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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:1741-1745, July 2004


Human Nutrition and Metabolism

Very Low-Fat (12%) and High Monounsaturated Fat (35%) Diets Do Not Differentially Affect Abdominal Fat Loss in Overweight, Nondiabetic Women1

Peter M. Clifton2, Manny Noakes and Jennifer B. Keogh

CSIRO Health Sciences and Nutrition, Adelaide BC, South Australia 5000

2To whom correspondence should be addressed. E-mail: peter.clifton{at}hsn.csiro.au.


    ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Studies in women with type 2 diabetes demonstrated adverse effects on body fat distribution of a low-fat diet relative to a high monounsaturated fat diet. We performed a randomized 12-wk parallel design study of two 6000-kJ diets: 35% energy from fat (high monounsaturated fat diet, HIMO), or 12% energy from fat (very low-fat diet, VLF) to determine whether this also occurred in nondiabetic women. Body fat distribution, fasting plasma glucose, blood pressure, and fasting serum lipids were measured at wk 0 and 12 in 62 women (BMI > 27 kg/m2). Weight loss (9.5 ± 2.4 vs. 9.4 ± 3.4 kg, VLF vs. HIMO) and total fat loss (6.1 ± 2.4 vs. 6.3 ± 2.7 kg, VLF vs. HIMO) did not differ in the groups. There was a diet x menopausal status interaction in lean mass changes (P = 0.005) such that in premenopausal women, HIMO produced a lower loss of lean mass than the low-fat diet (0.4 ± 2.3 vs. 2.9 ± 2.7 kg, P = 0.006) with the opposite but nonsignificant effect seen in postmenopausal women. There was a greater decrease in total plasma cholesterol in women who consumed VLF compared with those who consumed HIMO (0.82 ± 0.0.51 vs. 0.50 ± 0.48 mmol/L, P < 0.001 for time, P < 0.05 for diet effect). This was also true for the change in HDL cholesterol (0.18 ± 0.23 vs. 0.04 ± 0.19 mmol/L, VLF and HIMO, respectively, P < 0.001 for time, P < 0.05 for diet effect). The LDL/HDL ratio was reduced in both groups with no effect of diet (0.16 ± 0.51 vs. 0.16 ± 0.45, VLF and HIMO, respectively, P < 0.05). In conclusion, weight, total fat mass, and regional fat mass loss did not differ in the 2 groups of women but there was an apparent preservation of lean mass in premenopausal women consuming HIMO.


KEY WORDS: • fat mass • lean mass • monounsaturated fat • weight loss

Obesity is a risk factor for cardiovascular disease but in women, abdominal obesity, defined by a large waist circumference (≥76.2 cm) or high waist to hip ratio (≥0.76) is a stronger risk factor for heart disease (1), stroke (2), and type 2 diabetes (3) than BMI. In cross-sectional surveys, type 2 diabetes is strongly associated with a high waist to hip ratio (4). Recently Snijder et al. (5) reported that large hip and thigh circumferences were associated with a lower risk of type 2 diabetes, whereas a larger waist circumference was associated with a higher risk.

Dietary macronutrient composition can potentiate the improvement in cardiovascular risk factors achieved with weight loss. We showed that a high monounsaturated fat weight loss diet resulted in comparable or greater improvements in cardiovascular risk factors compared with a very low-fat diet in overweight and obese men and women, with and without diabetes (6,7).

Dietary macronutrient composition may also influence body composition. In 2 studies by Walker et al. (8,9), one in energy balance and one that was energy restricted, subjects with type 2 diabetes experienced an adverse effect on the ratio of upper body to lower body fat after consumption of a high-carbohydrate/low-fat diet compared with a high monounsaturated fat diet, which produced no change in this ratio. Piers et al. (10) observed apparent weight and fat loss when monounsaturated fat was substituted for saturated fat in nondiabetic men. These findings have not been confirmed elsewhere; if they are true, they may have important implications for the prevention of cardiovascular disease by the use of a diet enriched in monounsaturated fats. The aim of the current study, therefore, was to establish whether the changes observed by Walker et al. (8,9) could be reproduced in a weight loss study in nondiabetic women in which significant losses in total fat mass were achieved.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Subjects. Women (n = 70) with BMI > 27 kg/m2 without diabetes (fasting glucose < 7.0 mmol/L) were selected after recruitment by public advertisement. Subjects were matched for BMI and self-reported menopausal status but not for abdominal fat or waist/hip ratios. Subjects who had liver or renal disease, who were taking medication likely to affect lipid metabolism, or who consumed >40 g ethanol/d were excluded. Approval was obtained from the Commonwealth Scientific and Industrial Research Organization Human Ethics Committee and informed, written consent was obtained from the volunteers.

