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Skeletal maturation in Indonesian and white children assessed with hand-wrist and cervical vertebrae methods
ORIGINAL ARTICLE
Skeletal maturation in Indonesian and white children assessed with hand-wrist and cervical vertebrae methods Benny M. Soegiharto,a Susan J. Cunningham,b and David R. Molesc London, United Kingdom Introduction: The purpose of this study was to describe the stages of skeletal maturity of Deutero-Malay Indonesian children according to the hand-wrist and cervical vertebrae methods and to compare them with white children. Methods: The study included 2167 patients with hand-wrist radiographs and lateral cephalometric radiographs. Of these, there were 648 Indonesian boys, 303 white boys (age range of boys, 10-17 years), 774 Indonesian girls, and 442 white girls (age range of girls, 8-15 years). The skeletal maturation index (SMI) was used to evaluate the stages of skeletal maturity from hand-wrist radiographs, and the cervical vertebrae maturation (CVM) index was used to evaluate the stages of skeletal maturity from lateral cephalometric radiographs. One observer made all observations, and a repeatability study was undertaken. Results: Box-and-whisker plots were used to show the age distribution on attainment of each maturation stage based on the SMI and CVM. On average, both the SMI and the CVM showed that white children attained each maturation stage about 0.5 to 1 year earlier than their Indonesian peers, although the differences were less obvious in girls than in boys. Multiple regression analysis was used to predict the SMI from the chronologic age. Both the Indonesian and the white boys groups showed a good relationship between predicted SMI and chronologic age (R2 ⫽ 0.728 and 0.739, respectively), as did the Indonesian and white girls groups (R2 ⫽ 0.755 and 0.748, respectively). Further multiple regression analyses used to investigate the differences in the ages of attainment of skeletal development between Indonesian and white subjects indicated that, across the age ranges investigated, on average for a particular age, the white boys were 1 SMI stage ahead of the Indonesian boys, and the white girls were about 0.5 SMI stage ahead of their Indonesian peers. Because the CVM has only 5 categories, it was not considered appropriate to use this form of multiple regression analysis. Conclusions: The findings confirmed marked variations in the chronologic ages for each skeletal maturity stage and also showed differences between the timing of skeletal maturity with both the SMI and the CVM between the sexes and the ethnic groups. These differences should be considered during orthodontic diagnosis and treatment planning. (Am J Orthod Dentofacial Orthop 2008;134: 217-26)
T
he evaluation of craniofacial growth is an essential part of diagnosis and treatment planning in orthodontics, especially when growth modification is needed. Many clinicians believe that orthodontic treatment is more effective if it is started during a period of rapid pubertal growth.1 It has been suggested that growth modification treatment for the maxilla (eg, with
From the UCL-Eastman Dental Institute for Oral Health Care Sciences, London, United Kingdom. a Research graduate; currently lecturer, Faculty of Dentistry, University of Indonesia, Jakarta, Indonesia. b Senior lecturer and honorary consultant, Unit of Orthodontics. c Senior lecturer, Health Services Research. Reprint requests to: Benny M. Soegiharto, Unit of Orthodontics, UCL-Eastman Dental Institute for Oral Health Care Sciences, 256, Grays Inn Road, London WC1X 8LD, United Kingdom; e-mail, [email protected]. Submitted, February 2006; revised and accepted, July 2006. 0889-5406/$34.00 Copyright © 2008 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2006.07.037
protraction headgear) should be started before the peak pubertal growth of the maxilla,2 and growth modification for the mandible (eg, functional appliances) has been shown to be more effective during the peak of mandibular growth rather than before this stage.3-5 Certain parameters have been suggested to identify the stages of growth— chronologic age, dental development, sexual maturation and voice change, and increase in body height. The use of radiographs, such as hand-wrist radiographs, has also been advocated.6,7 Several human growth studies have shown that the timing of the pubertal growth of the craniofacial region is closely related to specific ossification events and stages observed in the hand-wrist area of the skeleton; therefore, hand-wrist radiographs have proved to be a valuable diagnostic tool in orthodontics.6-9 Björk and Helm10 suggested that the MP3Cap stage (the middle phalanx of the third finger has its epiphysis caps the 217
218 Soegiharto, Cunningham, and Moles
diaphysis) was closely related to the timing of the peak pubertal growth spurt. However, there is also criticism about the use of hand-wrist radiographs; some researchers claim that they have limited value for prediction of pubertal growth because the complexity in identification of landmarks can lead to inaccurate predictions. In addition, the child is exposed to additional radiation.11,12 In view of the limitations and disadvantages of hand-wrist radiographs, Lamparski13 introduced a method that uses the cervical vertebral maturation (CVM) index to assess skeletal maturation, and some authors have found it to be effective and clinically reliable for assessing skeletal maturity.14-19 It has been suggested that the peak pubertal growth spurt occurs between stages 2 and 3, when concavity has started to develop on the third vertebrae (stage 2) or also started on the fourth vertebrae (stage 3).17 This method eliminates the need for additional radiographic exposure because the vertebrae are already recorded on most routine lateral cephalometric radiographs. Ethnic and sex variations in the timing of skeletal maturation have also been noted.20-23 Several reports have been published on the use of hand-wrist and cervical vertebrae skeletal development in orthodontics in various ethnic groups.6,24-27 Unfortunately, there is limited information about the skeletal development of many ethnic groups including Indonesian children of Deutero-Malay origin. Therefore, the objectives of this study were to investigate the stages of skeletal maturity of Deutero-Malay Indonesian children by using hand-wrist and cervical vertebrae skeletal development and to compare these findings with white children. The findings of this study will add to the database of information and provide a valid clinical tool for orthodontic diagnosis and treatment planning. MATERIAL AND METHODS
This was a cross-sectional study with hand-wrist and lateral cephalometric radiographs from Indonesian children of Deutero-Malay ethnic origin. The data came from school children in Jakarta, Indonesia, and its vicinity, and the radiographs were taken during routine orthodontic examinations. Data for the white patients were obtained from preexisting radiographs taken as part of routine orthodontic assessment at the Department of Orthodontics, Eastman Dental Center, University of Rochester Medical Center, Rochester, NY. The age ranges were 10 to 17 years for the boys and 8 to 15 years for the girls. These age ranges were
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Table I. Patient distribution based on chronologic age for Indonesian and white groups Indonesian Age (y) Boys 10 11 12 12.5 13 13.5 14 14.5 15 16 17 Total Girls 8 9 9.5 10 10.5 11 11.5 12 12.5 13 14 15 Total
White
n
%
n
%
73 105 53 45 36 50 60 36 96 52 42 648
11.3 16.2 8.2 6.9 5.6 7.7 9.3 5.6 14.8 8.0 6.5 100
35 30 25 29 20 35 19 21 44 28 17 303
11.6 9.9 8.3 9.6 6.6 11.6 6.3 6.9 14.5 9.2 5.6 100
81 51 46 48 45 54 56 65 54 85 108 81 774
10.5 6.6 5.9 6.2 5.8 7.0 7.2 8.4 7.0 11.0 14.0 10.5 100
17 9 10 16 17 26 40 37 44 73 65 88 442
3.8 2.0 2.3 3.6 3.8 5.9 9.0 8.4 10.0 16.5 14.7 19.9 100
selected based on the assumption that girls reach skeletal maturation earlier than boys (Table I).28 Patients were included if they fulfilled the following criteria: (1) Deutero-Malay or white ethnic origin, (2) physically healthy with no relevant medical conditions, (3) Angle Class I molar relationship with normal overjet and overbite, (4) no previous orthodontic treatment, and (5) lateral cephalometric and hand-wrist radiographc taken at the same time with good clarity and contrast. The hand-wrist radiographs were observed in a darkened room, and a black surround was used on the light box to eliminate excess light and facilitate landmark identification. Each radiograph was then classified according to the skeletal maturation index (SMI) as described by Fishman.7 The CVM was assessed by using lateral cephalometric radiographs. Observation was similarly done in a darkened room with a black surround. The outlines of the cervical vertebrae (C2-C4) were traced on 0.003-in thick matte acetate cephalometric tracing paper (GAC International, Bohemia, NY) with a 0.5-mm diameter (2B) mechanical lead pencil. The
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American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table II.
SMI and CVM repeatability results
Ethnic group Indonesian Indonesian White White
Table III.
