Top

Journal of the International Society of Sports Nutrition

Published in:

Open Access 01-12-2014 | Review

Metabolic adaptation to weight loss: implications for the athlete

Authors: Eric T Trexler, Abbie E Smith-Ryan, Layne E Norton

Published in: Journal of the International Society of Sports Nutrition | Issue 1/2014

Abstract

Optimized body composition provides a competitive advantage in a variety of sports. Weight reduction is common among athletes aiming to improve their strength-to-mass ratio, locomotive efficiency, or aesthetic appearance. Energy restriction is accompanied by changes in circulating hormones, mitochondrial efficiency, and energy expenditure that serve to minimize the energy deficit, attenuate weight loss, and promote weight regain. The current article reviews the metabolic adaptations observed with weight reduction and provides recommendations for successful weight reduction and long term reduced-weight maintenance in athletes.

Available only for authorised users

Rossow LM, Fukuda DH, Fahs CA, Loenneke JP, Stout JR: Natural bodybuilding competition preparation and recovery: a 12-month case study. Int J Sports Physiol Perform. 2013, 8: 582-592.PubMed

Maestu J, Eliakim A, Jurimae J, Valter I, Jurimae T: Anabolic and catabolic hormones and energy balance of the male bodybuilders during the preparation for the competition. J Strength Cond Res. 2010, 24: 1074-1081. 10.1519/JSC.0b013e3181cb6fd3.CrossRefPubMed

Yoon J: Physiological profiles of elite senior wrestlers. Sports Med. 2002, 32: 225-233. 10.2165/00007256-200232040-00002.CrossRefPubMed

Franchini E, Del Vecchio FB, Matsushigue KA, Artioli GG: Physiological profiles of elite judo athletes. Sports Med. 2011, 41: 147-166. 10.2165/11538580-000000000-00000.CrossRefPubMed

Deutz RC, Benardot D, Martin DE, Cody MM: Relationship between energy deficits and body composition in elite female gymnasts and runners. Med Sci Sports Exerc. 2000, 32: 659-668.CrossRefPubMed

Wilmore JH, Brown CH, Davis JA: Body physique and composition of the female distance runner. Ann N Y Acad Sci. 1977, 301: 764-776. 10.1111/j.1749-6632.1977.tb38245.x.CrossRefPubMed

Dulloo AG, Jacquet J: Adaptive reduction in basal metabolic rate in response to food deprivation in humans: a role for feedback signals from fat stores. Am J Clin Nutr. 1998, 68: 599-606.PubMed

Maclean PS, Bergouignan A, Cornier MA, Jackman MR: Biology’s response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol. 2011, 301: R581-R600. 10.1152/ajpregu.00755.2010.PubMedCentralCrossRefPubMed

MacLean PS, Higgins JA, Jackman MR, Johnson GC, Fleming-Elder BK, Wyatt HR, Melanson EL, Hill JO: Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol. 2006, 290: R1577-R1588. 10.1152/ajpregu.00810.2005.CrossRefPubMed

10.

Maestu J, Jurimae J, Valter I, Jurimae T: Increases in ghrelin and decreases in leptin without altering adiponectin during extreme weight loss in male competitive bodybuilders. Metabolism. 2008, 57: 221-225. 10.1016/j.metabol.2007.09.004.CrossRefPubMed

11.

Lichtman SW, Pisarska K, Berman ER, Pestone M, Dowling H, Offenbacher E, Weisel H, Heshka S, Matthews DE, Heymsfield SB: Discrepancy between self-reported and actual caloric intake and exercise in obese subjects. N Engl J Med. 1992, 327: 1893-1898. 10.1056/NEJM199212313272701.CrossRefPubMed

12.

Garriguet D: Under-reporting of energy intake in the Canadian community health survey. Health Rep. 2008, 19: 37-45.PubMed

13.

Doucet E, St-Pierre S, Almeras N, Despres JP, Bouchard C, Tremblay A: Evidence for the existence of adaptive thermogenesis during weight loss. Br J Nutr. 2001, 85: 715-723. 10.1079/BJN2001348.CrossRefPubMed

14.

Rosenbaum M, Hirsch J, Gallagher DA, Leibel RL: Long-term persistence of adaptive thermogenesis in subjects who have maintained a reduced body weight. Am J Clin Nutr. 2008, 88: 906-912.PubMed

15.

