In vivoevidence of an age-related increase in ATP cost of contraction in the plantar flexor muscles

Abstract

Impaired skeletal muscle efficiency potentially contributes to the age-related decline in exercise capacity and may explain the altered haemodynamic response to exercise in the elderly. Thus we examined whether (i) the ATP cost of contraction increases with age, and (ii) this results in altered convective O(2) delivery to maintain microvascular oxygenation in the calf muscle. To this aim, we used an integrative experimental approach combining (31)P-MRS (magnetic resonance spectroscopy), Doppler ultrasound imaging and NIRS (near-IR spectroscopy) during dynamic plantar flexion exercise at 40% of WR(max) (maximal power output) in 20 healthy young and 20 older subjects matched for physical activity. The ATP cost of contraction was significantly higher in the old (7.2±4.1 mM/min per W) compared with the young (2.4±1.9 mM/min per W; P<0.05) and this was only significantly correlated with the plantar flexion WR(max) value in the old subjects (r=-0.52; P<0.05). Even when differences in power output were taken into account, end-exercise blood flow (old, 259±168 ml/min per W and young, 134±40 ml/min per W; P<0.05) and convective O(2) delivery (old, 0.048±0.031 l/min per W and young, 0.026±0.008 l/min per W; P<0.05) were greater in the old in comparison with the young subjects. In contrast, the NIRS oxyhaemoglobin, deoxyhaemoglobin and microvascular oxygenation indices were not significantly different between the groups (P>0.05). Therefore the present study reveals that, although the peripheral haemodynamic responses to plantar flexion exercise appear to be appropriate, the elevated energy cost of contraction and associated reduction in the WR(max) value in this muscle group may play a role in limiting exercise capacity with age.

Older men are more fatigable than young when matched for maximal power and knee extension angular velocity is unconstrained

“…This likely indicates that the isokinetic contractions were less energetically demanding than the isotonic contractions for both age groups. Thus, based on previous studies (Layec et al 2014), it seems that the greater fatigability reported here for the isotonic contractions could reflect a larger metabolic cost per contraction during the isotonic task for the older men than young.…”

“…However, the metabolic demand of shortening contractions is greater than that of sustained isometric contractions (Newham et al 1995), and the enhanced energetic cost likely mitigates any age-related metabolic advantage. For example, during constant load sub-maximal isotonic plantar flexions at an effort equivalent to~40 % maximal power output, Layec et al (2014) found that the ATP cost per contraction was remarkably higher for older adults than young. Moreover, this increased energy usage was correlated with age-related impairments in plantar flexor power.…”

“…However, metabolic economy is the same during brief isometric MVCs (Christie et al 2014), and the ATP cost per contraction is even greater during submaximal isotonic plantar flexions (Layec et al 2014) compared with young. During shortening contractions in which joint angular velocity is unconstrained (i.e., isotonic), muscle power is substantially impaired in older individuals.…”

“…Because the torque-power relationship shifted downward and to the left similarly in both tasks and age groups, it seems that the velocity component of power was not a contributing factor to the greater fatigue exhibited by the older men than young when both age groups were matched for maximal power. Although age-related velocity impairments are critical during certain dynamic tasks (Petrella et al 2005;McNeil and Rice 2007;Dalton et al 2010b;Callahan and KentBraun 2011;Dalton et al 2012), other age-related factors, such as reduced metabolic economy or increased ATP cost per contraction (Layec et al 2014;Layec et al 2015), are likely limiting mechanisms of contractile performance during repetitive isotonic contractions when age groups are matched for maximal power.…”

Evaluation of in vivo mitochondrial bioenergetics in skeletal muscle using NMR and optical methods

“…In healthy muscles ATPmax correlates with mitochondrial content measured by citrate synthase activity and ex vivo respiratory capacity in human muscle[41], mitochondrial volume density by EM[42, 43], and maximal mitochondrial respiratory capacity in permeabilized fibers[44]. Multiple studies have found that ATPmax decreases in aged skeletal muscles in mice and humans and increases following exercise training[35, 36, 45], although whether the lower ATPmax is an intrinsic aspect of aging muscle or due to changes in physical activity with age remains controversial[46, 47]. Interestingly, recent work has demonstrated that under conditions of skeletal muscle dysfunction or stress the relationship between ex vivo measures of mitochondria capacity and in vivo ATPmax is not as consistent[34, 35] suggesting that a stressed cellular environment exerts another level of control over mitochondrial function that may not be reflected in ex vivo assays (discussed below).…”