Regional Subcutaneous-Fat Loss Induced by Caloric Restriction in Obese Women
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1 Regional Subcutaneous-Fat Loss Induced by Caloric Restriction in Obese Women Jack Wang, Blandine Laferrère, John C. Thornton, Richard N. Pierson, Jr., and F. Xavier Pi-Sunyer Abstract WANG, JACK, BLANDINE LAFERRÈRE, JOHN C. THORNTON, RICHARD N. PIERSON, JR., and F. XAVIER PI-SUNYER. Regional subcutaneous-fat loss induced by caloric restriction in obese women. Obes Res. 2002;10: Objective: With anthropometric models using skinfolds and circumferences, we studied changes in the percentage of subcutaneous fat in the total cross-sectional area (SF%) at four body sites in obese women, before and after weight loss induced by 6 months of caloric restriction. Research Methods and Procedures: In 61 obese women [31 African Americans and 30 whites; ages, 24 to 68 years; body mass index (BMI), 28kg/m 2 ], we measured SF% at the midpoint of the upper arm and thigh and the waistline and hipline, and we measured the percentage of total body fat by DXA before (Obs#1) and after (Obs#2) a 6-month nonintervention control period and then after 6 months on a 1200 kcal/d diet (Obs#3). Results: The mean body weight and BMI increased (1.8 kg and 0.61 kg/m 2 ; p ), but there were no significant changes in any other body composition measurements from Obs#1 to Obs#2. The means of Obs#3 for weight and BMI decreased by 11%, and the percentage of total body fat decreased by 13% of Obs#2 mean values (p ). The mean SF% at each site decreased 7.6% to 18.0% of the Obs#2 mean values (p 0.001). The SF% decreases were greater at mid-arm and mid-thigh than in the cross-sectional regions at the waistline and hipline (p 0.05). There was no interaction between age or ethnicity (p 0.2). Conclusions: In obese women, caloric restriction alone reduces anthropometrically measured subcutaneous fat proportionally more in peripheral than in central regions. Received for review July 23, Accepted for publication in final form May 17, Body Composition Unit and Obesity Research Center, Department of Medicine, St. Luke s- Roosevelt Hospital, Columbia University, New York, New York. Address correspondence to Jack Wang, Body Composition Unit, St. Luke s-roosevelt Hospital, 1111 Amsterdam Avenue, New York, NY jw9@columbia.edu Copyright 2002 NAASO Key words: obesity, caloric restriction, anthropometrics, subcutaneous fat Introduction Many studies have reported associations of central obesity with hypertension, diabetes, and heart disease (1,2). These associations were independent of the degree of obesity, but dependent on fat distribution (2). Therefore, it is important to better understand the impact of caloric restriction not only on total body-fat loss, but also on fat distribution. Most previous studies have assessed the impact of caloric restriction on weight and total body fat as the primary outcomes. Cordero-MacIntyre et al. (3), however, have recently studied the effect of a 1200-kcal diet on skinfold thickness and regional body composition measured by DXA in postmenopausal women. However, these two techniques measure different aspects of subcutaneous-fat distribution. Lovejoy et al. (4) made comparisons of measured regionalfat distribution by DXA between African-American and white women. To our knowledge, there are no studies comparing changes in subcutaneous-fat amount at different regions during caloric restriction in both African-American and white obese women. Thus, how subcutaneous-fat amounts change in different body regions during weight loss by caloric restriction remains unknown. Lack of easily applicable techniques for measuring such changes in obesity is probably the main reason. We have shown previously, using skinfolds and circumferences, that subcutaneous-fat area can be calculated as a percentage of a cross-sectional area for the body location where the circumference and skinfold thickness are measured (5). In a longitudinal body-composition study, a detailed body-composition evaluation, including anthropometrics, was performed before and after a 6-month nonintervention control period and then after 6 months on 1200 kcal/d diet in obese African-American and white women. With this database, we tested the hypothesis that caloric restriction reduces subcutaneous fat proportionally more in central regions than in peripheral regions in obese women. OBESITY RESEARCH Vol. 10 No. 9 September