Rosenbaum M, Leibel RL: Adaptive thermogenesis in humans. Int J Obes. 2010, 34 (Suppl 1): S47-S55.CrossRef

16.

Asami DK, McDonald RB, Hagopian K, Horwitz BA, Warman D, Hsiao A, Warden C, Ramsey JJ: Effect of aging, caloric restriction, and uncoupling protein 3 (UCP3) on mitochondrial proton leak in mice. Exp Gerontol. 2008, 43: 1069-1076. 10.1016/j.exger.2008.09.010.PubMedCentralCrossRefPubMed

17.

Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME: Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Regul Integr Comp Physiol. 2004, 286: E852-E861.

18.

Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME: Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab. 2005, 289: E429-E438. 10.1152/ajpendo.00435.2004.CrossRefPubMed

19.

Hagopian K, Harper ME, Ram JJ, Humble SJ, Weindruch R, Ramsey JJ: Long-term calorie restriction reduces proton leak and hydrogen peroxide production in liver mitochondria. Am J Physiol Endocrinol Metab. 2005, 288: E674-E684.CrossRefPubMed

20.

Kim B: Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid. 2008, 18: 141-144. 10.1089/thy.2007.0266.CrossRefPubMed

21.

Margetic S, Gazzola C, Pegg GG, Hill RA: Leptin: a review of its peripheral actions and interactions. Int J Obes Relat Metab Disord. 2002, 26: 1407-1433. 10.1038/sj.ijo.0802142.CrossRefPubMed

22.

Rooyackers OE, Nair KS: Hormonal regulation of human muscle protein metabolism. Annu Rev Nutr. 1997, 17: 457-485. 10.1146/annurev.nutr.17.1.457.CrossRefPubMed

23.

Strohacker K, McCaffery JM, Maclean PS, Wing RR: Adaptations of leptin, ghrelin or insulin during weight loss as predictors of weight regain: a review of current literature. Int J Obes. 2013, 1-9.http://www.nature.com/ijo/journal/vaop/ncurrent/full/ijo2013118a.html,

24.

Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Shirakami G, Usui T, Shimatsu A, Doi K, Hosoda H, Kojima M, Kangawa K, Nakao K: Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab. 2001, 86: 4753-4758. 10.1210/jcem.86.10.7885.CrossRefPubMed

25.

De Maddalena C, Vodo S, Petroni A, Aloisi AM: Impact of testosterone on body fat composition. J Cell Physiol. 2012, 227: 3744-3748. 10.1002/jcp.24096.CrossRefPubMed

26.

Simmons PS, Miles JM, Gerich JE, Haymond MW: Increased proteolysis. An effect of increases in plasma cortisol within the physiologic range. J Clin Invest. 1984, 73: 412-420. 10.1172/JCI111227.PubMedCentralCrossRefPubMed

27.

Zakrzewska KE, Cusin I, Sainsbury A, Rohner-Jeanrenaud F, Jeanrenaud B: Glucocorticoids as counterregulatory hormones of leptin: toward an understanding of leptin resistance. Diabetes. 1997, 46: 717-719. 10.2337/diab.46.4.717.CrossRefPubMed

28.

Hagmar M, Berglund B, Brismar K, Hirschberg AL: Body composition and endocrine profile of male Olympic athletes striving for leanness. Clin J Sport Med. 2013, 23: 197-201. 10.1097/JSM.0b013e31827a8809.CrossRefPubMed

29.

Weyer C, Walford RL, Harper IT, Milner M, MacCallum T, Tataranni PA, Ravussin E: Energy metabolism after 2 y of energy restriction: the biosphere 2 experiment. Am J Clin Nutr. 2000, 72: 946-953.PubMed

30.

Witbracht MG, Laugero KD, Van Loan MD, Adams SH, Keim NL: Performance on the Iowa gambling task is related to magnitude of weight loss and salivary cortisol in a diet-induced weight loss intervention in overweight women. Physiol Behav. 2012, 106: 291-297. 10.1016/j.physbeh.2011.04.035.CrossRefPubMed

31.

