Fiber Rearrangement and Matrix Compression in Soft Tissues: Multiscale Hypoelasticity and Application to Tendon

Front Bioeng Biotechnol. 2021 Oct 12:9:725047. doi: 10.3389/fbioe.2021.725047. eCollection 2021.

Abstract

It is widely accepted that the nonlinear macroscopic mechanical behavior of soft tissue is governed by fiber straightening and re-orientation. Here, we provide a quantitative assessment of this phenomenon, by means of a continuum micromechanics approach. Given the negligibly small bending stiffness of crimped fibers, the latter are represented through a number of hypoelastic straight fiber phases with different orientations, being embedded into a hypoelastic matrix phase. The corresponding representative volume element (RVE) hosting these phases is subjected to "macroscopic" strain rates, which are downscaled to fiber and matrix strain rates on the one hand, and to fiber spins on the other hand. This gives quantitative access to the fiber decrimping (or straightening) phenomenon under non-affine conditions, i.e. in the case where the fiber orientations cannot be simply linked to the macroscopic strain state. In the case of tendinous tissue, such an RVE relates to the fascicle material with 50 μm characteristic length, made up of crimped collagen bundles and a gel-type matrix in-between. The fascicles themselves act as parallel fibers in a similar matrix at the scale of a tissue-related RVE with 500 μm characteristic length. As evidenced by a sensitivity analysis and confirmed by various mechanical tests, it is the initial crimping angle which drives both the degree of straightening and the shape of the macroscopic stress-strain curve, while the final linear portion of this curve depends almost exclusively on the collagen bundle elasticity. Our model also reveals the mechanical cooperation of the tissue's key microstructural components: while the fibers carry tensile forces, the matrices undergo hydrostatic pressure.

Keywords: fiber decrimping; homogenized stiffness; micromechanics; multiscale hypoelasticity; scale-dependent strain.