Abstract
Background:
Visceral adipose tissue (VAT) is associated with greater obesity-related metabolic disturbance. Many studies have reported preferential loss of VAT with weight loss.
Objective:
This systematic review looks for factors associated with preferential loss of VAT relative to subcutaneous abdominal fat (SAT) during weight loss.
Design:
Medline and Embase were searched for imaging-based measurements of VAT and subcutaneous abdominal adipose tissue (SAT) before and after weight loss interventions. We examine for factors that influences the percentage change in VAT versus SAT (%δV/%δS) with weight loss. Linear regression analyses were performed on the complete data set and on subgroups of studies. Factors examined included percentage weight loss, degree of caloric restriction, exercise, initial body mass index (BMI), gender, time of follow-up and baseline VAT/SAT.
Results:
There were 61 studies with a total of 98 cohort time points extracted. Percentage weight loss was the only variable that influenced %δV/%δS (r=−0.29, P=0.005). Modest weight loss generated preferential loss of VAT, but with greater weight loss this effect was attenuated. The method of weight loss was not an influence with one exception. Very-low-calorie diets (VLCDs) provided exceptional short-term (<4 weeks) preferential VAT loss. But this effect was lost by 12–14 weeks.
Conclusions:
Visceral adipose tissue is lost preferentially with modest weight loss, but the effect is attenuated with greater weight loss. Acute caloric restriction, using VLCD, produces early preferential loss of VAT. These observations may help to explain the metabolic benefits of modest weight loss.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Murphy EJ . Stable isotope methods for the in vivo measurement of lipogenesis and triglyceride metabolism. J Anim Sci 2006; 84 (Suppl): E94–E104.
Matsuzawa Y . The metabolic syndrome and adipocytokines. FEBS Lett 2006; 580: 2917–2921.
Bousquet-Melou A, Galitzky J, Lafontan M, Berlan M . Control of lipolysis in intra-abdominal fat cells of nonhuman primates: comparison with humans. J Lipid Res 1995; 36: 451–461.
Regitz-Zagrosek V, Lehmkuhl E, Weickert MO . Gender differences in the metabolic syndrome and their role for cardiovascular disease. Clin Res Cardiol 2006; 95: 136–147.
Arner P . Insulin resistance in type 2 diabetes: role of fatty acids. Diabetes Metab Res Rev 2002; 18 (Suppl 2): S5–S9.
Cancello R, Tordjman J, Poitou C, Guilhem G, Bouillot JL, Hugol D et al. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 2006; 55: 1554–1561.
Smith SR, Zachwieja JJ . Visceral adipose tissue: a critical review of intervention strategies. Int J Obes Relat Metab Disord 1999; 23: 329–335.
Okura T, Nakata Y, Tanaka K . Effects of exercise intensity on physical fitness and risk factors for coronary heart disease. Obes Res 2003; 11: 1131–1139.
Weinsier RL, Hunter GR, Gower BA, Schutz Y, Darnell BE, Zuckerman PA . Body fat distribution in white and black women: different patterns of intraabdominal and subcutaneous abdominal adipose tissue utilization with weight loss. Am J Clin Nutr 2001; 74: 631–636.
Purnell JQ, Kahn SE, Albers JJ, Nevin DN, Brunzell JD, Schwartz RS . Effect of weight loss with reduction of intra-abdominal fat on lipid metabolism in older men. J Clin Endocrinol Metab 2000; 85: 977–982.
Leenen R, van der Kooy K, Droop A, Seidell JC, Deurenberg P, Weststrate JA et al. Visceral fat loss measured by magnetic resonance imaging in relation to changes in serum lipid levels of obese men and women. Arterioscler Thromb 1993; 13: 487–494.
Leenen R, van der Kooy K, Seidell JC, Deurenberg P, Koppeschaar HP . Visceral fat accumulation in relation to sex hormones in obese men and women undergoing weight loss therapy. J Clin Endocrinol Metab 1994; 78: 1515–1520.
Kockx M, Leenen R, Seidell J, Princen HM, Kooistra T . Relationship between visceral fat and PAI-1 in overweight men and women before and after weight loss. Thromb Haemost 1999; 82: 1490–1496.
van der Kooy K, Leenen R, Seidell JC, Deurenberg P, Droop A, Bakker CJ . Waist–hip ratio is a poor predictor of changes in visceral fat. Am J Clin Nutr 1993; 57: 327–333.
