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Assessment of bone ages: Is the Greulich-Pyle method sufficient for Turkish boys?

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Assessment of bone ages: Is the Greulich-Pyle method sufficient for Turkish boys?

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The Greulich-Pyle (GP) Atlas of skeletal maturation has been prepared in white children who born between 1917 and 1942 in the USA, and is frequently used for assessment of skeletal maturity. In this study, we investigated whether or not the GP method is sufficient for Turkish children for the determination of the skeletal age. Plain radiographies of left hands and wrists of 225 healthy boys between 7 and 17 years of age were taken. Pubic hair (PH) stages of boys were determined by using the Tanner criteria. Mean chronological ages and mean skeletal ages according to GP Atlas were compared for each age groups and each PH stage. Mean skeletal ages were delayed 0.61, 0.72, 0.54, 0.39, 0.25, 0.39, and 0.32 years than the mean chronological ages in the 7-13 years age groups, respectively, and advanced 0.13, 0.01, 0.89, and 0.52 years in the 14-17 years age groups. In PH stages 1, 2, and 3, mean skeletal ages were delayed 0.67, 0.51 and 0.40 years than the mean chronological ages, respectively. In PH stages 4 and 5, mean skeletal ages were advanced 0.66 and 0.76 years than mean chronological ages. The results suggest that Turkish boys may have a different tempo of skeletal maturation during pubertal development from that of American children which GP standards were derived. Therefore, GP Atlas is not completely applicable to Turkish boys but can be used with some modification.
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The degree of skeletal development is a reflection of the
degree of physiological maturation of a subject.1,2 The
importance of bone ages in evaluating an adolescent’s
physical development was shown to be as important as the
chronological ages.3In addition, the determination of skeletal
age indicates how much growth remains for a child and
allows the prediction of final height.1Also, the assessment
of skeletal maturity is an important method in the evaluation,
follow up and the timing of therapy of children with growth
disorders such as constitutional growth retardation and
growth hormone deficiency, and endocrinological diseases
such as hypothyroidism, congenital adrenal hyperplasia and
precocious puberty.4–6
Although the newly developed ultrasonographic method
promises to permit a safe and cost-effective assessment of
skeletal age, Castriota-Scanderbeg et al. reported that its low
accuracy makes it currently unsuitable for clinical use.7
Therefore, radiographic methods maintain their importance.
Although there are some differences in socioeconomic status
and genetic constitution among the populations from which
these standards were derived and the Turkish population, the
Greulich-Pyle (GP) Atlas8of skeletal maturation is frequently
used. It is used for the assessment of skeletal maturity in
Turkey, because of the simplicity and applicability, and the
absence of an atlas for Turkish children.9,10 In this study, we
investigated to what extent GP method is suitable for
assessment of skeletal maturity of Turkish children.
Methods
The study group consisted of 225 healthy boys aged between
7 and 17 years living in Sanliurfa City, in the south-east
region of Turkey. After obtaining informed consent, a
pediatrician examined them in order to determine whether
Pediatrics International (2001) 43, 662–665
Original Article
Assessment of bone ages: Is the Greulich-Pyle method sufficient for
Turkish boys?
AHMET KOC,1MUSTAFA KARAOGLANOGLU,2MURAT ERDOGAN,2MUSTAFA KOSECIK1
AND YASAR CESUR3
Departments of 1Pediatrics and 2Radiology, Faculty of Medicine, Harran University, Sanliurfa,
3Department of Pediatrics, Endocrinology Unit, Faculty of Medicine, Hacettepe University, Ankara,
Turkey
Abstract BBaacckkggrroouunndd: The Greulich-Pyle (GP) Atlas of skeletal maturation has been prepared in white children who
born between 1917 and 1942 in the USA, and is frequently used for assessment of skeletal maturity. In this
study, we investigated whether or not the GP method is sufficient for Turkish children for the determination
of the skeletal age.
MMeetthhooddss: Plain radiographies of left hands and wrists of 225 healthy boys between 7 and 17 years of age
were taken. Pubic hair (PH) stages of boys were determined by using the Tanner criteria. Mean chronological
ages and mean skeletal ages according to GP Atlas were compared for each age groups and each PH stage.
RReessuullttss: Mean skeletal ages were delayed 0.61, 0.72, 0.54, 0.39, 0.25, 0.39, and 0.32 years than the mean
chronological ages in the 7–13 years age groups, respectively, and advanced 0.13, 0.01, 0.89, and 0.52 years
in the 14–17 years age groups. In PH stages 1, 2, and 3, mean skeletal ages were delayed 0.67, 0.51 and
0.40 years than the mean chronological ages, respectively. In PH stages 4 and 5, mean skeletal ages were
advanced 0.66 and 0.76 years than mean chronological ages.