Sex
Kappa value for SMI
Agreement
Kappa value for CVM
Agreement
Boys Girls Boys Girls
0.75 0.89 0.86 0.82
Substantial Good Good Good
0.85 0.97 0.94 0.95
Good Good Good Good
Patients classified according to the SMI method Age
SMI stage Boys 1 (PP2⫽) 2 (MP3⫽) 3 (MP5⫽) 4 (S) 5 (DP3Cap) 6 (MP3Cap) 7 (MP5Cap) 8 (DP3U) 9 (PP3U) 10 (MP3U) 11 (RU) Girls 1 (PP2⫽) 2 (MP3⫽) 3 (MP5⫽) 4 (S) 5 (DP3Cap) 6 (MP3Cap) 7 (MP5Cap) 8 (DP3U) 9 (PP3U) 10 (MP3U) 11 (RU)
Indonesian patients (n)
%
Mean (y)
126 94 95 54 4 31 102 45 8 72 17
19.4 14.5 14.7 8.3 0.6 4.8 15.7 6.9 1.2 11.1 2.6
102 106 76 70 4 51 117 96 15 116 21
13.2 13.7 9.8 9.0 0.5 6.6 15.1 12.4 1.9 15.0 2.7
Age SD
White patients (n)
%
Mean (y)
SD
11.22 11.95 12.53 13.35 14.28 14.61 14.70 15.28 15.52 16.00 17.35
1.06 1.26 1.07 1.21 1.12 0.95 1.12 0.83 0.83 0.93 0.58
21 26 33 22 21 32 51 27 6 41 23
6.9 8.6 10.9 7.3 6.9 10.6 16.8 8.9 2.0 13.5 7.6
10.66 11.29 12.23 12.20 13.04 13.17 14.54 14.96 16.05 15.72 16.85
0.79 1.13 1.08 1.24 0.81 0.98 1.11 0.88 1.39 1.08 0.90
8.97 9.86 10.76 11.04 11.91 11.77 12.77 13.36 13.99 14.42 15.26
0.84 1.09 1.34 1.22 1.38 0.99 1.11 1.01 1.16 1.01 0.40
18 16 13 39 17 55 56 48 4 91 85
4.1 3.6 2.9 8.8 3.8 12.4 12.7 10.9 0.9 20.6 19.2
8.77 9.92 10.86 11.05 11.33 12.28 12.71 13.25 13.99 14.33 15.27
0.85 1.51 1.19 0.94 0.97 1.03 0.99 0.99 0.98 1.11 0.85
CVM readings were then classified into the stages described by Baccetti et al.17 To establish intraoperator repeatability, 300 subjects (100 Indonesian subjects and 50 white subjects of each sex) were randomly selected for reobservation of both methods used in this study. All observations were repeated within 1 month, and no more than 20 radiographs were observed on any session to minimize errors caused by operator fatigue. STATISTICAL ANALYSIS
The results were analyzed with SPSS for Windows software (version 12.0.1, SPSS UK, Woking, Surrey, United Kingdom). For the repeatability study, Cohen’s kappa statistic was used to assess agreement between the 2 measurements based on categorical variables.
For the main study, box-and-whisker plots were used to summarize the age distribution for each skeletal development stage for both the SMI and the CVM. In addition, multiple regression was used to predict the SMI from the chronologic age, and to investigate whether there was any difference in skeletal maturity in relation to age between the 2 ethnic groups. To predict the SMI from the chronologic age in each sex and ethnic subgroup, the statistical model was: y ⫽ b o ⫹ b1 x ⫹ b2 x 2 where y was the predicted Fishman stage, bo was the constant, b1 and b2 were regression coefficients, x was age, and x2 was age squared. To investigate the differences in the age of attainment of skeletal development between Indonesian and
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American Journal of Orthodontics and Dentofacial Orthopedics August 2008
gender: Boys ethnic group
11
Indonesian White
gender: Boys
10
ethnic group Indonesian
9
White
5
8
4
6
CVM Stage
SMI Stage
7
5
3
4 2
3
2 1
1
10.0
11.0
12.0
13.0
14.0
15.0
16.0
17.0
10.0
11.0
12.0
Age Group
13.0
14.0
15.0
16.0
17.0
Age Group
Fig 1. A box-and-whisker plot of the chronologic age on the attainment of each SMI developmental stage for Indonesian and white boys.
Fig 3. A box-and-whisker plot of the chronologic age on the attainment of each CVM developmental stage for Indonesian and white boys.
gender: Girls ethnic group 11
Indonesian White
gender: Girls
10
ethnic group Indonesian White
5
9
8 4
CVM Stage
SMI Stage
7
6
5
3
4 2
3
2 1
1
8.0
9.0
10.0
11.0
12.0
13.0
14.0
15.0
Age Group
8.0
9.0
10.0
11.0
12.0
13.0
14.0
15.0
Age Group
Fig 2. A box-and-whisker plot of the chronologic age on the attainment of each SMI developmental stage for Indonesian and white girls.
Fig 4. A box-and-whisker plot of the chronologic age on the attainment of each CVM developmental stage for Indonesians and white girls.
white subjects, further multiple regression analyses were undertaken. The earlier models were extended to include a dummy variable to code for ethnicity (0 for Indonesians, 1 for whites).
general, white children tend to develop earlier compared with Indonesians, including the pubertal growth spurt. For example, stage 6 (MP3Cap), which is considered to represent peak pubertal growth, was typically attained at age 13 years in white children, but Indonesian children reached the same stage at 14.5 years. There was an exception for stage 9 (PP3U), when the Indonesians developed slightly earlier. However, few patients were classified into this stage, and the result could be a consequence of random error. Girls (Fig 2) had a similar pattern; the white children reached each developmental stage earlier than
RESULTS
The kappa results for both the SMI and the CVM showed substantial or good intraoperator agreement for both sex and ethnic groups (Table II). Table III and Figure 1 report the distribution of chronologic age on the attainment of each SMI developmental stage for boys in both ethnic groups. In
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Table IV.
Patients classified according to the CVM method Age
CVM stage Boys 1 2 3 4 5 Girls 1 2 3 4 5
Table V.
