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Relation of body mass index and waist-to-height ratio to

cardiovascular disease risk factors in children and adolescents:


the Bogalusa Heart Study1 4
David S Freedman, Henry S Kahn, Zuguo Mei, Laurence M Grummer-Strawn, William H Dietz, Sathanur R Srinivasan,
and Gerald S Berenson

ABSTRACT among children (10), several indexes of abdominal obesity are


Background: Several investigators have concluded that the waist- associated with CVD risk factors among children and adoles-
to-height ratio is more strongly associated with cardiovascular dis- cents (1116).
ease risk factors than is the body mass index (BMI; in kg/m2). The waist-to-height ratio was first used in the Framingham

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Objectives: We examined the relation of the BMI-for-age z score Study (17), and several studies of children (1315) and adults
and waist-to-height ratio to risk factors (lipids, fasting insulin, and (18, 19) have concluded that this ratio is more strongly associated
blood pressures). We also compared the abilities of these 2 indexes with CVD risk factors than is the body mass index (BMI; in
to identify children with adverse risk factors. kg/m2). In addition, waist-to-height ratio may be simpler to use.
Design: Children aged 517 y (n 2498) in the Bogalusa Heart For example, because waist-to-height ratio is only weakly asso-
Study were evaluated. ciated with age, measures among children do not have to be
Results: As assessed by the ability of the 2 indexes to 1) account for expressed relative to their sex and age peers [by using z scores
the variability in each risk factor and 2) correctly identify children (20)] as do measures of BMI. In addition, the same cutoff (eg,
with adverse values, the predictive abilities of the BMI-for-age z 0.5) could possibly be used to identify adverse measures of waist-
score and waist-to-height ratio were similar. Waist-to-height ratio to-height ratio among both children and adults (21, 22), which
was slightly better (0.01 0.02 higher R2 values, P 0.05) in pre- would simplify the expression of obesity-related disease risk.
dicting concentrations of total-to-HDL cholesterol ratio and LDL However, relatively few studies have examined the relation of
cholesterol, but BMI was slightly better in identifying children with waist-to-height ratio to CVD risk factors, and it is important to
high systolic blood pressure (0.03 higher R2, P 0.05) in predicting examine these associations in other data.
measures of fasting insulin and systolic and diastolic blood pres- The current study compares the relation of BMI and waist-to-
sures. On the basis of an overall index of the 6 risk factors, no height ratio to measures of lipids, fasting insulin, and blood
difference was observed in the predictive abilities of BMI-for-age pressure among 517-y-olds (n 2498) in the Bogalusa Heart
and waist-to-height ratio, with areas under the curves of 0.85 and Study. In addition, we examine the abilities of these 2 indexes to
0.86 (P 0.30) and multiple R2 values of 0.320 and 0.318 (P correctly identify children with adverse risk factors.
0.79). This similarity likely results from the high intercorrelation (R2
0.78) between the 2 indexes.
Conclusions: BMI-for-age and waist-to-height ratio do not differ in SUBJECTS AND METHODS
their abilities to identify children with adverse risk factors. Although
waist-to-height ratio may be preferred because of its simplicity, Study population
additional longitudinal data are needed to examine its relation to The Bogalusa (Louisiana) Heart Study is a community-based
disease. Am J Clin Nutr 2007;86:33 40. (Ward 4 of Washington Parish) study of CVD risk factors in early
life (23). Seven cross-sectional examinations of schoolchildren
KEY WORDS BMI, body mass index, waist, height, waist-to- were conducted since 1973, and the current analyses are based on
height ratio, children, lipids, blood pressure, insulin
1
From the Divisions of Nutrition and Physical Activity (DSF, ZM,
LMG-S, and WHD) and Diabetes Translation (HSK), Centers for Disease
INTRODUCTION Control and Prevention, Atlanta, GA, and the Tulane Center for Cardiovas-
Vague (1) was the first to observe that women with android cular Health, Tulane University School of Public Health and Tropical Med-
obesity had a high prevalence of diabetes and atherosclerosis. icine, New Orleans, LA (SRS and GSB).
2
Subsequent studies have shown that abdominal obesity, as mea- The findings and conclusions in this report are those of the authors and
not necessarily those of the CDC.
sured by the waist circumference or related indexes such as the 3
Supported by grant no. AG-16592 from the National Institutes of Aging.
waist-to-hip ratio, is associated with the subsequent development 4
Address reprint requests to DS Freedman, CDC K-26, 4770 Buford
of type 2 diabetes (25) and ischemic heart disease (6 8), as well Highway, Atlanta GA 30341. E-mail: dfreedman@cdc.gov.
as with risk factors for cardiovascular disease (CVD) (9). Fur- Received September 26, 2006.
thermore, despite the relatively low amount of intraabdominal fat Accepted for publication March 16, 2007.

