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Tooth mineralization as an indicator of the pubertal growth spurt
Tooth mineralization as an indicator the pubertal growth spurt
of
Seymour Chertkow, B.D.S., Dip.Orth., H.Dip.Dent. Johannesburg,
South Africa
The commencement of adolescent peak growth velocity in body height and facial growth is closely related in timing to certain ossijcation events which occur in the hand and wrist. An investigation into calcijication patterns of the teeth revealed a high degree of correlation between the stage of mineralization of the lower canine and these events. The possibility of the use of this tooth as a maturational indicator of the pubertal growth spurt is discussed. Key words: Pubertal maturation,
growth
spurt,
maturation,
tooth
calcification,
skeletal
sesamoid
H
uman growth is characterized by considerable variation in the rate of progress of different persons toward physiologic maturity. Chronologic age may have little or no place in the assessment of the maturational state of a child, and it is not a critical factor in the evaluation of over-all growth potential. A close relationship has been shown to exist between the circumpubertal increase in stature and acceleration in the growth of the craniofacial structures.4j 11, 15, I6 In the planning of orthodontic treatment, anticipation of future growth potential of the facial skeleton is essential to ensure the successful outcome of mechanotherapy in the treatment of dentofacial deformities. In order to assess the From the Presented May 5-9, This study Committee
Department of Orthodontics, School of Dentistry, University of the Witwatersrand. at the annual meeting of the American Association of Orthodontists, Washington, D.C., 1979. was supported by the Medical Research Council of South Africa and the Senate Research of the University of the Witwatersrand.
Seymour OOOZ-9416/80/010079+13$01.30/0
0
Chertkow,
B.D.S.,
1980 The C. V. Mosby
Dip. Co
Orth.,
H. Dip.
Dent,
PHV. !
’
2
1 lb
Fig. 1. Relationship between and capping of the epiphysis velocity (P. H. V.).
11
12
15 Aqe (Years)
14
1'5
ossification times of the hook of the hamate (H), adductor sesamoid (S), of the middle phalanx of the third finger (M.f.3 [Cap]) and peak height
significance of this growth potential, it is essential to establish whether the pubertal growth spurt of that patient has been reached or completed. The onset of the adolescent growth spurt and the related increase in craniofacial dimension may be recognized by the determination of annual growth increments in height over a long period of time. Unfortunately, repeated observations are required while the increase in growth velocity may only be recognized retrospectively, thus limiting the value of direct measurement in the recognition of the onset of puberty. Assessment of maturation based on the radiographic appearance of the calcified structures of the hand and wrist is not subject to these limitations. Greulich and Pyle9 and Tanner and associates” have provided radiographic standards for comparison of physical maturity of the individual child with that of normal children of similar age and sex, the former by visual comparison known as the “atlas method” and the latter by the rating of individual bones using a biologically weighted scoring system. In orthodontic practice, however, it may be more relevant to evaluate the development of the patient in relation to his own growth potential in order to assess whether peak velocity growth is imminent, present, or completed. This presupposes a relationship between recognizable stages of skeletal maturation of the hand and wrist and the pubertal growth spurt. A number of indicators have been described in the literature. Among those most commonly used are the onset of calcification of the adductor sesamoid of the thumb,3-s, lo the state of calcification of the hook of the hamate, and capping of the epiphysis of the middle phalanx of the third finger. 2, g, lo The relationship between these
Volume 11 Number 1
Tooth
Fig.
2. Radiographic
appearance
of early
minercrlization
calcification
and
pubertal
of the adductor
growth
spurt
81
sesamoid.
indicators and peak height velocity is shown in Fig. 1. Unfortunately, little is known of the relationship between the onset of puberty and dental maturation. Studies have shown that correlations between tooth mineralization and other parameters of physical development are generally low,‘, ** while there is little more than slight covariation between tooth eruption and the adolescent growth spurt. I4 The present study investigates the relationship between the stages of mineralization of various teeth and other maturational indicators of the pubertal growth spurt among black and white South African boys and girls. Methods and materials Data were obtained from the records of 197 patients taken from the files of an orthodontic practice and the Orthodontic Department of the School of Dentistry, University of the Witwatersrand. All participants were well nourished and free of any known serious illness. The sample included sixty-six white and twenty-two black boys and ninety-three white and sixteen black girls, none of whom had received orthodontic therapy previously. Panoramic dental or lateral oblique radiographs of the left mandible and maxilla, together with radiographic views of the left hand and wrist, taken from the clinical records of these patients were examined. Selection of participants was based on the observation of radiographic evidence of early calcification of the adductor sesamoid of the thumb on the hand-wrist radiograph.
@C@ G
f&@
appearance
”
i”= H ‘ Q
f&E@) Fig. 3. Diagrammatic teeth.
