Abstract
Understanding the mechanisms of deformation of biological materials is important for improved diagnosis and therapy, fundamental investigations in mechanobiology, and applications in tissue engineering. Here we demonstrate the essential role of interstitial fluid mobility in determining the mechanical properties of soft tissues. Opposite to the behavior expected for a poroelastic material, the tissue volume of different collagenous membranes is observed to strongly decrease with tensile loading. Inverse poroelasticity governs monotonic and cyclic responses of soft biomembranes, and induces chemo-mechanical coupling, such that tensile forces are modulated by the chemical potential of the interstitial fluid. Correspondingly, the osmotic pressure varies with mechanical loads, thus providing an effective mechanism for mechanotransduction. Water mobility determines the tissue’s ability to adapt to deformation through compaction and dilation of the collagen fiber network. In the near field of defects this mechanism activates the reversible formation of reinforcing collagen structures which effectively avoid propagation of cracks.
Highlights
Understanding the mechanisms of deformation of biological materials is important for improved diagnosis and therapy, fundamental investigations in mechanobiology, and applications in tissue engineering
We show this on the basis of UA and biaxial tensile experiments on human amniotic membrane, bovine liver (Glisson’s) capsule and porcine pericardium, i.e., three different types of biological tissues
The osmotic pressure varies with mechanical loads and, vice-versa, the level of tension for a given deformation depends on the chemical potential of the interstitial fluid
Summary
Understanding the mechanisms of deformation of biological materials is important for improved diagnosis and therapy, fundamental investigations in mechanobiology, and applications in tissue engineering. While the important role of water in creating residual stresses in tissues by swelling has been identified[17], and its impact on the mechanics of collagen on a molecular scale was recently highlighted[18], the present data demonstrate the key role of water mobility in determining the tissue response, and identify an essential deformation mechanism with far-reaching implications for the biomechanics and mechanobiology of soft biological tissues We show this on the basis of UA and biaxial tensile experiments on human amniotic membrane (hAM), bovine liver (Glisson’s) capsule (bGC) and porcine pericardium (pPC), i.e., three different types of biological tissues. The in-plane lateral contraction in UA tensile tests is by a factor of 5 to 10 larger than the one expected for isotropic incompressible materials[23, 26] (Supplementary Fig. 1c) and both this contraction and the volume reduction data are highly reproducible as opposed to the typically large variability of the corresponding tension-elongation curves (Supplementary Fig. 1b–d)
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