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Energy expenditure in African American and white boys and girls in a 2-y follow-up of the Baton Rouge Children's Study^1,2,3

¹ From the Pennington Biomedical Research Center, Baton Rouge, LA.

² Supported by the National Institute of Child Health and Human Development (HD-28020) and the Coypu Foundation.

³ Address reprint requests to JP DeLany, Pennington Biomedical Research Center, 6400 Perkins Road, Baton Rouge, LA 70808-4124. E-mail: delanyjp{at}pbrc.edu.

See corresponding editorial on page 181.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: Previously reported race and sex differences in energy expenditure (EE) may play a role in body fat gain.

Objective: The purpose of the study was to determine the relations between race, sex, Tanner stage, and EE.

Design: We conducted a 2-y follow-up study of EE in 114 African American (AA) and white girls and boys aged 12.7 ± 0.1 y ( ± SE), who were stratified as obese or lean and were part of the Baton Rouge Children's Study. Total daily EE (TDEE) was measured by using doubly labeled water. Resting metabolic rate (RMR) and thermic effect of food were measured by using indirect calorimetry.

Results: White children had significantly higher TDEE and RMR than did AA children when fat-free mass was considered. Boys had significantly higher TDEE and RMR than did girls, even after adjustment for differences in size. TDEE and RMR were significantly higher in obese children, as a result of their greater fat-free mass and body fat, than in lean children. Activity-related EE did not differ significantly between obese and lean children. There was a strong relation between initial and 2-y TDEE and RMR. There was a significant decrease in activity-related EE in both racial groups. AA children had significantly more lean limb mass than did white children.

Conclusions: Average TDEE did not change over 2 y, but RMR increased significantly, and activity-related EE decreased significantly. Differences in trunk and limb lean mass of white and AA children may explain some of the ethnic differences in EE. The decrease in physical activity over 2 y may contribute to the risk of obesity.

Key Words: Resting metabolic rate • thermic effect of food • doubly labeled water • total daily energy expenditure • physical activity • obesity • children • lean mass distribution • Baton Rouge Children's Study

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Childhood obesity is increasing rapidly in the United States, particularly among African Americans (1). Because obesity in childhood and adolescence predicts adult obesity, the period of transition from childhood to adolescence is critical to the detection and prevention of obesity (2, 3). Childhood obesity is a particularly troubling health problem because it is associated with other risk factors for disease, such as insulin resistance and higher LDL cholesterol (4).

We previously showed that total daily energy expenditure (TDEE) and resting metabolic rate (RMR) are higher in obese preadolescent children than in lean preadolescent children and that obese children underestimate their energy intakes more than do lean children (5, 6). However, after adjustment for fat-free mass (FFM) and fat mass, this difference in TDEE between lean and obese children disappeared. Other investigators also showed that TDEE, RMR, or both are at least as high in obese children as they are in lean children (7–9).

Race and sex differences in TDEE of children have been observed. In our initial study, white children had a higher TDEE and RMR than did African American children, even after accounting for differences in body composition. However, a lower RMR was observed when white boys were compared with African American boys. A lower RMR was reported in African American girls than in white girls (10–14). On the other hand, in a study of 98 children among whom the numbers of African American and white girls and boys were approximately equal, Sun et al (15) found no racial effect on RMR, although the boys had a higher RMR than did the girls. However, in most studies examining RMR in African American and white children, a lower RMR has been observed in the African American children than in the white children (see Table 6 in 5). One explanation for this might be differences in the distributions of FFM between trunk and limbs that were proposed to account for some of the differences between groups of women (16, 17).

TDEE and activity-related energy expenditure (AEE) were higher in the boys than in the girls, even after adjustment for differences in body composition (5). We report the 2-y follow-up data from the Baton Rouge Children's Study, which examined the components of energy expenditure (EE) in a large group of African American and white girls and boys (5). On the basis of earlier observations of an ethnic difference in EE between boys, but not between girls, we hypothesized that, in this follow-up study, we would find both ethnic and sex differences in components of EE, some of which could be explained by differences in regional distribution of lean body mass.

