Racial differences in energy expenditure and aerobic fitness in premenopausal women

¹ From the Division of Physiology and Metabolism, Departments of Human Studies and Nutrition Sciences, University of Alabama at Birmingham.

² Supported by the National Institutes of Health (grants R01 DK 49779 and R01 DK 51684), the NIH General Clinical Research Center (grant RR-32), and the University of Alabama at Birmingham University Wide Obesity Research Nutrition Research Center. Entrees for lunch and dinner were provided by Nestle Food Co, Solon, OH.

³ Address reprint requests to GR Hunter, Room 205, Education Building, 901 South 13th Street, University of Alabama at Birmingham, Birmingham, AL 35294-1250. E-mail: ghunter{at}uab.edu.

ABSTRACT  
Background: Aerobic fitness, or maximal oxygen uptake ( Objective: The objective of this study was to compare sleeping EE (SEE), resting EE (REE), free-living total EE (TEE), and Design: Eighteen African American and 17 white premenopausal women were matched for weight, percentage body fat, and age. SEE and REE were measured in a room calorimeter and Results: The African American women had significantly more limb lean tissue and significantly less trunk lean tissue than did the white women. The African American women also had significantly lower SEE (6.9%), REE (7.5%), TEE (9.6%), and Conclusions: African American women had lower aerobic fitness than did white women, independent of differences in lean tissue or AEE. Diminished racial differences in SEE, REE, and TEE after adjustment for trunk lean tissue suggest that low EE in African American women is mediated by low volumes of metabolically active organ mass.

Key Words: African American women • white women • aerobic fitness • energy expenditure • obesity • body composition • fat mass • fat-free mass • lean tissue

INTRODUCTION  
Public awareness of obesity has increased, as evidenced by national trends toward greater use of low-energy food products (1). However, the incidence of obesity continues to increase in the United States despite acknowledgment that obesity is one of our nation's most serious health problems (2). Obesity is more prevalent in African American women than in white women (3); almost 50% of African American women are identified as overweight, whereas 33% of white women are overweight (2).

Several recent studies showed lower resting energy expenditures (REEs) in African American girls (4, 5) and women (6–8) than in their white counterparts. Racial differences persisted after adjustment of REE for fat-free mass (FFM) and in some cases for lean mass (FFM minus bone mass). However, not all studies showed a racial difference (9). Several other factors can affect REE and could conceivably mediate racial differences (eg, exercise training) (10). In addition, not all FFM has the same metabolic activity. For example, organs are known to have higher metabolic rates than do bone and muscle (11–13). Variations in FFM hydration could also affect estimations of metabolically active tissue.

Aerobic fitness, or maximal oxygen uptake (O₂max was shown to be related to longevity, independent of obesity (14). African American children were found to have lower aerobic capacity than white children (15, 16) and African American men were shown to have a greater percentage of type II muscle fibers ( The purpose of this study was to compare
SUBJECTS AND METHODS  
Subjects
The subjects were 18 African American and 17 white premenopausal women who were matched for body weight, percentage body fat, and age. Because of missing data for total body water and free-living total energy expenditure (TEE), percentage body fat, FFM, TEE, and AEE analyses were based on data for 16 African American women and 16 white women. The subjects were selected from a larger ongoing study designed to measure metabolic factors that may predispose women to obesity. All subjects were of normal weight [body mass index (BMI; in kg/m²) <25] and were free of any metabolic disorders and medications that may affect REE or Before testing, the subjects remained weight stable for 4 wk; during that time, the subjects were weighed 5 d each week. During the 2 wk immediately before testing and for the 2 wk of TEE measurement, all meals were provided through the clinical research center to ensure weight stability of <1% variation and to maintain macronutrient intake constant at 20% fat, 16% protein, and 64% carbohydrate. Entrees for lunch and dinner included Stouffer's Lean Cuisine (Nestle Food Co, Solon, OH).

Measurement of total energy expenditure
TEE was measured over 14 d of controlled-diet and energy-balance conditions by using the doubly labeled water technique. The previously described protocol (18) has a theoretical error of <5%. Samples were analyzed in triplicate for H₂¹⁸O and ²H₂O by isotope ratio mass spectrometry at the University of Alabama at Birmingham, as described previously (19). When all samples were reanalyzed for ²H and ¹⁸O in 7 subjects, values of TEE were in close agreement (CV: 4.3%), as described previously (19). Carbon dioxide production rates were determined by using a fixed assumption for the dilution space ratio (1.0427) using equation R2 of Speakman et al (20) and energy expenditure was calculated by using de Weir's equation 12 (21) with a mean value for the dietary food quotient of 0.92 obtained from the foods provided.

Assessment of free-living activity-related energy expenditure
AEE was estimated by subtracting sleeping energy expenditure (SEE) from TEE after reducing TEE by 10% to account for the thermic response to meals. SEE was used instead of REE to estimate AEE because SEE was based on a much longer period of assessment and had a 45% lower SD than did REE.