2 Subjects and Methods Data obtained from 61 obese women are included in this report. The inclusion criteria were as follows: African- American or white women; ages 24 to 68 years; body mass index (BMI) 28 kg/m 2, but not weighing 250 lbs (due to the ability of the DXA scan system); and not on medication affecting bone homeostasis (oral contraceptives, hormone replacement therapy, calcitonin, fluoride, steroids or diuretics). All subjects were healthy according to medical history, physical examination, and routine blood chemistry analyses. Each subject had body-composition evaluations before (Obs#1) and after a 6-month nonintervention control period (Obs#2), and then after 6 months on a caloric-restriction diet of 1200 kcal/d (Obs#3) with a full or partial formula diet with weekly visits to our outpatient weight-loss center. The formula contains 24% protein, 10% fat, and 66% carbohydrates. The women were instructed not to change their level of physical activity during the entire study. The percentage of total body fat and fat mass in the arms, legs, and trunk regions were measured by a whole-body DXA scan using Lunar model DPX-L (Madison, WI), with a precision of 1.2%. The anthropometric measurements are four body circumferences measured with the Dritz sewing tape (mid-arm, mid-thigh, waist, and hip), with an average precision of 1 cm, and five skinfold thicknesses using Lange calipers (triceps and biceps, mid-thigh, umbilicus, and abdomen (5 cm below the umbilicus), having an average precision of 2.5 mm. All measurements were performed while the subject wore a hospital gown with minimum underwear. The study was approved by the St. Luke s-roosevelt Hospital Internal Review Board (IRB) and informed consent was obtained from each subject. Subcutaneous-fat areas at the cross-sectional areas of mid-arm and mid-thigh, and at the locations for waist- and hip-circumference measurement were calculated using the models described previously (5), as shown below: The mid-arm subcutaneous-fat area (ASF mm 2 ) D 2 / 4 d 2 /4, where D is the diameter of the whole crosssection (D mid-arm circumference/ ), d is the diameter of the lean area (d D (triceps biceps)/2), and ASF mm 2 is the subcutaneous-fat area and the percentage of subcutaneous-fat in the total cross-section (ASF%) {ASF mm 2 /( D 2 /4)} 100%. The subcutaneous-fat area for the mid-thigh was calculated using skinfold thickness, and the circumference was measured at the mid-thigh (TSF mm 2 ). For the waist (WSF mm 2 ), subcutaneous-fat area was calculated using umbilicus skinfold thickness and waist circumference; for the hip (HSF mm 2 ), it was calculated using abdomen skinfold thickness (5 cm below the umbilicus) and hip circumference. The percentage of subcutaneous-fat area in the cross-sectional area for each site was calculated as (subcutaneous-fat area/total cross-sectional area) 100%. Means and SDs were calculated for each measured variable at each observation. The paired Student s t test was used to test the hypothesis that the mean change in measured value between observations was equal to zero. Repeated-measures ANOVA was used to test the hypothesis that the mean values of the percentage reductions at the four sites were equal. Fisher s least significant difference procedure was used to perform multiple comparisons among the means. The Student s t test was used to test the hypothesis that the mean percentage reduction were equal for African- American and white women. Correlations between age and the study variables were calculated. All comparisons were made within subjects. Therefore, age was controlled for all statistical analyses. The level of significance for all statistical tests of hypothesis was p All statistical calculations were performed using the SAS statistical software package (Computer Resource Center, Santa Monica, CA). Because our goal was to study the changes in fat distribution before and after a 6-month diet for weight loss, we only made the comparisons between Obs#2 and Obs#3 for all of the anthropometric measurements in this report. Results The means of body weight and BMI at the end of the 6-month nonintervention period (Obs#2) were 1.8 kg and 0.6 kg/m 2 higher than the means at Obs#1, respectively (p ). Because the purpose of the study was to investigate the effect of dieting on fat distribution, results measured immediately before the hypocaloric-diet period (Obs#2) were used as baseline values for comparisons before and after interventions. Table 1 shows the means and SDs of age, weight, height, BMI, and the percentage of total body fat before (Obs#2) and after the 6-month caloric restriction (Obs#3). After the 6-month caloric restriction, weight and BMI were each significantly reduced by 11%. and total body fat was reduced by 13% (p ). Figure 1 shows that the 6-month caloric restriction reduced circumferences at the four sites significantly (p ). The reduction as a percentage of the baseline (Obs#2) ranged from 6.1% for the mid-thigh to 7.8% for the waist. The reduction percentages were similar at the four sites. Figure 2 shows that skinfold thickness was significantly reduced at the five sites after the 6-month diet period (p ). The reductions as percentages of the baseline (Obs#2) ranged from 14.9% for the umbilicus to 24% for the biceps. Although there were no statistically significant differences among the study sites for the percentage of reduction, the magnitude of the reductions in mid-arm and mid-thigh were more than in the trunk regions. Figure 3 shows that subcutaneous-fat areas were significantly reduced at each of the four cross-sectional sites (p 0.001). The reduction as a percentages of baseline (Obs#2) were 18.0% at the mid-arm, 15.2% at the mid-thigh, and 886 OBESITY RESEARCH Vol. 10 No. 9 September 2002
