Effects of Weight Loss on Adipose Tissue Distribution
Managing CMRKey Points
- Visceral fat is a strong predictor of metabolic abnormalities, disease, and mortality.
- As little as 20 minutes of daily exercise can reduce visceral fat by 10%. Increasing exercise to 60 minutes a day can lead to even greater reductions (~30%).
- Reducing daily caloric intake by 400 to 700 kcal can cause a 15 to 30% reduction in visceral fat.
- For a given amount of weight loss, exercise preserves muscle mass and causes greater reductions in total and visceral fat compared to diet-induced weight loss.
- Although reducing body weight causes the greatest reduction in visceral fat, exercise training can significantly reduce visceral fat, even when weight is maintained.
Weight Loss and Abdominal Obesity
In the 1950s, Jean Vague [1] noted that upper body or android obesity was an important predictor of atherosclerosis, diabetes, gout, and other diseases. While the association between abdominal obesity and metabolic risk may be explained by excess fat accumulation in either of two distinct depots within the abdomen, namely visceral fat and abdominal subcutaneous fat, the literature points to visceral fat as the depot that carries the greatest health risk. Independent of subcutaneous abdominal fat, visceral fat is a strong predictor of dyslipidemia [2,3], glucose intolerance [4,5], insulin resistance [6], systemic inflammation [7], hypertension [8], cardiovascular disease [9], type 2 diabetes [10], and all-cause mortality [11]. Accordingly, the ability of exercise and/or diet to significantly reduce body weight and visceral fat is a key consideration for reducing the health risk among abdominally obese patients.
Exercise-induced Weight Loss and Visceral Fat Reduction
Cross-sectional data shows that individuals who are more physically active have lower amounts of visceral fat [12,13,14]. Even for a given degree of obesity, individuals who are more active tend to have the lowest levels of visceral fat compared to their sedentary counterparts [15,16]. In addition, numerous intervention studies have demonstrated that exercise training can reduce visceral fat through weight loss [17-28].
It was originally suggested that exercise alone produced only a marginal (1 to 2 kg) decrease in body weight [29]. These earlier conclusions were based on evidence from intervention studies wherein the prescribed negative energy balance was too low to induce substantive weight loss [30]. The literature suggests, however, that exercise can produce a wide array of visceral fat changes, from a minor reduction of approximately 5% [21] up to a 50% reduction [20]. These changes also correspond to a wide array of reductions in body weight. In general, the highest levels of exercise cause the highest energy deficit, which leads to greater weight loss and a greater reduction in visceral fat. For example, approximately 60 minutes of daily exercise over 3 months caused a 1.0 and 0.7 kg (-28 and -26%) reduction in visceral fat along with a 7.7 and 6.6 kg weight loss in obese men and women, respectively [17,18].
Conversely, approximately 20 to 25 minutes of daily exercise reduced visceral fat by only 6 to 10%, for a modest weight loss of 1.4 to 1.8 kg in overweight women [21] and obese women with diabetes [31]. Illustrating a dose-response relationship between exercise dose, weight loss, and visceral fat loss, Irwin et al. [21] found that women who were highly active (>28 min/day) lost 6.9% of visceral fat, compared to a 5.9% loss among intermediate active (19 to 28 min/day), a 3.4% loss in low active (≤18 min/day), and a 0.1% gain in controls over a year-long intervention.
For a given amount of exercise-induced weight loss, the relative amount of visceral fat lost is generally greater than the amount of abdominal subcutaneous fat lost [17,18,24,26,28,31,32]. This suggests that visceral fat may be more sensitive to exercise-induced weight loss than other fat depots. In general, exercise training reduces visceral fat by approximately 0.5 kg for every 4 kg of body weight lost in both men and women [17,18]. Also, it appears that as little as 20 minutes of daily exercise with an energy expenditure of less than 1,500 kcal/week can spur modest reductions in visceral fat (5 to 10%). Increasing daily exercise to 60 minutes with an energy expenditure of 3,500 to 4,500 kcal/week causes much greater reductions in visceral fat (~30%). While visceral fat cannot be readily measured, waist circumference is recommended as a reliable measure of visceral fat [33,34].
Diet-induced Weight Loss and Visceral Fat Reduction
The second weight reduction method focuses on energy intake. A calorie-restricted diet has traditionally been the cornerstone of obesity reduction treatment [35]. A number of studies have assessed the effects of chronic caloric restriction on weight loss and visceral fat reduction [17,18,26,36-43]. Much like in exercise interventions, there are a range of responses in terms of weight loss (5 to 18 kg) and visceral fat reduction (15 to 47%) with varying degrees of caloric restriction (from a 400 kcal/day reduction to a very low calorie diet of 800 kcal/day). The interventions that prescribe a very low calorie diet ranging from 800 to 1,200 kcal/day and lasting 3-6 months tend to produce the most marked reductions in weight (10 to 18 kg) and visceral fat (24 to 47%) [36,40,41]. The more moderate approaches that reduce caloric intake by 400 to 700 kcal/day produce more modest reductions in body weight (5 to 9 kg) and visceral fat (15 to 30%) [17, 18, 37-39, 42]. Overall, approximately 3 months of a 500 kcal/day reduction in caloric intake is enough to reduce body weight by approximately 5 kg and visceral fat by about 0.5 kg [17,18].
