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Pubertal African-American Girls Expend Less Energy at Rest and During Physical Activity than Caucasian Girls¹

United States Department of Agriculture/Agricultural Research Service Children’s Nutrition Research Center (W.W.W., N.F.B., K.J.E., J.E.S., E.O.S.) and Texas Children’s Hospital (A.C.H., R.B.H.), Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030

Address all correspondence and requests for reprints to: William W. Wong, Ph.D., United States Department of Agriculture/Agricultural Research Service Children’s Nutrition Research Center, 1100 Bates Street, Houston, Texas 77030. E-mail: wwong{at}bcm.tmc.edu

	Abstract

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Between 1963 and 1991, the most dramatic increases in the prevalence of overweight in the United States have been reported in African-American girls. Lower basal energy expenditure and lack of physical activity are believed to be risk factors for excessive weight gain. We hypothesized that energy expenditure at rest and during physical activity are lower in pubertal African-American girls than in Caucasian girls. Basal metabolic rate and sleeping energy expenditure of 40 Caucasian and 41 African-American pubertal girls (matched for age, physical characteristics, body fat, and energy intake) were measured by whole-room calorimetry, energy expended for physical activity by the doubly labeled water method, sexual maturity by physical examination, body composition by dual-energy x-ray absorptiometry, physical fitness by treadmill testing, and energy intake by 3-day food record. After adjusting for soft lean tissue mass, the basal energy expenditure (1333 ± 132 vs. 1412 ± 132 kcal/day, P = 0.01) and energy expended for physical activity (809 ± 637 vs. 1271 ± 162 kcal/day, P < 0.01) were significantly lower in the African-American girls than in the Caucasian girls. The differences remained the same after controlling for differences in sexual maturity and/or physical fitness. The lower energy expenditure of the pubertal African-American girls suggests that they are at a higher risk of becoming overweight than their Caucasian counterparts.

	Introduction

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OBESITY is a major health problem in the United States because of its association with increased risk of hypertension, coronary heart disease, diabetes, cancer, and many other medical ailments (1, 2). The National Health and Nutrition Examination Survey III (3, 4) indicated that approximately 33% of American adults and 22% of American children and adolescents are overweight. The prevalence of overweight in African-American women is twice that in Caucasian women, after adjustment for socioeconomic status (5, 6). More importantly, the most dramatic increases in the prevalence of overweight over the past 30 yr have been observed in African-American girls, with age range-related increases of 80–150%, compared with an average increase of 35% in Caucasian girls (4). Overweight children are at high risk of becoming overweight adults (7).

The etiology of overweight is multifactorial. Lower energy expenditure is hypothesized to be one of the contributing factors favoring positive energy balance that leads to overweight. Three recent studies reported a lower resting metabolic rate in prepubertal African-American children than in Caucasian children (8, 9, 10). The relationship between lower basal energy expenditure and excessive weight gain is controversial (11, 12, 13). Lack of physical activity, however, has been shown to be positively correlated with future weight gain in moderately obese women (13) and in children and adolescents (14, 15, 16). Because physical activity decreases through adolescence in girls (17) and fat accumulation accelerates during puberty in girls (18), lower energy expenditure during puberty may represent a greater risk for excessive weight gain in African-American girls than in Caucasian girls. We hypothesized that rates of energy expenditure at rest and during physical activity in pubertal African-American girls are lower than those of Caucasian girls.

	Materials and Methods

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Subjects

Forty Caucasian and 41 African-American girls (Table 1) with greater than or equal to Tanner stage 3 of breast and pubic hair development (19) were studied. The subjects qualified for the study when both parents and grandparents were of the same ethnicity. All subjects were healthy and nondiabetic at the time of the study, based on medical history, vital signs, standard clinical blood chemistries, and physical examination. The protocol was approved by the Human Research Committee at Baylor College of Medicine. All subjects and their parents gave written informed consent. Body weight and height of each subject were measured to the nearest 0.1 kg and 1 mm, respectively, by one investigator. Body mass index (BMI) was calculated as:

(1)

Breast and pubic hair development was determined by a physician according to the Tanner stages of classification (19).

The aerobic capacity of each girl (O_2max) was measured on a motorized treadmill until volitional exhaustion (20). Oxygen consumption rate (O₂) and carbon dioxide production rate (CO₂) were measured continuously by electronic metabolic analyzers, with the treadmill speed and elevation increased at 3-min intervals. O_2max was achieved when O₂ reached a plateau value and the respiratory exchange ratio exceeded 1.05 or when the heart rate was within 95% of the age-predicted maximum.