CCoonncclluussiioonn: The results suggest that Turkish boys may have a different tempo of skeletal maturation during
pubertal development from that of American children which GP standards were derived. Therefore, GP Atlas
is not completely applicable to Turkish boys but can be used with some modification.
Key words bone age, chronological age, pubic hair stage, radiography, skeletal maturation.
Correspondence: Dr Ahmet Koc, Harran University Faculty of
Medicine, Research Hospital, Department of Pediatrics, 63 100
Sanliurfa, Turkey. Email: ahmetkoc1@hotmail.com
Received 16 August 2000; revised 19 April 2001; accepted
25 May 2001.
they had any diseases that could effect biological develop-
ment and maturity. Their weight and heights were measured.
The boys whose weight and height were smaller than third
percentiles and greater than 97th percentiles according to
weight and height standards for Turkish Children developed
by Neyzi et al.11 and children with chronic disease were
excluded from the investigation. Genital examinations of all
the students were performed by the same pediatrician, and
the Tanner criteria were applied for the determination of
pubic hair (PH) stage.11
The conventional roentgenograms of left hands and wrists
were taken and skeletal ages were rated by using the GP
Atlas8by two radiologists and one pediatrician separately,
without any knowledge about the children’s chronological
ages. The average of the three results was accepted as the
bone ages of children. The wrist roentgenograms were
compared with the GP Atlas and the age of the closest
picture was taken as bone age of the film. If the bone age of
the film was between the age of two pictures, but not
appropriate to each picture, the average ages of two pictures
were accepted as the film bone age.
Mean chronological and skeletal ages of boys in each age
groups were compared with Wilcoxon signed ranks test, a
non-parametric test. Children were also divided in five
groups according to PH stages. Mean chronological ages of
each group were compared with bone ages by using
Wilcoxon signed ranks test.
Results
Mean chronological and skeletal ages of children according
to age groups are given in Table 1 and shown in Fig. 1. In
the 7–13 years age group, mean skeletal ages were delayed
0.61, 0.72, 0.54, 0.39, 0.25, 0.39, and 0.32 years than mean
chronological ages, respectively (P=0.003, P=0.023,
P=0.053, P=0.045, P=0.204, P=0.021 and P=0.162).
In the 14–17 years age group, mean skeletal ages were
advanced 0.13, 0.01, 0.89, and 0.52 years than mean chrono-
logical ages, respectively (P=0.435, P=0.913, P=0.004,
and P=0.144).
The number of children and mean chronological and
skeletal ages according to PH stages are shown in Table 2. In
the PH 1, PH 2 and PH 3 groups, mean skeletal ages were
0.67, 0.51 and 0.40 years delayed than the mean chrono-
logical ages, respectively (P<0.001, P=0.003 and P=0.015).
In the PH 4 and PH 5 groups, mean skeletal ages were 0.66
and 0.76 years advanced than the mean chronological ages
(P<0.001 and P<0.001). Although these results were
Assessment of bone ages by using GP Atlas 663
Table 1 Mean chronological and skeletal ages of boys according to age group
Age groups nMean Mean Differences zP-value
chronological ages skeletal ages (years~SD)
(years~SD) (years~SD)
7 11 7.0~0.24 6.39~0.75 – 0.61~0.59 2.934 0.003
8 14 8.0~0.24 7.28~1.1 – 0.72~0.91 2.272 0.023
9 15 8.99~0.23 8.45~1.16 0.54~1.02 1.931 0.053
10 28 9.99~0.22 9.60~0.98 – 0.39~0.88 2.005 0.045
11 20 11.05~0.24 10.80~0.69 – 0.25~0.72 1.272 0.204
12 30 12.02~0.23 11.63~0.84 – 0.39~0.87 2.305 0.021
13 42 13.07~0.25 12.75~1.35 – 0.32~1.31 1.400 0.162
14 30 14.05~0.24 14.18~1.23 +0.13~1.24 0.782 0.435
15 18 15.05~0.24 15.06~1.20 +0.01~1.04 0.109 0.913
16 13 15.99~0.22 16.88~0.86 +0.89~0.75 2.902 0.004
17 4 16.98~0.17 17.50~0.58 +0.52~0.51 1.461 0.144
Fig. 1 The distribution of chronological ages and skeletal ages
according to the Greulich-Pyle atlas for each age group. (),
chronologic age; ( ), skeletal age.
statistically significant, the mean differences were not more
than two standard deviations of GP standards.
