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ABSTRACT This study evaluated the influence of height growth and nu-
tritional status on skeletal maturation of the knee and hand-wrist. Radio-
graphs of 589 subjects (250 girls and 339 boys) from 2 to 15 years were rated
according to Greulich-Pyle, TW-20 bone and TW-RUS, RWT knee, and FELS
hand-wrist methods and a method combining FELS and RWT indicators. The
subjects were referred to the Genoa University Paediatric Department from
1980 to 1987 for short stature, simple obesity, or acute diseases. Bone age was
closer to chronological age using the RWT knee method rather than the
hand-wrist methods, while bone age assessed at the hand-wrist was closely
related to height and BMI. When skeletal maturation was delayed, Greulich-
Pyle, TW-20-bone, TW-RUS, and FELS bone ages tended to be lower than
RWT knee estimates. Conversely, if maturation was advanced the hand-wrist
estimates tended to be higher than RWT knee bone ages. The combined
estimates are close to FELS bone age values. These findings show true in-
traindividual variability of skeletal maturity at the hand-wrist and knee. A
certain “laziness” in knee maturation seems to be confirmed. Am. J. Hum.
Biol. 12:610–615, 2000. © 2000 Wiley-Liss, Inc.
PROD #M98076R
SKELETAL MATURITY AT HAND-WRIST AND KNEE 611
wrist and antero-posterior radiographs of TABLE 1. Height SDS and BMI-SDS distributions for
the knee were taken under standard condi- age and sex (mean and SE)
tions and assessed according to the Sample
Greulich-Pyle (1959), TW-20 bone, and TW- Age size n Height—SDS BMI—SDS
RUS (Tanner et al., 1983), RWT knee years Boys Girls Boys Girls Boys Girls
(Roche et al., 1975), and FELS hand-wrist 2–3 21 25 −0.18 −0.47 −0.03 −0.17
(Roche et al., 1988) methods, and a method (0.30) (0.25) (0.48) (0.29)
4–5 37 24 −0.79 −0.28 −0.22 1.03
using all the FELS hand-wrist and RWT (0.28) (0.31) (0.55) (0.56)
knee maturity indicators (Roche et al., 6–7 44 40 −0.22 −0.14 1.03 2.10
1988). According to the FELS and RWT (0.25) (0.21) (0.45) (0.39)
methods, the graded indicators were se- 8–9 54 54 −0.17 −0.11 0.04 1.91
(0.24) (0.22) (0.49) (0.29)
lected on the basis of chronological age and 10–11 67 52 −0.39 −0.17 1.76 1.29
sex. When the initially assigned skeletal age (0.19) (0.20) (0.31) (0.29)
differed from chronological age by more 12–13 70 47 −1.06 −1.35 1.12 1.08
than ± 1.5 years, further assessments were (0.21) (0.24) (0.31) (0.42)
14–15 46 8 −2.51 −0.60 −0.47 0.84
made using the indicators appropriate for (0.19) (0.54) (0.23) (0.81)
the first assigned skeletal age. The assessor
(MV) was experienced in working with all of
the methods and had a high level of repro- closer to chronological age with the RWT
ducibility (between observers) and repeat- knee method compared to the other meth-
ability (within observer) for all methods ods. The FELS and combined methods yield
(Vignolo et al., 1989, 1990). Radiographs of very similar mean values of relative bone
589 subjects (250 girls and 339 boys) from 2 age in each sex and age class.
to 15 years were rated. Height and weight of The relationships between Greulich-Pyle,
all subjects were measured. Height mea- TW-20 bone, TW-RUS, RWT knee, FELS
surements were standardized according to hand-wrist, and combined FELS-RWT rela-
British reference values (Tanner and White- tive bone ages vs. height-SDS and BMI-SDS
house, 1976). The body mass index (BMI: are illustrated in Figures 2 and 3, respec-
weight/height2) value was calculated for tively.
