Regional Subcutaneous-Fat Loss Induced by Caloric Restriction in Obese Women

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Regional Subcutaneous-Fat Loss Induced by Caloric Restriction in Obese Women Jack Wang, Blandine Laferre `re, John C. Thornton, Richard N. Pierson, Jr., and F. Xavier Pi-Sunyer Abstract WANG, JACK, BLANDINE LAFERRE ` RE, 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;10:885– 890. 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 0.0001), 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 0.0001). 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 pro- portionally more in peripheral than in central regions. 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). There- fore, 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 re- cently 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 regional- fat 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 circum- ferences, 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 mea- sured (5). In a longitudinal body-composition study, a detailed body-composition evaluation, including anthropo- metrics, was performed before and after a 6-month nonin- tervention 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. Received for review July 23, 2001. Accepted for publication in final form May 17, 2002. 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 10025. E-mail: [email protected] Copyright © 2002 NAASO OBESITY RESEARCH Vol. 10 No. 9 September 2002 885

Transcript of Regional Subcutaneous-Fat Loss Induced by Caloric Restriction in Obese Women

Regional Subcutaneous-Fat Loss Induced byCaloric Restriction in Obese WomenJack Wang, Blandine Laferrere, John C. Thornton, Richard N. Pierson, Jr., and F. Xavier Pi-Sunyer

AbstractWANG, JACK, BLANDINE LAFERRERE, JOHN C.THORNTON, RICHARD N. PIERSON, JR., and F.XAVIER PI-SUNYER. Regional subcutaneous-fat lossinduced by caloric restriction in obese women. Obes Res.2002;10:885–890.Objective: With anthropometric models using skinfolds andcircumferences, we studied changes in the percentage ofsubcutaneous fat in the total cross-sectional area (SF%) atfour body sites in obese women, before and after weight lossinduced 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/m2], we measured SF% atthe midpoint of the upper arm and thigh and the waistlineand hipline, and we measured the percentage of total bodyfat by DXA before (Obs#1) and after (Obs#2) a 6-monthnonintervention control period and then after 6 months on a1200 kcal/d diet (Obs#3).Results: The mean body weight and BMI increased (1.8 kgand 0.61 kg/m2; p � 0.0001), but there were no significantchanges in any other body composition measurements fromObs#1 to Obs#2. The means of Obs#3 for weight and BMIdecreased by 11%, and the percentage of total body fatdecreased by 13% of Obs#2 mean values (p � 0.0001). Themean SF% at each site decreased 7.6% to 18.0% of theObs#2 mean values (p � 0.001). The SF% decreases weregreater at mid-arm and mid-thigh than in the cross-sectionalregions at the waistline and hipline (p � 0.05). There wasno interaction between age or ethnicity (p � 0.2).Conclusions: In obese women, caloric restriction alonereduces anthropometrically measured subcutaneous fat pro-portionally more in peripheral than in central regions.

Key words: obesity, caloric restriction, anthropometrics,subcutaneous fat

IntroductionMany studies have reported associations of central

obesity with hypertension, diabetes, and heart disease(1,2). These associations were independent of the degreeof obesity, but dependent on fat distribution (2). There-fore, it is important to better understand the impact ofcaloric restriction not only on total body-fat loss, but alsoon fat distribution.

Most previous studies have assessed the impact of caloricrestriction on weight and total body fat as the primaryoutcomes. Cordero-MacIntyre et al. (3), however, have re-cently studied the effect of a 1200-kcal diet on skinfoldthickness and regional body composition measured by DXAin postmenopausal women. However, these two techniquesmeasure different aspects of subcutaneous-fat distribution.Lovejoy et al. (4) made comparisons of measured regional-fat distribution by DXA between African-American andwhite women. To our knowledge, there are no studiescomparing changes in subcutaneous-fat amount at differentregions during caloric restriction in both African-Americanand white obese women. Thus, how subcutaneous-fatamounts change in different body regions during weightloss by caloric restriction remains unknown. Lack of easilyapplicable techniques for measuring such changes in obesityis probably the main reason.

