Reduced metabolic efficiency in sedentary eucaloric conditions predicts greater weight regain in adults with obesity following sustained weight loss.


Journal

International journal of obesity (2005)
ISSN: 1476-5497
Titre abrégé: Int J Obes (Lond)
Pays: England
ID NLM: 101256108

Informations de publication

Date de publication:
04 2021
Historique:
received: 28 07 2020
accepted: 04 01 2021
revised: 18 11 2020
pubmed: 23 1 2021
medline: 13 1 2022
entrez: 22 1 2021
Statut: ppublish

Résumé

Successful long-term weight loss maintenance after caloric restriction (CR) is rarely achieved. Besides known metabolic, behavioural, and cognitive factors, 24-hour energy expenditure (24hEE) relative to body size (i.e., metabolic efficiency) might influence subsequent weight loss maintenance. Eleven participants with obesity (BMI = 39.0 ± 8.7 kg/m After 6-week CR, participants lost 8.5 ± 2.7% weight (FFM: -6.3 ± 3.6 kg, FM: -3.4 ± 1.2 kg) but regained 5.1 ± 8.0% 1 year following CR, which was mostly due to FFM regain (+5.7 ± 5.5 kg) and unchanged FM. A relatively higher 24hEE by 100 kcal/day prior to CR was associated with an average greater rate of weight regain by +0.3 kg/month during follow-up and a greater final weight regain by +5.1 kg after 1 year of follow-up. These results suggest that reduced metabolic efficiency in 24hEE during eucaloric, sedentary conditions may predict greater weight regain after CR-induced weight loss.

Sections du résumé

BACKGROUND
Successful long-term weight loss maintenance after caloric restriction (CR) is rarely achieved. Besides known metabolic, behavioural, and cognitive factors, 24-hour energy expenditure (24hEE) relative to body size (i.e., metabolic efficiency) might influence subsequent weight loss maintenance.
METHODS
Eleven participants with obesity (BMI = 39.0 ± 8.7 kg/m
RESULTS
After 6-week CR, participants lost 8.5 ± 2.7% weight (FFM: -6.3 ± 3.6 kg, FM: -3.4 ± 1.2 kg) but regained 5.1 ± 8.0% 1 year following CR, which was mostly due to FFM regain (+5.7 ± 5.5 kg) and unchanged FM. A relatively higher 24hEE by 100 kcal/day prior to CR was associated with an average greater rate of weight regain by +0.3 kg/month during follow-up and a greater final weight regain by +5.1 kg after 1 year of follow-up.
CONCLUSION
These results suggest that reduced metabolic efficiency in 24hEE during eucaloric, sedentary conditions may predict greater weight regain after CR-induced weight loss.

Identifiants

pubmed: 33479452
doi: 10.1038/s41366-021-00748-y
pii: 10.1038/s41366-021-00748-y
pmc: PMC8009858
mid: NIHMS1659833
doi:

