Heterogeneous effects of old age on human muscle oxidative capacity in vivo: a systematic review and meta-analysis

Fitzgerald, Liam F.; Christie, Anita; Kent, Jane A.

doi:10.1139/apnm-2016-0195

Cited by 26 publications

(37 citation statements)

References 63 publications

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“…In addition, a recent meta‐analysis of 22 studies using PCr recovery kinetics to estimate muscle oxidative capacity revealed that the muscle oxidative capacity is actually higher or does not differ in old compared to young adults for muscles of the upper extremity and the ankle plantarflexor and dorsiflexor muscles (Fitzgerald et al . ). The disparate findings between muscle groups and across studies on the knee extensors suggests that other factors, such as the patterns of use and disuse of the muscle (Kitahara et al .…”

Section: Discussionmentioning

confidence: 97%

“…), which are all muscle groups with similar or greater muscle oxidative capacity in old compared to young adults (Fitzgerald et al . ; Kent & Fitzgerald, ). By contrast, there is evidence from the ankle plantarflexors that old adults have an increased ATP cost of contraction during dynamic exercise compared to young adults, which is independent of the ability of the cardiovascular system to perfuse the working muscle (Layec et al .…”

Section: Discussionmentioning

confidence: 99%

“…) particularly for muscle groups other than the knee extensors (Fitzgerald et al . ). Interpreted together, it is possible that the large energetic demand during concentric contractions (Ryschon et al .…”

Section: Introductionmentioning

confidence: 97%

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Bioenergetic basis for the increased fatigability with ageing

Sundberg

Prost

Fitts

et al. 2019

The Journal of Physiology

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Key points The mechanisms for the age‐related increase in fatigability during dynamic exercise remain elusive. We tested whether age‐related impairments in muscle oxidative capacity would result in a greater accumulation of fatigue causing metabolites, inorganic phosphate (Pi), hydrogen (H+) and diprotonated phosphate (H2PO4−), in the muscle of old compared to young adults during a dynamic knee extension exercise. The age‐related increase in fatigability (reduction in mechanical power) of the knee extensors was closely associated with a greater accumulation of metabolites within the working muscle but could not be explained by age‐related differences in muscle oxidative capacity. These data suggest that the increased fatigability in old adults during dynamic exercise is primarily determined by age‐related impairments in skeletal muscle bioenergetics that result in a greater accumulation of metabolites. Abstract The present study aimed to determine whether the increased fatigability in old adults during dynamic exercise is associated with age‐related differences in skeletal muscle bioenergetics. Phosphorus nuclear magnetic resonance spectroscopy was used to quantify concentrations of high‐energy phosphates and pH in the knee extensors of seven young (22.7 ± 1.2 years; six women) and eight old adults (76.4 ± 6.0 years; seven women). Muscle oxidative capacity was measured from the phosphocreatine (PCr) recovery kinetics following a 24 s maximal voluntary isometric contraction. The fatiguing exercise consisted of 120 maximal velocity contractions (one contraction per 2 s) against a load equivalent to 20% of the maximal voluntary isometric contraction. The PCr recovery kinetics did not differ between young and old adults (0.023 ± 0.007 s−1 vs. 0.019 ± 0.004 s−1, respectively). Fatigability (reductions in mechanical power) of the knee extensors was ∼1.8‐fold greater with age and was accompanied by a greater decrease in pH (young = 6.73 ± 0.09, old = 6.61 ± 0.04) and increases in concentrations of inorganic phosphate, [Pi], (young = 22.7 ± 4.8 mm, old = 32.3 ± 3.6 mm) and diprotonated phosphate, [H2PO4−], (young = 11.7 ± 3.6 mm, old = 18.6 ± 2.1 mm) at the end of the exercise in old compared to young adults. The age‐related increase in power loss during the fatiguing exercise was strongly associated with intracellular pH (r = –0.837), [Pi] (r = 0.917) and [H2PO4−] (r = 0.930) at the end of the exercise. These data suggest that the age‐related increase in fatigability during dynamic exercise has a bioenergetic basis and is explained by an increased accumulation of metabolites within the muscle.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