We have shown previously, using skinfolds and circum-ferences, that subcutaneous-fat area can be calculated as apercentage of a cross-sectional area for the body locationwhere the circumference and skinfold thickness are mea-sured (5). In a longitudinal body-composition study, adetailed body-composition evaluation, including anthropo-metrics, was performed before and after a 6-month nonin-tervention control period and then after 6 months on 1200kcal/d diet in obese African-American and white women.With this database, we tested the hypothesis that caloricrestriction reduces subcutaneous fat proportionally more incentral regions than in peripheral regions in obese women.

Received for review July 23, 2001.Accepted for publication in final form May 17, 2002.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-RooseveltHospital, 1111 Amsterdam Avenue, New York, NY 10025.E-mail: [email protected] © 2002 NAASO

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Subjects and MethodsData 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 massindex (BMI) �28 kg/m2, but not weighing �250 lbs (due tothe ability of the DXA scan system); and not on medicationaffecting bone homeostasis (oral contraceptives, hormonereplacement therapy, calcitonin, fluoride, steroids or diuret-ics). 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 dietof 1200 kcal/d (Obs#3) with a full or partial formula dietwith weekly visits to our outpatient weight-loss center. Theformula contains 24% protein, 10% fat, and 66% carbohy-drates. The women were instructed not to change their levelof 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-bodyDXA scan using Lunar model DPX-L (Madison, WI), witha precision of � 1.2%. The anthropometric measurementsare four body circumferences measured with the Dritz sew-ing tape (mid-arm, mid-thigh, waist, and hip), with anaverage precision of � 1 cm, and five skinfold thicknessesusing Lange calipers (triceps and biceps, mid-thigh, umbi-licus, and abdomen (5 cm below the umbilicus), having anaverage precision of � 2.5 mm. All measurements wereperformed while the subject wore a hospital gown withminimum 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 ofmid-arm and mid-thigh, and at the locations for waist- andhip-circumference measurement were calculated using themodels described previously (5), as shown below:

● The mid-arm subcutaneous-fat area (ASFmm2) � �D2/

4 � �d2/4, where D is the diameter of the whole cross-section (D � mid-arm circumference/�), d is the diameterof the lean area (d � D � (triceps � biceps)/2), andASF mm

2 is the subcutaneous-fat area and the percentageof subcutaneous-fat in the total cross-section (ASF%) �{ASF mm

2/(�D2/4)} � 100%.● The subcutaneous-fat area for the mid-thigh was calcu-

lated using skinfold thickness, and the circumferencewas measured at the mid-thigh (TSFmm

2). For the waist(WSFmm

2), subcutaneous-fat area was calculated usingumbilicus skinfold thickness and waist circumference; forthe hip (HSFmm

2), it was calculated using abdomen skin-fold thickness (5 cm below the umbilicus) and hip cir-cumference. The percentage of subcutaneous-fat area in thecross-sectional area for each site was calculated as (subcu-taneous-fat area/total cross-sectional area) � 100%.

Means and SDs were calculated for each measured vari-able at each observation. The paired Student’s t test wasused to test the hypothesis that the mean change in mea-sured value between observations was equal to zero. Re-peated-measures ANOVA was used to test the hypothesisthat the mean values of the percentage reductions at the foursites were equal. Fisher’s least significant difference proce-dure was used to perform multiple comparisons among themeans. The Student’s t test was used to test the hypothesisthat the mean percentage reduction were equal for African-American and white women. Correlations between age andthe study variables were calculated. All comparisons weremade within subjects. Therefore, age was controlled for allstatistical analyses. The level of significance for all statis-tical tests of hypothesis was p � 0.05. All statistical calcu-lations were performed using the SAS statistical softwarepackage (Computer Resource Center, Santa Monica, CA).Because our goal was to study the changes in fat distributionbefore and after a 6-month diet for weight loss, we onlymade the comparisons between Obs#2 and Obs#3 for all ofthe anthropometric measurements in this report.