    Study design and dietary methodology. The women were matched by BMI and age, blocked into 2 groups and randomly assigned to consume a 6000-kJ diet either high in monounsaturated fat diet (HIMO)3 with 35% energy from fat, 20% energy from monounsaturated fat, and 6% energy from saturated fat or a very low-fat diet (VLF) with 12% energy from fat, 4% energy as monounsaturated fat, and 4% energy from saturated fat for 12 wk. Protein intake provided 21% of energy. A prescriptive diet plan (Table 1) and daily menu were provided. Key foods low in total fat or high in monounsaturated fat were supplied to the respective groups to promote compliance (Table 1). In addition, all subjects received breakfast cereals and bread. The key dietary differences were achieved by providing those consuming VLF with low-fat biscuits, raisins, and a canola oil spray for cooking, and those consuming HIMO with biscuits made with canola oil, potato crisps cooked in high-oleic sunflower oil, and canola oil for cooking. Subjects were interviewed by a dietitian every 2 wk and kept 3-d food records that were calculated using Diet 1 Nutrient Calculation software (Xyris Software). The need to keep exercise levels to pretrial levels was emphasized.


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TABLE 1 Prescribed diets and foods supplied to subjects

 
Blood samples were taken from fasting subjects on 2 consecutive days at wk 0, 4, 8, and 12, and means were calculated. Weight was measured on these occasions as were systolic (SBP) and diastolic blood pressure (DBP), plasma glucose, serum total cholesterol (TC), triglycerides (TG), HDL cholesterol (HDL-C), and LDL cholesterol (LDL-C) (calculated). Blood pressure (Critikon Dinamap, Vital signs monitor 8100, GE Medical Systems) was measured 3 times after subjects had rested quietly for 5 min and the results averaged.

    Laboratory methods. Venous blood samples (20 mL) were taken after an overnight fast of ≥12 h, into tubes containing either Na2EDTA (1 g/L final concentration) as anticoagulant for lipid measurements or sodium fluoride/EDTA for glucose. Plasma was separated by low-speed centrifugation at 600 x g for 10 min at 5°C (Beckman GS-6R) and frozen at –20°C. At the end of the study, all samples from each subject were analyzed within the same analytical run. Serum TC, TG, and plasma glucose concentrations were measured on a Cobas-Bio centrifugal analyzer (Roche Diagnostica) using enzymatic kits (Hoffmann-La Roche Diagnostica; catalog numbers 2016630, 2016648 and 1447513,respectively) and control sera. Plasma HDL-C concentrations were measured using an HDL direct kit (Roche Diagnostic Systems; catalog number 2016630). Insulin was measured by RIA using kits (Phadeseph Insulin RIA, Pharmacia & Upjohn, catalog number 10–9169-01). The following modification of the Friedewald equation (11) for molar concentrations was used to calculate LDL-C in mmol/L: TC – TG/2.18 – HDL-C.

    Height and weight. Stature was measured to the nearest 0.1 cm using a stadiometer (SECA) with subjects barefoot in the free-standing position. Body weight was measured with subjects wearing light clothing with no shoes to the nearest 0.05 kg, using calibrated electronic digital scales (Mercury, AMZ 14).

    Body composition and fat distribution. For assessment of body fat distribution, all subjects underwent a dual energy X-ray absorptiometry scan (DEXA) (Norland XR36, Norland Corporation) at wk 0 and 12. Subjects were required to fast for the 15-min test and received only a very low dose of radiation (3–5 µSv). The CV was 2.3 ± 0.9% for total fat mass and 2.1 ± 0.4% for total lean mass. Fat and lean tissue were measured in specific regions (Fig. 1). Abdominal fat was defined as midriff fat plus pelvic fat. Trunk or upper body fat was defined as the combination of fat in the chest, midriff, and pelvic regions. The results were used to assess total, regional, and percentage lean and fat mass before and after weight loss.