CVM stage 1 2 3 4 5
Indonesian patients (n)
%
Mean (y)
253 117 159 100 19
39.0 18.1 24.5 15.4 2.9
269 95 226 177 7
34.8 12.3 29.2 22.9 0.9
Age SD
White patients (n)
%
Mean (y)
SD
11.73 12.82 14.76 15.80 17.03
1.24 1.34 1.09 0.99 0.94
72 34 114 66 17
23.8 11.2 37.6 21.8 5.6
11.38 12.44 14.07 15.54 16.84
1.15 1.18 1.34 1.23 1.00
9.69 11.19 12.83 14.15 14.68
1.18 1.39 1.25 1.19 1.03
44 51 125 187 35
10.0 11.5 28.3 42.3 7.9
9.55 11.11 12.58 14.26 15.33
1.35 0.89 1.09 1.29 0.81
Mean chronologic ages in years (SD) and CVM compared with different ethnic groups in previous studies Grave and Townsend18
This study
This study
Aborigines
Indonesians
Whites
Boys
Girls
Boys
Girls
Boys
Girls
10.97 (1.14) 12.08 (0.96) 13.45 (0.90) 14.67 (0.78) 15.62 (0.71)
9.67 (1.06) 10.80 (1.05) 12.17 (1.07) 13.39 (1.10) 14.67 (1.14)
11.73 (1.24) 12.82 (1.34) 14.76 (1.09) 15.80 (0.99) 17.03 (0.94)
9.69 (1.18) 11.19 (1.39) 12.83 (1.25) 14.15 (1.19) 14.68 (1.03)
11.38 (1.15) 12.44 (1.18) 14.07 (1.34) 15.54 (1.23) 16.84 (1.00)
9.55 (1.35) 11.11 (0.89) 12.58 (1.09) 14.26 (1.29) 15.33 (0.81)
the Indonesians. The exception to this was stage 6 (MP3Cap), which was about 6 months earlier in the Indonesian girls (11.5 years), than in their white peers (12 years). The Indonesian girls also reached stage 5 (DP3Cap) at approximately 12.5 years, whereas the white girls reached the same stage at approximately 11 years. However, only a few patients were classified into this stage; thus, the result could be spurious. Skeletal development by using the CVM method17 showed the same trend as the SMI (Table IV). In general, the white children reached each developmental stage earlier than the Indonesians. For example, the white boys reached peak pubertal growth (stage 3) at approximately 14 years, whereas the Indonesians reached it at approximately 14.5 years (Fig 3). Again, the differences in the girls were less obvious than in the boys. The pubertal growth spurt (stage 3) occurred at approximately 12.5 years for white girls and 12.8 years for Indonesian girls (Fig 4). Mean chronologic ages of each CVM stage of the Indonesian and white children were compared with those of Australian Aborigines,18 and the results are reported in Table V. The mean chronologic ages of some SMI stages for Indonesian and white children
were compared with previously published data for various ethnic groups: Australian Aborigines,6 whites, 7 Chinese/Taiwanese,29 Thais,30 and Turkish,31 with the results shown in Table VI. Multiple regression analysis was used to predict SMI from the chronologic age. Both the Indonesian and the white boys showed high R2 values of 0.728 and 0.739, respectively (complete results in Table VII). Figure 5 shows the general trend of the attainment of each SMI stage for both ethnic groups in relation to chronologic age. It shows that, during the pubertal growth spurt period, there were differences between the Indonesian and white children; the white children reached each SMI stage earlier than did the Indonesians. However, about the age of 17 years, the Indonesian children appeared to equalize with the white ones. Both the Indonesian and white girls showed high R2 values (0.755 and 0.748, respectively). Figure 6 illustrates the predicted SMI stage for these girls. It shows that, even though there were differences in the attainment of each SMI stage, with the white girls seeming to develop earlier than the Indonesians, these differences were not as obvious as in the male group. In addition,
222 Soegiharto, Cunningham, and Moles
Table VI.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Mean chronologic age (SD) and SMI compared with different ethnic groups in previous studies Grave and Brown6
Fishman7
Chang et al29
Aborigines
Whites
Chinese/Taiwanese
SMI stage
Boys
Girls
Boys
Girls
Boys
Girls
MP3⫽ S MP3Cap DP3U MP3U
11.2 (1.3) 13.5 (0.9) 14 (0.8) 15.4 (0.7) 16 (0.9)
9.7 (1.0) 11.3 (1.3) 12.4 (1.2) 13.1 (1.0) 14.3 (1.1)
11.68 (1.06) 12.33 (1.09) 13.75 (1.06) 15.11 (1.03) 16.40 (1.00)
10.58 (0.88) 11.22 (1.11) 12.06 (0.96) 13.10 (0.87) 14.77 (0.96)
12.04 (0.94) 13.06 (0.91) 14.07 (0.87) 14.96 (1.00) 15.91 (0.96)
9.8 (1.00) 11.20 (0.80) 12.57 (0.85) 13.45 (1.03) 14.32 (1.05)
gender: Boys Unstandardized Predicted Value (White) age
11
10
95% L CI for fishman individual (White) age
9
S M I S t a g e
95% U CI for fishman individual (White) age
8
7
Unstandardized Predicted Value (Indo) age
6
95% L CI for fishman individual (Indo) age
5
95% U CI for fishman individual (Indo) age
4
3
2
1
10
11
12
13
14
15
16
17
Age Group Fig 5. Predicted SMI stage in relation to chronologic age (Indonesian and white boys).
about age 15, the growth of the Indonesian and the white girls appeared to equalize. In the direct comparisons between ethnic groups, the regression coefficients were 1.001 for boys (95% CI, 0.777-1.226) and 0.494 for girls (95% CI, 0.3050.682), indicating that, across the age ranges investigated, on average for a particular age, the white boys were 1 SMI stage ahead of the Indonesians, and the white girls were approximately 0.5 SMI stage ahead of their Indonesian peers (complete results in Table VIII).
DISCUSSION
The kappa values for the SMI showed substantial to good intraoperator agreement for both sexes and ethnic groups. The results indicated acceptable repeatability for this method. The SMI is an organized and relatively simple way to observe skeletal maturity: it uses 11 anatomic sites on the phalanges, adductor sesamoid, and radius, excluding the carpal bones. The kappa values for the CVM were generally
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American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table VI.
Continued.
Krailassiri et al30
Uysal et al31
This study
This study
Thais
Turks
Indonesians
Whites
Boys
Girls
Boys
Girls
Boys
Girls
Boys
Girls
11.2 (1.5) 11.6 (1.3) 13.2 (1.2) 14.3 (0.8) 15.4 (1.7)
9.7 (1.0) 10.2 (1.2) 11.4 (1.3) 12.6 (1.4) 14.1 (1.5)
12.01 (2.08) 13.05 (2.03) 13.11 (3.01) 15.01 (1.04) 15.05 (2.05)
9.06 (1.04) 11.01 (2.10) 12.03 (1.00) 13.02 (1.01) 13.07 (0.10)
11.95 (1.26) 13.35 (1.21) 14.61 (0.95) 15.28 (0.83) 16.00 (0.93)
9.86 (1.09) 11.04 (1.22) 11.77 (0.99) 13.36 (1.01) 14.42 (1.01)
11.29 (1.13) 12.20 (1.24) 13.17 (0.98) 14.96 (0.88) 15.72 (1.08)
9.92 (1.51) 11.05 (0.94) 12.28 (1.03) 13.25 (0.99) 14.33 (1.11)
gender: Girls Unstandardized Predicted Value (White) age
11
10
95% L CI for fishman individual (White) age
9
S M I S t a g e
95% U CI for fishman individual (White) age
8
7
Unstandardized Predicted Value (Indo) age
6
95% L CI for fishman individual (Indo) age
5
95% U CI for fishman individual (Indo) age
4
3
2
1
8
9
10
11
12
13
14
15
Age Group Fig 6. Predicted SMI stage in relation to chronologic age (Indonesian and white girls).
higher compared with the SMI and also showed good intraoperator agreement for both sexes and ethnic groups. The main advantage of this method is that it requires the observation of only the second to the fourth vertebrae, and this area is visible on most lateral cephalometric radiographs; thus, an additional radiograph is not required. The results of this repeatability study are similar to those of Ballrick et al,32 who found good kappa scores (0.82) with the CVM classification. This study confirmed marked variation in chrono-
logic age for skeletal maturation when observed by both SMI and CVM and therefore confirmed that chronologic age is not a reliable clinical tool to assess a patient’s maturity stage in isolation for diagnosis and treatment planning in orthodontics (Figs 1-4). When the mean chronologic ages of selected SMI stages of the children in this study were compared with published data for other ethnic groups, the Aboriginal boys reached the peak growth spurt half a year earlier than did the Indonesian boys. A similar trend can be
224 Soegiharto, Cunningham, and Moles
Table VII.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Regression analysis results for Indonesian and white subjects Unstandardized coefficient Age (b1)
Constant (b0) Ethnic group Boys Indonesian White Girls Indonesian White
Age squared (b2)
R2
b0
95% CI (lower)
95% CI (upper)
P
b1
95% CI (lower)
95% CI (upper)
P
b2
95% CI (lower)
95% CI (upper)
P
0.728 0.739
⫺3.439 ⫺12.190
⫺8.984 ⫺18.939
2.107 ⫺5.442
0.224 ⬍0.001
⫺0.119 1.410
⫺0.947 0.415
0.708 2.405
0.224 0.006
0.053 ⫺0.006
0.022 ⫺0.042
0.083 0.031
0.001 0.764
0.755 0.748
⫺8.339 ⫺13.097
⫺11.759 ⫺17.654
⫺4.918 ⫺8.54
⬍0.001 ⬍0.001
1.039 1.939
0.448 1.208
1.629 2.670
0.001 0.000
0.011 ⫺0.027
⫺0.014 ⫺0.056
0.035 0.002
0.407 0.068