Am J Clin Nutr 2007;86:33 40. Printed in USA. 2007 American Society for Nutrition 33
34 FREEDMAN ET AL

the 19931994 examination. Written informed consent was ob- Risk factors
tained from all parents, and study protocols were approved by Concentrations of serum total cholesterol and triacylglycerols
human subjects review committees at the Tulane University were measured by using enzymatic procedures in a centralized
School of Public Health and Tropical Medicine. laboratory that met the requirements of the CDCs Lipid Stan-
Of the 3135 children and adolescents (aged 517 y) examined, dardization Program. For LDL- and HDL-cholesterol measure-
we excluded 9 girls who reported being pregnant, 7 children who ments, we used a combination of heparin-calcium precipitation
were not white or black, 30 children who reported taking insulin and agar-agarose gel electrophoresis (27). Plasma insulin mea-
(or were unsure), 13 children for whom we did not have a systolic surements were obtained with the use of a radioimmunoassay
(SBP) or diastolic (DBP) blood pressure measurement, and 14 procedure (Phadebas Insulin Kit; Pharmacia Diagnostics AB,
children for whom information on measurements of waist, Uppsala, Sweden).
weight, or height was missing; these categories were not mutu- As previously described (23), sitting SBP and DBP in the right
ally exclusive. Of the remaining 3066 children, cholesterol (total, arm were measured 6 times by trained observers with a mer-
LDL, and HDL) and triacylglycerol determinations were avail- cury sphygmomanometer (Baumanometer; WA Baum Co Inc,
able for 2961. Nonfasting children were excluded from the anal- Copiague, NY). The cuff size was based on the length and
yses of triacylglycerol and fasting insulin concentrations, and circumference of the upper arm and was chosen to be as large
another 130 children did not have an insulin determination. After as possible without having the elbow skin crease obstruct the
these exclusions, sample sizes for the various risk factors are stethoscope (28).
3066 (for SBP and DBP), 2961 (for LDL and HDL cholesterol), The distributions of lipid and lipoprotein concentrations in the
2624 (for triacylglycerol), and 2494 (for insulin). Bogalusa Study were similar to those in the third National Health
Because obesity is associated positively with LDL cholesterol