Is Exercise or Diet Better at Reducing Visceral Fat?
Since weight loss generally causes a reduction in visceral fat, the interventions that produce the greatest weight loss will inevitably cause the greatest loss of visceral fat. Caloric restriction is better at inducing significant weight loss than exercise. This is supported by the degree of weight loss reported among diet versus exercise weight loss studies (5 to 18 kg versus 1 to 8 kg reduction, respectively). For example, some of the very low calorie diets prescribed limited patients’ caloric intake to only 800 kcal/day [36], which is a very large (2,000 kcal/day) energy deficit for an obese adult man. In order for that obese man to produce the same energy deficit and expend 2,000 kcal, he would require approximately 3 hours of daily, moderate-intensity exercise [17].
However, if the goal is moderate weight loss, exercise and diet are equally effective. Carefully controlled studies have shown that when reduction of caloric intake is equal to the calories expended through exercise, which creates an equivalent energy deficit, the weight loss is identical between strategies [17,18].
Although diet and exercise may both lower body weight equally, the composition of the weight lost differs according to the strategy used (Figure 1). It has been shown repeatedly that for a given weight loss, exercisers lose more fat mass than dieters [17,18,24,38]. Exercise therefore seems to prevent or at least attenuate the loss of lean muscle mass that occurs during diet-induced weight loss [17,18,24,38].
The ability of diet to induce a marked caloric deficit, combined with the ability of exercise to maintain muscle mass and readily mobilize fat from the visceral depot, likely provides the best of both worlds [45, 46]. Data from the National Weight Control Registry suggests that individuals who are most successful at attaining and maintaining significant weight loss are likely to use a combination of diet and exercise to achieve their goal [47]. Additionally, during weight loss interventions, physical exercise has been shown to improve cardiorespiratory fitness [17,18], which would be expected to further reduce risk of morbidity and mortality independent of changes in weight and visceral fat [48-50]. The combination of diet and exercise is therefore the ideal strategy for losing weight and reducing visceral fat.
Exercise Without Weight Loss and Visceral Fat Reduction
Although weight loss is the ideal outcome of chronic exercise in overweight individuals, the evidence suggests that even when body mass does not change, regular exercise can markedly reduce visceral fat and shrink waist circumference accordingly [17,18,25,26,51,54] (Figure 2). For example, approximately two months of regular, moderate-intensity aerobic exercise can substantially reduce visceral fat (-41 to -45%) without causing weight change in samples of type 2 diabetic patients (45, 46). Even non-obese premenopausal women experience a significant reduction in visceral fat (-25%) after 6 months of aerobic exercise despite no significant change in weight [53]. Several studies have specifically examined the effect of exercise on abdominal adiposity when weight is maintained by having study participants consume compensatory kilocalories equivalent to the amount expended during exercise [17,18,54]. The length of each intervention was roughly 3 months and consisted of an energy expenditure of approximately 3,500 kcal/week. The primary findings suggest that in obese Caucasian men and women, as well as in individuals with type 2 diabetes, exercise training can significantly reduce total and abdominal obesity even with little or no change in body weight.
Although the above suggests that regular exercise can reduce visceral adiposity independent of weight loss, it is important to note that exercisers who lose weight generally lose more visceral fat than exercisers who maintain body weight [17, 18] (Figure 2). From a clinical perspective, exercise-induced weight loss therefore causes the greatest reduction in visceral fat and the greatest improvements in metabolic status. However, given the challenges associated with losing large amounts of weight, it is equally important to reduce visceral adiposity and related health risk with minimal weight loss.
Sex and Visceral Fat Reduction With Weight Loss
A number of studies that have failed to find significant reductions in visceral fat in women have raised the possibility that women may be resistant to exercise and/or diet-induced reductions in visceral fat [24,42,55,57]. For example, 16 months of supervised aerobic exercise at the same exercise intensity and of the same duration reduced 5% of the visceral fat in young men but failed to produce a significant reduction in young women [24]. Further evidence from a trial using either diet or diet with exercise suggests a similar pattern [42]. In that study, even though both sexes lost approximately 8.5 kg of body weight in response to the diet-only intervention, the men reduced their visceral fat by 1.4 kg compared to only 0.4 kg for the women.