ResultsThe means of body weight and BMI at the end of the

6-month nonintervention period (Obs#2) were 1.8 kg and0.6 kg/m2 higher than the means at Obs#1, respectively(p � 0.0001). Because the purpose of the study was toinvestigate the effect of dieting on fat distribution, resultsmeasured immediately before the hypocaloric-diet period(Obs#2) were used as baseline values for comparisons be-fore and after interventions. Table 1 shows the means andSDs of age, weight, height, BMI, and the percentage of totalbody fat before (Obs#2) and after the 6-month caloricrestriction (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 � 0.0001).

Figure 1 shows that the 6-month caloric restriction re-duced circumferences at the four sites significantly (p �0.0001). The reduction as a percentage of the baseline(Obs#2) ranged from 6.1% for the mid-thigh to 7.8% for thewaist. The reduction percentages were similar at the four sites.

Figure 2 shows that skinfold thickness was significantlyreduced at the five sites after the 6-month diet period (p �0.0001). The reductions as percentages of the baseline(Obs#2) ranged from 14.9% for the umbilicus to 24% forthe biceps. Although there were no statistically significantdifferences among the study sites for the percentage ofreduction, the magnitude of the reductions in mid-arm andmid-thigh were more than in the trunk regions.

Figure 3 shows that subcutaneous-fat areas were signifi-cantly 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

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7.6% and 11.8% at the cross-section where waist and hipcircumferences were measured, respectively. There werestatistically significantly differences among the mean per-centage reductions (p � 0.001, ANOVA). The reductionsin the mid-arm were significantly larger than waist andhip regions. The reductions in the mid-thigh were signifi-cantly larger than in the abdominal region, but not than thehip region.

There were no significant correlations between age andSF% reduction in either ethnic group. Race had no signifi-cant influence in any of the statistical outcomes (p � 0.2).

Table 2 shows the changes in DXA-measured fat mass inthe arm, leg, and trunk regions. All the changes werestatistically significant (p � 0.0001). Although there wereno significant differences among the regions for the per-centage of reduction in fat mass from baseline, the magni-tude of the reduction in each region was similar to theresults estimated by the anthropometric models.

DiscussionAfter the 6-month caloric restriction, these obese women

lost an average of 11% of their baseline weight measured atthe completion of a 6-month nonintervention period. Thedata indicates that the decreases in skinfold thickness werehigher than the decreases in circumferences for each mea-sured body region. It also indicates that the magnitude ofdecreases in skinfold thickness in the peripheral regionswere larger than the trunk regions.

This is one of the first reports using anthropometricmeasurements and models showing that moderate caloricrestriction proportionally reduces subcutaneous fat in theperipheral regions more than in the central region in obeseAfrican-American and white women. These results suggestthat whereas moderate caloric restriction reduces total bodyfat and central-fat mass, both of which are associated withrisk factor improvements, it does not lower the ratio of

Table 1. Weight, height, body mass index (BMI) and DXA-measured percentage of total body fat of the 61studied subjects before and after a 6-month caloric-restriction diet (mean � SD)

Time Age (years) Weight (kg) Height (cm) BMI (kg/m2)Percentage of total

body fat

Before 45.7 � 10.9 96 � 11 163 � 7 36 � 4 46 � 4After 46.3 � 11.1 85 � 11 163 � 7 32 � 4 40 � 6Changes �11 � 7 0 �4 � 3 �6 � 4Changes as percentage of prediet values �11% 0 �11% �13%

p � 0.0001 for all changes.

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 � 0.0001). Thechanges (after � before) as the percentage of pre-caloric restric-tion values were not significantly different among sites (leastsignificant difference � 2.3%).