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FIGURE 1 Regional fat distribution measured by DEXA.

 
    Waist and hip circumference. Waist and hip measurements were also taken before and after dietary intervention. Waist circumference was measured directly on the skin as the smallest dimension between the lower rib margin and the iliac crest. The hip circumference was taken at the maximum extension of the buttocks.

    Statistical analysis. Data are expressed as means ± SD unless otherwise stated. Repeated-measures ANOVA was performed taking time as the within-subject factor and diet as the between-subject factor. If the diet x time interaction was significant, a comparison of diets at each time point was carried out. The data were also analyzed to detect end-point changes by diet and menopausal status using a 2-way ANOVA with weight change as a covariate. Analyses were performed with SPSS 8.0 for Windows statistical software. Differences were considered significant at P < 0.05.


    RESULTS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Eight subjects (4 from each dietary intervention) withdrew because of inability to maintain compliance or because of work or travel commitments. The characteristics of the 2 groups at baseline (Table 2) did not differ with respect to age, BMI, SBP and DBP, or waist to hip ratio. Twenty-four women were postmenopausal. The number of postmenopausal women was also similar in each group.


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TABLE 2 Baseline characteristics of subjects1

 
Dietary intake was calculated from 18 d of food records (Table 3). Total fat, carbohydrate, saturated fat, monounsaturated fat, and polyunsaturated fat intakes differed between the groups (P < 0.01). Energy intake did not differ.


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TABLE 3 Macronutrient and fatty acid intakes by nondiabetic overweight women consuming a diet high in monounsaturated fat (HIMO) or a very low-fat (VLF) diet1, 2

 
Weight loss did not differ between the groups (9.5 ± 2.4 vs. 9.4 ± 3.4 kg) nor did total fat loss (6.1 ± 2.4 kg vs. 6.3 ± 2.7 kg) VLF vs. HIMO, respectively. Total fat mass fell 14% in both groups, from 42.3 ± 11.2 to 36.2 ± 10.2 kg in subjects consuming VLF, and from 44.1 ± 8.5 to 37.9 ± 8.0 kg in those consuming HIMO (P < 0.01 for time with no effect of diet). The trunk fat:leg fat ratio also fell from 1.57 ± 0.23 to 1.54 ± 0.22 in the VLF group, and from 1.60 ± 0.34 to 1.57 ± 0.31 in the HIMO group (P < 0.01 for time, with no effect of diet).

Abdominal fat was reduced 18% from 9.9 ± 2.4 to 8.1 ± 2.2 in the VLF group, and 17% from 10.4 ± 2.2 to 8.7 ± 2.2 in the HIMO group (P < 0.01 for time with no effect of diet). Lean mass also fell 5% from 46.8 ± 5.0 to 44.6 ± 4.9 in the VLF group and 3% from 45.3 ± 5.7 to 44.0 ± 5.7 in the HIMO group (P < 0.01 for time with no effect of diet).

Waist circumference decreased with no effect of diet from 101.2 ± 9.0 to 94.5 ± 9.0 in the VLF group and from 102.1 ± 9.2 to 95.4 ± 8.5 in the HIMO group (P < 0.001 for time). The waist:hip ratio did not change (0.85 ± 0.05 to 0.84 ± 0.4, 0.83 ± 0.06 to 0.84 ± 0.06 in the VLF and HIMO groups, respectively).

There was a significant effect of menopausal status on the amount of trunk fat (arms, trunk and abdomen) such that postmenopausal women lost more trunk fat when consuming VLF (Table 4). Postmenopausal women also lost more abdominal fat than premenopausal women (2.0 ± 0.8 vs. 1.6 ± 0.8 kg, P < 0.05). There was a diet x menopausal status interaction in lean mass changes (P = 0.005) (Table 4). Most of this effect occurred in the premenopausal women for whom the high monounsaturated diet produced a lower loss of lean mass than the very low-fat diet (P = 0.006). In postmenopausal women, the opposite occurred and was not significant (P = 0.195). The contrast between pre- and postmenopausal women consuming the high monounsaturated fat diet was also significant (P = 0.035). Thus the HIMO is especially beneficial in premenopausal women.


