The effects of age on kinetics of oxygen uptake and phosphocreatine in humans during exercise

Chilibeck, PD; Paterson, D. H.; McCreary, C.; Marsh, Greg D.; Cunningham, D. A.; Thompson, R. Terry

doi:10.1113/expphysiol.1998.sp004087

Cited by 47 publications

(44 citation statements)

References 27 publications

(57 reference statements)

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“…This result is consistent with previous studies of muscle bioenergetics in aging (7,43,48,49). The current study also extends information regarding submaximal contraction intensities (7,43), where we found a greater oxidative ratio in both older groups compared with young at 50% MVC, but not at 20% MVC. This greater relative ATP OX in the older groups is also consistent with our observed main effect of group for the absolute ATP OX (Fig.…”

Section: Atp Productionsupporting

confidence: 82%

Human skeletal muscle metabolic economy in vivo: effects of contraction intensity, age, and mobility impairment

Christie

Tonson

Larsen

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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Christie AD, Tonson A, Larsen RG, DeBlois JP, Kent JA. Human skeletal muscle metabolic economy in vivo: effects of contraction intensity, age, and mobility impairment. Am J Physiol Regul Integr Comp Physiol 307: R1124 -R1135, 2014. First published August, 27, 2014; doi:10.1152/ajpregu.00083.2014.-We tested the hypothesis that older muscle has greater metabolic economy (ME) in vivo than young, in a manner dependent, in part, on contraction intensity. Twenty young (Y; 24 Ϯ 1 yr, 10 women), 18 older healthy (O; 73 Ϯ 2, 9 women) and 9 older individuals with mild-to-moderate mobility impairment (OI; 74 Ϯ 1, 7 women) received stimulated twitches (2 Hz, 3 min) and performed nonfatiguing voluntary (20, 50, and 100% maximal; 12 s each) isometric dorsiflexion contractions. Torque-time integrals (TTI; Nm·s) were calculated and expressed relative to maximal fat-free muscle cross-sectional area (cm 2 ), and torque variability during voluntary contractions was calculated as the coefficient of variation. Total ATP cost of contraction (mM) was determined from flux through the creatine kinase reaction, nonoxidative glycolysis and oxidative phosphorylation, and used to calculate ME (Nm·s·cm Ϫ2 ·mM ATP Ϫ1 ). While twitch torque relaxation was slower in O and OI compared with Y (P Յ 0.001), twitch TTI, ATP cost, and economy were similar across groups (P Ն 0.15), indicating comparable intrinsic muscle economy during electrically induced isometric contractions in vivo. During voluntary contractions, normalized TTI and total ATP cost did not differ significantly across groups (P Ն 0.20). However, ME was lower in OI than Y or O at 20% and 50% MVC (P Յ 0.02), and torque variability was greater in OI than Y or O at 20% MVC (P Յ 0.05). These results refute the hypothesis of greater muscle ME in old age, and provide support for lower ME in impaired older adults as a potential mechanism or consequence of age-related reductions in functional mobility. bioenergetics; mitochondria; creatine kinase; glycolysis; oxidative phosphorylation WHILE MANY OF THE CHANGES in neuromuscular properties that occur with advanced age, such as declines in strength and contractile velocity (5, 64), can be detrimental to physical function, some age-related physiological changes may act in a compensatory manner and, thereby, help maintain function to some degree. For instance, it has been suggested that a greater proportion of type I muscle fibers (35,55,56), slowed contractile properties (62, 71), and slower motor unit discharge rates, particularly during maximal contractions (8,12,37,38,68), may place older muscle at an economic advantage (41, 49). While age-related differences in muscle metabolic economy (ME; mass-normalized torque produced per unit ATP consumed) have been shown in rat muscle (13, 32), a systematic analysis of muscle ME in aging humans has only recently begun (41,54). Such a focus on muscle ME is critical to informing studies of age-related changes in the energy cost of whole body activities, such as walking, which generally involve measures of...

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Section: Atp Productionsupporting

confidence: 82%

Human skeletal muscle metabolic economy in vivo: effects of contraction intensity, age, and mobility impairment

Christie

Tonson

Larsen

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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“…With regard to in vivo oxidative capacity of the MG, the present results are consistent with two prior studies (Chilibeck et al 1998;Wray et al 2009). They are not consistent with the results of one in vivo study (McCully et al 1991) and two in vitro (enzyme activities) studies (Coggan et al 1992;Houmard et al 1998), all of which showed lower oxidative capacity in the O subjects.…”

Section: Age and Oxidative Capacitysupporting

confidence: 82%

“…The TA is largely composed of type I fibers (75 % type I; Gregory et al 2001), while the MG is mixed in fibertype composition (50 % type I; Edgerton et al 1975). Furthermore, while most studies of the TA do not report lower oxidative capacity in O adults (Kent-Braun and Ng 2000; Lanza et al 2005Lanza et al , 2007Larsen et al 2012b;Tevald et al 2010), reports on the MG differ, with studies reporting either lower (McCully et al 1991;Coggan et al 1992;Houmard et al 1998) or similar (Chilibeck et al 1998;Wray et al 2009) oxidative capacity in O compared to Y adults. Based on the previously discussed evidence that age-related changes in several aspects of muscle performance are smaller in the TA than the MG, we hypothesized that oxidative capacity would be preserved in the TA, but not the MG, of O subjects.…”

Section: Introductionmentioning

confidence: 95%

“…For example, oxidative capacity, which is one measure of mitochondrial function, has been reported by some to decline in older (O) adults (Conley et al 2000;Short et al 2005;Coggan et al 1992;McCully et al 1991;Pastoris et al 2000;Karakelides et al 2010), while others report no change with aging Larsen et al 2012b;Hutter et al 2007;Rasmussen et al 2003;Tevald et al 2010;Chilibeck et al 1998). A number of factors, including the means of assessing mitochondrial function, the health and physical activity (PA) status of the study participants, and the muscle group studied, apparently contribute to these conflicting findings (Larsen et al 2012b).…”

