Introduction. and waist ± hip ratio (WHR) have been recognized as useful alternatives to visceral fat measurement in epidemiological studies.

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1 (2000) 24, 1026±1031 ß 2000 Macmillan Publishers Ltd All rights reserved 0307±0565/00 $ Critical value for the index of body fat distribution based on waist and hip circumferences and stature in obese girls K Asayama 1 *, T Oguni 2, K Hayashi 3, K Dobashi 1, Y Fukunaga 2, K Kodera 1, H Tamai 3 and S Nakazawa 1 1 Department of Pediatrics, Yamanashi Medical University, Tamahocho, Nakakomagun, Yamanashi, Japan; 2 Department of Pediatrics, Osaka Medical University, Takatsuki, Osaka, Japan; and 3 Department of Basic Allied Medicine, School of Health Sciences, Faculty of Medicine, Gunma University, Maebashi, Gunma, Japan OBJECTIVE: To determine the critical value for the standard deviation score (SDS) of waist ± hip ratio (WHR)=height (Ht), as an age-adjusted measure of body fat distribution, in relation to occurrence of biochemical complications in obese girls. DESIGN: Cross-sectional, clinical study. The (WHR=Ht)-SDS was calculated as described previously. Obese girls were classi ed into two groups according to the occurrence of abnormal values in either serum triglyceride, alanine aminotransferase or insulin level. The criteria for obesity were subjected to the receiver operating characteristic (ROC) analysis. SUBJECTS: One-hundred and twenty-four outpatient Japanese obese girls, ranging in age from 9 to 15 y. MEASUREMENTS: Height, body weight, waist girth and hip girth as anthropometric measures. Percentage overweight, waist girth, WHR and (WHR=Ht)-SDS as criteria for obesity. Clinical laboratory analysis for fasting blood samples of obese children. RESULTS: Fifty-nine girls were classi ed into the no complication group, and 65 girls into the complication group. Those with complications were older, more obese, and their waist girth and WHR were larger, than the girls without complications. The (WHR=Ht)-SDS was >2-fold higher and lipoprotein pro le was more atherogenic in the complication group than in the no complication group. Among the four criteria of obesity, (WHR=Ht)-SDS gave the ROC curve skewed furthest into the top left corner of the diagram. Both sensitivity and speci city for (WHR=Ht)-SDS were >80% at the critical value of The sensitivity for waist girth was as high as that for speci city for the rest of the criteria were < 80%. CONCLUSION: Only (WHR=Ht)-SDS showed high enough sensitivity and speci city to predict metabolic derangement in the present obese girls. (WHR=Ht)-SDS can serve as the diagnostic criterion that classi es obesity in Japanese adolescent girls into two types. (2000) 24, 1026±1031 Keywords: obesity; body fat distribution; lipoproteins; insulin; fatty liver; children and adolescents Introduction Hypertriglyceridemia, hyperinsulinemia and an elevation of serum transaminase level due to fatty liver are the most common abnormalities in clinical blood biochemistry associated with childhood obesity. 1 Metabolic derangement induced by obesity is more signi cantly linked to accumulation of visceral fat than to that of subcutaneous fat. 2±4 The body fat patternings such as upper body obesity and abdominal obesity re ect visceral fat accumulation. Anthropometric measures such as waist girth, 5±8 abdominal sagittal diameter 9,10 11 ± 13 and waist ± hip ratio (WHR) have been recognized as useful alternatives to visceral fat measurement in epidemiological studies. *Correspondence: K Asayama, Department of Pediatrics, Yamanashi Medical University, 1110 Shimokato, Tamahocho, Nakakomagun, Yamanashi 409 ± 3898, Japan. kasayama@res.yamanashi-med.ac.jp Received 8 September 1999; revised 25 January 2000; accepted 7 April 2000 The normal value of WHR changes depending on the age of children and adolescents, 1,14 discouraging the use of this measure as anthropometric standard in this age group. We previously assumed that standardization of the criteria for obesity in children and adolescents should be based on the actual measures of body build observed in a large population including nonobese and obese subjects. 15 In such large population (n ˆ 1057) of Japanese school children, standard deviation scores (SDS) of WHR=height (Ht) turned out to be an index of body fat distribution adjusted for children between 6 and 15 y of age. 15 This index was deduced from the result of the principal component analysis. WHR=Ht, representing a body shape measure adjusted by the general size of an individual, gave a highly robust linear regression equation for age by gender. The age-dependence of the criteria for obesity was evaluated in the control children by each sex. 16 The waist girth and WHR were considered to be age-dependent variables, but percentage overweight and WHR=Ht SDS were age-independent variables. 16 The height-dependence of the waist girth