3 Table 1. Weight, height, body mass index (BMI) and DXA-measured percentage of total body fat of the 61 studied subjects before and after a 6-month caloric-restriction diet (mean SD) Time Age (years) Weight (kg) Height (cm) BMI (kg/m 2 ) Percentage of total body fat Before After Changes Changes as percentage of prediet values 11% 0 11% 13% p for all changes. 7.6% and 11.8% at the cross-section where waist and hip circumferences were measured, respectively. There were statistically significantly differences among the mean percentage reductions (p 0.001, ANOVA). The reductions in the mid-arm were significantly larger than waist and hip regions. The reductions in the mid-thigh were significantly larger than in the abdominal region, but not than the hip region. There were no significant correlations between age and SF% reduction in either ethnic group. Race had no significant influence in any of the statistical outcomes (p 0.2). Table 2 shows the changes in DXA-measured fat mass in the arm, leg, and trunk regions. All the changes were statistically significant (p ). Although there were no significant differences among the regions for the percentage of reduction in fat mass from baseline, the magnitude of the reduction in each region was similar to the results estimated by the anthropometric models. Discussion After the 6-month caloric restriction, these obese women lost an average of 11% of their baseline weight measured at the completion of a 6-month nonintervention period. The data indicates that the decreases in skinfold thickness were higher than the decreases in circumferences for each measured body region. It also indicates that the magnitude of decreases in skinfold thickness in the peripheral regions were larger than the trunk regions. This is one of the first reports using anthropometric measurements and models showing that moderate caloric restriction proportionally reduces subcutaneous fat in the peripheral regions more than in the central region in obese African-American and white women. These results suggest that whereas moderate caloric restriction reduces total body fat and central-fat mass, both of which are associated with risk factor improvements, it does not lower the ratio of Figure 1: Means of circumferences in millimeters measured before (solid bars) and after (open bars) a 6-month caloric-restriction diet; all changes were statistically significant (p ). The changes (after before) as the percentage of pre-caloric restriction values were not significantly different among sites (least significant difference 2.3%). Figure 2: Means of skinfold thicknesses in millimeters measured before (solid bars) and after (open bars) a 6-month caloric-restriction diet; all changes were statistically significant (p ). The changes (after before) as the percentage of pre-caloric restriction values varied by sites: changes in the mid-arm and mid-thigh sites were larger than changes in the waist and hip regions (least-significant difference 10%). OBESITY RESEARCH Vol. 10 No. 9 September
4 Figure 3: Means of subcutaneous fat area as the percentage of cross-sectional areas measured before (solid bars) and after (open bars) 6-month caloric restriction. All changes were statistically significant (p 0.001). The changes (after before) as the percentage of pre-caloric restriction values varied by sites: changes in the mid-arm region were larger than changes in waist and hip sites, and changes in mid-thigh region were larger than waist (least-significant difference 10%). central-to-peripheral subcutaneous fatness. For example, our results show that the ratio of waist-to-hip circumference and the ratio of central-to-peripheral subcutaneous-fat area at baseline were almost identical to that measured after the 6-month diet restriction (ratio of waist-to-hip circumferences: at baseline vs after the 6-month diet restrictions; ratio of central to peripheral region subcutaneous-fat areas: at baseline vs after the 6-month diet restriction). This observed effect of caloric restriction on fat-distribution pattern was not influenced by either age or ethnicity. Recently, Cordero-MacIntyre et al. (3) reported that using a 3-month caloric-restriction diet in 49 postmenopausal white obese women resulted in significant reductions in arm and leg skinfolds, but no changes in abdominal skinfolds; these results are different from our findings. The prevalence of obesity in the United States has increased steadily over the past 20 years. Many studies have reported correlations between health risk and central adiposity. Reduction of body fatness, especially in the central region, has been increasingly considered a primary