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TABLE 4 Change in body composition in nondiabetic overweight women consuming a diet high in monounsaturated fat (HIMO) or a very low-fat (VLF) diet by menopausal status1

 
Serum lipids declined during the course of the study (Table 5). TC fell by 0.82 ± 0.50 mmol/L in the VLF group and 0.50 ± 0.47 mmol/L in the HIMO group with a diet interaction (P < 0.001 for time, P < 0.05 for diet effect). HDL cholesterol fell to a greater extent in the VLF group, 0.18 ± 0.23 mmol/L, compared with 0.04 ± 0.19 mmol/L for the HIMO group (P = 0.01 for diet effect, P < 0.01 for time) but the change in LDL-C did not differ between diets, with 0.52 ± 0.49 mmol/L for the VLF group and 0.31 ± 0.43 mmol/L for the HIMO group (P < 0.01 for time). TG fell in both groups (P < 0.05 for time), with no effect of diet. The LDL/HDL ratio was reduced from 2.25 ± 0.94 to 2.09 ± 0.83 in the VLF group compared with 2.26 ± 0.76 to 2.09 ± 0.72 in the HIMO group (P < 0.05 for time with no effect of diet).


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TABLE 5 Changes in serum lipids, plasma glucose, plasma insulin, and blood pressure after weight loss in nondiabetic overweight women consuming a diet high in monounsaturated fat (HIMO) or a very low-fat (VLF) diet1

 
Fasting plasma glucose changes were small, 0.07 ± 0.32 mmol/L for the VLF group compared with 0.11 ± 0.39 mmol/L for the HIMO group (P < 0.05; Table 5). Blood pressure declined to the same extent in both groups (Table 5).


    DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
In this study, a very low-fat weight loss diet compared with a high monounsaturated weight loss diet did not have differential effects on fat distribution. We confirmed previous findings that weight loss was the same when either HIMO or VLF diets were consumed under energy-restricted conditions (6,1214). However, in contrast to the findings of Walker et al. (8,9), the amount of fat and lean tissue lost and the distribution of the loss did not differ between the groups. In Walker’s initial study, designed for weight stability, subjects with type 2 diabetes lost weight (~1.0 kg) and body fat (~0.8 kg) after consumption of either a very low-fat or a high monounsaturated fat diet; however, the ratio of upper to lower body fat increased after consumption of the very low-fat diet and did not change after the high monounsaturated fat period. Similarly, in a weight loss study, subjects with type 2 diabetes lost ~1.0 kg, and fat was lost mainly from the lower body (–0.7 kg) when consuming the low-fat diet. However, there were no significant differences in the change in upper body fat in either study. Abdominal fat per se is the major contributor to the enhanced cardiovascular risk of obesity (15). However, although the fat loss achieved in our study (>7 kg) was much greater, we did not observe these changes. The previous studies were both very small; dietary compliance was clearly a major issue because minimal weight loss occurred in the weight loss study, thereby casting doubt on the adherence to the macronutrient prescription. Women with type 2 diabetes may have a reduced ability to conserve lower body fat or may be resistant to upper body fat loss, phenomena that do not occur in nondiabetic women. In a cross-sectional study of women with and without type 2 diabetes, Stoney et al. (16) observed that although total body fat was similar, women with diabetes had less lower body fat. However, to our knowledge, there is no evidence that insulin resistance predisposes to these differences.

Similar to our findings, Archer et al. (17) reported reductions in body weight, waist circumference, and total, visceral, and subcutaneous adipose tissue in men following either a high monounsaturated fat diet or a low-fat high carbohydrate diet with no difference between diets and no differential effect on body composition.

In the present study, there was a differential effect of menopausal status on fat distribution such that postmenopausal women lost 2.0 kg abdominal fat (21% total weight loss) compared with a loss of 1.6 kg (17% total weight loss) in premenopausal women, a difference that was independent of baseline abdominal fat. Menopause is associated with weight gain and a shift to abdominal fat distribution (18,19), changes that can be ameliorated by hormone replacement therapy (20) and may be related to an increase in free testosterone index (21). It might therefore be expected that postmenopausal women would have a greater proportion of abdominal fat. However, at baseline, the postmenopausal subjects did not have more abdominal fat. There are few studies of body composition changes before and after weight loss in both pre- and postmenopausal women. In contrast to our findings, Park and Lee (22) reported reduced loss of visceral adipose tissue in postmenopausal compared with premenopausal women with a similar change in overall fat mass. Zamboni et al. (23) observed the same body fat distribution before weight loss and after regain of weight in both pre- and postmenopausal women. The disparity in these findings requires clarification.