Figure 2: Means of skinfold thicknesses in millimeters measuredbefore (solid bars) and after (open bars) a 6-month caloric-restric-tion diet; all changes were statistically significant (p � 0.0001).The changes (after � before) as the percentage of pre-caloricrestriction values varied by sites: changes in the mid-arm andmid-thigh sites were larger than changes in the waist and hipregions (least-significant difference � 10%).

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central-to-peripheral subcutaneous fatness. For example,our results show that the ratio of waist-to-hip circumferenceand the ratio of central-to-peripheral subcutaneous-fat areaat baseline were almost identical to that measured after the6-month diet restriction (ratio of waist-to-hip circumfer-ences: 0.820 � 0.0.12 at baseline vs. 0.819 � 0.12 after the6-month diet restrictions; ratio of central to peripheral re-gion subcutaneous-fat areas: 2.47 � 0.51 at baseline vs.2.58 � 0.43 after the 6-month diet restriction). This ob-served effect of caloric restriction on fat-distribution patternwas not influenced by either age or ethnicity. Recently,Cordero-MacIntyre et al. (3) reported that using a 3-monthcaloric-restriction diet in 49 postmenopausal white obesewomen resulted in significant reductions in arm and legskinfolds, but no changes in abdominal skinfolds; theseresults are different from our findings.

The prevalence of obesity in the United States has in-creased steadily over the past 20 years. Many studies havereported correlations between health risk and central adi-posity. Reduction of body fatness, especially in the centralregion, has been increasingly considered a primary factorfor reducing these health risks. Most of the epidemiologicaldata strongly suggest that caloric intake is a major contrib-utor to obesity (6). As a result, numerous investigators haverestricted dietary intake as a treatment for obesity. Pi-Sunyer has warned the public that extreme caloric restric-tion may be harmful, and individuals should not take suchan approach without direct physician supervision (7).George et al. reported that dietary-fat content has a positiverelationship 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 ad-iposity in middle-aged men (9). Golay et al. reported thatweight loss was similar in obese subjects either on a low- orhigh-carbohydrate diet (10). The main purpose of this re-search project, which generated the database presented inthis report, was to study the effects of a 6-month moder-ate calorie restricted balanced diet inducing 10% weightloss on bone density in obese women (11). Neither thediet composition nor the level of caloric restriction was apart of the study.

Murakami et al. performed a study of subcutaneous-fatdistribution and body size among Japanese women in theirearly 20s and again 5 years later by measuring skinfoldthickness at 14 points on the body (12). They found signif-icant increases in subcutaneous fat at the lower trunk, suchas the waist and intragluteal regions. They concluded thatdecreased physical activity with age as observed by ques-tionnaires might have contributed to such changes. In ourstudy, participants were asked not to change their physical-activity pattern throughout the study period. Therefore, theobserved weight loss and changes in fat and fat distributionwere purely diet-induced.

Tracking changes in fat distribution in a longitudinalstudy requires accurate and precise assessment methods.Although CT and magnetic resonance imaging (MRI) are

Figure 3: Means of subcutaneous fat area as the percentage ofcross-sectional areas measured before (solid bars) and after (openbars) 6-month caloric restriction. All changes were statisticallysignificant (p � 0.001). The changes (after � before) as thepercentage of pre-caloric restriction values varied by sites: changesin the mid-arm region were larger than changes in waist and hipsites, and changes in mid-thigh region were larger than waist(least-significant difference � 10%).

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 5.6 � 1.8 16.0 � 3.3 20.0 � 3.9After 4.2 � 1.4 12.8 � 3.3 15.7 � 4.3Changes �1.4 � 1.8 �3.2 � 2.2 �4.3 � 3.0Changes as percentage of prediet values �25% �21%0 �21%

p � 0.0001 for all changes.

