Metabolic adaptation is an illusion, only present when participants are in negative energy balance

Catia Martins, Jessica Roekenes, Saideh Salamati, Barbara A Gower, Gary R Hunter, Catia Martins, Jessica Roekenes, Saideh Salamati, Barbara A Gower, Gary R Hunter

Abstract

Background: The existence of metabolic adaptation, following weight loss, remains a controversial issue. To our knowledge, no study has evaluated the role of energy balance (EB) in modulating metabolic adaptation.

Objectives: The aim of this study was to determine if metabolic adaptation, at the level of resting metabolic rate (RMR), is modulated by participants' EB status. A secondary aim was to investigate if metabolic adaptation was associated with weight regain.

Methods: Seventy-one individuals with obesity (BMI: 34.6 ± 3.4 kg/m2; age: 45.4 ± 8.2 y; 33 men) enrolled in a 1000-kcal/d diet for 8 wk, followed by 4 wk of weight stabilization and a 9-mo weight loss maintenance program. Body weight/composition and RMR were measured at baseline, week 9 (W9), week 13 (W13), and 1 y (1Y). Metabolic adaptation was defined as a significantly different (lower or higher) measured compared with predicted RMR.

Results: Participants lost on average 14 kg by W9, followed by weight stabilization at W13, and regained 29% of their initial weight loss at 1Y. Metabolic adaptation was found at W9 (-92 ± 110 kcal/d, P < 0.001) and W13 (-38 ± 124 kcal/d, P = 0.011) but was not correlated with weight regain. A significant reduction in metabolic adaptation was seen between W9 and W13 (-53 ± 101 kcal/d, P < 0.001). In a subset of participants who gained weight between W9 and W13 (n = 33), no metabolic adaptation was seen at W13 (-26.8 ± 121.5 kcal/d, P = 0.214). In a subset of participants with data at all time points (n = 45), metabolic adaptation was present at W9 and W13 (-107 ± 102 kcal/d, P < 0.001 and -49 ± 128 kcal/d, P = 0.013) but not at 1Y (-7 ± 129, P = 0.701).

Conclusion: After weight loss, metabolic adaptation at the level of RMR is dependent on the EB status of the participants, being reduced to half after a period of weight stabilization. Moreover, metabolic adaptation does not predict weight regain at 1Y follow-up. These trials were registered at clinicaltrials.gov as NCT02944253 and NCT03287726.

Keywords: adaptive thermogenesis; metabolic adaptation; resting metabolic rate; weight loss; weight regain.

Copyright © The Author(s) on behalf of the American Society for Nutrition 2020.

Figures

FIGURE 1
FIGURE 1
Flowchart for the study.