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and Nutrition Examination (NHANES III) conducted from 1988
and negatively with HDL cholesterol, we did not examine asso- to 1994 (29). For example, the 90th percentiles of LDL choles-
ciations with total cholesterol. However, the ratio of total cho- terol among 1215-y-old white children (data were not cross-
lesterol to HDL cholesterol (total:HDL cholesterol) is included classified by race, sex, or age group) in NHANES III were 122
in the analyses. mg/dL (whites) and 133 mg/dL (blacks); corresponding values in
the Bogalusa Study were 127 mg/dL (whites) and 133 mg/dL
General examinations (blacks). Similarly, the 10th percentiles of HDL cholesterol were
35 mg/dL (boys) and 36 mg/dL (girls) among 1215-y-olds in
Height was measured to the nearest 0.1 cm with the use of an
NHANES III and were 37 mg/dL among both boys and girls in
Iowa Height Board, and weight was measured to the nearest 0.1
the Bogalusa Study. However, because of differences in methods
kg with the use of a balance beam metric scale; BMI was calcu-
of measuring blood pressure (28), recorded measures of blood
lated as a measure of relative weight. No adjustments were made pressure are 510 mm Hg lower in the Bogalusa Study than in
for the weight of the gown, underpants, or socks that were worn other studies.
during the examination.
BMI z scores were calculated from the 2000 Centers for Dis-
ease Control and Prevention (CDC) Growth Charts (20, 24) to Measures of adverse risk factors
account for the differences in BMIs by sex and age. These growth Because measures of lipids, insulin, and blood pressures vary
charts express the BMIs of children in the current study relative substantially by sex and age, we defined adverse measures in
to their sex and age peers in the United States between 1963 and relation to a childs sex and age peers in the Bogalusa Study
1980; the calculated z scores are termed BMI-for-age in the sample. After log-transformation of measures of the risk factors
current analyses. (BMIs among 5-y-olds in the CDC Growth to improve normality, each risk factor was regressed on sex, race,
Charts also include data from 1988 1994.) Overweight is de- and age. Age was modeled with the use of restricted cubic splines
fined as a BMI-for-age z score 1.645 (corresponding to the with 5 knots (see Statistical analyses) (30), and we allowed for
95th percentile of normally distributed data) of these growth interactions with age (age BMI and age waist-to-height
charts (25, 26). BMI-for-age z scores were used in all analyses in ratio) in the prediction of each risk factor. Regression models for
the current study. BMI-for-age percentiles are used only to clas- SBP and DBP also included height (cubic splines) as a predictor.
sify children into 4 categories in one table that cross-classifies The standardized residuals (adjusted risk factor measures) from
BMI-for-age and waist-to-height ratio. these models represent measures relative to children of the same
The waist circumference was measured midway between the sex, race, and age. All adjusted risk factors had a mean SD
rib cage and the superior border of the iliac crest while the child value of 0 1.0. With the exception of HDL cholesterol (10th
was standing. Three measurements were obtained with a non- percentile), adverse risk factor measures were defined as a mea-
stretchable tape, and the mean value was used in the calculation sure 90th percentile.
of the waist-to-height ratio. In analyses that compared the abil- Although the identification of children with adverse risk fac-
ities of BMI and waist-to-height ratio to correctly identify chil- tors in the current study is based solely on the distribution of risk
dren with adverse risk factors, we dichotomized waist-to-height factors in the Bogalusa Study, the use of cutoffs from NHANES
ratio at 0.512 (without considering the childs sex or age) so that III (29) identified similar children with adverse concentrations of
the same proportion (17%) of children would be overweight and lipids and lipoproteins. For example, all of the 1215-y-olds
have a high waist-to-height ratio. (whites and blacks combined; n 106) in the current study who
On each examination day, a 10% sample of the children was were classified as having a high LDL-cholesterol concentration
randomly selected to be reexamined 23 h later by the same (according to the Bogalusa Study cutoffs) also had a concentra-
observer. We use these data to compare the reproducibilities of tion 90th percentile (119 mg/dL) in NHANES III. However, 45
BMI and waist-to-height ratio. (5%) of the 950 children aged 1215 y who we considered to have
CHILDHOOD BMI, WAIST-HEIGHT RATIO, AND CARDIOVASCULAR RISK 35
a normal LDL-cholesterol concentration were in the 90th or waist-to-height ratio to a model already containing age, sex,
percentile in NHANES III. [It should be noted that some esti- and race. Continuous variables were modeled by using restricted
mates of the 90th percentile in NHANES III were considered to cubic splines with 5 knots (30) to allow for nonlinearity, and we
be unstable because of the relatively small sample size (29).] allowed for an interaction between each index and age. In con-
Because of differences in methods of measuring blood pressure trast to the use of higher-order polynomials, models based on
(28), few children in the Bogalusa Study had a SBP or DBP splines do not have peaks and valleys, and the fit in one region
90th percentile of the National High Blood Pressure Education does not influence the fit in all other regions of the data.
Program (31). To assess the differences between the R2 values of models that
The risk factor sum was used as a summary measure of the 6 contained either BMI-for-age or waist-to-height ratio, we first
risk factors and was derived by combining adjusted measures of calculated predicted risk factor measures from each model. We
triacylglycerols, LDL cholesterol, HDL cholesterol, fasting in- then examined the statistical significance of the difference in the
sulin, SBP, and DBP. Adjusted measures of most risk factors correlation between the actual risk factor measures and the 2 sets
were simply added together, but adjusted measures of HDL cho- of predicted risk factor measures coefficients (36). We also ex-
lesterol were subtracted from the total. In addition, because of the amined whether the relation of BMI-for-age and waist-to-height
high correlation (r 0.66) between SBP and DBP, these 2 ratio to each risk factor was nonlinear.
characteristics were first divided by 2. The resulting risk factor We then cross-classified categories of BMI-for-age (50th
sum had a mean SD value of 0 2.9 (range: 111). Correla- percentile, 50th 84th percentile, 85th94th percentile, and
tions between the risk factor sum and the individual risk factors 95th percentile) and waist-to-height ratio. Cutoffs for the 4
ranged from r 0.37 (DBP) to r 0.73 (triacylglycerols); the categories of waist-to-height ratio were selected so that the num-
association with HDL cholesterol was r 0.59. ber of children in each category would equal the number in the