	SUBJECTS AND METHODS

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Subjects
Children enrolled in the Baton Rouge Children's Study (5) were contacted to repeat measures of EE and body composition made 2 y earlier. By design, all children were initially at or below Tanner stage 2: 101 were at stage 1 and 30 were at stage 2. Once enrolled in the study, the children were further stratified as lean or obese according to the criteria used during the initial examination, which were based on the percentage body fat as determined by dual-energy X-ray absorptiometry (DXA; 5). Children were classified as lean if they had <25% body fat and obese if they had >25% body fat. Each child and a parent or guardian signed a consent form approved by the Louisiana State University Institutional Review Board, which also gave ethical approval for the study overall.

General protocol
The general protocol was the same as that for the original study (5). At least one parent or guardian attended an information session at the Pennington Center on a weekend. Body composition, Tanner stage, and RMR were assessed during this information session, and the thermic effect of food (TEF) and TDEE were measured at the school in a mobile laboratory (5).

Within a few days of determination of body composition, a second 30-min RMR measure was taken. The children then ate a standard meal, which was followed by measurement of metabolic rate for 3 h to estimate TEF. On another day, the children were dosed with doubly labeled water (DLW; ²H₂¹⁸O) for measurement of TDEE.

Doubly labeled water measurement of total daily energy expenditure
The DLW method for measurement of TDEE was conducted during the week when RMR was measured as described previously (5). Children were dosed with DLW containing 0.3 g H₂¹⁸O/kg total body water and 0.14 g ²H₂O/kg total body water. Morning urine samples were obtained on days 1, 2, 8, and 9 after the administration of the DLW. The ¹⁸O and ²H isotope abundances were measured as described previously. The mean daily carbon dioxide production was calculated according to Schoeller et al (18) by using revised dilution space constants (19). EE was calculated by multiplying the calculated rate of carbon dioxide production by the energy equivalent of carbon dioxide for an estimated respiratory quotient of 0.86.

Once TDEE was determined and RMR and TEF were measured, AEE was calculated as follows:

(1)

The TEF used in this calculation was the percentage of meal energy expended above RMR times the estimated total daily intake (estimated as TDEE, assuming energy balance).

Indirect calorimetry
RMR and TEF were measured in a mobile metabolic laboratory, which was driven to the school each day. Metabolic rate was calculated by using the Weir equation (20) assuming a constant urinary nitrogen amount of 8.2 g for the RMR and measured urinary nitrogen for the TEF. Children arrived fasted and rested for 30 min before the hood was put over their heads. After the measurement of RMR for 30 min, the children emptied their bladder. They then ingested a meal (35% of measured RMR) consisting of Ensure (10.9% of energy as protein, 54.3% as carbohydrate, and 34.9% as fat; Ross Laboratories, Columbus, OH). Metabolic rate was measured for 3 h with zero time being the completion of the meal. At the end of the 3-h period, each subject completely emptied his or her bladder, and the urine was collected for measurement of urinary nitrogen. EE during the RMR was subtracted from the EE after the meal to determine the absolute TEF. The increased EE after a meal was divided by the total meal size to calculate the percentage of meal energy expended.

Body composition
Body composition was assessed by using a 4-compartment model developed in these children (21). This model includes bone mineral content measured by DXA, density measured by underwater weighing, and total body water measured by isotope dilution (as part of the DLW procedure). The distribution of lean mass was assessed by using DXA.

Data analysis
The components of EE were compared by using the general linear model analysis of variance (SAS release 8.02 for WINDOWS; SAS Institute Inc, Cary, NC). Data are presented as least-squares means ± SEMs by using the full model including race, sex, and obesity status. Various indexes were used in the analysis of variance models as covariates to adjust for differences in body composition. The change in EE components was analyzed with analysis of variance by using the full model including race, sex, and obesity status, with no adjustments. Post hoc tests for differences in group means were accomplished by using Tukey's multiple-comparison adjustment. Simple regression analysis was conducted on initial and follow-up EEs. A stepwise variable selection process was used to develop a model to explain the variance in RMR.