Section: Introductionmentioning

confidence: 95%

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Effect of age on in vivo oxidative capacity in two locomotory muscles of the leg

Tevald

Foulis

Kent

2014

AGE

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To determine the effects of age and sex on in vivo mitochondrial function of distinct locomotory muscles, the tibialis anterior (TA) and medial gastrocnemius (MG), of young (Y; 24±3 years) and older (O; 69±4) men (M) and women (W) of similar overall physical activity (PA) was compared. In vivo mitochondrial function was measured using phosphorus magnetic resonance spectroscopy, and PA and physical function were measured in all subjects. Overall PA was similar among the groups, although O (n=17) had fewer daily minutes of moderate-to-vigorous PA (p=0.001), and slowed physical function (p<0.05 for all variables), compared with Y (n=17). In TA, oxidative capacity (V max ; mM s −1 ) was higher in O than Y (p<0.001; Y= 0.90±0.12; O=1.12±0.18). There was no effect of age in MG (p =0.5; Y= 0.91 ± 0.17; O = 0.96 ± 0.24), but women had higher oxidative capacity than men (p= 0.007; M=0.84±0.18; W=1.03±0.18). In vivo mitochondrial function was preserved in healthy O men and women, despite lower intensity PA and physical function in this group. The extent to which compensatory changes in gait may be responsible for this preservation warrants further investigation. Furthermore, women had higher oxidative capacity in the MG, but not the TA.

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“…Skeletal muscle energetics were assessed through 31 P NMR spectroscopy (Fig. 1B), and from this spectra PCr depletion and recovery kinetics were evaluated as an index of muscle oxidative demand and capacity, respectively (6,14,24). Both of these measurements are unique in that they allow for the probing of perfusion and metabolism in a noninvasive manner with very high-spatial and temporal resolution and do so in a focused ROI within the exercising muscle tissue.…”

Section: Discussionmentioning

confidence: 99%

Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics

Wray

Nishiyama

Wary

et al. 2009

American Journal of Physiology-Heart and Circulatory Physiology

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Wray DW, Nishiyama SK, Monnet A, Wary C, Duteil SS, Carlier PG, Richardson RS. Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics. Am J Physiol Heart Circ Physiol 297: H1870 -H1875, 2009. First published September 18, 2009 doi:10.1152/ajpheart.00709.2009.-We sought to examine the potential role of oxidative stress on skeletal muscle function with advancing age. Nuclear magnetic resonance (NMR) was employed to simultaneously assess muscle perfusion (arterial spin labeling) and energetics ( 31 P NMR spectroscopy) in the lower leg of young (26 Ϯ 5 yr, n ϭ 6) and older (70 Ϯ 5 yr, n ϭ 6) healthy volunteers following the consumption of either placebo (PL) or an oral antioxidant (AO) cocktail (vitamins C and E and ␣-lipoic acid), previously documented to decrease plasma free radical concentration. NMR measurements were made during and after 5 min of moderate intensity (Ϸ5 W) plantar flexion exercise. AO administration significantly improved end-exercise perfusion (AO, 50 Ϯ 5, and PL, 43 Ϯ 4 ml⅐ 100 g Ϫ1 ⅐ min Ϫ1 ) and postexercise perfusion area under the curve (AO, 1,286 Ϯ 236, and PL, 866 Ϯ 144 ml/100 g) in older subjects, whereas AO administration did not alter hemodynamics in the young group. Concomitantly, muscle oxidative capacity (time constant of phosphocreatine recovery, ) was improved following AO in the older (AO, 43 Ϯ 1, and PL, 51 Ϯ 7 s) but not the young (AO, 54 Ϯ 5, and PL, 48 Ϯ 7 s) group. These findings support the concept that oxidative stress may be partially responsible for the age-related decline in skeletal muscle perfusion during physical activity and reveal a muscle metabolic reserve capacity in the elderly that is accessible under conditions of improved perfusion. leg blood flow; oxidative capacity; exercise; nuclear magnetic resonance WITH ADVANCING AGE, structural and functional changes in the peripheral vasculature develop with potentially deleterious consequences, including a diminished perfusion of skeletal muscle both at rest and during exercise (3,7,8,22,25,26,30,36). The detrimental effects of this age-associated decline in muscle perfusion and the associated decrement in O 2 delivery could be closely linked to muscle energetics, as evidenced by the previously demonstrated decline in skeletal muscle oxidative capacity under O 2 supply-limited conditions in young, healthy individuals (15, 16). Despite the potentially negative impact of these age-associated changes, the practical consequence of reduced skeletal muscle blood flow in this cohort remains poorly understood.The paucity of information concerning the effects of reduced perfusion on muscle function with healthy aging may be due in part to the difficulty of simultaneously assessing perfusion and metabolism within skeletal muscle. Using multiparametric nuclear magnetic resonance (NMR) techniques, we have begun to address this issue and have recently documented that the age-related decline in bulk limb blood flow is also evident when perfusion within the skeletal muscle is examined duri...

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The effects of age on kinetics of oxygen uptake and phosphocreatine in humans during exercise

Cited by 47 publications

References 27 publications

Human skeletal muscle metabolic economy in vivo: effects of contraction intensity, age, and mobility impairment

Human skeletal muscle metabolic economy in vivo: effects of contraction intensity, age, and mobility impairment

Effect of age on in vivo oxidative capacity in two locomotory muscles of the leg

Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics

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