In stark contrast, several well-controlled studies have reported that exercise can significantly reduce visceral fat (5 to 30%) in women, much like in men [18,20,21,53,57]. For example, 14 weeks of a 700 kcal/day deficit through diet or exercise has been shown to significantly reduce visceral fat (21 to 30%) in association with a 5 to 6 kg weight loss [18]. Another study demonstrated that both men and women reduced visceral fat in response to the same aerobic exercise prescription, though the reduction was slightly smaller in women (-7 and -5% in men and women, respectively) [57].
With respect to exercise-induced visceral fat reduction, studies that claim women are resistant to visceral fat loss may be confounded by sex differences in exercise energy expenditure. Since men have a greater exercise capacity compared to women [58], matching men and women on exercise intensity and duration alone results in a higher exercise energy expenditure in men and, consequently, a higher expected total and visceral fat loss. It has also been noted that the amount of visceral fat lost through intervention is contingent on the initial amount of visceral fat [59]. Women generally have less visceral fat than men [60], which may also play a role in any sex differences. In light of these findings, it seems doubtful that women are actually resistant to visceral fat loss. However, further research is needed to shed light on any possible sex differences in visceral fat reduction.
Numerous cross-sectional studies have found that for a given amount of total fat mass, Asians have more visceral fat than Caucasians [61], who in turn have more visceral fat than African-Americans [62-64]. Racial differences in visceral fat reduction may therefore be a possibility. Unfortunately, most of the current literature is based mainly on Caucasian populations, which hinders the identification of any possible racial differences. The limited evidence available suggests that Caucasians and African Americans do not differ in terms of visceral fat loss in response to a 20 week exercise intervention [57]. More research is needed to pinpoint the influence of race on visceral fat reduction.
Abdominal obesity has long been identified as the phenotype that conveys the greatest health risk, independent of total body weight. Whether it is induced through exercise and/or diet, weight loss leads to a marked reduction in visceral adiposity. As little as 20 to 60 minutes of daily exercise or a 400 to 700 kcal/day energy restriction can cause a 10 to 30% reduction in visceral fat. For a given amount of weight loss, exercise can induce a greater relative reduction in visceral fat and better maintain muscle mass. Lastly, of key importance is the notion that total body weight needs not change for visceral fat to decrease significantly. The waist circumference tape may therefore be a more reliable marker of obesity treatment success than the bathroom scale.
References
-
Vague J. The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. Am J Clin Nutr 1956; 4: 20-34.
-
Nguyen-Duy TB, Nichaman MZ, Church TS, et al. Visceral fat and liver fat are independent predictors of metabolic risk factors in men. Am J Physiol Endocrinol Metab 2003; 284: E1065-71.
-
Nieves DJ, Cnop M, Retzlaff B, et al. The atherogenic lipoprotein profile associated with obesity and insulin resistance is largely attributable to intra-abdominal fat. Diabetes 2003; 52: 172-9.
PubMed ID: 12502509
-
Brochu M, Starling RD, Tchernof A, et al. Visceral adipose tissue is an independent correlate of glucose disposal in older obese postmenopausal women. J Clin Endocrinol Metab 2000; 85: 2378-84.
PubMed ID: 10902782
-
Janssen I, Fortier A, Hudson R, et al. Effects of an energy-restrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women. Diabetes Care 2002; 25: 431-8.
PubMed ID: 11874926
-
Ross R, Aru J, Freeman J, et al. Abdominal adiposity and insulin resistance in obese men. Am J Physiol Endocrinol Metab 2002; 282: E657-63
PubMed ID: 11832370
-
Forouhi NG, Sattar N and McKeigue PM. Relation of C-reactive protein to body fat distribution and features of the metabolic syndrome in Europeans and South Asians. Int J Obes Relat Metab Disord 2001; 25: 1327-31.
PubMed ID: 11571595
-
Hayashi T, Boyko EJ, Leonetti DL, et al. Visceral adiposity is an independent predictor of incident hypertension in Japanese Americans. Ann Intern Med 2004; 140: 992-1000.
PubMed ID: 15197016
-
Fujimoto WY, Bergstrom RW, Boyko EJ, et al. Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care 1999; 22: 1808-12.
PubMed ID: 10546012
-
Boyko EJ, Fujimoto WY, Leonetti DL, et al. Visceral adiposity and risk of type 2 diabetes: a prospective study among Japanese Americans. Diabetes Care 2000; 23: 465-71.
PubMed ID: 10857936
-
Kuk JL, Katzmarzyk PT, Nichaman MZ, et al. Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring) 2006; 14: 336-41.
PubMed ID: 16571861
-
Kanaley JA, Sames C, Swisher L, et al. Abdominal fat distribution in pre- and postmenopausal women: The impact of physical activity, age, and menopausal status. Metabolism 2001; 50: 976-82.
PubMed ID: 11474488
-
Major GC, Piché ME, Bergeron J, et al. Energy expenditure from physical activity and the metabolic risk profile at menopause. Med Sci Sports Exerc 2005; 37: 204-12.
