Finite element analysis of biological soft tissue surrounded by a deformable membrane that controls transmembrane flow

Background

Many biological soft tissues are hydrated porous hyperelastic materials, which consist of a complex solid skeleton with fine voids and fluid filling these voids. Mechanical interactions between the solid and the fluid in hydrated porous tissues have been analyzed by finite element methods (FEMs) in which the mixture theory was introduced in various ways. Although most of the tissues are surrounded by deformable membranes that control transmembrane flows, the boundaries of the tissues have been treated as rigid and/or freely permeable in these studies. The purpose of this study was to develop a method for the analysis of hydrated porous hyperelastic tissues surrounded by deformable membranes that control transmembrane flows.

Results

For this, we developed a new nonlinear finite element formulation of the mixture theory, where the nodal unknowns were the pore water pressure and solid displacement. This method allows the control of the fluid flow rate across the membrane using Neumann boundary condition. Using the method, we conducted a compression test of the hydrated porous hyperelastic tissue, which was surrounded by a flaccid impermeable membrane, and a part of the top surface of this tissue was pushed by a platen. The simulation results showed a stress relaxation phenomenon, resulting from the interaction between the elastic deformation of the tissue, pore water pressure gradient, and the movement of fluid. The results also showed that the fluid trapped by the impermeable membrane led to the swelling of the tissue around the platen.

Conclusions

These facts suggest that our new method can be effectively used for the analysis of a large deformation of hydrated porous hyperelastic material surrounded by a deformable membrane that controls transmembrane flow, and further investigations may allow more realistic analyses of the biological soft tissues, such as brain edema, brain trauma, the flow of blood and lymph in capillaries and pitting edema.

     

Measurement of the hyperelastic properties of ex vivo brain tissue slices

The elastic and hyperelastic properties of brain tissue are of interest to the medical research community as there are several applications where accurate characterization of these properties is crucial for an accurate outcome. The linear response is applicable to brain elastography, while the non-linear response is of interest for surgical simulation programs. Because of the biological differences between gray and white matter, it is reasonable to expect a difference in their mechanical properties. The goal of this work is to characterize the elastic and hyperelastic properties of the brain gray and white matter. In this method, force-displacement data of these tissues were acquired from 25 different brain samples using an indentation apparatus. These data were processed with an inverse problem algorithm using finite element method as the forward problem solver. Young's modulus and the hyperelastic parameters corresponding to the commonly used Polynomial, Yeoh, Arruda-Boyce, and Ogden models were obtained. The parameters characterizing the linear and non-linear mechanical behavior of gray and white matters were found to be significantly different. Young's modulus was 1787±186 and 1195±157Pa for white matter and gray matter, respectively. Among hyperelastic models, due to its accuracy, fewer parameters and shorter computational time requirements, Yeoh model was found to be the most suitable. Due to the significant differences between the linear and non-linear tissue response, we conclude that incorporating these differences into brain biomechanical models is necessary to increase accuracy.     

Optimizing cardiac material parameters with a genetic algorithm

Determining the unknown material parameters of intact ventricular myocardium can be challenging due to highly nonlinear material behavior. Previous studies combining a gradient-search optimization procedure with finite element analysis (FEA) were limited to two-dimensional (2D) models or simplified three-dimensional (3D) geometries. Here we present a novel scheme to estimate unknown material parameters for ventricular myocardium by combining a genetic algorithm (GA) with nonlinear finite element analysis. This approach systematically explores the domain of the material parameters. The objective function to minimize was the error between simulated strain data and finite element model strains. The proposed scheme was validated for a 2D problem using a realistic material law for ventricular myocardium. Optimized material parameters were generally within 0.5% of the true values. To demonstrate the robustness of the new scheme, unknown material parameters were also determined for a realistic 3D heart model with an exponential hyperelastic material law. When using strains from two material points, the algorithm converged to parameters within 5% of the true values. We conclude that the proposed scheme is robust when estimating myocardial material parameters in 2D and 3D models.     