2 and WHR=Ht SDS was also evaluated by log=log regression. The contribution of height to the variation of WHR=Ht SDS was only 5%, while that of waist girth was approximately 40% in both sexes. 16 Further, (WHR=Ht)-SDS more strikingly distinguished obese children with biochemical complications from those without it than percentage overweight, WHR and waist girth did. 16 Male-type obesity 17,18 is more closely related to the complications than female-type obesity. Metabolic derangement is more common in boys than in girls of the same degree of obesity. 19 The degree of overweight and adiposity had less impact on metabolic derangement than that of body fat distribution in obese girls. 1,16 In general, biochemical complications as well as excess weight in obese children tend to worsen during growth. Thus, determining a critical value of an index of body fat distribution for occurrence of abnormal blood biochemistry is of particular importance in adolescent girls. The present study was designed to further characterize the clinical utility of (WHR=Ht)-SDS in obese girls aged 9 ± 15 y. By the analysis of the receiver operating characteristic (ROC) curve of (WHR=Ht)- SDS along with those of other criteria for obesity, we calculated a critical value for each criterion and then evaluated which anthropometric index was most powerful in detecting the occurrence of biochemical abnormalities in these children. Materials and methods Subjects A total of 124 obese Japanese girls who visited the Clinic for Obese Children in either Yamanashi Medical University, Yamanashi, or Hirakata Municipal Hospital, Osaka, Japan were enrolled in the present study. A child was considered to be obese when the body weight exceeded 120% of the standard body weight, which is de ned as the mean body weight corresponding to the height for that age obtained from national statistics for Japanese school children. The age of the subjects ranged from 9 to 15 y. They had no endocrine, metabolic or renal diseases other than obesity. They were instructed to visit the clinic in the morning, after an overnight fast. Blood was then drawn and, at the same time, they were subjected to anthropometric measurements including height, body weight, waist girth and hip girth. The Human Study Committee of Yamanashi Medical University approved this study. Informed consent was obtained either from each subject or from his or her parents as appropriate. Anthropometric measurements Anthropometric measurements were performed, as described previously. 1,15,16 In brief, height 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 waist girth at the level of the umbilicus, and hip girth at the level of maximum extension of the buttocks, to the nearest 0.1 cm, with the subject standing and following a normal expiration. The percentage overweight was calculated using a small programmed calculator (Pocket Growth Checker GEN-185, Sumitomo Pharmaceuticals Co., Osaka, Japan), based on the data collected in a 1990 nationwide survey of school children. The (WHR=Ht)-SDS was calculated for each sex, according to the previously described method. 16 The formulas used in the calculations were as follows: [(WHR=Ht (m)-( Age (year)))= ] for boys and [(WHR=Ht (m) ± ( ± Age (year)))= ] for girls. Biochemical analyses Serum total cholesterol (TC), triglyceride (TG), highdensity lipoprotein-cholesterol (HDL-C), apolipoproteins A 1,A 2, and B, and serum insulin were measured in the clinical laboratories of both hospitals. Normal values for these biochemical data differed minimally between the laboratories of the both hospitals. Lowdensity lipoprotein-cholesterol (LDL-C) was calculated from the Friedwald equation (LDL-C ˆ TC 7 HDL-C 7 TG=2.18). 21 The reference values of the serum biochemical indices were obtained from fasting samples of 121 nonobese children as described previously. 22 This group consisted of 69 boys and 52 girls, ranging in age from 6 to 15 (mean 10.0) y and with no history of endocrine, metabolic or renal diseases. There were no appreciable genderrelated differences among the clinical laboratory data in these children. The normal range was de ned as the values between the 10 and 90 percentile levels of the reference samples. TG >1.28 mmol=l, alanine aminotransferase (ALT) >29 U=l and insulin >115 pmol=l were considered to be abnormal. Obese girls were classi ed into two groups according to the occurrence of abnormal values in either serum TG, ALT or insulin level. Those who had abnormal values in at least one of these three indices were assigned to complication group and those without it to no complication group. This criteria for classi cation of the patients was the same as in our previous paper. 16 Statistical methods Data are presented as the means and standard errors of means (s.e.m.). Since the data for TG, ALT and insulin were signi cantly skewed, they were transformed logarithmically before performing a statistic analysis. The difference between the two means was estimated by the unpaired Student's t-test. The values were considered to be statistically signi cant at P < The receiver operating characteristic 1027