PubMed ID: 15692314
-
Hunter GR, Kekes-Szabo T, Treuth MS, et al. Intra-abdominal adipose tissue, physical activity and cardiovascular risk in pre- and post-menopausal women. Int J Obes Relat Metab Disord 1996; 20: 860-5.
PubMed ID: 8880355
-
Wong SL, Katzmarzyk P, Nichaman MZ, et al. Cardiorespiratory fitness is associated with lower abdominal fat independent of body mass index. Med Sci Sports Exerc 2004; 36: 286-91.
PubMed ID: 14767252
-
Janssen I, Katzmarzyk PT, Ross R, et al. Fitness alters the associations of BMI and waist circumference with total and abdominal fat. Obes Res 2004; 12: 525-37.
PubMed ID: 15044671
-
Ross R, Dagnone D, Jones PJ, et al. Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial. Ann Intern Med 2000; 133: 92-103.
PubMed ID: 10896648
-
Ross R, Janssen I, Dawson J, et al. Exercise-induced reduction in obesity and insulin resistance in women: a randomized controlled trial. Obes Res 2004; 12: 789-98.
PubMed ID: 15166299
-
Boudou P, De Kerviler E, Vexiau P, et al. Effects of a single bout of exercise and exercise training on steroid levels in middle-aged type 2 diabetic men: relationship to abdominal adipose tissue distribution and metabolic status. Diabetes Metab 2000; 26: 450-7.
PubMed ID: 11173715
-
Park SK, Park JH, Kwon YC, et al. The effect of combined aerobic and resistance exercise training on abdominal fat in obese middle-aged women. J Physiol Anthropol Appl Human Sci 2003; 22: 129-35.
PubMed ID: 12808225
-
Irwin ML, Yasui Y, Ulrich CM, et al. Effect of exercise on total and intra-abdominal body fat in postmenopausal women: a randomized controlled trial. JAMA 2003; 289: 323-30.
PubMed ID: 12525233
-
Slentz CA, Duscha BD, Johnson JL, et al. Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE–a randomized controlled study. Arch Intern Med 2004; 164: 31-9.
PubMed ID: 14718319
-
Stewart KJ, Bacher AC, Turner K, et al. Exercise and risk factors associated with metabolic syndrome in older adults. Am J Prev Med 2005; 28: 9-18.
PubMed ID: 15626550
-
Donnelly JE, Hill JO, Jacobsen DJ, et al. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch Intern Med 2003; 163: 1343-50.
PubMed ID: 12796071
-
Ross R and Bradshaw AJ. The future of obesity reduction: beyond weight loss. . Nat Rev Endocrinol 2009; 5: 319–26.
PubMed ID: 19421242
-
Ross R, Soni S and Houle S. Negative energy balance induced by exercise or diet: effects on visceral adipose tissue and liver fat. Nutrients 2020; 12: 891.
PubMed ID: 32218121
-
Neeland IJ, Ross R, Després JP, et al. Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement. Lancet Diabetes Endocrinol 2019; 9: 715-25.
PubMed ID: 31301983
-
Rao S, Pandey A, Garg S, et al. Effect of exercise and pharmacological interventions on visceral adiposity: a systematic review and meta-analysis of long-term randomized controlled trials. Mayo Clin Proc 2019; 94: 211-24.
PubMed ID: 30711119
-
Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults–The Evidence Report. National Institutes of Health. Obes Res 1998; 6 Suppl 2: 51S-209S.
PubMed ID: 9813653
-
Ross R, Freeman JA and Janssen I. Exercise alone is an effective strategy for reducing obesity and related comorbidities. Exerc Sport Sci Rev 2000; 28: 165-70.
PubMed ID: 11064850
-
Giannopoulou I, Ploutz-Snyder LL, Carhart R, et al. Exercise is required for visceral fat loss in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 2005; 90: 1511-8.
PubMed ID: 15598677
-
Cuff DJ, Meneilly GS, Martin A, et al. Effective exercise modality to reduce insulin resistance in women with type 2 diabetes. Diabetes Care 2003; 26: 2977-82.
PubMed ID: 14578226
-
Pouliot M-C, Després JP, Lemieux S, et al. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994; 73: 460-8.
PubMed ID: 8141087
-
Ross R, Neeland IJ, Yamashita S, et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020; 16: 177-89.
PubMed ID: 32020062
-
Williamson DF, Serdula MK, Anda RF, et al. Weight loss attempts in adults: goals, duration, and rate of weight loss. Am J Public Health 1992; 82: 1251-7.
PubMed ID: 1503167
-
Goodpaster BH, Kelley DE, Wing RR, et al. Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 1999; 48: 839-47.
PubMed ID: 10102702
-
Rissanen P, Makimattila S, Vehmas T, et al. Effect of weight loss and regional fat distribution on plasma leptin concentration in obese women. Int J Obes Relat Metab Disord 1999; 23: 645-9.