Whole-room indirect calorimetry

Four room respiration calorimeters were used in the study (21). Each subject entered the respiration chamber at 0800 h and ate breakfast at 0830 h, lunch at 1200 h, and dinner at 1730 h. All subjects received a standardized diet consisting of approximately 30% fat, 50% carbohydrate, and 20% protein. Their energy requirements during the calorimetric visit were estimated to be 1.5 times their predicted basal metabolic rates according to their ages, body weights, and heights, using the Schofield’s equations (22). No food or drink other than water was allowed after 1900 h. All subjects remained awake until bedtime, at 2200 h. Sleeping energy expenditure was measured between 2200 h and 0650 h the next morning. At 0650 h the next morning, the subject was awakened, urinated, and returned to bed. At 0720 h, the subject was reawakened if she was asleep, and instructed to find a comfortable position in bed and to refrain from movement for the next 40 min. To eliminate the contribution of any physical activity to basal metabolic rate, only the O₂ and CO₂ data with activity counts 50 (Doppler microwave sensor D9/50, Microwave Sensors, Ann Arbor, MI) during the 40-min measurement period were converted to basal metabolic rate, as (23): basal metabolic rate (kcal/day) = (3.941 x O₂) + (1.106 x CO₂). Sleeping energy expenditure was measured to obtain a longer and more accurate estimate of basal energy expenditure, because basal metabolic rate can be affected by a child’s state, i.e. anxiety, impatience, and ability to stay motionless for 40 min. The Weir equation (23) also was used to convert the O₂ and CO₂ measurements during sleep into sleeping energy expenditure. A 24-h urine sample was collected from each subject while she was in the calorimeter, to determine the urinary nitrogen excretion rate.

Doubly labeled water method (²H₂¹⁸O)

The total energy expenditure of each subject under free-living conditions, which could not be measured by whole-room indirect calorimetry, was estimated using the ²H₂¹⁸O method. After each subject exited the calorimeter, baseline plasma and saliva samples were collected. Each subject then received, by mouth, 100 mg ²H₂O and 125 mg ¹⁸O as H₂¹⁸O (Isotec Inc., Miamisburg, OH) per kilogram body weight. The container holding the ²H₂¹⁸O was rinsed three times with 50 mL of water, and the subject ingested all the rinses. The subject collected one daily saliva sample at home for the next 10 days. Immediately before her departure, a 3-h postdose plasma sample was collected. To minimize fluctuation in the basal ²H and ¹⁸O abundance in body water, all subjects resumed their usual diets at home and refrained from travel for the next 10 days. Plasma and saliva samples were prepared for hydrogen and oxygen isotope ratio measurements by gas-isotope-ratio mass spectrometry (24, 25). The isotope dilution spaces for ²H (N_H) and ¹⁸O (N_O) were calculated as follows:

(2)

where D is the dose of ²H₂O or H₂¹⁸O in grams; A is the amount of laboratory water, in grams, used in the dose dilution; is the amount of ²H₂O or H₂¹⁸O, in grams, added to the laboratory water in the dose dilution; E is the rise in ²H or ¹⁸O abundance, per mil, in the laboratory water after the addition of the isotopic water; E_d is the rise in ²H or ¹⁸O abundance, per mil, in the 3-h postdose plasma sample. CO₂ was calculated from the fractional turnover rates of ²H (k_H) and ¹⁸O (k_O) and the isotope dilution spaces as follows (26, 27): CO₂ (mol/day) = 0.4584 x [(k_O x N_O) - (k_H x N_H)]. The CO₂ was converted to free-living energy expenditure as follows (23): free-living energy expenditure (kcal/day) = (3.941 x O₂) + (1.106 x CO₂) - (2.17 x U_N), where O₂, in liters, is calculated from the 24-h respiratory quotient (RQ), measured by calorimetry, using the relationship O₂ = CO₂/RQ (28), and U_N is the 24-h urinary nitrogen excretion in grams. Energy expended for physical activity was calculated by subtracting basal metabolic rate and diet-induced thermogenesis from free-living energy expenditure. Diet-induced thermogenesis was assumed to be 10% of free-living energy expenditure.

Body composition measurement

A Hologic QDR-2000 instrument (Hologic, Inc., Waltham, MA) was used to assess the body composition of each subject. The scanning software (version 5.56) is appropriate for the weight range of our study subjects, and the accuracy of the fat mass and bone mineral content measurements is independent of pubertal development (29). Fat-free mass, in kilograms, was the difference between body weight and fat mass. Because skeletal bone mass, a nonmetabolic component of fat-free mass, is higher in African-American girls than in Caucasian girls (30), soft lean tissue mass was obtained by subtracting bone mass from fat-free mass as follows (31): soft lean tissue mass (kg) = (fat-free mass) - (1.9 x bone mineral content).

