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Original Research Communications |
1 From the Division of Gastroenterology and Nutrition, Departments of Pediatrics and Nutrition Sciences, and the Department of Medicine, General Clinical Research Center, Medical Statistics Unit, Comprehensive Cancer Center, University of Alabama at Birmingham.
2 Supported by grants DK02244 and RR00032 from the National Institutes of Health, the Children's Hospital Research Foundation, and the Knoll Pharmaceutical Company (grant to RFC). 3 Address reprint requests to R Figueroa-Colon, 2400 West Lloyd Expressway (R20), Evansville, IN 47721. E-mail: rfiguero{at}usnotes.bms.com.
| ABSTRACT |
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Objective: The aim of this study was to examine potential predictors of changes in total or percentage body fat over 2.7 y in premenarcheal girls.
Design: We studied 47 normal-weight prepubertal girls aged 4.88.9 y in 3 visits. The girls' age, total and percentage body fat at baseline, sleep EE (SEE) and activity-related EE (AEE) adjusted for fat-free mass (FFM) and total body fat, mothers' and fathers' total and percentage body fat and FFM at baseline, and time to follow-up visits were measured; 24-h EE and SEE were measured by whole-room indirect calorimetry. AEE was calculated as TEE minus (SEE + 0.1 TEE), with the assumption that the thermic effect of food was 10% of TEE. The girls' body composition was measured at each visit and that of the parents was measured at the time of the girls' enrollment by using dual-energy X-ray absorptiometry.
Results: From baseline to the first (
: 1.6 y) and the second (
: 2.7 y) follow-up visits, the girls' mean (±SD) change in total fat adjusted for FFM was 1.2 ± 2.7 and 3.3 ± 4.0 kg, respectively, and the mean change in percentage body fat was -2.0 ± 5.0% and -0.8 ± 5.9%, respectively. Fathers' total and percentage body fat were the main predictors of changes in the girls' total and percentage body fat. For the first follow-up visit, SEE, girls' age at baseline, and AEE were significant predictors of percentage body fat.
Conclusion: Fathers' total and percentage body fat were predictors of changes in body fat of premenarcheal girls during a 2.7-y period.
Key Words: Premenarcheal girls body fat fat-free mass body composition total energy expenditure sleep energy expenditure activity-related energy expenditure obesity predictors parents
| INTRODUCTION |
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Whole-room indirect calorimetry is an accurate and reliable method for measuring 24-h EE, especially sleep EE (SEE), under well-controlled conditions (8). Measured components include REE (which comprises SEE and the energy cost of arousal), the thermic effect of food, and AEE. The 24-h whole-room indirect calorimeter imposes an artificial restriction on activity and living conditions compared with free-living conditions, and this reduces TEE. The objectives of this study were to use whole-room indirect calorimetry to examine potential predictors of changes in total and percentage body fat during a 2.7-y period and to develop prediction equations for individual estimation of total and percentage body fat in premenarcheal girls. The values measured were girls' age, total and percentage body fat at baseline, SEE and AEE adjusted for fat-free mass (FFM) and body fat, mothers' and fathers' total and percentage body fat and FFM at baseline, and time to follow-up visits.
| SUBJECTS AND METHODS |
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Whole-room indirect calorimetry
The indirect calorimetric chamber was described previously (8). Briefly, the chamber has a total volume of 18400 L (3.38 x 2.11 x 2.58 m). When furniture is in the chamber, the net volume is 16300 L. This relatively small chamber is comfortable and is an appropriate size for studies in children. The chamber is equipped with a chairfoldout bed, desk, chair, lamp, refrigerator, toilet, sink, television, videocassette recorder, intercom system, and telephone. The girls were allowed to occupy their time as they wished without any restrictions on activity, which included reading, writing, drawing, watching television or movies, playing video games, napping, and other sedentary EE activities. There was a living area located outside the chamber where the parents or a researcher could stay and interact freely with the girls through a window by using an intercom system. An airlock window (78.1 x 33.7 cm) allowed the passage of food and materials to the girls while they were inside the chamber. Two windows (116.2 x 77.1 cm) provided a view of a large room, and a third window (54.6 x 49.5 cm) on the door (2.07 x 0.908 m) provided a view of the equipment operations room. The door had an air gasket that was inflated to form a seal against a smooth aluminum surface secured to the door frame.
Temperature was controlled by an air conditioning and heating system in which air was passed from the air conditioner and 2 heaters continuously through a mixing chamber that allowed a constant temperature of air circulating in the room. A temperature controller (model CN9000A; Omega Engineering, Inc, Stamford, CT) was used to maintain a constant temperature of 24.0 ± 0.5°C during the 24-h test. A barometer (model PX96116A5V; Omega), powered by a 4-channel flow meter (model HFM-200 FAST; Teledyne Electronic Technologies, Hasting Instruments, Hampton, VA), measured the barometric pressure. Humidity and temperature were also measured (model HX12, Omega). The wire connections for these instruments were connected to the equipment operations room through a water-filled trap between the whole-room calorimeter and the equipment operations room.
