New age-adjusted measure of body fat distribution in

International Journal of Obesity (1997) 21, 594±599
ß 1997 Stockton Press All rights reserved 0307±0565/97 $12.00
New age-adjusted measure of body fat
distribution in children and adolescents:
standardization of waist-hip ratio using
multivariate analysis
K Asayama1, K Hayashi2,3, Y Kawada1, T Nakane1, N Uchida1, H Hayashibe1, K Kawasaki2 and S Nakazawa1
1
Department of Pediatrics, Yamanashi Medical University, 1110 Shimokato, Tamahocho, Nakakomagun, Yamanashi 409-38, Japan;
Biostatistics Department, Yamanouchi Pharmaceutical Co., 1-1-8 Azusawa, Itabashiku, Tokyo 174, Japan; and 3 Present address:
Department of Basic Allied Medicine, School of Health Sciences, Faculty of Medicine, Gunma University, 3-39-15 Showa-machi,
Maebashi, Gunma 371, Japan
2
OBJECTIVES: To explore a new anthropometric index of body fat distribution adjusted for ages ranging from 6±15 y in
both boys and girls.
DESIGN: Sex, age, and 11 anthropometric variables were subjected to principal component analysis. Based on these
results, we developed a new anthropometric index, namely an age-adjusted measure of body fat distribution. This
index was evaluated statistically for suitability of use in epidemiological surveys.
SUBJECTS: Japanese children, including obese and nonobese subjects, in one elementary and one junior high school
in Yamanashi Prefecture, Japan: 508 boys and 549 girls whose ages ranged from 6 y 1 mon±15 y.
MEASUREMENTS: Measurements included the height (Ht), body weight, circumference of the waist, hip and thigh.
Body mass index, the ratios of the waist, hip or thigh to the Ht, waist-hip ratio (WHR) and waist-thigh ratio were
calculated.
RESULTS: The ®rst principal component (PC 1) accounted for 49.8% of the total variation, and was interpreted as an
indicator of the general size of an individual. PC 2 accounted for 25.9%, and was interpreted as a shape measure that
indicates body fat distribution. Calculation of WHR/Ht, a parameter that represented PC 2 adjusted by PC 1, gave an
highly robust linear regression equation for age by gender. The residuals from the regression line for WHR/Ht deviated
from normal distribution only in the boys, whereas the mean residual was nearly zero and distribution of the residuals
was similar in three age subgroups by gender, supporting the use of the common standard deviation score in all age
groups as an indicator of body fat distribution.
CONCLUSION: The common standard deviation score of WHR/Ht can serve as an epidemiological index of body fat
distribution adjusted for ages between 6 and 15 y.
Keywords: anthropometric methods; body fat distribution; children and adolescents; principal component analysis;
regression analysis
Introduction
Biochemical risk factors for atherosclerosis in children are more common among those who are obese.1
Anthropometric standards that can predict such potential health problems should be established for use in
the school or clinical setting. The amount of intraabdominal fat is more signi®cantly related to metabolic derangement induced by obesity than is the
amount of subcutaneous fat. Although in previous
reports, anthropometric measurement did not always
re¯ect the amount of intra-abdominal fat,2,3 evidence
suggests that waist-hip ratio (WHR) is useful in
evaluating the risk factors for atherosclerosis in
adults4±6 and children.7±10 At least in adults, WHR is
generally accepted as a measure that re¯ects the
Correspondence: Dr K Asayama.
Received 29 November 1996; revised 18 March 1997; accepted
20 March 1997
distribution of fat between intra-abdominal and subcutaneous sites.
Findings in several previous studies of children
have discouraged the use of WHR as an epidemiological index of body fat distribution. However, several
factors need to be considered in deciding whether
WHR, and related anthropometric indices, are suitable
for estimating the extent of abdominal obesity in
children. Changes in body composition, adiposity
and distribution of body fat during the growth and
development of children are well established.9±11 In
general, biochemical complications as well as excess
weight in obese children tend to worsen during
growth,1 whereas the normal values for WHR
decrease with age.10,12 Accordingly, an arithmetical
adjustment for age using analysis of covariance is not
very successful in obese children and adolescents.
Standardization of the criteria for obesity should be
based on the actual measures of body build observed
in a large population of children.
