Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults

Abstract

Background: Lower ambulatory performance with aging may be related to a reduced oxidative capacity within skeletal muscle. This study examined the associations between skeletal muscle mitochondrial capacity and efficiency with walking performance in a group of older adults.

Methods: Thirty-seven older adults (mean age 78 years; 21 men and 16 women) completed an aerobic capacity (VO2 peak) test and measurement of preferred walking speed over 400 m. Maximal coupled (State 3; St3) mitochondrial respiration was determined by high-resolution respirometry in saponin-permeabilized myofibers obtained from percutanous biopsies of vastus lateralis (n = 22). Maximal phosphorylation capacity (ATPmax) of vastus lateralis was determined in vivo by (31)P magnetic resonance spectroscopy (n = 30). Quadriceps contractile volume was determined by magnetic resonance imaging. Mitochondrial efficiency (max ATP production/max O2 consumption) was characterized using ATPmax per St3 respiration (ATPmax/St3).

Results: In vitro St3 respiration was significantly correlated with in vivo ATPmax (r (2) = .47, p = .004). Total oxidative capacity of the quadriceps (St3*quadriceps contractile volume) was a determinant of VO2 peak (r (2) = .33, p = .006). ATPmax (r (2) = .158, p = .03) and VO2 peak (r (2) = .475, p < .0001) were correlated with preferred walking speed. Inclusion of both ATPmax/St3 and VO2 peak in a multiple linear regression model improved the prediction of preferred walking speed (r (2) = .647, p < .0001), suggesting that mitochondrial efficiency is an important determinant for preferred walking speed.

Conclusions: Lower mitochondrial capacity and efficiency were both associated with slower walking speed within a group of older participants with a wide range of function. In addition to aerobic capacity, lower mitochondrial capacity and efficiency likely play roles in slowing gait speed with age.

Figures

Figure 1.

Concept map illustrating age-related changes in muscle physiology and how they contribute to reduced walking speed in older adults. This study examined the relationships between muscle mitochondrial capacity/efficiency, aerobic capacity, and walking speed in older adults. VO2 peak = maximal oxygen consumption during maximal dynamic exercise. This is an index of whole-body aerobic capacity.

Figure 2.

Pearson correlation of maximum respiratory capacity with maximum oxidative phosphorylation in muscle. State 3 respiration in permeabilized fiber bundles was determined by high-resolution respirometry. Maximum oxidative phosphorylation (ATPmax) elicited by exercise was determined by phosphorus magnetic resonance spectroscopy (31P MRS). DW = dry weight.

Figure 3.

Pearson correlation of whole-body aerobic capacity with muscle oxidative capacity. Aerobic capacity (VO2 peak) was determined by a graded exercise test. Muscle oxidative capacity was defined as the product of State 3 respiration and quadriceps contractile volume (State 3 respiration * quadriceps contractile volume). DW = dry weight.

Figure 4.

Pearson correlation of preferred walking speed with whole-body aerobic capacity and muscle mitochondrial capacity. Panel (A): preferred walking speed versus VO2 peak. Panel (B): preffered walking speed versus ATPmax. Aerobic capacity normalized to body weight (mL/kgBW/min) was determined by a graded exercise test. Preferred walking speed was determined over a 400-m walk test. ATPmax was determiend by 31P magnetic resonance spectroscopy.

Figure 5.

Pearson correlation of predicted preferred walking speed versus measured preferred walking speed. Walking speed was predicted from aerobic capacity (VO2 peak) and muscle mitochondrial efficiency (ATPmax/State 3) by multiple linear regression (Table 2). Measured preferred walking speed was determined over a 400-m walk test.