each subject and standardized using the ref- Relative bone age is closely related to
erence values of Rolland-Cachera et al. height-SDS in all methods based on the
(1982). The BMI appears to be an appropri- hand-wrist, while the dependence of RWT
ate single measure of nutritional status bone age on height-SDS is rather less
(Power et al., 1997). prominent. The contribution of RWT to the
combined estimate does not appear to
RESULTS weaken the dependence of FELS bone age
Sample size, mean and SE of height SDS on height-SDS.
and BMI-SDS for age and sex are reported Hand-wrist relative bone ages appear to
in Table 1. Mean height and mean BMI be also related to BMI-SDS; their increase is
were, respectively, somewhat lower and particularly large in overweight children
higher than the reference values, due to the (Fig. 3). The dependence of knee-RWT bone
high prevalence of subjects who were over- age upon BMI-SDS is less evident. The con-
weight and of short stature. Means ± SE of tribution of RWT to the combined estimate
Greulich-Pyle, TW-20 bone, TW-RUS, RWT, does not appear to weaken the dependence
FELS, and the combined FELS-RWT skel- of FELS bone age on BMI-SDS.
etal age estimates by age group and sex are Furthermore, skeletal maturation delay
reported in Table 2. (relative skeletal age <−1.5 years) or ad-
The relationship between relative bone vancement (relative skeletal age >1.5 years)
age (i.e., difference between bone age and were observed more frequently when skel-
chronological age) and chronological age as etal age was estimated by methods using
assessed by the different methods is shown the hand-wrist than by RWT knee method
in Figure 1. The shape of the relationship is (see Table 3).
roughly similar in boys and girls, but in Figure 4 shows the distribution of
girls the bone age values were more ad- Greulich-Pyle relative bone age conditional
vanced independently of the method used. on RWT relative bone age. When skeletal
The difference between the sexes is particu- maturation is delayed or normal, Greulich-
larly prominent using TW-RUS. Bone age is Pyle bone age tends to be lower than RWT
TABLE 2. Mean and SE (years) of chronological age, Greulich-Pyle, TW-20 bones, TW-RUS, FELS, and combined FELS-RWT estimates by age groups and sex
Chronological Combined
Age age Greulich-Pyle TW-20 bones TW-RUS Hand-wrist FELS Knee-RWT FELS-RWT
class Boys Girls Boys Girls Boys Girls Boys Girls Boys Girls Boys Girls Boys Girls
2–3 2.99 2.90 2.84 2.61 2.87 2.52 3.03 2.82 2.90 2.61 3.02 2.70 2.91 2.65
(0.11) (0.12) (0.18) (0.12) (0.19) (0.12) (0.19) (0.13) (0.19) (0.16) (0.15) (0.14) (0.17) (0.15)
4–5 4.96 5.01 4.26 4.92 4.24 4.76 4.41 4.87 4.53 5.00 4.50 4.86 4.50 4.98
(0.09) (0.13) (0.19) (0.28) (0.19) (0.28) (0.19) (0.31) (0.20) (0.26) (0.18) (0.17) (0.19) (0.24)
6–7 6.97 6.98 6.59 7.05 6.76 7.01 6.70 7.18 6.87 7.17 6.99 6.85 6.91 7.13
(0.09) (0.09) (0.27) (0.23) (0.31) (0.24) (0.29) (0.25) (0.28) (0.24) (0.24) (0.18) (0.27) (0.23)
8–9 9.17 9.06 9.00 9.29 9.16 9.35 9.06 9.73 9.31 9.65 9.28 9.51 9.29 9.64
(0.07) (0.07) (0.27) (0.21) (0.26) (0.25) (0.27) (0.26) (0.27) (0.25) (0.20) (0.15) (0.26) (0.23)
10–11 11.01 11.05 10.78 11.19 10.95 11.32 10.95 11.85 11.06 11.61 11.34 11.52 11.11 11.61
(0.07) (0.08) (0.21) (0.19) (0.25) (0.18) (0.26) (0.21) (0.24) (0.17) (0.16) (0.15) (0.22) (0.16)
12–13 13.04 12.93 12.25 12.83 12.66 12.79 12.81 13.27 12.63 13.17 13.10 13.22 12.71 13.14
(0.07) (0.08) (0.20) (0.29) (0.23) (0.24) (0.24) (0.26) (0.22) (0.29) (0.13) (0.20) (0.20) (0.26)
14–15 14.75 14.73 12.92 14.51 13.47 13.96 13.51 14.52 13.38 14.71 13.90 14.43 13.50 14.53
(0.09) (0.17) (0.18) (0.46) (0.21) (0.36) (0.22) (0.35) (0.19) (0.72) (0.12) (0.41) (0.17) (0.59)
SKELETAL MATURITY AT HAND-WRIST AND KNEE 613
Fig. 1. Relationships of relative bone ages (i.e., the difference between bone age and chronological age) to
chronological ages (mean ± SE) in boys (䊐---䊐) and in girls (䊏—䊏).