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The risk factor sum was highly correlated (r 0.97) with the corresponding BMI-for-age category. We focused on measures
first principal component (32) of the 6 risk factors. Furthermore, of the risk factor sum among children whose BMI-for-age stra-
with the exception of LDL-cholesterol concentrations (r 0.39), tum was lower or higher (discordant) than the corresponding
the absolute value of the correlation coefficients with the first waist-to-height ratio stratum. We also show the relation of waist-
principal component ranged from 0.50 (HDL cholesterol) to 0.70 to-height ratio to BMI-for-age by using lowess to smooth the data
(triacylglycerols). (The second principal component was diffi- (37).
cult to interpret because it contrasted measures of DBP, SBP, and In addition to determining whether differences between BMI-
HDL cholesterol with measures of triacylglycerols and fasting for-age and waist-to-height ratio were statistically significant,
insulin, and it was not considered further.) Although risk factor we also focused on the magnitudes of the differences in the AUCs
summaries can be derived by adding together the number of and R2 values for each risk factor. It should be realized that a
adverse risk factors (16, 33), our method allows the risk factor small difference between the 2 indexes, which indicates that their
sum to be used as a continuous variable. predictive abilities are similar, could be statistically significant.
However, this small difference would have little practical im-
Statistical analyses portance.
The analyses, which were performed with the use of SAS
software (version 9.1; SAS Institute Inc, Cary, NC) and R [ver-
sion 2.4.1; R Foundation for Statistical Computing, Vienna, Aus- RESULTS
tria (34)], first examined the ability of BMI-for-age and waist- Mean measures of various characteristics are shown in Table
to-height ratio to identify children with adverse measures of each 1. The mean BMI-for-age z score was 0.46, and 17% of the
risk factor. We calculated the positive predictive value (the pro- children were overweight; BMIs did not differ significantly be-
portion of children with a high BMI or waist-to-height ratio who tween boys and girls. The mean waist-to-height ratio was 0.458,
actually have adverse risk factors) and the sensitivity (the pro- and measures of waist, height, waist-to-height ratio, and SBP
portion of children with adverse risk factors who have a high BMI were slightly but significantly higher among boys than among
or waist-to-height ratio) for each risk factor. Because these val- girls. In contrast, girls had slightly but significantly higher con-
ues depend on the cutoff used for BMI and waist-to-height ratio, centrations of total cholesterol:HDL cholesterol, triacylglycer-
we also examined the receiver operating characteristic curve for ols, LDL cholesterol, and fasting insulin than did boys. Measures
each risk factor. These curves are constructed by plotting the of the risk factor sum, an overall summary of the 6 age- and
sensitivity at each value of BMI-for-age or waist-to-height ratio sex-adjusted risk factors, ranged from 9 to 11, with a mean
compared with the corresponding 1-specificity, and the area un- value of 0. Age was associated with BMI (r 0.48), waist
der the curve (AUC) quantifies the screening performance over circumference (r 0.59), and height (r 0.90) but not with
all cutoffs. An AUC of 0.5 indicates that the screening test is no BMI-for-age (r 0.02) or waist-to-height ratio (r 0.01).
better than chance, and 1.0 indicates perfect classification. The Among the 276 children who were reexamined by the same
statistical significance of the difference (35) in AUCs between observer, the intraclass correlations between the repeated mea-
BMI and waist-to-height ratio was calculated by using MED- surements were 0.997 (BMI) and 0.949 (waist-to-height ratio),
CALC software (version 9.1.0.1; MedCalc Software, Mari- and the coefficients of variation were 1% (BMI) and 3% (waist-
akerke, Belgium). to-height ratio).
Regression models were also used to quantify the prediction of The abilities of BMI-for-age and waist-to-height ratio to cor-
risk factor measures by both indexes. (The original, unadjusted rectly identify children with adverse risk factors are compared in
measures of the risk factors were used as the dependent variable Table 2. The AUCs, positive predictive values, and sensitivities
in these models.) These analyses compared the increases in the varied substantially across risk factors, with the most accurate
multiple R2 values achieved by adding either BMI-for-age z score classification seen for fasting insulin concentrations. For each
36 FREEDMAN ET AL

TABLE 1 (sensitivities of 0.426 and 0.463 for total cholesterol:HDL cho-


Characteristics of the subjects1 lesterol). On the basis of statistically significant (P 0.05) dif-
Boys Girls ferences in the AUCs, BMI-for-age was a slightly better predic-
(n 1501) (n 1565) tor of adverse SBP measures, whereas waist-to-height ratio was
a slightly better predictor of adverse concentrations of total cho-
Age (y) 11 32 11 3
Black (%) 43 44
lesterol:HDL cholesterol. (All differences, however, were
BMI (kg/m2) 20.0 4.8 20.2 5.2 0.03.) The abilities of BMI-for-age and waist-to-height ratio to
BMI-for-age z score 0.5 1.1 0.4 1.1 correctly identify children with adverse measures of the risk
Overweight (%) 17 16 factor sum were similar (AUCs of 0.85 and 0.86). We also ex-
Waist circumference (cm) 68 143 66 123 amined possible differences in the AUCs for the risk factor sum
Height (cm) 148 203 145 173 by race, sex, and age group (11 y or 11 y old). Although some
Waist-to-height ratio 0.46 0.063 0.45 0.063 differences were observed across strata (eg, the AUC for waist-
Total-to-HDL cholesterol ratio 3.2 0.83 3.4 0.93
to-height ratio was 0.87 among white children and 0.82 among
Triacylglycerols (mg/dL)4 67 (52, 92)5 73 (57, 98)5
LDL cholesterol (mg/dL) 101 253 104 263
black children), within each strata, the AUCs for BMI-for-age
HDL cholesterol (mg/dL) 54 12 53 12 and waist-to-height ratio were almost identical.
Fasting insulin (mU/L)4 8.6 (6.4, 12.0)5 10.0 (7.7, 14.0)5 We then compared the additional information, quantified by
SBP (mm Hg) 103 103 102 103 the multiple R2, provided by BMI-for-age and waist-to-height
DBP (mm Hg) 62 9 62 9 ratio in predicting measures of the various risk factors (Table 3).
Risk factor sum 03 03 Race, sex, and age (first column) could account for 4% (LDL

