European Journal of Clinical Nutrition (1999) 53, 468±472 ß 1999 Stockton Press. All rights reserved 0954±3007/99 $12.00 http://www.stockton-press.co.uk/ejcn Differences in the relationship between body fat and body mass index between two different Indonesian ethnic groups: The effect of body build S Gurrici1, Y Hartriyanti1, JGAJ Hautvast2 and P Deurenberg2* 1 School of Public Health, Gedung D Lt.II, University of Indonesia, Depok, Indonesia; 2Department of Human Nutrition and Epidemiology, Wageningen Agricultural University, The Netherlands Objective: To study the relationship between body fat percent (BF%) and body mass index (BMI) in two different Indonesian ethnic groups (Malays and Chinese) and to relate differences in the relationship to differences in body build and slenderness. Design: Cross-sectional study. Subjects: Except for ethnicity, not specially selected populations living on Java (Depok, south of Jakarta: Malay Indonesians, n 117) and on Sulawesi (Makale, north of Ujung Pandang: Chinese Indonesians, n 109). Measurements: Weight, height, sitting height, waist and hip circumferences and skeletal widths were measured. BMI was calculated and BF% was predicted from BMI, age and sex using a (Dutch) Caucasian prediction formula. Slenderness was expressed as the ratio of weight : sum of knee and wrist width. BF% assessed by deuterium oxide dilution was used as a reference. Results: BF% in the male and female Malay Indonesians was 24.6 7.0 and 35.6 5.6% respectively which was not signi®cantly different from the values in the male and female Chinese Indonesians (24.0 4.3 and 33.8 6.9%). BMI and age were signi®cantly lower in the Malay Indonesians. Malay Indonesians had a more slender body build in terms of skeletal widths compared to the Chinese Indonesians, and they had a higher slenderness index. BF% predicted from BMI using a Caucasian prediction formula was underestimated by 5.8 4.8% and 7.7 3.8% in the male and female Malay Indonesians but only by 1.3 3.0% and 1.7 3.7% in the male and female Chinese Indonesians. After correction for differences in age, sex and BF% the Malay Indonesians had a 1.7 0.3 kg=m2 (P < 0.0001) lower BMI than the Chinese Indonesians. After correcting for body build and relative sitting height the difference lowered to 0.9 0.4 kg=m2 (P < 0.02). Conclusions: The study con®rmed the results of an earlier study that Indonesians have a higher BF% at the same BMI compared to Caucasians, but that there are apparently also differences among Indonesian subgroups. These differences are at least partly related to differences in body build. Keywords: body fat percent; body mass index; body build; obesity; cut-off values; Indonesians; Malays; Chinese; race; ethnicity Introduction In obesity or adiposity the body fat percent (BF%) exceeds 25% in males and 35% in females (WHO, 1995; Deurenberg et al, 1998). BF% can be measured by a number of methods (Forbes, 1987; Lukaski, 1987; Deurenberg 1992), but most of them are rather laborious and not suitable for use in epidemiological surveys. In several studies a high correlation was found between body mass index (BMI) and BF% when age and sex are taken into account (Womersley & Durnin, 1977; Deurenberg et al, 1991; Gallagher et al, 1996), and therefore in most epidemiological studies BMI is used as an indicator of body fatness. The World Health * Correspondence: Dr Paul Deurenberg, Department of Human Nutrition and Epidemiology, Wageningen Agricultural University, Bomenweg 2, 6703 HD Wageningen, The Netherlands. E-mail: [email protected] Guarantor: S Gurrici. Contributors: Organization of the study was done by Gurrici for the Indonesian part and by Deurenberg and Hautvast for the Dutch part. The practical measurements were performed by Gurrici, Hartriyanti and Deurenberg. Data analysis was done by Hartriyanti and Deurenberg. Paper writing and discussion was a joint effort of all four authors. Received 7 September 1998; revised 7 January 1999; accepted 11 January 1999 Organization (WHO) suggests cut-off points for overweight and obesity at a BMI value 25 kg=m2 and 30 kg=m2 respectively (WHO, 1995, 1998). There are indications that the relationship between BMI and BF% is different among ethnic groups (Deurenberg et al, 1998). Recently we showed in a comparative study that Indonesians living in Palembang, Sumatra, have generally 4.8 percent points more body fat compared to Dutch subjects, having the same weight, height, age and sex. Indonesian having the same BF%, age and sex generally have a 2.9 kg=m2 lower BMI compared to the Dutch (Guricci et al, 1998). Differences between ethnic groups in the BMI=BF% relation are also found in other studies (Swinburn et al, 1996; Wang et al, 1994; Luke et al, 1997), but not in all (Gallagher et al, 1996; Deurenberg et al, 1997). These differences among ethnic groups could be due to differences in physical activity, people with lower physical