Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats

The phenotype of sarcopenic obesity is frequently associated with impaired muscle strength and performance. Ectopic lipid deposition may interfere with muscle anabolic response especially during aging. Evidence is scarce concerning the potential interplay among aging and nutrient imbalance on skelet...

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Main Authors: Eleonora Poggiogalle, Fanny Rossignon, Aude Carayon, Fréderic Capel, Jean-Paul Rigaudière, Sarah De Saint Vincent, Olivier Le-Bacquer, Jérôme Salles, Christophe Giraudet, Véronique Patrac, Patrice Lebecque, Stéphane Walrand, Yves Boirie, Vincent Martin, Christelle Guillet
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
Series:Frontiers in Physiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2021.749049/full
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author Eleonora Poggiogalle
Eleonora Poggiogalle
Fanny Rossignon
Aude Carayon
Fréderic Capel
Jean-Paul Rigaudière
Sarah De Saint Vincent
Olivier Le-Bacquer
Jérôme Salles
Christophe Giraudet
Véronique Patrac
Patrice Lebecque
Stéphane Walrand
Yves Boirie
Vincent Martin
Vincent Martin
Christelle Guillet
author_facet Eleonora Poggiogalle
Eleonora Poggiogalle
Fanny Rossignon
Aude Carayon
Fréderic Capel
Jean-Paul Rigaudière
Sarah De Saint Vincent
Olivier Le-Bacquer
Jérôme Salles
Christophe Giraudet
Véronique Patrac
Patrice Lebecque
Stéphane Walrand
Yves Boirie
Vincent Martin
Vincent Martin
Christelle Guillet
author_sort Eleonora Poggiogalle
collection DOAJ
description The phenotype of sarcopenic obesity is frequently associated with impaired muscle strength and performance. Ectopic lipid deposition may interfere with muscle anabolic response especially during aging. Evidence is scarce concerning the potential interplay among aging and nutrient imbalance on skeletal muscle functionality. The objective of the present study was to investigate the impact of protein intake in the context of an obesogenic diet on skeletal muscle functional properties and intramuscular lipid infiltration. Two groups of forty-two adult and thirty-seven old male Wistar rats were randomly divided into four groups: isocaloric standard diet (12% protein, 14% lipid, as ST12); isocaloric standard (high-protein) diet (25% protein, 14% lipid, ST25); hypercaloric high-fat (normal-protein) diet (12% protein, 45% lipid, HF12); and hypercaloric high-fat (high-protein) diet (25% protein, 45% lipid, HF25). The nutritional intervention lasted 10 weeks. Total body composition was measured through Echo-MRI. Lipids were extracted from tibialis anterior muscle and analyzed by gas-liquid chromatography. The functional properties of the plantarflexor muscles were evaluated in vivo on an isokinetic dynamometer. Maximal torque was assessed from the torque-frequency relationship in isometric condition and maximal power was evaluated from the torque-velocity relationship in concentric condition. In adult rats high-protein intake combined with high-fat diet determined a lower decrease in relative isometric torque, normalized to either FFM or body weight, compared with adult rats fed a high-fat normal-protein diet. High-fat diet was also detrimental to relative muscle power, as normalized to body weight, that decreased to a larger extent in adult rats fed a high-fat normal-protein diet than their counterparts fed a normal-fat, high-protein diet. The effect of high-fat diet observed in adults, with the enhanced protein intake (25%) conferring some kind of protection against the negative effects of HFD, may be linked to the reduced intramuscular fat in this group, which may have contributed to preserve, at least partly, the contractile properties. A potential role for high-protein diet in preventing ectopic lipid deposition needs to be explored in future research. Detrimental effects of high- fat diet on skeletal muscle performance are mitigated by high- protein intake in adult rats but not in old rats.
