Acta Diabetol (2003) 40:S305–S308 DOI 10.1007/s00592-003-0094-y

© Springer-Verlag 2003

J. Wang • J.C. Thornton • S.B. Heymsfield • R.N. Pierson Jr.

The relationship between body mass index and body cell mass in African-American, Asian, and Caucasian adults

Abstract The objective of this study was to investigate the relationship between body mass index (BMI, kg/m2) and body cell mass (BCM) estimated from total body potassium (TBK) measured by whole body 40K counting in healthy 284 African-Americans (AA), 269 Asians (A) and 536 Caucasians (C) aged 18–107 years and to study the effects of age, sex, and race on the relationship. Body fat and fatfree mass (FFM) were measured by dual-energy X-ray absorptiometry (DXA). There was a significant positive correlation between BCM and BMI. For a given BMI, A had lower BCM but decreased less per year of age than AA and C, and males had higher BCM than females in each ethnic group. The fraction, BCM/FFM decreased with BMI in all subgroups by race, sex, and age, and males decreased more per age and AA decrease more than A and C. Not only the BCM–BMI relationship but also BCM/FFM vs. BMI is important to health. Key words Body composition • Body cell mass • Body mass index • Total body potassium

Background All bodily functions, including energy expenditure, are carried out in the body cell mass (BCM) [1]. The decrease in absolute energy expenditure and physical ability with aging in adults of both sexes is mostly the result of a fall in BCM with age [2, 3]. Patients with reduced BCM down to 60% of projected normal value have an increased risk of death [4]. Previous studies have suggested that the wellknown U-shape relationship between body mass index (BMI) and mortality is probably due to extremely low or high fat and fat-free mass content at each of the two ends of the U curve [5]. However, no attempt has been made to study the relationship between BMI and BCM in adults. Since more than 98% of total body potassium (TBK) is in the BCM, Moore et al. suggested estimating BCM by measuring TBK [1]. The objective of this study was to investigate the relationship between BMI and BCM in a group of healthy African-American (AA), Asian (A), and Caucasian (C) adults, and the effects of age, sex, and race on the relationship.

Subjects and methods

J. Wang () • J.C. Thornton • S.B. Heymsfield • R.N. Pierson Jr. Body Composition Unit St. Luke’s-Roosevelt Hospital-Columbia University 1111 Amsterdam Avenue, New York, NY 10025, USA E-mail: [email protected]

One thousand and eighty-nine adults [459 males (m) and 630 females (f); 284 AA, 269 A, and 536 C, age ranging from 18 to 107 years, BMI ranging from 15 to 47 kg/m2] were included in this study. Weight and height were measured and BMI was calculated kg/m2. TBK was measured in a 4-π whole body 40K counter corrected for anthropometric factor [6, 7], BCM (kg) was estimated as TBK (meq)x0.00833 [1], and body fat and FFM were measured by dual-energy X-ray absorptiometry (DXA) [8]. Regression analyses were used to study the relationship and the effects of age, sex, and race on the relationship. All statistical calculations were performed using STATA software (STATA Corporation, College Station, TX).

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Results Figure 1 shows the effect of race, sex, and age on the BCMBMI relationship. BCM increased with increases in BMI in all subgroups at any given age, as shown in this figure for subjects at the ages 30 and 50. Males had higher slopes than females and A males had the highest slopes at all ages (here shown at ages 30 and 50). Our modeling indicated that age did not affect the slope in any subgroup. The slopes in females were less than in males. As in males, A females also had the highest slopes among the three races at given age.

Figure 2 shows that when BCM was expressed as a fraction of FFM (BCM/FFM), it decreased significantly with BMI in the entire group as well as in all of the six subgroups by race and sex. Race, sex, and age had no effect on the slopes. AA had higher BCM/FFM at age 30. However, at age 50, there were no significant differences among the three groups. Females had lower BCM/FFM than males, but had similar age and race effects as in males. Table 1 shows the adjusted means for BCM and BCM/FFM at the mean age of 51.2 years and BMI of 24.5 kg/m2.

Fig. 1 The effect of race, sex, and age on the relationship between BCM body cell mass (kg) and BMI body mass index (kg/m2) (r2=0.83) AA, C(F-50Y), AfricanAmerican and Caucasian female at age 50 years; AA, C(M-50Y), African-American and Caucasian male at age 50 years; A(F-50Y), Asian female at age 50 years; A(M-50Y), Asian male at age 50 years; AA, C(F-30Y), AfricanAmerican and Caucasian female at age 30 years; AA,C(M-30Y), African-American and Cauasian male at age 30 years; A(F-30Y), Asian female at age 30 years, A(M-30Y), Asian male at age 30 years

Fig. 2 The effect of race, sex and age on the relationship between the ratio of body cell mass to fat-free mass BCM/FFM and body mass index (BMI, kg/m2) A, C(F-50Y), Asian and Caucasian female at age 50 years; A, C(M-50Y), Asian and Caucasian male at age 50 years; AA(F-50Y), African American female at age 50 years; AA(M50Y), African-American male at age 50 years; A,C(F-30Y), Asian and Caucasian female at age 30 years; A, C(M-30Y), Asian and Caucasian male at age 30 years; AA(F-30Y), African-American female at age 30 years; AA (M-30Y), African-American male at age 30 years

J. Wang et al.: The relationship between body mass index and body cell mass Table 1 Adjusted means for body cell mass (BCM) and body cell mass/fat-free mass (BCM/FFM) at the mean age of 51.2 years and body mass index of 24.5 kg/m2 Race and sex BCM, kg BCM/FFM