References

    1. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332:621–8.
    1. 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(4):906–12.
    1. Froidevaux F, Schutz Y, Christin L, Jequier E. Energy expenditure in obese women before and during weight loss, after refeeding, and in the weight-relapse period. Am J Clin Nutr. 1993;57(1):35–42.
    1. Fothergill E, Guo J, Howard L, Kerns JC, Knuth ND, Brychta R, Chen KY, Skarulis MC, Walter M, Walter PJ et al. . Persistent metabolic adaptation 6 years after "The Biggest Loser" competition. Obesity. 2016;24(8):1612–19.
    1. Camps SG, Verhoef SP, Westerterp KR. Weight loss, weight maintenance, and adaptive thermogenesis. Am J Clin Nutr. 2013;97(5):990–4.
    1. Johannsen DL, Knuth ND, Huizenga R, Rood JC, Ravussin E, Hall KD. Metabolic slowing with massive weight loss despite preservation of fat-free mass. J Clin Endocrinol Metab. 2012;97(7):2489–96.
    1. Weinsier RL, Nagy TR, Hunter GR, Darnell BE, Hensrud DD, Weiss HL. Do adaptive changes in metabolic rate favor weight regain in weight-reduced individuals? An examination of the set-point theory. Am J Clin Nutr. 2000;72(5):1088–94.
    1. Weinsier RL, Hunter GR, Zuckerman PA, Darnell BE. Low resting and sleeping energy expenditure and fat use do not contribute to obesity in women. Obes Res. 2003;11(8):937–44.
    1. Wyatt HR, Grunwald GK, Seagle HM, Klem ML, McGuire MT, Wing RR, Hill JO. Resting energy expenditure in reduced-obese subjects in the National Weight Control Registry. Am J Clin Nutr. 1999;69(6):1189–93.
    1. Larson DE, Ferraro RT, Robertson DS, Ravus E. Energy metabolism in weight-stable postobese individuals. Am J Clin Nutr. 1995;62:735–9.
    1. Ostendorf DM, Melanson EL, Caldwell AE, Creasy SA, Pan Z, MacLean PS, Wyatt HR, Hill JO, Catenacci VA. No consistent evidence of a disproportionately low resting energy expenditure in long-term successful weight-loss maintainers. Am J Clin Nutr. 2018;108(4):658–66.
    1. Amatruda JM, Statt MC, Welle SL. Total and resting energy expenditure in obese women reduced to ideal body weight. J Clin Invest. 1993;92(3):1236–42.
    1. Dulloo AG, Jacquet J, Montani JP, Schutz Y. Adaptive thermogenesis in human body weight regulation: more of a concept than a measurable entity?. Obes Rev. 2012;13(Suppl 2):105–21.
    1. Dulloo AG, Schutz Y. Adaptive thermogenesis in resistance to obesity therapies: issues in quantifying thrifty energy expenditure phenotypes in humans. Curr Obes Rep. 2015;4(2):230–40.
    1. Celi FS, Le TN, Ni B. Physiology and relevance of human adaptive thermogenesis response. Trends Endocrinol Metab. 2015;26(5):238–47.
    1. Rosenbaum M, Leibel RL. Adaptive thermogenesis in humans. Int J Obes. 2010;34(Suppl 1):S47–55.
    1. Major GC, Doucet E, Trayhurn P, Astrup A, Tremblay A. Clinical significance of adaptive thermogenesis. Int J Obes. 2007;31(2):204–12.
    1. Flatt JP. Exaggerated claim about adaptive thermogenesis. Int J Obes. 2007;31(10):1626; author reply 7–8.
    1. Kuchnia A, Huizenga R, Frankenfield D, Matthie JR, Earthman CP. Overstated metabolic adaptation after "The Biggest Loser" intervention. Obesity. 2016;24(10):2025.
    1. Larson DE, Ferraro RT, Robertson DS, Ravussin E. Energy metabolism in weight-stable postobese individuals. Am J Clin Nutr. 1995;62(4):735–9.
    1. Martins C, Gower BA, Hill JO, Hunter GR. Metabolic adaptation is not a major barrier to weight loss maintenance. Am J Clin Nutr. [epub ahead of print 9 May 2020].
    1. Henry CJ, Lightowler HJ, Marchini J. Intra-individual variation in resting metabolic rate during the menstrual cycle. Br J Nutr. 2003;89(6):811–17.
    1. Brennan IM, Feltrin KL, Nair NS, Hausken T, Little TJ, Gentilcore D, Wishart JM, Jones KL, Horowitz M, Feinle-Bisset C. Effects of the phases of the menstrual cycle on gastric emptying, glycemia, plasma GLP-1 and insulin, and energy intake in healthy lean women. Am J Physiol Gastrointest Liver Physiol. 2009;297(3):G602–10.
    1. Curtis V, Henry CJ, Ghusain-Choueiri A. Basal metabolic rate of women on the contraceptive pill. Eur J Clin Nutr. 1996;50(5):319–22.