Gower BA, Weinsier RL, Jordan JM, Hunter GR, Desmond R . Effects of weight loss on changes in insulin sensitivity and lipid concentrations in premenopausal African American and White women. Am J Clin Nutr 2002; 76: 923–927.
Pasquali R, Gambineri A, Biscotti D, Vicennati V, Gagliardi L, Colitta D et al. Effect of long-term treatment with metformin added to hypocaloric diet on body composition, fat distribution, and androgen and insulin levels in abdominally obese women with and without the polycystic ovary syndrome. J Clin Endocrinol Metab 2000; 85: 2767–2774.
Alvarez GE, Davy BM, Ballard TP, Beske SD, Davy KP . Weight loss increases cardiovagal baroreflex function in obese young and older men. Am J Physiol Endocrinol Metab 2005; 289: E665–E669.
Tiikkainen M, Bergholm R, Rissanen A, Aro A, Salminen I, Tamminen M et al. Effects of equal weight loss with orlistat and placebo on body fat and serum fatty acid composition and insulin resistance in obese women. Am J Clin Nutr 2004; 79: 22–30.
Okura T, Nakata Y, Lee DJ, Ohkawara K, Tanaka K . Effects of aerobic exercise and obesity phenotype on abdominal fat reduction in response to weight loss. Int J Obes (London) 2005; 29: 1259–1266.
van Rossum EF, Nicklas BJ, Dennis KE, Berman DM, Goldberg AP . Leptin responses to weight loss in postmenopausal women: relationship to sex-hormone binding globulin and visceral obesity. Obes Res 2000; 8: 29–35.
Tchernof A, Starling RD, Turner A, Shuldiner AR, Walston JD, Silver K et al. Impaired capacity to lose visceral adipose tissue during weight reduction in obese postmenopausal women with the Trp64Arg beta3-adrenoceptor gene variant. Diabetes 2000; 49: 1709–1713.
Rice B, Janssen I, Hudson R, Ross R . Effects of aerobic or resistance exercise and/or diet on glucose tolerance and plasma insulin levels in obese men. Diabetes Care 1999; 22: 684–691.
Weits T, van der Beek EJ, Wedel M, Hubben MW, Koppeschaar HP . Fat patterning during weight reduction: a multimode investigation. Neth J Med 1989; 35: 174–184.
Okura T, Tanaka K, Nakanishi T, Lee DJ, Nakata Y, Wee SW et al. Effects of obesity phenotype on coronary heart disease risk factors in response to weight loss. Obes Res 2002; 10: 757–766.
Fujioka S, Matsuzawa Y, Tokunaga K, Kawamoto T, Kobatake T, Keno Y et al. Improvement of glucose and lipid metabolism associated with selective reduction of intra-abdominal visceral fat in premenopausal women with visceral fat obesity. Int J Obes 1991; 15: 853–859.
Janssen I, Ross R . Effects of sex on the change in visceral, subcutaneous adipose tissue and skeletal muscle in response to weight loss. Int J Obes Relat Metab Disord 1999; 23: 1035–1046.
Tchernof A, Nolan A, Sites CK, Ades PA, Poehlman ET . Weight loss reduces C-reactive protein levels in obese postmenopausal women. Circulation 2002; 105: 564–569.
Thong FS, Hudson R, Ross R, Janssen I, Graham TE . Plasma leptin in moderately obese men: independent effects of weight loss and aerobic exercise. Am J Physiol Endocrinol Metab 2000; 279: E307–E313.
Kelley DE, Kuller LH, McKolanis TM, Harper P, Mancino J, Kalhan S . Effects of moderate weight loss and orlistat on insulin resistance, regional adiposity, and fatty acids in type 2 diabetes. Diabetes Care 2004; 27: 33–40.
Tiikkainen M, Bergholm R, Vehkavaara S, Rissanen A, Hakkinen AM, Tamminen M et al. Effects of identical weight loss on body composition and features of insulin resistance in obese women with high and low liver fat content. Diabetes 2003; 52: 701–707.
