Clinical Science (1994) 87, 581-586 (Printed in Great Britain) 581 Regional fat distribution by dual-energy X-ray absorptiometry: comparison with anthropometry and application in a clinical trial of growth hormone and exercise Dennis R. TAAFFE, Barbara LEWIS and Robert MARCUS Musculoskeletal Research laboratory, Aging Study Unit, Geriatric Research, Education and Clinical Center, Veterans Affairs Medical Center, Palo Alto, CA, U.S.A., and Department of Medicine, Stanford University, Stanford, CA, U.S.A. (Received 10 March/l5 June 1994; accepted 4 July 1994) 1. The purpose of this study was to determine the suitability of ratios derived from dual-energy X-ray absorptiometry (DXA) whole body scans to assess regional fat distribution in older men and women by comparing them with the waist-to-hip ratio (WHR) and to evaluate their clinical utility by applying them in a clinical trial involving resistance exercise and recombinant human growth hormone. 2. Sixty-four healthy older adults (39 women and 25 men), aged 65-82 years, served as subjects. The ratios of trunk fat-to-total fat, trunk fat-to-body weight, trunk fat-to-limb fat and trunk fat % were determined by DXA. WHR was assessed on the same day, as was the ratio of subscapular/triceps skinfolds in men. Cardiovascular disease risk factors, functional capacity and serum lipids were also assessed. 3. A moderate relationship ( r = 0.360.54) between the WHR- and DXA-derived ratios were observed for both men and women. Both DXA and WHR showed similar associations with cardiovascular disease risk factors. However, in men, all DXA ratios were able to detect subtle changes in regional fat distribution resulting from daily administration of recombinant human growth hormone in conjunction with resistance exercise for 10 weeks, whereas the WHR or subscapular/triceps ratios did not. 4. This suggests that DXA-derived ratios may be more sensitive than conventional anthropometric methods in the assessment and categorization of body fat distribution. INTRODUCTION It is well recognized for health risk that in addition to adiposity, site of body fat deposition is crucial. Central obesity is associated with an increased risk for cardiovascular disease (CVD) and metabolic disease as well as overall mortality, whereas gluteal-femoral pattern obesity is not [l81. Assessment of adipose tissue distribution is conventionally undertaken anthropometrically using girths such as the waist and hip or by skinfolds at several sites on the trunk and extremities. These measurements can then be used in ratios that partition body fat into central and peripheral or upper and lower body portions, such as the subscapular-to-triceps [2] and waist-to-hip ratios (WHRs). Of the anthropometric methods, the WHR is the most widely used in epidemiological and clinical research and practice [8]. However, the WHR, which is dependent on pelvic skeletal structure, does not differentiate between fat and fat-free tissues and is prone to several methodological problems [9-111. Direct quantitative techniques, computed tomography [12, 131 and magnetic resonance imaging [14, 151, have therefore been proposed to examine regional fat distribution, however, the equipment is expensive and not readily available. In addition, computed tomography subjects the individual to a relatively high radiation dose. Recent modification of dual-energy X-ray absorptiometry (DXA) software to measure whole body and regional tissue composition lends itself to examining fat distribution in individuals [16, 171, especially in populations unable to undergo standard anthropometric assessment, such as the very old, the sick, and nonambulatory individuals. With the expanded use and availability of DXA to assess body composition, the purpose of this study was to evaluate the clinical utility of ratios of fat distribution derived from DXA by addressing the following three issues: (1) the ability of these ratios to simulate the WHR in older men and women, a population with increased total and central fat mass Key words: duaknergy X-ray absorptiometry, growth hormone, older men and women, regional fat distribution, resistance