activity level having relatively less muscle mass and thus more fat mass at the same body weight. Although this is certainly true at an individual level (for example, a body builder compared to an obese subject with a very sedentary life style) it may not be the only possible explanation at a population level. Also, body build could be responsible for a different BMI=BF% relationship. Norgan discussed in several papers the impact Relationship between BF% and BMI in Indonesia S Gurrici et al of relative sitting height (in fact leg length) on BMI (Norgan, 1994a, b), but this effect was not found by others (Fehily et al, 1990). Also body build in term of frame size and thus skeletal mass could be responsible for a different relationship between BMI and BF% (Deurenberg et al, 1998; Guricci et al, 1998; Fehily et al, 1990; Rookus et al, 1985). In addition, a more stocky build is likely to coincide with more muscle and connective tissue and would for that reason add to a higher fat free mass=fat mass ratio at the same BMI. To test the hypothesis that differences in body build can be responsible for differences in the BMI=BF% relationship, two Indonesian population groups of different ethnic background were studied. The study is part of a larger epidemiological study carried out in Indonesia to get insight into body composition and body composition differences between ethnic groups. until analyses. Deuterium in plasma was analysed by infrared spectroscopy after sublimation of the plasma (Lukaski & Johnson, 1985). Total body water (TBW) was calculated from the given dose and the deuterium concentration in plasma, after correcting for 5% non-aqueous dilution of deuterium (Forbes, 1987). Fat free mass (FFM) was assessed from TBW assuming 0.726% hydration of the FFM (Pace & Rathbun, 1945). BF% was calculated as 100* weight ÿ FFM=weight BF% was also predicted from BMI with age- and sexspeci®c prediction formulas using a formula developed in a Dutch population (Deurenberg, 1992): BF% 1:20*BMI 0:23*age ÿ 10:8*sex ÿ 5:4 1 and a formula developed in an Indonesian population (Guricci et al, 1998): BF% 1:30*BMI ÿ 9:8*sex 6:4 Subjects and methods Subjects from two different ethnic groups participated in the study. The measurements were performed at two different sites in Indonesia within two weeks and the same investigators performed the same standardised measurements. In Depok, located on Java, about 40 km south of Jakarta, 117 Malay Indonesians were measured. Most of them were co-workers of the University of Indonesia. In Makale, a small city on Sulawesi, about 250 km north of Ujung Pandang, 109 subjects of Chinese ancestry were measured. They were predominately personnel of a regional public health centre. At both study sites the subjects were measured in the morning hours, at least 2 hours postprandial but most of them were in the fasting state from the preceding evening. Body weight was measured without shoes on an electronic weighing scale, accurate to 0.1 kg. To correct for clothing 1 kg was subtracted from the readings. Body height (without shoes) was measured to the nearest 0.5 cm with a wall-mounted stadiometer. Body mass index (BMI, weight=height2, kg=m2) was calculated. Sitting height was also measured and relative sitting height was calculated as sitting height=standing height. Skinfold thickness was measured at four sites (biceps, triceps, subscapular, supra-iliac) on the left side of the body, and body fat percent (BF%) was calculated according to Durnin & Womersley (1974). Waist circumference was measured midway between the lower rib margin and the iliac-crest to the nearest 0.5 cm. Hip circumference was measured over the great trochanters to the nearest 0.5 cm. From waist circumference BF% was predicted using the formula of Lean et al (1996). Wrist width (over the radius and the ulna) and knee width (over the femur) was measured to the nearest mm on the left and right side of the body. Mean values of left and right sides were used in calculations. Skeletal mass was predicted using the formulas of von DoÈbeln (1959), based on height, knee and wrist width. An index of slenderness was calculated as height=(sum of wrists and knee widths). Obviously, a higher index indicates a more slender body build. After the anthropometric measurements had been taken, the subjects drank an accurately (to 0.01 g) weighed dose of 10 g deuterium oxide. After 2.5 ± 3 h a venous blood sample was drawn and plasma was separated and stored at 7 10 C 2 Data were analysed using SPSS (release 7.5) for Windows (SPSS=Windows, 1995). Differences between variables in the same subjects were tested by Student's paired t-test. Differences between groups were tested by analysis of (co)variance, using the GLM procedure. Stepwise multiple linear regression was used with gender and site coded as dummy variable (females 0, males 1; Depok 0, Makale 1). Differences between measured