Ross R, Dagnone D, Jones PJ, Smith H, Paddags A, Hudson R 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.
Lovejoy JC, Bray GA, Greeson CS, Klemperer M, Morris J, Partington C et al. Oral anabolic steroid treatment, but not parenteral androgen treatment, decreases abdominal fat in obese, older men. Int J Obes Relat Metab Disord 1995; 19: 614–624.
Kanai H, Tokunaga K, Fujioka S, Yamashita S, Kameda-Takemura KK, Matsuzawa Y . Decrease in intra-abdominal visceral fat may reduce blood pressure in obese hypertensive women. Hypertension 1996; 27: 125–129.
Gambineri A, Pagotto U, Tschop M, Vicennati V, Manicardi E, Carcello A et al. Anti-androgen treatment increases circulating ghrelin levels in obese women with polycystic ovary syndrome. J Endocrinol Invest 2003; 26: 629–634.
Ross R, Janssen I, Dawson J, Kungl AM, Kuk JL, Wong SL et al. Exercise-induced reduction in obesity and insulin resistance in women: a randomized controlled trial. Obes Res 2004; 12: 789–798.
Nicklas BJ, Dennis KE, Berman DM, Sorkin J, Ryan AS, Goldberg AP . Lifestyle intervention of hypocaloric dieting and walking reduces abdominal obesity and improves coronary heart disease risk factors in obese, postmenopausal, African-American and Caucasian women. J Gerontol A Biol Sci Med Sci 2003; 58: 181–189.
Park HS, Sim SJ, Park JY . Effect of weight reduction on metabolic syndrome in Korean obese patients. J Korean Med Sci 2004; 19: 202–208.
Giannopoulou I, Ploutz-Snyder LL, Carhart R, Weinstock RS, Fernhall B, Goulopoulou S et al. Exercise is required for visceral fat loss in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 2005; 90: 1511–1518.
Ross R, Rissanen J . Mobilization of visceral and subcutaneous adipose tissue in response to energy restriction and exercise. Am J Clin Nutr 1994; 60: 695–703.
Nakamura M, Tanaka M, Kinukawa N, Abe S, Itoh K, Imai K et al. Association between basal serum and leptin levels and changes in abdominal fat distribution during weight loss. J Atheroscler Thromb 2000; 6: 28–32.
Park HS, Lee K . Greater beneficial effects of visceral fat reduction compared with subcutaneous fat reduction on parameters of the metabolic syndrome: a study of weight reduction programmes in subjects with visceral and subcutaneous obesity. Diabet Med 2005; 22: 266–272.
Pare A, Dumont M, Lemieux I, Brochu M, Almeras N, Lemieux S et al. Is the relationship between adipose tissue and waist girth altered by weight loss in obese men? Obes Res 2001; 9: 526–534.
Conway JM, Yanovski SZ, Avila NA, Hubbard VS . Visceral adipose tissue differences in black and white women. Am J Clin Nutr 1995; 61: 765–771.
Stallone DD, Stunkard AJ, Wadden TA, Foster GD, Boorstein J, Arger P . Weight loss and body fat distribution: a feasibility study using computed tomography. Int J Obes 1991; 15: 775–780.
Goodpaster BH, Kelley DE, Wing RR, Meier A, Thaete FL . Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 1999; 48: 839–847.
Laaksonen DE, Kainulainen S, Rissanen A, Niskanen L . Relationships between changes in abdominal fat distribution and insulin sensitivity during a very low calorie diet in abdominally obese men and women. Nutr Metab Cardiovasc Dis 2003; 13: 349–356.
Gray DS, Fujioka K, Colletti PM, Kim H, Devine W, Cuyegkeng T et al. Magnetic-resonance imaging used for determining fat distribution in obesity and diabetes. Am J Clin Nutr 1991; 54: 623–627.
Zamboni M, Armellini F, Turcato E, Todesco T, Bissoli L, Bergamo-Andreis IA et al. Effect of weight loss on regional body fat distribution in premenopausal women. Am J Clin Nutr 1993; 58: 29–34.