Age-adjusted measure of body fat distribution
K Asayama et al
The values and physiological signi®cance of WHR
differ between the races.13 Japanese people have a
different genetic background, as well as lifestyle, as
compared with other cultures. Their body build also
differs. In our previous study, after adjusting for age
using linear regression equations for nonobese subjects, the standard deviation score (SDS) for WHR
was found to be correlated with the serum levels of
lipids and apolipoproteins in obese Japanese children
attending elementary school (namely 6±12 y old).
Indices for being overweight or for adiposity were
unrelated to such serum biochemical ®ndings, especially in the girls.14
The present study was designed to develop a new
anthropometric index of body fat distribution in boys
and girls that was adjusted for age ranging from 6±
15 y. The distribution pattern of the value of WHR in
cohorts is skewed to the right, as with body mass
index. It is well known that, in girls, the normal value
of WHR declines rapidly during adolescence.12 To
solve these problems, we evaluated data from a large
group of children by means of principal component
analysis (PCA). A new anthropometric index that was
statistically valid in this age group was constructed
according to the results of PCA.
Materials and methods
Subjects
A total of 1057 Japanese children who attended one
elementary or one junior high school in Yamanashi
Prefecture, Japan, were subjected to anthropometric
measurements. There were 508 boys and 549 girls
who ranged in age from 6 y 1 mon±15 y (Table 1). The
subjects included both obese and nonobese children,
and were subdivided into three groups by age and
separated according to sex (Table 1). This survey was
approved by the Ethics Committee of Yamanashi
Medical University, Japan. Informed parental consent
for participation in this survey was obtained.
Anthropometric measurements
Anthropometric measurements were performed, as
described previously,14 by the medical staff in the
Department of Paediatrics, Yamanashi Medical University. In brief, height (Ht) was measured to the
nearest 0.1 cm and body weight to the nearest 0.1 kg
using a stadiometer. A plastic measuring tape was
used to determine the circumference of the waist at
the level of the umbilicus, and that of the hip at the
level of maximum extension of the buttocks, to the
nearest 0.1 cm, with the subject standing and following a normal expiration. Thigh circumference was
measured 3 cm above the upper border of the patella
on the left side if the subject was right-handed, and on
the right side if the subject was left-handed.
Body mass index (BMI) was calculated for each
subject by dividing the body weight (in kilograms) by
the Ht2 (in meters). To express body shape, we
calculated the ratio of the waist, hip or thigh to
height, respectively, waist-to-hip circumference ratio
(WHR) and waist-to-thigh circumference ratio
(WTR).
Table 1 Characteristics of the study population: basic statistics of the anthropometric measurements
Age group (year)
Numbers (boys/girls)
Age (y)
Ht (cm)
Weight (kg)
Waist (cm)
Hip (cm)
Thigh (cm)
BMI (kg/m2)
Waist/Ht
Hip/Ht
Thigh/Ht
WHR
WTR
WHR/Ht
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
M s.d.
range
6^<9
9^<12
12^15
All subjects
185 (96/89)
7.57 0.82
(6.17±8.96)
121.9 7.3
(104.0±140.8)
24.4 5.0
(14.2±41.2)
54.7 5.9
(44.8±85.0)
64.3 5.6
(50.0±82.6)
29.8 3.3
(23.3±39.3)
16.3 2.2
(13.0±26.3)
0.449 0.044
(0.373±0.689)
0.528 0.035
(0.462±0.669)
0.244 0.023
(0.200±0.318)
0.850 0.046
(0.754±1.029)
1.84 0.12
(1.48±2.40)
0.700 0.064
(0.576±0.942)
250 (116/134)
10.46 0.89
(9.01±11.99)
138.5 8.3
(118.3±168.3)
33.9 8.1
(20.6±62.5)
60.4 7.8
(47.2±90.0)
73.1 7.4
(58.0±98.4)
33.7 4.0
(17.0±47.1)
17.5 2.9
(12.7±27.6)
0.436 0.047
(0.351±0.606)
0.527 0.036
(0.454±0.651)
0.243 0.024
(0.139±0.319)
0.825 0.049
(0.728±1.026)
1.80 0.14
(1.49±2.99)
0.598 0.051
(0.459±0.743)
622 (296/326)
13.50 0.89
(12.00±15.01)
156.5 8.2
(134.4±182.5)
48.1 9.0
(28.4±82.0)
64.6 6.9
(50.7±99.0)
84.5 6.8
(67.5±111.0)
37.8 3.8
(28.1±50.6)
19.5 2.7
(13.5±32.8)
0.413 0.041
(0.337±0.642)
0.540 0.039
(0.460±0.698)
0.242 0.023
(0.190±0.347)
0.766 0.060
(0.632±0.978)
1.71 0.13
(1.34±2.27)
0.491 0.048
(0.389±0.733)
1057 (508/549)
11.75 2.45
(6.17±15.01)
146.2 15.6
(104.0±182.5)
40.6 12.5
(14.2±82.0)
61.9 7.9
(44.8±99.0)
78.3 10.4
(50.0±111.0)
35.4 4.9
(17.0±50.6)
18.5 3.0
(12.7±32.8)
0.425 0.045
(0.337±0.689)
0.535 0.038
(0.454±0.698)
0.242 0.023
(0.139±0.347)
0.794 0.065
(0.632±1.029)
1.76 0.14
(1.34±2.99)
0.553 0.096
(0.389±0.942)
Abbreviations: M s.d. indicates mean standard deviation; Ht, height; BMI indicates body mass index (weight/
height2); WHR, waist±hip ratio; WTR, waist±thigh ratio.