seen when the Indonesian boys are compared with other Asian (Chinese and Thai) and Turkish children. The Indonesian girls reached their peak growth spurt approximately 0.5 to 1 year earlier compared with the other ethnic groups, except for the Turkish and Thai children. The Turkish girls developed earlier than did the Indonesians, except at the peak pubertal growth spurt stage (stage 6 or MP3Cap); they reached this stage at 12 years rather than 11.5 years for the Indonesians. The Thai girls reached the peak pubertal growth spurt stage 1 year earlier than did the Indonesians. There are few data to compare the mean chronologic age and CVM stage between Indonesian children and other ethnic groups because previous studies used different classifications. Grave and Townsend18 supplied data similar to our study. On average, the girls attained each CVM stage earlier than the boys, regardless of ethnicity. The Aboriginal and white girls reached each CVM stage earlier than did the Indonesians. The Indonesian boys reached each CVM stage typically later compared with the other 2 ethnic groups. When comparing American blacks and whites, Faulkner and Harris33 found that the girls preceded the boys by 1.5 years. Interestingly, in their sample, they found no differences in the timing of skeletal maturation between American blacks and whites. The smaller amount of variation shown in the CVM than in the SMI for both sex groups might be because of fewer categories in the CVM method. Skeletal maturation has been shown to occur in identical and defined stages between ethnic groups.22,34 However, the differences in timing of skeletal maturation between ethnic groups might be due to factors other than genetic differences— eg, environmental conditions, socioeconomic status, nutrition, hygiene conditions, and regional and climatic differences. Persons with a less favorable environment might have delayed skeletal maturation.20-23 Some studies have shown that skeletal maturation in
malnourished children was delayed when compared with healthy children.35,36 Although Indonesia has achieved impressive public health gains in recent decades, child malnutrition remains a serious problem.37 This could be a reason that Indonesians attained each skeletal maturation stage typically later than other ethnic groups. However, these patients were clearly of a social class that could obtain orthodontic treatment and therefore might not represent the whole Indonesian population. Sexual dimorphism in the velocity of growth, the timing of the adolescent growth spurt, overall size, and the attainment age of skeletal maturation are well known.38 On average, girls mature earlier than boys; they reach puberty at approximately 10 years, attain the peak pubertal spurt at 12 years, and reach the end of the growth spurt about 15 years of age. In contrast, boys reach puberty at approximately 12 years, attain the peak pubertal spurt at 14 years, and reach the end of the growth spurt about 17 years.28 Multiple regression analysis was undertaken only for the SMI, not for the CVM. In regression analysis, ideally, a continuous scale is required or, at least, an ordinal scale with a sufficient number of categories. Because the CVM has only 5 categories, it was not considered appropriate to analyze the CVM data in this way. Multiple regression analyses were used to define models that could predict the SMI stage by using chronologic age as the explanatory variable. The variability of the dependent variable is characterized by the R2 value. It is considered to be high for biologic data when it is from 30% to 67%.39 In our study, the results showed that, on average, the R2 values for both sex groups were above 0.7, or 70%. Therefore, perhaps not surprisingly, chronologic age is highly predictive of SMI stage for both ethnic groups. However, in a sample with a broad range of ages, the correlation values tend to be higher than in a sample with a narrower age range. To compare directly the skeletal maturation be-
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Table VIII.
Regression analysis of the differences in the age of attainment of skeletal development between Indonesian and white subjects Unstandardized coefficient Age (b1)
Constant (b0) Sex Boys Girls
R2
b0
95% CI (lower)
95% CI (upper)
0.740 0.774
⫺7.290 ⫺10.432
⫺11.595 ⫺13.014
⫺2.984 ⫺7.849
P 0.001 ⬍0.001
b1
95% CI (lower)
95% CI (upper)
0.482 1.411
⫺0.158 0.976
1.122 1.846
P 0.140 ⬍0.001
*The ethnic group regression coefficient represents the average increased value of the predicted SMI in whites relative to Indonesians.
tween the 2 ethnic groups, further multiple regression analyses were undertaken, and, on average, the white subjects developed earlier by 1 SMI stage than their Indonesian peers, although the difference was less in girls—white girls were approximately 0.5 SMI stage ahead of their Indonesian peers. CONCLUSIONS
This study confirmed the variation in chronologic age for each stage of skeletal maturity. On average, the white children attained each stage of the SMI and the CVM about 0.5 to 1 year earlier than their Indonesian peers, although the differences were less obvious in girls. Our findings showed that there are differences between the timing of skeletal maturity between sexes and ethnic groups. Therefore, these differences should be considered during orthodontic diagnosis and treatment planning. We thank all staff from the Department of Orthodontics, Eastman Dental Center, University of Rochester Medical Center, Rochester, NY (in particular, Stephanos Kyrkanides, Leonard Fishman, and Mary Therese Whelehan) for giving us full access to their patient database for this study. REFERENCES 1. Proffit WR. Treatment timing: effectiveness and efficiency. In: McNamara JA Jr, Kelly KA, editors. Treatment timing: orthodontics in four dimensions. Vol. 39. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 2002. p. 13-24. 2. Baccetti T, Franchi L, McNamara JA. The cervical vertebral maturatioin (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod 2005;11: 119-29. 3. Pancherz H, Hägg U. Dentofacial orthopedics in relation to somatic maturation. Am J Orthod 1985;88:273-87. 4. Baccetti T, Franchi L, Toth LR, McNamara JA. Treatment timing for Twin-block therapy. Am J Orthod Dentofacial Orthop 2000;118:159-70.
5. Faltin K, Faltin RM, Baccetti T, Franchi L, Ghiozzi B, McNamara JA. Long-term effectiveness and treatment timing for bionator therapy. Angle Orthod 2003;73:221-30. 6. Grave KC, Brown T. Skeletal ossification and the adolescent growth spurt. Am J Orthod 1976;69:611-9. 7. Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52:88-112. 8. Bowden BD. Sesamoid bone appearance as an indicator of adolescence. Aust Orthod J 1971;2:242-8. 9. Flores-Mir C, Nebbe B, Major PW. Use of skeletal maturation based on hand-wrist radiographic analysis as a predictor of facial growth: a systematic review. Angle Orthod 2004;74: 118-24. 10. Björk A, Helm S. Prediction of the age of maximum pubertal growth in body height. Angle Orthod 1967;37:134-43. 11. Houston WJB, Miller JC, Tanner JM. Prediction of the timing of the adolescent growth spurt from ossification events in handwrist films. Br J Orthod 1979;6:145-52. 12. Moore RN, Moyer BA, DuBois LM. Skeletal maturation and craniofacial growth. Am J Orthod Dentofacial Orthop 1990;98: 33-40. 13. Lamparski DG. Skeletal age assessment utilizing cervical vertebrae [thesis]. Pittsburgh: University of Pittsburgh; 1972. 14. O’Reilly MT, Yanniello GJ. Mandibular growth changes and maturation of cervical vertebrae. A longitudinal cephalometric study. Angle Orthod 1988;58:179-84. 15. Hassel B, Farman AG. Skeletal maturation evaluation using cervical vertebrae. Am J Orthod Dentofacial Orthop 1995;107: 58-66. 16. Franchi L, Baccetti T, McNamara JA. Mandibular growth as related to cervical vertebral maturation and body height. Am.J Orthod Dentofacial Orthop 2000;118:335-40. 17. Baccetti T, Franchi L, Mc Namara JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod 2002;72:316-23. 18. Grave K, Townsend G. Cervical vertebral maturation as a predictor of the adolescent growth spurt. Aust J Orthod 2003;19: 25-31. 19. Flores-Mir C, Burgess CA, Champney M, Jensen RJ, Pitcher MR, Major PW. Correlation of skeletal maturation stages determined by cervical vertebrae and hand-wrist evaluations. Angle Orthod 2006;76:1-5. 20. Cole AJ, Webb L, Cole TJ. Bone age estimation: a comparison of methods. Br J Radiol 1988;61:683-6. 21. Ontell FK, Ivanovic M, Ablin DS, Barlow TW. Bone age in children of diverse ethnicity. Am J Roentgenol 1996;167:1395-8.
