Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior

Abstract

There is discrepancy in the literature regarding the degree to which old age affects muscle bioenergetics. These discrepancies are likely influenced by several factors, including variations in physical activity (PA) and differences in the muscle group investigated. To test the hypothesis that age may affect muscles differently, we quantified oxidative capacity of tibialis anterior (TA) and vastus lateralis (VL) muscles in healthy, relatively sedentary younger (8 YW, 8 YM; 21-35 years) and older (8 OW, 8 OM; 65-80 years) adults. To investigate the effect of physical activity on muscle oxidative capacity in older adults, we compared older sedentary women to older women with mild-to-moderate mobility impairment and lower physical activity (OIW, n = 7), and older sedentary men with older active male runners (OAM, n = 6). Oxidative capacity was measured in vivo as the rate constant, k(PCr), of postcontraction phosphocreatine recovery, obtained by (31)P magnetic resonance spectroscopy following maximal isometric contractions. While k(PCr) was higher in TA of older than activity-matched younger adults (28%; p = 0.03), older adults had lower k(PCr) in VL (23%; p = 0.04). In OIW compared with OW, k(PCr) was lower in VL (∼45%; p = 0.01), but not different in TA. In contrast, OAM had higher k(PCr) than OM (p = 0.03) in both TA (41%) and VL (54%). In older adults, moderate-to-vigorous PA was positively associated with k(PCr) in VL (r = 0.65, p < 0.001) and TA (r = 0.41, p = 0.03). Collectively, these results indicate that age-related changes in oxidative capacity vary markedly between locomotory muscles, and that altered PA behavior may play a role in these changes.

Fig. 1

Recovery of PCr following contraction in 1 subject. Phosphocreatine (PCr, % of rest) recovered in an exponential manner following a 24-s maximal voluntary isometric contraction of vastus lateralis in a representative young male subject. Recovery data are fit with a mono-exponential equation. Under these conditions, the rate constant of this fit (k_PCr) reflects the capacity of the muscle for oxidative ATP production in vivo.

Fig. 2

Muscle oxidative capacity in tibialis anterior (TA) and vastus lateralis (VL). (A) In younger adults (n = 16), k_PCr was higher in VL than TA (*p = 0.02), while older adults (n = 16) had higher k_PCr in TA than VL (^†p = 0.04). Compared with younger participants, the older participants had higher k_PCr in TA (^‡p = 0.03), but lower k_PCr in VL (^§p = 0.04). (B) In VL, but not TA, k_PCr was lower in older, physically-impaired women (OIW, n = 7) compared with older, unimpaired women (OW, n = 8; *p = 0.01). Additionally, k_PCr of TA was higher than VL (^†p = 0.01). (C) Older active men (OAM, n = 6) had higher k_PCr than relatively sedentary older men (OM, n = 8) in both TA and VL (*p = 0.03), and k_PCr was higher in TA than in VL (^†p = 0.01). Data are means ± SD.

Fig. 3

Associations between muscle oxidative capacity and daily minutes of moderate- to vigorous-intensity physical activity (MVPA) in older adults. There was a modest positive association between MVPA and k_PCr in tibialis anterior (TA) (top panel, p = 0.03, n = 29), and a stronger association between MVPA and k_PCr in vastus lateralis (VL) (bottom panel, p < 0.001, n = 26). Data from 2 OIW and 1 OW are missing for k_PCr in the VL because of technical problems. OM, older healthy men; OW, older healthy women; OAM, older active men; OIW, older women with mobility impairments.