,... ., Q
of stages
C to H of tooth
development
for unl- and
multiradicular
Although the sesamoid varies in size from one person to another, the following criteria were applied in the assessment of early calcification5 (Fig. 2): 1. A sesamoid diameter of approximately 1 mm. 2. The presence of an ill-defined feathery outline. 3. Incomplete calcification resulting in poor radiopacity The skeletal age of each participant was assessed by the T.W.2 method described by Tanner and colleagues. lx The dental radiographs were examined and tooth mineralization on the left side was rated according to the method described by Demirjian and associates’ in which eight stages of calcification, A to H. are described for each tooth. The stages ascribed to teeth in this study ranged from C to H. Each of these stages may be recognized by the following criteria (Fig. 3): Stage C. Enamel formation has been completed at the occlusal surface. and dentine formation has commenced. The pulp chamber is curved, and no pulp horns are visible. Stage D. Crown formation has been completed to the level of the amelocemental junction. Root formation has commenced. The pulp horns are beginning to differentiate, but the walls of the pulp chamber remain curved. Stuge E. The root length remains shorter than the crown height. The walls of the pulp chamber are straight, and the pulp horns have become more differentiated than in the previous stage. In molars the radicular bifurcation has commenced to calcify. Stage F. The walls of the pulp chamber now form an isosceles triangle, and the root length is equal to or greater than the crown height. In molars the bifurcation has developed sufficiently to give the roots a distinct form. Stage G. The walls of the root canal are now parallel, but the apical end is partially open. In molars only the distal root is rated. Stage H. The root apex is completely closed (distal root in molars). The periodontal membrane surrounding the root and apex is uniform in width throughout. The maxillary posterior teeth were omitted from the study, as superimposition of calcified structures in this area rendered accurate assessment of the state of development of these teeth virtually impossible. Incisors as well as first molars were not rated, as apical closure had already taken place. Third molars were also excluded from the study. The
Volume 71 Number
Tooth
1
mineralization
and pubertal
growth
83
spurt
Table I. Distribution of stagesof calcification among white boys and girls Boys
I
Lower canine
c D E F G H Total
4 39 21 64
Lower jrst premolar
-
2 8 12 42 64
2 52 12 66
-
-
-
2 19 23
6 22 28
17 60
-
21 65
10 66
11 88
6 72
4 36 33
14 50 21
2 19 49 19
15 93
19 92
5 90
2 93
Table II. Distribution of stagesof calcification among black boys and girls
I
Boys
Stage of calcifi-
cation
Upper canine I
C D E F G
H Total
I
Lower canine I
Girls
I
Lower jirst premolar
-
-
-
-
-
-
1 4 16 21
2 8 12 ii
-
-
-
21
1 21
22
22
1 21 22
-
1 15 16
1 15 16
-
1 1 1 13 16
1 2 4
1 1 10 4 16
9 16
Table Ill. Ages (in years) at early calcification of the adductor sesamoid Chronologic Subjects White Boys Girls Black Boys Girls
Sample
size
age
Skeletal
age
Mean
S.D.
Mean
S.D.
66 93
13.22 11.3
1.15 .95
13.30 11.22
.51 .44
22 16
14.11 12.57
1.06 1.05
13.35 11.4
.44 .52
teeth examined were thus the maxillary and mandibular canines, first and second premolars, and mandibular second molars. The lower first premolars were congenitally absent in three white children, while agenesis of the second premolars was seen in one black and three white children. In seven participants the state of development of the maxillary canines could not be accurately assessed because of the superimposition of the palatal shelves over the developing root on the radiograph. These teeth were excluded from the sample. The distribution of the stages of root formation for each of the teeth studied is summarized in Tables I and II.
&per Canine
Stages of Calcification Fig. 4. Histogram white
depicting
percentage
distribution
of stages
of calcification
of upper
canines
among
children.
0'
Fig. 5. Percentage Statistical
methods
I c
distribution
I
D
'
of stages
’
E
/
of calcification
of lower
canines
among
white
children.
and results
The mean chronologic and skeletal ages of both black and white boys and girls were calculated in order to determine the variation in the age of early radiographic evidence of calcification of the adductor sesamoid between the various groups (Table III). The mean chronologic age at appearance of the sesamoid is accelerated by 1 year among the white participants. This retardation of skeletal development among South African black children compared to the Caucasoid peer group is a phenomenon which is well documented in the literature. ‘a However, the means of the skeletal ages do not differ significantly from one another and are comparable to the mean age at onset of calcification of the adductor sesamoid reported in numerous other studies.X. n. I7 In order to study the relationships between the state of mineralization of the teeth and this stage of skeletal maturation, the percentage distribution of the stages of calcification
Vollrme 77 Number 1
Tooth mineralization
growth spurt
and pubertal
85
Lower First Premolar
Stages of Calcification Fig.
6. Percentage
distribution
of stages
of calcification
of lower
first
premolars
among
white
children.
LowersecondPremolar
.E loo- IMales Ii‘L’ so q Females z
s0
i g
f: .lc-
i
T”,: 0 I
C
Fig. 7. Percentage children.
distribution
I
1 / D’E FT-G stages of Calciiiation of stages
of calcification
of lower
/
H
second
premolars
among
white
for each of the teeth studied was calculated. Sex and racial differences in the pattern of mineralization of the various teeth were noted. The percentage distribution of calcification stages in each population group for the various teeth may be illustrated by means of histograms (Figs. 4 to 13). Marked differences are clearly depicted in the distribution of stages of mineralization among the various teeth. The uniformity of the rate of development of the mandibular canine (Figs. 5 and 10) contrasts sharply with the far wider distribution of calcification stages of the remaining teeth. Marked racial differences are evident in the patterns of calcification of the teeth studied. Tooth development is accelerated among black children to the extent that the majority of teeth examined radiographically in this group are completely developed, with apical closure having already occurred (Figs. 9 to 13).
Lower Second Molar
Stages of Calcification Fig. 8. Percentage
distribution
of stages
of calcification
Upper
1 I .s 2 5 0
,oO- 0 9o. 80, 7060,
molars
among
white
children.
Canine
distribution
of stages
I
-‘*g-~---T Stages
9. Percentage
second
Males Females
7-
Fig.
of lower
H
of Calcification
of calcification
of upper
canines
among
-
black
children.