226 Soegiharto, Cunningham, and Moles
Table VIII.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Continued. Unstandardized coefficient Ethnic group (b3)
Age squared (b2) b2
0.030 ⫺0.005
95% CI (lower)
95% CI (upper)
P
b3
95% CI (lower)
95% CI (upper)
P
0.007 ⫺0.023
0.0053 0.012
0.012 0.548
1.001* 0.494*
0.777 0.305
1.226 0.682
⬍0.001 ⬍0.001
22. Schemeling A, Reisinger W, Loreck D, Vendura K, Markus W, Geserick G. Efects of ethnicity on skeletal maturation: consequences for forensic age estimations. Int J Legal Med 2000;113: 253-8. 23. Rogol AD, Roemmich JN, Clark PA. Growth at puberty. J Adolesc Health 2002;31:192-200. 24. Chang HP, Liao CH, Yang YH, Chang HF, Chen KC. Correlation of cervical vertebrae maturation with hand-wrist maturation in children. Kaoshiung J Med Sci 2001;17:29-35. 25. San Román P, Palma JC, Oteo MD, Nevado E. Skeletal maturation determined by cervical vertebrae development. Eur J Orthod 2002;24:303-11. 26. Grave K, Townsend G. Hand-wrist and cervical vertebral maturation indicators: how can these events be used to time Class II treatment? Aust J Orthod 2003;19:33-45. 27. Mitani H, Sato K. Comparison of mandibular growth with other variables during puberty. Angle Orthod 1992;62:217-22. 28. Taranger J, Hägg U. The timing and duration of adolescent growth. Acta Odontol Scand 1980;38:57-67. 29. Chang HP, Wu KM, Chen KC. A cross-sectional study on the skeletal development of the hand and wrist from preadolescence to early adulthood among Chinese in Taiwan. Chin Dent J 1990;9:1-11. 30. Krailassiri S, Anuwongnukroh N, Dechkunakorn S. Relationship between dental calcification stages and skeletal maturity indicators in Thai individuals. Angle Orthod 2002;72:155-66. 31. Uysal T, Sari Z, Ramoglu SI, Basciftci FA. Relationship between dental and skeletal maturity in Turkish subjects. Angle Orthod 2004;74:657-64.
32. Ballrick J, Fields H, Vig KWL, Beck FM, Germak T, Baccetti T, et al. Reliability and validity of cervical vertebral maturation and hand-wrist radiographs. IADR abstract. Available at: http:// iadr.confex.com/iadr/2005Balt/techprogram/abstract_62129.htm. Accessed November 2, 1995. 33. Faulkner CT, Harris EF. Race and sex differences in tempos of cervical vertebral maturation. IADR abstract. Available at: http:// iadr.confex.com/iadr/2004Hawaii/techprogram/abstract_44058. htm. Accessed November 2, 1995. 34. Wingerd J, Peritz E, Sproul A. Race and stature differences in the skeletal maturation of the hand and wrist. Ann Hum Biol 1974;1:201-9. 35. Saxena S, Saxena NB. Skeletal maturation of hands and wrists in normal and malnourished children. Indian J Pediatr 1980; 47:187-91. 36. Gross R, Landfried B, Herman S. Height and weight as a reflection of the nutritional situation of school-aged children working and living in the streets of Jakarta. Soc Sci Med 1996;43:453-8. 37. Waters H, Saadah F, Surbakti S, Heywood P. Weight-for-age malnutrition in Indonesian children, 1992-1999. Int J Epidemiol 2004;33:589-95. 38. Tanner JM, Whitehouse RH, Marubini E, Resele LF. The adolescent growth spurt of boys and girls of the Harpenden Growth Study. Ann Hum Biol 1976;3:109-26. 39. Dibbets JMH, Trotman C, McNamara JA, Van Der Weele LT, Janosky JE. Multiple linear regression as analytical tool in cephalometric studies. Br J Orthod 1997;24:61-6.
Skeletal maturation in Indonesian and white children assessed with hand-wrist and cervical vertebrae methods Benny M. Soegiharto,a Susan J. Cunningham,b and David R. Molesc London, United Kingdom Introduction: The purpose of this study was to describe the stages of skeletal maturity of Deutero-Malay Indonesian children according to the hand-wrist and cervical vertebrae methods and to compare them with white children. Methods: The study included 2167 patients with hand-wrist radiographs and lateral cephalometric radiographs. Of these, there were 648 Indonesian boys, 303 white boys (age range of boys, 10-17 years), 774 Indonesian girls, and 442 white girls (age range of girls, 8-15 years). The skeletal maturation index (SMI) was used to evaluate the stages of skeletal maturity from hand-wrist radiographs, and the cervical vertebrae maturation (CVM) index was used to evaluate the stages of skeletal maturity from lateral cephalometric radiographs. One observer made all observations, and a repeatability study was undertaken. Results: Box-and-whisker plots were used to show the age distribution on attainment of each maturation stage based on the SMI and CVM. On average, both the SMI and the CVM showed that white children attained each maturation stage about 0.5 to 1 year earlier than their Indonesian peers, although the differences were less obvious in girls than in boys. Multiple regression analysis was used to predict the SMI from the chronologic age. Both the Indonesian and the white boys groups showed a good relationship between predicted SMI and chronologic age (R2 ⫽ 0.728 and 0.739, respectively), as did the Indonesian and white girls groups (R2 ⫽ 0.755 and 0.748, respectively). Further multiple regression analyses used to investigate the differences in the ages of attainment of skeletal development between Indonesian and white subjects indicated that, across the age ranges investigated, on average for a particular age, the white boys were 1 SMI stage ahead of the Indonesian boys, and the white girls were about 0.5 SMI stage ahead of their Indonesian peers. Because the CVM has only 5 categories, it was not considered appropriate to use this form of multiple regression analysis. Conclusions: The findings confirmed marked variations in the chronologic ages for each skeletal maturity stage and also showed differences between the timing of skeletal maturity with both the SMI and the CVM between the sexes and the ethnic groups. These differences should be considered during orthodontic diagnosis and treatment planning. (Am J Orthod Dentofacial Orthop 2008;134: 217-26)
T
he evaluation of craniofacial growth is an essential part of diagnosis and treatment planning in orthodontics, especially when growth modification is needed. Many clinicians believe that orthodontic treatment is more effective if it is started during a period of rapid pubertal growth.1 It has been suggested that growth modification treatment for the maxilla (eg, with
From the UCL-Eastman Dental Institute for Oral Health Care Sciences, London, United Kingdom. a Research graduate; currently lecturer, Faculty of Dentistry, University of Indonesia, Jakarta, Indonesia. b Senior lecturer and honorary consultant, Unit of Orthodontics. c Senior lecturer, Health Services Research. Reprint requests to: Benny M. Soegiharto, Unit of Orthodontics, UCL-Eastman Dental Institute for Oral Health Care Sciences, 256, Grays Inn Road, London WC1X 8LD, United Kingdom; e-mail, [email protected]. Submitted, February 2006; revised and accepted, July 2006. 0889-5406/$34.00 Copyright © 2008 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2006.07.037
protraction headgear) should be started before the peak pubertal growth of the maxilla,2 and growth modification for the mandible (eg, functional appliances) has been shown to be more effective during the peak of mandibular growth rather than before this stage.3-5 Certain parameters have been suggested to identify the stages of growth— chronologic age, dental development, sexual maturation and voice change, and increase in body height. The use of radiographs, such as hand-wrist radiographs, has also been advocated.6,7 Several human growth studies have shown that the timing of the pubertal growth of the craniofacial region is closely related to specific ossification events and stages observed in the hand-wrist area of the skeleton; therefore, hand-wrist radiographs have proved to be a valuable diagnostic tool in orthodontics.6-9 Björk and Helm10 suggested that the MP3Cap stage (the middle phalanx of the third finger has its epiphysis caps the 217
218 Soegiharto, Cunningham, and Moles