Modeling Soft Tissue Damage and Failure Using a Combined Particle/Continuum Approach

Biological soft tissues experience damage and failure as a result of injury, disease, or simply age; examples include torn ligaments and arterial dissections. Given the complexity of tissue geometry and material behavior, computational models are often essential for studying both damage and failure. Yet, because of the need to account for discontinuous phenomena such as crazing, tearing, and rupturing, continuum methods are limited. Therefore, we model soft tissue damage and failure using a particle/continuum approach. Specifically, we combine continuum damage theory with Smoothed Particle Hydrodynamics (SPH). Because SPH is a meshless particle method, and particle connectivity is determined solely through a neighbor list, discontinuities can be readily modeled by modifying this list. We show, for the first time, that an anisotropic hyperelastic constitutive model commonly employed for modeling soft tissue can be conveniently implemented within a SPH framework and that SPH results show excellent agreement with analytical solutions for uniaxial and biaxial extension as well as finite element solutions for clamped uniaxial extension in 2D and 3D. We further develop a simple algorithm that automatically detects damaged particles and disconnects the spatial domain along rupture lines in 2D and rupture surfaces in 3D. We demonstrate the utility of this approach by simulating damage and failure under clamped uniaxial extension and in a peeling experiment of virtual soft tissue samples. In conclusion, SPH in combination with continuum damage theory may provide an accurate and efficient framework for modeling damage and failure in soft tissues.     

Spherical indentation of soft matter beyond the Hertzian regime: numerical and experimental validation of hyperelastic models

The lack of practicable nonlinear elastic contact models frequently compels the inappropriate use of Hertzian models in analyzing indentation data and likely contributes to inconsistencies associated with the results of biological atomic force microscopy measurements. We derived and validated with the aid of the finite element method force-indentation relations based on a number of hyperelastic strain energy functions. The models were applied to existing data from indentation, using microspheres as indenters, of synthetic rubber-like gels, native mouse cartilage tissue, and engineered cartilage. For the biological tissues, the Fung and single-term Ogden models achieved the best fits of the data while all tested hyperelastic models produced good fits for the synthetic gels. The Hertz model proved to be acceptable for the synthetic gels at small deformations (strain < 0.05 for the samples tested), but not for the biological tissues. Although this finding supports the generally accepted view that many soft materials can be assumed to be linear elastic at small deformations, the nonlinear models facilitate analysis of intrinsically nonlinear tissues and large-strain indentation behavior.     

Quantifying nonlinear anisotropic elastic material properties of biological tissue by use of membrane inflation

Determination of material parameters for soft tissue frequently involves regression of material parameters for nonlinear, anisotropic constitutive models against experimental data from heterogeneous tests. Here, parameter estimation based on membrane inflation is considered. A four parameter nonlinear, anisotropic hyperelastic strain energy function was used to model the material, in which the parameters are cast in terms of key response features. The experiment was simulated using finite element (FE) analysis in order to predict the experimental measurements of pressure versus profile strain. Material parameter regression was automated using inverse FE analysis; parameter values were updated by use of both local and global techniques, and the ability of these techniques to efficiently converge to a best case was examined. This approach provides a framework in which additional experimental data, including surface strain measurements or local structural information, may be incorporated in order to quantify heterogeneous nonlinear material properties.     

Finite element simulation of skeletal muscular structures obtained from images of histological serial sections

In this study, we present a method for the three-dimensional reconstruction of objects obtained from histological serial sections (exemplified by those of a pennate striated skeletal muscle) and its application to the finite element method. A hyperelastic material model is used for modeling biological soft tissue. The reconstruction process relies on the direct construction of a volumetric mesh using an octree approach which leads to a stable finite element method. Stability can be expressed in the spectral matrix condition number. To visualize stress patterns within the underlying anatomy the simulation results are projected onto images of the histological scenario.     

A hyperelastic and almost incompressible material model as an approach to intervertebral disc analysis

The literature contains many references to intervertebral disc analysis using experimental techniques which represent a basis for analytical and numerical approaches. The scatter of experimental results may be one reason for difficulties in interpretation. Apart from analytical approaches, which often seen inadequate to deal with the peculiar complexities of the problem, numerical techniques are reliable and can lead to significant results. In this work, a formulation based on the finite element method is described, adopting a nonlinear model with hyperelastic material configuration. Particular attention is paid to modelling the material constituting the nucleus, involving incompressibility characteristics and avoiding simulation techniques. This approach allows the mechanical behaviour of the real configuration of the disc to be investigated and also provides a reliable analysis of disc degeneration phenomena. The theoretical and operational aspects of the formulation are reported. The results obtained are compared with responses from various numerical and experimental data.     