Sexual differences in the rate of calcification of the teeth are present. A definite trend toward acceleration in tooth mineralization among boys is evident in all the teeth except the mandibular canine, which exhibits a strong similarity between boys and girls in its calcification pattern. The chi-square statistic was applied to the tooth calcification data in order to test the reliability of the results depicted graphically.‘” As the majority of the teeth studied in the black children had reached maturity, statistical analysis of the data relating to this group was not undertaken. In the white group, calcification Stages C and D were combined with Stage E for the purpose of applying this test as a result of the small numbers occurring in these groups. The chi-square values were highly significant at the 1 percent level. The major contribution came from stages F and G of the mandibular canine, indicating that the observed distribution of the stages of mineralization of this tooth differs sufficiently to reject the null hypothesis at the 1 percent level of significance.
Volume 71 Number 1
Tooth
Lower
.g
,00-
mineralization
and pubertal
growth
spurt
87
Canine
m Males 0 Females
-
go-
Yg 3 80775
70-
fi
60-
g
50-
2 c $
40-
&
20-
30-
a
loO-
’
1
D
C
I
Stages Fig.
10. Percentage
distribution
of stages
d-l
1
E
F
I
G
H
of Calcification
of calcification
of lower
canines
among
black
children
Lower First Premolar - m Males ,Oo- 0 Females ‘;E 90 _ 3 g 805
70-
a
60-
Q E
::30-
8 $ a
20lo0
I
I
C
D
distribution
of stages
. Fig. 11. Percentage
l-l
m
n
F Stagf3 of Calcifiitii E
of calcification
of lower
G
first premolars
H
among
black
children.
The chi-square statistic was then applied to test for differences between boys and girls in the distribution of stages of mineralization for each group of teeth. Chi-square values were significant at the 1 percent level for all teeth except the mandibular canine, indicating a strong sex-specific pattern of mineralization for these teeth. No significant sexual dimorphism was evident in the calcification pattern of the mandibular canine. In order to explore the relationship between the development of the mandibular canine and other indicators of the pubertal growth spurt, the state of maturity of this tooth was related to the degree of calcification of the hook of the hamate and the state of development of the epiphysis of the middle phalanx of the third finger (Table IV). It is noteworthy that, among participants displaying an immature state of development of the mandibular canine, the other indicators have likewise not yet made their appearance. Conversely, in those patients in whom apical closure of the mandibular canine has already taken place, the hook of the hamate is fully formed in all cases, and capping of the middle phalanx of the third finger by its epiphysis may be noted in the majority of patients.
Lower
n ,00-
Second
Premolar
Males Females
n
90*o7060, so403020IO0’
-7
, c
I
I D
r
Stages Fig. 12. Percentage
distribution
of stages
r-l E
r F
I
I G
I
H
c
of Calcification of calcification
of lower
second
premolars
among
black
children.
Second
Lower
n 0
Molar
Males Females
70-
fi $” a E 8 b a
60-
‘lo30*O loi-l
0
Fig. 13. Percentage
C
D
distribution
of stages
’ E ’ F ’ Stages of Calcification of calcification
of lower
G
second
’
molars
H
among
!
black
children.
This observation tends to indicate the existence of a close relationship between the state of maturation of the mandibular canine and the time of appearance of the maturational indicators discussed. Discussion
The role of the adductor sesamoid of the thumb, the hook of the hamate, and the epiphysis of the middle phalanx of the third finger as indicators of the pubertal growth spurt has been described by numerous workers.2-“~ $‘. lo However, little correlation has been shown to exist between the appearance of these indicators and the over-all maturational state of the dentition. I, 6, I2 In the sample used, the pattern of mineralization of the various teeth studied varied from tooth to tooth. In accordance with the findings of Lewis and Garn” and others 6. I4 no close relationship could be shown to exist between the state of development of the ;ower premolars and second molars and the maturational state of the patient.
Volume II Number 1
Tooth
mineralization
and
pubertal
growth
spurt
89
Table IV. Relationship between the state of maturity of the lower canine and the development of the hook of the hamate as well as the epiphysis of the middle phalanx of the third finger State of calc@cation of hook of hamate
Total
Canine stage F Males 4 Females 6 Canine stage G Males 52 Females 72 Canine stage H Males 12 Females 15
Incompletely calcijed
3 6
Calcification of epiphysis of middle phalanx of third finger
Completely calcijied
1 0
18 14
34 68
0
12 15
0
Epihysis equal in width to diaphysis
4 6 33 30 4 1
Epiphysis caps diaphysis
0 0 19 42 8 14
The maturation patterns of these teeth varied widely, with a distinct tendency toward acceleration in the rate of mineralization among the boys in both racial groups. The range of distribution of the stages of calcification relating to both the maxillary and mandibular canines was far narrower, with the majority of teeth having developed to the stage prior to apical closure (Stage G) in white children. The state of development of the mandibular canine in particular was closely related to this stage of skeletal maturity, with 77 percent of the white girls and 78 percent of the white boys having reached this stage of development. The dental maturation pattern among black boys and girls was accelerated, confirming a well-documented observation. rg Both upper and lower canines as well as the first premolars were fully developed, with apical closure having already occurred. Significant sex differences in the distribution of the stages of tooth mineralization were evident in all the teeth, with the exception of the mandibular canines. In general, tooth development in boys tended to be accelerated in relation to skeletal maturity as compared to girls. No significant sex differences were evident in the state of development of the mandibular canines. Among the white children, completion of root formation prior to apical closure (Stage G) coincided with the appearance of other maturational indicators of the pubertal growth spurt, with only an insignificant number of teeth not having reached this stage. In fact, among those participants who presented with an earlier stage of development of this tooth, none of the other indicators of the pubertal growth spurt were visible except the onset of calcification of the sesamoid. Among the black children, however, these relationships could not be verified, as apical closure had already occurred. The close relationship between calcijcation Stage G of the mandibular canine and other maturational indicators of the pubertal growth spurt among Caucasoid children therefore raises the possibility of the use of this tooth as an indicator of approaching adolescence. Ease of recognition of this stage of development of the tooth, together with the free availability of intraoral or panoramic radiographs in an orthodontic or pedodontic practice, would make the assessment of onset of puberty possible in children of Caucasoid
