Insights into central and peripheral factors affecting the “oxidative performance” of skeletal muscle in aging

Abstract

During exercises with relatively small muscle masses, limitations to exercise performance by the cardiovascular system should be significantly reduced, allowing one to fully-test the "oxidative potential" of the investigated muscles. Ten elderly males (E, 77.8 +/- 2.9 years [x +/- SD]) and eight young controls (Y, 26.6 +/- 3.0) underwent incremental exercises to voluntary exhaustion on a dynamic leg-extension (dominant limb) machine (knee-extension, KE) and on a cycloergometer (CYCLO). During KE the load was increased every 3 min to loads corresponding to 20, 40 and 60% of the force of one-repetition maximum (1RM). The following variables were determined (vastus lateralis muscle): concentration changes of deoxygenated haemoglobin and myoglobin (Delta[deoxy(Hb + Mb)]) by near-infrared spectroscopy (NIRS), expressed as percentage of the maximal value obtained during transient limb ischemia, and taken as an index of O2 extraction; root mean square (RMS) and median power frequency (MDF) by electromyography. The total lifted load during KE and peak workload during CYCLO were lower in E versus Y (620.4 +/- 321.9 kg vs. 1347.4 +/- 458.7; 113.5 +/- 23.9 W vs. 224.3 +/- 41.0, respectively). During CYCLO Delta[deoxy(Hb + Mb)] peak (i.e. the value determined at exhaustion) was lower in E (44.5 +/- 17.7%) versus Y (67.1 +/- 22.9), whereas during KE Delta[deoxy(Hb + Mb)] peak was higher in E (56.8 +/- 20.9%) versus Y (38.6 +/- 15.8). "Thresholds", that is abrupt increases in RMS slopes, were detected in Y but not in E, suggesting less recruitment or a preferential atrophy of type 2 fibers in the elderly. These findings, associated with the preserved capacity of O2 extraction, suggest a shift towards oxidative metabolism in skeletal muscles of 78 year-old subjects, which could preserve, at least in part, their capacity to carry out exercise.

Effect of ageing on hypoxic exercise cardiorespiratory, muscle and cerebral oxygenation responses in healthy humans

“…In the present study, normoxic exercise induced similar changes in vastus lateralis NIRS parameters in young and older individuals; however, the hypoxia-induced larger increase in vastus lateralis HHb during exercise in young subjects suggests significantly greater deoxygenation and oxygen extraction in response to hypoxia compared with older subjects. Hence, although some previous data suggested impaired muscle hypoxic vasodilator responses at rest with ageing (Ferri et al 2007;Kirby et al 2012), the present study does not suggest an impairment in muscle hypoxic response during exercise in older compared with young subjects. This greater hypoxia-induced increase in oxygen extraction may be needed because, despite the larger absolute power output and therefore oxygen requirement during exercise in young individuals, a similar increase in vastus lateralis muscle blood flow (as suggested by similar HbO 2 and HbTot during exercise in both groups) was observed in young compared with older subjects.…”

“…Only one study recently evaluated the hypoxic cerebrovascular response in older individuals at rest and reported blunted cerebral blood velocity sensitivity to hypoxia compared with young control subjects (Hartmann et al 2015). At the muscle level, reduced oxygenation has been reported in older individuals at rest and during exercise in normoxia (Costes et al 1999;Ferri et al 2007). Some results suggest that the muscle vasodilator response to hypoxia may be reduced at rest in the elderly (Kirby et al 2012) and either reduced or similar during exercise (Casey et al 2011;Limberg et al 2012) in older individuals compared with young control subjects.…”

Near-infrared spectroscopy detects age-related differences in skeletal muscle oxidative function: promising implications for geroscience

“…The exact mechanism responsible for the observed agerelated decline in skeletal muscle oxidative function is beyond the scope of the present investigation, but is likely multifactorial. Aging has indeed been associated with a marked reduction in mitochondrial-specific oxidative enzymes (Cooper et al 1992;Boffoli et al 1994;Rooyackers et al 1996), mitochondrial DNA mutations (Cooper et al 1992;Boffoli et al 1994;Michikawa et al 1999), oxidative damage by reactive oxygen species (Papa 1996), reduced synthesis of mitochondrial proteins (Rooyackers et al 1996), and increased ATP and/or oxidative cost during exercise (Ferri et al 2007;Layec et al 2014). However, several studies have challenged the concept that aging itself affects muscle bioenergetics (Kutsuzawa et al 2001;Carlson et al 2008;Tevald et al 2014), and instead suggest that muscle oxidative function is far more dependent on the muscle group studied (Kent-Braun and Ng 2000;Lanza et al 2005Lanza et al , 2007Larsen et al 2012) (locomotor vs. nonlocomotor) and/or the physical activity level of the individual (Brierley et al 1996;Rasmussen et al 2003;Rimbert et al 2004;Larsen et al 2012).…”

Age and microvascular responses to knee extensor exercise in women

“…There were no age-group differences for comparisons at rest or during exercise Eur J Appl Physiol (2008) 103:343-351 349 oxidative capacity declines by as much as 50% in the leg in older humans (Conley et al 2000). Changes in fiber type (Coggan et al 1992;Short et al (2005), motor unit recruitment (Ferri et al 2007) and reductions in flow directed to oxidative fibers (Musch et al 2004) with age may also influence muscle metabolism and alter the relation between leg _ VO 2 and absolute work. Alternatively, the NIRS-derived measure of microvascular blood volume-the estimated change in the total hemoglobin (HHb + O 2 Hb) signal relative to rest-was not significantly different between young and older women during exercise in the current study (Fig.…”

“…Data regarding compensatory changes in oxygen extraction in aged individuals who exhibit reduced leg blood flow during dynamic exercise are equivocal, with reports of both greater leg oxygen extraction during cycling exercise in middle-aged (Wahren et al 1974), older sedentary ) and older trained (Proctor et al 1998) men as well as similar oxygen extraction in older sedentary men (Beere et al 1999) and older normally active women (Proctor et al 2003). Limited data regarding knee extensor exercise are similarly ambiguous Ferri et al 2007;Lawrenson et al 2003); discrepancies may be attributable to the age, fitness or sex of the subject populations studied as well as the methodology used to investigate oxygen extraction (i.e., direct vs. indirect measurements). Using NIRS based estimates of microvascular oxygenation, we did not find evidence of augmented oxygen extraction in older women ( Fig.…”