Investigating Passive Muscle Mechanics With Biaxial Stretch.

Benjamin B Wheatley

doi:10.3389/fphys.2020.01021

Abstract

IntroductionThe passive stiffness of skeletal muscle can drastically affect muscle function in vivo, such as the case for fibrotic tissue or patients with cerebral palsy. The two constituents of skeletal muscle that dominate passive stiffness are the intracellular protein titin and the collagenous extracellular matrix (ECM). However, efforts to correlate stiffness and measurements of specific muscle constituents have been mixed, and thus the complete mechanisms for changes to muscle stiffness remain unknown. We hypothesize that biaxial stretch can provide an improved approach to evaluating passive muscle stiffness.MethodsWe performed planar biaxial materials testing of passively stretched skeletal muscle and identified three previously published datasets of uniaxial materials testing. We developed and employed a constitutive model of passive skeletal muscle that includes aligned muscle fibers and dispersed ECM collagen fibers with a bimodal von Mises distribution. Parametric modeling studies and fits to experimental data (both biaxial and previously published) were completed.ResultsBiaxial data exhibited differences in time dependent behavior based on orientation (p < 0.0001), suggesting different mechanisms supporting load in the direction of muscle fibers (longitudinal) and in the perpendicular (transverse) directions. Model parametric studies and fits to experimental data exhibited the robustness of the model (<20% error) and how differences in tissue stiffness may not be observed in uniaxial longitudinal stretch, but are apparent in biaxial stretch.ConclusionThis work presents novel materials testing data of passively stretched skeletal muscle and use of constitutive modeling and finite element analysis to explore the interaction between stiffness, constituent variability, and applied deformation in passive skeletal muscle. The results highlight the importance of biaxial stretch in evaluating muscle stiffness and in further considering the role of ECM collagen in modulating passive muscle stiffness.

Highlights

The passive stiffness of skeletal muscle can drastically affect muscle function in vivo, such as the case for fibrotic tissue or patients with cerebral palsy
The two constituents that are recognized as the major contributors to the tensile stiffness of passive skeletal muscle are (1) muscle fibers, and (2) the collagenous extracellular matrix (ECM) that provides the hierarchical organization of skeletal muscle (Huijing, 1999; Gillies and Lieber, 2011; Brynnel et al, 2018; Meyer and Lieber, 2018)
We propose the use of computational modeling – in particular finite element analysis (FEA) – to study the passive response of skeletal muscle under both uniaxial and biaxial stretch

Summary

Introduction

The passive stiffness of skeletal muscle can drastically affect muscle function in vivo, such as the case for fibrotic tissue or patients with cerebral palsy. The human body is comprised of roughly 40% skeletal muscle – the tissue that drives locomotion, enables fine movements, and provides the capability to breathe in humans and animals alike. This is due to the innate ability of skeletal muscle to generate contractile force and drive movement of our musculoskeletal system. The two constituents that are recognized as the major contributors to the tensile stiffness of passive skeletal muscle are (1) muscle fibers (cells), and (2) the collagenous extracellular matrix (ECM) that provides the hierarchical organization of skeletal muscle (Huijing, 1999; Gillies and Lieber, 2011; Brynnel et al, 2018; Meyer and Lieber, 2018). It should be noted here that throughout the manuscript we use the term “stiffness” to represent the intricate non-linear, anisotropic, and variable tensile material properties of passive skeletal muscle, and not the structural property k often used in Hooke’s Law that characterizes the structural stiffness of a physical object with specific dimensions and material properties

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