Figs. 14 and 15. Radiographs development
and
some
skeletal
of two 1 I-year-old girls illustrating the relatlonship indicators of the pubertal growth spurt
between
lower
canine
origin without the necessity of resorting to the use of hand-urtst radiographs or serial recordings of annual increases in stature. Hand-wrist films and panoramic radiographs of two girls, taken from the clinical records of these patients prior to orthodontic treatment, clearly show the relationships of the developing mandibular canines to other maturational indicators of the pubertal growth spurt (Figs. 14 and 15). In both cases the skeletal indicators are present in the hand-wrist has commenced, the hook of the hamate is radiographs; calcification of the sesamoid completely calcified, and the epiphysis of the middle phalanx of the third tinger caps the diaphysis. In assessing dental development. the over-all rate of maturation varies considerably between the two children. with the exception of the mandibular canines. These teeth exhibit a similar degree of calcification in both cases. having reached the stage of completion of root formation prior to apical closure (Stage Gi despite the gross variation in their state of eruption. Summary
The relationship between the state of maturation of the maxillary and mandibular canines and the lower premolars and second molars and known skeletal indicators of the pubertal growth spurt was investigated. Data were obtained from the records of 197 children (159 white and 38 black). Completion of root formation of the mandibular canine prior to apical closure was closely related to the appearance of other maturational indicators among white children. No significant sex differences were noted in the state of maturation of this tooth. Correla-
Volume 77 Number I
Tooth
minerali;ation
and puhertul
growth
spurt
91
tions among the remaining teeth studied were low, the distribution of calcification stages being widely dispersed, with significant sexual dimorphism evident. In the black children, apical closure of the canine root had already occurred, as was the case with a large proportion of the remaining teeth studied. For this reason, meaningful interpretation of the relationship between the state of development of the mandibular canine and the maturational indicators discussed earlier was impossible. The findings of this study indicate that the completion of root formation of the mandibular canine tooth prior to apical closure may be used clinically as a maturity indicator of the pubertal growth spurt with a similar degree of confidence as some of the other indicators described on the hand-wrist radiograph among children of Caucasoid origin. Unfortunately, racial variations exist in the relationship between the state of maturity of this tooth and other parameters of development, as was shown in the present study. Caution should thus be exercised in the application of this finding to other racial groups. REFERENCES I. Anderson, D. L., Thompson, G. W., and Popovitch, F.: Interrelationships of dental maturity, skeletal maturity, height and weight from age 4 to 14 years, Growth 39: 453-462, 1975. 2. Bjork, A.: Timing of interceptive orthodontic measures based on stages of maturation, 48th Congress Trans. Eur. Orthod. Sot., pp. 61-74, 1972. 3. Bjork, A., and Helm, S.: Prediction of the age of maximum pubertal growth in body height, Angle Orthod. 37: 134-143, 1967. 4. Brown, T., Barrett, M. J., and Grave, K. C.: Facial growth and skeletal maturation at adolescence, Dan. Dent. J. 75: 1121-1222, 1971. 5. Chapman, S. M.: Ossification of the adductor sesamoid and the adolescent growth spurt, Angle Orthod. 42: 236-244, 1972. 6. Chertkow, S., and Fatti, P. L.: The relationship between tooth mineralization and early radiographic evidence of adductor sesamoid calcification, Angle Otthod., October, 1979, 7. Demirjian, A., Goldstein, H., and Tanner, J. M.: A new system of dental age assessment, Hum. Biol. 45: 211-227, 1973. 8. Gam, S. M., and Rohman, C. G.; The adductor sesamoid of the thumb, Am. J. Phys. Anthropol. 20: 297-302, 1962. 9. Greulich, W. W., and Pyle, S. I.: Radiographic atlas of skeletal development of the hand and wrist. ed. 2, Stanford, Calif., 1959, Stanford University Press. 10. Helm, S., Siersback-Nielsen, S., Skieler, V., and Bjork, A: Skeletal maturation of the hand in relation to maximum pubertal growth in body height, Dan. Dent. J. 75: 1223-1234, 1971. 11. Hunter, C. J.: The correlation of facial growth with body height and skeletal maturation at adolescence, Angle Orthod. 36: 44-54, 1966. 12. Lewis, A. B., and Garn, S. M.: The relationship between tooth formation and other maturational factors, Angle Orthod. 30: 70-77, 1960. 13. Maxwell, A. E.: Analysing qualitative data, London, 1975, Chapman & Hall. 14. Meredith, H. V.: Relation between the eruption of selected mandibular permanent teeth and the circumpubertal acceleration in stature, J. Dent. Child. 26: 75-78, 1959. 15. Nanda, R. S.: The rates of growth of several facial components measured from serial cephalometric roentgenograms, AM. J. ORTHOD. 41: 658-673, 1955. 16. Roche, A. F., and Lewis, A. B.: Late growth changes in the cranial base. In Boersma, J. F. (editor): Symposium on development of the basicranium, DHEW Publication No, (NIH) 76-989, Washington, 1976, United States Department of Health, Education and Welfare. 17. Roche. A. F., Roberts, J., and Hammill, V. V.: Skeletal maturity of youths 12-17 years: Vita1 and health statistics. National Health Survey, Series 11, No. 160, 1976. 18. Tanner, J. M., Whitehouse, R. H., Marshall, W. A., Healy, M. J. R., and Goldstein, H.: Assessment of skeletal maturity and prediction of adult height (T.W.2 method), London, 1975, Academic Press. 19. Tobias, P. V.: Some aspects of the biology of the Bantu-speaking African, The Leech 28: 3-12, 1958.
