The anisotropic mechanical behaviour of passive skeletal muscle tissue subjected to large tensile strain

Abstract

The anisotropic mechanical behaviour of passive skeletal muscle tissue subjected to large tensile strain, Journal of the Mechanical Behavior of Biomedical Materials, http://dx.doi.org/10. 1016/j.jmbbm.2012.09.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AbstractThe passive mechanical properties of muscle tissue are important for many biomechanics applications. However, significant gaps remain in our understanding of the three-dimensional tensile response of passive skeletal muscle tissue to applied loading. In particular, the nature of the anisotropy remains unclear and the response to loading at intermediate fibre directions and the Poisson's ratios in tension have not been reported. Accordingly, tensile tests were performed along and perpendicular to the muscle fibre direction as well as at 30, 45 and 60 degrees to the muscle fibre direction in samples of Longissimus dorsi muscle taken from freshly slaughtered pigs. Strain was measured using an optical non-contact method. The results show the transverse or cross fibre (TT') direction is broadly linear and is the stiffest (77kPa stress at a stretch of 1.1), but that failure occurs at low stretches (approximately λ = 1.15). In contrast the longitudinal or fibre direction (L) is nonlinear and much less stiff (10kPa stress at a stretch of 1.1) but failure occurs at higher stretches (approximately λ = 1.65). An almost sinusoidal variation in stress response was observed at intermediate angles. The following Poisson's ratios were measured: Ѵ LT = Ѵ LT' = 0.47, Ѵ TT' = 0.28 and Ѵ TL = 0.74. These observations have not been previously reported and they contribute significantly to our understanding of the three dimensional deformation response of skeletal muscle tissue.

How does tissue preparation affect skeletal muscle transverse isotropy?

“…Some modeling studies of passive skeletal muscle assume the longitudinal direction is stiffer than the transverse direction (Calvo et al, 2010; Grasa et al, 2011; Hernández-Gascón et al, 2013; Lu et al, 2010). While this is supported by some experimental work (Morrow et al, 2010), there is also data which identifies a stiffer transverse response as compared to the longitudinal direction (Nie et al, 2011; Takaza et al, 2012). These differences may be the result of disparities in experimental protocol and anatomical or species variations, although they are more likely the result of rigor mortis, which results in a stiffening of the tissue (Van Ee et al, 2000; Van Loocke et al, 2006).…”

“…In the case of skeletal muscle these passive properties have a multifaceted purpose: allowing for the transmission of internal force generated at muscle fibers to tendons (Gindre et al, 2013; Huijing, 1999), storing energy during locomotion (Cavanagh and Komi, 1979; Ettema, 1996), and maintaining proper resting length for maximum force generation (Fridén and Lieber, 1998). Muscle fiber alignment results in tissue transverse isotropy (Morrow et al, 2010; Pietsch et al, 2014; Takaza et al, 2012; Van Loocke et al, 2006) as the material properties of the aligned fibers differ from those of the organized extracellular matrix (Meyer and Lieber, 2011). …”

Finite element implementation of a new model of slight compressibility for transversely isotropic materials

“…Certainly such identifications would benefit from tests in different directions (tension, shear, multiaxial loadings) while measuring the volume ratio to make sure that the behaviour is well represented in various loading scenarios. We emphasize the scarcity of such combined experimental data in the literature for transversely isotropic materials, with only for example the work of Takaza et al (2013) for passive muscle tissue. It is also noted that compressibility measurements would be particularly interesting and are strongly needed to feed such models and improve the accuracy of the volumetric response.…”

Skeletal muscle tissue engineering: strategies for volumetric constructs

“…Moreover, the rate of degradation, and the mechanical and topographical characteristics of the scaffold modify the behavior of the surrounding cells (Zhang et al, 2014), and therefore of the vascular compartment; uniform, randomized geometry, such as interconnected pore networks, facilitate the vascularization process, without imparting a definitive structure of the vascular compartment (Levenberg et al, 2005). However, since a functional design is proved to be advantageous in the integration of SMTE constructs (Koffler et al, 2011), and given that the process of vascularization is inextricably bound to the structural development of living tissues (Tirziu and Simons, 2009; Lesman et al, 2010), it is reasonable to assume that the presence of a defined architecture prior to implantation will inform the structure of the resulting implant, facilitating its integration in tissues characterized by a high degree of anisotropy such as skeletal muscle (Takaza et al, 2013). …”

“…The fine structure is particularly evident in decellularized muscles, where the bare extracellular matrix (ECM) forms structures not unlike bundles of flexible straws (Lieber and Fridén, 2000), which is the principal component of the muscle's anisotropic response to stress (Takaza et al, 2013). Blood vessels run along the fascicles in the perimysium and penetrate into the endomysium, forming capillaries that project around the myofibers; due to the elevated metabolic need of the skeletal muscle tissue, each myofiber is connected to a capillary (Figure 1).…”