Fig. 2. Relationships of relative bone ages to height-SDS (mean ± SE) in boys (䊐---䊐) and in girls (䊏—䊏).
bone age. If skeletal maturation is ad- method, differences of more than 2 years
vanced, Greulich-Pyle bone age tends to be were found in about 5% of children. When
higher than RWT bone age. Differences of skeletal maturation is delayed, the com-
more than 2 years were observed in about bined bone ages (FELS+RWT indicators)
3% of children. Similar results were ob- tend to be lower than the RWT bone ages
served when the RWT method was com- (Fig. 5). When skeletal maturation is ad-
pared with the TW-20-bone, TW-RUS, and vanced, the combined bone ages tend to be
FELS methods. As regards the TW-RUS higher than RWT bone ages. Differences of
614 G. AICARDI ET AL.
Fig. 3. Relationships of relative bone ages to BMI-SDS (mean ± SE) in boys (䊐---䊐) and in girls (䊏—䊏).
TABLE 3. Subjects with skeletal maturation delay or advancement determined by different methods
TW-20 Hand-wrist Combined
Greulich-Pyle bones TW-RUS FELS Knee-RWT FELS-RWT
Skeletal age % % % % % %
Delay 25,4 21,7 21,7 20,3 7,5 18,3
(relative skeletal age
ⱕ−1.5 years)
Advancement 15,7 15,1 22,0 19,4 10,6 17,6
(relative skeletal age
>1.5 years)
more than 2 years were observed only in of the skeleton should be considered. These
about 1% of children. Interindividual vari- differences are usually related to the inter-
ability of the combined estimates was lower action of factors such as differences between
than that of the estimates based only on methods, observer errors, and true biologi-
hand-wrist indicators. The combined esti- cal variations in maturity.
mates were close to FELS bone age values, In the present study, quite similar differ-
the large majority of differences being ences were observed between RWT knee es-
within ±6 months. However, when skeletal timates and hand-wrist assessments ob-
maturation is delayed, the combined bone tained by the Greulich-Pyle, TW, and FELS
ages tend to be higher than FELS bone ages. methods, which are very different in their
If skeletal maturation is advanced, the com- source samples, statistical basis, and appli-
bined bone ages tend to be lower than FELS cation. This seems to indicate that the ob-
bone age. served differences are independent of the
methods used and that there is a true intra-
DISCUSSION
individual variability in maturity levels of
Since there are differences between as- the hand-wrist and knee.
sessments of various skeletal areas by dif- The bone ages from the RWT method
ferent methods, biological limitations of the were closer to the chronological ages than
estimates of maturity of an individual ob- those from the other methods using the
tained from the evaluation of only one part hand-wrist, while bone age assessed at
SKELETAL MATURITY AT HAND-WRIST AND KNEE 615