of
Seymour Chertkow, B.D.S., Dip.Orth., H.Dip.Dent. Johannesburg,
South Africa
The commencement of adolescent peak growth velocity in body height and facial growth is closely related in timing to certain ossijcation events which occur in the hand and wrist. An investigation into calcijication patterns of the teeth revealed a high degree of correlation between the stage of mineralization of the lower canine and these events. The possibility of the use of this tooth as a maturational indicator of the pubertal growth spurt is discussed. Key words: Pubertal maturation,
growth
spurt,
maturation,
tooth
calcification,
skeletal
sesamoid
H
uman growth is characterized by considerable variation in the rate of progress of different persons toward physiologic maturity. Chronologic age may have little or no place in the assessment of the maturational state of a child, and it is not a critical factor in the evaluation of over-all growth potential. A close relationship has been shown to exist between the circumpubertal increase in stature and acceleration in the growth of the craniofacial structures.4j 11, 15, I6 In the planning of orthodontic treatment, anticipation of future growth potential of the facial skeleton is essential to ensure the successful outcome of mechanotherapy in the treatment of dentofacial deformities. In order to assess the From the Presented May 5-9, This study Committee
Department of Orthodontics, School of Dentistry, University of the Witwatersrand. at the annual meeting of the American Association of Orthodontists, Washington, D.C., 1979. was supported by the Medical Research Council of South Africa and the Senate Research of the University of the Witwatersrand.
Seymour OOOZ-9416/80/010079+13$01.30/0
0
Chertkow,
B.D.S.,
1980 The C. V. Mosby
Dip. Co
Orth.,
H. Dip.
Dent,
PHV. !
’
2
1 lb
Fig. 1. Relationship between and capping of the epiphysis velocity (P. H. V.).
11
12
15 Aqe (Years)
14
1'5
ossification times of the hook of the hamate (H), adductor sesamoid (S), of the middle phalanx of the third finger (M.f.3 [Cap]) and peak height
significance of this growth potential, it is essential to establish whether the pubertal growth spurt of that patient has been reached or completed. The onset of the adolescent growth spurt and the related increase in craniofacial dimension may be recognized by the determination of annual growth increments in height over a long period of time. Unfortunately, repeated observations are required while the increase in growth velocity may only be recognized retrospectively, thus limiting the value of direct measurement in the recognition of the onset of puberty. Assessment of maturation based on the radiographic appearance of the calcified structures of the hand and wrist is not subject to these limitations. Greulich and Pyle9 and Tanner and associates” have provided radiographic standards for comparison of physical maturity of the individual child with that of normal children of similar age and sex, the former by visual comparison known as the “atlas method” and the latter by the rating of individual bones using a biologically weighted scoring system. In orthodontic practice, however, it may be more relevant to evaluate the development of the patient in relation to his own growth potential in order to assess whether peak velocity growth is imminent, present, or completed. This presupposes a relationship between recognizable stages of skeletal maturation of the hand and wrist and the pubertal growth spurt. A number of indicators have been described in the literature. Among those most commonly used are the onset of calcification of the adductor sesamoid of the thumb,3-s, lo the state of calcification of the hook of the hamate, and capping of the epiphysis of the middle phalanx of the third finger. 2, g, lo The relationship between these
Volume 11 Number 1
Tooth
Fig.
2. Radiographic
appearance
of early
minercrlization
calcification
and
pubertal
of the adductor
growth
spurt
81
sesamoid.
indicators and peak height velocity is shown in Fig. 1. Unfortunately, little is known of the relationship between the onset of puberty and dental maturation. Studies have shown that correlations between tooth mineralization and other parameters of physical development are generally low,‘, ** while there is little more than slight covariation between tooth eruption and the adolescent growth spurt. I4 The present study investigates the relationship between the stages of mineralization of various teeth and other maturational indicators of the pubertal growth spurt among black and white South African boys and girls. Methods and materials Data were obtained from the records of 197 patients taken from the files of an orthodontic practice and the Orthodontic Department of the School of Dentistry, University of the Witwatersrand. All participants were well nourished and free of any known serious illness. The sample included sixty-six white and twenty-two black boys and ninety-three white and sixteen black girls, none of whom had received orthodontic therapy previously. Panoramic dental or lateral oblique radiographs of the left mandible and maxilla, together with radiographic views of the left hand and wrist, taken from the clinical records of these patients were examined. Selection of participants was based on the observation of radiographic evidence of early calcification of the adductor sesamoid of the thumb on the hand-wrist radiograph.
@C@ G
f&@
appearance
”
i”= H ‘ Q
f&E@) Fig. 3. Diagrammatic teeth.