PubMed ID: 10411239
-
Racette SB, Weiss EP, Villareal DT, et al. One year of caloric restriction in humans: feasibility and effects on body composition and abdominal adipose tissue. J Gerontol A Biol Sci Med Sci 2006; 61: 943-50.
PubMed ID: 16960025
-
You T, Berman DM, Ryan AS, et al. Effects of hypocaloric diet and exercise training on inflammation and adipocyte lipolysis in obese postmenopausal women. J Clin Endocrinol Metab 2004; 89: 1739-46.
PubMed ID: 15070939
-
Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006; 29: 1337-44.
PubMed ID: 16732018
-
Purnell JQ, Kahn SE, Albers JJ, et al. Effect of weight loss with reduction of intra-abdominal fat on lipid metabolism in older men. J Clin Endocrinol Metab 2000; 85: 977-82.
PubMed ID: 10720026
-
Redman LM, Heilbronn LK, Martin CK, et al. Effect of calorie restriction with or without exercise on body composition and fat distribution. J Clin Endocrinol Metab 2007; 92: 865-72.
PubMed ID: 17200169
-
Weiss EP and Holloszy JO. Improvements in body composition, glucose tolerance, and insulin action induced by increasing energy expenditure or decreasing energy intake. J Nutr 2007; 137: 1087-90.
PubMed ID: 17374683
-
Tzankoff SP and Norris AH. Effect of muscle mass decrease on age-related BMR changes. J Appl Physiol 1977; 43: 1001-6.
PubMed ID: 606683
-
Ross R, Pedwell H and Rissanen J. Effects of energy restriction and exercise on skeletal muscle and adipose tissue in women as measured by magnetic resonance imaging. Am J Clin Nutr 1995; 61: 1179-85.
PubMed ID: 7762515
-
Ross R, Rissanen J, Pedwell H, et al. Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. J Appl Physiol 1996; 81: 2445-55.
PubMed ID: 9018491
-
Klem ML, Wing RR, McGuire MT, et al. A descriptive study of individuals successful at long-term maintenance of substantial weight loss. Am J Clin Nutr 1997; 66: 239-46.
PubMed ID: 9250100
-
Wei M, Kampert JB, Barlow CE, et al. Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men. JAMA 1999; 282: 1547-53.
PubMed ID: 10546694
-
Ross R, Blair SN, Arena R, et al. Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation 2016; 134: e653-99.
PubMed ID: 27881567
-
Lee S, Kuk JL, Katzmarzyk PT, et al. Cardiorespiratory fitness attenuates metabolic risk independent of abdominal subcutaneous and visceral fat in men. Diabetes Care 2005; 28: 895-901.
PubMed ID: 15793192
-
Boudou P, Sobngwi E, Mauvais-Jarvis F, et al. Absence of exercise-induced variations in adiponectin levels despite decreased abdominal adiposity and improved insulin sensitivity in type 2 diabetic men. Eur J Endocrinol 2003; 149: 421-4.
PubMed ID: 14585088
-
Mourier A, Gautier JF, De Kerviler E, et al. Mobilization of visceral adipose tissue related to the improvement in insulin sensitivity in response to physical training in NIDDM. Effects of branched-chain amino acid supplements. Diabetes Care 1997; 20: 385-91.
PubMed ID: 9051392
-
Thomas EL, Brynes AE, McCarthy J, et al. Preferential loss of visceral fat following aerobic exercise, measured by magnetic resonance imaging. Lipids 2000; 35: 769-76.
PubMed ID: 10941878
-
Lee S, Kuk JL, Davidson LE, et al. Exercise without weight loss is an effective strategy for obesity reduction in obese individuals with and without Type 2 diabetes. J Appl Physiol 2005; 99: 1220-5.
PubMed ID: 15860689
-
Donnelly JE, Jacobsen DJ, Heelan KS, et al. The effects of 18 months of intermittent vs. continuous exercise on aerobic capacity, body weight and composition, and metabolic fitness in previously sedentary, moderately obese females. Int J Obes Relat Metab Disord 2000; 24: 566-72.
PubMed ID: 10849577
-
Snyder KA, Donnelly JE, Jabobsen DJ, et al. The effects of long-term, moderate intensity, intermittent exercise on aerobic capacity, body composition, blood lipids, insulin and glucose in overweight females. Int J Obes Relat Metab Disord 1997; 21: 1180-9.
PubMed ID: 9426387
-
Wilmore JH, Després JP, Stanforth PR, et al. Alterations in body weight and composition consequent to 20 wk of endurance training: the HERITAGE Family Study. Am J Clin Nutr 1999; 70: 346-52.
PubMed ID: 10479196
-
Astrand I. Aerobic work capacity in men and women with special reference to age. Acta Physiol Scand Suppl. 1960; 49: 1-92.
PubMed ID: 13794892
-
Leenen R, van der Kooy K, Deurenberg P, et al. Visceral fat accumulation in obese subjects: relation to energy expenditure and response to weight loss. Am J Physiol 1992; 263: E913-9.