Types de publication

Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

840-849

Subventions

Organisme : Intramural NIH HHS
ID : ZIA DK069029
Pays : United States

Références

Jensen MD, Ryan DH, Apovian CM, Ard JD, Comuzzie AG, Donato KA, et al. 2013 AHA/ACC/TOS guideline for the management of overweight and obesity in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society. J Am college Cardiol. 2014;63:2985–3023.
doi: 10.1016/j.jacc.2013.11.004
Wing RR, Phelan S. Long-term weight loss maintenance. Am J Clin Nutr. 2005;82 Suppl 1:222S–25S.
pubmed: 16002825 doi: 10.1093/ajcn/82.1.222S
Muller MJ, Bosy-Westphal A. Adaptive thermogenesis with weight loss in humans. Obesity (Silver Spring). 2013;21:218–28.
doi: 10.1002/oby.20027
Van Baak MA, Mariman ECM. Mechanisms of weight regain after weight loss — the role of adipose tissue. Nat Rev Endocrinol. 2019;15:274–87.
pubmed: 30655624 doi: 10.1038/s41574-018-0148-4
Camps SG, Verhoef SP, Westerterp KR Weight loss, weight maintenance, and adaptive thermogenesis. Am J Clin Nutr. 2013;97:990–4. https://doi.org/10.3945/ajcn.112.050310 . Epub 2013 Mar 27.
Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332:621–8.
pubmed: 7632212 doi: 10.1056/NEJM199503093321001
Redman LM, Smith SR, Burton JH, Martin CK, Il’Yasova D, Ravussin E. Metabolic slowing and reduced oxidative damage with sustained caloric restriction support the rate of living and oxidative damage theories of aging. Cell Metab. 2018;27:805–15.e4.
pubmed: 29576535 pmcid: 5886711 doi: 10.1016/j.cmet.2018.02.019
Heinitz S, Hollstein T, Ando T, Walter M, Basolo A, Krakoff J et al. Early adaptive thermogenesis is a determinant of weight loss after six weeks of caloric restriction in overweight subjects. Metabolism 2020; In Press Journal Pre-Proof.
Rosenbaum M, Vandenborne K, Goldsmith R, Simoneau J-A, Heymsfield S, Joanisse DR, et al. Effects of experimental weight perturbation on skeletal muscle work efficiency in human subjects. Am J Physiol-Regul Integr Comp Physiol. 2003;285:R183–92.
pubmed: 12609816 doi: 10.1152/ajpregu.00474.2002
Goldsmith R, Joanisse DR, Gallagher D, Pavlovich K, Shamoon E, Leibel RL, et al. Effects of experimental weight perturbation on skeletal muscle work efficiency, fuel utilization, and biochemistry in human subjects. Am J Physiol Regul Integr Comp Physiol. 2010;298:R79–88.
pubmed: 19889869 doi: 10.1152/ajpregu.00053.2009
Dulloo AG, Miles-Chan JL, Schutz Y. Collateral fattening in body composition autoregulation: its determinants and significance for obesity predisposition. Eur J Clin Nutr. 2018;72:657–64.
pubmed: 29559726 pmcid: 5945583 doi: 10.1038/s41430-018-0138-6
Dulloo AG. Collateral fattening: When a deficit in lean body mass drives overeating. Obesity. 2017;25:277–9.
pubmed: 28078821 doi: 10.1002/oby.21734
Jacquet P, Schutz Y, Montani J-P, Dulloo A How dieting might make some fatter: modeling weight cycling toward obesity from a perspective of body composition autoregulation. Int J Obesity. 2020;44:1243–53.
Ellis AC, Hyatt TC, Hunter GR, Gower BA. Respiratory quotient predicts fat mass gain in premenopausal women. Obesity (Silver Spring, Md.). 2010;18:2255–9.
doi: 10.1038/oby.2010.96
Valtueña S, Salas-Salvadó J, Lorda P. The respiratory quotient as a prognostic factor in weight-loss rebound. Int J Obesity. 1997;21:811–7.
doi: 10.1038/sj.ijo.0800480
Hainer V, Kunesová M, Parízková J, Stich V, Mikulová R, Slabá S. Respiratory quotient in obesity: its association with an ability to retain weight loss and with parental obesity. Sb Lek. 2000;101:99–104.
pubmed: 10953639
Thom G, Dombrowski SU, Brosnahan N, Algindan YY, Rosario Lopez-Gonzalez M, Roditi G, et al. The role of appetite-related hormones, adaptive thermogenesis, perceived hunger and stress in long-term weight-loss maintenance: a mixed-methods study. Eur J Clin Nutr. 2020;74:622–32.
pubmed: 32020057 doi: 10.1038/s41430-020-0568-9
Weise CM, Hohenadel MG, Krakoff J, Votruba SB. Body composition and energy expenditure predict ad-libitum food and macronutrient intake in humans. Int J Obes. 2014;38:243–51.
doi: 10.1038/ijo.2013.85