,... ., Q
of stages
C to H of tooth
development
for unl- and
multiradicular
Although the sesamoid varies in size from one person to another, the following criteria were applied in the assessment of early calcification5 (Fig. 2): 1. A sesamoid diameter of approximately 1 mm. 2. The presence of an ill-defined feathery outline. 3. Incomplete calcification resulting in poor radiopacity The skeletal age of each participant was assessed by the T.W.2 method described by Tanner and colleagues. lx The dental radiographs were examined and tooth mineralization on the left side was rated according to the method described by Demirjian and associates’ in which eight stages of calcification, A to H. are described for each tooth. The stages ascribed to teeth in this study ranged from C to H. Each of these stages may be recognized by the following criteria (Fig. 3): Stage C. Enamel formation has been completed at the occlusal surface. and dentine formation has commenced. The pulp chamber is curved, and no pulp horns are visible. Stage D. Crown formation has been completed to the level of the amelocemental junction. Root formation has commenced. The pulp horns are beginning to differentiate, but the walls of the pulp chamber remain curved. Stuge E. The root length remains shorter than the crown height. The walls of the pulp chamber are straight, and the pulp horns have become more differentiated than in the previous stage. In molars the radicular bifurcation has commenced to calcify. Stage F. The walls of the pulp chamber now form an isosceles triangle, and the root length is equal to or greater than the crown height. In molars the bifurcation has developed sufficiently to give the roots a distinct form. Stage G. The walls of the root canal are now parallel, but the apical end is partially open. In molars only the distal root is rated. Stage H. The root apex is completely closed (distal root in molars). The periodontal membrane surrounding the root and apex is uniform in width throughout. The maxillary posterior teeth were omitted from the study, as superimposition of calcified structures in this area rendered accurate assessment of the state of development of these teeth virtually impossible. Incisors as well as first molars were not rated, as apical closure had already taken place. Third molars were also excluded from the study. The
Volume 71 Number
Tooth
1
mineralization
and pubertal
growth
83
spurt
Table I. Distribution of stagesof calcification among white boys and girls Boys
I
Lower canine
c D E F G H Total
4 39 21 64
Lower jrst premolar
-
2 8 12 42 64
2 52 12 66
-
-
-
2 19 23
6 22 28
17 60
-
21 65
10 66
11 88
6 72
4 36 33
14 50 21
2 19 49 19
15 93
19 92
5 90
2 93
Table II. Distribution of stagesof calcification among black boys and girls
I
Boys
Stage of calcifi-
cation
Upper canine I
C D E F G
H Total
I
Lower canine I
Girls
I
Lower jirst premolar
-
-
-
-
-
-
1 4 16 21
2 8 12 ii
-
-
-
21
1 21
22
22
1 21 22
-
1 15 16
1 15 16
-
1 1 1 13 16
1 2 4
1 1 10 4 16
9 16
Table Ill. Ages (in years) at early calcification of the adductor sesamoid Chronologic Subjects White Boys Girls Black Boys Girls
Sample
size
age
Skeletal
age
Mean
S.D.
Mean
S.D.
66 93
13.22 11.3
1.15 .95
13.30 11.22
.51 .44
22 16
14.11 12.57
1.06 1.05
13.35 11.4
.44 .52
teeth examined were thus the maxillary and mandibular canines, first and second premolars, and mandibular second molars. The lower first premolars were congenitally absent in three white children, while agenesis of the second premolars was seen in one black and three white children. In seven participants the state of development of the maxillary canines could not be accurately assessed because of the superimposition of the palatal shelves over the developing root on the radiograph. These teeth were excluded from the sample. The distribution of the stages of root formation for each of the teeth studied is summarized in Tables I and II.
&per Canine
Stages of Calcification Fig. 4. Histogram white
depicting
percentage
distribution
of stages
of calcification
of upper
canines
among
children.
0'
Fig. 5. Percentage Statistical
methods
I c
distribution
I
D
'
of stages
’
E
/
of calcification
of lower
canines
among
white
children.
and results
The mean chronologic and skeletal ages of both black and white boys and girls were calculated in order to determine the variation in the age of early radiographic evidence of calcification of the adductor sesamoid between the various groups (Table III). The mean chronologic age at appearance of the sesamoid is accelerated by 1 year among the white participants. This retardation of skeletal development among South African black children compared to the Caucasoid peer group is a phenomenon which is well documented in the literature. ‘a However, the means of the skeletal ages do not differ significantly from one another and are comparable to the mean age at onset of calcification of the adductor sesamoid reported in numerous other studies.X. n. I7 In order to study the relationships between the state of mineralization of the teeth and this stage of skeletal maturation, the percentage distribution of the stages of calcification
Vollrme 77 Number 1
Tooth mineralization
growth spurt
and pubertal
85
Lower First Premolar
Stages of Calcification Fig.
6. Percentage
distribution
of stages
of calcification
of lower
first
premolars
among
white
children.
LowersecondPremolar
.E loo- IMales Ii‘L’ so q Females z
s0
i g
f: .lc-
i
T”,: 0 I
C
Fig. 7. Percentage children.
distribution
I
1 / D’E FT-G stages of Calciiiation of stages
of calcification
of lower
/
H
second
premolars
among
white
for each of the teeth studied was calculated. Sex and racial differences in the pattern of mineralization of the various teeth were noted. The percentage distribution of calcification stages in each population group for the various teeth may be illustrated by means of histograms (Figs. 4 to 13). Marked differences are clearly depicted in the distribution of stages of mineralization among the various teeth. The uniformity of the rate of development of the mandibular canine (Figs. 5 and 10) contrasts sharply with the far wider distribution of calcification stages of the remaining teeth. Marked racial differences are evident in the patterns of calcification of the teeth studied. Tooth development is accelerated among black children to the extent that the majority of teeth examined radiographically in this group are completely developed, with apical closure having already occurred (Figs. 9 to 13).
Lower Second Molar
Stages of Calcification Fig. 8. Percentage
distribution
of stages
of calcification
Upper
1 I .s 2 5 0
,oO- 0 9o. 80, 7060,
molars
among
white
children.
Canine
distribution
of stages
I
-‘*g-~---T Stages
9. Percentage
second
Males Females
7-
Fig.
of lower
H
of Calcification
of calcification
of upper
canines
among
-
black
children.
Sexual differences in the rate of calcification of the teeth are present. A definite trend toward acceleration in tooth mineralization among boys is evident in all the teeth except the mandibular canine, which exhibits a strong similarity between boys and girls in its calcification pattern. The chi-square statistic was applied to the tooth calcification data in order to test the reliability of the results depicted graphically.‘” As the majority of the teeth studied in the black children had reached maturity, statistical analysis of the data relating to this group was not undertaken. In the white group, calcification Stages C and D were combined with Stage E for the purpose of applying this test as a result of the small numbers occurring in these groups. The chi-square values were highly significant at the 1 percent level. The major contribution came from stages F and G of the mandibular canine, indicating that the observed distribution of the stages of mineralization of this tooth differs sufficiently to reject the null hypothesis at the 1 percent level of significance.
