Physiological determinants of mechanical efficiency during advanced ageing and disuse

Author:

Venturelli Massimo1ORCID,Morgan Garrett R.23,Tarperi Cantor1,Zhao Jia2,Naro Fabio4,Reggiani Carlo5ORCID,Donato Anthony J.236,Richardson Russell S.267,Schena Federico1

Affiliation:

1. Department of Neurosciences, Biomedicine and Movement Sciences University of Verona Verona Italy

2. Division of Geriatrics, Department of Internal Medicine University of Utah School of Medicine University of Utah Salt Lake City Utah USA

3. The Murtha Cancer Center at Walter Reed Bethesda Bethesda Maryland USA

4. DAHFMO Unit of Histology and Medical Embryology Sapienza University Rome Italy

5. Department of Biomedical Sciences University of Padua Padua Italy

6. George E. Whalen Department of Veterans Affairs Medical Center Geriatric Research, Education, and Clinical Center Salt Lake City Utah USA

7. Department of Exercise and Sport Science University of Utah Salt Lake City Utah USA

Abstract

AbstractThis study aimed to determine which physiological factors impact net efficiency (ηnet) in oldest‐old individuals at different stages of skeletal muscle disuse. To this aim, we examined ηnet, central haemodynamics, peripheral circulation, and peripheral factors (skeletal muscle fibre type, capillarization and concentration of mitochondrial DNA [mtDNA]). Twelve young (YG; 25 ± 2 years), 12 oldest‐old mobile (OM; 87 ± 3 years), and 12 oldest‐old immobile (OI; 88 ± 4 years) subjects performed dynamic knee extensor (KE) and elbow flexors (EF) exercise. Pulmonary oxygen uptake, photoplethysmography, Doppler ultrasound and muscle biopsies of the vastus lateralis and biceps brachii were used to assess central and peripheral adaptations to advanced ageing and disuse. Compared to the YG (12.1 ± 2.4%), the ηnet of lower‐limb muscle was higher in the OM (17.6 ± 3.5%, P < 0.001), and lower in the OI (8.9 ± 1.9%, P < 0.001). These changes in ηnet during KE were coupled with significant peripheral adaptations, revealing strong correlations between ηnet and the proportion of type I muscle fibres (r = 0.82), as well as [mtDNA] (r = 0.77). No differences in ηnet were evident in the upper‐limb muscles between YG, OM and OI. In view of the differences in limb‐specific activity across the lifespan, these findings suggest that ηnet is reduced by skeletal muscle inactivity and not by chronological age, per se. Likewise, this study revealed that the age‐related changes in ηnet are not a consequence of central or peripheral haemodynamic adaptations, but are likely a product of peripheral changes related to skeletal muscle fibre type and mitochondrial density. imageKey points Although the effects of ageing and muscle disuse deeply impact the cardiovascular and skeletal muscle function, the combination of these factors on the mechanical efficiency are still a matter of debate. By measuring both upper‐ and lower‐limb muscle function, which experience differing levels of disuse, we examined the influence of central and peripheral haemodynamics, and skeletal muscle factors linked to mechanical efficiency. Across the ages and degree of disuse, upper‐limb muscles exhibited a preserved work economy. In the legs the oldest‐old without mobility limitations exhibited an augmented mechanical efficiency, which was reduced in those with an impairment in ambulation. These changes in mechanical efficiency were associated with the proportion of type I muscle fibres. Recognition that the mechanical efficiency is not simply age‐dependent, but the consequence of inactivity and subsequent skeletal muscle changes, highlights the importance of maintaining physical activity across the lifespan.

Publisher

Wiley

Subject

Physiology

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