CoChat
Sign Up
Cited by 43

The DOI matches its Crossref record; 14 of the 14 references it cites were found in a registry or an index.

Tissue losses and metabolic adaptations both contribute to the reduction in resting metabolic rate following weight loss

Martin, Alexandra, Fox, Darius, Murphy, Chaise A., Hofmann, Hande, Koehler, Karsten·2022·International Journal of Obesity
DOI 10.1038/s41366-022-01090-7PMC PMC9151388

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Objective: To characterize the contributions of the loss of energy-expending tissues and metabolic adaptations to the reduction in resting metabolic rate (RMR) following weight loss. Methods: A secondary analysis was conducted on data from the Comprehensive Assessment of Long-term Effects of Reducing Intake of Energy study. Changes in RMR, body composition, and metabolic hormones were examined over 12 months of calorie restriction in 109 individuals. The contribution of tissue losses to the decline in RMR was determined by weighing changes in the size of energy-expending tissues and organs (skeletal muscle, adipose tissue, bone, brain, inner organs, residual mass) assessed by dual-energy X-ray absorptiometry with their tissue-specific metabolic rates. Metabolic adaptations were quantified as the remaining reduction in RMR. Results: RMR was reduced by 101 ± 12 kcal/d as participants lost 7.3 ± 0.2 kg (both p < 0.001). On average, 60% of the total reduction in RMR were explained by energy-expending tissues losses, while 40% were attributed to metabolic adaptations. The loss of skeletal muscle mass (1.0 ± 0.7 kg) was not significantly related to RMR changes ( r = 0.14, p = 0.16), whereas adipose tissue losses (7.2 ± 3.0 kg) were positively associated with the reduction in RMR ( r = 0.42, p < 0.001) and metabolic adaptations ( r = 0.31, p < 0.001). Metabolic adaptations were correlated with declines in leptin ( r = 0.27, p < 0.01), triiodothyronine ( r = 0.19, p < 0.05), and insulin ( r = 0.25, p < 0.05). Conclusions: During weight loss, tissue loss and metabolic adaptations both contribute to the reduction in RMR, albeit variably. Contrary to popularly belief, it is not skeletal muscle, but rather adipose tissue losses that seem to drive RMR reductions following weight loss. Future research should target personalized strategies addressing the predominant cause of RMR reduction for weight maintenance.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41366-022-01090-7

Cites

14 of 14 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Martin et al. secondary analysis of CALERIE: over 12 months of caloric restriction (25% deficit) in 109 subjects, ~11% weight loss (8 kg) reduced RMR by ~100 kcal (~7%); only 60% of the reduction in RMR (60 kcal/day) could be explained by losses of metabolically active tissues (lean mass and fat mass), while the remaining 40% (40 kcal/day) was due to metabolic adaptations correlated with

    “Martin et al. [187] conducted a secondary analysis of the CALERIE study [188]. Body composition and metabolic changes were examined over 12 months of caloric restriction (25% deficit) in 109 subjects. As a result of ~11% weight loss (8 kg), the RMR was reduced by ~100 kcal (~7%) in healthy normal weight and overweight subjects. The intriguing finding was that only 60% of the reduction in RMR (60”

    From International Society of Sports Nutrition position stand: diets for body weight reduction (2026) · cites this paper as [187]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 30