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spelling doaj.art-1049db00a6074c4498520734e2783ee32022-12-21T17:21:54ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-01-011210.3389/fphys.2021.749049749049Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old RatsEleonora Poggiogalle0Eleonora Poggiogalle1Fanny Rossignon2Aude Carayon3Fréderic Capel4Jean-Paul Rigaudière5Sarah De Saint Vincent6Olivier Le-Bacquer7Jérôme Salles8Christophe Giraudet9Véronique Patrac10Patrice Lebecque11Stéphane Walrand12Yves Boirie13Vincent Martin14Vincent Martin15Christelle Guillet16Medical Pathophysiology, Food Science and Endocrinology Section, Department of Experimental Medicine, Sapienza University of Rome, Rome, ItalyINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceAME2P, Université Clermont Auvergne, Clermont-Ferrand, FranceInstitut Universitaire de France, Paris, FranceINRA, UNH, Unité de Nutrition Humaine, CRNH Auvergne, Clermont Auvergne University, Clermont-Ferrand, FranceThe phenotype of sarcopenic obesity is frequently associated with impaired muscle strength and performance. Ectopic lipid deposition may interfere with muscle anabolic response especially during aging. Evidence is scarce concerning the potential interplay among aging and nutrient imbalance on skeletal muscle functionality. The objective of the present study was to investigate the impact of protein intake in the context of an obesogenic diet on skeletal muscle functional properties and intramuscular lipid infiltration. Two groups of forty-two adult and thirty-seven old male Wistar rats were randomly divided into four groups: isocaloric standard diet (12% protein, 14% lipid, as ST12); isocaloric standard (high-protein) diet (25% protein, 14% lipid, ST25); hypercaloric high-fat (normal-protein) diet (12% protein, 45% lipid, HF12); and hypercaloric high-fat (high-protein) diet (25% protein, 45% lipid, HF25). The nutritional intervention lasted 10 weeks. Total body composition was measured through Echo-MRI. Lipids were extracted from tibialis anterior muscle and analyzed by gas-liquid chromatography. The functional properties of the plantarflexor muscles were evaluated in vivo on an isokinetic dynamometer. Maximal torque was assessed from the torque-frequency relationship in isometric condition and maximal power was evaluated from the torque-velocity relationship in concentric condition. In adult rats high-protein intake combined with high-fat diet determined a lower decrease in relative isometric torque, normalized to either FFM or body weight, compared with adult rats fed a high-fat normal-protein diet. High-fat diet was also detrimental to relative muscle power, as normalized to body weight, that decreased to a larger extent in adult rats fed a high-fat normal-protein diet than their counterparts fed a normal-fat, high-protein diet. The effect of high-fat diet observed in adults, with the enhanced protein intake (25%) conferring some kind of protection against the negative effects of HFD, may be linked to the reduced intramuscular fat in this group, which may have contributed to preserve, at least partly, the contractile properties. A potential role for high-protein diet in preventing ectopic lipid deposition needs to be explored in future research. Detrimental effects of high- fat diet on skeletal muscle performance are mitigated by high- protein intake in adult rats but not in old rats.https://www.frontiersin.org/articles/10.3389/fphys.2021.749049/fullsarcopenic obesitydynapeniamuscle lipid contentmuscle functionaging
spellingShingle Eleonora Poggiogalle
Eleonora Poggiogalle
Fanny Rossignon
Aude Carayon
Fréderic Capel
Jean-Paul Rigaudière
Sarah De Saint Vincent
Olivier Le-Bacquer
Jérôme Salles
Christophe Giraudet
Véronique Patrac
Patrice Lebecque
Stéphane Walrand
Yves Boirie
Vincent Martin
Vincent Martin
Christelle Guillet
Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
Frontiers in Physiology
sarcopenic obesity
dynapenia
muscle lipid content
muscle function
aging
title Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
title_full Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
title_fullStr Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
title_full_unstemmed Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
title_short Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats
title_sort deleterious effect of high fat diet on skeletal muscle performance is prevented by high protein intake in adult rats but not in old rats
topic sarcopenic obesity
dynapenia
muscle lipid content
muscle function
aging
url https://www.frontiersin.org/articles/10.3389/fphys.2021.749049/full
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