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1
The numbers of children with missing data for the individual risk cholesterol) to 34% (DBP) of the variability in the individual risk
factors ranged from 0 (SBP and DBP) to 572 (fasting insulin). There were 573 factors. BMI-for-age and waist-to-height ratio (second and third
children with missing information on the risk factor sum. SBP, systolic blood columns) could account for an additional 3% (BMI-for-age com-
pressure; DBP, diastolic blood pressure. pared with LDL cholesterol and waist-to-height ratio compared
2
x SD (all such values). with DBP) to 27% (BMI-for-age compared with fasting insulin)
3
Significant difference for sex, P 0.001 (t test).
4 of the variability in risk factor measures. Although some of the
Values are median; 25th and 75th percentiles in parentheses.
5
Significant difference for sex, P 0.001 (t test, or Wilcoxon test for
differences between the 2 indexes were statistically significant,
triacylglycerols or fasting insulin). the magnitudes of all differences were small. For example, al-
though waist-to-height ratio was a better (P 0.001) predictor of
total cholesterol:HDL cholesterol, the difference in R2 values
was only 0.024. Similarly, BMI-for-age was a better predictor of
risk factor, however, only small differences were observed be- measures of fasting insulin, SBP, and DBP, but the largest R2
tween the accuracies of the BMI-for-age and waist-to-height difference was 0.034. The prediction of the risk factor sum by the
ratio. The largest differences between any of the AUCs, positive 2 indexes was almost identical (R2 0.32 for each index) As
predictive values, and sensitivities of the 2 indexes were 0.037 indicated in the final column, the use of the 2 indexes together

TABLE 2
Classification of adverse risk factor by BMI-for-age z score and waist-to-height ratio1

Area under the curve Positive predictive value Sensitivity

BMI-for-age Waist-to-height BMI-for-age Waist-to-height BMI-for-age Waist-to-height


Risk factor2 Subjects z score ratio z score ratio3 z score ratio3
n
Total-to-HDL cholesterol ratio 2961 0.734 0.764 0.26 0.28 0.43 0.46
Triacylglycerols 2624 0.74 0.75 0.28 0.28 0.47 0.48
LDL cholesterol 2961 0.61 0.62 0.16 0.18 0.27 0.30
HDL cholesterol 2961 0.67 0.68 0.21 0.22 0.35 0.36
Fasting insulin 2494 0.81 0.79 0.34 0.33 0.57 0.56
SBP 3066 0.684 0.654 0.19 0.20 0.33 0.33
DBP 3066 0.59 0.60 0.13 0.14 0.22 0.24
Risk factor sum 2493 0.85 0.86 0.38 0.38 0.64 0.65
1
The area under the curve summarizes the sensitivity and specificity of BMI-for-age and waist-to-height ratio over all values of the index (see Subjects
and Methods). Positive predictive value is the proportion of children with a high BMI-for-age (or waist-to-height ratio) who had an adverse risk factor.
Sensitivity is the proportion of children with an adverse risk factor who had a high BMI-for-age (or waist-to-height ratio). SBP, systolic blood pressure; DBP,
diastolic blood pressure.
2
The race-, sex-, and age-adjusted risk factors were used in the analyses.
3
The cutoff (0.512) for waist-to-height ratio was selected so that equal (17%) proportions of the children would be overweight and would have a high
waist-to-height ratio.
4
Significant difference in area under the curve, P 0.05 [as assessed by formulas in Hanely et al (35)]. The SE of each area under the curve difference
was 0.01.
CHILDHOOD BMI, WAIST-HEIGHT RATIO, AND CARDIOVASCULAR RISK 37
TABLE 3
Variability in risk factors that can be accounted for by BMI-for-age z scores or waist-to-height ratios in various regression models1
Increase in multiple R2 values

Multiple R2 values BMI-for-age z


based on race, sex, BMI-for-age Waist-to- score and waist-
Risk factor2 Subjects and age z score height ratio to-height ratio
n
Total-to-HDL cholesterol ratio 2961 0.05 0.143 0.163 0.16
Triacylglycerols 2624 0.10 0.12 0.13 0.14
LDL cholesterol 2961 0.04 0.033 0.043 0.05
HDL cholesterol 2961 0.13 0.09 0.09 0.10
Fasting insulin 2494 0.21 0.273 0.243 0.28
SBP 3066 0.29 0.083 0.053 0.09
DBP 3066 0.34 0.063 0.033 0.06
Risk factor sum 2493 0 0.32 0.32 0.34
1
Age, BMI-for-age, and waist-to-height ratio were modeled by using restricted cubic splines with 5 knots. Regression models also contained the interaction
between BMI-for-age z score or waist-to-height ratio with age. SBP, systolic blood pressure; DBP, diastolic blood pressure.
2
The original, unadjusted risk factors were used as the dependent variable. The multiple R2 for the model predicting the risk factor sum from race, sex,
and age is 0 because the risk factor sum is based on standardized measures of the risk factors.