Discussion
The onset or progress of pubertal development may show
striking variability in various populations and it may be
affected by many factors such as socioeconomic, genetic,
racial and environmental factors.1,9,13 Therefore, it is
expected that there should be some differences of skeletal
maturation among various populations.14–16
The GP Atlas has been prepared in white children from a
high socioeconomic level, who were born between 1917 and
1942, in the USA.8,14 With the increased realization (in the
mid-1950s) that medically unnecessary radiation should be
avoided, serial roentgen examinations of study populations
were discontinued and later studies of skeletal maturation
have become cross-sectional.4
In the same geographic area from which the GP standards
originated, Loder et al. reported that black girls were
skeletally advanced by 0.4–0.7 years, except during middle
childhood, and white boys were skeletally delayed during
middle childhood by 0.9 years and late childhood by
0.4 years, but they were advanced during the adolescent
years by 0.5 years according to the GP Atlas.14 While
Vignolo et al. reported that the modified GP Atlas was
suitable for Italian population, Wenzel et al. reported that
skeletal ages by using GP Atlas showed some major
deviations at and after puberty in Austrian children,
especially in boys.17,18 In the Pakistani study by Shaikh et al.
the mean skeletal age of males from 8 to 15 years and
females from 8 to 13 years were 1 year and 0.5 years
retarded than the GP standards, respectively.19 However,
males after 15 years and females after 13 years have been
found advanced in their skeletal age.
As shown in Tables 1,2 and Fig. 1, there were important
differences among our cases’ mean chronological ages and
skeletal ages according to the GP Atlas. In prepubertal (PH
1), and early pubertal periods (PH 2, PH 3), mean skeletal
ages were statistically delayed than the mean chronological
ages. In contrast, mean skeletal ages were 0.66 and 0.76 years
advanced than mean chronological ages in PH 4 and PH 5
stages, respectively. These differences were also statistically
important.
Racial, socioeconomic and environmental differences
between Turkish children and the children’s group that the
GP Atlas was derived may cause differences in sexual
development and skeletal maturation. In the Turkish study
by Kinik et al. the mean skeletal ages by using GP Atlas
were 0.76 and 0.43 years delayed than the mean chrono-
logical ages in PH 2 and PH 3 groups, respectively.9In the
PH 4 and PH 5 groups, mean skeletal ages were 0.06 and
0.44 years advanced than mean chronological ages, respec-
tively. Kinik et al. also reported that their study group’s
mean skeletal ages were 0.6 years delayed in the PH 2 and
PH 3 groups, and 0.2 years and 0.9 years advanced in the
PH 4 and PH 5 groups when compared to that in Waaler et
al. study.9,20 These differences have been explained by racial,
genetic and environmental factors and their effects. Early
and late pubertal periods’ results of the present study and the
Kinik et al. study were similar; mean skeletal ages according
to GP were delayed in early pubertal periods and advanced
in late pubertal periods in each of the studies.9These results
indicate that Turkish children may have a different rhythm
of skeletal maturation during pubertal development from that
of American children from whom GP standards were derived.
When the results of the previous and this study are
evaluated in combination, we believe that some modification
of the GP atlas for each population, as well as the Turkish
population, may be necessary both for better results and to
minimize the mistakes.
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Table 2 Mean chronological and skeletal ages according to pubic hair stage
Pubic hair stages No Chronological ages Skeletal ages Differences zP-value
(years~SD) (years~SD) (years~SD)
PH 1 73 9.37~1.70 8.70~1.86 0.67~1.08 5.053 <0.001
PH 2 61 11.95~1.34 11.44~1.31 – 0.51~1.12 2.945 =0.003
PH 3 36 13.22~1.02 12.82~1.34 – 0.40~0.04 2.428 =0.015
PH 4 33 14.31~1.04 14.97~1.20 +0.66~0.86 3.808 <0.001
PH 5 22 15.60~0.98 16.37~1.08 +0.76~0.60 3.910 <0.001
PH, pubic hair.
Assessment of bone ages by using GP Atlas 665
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Skeletal maturity was assessed in 637 Austrian children from 7 to 16 years of age. The Greulich-Pyle and the Tanner-Whitehouse-2 (RUS and TW 20-bone) methods were used. The GP ages showed some major deviations at and after puberty, especially in boys. The RUS and 20-bone ages conformed more closely to the standards although a general advancement in RUS ages was seen in girls after the age of 10½. A similar pattern in RUS ages has been reported for other populations and may indicate a secular trend. Bei 637 österreichischen Kindern des Alters 7–16 Jahren wurde die Skelettreife bestimmt. Die Methoden Greulich-Pyle und Tanner-Whitehouse-2 (RUS und TW 20-Knochen) wurden benutzt. Die GP-Alter zeigten zur und nach der Pubertät einige größere Abweichungen, besonders bei Knaben. Die RUS- und 20-Knochen-Alter stimmten mit den Standards enger überein, obwohl ein allgemeiner Vorsprung im RUS-Alter bei Mädchen nach dem Alter 10½ gefunden wurde. Eine ähnliche Verteilung der RUS-Alter wurde für andere Bevölkerungen berichtet, was einen Hinweis auf einen säkularen Trend bedeuten könnte. La maturité osseuse a été établie chez 637 enfants autrichiens de 7 à 16 ans d'âge. Les méthodes de Greulich-Pyle et de Tanner-Whitehouse-2 (RUS et TW 20 os) ont été employées. Les âges GP montraient quelques déviations majeures à et après la puberté, particulièrement chez les garçons. Les âges RUS et 20 os s'accordaient plus étroitement aux normes quoiqu'une précocité générale en âges RUS soit constatée chez les filles après l'âge de 10 ans et demi. Une configuration semblable des âges RUS a été rapportée pour d'autres populations et peut indiquer une tendance séculaire.
