Does Dietary-Induced Obesity in Old Age Impair the Contractile Performance of Isolated Mouse Soleus, Extensor Digitorum Longus and Diaphragm Skeletal Muscles?

Abstract

Ageing and obesity independently have been shown to significantly impair isolated muscle contractile properties, though their synergistic effects are poorly understood. We uniquely examined the effects of 9 weeks of a high-fat diet (HFD) on isometric force, work loop power output (PO) across a range of contractile velocities, and fatigability of 79-week-old soleus, extensor digitorum longus (EDL) and diaphragm compared with age-matched lean controls. The dietary intervention resulted in a significant increase in body mass and gonadal fat pad mass compared to the control group. Despite increased muscle mass for HFD soleus and EDL, absolute isometric force, isometric stress (force/CSA), PO normalised to muscle mass and fatigability was unchanged, although absolute PO was significantly greater. Obesity did not cause an alteration in the contractile velocity that elicited maximal PO. In the obese group, normalised diaphragm PO was significantly reduced, with a tendency for reduced isometric stress and fatigability was unchanged. HFD soleus isolated from larger animals produced lower maximal PO which may relate to impaired balance in older, larger adults. The increase in absolute PO is smaller than the magnitude of weight gain, meaning in vivo locomotor function is likely to be impaired in old obese adults, with an association between greater body mass and poorer normalised power output for the soleus. An obesity-induced reduction in diaphragm contractility will likely impair in vivo respiratory function and consequently contribute further to the negative cycle of obesity.

Keywords: ageing; muscle; obesity; power; work loop.

Figure 1

The effect of 9 weeks of a high-fat diet (HFD) on the absolute maximal isometric force (A,C) and maximal isometric stress (B,D,E) of isolated mouse soleus (A,B), EDL (C,D) and diaphragm (E) from 79-week-old mice. n = 10 per muscle per group. Absolute force is not presented for diaphragm due to slight differences in the segment of the diaphragm taken for each experiment. The • symbol indicates a statistical tendency (P = 0.08) for isometric stress to be lower in the HFD group (ES = 0.78).

Figure 2

The effect of 9 weeks of a high-fat diet (HFD) on the power output-cycle frequency relationship for absolute power output (PO) (milliWatts; A,C) and normalised PO (Watts per kilogram of muscle mass; B,D,E) of isolated mouse soleus (A,B), EDL (C,D) and diaphragm (E) for the control or HFD groups. n = 10 per muscle. Absolute power is not presented for diaphragm due to slightly different segments of the diaphragm being used for each experiment. A * symbol denotes a significant difference in power output between each experimental group at a given cycle frequency.

Figure 3

The relationship between whole animal body mass and normalized work loop power for control (A,C,E) and HFD (B,D,F) soleus (A,B), EDL (C,D) and diaphragm (E,F) experimental groups. n = 10 per muscle per group. For figure (B) the lines represent a first-order polynomial fitted to the data using a least squares regression and the 95% confidence limits of this line.

Figure 4

The effect of dietary-induced obesity on 79-week-old mice on diaphragm work loop shapes for the control (solid) or HFD (dashed) groups at a cycle frequency of 7 Hz, where maximal power output was elicited. Figures plotted as force against strain amplitude (%L₀). The third work loop of the set of four work loop stimulations is shown for each group. Work loops interpreted in the anticlockwise direction from 0 of strain amplitude.

Figure 5

The effect of 9 weeks of a HFD on the fatigue resistance (A,C,E) and recovery of power (B,D,F) of maximally stimulated mouse soleus (A,B), EDL (C,D) and diaphragm (E,F) for the control and HFD groups. Values presented as mean ± S.E.M. A * denotes a significant (P < 0.05) difference in recovery of power between experimental groups at a given time point.