Body-composition measures
Four-compartment model
The body-composition criterion method used was body fat determined by the 4-compartment model, as described by Baumgartner et al (22). This model assumes densities of 900 g/L for fat, 990 g/L for water, 3042 g/L for bone mineral, and 1340 g/L for the unmeasured fraction of the body composed of protein and glycogen. The model calculates percentage body fat from the independent measures of total body density (by underwater weight, as described below), the fraction of body weight that is water (by isotope dilution, as described below), and the fraction of body weight that is minerals [by dual-energy X-ray absorptiometry (DXA), as described below].

Total body water
Total body water was determined by isotope-dilution techniques using water labeled with both ²H and ¹⁸O, as described previously (18). Briefly, a mixed dose of doubly labeled water was administered orally after a baseline urine sample (10 mL) was collected. The isotope loading dose was 0.1 and 0.08 g ¹⁸O and ²H, respectively, per kilogram of body mass. Two samples were collected the morning after doses were administered and an additional 2 samples were collected in the morning 14 d later. All samples were analyzed in triplicate for ²H and ¹⁸O by using the off-line zinc-reduction method (23) and equilibration technique (24), respectively, as described previously (25). Zero-time enrichments of ²H and ¹⁸O were calculated from the intercepts of the semilogarithmic plot of isotope enrichment in urine versus time after dosage. Isotope-dilution spaces were calculated by using the equation of Coward (26). Total body water was taken as the average of the ¹⁸O dilution space divided by 1.01 and the ²H dilution space divided by 1.04. FFM was estimated from total body water by assuming that fat-free tissue has a hydration constancy of 73.2% (27–29), and FM was estimated from the difference between body mass and FFM.

Dual-energy X-ray absorptiometry
Bone mineral content and regional lean tissue (trunk, arm, and leg) were measured by DXA (DPX-L; Lunar Radiation Corp, Madison, WI). Limb lean tissue was determined by summing arm and leg lean tissue. The scans were analyzed by using ADULT, version 1.33 (Lunar Radiation Corp). Bone mineral content was used in the calculation of percentage body fat by using the 4-compartment model (22). DXA lean tissue (soft lean tissue does not include estimates of bone mass) was used as an adjustment variable in the analysis of REE, SEE, and Body density
Densitometry was determined by underwater weighing; residual volume was measured simultaneously by a closed-circuit oxygen-dilution technique (30). Body weight was measured by using an electronic scale; a fasting measurement and a measurement immediately after voiding in the morning were taken. The CV for repeat tests of body density on separate days in our laboratory was 0.3%.

Aerobic fitness
O₂max ( Measurement of REE and SEE
The subjects spent 23 h in a whole-room respiration calorimeter (3.38 x 2.11 x 2.58 m). The design characteristics and calibration of the calorimeter were described previously (32). Oxygen consumption and carbon dioxide production were measured continuously with a magnetopneumatic differential oxygen analyzer (Magnos 4G; Hartmann & Braun, Frankfurt, Germany) and the NDIR industrial photometer differential carbon dioxide analyzer (Uras 3G; Hartmann & Braun). The calorimeter was calibrated before each subject entered the chamber. The zero calibration was carried out simultaneously for both analyzers. The full scale was set at 0–1% for the carbon dioxide analyzer and at 0–2% for the oxygen analyzer.

Each subject entered the calorimeter at 0800. Although metabolic data were collected throughout the 23-h stay, only sleeping and resting metabolic data are reported. The onset of sleep was determined to be when the lights were turned off, between 2130 and 2300 in all cases. Sleep as defined may have included some resting awake time while the subject was falling asleep. Radar motion sensors used to detect spontaneous physical activity indicated that the subjects were inactive during the sleep period. The subjects were awakened at 0630 on their second morning in the calorimeter. REE was then measured for 30 min before the subjects left the calorimeter at 0700. Energy expenditure was calculated by using the de Weir equation (21). REE and SEE were extrapolated over 24 h and expressed as kJ/d.

Statistics
Two-tailed independent t tests were used to test differences between the African American and white women in the descriptive and body-composition variables. One-tailed independent t tests were used to determine differences between the 2 groups of women in the metabolic variables because prior research indicated that African American women have lower REEs than do white women (6–8). Because both prior physical activity and muscle mass may affect measurement of
RESULTS  
Descriptive and body-composition variables are shown in Table 1. No significant differences between racial groups were seen for age, weight, BMI, or FFM. There was a small but significant difference in percentage body fat and FM between the African American and white women. The white women had significantly more trunk lean tissue (12%) than did the African American women; the African American women had 6.3% more limb lean tissue than did the white women, although the difference was not significant. To ensure that racial comparisons in trunk and limb lean tissue were not confounded by the small and nonsignificant total FFM differences between the African American and white women, trunk and limb lean tissue were also analyzed with ANCOVA, with FFM as an adjustment variable. The difference in trunk lean tissue remained significant and the difference in limb lean tissue became significant; the African American women had higher limb and lower trunk lean tissue than did the white women.

