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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2008-1024
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The Journal of Clinical Endocrinology & Metabolism Vol. 93, No. 11 4547-4551
Copyright © 2008 by The Endocrine Society

BRIEF REPORT

Fat Oxidation in Black and White Youth: A Metabolic Phenotype Potentially Predisposing Black Girls to Obesity

SoJung Lee and Silva A. Arslanian

Weight Management and Wellness Center (S.L., S.A.A.), and Division of Pediatric Endocrinology, Metabolism and Diabetes Mellitus (S.A.A.), Children’s Hospital of Pittsburgh of University of Pittsburgh Medical Center, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213

Address all correspondence and requests for reprints to: Silva Arslanian, M.D., Richard L. Day Professor of Pediatrics, University of Pittsburgh, School of Medicine, Director, Weight management and Wellness Center, Director, Pediatric Clinical and Translational Research Center, Children’s Hospital of Pittsburgh, 3705 Fifth Avenue, Pittsburgh, Pennsylvania 15213. E-mail: Silva.Arslanian{at}chp.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Introduction: The prevalence of obesity is higher in Blacks with racial divergence in adiposity in girls starting during adolescence. Our hypothesis is that in Black children, puberty associated increase in fat oxidation is diminished and could play a role in predisposing to fat accretion triggered during puberty. Thus, we examined the relationships between race, pubertal development, and postabsorptive fat oxidation in youth.

Subjects and Methods: This was a cross-sectional design of healthy Black (n = 50) and white (n = 51) youth. Resting metabolic rate (RMR) and substrate oxidation rate were measured after an overnight fast with indirect calorimetry. Body composition was measured by dual-energy x-ray absorptiometry.

Results and Discussion: Within each race, RMR (kcal/kg fat free mass · min) was lower (puberty effect; P < 0.05) in the pubertal vs. prepubertal group independent of gender. In girls, RMR was lower (race effect; P < 0.05) in Blacks vs. whites. In girls but not boys, Blacks had lower (race effect; P = 0.033) fat oxidation (µmol/kg fat free mass · min) compared with whites independent of pubertal status. Furthermore, the difference in fat oxidation between the prepubertal vs. pubertal groups tended to be greater (puberty x race interaction; P = 0.089) in white girls (3.7 ± 0.5 vs. 6.5 ± 0.5) than in Black girls (3.4 ± 0.6 vs. 4.5 ± 0.5). These data suggest that the lower fat oxidation and RMR during puberty in Black girls could be a risk factor predisposing to obesity. This metabolic phenotype could potentially explain the divergence in adiposity in Black girls during adolescence against the backdrop of an obesogenic environment.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
The most recent National Health and Nutrition Examination Survey reports that between 1999 and 2004, the prevalence of at risk of overweight [body mass index (BMI) ≥ 85th percentile or overweight BMI ≥ 95th percentile in youth (12–19 yr)] has continuously increased from 30–34.4% and 14.8–17.4%, respectively (1). Similar to the previous National Health and Nutrition Examination Survey report (2), racial disparities persist, particularly in girls, such that 25% of Black girls (12–19 yr) are now considered overweight compared with 15% of white girls of similar age (1). The National Heart, Lung, and Blood Institute Growth and Health Study shows that the racial divergence in adiposity starts during adolescence in girls (3).

Although the mechanisms explaining the racial differential in the rates of childhood obesity are not fully understood, high-energy intake (4), low-physical activity level (5, 6), and sedentary behavior (e.g. increased television watching) (6) have been reported in Black vs. white girls. However, in adult women the racial differences in the prevalence of obesity remain after accounting for these environmental factors (7), suggesting inherent metabolic/physiological differences between the two racial groups.

Reduced postabsorptive fat oxidation is one of the contributing factors leading to positive energy balance and, therefore, future weight gain (8). It has been reported that in adults, Black lean women have significantly lower fat oxidation both at rest and during physical activity compared with their matched white peers (9). In a longitudinal study of adult Pima Indians, individuals with low fat oxidation were at 2.5 times greater risk for future weight gain (≥5 kg) compared with those with high-fat oxidation independent of 24-h resting metabolic rate (RMR) (8).

