Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults

Abstract Background The concept of mitochondrial dysfunction in ageing muscle is highly controversial. In addition, emerging evidence suggests that reduced muscle oxidative capacity and efficiency underlie the aetiology of mobility loss in older adults. Here, we hypothesized that studying well‐pheno...

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Main Authors: Giovanna Distefano, Robert A. Standley, Xiaolei Zhang, Elvis A. Carnero, Fanchao Yi, Heather H. Cornnell, Paul M. Coen
Format: Article
Language:English
Published: Wiley 2018-04-01
Series:Journal of Cachexia, Sarcopenia and Muscle
Subjects:
Online Access:https://doi.org/10.1002/jcsm.12272
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spelling doaj-588cd1efe4774b278ab7aeac197c1b832020-11-24T21:40:42ZengWileyJournal of Cachexia, Sarcopenia and Muscle2190-59912190-60092018-04-019227929410.1002/jcsm.12272Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adultsGiovanna Distefano0Robert A. Standley1Xiaolei Zhang2Elvis A. Carnero3Fanchao Yi4Heather H. Cornnell5Paul M. Coen6Translational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USATranslational Research Institute for Metabolism and Diabetes Florida Hospital 301 East Princeton Street Orlando FL 32804 USAAbstract Background The concept of mitochondrial dysfunction in ageing muscle is highly controversial. In addition, emerging evidence suggests that reduced muscle oxidative capacity and efficiency underlie the aetiology of mobility loss in older adults. Here, we hypothesized that studying well‐phenotyped older cohorts across a wide range of physical activity would unveil a range of mitochondrial function in skeletal muscle and in turn allow us to more clearly examine the impact of age per se on mitochondrial energetics. This also enabled us to more clearly define the relationships between mitochondrial energetics and muscle lipid content with clinically relevant assessments of muscle and physical function. Methods Thirty‐nine volunteers were recruited to the following study groups: young active (YA, n = 2 women/8 men, age = 31.2 ± 5.4 years), older active (OA, n = 2 women/8 men, age = 67.5 ± 2.7 years), and older sedentary (OS, n = 8 women/11 men, age = 70.7 ± 4.7 years). Participants completed a graded exercise test to determine fitness (VO2peak), a submaximal exercise test to determine exercise efficiency, and daily physical activity was recorded using a tri‐axial armband accelerometer. Mitochondrial energetics were determined by (i) 31P magnetic resonance spectroscopy and (ii) respirometry of fibre bundles from vastus lateralis biopsies. Quadriceps function was assessed by isokinetic dynamometry and physical function by the short physical performance battery and stair climb test. Results Daily physical activity energy expenditure was significantly lower in OS, compared with YA and OA groups. Despite fitness being higher in YA compared with OA and OS, mitochondrial respiration, maximum mitochondrial capacity, Maximal ATP production/Oxygen consumption (P/O) ratio, and exercise efficiency were similar in YA and OA groups and were significantly lower in OS. P/O ratio was correlated with exercise efficiency. Time to complete the stair climb and repeated chair stand tests were significantly greater for OS. Interestingly, maximum mitochondrial capacity was related to muscle contractile performance and physical function. Conclusions Older adults who maintain a high amount of physical activity have better mitochondrial capacity, similar to highly active younger adults, and this is related to their better muscle quality, exercise efficiency, and physical performance. This suggests that mitochondria could be an important therapeutic target for sedentary ageing associated conditions including sarcopenia, dynapenia, and loss of physical function.https://doi.org/10.1002/jcsm.12272AgeingCardiovascular fitnessSkeletal muscleMitochondriaPhysical function
collection DOAJ
language English
format Article
sources DOAJ
author Giovanna Distefano
Robert A. Standley
Xiaolei Zhang
Elvis A. Carnero
Fanchao Yi
Heather H. Cornnell
Paul M. Coen
spellingShingle Giovanna Distefano
Robert A. Standley
Xiaolei Zhang
Elvis A. Carnero
Fanchao Yi
Heather H. Cornnell
Paul M. Coen
Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
Journal of Cachexia, Sarcopenia and Muscle
Ageing
Cardiovascular fitness
Skeletal muscle
Mitochondria
Physical function
author_facet Giovanna Distefano
Robert A. Standley
Xiaolei Zhang
Elvis A. Carnero
Fanchao Yi
Heather H. Cornnell
Paul M. Coen
author_sort Giovanna Distefano
title Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
title_short Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
title_full Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
title_fullStr Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
title_full_unstemmed Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
title_sort physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults
publisher Wiley
series Journal of Cachexia, Sarcopenia and Muscle
issn 2190-5991
2190-6009
publishDate 2018-04-01
description Abstract Background The concept of mitochondrial dysfunction in ageing muscle is highly controversial. In addition, emerging evidence suggests that reduced muscle oxidative capacity and efficiency underlie the aetiology of mobility loss in older adults. Here, we hypothesized that studying well‐phenotyped older cohorts across a wide range of physical activity would unveil a range of mitochondrial function in skeletal muscle and in turn allow us to more clearly examine the impact of age per se on mitochondrial energetics. This also enabled us to more clearly define the relationships between mitochondrial energetics and muscle lipid content with clinically relevant assessments of muscle and physical function. Methods Thirty‐nine volunteers were recruited to the following study groups: young active (YA, n = 2 women/8 men, age = 31.2 ± 5.4 years), older active (OA, n = 2 women/8 men, age = 67.5 ± 2.7 years), and older sedentary (OS, n = 8 women/11 men, age = 70.7 ± 4.7 years). Participants completed a graded exercise test to determine fitness (VO2peak), a submaximal exercise test to determine exercise efficiency, and daily physical activity was recorded using a tri‐axial armband accelerometer. Mitochondrial energetics were determined by (i) 31P magnetic resonance spectroscopy and (ii) respirometry of fibre bundles from vastus lateralis biopsies. Quadriceps function was assessed by isokinetic dynamometry and physical function by the short physical performance battery and stair climb test. Results Daily physical activity energy expenditure was significantly lower in OS, compared with YA and OA groups. Despite fitness being higher in YA compared with OA and OS, mitochondrial respiration, maximum mitochondrial capacity, Maximal ATP production/Oxygen consumption (P/O) ratio, and exercise efficiency were similar in YA and OA groups and were significantly lower in OS. P/O ratio was correlated with exercise efficiency. Time to complete the stair climb and repeated chair stand tests were significantly greater for OS. Interestingly, maximum mitochondrial capacity was related to muscle contractile performance and physical function. Conclusions Older adults who maintain a high amount of physical activity have better mitochondrial capacity, similar to highly active younger adults, and this is related to their better muscle quality, exercise efficiency, and physical performance. This suggests that mitochondria could be an important therapeutic target for sedentary ageing associated conditions including sarcopenia, dynapenia, and loss of physical function.
topic Ageing
Cardiovascular fitness
Skeletal muscle
Mitochondria
Physical function
url https://doi.org/10.1002/jcsm.12272
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