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.

A total of 37 human and 33 murine skin samples were subjected to uniaxial monotonic, cyclic, and relaxation experiments. Detailed analysis of the three-dimensional kinematic response showed that skin volume is significantly reduced as a consequence of a tensile elongation. This behavior is most pronounced in monotonic but persists in cyclic tests. The dehydration associated with volume loss depends on the osmolarity of the environment, so that tension relaxation changes as a consequence of modifying the ionic strength of the environmental bath. Similar to ex vivo observations, complementary in vivo stretching experiments on human volar forearms showed strong in-plane lateral contraction. A biphasic homogenized model is proposed which allows representing all relevant features of the observed mechanical response.

The interstitial fluid plays an important role for the deformability of soft biological tissues. While its high bulk modulus is often taken as an argument for tissue incompressibility, its ability to move through the interstitial space and across the boundary permits reversible changes of tissue volume through fluid exchange with the environment, which in turn is affected by the osmotic activity of the tissue constituents. Such coupled phenomena of fluid flow and deformation are characteristic both for hydrated biological tissues and swelling polymers, typically treated within the theory of porous media and chemoelasticity, respectively. In this contribution, the two theories are reconciled for biphasic materials with incompressible constituents and an inviscid liquid phase. Based on this analogy, and starting from the chemoelastic approach, a lean theoretical framework for the modelling of biphasic chemomechanical effects in soft biological tissues is presented. It provides access to fluid flux, variations in chemical potential and osmotic pressure in addition to stress and strain in the tissue. The framework is exemplified in application to arterial tissue, modifying and complementing an established monophasic, incompressible model, and the benefits of the alternative chemomechanical representation are illustrated in numerical examples.

Modelling and simulation in mechanobiology play an increasingly important role to unravel the complex mechanisms that allow resident cells to sense and respond to mechanical cues. Many of the in vivo mechanical loads occur on the tissue length scale, thus raising the essential question how the resulting macroscopic strains and stresses are transferred across the scales down to the cellular and subcellular levels. Since cells anchor to the collagen fibres within the extracellular matrix, the reliable representation of fibre deformation is a prerequisite for models that aim at linking tissue biomechanics and cell mechanobiology. In this paper, we consider the two-scale mechanical response of an affine structural model as an example of a continuum mechanical approach and compare it with the results of a discrete fibre network model. In particular, we shed light on the crucially different mechanical properties of the ‘fibres’ in these two approaches. While assessing the capability of the affine structural approach to capture the fibre kinematics in real tissues is beyond the scope of our study, our results clearly show that neither the macroscopic tissue response nor the microscopic fibre orientation statistics can clarify the question of affinity.

No abstract

Probing mechanical properties of cells has been identified as a means to infer information on their current state, e.g. with respect to diseases or differentiation. Oocytes have gained particular interest, since mechanical parameters are considered potential indicators of the success of in vitro fertilisation procedures. Established tests provide the structural response of the oocyte resulting from the material properties of the cell’s components and their disposition. Based on dedicated experiments and numerical simulations, we here provide novel insights on the origin of this response. In particular, polarised light microscopy is used to characterise the anisotropy of the zona pellucida, the outermost layer of the oocyte composed of glycoproteins. This information is combined with data on volumetric changes and the force measured in relaxation/cyclic, compression/indentation experiments to calibrate a multi-phasic hyper-viscoelastic model through inverse finite element analysis. These simulations capture the oocyte’s overall force response, the distinct volume changes observed in the zona pellucida, and the structural alterations interpreted as a realignment of the glycoproteins with applied load. The analysis reveals the presence of two distinct timescales, roughly separated by three orders of magnitude, and associated with a rapid outflow of fluid across the external boundaries and a long-term, progressive relaxation of the glycoproteins, respectively. The new results allow breaking the overall response down into the contributions from fluid transport and the mechanical properties of the zona pellucida and ooplasm. In addition to the gain in fundamental knowledge, the outcome of this study may therefore serve an improved interpretation of the data obtained with current methods for mechanical oocyte characterisation.

The power law in terms of stretch, the truncated series representation and the Valanis–Landel hypothesis are distinguished features of Ogden’s strain-energy density function. While they represent a set of special constitutive choices, they have also been shown recently to allow a particular molecular statistical interpretation of the model, where each of these ingredients can be associated with a step in the development of the strain-energy density of the polymer network from the statistical mechanics of long-chain molecules. The schematic of this perspective brings us into a position to vary these steps individually. By this means, Ogden’s theory can be embedded in a certain family of models within the large class of isotropic hyperelastic materials, whose members can be identified as close and distant ‘relatives’. This article is part of the theme issue ‘The Ogden model of rubber mechanics: Fifty years of impact on nonlinear elasticity’.

A relation is established between a recently proposed single-phase model for human amnion [1], in which an internal state variable accounts for viscoelastic volume changes due to fluid outflow, and an explicitly bi-phasic representation.