Data acquisition involved analogue outputs of the analyzers, flow meter, temperature, humidity, and barometric probes to be processed by a computer (Gateway 2000 4DX-66; Gateway, Sioux Falls, SD) via an analogue-to-digital converter (AT-Mid-16X; National Instruments, Austin, TX), by using a computer acquisition program (LABVIEW for WINDOWS, National Instruments). Under this system, oxygen consumption, carbon dioxide production, and respiratory quotient are reported every 15 min.
The whole-room calorimeter was calibrated before each girl's entry into the chamber. The girls entered the room at
0800 and spent 23 h in the chamber. Girls exited the room at
0700, allowing time for calibration and sanitation of the chamber before the next girl entered. TEE (in kJ/d) was extrapolated over 24 h by using mean EE during the awake state only. SEE was measured by averaging EE from the time each girl went to sleep until the time she was awakened, both times by direct observation by the researcher. AEE was calculated as TEE minus (SEE + 0.1 TEE), with the assumption that the thermic effect of food is 10% of TEE. Reported previously, the Pearson's correlation coefficient (r), P value, and total CV for the 61 intraindividual measurements between 2 baseline visits, 6 wk apart, were r = 0.76, P < 0.0001, and CV = 5.3% for TEE and r = 0.63, P < 0.0001, and CV = 5.6% for SEE (8).
Body composition
Dual-energy X-ray absorptiometry (DXA) (DPX-L; LUNAR Radiation Corp, Madison, WI) was used to assess total body composition of the girls at each visit. DXA involves minimal ionizing radiation (<1 mSv). The girls were scanned by using the pediatric medium mode. The scans were analyzed by using pediatric DPX-L software (version 1.5e; LUNAR Radiation Corp) for body-composition analyses (11). The parents were scanned by using the adult slow mode. The scans were analyzed by using adult DPX-L software (version 3.6z; LUNAR Radiation Corp) for body-composition analyses (11). DXA allows for determination of total and regional body composition (fat, soft lean tissue, and bone mineral content). FFM is defined as soft lean mass plus bone mineral content. The scanning arm moves from head to foot and counts photon attenuation rates from the X-ray source within the surface area of the table. During the scan, each girl lay quietly on the table for 20 min. All scans were performed and analyzed by the same laboratory technician. Reported previously, the Pearson's correlation coefficient, P value, and total CV for the 61 intraindividual measurements by DXA between 2 baseline visits, 6 wk apart, were r = 0.96, P < 0.03, and CV = 6.55% for total body fat; r = 0.91, P < 0.03, and CV = 5.69% for percentage body fat; and r = 0.96, P < 0.001, and CV = 2.3% for FFM (12).
Statistical analyses
The descriptive data were reported as means ± SDs. Statistical analyses were performed by using SAS 6.12 for WINDOWS (SAS Institute, Cary, NC) and S-PLUS 4.5 for WINDOWS (MathSoft Inc, Seattle). The relation between changes in girls' total and percentage body fat and potential predictors (age, total and percentage body fat at baseline, SEE and AEE adjusted for FFM and body fat, mothers' and fathers' total and percentage body fat and FFM at baseline, and time to follow-up visits) was assessed by multiple regression analysis. The stepwise elimination procedure was used to establish the optimal model. Regression equations are presented with R2 values, and any variable with a P value <0.05 for the last determinant added are presented. Correlations between variables were determined by using Pearson's correlation coefficient. The correlation matrix of all variables at baseline (Table 2
) showed that FFM was correlated with age, total body fat, SEE, and AEE. Thus, to remove the confounding effect in this model, we considered age, SEE, and AEE adjusted for FFM and body fat. In general, the adjustment procedure was made according to Ravussin and Bogardus (13) by using the following equation:
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| RESULTS |
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All the girls were offered an identical menu and were allowed to make their own food selections. The energy compositions of the lunches and evening meals were similar for all the girls. When the girls' energy intake was compared with their total body fat by DXA, no significant differences were observed. We believe that it is unlikely that the evening meal had a significant effect on SEE because the last main meal was consumed between 1700 and 1800. The girls went to bed no earlier than 2100, usually at
2200, and SEE was based on a period of
89 h, beginning 35 h after the meal. Therefore, the postprandial period occurred before the girls went to sleep.
From the baseline visit to the first follow-up visit, the girls' mean change in total body fat adjusted for FFM was 1.2 ± 2.7 kg and the mean change in percentage body fat was -2.0 ± 5.0%. From the baseline visit to the second follow-up visit, the girls' mean change in total body fat adjusted for FFM was 3.3 ± 4.0 kg and the mean change in percentage body fat was -0.8 ± 5.9%. The change in total body fat between the baseline visit and the first follow-up visit was regressed on all study variables, including interaction of total body fat with time to first follow-up visit, SEE adjusted for FFM and body fat interaction with time from baseline to first follow-up visit, and AEE adjusted for FFM and body fat interaction with time from baseline to first follow-up visit. Total body fat and FFM were highly correlated at baseline (Table 2
). Thus, the change in total body fat was adjusted for FFM. The change in EE was adjusted for FFM and body fat. As shown in Table 3
, for the change in total body fat between the baseline visit and the first follow-up visit, SEE and fathers' total body fat were significant predictors of body fat in the girls. Note that the girls' SEE was positively predictive of their body fat gain (ie, a higher rather than a lower SEE tended to predict body fat gain). As more time elapsed (ie, between baseline and the second follow-up visit), fathers' total body fat was the only significant predictor of changes in the girls' body fat. The relation between fathers' percentage body fat and SEE adjusted for body fat and their daughters' changes in percentage body fat between baseline and the first follow-up visit is shown in Table 4
. Girls' age at baseline and AEE adjusted for FFM were significant predictors of percentage body fat between baseline and the first follow-up visit. The only significant variable for change in percentage body fat between baseline and the second follow-up visit was the fathers' percentage body fat.