exercise. Abbreviations: BMI, body mass index; CHOL, total cholesterol: CVD, cardiovascular disease; DXA. dual energy X-ray absorptiometry; GH. growth hormone; MET, metabolic equivalent; LBM, lean body mass; PL, placebo; rhGH, recombinant human growth hormone; TrF, trunk fat; TrF/LimF. trunk-fat-telimb fat: TrF/BW. trunk-fat-to-body weight; TrFjTotF. trunk fat-to-total fat: TRIG, triacylglycerol; WHR, waist-to-hip ratio. Correspondence: Dr Dennis R. Taaffe. GRECC 182-8, Veterans Affairs Medical Center, 3801 Miranda Avenue, Palo Alto, CA 94304, U.S.A. 582 D. R. Taaffe et al. [18, 191 and an increased risk for cardiovascular disease [20, 213; (2) the relationship of DXA ratios and the WHR to selected CVD risk factors (functional capacity and serum lipids); and (3) the sensitivity of DXA-derived ratios versus conventional anthropometric methods in determining longitudinal changes in body fat distribution. To evaluate the last point we monitored the changes in body composition of a group of older men who were participating in a trial of resistance exercise and recombinant human growth hormone (rhGH). MET H0DS Subjects Sixty-four healthy older adults, 39 women (65-82 years) and 25 men (66-79 years) with a body mass index (BMI) of < 30 kg/m*, recruited to participate in exercise studies, served as subjects. All participants completed a screening procedure that consisted of a health history questionnaire, physical examination, multiphasic laboratory profile, maximal exercise stress test, and lateral thoracic and lumbar spine radiographs. All subjects were apparently healthy, free of disease and disorders that would prohibit them from participating in a vigorous exercise programme. Activity history upon entry revealed participants were sedentary to moderately active. Eighteen of the women were taking exogenous oestrogen. The procedures were approved by the Human Subjects Committee of Stanford University, and all subjects gave written consent. Exercise protocol The 25 men participated in a randomized doubleblind, placebo-controlled exercise trial to determine whether the administration of rhGH enhanced the muscle strength response to a programme of progressive resistance exercise. Individuals initially underwent a 14 week training period to invoke a trained state and achieve a levelling off in muscle strength. Subjects then received daily injections of either rhGH (0.02 mg/kg body weight; Somatropin; Genentech, Inc., San Francisco, CA, U.S.A.) or an equal volume of placebo (PL) (Genentech, Inc.) while continuing to train for an additional 10 weeks. Eighteen subjects completed the 24 week training programme. Muscle strength results of this trial will be separately reported. Briefly, the training programme consisted of progressive resistance exercise, three sessions per week. Each session consisted of a circuit of 10 exercises involving major upper and lower body muscle groups using Universal (Universal Gym Equipment, Cedar Rapids, I A , U.S.A.) and Nautilus (Nautilus Sports/Medical Industries, Inc, Independence, VA, U.S.A.) equipment. Subjects performed three sets of eight repetitions for each exercise at an initial intensity equal to 75% of their individual one- repetition maximum (1-RM), which is the maximal weight an individual can lift one time with acceptable form. To assure the progressive nature of the programme, 1-RM values for all exercises were recorded every two weeks. Body composition analysis Lean body mass (LBM, kg), fat mass (kg), and percentage body fat were assessed by DXA (Hologic Q D R lOOO/W, Waltham, MA, U.S.A., software version 5.47). In addition, trunk mass, limb mass, and bone-free lean mass of the limbs and trunk were derived from the whole body scan. The scan time was approximately 14min with a whole body radiation dose of < 1 mrem. The coefticient of variation for replicate measurements in our laboratory is < I % for LBM, fat mass (kg), percentage body fat, limb mass, trunk mass and trunk lean mass, and 1.1% for limb lean mass. Body fat distribution The ratios of trunk fat-to-total fat (TrF/TotF), trunk fat-to-body weight (TrF/BW), trunk fat-tolimb fat (TrF/LimF), and trunk fat % (TrFO/,;trunk mass comprised of trunk fat) were derived from DXA (Hologic, lOOO/W) whole body scans. Default segmentation lines for whole body analysis were placed at specific anatomic landmarks that divided the body into upper limbs, lower limbs, trunk, and head. To define the upper limb as a separate segment a vertical line was extended between the head of the humerus and the glenoid fossa of the scapula. An oblique line placed through the femoral neck demarcates the lower limbs from the trunk. This segment includes the lateral portion of the hip region and hence gluteal-femoral subcutaneous fat. The head is separated from the trunk by a horizontal line placed inferior to the mandible, therefore the trunk includes the thorax, abdomen, pelvis, and the superior medial portion of the thigh. Limb fat comprises the sum of both upper and lower limbs. The precision error (coefficient of variation for duplicate comparisons) in our laboratory for upper limb fat mass is 2.3%, for lower limb fat mass 1.1%, trunk fat mass 1.9%, and trunk percentage fat 1.4%. In the men, we also assessed peripheral and central fat distribution by measuring triceps and subscapular skinfolds in triplicate with Lange calipers (Cambridge Instruments, Cambridge, MD, U.S.A.). WHR Circumference measures were performed in triplicate with the subject in the standing position. Waist circumference was measured at the natural waistline between the lower rib margin and the iliac crest. When the natural waistline was not discernible the waist was measured at the umbilicus. Hip circumference was measured at the level of widest circumfer- Regional fat distribution and dual-energy X-ray absorptiometry ence over the buttocks. Both measures were rounded to the nearest 0.1 cm. Table I.Subject characteristics. Values are mean f SEM. Statistical significance: *P<O.O5, tP<0.001 for women compared with men. Functional exercise capacity Peak functional capacity or physical fitness was determined by a symptom-limited maximal graded treadmill test using a modified Balke protocol [22]. Treadmill speed was kept constant at 2.2 miles/h with the grade increasing l%/min from the initial grade of 0%. Blood pressure, heart rate and ECG were monitored throughout the test. Functional capacity in metabolic equivalents (METs) was determined indirectly by treadmill speed and grade [23]. Lipid profiles Total cholesterol (CHOL) and triacylglycerol (TRIG) were determined from fasting serum samples. Total cholesterol was measured using cholesterol esterase on a Technicom SMAC 3 System and triacyglycerol was determined using an enzymatic method on the Kodak Ektachem 700. Statistical analysis Data were analysed with a statistical software package (Statview 11, Abacus Concepts Inc., Berkeley, CA, U.S.A.). Differences between men and women were determined by two-tailed unpaired t tests, as were differences between women taking exogenous oestrogen and those not taking oestrogen. Linear regression was used to examine the relationship between variables. Correlation coefficients were derived from the linear regression program. A two-way (group x time) repeated measures analysis of variance was used to determine the changes in body composition resulting from the exercise and rhGH intervention programme. Where appropriate, the Scheffe test was employed to locate the source of significant differences. An alpha level of 0.05 was required for significance. Results are given as meansfSEM. RESULTS Characteristics of the study group are shown in Table 1. There were no significant differences in any measured variable between women taking exogenous oestrogen and those not taking oestrogen, therefore results for these groups are pooled. There was no difference between men and women in age. However, men were taller, heavier, had a higher LBM and lower percentage body fat than women. Total body fat was significantly greater in women, with the difference due to an increased limb fat mass. As expected, the WHR was higher in men as were the DXA ratios of TrF/LimbF and TrF/ TotF (Table 2). As men had a significantly higher body weight and trunk mass than women, the ratio of TrF/BW and TrF% were