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3
Significant P 0.05 difference in multiple R2 values of a model containing BMI-for-age z score and a model containing waist-to-height ratio in the
prediction of risk factor measures, P 0.05. To calculate statistical significance, predicted measures of each risk factor were first calculated from the 2 regression
models. The difference in the correlations between these predicted and actual measures was assessed as suggested by Meng et al (36).

yielded multiple R2 values that were only slightly higher than had a high BMI-for-age relative to waist-to-height ratio (6 upper
those obtained with the use of either index. For example, the right cells; x 0.21) was almost identical to the mean measure
multiple R2 for the risk factor sum based on both BMI-for-age among children who had a high waist-to-height ratio relative to
and waist-to-height ratio was 0.34, whereas the R2 for each index BMI-for-age (6 lower left cells; x 0.19; P 0.88). Compa-
alone was 0.32. rable analyses for the individual risk factors indicated that chil-
Despite the similarity of the multiple R2 values for the 2 in- dren with a relatively high waist-to-height ratio had slightly
dexes, additional analyses indicated that associations with BMI-
for-age were more curvilinear than those with waist-to-height
ratio. Predicted measures of several risk factors based on regres- 120 120

sion models containing either BMI-for-age (left panels) or waist- SBP (mm Hg)
100 100
to-height ratio (right panels) for an 11-y-old white girl are shown
in Figure 1. (Predicted measures for boys and black children TG
80 80
would be shifted vertically, but they would parallel the curves in (mg/dL)
Figure 1.) Nonlinearity was most evident in the relation of BMI- 60 60
for-age to concentrations of triacylglycerol (upper left panel), HDL-C
fasting insulin, and the risk factor sum (bottom left panel) but was 40 (mg/dL) 40
also observed for SBP and HDL cholesterol. Furthermore, for -2 -1 0 1 2 3 0.4 0.5 0.6 0.7

each risk factor, the strength of the association increased (steeper 25 25


slope) at higher measures of BMI-for-age. Associations with
Fasting
waist-to-height ratio (right panels), in contrast, were more linear, 20 insulin 20
and the difference between the 2 indexes was particularly evident (U/L)
for triacylglycerol concentrations. Although waist-to-height ra- 15 15
tio showed a nonlinear association (P 0.001) with fasting
insulin concentrations, the change in slope was less marked than 10 10
RF Sum
with BMI-for-age.
We then examined measures of the risk factor sum among 5 5
children after a cross-classification of categories of BMI-for-age -2 -1 0 1 2 3 0.4 0.5 0.6 0.7
and waist-to-height ratio (Table 4). Waist-to-height ratio mea- BMI-for-age z score Waist-to-height ratio
sures were categorized so that equal numbers of children would
FIGURE 1. The relation of BMI-for-age z score (left) and waist-to-height
be in each waist-to-height ratio and BMI group. Despite the small
ratio (right) to risk factor (RF) measures. Predicted measures (for an 11-y-old
number of children in some of the discordant categories (cells white girl) were calculated from regression models that included BMI-for-
above and below the shaded diagonal), the mean risk factor sum age or waist-to-height ratio, in addition to age, sex, race, and the interaction
tended to increase with measures of both BMI-for-age and waist- of BMI-for-age (or waist-to-height ratio) with age. Continuous variables
to-height ratio. Because of residual confounding, however, these were modeled by using splines with 5 knots, and the nonlinear effect of
BMI-for-age was statistically significant (P 0.001) for each of the 5 RFs.
apparent independent effects should be interpreted cautiously. So that the RF sum and fasting insulin could be plotted in the same figure, 9.0
A comparison of measures of the risk factor sum in the 2 discor- was added to the former. The units for each RF are shown in parentheses.
dant groups indicated that the mean measure among those who SBP, systolic blood pressure; TG, triacylglycerols.
38 FREEDMAN ET AL

TABLE 4
Measures of the risk factor sum cross-classified by BMI-for-age and waist-to-height ratio1

BMI-for-age percentile

50th 84th 85th94th 95th


50th Percentile Percentile Percentile Percentile
Waist-to-height ratio (n 869) (n 825) (n 382) (n 417)