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well-accepted techniques in subjects with weights in thenormal range (13,14), they are not widely available and areexpensive. Because �50% of total body fat is located in thesubcutaneous regions, skinfold thickness has been consid-ered a practical and simple approach for assessing subcuta-neous fat (15). Models using tricep skinfold and circumfer-ence, measured at the mid-arm to predict cross-sectionalskeletal muscle area at mid-arm, have been used for morethan two decades (16). Previous studies using skinfolds andcircumferences have shown reliabilities for estimating bodycomposition that are higher than those using bio-impedance(17,18). Recent studies have further demonstrated that an-thropometric measurements are reliable estimators of CT-or MRI-measured body-fat distribution and skeletal muscleand body-fat distributions (13,14).

Estimation of subcutaneous-fat area from anthropometryis based on many assumptions. But this is also true for othertraditional, as well as new methods, for measurement ofbody composition. For example, DXA is considered a reli-able method for determining total and regional adiposity.However, it is important to mention a well-known technicallimitation about the DXA technique: DXA-determined ad-iposity does not include fat existing in any scan regionscontaining bone. Because ribs occupy a large portion of thetruncal region, DXA may not provide reliable fat measure-ment for the entire truncal region.

One of the objectives of this study was to estimatechanges in the amount of subcutaneous fat using widelyavailable, easy, and inexpensive anthropometric measure-ments during weight loss. In a recently completed study tovalidate these anthropometric models with MRI in 23adults, we found that the MRI measured subcutaneous-fatareas were highly correlated with the values estimated withanthropometric models at each region; with r2 ranging 0.78for the trunk region to 0.92 for the mid-thigh (19).

Our models measure subcutaneous-fat area at cross-sec-tional sites, which reflects subcutaneous-fat distribution moreaccurately than measurements of skinfold thickness or circum-ference alone. However, the lack of precision of this inexpen-sive and widely available field technique has been a majorconcern to many investigators. Even using the same caliper,but with different jaw pressure, may give different skinfoldresults (20). Standardization of measurement instrumentationand protocols and well-trained observers can greatly reduceinter- and intra-observer errors (21). In our laboratory, anthro-pometric measurements have been performed routinely formore than three decades using the same type of caliper (LangeCaliper) and measuring tape (Dritz) and the same measurementprotocols. We require that any observer must have a measuringprecision �2% for circumferences and �10% for skinfolds(20); they must also show no significant differences from theobserver who has performed more than one third of the 5,000subject measurements and conducted the training during thepast 25 years.

In summary, this study demonstrates that anthropometricmeasurements are an easily applicable technique for study-ing changes in regional subcutaneous-fat distribution inobese women. Caloric restriction alone proportionallyreduces subcutaneous fat more in peripheral than in cen-tral regions in obese women. This study suggests that ca-loric restriction alone reduces the degree of obesity, butdoes not improve the ratio of central-to-peripheral subcuta-neous-fat distribution in either African-American or whiteobese women.

AcknowledgmentsSupported by National Institute of Diabetes and Digestive

and Kidney Diseases Grant 42618.

References1. Freedman DS, Serdula MK, Srinivasan SR, Berenson GS.

Relation of circumferences and skinfold thicknesses to lipidand insulin concentrations in children and adolescents: theBogalusa Heart Study. Am J Clin Nutr. 1999;69:308–17.

2. Gillum RF, Mussolino ME, Madans JH. Body fat distribu-tion and hypertension incidence in women and men. TheNHANES I Epidemiologic Follow-up Study. Int J Obes RelatMetab Disord. 1998;22:127–34.

3. Cordero-MacIntyre ZR, Peters W, Libanatl CR, Espana RC,Howell WH, Lohman TG. Effect of a weight-reduction pro-gram on total body and regional body composition in obesepostmenopausal women. Ann N Y Acad Sci. 2000;904:526–35.

4. Lovejoy JC, Smith SR, Rood JC. Comparison of regional fatdistribution and health risk factors in middle-aged white andAfrican American women: The Healthy Transitions Study.Obes Res. 2001;9:10–16.