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Since the end of the 2nd World War, Japan has seen quite rapid socioeconomical development. With this development the physical size of Japanese children has increased, but the final size, especially the stature, is still shorter than that of Americans or Europeans. Bone maturation velocities were compared among Japanese and Chinese children and adolescents aged 7 to 18 (in 1986) and English TW2-subjects, using the TW2 method. Asian children and adolescents may have a different tempo of skeletal maturation during pubertal growth from that of English children and adolescents. This, probably genetic, difference in the tempo of skeletal maturation, especially that of RUS, between Japanese and English during pubertal growth may be one of the main causes of the final difference in the stature of the two groups.
Article
Normal pubertal development is characterized by major physical alterations: sexual maturation, changes in body composition, and rapid skeletal growth. Breast development is the first manifestation of puberty in approximately 85% of girls; the normal age for initial breast development is 8 to 13 years. Menarche generally occurs within 2 years of the onset of breast development, with a mean age in American girls of 12.8 years. In boys, the first manifestation of puberty is testicular enlargement; the normal age for initial signs of puberty is 9 to 14 years in males. Pubic hair in boys generally appears 18 to 24 months after the onset of testicular growth and is often conceived as the initial marker of sexual maturation by male adolescents. Skeletal growth is one of the most striking characteristics of puberty. Linear-growth velocity begins to increase in males at genital stage III and pubic-hair stage II, but peak height velocity is not attained until age 14 years in boys and 12 years in girls. Lean body mass, which primarily reflects muscle mass, begins to increase during early puberty in both boys and girls. Fat mass increases during the late stages of puberty in girls. Sex differences in the adolescent growth spurt produce the characteristics sexual dimorphism in shape and proportions seen in young adults.
Article
Reference data for skeletal maturity (TW2 method) of the hand and wrist are provided for large representative samples of Belgian boys and girls. The sample of Belgian boys consisted of 21,174 boys aged 12 to 20 years studied in a nationwide cross-sectional and longitudinal study on the physical fitness of secondary schoolboys (1969-1974). The girls' sample consisted of 9698 6-19-year-old Flemish girls studied cross-sectionally (1979-1980). Both samples were multi-stage stratified cluster samples of entire school classes. All skeletal maturity assessments of the boys were made by the same observer (GB). His estimations agreed quite closely with those of the originators of the method. The skeletal age assessments of the girls were made by two observers trained by GB. Both observers showed high intraobserver reliability after training, and during the assessments. Moreover their ratings compared favourably with those of GB and the originators of the method. Smoothed percentile curves of the maturity scores (TW2-20 bone, RUS and CARP scores) were calculated by means of cubic splines using a stepwise regression procedure for the selection of suitable knots. In the boys, the TW2 scores (20 bone and RUS) increase linearly between 12 and 14.5 years of age, slow down for a while, and then increase again, while the CARP scores increase linearly between 12 and 15 years of age. In girls, the 20-bone maturity scores increase nearly linearly from 6 through 9.5 years of age, accelerate until 11.0 years followed by a smaller increase; RUS scores increase curvilinearly from 6 years of age onwards; and Carp scores increase almost linearly between 6.0 and 12.5 years of age. Belgian boys are advanced in RUS scores but are delayed for the carpal bones as compared with the British standards. The Belgian girls show advancement for both scales as compared with the British reference data. The skeletal maturation of youths from several other continental European countries corresponds more closely with the Belgian than with the British data. The reference data presented herein most probably provide suitable standards for youths of West-European countries.
Article
Modified Greulich-Pyle (GP), Tanner et al. 2, radius, ulna and short bones (TW2-RUS), TW2-20-bone and Roche-Wainer-Thissen RWT (knee) skeletal age assessments were made in an Italian population sample of 128 males and 93 females aged 4.1-16.9 years. All the scales appear to be well-suited to the Italian population despite minor differences. A very high correlation was found between the assessment of knee skeletal ages by the RWT method and that of the hand-wrist by the GP and TW2 systems in the same subject without sex and age-associated variations.