diaphysis) was closely related to the timing of the peak pubertal growth spurt. However, there is also criticism about the use of hand-wrist radiographs; some researchers claim that they have limited value for prediction of pubertal growth because the complexity in identification of landmarks can lead to inaccurate predictions. In addition, the child is exposed to additional radiation.11,12 In view of the limitations and disadvantages of hand-wrist radiographs, Lamparski13 introduced a method that uses the cervical vertebral maturation (CVM) index to assess skeletal maturation, and some authors have found it to be effective and clinically reliable for assessing skeletal maturity.14-19 It has been suggested that the peak pubertal growth spurt occurs between stages 2 and 3, when concavity has started to develop on the third vertebrae (stage 2) or also started on the fourth vertebrae (stage 3).17 This method eliminates the need for additional radiographic exposure because the vertebrae are already recorded on most routine lateral cephalometric radiographs. Ethnic and sex variations in the timing of skeletal maturation have also been noted.20-23 Several reports have been published on the use of hand-wrist and cervical vertebrae skeletal development in orthodontics in various ethnic groups.6,24-27 Unfortunately, there is limited information about the skeletal development of many ethnic groups including Indonesian children of Deutero-Malay origin. Therefore, the objectives of this study were to investigate the stages of skeletal maturity of Deutero-Malay Indonesian children by using hand-wrist and cervical vertebrae skeletal development and to compare these findings with white children. The findings of this study will add to the database of information and provide a valid clinical tool for orthodontic diagnosis and treatment planning. MATERIAL AND METHODS
This was a cross-sectional study with hand-wrist and lateral cephalometric radiographs from Indonesian children of Deutero-Malay ethnic origin. The data came from school children in Jakarta, Indonesia, and its vicinity, and the radiographs were taken during routine orthodontic examinations. Data for the white patients were obtained from preexisting radiographs taken as part of routine orthodontic assessment at the Department of Orthodontics, Eastman Dental Center, University of Rochester Medical Center, Rochester, NY. The age ranges were 10 to 17 years for the boys and 8 to 15 years for the girls. These age ranges were
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Table I. Patient distribution based on chronologic age for Indonesian and white groups Indonesian Age (y) Boys 10 11 12 12.5 13 13.5 14 14.5 15 16 17 Total Girls 8 9 9.5 10 10.5 11 11.5 12 12.5 13 14 15 Total
White
n
%
n
%
73 105 53 45 36 50 60 36 96 52 42 648
11.3 16.2 8.2 6.9 5.6 7.7 9.3 5.6 14.8 8.0 6.5 100
35 30 25 29 20 35 19 21 44 28 17 303
11.6 9.9 8.3 9.6 6.6 11.6 6.3 6.9 14.5 9.2 5.6 100
81 51 46 48 45 54 56 65 54 85 108 81 774
10.5 6.6 5.9 6.2 5.8 7.0 7.2 8.4 7.0 11.0 14.0 10.5 100
17 9 10 16 17 26 40 37 44 73 65 88 442
3.8 2.0 2.3 3.6 3.8 5.9 9.0 8.4 10.0 16.5 14.7 19.9 100
selected based on the assumption that girls reach skeletal maturation earlier than boys (Table I).28 Patients were included if they fulfilled the following criteria: (1) Deutero-Malay or white ethnic origin, (2) physically healthy with no relevant medical conditions, (3) Angle Class I molar relationship with normal overjet and overbite, (4) no previous orthodontic treatment, and (5) lateral cephalometric and hand-wrist radiographc taken at the same time with good clarity and contrast. The hand-wrist radiographs were observed in a darkened room, and a black surround was used on the light box to eliminate excess light and facilitate landmark identification. Each radiograph was then classified according to the skeletal maturation index (SMI) as described by Fishman.7 The CVM was assessed by using lateral cephalometric radiographs. Observation was similarly done in a darkened room with a black surround. The outlines of the cervical vertebrae (C2-C4) were traced on 0.003-in thick matte acetate cephalometric tracing paper (GAC International, Bohemia, NY) with a 0.5-mm diameter (2B) mechanical lead pencil. The
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American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table II.
SMI and CVM repeatability results
Ethnic group Indonesian Indonesian White White
Table III.
Sex
Kappa value for SMI
Agreement
Kappa value for CVM
Agreement
Boys Girls Boys Girls
0.75 0.89 0.86 0.82
Substantial Good Good Good
0.85 0.97 0.94 0.95
Good Good Good Good
Patients classified according to the SMI method Age
SMI stage Boys 1 (PP2⫽) 2 (MP3⫽) 3 (MP5⫽) 4 (S) 5 (DP3Cap) 6 (MP3Cap) 7 (MP5Cap) 8 (DP3U) 9 (PP3U) 10 (MP3U) 11 (RU) Girls 1 (PP2⫽) 2 (MP3⫽) 3 (MP5⫽) 4 (S) 5 (DP3Cap) 6 (MP3Cap) 7 (MP5Cap) 8 (DP3U) 9 (PP3U) 10 (MP3U) 11 (RU)
Indonesian patients (n)
%
Mean (y)
126 94 95 54 4 31 102 45 8 72 17
19.4 14.5 14.7 8.3 0.6 4.8 15.7 6.9 1.2 11.1 2.6
102 106 76 70 4 51 117 96 15 116 21
13.2 13.7 9.8 9.0 0.5 6.6 15.1 12.4 1.9 15.0 2.7
Age SD
White patients (n)
%
Mean (y)
SD
11.22 11.95 12.53 13.35 14.28 14.61 14.70 15.28 15.52 16.00 17.35
1.06 1.26 1.07 1.21 1.12 0.95 1.12 0.83 0.83 0.93 0.58
21 26 33 22 21 32 51 27 6 41 23
6.9 8.6 10.9 7.3 6.9 10.6 16.8 8.9 2.0 13.5 7.6
10.66 11.29 12.23 12.20 13.04 13.17 14.54 14.96 16.05 15.72 16.85
0.79 1.13 1.08 1.24 0.81 0.98 1.11 0.88 1.39 1.08 0.90
8.97 9.86 10.76 11.04 11.91 11.77 12.77 13.36 13.99 14.42 15.26
0.84 1.09 1.34 1.22 1.38 0.99 1.11 1.01 1.16 1.01 0.40
18 16 13 39 17 55 56 48 4 91 85
4.1 3.6 2.9 8.8 3.8 12.4 12.7 10.9 0.9 20.6 19.2
8.77 9.92 10.86 11.05 11.33 12.28 12.71 13.25 13.99 14.33 15.27
0.85 1.51 1.19 0.94 0.97 1.03 0.99 0.99 0.98 1.11 0.85
CVM readings were then classified into the stages described by Baccetti et al.17 To establish intraoperator repeatability, 300 subjects (100 Indonesian subjects and 50 white subjects of each sex) were randomly selected for reobservation of both methods used in this study. All observations were repeated within 1 month, and no more than 20 radiographs were observed on any session to minimize errors caused by operator fatigue. STATISTICAL ANALYSIS
The results were analyzed with SPSS for Windows software (version 12.0.1, SPSS UK, Woking, Surrey, United Kingdom). For the repeatability study, Cohen’s kappa statistic was used to assess agreement between the 2 measurements based on categorical variables.
For the main study, box-and-whisker plots were used to summarize the age distribution for each skeletal development stage for both the SMI and the CVM. In addition, multiple regression was used to predict the SMI from the chronologic age, and to investigate whether there was any difference in skeletal maturity in relation to age between the 2 ethnic groups. To predict the SMI from the chronologic age in each sex and ethnic subgroup, the statistical model was: y ⫽ b o ⫹ b1 x ⫹ b2 x 2 where y was the predicted Fishman stage, bo was the constant, b1 and b2 were regression coefficients, x was age, and x2 was age squared. To investigate the differences in the age of attainment of skeletal development between Indonesian and
220 Soegiharto, Cunningham, and Moles
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
gender: Boys ethnic group
11
Indonesian White
gender: Boys
10
ethnic group Indonesian
9
White
5
8
4
6
CVM Stage
SMI Stage
7
5
3
4 2
3
2 1
1
10.0
11.0
12.0
13.0
14.0
15.0
16.0
17.0
10.0
11.0
12.0
Age Group
13.0
14.0
15.0
16.0
17.0
Age Group
Fig 1. A box-and-whisker plot of the chronologic age on the attainment of each SMI developmental stage for Indonesian and white boys.
Fig 3. A box-and-whisker plot of the chronologic age on the attainment of each CVM developmental stage for Indonesian and white boys.
gender: Girls ethnic group 11
Indonesian White
gender: Girls
10
ethnic group Indonesian White
5
9
8 4
CVM Stage
SMI Stage
7
6
5
3
4 2
3
2 1
1
8.0
9.0
10.0
11.0
12.0
13.0
14.0
15.0
Age Group
8.0
9.0
10.0
11.0
12.0
13.0
14.0
15.0
Age Group
Fig 2. A box-and-whisker plot of the chronologic age on the attainment of each SMI developmental stage for Indonesian and white girls.
Fig 4. A box-and-whisker plot of the chronologic age on the attainment of each CVM developmental stage for Indonesians and white girls.
white subjects, further multiple regression analyses were undertaken. The earlier models were extended to include a dummy variable to code for ethnicity (0 for Indonesians, 1 for whites).
general, white children tend to develop earlier compared with Indonesians, including the pubertal growth spurt. For example, stage 6 (MP3Cap), which is considered to represent peak pubertal growth, was typically attained at age 13 years in white children, but Indonesian children reached the same stage at 14.5 years. There was an exception for stage 9 (PP3U), when the Indonesians developed slightly earlier. However, few patients were classified into this stage, and the result could be a consequence of random error. Girls (Fig 2) had a similar pattern; the white children reached each developmental stage earlier than
RESULTS
The kappa results for both the SMI and the CVM showed substantial or good intraoperator agreement for both sex and ethnic groups (Table II). Table III and Figure 1 report the distribution of chronologic age on the attainment of each SMI developmental stage for boys in both ethnic groups. In
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American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table IV.