5. Wang J, Thornton JC, Russell M, Burastero S, HeymsfieldB, Pierson RN Jr. Asians have lower body mass index (BMI)but higher percent body fat than do whites: comparisons ofanthropometric measurements. Am J Clin Nutr. 1994;60:23–8.

6. Harnack LJ, Jeffrey RW, Boutelle KN. Temporal trendsand energy intake in the United States: an ecologic perspec-tive. Am J Clin Nutr. 2000;71:1478–84.

7. 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, BouchardC. Effect of dietary fat content on total and regional adiposityin men and women. Int J Obesity. 1990;14:1085–94.

9. Dreon DM, Frey-Hewitt B, Ellsworth N, Williams P, TerryRB, Wood PD. Dietary fat:carbohydrate ratio and obesity inmiddle-aged men. Am J Clin Nutr. 1988;47:995–1000.

10. Golay A, Allaz AF, Morel Y, de Tonnac N, Tankova S,Reaven G. Similar weight loss with low- or high-carbohy-drate diets. Am J Clin Nutr. 1996;63:174–8.

11. Laferrere B, Funkhouser A, Thornton JC, Pi-Sunyer FX.Total body calcium in obese women: validation of dual-energyx-ray absorptiometry against in vivo neutron activation anal-ysis. Ann N Y Acad Sci. 2000;904:507–13.

12. Murakami M, Hikima R, Arai S, Yamazaki K, Iizuka S,Tochihara Y. Short-term longitudinal changes in subcutane-

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OBESITY RESEARCH Vol. 10 No. 9 September 2002 889

ous fat distribution and body size among Japanese women inthe third decade of life. App Hum Sci. 1999;18:1–9.

13. Goran MI, Gower BA, Treuth M, Nagy TR. Prediction ofintra-abdominal and subcutaneous abdominal adipose tissue inhealthy pre-pubertal children. Int J Obes. 1998;22:549–58.

14. Rolland-Cachera MF, Brambilla P, Manzoni P, Akrout M,Sironi S, Del Maschio A, Chiumello G. Body compositionassessed on the basis of arm circumference and triceps skin-fold thickness: a new index validated in children by magneticresonance imaging. Am J Clin Nutr. 1997;65:1709–13.

15. Lohman TG, Roche, AF, Martorell R, eds. AnthropometricStandardization Reference Manual. Champaign, IL: HumanKinetics; 1988 pp. 8–80.

16. Frisancho AR. New norms of upper limb fat and muscle areafor assessment of nutritional status. Am J Clin Nutr. 1981;34:2540–2545.

17. Gualdi-Russo E, Toselli S, Squintani L. Remarks on meth-ods for estimating body composition parameters: reliability of

skinfold and multiple frequency bioelectric impedance meth-ods. Z Morphol Anthropol. 1997;81:321–31.

18. Wattanapenpaiboon N, Lukito W, Strauss BJ, Hsu-HageBH, Wahlqvist ML, Stroud DB. Agreement of skinfoldmeasurement and bioelectrical impedance analysis (BIA)methods with dual energy X-ray absorptiometry (DEXA) inestimating total body fat in Anglo-Celtic Australians. Int JObes Relat Metab Disord. 1998;22:854–60.

19. He Q, Wang J, Engelson ES, Kotler DP. Ability of ananthropometric model to track changes in subcutaneous adi-pose tissue area [Abstract]. FASEB J. 2002;16:A1024.

20. Gore CJ, Carlyon RG, Franks SW, Woolford SM. Skin-fold thickness varies directly with spring coefficient andinversely with jaw pressure. Med Sci Sports Exerc. 2000;32:540 – 6.

21. Wang J, Thornton JC, Kolesnik S, Pierson RN, Jr. An-thropometry in body composition: an overview. Ann N Y AcadSci. 2000;904:317–26.

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