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Allometric relationship between changes of visceral fat and total fat mass

International Journal of Obesity volume 32, pages 845–852 (2008)Cite this article

Abstract

Objective:

To elucidate the mathematical relationship between changes of visceral adipose tissue (VAT) and total body fat mass (FM) during weight loss.

Design:

We hypothesized that changes of VAT mass are allometrically related to changes of FM, regardless of the type of weight-loss intervention, as defined by the differential equation dVAT/dFM=k × VAT/FM, where k is a dimensionless constant. We performed a systematic search of the published literature for studies that included measurements of VAT changes via magnetic resonance imaging (MRI) or computed tomography (CT) imaging along with measurements of FM changes by dual-energy X-ray absorptiometry, hydrodensitometry, air-displacement plethysmography or whole-body MRI or CT imaging. We then examined whether or not the data could be explained by the allometric model.

Result:

We found 37 published studies satisfying our search criteria, representing 1407 men and women of various ethnicities, degrees of adiposity and weight-loss interventions. The hypothesized allometric equation relating changes of VAT and FM accurately modeled the data for both men and women and for all methods of weight loss studied. The best-fit value for the dimensionless constant was k=1.3±0.1 and the resulting model had an R2=0.73.

Conclusion:

This is the first report to reveal an allometric relationship between changes of VAT and FM that holds for both genders as well as a wide variety of weight-loss interventions including bariatric surgery, caloric restriction with or without exercise and exercise alone. We conclude that changes of VAT are primarily determined by FM changes as well as the initial VAT to FM ratio.

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References

  1. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 2007; 116: 39–48.

    Article  PubMed  Google Scholar 

  2. Bjorntorp P . ‘Portal’ adipose tissue as a generator of risk factors for cardiovascular disease and diabetes. Arteriosclerosis 1990; 10: 493–496.

    Article  CAS  PubMed  Google Scholar 

  3. Despres JP, Lemieux I . Abdominal obesity and metabolic syndrome. Nature 2006; 444: 881–887.

    Article  CAS  PubMed  Google Scholar 

  4. Wajchenberg BL . Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697–738.

    Article  CAS  PubMed  Google Scholar 

  5. Smith SR, Zachwieja JJ . Visceral adipose tissue: a critical review of intervention strategies. Int J Obes Relat Metab Disord 1999; 23: 329–335.

    Article  CAS  PubMed  Google Scholar 

  6. Huxley J . Problems of Relative Growth. Methuen & Co. Ltd.: London, 1932.

    Google Scholar 

  7. Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J et al. Visceral adipose tissue: relations between single-slice areas and total volume. Am J Clin Nutr 2004; 80: 271–278.

    Article  CAS  PubMed  Google Scholar 

  8. Brett MT . When is a correlation between non-independent variables ‘spurious’? OIKOS 2004; 105: 647–656.

    Article  Google Scholar 

  9. Brochu M, Tchernof A, Turner AN, Ades PA, Poehlman ET . Is there a threshold of visceral fat loss that improves the metabolic profile in obese postmenopausal women? Metab Clin Exp 2003; 52: 599–604.

    Article  CAS  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. 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.

    CAS  PubMed  Google Scholar 

  12. 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.

    CAS  PubMed  Google Scholar 

  13. Doucet E, St-Pierre S, Almeras N, Mauriege P, Despres JP, Richard D et al. Fasting insulin levels influence plasma leptin levels independently from the contribution of adiposity: evidence from both a cross-sectional and an intervention study. J Clin Endocrinol Metab 2000; 85: 4231–4237.

    CAS  PubMed  Google Scholar 

  14. Doucet E, St-Pierre S, Almeras N, Imbeault P, Mauriege P, Pascot A et al. Reduction of visceral adipose tissue during weight loss. Eur J Clin Nutr 2002; 56: 297–304.

    Article  CAS  PubMed  Google Scholar 

  15. Engelson ES, Agin D, Kenya S, Werber-Zion G, Luty B, Albu JB et al. Body composition and metabolic effects of a diet and exercise weight loss regimen on obese, HIV-infected women. Metab Clin Exp 2006; 55: 1327–1336.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. Gletsu N, Lin E, Khaitan L, Lynch SA, Ramshaw B, Raziano R et al. Changes in C-reactive protein predict insulin sensitivity in severely obese individuals after weight loss surgery. J Gastrointest Surg 2005; 9: 1119–1126; discussion 1127–1118.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. 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.

    Article  CAS  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  Google Scholar 

  23. Larson-Meyer DE, Heilbronn LK, Redman LM, Newcomer BR, Frisard MI, Anton S 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: 1337–1344.

    Article  PubMed  Google Scholar 

  24. Lin E, Phillips LS, Ziegler TR, Schmotzer B, Wu K, Gu LH et al. Increases in adiponectin predict improved liver, but not peripheral, insulin sensitivity in severely obese women during weight loss. Diabetes 2007; 56: 735–742.

    Article  CAS  PubMed  Google Scholar 

  25. Lynch NA, Nicklas BJ, Berman DM, Dennis KE, Goldberg AP . Reductions in visceral fat during weight loss and walking are associated with improvements in VO(2 max). J Appl Physiol 2001; 90: 99–104.

    Article  CAS  PubMed  Google Scholar 

  26. 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 2003; 58: 181–189.

    Article  Google Scholar 

  27. 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.

    Article  PubMed  Google Scholar 

  28. 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.