lower in men. 583 Age (yean) Height (cm) Weight (kg) BMI (kg/mz) LBM (kg) Body fat (%) Body fat (kg) Trunk mass (kg) Limb mass (kg) Trunk fat (kg) Limb fat (kg) METs CHOL (mmol/l) TRIG (mmol/l) Women Men (n = 39) (n = 25) 68.5 f 0.6 161.7+ 1.0 65.4 k I.3 25.0 f 0.4 43.0 f 0.5 33.6k1.1 22.4+ 1.1 32.7 f 0.7 28.3 f0.7 9.9 f 0.6 11.7 0.6 6.6 0.3 5.90 f0.16 I .35 k 0.1 I 69.9 & 0.7 176.5+_1.6t 81.8 f 2.1 t 26.3 0.5 63.0 +_ I.4t 22.5 f 0.9t 18.5kl.l* 41.9+ I.2t 34.8 f 0.9t 9.4 f 0.6 8.4f0.5t 9.0 f 0.27 5.74 fO.18 1.66 k0.16 + + Table 2. Ratios of fat distribution by anthropometry and DXA. Values are means SEM. Statistical significance: *P < 0.001 for women compared with men. WHR TrF/LimbF TrF/TotF TrF/BW TrF% Women (n = 39) Men (n = 25) 0.803 +O.OlO 0.837 k0.036 0.431 +O.OlO 0. I47 f0.007 29.4 f I.3 0.968 f0.010* 1.125 fO.M3* 0.497 f0.0IO* 0. II3 f 0.006' 22.0f I.o* Table 3. Relationship of DXA ratios ( x variable) to W H R ( y variable). Abbreviations: SEE, standard error of the estimate, NS. not significant. x variable Regression equation R SEE Significance - Women (n = 39) TrF/LimbF TrF/TotF TrF/BW TrF% y = 0.666 +0.164~ y =0.573 +0.533~ y=O.71 I + 0 . 6 2 5 ~ y =0.722 +0.003x 0.54 0.53 0.43 0.36 0.055 0.055 Men (n = 25) TrF/Limb TrF/TotF TrF/BW TrF% y = 0.884 y = 0.792 y = 0.873 y = 0.873 +0.075~ +0.353~ +0.842~ +0.004~ 0.36 0.38 0.50 0.46 0.045 0.045 0.059 0.061 0.042 0.043 P<0.001 P<O.Wl P<O.Ol P <0.05 NS NS P<O.Ol P <0.05 Men had a significantly higher functional capacity then women, however, there were no gender differences in total cholesterol or triacylglycerol. DXA ratios and WHR As older men and women represent two distinct populations, comparisons between DXA-derived ratios and the WHR were stratified by gender. As shown in Table 3, a moderate relationship exists for all DXA-derived ratios and the WHR. The strongest relationship between the WHR and DXA ratio for D. R. Taaffe et al. 584 Table 4. Correlation between ratios of fat distribution and CVD risk factors in women and men. Statistical significance: *P <0.05. tP<0.01. :P<O.005. Ratio METs CHOL TRIG Table 5. Whole body and regional composition assessment at base line and 14 and 24 weeks for rhGH and exercise trial. Values are means fSEM. Scheffe test (P<0.05): ’baseline versus 14 weeks, bbaseline versus 24 weeks, (14 weeks versus 24 weeks. 14 weeks Baseline Women (n = 39) WHR TrF/LimbF TrF/TotF TrF/BW TrF% Men (n = 25) WHR TrF/LimbF TrF/TotF TrF/BW TrF% -0.24 -0.13 -0.16 - 0.40* - 0.44t -0.35 - 0.08 -0.15 - 0.49* - 0.49* 0.23 0.36* 0.36* 0.27 0.22 0.47: 0.33* 0.36* 0.35* 0.33* Body weight (kg) 0.34 0.21 0.29 0.36 0.35 0.13 0.25 0.22 0.06 0.03 men was that of TrF/BW (r=0.50, P<O.Ol) and for women TrF/LimbF ( r = 0.54, P < 0.001). WHR, D X A ratios and CVD risk factors Both the WHR- and DXA-derived ratios showed similar associations with functional capacity, as determined by MET level, and lipid levels for women and men (Table 4). For both women and men, all ratios were negatively correlated with MET level; however, only TrF/BW and TrFX reached statistical significance. All ratios were significantly correlated with triacylglycerol levels in women; however, only the DXA ratios of TrF/LimbF and TrF/TotF were significantly related to total cholesterol. For lipid levels in men, none of the ratios achieved statistical significance. Clinical application of D X A ratios Eighteen men completed the 24 week study (rhGH = 10, PL = 8) which produced substantial increases in muscle strength in both groups. However, two men in the rhGH group experienced oedema and were omitted from the body composition analysis. Although body weight did not change in either group, the rhGH group experienced a significant increase in LBM and a significant decrease in fat mass between baseline and 24 weeks (Table 5). Standard anthropometric assessment using the WHR and the ratio of subscapular/triceps skinfolds indicated no change in regional body fat distribution following either 14 or 24 weeks of training (Table 6). However, both trunk and limb fat mass determined by DXA declined over the course of the intervention period in the rhGH group. DXAderived ratios of