Tomiyama AJ, Mann T, Vinas D, Hunger JM, Dejager J, Taylor SE: Low calorie dieting increases cortisol. Psychosom Med. 2010, 72: 357-364. 10.1097/PSY.0b013e3181d9523c.PubMedCentralCrossRefPubMed

32.

Sumithran P, Prendergast LA, Delbridge E, Purcell K, Shulkes A, Kriketos A, Proietto J: Long-term persistence of hormonal adaptations to weight loss. N Engl J Med. 2011, 365: 1597-1604. 10.1056/NEJMoa1105816.CrossRefPubMed

33.

Rosenbaum M, Goldsmith R, Bloomfield D, Magnano A, Weimer L, Heymsfield S, Gallagher D, Mayer L, Murphy E, Leibel RL: Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Invest. 2005, 115: 3579-3586. 10.1172/JCI25977.PubMedCentralCrossRefPubMed

34.

Bryner RW, Ullrich IH, Sauers J, Donley D, Hornsby G, Kolar M, Yeater R: Effects of resistance vs. aerobic training combined with an 800 calorie liquid diet on lean body mass and resting metabolic rate. J Am Coll Nutr. 1999, 18: 115-121. 10.1080/07315724.1999.10718838.CrossRefPubMed

35.

Mettler S, Mitchell N, Tipton KD: Increased protein intake reduces lean body mass loss during weight loss in athletes. Med Sci Sports Exerc. 2010, 42: 326-337.CrossRefPubMed

36.

Layman DK, Boileau RA, Erickson DJ, Painter JE, Shiue H, Sather C, Christou DD: A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. J Nutr. 2003, 133: 411-417.PubMed

37.

Bopp MJ, Houston DK, Lenchik L, Easter L, Kritchevsky SB, Nicklas BJ: Lean mass loss is associated with low protein intake during dietary-induced weight loss in postmenopausal women. J Am Diet Assoc. 2008, 108: 1216-1220. 10.1016/j.jada.2008.04.017.PubMedCentralCrossRefPubMed

38.

Ravussin E, Burnand B, Schutz Y, Jequier E: Energy expenditure before and during energy restriction in obese patients. Am J Clin Nutr. 1985, 41: 753-759.PubMed

39.

Leibel RL, Rosenbaum M, Hirsch J: Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995, 332: 621-628. 10.1056/NEJM199503093321001.CrossRefPubMed

40.

Weigle DS: Contribution of decreased body mass to diminished thermic effect of exercise in reduced-obese men. Int J Obes. 1988, 12: 567-578.PubMed

41.

Weigle DS, Brunzell JD: Assessment of energy expenditure in ambulatory reduced-obese subjects by the techniques of weight stabilization and exogenous weight replacement. Int J Obes. 1990, 14 (Suppl 1): 69-77. discussion 77–81PubMed

42.

Doucet E, Imbeault P, St-Pierre S, Almeras N, Mauriege P, Despres JP, Bouchard C, Tremblay A: Greater than predicted decrease in energy expenditure during exercise after body weight loss in obese men. Clin Sci. 2003, 105: 89-95. 10.1042/CS20020252.CrossRefPubMed

43.

Rosenbaum M, Vandenborne K, Goldsmith R, Simoneau JA, Heymsfield S, Joanisse DR, Hirsch J, Murphy E, Matthews D, Segal KR, Leibel RL: Effects of experimental weight perturbation on skeletal muscle work efficiency in human subjects. Am J Physiol Regul Integr Comp Physiol. 2003, 285: R183-192.CrossRefPubMed

44.

Tappy L: Thermic effect of food and sympathetic nervous system activity in humans. Reprod Nutr Dev. 1996, 36: 391-397. 10.1051/rnd:19960405.CrossRefPubMed

45.

Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C: Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986, 78: 1568-1578. 10.1172/JCI112749.PubMedCentralCrossRefPubMed

46.

Miles CW, Wong NP, Rumpler WV, Conway J: Effect of circadian variation in energy expenditure, within-subject variation and weight reduction on thermic effect of food. Eur J Clin Nutr. 1993, 47: 274-284.PubMed

47.

Levine JA: Non-exercise activity thermogenesis (NEAT). Best Pract Res Clin Endocrinol Metab. 2002, 16: 679-702. 10.1053/beem.2002.0227.CrossRefPubMed

48.