factor for reducing these health risks. Most of the epidemiological data strongly suggest that caloric intake is a major contributor to obesity (6). As a result, numerous investigators have restricted dietary intake as a treatment for obesity. Pi- Sunyer has warned the public that extreme caloric restriction may be harmful, and individuals should not take such an approach without direct physician supervision (7). George et al. reported that dietary-fat content has a positive relationship with fat distribution in both women and men (8). Dreon et al. demonstrated that not just dietary fat alone, but rather the dietary-fat/carbohydrate ratio, influences adiposity in middle-aged men (9). Golay et al. reported that weight loss was similar in obese subjects either on a low- or high-carbohydrate diet (10). The main purpose of this research project, which generated the database presented in this report, was to study the effects of a 6-month moderate calorie restricted balanced diet inducing 10% weight loss on bone density in obese women (11). Neither the diet composition nor the level of caloric restriction was a part of the study. Murakami et al. performed a study of subcutaneous-fat distribution and body size among Japanese women in their early 20s and again 5 years later by measuring skinfold thickness at 14 points on the body (12). They found significant increases in subcutaneous fat at the lower trunk, such as the waist and intragluteal regions. They concluded that decreased physical activity with age as observed by questionnaires might have contributed to such changes. In our study, participants were asked not to change their physicalactivity pattern throughout the study period. Therefore, the observed weight loss and changes in fat and fat distribution were purely diet-induced. Tracking changes in fat distribution in a longitudinal study requires accurate and precise assessment methods. Although CT and magnetic resonance imaging (MRI) are Table 2. Fat mass measured by DXA in arms, legs, and trunk before and after a 6-month caloric-restriction diet (mean SD) Time Fat in arms (kg) Fat in legs (kg) Fat in trunk (kg) Before After Changes Changes as percentage of prediet values 25% 21%0 21% p for all changes. 888 OBESITY RESEARCH Vol. 10 No. 9 September 2002
5 well-accepted techniques in subjects with weights in the normal range (13,14), they are not widely available and are expensive. Because 50% of total body fat is located in the subcutaneous regions, skinfold thickness has been considered a practical and simple approach for assessing subcutaneous fat (15). Models using tricep skinfold and circumference, measured at the mid-arm to predict cross-sectional skeletal muscle area at mid-arm, have been used for more than two decades (16). Previous studies using skinfolds and circumferences have shown reliabilities for estimating body composition that are higher than those using bio-impedance (17,18). Recent studies have further demonstrated that anthropometric measurements are reliable estimators of CTor MRI-measured body-fat distribution and skeletal muscle and body-fat distributions (13,14). Estimation of subcutaneous-fat area from anthropometry is based on many assumptions. But this is also true for other traditional, as well as new methods, for measurement of body composition. For example, DXA is considered a reliable method for determining total and regional adiposity. However, it is important to mention a well-known technical limitation about the DXA technique: DXA-determined adiposity does not include fat existing in any scan regions containing bone. Because ribs occupy a large portion of the truncal region, DXA may not provide reliable fat measurement for the entire truncal region. One of the objectives of this study was to estimate changes in the amount of subcutaneous fat using widely available, easy, and inexpensive anthropometric measurements during weight loss. In a recently completed study to validate these anthropometric models with MRI in 23 adults, we found that the MRI measured subcutaneous-fat areas were highly correlated with the values estimated with anthropometric models at each region; with r 2 ranging 0.78 for the trunk region to 0.92 for the mid-thigh (19). Our models measure subcutaneous-fat area at cross-sectional sites, which reflects subcutaneous-fat distribution more accurately than measurements of skinfold thickness or circumference alone. However, the lack of precision of this inexpensive and widely available field technique has been a major concern to many investigators. Even using the same caliper, but with different jaw pressure, may give different skinfold results (20). Standardization of measurement instrumentation and protocols and well-trained observers can greatly reduce inter- and intra-observer errors (21). In our laboratory, anthropometric measurements have been performed routinely for more than three decades using the same type of caliper (Lange Caliper) and