Dynamic finite element implementation of nonlinear,anisotropic hyperelastic biological membranes

We present a novel method for the implementation of hyperelastic finite strain, non-linear strain-energy functions for biological membranes in an explicit finite element environment. The technique is implemented in LS-DYNA but may also be implemented in any suitable non-linear explicit code. The constitutive equations are implemented on the foundation of a co-rotational uniformly reduced Hughes-Liu shell. This shell is based on an updated-Lagrangian formulation suitable for relating Cauchy stress to the rate-of-deformation, i.e. hypo-elasticity. To accommodate finite deformation hyper-elastic formulations, a co-rotational deformation gradient is assembled over time, resulting in a formulation suitable for pseudo-hyperelastic constitutive equations that are standard assumptions in biomechanics. Our method was validated by comparison with (1) an analytic solution to a spherically-symmetric dynamic membrane inflation problem, incorporating a Mooney-Rivlin hyperelastic equation and (2) with previously published finite element solutions to a non-linear transversely isotropic inflation problem. Finally, we implemented a transversely isotropic strain-energy function for mitral valve tissue. The method is simple and accurate and is believed to be generally useful for anyone who wishes to model biologic membranes with an experimentally driven strain-energy function.     

Simple shear testing of parallel-fibered planar soft tissues

The simple shear test may provide unique information regarding the material response of parallel-fibered soft tissues because it allows the elimination of the dominant fiber material response from the overall stresses. However, inhomogeneities in the strain field due to clamping and free edge effects have not been documented. The finite element method was used to study finite simple shear of simulated ligament material parallel to the fiber direction. The effects of aspect ratio, clamping prestrain, and bulk modulus were assessed using a transversely isotropic, hyperelastic material model. For certain geometries, there was a central area of uniform strain. An aspect ratio of 1:2 for the fiber to cross-fiber directions provided the largest region of uniform strain. The deformation was nearly isochoric for all bulk moduli indicating this test may be useful for isolating solid viscoelasticity from interstitial flow effects. Results suggest this test can be used to characterize the matrix properties for the type of materials examined in this study, and that planar measurements will suffice to characterize the strain. The test configuration may be useful for the study of matrix, fiber-matrix, and fiber-fiber material response in other types of parallel-fibered transversely isotropic soft tissues.     

MRI-based experimentations of fingertip flat compression: Geometrical measurements and finite element inverse simulations to investigate material property parameters

Modeling human-object interactions is a necessary step in the ergonomic assessment of products. Fingertip finite element models can help investigating these interactions, if they are built based on realistic geometrical data and material properties. The aim of this study was to investigate the fingertip geometry and its mechanical response under compression, and to identify the parameters of a hyperelastic material property associated to the fingertip soft tissues.Fingertip compression tests in an MRI device were performed on 5 subjects at either 2 or 4 N and at 15° or 50°. The MRI images allowed to document both the internal and external fingertip dimensions and to build 5 subject-specific finite element models. Simulations reproducing the fingertip compression tests were run to obtain the material property parameters of the soft tissues.Results indicated that two ellipses in the sagittal and longitudinal plane could describe the external fingertip geometry. The internal geometries indicated an averaged maximal thickness of soft tissues of 6.4 ± 0.8 mm and a 4 ± 1 mm height for the phalanx bone. The averaged deflections under loading went from 1.8 ± 0.3 mm at 2 N, 50° to 3.1 ± 0.2 mm at 4 N, 15°. Finally, the following set of parameters for a second order hyperelastic law to model the fingertip soft tissues was proposed: C₀₁ = 0.59 ± 0.09 kPa and C₂₀ = 2.65 ± 0.88 kPa.These data should facilitate further efforts on fingertip finite element modeling.     

The micromechanical environment of intervertebral disc cells determined by a finite deformation,anisotropic, and biphasic finite element model

Cellular response to mechanical loading varies between the anatomic zones of the intervertebral disc. This difference may be related to differences in the structure and mechanics of both cells and extracellular matrix, which are expected to cause differences in the physical stimuli (such as pressure, stress, and strain) in the cellular micromechanical environment. In this study, a finite element model was developed that was capable of describing the cell micromechanical environment in the intervertebral disc. The model was capable of describing a number of important mechanical phenomena: flow-dependent viscoelasticity using the biphasic theory for soft tissues; finite deformation effects using a hyperelastic constitutive law for the solid phase; and material anisotropy by including a fiber-reinforced continuum law in the hyperelastic strain energy function. To construct accurate finite element meshes, the in situ geometry of IVD cells were measured experimentally using laser scanning confocal microscopy and three-dimensional reconstruction techniques. The model predicted that the cellular micromechanical environment varies dramatically between the anatomic zones, with larger cellular strains predicted in the anisotropic anulus fibrosus and transition zone compared to the isotropic nucleus pulposus. These results suggest that deformation related stimuli may dominate for anulus fibrosus and transition zone cells, while hydrostatic pressurization may dominate in the nucleus pulposus. Furthermore, the model predicted that micromechanical environment is strongly influenced by cell geometry, suggesting that the geometry of IVD cells in situ may be an adaptation to reduce cellular strains during tissue loading.     