Basolo A, Votruba SB, Heinitz S, Krakoff J, Piaggi P. Deviations in energy sensing predict long-term weight change in overweight native Americans. Metabolism. 2018;82:65–71.
pubmed: 29305947 pmcid: 5930127 doi: 10.1016/j.metabol.2017.12.013
Piaggi P, Thearle MS, Krakoff J, Votruba SB. Higher daily energy expenditure and respiratory quotient, rather than fat-free mass, independently determine greater ad libitum overeating. J Clin Endocrinol Metab. 2015;100:3011–20.
pubmed: 26086330 pmcid: 4524995 doi: 10.1210/jc.2015-2164
Piaggi P, Vinales KL, Basolo A, Santini F, Krakoff J. Energy expenditure in the etiology of human obesity: spendthrift and thrifty metabolic phenotypes and energy-sensing mechanisms. J Endocrinol Investig. 2018;41:83–9.
doi: 10.1007/s40618-017-0732-9
Blundell JE, Caudwell P, Gibbons C, Hopkins M, Naslund E, King N, et al. Role of resting metabolic rate and energy expenditure in hunger and appetite control: a new formulation. Dis Model Mech. 2012;5:608–13.
pubmed: 22915022 pmcid: 3424457 doi: 10.1242/dmm.009837
Blundell JE, Tremblay A. Appetite control and energy (fuel) balance. Nutr Res Rev. 1995;8:225–42.
pubmed: 19094287 doi: 10.1079/NRR19950014
Piaggi P. Metabolic Determinants of Weight Gain in Humans. Obesity. 2019;27:691–9.
pubmed: 31012296 doi: 10.1002/oby.22456
Blundell JE, Finlayson G, Gibbons C, Caudwell P, Hopkins M. The biology of appetite control: do resting metabolic rate and fat-free mass drive energy intake? Physiol Behav. 2015;152:473–8.
pubmed: 26037633 doi: 10.1016/j.physbeh.2015.05.031
Dulloo AG, Jacquet J, Miles-Chan JL, Schutz Y. Passive and active roles of fat-free mass in the control of energy intake and body composition regulation. Eur J Clin Nutr. 2017;71:353–7.
pubmed: 27966570 doi: 10.1038/ejcn.2016.256
Reinhardt M, Thearle MS, Ibrahim M, Hohenadel MG, Bogardus C, Krakoff J, et al. A human thrifty phenotype associated with less weight loss during caloric restriction. Diabetes. 2015;64:2859–67.
pubmed: 25964395 pmcid: 4512223 doi: 10.2337/db14-1881
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010; 33 Suppl 1:S62–9.
Ferraro R, Boyce VL, Swinburn B, De Gregorio M, Ravussin E. Energy cost of physical activity on a metabolic ward in relationship to obesity. Am J Clin Nutr. 1991;53:1368–71.
pubmed: 2035463 doi: 10.1093/ajcn/53.6.1368
Thearle MS, Pannacciulli N, Bonfiglio S, Pacak K, Krakoff J. Extent and determinants of thermogenic responses to 24 h of fasting, energy balance, and five different overfeeding diets in humans. J Clin Endocrinol Metab. 2013;98:2791–9.
pubmed: 23666976 pmcid: 3701281 doi: 10.1210/jc.2013-1289
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;78:1568–78.
pubmed: 3782471 pmcid: 423919 doi: 10.1172/JCI112749
Hollstein T, Piaggi P Supplemental Material - Reduced energy efficiency in eucaloric conditions at low energy turnover predicts long-term weight regain in overweight subjects following sustained caloric restriction and weight loss. In: Harvard Dataverse (Link: https://doi.org/10.7910/DVN/U5SFTH) , 2020.
Piaggi P, Thearle MS, Bogardus C, Krakoff J. Lower energy expenditure predicts long-term increases in weight and fat mass. J Clin Endocrinol Metab. 2013;98:E703–7.
pubmed: 23418317 pmcid: 3615206 doi: 10.1210/jc.2012-3529
Heinitz S, Hollstein T, Ando T, Walter M, Basolo A, Krakoff J, et al. Early adaptive thermogenesis is a determinant of weight loss after six weeks of caloric restriction in overweight subjects. Metabolism. 2020;110:154303.
pubmed: 32599082 doi: 10.1016/j.metabol.2020.154303
Ellis MV. Repeated measures designs. Couns Psychol. 1999;27:552–78.
doi: 10.1177/0011000099274004
Marshall JA, Scarbro S, Shetterly SM, Jones RH. Improving power with repeated measures: diet and serum lipids. Am J Clin Nutr. 1998;67:934–9.
pubmed: 9583852 doi: 10.1093/ajcn/67.5.934
Keys A, Brožek J, Henschel A, Mickelsen O, Taylor HL The biology of human starvation. Oxford, England, Univ. of Minnesota Press (2 vols). 1950.
Sumithran P, Proietto J. The defence of body weight: a physiological basis for weight regain after weight loss. Clin Sci. 2013;124:231–41.
doi: 10.1042/CS20120223
