A biphasic microstructural model of skeletal muscle to study structure-function mechanisms under multiaxial tensile and compressive conditions

Abstract

The passive material properties of skeletal muscle are key to proper force transmission, and changes to muscle microstructure can have deleterious effects on whole tissue function. However, to the best of the authors’ knowledge, it is not currently possible to predict the passive material properties of skeletal muscle with microstructural measurements such as titin isoform type and/or extracellular matrix collagen content, type, or organization. The goals of this work were to 1) develop an experimental dataset at the tissue length scale of passive skeletal muscle under multiaxial loading conditions, 2) develop a biphasic microstructural model of skeletal muscle, and 3) calibrate, validate, and implement such a model. Experimental planar biaxial and semi-confined compression experiments, with intramuscular pressure measurements, were conducted. A microstructural finite element model was developed using the GIBBON toolbox based on a Voronoi-like structure and a multi-domain biphasic, anisotropic, hyper-viscoelastic constitutive approach was used to model muscle fibers and the extracellular matrix. Following model calibration and validation to experimental data (with root mean square error values ranging from 0.5 % - 21 %), a parametric study suggested that tensile properties of the muscle fibers and extracellular matrix affected anisotropic tensile stress-stretch behavior to the greatest extent, while permeability greatly affected compressive stress-stretch behavior. Some parameters, such as extracellular matrix volume fraction and muscle fiber bulk modulus, affected both tensile and compressive stress-stretch behavior. Future work to expand this model into specific impairment conditions or to simulations of whole muscle would be a benefit to the field.

Statement of significance

Skeletal muscle is the primary driver of human locomotion. To better understand how healthy and impaired muscle functions towards the prevention of muscle-related impairments, we can use computational modeling. In this study, we developed a new model of the microstructure of muscle tissue that incorporates fluid, which is typically neglected in computer models of muscle tissue. Collectively, the work suggests that interactions between different tissue components, specifically muscle cells, the extracellular matrix, and fluid can collectively contribute to the mechanical behavior of muscle tissue. Our results can be used to build better computer models of muscle tissue and study specific mechanisms – such as fluid flow in muscle tissue – as ways to prevent muscle injuries such as a pressure ulcer.