595
Age-adjusted measure of body fat distribution
K Asayama et al
596
Statistical analyses
Data are presented as means and standard deviations
(s.d.). At the ®rst stage of the present study, all
samples (n ˆ 1057) were pooled, and gender 0 indicating boys and 1 the girls, age, and 11 anthropometric variables (Table 1) were subjected to PCA.
Then we explored a new anthropometric index that
would represent an age-adjusted measure of body fat
distribution by utilizing various statistical methods.
Other statistical methods used were linear regression
analysis, Shapiro±Wilks test for normality, Kruskal±
Wallis and Median tests for the difference in the
central values, and the Kolmogorov±Smirnov twosample test for the comparison of the distribution of
variables in different subgroups. All P-values are twosided. A level P < 0.05 was accepted as statistically
signi®cant. Statistical analyses were performed using
Statistical Analysis System software (SAS Institute
Inc., Cary, NC, USA).
Results
The means s.d. and ranges of anthropometric measures in the three age subgroups are summarized in
Table 1. The mean values for Ht, body weight, waist,
hip and thigh were greater in the older groups than in
the younger groups, indicating that the body size
increased with age. Similarly, the BMI tended to
increase with age. On the other hand, both WHR
and WTR showed a gradual decrease with age.
Table 2 summarizes the results of PCA in the
subjects studied. We retained factor loadings and
respective scores for the ®rst four major axes, which
jointly accounted for 96.2% of the total variation.
Only the ®rst three principal components (PC) exhibited eigen-values greater than 1. PCA clearly separated the variables that gave different loadings to the
respective axes. The ®rst PC accounted for 49.8% of
the total variation, and could serve as a credible
indicator of an individual's general size. PC 2
accounted for 25.9% of the total variation, and was
considered to be a measure of shape that indicated
body fat distribution, being mainly loaded by waist/Ht
and WHR in contrast with size variables. PC 3 and 4
were factors for combinations of gender and the
several variables for shape.
The factor patterns were plotted by assigning PC 1
to the ordinate and PC 2 to the abscissa (Figure 1).
The ®gure clearly contrasts the different characteristic
between BMI (index for being overweight) and WHR
(index of body fat distribution). WHR was divided by
the Ht (in meters) of each individual, in an attempt to
obtain a new measure of body fat distribution adjusted
for body size. Among the size variables studied here,
Ht appeared to be the most suitable for standardizing
the WHR because it is normally distributed in the
general population and it is the standard measure for
linear growth. Since our previous study revealed that
WHR was signi®cantly smaller in girls than in boys
even in ages younger than 12 y old,14 data for boys
and girls were treated separately in the further analyses.