Energy intake

At the laboratory, each subject received instructions from a dietitian on the appropriate completion of a 3-day food record at home, including one weekend day. Each subject practiced the procedure during her stay in the respiration chamber. These instructions also were given to the parent(s). Energy intake was calculated from the food records using the Minnesota Nutrition Data System (ND 2.4, Nutrition Coordinating Center, University of Minnesota, MN, 1993).

Statistical analyses

Because soft lean tissue mass has been shown to be the major determinant of energy expenditure in children, adolescents, and adults, whereas fat mass was only a minor contributor to energy expenditure in obese subjects (32, 33), all energy expenditure measurements were normalized to soft lean tissue mass (the mathematical ratio method) before statistical analysis. A t test was used to compare ethnic groups, with respect to age, physical characteristics, body composition, O_2max, energy intake, and all measures of energy expenditure. Because Tanner stages of pubertal development are not continuous variables, -square was used to compare groups on sexual maturity. Because the mathematical ratio method has been shown to yield erroneous conclusions, regarding differences in energy expenditure (34), analysis of covariance also was used to determine the effect of race on all measures of energy expenditure, while controlling for soft lean tissue mass. Interactions between covariates and race were assessed. All statistical analyses were performed using standardized software (SPSS for Windows, version 7.5.1, SPSS, Inc., Chicago, IL).

	Results

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Age, physical characteristics, sexual maturity, and energy intake of study subjects

Age, physical characteristics, sexual maturity, and energy intake of the two groups are given in Table 1. The African-American and Caucasian girls were well matched for age, body weight, height, and BMI. The African-American girls, however, were sexually more mature than the Caucasian girls. Neither the total energy intake, estimated from the 3-day food records, nor the calorie intakes of the macronutrients (expressed as percentages of total energy intake) were significantly different between the two groups.

O_2max and body composition of study subjects

As shown in Table 2, the O_2max of the African-American girls was significantly lower than those of the Caucasian girls. However, the bone mineral content, bone mass, fat-free mass, and soft lean tissue mass of the African-American girls were significantly higher than those of the Caucasian girls. No difference in fat mass, expressed either in absolute kilograms or in percentage of body weight, was observed between the two groups.

View this table: [in this window] [in a new window]   Table 2. O2 max and body composition of Caucasian and African-American subjects

Sleeping energy expenditure and basal metabolic rate of the African-American and Caucasian girls are summarized in Table 3. All calorimetric measures of energy expenditure, after normalization to soft lean tissue mass (by the mathematical ratio method) or after adjustment for soft lean tissue mass (by analysis of covariance), were significantly lower in the African-American girls than in the Caucasian girls. The racial differences in the calorimetric measures of energy expenditure remained significant after inclusion of sexual maturity and/or O_2max in the analysis of covariance. Fat mass was not included in the analysis because it was not different between the two groups, one of the criteria considered as a covariate. No significant interactions were observed between race and any of the covariates in the analyses, indicating that the racial differences in basal energy expenditure were not affected by the size of soft lean tissue mass, the stages of pubertal development, or physical fitness.

Total energy expenditure and energy expended for physical activity under free-living conditions (measured by the doubly labeled water method) are summarized in Table 4. The isotope dilution spaces (N_H, N_O) were higher in the African-American girls than in the Caucasian girls, whereas the fractional turnover rates of ²H and ¹⁸O were higher among the Caucasian girls than in the African-American girls. No significant differences were observed in the 24-h RQ or U_N rate between the two groups. Total energy expenditure and energy expended for physical activity under free-living conditions, after normalization to soft lean tissue mass (by the mathematical ratio method) or after adjustment for soft lean tissue mass (by analysis of covariance), were significantly lower in the African-American girls than in the Caucasian girls. The racial differences in total energy expenditure and energy expended for physical activity remained significant after inclusion of sexual maturity and/or O_2max in the analysis. Again, no significant interactions were observed between race and any of the covariates in the analyses.

	Discussion

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Our data (Table 3), together with those reported recently by Kaplan et al. (8), Morrison et al. (9), and Yanovski et al. (10), clearly demonstrate the existence of a lower basal energy expenditure in prepubertal and pubertal African-American girls, compared with Caucasian girls. In this study, the sleeping energy expenditure and basal metabolic rate of the African-American girls were 62 and 78 kcal/day, respectively, lower than those of the Caucasian girls. Although Ravussin et al. (12) observed a direct relationship between a lower resting metabolic rate and later weight gain in 95 southwestern American Indian adults, over a period of 2–4 yr, the same group reported that a low resting metabolic rate was not related to later weight gain in a larger study of 130 southwestern American Indian adults (11). In a study of 24 moderately obese women, over a period of 4 yr, Weinsier et al. (13) reported that the small differences in basal energy expenditure recorded were insufficient to account for later weight gain. However, the authors (13) were able to detect a significant relationship between lower self-reported physical activity and weight gain in these women.