	RESULTS

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We enrolled 114 of the original 131 children in the follow-up study. Subject characteristics according to race, sex, and obesity status are given in Table 1. The racial and sex distributions were approximately equal. FFM, body fat, and percentage body fat measured by using a 4-compartment model developed during the initial measurements are given for each group. The African American children had more FFM and a higher body mass index (in kg/m²) than did the white children. There were several sex differences: boys were heavier, had a higher body mass index, and had more FFM than did girls (Table 1). Body fat (kg) and percentage body fat did not differ significantly between the races or the sexes, although there was a sex x obesity interaction for body fat and percentage body fat. For body fat, values for the lean girls and lean boys did not differ significantly, but the obese boys had significantly more body fat than did the obese girls (24.7 ± 1.2 and 19.9 ± 1.2 kg, respectively). Although there was also a significant interaction for percentage body fat, the mean values for lean (21.7 ± 1.4% and 19.8 ± 1.0%) and obese (34.5 ± 1.1% and 37.3 ± 1.0%) girls and boys, respectively, did not differ significantly. The African American children oxidized significantly more fat during TEF than did the white children (lower respiratory quotient during TEF; see Table 1).

Table 2

Table 3

As expected, the obese children were significantly heavier than were the lean children, and they had significantly higher values for all measures of body composition (Table 1). Unadjusted TDEE and RMR were significantly higher in the obese children than in the lean children (Table 2). After adjustment for FFM, the obese children still had a significantly higher RMR than did the lean children. However, this difference disappears after adjustment for both FFM and fat mass and after adjustment for surface area. As expected, TDEE (P < 0.01) and AEE (P < 0.066) were lower in the obese children after adjustment for body weight.

EE for each of the race x sex x obesity groups, adjusted for FFM, is given in Table 4. There were no significant interactions.

We next compared the unadjusted components of EE at the end of the 2-y follow-up with those observed at the initial examination (5; Figure 1). There was no significant change in TDEE, but there was a significant increase in RMR in all subgroups. A decrease in energy expended in physical activity was observed in all groups. Although there was no significant change in TDEE, the change in TDEE between the boys and girls differed significantly.

View larger version (31K): [in this window] [in a new window]   FIGURE 1.. Mean (±SE) changes in components of energy expenditure over 2 y. AA, African American; TDEE, total daily energy expenditure; RMR, resting metabolic rate; AEE, activity-related energy expenditure. ANOVA was conducted by using the full model including race, sex, and obesity status, with no adjustments. The change in TDEE in any group did not differ significantly from 0. However, the change in TDEE differed significantly (P < 0.05) between the boys and the girls. RMR increased significantly in all groups, whereas AEE decreased significantly in all groups. None of the group comparisons were significant for RMR or AEE.

Figure 2

View larger version (19K): [in this window] [in a new window]   FIGURE 2.. Comparison of initial and 2-y follow-up total daily energy expenditure (TDEE) for each subject (n = 114; arranged from lowest to highest initial TDEE).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

We have confirmed our earlier observation that white children have a significantly higher TDEE and RMR than do African American children, even after adjustment for differences in body composition. The white children had a significantly higher RMR than did the African American children after adjustment for FFM and after adjustment for both FFM and fat mass. However, after adjustment for body surface area, the difference was not significant (P < 0.07; Table 2). In the previous examination of these children, there was a significant race x sex interaction (P < 0.005), with a significantly higher RMR observed only when the white boys were compared with the African American boys (5). There was no significant race x sex interaction in the current study (P < 0.36), although the racial difference was more apparent between the white and African American boys (7.27 ± 0.15 compared with 6.76 ± 0.15, respectively; P < 0.092) than between the white and African American girls (6.56 ± 0.18 compared with 6.34 ± 0.16; P < 0.80). In a stepwise variable selection process to develop a model to explain the variance in RMR, FFM was the first variable entered into the model; it explained 39% of the variance, and fat mass accounted for 7% (P < 0.0005), sex accounted for 6% (P < 0.0005), and race accounted for 2% of the variance (P < 0.04). Thus, after adjustment for FFM, fat mass, and sex, race accounted for only 2% of the variance, but it did improve the model.