measuring tape (Dritz) and the same measurement protocols. We require that any observer must have a measuring precision 2% for circumferences and 10% for skinfolds (20); they must also show no significant differences from the observer who has performed more than one third of the 5,000 subject measurements and conducted the training during the past 25 years. In summary, this study demonstrates that anthropometric measurements are an easily applicable technique for studying changes in regional subcutaneous-fat distribution in obese women. Caloric restriction alone proportionally reduces subcutaneous fat more in peripheral than in central regions in obese women. This study suggests that caloric restriction alone reduces the degree of obesity, but does not improve the ratio of central-to-peripheral subcutaneous-fat distribution in either African-American or white obese women. Acknowledgments Supported by National Institute of Diabetes and Digestive and Kidney Diseases Grant References 1. Freedman DS, Serdula MK, Srinivasan SR, Berenson GS. Relation of circumferences and skinfold thicknesses to lipid and insulin concentrations in children and adolescents: the Bogalusa Heart Study. Am J Clin Nutr. 1999;69: Gillum RF, Mussolino ME, Madans JH. Body fat distribution and hypertension incidence in women and men. The NHANES I Epidemiologic Follow-up Study. Int J Obes Relat Metab Disord. 1998;22: Cordero-MacIntyre ZR, Peters W, Libanatl CR, Espana RC, Howell WH, Lohman TG. Effect of a weight-reduction program on total body and regional body composition in obese postmenopausal women. Ann N Y Acad Sci. 2000;904: Lovejoy JC, Smith SR, Rood JC. Comparison of regional fat distribution and health risk factors in middle-aged white and African American women: The Healthy Transitions Study. Obes Res. 2001;9: Wang J, Thornton JC, Russell M, Burastero S, Heymsfield B, Pierson RN Jr. Asians have lower body mass index (BMI) but higher percent body fat than do whites: comparisons of anthropometric measurements. Am J Clin Nutr. 1994;60: Harnack LJ, Jeffrey RW, Boutelle KN. Temporal trends and energy intake in the United States: an ecologic perspective. Am J Clin Nutr. 2000;71: Pi-Sunyer XF. The role of very-low-calorie diets in obesity. Am J Clin Nutr. 1992;56:240S 243S. 8. George LA, Temblay A, Depres JP, Leblanc C, Bouchard C. Effect of dietary fat content on total and regional adiposity in men and women. Int J Obesity. 1990;14: Dreon DM, Frey-Hewitt B, Ellsworth N, Williams P, Terry RB, Wood PD. Dietary fat:carbohydrate ratio and obesity in middle-aged men. Am J Clin Nutr. 1988;47: Golay A, Allaz AF, Morel Y, de Tonnac N, Tankova S, Reaven G. Similar weight loss with low- or high-carbohydrate diets. Am J Clin Nutr. 1996;63: Laferrere B, Funkhouser A, Thornton JC, Pi-Sunyer FX. Total body calcium in obese women: validation of dual-energy x-ray absorptiometry against in vivo neutron activation analysis. Ann N Y Acad Sci. 2000;904: Murakami M, Hikima R, Arai S, Yamazaki K, Iizuka S, Tochihara Y. Short-term longitudinal changes in subcutane- OBESITY RESEARCH Vol. 10 No. 9 September
6 ous fat distribution and body size among Japanese women in the third decade of life. App Hum Sci. 1999;18: Goran MI, Gower BA, Treuth M, Nagy TR. Prediction of intra-abdominal and subcutaneous abdominal adipose tissue in healthy pre-pubertal children. Int J Obes. 1998;22: Rolland-Cachera MF, Brambilla P, Manzoni P, Akrout M, Sironi S, Del Maschio A, Chiumello G. Body composition assessed on the basis of arm circumference and triceps skinfold thickness: a new index validated in children by magnetic resonance imaging. Am J Clin Nutr. 1997;65: Lohman TG, Roche, AF, Martorell R, eds. Anthropometric Standardization Reference Manual. Champaign, IL: Human Kinetics; 1988 pp Frisancho AR. New norms of upper limb fat and muscle area for assessment of nutritional status. Am J Clin Nutr. 1981;34: Gualdi-Russo E, Toselli S, Squintani L. Remarks on methods for estimating body composition parameters: reliability of skinfold and multiple frequency bioelectric impedance methods. Z Morphol Anthropol. 1997;81: Wattanapenpaiboon N, Lukito W, Strauss BJ, Hsu-Hage BH, Wahlqvist ML, Stroud DB. Agreement of skinfold measurement and bioelectrical impedance analysis (BIA) methods with dual energy X-ray absorptiometry (DEXA) in estimating total body fat in Anglo-Celtic Australians. Int J Obes Relat Metab Disord. 1998;22: He Q, Wang J, Engelson ES, Kotler DP. Ability of an anthropometric model to track changes in subcutaneous adipose tissue area [Abstract]. FASEB J. 2002;16:A Gore CJ, Carlyon RG, Franks SW, Woolford SM. Skinfold thickness varies directly with spring coefficient and inversely with jaw pressure. Med Sci Sports Exerc. 2000; 32: Wang J, Thornton JC, Kolesnik S, Pierson RN, Jr. Anthropometry in body composition: an overview. Ann N Y Acad Sci. 2000;904: OBESITY RESEARCH Vol. 10 No. 9 September 2002
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