Method for characterizing viscoelasticity of human gluteal tissue

Characterizing compressive transient large deformation properties of biological tissue is becoming increasingly important in impact biomechanics and rehabilitation engineering, which includes devices interfacing with the human body and virtual surgical guidance simulation. Individual mechanical in vivo behaviour, specifically of human gluteal adipose and passive skeletal muscle tissue compressed with finite strain, has, however, been sparsely characterised. Employing a combined experimental and numerical approach, a method is presented to investigate the time-dependent properties of in vivo gluteal adipose and passive skeletal muscle tissue. Specifically, displacement-controlled ramp-and-hold indentation relaxation tests were performed and documented with magnetic resonance imaging. A time domain quasi-linear viscoelasticity (QLV) formulation with Prony series valid for finite strains was used in conjunction with a hyperelastic model formulation for soft tissue constitutive model parameter identification and calibration of the relaxation test data. A finite element model of the indentation region was employed. Strong non-linear elastic but linear viscoelastic tissue material behaviour at finite strains was apparent for both adipose and passive skeletal muscle mechanical properties with orthogonal skin and transversal muscle fibre loading. Using a force-equilibrium assumption, the employed material model was well suited to fit the experimental data and derive viscoelastic model parameters by inverse finite element parameter estimation. An individual characterisation of in vivo gluteal adipose and muscle tissue could thus be established. Initial shear moduli were calculated from the long-term parameters for human gluteal skin/fat: G(∞,S/F)=1850 Pa and for cross-fibre gluteal muscle tissue: G(∞,M)=881 Pa. Instantaneous shear moduli were found at the employed ramp speed: G(0,S/F)=1920 Pa and G(0,M)=1032 Pa.     

Large strain behaviour of brain tissue in shear: some experimental data and differential constitutive model.

In this paper, some experimental measurements of the behaviour of bovine brain tissue under large shear strains in vitro are reported, and a constitutive model which is consistent with the data is developed. It was determined that brain tissue is not strain-time separable, showing slower relaxation at higher strains, and that the stresses in shear are not linear with increasing shear strain. The new constitutive model is a differential model, including both an "elastic" term, of the Mooney type and a nonlinear viscoelastic term. The latter allows for the change in relaxation behaviour with strain, by modifying an upper convected multimode Maxwell model with a damping function. The model shows good agreement with the experimental shear results and could be used to describe other types of data.     

A model for the compressible,viscoelastic behavior of human amnion addressing tissue variability through a single parameter

A viscoelastic, compressible model is proposed to rationalize the recently reported response of human amnion in multiaxial relaxation and creep experiments. The theory includes two viscoelastic contributions responsible for the short- and long-term time-dependent response of the material. These two contributions can be related to physical processes: water flow through the tissue and dissipative characteristics of the collagen fibers, respectively. An accurate agreement of the model with the mean tension and kinematic response of amnion in uniaxial relaxation tests was achieved. By variation of a single linear factor that accounts for the variability among tissue samples, the model provides very sound predictions not only of the uniaxial relaxation but also of the uniaxial creep and strip-biaxial relaxation behavior of individual samples. This suggests that a wide range of viscoelastic behaviors due to patient-specific variations in tissue composition can be represented by the model without the need of recalibration and parameter identification.     

A strain-hardening bi-power law for the nonlinear behaviour of biological soft tissues

Biological soft tissues exhibit a strongly nonlinear viscoelastic behaviour. Among parenchymous tissues, kidney and liver remain less studied than brain, and a first goal of this study is to report additional material properties of kidney and liver tissues in oscillatory shear and constant shear rate tests. Results show that the liver tissue is more compliant but more strain hardening than kidney. A wealth of multi-parameter mathematical models has been proposed for describing the mechanical behaviour of soft tissues. A second purpose of this work is to develop a new constitutive law capable of predicting our experimental data in the both linear and nonlinear viscoelastic regime with as few parameters as possible. We propose a nonlinear strain-hardening fractional derivative model in which six parameters allow fitting the viscoelastic behaviour of kidney and liver tissues for strains ranging from 0.01 to 1 and strain rates from 0.0151 s^?1 to 0.7 s^?1.     