Patients classified according to the CVM method Age
CVM stage Boys 1 2 3 4 5 Girls 1 2 3 4 5
Table V.
CVM stage 1 2 3 4 5
Indonesian patients (n)
%
Mean (y)
253 117 159 100 19
39.0 18.1 24.5 15.4 2.9
269 95 226 177 7
34.8 12.3 29.2 22.9 0.9
Age SD
White patients (n)
%
Mean (y)
SD
11.73 12.82 14.76 15.80 17.03
1.24 1.34 1.09 0.99 0.94
72 34 114 66 17
23.8 11.2 37.6 21.8 5.6
11.38 12.44 14.07 15.54 16.84
1.15 1.18 1.34 1.23 1.00
9.69 11.19 12.83 14.15 14.68
1.18 1.39 1.25 1.19 1.03
44 51 125 187 35
10.0 11.5 28.3 42.3 7.9
9.55 11.11 12.58 14.26 15.33
1.35 0.89 1.09 1.29 0.81
Mean chronologic ages in years (SD) and CVM compared with different ethnic groups in previous studies Grave and Townsend18
This study
This study
Aborigines
Indonesians
Whites
Boys
Girls
Boys
Girls
Boys
Girls
10.97 (1.14) 12.08 (0.96) 13.45 (0.90) 14.67 (0.78) 15.62 (0.71)
9.67 (1.06) 10.80 (1.05) 12.17 (1.07) 13.39 (1.10) 14.67 (1.14)
11.73 (1.24) 12.82 (1.34) 14.76 (1.09) 15.80 (0.99) 17.03 (0.94)
9.69 (1.18) 11.19 (1.39) 12.83 (1.25) 14.15 (1.19) 14.68 (1.03)
11.38 (1.15) 12.44 (1.18) 14.07 (1.34) 15.54 (1.23) 16.84 (1.00)
9.55 (1.35) 11.11 (0.89) 12.58 (1.09) 14.26 (1.29) 15.33 (0.81)
the Indonesians. The exception to this was stage 6 (MP3Cap), which was about 6 months earlier in the Indonesian girls (11.5 years), than in their white peers (12 years). The Indonesian girls also reached stage 5 (DP3Cap) at approximately 12.5 years, whereas the white girls reached the same stage at approximately 11 years. However, only a few patients were classified into this stage; thus, the result could be spurious. Skeletal development by using the CVM method17 showed the same trend as the SMI (Table IV). In general, the white children reached each developmental stage earlier than the Indonesians. For example, the white boys reached peak pubertal growth (stage 3) at approximately 14 years, whereas the Indonesians reached it at approximately 14.5 years (Fig 3). Again, the differences in the girls were less obvious than in the boys. The pubertal growth spurt (stage 3) occurred at approximately 12.5 years for white girls and 12.8 years for Indonesian girls (Fig 4). Mean chronologic ages of each CVM stage of the Indonesian and white children were compared with those of Australian Aborigines,18 and the results are reported in Table V. The mean chronologic ages of some SMI stages for Indonesian and white children
were compared with previously published data for various ethnic groups: Australian Aborigines,6 whites, 7 Chinese/Taiwanese,29 Thais,30 and Turkish,31 with the results shown in Table VI. Multiple regression analysis was used to predict SMI from the chronologic age. Both the Indonesian and the white boys showed high R2 values of 0.728 and 0.739, respectively (complete results in Table VII). Figure 5 shows the general trend of the attainment of each SMI stage for both ethnic groups in relation to chronologic age. It shows that, during the pubertal growth spurt period, there were differences between the Indonesian and white children; the white children reached each SMI stage earlier than did the Indonesians. However, about the age of 17 years, the Indonesian children appeared to equalize with the white ones. Both the Indonesian and white girls showed high R2 values (0.755 and 0.748, respectively). Figure 6 illustrates the predicted SMI stage for these girls. It shows that, even though there were differences in the attainment of each SMI stage, with the white girls seeming to develop earlier than the Indonesians, these differences were not as obvious as in the male group. In addition,
222 Soegiharto, Cunningham, and Moles
Table VI.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Mean chronologic age (SD) and SMI compared with different ethnic groups in previous studies Grave and Brown6
Fishman7
Chang et al29
Aborigines
Whites
Chinese/Taiwanese
SMI stage
Boys
Girls
Boys
Girls
Boys
Girls
MP3⫽ S MP3Cap DP3U MP3U
11.2 (1.3) 13.5 (0.9) 14 (0.8) 15.4 (0.7) 16 (0.9)
9.7 (1.0) 11.3 (1.3) 12.4 (1.2) 13.1 (1.0) 14.3 (1.1)
11.68 (1.06) 12.33 (1.09) 13.75 (1.06) 15.11 (1.03) 16.40 (1.00)
10.58 (0.88) 11.22 (1.11) 12.06 (0.96) 13.10 (0.87) 14.77 (0.96)
12.04 (0.94) 13.06 (0.91) 14.07 (0.87) 14.96 (1.00) 15.91 (0.96)
9.8 (1.00) 11.20 (0.80) 12.57 (0.85) 13.45 (1.03) 14.32 (1.05)
gender: Boys Unstandardized Predicted Value (White) age
11
10
95% L CI for fishman individual (White) age
9
S M I S t a g e
95% U CI for fishman individual (White) age
8
7
Unstandardized Predicted Value (Indo) age
6
95% L CI for fishman individual (Indo) age
5
95% U CI for fishman individual (Indo) age
4
3
2
1
10
11
12
13
14
15
16
17
Age Group Fig 5. Predicted SMI stage in relation to chronologic age (Indonesian and white boys).
about age 15, the growth of the Indonesian and the white girls appeared to equalize. In the direct comparisons between ethnic groups, the regression coefficients were 1.001 for boys (95% CI, 0.777-1.226) and 0.494 for girls (95% CI, 0.3050.682), indicating that, across the age ranges investigated, on average for a particular age, the white boys were 1 SMI stage ahead of the Indonesians, and the white girls were approximately 0.5 SMI stage ahead of their Indonesian peers (complete results in Table VIII).
DISCUSSION
The kappa values for the SMI showed substantial to good intraoperator agreement for both sexes and ethnic groups. The results indicated acceptable repeatability for this method. The SMI is an organized and relatively simple way to observe skeletal maturity: it uses 11 anatomic sites on the phalanges, adductor sesamoid, and radius, excluding the carpal bones. The kappa values for the CVM were generally
Soegiharto, Cunningham, and Moles 223
American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table VI.
Continued.
Krailassiri et al30
Uysal et al31
This study
This study
Thais
Turks
Indonesians
Whites
Boys
Girls
Boys
Girls
Boys
Girls
Boys
Girls
11.2 (1.5) 11.6 (1.3) 13.2 (1.2) 14.3 (0.8) 15.4 (1.7)
9.7 (1.0) 10.2 (1.2) 11.4 (1.3) 12.6 (1.4) 14.1 (1.5)
12.01 (2.08) 13.05 (2.03) 13.11 (3.01) 15.01 (1.04) 15.05 (2.05)
9.06 (1.04) 11.01 (2.10) 12.03 (1.00) 13.02 (1.01) 13.07 (0.10)
11.95 (1.26) 13.35 (1.21) 14.61 (0.95) 15.28 (0.83) 16.00 (0.93)
9.86 (1.09) 11.04 (1.22) 11.77 (0.99) 13.36 (1.01) 14.42 (1.01)
11.29 (1.13) 12.20 (1.24) 13.17 (0.98) 14.96 (0.88) 15.72 (1.08)
9.92 (1.51) 11.05 (0.94) 12.28 (1.03) 13.25 (0.99) 14.33 (1.11)
gender: Girls Unstandardized Predicted Value (White) age
11
10
95% L CI for fishman individual (White) age
9
S M I S t a g e
95% U CI for fishman individual (White) age
8
7
Unstandardized Predicted Value (Indo) age
6
95% L CI for fishman individual (Indo) age
5
95% U CI for fishman individual (Indo) age
4
3
2
1
8
9
10
11
12
13
14
15
Age Group Fig 6. Predicted SMI stage in relation to chronologic age (Indonesian and white girls).