In cross-sectional and longitudinal studies, we have previously demonstrated that puberty is characterized by higher rates of fat oxidation compared with prepuberty and adulthood (10, 11, 12). These higher rates of fat oxidation correlate with IGF-I, which increases during puberty (10, 12). It is currently unknown whether there are racial differences in postabsorptive fat oxidation in youth, particularly related to the pubertal period. Thus, we examined the relationships between race and puberty on postabsorptive fat oxidation in normal weight boys and girls. We hypothesized that in Black girls, puberty associated increase in fat oxidation is diminished compared with their white peers, and could play a role in predisposing to fat accumulation triggered during puberty.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects consisted of healthy nonoverweight (BMI < 95th percentile) Black (n = 50) and white (n = 51) prepubertal [mean, 9.9 ± 0.2; range, 8.0–11.9 yr) and pubertal [mean, 12.8 ± 0.2; range: 9.9–15.3 yr) youth, some of whom were reported previously (13). Study participants were recruited through newspaper advertisements in the greater Pittsburgh area, flyers posted in the city public transportation, and posters placed on campus. Racial background was verified by self-identification in three generations. The investigation was approved by the institutional review board and performed in the Pediatric Clinical and Translational Research Center at Children’s Hospital of Pittsburgh. Parental informed consent and child assent were obtained from all participants. Pubertal development was assessed by physical examination according to Tanner criteria (breast development in females, genital development in males, and pubic hair in both), and was confirmed by measurement of plasma testosterone in males, estradiol in females, and dehydroepiandrosterone sulfate in both.

All subjects were admitted to the Pediatric Clinical and Translational Research Center on the previous day, for testing on the following morning after a 10- to 12-h overnight fast. RMRs were measured for 30 min using an open-circuit indirect calorimetry (DeltaTrac, Anaheim, CA), and substrate oxidation was calculated according to Frayn formulas (11). Total body fat was assessed by dual-energy x-ray absorptiometry.

Cardiorespiratory fitness (peak oxygen consumption) was performed in 35 Blacks and 40 whites as shown by us previously (14). A 24-h weekday food recall was administered by a trained nutritionist in 37 Blacks and 42 whites as reported by us previously (15). Statistical procedures were performed using SPSS (Version 15; SPSS, Inc., Chicago, IL). Race and pubertal group [prepuberty (Tanner I) vs. puberty (Tanner II-V)] differences (statistical significance, P < 0.05) in the anthropometric/metabolic variables were assessed using 2 x 2 ANOVA. Race and puberty group were entered as categorical variables, and dependent variables (e.g. RMR, fat oxidation, etc.) were entered as continuous variables. Differences in fat oxidation between the pubertal and prepubertal groups were compared using independent t tests.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Within each gender, Blacks and whites did not differ (P > 0.05) with respect to age and total adiposity (Table 1Go). Within each race, the pubertal group had higher (P < 0.05) fat mass (FM) in girls alone, and higher (P < 0.05) fat free mass (FFM) in both boys and girls. Independent of gender, cardiorespiratory fitness was significantly (P < 0.05) lower in Blacks vs. whites. The 24-hr diet recall revealed no racial effect on dietary composition in girls (data not shown). However, in boys, carbohydrate intake was lower in Black vs. white prepubertal (49.8 ± 4.2% vs. 58.3 ± 2.6%) and pubertal (49.4 ± 3.5% vs. 54.5 ± 2.3%) groups [race effect, P = 0.047; puberty effect, P = not significant (NS)].


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  		TABLE 1. Subject characteristics

 
Within each race, RMR adjusted for FFM (kcal/kg FFM · min) was lower in the pubertal vs. prepubertal group independent of gender (puberty effect, P < 0.05) (Fig. 1Go, A and B). In girls but not boys, RMR was lower in Blacks vs. whites (race effect, P < 0.05) (Fig. 1BGo). Within each race, fat oxidation, whether it is expressed as absolute (µmol/min) or relative to FM (µmol/kg FM · min), was higher in pubertal vs. prepubertal boys, with a similar tendency when data were expressed relative to FFM (puberty effect, P = 0.085) (Fig. 1CGo). In pubertal girls, Blacks had lower fat oxidation compared with whites when the data were expressed per body weight (µmol/kg · min) or FFM (µmol/kg FFM · min) (race effect, P = 0.033; Fig. 1DGo). The differences in fat oxidation (relative to body weight, FM and FFM) between the pubertal and prepubertal groups were significant in white girls ({Delta}1.87 ± 0.46, {Delta}8.64 ± 3.04, and {Delta}2.80 ± 0.68, respectively; P < 0.01 for all), but not in Black girls ({Delta}0.74 ± 0.53, {Delta}0.56 ± 3.35, and {Delta} 1.06 ± 0.73, respectively; P > 0.1 for all). Our observation that in girls, but not boys, Blacks have significantly lower fat oxidation than their white peers remained unchanged when the data (µmol/min) were adjusted either for body weight, FM, or FFM using analysis of covariance (data not shown).


Figure 1
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  		FIG. 1. Postabsorptive RMR and fat oxidation in boys and girls ({blacksquare}: Blacks; {square}: whites).