Pasman WJ, Saris WHM, Westerterp-Plantenga MS. Predictors of weight maintenance. Obesity Research. 1999;7:43–50.
pubmed: 10023729 doi: 10.1002/j.1550-8528.1999.tb00389.x
Muller MJ, Enderle J, Pourhassan M, Braun W, Eggeling B, Lagerpusch M, et al. Metabolic adaptation to caloric restriction and subsequent refeeding: the Minnesota Starvation Experiment revisited. Am J Clin Nutr. 2015;102:807–19.
pubmed: 26399868 doi: 10.3945/ajcn.115.109173
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;88:906–12.
pubmed: 18842775 doi: 10.1093/ajcn/88.4.906
Fothergill E, Guo J, Howard L, Kerns JC, Knuth ND, Brychta R, et al. Persistent metabolic adaptation 6 years after “The Biggest Loser” competition. Obesity (Silver Spring). 2016;24:1612–9.
doi: 10.1002/oby.21538
Bosy-Westphal A, Schautz B, Lagerpusch M, Pourhassan M, Braun W, Goele K, et al. Effect of weight loss and regain on adipose tissue distribution, composition of lean mass and resting energy expenditure in young overweight and obese adults. Int J Obesity. 2013;37:1371.
doi: 10.1038/ijo.2013.1
Rosenbaum M, Goldsmith RL, Haddad F, Baldwin KM, Smiley R, Gallagher D, et al. Triiodothyronine and leptin repletion in humans similarly reverse weight-loss-induced changes in skeletal muscle. Am J Physiol-Endocrinol Metab. 2018;315:E771–9.
pubmed: 29920214 pmcid: 6293163 doi: 10.1152/ajpendo.00116.2018
Rosenbaum M, Heaner M, Goldsmith RL, Christian Schulze P, Shukla A, Shen W, et al. Resistance training reduces skeletal muscle work efficiency in weight‐reduced and non–weight‐reduced subjects. Obesity. 2018;26:1576–83.
pubmed: 30260099 doi: 10.1002/oby.22274
Hopkins M, Finlayson G, Duarte C, Whybrow S, Ritz P, Horgan GW, et al. Modelling the associations between fat-free mass, resting metabolic rate and energy intake in the context of total energy balance. Int J Obesity. 2016;40:312–8.
doi: 10.1038/ijo.2015.155
McNeil J, Lamothe G, Cameron JD, Riou M-È, Cadieux S, Lafrenière J, et al. Investigating predictors of eating: is resting metabolic rate really the strongest proxy of energy intake? Am J Clin Nutr. 2017;106:1206–12.
pubmed: 28877891
Caudwell P, Finlayson G, Gibbons C, Hopkins M, King N, Näslund E, et al. Resting metabolic rate is associated with hunger, self-determined meal size, and daily energy intake and may represent a marker for appetite. Am J Clin Nutr. 2012;97:7–14.
pubmed: 23193010 doi: 10.3945/ajcn.111.029975
Hollstein T, Piaggi P Metabolic factors determining the susceptibility to weight gain: current evidence. Curr Obes Rep. 2020;9:121–35.
Hollstein T, Ando T, Basolo A, Krakoff J, Votruba SB, Piaggi P Metabolic response to fasting predicts weight gain during low-protein overfeeding in lean men: further evidence for spendthrift and thrifty metabolic phenotypes. Am J Clin Nutr. 2019;110:593–604.
Hollstein T, Basolo A, Ando T, Votruba SB, Walter M, Krakoff J et al. Recharacterizing the metabolic state of energy balance in thrifty and spendthrift phenotypes. J Clin Endocrinol Metab. 2020;105:1375–92.
Pannacciulli N, Salbe AD, Ortega E, Venti CA, Bogardus C, Krakoff J. The 24-h carbohydrate oxidation rate in a human respiratory chamber predicts ad libitum food intake. Am J Clin Nutr. 2007;86:625–32.
pubmed: 17823426 pmcid: 2128058
Kerns JC, Guo J, Fothergill E, Howard L, Knuth ND, Brychta R, et al. Increased physical activity associated with less weight regain six years after “The Biggest Loser” competition. Obesity. 2017;25:1838–43.
pubmed: 29086499 doi: 10.1002/oby.21986
Ostendorf DM, Caldwell AE, Creasy SA, Pan Z, Lyden K, Bergouignan A, et al. Physical activity energy expenditure and total daily energy expenditure in successful weight loss maintainers. Obesity. 2019;27:496–504.
pubmed: 30801984 doi: 10.1002/oby.22373
Hägele FA, Büsing F, Nas A, Hasler M, Müller MJ, Blundell JE, et al. Appetite control is improved by acute increases in energy turnover at different levels of energy balance. J Clin Endocrinol Metab. 2019;104:4481–91.
pubmed: 31305927 doi: 10.1210/jc.2019-01164
Montesi L, El Ghoch M, Brodosi L, Calugi S, Marchesini G, Dalle Grave R. Long-term weight loss maintenance for obesity: a multidisciplinary approach. Diabetes Metab Syndr Obesity. 2016;9:37.