0.426 (n 869) 1.5 2.3 (623) 1.0 2.4 (240) 1.6 2.9 (4) 0.9 3.3 (2)
0.4260.466 (n 825) 1.0 2.5 (233) 0.4 2.4 (468) 0.2 2.5 (115) 1.1 1.7 (9)
0.4670.512 (n 382) 1.4 2.0 (13) 0.4 2.4 (107) 1.1 2.6 (187) 1.6 2.4 (75)
0.513 (n 417) (0) 0.7 2.2 (10) 1.6 2.8 (76) 3.3 2.5 (331)
1
All values are x SD; n in parentheses. Four hundred forty-five children had a high BMI-for-age relative to waist-to-height ratio (6 upper right cells);
439 children had a high waist-to-height ratio relative to BMI-for-age (6 lower left cells), and 1609 children were concordant for measures of BMI-or-age and
waist-to-height ratio (shaded cells along diagonal).

higher concentrations of total cholesterol:HDL cholesterol and DISCUSSION


LDL cholesterol, whereas those with a high BMI-for-age had Our results show that there is little difference in the abilities of
slightly higher concentrations of fasting insulin (P 0.05 for BMI-for-age and waist-to-height ratio to identify children with

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each difference). adverse CVD risk factors. In general, waist-to-height ratio
Measures of BMI-for-age and waist-to-height ratio for each showed slightly stronger associations with lipid and lipoprotein
child, with the triangles representing children who had a high risk concentrations, whereas BMI-for-age showed slightly stronger
factor sum, are shown in Figure 2. The strong association be- associations with measures of fasting insulin and blood pres-
tween the 2 indexes is evident, and regression models indicated sures. Although some of the differences between the 2 indexes
that measures of BMI-for-age could account for 78% of the were statistically significant, the AUCs, positive predictive val-
variability in measures of waist-to-height ratio. Furthermore, the ues, sensitivities, and multiple R2 values were similar for each
identification of high measures of the risk factor sum by waist- risk factor. Furthermore, the use of both BMI-for-age and waist-
to-height ratio (horizontal line) and BMI-for-age (vertical line) to-height ratio resulted in only slightly better prediction of risk
did not differ. Of the 250 children with a high risk factor sum, 145 factors than that achieved with only one index. The strong asso-
(58%) had high measures of both indexes (upper right), 14 (6%) ciation between BMI-for-age and waist-to-height ratio (R2
had high measures of BMI-for-age only (lower right), 15 (6%) 0.78) probably accounts for their similar predictive abilities, as
had high measures of waist-to-height ratio only (upper left), and well as for the small amount of additional information obtained
76 (30%) did not have high measures of either (lower left).
by using the 2 indexes together.
Various indexes of abdominal obesity (such as waist circum-
ference, waist-to-hip ratio, and waist-to-height ratio) are associ-
0.8 ated with adverse risk factors among children (1315) and are
predictive of type 2 diabetes and CVD in adulthood (2 8). The
limitations of these indexes, however, should be considered. For
0.7 example, although waist circumference is correlated with the
amount of intraabdominal visceral fat, which may be the most
Waist-to-height ratio