We also observed diet x menopause interactions with respect to lean mass because there appeared to be a preservation of lean mass with consumption of the HIMO diet in premenopausal women. To our knowledge, this has not been reported before. However, we are unable to explain why this effect occurred, and it requires confirmation in further studies.

Both diets reduced LDL-C by 9–16% (another major coronary risk factor) and plasma TG by 18–22%. However HDL-C, which is associated with protection from cardiovascular disease, was reduced 12% by the very low-fat diet and by only 4% by the high monounsaturated fat diet. The LDL:HDL ratio, a powerful predictor of cardiovascular disease risk (24), was reduced by both diets.

In conclusion, in the present study, weight, total fat mass, and regional fat mass loss did not differ with consumption of either a very low-fat or a high monounsaturated weight loss diet. We also observed a diet x menopause interaction with an apparent preservation of lean mass with consumption of the high monounsaturated fat diet in premenopausal women. These findings have to be confirmed in future studies.


    ACKNOWLEDGMENTS
 
We acknowledge the skills of the Commonwealth Scientific and Industrial Research Organization Clinical Research Unit Team, in particular Ms. Kay Pender, Ms. Anne McGuffin, Sr., Marcia Parrish, and Dr. Leonie Heilbronn, in conducting the study.


    FOOTNOTES
 
1 Supported in part by Meadow Lea Foods Australia. Back

3 Abbreviations used: DBP, diastolic blood pressure; DEXA, dual energy X-ray absorptiometry; HDL-C, HDL cholesterol; HIMO, high in monounsaturated fat diet; LDL-C, LDL cholesterol; SBP, systolic blood pressure; TC, total cholesterol; TG, triglycerides; VLF, very low-fat diet. Back

Manuscript received 11 March 2004. Initial review completed 29 March 2004. Revision accepted 26 April 2004.


    LITERATURE CITED
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

1. Rexrode, K. M., Carey, V. J., Hennekens, C. H., Walters, E. E., Colditz, G. A., Stampfer, M. J., Willett, W. C. & Manson, J. E. (1998) Abdominal adiposity and coronary heart disease in women. J. Am. Med. Assoc. 280:1843-1848.[Abstract/Free Full Text]

2. Folsom, A. R., Prineas, R. J., Kaye, S. A. & Munger, R. G. (1990) Incidence of hypertension and stroke in relation to body fat distribution and other risk factors in older women. Stroke 21:701-706.[Abstract/Free Full Text]

3. Carey, V. J., Walters, E. E., Colditz, G. A., Solomon, C. G., Willett, W. C., Rosner, B. A., Speizer, F. E. & Manson, J. E. (1997) Body fat distribution and risk of non-insulin-dependent diabetes mellitus in women. The Nurses’ Health Study. Am. J. Epidemiol. 145:614-619.[Abstract/Free Full Text]

4. Han, T. S., Feskens, E. J., Lean, M. E. & Seidell, J. C. (1998) Associations of body composition with Type 2 diabetes mellitus. Diabetes Med. 15:129-135.[Medline]

5. Snijder, M. B., Dekker, J. M., Visser, M., Bouter, L. M., Stehouwer, C. D., Kostense, P. J., Yudkin, J. S., Heine, R. J., Nijpels, G. & Seidell, J. C. (2003) Associations of hip and thigh circumferences independent of waist circumference with the incidence of type 2 diabetes: the Hoorn Study. Am. J. Clin. Nutr. 77:1192-1197.[Abstract/Free Full Text]

6. Noakes, M. & Clifton, P. M. (2000) Changes in plasma lipids and other cardiovascular risk factors during 3 energy-restricted diets differing in total fat and fatty acid composition. Am. J. Clin. Nutr. 71:706-712.[Abstract/Free Full Text]

