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.

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 (ATP_max) 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 ATP_max. 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. ATP_max 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 (ATP_max/State 3) by multiple linear regression (Table 2). Measured preferred walking speed was determined over a 400-m walk test.