    Article  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. Redman LM, Heilbronn LK, Martin CK, Alfonso A, Smith SR, Ravussin E . Effect of calorie restriction with or without exercise on body composition and fat distribution. J Clin Endocrinol Metab 2007; 92: 865–872.

    Article  CAS  PubMed  Google Scholar 

  31. 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.

    Article  CAS  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. Ross R, Rissanen J, Pedwell H, Clifford J, Shragge P . Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. J Appl Physiol 1996; 81: 2445–2455.

    Article  CAS  PubMed  Google Scholar 

  34. Ross R, Rissanen J, Hudson R . Sensitivity associated with the identification of visceral adipose tissue levels using waist circumference in men and women: effects of weight loss. Int J Obes Relat Metab Disord 1996; 20: 533–538.

    CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. 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.

    Article  PubMed  Google Scholar 

  37. Ryan AS, Nicklas BJ . Reductions in plasma cytokine levels with weight loss improve insulin sensitivity in overweight and obese postmenopausal women. Diabetes Care 2004; 27: 1699–1705.

    Article  PubMed  Google Scholar 

  38. Ryan AS, Nicklas BJ, Berman DM . Aerobic exercise is necessary to improve glucose utilization with moderate weight loss in women. Obesity (Silver Spring) 2006; 14: 1064–1072.

    Article  CAS  Google Scholar 

  39. Santosa S, Demonty I, Lichtenstein AH, Jones PJ . Cholesterol metabolism and body composition in women: the effects of moderate weight loss. Int J Obes 2007; 31: 933–941.

    Article  CAS  Google Scholar 

  40. Shadid S, Jensen MD . Effects of pioglitazone versus diet and exercise on metabolic health and fat distribution in upper body obesity. Diabetes Care 2003; 26: 3148–3152.

    Article  CAS  PubMed  Google Scholar 

  41. 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.

    Article  CAS  PubMed  Google Scholar 

  42. Thamer C, Machann J, Stefan N, Haap M, Schafer S, Brenner S et al. High visceral fat mass and high liver fat are associated with resistance to lifestyle intervention. Obesity (Silver Spring) 2007; 15: 531–538.

    Article  Google Scholar 

  43. 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 2000; 279: E307–313.

    CAS  Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Article  CAS  PubMed  Google Scholar 

  46. Press W, Flannery B, Teukolsky S, Vetterling W . Numerical Recipes: the Art of Scientific Computing. Cambridge University Press: New York, 1986.

    Google Scholar 

  47. Mauriege P, Marette A, Atgie C, Bouchard C, Theriault G, Bukowiecki LK et al. Regional variation in adipose tissue metabolism of severely obese premenopausal women. J Lipid Res 1995; 36: 672–684.

    CAS  PubMed  Google Scholar 

  48. Mittelman SD, Van Citters GW, Kirkman EL, Bergman RN . Extreme insulin resistance of the central adipose depot in vivo. Diabetes 2002; 51: 755–761.

    Article  CAS  PubMed  Google Scholar 

  49. Sniderman AD, Bhopal R, Prabhakaran D, Sarrafzadegan N, Tchernof A . Why might South Asians be so susceptible to central obesity and its atherogenic consequences? The adipose tissue overflow hypothesis. Int J Epidemiol 2007; 36: 220–225.

    Article  PubMed  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. Mayer L, Walsh BT, Pierson Jr RN, Heymsfield SB, Gallagher D, Wang J et al. Body fat redistribution after weight gain in women with anorexia nervosa. Am J Clin Nutr 2005; 81: 1286–1291.

    Article  CAS  PubMed  Google Scholar 

  52. Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G et al. The response to long-term overfeeding in identical twins. N Engl J Med 1990; 322: 1477–1482.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Vipul Periwal for his suggestions regarding the Monte-Carlo simulations, Wei Shen for providing us with unpublished regression equations for translating single slice CT images to VAT volumes and Carson Chow, Nick Knuth and Daniel Holmes for their insightful comments on the manuscript. This work was supported in part by the Intramural Research Program of the National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. CEH was supported by the European Union through the Network of Excellence BioSim, Contract No. LSHB-CT-2004-005137, and the Danish Ministry of Science Technology and Innovation and Novo Nordisk, CORA through the Industrial PhD Initiative.

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Authors and Affiliations

  1. Department of Physics, Technical University of Denmark, Kongens Lyngby, Denmark

    C E Hallgreen

  2. Laboratory of Biological Modeling, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA

    K D Hall

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  1. C E Hallgreen
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Correspondence to K D Hall.

Appendix

Appendix

We hypothesized that the VAT and FM changes are allometrically related according to the following differential equation involving the infinitesimal changes dVAT and dFM:

However, only macroscopic changes ΔVAT and ΔFM can be measured, so we must therefore determine the expected relationship for macroscopic changes ΔVAT and ΔFM if the system is described by the allometric equation. Equation (A1) has the general solution:

Therefore, a macroscopic change of VAT is given by

Using the binomial expansion we obtain

Therefore,

ΔFM is typically small compared with FM, and for the data examined in this study ΔFM/FM=−0.2±0.08. Therefore, the sum contains terms that become progressively smaller and the first term of the sum is proportional to ∣ΔFM/FM2∣≪1. Therefore, the allometric equation is well approximated by the relationship studied in the present report:

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Hallgreen, C., Hall, K. Allometric relationship between changes of visceral fat and total fat mass. Int J Obes 32, 845–852 (2008). https://doi.org/10.1038/sj.ijo.0803783

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