We next evaluated the correlation of WHR/Ht with
age in each gender, and compared that to the correlation of waist/Ht and WHR with age. Table 3 summarizes the univariate linear regression analysis
assigning age as an independent variable. In both
sexes, the correlation with age was highly signi®cant
for waist/Ht, WHR, as well as WHR/Ht. The r2 values
indicated that the linear association of WHR/Ht with
age in both sexes was more stable than was the
association of waist/Ht and WHR with age: the
correlation coef®cient of WHR/Ht with age was
0.900 for the boys and 0.922 for the girls (Figures 2
and 3). This close linear association of the two
parameters in both sexes clearly indicates that
WHR/Ht can be adjusted for age by simply introducing a linear function, and that the residual (namely
the deviation of the observed value of WHR/Ht from
Table 2 Results of principal component analysis (n ˆ 1057)
Gender
Age
Ht
Weight
BMI
Waist
Hip
Thigh
Waist/Ht
Hip/Ht
Thigh/Ht
WHR
WTR
Eigen-value
Proportion
Cumulative
Factor1
Factor 2
Factor 3
Factor 4
0.0873
0.7379
0.7637
0.9505
0.9103
0.8572
0.9667
0.9653
0.2489
0.6784
0.5496
70.2713
70.3282
6.4740
0.4980
0.4980
70.2481
70.5387
70.4914
70.1259
0.3476
0.3809
70.1780
0.0185
0.9615
0.4078
0.5842
0.8514
0.5504
3.3668
0.2590
0.7570
70.7524
0.2584
0.3907
0.2311
70.0616
0.3033
0.0318
70.0093
70.0392
70.5108
70.4491
0.3740
0.5001
1.7899
0.1377
0.8947
0.5253
0.0525
0.0462
0.0473
0.0346
0.1018
0.1479
70.2151
0.0671
0.1976
70.3750
70.0844
0.5679
0.8766
0.0674
0.9621
Abbreviations are the same as in Table 1.
Figure 1 Factor patterns in principal component analysis.
Factor loadings are plotted assigning the ®rst principal component to the ordinate and the second component to the abscissa.
Abbreviations: Ht, height; BMI, body mass index; WHR, waist-hip
ratio; WTR, waist-thigh ratio.
Age-adjusted measure of body fat distribution
K Asayama et al
597
Table 3 Univariate linear regression analysis of Waist/Ht, WHR
and WHR/Ht
P-value
r2
0.00967
0.00081
0.00861
0.00071
<0.0001
<0.0001
<0.0001
<0.0001
0.1020
0.94874
70.01035
0.98656
70.01892
WHR
0.00956
0.00080
0.00882
0.00073
<0.0001
<0.0001
<0.0001
<0.0001
0.2481
0.96607
70.03364
0.95321
70.03555
WHR/Ht
0.000892
<0.0001
0.00075
<0.0001
0.00797
<0.0001
0.00066
<0.0001
Estimate
SE
a
b
a
b
0.50387
70.00614
0.48613
70.00575
a
b
a
b
a
b
a
b
Waist/Ht
Boys
Girls
Boys
Girls
Boys
Girls
0.1060
0.5498
0.8004
0.8410
Y ˆ a ‡ b 6 Age.
the expected value of the linear regression equation)
for each individual can be an age-adjusted estimate of
body fat distribution.
To further optimize the residual of WHR/Ht for
clinical use, we calculated the SDS of WHR/Ht using
common s.d. for all age subgroups. We examined the
statistical characteristics of this parameter to determine whether it could be used as a clinical index of
body fat distribution in children and adolescents. We
statistically evaluated the residuals (or SDS) of WHR/
Ht to determine the normality of the distribution as a
whole, and to compare the central values and distribution pattern in three different age subgroups by sex.
The histograms of the SDS of WHR/Ht for the boys
and girls are shown in the Figures 4 and 5. The
normality of the distribution of the residuals was
accepted at P ˆ 0.8083 for the girls, but was rejected
at P ˆ 0.0025 for the boys as determined by the
Shapiro±Wilk test.
The central values did not differ signi®cantly
between the three age subgroups for each gender as
determined by Kruskal±Wallis and Median tests. Each
pair of data from the different age groups showed no
Figure 2 Correlation of WHR/Ht with age in boys (n ˆ 508). WHR
is divided by Ht (m). Pearson's correlation coef®cient is indicated
by r. The relationship between the two variables is very close.
Figure 3 Correlation of WHR/Ht with age in girls (n ˆ 549). The r
indicates the Pearson's correlation coef®cient. The relationship
between the two variables is very close.
signi®cant difference in distribution from each other
as determined in the boys and girls by Kolmogorov±
Smirnov two-sample test. Thus, the uniformity of
the central values and distribution in three different
subgroups for each gender supported the use of
the common SD for the calculation of SDS for
WHR/Ht.
Figure 4 Histogram of the common SDS of WHR/Ht in boys.
The distribution slightly deviates from normal (see text), but
does not look highly skewed.
Figure 5 Histogram of the common SDS of WHR/Ht in girls. The
distribution does not signi®cantly deviate from normal (see text).