TrF/LimbF, TrF/TotF, TrF/BW and TrF% all decreased between baseline and 24 weeks, the difference occurring after rhGH administration for 10 weeks, that is, from week 14 to 24. DISCUSSION Results of this study indicate a moderate relation- 24 weeks rhGH PL 77.6 f4.6 83.5 f4.3 76.9 f4.5 83.9 f4.4 77.5 f4.4 83.3 f4.5 LBM (kg)’ rhGH PL 60.5 f2.8 64.5 f2.8 61.1 f3.0 65.2f 2.7 62.5 f3.0b 64.7 f2.3’ Fat mass (kg)’ rhGH PL 17. I f2.3 19.0 f I .8 15.8f 1.9 18.6 f2.0 I5.0f 1.91.b 18.6 f2.4 Trunk lean mass (g) rhGH PL 31028k 1491 32682 f I592 31410+ I430 33044 f 1472 31683f 1604 Trunk fat mass (g)* PL 8613f 1405 9345 f981 7913f1193 9199f I100 7199f1178b 9129f 1286 Limb lean mass (g)’ rhGH PL 23694 f I I35 25191 f 1080 23850 f 1250 25528 f I180 Lomb fat mass (g)’ rhGH PL 7554 f978 8740 f890 6980 f708 8492 f927 32441 f I343 2-f 1253b,c 25500 k 901 6926 f781 8499fII50 *Main effect of time (F=6.21-3.96. P<O.O3). Table 6. Body fat distribution at baseline and 14 and 24 weeks for rhGH and exercise trial. Values are meanrf SEM. ScheHe test (P<O.O5): ’baseline versus 24 weeks, b14 versus 24 weeks. Baseline 14 weeks 24 weeks 0.972 f0.022 0.970f0.016 0.974 f0.028 0.973 fO.018 0.972 f0.029 0.984f0.016 Subscap/Tri sk* rhGH PL I .81 f0.25 2.36 k 0.39 1.78 f0. I4 2.22 f0.33 I .78 f0.16 2.33 f0.35 TrFiLimbFt rhGH PL 1.117fO.097 1.079f0.077 1.1 18fO.101 1.085f0.072 1.024f0.105a~b 1.078f0.083 TrF/TotFt rhGH PL 0.491 f0.024 0.488 f0.0 I7 0.489 f0.024 0.489 kO.015 0.465 f0.026a,b 0.484 f0.0 I8 TrF/BWt rhGH PL 0. I07 f0.012 0.1 10 fO.008 0.100fO.011 0.108 +0.008 0.05llfO.01 I2.b 0. I07 f0.010 TrF%t rhGH PL 20.6 & 2.2 21.6f 1.3 19.3f 1.9 21.0f 1.5 17.7 f2.0’,b 21.0f 1.8 WHR rhGH PL *Subscapular/triceps skinfold. tMain effect of time (F=9.33-5.84, P<O.OI). ship between the WHR- and DXA-derived ratios of fat distribution obtained from a whole body scan. However, DXA-derived ratios detected changes in regional fat distribution resulting from a combination of resistance exercise and rhGH intervention, Regional fat distribution and duaknergy X-ray absorptiometry whereas the WHR or subscapular/triceps ratios did not, suggesting DXA-derived ratios are more sensitive than conventional anthropometric methods to assess and categorize body fat distribution. Due to the importance of body fat distribution, specifically central in relation to peripheral fat, DXA-derived ratios in this study were aimed at partitioning trunk fat from the remainder of the body or in reference to the body as a unit. The ratio TrF/LimbF segments the body into central and peripheral portions, with LimbF a combination of upper and lower extremity limb fat. TrF/TotF examines central fat in relation to body fat mass while TrF/BW assesses trunk fat in relation to total body tissue mass. The index TrF%, is a localized measurement of central fat mass, relating trunk fat to trunk mass. The moderate relationships found between DXAderived ratios and the WHR in this study are similar to that reported by Fuller et al. [l 11 for the DXA ratio of trunk fat/leg fat and the WHR in young adults. By using WHR as a criterion, we do not suggest that WHR is the gold standard for assessing fat distribution and that alternative methods must agree highly with it. Nevertheless, we recognize that the WHR is widely used and established in cross-sectional [19, 241, longitudinal [7, 251, and intervention [26, 271 studies and that it is a robust predictor of disease risk and mortality [l, 2, 4-71. Although a modest association exists between DXA-derived ratios and WHR, both methods of examining fat distribution are similarly related to CVD risk factors in our elderly population. It is apparent that a high central deposition of adipose tissue leads to increased triacylglycerol and to a lesser extent cholesterol levels in older women. The adverse lipid profiles increase the risk of cardiovascular morbidity and mortality [28]. However, TrF/ BW and TrF% were the only measures of fat distribution that correlated significantly to functional capacity, which independently predicts cardiovascular mortality in healthy older individuals [20, 291. Although functional capacity or maximal exercise capacity