Do skeletal muscle composition and gene expression as well as acute exercise-induced serum adaptations in older adults depend on fitness status?

Daniel A Bizjak, Martina Zügel, Uwe Schumann, Mark A Tully, Dhayana Dallmeier, Michael Denkinger, Jürgen M Steinacker, Daniel A Bizjak, Martina Zügel, Uwe Schumann, Mark A Tully, Dhayana Dallmeier, Michael Denkinger, Jürgen M Steinacker

Abstract

Background: Inactive physical behavior among the elderly is one risk factor for cardiovascular disease, immobility and increased all-cause mortality. We aimed to answer the question whether or not circulating and skeletal muscle biomarkers are differentially expressed depending on fitness status in a group of elderly individuals.

Methods: Twenty-eight elderly individuals (73.36 ± 5.46 years) participated in this exploratory study after participating as part of the multinational SITLESS-clinical trial (implementation of self-management and exercise programs over 16 weeks). A cardiopulmonary exercise test (CPX) and resting skeletal muscle biopsy were performed to determine individual physiological performance capacity. Participants were categorized into a high physical fitness group (HPF) and a low physical fitness group (LPF) depending on peak oxygen uptake (VO2peak). Serum blood samples were taken before (pre) and after (post) CPX and were examined regarding serum BDNF, HSP70, Kynurenine, Irisin and Il-6 concentrations. Skeletal muscle tissue was analyzed by silver staining to determine the myosin heavy chain (MyHC) composition and selected genes by qRT-PCR.

Results: HPF showed lower body weight and body fat, while skeletal muscle mass and oxygen uptake at the first ventilatory threshold (VO2T1) did not differ between groups. There were positive associations between VO2peak and VO2VT1 in HPF and LPF. MyHC isoform quantification revealed no differences between groups. qRT-PCR showed higher expression of BDNF and BRCA1 in LPF skeletal muscle while there were no differences in other examined genes regarding energy metabolism. Basal serum concentrations of Irisin were higher in HPF compared to LPF with a trend towards higher values in BDNF and HSP70 in HPF. Increases in Il-6 in both groups were observed post.

Conclusions: Although no association between muscle composition/VO2peak with fitness status in older people was detected, higher basal Irisin serum levels in HPF revealed slightly beneficial molecular serum and muscle adaptations.

Trial registration: ClinicalTrials.gov, NCT02629666 . Registered 19 November 2015.

Keywords: Health services for older individuals; Molecular adaptations; Physical fitness; Sedentary behavior; Skeletal muscle.

Conflict of interest statement

The authors declare that they have no financial or non-financial competing interests.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
Schematic overview of the study design. After SITLESS, participants were asked to participate in this sub-study. A muscle biopsy was conducted at least one week before the CPX. Muscle samples were used for Myosin-Heavy chain (MyH) isoform composition and gene expression analysis. Blood was sampled before (pre) and directly after the CPX (post), and serum protein expression determined. Participants were classified according to the VO2peak measured during CPX by spiroergometry into HPF and LPF. (SITLESS: multinational 16-week long-intervention study to promote physical activity in the elderly population; CPX: cardiopulmonary exercise test; VO2peak: peak oxygen consumption; HPF: high physical fitness group; LPF: low physical fitness group)
Fig. 2
Fig. 2
Differences in aerobic capacity and anthropometry in HPF and LPF. A HPF showed significantly higher VO2peak/kg values compared with LPF (p < 0.001) with no difference in first ventilatory threshold VO2VT1. B Skeletal muscle mass (SSM) was statistically not different between the groups while body fat was higher in LPF (p < 0.001)
Fig. 3
Fig. 3
Correlation of variables known to affect performance, and which are changing during ageing. A Correlation of skeletal muscle mass (SMM) and VO2peak revealed no association in HPF or LPF. B No association was observed regarding age and SMM in both groups
Fig. 4
Fig. 4
MyHC fiber type composition of HPF and LPF. No differences were observed either in Type I fibers (HPF 17.53 ± 5.76%; LPF = 17.06 ± 5.55%), Typ IIa (HPF 36.43 ± 4.34%; LPF = 37.58 ± 4.02%) or Type IId/x fibers (HPF 46.03 ± 3.76%; LPF = 45.37 ± 5.14%)
Fig. 5
Fig. 5
Changes in serum concentrations of molecules involved in ageing, muscle damage and neurotrophic adaptation. HPF and LPF were examined after an acute exercise test (pre vs. post). A HSP70 showed non-significant higher basal values in HPF (p = 0.069) compared to LPF. B Plasma levels of BDNF were non-significantly higher in HPF pre and post. C Irisin concentrations were pre higher in HPF compared to LPF, but this difference was blunted post. D Serum concentration of inflammation marker Il-6 increased post in HPF and LPF. E Kynurenine did not differ in both groups, but due to an increase in LPF and a decrease in HPF post a tendency for different adaptations (p = 0.0927) was observed

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