Auteurs

Tim Hollstein (T)

Obesity and Diabetes Clinical Research Section, Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Diseases, Phoenix, AZ, USA.
Division of Endocrinology, Diabetology and Clinical Nutrition, Department of Internal Medicine 1, University of Kiel, Kiel, Germany.

Sascha Heinitz (S)

Department of Internal Medicine, Clinic for Endocrinology and Nephrology, University of Leipzig, Leipzig, Germany.
Helmholtz Institute for Metabolic, Obesity and Vascular Research (HI-MAG) of the Helmholtz Zentrum München at the University of Leipzig and University Hospital Leipzig, Leipzig, Germany.

Alessio Basolo (A)

Obesity and Diabetes Clinical Research Section, Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Diseases, Phoenix, AZ, USA.

Jonathan Krakoff (J)

Obesity and Diabetes Clinical Research Section, Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Diseases, Phoenix, AZ, USA.

Susanne B Votruba (SB)

Obesity and Diabetes Clinical Research Section, Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Diseases, Phoenix, AZ, USA.

Paolo Piaggi (P)

Obesity and Diabetes Clinical Research Section, Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Diseases, Phoenix, AZ, USA. paolo.piaggi@nih.gov.
Department of Information Engineering, University of Pisa, Pisa, Italy. paolo.piaggi@nih.gov.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH