A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery

Abstract Background Muscle atrophy and strength loss are common adverse outcomes following bariatric surgery. This randomized, controlled trial investigated the effects of exercise training on bariatric surgery‐induced loss of muscle mass and function. Additionally, we investigated the effects of th...

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Main Authors: Saulo Gil, John P. Kirwan, Igor H. Murai, Wagner S. Dantas, Carlos Alberto Abujabra Merege‐Filho, Sujoy Ghosh, Samuel K. Shinjo, Rosa M.R. Pereira, Walcy R. Teodoro, Sheylla M. Felau, Fabiana B. Benatti, Ana L. deSá‐Pinto, Fernanda Lima, Roberto deCleva, Marco Aurélio Santo, Bruno Gualano, Hamilton Roschel
Format: Article
Language:English
Published: Wiley 2021-12-01
Series:Journal of Cachexia, Sarcopenia and Muscle
Subjects:
Online Access:https://doi.org/10.1002/jcsm.12815
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author Saulo Gil
John P. Kirwan
Igor H. Murai
Wagner S. Dantas
Carlos Alberto Abujabra Merege‐Filho
Sujoy Ghosh
Samuel K. Shinjo
Rosa M.R. Pereira
Walcy R. Teodoro
Sheylla M. Felau
Fabiana B. Benatti
Ana L. deSá‐Pinto
Fernanda Lima
Roberto deCleva
Marco Aurélio Santo
Bruno Gualano
Hamilton Roschel
author_facet Saulo Gil
John P. Kirwan
Igor H. Murai
Wagner S. Dantas
Carlos Alberto Abujabra Merege‐Filho
Sujoy Ghosh
Samuel K. Shinjo
Rosa M.R. Pereira
Walcy R. Teodoro
Sheylla M. Felau
Fabiana B. Benatti
Ana L. deSá‐Pinto
Fernanda Lima
Roberto deCleva
Marco Aurélio Santo
Bruno Gualano
Hamilton Roschel
author_sort Saulo Gil
collection DOAJ
description Abstract Background Muscle atrophy and strength loss are common adverse outcomes following bariatric surgery. This randomized, controlled trial investigated the effects of exercise training on bariatric surgery‐induced loss of muscle mass and function. Additionally, we investigated the effects of the intervention on molecular and histological mediators of muscle remodelling. Methods Eighty women with obesity were randomly assigned to a Roux‐en‐Y gastric bypass (RYGB: n = 40, age = 42 ± 8 years) or RYGB plus exercise training group (RYGB + ET: n = 40, age = 38 ± 7 years). Clinical and laboratory parameters were assessed at baseline, and 3 (POST3) and 9 months (POST9) after surgery. The 6 month, three‐times‐a‐week, exercise intervention (resistance plus aerobic exercise) was initiated 3 months post‐surgery (for RYGB + ET). A healthy, lean, age‐matched control group was recruited to provide reference values for selected variables. Results Surgery resulted in a similar (P = 0.66) reduction in lower‐limb muscle strength in RYGB and RYGB+ET (−26% vs. −31%), which was rescued to baseline values in RYGB + ET (P = 0.21 vs. baseline) but not in RYGB (P < 0.01 vs. baseline). Patients in RYGB+ET had greater absolute (214 vs. 120 kg, P < 0.01) and relative (2.4 vs. 1.4 kg/body mass, P < 0.01) muscle strength compared with RYGB alone at POST9. Exercise resulted in better performance in timed‐up‐and‐go (6.3 vs. 7.1 s, P = 0.05) and timed‐stand‐test (18 vs. 14 repetitions, P < 0.01) compared with RYGB. Fat‐free mass was lower (POST9‐PRE) after RYBG than RYGB + ET (total: −7.9 vs. −4.9 kg, P < 0.01; lower‐limb: −3.8 vs. −2.7 kg, P = 0.02). Surgery reduced Types I (~ − 21%; P = 0.99 between‐group comparison) and II fibre cross‐sectional areas (~ − 27%; P = 0.88 between‐group comparison), which were rescued to baseline values in RYGB+ET (P > 0.05 vs. baseline) but not RYGB (P > 0.01 vs. baseline). RYGB + ET showed greater Type I (5187 vs. 3898 μm2, P < 0.01) and Type II (5165 vs. 3565 μm2, P < 0.01) fCSA than RYGB at POST9. RYGB + ET also resulted in increased capillarization (P < 0.01) and satellite cell content (P < 0.01) than RYGB at POST9. Gene‐set normalized enrichment scores for the muscle transcriptome revealed that the ubiquitin‐mediated proteolysis pathway was suppressed in RYGB + ET at POST9 vs. PRE (NES: −1.7; P < 0.01), but not in RYGB. Atrogin‐1 gene expression was lower in RYGB + ET vs. RYGB at POST9 (0.18 vs. 0.71‐fold change, P < 0.01). From both genotypic and phenotypic perspectives, the muscle of exercised patients resembled that of healthy lean individuals. Conclusions This study provides compelling evidence—from gene to function—that strongly supports the incorporation of exercise into the recovery algorithm for bariatric patients so as to counteract the post‐surgical loss of muscle mass and function.