3 1028 (ROC) curves were analyzed by MedCalc software version , provided from Dr Frank Schoonjans, Mariakerke, Belgium. The rest of statistical analyses were performed using SPSS version 8.01J (SPSS Inc., Chicago, IL). Results Anthropometric data for obese girls Fifty-nine of 124 girls were classi ed into no complication group, and 65 girls into complication group (Table 1). The girls with complications were older than those without it. The body sizes including height, body weight, waist girth and hip girth were also larger in the girls with complications than those without it. The girls with complications were more obese, and their WHR were larger, than those without complications were. The (WHR=Ht)-SDS was > 2-fold higher in the complication group than in the no complication group. Biochemical data for obese girls According to the selection criteria, TG ( vs mmol=l), ALT (36 3 vs 17 1U=l) and insulin ( vs 75 4 pmol=l) were approximately 2-fold higher in the complication group than in the no complication group. The HDL-C and apo A 1 were lower, and conversely apo B and apob=apo A 1 were higher, in the complication group than in the no Table 1 Anthropometric data for the obese girls No complication (n ˆ 59) Complications (n ˆ 65) Age (y) ** Ht (cm) * Body weight (kg) ** Waist (cm) ** Hip (cm) ** Percentage overweight ** WHR ** WHR=Ht (WHR=Ht)-SDS ** Data are mean s.e.m. Student's t-test (unpaired). *P < 0.01; **P < complication group (Table 2). The levels of TC, LDL- C and apo A 2 were similar in both groups. Relationship between the criteria for obesity and biochemical ndings Table 3 summarizes the age-adjusted correlation between the criteria for obesity and biochemical data in all obese girls. All four criteria for obesity were closely correlated with ALT, insulin and TG. Both WHR and (WHR=Ht)-SDS were also closely related with TC, LDL-C, apo A 2, apo B and apo B= apo A 1, whereas percentage overweight and waist girth were less closely associated with such biochemical parameters. HDL-C were inversely correlated with percentage overweight but not with other indices. Apo A 1 was correlated with neither of the criteria for obesity. Table 2 Biochemical data for the obese girls No complication (n ˆ 59) Complications (n ˆ 65) Normal range a Total cholesterol (mmol=l) ± 5.06 HDL-cholesterol (mmol=l) ** 1.09 ± 1.73 LDL-cholesterol (mmol=l) ± 3.14 Apo A 1 (mmol=l) * 36.2 ± 54.6 Apo A 2 (mmol=l) ± 22.4 Apo B (mmol=l) ** 1.02 ± 1.60 Apo B=Apo A 1 (10 2 ) ** 2.25 ± 3.67 HDL, high-density lipoproteins; LDL, low-density lipoproteins. Data are mean s.e.m. Student's t-test (unpaired). a 10 and 90 percentile values for 121 nonobese children. 22 *P < 0.05; **P < Table 3 Correlation between the criteria for obesity and biochemical data in the obese girls (n ˆ 124) Correlation coefficients (r) a Percentage overweight Waist WHR (WHR=Ht)-SDS ALT b 0.390*** 0.427*** 0.474*** 0.436*** Insulin b 0.314** 0.383*** 0.418*** 0.294** Triglyceride b 0.299** 0.243** 0.310** 0.297** Total cholesterol * 0.328*** 0.329*** HDL-cholesterol * LDL-cholesterol * 0.299** 0.295** Apo A Apo A ** 0.400*** Apo B 0.226* 0.281** 0.366*** 0.346*** Apo B=Apo A * 0.265** 0.322** 0.294** a Correlation was adjusted for age as a covariate. b Data were transformed logarithmically before performing a correlation analysis. *P < 0.05; **P < 0.001; ***P <

4 ROC analysis of the criteria for obesity Figure 1 depicts the ROC curves for the four criteria of obesity. Among all criteria, (WHT=Ht)-SDS gives the curve skewed furthest into the top left corner of the diagram. The results of ROC analysis are summarized in Table 4. Again (WHR=Ht)-SDS has the largest area under the ROC curve among the four criteria studied. Waist girth has the second largest area under the ROC curve among the four criteria studied. Waist girth has the second largest area under the curve (AUC). The AUC for percentage overweight and WHR are smaller than those for the waist girth and (WHR=Ht)-SDS. The AUC for (WHR=Ht)-SDS was signi cantly larger than those for percentage overweight and WHR. The AUC for waist girth was also signi cantly larger than that for percentage overweight, but the difference between the AUC for waist girth and that for WHR was not signi cant. Both sensitivity and speci city for percentage overweight and WHR at the given respective cut-off points were < 80%. On the other hand, those for (WHR=Ht)- SDS were > 80% at the critical value of 2.00, which was obtained as the best t model. The sensitivity for waist girth was as high as that for (WHR=Ht)-SDS, whereas the speci city for waist girth was similar to those for percentage overweight and WHR. Figure 1 Receiver operating characteristic curves of the criteria for obesity. The obese girls (n ˆ 124) were classi ed into two groups according to the occurrence of abnormal values in either triglyceride, alanine aminotransferase or insulin. The curves were depicted by MedCalc software. Thick hatched line: percentage overweight; thin solid line: waist ± hip ratio (WHR); thick solid line: (WHR=Ht)-SDS; and thin hatched line: waist girth. Discussion The obese girls with complications were older and more obese than those without complication, conforming to the previous observations 20 that biochemical complications as well as excess weight in obese children tend to worsen during growth. Their (WHR=Ht)-SDS value was much higher than that of the no complication group, indicating that they were more centrally obese, and that abdominal obesity was linked to metabolic derangement in these obese girls. In our previous study, WHR=Ht SDS was independent of age and minimally affected by the height in control children while it was closely correlated with age in obese children. 