Leibel RL, Hirsch J: Diminished energy requirements in reduced-obese patients. Metabolism. 1984, 33: 164-170. 10.1016/0026-0495(84)90130-6.CrossRefPubMed

49.

Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD: Mitochondrial proton and electron leaks. Essays Biochem. 2010, 47: 53-67. 10.1042/bse0470053.PubMedCentralCrossRefPubMed

50.

Rolfe DF, Brand MD: Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol. 1996, 271: C1380-1389.PubMed

51.

Rolfe DF, Brown GC: Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 1997, 77: 731-758.PubMed

52.

Rolfe DF, Newman JM, Buckingham JA, Clark MG, Brand MD: Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol. 1999, 276: C692-699.PubMed

53.

Thrush AB, Dent R, McPherson R, Harper ME: Implications of mitochondrial uncoupling in skeletal muscle in the development and treatment of obesity. FEBS J. 2013, 280: 5015-5029. 10.1111/febs.12399.CrossRefPubMed

54.

Zurlo F, Larson K, Bogardus C, Ravussin E: Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest. 1990, 86: 1423-1427. 10.1172/JCI114857.PubMedCentralCrossRefPubMed

55.

Esterbauer H, Oberkofler H, Dallinger G, Breban D, Hell E, Krempler F, Patsch W: Uncoupling protein-3 gene expression: reduced skeletal muscle mRNA in obese humans during pronounced weight loss. Diabetologia. 1999, 42: 302-309. 10.1007/s001250051155.CrossRefPubMed

56.

Vidal-Puig A, Rosenbaum M, Considine RC, Leibel RL, Dohm GL, Lowell BB: Effects of obesity and stable weight reduction on UCP2 and UCP3 gene expression in humans. Obes Res. 1999, 7: 133-140. 10.1002/j.1550-8528.1999.tb00694.x.CrossRefPubMed

57.

Schrauwen P, Xia J, Bogardus C, Pratley RE, Ravussin E: Skeletal muscle uncoupling protein 3 expression is a determinant of energy expenditure in Pima Indians. Diabetes. 1999, 48: 146-149. 10.2337/diabetes.48.1.146.CrossRefPubMed

58.

Harper ME, Dent RM, Bezaire V, Antoniou A, Gauthier A, Monemdjou S, McPherson R: UCP3 and its putative function: consistencies and controversies. Biochem Soc Trans. 2001, 29: 768-773. 10.1042/BST0290768.CrossRefPubMed

59.

Cannon B, Nedergaard J: Brown adipose tissue: function and physiological significance. Physiol Rev. 2004, 84: 277-359. 10.1152/physrev.00015.2003.CrossRefPubMed

60.

Rothwell NJ, Stock MJ: Effect of chronic food restriction on energy balance, thermogenic capacity, and brown-adipose-tissue activity in the rat. Biosci Rep. 1982, 2: 543-549. 10.1007/BF01314214.CrossRefPubMed

61.

Young JB, Saville E, Rothwell NJ, Stock MJ, Landsberg L: Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. J Clin Invest. 1982, 69: 1061-1071. 10.1172/JCI110541.PubMedCentralCrossRefPubMed

62.

Harper ME, Brand MD: The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem. 1993, 268: 14850-14860.PubMed

63.

Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR: Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009, 360: 1509-1517. 10.1056/NEJMoa0810780.PubMedCentralCrossRefPubMed

64.

Valle A, Catala-Niell A, Colom B, Garcia-Palmer FJ, Oliver J, Roca P: Sex-related differences in energy balance in response to caloric restriction. Am J Physiol Endocrinol Metab. 2005, 289: E15-22. 10.1152/ajpendo.00553.2004.CrossRefPubMed

65.

Harper ME, Dent R, Monemdjou S, Bezaire V, Van Wyck L, Wells G, Kavaslar GN, Gauthier A, Tesson F, McPherson R: Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes. 2002, 51: 2459-2466. 10.2337/diabetes.51.8.2459.CrossRefPubMed

66.

Chaston TB, Dixon JB, O’Brien PE: Changes in fat-free mass during significant weight loss: a systematic review. Int J Obes. 2007, 31: 743-750.

67.

