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  • Original Article
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Insulin and extremity muscle mass in overweight and obese women

Abstract

Background:

Obesity disproportionately affects women, especially those of African descent, and is associated with increases in both fat and muscle masses.

Objective:

Although increased extremity muscle mass may be compensatory to fat mass load, we propose that elevated insulin levels resulting from diminished insulin sensitivity may additionally contribute to extremity muscle mass in overweight or obese women.

Methods:

The following measurements were performed in 197 non-diabetic women (57% black, 35% white; age 46±11 years (mean±s.d.), body mass index (BMI) range 25.0–57.7 kg m−2): dual-energy X-ray absorptiometry for fat and extremity muscle masses; exercise performance by duration and peak oxygen consumption (VO2 peak) during graded treadmill exercise; fasting insulin and, in 183 subjects, insulin sensitivity index (SI) calculated from the minimal model.

Results:

SI (range 0.5–14.1 l mU−1min−1) was negatively, and fasting insulin (range 1.9–35.6 μU ml−1) positively associated with extremity muscle mass (both P<0.001), independent of age and height. Sixty-seven percent of women completed 6 months of participation in a weight loss and exercise program: we found a significant association between reduction in fasting insulin and a decrease in extremity muscle mass (P=0.038), independent of reduction in fat mass or improvement in exercise performance by VO2 peak and exercise duration, and without association with change in SI or interaction by race.

Conclusions:

Hyperinsulinemia in overweight or obese women is associated with increased extremity muscle mass, which is partially reversible with reduction in fasting insulin concentration, consistent with the stimulatory effects of insulin on skeletal muscle.

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References

  1. Wilson PW, D’Agostino RB, Sullivan L, Parise H, Kannel WB . Overweight and obesity as determinants of cardiovascular risk: the Framingham experience. Arch Intern Med 2002; 162: 1867–1872.

    Article  Google Scholar 

  2. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX et al. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2006; 113: 898–918.

    Article  Google Scholar 

  3. Jensen MK, Chiuve SE, Rimm EB, Dethlefsen C, Tjønneland A, Joensen AM et al. Obesity, behavioral lifestyle factors and risk of acute coronary events. Circulation 2008; 117: 3062–3069.

    Article  Google Scholar 

  4. Flegal KM, Carroll MD, Ogden CL, Curtin LR . Prevalence and trends in obesity among US adults 1999-2008. JAMA 2010; 303: 235–241.

    Article  CAS  Google Scholar 

  5. Albu JB, Kovera AJ, Allen L, Wainwright M, Berk E, Raja-Khan N et al. Independent association of insulin resistance with larger amounts of intermuscular adipose tissue and a greater acute insulin response to glucose in African American than in white nondiabetic women. Am J Clin Nutr 2005; 82: 1210–1217.

    Article  CAS  Google Scholar 

  6. Kimball SR, Farrell PA, Jefferson LS . Invited review: role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise. J Appl Physiol 2002; 93: 1168–1180.

    Article  CAS  Google Scholar 

  7. Prod’homme M, Balage M, Debras E, Farges MC, Kimball S, Jefferson L et al. Differential effects of insulin and dietary amino acids on muscle protein synthesis in adult and old rats. J Physiol 2005; 563: 235–248.

    Article  Google Scholar 

  8. Glass DJ . Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 2003; 5: 87–90.

    Article  CAS  Google Scholar 

  9. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI . Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004; 350: 664–671.

    Article  CAS  Google Scholar 

  10. Ortiz O, Russell M, Daley TL, Baumgartner RN, Waki M, Lichtman S et al. Differences in skeletal muscle mass and bone mineral mass between black and white females and their relevance to estimates of body composition. Am J Clin Nutr 1992; 55: 8–13.

    Article  CAS  Google Scholar 

  11. United States Department of Agriculture. USDA's MyPlate 2011, 〈http://www.choosemyplate.gov/〉.

  12. United States Department of Agriculture. Dietary Guidelines for Americans 2011, 〈http://www.health.gov/dietaryguidelines/〉.

  13. Rothney MP, Brychta RJ, Schaefer EV, Chen KY, Skarulis MC . Body composition measured by dual-energy X-ray absorptiometry half-body scans in obese adults. Obesity 2009; 17: 1281–1286.

    PubMed  Google Scholar 

  14. Sumner AE, Luercio MF, Frempong BA, Ricks M, Sen S, Kushner H et al. Validity of the reduced-sample-insulin-modified-frequently sampled intravenous glucose tolerance test using the nonlinear regression approach. Metabolism 2009; 58: 220–225.

    Article  CAS  Google Scholar 

  15. Boston RC, Stefanovski D, Moate PJ, Sumner AE, Watanabe RM, Bergman RN . MINMOD Millennium: A computer program to calculate glucose effectiveness and insulin sensitivity from the frequently sampled intravenous glucose tolerance test. Diabetes Technol Ther 2003; 5: 1003–1015.