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Bioenergetic basis for the increased fatigability with ageing

Sundberg

Prost

Fitts

et al. 2019

The Journal of Physiology

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“…Lanza et al (2005) previously reported a greater relative reliance on oxidative phosphorylation with age during a 60 s maximal voluntary isometric contraction of the dorsiflexor muscles, Journal Club J Physiol 597.2 which resulted in a significantly higher pH and lower [P i ] in older compared with young muscle. However, unlike the dorsiflexor muscles, oxidative capacity of the knee extensors is significantly lower in older compared with young adults (Fitzgerald et al 2016). The ATP cost of contraction is also higher during dynamic compared with isometric contractions.…”

mentioning

confidence: 95%

“…However, unlike the dorsiflexor muscles, oxidative capacity of the knee extensors is significantly lower in older compared with young adults (Fitzgerald et al . ). The ATP cost of contraction is also higher during dynamic compared with isometric contractions.…”

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confidence: 97%

Potential cellular and energetic mechanisms for age‐related differences in skeletal muscle fatigue

Foster

Fitzgerald

Bartlett

et al. 2018

The Journal of Physiology

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Matrisome, innervation and oxidative metabolism affected in older compared with younger males with similar physical activity

Lagerwaard

Nieuwenhuizen

Bunschoten

et al. 2021

J cachexia sarcopenia muscle

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Background Due to the interaction between skeletal muscle ageing and lifestyle factors, it is often challenging to attribute the decline in muscle mass and quality to either changes in lifestyle or to advancing age itself. Because many of the physiological factors affecting muscle mass and quality are modulated by physical activity and physical activity declines with age, the aim of this study is to better understand the effects of early ageing on muscle function by comparing a population of healthy older and young males with similar physical activity patterns. Methods Eighteen older (69 ± 2.0 years) and 20 young (22 ± 2.0 years) males were recruited based on similar self-reported physical activity, which was verified using accelerometry measurements. Gene expression profiles of vastus lateralis biopsies obtained by RNA sequencing were compared, and key results were validated using quantitative polymerase chain reaction and western blot. Results Total physical activity energy expenditure was similar between the young and old group (404 ± 215 vs. 411 ± 189 kcal/day, P = 0.11). Three thousand seven hundred ninety-seven differentially expressed coding genes (DEGs) were identified (adjusted P-value cut-off of <0.05), of which 1891 were higher and 1906 were lower expressed in the older muscle. The matrisome, innervation and inflammation were the main upregulated processes, and oxidative metabolism was the main downregulated process in old compared with young muscle. Lower protein levels of mitochondrial transcription factor A (TFAM, P = 0.030) and mitochondrial respiratory Complexes IV and II (P = 0.011 and P = 0.0009, respectively) were observed, whereas a trend was observed for Complex I (P = 0.062), in older compared with young muscle. Protein expression of Complexes I and IV was significantly correlated to mitochondrial capacity in the vastus lateralis as measured in vivo (P = 0.017, R 2 = 0.42 and P = 0.030, R 2 = 0.36). A trend for higher muscle-specific receptor kinase (MUSK) protein levels in the older group was observed (P = 0.08). Conclusions There are clear differences in the transcriptome signatures of the vastus lateralis muscle of healthy older and young males with similar physical activity levels, including significant differences at the protein level. By disentangling physical activity and ageing, we appoint early skeletal muscle ageing processes that occur despite similar physical activity. Improved understanding of these processes will be key to design targeted anti-ageing therapies.

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Heterogeneous effects of old age on human muscle oxidative capacity in vivo: a systematic review and meta-analysis

Cited by 26 publications

References 63 publications

Bioenergetic basis for the increased fatigability with ageing

Bioenergetic basis for the increased fatigability with ageing

Potential cellular and energetic mechanisms for age‐related differences in skeletal muscle fatigue

Matrisome, innervation and oxidative metabolism affected in older compared with younger males with similar physical activity

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