Bosello O, Zamboni M, Armellini F, Zocca I, Bergamo Andreis IA, Smacchia C et al. Modifications of abdominal fat and hepatic insulin clearance during severe caloric restriction. Ann Nutr Metab 1990; 34: 359–365.
Zamboni M, Armellini F, Turcato E, Micciolo R, Desideri S, Bergamo-Andreis IA et al. Effect of regain of body weight on regional body fat distribution: comparison between pre- and postmenopausal obese women. Obes Res 1996; 4: 555–560.
Chowdhury B, Kvist H, Andersson B, Bjorntorp P, Sjostrom L . CT-determined changes in adipose tissue distribution during a small weight reduction in obese males. Int J Obes Relat Metab Disord 1993; 17: 685–691.
De Pergola G, Zamboni M, Pannacciulli N, Turcato E, Giorgino F, Armellini F et al. Divergent effects of short-term, very-low-calorie diet on insulin-like growth factor-I and insulin-like growth factor binding protein-3 serum concentrations in premenopausal women with obesity. Obes Res 1998; 6: 408–415.
Ibanez J, Izquierdo M, Arguelles I, Forga L, Larrion JL, Garcia-Unciti M et al. Twice-weekly progressive resistance training decreases abdominal fat and improves insulin sensitivity in older men with type 2 diabetes. Diabetes Care 2005; 28: 662–667.
Irwin ML, Yasui Y, Ulrich CM, Bowen D, Rudolph RE, Schwartz RS et al. Effect of exercise on total and intra-abdominal body fat in postmenopausal women: a randomized controlled trial. JAMA 2003; 289: 323–330.
Savage PD, Brochu M, Poehlman ET, Ades PA . Reduction in obesity and coronary risk factors after high caloric exercise training in overweight coronary patients. Am Heart J 2003; 146: 317–323.
Miyatake N, Nishikawa H, Morishita A, Kunitomi M, Wada J, Suzuki H et al. Daily walking reduces visceral adipose tissue areas and improves insulin resistance in Japanese obese subjects. Diabetes Res Clin Pract 2002; 58: 101–107.
Despres JP, Pouliot MC, Moorjani S, Nadeau A, Tremblay A, Lupien PJ et al. Loss of abdominal fat and metabolic response to exercise training in obese women. Am J Physiol 1991; 261: E159–E167.
Mourier A, Gautier JF, De Kerviler E, Bigard AX, Villette JM, Garnier JP 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: 385–391.
Kim DM, Yoon SJ, Ahn CW, Cha BS, Lim SK, Kim KR et al. Sibutramine improves fat distribution and insulin resistance, and increases serum adiponectin levels in Korean obese nondiabetic premenopausal women. Diabetes Res Clin Pract 2004; 66 (Suppl 1): S139–S144.
Yip I, Go VL, Hershman JM, Wang HJ, Elashoff R, DeShields S et al. Insulin–leptin–visceral fat relation during weight loss. Pancreas 2001; 23: 197–203.
Kamel EG, McNeill G, Van Wijk MC . Change in intra-abdominal adipose tissue volume during weight loss in obese men and women: correlation between magnetic resonance imaging and anthropometric measurements. Int J Obes Relat Metab Disord 2000; 24: 607–613.
Busetto L, Perini P, Giantin V, Valente P, Segato G, Belluco C et al. Relationship between energy expenditure and visceral fat accumulation in obese women submitted to adjustable silicone gastric banding (ASGB). Int J Obes Relat Metab Disord 1995; 19: 227–233.
Phillips ML, Lewis MC, Chew V, Kow L, Slavotinek JP, Daniels L et al. The early effects of weight loss surgery on regional adiposity. Obes Surg 2005; 15: 1449–1455.
Busetto L, Tregnaghi A, Bussolotto M, Sergi G, Beninca P, Ceccon A et al. Visceral fat loss evaluated by total body magnetic resonance imaging in obese women operated with laparascopic adjustable silicone gastric banding. Int J Obes Relat Metab Disord 2000; 24: 60–69.
Busetto L, Tregnaghi A, De Marchi F, Segato G, Foletto M, Sergi G et al. Liver volume and visceral obesity in women with hepatic steatosis undergoing gastric banding. Obes Res 2002; 10: 408–411.