Age-adjusted measure of body fat distribution
K Asayama et al
598
Discussion
The present study explored an index of body fat
distribution that was adjusted for ages ranging from
6±15 y for each sex. The PCA successfully contrasted
the size and shape variables in the present group of
children and adolescents. WHR divided by Ht was
considered to represent PC 2 adjusted by PC 1. This
estimate gave an extremely robust linear regression by
age for each sex. Further statistical tests of normality
revealed that the distribution of the residuals for
WHR/Ht was deviated somewhat from normality
only in the boys, whereas the central values and the
distribution were similar in the three age groups of
each sex. Thus, the common SDS of the WHR/Ht was
veri®ed to be a potential measure of body fat distribution over age in the population studied.
The contribution of the androgyny of fat patterning
to metabolic derangement seen in childhood obesity is
supported by the previous observation that metabolic
derangement is more common at older ages and in
boys, than at younger ages and in girls.15 In a study of
obese women, metabolic derangement was linked to
the WHR, but not to the indices for overweight or
adiposity.6 In adult men, sagittal diameter and WHR
were considered almost equally good indices for
predicting metabolic risk.16 A lipoprotein abnormality
was better re¯ected in the BMI in nonobese, but in the
WHR in the obese young adults in Taiwan.17
In children, the WHR appears to be a useful index
when the age and sex of the subjects studied are
relatively uniform. Waist measurement was reported
to correlate with a potentially atherogenic lipoprotein
pro®le in obese 12 and 14 y old children.18 Improvement of the atherogenic risk-factor pro®le during
weight reduction was more marked in obese adolescent girls with a higher than, in those with lower,
WHR.19 In cross-sectional studies that dealt with both
children and adolescents in one group,20 WHR per se
did not appear to be as good an index as observed in
adults.6,16,17 WHR was reported to be higher in boys
than in girls throughout pediatric ages, and to decrease
gradually in boys with age, while there were two sharp
reductions at ages 10±13 y and 13±16 y in girls
because of the marked increase in hip circumference
at 13 y but a decrease in waist circumference from 13±
17 y.12 These results indicate the need for establishing
an age-adjusted estimate of body fat distribution in the
pediatric age group.
There is some debate whether WHR measures the
amount of visceral adipose tissue.2 Ross et al21
reported that in adult men and women the amount
of visceral adipose tissue, as measured by magnetic
resonance image (MRI), analysis was greater at 10±
15 cm above than at the level of lumbar spine 4 and 5
and that this level corresponded to the level of the last
rib. They thought that waist circumference measured
at this level was a better predictor than that measured
at the level of umbilicus. Likewise, the amount of
intra-abdominal fat measured by MRI did not correlate with WHR in obese and nonobese adolescents.3
Unlike the ®ndings in adults, the amount of intraabdominal fat in children was much less than that of
subcutaneous fat.3 Thus, the measurement of visceral
adipose tissue by MRI has its limitations, and it may
be relatively imprecise for studying children.19 Even a
study in adults failed to demonstrate a relationship
between the amount of visceral adipose tissue and
serum lipid levels.22 Armellini et al5 reported that the
WHR correlated with resting metabolic rate in obese
women, but that the amount of visceral adipose tissue
did not. These results suggest that the WHR is a
unique index of body fat distribution that re¯ects
individual metabolic activity, and is not just an alternative to measurement of visceral fat by an imaging
technique.
In the present study subjects, the ratio of WHR to
Ht was expressed as an extremely robust linear function of age for each sex. This implies that Ht and age
are the two major determinants of normal value of
WHR in Japanese children with ages ranging from 6±
15 y. Thus, change in the normal value of WHR by
age in each sex appears to largely depend on the factor
of linear growth. The SDS of the WHR/Ht would be
useful in performing cross-sectional studies dealing
with body fat distribution in children and adolescents.
Since the population used here is comprised of children with various ages in one group, this estimate
should be equally good for individuals with any given
age in this range. Thus, the SDS of the WHR/Ht is
also suitable for longitudinal study. This new anthropometric index can help to resolve a problem of
limited applicability of WHR to the study of children
and adolescents. The usefulness of this new ratio has
to be veri®ed with other groups of children originating
from different races. Further study will elucidate the
physiological signi®cance of the SDS of the WHR/Ht,
and the relevance of abdominal obesity in children to
the risk of atherosclerosis.
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