Identifying heterogeneous anisotropic properties in cerebral aneurysms: a pointwise approach

The traditional approaches of estimating heterogeneous properties in a soft tissue structure using optimization-based inverse methods often face difficulties because of the large number of unknowns to be simultaneously determined. This article proposes a new method for identifying the heterogeneous anisotropic nonlinear elastic properties in cerebral aneurysms. In this method, the local properties are determined directly from the pointwise stress–strain data, thus avoiding the need for simultaneously optimizing for the property values at all points/regions in the aneurysm. The stress distributions needed for a pointwise identification are computed using an inverse elastostatic method without invoking the material properties in question. This paradigm is tested numerically through simulated inflation tests on an image-based cerebral aneurysm sac. The wall tissue is modeled as an eight-ply laminate whose constitutive behavior is described by an anisotropic hyperelastic strain energy function containing four parameters. The parameters are assumed to vary continuously in the sac. Deformed configurations generated from forward finite element analysis are taken as input to inversely establish the parameter distributions. The delineated and the assigned distributions are in excellent agreement. A forward verification is conducted by comparing the displacement solutions obtained from the delineated and the assigned material parameters at a different pressure. The deviations in nodal displacements are found to be within 0.2% in most part of the sac. The study highlights some distinct features of the proposed method, and demonstrates the feasibility of organ level identification of the distributive anisotropic nonlinear properties in cerebral aneurysms.     

The influence of the material properties on the biomechanical behavior of the pelvic floor muscles during vaginal delivery

In this work, a finite element model intends to represent the effects that the passage of a fetal head can induce on the muscles of the pelvic floor, from a mechanical point of view.The finite element method is a valuable tool, that is contributing to the clarification of the mechanisms behind pelvic floor disorders related to vaginal deliveries, although some care is necessary in order to obtain correct results. The present work shows how the variation of the material parameters, used in the constitutive model, can affect the obtained results from a finite element simulation. The constitutive equation adopted in this work for the pelvic floor muscles is a modified form of the incompressible transversely isotropic hyperelastic model proposed earlier by Humphrey and Yin.Results for the pelvic floor strain and stresses obtained during the passage of the fetus head are presented. The results show the importance of the material parameters and the need for a correct constitutive model.     

Viscoelastic material properties of the myocardium and cardiac jelly in the looping chick heart

Accurate material properties of developing embryonic tissues are a crucial factor in studies of the mechanics of morphogenesis. In the present work, we characterize the viscoelastic material properties of the looping heart tube in the chick embryo through nonlinear finite element modeling and microindentation experiments. Both hysteresis and ramp-hold experiments were performed on the intact heart and isolated cardiac jelly (extracellular matrix). An inverse computational method was used to determine the constitutive relations for the myocardium and cardiac jelly. With both layers assumed to be quasilinear viscoelastic, material coefficients for an Ogden type strain-energy density function combined with Prony series of two terms or less were determined by fitting numerical results from a simplified model of a heart segment to experimental data. The experimental and modeling techniques can be applied generally for determining viscoelastic material properties of embryonic tissues.     

Spherical indentation method for determining the constitutive parameters of hyperelastic soft materials

A comprehensive study on the spherical indentation of hyperelastic soft materials is carried out through combined theoretical, computational, and experimental efforts. Four widely used hyperelastic constitutive models are studied, including neo-Hookean, Mooney–Rivlin, Fung, and Arruda–Boyce models. Through dimensional analysis and finite element simulations, we establish the explicit relations between the indentation loads at given indentation depths and the constitutive parameters of materials. Based on the obtained results, the applicability of Hertzian solution to the measurement of the initial shear modulus of hyperelastic materials is examined. Furthermore, from the viewpoint of inverse problems, the possibility to measure some other properties of a hyperelastic material using spherical indentation tests, e.g., locking stretch, is addressed by considering the existence, uniqueness, and stability of the solution. Experiments have been performed on polydimethylsiloxane to validate the conclusions drawn from our theoretical analysis. The results reported in this study should help identify the extent to which the mechanical properties of hyperelastic materials could be measured from spherical indentation tests.