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spelling doaj.art-43dfba5d86c14dcbb0f9ca8d426f8b672024-04-16T23:38:46ZengWileyJournal of Cachexia, Sarcopenia and Muscle2190-59912190-60092021-12-011261440145510.1002/jcsm.12815A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgerySaulo Gil0John P. Kirwan1Igor H. Murai2Wagner S. Dantas3Carlos Alberto Abujabra Merege‐Filho4Sujoy Ghosh5Samuel K. Shinjo6Rosa M.R. Pereira7Walcy R. Teodoro8Sheylla M. Felau9Fabiana B. Benatti10Ana L. deSá‐Pinto11Fernanda Lima12Roberto deCleva13Marco Aurélio Santo14Bruno Gualano15Hamilton Roschel16Applied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilIntegrated Physiology and Molecular Medicine Laboratory, Pennington Biomedical Research Center Louisiana State University Baton Rouge LA USAApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilIntegrated Physiology and Molecular Medicine Laboratory, Pennington Biomedical Research Center Louisiana State University Baton Rouge LA USAApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilLaboratory of Computational Biology, Pennington Biomedical Research Center Louisiana State University Baton Rouge LA USARheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilRheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilRheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilRheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilRheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilGastroenterology Department, Digestive Surgery Division Department of Digestive Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilGastroenterology Department, Digestive Surgery Division Department of Digestive Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo BrazilApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilApplied Physiology & Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP Universidade de São Paulo São Paulo SP BrazilAbstract Background Muscle atrophy and strength loss are common adverse outcomes following bariatric surgery. This randomized, controlled trial investigated the effects of exercise training on bariatric surgery‐induced loss of muscle mass and function. Additionally, we investigated the effects of the intervention on molecular and histological mediators of muscle remodelling. Methods Eighty women with obesity were randomly assigned to a Roux‐en‐Y gastric bypass (RYGB: n = 40, age = 42 ± 8 years) or RYGB plus exercise training group (RYGB + ET: n = 40, age = 38 ± 7 years). Clinical and laboratory parameters were assessed at baseline, and 3 (POST3) and 9 months (POST9) after surgery. The 6 month, three‐times‐a‐week, exercise intervention (resistance plus aerobic exercise) was initiated 3 months post‐surgery (for RYGB + ET). A healthy, lean, age‐matched control group was recruited to provide reference values for selected variables. Results Surgery resulted in a similar (P = 0.66) reduction in lower‐limb muscle strength in RYGB and RYGB+ET (−26% vs. −31%), which was rescued to baseline values in RYGB + ET (P = 0.21 vs. baseline) but not in RYGB (P < 0.01 vs. baseline). Patients in RYGB+ET had greater absolute (214 vs. 120 kg, P < 0.01) and relative (2.4 vs. 1.4 kg/body mass, P < 0.01) muscle strength compared with RYGB alone at POST9. Exercise resulted in better performance in timed‐up‐and‐go (6.3 vs. 7.1 s, P = 0.05) and timed‐stand‐test (18 vs. 14 repetitions, P < 0.01) compared with RYGB. Fat‐free mass was lower (POST9‐PRE) after RYBG than RYGB + ET (total: −7.9 vs. −4.9 kg, P < 0.01; lower‐limb: −3.8 vs. −2.7 kg, P = 0.02). Surgery reduced Types I (~ − 21%; P = 0.99 between‐group comparison) and II fibre cross‐sectional areas (~ − 27%; P = 0.88 between‐group comparison), which were rescued to baseline values in RYGB+ET (P > 0.05 vs. baseline) but not RYGB (P > 0.01 vs. baseline). RYGB + ET showed greater Type I (5187 vs. 3898 μm2, P < 0.01) and Type II (5165 vs. 3565 μm2, P < 0.01) fCSA than RYGB at POST9. RYGB + ET also resulted in increased capillarization (P < 0.01) and satellite cell content (P < 0.01) than RYGB at POST9. Gene‐set normalized enrichment scores for the muscle transcriptome revealed that the ubiquitin‐mediated proteolysis pathway was suppressed in RYGB + ET at POST9 vs. PRE (NES: −1.7; P < 0.01), but not in RYGB. Atrogin‐1 gene expression was lower in RYGB + ET vs. RYGB at POST9 (0.18 vs. 0.71‐fold change, P < 0.01). From both genotypic and phenotypic perspectives, the muscle of exercised patients resembled that of healthy lean individuals. Conclusions This study provides compelling evidence—from gene to function—that strongly supports the incorporation of exercise into the recovery algorithm for bariatric patients so as to counteract the post‐surgical loss of muscle mass and function.https://doi.org/10.1002/jcsm.12815Muscle atrophyObesityBariatric surgeryMuscle function
spellingShingle Saulo Gil
John P. Kirwan
Igor H. Murai
Wagner S. Dantas
Carlos Alberto Abujabra Merege‐Filho
Sujoy Ghosh
Samuel K. Shinjo
Rosa M.R. Pereira
Walcy R. Teodoro
Sheylla M. Felau
Fabiana B. Benatti
Ana L. deSá‐Pinto
Fernanda Lima
Roberto deCleva
Marco Aurélio Santo
Bruno Gualano
Hamilton Roschel
A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
Journal of Cachexia, Sarcopenia and Muscle
Muscle atrophy
Obesity
Bariatric surgery
Muscle function
title A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
title_full A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
title_fullStr A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
title_full_unstemmed A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
title_short A randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
title_sort randomized clinical trial on the effects of exercise on muscle remodelling following bariatric surgery
topic Muscle atrophy
Obesity
Bariatric surgery
Muscle function
url https://doi.org/10.1002/jcsm.12815
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