Volume 71 Number 1
Tooth
Lower
.g
,00-
mineralization
and pubertal
growth
spurt
87
Canine
m Males 0 Females
-
go-
Yg 3 80775
70-
fi
60-
g
50-
2 c $
40-
&
20-
30-
a
loO-
’
1
D
C
I
Stages Fig.
10. Percentage
distribution
of stages
d-l
1
E
F
I
G
H
of Calcification
of calcification
of lower
canines
among
black
children
Lower First Premolar - m Males ,Oo- 0 Females ‘;E 90 _ 3 g 805
70-
a
60-
Q E
::30-
8 $ a
20lo0
I
I
C
D
distribution
of stages
. Fig. 11. Percentage
l-l
m
n
F Stagf3 of Calcifiitii E
of calcification
of lower
G
first premolars
H
among
black
children.
The chi-square statistic was then applied to test for differences between boys and girls in the distribution of stages of mineralization for each group of teeth. Chi-square values were significant at the 1 percent level for all teeth except the mandibular canine, indicating a strong sex-specific pattern of mineralization for these teeth. No significant sexual dimorphism was evident in the calcification pattern of the mandibular canine. In order to explore the relationship between the development of the mandibular canine and other indicators of the pubertal growth spurt, the state of maturity of this tooth was related to the degree of calcification of the hook of the hamate and the state of development of the epiphysis of the middle phalanx of the third finger (Table IV). It is noteworthy that, among participants displaying an immature state of development of the mandibular canine, the other indicators have likewise not yet made their appearance. Conversely, in those patients in whom apical closure of the mandibular canine has already taken place, the hook of the hamate is fully formed in all cases, and capping of the middle phalanx of the third finger by its epiphysis may be noted in the majority of patients.
Lower
n ,00-
Second
Premolar
Males Females
n
90*o7060, so403020IO0’
-7
, c
I
I D
r
Stages Fig. 12. Percentage
distribution
of stages
r-l E
r F
I
I G
I
H
c
of Calcification of calcification
of lower
second
premolars
among
black
children.
Second
Lower
n 0
Molar
Males Females
70-
fi $” a E 8 b a
60-
‘lo30*O loi-l
0
Fig. 13. Percentage
C
D
distribution
of stages
’ E ’ F ’ Stages of Calcification of calcification
of lower
G
second
’
molars
H
among
!
black
children.
This observation tends to indicate the existence of a close relationship between the state of maturation of the mandibular canine and the time of appearance of the maturational indicators discussed. Discussion
The role of the adductor sesamoid of the thumb, the hook of the hamate, and the epiphysis of the middle phalanx of the third finger as indicators of the pubertal growth spurt has been described by numerous workers.2-“~ $‘. lo However, little correlation has been shown to exist between the appearance of these indicators and the over-all maturational state of the dentition. I, 6, I2 In the sample used, the pattern of mineralization of the various teeth studied varied from tooth to tooth. In accordance with the findings of Lewis and Garn” and others 6. I4 no close relationship could be shown to exist between the state of development of the ;ower premolars and second molars and the maturational state of the patient.
Volume II Number 1
Tooth
mineralization
and
pubertal
growth
spurt
89
Table IV. Relationship between the state of maturity of the lower canine and the development of the hook of the hamate as well as the epiphysis of the middle phalanx of the third finger State of calc@cation of hook of hamate
Total
Canine stage F Males 4 Females 6 Canine stage G Males 52 Females 72 Canine stage H Males 12 Females 15
Incompletely calcijed
3 6
Calcification of epiphysis of middle phalanx of third finger
Completely calcijied
1 0
18 14
34 68
0
12 15
0
Epihysis equal in width to diaphysis
4 6 33 30 4 1
Epiphysis caps diaphysis
0 0 19 42 8 14
The maturation patterns of these teeth varied widely, with a distinct tendency toward acceleration in the rate of mineralization among the boys in both racial groups. The range of distribution of the stages of calcification relating to both the maxillary and mandibular canines was far narrower, with the majority of teeth having developed to the stage prior to apical closure (Stage G) in white children. The state of development of the mandibular canine in particular was closely related to this stage of skeletal maturity, with 77 percent of the white girls and 78 percent of the white boys having reached this stage of development. The dental maturation pattern among black boys and girls was accelerated, confirming a well-documented observation. rg Both upper and lower canines as well as the first premolars were fully developed, with apical closure having already occurred. Significant sex differences in the distribution of the stages of tooth mineralization were evident in all the teeth, with the exception of the mandibular canines. In general, tooth development in boys tended to be accelerated in relation to skeletal maturity as compared to girls. No significant sex differences were evident in the state of development of the mandibular canines. Among the white children, completion of root formation prior to apical closure (Stage G) coincided with the appearance of other maturational indicators of the pubertal growth spurt, with only an insignificant number of teeth not having reached this stage. In fact, among those participants who presented with an earlier stage of development of this tooth, none of the other indicators of the pubertal growth spurt were visible except the onset of calcification of the sesamoid. Among the black children, however, these relationships could not be verified, as apical closure had already occurred. The close relationship between calcijcation Stage G of the mandibular canine and other maturational indicators of the pubertal growth spurt among Caucasoid children therefore raises the possibility of the use of this tooth as an indicator of approaching adolescence. Ease of recognition of this stage of development of the tooth, together with the free availability of intraoral or panoramic radiographs in an orthodontic or pedodontic practice, would make the assessment of onset of puberty possible in children of Caucasoid