detrimental fat depot (9), it is also associated with subcutaneous


0.6
abdominal fat and with total body fat (38, 39). In addition, a
recent study of adults found that waist-to-height ratio and BMI
were more strongly associated with each other (r 0.85 0.91)
0.512 than with percentage of body fat (r 0.69 0.76), as determined
0.5
by air-displacement plethysmography (19). These associations
emphasize the potential problems in using waist-to-height ratio
and BMI as indexes of abdominal and generalized adiposity,
0.4 respectively. The interpretation of associations with BMI and
CDC 95th percentile waist-to-height ratio is further complicated by the possible rela-
tion of disease risk to height (40), which is in the denominator of
0.3 both indexes.
-2 -1 0 1 2 3
Some investigators have concluded that, compared with BMI,
waist-to-height ratio is more strongly associated with CVD risk
BMI-for-age z score factors among children (1315) and adults (18, 19). It has been
FIGURE 2. Each point represents the BMI-for-age z score and waist-to- emphasized, however, that many of the differences between
height ratio of an individual child, and the overlaid curve was constructed by waist-to-height ratio and BMI are relatively small (19). For ex-
using lowess. , children with an adverse risk factor (RF) sum. The vertical
line represents the cutoff for overweight (a z score of 1.654 corresponding to
ample, Hara et al (14) reported that the logarithm of a risk factor
the 95th percentile), and the horizontal line is the cutoff (0.512) for waist- score showed correlations of r 0.50 (waist-to-height ratio) and
to-height ratio. CDC, Centers for Disease Control and Prevention. r 0.45 (BMI), and Hsieh et al (33) reported correlations of r
CHILDHOOD BMI, WAIST-HEIGHT RATIO, AND CARDIOVASCULAR RISK 39
0.37 (waist-to-height ratio) and r 0.33 (BMI) with a morbidity necessary to express measures as percentiles or z scores, relative
index among men. The slightly stronger relation of BMI-for- to a reference population, as is the case for BMI. (The correlation
age (compared with waist-to-height ratio) to measures of SBP between unadjusted and sex- and age-adjusted measures of
and DBP that we observed was also noted by others (15, 19). waist-to-height ratio was r 0.99, and the use of either adjusted
Several explanations are possible for the contrasting findings or unadjusted measures yielded virtually identical results.) The
about the relative importance of BMI-for-age and waist-to- calculation of waist-to-height ratio is also simpler, requiring only
height ratio. Various subsets of risk factors have been included in the division of numbers in the same units. Furthermore, the
each study, and only one previous study included an index of possible use of a single cutoff (0.5) to identify adverse measures
insulin resistance (19). (Of the risk factors we examined, fasting among both children and adults (21) would result in a simple
insulin concentrations showed the strongest association with public health message: Keep your waist circumference to less
BMI.) Furthermore, a study of 36 obese children found that than half your height. In the current study, 85% of overweight
insulin resistance was more strongly associated with total fat children had a waist-to-height ratio 0.5.
mass than with visceral abdominal fat (41). The weaker associ- However, the disease risks associated with BMI have been
ations with BMI that were found in previous studies of children studied much more extensively than have those for waist-to-
may be due to the investigators use of BMI rather than BMI- height ratio, and additional longitudinal data on waist-to-height
for-age (13, 14) or due to the fact that associations with BMI- ratio are needed. Furthermore, although the relation of childhood
for-age were constrained to be linear (14 16, 19). We found that BMIs to those in adulthood was examined in numerous studies
forcing the association with concentrations of fasting insulin to (reviewed in reference 44), we know of no study that has exam-
be linear reduced the R2 for BMI-for-age from 0.48 (nonlinear) to ined the tracking of waist-to-height ratios. In addition, although
0.43 (linear), whereas the R2 for waist-to-height ratio decreased the reproducibility of waist circumference measurements is high

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from 0.45 only to 0.44. These nonlinear associations may arise (45), we and others have found that it is lower than that of BMI
because BMI-for-age is a good indicator of adiposity among (19). This difference may limit the ability of waist-to-height ratio
relatively fat children, but it is an index of both fat and fat-free to detect small changes in obesity-related risk. Furthermore,
mass among thinner children (42). If BMI-for-age differences waist circumference has been measured at numerous sites be-
among some relatively thin (eg, BMI-for-age z score 1.0) tween the lowest rib and iliac crest, and there are differences
children largely reflect differences in fat-free mass, it would be between the recommendations of the Anthropometric Standard-
expected that the relation of BMI-for-age to risk factor measures ization Reference Manual (46), the World Health Organization,
would be flatter (Figure 1) among these children. and the National Institutes of Health (reviewed in reference 45).
The current study has several potential limitations that should Small changes in the location of the waist measurement can alter
be considered. Although the sample was not randomly selected, associations with risk factor measures (47 49) and possibly with
measures of BMI, lipids, and lipoproteins were fairly comparable disease risk.
to those reported in national studies (29). However, because of In summary, we found that waist-to-height ratio and BMI-for-
differences in methods of measuring blood pressure (28), few age showed similar associations with CVD risk factors. Al-
children in the Bogalusa Study had an SBP or a DBP 90th though the use of waist-to-height ratio among children has the
percentile of the National High Blood Pressure Education Pro- potential to simplify the assessment of obesity-related risk, ad-
gram (31). Furthermore, although it can be difficult to compare ditional information is needed on the tracking of waist-to-height
the magnitudes of the observed associations across studies be- ratio from childhood to adulthood, as are data relating waist-to-
cause of differences in statistical modeling techniques, age height ratio to morbidity and mortality.
ranges, and the specific anthropometric index examined, the
The authors responsibilities were as followsDSF: analyzed data, in-
magnitudes of the associations that we observed between BMI- terpreted results, and wrote the manuscript; HSK: interpreted results; ZM and
for-age and the examined risk factors agree well with those of LMG-S: analyzed data, interpreted results, and formulated study objectives;
other studies (43). WHD: formulated study objectives and drafted the manuscript; SRS and
Although several prospective studies found the indexes of GSB (principal investigator): data collection; and all authors: revised the
abdominal obesity to be stronger predictors of CVD and type 2 manuscript. None of the authors had a personal or financial conflict of
diabetes than is BMI (4 7), there are conflicting findings. For interest.
example, the predictive abilities of BMI and waist-to-height ratio
for type 2 diabetes among Pima Indians were almost identical (3),
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