PubMed ID: 1443124
-
Enzi G, Gasparo M, Biondetti PR, et al. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 1986; 44: 739-46.
PubMed ID: 3788827
-
Park YW, Allison DB, Heymsfield SB, et al. Larger amounts of visceral adipose tissue in Asian Americans. Obes Res 2001; 9: 381-7.
PubMed ID: 11445659
-
Després JP, Couillard C, Gagnon J, et al. Race, visceral adipose tissue, plasma lipids, and lipoprotein lipase activity in men and women: the Health, Risk Factors, Exercise Training, and Genetics (HERITAGE) family study. Arterioscler Thromb Vasc Biol 2000; 20: 1932-8.
PubMed ID: 10938014
-
Lovejoy JC, de la Bretonne JA, Klemperer M, et al. Abdominal fat distribution and metabolic risk factors: effects of race. Metabolism 1996; 45: 1119-24.
PubMed ID: 8781299
-
Hill JO, Sidney S, Lewis CE, et al. Racial differences in amounts of visceral adipose tissue in young adults: the CARDIA (Coronary Artery Risk Development in Young Adults) study. Am J Clin Nutr 1999; 69: 381-7.
PubMed ID: 10075320
Vague J. The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. Am J Clin Nutr 1956; 4: 20-34.
Nguyen-Duy TB, Nichaman MZ, Church TS, et al. Visceral fat and liver fat are independent predictors of metabolic risk factors in men. Am J Physiol Endocrinol Metab 2003; 284: E1065-71.
Nieves DJ, Cnop M, Retzlaff B, et al. The atherogenic lipoprotein profile associated with obesity and insulin resistance is largely attributable to intra-abdominal fat. Diabetes 2003; 52: 172-9.
PubMed ID: 12502509Brochu M, Starling RD, Tchernof A, et al. Visceral adipose tissue is an independent correlate of glucose disposal in older obese postmenopausal women. J Clin Endocrinol Metab 2000; 85: 2378-84.
PubMed ID: 10902782Janssen I, Fortier A, Hudson R, et al. Effects of an energy-restrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women. Diabetes Care 2002; 25: 431-8.
PubMed ID: 11874926Ross R, Aru J, Freeman J, et al. Abdominal adiposity and insulin resistance in obese men. Am J Physiol Endocrinol Metab 2002; 282: E657-63
PubMed ID: 11832370Forouhi NG, Sattar N and McKeigue PM. Relation of C-reactive protein to body fat distribution and features of the metabolic syndrome in Europeans and South Asians. Int J Obes Relat Metab Disord 2001; 25: 1327-31.
PubMed ID: 11571595Hayashi T, Boyko EJ, Leonetti DL, et al. Visceral adiposity is an independent predictor of incident hypertension in Japanese Americans. Ann Intern Med 2004; 140: 992-1000.
PubMed ID: 15197016Fujimoto WY, Bergstrom RW, Boyko EJ, et al. Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care 1999; 22: 1808-12.
PubMed ID: 10546012Boyko EJ, Fujimoto WY, Leonetti DL, et al. Visceral adiposity and risk of type 2 diabetes: a prospective study among Japanese Americans. Diabetes Care 2000; 23: 465-71.
PubMed ID: 10857936Kuk JL, Katzmarzyk PT, Nichaman MZ, et al. Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring) 2006; 14: 336-41.
PubMed ID: 16571861Kanaley JA, Sames C, Swisher L, et al. Abdominal fat distribution in pre- and postmenopausal women: The impact of physical activity, age, and menopausal status. Metabolism 2001; 50: 976-82.
PubMed ID: 11474488Major GC, Piché ME, Bergeron J, et al. Energy expenditure from physical activity and the metabolic risk profile at menopause. Med Sci Sports Exerc 2005; 37: 204-12.
PubMed ID: 15692314Hunter GR, Kekes-Szabo T, Treuth MS, et al. Intra-abdominal adipose tissue, physical activity and cardiovascular risk in pre- and post-menopausal women. Int J Obes Relat Metab Disord 1996; 20: 860-5.
PubMed ID: 8880355Wong SL, Katzmarzyk P, Nichaman MZ, et al. Cardiorespiratory fitness is associated with lower abdominal fat independent of body mass index. Med Sci Sports Exerc 2004; 36: 286-91.
PubMed ID: 14767252Janssen I, Katzmarzyk PT, Ross R, et al. Fitness alters the associations of BMI and waist circumference with total and abdominal fat. Obes Res 2004; 12: 525-37.
PubMed ID: 15044671Ross R, Dagnone D, Jones PJ, et al. Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial. Ann Intern Med 2000; 133: 92-103.
PubMed ID: 10896648Ross R, Janssen I, Dawson J, et al. Exercise-induced reduction in obesity and insulin resistance in women: a randomized controlled trial. Obes Res 2004; 12: 789-98.