View this table:
TABLE 1.. Descriptive and body-composition measures in African American and white women¹  
SEE, REE, and TEE results are shown in Table 2. The African American women had a significantly lower absolute SEE (difference of 373 kJ/d), REE (difference of 506 kJ/d), and TEE (difference of 871 kJ/d) than did the white women despite having a comparable FFM. The 356-kJ/d lower total EE of the African American women while the women were in the room calorimeter and the 381-kJ/d lower AEE did not represent significant differences. The differences in SEE, REE, and TEE persisted after adjustment for AEE and
View this table:
TABLE 2.. Energy expenditure differences between African American and white women¹  
Consistent with the fact that organ mass (found only in the trunk lean tissue area) accounts for a higher metabolic rate than do bone or muscle mass, we found that trunk lean tissue was more highly related to SEE and REE than was limb lean tissue (Figures 1 and 2). In fact, limb lean tissue was totally unrelated to REE.
View larger version (14K):
FIGURE 1. . Relation between limb lean tissue and sleeping energy expenditure (R = 0.39, P < 0.03) and between limb lean tissue and resting energy expenditure (R = 0.20, P > 0.24) in 18 African American (•) and 17 white () women.

 

View larger version (14K):
FIGURE 2. . Relation between trunk lean tissue and sleeping energy expenditure (R = 0.77, P < 0.001) and between trunk lean tissue and resting energy expenditure (R = 0.57, P < 0.001) in 18 African American (•) and 17 white () women.

 

View this table:
TABLE 3.. Maximal exercise test results in African American and white women¹  

DISCUSSION  
Several studies showed that REE is significantly lower in African American children than in white children (4, 5), lower in obese African American women than in obese white women (6–8), and lower in normal-weight young African American women than in normal-weight young white women (33). Weyer et al (34) found that African American women had lower SEEs than did white women. However, in a study of white and African American children, racial differences were not found in all children (9). Ours is the first study to show that SEE, REE, and TEE were all lower in African American than in white normal-weight women. These differences were independent of FFM, AEE, O₂max than did age- and FFM-matched white women, as we showed previously in African American and white children ( The finding of higher limb lean tissue and lower trunk lean tissue in African American women than in white women was surprising, although it was reported that African American women have higher proportions of limb skeletal muscle than do white women (35, 36). All the women in our study were sedentary and none participated in strength-training programs. In addition, the nonsignificantly lower AEE and significantly lower Limb lean tissue consists primarily of muscle, whereas trunk lean tissue includes both muscle and organ mass. The DXA scan allows regional analysis of soft lean tissue mass and FM but cannot differentiate between soft muscle and organ tissue. However, there is no reason to believe that limb muscle mass is not related to trunk muscle mass, ie, that persons with a relatively large limb muscle mass should not have a relatively large trunk muscle mass. It was reported previously that African American women have longer limbs than do white women of similar height (35). It is possible that the lean tissue differences in trunk and limb were due to differences in limb and trunk length. We did not measure limb or trunk length in this study but the previous study showed limb length differences of only 2.5%. In contrast, we found 12.2% more trunk lean tissue in the white women than in the African American women, suggesting that differences in limb and trunk lean tissue are not solely a function of differences in limb and trunk length. In addition, it is well established that bone densities tend to be higher in African American persons than in white persons. It is logical that African American persons also tend to have more muscle mass, because muscle mass and bone density are related (36). Differences in bone density between African American and white persons are consistent with the differences in lean tissue found in this study and others (35, 36). Because it is known that African American women have more dense bones and thus more bone mineral content than do white women (37), it is possible that FFM was overestimated in the African American women, which would account for the lower adjusted REE reported in the other studies. We avoided this limitation by using a 4-compartment model that includes bone mineral content, total body water, and body density in the analysis.

Svendson et al (38) showed that DXA-derived trunk lean tissue is more highly related to REE than is appendicular lean tissue, supporting the hypothesis that trunk lean tissue is related to metabolically active visceral organs. We also showed stronger correlations of trunk lean tissue with both SEE and REE than with limb lean tissue (Figures 1 and 2). Sparti et al (39) did not find an independent relation (after adjustment for FFM) between REE and organ mass (left ventricular mass, liver, and kidney mass estimated from a combination of M-mode echocardiography and computed tomography) in a group of young white subjects. It is possible that the sample was relatively homogeneous in regard to the ratio of organ mass to FFM. If this were the case, the variability of relative organ mass would be truncated, reducing the probability of finding a relation with REE.

The sedentary African American women in our study had lower AEE was used as an adjustment variable to determine whether differences in O₂max in African American persons (15, In summary, the results of this study suggest that African American premenopausal women have lower SEE, REE, TEE, and

ACKNOWLEDGMENTS  
We are appreciative of the efforts of Susan Davies, Harry Vaughn, and Robert Petri in the conduct of this study.

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