7. Heilbronn, L. K., Noakes, M. & Clifton, P. M. (1999) Effect of energy restriction, weight loss, and diet composition on plasma lipids and glucose in patients with type 2 diabetes. Diabetes Care 22:889-895.[Abstract]

8. Walker, K. Z., O’Dea, K., Johnson, L., Sinclair, A. J., Piers, L. S., Nicholson, G. C. & Muir, J. G. (1996) Body fat distribution and non-insulin-dependent diabetes: comparison of a fiber-rich, high-carbohydrate, low-fat (23%) diet and a 35% fat diet high in monounsaturated fat. Am. J. Clin. Nutr. 63:254-260.[Abstract/Free Full Text]

9. Walker, K. Z., O’Dea, K. & Nicholson, G. C. (1999) Dietary composition affects regional body fat distribution and levels of dehydroepiandrosterone sulphate (DHEAS) in post-menopausal women with Type 2 diabetes. Eur. J. Clin. Nutr. 53:700-705.[Medline]

10. Piers, L. S., Walker, K. Z., Stoney, R. M., Soares, M. J. & O’Dea, K. (2003) Substitution of saturated with monounsaturated fat in a 4-week diet affects body weight and composition of overweight and obese men. Br. J. Nutr. 90:717-727.[Medline]

11. Friedewald, W. T., Levy, R. I. & Fredrickson, D. S. (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18:499-502.[Abstract]

12. Golay, A., Allaz, A. F., Morel, Y., de Tonnac, N., Tankova, S. & Reaven, G. (1996) Similar weight loss with low- or high-carbohydrate diets. Am. J. Clin. Nutr. 63:174-178.[Abstract/Free Full Text]

13. Gumbiner, B., Low, C. C. & Reaven, P. D. (1998) Effects of a monounsaturated fatty acid-enriched hypocaloric diet on cardiovascular risk factors in obese patients with type 2 diabetes. Diabetes Care 21:9-15.[Abstract]

14. Pelkman, C. L., Fishell, V. K., Maddox, D. H., Pearson, T. A., Mauger, D. T. & Kris-Etherton, P. M. (2004) Effects of moderate-fat (from monounsaturated fat) and low-fat weight-loss diets on the serum lipid profile in overweight and obese men and women. Am. J. Clin. Nutr. 79:204-212.[Abstract/Free Full Text]

15. Despres, J. P. (1994) Dyslipidaemia and obesity. Baillieres Clin. Endocrinol. Metab. 8:629-660.[Medline]

16. Stoney, R. M., Walker, K. Z., Best, J. D., Ireland, P. D., Giles, G. G. & O’Dea, K. (1998) Do postmenopausal women with NIDDM have a reduced capacity to deposit and conserve lower-body fat?. Diabetes Care 21:828-830.[Abstract]

17. Archer, W. R., Lamarche, B., Deriaz, O., Landry, N., Corneau, L., Despres, J. P., Bergeron, J., Couture, P. & Bergeron, N. (2003) Variations in body composition and plasma lipids in response to a high-carbohydrate diet. Obes. Res. 11:978-986.[Medline]

18. Lovejoy, J. C. (2003) The menopause and obesity. Prim. Care 30:317-325.[Medline]

19. Sorensen, M. B. (2002) Changes in body composition at menopause-age, lifestyle or hormone deficiency?. J. Br. Meno. Soc. 8:137-140.

20. Arabi, A., Garnero, P., Porcher, R., Pelissier, C., Benhamou, C. L. & Roux, C. (2003) Changes in body composition during post-menopausal hormone therapy: a 2 year prospective study. Hum. Reprod. 18:1747-1752.[Abstract/Free Full Text]

21. Guthrie, J. R., Dennerstein, L., Taffe, J. R., Ebeling, P. R., Randolph, J. F., Burger, H. G. & Wark, J. D. (2003) Central abdominal fat and endogenous hormones during the menopausal transition. Fertil. Steril. 79:1335-1340.[Medline]

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23. Zamboni, M., Armellini, F., Turcato, E., Micciolo, R., Desideri, S., Bergamo-Andreis, I. A. & Bosello, O. (1996) Effect of regain of body weight on regional body fat distribution: comparison between pre- and postmenopausal obese women. Obes. Res. 4:555-560.[Medline]

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