and predicted values (residuals) were evaluated with the technique described by Bland & Altman (1986). Differences were regarded as statistical signi®cant if P < 0.05 (two-sided, where appropriate). Values are given as mean s.d., unless otherwise indicated. Results Table 1 gives some physical characteristics of the subjects. The subjects in Depok were younger and were slightly taller compared to the subjects in Makale. Relative sitting height was slightly different between the two sites but was signi®cant only in males. BF% as assessed by deuterium oxide dilution was not different between males in Depok and Makale, but the sum of skinfolds was lower, although not signi®cant (P 0.11) in Depok. Wrist and knee widths were signi®cantly lower in the subjects in Depok. This is more noticeable as the subjects in Depok were taller. The slenderness index height=(sum wrist and knee width) was greater (P < 0.05) in the Depok subjects, especially in females (11.65 0.50 and 12.63 0.72 in Depok males and females compared to 11.23 0.50 and 11.60 0.65 in Makale males and females respectively). Calculated skeletal mass was 9.7 0.9 kg and 7.2 0.7 kg in Depok and 9.6 1.1 and 7.3 0.7 kg in Makale in males and females respectively, which is not signi®cantly different between the sites within the gender groups. After correcting for the lower body height in the Makale subjects', skeletal mass was 0.7 0.1 kg (mean s.e.) lower in the Depok females and 0.3 0.1 kg lower in the Depok males, compared to Makale females and males respectively. In Table 2, BF% as measured and as predicted, using prediction formulas from the literature, is given. Most prediction formulas did not give valid results. The bias was generally more pronounced in females and more 469 Relationship between BF% and BMI in Indonesia S Gurrici et al 470 Table 1 Characteristics of the subjects (mean s.d.) Depok Age (y) Height (cm) Sitting height (cm) Relative sitting height Weight (kg) Body mass index (kg=m2) Sum four skinfolds (mm) Wrist width (mm) Knee width (mm) Waist circumference (cm) Hip circumference (cm) Body fat (%) Makale Males (n 59) Females (n 58) Males (n 48) Females (n 61) 34.0* 10.1 164.8* 5.6 84.4* 2.7 0.52* 0.01 61.4ns 9.3 22.6* 3.1 53.0ns 21.4 52.1* 2.9 88.5* 5.5 80.5ns 9.0 90.5ns 6.5 24.6ns 7.0 30.6* 10.0 154.3* 5.3 80.0* 2.7 0.52ns 0.01 52.3ns 8.0 21.9* 2.7 69.4ns 19.7 44.3* 3.4 78.3* 5.9 77.0ns 8.1 91.0ns 5.6 35.6ns 5.6 44.1 9.4 161.5 5.9 85.4 4.1 0.53 0.01 62.7 9.4 24.0 3.0 60.3 24.7 52.7 2.4 91.3 6.2 83.5 10.0 91.4 6.2 24.0 6.3 42.5 8.4 149.6 3.6 79.0 2.4 0.53 0.01 51.6 8.3 23.1 3.7 69.4 21.8 47.0 2.7 82.4 6.7 79.3 9.9 90.5 7.7 33.8 6.9 *P < 0.05, ns not signi®cant between the two study sites within the gender group. Table 2 Body fat as assessed by deuterium oxide dilution and as predicted using prediction formulas from the literature (mean s.d.) Depok BF% assessed by: 1 Deuterium oxide dilution Body mass index2 Body mass index3 Skinfold thickness4 Waist circumference5 Makale Males Females Males Females 24.6* 7.0 18.7* 5.0 26.5 4.1 21.8* 6.7 17.6* 5.5 35.6 5.6 28.0* 4.6 35.0 3.5 31.9* 4.8 32.5ns 4.7 24.0 6.3 22.7* 4.7 28.3* 3.9 25.9* 7.1 22.7* 4.7 33.8 6.9 32.0* 5.4 36.5* 4.8 34.1* 5.3 34.8* 5.4 * P < 0.01 from deuterium oxide dilution; ns not signi®cant from deuterium oxide dilution Assuming a 73% hydration of the fat free mass (Pace & Rathbun, 1945) 2 Using the prediction formula: BF% 1.20*BMI 0.23*age 7 10.8*sex 7 5.4 (Deurenberg et al, 1991) 3 Using the prediction formula: BF% 1.30*BMI 7 9.8*sex 6.4 (Guricci et al, 1998) 4 Using the age and sex speci®c prediction equations of Durnin & Womersley (1974) 5 Using the prediction equations 0.567*waist 0.101*age 7 31.8 for males and 0.439*waist 0.221*age 7 9.4 for females (Lean et al, 1996). 1 pronounced in Depok, except for the prediction based on waist circumference. A prediction equation for BF% based on BMI developed in another Indonesian population) gave valid results in the Depok group but overestimated BF% in the Makale group. Figure 1 gives the Bland & Altman plots for the difference between measured (from deuterium oxide dilution) and predicted BF% from BMI against BF% as assessed by deuterium oxide dilution for the two sites per sex. The correlation of the residual with BF% is relatively high. In Table 3 the partial correlation (after correcting for BF%) is given between the residuals of predicted BF% using equation (1) and parameters of body build, including relative sitting height. The partial correlation is highest for `slenderness' in both sexes and after correcting for level of body fatness and slenderness no other parameter remained signi®cant. Generally the correlations were higher in females. Analysis of co-variance was performed to test the effect of slenderness on the relation between BMI and BF%. After correcting for differences in BF%, age and sex (explained Figure 1 Residuals of measured and predicted BF% in