Figs. 14 and 15. Radiographs development
and
some
skeletal
of two 1 I-year-old girls illustrating the relatlonship indicators of the pubertal growth spurt
between
lower
canine
origin without the necessity of resorting to the use of hand-urtst radiographs or serial recordings of annual increases in stature. Hand-wrist films and panoramic radiographs of two girls, taken from the clinical records of these patients prior to orthodontic treatment, clearly show the relationships of the developing mandibular canines to other maturational indicators of the pubertal growth spurt (Figs. 14 and 15). In both cases the skeletal indicators are present in the hand-wrist has commenced, the hook of the hamate is radiographs; calcification of the sesamoid completely calcified, and the epiphysis of the middle phalanx of the third tinger caps the diaphysis. In assessing dental development. the over-all rate of maturation varies considerably between the two children. with the exception of the mandibular canines. These teeth exhibit a similar degree of calcification in both cases. having reached the stage of completion of root formation prior to apical closure (Stage Gi despite the gross variation in their state of eruption. Summary
The relationship between the state of maturation of the maxillary and mandibular canines and the lower premolars and second molars and known skeletal indicators of the pubertal growth spurt was investigated. Data were obtained from the records of 197 children (159 white and 38 black). Completion of root formation of the mandibular canine prior to apical closure was closely related to the appearance of other maturational indicators among white children. No significant sex differences were noted in the state of maturation of this tooth. Correla-
Volume 77 Number I
Tooth
minerali;ation
and puhertul
growth
spurt
91
tions among the remaining teeth studied were low, the distribution of calcification stages being widely dispersed, with significant sexual dimorphism evident. In the black children, apical closure of the canine root had already occurred, as was the case with a large proportion of the remaining teeth studied. For this reason, meaningful interpretation of the relationship between the state of development of the mandibular canine and the maturational indicators discussed earlier was impossible. The findings of this study indicate that the completion of root formation of the mandibular canine tooth prior to apical closure may be used clinically as a maturity indicator of the pubertal growth spurt with a similar degree of confidence as some of the other indicators described on the hand-wrist radiograph among children of Caucasoid origin. Unfortunately, racial variations exist in the relationship between the state of maturity of this tooth and other parameters of development, as was shown in the present study. Caution should thus be exercised in the application of this finding to other racial groups. REFERENCES I. Anderson, D. L., Thompson, G. W., and Popovitch, F.: Interrelationships of dental maturity, skeletal maturity, height and weight from age 4 to 14 years, Growth 39: 453-462, 1975. 2. Bjork, A.: Timing of interceptive orthodontic measures based on stages of maturation, 48th Congress Trans. Eur. Orthod. Sot., pp. 61-74, 1972. 3. Bjork, A., and Helm, S.: Prediction of the age of maximum pubertal growth in body height, Angle Orthod. 37: 134-143, 1967. 4. Brown, T., Barrett, M. J., and Grave, K. C.: Facial growth and skeletal maturation at adolescence, Dan. Dent. J. 75: 1121-1222, 1971. 5. Chapman, S. M.: Ossification of the adductor sesamoid and the adolescent growth spurt, Angle Orthod. 42: 236-244, 1972. 6. Chertkow, S., and Fatti, P. L.: The relationship between tooth mineralization and early radiographic evidence of adductor sesamoid calcification, Angle Otthod., October, 1979, 7. Demirjian, A., Goldstein, H., and Tanner, J. M.: A new system of dental age assessment, Hum. Biol. 45: 211-227, 1973. 8. Gam, S. M., and Rohman, C. G.; The adductor sesamoid of the thumb, Am. J. Phys. Anthropol. 20: 297-302, 1962. 9. Greulich, W. W., and Pyle, S. I.: Radiographic atlas of skeletal development of the hand and wrist. ed. 2, Stanford, Calif., 1959, Stanford University Press. 10. Helm, S., Siersback-Nielsen, S., Skieler, V., and Bjork, A: Skeletal maturation of the hand in relation to maximum pubertal growth in body height, Dan. Dent. J. 75: 1223-1234, 1971. 11. Hunter, C. J.: The correlation of facial growth with body height and skeletal maturation at adolescence, Angle Orthod. 36: 44-54, 1966. 12. Lewis, A. B., and Garn, S. M.: The relationship between tooth formation and other maturational factors, Angle Orthod. 30: 70-77, 1960. 13. Maxwell, A. E.: Analysing qualitative data, London, 1975, Chapman & Hall. 14. Meredith, H. V.: Relation between the eruption of selected mandibular permanent teeth and the circumpubertal acceleration in stature, J. Dent. Child. 26: 75-78, 1959. 15. Nanda, R. S.: The rates of growth of several facial components measured from serial cephalometric roentgenograms, AM. J. ORTHOD. 41: 658-673, 1955. 16. Roche, A. F., and Lewis, A. B.: Late growth changes in the cranial base. In Boersma, J. F. (editor): Symposium on development of the basicranium, DHEW Publication No, (NIH) 76-989, Washington, 1976, United States Department of Health, Education and Welfare. 17. Roche. A. F., Roberts, J., and Hammill, V. V.: Skeletal maturity of youths 12-17 years: Vita1 and health statistics. National Health Survey, Series 11, No. 160, 1976. 18. Tanner, J. M., Whitehouse, R. H., Marshall, W. A., Healy, M. J. R., and Goldstein, H.: Assessment of skeletal maturity and prediction of adult height (T.W.2 method), London, 1975, Academic Press. 19. Tobias, P. V.: Some aspects of the biology of the Bantu-speaking African, The Leech 28: 3-12, 1958.