higher compared with the SMI and also showed good intraoperator agreement for both sexes and ethnic groups. The main advantage of this method is that it requires the observation of only the second to the fourth vertebrae, and this area is visible on most lateral cephalometric radiographs; thus, an additional radiograph is not required. The results of this repeatability study are similar to those of Ballrick et al,32 who found good kappa scores (0.82) with the CVM classification. This study confirmed marked variation in chrono-
logic age for skeletal maturation when observed by both SMI and CVM and therefore confirmed that chronologic age is not a reliable clinical tool to assess a patient’s maturity stage in isolation for diagnosis and treatment planning in orthodontics (Figs 1-4). When the mean chronologic ages of selected SMI stages of the children in this study were compared with published data for other ethnic groups, the Aboriginal boys reached the peak growth spurt half a year earlier than did the Indonesian boys. A similar trend can be
224 Soegiharto, Cunningham, and Moles
Table VII.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Regression analysis results for Indonesian and white subjects Unstandardized coefficient Age (b1)
Constant (b0) Ethnic group Boys Indonesian White Girls Indonesian White
Age squared (b2)
R2
b0
95% CI (lower)
95% CI (upper)
P
b1
95% CI (lower)
95% CI (upper)
P
b2
95% CI (lower)
95% CI (upper)
P
0.728 0.739
⫺3.439 ⫺12.190
⫺8.984 ⫺18.939
2.107 ⫺5.442
0.224 ⬍0.001
⫺0.119 1.410
⫺0.947 0.415
0.708 2.405
0.224 0.006
0.053 ⫺0.006
0.022 ⫺0.042
0.083 0.031
0.001 0.764
0.755 0.748
⫺8.339 ⫺13.097
⫺11.759 ⫺17.654
⫺4.918 ⫺8.54
⬍0.001 ⬍0.001
1.039 1.939
0.448 1.208
1.629 2.670
0.001 0.000
0.011 ⫺0.027
⫺0.014 ⫺0.056
0.035 0.002
0.407 0.068
seen when the Indonesian boys are compared with other Asian (Chinese and Thai) and Turkish children. The Indonesian girls reached their peak growth spurt approximately 0.5 to 1 year earlier compared with the other ethnic groups, except for the Turkish and Thai children. The Turkish girls developed earlier than did the Indonesians, except at the peak pubertal growth spurt stage (stage 6 or MP3Cap); they reached this stage at 12 years rather than 11.5 years for the Indonesians. The Thai girls reached the peak pubertal growth spurt stage 1 year earlier than did the Indonesians. There are few data to compare the mean chronologic age and CVM stage between Indonesian children and other ethnic groups because previous studies used different classifications. Grave and Townsend18 supplied data similar to our study. On average, the girls attained each CVM stage earlier than the boys, regardless of ethnicity. The Aboriginal and white girls reached each CVM stage earlier than did the Indonesians. The Indonesian boys reached each CVM stage typically later compared with the other 2 ethnic groups. When comparing American blacks and whites, Faulkner and Harris33 found that the girls preceded the boys by 1.5 years. Interestingly, in their sample, they found no differences in the timing of skeletal maturation between American blacks and whites. The smaller amount of variation shown in the CVM than in the SMI for both sex groups might be because of fewer categories in the CVM method. Skeletal maturation has been shown to occur in identical and defined stages between ethnic groups.22,34 However, the differences in timing of skeletal maturation between ethnic groups might be due to factors other than genetic differences— eg, environmental conditions, socioeconomic status, nutrition, hygiene conditions, and regional and climatic differences. Persons with a less favorable environment might have delayed skeletal maturation.20-23 Some studies have shown that skeletal maturation in
malnourished children was delayed when compared with healthy children.35,36 Although Indonesia has achieved impressive public health gains in recent decades, child malnutrition remains a serious problem.37 This could be a reason that Indonesians attained each skeletal maturation stage typically later than other ethnic groups. However, these patients were clearly of a social class that could obtain orthodontic treatment and therefore might not represent the whole Indonesian population. Sexual dimorphism in the velocity of growth, the timing of the adolescent growth spurt, overall size, and the attainment age of skeletal maturation are well known.38 On average, girls mature earlier than boys; they reach puberty at approximately 10 years, attain the peak pubertal spurt at 12 years, and reach the end of the growth spurt about 15 years of age. In contrast, boys reach puberty at approximately 12 years, attain the peak pubertal spurt at 14 years, and reach the end of the growth spurt about 17 years.28 Multiple regression analysis was undertaken only for the SMI, not for the CVM. In regression analysis, ideally, a continuous scale is required or, at least, an ordinal scale with a sufficient number of categories. Because the CVM has only 5 categories, it was not considered appropriate to analyze the CVM data in this way. Multiple regression analyses were used to define models that could predict the SMI stage by using chronologic age as the explanatory variable. The variability of the dependent variable is characterized by the R2 value. It is considered to be high for biologic data when it is from 30% to 67%.39 In our study, the results showed that, on average, the R2 values for both sex groups were above 0.7, or 70%. Therefore, perhaps not surprisingly, chronologic age is highly predictive of SMI stage for both ethnic groups. However, in a sample with a broad range of ages, the correlation values tend to be higher than in a sample with a narrower age range. To compare directly the skeletal maturation be-
Soegiharto, Cunningham, and Moles 225
American Journal of Orthodontics and Dentofacial Orthopedics Volume 134, Number 2
Table VIII.
Regression analysis of the differences in the age of attainment of skeletal development between Indonesian and white subjects Unstandardized coefficient Age (b1)
Constant (b0) Sex Boys Girls
R2
b0
95% CI (lower)
95% CI (upper)
0.740 0.774
⫺7.290 ⫺10.432
⫺11.595 ⫺13.014
⫺2.984 ⫺7.849
P 0.001 ⬍0.001
b1
95% CI (lower)
95% CI (upper)
0.482 1.411
⫺0.158 0.976
1.122 1.846
P 0.140 ⬍0.001
*The ethnic group regression coefficient represents the average increased value of the predicted SMI in whites relative to Indonesians.
tween the 2 ethnic groups, further multiple regression analyses were undertaken, and, on average, the white subjects developed earlier by 1 SMI stage than their Indonesian peers, although the difference was less in girls—white girls were approximately 0.5 SMI stage ahead of their Indonesian peers. CONCLUSIONS
This study confirmed the variation in chronologic age for each stage of skeletal maturity. On average, the white children attained each stage of the SMI and the CVM about 0.5 to 1 year earlier than their Indonesian peers, although the differences were less obvious in girls. Our findings showed that there are differences between the timing of skeletal maturity between sexes and ethnic groups. Therefore, these differences should be considered during orthodontic diagnosis and treatment planning. We thank all staff from the Department of Orthodontics, Eastman Dental Center, University of Rochester Medical Center, Rochester, NY (in particular, Stephanos Kyrkanides, Leonard Fishman, and Mary Therese Whelehan) for giving us full access to their patient database for this study. REFERENCES 1. Proffit WR. Treatment timing: effectiveness and efficiency. In: McNamara JA Jr, Kelly KA, editors. Treatment timing: orthodontics in four dimensions. Vol. 39. Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development; University of Michigan; 2002. p. 13-24. 2. Baccetti T, Franchi L, McNamara JA. The cervical vertebral maturatioin (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod 2005;11: 119-29. 3. Pancherz H, Hägg U. Dentofacial orthopedics in relation to somatic maturation. Am J Orthod 1985;88:273-87. 4. Baccetti T, Franchi L, Toth LR, McNamara JA. Treatment timing for Twin-block therapy. Am J Orthod Dentofacial Orthop 2000;118:159-70.
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226 Soegiharto, Cunningham, and Moles
Table VIII.
American Journal of Orthodontics and Dentofacial Orthopedics August 2008
Continued. Unstandardized coefficient Ethnic group (b3)
Age squared (b2) b2
0.030 ⫺0.005
95% CI (lower)
95% CI (upper)
P
b3
95% CI (lower)
95% CI (upper)
P
0.007 ⫺0.023
0.0053 0.012
0.012 0.548
1.001* 0.494*
0.777 0.305
1.226 0.682
⬍0.001 ⬍0.001
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