Although soft lean tissue mass is the major determinant of energy expenditure (32, 33), Tanner stages of pubertal development were included in the analysis because the African-American girls were sexually more mature than the Caucasian girls, in spite of their similar chronological ages and physical characteristics (Table 1). The advanced sexual maturation of the African-American girls is consistent with earlier studies showing that the mean age of onset of breast and pubic hair development is 1–2 yr earlier in African-American girls than in Caucasian girls (35). More importantly, the magnitude of the differences in energy expenditure between the two ethnic groups in this study remained unchanged when sexual maturity was included in the analysis. This is in agreement with the observation by Molnar and Schutz (32) that pubertal development has no effect on energy expenditure in children and adolescents after controlling for fat-free mass. As shown in Table 2, the O_2max of the African-American girls was 15% lower than that of the Caucasian girls. This result is similar to that reported by Trowbridge et al. (36). Inclusion of O_2max in the analysis did not change the outcome, confirming that soft lean tissue mass is the major determinant of energy expenditure. The lower O_2max observed in the African-American girls might be related to a lower percentage of type I fibers in their skeletal muscle, compared with Caucasians. African-American men have been shown to have a lower percentage of type I fibers than Caucasian men (37), and their O_2max has been shown to be highly correlated with the percentage of type I fibers in their skeletal muscle (38). However, a muscle biopsy, which was not done in this study, would be required to confirm this relationship in African-American girls. Our results (Table 4) clearly demonstrated that energy expended for physical activity under free-living conditions was significantly lower in the African-American girls than in the Caucasian girls. Therefore, the lower level of physical activity in the African-American girls might have contributed to their lower aerobic fitness level.

As shown in Table 4, the average total energy expenditure and energy expended by pubertal African-American girls for physical activity under free-living conditions were, respectively, 410 and 462 kcal/day lower than the Caucasian girls’ rates, after adjustment of soft lean tissue mass, by analysis of covariance. The magnitude of the difference was approximately 6-fold higher than that of the basal metabolic rate. This is in contrast to the study by Trowbridge et al. (36), showing no difference in total energy expenditure and energy expended for physical activity, under free-living conditions, between prepubertal African-American and Caucasian girls. Their inability to detect a significant difference between the two ethnic groups might have been attributable to an insufficient number of study subjects (18 Caucasian and 27 African-American girls).

Because a lack of physical activity has a positive correlation with excessive weight gain (13, 39), and greater increases in adiposity have been documented in pubertal African-American girls than in Caucasian girls (40), the substantially lower total energy expended for physical activity, under free-living conditions, in the pubertal African-American girls suggests that they are at increased risk of excessive fat gain, compared with the Caucasian girls. Therefore, any programs to minimize or prevent overweight in African-American women must take into account the lower energy expenditure for physical activity in this population during childhood, as well as in adulthood. Specifically, this study suggests that greater caloric restriction and physical activity are indicated for African-American girls than for Caucasian girls. Our subjects were recruited from middle-income families. It has been shown that children of low socioeconomic status have lower levels of physical activity and higher body weight (41). Therefore, it is possible that energy expenditure for physical activity under free-living conditions is further reduced in African-American girls in low-income families. In other words, the risk of excessive weight gain might be highest among African-American girls in low-income families. Longitudinal studies, particularly in African-American girls of low socioeconomic status, are needed to evaluate the efficacy of increasing physical activity to control excessive weight gain and the ability to sustain positive physical activity behavior from childhood into adulthood.

	Acknowledgments

 
The authors are indebted to the volunteers; to the staff of the Metabolic Research Unit, for meeting the needs of the subjects during the study; to Dr. J. Hoyle in the Pediatric Department of Kelsey-Seybold West Clinic; Dr. M. desVignes-Kendrick, Director of the City of Houston Health and Human Services Department; Ms. X. Earlie, Director of Sciences of the Aldine Independent School District; Ms. S. Wooten, principal at the Teague Middle School; Dr. B. Shargey, dean of instruction, and Ms. C. C. Collins, principal at the High School for Health Professions; and Ms. K. Wallace for subject recruitment; Dr. J. Moon, Mr. M. Puyau, and Mr. F.A. Vohra, for the calorimetric measurements; Mr. R. J. Shypailo and Ms. J. Pratt, for the body composition measurements; Mrs. L. L. Clarke and Mr. S. Zhang, for the isotope ratio measurements; and to Ms. L. Loddeke, for editorial assistance in the preparation of the manuscript.

	Footnotes

 
¹ This work was funded, in part, with federal funds from the US Department of Agriculture, Agricultural Research Service, under Cooperative Agreement No. 58–7MNI-6–001. Disclaimer: The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organization imply endorsement by the US Government.

Received September 30, 1998.

Revised November 9, 1998.

Accepted November 16, 1998.

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