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| DISCUSSION |
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Reduced TEE was shown to be an important factor in the excessive weight gain of infants and children born to obese parents (1, 2). One study examined the relation between infant TEE and parental BMI in 124 infants at 12 wk of age (14). That study showed that no aspect of infant EE was related to parental BMI. Moreover, there was no significant difference between TEE of 2 subsets of infants born to parents with high (>30) and low (<20) BMI. In contrast, our study showed that there was a relation between the fathers' body fat and their daughters' SEE, AEE, and body fat.
In a retrospective study, the probability of obesity in young adulthood was examined in relation to the presence or absence of obesity at various times throughout childhood and the presence or absence of obesity in the child's parents (15). That study showed that obese children aged <3 y and without obese parents were at low risk of obesity in adulthood but that, among older children, obesity was an increasingly important predictor of adult obesity, regardless of whether the parents were obese. The effect of parental obesity on the risk of obesity in adulthood was most pronounced among obese and nonobese children aged <10 y. The risk of adult obesity was significantly greater if either parent was obese. Our cohort of normal-weight girls aged 4.88.9 y at the initiation of the study showed a relation between the fathers', but not the mothers', body fat and subsequent changes in the daughters' body fat.
Three cross-sectional studies in children and adolescents compared EE in obese and lean subjects (35). One study examined whether EE components (TEE, REE, and AEE) in 73 children aged 47 y were related to the children's body fatness or to the fatness of their parents (3). TEE was measured over 14 d by using doubly labeled water and AEE was derived by subtracting postprandial REE from TEE. Fat and FFM were measured in the children and their parents by using bioelectrical impedance analysis. The study showed no significant correlations between TEE, REE, and AEE in the children (after adjustment for FFM) and body fat in the children or body fat in their mothers or fathers (3). In another study the relation between EE and obesity was examined in 46 prepubertal children aged 1011 y (4). The children were grouped into levels of obesity based on tertiles of subscapular plus triceps skinfold thicknesses. TEE was measured over 8 d by using doubly labeled water and REE was measured by using indirect calorimetry. The study showed no significant differences in TEE, REE, or AEE among the 3 obesity levels after adjustment for FFM. The heaviest children had the same AEE and TEE as the leanest children while weighing 14 kg more, indicating that obese children had a lower activity level than did nonobese children.
In another study, REE and TEE were measured in 28 nonobese and 35 obese adolescents aged 1218 y by using indirect calorimetry and doubly labeled water (5). The investigators found that absolute values for REE and TEE were significantly greater in the obese adolescents. The ratio of TEE to REE was similar in the 2 groups, indicating that the proportion of TEE allocated between resting and nonresting states did not significantly differ between the obese and the nonobese adolescents. The investigators concluded that lower EE could not be responsible for the maintenance of obesity in adolescents.
Cross-sectional studies showed associations between various metabolic factors and obesity, but these relations cannot be interpreted as causal. In longitudinal studies, such relations come a step closer to showing causality, although the factors studied are still predictors and not necessarily causes. A recent longitudinal study examined whether childhood EE components or parental body composition were related to the rate of change of body fat over 4 y in prepubertal children of obese and nonobese parents (7). The researchers studied 75 white children, aged 47 y at study entry, over a 4-y period by taking annual measurements of body composition (by anthropometry and bioelectrical impedance analysis), REE (by indirect calorimetry), and TEE and AEE (by doubly labeled water). The major determinants of change in fat mass adjusted for FFM were sex (fat gain was greater in girls), fatness at baseline, and parental fatness. None of the components of EE was inversely related to change in fat mass. The researchers concluded that the main predictors of change in fat mass relative to FFM were sex, fatness at baseline, and parental fatness, but not reduced EE (7). However, the body fat percentages encountered in the study were as high as 39.2%, suggesting that several of the children were already overweight when the study began. The development of obesity may eliminate preexisting differences in EE (16).
The results of our study in prepubertal and premenarcheal girls, as well as studies in infants (1) and children (2), suggest that potential mechanisms for body fat gain, which are known to have a familial component, include low TEE, REE, and AEE and increased energy intake. In addition, our study showed that fathers' total or percentage body fat was predictive of long-term changes in total and percentage body fat in this cohort of premenarcheal girls. Collection of further longitudinal data is warranted to establish whether these results persist throughout puberty.
| ACKNOWLEDGMENTS |
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| REFERENCES |
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