The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese

Abstract

Skeletal muscle accumulates intramuscular fat through age and obesity. Muscle quality, a measure of muscle strength per unit size, decreases in these conditions. It is not clear how fat influences this loss in performance. Changes to structural parameters (e.g. fibre pennation and connective tissue properties) affect the muscle quality. This study investigated the mechanisms that lead to deterioration in muscle performance due to changes in intramuscular fat, pennation and aponeurosis stiffness. A finite-element model of the human gastrocnemius was developed as a fibre-reinforced composite biomaterial containing contractile fibres within the base material. The base-material properties were modified to include intramuscular fat in five different ways. All these models with fat generated lower fibre stress and muscle quality than their lean counterparts. This effect is due to the higher stiffness of the tissue in the fatty models. The fibre deformations influence their interactions with the aponeuroses, and these change with fatty inclusions. Muscles with more compliant aponeuroses generated lower forces. The muscle quality was further reduced for muscles with lower pennation. This study shows that whole-muscle force is dependent on its base-material properties and changes to the base material due to fatty inclusions result in reductions to force and muscle quality.

Keywords: ageing; connective tissue stiffness; fibre pennation; finite-elements; muscle model; obesity.

Figure 1.

Sample geometries of simplified human lateral gastrocnemius (LG) muscle with initial pennation of 10° (a) and 20° (b). Note that the change in cross-sectional area is only due to initial pennation because the fibre length and belly length are constant. Muscle tissue is shown in light grey and aponeuroses in dark grey. The belly and aponeuroses extended out of plane to a width of 55 mm.

Figure 2.

Stress–stretch curves for fat (dotted), base muscle (dashed) and whole muscle (base + fibres; solid) materials used in simulations. The slope of the curves at each stretch is a representative of tissue stiffness where the combined muscle tissue has a greater stiffness than the fat or muscle base materials.

Figure 3.

A muscle belly geometry with 15° pennation angle and 20% sparse fat distribution (M5 variant). The dots show the positions of the integration points with aponeuroses (grey), muscle (red) and fat (yellow) properties.

Figure 4.

The clump fat simulation. The integration points for a 15° muscle geometry (a) with cutting planes corresponding to transverse (b) and longitudinal (c) sections of the muscle. The muscle points are shown in red, fat points are in yellow and aponeurosis points are shown in grey. The deformed shape of the muscle belly at 20% activity (d) is coloured with a contour showing the magnitude of the displacement of the integration points. Comparison of the muscle belly force between the clumped-fat simulation, the lean variants M1–M2 and variant M5 that had a sparse distribution of extracellular fat for simulations with the same initial geometry and connective tissue properties, and X = 10 (e).

Figure 5.

Force–activation plots for the different variants M1–M6. Lines show variant M1 (black circles), M2 (red diamonds), M3 (blue squares), M4 (green triangles), M5 (purple inverted triangles) and M6 (orange stars) at 2% (a), 10% (b) and 20% (c) fat levels.

Figure 6.

Main effects of the fat level, model variant, pennation and aponeurosis stiffness on the final pennation, muscle fibre length, stress and force. Points show the least-squares means, with their standard errors.