Garthe I, Raastad T, Refsnes PE, Koivisto A, Sundgot-Borgen J: Effect of two different weight-loss rates on body composition and strength and power-related performance in elite athletes. Int J Sport Nutr Exerc Metab. 2011, 21: 97-104.PubMed

68.

Rodriguez NR, Di Marco NM, Langley S, American Dietetic A, Dietitians of C, American College of Sports M: American College of Sports Medicine position stand. Nutrition and athletic performance. Med Sci Sports Exerc. 2009, 41: 709-731.CrossRefPubMed

69.

Burke LM, Loucks AB, Broad N: Energy and carbohydrate for training and recovery. J Sports Sci. 2006, 24: 675-685. 10.1080/02640410500482602.CrossRefPubMed

70.

Paddon-Jones D, Westman E, Mattes RD, Wolfe RR, Astrup A, Westerterp-Plantenga M: Protein, weight management, and satiety. Am J Clin Nutr. 2008, 87: 1558S-1561S.PubMed

71.

Dirlewanger M, di Vetta V, Guenat E, Battilana P, Seematter G, Schneiter P, Jequier E, Tappy L: Effects of short-term carbohydrate or fat overfeeding on energy expenditure and plasma leptin concentrations in healthy female subjects. Int J Obes Relat Metab Disord. 2000, 24: 1413-1418. 10.1038/sj.ijo.0801395.CrossRefPubMed

72.

Chin-Chance C, Polonsky KS, Schoeller DA: Twenty-four-hour leptin levels respond to cumulative short-term energy imbalance and predict subsequent intake. J Clin Endocrinol Metab. 2000, 85: 2685-2691.PubMed

73.

Jenkins AB, Markovic TP, Fleury A, Campbell LV: Carbohydrate intake and short-term regulation of leptin in humans. Diabetologia. 1997, 40: 348-351. 10.1007/s001250050686.CrossRefPubMed

74.

Dulloo AG, Jacquet J, Girardier L: Poststarvation hyperphagia and body fat overshooting in humans: a role for feedback signals from lean and fat tissues. Am J Clin Nutr. 1997, 65: 717-723.PubMed

75.

Dulloo AG, Jacquet J, Montani JP: How dieting makes some fatter: from a perspective of human body composition autoregulation. Proc Nutr Soc. 2012, 71: 379-389. 10.1017/S0029665112000225.CrossRefPubMed

76.

Jackman MR, Steig A, Higgins JA, Johnson GC, Fleming-Elder BK, Bessesen DH, MacLean PS: Weight regain after sustained weight reduction is accompanied by suppressed oxidation of dietary fat and adipocyte hyperplasia. Am J Physiol Regul Integr Comp Physiol. 2008, 294: R1117-1129. 10.1152/ajpregu.00808.2007.CrossRefPubMed

77.

Saarni SE, Rissanen A, Sarna S, Koskenvuo M, Kaprio J: Weight cycling of athletes and subsequent weight gain in middleage. Int J Obes. 2006, 30: 1639-1644. 10.1038/sj.ijo.0803325.CrossRef

Title: Metabolic adaptation to weight loss: implications for the athlete
Authors: Eric T Trexler
Abbie E Smith-Ryan
Layne E Norton
Publication date: 01-12-2014
Publisher: BioMed Central
Published in: Journal of the International Society of Sports Nutrition / Issue 1/2014
Electronic ISSN: 1550-2783
DOI: https://doi.org/10.1186/1550-2783-11-7

At a glance: The STEP trials

Springer Medicine

Metabolic adaptation to weight loss: implications for the athlete

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2014

Amino acid supplementation and impact on immune function in the context of exercise

β-alanine supplementation improves tactical performance but not cognitive function in combat soldiers

Effects of short-term ingestion of Russian Tarragon prior to creatine monohydrate supplementation on whole body and muscle creatine retention and anaerobic sprint capacity: a preliminary investigation

Protective effect of a hydroethanolic extract from Bowdichia virgilioides on muscular damage and oxidative stress caused by strenuous resistance training in rats

Relationships between body image, nutritional supplement use, and attitudes towards doping in sport among adolescent boys: implications for prevention programs

Effects of energy drink major bioactive compounds on the performance of young adults in fitness and cognitive tests: a randomized controlled trial