17.0 1.8 36 ***
Second premolar 19.7 2.4 24 16.9 2.3 27 *** 17.0 1.7 34 ***
First molar 16.8 1.7 21 14.4 1.8 25 *** 14.3 1.7 34 ***
Second molar 17.4 2.4 27 14.5 2.3 26 *** 14.1 1.8 33 ***
Mandibular
Right central incisor 17.6 1.8 41 15.3 2.3 34 *** 14.7 1.9 46 ***
Lateral incisor 18.6 1.9 41 17.2 2.4 32 ** 15.9 1.8 45 ***
Canine 22.6 2.2 39 21.3 2.8 32 * 19.9 2.3 42 ***
First premolar 19.9 2.0 39 18.5 2.1 34 ** 17.6 1.9 40 ***
Second premolar 20.7 2.3 22 18.9 2.4 29 ** 18.5 1.7 36 ***
First molar 19.7 1.7 24 18.7 1.3 26 * 17.9 1.4 30 ***
Second molar 18.5 2.0 22 16.9 1.4 20 ** 17.3 1.6 31 **
Mandibular
Left central incisor 17.9 1.9 41 15.7 2.1 35 *** 14.7 1.9 43 ***
Lateral incisor 18.7 2.0 43 17.2 2.0 35 ** 16.1 1.9 44 ***
Canine 22.5 2.7 42 22.5 2.2 33 ns 19.7 2.1 40 ***
First premolar 19.4 1.9 37 19.0 2.2 34 ns 17.9 1.9 40 ***
Second premolar 21.1 2.1 20 19.2 2.4 28 ** 18.9 1.8 38 ***
First molar 20.3 1.6 19 18.8 2.1 25 * 18.0 1.4 29 ***
Second molar 18.9 2.0 22 17.5 1.5 20 * 17.3 1.8 34 **
Statistical testing by two-tailed t-test.
47,XXY males vs. population control men ( pa), 47,XXY males vs. population control women ( pb).
ns = not significant.* p < 0.05.** p < 0.01.*** p < 0.001.$ p < 0.1.
a r c h i v e s o f o r a l b i o l o g y 5 2 ( 2 0 0 7 ) 8 2 2 – 8 2 7 825
of girls) at birth and in the earlier stages of development can be
explained by this effect.22,23 It has been suggested that the loci
for the tooth growth promoting genes are on the proximal
portion of the long arm of the Y chromosome,28 and on the
short arm of the X chromosome.29 Molecular studies have
indicated that loci for human amelogenin, the main protein
component of the enamel organic matrix, are to be found on
the distal short arm of the X chromosome and possibly on the
proximal long arm of the Y chromosome, although the short
arm of the Y chromosome has also been suggested.24–26 The
transcriptional products of the X and Y amelogenin genes
seem to be both quantitatively and qualitatively different. The
Y chromosome locus encodes a functional protein, and its
level of expression is only 10% of that on the X chromosome.26
Earlier studies on permanent tooth root growth in
individuals with sex chromosome abnormalities have shown
increased root lengths in 47,XYY males or males with an extra
Y chromosome.12 Their tooth crown size is also increased
which is due to the increase in dentin and enamel thickness.22
The results for 46,XY females or females with male sex
chromosome complement and complete form of androgen
insensitivity syndrome have also shown increase in tooth
root30 and crown sizes, which are close to those in normal
men. Their crown size increase relative to normal women is
due to the dentin layer.22 The root dentin growth in 45,X
females or females with one X chromosome and 45,X/46,XX
females or females with normal XX and one X cell lines, is
reduced.15,31 Crown size reduction in both groups is mainly
due to the thin enamel layer, the dentin layer is close to that of
normal women.8,9,22 It has been suggested that tooth root
growth increase is caused by the X and Y chromosome genes
which promote crown dentin and enamel growth.15
The present results in Klinefelter (47,XXY) men show
increase in their completed permanent tooth root lengths;
growth increase has already appeared in their tooth crown size.
In terms of population dental developmental standards, the
Table 2 – Mean permanent tooth root lengths in maxilla and mandible of 47,XXY males and relative males
Tooth 47,XXY males Relative males
Mean (mm) S.D. N p Mean (mm) S.D. N
Maxillary
Right central incisor 21.1 2.9 15 ns 20.9 2.4 15
Lateral incisor 20.2 2.3 11 ns 20.0 2.6 11
Canine 22.8 3.6 11 $ 24.5 2.6 11
First premolar 20.6 1.6 10 ns 19.0 2.7 10
Second premolar 18.3 2.7 5 ns 19.8 3.3 5
First molar 17.5 1.7 10 $ 16.2 2.1 10
Second molar 17.4 2.9 8 ns 15.9 2.1 8
Maxillary
Left central incisor 21.5 2.8 13 ns 21.0 2.5 13
Lateral incisor 20.0 2.6 12 ns 20.0 1.4 12
Canine 23.9 3.2 8 ns 24.3 2.1 8
First premolar 19.5 2.0 10 ns 18.6 1.7 10
Second premolar 18.6 2.3 8 ns 17.9 1.7 8
First molar 17.0 1.6 9 ns 16.5 2.0 9
Second molar 17.8 1.5 9 * 15.2 2.5 9
Mandibular
Right central incisor 17.3 1.2 16 ns 16.3 1.5 16
Lateral incisor 18.0 1.4 18 ns 17.7 2.0 18
Canine 22.2 1.8 15 ns 22.3 2.6 15
First premolar 20.4 1.7 16 ns 19.2 3.1 16
Second premolar 20.8 2.3 8 ns 19.8 3.8 8
First molar 21.0 1.7 6 ns 19.2 2.8 6
Second molar 18.7 2.3 7 ns 17.3 3.9 7
Mandibular
Left central incisor 17.3 1.7 13 ns 17.2 2.1 13
Lateral incisor 18.5 2.1 18 ns 17.8 2.0 18
Canine 22.2 2.9 18 ns 22.4 2.6 18
First premolar 19.5 1.7 13 ns 18.9 3.3 13
Second premolar 20.5 3.2 7 ns 19.3 2.8 7
First molar 20.8 2.1 8 ns 19.5 2.3 8
Second molar 19.1 2.1 7 ns 17.7 3.2 7
Statistical testing by two-tailed t-test. 47,XXY males vs. relative males.
ns = not significant.* p < 0.05.$ p < 0.1.
a r c h i v e s o f o r a l b i o l o g y 5 2 ( 2 0 0 7 ) 8 2 2 – 8 2 7826
results indicate that root size increases in these men become
evident infinal formbeginning 8 years after birth uptotheage of
14 years, at least and expressing likely a continuous genetic
influence due to an extra X or Y chromosome. It is obvious that
the ‘‘addition’’ of the Y chromosome to XX complement has
greater influence on root growth than the ‘‘addition’’ of the X
chromosome to XY complement. Results on tooth root lengths
in normal men, women, 45,X and 45,X/46,XX females, together
with the present results in 47,XXY men indicate that the
promoting effect of the Y chromosome on the growth of the root
length is greater than that of the X chromosome. These
differential effects are conceivably causative factors in the
development of the sexual dimorphism in tooth root size.
Acknowledgements
The Kvantti research project was supported by the Emil
Aaltonen Foundation, the University of Turku Foundation and
the Academy of Finland. Professor Erkki Tammisalo con-
tributed to the performing of the radiographic examinations.
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