    Article  CAS  Google Scholar 

  16. Durheim MT, Slentz CA, Bateman LA, Mabe SK, Kraus WE . Relationships between exercise-induced reductions in thigh intermuscular adipose tissue, changes in lipoprotein particle size, and visceral adiposity. Am J Physiol Endocrinol Metab 2008; 295: E407–E412.

    Article  CAS  Google Scholar 

  17. Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, Schwartz AV et al. Decreased muscle strength and quality in older adults with type 2 diabetes. The Health, Aging, and Body Composition Study. Diabetes 2006; 55: 1813–1818.

    Article  CAS  Google Scholar 

  18. Gallagher D, Visser M, De Meersman RE, Sepúlveda D, Baumgartner RN, Pierson RN et al. Appendicular skeletal muscle mass: effects of age, gender and ethnicity. J Appl Physiol 1997; 83: 229–239.

    Article  CAS  Google Scholar 

  19. Houmard JA, O’Neill DS, Zheng D, Hickey MS, Dohm GL . Impact of hyperinsulinemia on myosin heavy chain gene regulation. J Appl Physiol 1999; 86: 1828–1832.

    Article  CAS  Google Scholar 

  20. Lam CS, Chen MH, Lacey SM, Yang Q, Sullivan LM, Xanthakis V et al. Circulating insulin-like growth factor-1 and its binding protein-3: metabolic and genetic correlates in the community. Arterioscler Thromb Vasc Biol 2010; 30: 1479–1484.

    Article  CAS  Google Scholar 

  21. Holmang A, Yoshida N, Jennische E, Waldenstrom A, Bjorntorp P . The effects of hyperinsulinemia on myocardial mass, blood pressure regulation and central hemodynamics in rats. Eur J Clin Invest 1996; 26: 973–978.

    Article  CAS  Google Scholar 

  22. Sitnick M, Bodine SC, Rutledge JC . Chronic high feeding attenuates load-induced hypertrophy in mice. J Physiol 2009; 587: 5753–5765.

    Article  CAS  Google Scholar 

  23. Katta A, Kundla S, Kakarla SK, Wu M, Fannin J, Paturi S et al. Impaired overload-induced hypertrophy is associated with diminished mTOR signaling in insulin-resistant skeletal muscle of the obese Zucker rat. Am J Physiol Regul Integr Comp Physiol 2010; 299: R1666–R1675.

    Article  CAS  Google Scholar 

  24. Ryan AS, Nicklas BJ, Berman DM . Racial differences in insulin resistance and mid-thigh fat deposition in postmenopausal women. Obes Res 2002; 10: 336–344.

    Article  Google Scholar 

  25. Ingram KH, Lara-Castro C, Gower BA, Makowsky R, Allison DB, Newcomer BR et al. Intramyocellular lipid and insulin resistance: differential relationships in European and African Americans. Obesity 2011; 19: 1469–1475.

    Article  CAS  Google Scholar 

  26. Holmang A, Brzezinska Z, Bjorntorp P . Effects of hyperinsulinemia on muscle fiber composition and capillarization in rats. Diabetes 1993; 42: 1073–1081.

    Article  CAS  Google Scholar 

  27. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR et al. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002; 282: E1191–E1196.

    Article  CAS  Google Scholar 

  28. Nyholm B, Qu Z, Kaal A, Pedersen SB, Gravholt CH, Andersen JL et al. Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 1997; 46: 1822–1828.

    Article  CAS  Google Scholar 

  29. Wang X, You T, Lenchik L, Nicklas BJ . Resting energy expenditure changes with weight loss: racial differences. Obesity 2010; 18: 86–91.

    Article  Google Scholar 

  30. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med 2011; 364: 1218–1229.

    Article  CAS  Google Scholar 

  31. Carty CL, Kooperberg C, Neuhouser ML, Tinker L, Howard B, Wactawski-Wende J et al. Low-fat dietary pattern and change in body-composition traits in the Women’s Health Initiative Dietary Modification Trial. Am J Clin Nutr 2011; 93: 516–524.

    Article  CAS  Google Scholar 

  32. Levine JA, Abboud L, Barry M, Reed JE, Sheedy PF, Jensen MD . Measuring leg muscle and fat mass in humans: comparison of CT and dual-energy X-ray absorptiometry. J Appl Physiol 2000; 88: 452–456.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the contributions of Janet Dejesus, Rachel Permuth-Levine, Nancy Sebring, Amber Courville, Rita Lapointe, Diane Dellavalle, Greg McMahon, Catherine Marinac, Rachel Perron, Chris Idelson and Megan Sabo to this study. This research was supported by the intramural research programs of the National Heart, Lung, and Blood Institute and the National Institute of Diabetes, and Digestive and Kidney Diseases, National Institutes of Health.

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Correspondence to R O Cannon III.

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Leon, B., Jenkins, S., Pepin, K. et al. Insulin and extremity muscle mass in overweight and obese women. Int J Obes 37, 1560–1564 (2013). https://doi.org/10.1038/ijo.2013.45

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