PubMed ID: 15166299Boudou P, De Kerviler E, Vexiau P, et al. Effects of a single bout of exercise and exercise training on steroid levels in middle-aged type 2 diabetic men: relationship to abdominal adipose tissue distribution and metabolic status. Diabetes Metab 2000; 26: 450-7.
PubMed ID: 11173715Park SK, Park JH, Kwon YC, et al. The effect of combined aerobic and resistance exercise training on abdominal fat in obese middle-aged women. J Physiol Anthropol Appl Human Sci 2003; 22: 129-35.
PubMed ID: 12808225Irwin ML, Yasui Y, Ulrich CM, et al. Effect of exercise on total and intra-abdominal body fat in postmenopausal women: a randomized controlled trial. JAMA 2003; 289: 323-30.
PubMed ID: 12525233Slentz CA, Duscha BD, Johnson JL, et al. Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE–a randomized controlled study. Arch Intern Med 2004; 164: 31-9.
PubMed ID: 14718319Stewart KJ, Bacher AC, Turner K, et al. Exercise and risk factors associated with metabolic syndrome in older adults. Am J Prev Med 2005; 28: 9-18.
PubMed ID: 15626550Donnelly JE, Hill JO, Jacobsen DJ, et al. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch Intern Med 2003; 163: 1343-50.
PubMed ID: 12796071Ross R and Bradshaw AJ. The future of obesity reduction: beyond weight loss. . Nat Rev Endocrinol 2009; 5: 319–26.
PubMed ID: 19421242Ross R, Soni S and Houle S. Negative energy balance induced by exercise or diet: effects on visceral adipose tissue and liver fat. Nutrients 2020; 12: 891.
PubMed ID: 32218121Neeland IJ, Ross R, Després JP, et al. Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement. Lancet Diabetes Endocrinol 2019; 9: 715-25.
PubMed ID: 31301983Rao S, Pandey A, Garg S, et al. Effect of exercise and pharmacological interventions on visceral adiposity: a systematic review and meta-analysis of long-term randomized controlled trials. Mayo Clin Proc 2019; 94: 211-24.
PubMed ID: 30711119Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults–The Evidence Report. National Institutes of Health. Obes Res 1998; 6 Suppl 2: 51S-209S.
PubMed ID: 9813653Ross R, Freeman JA and Janssen I. Exercise alone is an effective strategy for reducing obesity and related comorbidities. Exerc Sport Sci Rev 2000; 28: 165-70.
PubMed ID: 11064850Giannopoulou I, Ploutz-Snyder LL, Carhart R, et al. Exercise is required for visceral fat loss in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 2005; 90: 1511-8.
PubMed ID: 15598677Cuff DJ, Meneilly GS, Martin A, et al. Effective exercise modality to reduce insulin resistance in women with type 2 diabetes. Diabetes Care 2003; 26: 2977-82.
PubMed ID: 14578226Pouliot M-C, Després JP, Lemieux S, et al. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994; 73: 460-8.
PubMed ID: 8141087Ross R, Neeland IJ, Yamashita S, et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020; 16: 177-89.
PubMed ID: 32020062Williamson DF, Serdula MK, Anda RF, et al. Weight loss attempts in adults: goals, duration, and rate of weight loss. Am J Public Health 1992; 82: 1251-7.
PubMed ID: 1503167Goodpaster BH, Kelley DE, Wing RR, et al. Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 1999; 48: 839-47.
PubMed ID: 10102702Rissanen P, Makimattila S, Vehmas T, et al. Effect of weight loss and regional fat distribution on plasma leptin concentration in obese women. Int J Obes Relat Metab Disord 1999; 23: 645-9.
PubMed ID: 10411239Racette SB, Weiss EP, Villareal DT, et al. One year of caloric restriction in humans: feasibility and effects on body composition and abdominal adipose tissue. J Gerontol A Biol Sci Med Sci 2006; 61: 943-50.
PubMed ID: 16960025You T, Berman DM, Ryan AS, et al. Effects of hypocaloric diet and exercise training on inflammation and adipocyte lipolysis in obese postmenopausal women. J Clin Endocrinol Metab 2004; 89: 1739-46.
PubMed ID: 15070939Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006; 29: 1337-44.
PubMed ID: 16732018Purnell JQ, Kahn SE, Albers JJ, et al. Effect of weight loss with reduction of intra-abdominal fat on lipid metabolism in older men. J Clin Endocrinol Metab 2000; 85: 977-82.
PubMed ID: 10720026Redman LM, Heilbronn LK, Martin CK, et al. Effect of calorie restriction with or without exercise on body composition and fat distribution. J Clin Endocrinol Metab 2007; 92: 865-72.