  1. Ryan DH, Kahan S. Guideline Recommendations for Obesity Management. Med Clin North Am. 2018;102:49–63. · DOI · Paper page
  2. Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T, Caplan W, et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc. 2007;107:1755–67. · DOI · Paper page
  3. Anastasiou CA, Karfopoulou E, Yannakoulia M. Weight regaining: from statistics and behaviors to physiology and metabolism. Metabolism. 2015;64:1395–407. · DOI
  4. Astrup A, Buemann B, Christensen NJ, Madsen J, Gluud C, Bennett P, et al. The contribution of body composition, substrates, and hormones to the variability in energy expenditure and substrate utilization in premenopausal women. J Clin Endocrinol Metab. 1992;74:279–86.
  5. Lazzer S, Bedogni G, Lafortuna CL, Marazzi N, Busti C, Galli R, et al. Relationship between basal metabolic rate, gender, age, and body composition in 8,780 white obese subjects. Obesity (Silver Spring, Md). 2010;18:71–8. · DOI
  6. Connolly J, Romano T, Patruno M. Selections from current literature: effects of dieting and exercise on resting metabolic rate and implications for weight management. Fam Pract. 1999;16:196–201. · DOI
  7. Goele K, Bosy-Westphal A, Rumcker B, Lagerpusch M, Müller MJ. Influence of changes in body composition and adaptive thermogenesis on the difference between measured and predicted weight loss in obese women. Obesity Facts. 2009;2:105–9. · DOI · Paper page
  8. Elia M. Organ and tissue contribution to metabolic rate IN Energy metabolism: tissue determinant and cellular corrolaries. New York, NY: Raven Press; 1992.
  9. Gallagher D, Kelley DE, Thornton J, Boxt L, Pi-Sunyer X, Lipkin E, et al. Changes in skeletal muscle and organ size after a weight-loss intervention in overweight and obese type 2 diabetic patients. Am J Clin Nutr. 2017;105:78–84. · DOI · Paper page
  10. Bosy-Westphal A, Braun W, Schautz B, Müller MJ. Issues in characterizing resting energy expenditure in obesity and after weight loss. Front Physiol. 2013;4:47. · DOI
  11. Müller 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. · DOI · Paper page
  12. Knuth ND, Johannsen DL, Tamboli RA, Marks-Shulman PA, Huizenga R, Chen KY. et al.Metabolic adaptation following massive weight loss is related to the degree of energy imbalance and changes in circulating leptin.Obesity (Silver Spring. Md).2014;22:2563–9.
  13. Koehler K, Williams NI, Mallinson RJ, Southmayd EA, Allaway HC, De Souza MJ. Low resting metabolic rate in exercise-associated amenorrhea is not due to a reduced proportion of highly active metabolic tissue compartments. Am J Physiol Endocrinol Metab. 2016;311:E480–7. · DOI
  14. Kosmiski L, Schmiege SJ, Mascolo M, Gaudiani J, Mehler PS. Chronic starvation secondary to anorexia nervosa is associated with an adaptive suppression of resting energy expenditure. J Clin Endocrinol Metab. 2014;99:908–14. · DOI
  15. Rochon J, Bales CW, Ravussin E, Redman LM, Holloszy JO, Racette SB, et al. Design and conduct of the CALERIE study: comprehensive assessment of the long-term effects of reducing intake of energy. J Gerontol Series A, Biol Sci Med Sci. 2011;66:97–108. · DOI
  16. 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 · DOI · Paper page
  17. 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, Md). 2016;24:1612–9. · DOI · Paper page
  18. Tremblay A, Chaput JP. Adaptive reduction in thermogenesis and resistance to lose fat in obese men. Br J Nutr. 2009;102:488–92. · DOI
  19. Das SK, Roberts SB, Bhapkar MV, Villareal DT, Fontana L, Martin CK, et al. Body-composition changes in the Comprehensive Assessment of Long-term Effects of Reducing Intake of Energy (CALERIE)-2 study: a 2-y randomized controlled trial of calorie restriction in nonobese humans. Am J Clin Nutr. 2017;105:913–27. · DOI · Paper page
  20. Bosy-Westphal A, Kossel E, Goele K, Later W, Hitze B, Settler U, et al. Contribution of individual organ mass loss to weight loss-associated decline in resting energy expenditure. Am J Clin Nutr. 2009;90:993–1001. · DOI · Paper page
  21. Bosy-Westphal A, Reinecke U, Schlorke T, Illner K, Kutzner D, Heller M, et al. Effect of organ and tissue masses on resting energy expenditure in underweight, normal weight and obese adults. Int J Obes Relat Metab Disord. 2004;28:72–9. · DOI
  22. Hayes M, Chustek M, Wang Z, Gallagher D, Heshka S, Spungen A, et al. DXA: potential for creating a metabolic map of organ-tissue resting energy expenditure components. Obes Res. 2002;10:969–77. · DOI
  23. Pourhassan M, Bosy-Westphal A, Schautz B, Braun W, Gluer CC, Müller MJ. Impact of body composition during weight change on resting energy expenditure and homeostasis model assessment index in overweight nonsmoking adults. Am J Clin Nutr. 2014;99:779–91. · DOI
  24. Camps SG, Verhoef SP, Westerterp KR. Weight loss, weight maintenance, and adaptive thermogenesis. Am J Clin Nutr. 2013;97:990–4. · DOI
  25. Coutinho SR, With E, Rehfeld JF, Kulseng B, Truby H, Martins C. The impact of rate of weight loss on body composition and compensatory mechanisms during weight reduction: a randomized control trial. Clin Nutr. 2018;37:1154–62. · DOI
  26. Menozzi R, Bondi M, Baldini A, Venneri MG, Velardo A, Del Rio G. Resting metabolic rate, fat-free mass and catecholamine excretion during weight loss in female obese patients. Br J Nutr. 2000;84:515–20. · DOI
  27. Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE, Rood J, et al. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. Jama. 2006;295:1539–48. · DOI · Paper page
  28. Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol. 1996;270:E1–19.
  29. 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. · DOI
  30. Forbes GB. Body fat content influences the body composition response to nutrition and exercise. Ann N Y Acad Sci. 2000;904:359–65. · DOI

Cited by

Sorted by citations

Metadata

Authors
Martin, A., Fox, D., Murphy, C. A., Hofmann, H., & Koehler, K.
ORCID
Venue
International Journal of Obesity
Publisher
Springer Science and Business Media LLC
Published
2022-02-18
Volume
46
Issue
6
Pages
1168-1175
ISSN
  • 0307-0565
  • 1476-5497
DOI
10.1038/s41366-022-01090-7
PMC
PMC9151388
Cited by
43
References
14
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review