reflects the amount and intensity of habitual physical activity, it also depends on genetic factors [30]. Both ratios correlated inversely with MET levels, indicating a more central distribution of body fat is related to a lower cardiovascular fitness level. Unlike the WHR and subscapular/triceps skinfold, the DXA-derived ratios were able to detect subtle changes in regional fat distribution resulting from administration of rhGH over a 10 week period. Both the WHR and subscapular/triceps skinfold ratios were unable to detect a change in fat distribution, even though there was a decrease in trunk and limb fat mass over the 24 week study period in the rhGH group. All DXA-derived ratios indicate that rhGH resulted in a preferential loss of central compared with peripheral fat. Rosenbaum et al. 585 [31] also report a preferential reduction in abdominal adipose tissue as determined by adipocyte lipid content subsequent to 3 months administration of exogenous growth hormone (GH) to GH-deficient children, which was similarly not detected by measuring body circumferences and skinfold thicknesses. A decrease in body fat with administration of rhGH has previously been observed in healthy older men [32], young adults [33], and GH-deficient adults [34, 351, reflecting the lipolytic characteristic of GH. Although a preferential reduction in central adipose tissue has been demonstrated in rhGH treated GH-deficient adults [35], the present study is the first to show a similar preferential loss of central adipose tissue in healthy older adults. Other recent studies have also added DXAderived ratios to other imaging techniques and WHR in evaluating body fat distribution. Svendsen et al. [26] used the DXA-derived ratio of abdominal/total fat mass in addition to the WHR in assessing regional changes in fat distribution in a study of diet and exercise in postmenopausal women. Pedersen et al. [36] used the DXA ratio of trunk fat/leg fat and WHR to examine regional fat distribution and insulin resistance in obese women. Williams and colleagues [25] used DXA ratios of trunk-to-total fat and leg fat-to-total fat, as well as the WHR, to examine the association of fat distribution and circulating dehydroepiandrosterone sulphate, and suggest that circumference ratios are less sensitive indexes of fat distribution than DXA measurements. Although DXA is viewed as a direct measure of whole body and regional adiposity, it is subject to limitations [37]. Unlike other imaging techniques, its two-dimensional nature prevents differentiation between intra- and extra-abdominal fat. In addition, it does not directly assess soft tissue anteroposterior to bone (pixels containing soft tissue and bone) but estimates it from soft tissue immediately adjacent to the bone [38]. Nevertheless, it permits an accurate and precise measure of whole body and regional tissue composition, having the ability to detect small changes, with a low radiation exposure [ l l , 391. In addition, indices of fat distribution apart from those examined in this study can also be derived from DXA, depending on the software version employed. Manually selected regions have previously been utilized by Ley et al. [17] in examining sex and menopause-related differences in fat distribution, but provided no advantage over regions derived from default settings. We recognize that major variations in adiposity and body thickness can influence the DXA measurement of both bone mineral and soft tissue [4&44]. In general, these confounding effects occur only when adiposity is excessive or body thickness exceeds 25cm [40, 441. This could potentially lead to errors when used to follow changes in body composition consequent to an intervention inducing significant changes in body weight. In the present 586 D. R. Taaffe et al. study, BMI for all subjects was below 30 kg/m2, and there was no change in body weight for either the rhGH or placebo group during the course of the exercise trial. Therefore, it is unlikely that this problem is an issue for the present analysis. In conclusion, this study suggests that DXAderived ratios from a whole body scan may be more sensitive than conventional anthropometric measurements in the assessment of regional fat distribution changes. These ratios may prove useful in assessing body fat distribution and changes occurring as a result of exercise and/or dietary intervention, especially in populations where anthropometric assessment is difficult such as in the obese, aged, and non-ambulatory individuals, and where subtle changes in tissue composition may be expected. ACKN 0W LEDGMENTS This study was supported by the Research Service of the Department of Veterans Affairs. REFERENCES I. Kissebah AH, Vydelingum N, Murray R, et al. Relation of body fat distribution to metabolic complications of obesity. J Clin Endocrinol Metab 1982; 54: 254-60. 2. Peiris AN, Hennes MI, Evans Dj, Wilson CR, Lee ME. Kissebah AH. Relationship of anthropometric measurements of body fat distribution to metabolic profile in premenopausal women. Acta Med Scand 1988; 723 (Suppl): 179-88. 3. Kaplan NM. The deadly quartet: upper-body obesity, glucose intolerance, hypertriglyceridemia, and hypertension. Arch Intern Med 1989; 149 1514-20. 4. Chumlea WC. Baumgartner RN. Garry PI. Rhyne RL, Nicholson C, Wayne S. Fat distribution and blood lipids in a sample of healthy elderly people. Int J Obesity 1992; 16: 125-33. 5. Lapidus L, Bengtsson C, Larsson B, Pennert K. Rybo E. Sjostrom L. Distribution of adipose tissue and risk of cardiovascular disease and death: a 12 year follow up of participants in the population study of women in Gothenburg, Sweden. Br Med J 1984; 289: 1257-61. 6. Lanson 8. Svardwdd K, Welin L. Wilhelmsen L. Bjorntorp P, Tibblin G. Abdominal adipose tissue distribution, obesity, and risk for cardiovascular disease and death: I3 year follow-up of participants in the study of men born 1913. Br Med 1 1984, 11)8: 1401-4. 7. Folsom AR. Kaye SA. Sellers TA, et al. Body fat distribution and >year risk of death in older women. j Am Med Asroc 1993; 269: 483-7. 8. Egger G. The case for using waist to hip ratio measurements in routine medical checks. Med 1 Aust 1992; 156: 280-5. 9. Weststrate ]A. Deurenberg P. van Tinteren H. Indices of body fat distribution and adiposity in Dutch children from birth to 18 years of age. Int J Obesity 1989; 13: 465-477. 10. Callaway CW, Chumlea WC, Bouchard C, e t al. Circumferences. In: Kohman TG, Roche AF, Martorell R, eds. Anthropometric standardization reference manual. Champaign, IL: Human Kinetics, 1988: 39-54. I I. Fuller NJ. Laskey MA, Elia M. Assessment of the composition of major body regions by duaknergy X-ray absorptiometry (DEXA), with special reference to limb muscle mass. Clin Physiol 1992 II: 253-66. 12. Ashwell M, Cole TJ. Dixon AK. Obesity: new insight into the anthropometric classification of fat distribution shown by computed tomography. Br Med J 1985; 2%. 1692-4. 13. Borkan GA. Hults DE. Gerzof SG, Robbins AH, Silbert CK. Age changes in body composition revealed by computed tomography. J Gerontol 1983; 38: 673-7. 14. van der Kooy K. Leenen R. Seidell IC. Deurenbern P. Droop A, Bakker CIG. Waist-hip ratio is a poor predictor b f changes in ;isceral fa;. Am J Clin Nitr 1993; 5 7 327-33. 15. Gerard EL, Snow RC, Kennedy DN. e t al. Overall body fat and regional fat distribution in young women: quantification with MR imaging. Am J Radio1 1991; 157: 99-104, 16. Dawson-Hughes B, Harris S. Regional changes in body composition by time of year in healthy postmenopausal women. Am J Clin Nutr 1992; 5& 307-13. 17. Ley CJ, Lees B. Stevenson JC. Sex- and menopause-rrxrciated changes in body-fat distribution. Am J Clin Nutr 1992; 55 950-4, 18. Novak LP. Aging, total body potassium, fat-free mass, and cell mass in males and female between ages 18 and 85 years. J Gerontol 1972; 2E 43843. 19. Schwartz RS. Shuman WP. Brandbury VL, et PI. Body fat distribution in healthy young and older men. J Gerontol 1990; 45 M181-5. 20. Kannel WE. Epidemiology of cardiovascular disease in the elderly: an assessment of risk factors. Cardiovasc Clin 1992; 22: 9-22. 21. Wenger NK. Cardiovascular disease in the elderly. Curr Prob Cardiol 1992; IT: &%90. 