AA,C-m

A-m

AA,C-f

A-f

24.5

22.5

16.2

14.5

0.4129

0.4109

0.3817

0.3797

AA, African-American; C, Caucasian; A, Asian; m, male; f, female

Discussion BMI has been the most widely used index for predictions of body fatness, nutrition status, and fitness for many decades because the variables for calculating BMI (weight and height) are easy to measure and are readily available. Predictions using BMI are important and of interest, but also can be misleading [9–11]. On the other hand, all bodily functions, including energy expenditure, are carried out in the BCM and a previous study documents that patients with BCM reduced down to 60% of normal value have an increased risk of death [4], but few studies have focused on BCM and its relationships to other body composition components, body fitness, and nutrition status. The only reliable predictor for BCM is TBK, which can only be accurately measured in a sophisticated whole-body 40K counting system [6]. However, such systems are only available at a few major research centers. Therefore, lack of information in this area is mainly due to a very limited number of instruments available to investigators. This report presents the relationship between two important body composition indices in a large adult cohort with three different racial backgrounds, and wide ranges in age and BMI. In this healthy adult population, BMI and BCM are positively related adjusting for age, sex, and race. However, when BCM expressed as a fraction of FFM (BCM/FFM), it decreased with BMI. This result might be explained as follows: in general, in nonathletic subjects as included in this study, increased weight and BMI are mainly due to increase in adiposity. Since adipose tissue contains a small amount of fat-free tissue, the extracellular water space (ECW) is about three times larger than intracellular water space (ICW) [12], and the increase in adiposity proportionally increases more ECW than ICW in the body. Since BCM contains only ICW, an increase in adiposity will also increase FFM by increasing ECW more than ICW, which results in a decrease in BCM/FFM ratio. This study suggests that subjects at the upper end of the U-curve relationship between mortality and BMI probably have proportionally lower BCM FFM. Reduction in BCM/FFM may be a risk to longevity. TBK is mainly found in skeletal muscle [1]. It is well known that men have more skeletal muscle than women and

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that skeletal muscle decreases with aging [2, 3, 13]. Therefore, the higher BCM in men than in women at any given BMI and the higher BCM in younger than older subjects in both sexes at given BMI are expected. In our previous studies, we found that A tend to have 2–4% more body fat and shorter arms and legs, therefore less skeletal muscle than age-, sex-, and BMI-matched C, [13, 14]. As shown in Fig. 1, at the lower end of the BCM vs. BMI curves, A tend to have lower BCM than AA and C, which agrees with previous studies. However, the slopes indicate that A tend to increase more BCM per unit of increase in BMI than AA and C in both sexes. Age did not have any effect on this relationship. The race effect on the BMI-BCM relationship observed in this study is somewhat a surprise finding. The only reason we can suggest for this is that, since subjects with higher BMI also tend to be taller than subjects with a lower BMI, taller A may have longer arms and legs, therefore, more skeletal muscle per BMI than short A. Our data suggest that the relationship between BMI and BCM/FFM may provide useful information in studies relating to obesity, nutrition assessment, and physical fitness.

References 1. Moore FD, Olesen KH, McMurray JD, Parker HV, Ball MR, Boyden CM (1963) The body cell mass and its supporting environment. Saunders, Philadelphia 2. Forbes GB (1987) Human body composition: growth, aging, nutirition, and activity. Springer, New York, pp 179–180 3. Novak LP (1972) Aging, total body potassium, fat-free mass, and cell mass in males and females between ages 18 and 85 years. J Gerontol 27:438–443 4. Kotler DP, Tierney AR, Wang J, Pierson RN Jr (1989) Magnitude of body-cell-mass depletion and the timing of death from wasting in AIDS. Am J Clin Nutr 50:444–447 5. Troino RP, Frongillo EA, Sobal J, Levitsky DA (1996) The relationship between bodyweight and morbity: a quantitative analysis of combined information from existing studies. Int J Obes 20:67–75 6. Pierson RN Jr, Lyn DHY, Phillips RA (1974) Total-body potassium in health: effect of age, sex, height, and fat. Am J Physiol 226:206–212 7. Pierson RN Jr, Wang J, Thornton JC, Van Itallie TB, Colt EWD (1984) Body potassium by four-pi 40K counting: an anthropometric correction. Am J Physiol 246:234–239 8. Mazess RB, Barden HS, Bisek JP, Hanson J (1990) Dualenergy x-ray absorptiometry for total-body and regional bone-mineral and soft-tissue composition. Am J Clin Nutr 51:1106–1112 9. Allison DB, Faith MS, Heo M, Kotler DP (1997) Hypothesis concerning the U-shaped relation between BMI and morality. Am J Epidemiol 146:339–349 10. Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72:694–701

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11. National Institutes of Health (2000) The practical guide identification, evaluation, and treatment of overweight and obesity in adults. NIH Publication Number 00–4084 12. Wang J, Pierson RN Jr (1976) Disparate hydration states of adipose and lean tissue require a new model for body water distribution in man. J Nutr 106:1678–1693 13. Gallagher D, Visser M, DeMeersman RE, Sepulveda D,

Baumgartner RN, Pierson RN Jr, Harris T, Heymsfield SB (1997) Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol 82:229–239 14. Wang J, Thornton JC, Russell M, Burastero S, Heymsfield SB, Pierson RN Jr (1994) Asians have lower body mass index (BMI) but higher fat percent than do whites: comparisons of anthropometric measurements. Am J Clin Nutr 60:23–28