    1. Nordic Council of Ministers Nordic nutrition recommendations. 5th ed Copenhagen: Narayana Press; 2012.
    1. Shiose K, Yamada Y, Motonaga K, Sagayama H, Higaki Y, Tanaka H, Takahashi H. Segmental extracellular and intracellular water distribution and muscle glycogen after 72-h carbohydrate loading using spectroscopic techniques. J Appl Physiol. 2016;121(1):205–11.
    1. Compher C, Frankenfield D, Keim N, Roth-Yousey L. Best practice methods to apply to measurement of resting metabolic rate in adults: a systematic review. J Am Diet Assoc. 2006;106(6):881–903.
    1. Scheers T, Philippaerts R, Lefevre J. Patterns of physical activity and sedentary behavior in normal-weight, overweight and obese adults, as measured with a portable armband device and an electronic diary. Clin Nutr. 2012;31(5):756–64.
    1. Olsson KE, Saltin B. Variation in total body water with muscle glycogen changes in man. Acta Physiol Scand. 1970;80(1):11–18.
    1. Kreitzman SN, Coxon AY, Szaz KF. Glycogen storage: illusions of easy weight loss, excessive weight regain, and distortions in estimates of body composition. Am J Clin Nutr. 1992;56:292S–3S.
    1. Weinsier RL, Hunter GR, Zuckerman PA, Redden DT, Darnell BE, Larson DE, Newcomer BR, Goran MI. Energy expenditure and free-living physical activity in black and white women: comparison before and after weight loss. Am J Clin Nutr. 2000;71(5):1138–46.
    1. Weinsier RL, Hunter GR, Desmond RA, Byrne NM, Zuckerman PA, Darnell BE. Free-living activity energy expenditure in women successful and unsuccessful at maintaining a normal body weight. Am J Clin Nutr. 2002;75(3):499–504.
    1. Newcomer BR, Larson-Meyer DE, Hunter GR, Weinsier RL. Skeletal muscle metabolism in overweight and post-overweight women: an isometric exercise study using (31)P magnetic resonance spectroscopy. Int J Obes. 2001;25(9):1309–15.
    1. Weinsier RL, Hunter GR, Schutz Y, Zuckerman PA, Darnell BE. Physical activity in free-living, overweight white and black women: divergent responses by race to diet-induced weight loss. Am J Clin Nutr. 2002;76(4):736–42.
    1. Borges JH, Carter SJ, Singh H, Hunter GR. Inverse relationship between changes of maximal aerobic capacity and changes in walking economy after weight loss. Eur J Appl Physiol. 2018;118(8):1573–8.
    1. Carter SJ, Rogers LQ, Bowles HR, Norian LA, Hunter GR. Inverse association between changes in energetic cost of walking and vertical accelerations in non-metastatic breast cancer survivors. Eur J Appl Physiol. 2019;119(11–12):2547–64.
    1. Hunter GR, McCarthy JP, Bryan DR, Zuckerman PA, Bamman MM, Byrne NM. Increased strength and decreased flexibility are related to reduced oxygen cost of walking. Eur J Appl Physiol. 2008;104(5):895–901.
    1. Fisher G, McCarthy JP, Zuckerman PA, Bryan DR, Bickel CS, Hunter GR. Frequency of combined resistance and aerobic training in older women. J Strength Cond Res. 2013;27(7):1868–76.
    1. Hunter GR, Byrne NM. Physical activity and muscle function but not resting energy expenditure impact on weight gain. J Strength Cond Res. 2005;19(1):225–30.
    1. Larew K, Hunter GR, Larson-Meyer DE, Newcomer BR, McCarthy JP, Weinsier RL. Muscle metabolic function, exercise performance, and weight gain. Med Sci Sports Exerc. 2003;35(2):230–6.
    1. Carter SJ, Hunter GR, Norian LA, Turan B, Rogers LQ. Ease of walking associates with greater free-living physical activity and reduced depressive symptomology in breast cancer survivors: pilot randomized trial. Support Care Cancer. 2018;26(5):1675–83.
    1. Brock DW, Chandler-Laney PC, Alvarez JA, Gower BA, Gaesser GA, Hunter GR. Perception of exercise difficulty predicts weight regain in formerly overweight women. Obesity (Silver Spring). 2010;18(5):982–6.
    1. Hunter GR, Weinsier RL, Zuckerman PA, Darnell BE. Aerobic fitness, physiologic difficulty and physical activity in black and white women. Int J Obes. 2004;28(9):1111–17.

Source: PubMed

Sponzoři a spolupracovníci

Zdravotní podmínky

Drogové intervence

3
Předplatit