relation to measured body fat in the Depok and the Makale population. (Measured minus predicted BF%: measured body fat percent by deuterium oxide dilution minus predicted body fat percent from the body mass index (formula from Deurenberg et al, 1991). j males; . females. Relationship between BF% and BMI in Indonesia S Gurrici et al Table 3 Partial correlation between residual of predicted body fat and measures of body build after correcting for level of body fatness BF% Correcting for Height Relative sitting height Skeletal mass Total width Slender BF% & slenderness Males Females Males Females 0.14ns 7 0.21* 7 0.15ns 7 0.36* 0.51* 0.27* 7 0.27* 7 0.33* 7 0.47* 0.55* 0.10ns 7 0.15ns 0.09ns 0.10ns ± 0.09ns 7 0.18ns 0.01ns 0.05ns ± *P < 0.05; ns not signi®cant. BF% body fat percent; slenderness height=(sum wrist and knee width). variance: 0.53) the Malay Indonesians (Depok) had a 1.7 0.3 kg=m2 (mean s.e.) lower BMI than the Chinese Indonesians (Makale). Additional correction for slenderness decreased the difference in BMI between the two population groups to 1.1 0.4 kg=m2 with an explained variance of 0.64. The effect of slenderness was highly signi®cant (P < 0.0001). Inclusion of relative sitting height in the model lowered the difference in BMI between the two groups to 0.9 0.4 kg=m2 (P < 0.02). Discussion The subjects participating in this study cannot be regarded as representative for the total population on Western Java (Depok) or on southern Sulawesi (Makale). For logistic reasons university workers and government employees were chosen for this study, but the subjects were not specially selected except for race. The population of Makale (Toraja land) is a special ethnic group with Chinese ancestry and is as such different from the subjects measured in Depok which did not include ethnic Chinese. Although the subjects in Makale were generally older and had a higher BMI their BF% was not higher and their skinfold thickness did not differ from the subjects in Depok. As age is a possible confounder in the relationship between BMI and BF%, age was adjusted in comparative analyses between the groups. In both population groups, BF% predicted with a Caucasian prediction formula (Deurenberg et al, 1991), using BMI, age and sex as predictive variables, underestimated the actual BF%, in Depok much more than in Makale. The results of this study con®rm results of previous studies in Indonesia on the relationship between BMI and BF%, showing higher BF% at relatively low levels of BMI compared to Caucasians (Guricci et al, 1998; KuÈpper et al, 1998). This phenomenon is not limited to Indonesians. Studies in other Asian population groups also found relatively high body fatness compared to the BMI (Wang et al, 1994; Stevens, 1997) but a study in Beijing Chinese could not con®rm this (Deurenberg et al, 1997). Other authors studied the relationship between BF% and BMI among different ethnic groups and sometimes came to different conclusions. Gallagher et al (1996) found no difference in the relationship between BF% and BMI between American Blacks and American Caucasians, living in New York. However, Luke et al (1997) found differences between Black populations living on Jamaica, Nigeria and in the USA. These authors ascribed the differences to differences in the level of energy intake in combination with physical activity. The reason for differences in the relationship between BMI and BF% among different ethnic groups is, however, unclear and could theoretically be due to several factors. Relative sitting height, known to be related to BMI, is slightly lower in the Depok group. According to Norgan (1994) the lower relative sitting height of 0.01 in the Depok population theoretically coincided with a lower BMI of 0.88 kg=m2. Correcting for this lower BMI would increase predicted BF% with about 1 percent point. However, in the present study relative sitting height and BMI were not correlated, neither in the total group, nor in sex and site de®ned subgroups, which could be partly due to the high variability in this parameter. A higher level of physical activity results in relatively more muscle tissue at the same body weight and could also be responsible for the different relationship between BMI and BF% (Wang et al, 1994). For the present study no information was available on physical activity of pattern of the subjects but it seems unlikely that differences in physical activity alone are responsible for the relatively large differences. The groups can be assumed to have the same activity pattern during working hours (of®ce work) and weather conditions in tropical countries do not invite strenuous physical activities during leisure time, therefore a large difference in physical activity due to leisure time activities seems unlikely. A third possibility is that subjects differ in body build, in fact in skeletal mass. Differences in skeletal mass in subjects