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

Abstract

<jats:p>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<jats:sub>PCr</jats:sub>, of postcontraction phosphocreatine recovery, obtained by<jats:sup>31</jats:sup>P magnetic resonance spectroscopy following maximal isometric contractions. While k<jats:sub>PCr</jats:sub>was higher in TA of older than activity-matched younger adults (28%; p = 0.03), older adults had lower k<jats:sub>PCr</jats:sub>in VL (23%; p = 0.04). In OIW compared with OW, k<jats:sub>PCr</jats:sub>was lower in VL (∼45%; p = 0.01), but not different in TA. In contrast, OAM had higher k<jats:sub>PCr</jats:sub>than OM (p = 0.03) in both TA (41%) and VL (54%). In older adults, moderate-to-vigorous PA was positively associated with k<jats:sub>PCr</jats:sub>in VL (r = 0.65, p &lt; 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.</jats:p>

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

“…These results provide strong new evidence that the current body of literature supports the hypothesis that the effects of age vary by muscle. It is likely that this difference across muscles is, in part, due to age-related differences in PA patterns, as suggested by Larsen et al (2012). It has also been suggested (Coggan et al 1990) that the lower maximal whole-body aerobic capacity of older adults, which results in day-to-day activities being performed at a higher relative workload, may be sufficient to result in training-like adaptations in some but not all muscles.…”

“…During locomotion, the tibialis anterior is recruited to a similar extent regardless of walking or running speed; conversely, recruitment of the vastus lateralis increases with speed (Cappellini et al 2006). As such, it has been suggested that higher intensity activities might be needed to preserve oxidative capacity in the KE; indeed, in vivo oxidative capacity in the vastus lateralis of older adults is significantly associated with daily minutes of moderate-to-vigorous PA (Larsen et al 2012). In contrast, DF oxidative D r a f t capacity may be preserved the by usual locomotory activities of healthy, community-dwelling older adults.…”

“…In 4 of the included studies, the number and type of medications that older adults were taking was not specifically addressed (Chilibeck et al 1998;Horská et al 2000;Kutsuzawa et al 2001;Waters et al 2003). In 10 of the included studies, no participants were taking any medications known to affect muscle or metabolic function (Christie et al 2014;Hart et al 2014;Johannsen et al 2011;Kent-Braun and Ng 2000;Lanza et al 2005;Lanza et al 2007;Larsen et al 2012;Layec et al 2015;Layec et al 2013;Tevald et al 2010). In 1 study, 9 out of 22 older women were receiving hormone replacement therapy (Conley et al 2000).…”

“…This rate thus reflects the maximal rate of oxidative phosphorylation in the volume of mitochondria present in the tissue. Currently, it is not clear whether muscle oxidative capacity declines in old age, as some investigators have reported lower oxidative capacity in older than younger individuals (Conley et al 2000;Johannsen et al 2011;Layec et al 2013;McCully et al 1993;Smith et al 1998;Taylor et al 1997), while others found no difference (Chilibeck et al 1998;Christie et al 2014;Hart et al 2014;Horská et al 2000;Kent-Braun and Ng 2000;Kutsuzawa et al 2001;Lanza et al 2005;Lanza et al 2007;Larsen et al 2012;Layec et al 2015;Taylor et al 1984;Tevald et al 2014;Tevald et al 2010;Wray et al 2009) or even a higher capacity in old compared with young (Larsen et al 2012;Tevald et al 2014). It seems that at least a portion of this discrepancy may be due to differences in potential modifiers of oxidative capacity across studies, such as muscle group, habitual physical activity (PA) status, and sex.…”

“…Because PA is well documented to decrease from adulthood into old D r a f t 5 age (Colley et al 2011;Troiano et al 2008), accounting for its effects in studies of agerelated changes in muscle oxidative capacity is essential. Likewise, results from recent studies indicate that different muscles, particularly those involved in locomotion, undergo different age-related changes in habitual loading patterns during movement; these differences have been suggested to explain a portion of the muscle-specific changes in oxidative capacity reported in old age (Larsen et al 2012 Therefore, the purpose of this systematic review and meta-analysis was to obtain a comprehensive, quantitative evaluation of the published literature on in vivo muscle oxidative capacity and aging. We hypothesized that oxidative capacity would be moderated by muscle group, PA, and sex.…”