16 Thus, the correlation pro le between age and anthropometric indices in the obese children differed from that in the control. The results suggested that the type of obesity changes with age in obese children. The older obese children tended to gain more fat at the umbilical level than the younger ones, and this was considered as the general worsening of body build during growth in obese children. The present nding that girls with complications are older than those without complication re ects the worsening of body fat distribution during growth. The levels of TC and LDL-C were similar in both groups. However, the lipoprotein pro le was more atherogenic in the complication group than in the no complication group, because HDL-C and apo A 1 were lower, apo B and apo B=apo A 1 ratio were higher in the former than in the latter. Impact of abdominal visceral fat accumulation on metabolic derangement is now under extensive study in adults. 5 ± 11,23,24 Abdominal visceral fat has recently been measured in children. 25,26 These studies have suggested that deleterious effects of visceral adipose tissue on lipid=lipoprotein risk factors seen in adults are already present in children. Predicting visceral fat from anthropometric measures such as waist girth, WHR and sagittal diameter has been attempted in both adults 8,10,27 and children. 28,29 Several recent adult studies have proposed that the waist girth better re ects visceral adipose tissue area, 5 insulin sensitivity 30 and glucose tolerance 31 than the WHR. Other investigators have suggested that sagittal diameter is a better correlate to visceral fat area than 1029 Table 4 ROC analysis of the criteria for obesity Percentage overweight Waist (cm) WHR WHR=Ht)-SDS The AUC a Cut-off value b Sensitivity (%) Speci city (%) Probability for comparison of ROC curves Percentage overweight Ð Waist Ð WHR Ð (WHR=Ht)-SDS Ð a Area under the ROC (receiver operating characteristic curves (mean s.e.m.). b The cut-off values were calculated as the best t model by MedCalc software.

5 1030 waist girth or WHR is. 10 However, WHR is still considered to be a good anthropometric surrogate of visceral adipose tissue in certain recent epidemiological studies in adults. 11,13,32 To date, no single anthropometric index has yet been generally accepted to be superior to others as a surrogate of visceral fat measurement. 11,27,29 WHR 33 but not visceral fat area 33,34 correlated with resting metabolic rate, suggesting that the anthropometric indices for body fat distribution are not just the alternatives to visceral fat measurement but also represent some aspect of physical tness. In univariate correlation analysis, all four criteria for obesity were equally well related to ALT, insulin and TG in the present obese girls. The normal value for WHR decreases sharply with growth in the girls of this age group. 14 Such physiological variability of the absolute value makes this index unsuitable for use as the clinical standard. Recently waist girth has been more commonly accepted as the anthropometric standard of abdominal obesity in adult studies than WHR. 5 ± 8,30,31,35 By calculating the optimal index powers minimizing the effect of Ht by linear regression analysis of log height vs log (waist girth), Han et al 36 reported that the height had no appreciable effect on the waist girth in adults. However, our previous study 16 revealed that the height signi cantly contributed to the variance in waist girth in children aged 6 ± 15 y. Thus, both waist girth and WHR are of limited use in children and adolescents because the normal values change depending on the age of subjects. The present ROC curves clearly indicated that (WHR=Ht)-SDS and waist girth were more optimal as the diagnostic criteria than percentage overweight or WHR. The data of speci city and sensitivity showed that (WHR=Ht)-SDS was a better criterion than the waist girth. (WHR=Ht)-SDS displayed by far the widest margin of difference between the two groups (ie greater than 2-fold) among all the criteria. The wide margin was certainly favorable for drawing a more optimal cut-off line of this index than in the case of the other indices. In fact, cut-off values for percentage overweight and waist girth, which were obtained as the computer best t model, were almost as low as the respective mean values for the no complication group, thereby giving low speci city to those indices. In conclusion, ROC analysis revealed that (WHR=Ht)-SDS was the best criterion of obesity among the four criteria studied here. Only (WHR=Ht)-SDS showed high enough sensitivity and speci city for predicting metabolic derangement in the present obese girls. Thus, (WHR=Ht)-SDS can serve as the diagnostic criterion that classi es the obesity in Japanese adolescent girls into two types. 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