with the same height are relatively small (von DoÈbeln, 1959), and several studies failed to show an impact of body build on the prediction of BF% from BMI (Fehily et al, 1990; Rookus et al, 1985; Baecke et al, 1982). However, it can be argued that a more slender build is coincided with less muscle and less connective tissue. This means that subjects with a slender build, having the same height and weight, will have a lower fat free mass=fat mass ratio, thus will have higher BF% at the same BMI. In the present study differences between measured and predicted BF% among the two studied groups were found. The group showing the highest underestimation of BF% from BMI had a more slender body build and an index of slenderness was signi®cantly correlated with the residual of measured and predicted body fat (Table 3). Compared to the Dutch population in which the prediction formula for body fat from BMI was developed (Deurenberg et al, 1992) both Indonesian groups were more slender, specially the Depok group and skeletal mass was lower (results not shown). The difference in BMI between the two population groups, after correcting for BF%, age and sex was 1.7 0.3 kg=m2. After correcting for slenderness and relative sitting height this difference decreased to 0.9 0.4 and was only borderline signi®cant (P < 0.02) from zero. The variation in measured minus predicted BF% is high and depends on the level of body fatness (Figure 1). This dependency on the level of body fatness is also found in other studies (Guricci et al, 1998; Deurenberg et al, 1997) and can be explained by the nature of the prediction formula: excess body weight has a higher fat=fat free ratio which is not accounted for in the formula. Thus the formula will underestimate at higher levels of body fatness. The mean BMI value of the Indonesian population is, however, not different from the BMI value of the Dutch population in which the prediction formula was developed (Deurenberg et al, 1991), hence, this can be no reason for the underestimation of BF% using this formula. The ratio of skeletal mass and FFM in the two Indonesian samples was 0.216 0.018 in females and 0.208 0.017 in males (P < 0.001). Assuming a constant 471 Relationship between BF% and BMI in Indonesia S Gurrici et al 472 fraction of the skeletal mass in the FFM, the lower skeletal mass (after correcting for height) in the Depok subjects can be calculated to coincide with a lower total FFM of 100=21.6*0.7 3.2 kg in females and 100=20.8*0.3 1.5 kg in males. Correcting for this amount of FFM, and assuming the same body weight, BF% can be calculated to increase to 30.5% in Depok females and to 22.7% in Depok males, which is closer but still signi®cantly different to the actual measured value of 35.6 and 24.6% in females and males respectively. These calculations show that differences in body build, in fact differences in slenderness do have an effect on the relationship between BF% and BMI, but also other factors might be involved. It could be that the anthropometric techniques used to assess body build are not accurate enough to pick up small differences in build, and body build is of course not only determined by the measured widths. Although the validity of the deuterium oxide methodology for assessing BF% is generally accepted, biased results could be obtained when assumptions are violated. The main assumption in the deuterium oxide method is a constant hydration fraction of the fat free mass of 0.73 and there could be differences in the hydration of the fat free mass among population groups. If the actual hydration factor in the Depok group were 0.71 instead of 0.73, the assessed BF% from deuterium oxide dilution would be lowered to 34.5% in females and to 23.0% in males. The main reasons for an abnormal low or high hydration of the fat free mass has been shown to be the ratio of extra-cellular water to intra-cellular water (Wang et al, in preparation). There are, however, no reasons to assume that the hydration of the fat free mass is lower, as ratios of determined extra-cellular water to total body water in the studied groups are not different and are equal to slightly higher compared to Caucasian groups (results not shown). To avoid all possible error sources in BF% determination, the use of a morecompartment models to assess body composition would be necessary, and radiological techniques (DXA) has to be used to get better information about body build. Conclusion The results of this study con®rm earlier ®ndings that Indonesians have higher BF% at lower BMI values compared to Caucasians. In addition the study shows that there are also differences among different Indonesian (ethnic) subgroups. The differences could be partly explained by differences in skeletal mass and inherent muscle mass=connective tissue mass. Other factors, yet unknown, may also be involved. 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