The race differences in EE could not be explained by differences in FFM determined from a 4-compartment model, nor by DXA or bone free lean mass. However, it was recently reported that the distribution of lean body mass may partially explain the age-related decrease in RMR in women, and that lean body mass in the trunk was associated with a greater RMR (16). This indicates that individual differences in the weight of the more metabolically active organs in the trunk may play a role in determining RMR. We previously examined whether the component organs of the lean body mass could improve the prediction of RMR, but were unable to show that it did (22). There are 2 reports in which lean mass in the trunk gave stronger correlations with RMR than did lean mass in the limbs, which indicates that the distribution of lean body mass may play a role in differences in RMR between individuals (16, 17). In our study, the correlations of RMR with lean mass of the trunk and lean mass of the limbs were nearly identical (0.61 compared with 0.60, respectively). However, when we examined the distribution of the lean mass measured with DXA, we found a difference by race (Table 3). Thus we conclude that the distribution of lean mass between the limbs and the trunk, which we assume reflects differences in the more metabolically active organs such as liver and kidneys, may explain some of the observed differences in RMR that are not explained by total FFM.

A higher RMR was observed at the original examination only when the white boys were compared with the white girls, but at the 2-y follow-up examination, this difference with the girls was apparent in both races. The sex differences appeared to be related to maturity. In the group with Tanner stage 2, there was no difference in RMR, whereas in the group with Tanner stage >2, RMR was significantly (P < 0.001) higher in the boys than in the girls. The boys also had a significantly higher lean mass in the limbs and trunk than did the girls (Table 4). When the distribution of lean mass was included, the boys still had a higher RMR than did the girls.

As expected, the obese children had a higher TDEE and RMR than did the lean children. After adjustment for FFM, there was no longer a difference in TDEE, although RMR was still higher in the obese children. When RMR was adjusted for FFM and fat mass or body surface area, there was no longer a significant difference in RMR between the lean and the obese children. Unadjusted AEE did not differ significantly between the lean and obese children, even though the obese children weighed >18 kg more than did the lean children. After adjustment of AEE for body weight (P < 0.07), the obese children tended to have a lower AEE than did the lean children.

When examining the change in EE over the 2-y interval, we observed the expected increase in RMR: these children gained, on average, nearly 12 kg over that time period. However, the lack of change in TDEE in these children over 2 y was quite surprising, and it means that the increase in RMR was nearly completely offset by a decrease in AEE. We had anticipated a lower AEE in the obese children, but the finding of a decrease in AEE over the 2 y in both the obese and the lean children was quite surprising, because one would expect AEE to increase as children mature. However, in a multicenter longitudinal study of 2379 African American and white girls from ages 9–10 y to 18–19 y, a significant decrease in physical activity was observed throughout the 10-y follow-up (23). The strength of the study was the large sample size and the consistency of the decline in activity with the use of 3 methods—an activity diary, a questionnaire, and an activity monitor (from years 3–5 of follow-up only). Whether this decrease in physical activity is associated with increased adiposity is under current investigation. A recent study of 15143 high school students found that increased levels of physical activity are associated with a lower body mass index (24).

In summary, in this reexamination of 114 children, we observed several race and sex differences in the major components of EE. The race difference in RMR was more apparent in the boys than in the girls. The race difference in RMR was eliminated by including the distribution of lean body mass (which differs significantly between African American and white children). The boys had higher TDEE, RMR, and AEE than did the girls, even after adjustment for differences in body weight. The obese children had significantly higher TDEE and RMR than did the lean children, but the obese children expended no more energy in physical activity and tended to have an even lower AEE than did the lean children after adjustment for the 18 kg of additional body weight observed in the obese children. Therefore, a lower AEE may be a risk for weight gain or maintenance of increased body weight in these obese children. Finally, during the important transition through adolescence, physical activity levels decreased in all of the subgroups, which indicates a potential risk of the development of obesity during this growth spurt.

	ACKNOWLEDGMENTS

 
GAB, JPD, and DWH designed the study; JPD and DWH collected the data; JV performed the statistical analysis; and JPD and GAB wrote the manuscript. GAB, JPD, DWH and JV have no affiliation with the Coypu Foundation, which partially funded this research.

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TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 

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