21. Hanson P. Clinical exercise testing. In: Blair SN, Painter P, Pate RR, Smith LK, Taylor C8, eds. Resource manual for guidelines for exercise testing and prescription. Philadelphia: Lea and Febiger, 1988: 205-22. 23. Guidelines for exercise testing and prescription. 4th ed. American College of Sports Medicine. Philadelphia: Lea and Febiger, 1991. 24. Shimokata H, Tobin ID, Muller DC, et al. Studies in the distribution of body I. Effects of age, sex, and obesity. J Gerontol 1989 44: M66-73. Iliams DP, Boyden TW, Pamenter RW. Lohman TG, Going SB. Relationship of body fat percentage and fat distribution with dehydroepiandrorterone sulfate in premenopausal women. J Clin Endocrinol Metab 1993; 77.W-5. 26. Svendsen OL. Hassager C, Christiansen C. Effect of an energy-restrictive diet, with or without exercise, on lean tissue mass, resting metabolic rate, cardiovascular risk factors, and bone in overweight postmenopausal women. Am J Med 1993; 95 1 3 1 4 . 27. Zamboni M, Armellini F, Turcato E, et al. Effect of weight loss on regional body fat distribution in premenopausal women. Am J Clin Nutr 1993; 58: 29-34. 28. Simons LA. Triglyceride levels and the risk of coronary heart disease: a view from Australia. Am J Cardiol 1992; 70: 14H-18H. 29. Sandvik L, Erikssen J, Thaulow E. Eriksren G, Mundal R, Rodahl K. Physical fitness as a predictor of mortality among healthy, middle-aged Norwegian men. N Engl j Med 1993; 328: 533-7. 30. Bouchard C. Lesage R, Lortie G. et al. Aerobic performance in brothers, dizygotic and monozygotic twins. Med Sci Sports Exerc 1986, 18: 639-46. 31. Rosenbaum M. Gertner JM, Leibel R. Effects of systemic growth hormone (GH) administration on regional adipose tissue distribution and metabolism in GHdeficient children. j Clin Endocrinol Metab 1989; 68: 1274-81. 32. Rudman D, Deller AG, Nagraj HS. et al. Effects of human growth hormone in men over 60 years old. N Engl J Med 1990; 3U: 1-6. 33. Crist DM, Peake GT. Egan PA, Waters DL. Body composition response to exogenous GH during training in highly conditioned athletes. J Appl Physiol 1988; 6 5 579-04. 34. J9rgensen JOL, Pedenen SA, Thuesen L, et al. Beneficial effects of growth hormone treatment in GHdeficient adults. Lancet 1989 i: 1221-5. 35. Salomon F. Cueno RC, Hesp R. Sonksen PH. The effects of treatment with recombinant human growth hormone on body composition and metabolism in adults with growth hormone deficiency. N Engl J Med 1989; 321: 1797403. 36. Pedersen SB, Wrglum JD, Schmitz 0.Bak IF, S9rensen NS, Richelsen B. Abdomonal obesity is associated with insulin resistance and reduced glycogen synthase activity in skeletal muscle. Metab Clin Exp 1993; 42: 998-1005. 37. Roubenoff R. Kehayias JJ, Dawson-Hughes B. Heymsfield SB. Use of duaknergy X-ray absorptiometry in body composition studies: not yet a 'gold standard'. Am 1 Clin Nutr 1993; 58. 589-91. 38. Svendson OL. Hassager C, Bergmann I, Christiansen C. Measurement of abdominal and intra-abdominal fat in postmenopausal women by dual energy X-ray absorptiometry and anthropometry: comparison with computerized tomography. Int J Obesity 1993; 17: 45-51. 39. Going SB. Massett MP. Hall MC, Bare LA, Root PA, Williams DP. Lohman TG. Detection of small changes in body composition by dual-energy X-ray absorptiometry. Am J Clin Nutr 1993; 57 845-50. 40. Wahner HW. Dunn WL, Brown ML. Morin RL, Riggs EL. Comparison of dual-energy X-ray absorptiometry and dual photon absorptiometry for bone mineral measurements of the lumbar spine. Mayo Clin Proc 1988; 0: 107544. 41. Hangartner TN, Johnston CC. Influence of fat on bone measurements with dual-energy absorptiometry. Bone Miner 1990; 9 71-81. 42. Haarbo J, Godredsen A, Hassager C, Christiansen C. Validation of body Composition by dual energy X-ray absorptiometry (DEXA). Clin Physiol 1991; II: 33141. 43. laskey MA, Lyttle KD, Flaxman ME, Barber RW. The influence of tissue depth and composition on the performance of the Lunar duaknergy X-ray absorptiometer wholebody scanning mode. Eur J Clin Nutr 1992; 46: 39-45. 44. )ebb SA, Goldberg GR. Elia M. DXA measurements of fat and bone mineral density in relation to depth and adiposity. In: Ellis KJ, Eastman ID. eds. Human body composition, New York: Plenum Press, 1993: 115-19.
© Copyright 2026 Paperzz