PubMed ID: 17200169Weiss EP and Holloszy JO. Improvements in body composition, glucose tolerance, and insulin action induced by increasing energy expenditure or decreasing energy intake. J Nutr 2007; 137: 1087-90.
PubMed ID: 17374683Tzankoff SP and Norris AH. Effect of muscle mass decrease on age-related BMR changes. J Appl Physiol 1977; 43: 1001-6.
PubMed ID: 606683Ross R, Pedwell H and Rissanen J. Effects of energy restriction and exercise on skeletal muscle and adipose tissue in women as measured by magnetic resonance imaging. Am J Clin Nutr 1995; 61: 1179-85.
PubMed ID: 7762515Ross R, Rissanen J, Pedwell H, et al. Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. J Appl Physiol 1996; 81: 2445-55.
PubMed ID: 9018491Klem ML, Wing RR, McGuire MT, et al. A descriptive study of individuals successful at long-term maintenance of substantial weight loss. Am J Clin Nutr 1997; 66: 239-46.
PubMed ID: 9250100Wei M, Kampert JB, Barlow CE, et al. Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men. JAMA 1999; 282: 1547-53.
PubMed ID: 10546694Ross R, Blair SN, Arena R, et al. Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation 2016; 134: e653-99.
PubMed ID: 27881567Lee S, Kuk JL, Katzmarzyk PT, et al. Cardiorespiratory fitness attenuates metabolic risk independent of abdominal subcutaneous and visceral fat in men. Diabetes Care 2005; 28: 895-901.
PubMed ID: 15793192Boudou P, Sobngwi E, Mauvais-Jarvis F, et al. Absence of exercise-induced variations in adiponectin levels despite decreased abdominal adiposity and improved insulin sensitivity in type 2 diabetic men. Eur J Endocrinol 2003; 149: 421-4.
PubMed ID: 14585088Mourier A, Gautier JF, De Kerviler E, et al. Mobilization of visceral adipose tissue related to the improvement in insulin sensitivity in response to physical training in NIDDM. Effects of branched-chain amino acid supplements. Diabetes Care 1997; 20: 385-91.
PubMed ID: 9051392Thomas EL, Brynes AE, McCarthy J, et al. Preferential loss of visceral fat following aerobic exercise, measured by magnetic resonance imaging. Lipids 2000; 35: 769-76.
PubMed ID: 10941878Lee S, Kuk JL, Davidson LE, et al. Exercise without weight loss is an effective strategy for obesity reduction in obese individuals with and without Type 2 diabetes. J Appl Physiol 2005; 99: 1220-5.
PubMed ID: 15860689Donnelly JE, Jacobsen DJ, Heelan KS, et al. The effects of 18 months of intermittent vs. continuous exercise on aerobic capacity, body weight and composition, and metabolic fitness in previously sedentary, moderately obese females. Int J Obes Relat Metab Disord 2000; 24: 566-72.
PubMed ID: 10849577Snyder KA, Donnelly JE, Jabobsen DJ, et al. The effects of long-term, moderate intensity, intermittent exercise on aerobic capacity, body composition, blood lipids, insulin and glucose in overweight females. Int J Obes Relat Metab Disord 1997; 21: 1180-9.
PubMed ID: 9426387Wilmore JH, Després JP, Stanforth PR, et al. Alterations in body weight and composition consequent to 20 wk of endurance training: the HERITAGE Family Study. Am J Clin Nutr 1999; 70: 346-52.
PubMed ID: 10479196Astrand I. Aerobic work capacity in men and women with special reference to age. Acta Physiol Scand Suppl. 1960; 49: 1-92.
PubMed ID: 13794892Leenen R, van der Kooy K, Deurenberg P, et al. Visceral fat accumulation in obese subjects: relation to energy expenditure and response to weight loss. Am J Physiol 1992; 263: E913-9.
PubMed ID: 1443124Enzi G, Gasparo M, Biondetti PR, et al. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 1986; 44: 739-46.
PubMed ID: 3788827Park YW, Allison DB, Heymsfield SB, et al. Larger amounts of visceral adipose tissue in Asian Americans. Obes Res 2001; 9: 381-7.
PubMed ID: 11445659Després JP, Couillard C, Gagnon J, et al. Race, visceral adipose tissue, plasma lipids, and lipoprotein lipase activity in men and women: the Health, Risk Factors, Exercise Training, and Genetics (HERITAGE) family study. Arterioscler Thromb Vasc Biol 2000; 20: 1932-8.
PubMed ID: 10938014Lovejoy JC, de la Bretonne JA, Klemperer M, et al. Abdominal fat distribution and metabolic risk factors: effects of race. Metabolism 1996; 45: 1119-24.
PubMed ID: 8781299Hill JO, Sidney S, Lewis CE, et al. Racial differences in amounts of visceral adipose tissue in young adults: the CARDIA (Coronary Artery Risk Development in Young Adults) study. Am J Clin Nutr 1999; 69: 381-7.
PubMed ID: 10075320