Jensen MD . Is visceral fat involved in the pathogenesis of the metabolic syndrome? Human model. Obesity (Silver Spring) 2006; 14 (Suppl 1): 20S–24S.
Janssen I, Fortier A, Hudson R, Ross R . 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: 431–438.
Kay SJ, Fiatarone Singh MA . The influence of physical activity on abdominal fat: a systematic review of the literature. Obes Rev 2006; 7: 183–200.
Thomas EL, Brynes AE, McCarthy J, Goldstone AP, Hajnal JV, Saeed N et al. Preferential loss of visceral fat following aerobic exercise, measured by magnetic resonance imaging. Lipids 2000; 35: 769–776.
Kabir M, Catalano KJ, Ananthnarayan S, Kim SP, Van Citters GW, Dea MK et al. Molecular evidence supporting the portal theory: a causative link between visceral adiposity and hepatic insulin resistance. Am J Physiol Endocrinol Metab 2005; 288: E454–E461.
Gasteyger C, Tremblay A . Metabolic impact of body fat distribution. J Endocrinol Invest 2002; 25: 876–883.
Schenk S, Goldenberg N, Horowitz JF . A single session of endurance exercise protects against fatty-acid induced insulin resistance: 644: 1:15 PM–1:30 PM. Med Sci Sports Exerc 2006; 38: S15–S16.
Siebler J, Galle PR . Treatment of nonalcoholic fatty liver disease. World J Gastroenterol 2006; 12: 2161–2167.
Swinburn BA, Nyomba BL, Saad MF, Zurlo F, Raz I, Knowler WC et al. Insulin resistance associated with lower rates of weight gain in Pima Indians. J Clin Invest 1991; 88: 168–173.
Poirier P, Despres JP . Exercise in weight management of obesity. Cardiol Clin 2001; 19: 459–470.
Drapeau V, Therrien F, Richard D, Tremblay A . Is visceral obesity a physiological adaptation to stress? Panminerva Med 2003; 45: 189–195.
Kreier F, Fliers E, Voshol PJ, Van Eden CG, Havekes LM, Kalsbeek A et al. Selective parasympathetic innervation of subcutaneous and intra-abdominal fat—functional implications. J Clin Invest 2002; 110: 1243–1250.
Arner P . Effects of testosterone on fat cell lipolysis. Species differences and possible role in polycystic ovarian syndrome. Biochimie 2005; 87: 39–43.
Arner P . Human fat cell lipolysis: biochemistry, regulation and clinical role. Best Pract Res Clin Endocrinol Metab 2005; 19: 471–482.
Nielsen S, Guo Z, Johnson CM, Hensrud DD, Jensen MD . Splanchnic lipolysis in human obesity. J Clin Invest 2004; 113: 1582–1588.
Acknowledgements
Timothy B Chaston—Contribution included design of the review, extraction of data, analysis of the data and writing the manuscript.
John B Dixon—Contribution included design of the review, assistance with the extraction of data, analysis of data and writing of the manuscript.
This study was funded by Monash University and there are no conflicts of interest to declare.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chaston, T., Dixon, J. Factors associated with percent change in visceral versus subcutaneous abdominal fat during weight loss: findings from a systematic review. Int J Obes 32, 619–628 (2008). https://doi.org/10.1038/sj.ijo.0803761
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.ijo.0803761
Keywords
This article is cited by
-
Role of obesity related inflammation in pathogenesis of peripheral artery disease in patients of type 2 diabetes mellitus
Journal of Diabetes & Metabolic Disorders (2023)
-
Comparisons of calorie restriction and structured exercise on reductions in visceral and abdominal subcutaneous adipose tissue: a systematic review
European Journal of Clinical Nutrition (2022)
-
Weight fluctuation, mortality, and cardiovascular disease in adults in 18 years of follow-up: Tehran Lipid and Glucose Study
Journal of Endocrinological Investigation (2022)
-
Prognostic significance of abdominal obesity and its post-diagnosis change in a Chinese breast cancer cohort
Breast Cancer Research and Treatment (2022)
-
Overweight, Obesity, and CVD Risk: a Focus on Visceral/Ectopic Fat
Current Atherosclerosis Reports (2022)