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
We observe that in girls but not boys, Blacks have significantly lower RMR than their white peers independent of pubertal status. Consistent with our hypothesis, the puberty associated increase in fat oxidation is diminished in Black girls compared with their white peers. These findings suggest that lower RMR and reduced fat oxidation during puberty in Black girls may be a metabolic risk phenotype predisposing them to future weight gain and obesity in an obesogenic environment.

The lower RMR in Blacks compared with whites has been shown in adults (16, 17) and children (18, 19, 20). In addition, during low and moderate-intensity exercise, Black women have lower rates of fat oxidation, 30 and 50%, respectively, than their white peers (9). Similarly, using the doubly labeled water method, Wong et al. (19) demonstrated that total energy expenditure and energy expended for physical activity under free-living conditions were approximately 410 and 462 kcal/d, respectively, lower in pubertal Black girls compared with white girls.

Several factors influence resting substrate oxidation, such as genetic factors, the amount of adipose tissue, level of feeding (positive vs. negative energy balance), and composition of the diet (21). However, the underlying mechanism(s) of racial differences in fat oxidation is still unclear. Our present finding of reduced fat oxidation in Black pubertal girls is not explained by the differences in adiposity because these values are similar between races. In addition, it is unlikely that the lower fat oxidation in Black girls is due to differences in food composition because diet composition is similar between Black vs. white girls.

Gallagher et al. (22) recently demonstrated that in adults, the mass of metabolically active organs (e.g. brain, liver, heart, kidney, and spleen) was significantly smaller in Blacks than in whites, and that the racial differences in RMR observed in this study disappeared once the mass of these organs was accounted. It is currently unknown whether this holds true in children. Although speculative, greater skeletal muscle mass (explaining only 20–30% of resting energy expenditure) and lower metabolically active organ mass (explaining 60–70% of resting energy expenditure) (23) with puberty in Black than in white youth may explain the racial difference in resting substrate utilization.

It is also plausible that our previously observed lower cardiorespiratory fitness and higher inactivity levels in Black vs. white normal weight children (24) may contribute to the lower RMR and decreased fat oxidation. It remains to be determined if both the smaller mass of metabolically active organs, lower cardiorespiratory fitness, and lower fat oxidation rates are biologically/genetically driven or environmentally determined. In favor of a potential biological mechanism in the literature on mitochondrial dysfunction and risk of obesity and type 2 diabetes, skeletal muscles of obese or type 2 diabetic individuals are characterized by a smaller skeletal muscle mitochondria size and reduced mitochondrial oxidative capacity (25). It is currently unknown whether racial differences in mitochondrial dysfunction exist. In a small study of young adult Black (n = 9) and white (n = 9) men, we demonstrated race-related variations in skeletal muscle oxidative metabolism, using 31phosphorous nuclear magnetic resonance spectroscopy, which potentially explained the lower peak oxygen consumption in Blacks (26). In this study (26), Black men had lower im pH and higher phosphorous/phosphocreatine during exercise, suggestive of a lower proportion of type I oxidative fibers and a higher proportion of type II glycolytic fibers. These observations are in agreement with Hunter et al. (27) who report a lower muscle oxidative capacity of the calf muscle and lower hemoglobin in Black lean women compared with their white peers. Currently, it remains to be determined if similar Black vs. white differences in skeletal muscle oxidative metabolism are present in childhood.

Limitations of this study warrant mention. Our study is a cross-sectional observation. Clearly, there is a need for longitudinal studies to investigate if the observed racial/gender differences in fat oxidation in the present study occur during the physiological transition from prepuberty to puberty. Patient-oriented research in pediatrics, especially in healthy normal weight children, with repeated measures over time, has several significant barriers making such investigations more difficult than in any adult population.

In summary, we observed that RMR and postabsorptive fat oxidation are substantially lower in Black vs. white girls, and this racial difference is more pronounced in the pubertal group. Such a metabolic phenotype could explain the racial divergence in adiposity in girls during adolescence. The underlying mechanism(s) for these observed racial differences is yet unclear and warrants further investigation.


   Acknowledgments
 
We thank the study participants and their parents, the previous pediatric endocrine fellows who contributed to this research during their training, and the Pediatric Clinical and Translational Research Center staff for their invaluable assistance.


   Footnotes
 
This research was funded by Grants R01-HD-27503, K24-HD-01357, and UL1 RR024153 CTSA (previously M01-RR-00084) (to S.A.A.). S.L. is supported by a Junior Faculty Award from the American Diabetes Association.

Disclosure Statement: The authors have nothing to declare.

First Published Online September 9, 2008

Abbreviations: BMI, Body mass index; FFM, fat free mass; FM, fat mass; NS, not significant; RMR, resting metabolic rate.

Received May 13, 2008.

Accepted August 28, 2008.


   References
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 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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