Root lengths in the permanent teeth of Klinefelter (47,XXY) men

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.

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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


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.


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


Canine 23.9 3.2 8 ns 24.3 2.1 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


Canine 22.2 1.8 15 ns 22.3 2.6 15



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


Canine 22.2 2.9 18 ns 22.4 2.6 18



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.


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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Root lengths in the permanent teeth of Klinefelter (47,XXY) men