Static versus dynamic gerbil tympanic membrane elasticity: derivation of the complex modulus

An accurate estimation of tympanic membrane stiffness is important for realistic modelling of middle ear mechanics. Tympanic membrane stiffness has been investigated extensively under either quasi-static or dynamic loading conditions. It is known that biological tissues are sensitive to strain rate. Therefore, in this work, the mechanical behaviour of the tympanic membrane was studied under both quasi-static and dynamic loading conditions. Experiments were performed on the pars tensa of four gerbil tympanic membranes. A custom-built indentation apparatus was used to perform in situ tissue indentations and testing was done applying both quasi-static and dynamic sinusoidal indentations up to 8.2?Hz. The unloaded shape of the tympanic membrane was measured and used to create specimen-specific finite element models to simulate the experiments. The frequency dependent Young's modulus of each specimen was then estimated by an inverse analysis in which the error between experimental and simulated indentation data was optimised for each indentation frequency separately. Using an 8?μm central region thickness, we found Young's moduli between 71 and 106?MPa (n = 4) at 0.2?Hz indentation frequency. A standard linear viscoelastic model and a viscoelastic model with a continuous relaxation spectrum were used to derive a complex modulus in the frequency domain. Due to experimental limitations, the indentation frequency upper limit was 8.2?Hz. The average relative modulus increase in this domain was 14% and the increase was the strongest below 6?Hz.     

Viscoelastic properties of passive skeletal muscle in compression—Cyclic behaviour

Skeletal muscle relaxation behaviour in compression has been previously reported, but the anisotropic behaviour at higher loading rates remains poorly understood. In this paper, uniaxial unconfined cyclic compression tests were performed on fresh porcine muscle samples at various fibre orientations to determine muscle viscoelastic behaviour. Mean compression level of 25% was applied and cycles of 2% and 10% amplitude were performed at 0.2–80 Hz. Under cycles of low frequency and amplitude, linear viscoelastic cyclic relaxation was observed. Fibre/cross-fibre results were qualitatively similar, but the cross-fibre direction was stiffer (ratio of 1.2). In higher amplitude tests nonlinear viscoelastic behaviour with a frequency dependent increase in the stress cycles amplitude was found (factor of 4.1 from 0.2 to 80 Hz).The predictive capability of an anisotropic quasi-linear viscoelastic model previously fitted to stress-relaxation data from similar tissue samples was investigated. Good qualitative results were obtained for low amplitude cycles but differences were observed in the stress cycle amplitudes (errors of 7.5% and 31.8%, respectively, in the fibre/cross-fibre directions). At higher amplitudes significant qualitative and quantitative differences were evident. A nonlinear model formulation was therefore developed which provided a good fit and predictions to high amplitude low frequency cyclic tests performed in the fibre/cross-fibre directions. However, this model gave a poorer fit to high frequency cyclic tests and to relaxation tests. Neither model adequately predicts the stiffness increase observed at frequencies above 5 Hz.Together with data previously presented, the experimental data presented here provide a unique dataset for validation of future constitutive models for skeletal muscle in compression.     

Material properties of the human calcaneal fat pad in compression: experiment and theory

The structural behaviour of the human heel pad has been studied extensively due to its ability to absorb shock, protect against excessive local stress, and reduce plantar pressures. However, the material properties of the tissue have not been adequately measured. These must be known in order to perform a finite element analysis of the effect of factors such as foot geometry and shoe/surface construction on heel pad function. Therefore, the purposes of this study were to (a) measure the viscoelastic behaviour of the fat pad in compression, and (b) to determine an appropriate constitutive equation to model the tissue. A series of unconfined compression tests were performed on 8 mm diameter cylinders of fat pad tissue, consisting of quasi-static, 175, 350 mm/s and stress-relaxation tests to 50% deformation. The tissue exhibited nonlinear, viscoelastic behaviour. No significant difference was found in the quasi-static behaviour between samples from different locations and orientations in the heel. The stress-relaxation tests were used to determine the time constant (τ₁=0.5 s), the 175 mm/s test to determine the relaxation coefficient (g₁=28), and the 350 mm/s compression test to determine the material constants (C₁₀₀=C₀₁₀=0.01, C₂₀₀=C₀₂₀=0.1 Pa) of a single-phase, hyperelastic, linear viscoelastic strain energy function (r²=0.98).     

A comparison of cartilage stress-relaxation models in unconfined compression: QLV and stretched exponential in combination with fluid flow

Cartilage exhibits nonlinear viscoelastic behaviour. Various models have been proposed to explain cartilage stress relaxation, but it is unclear whether explicit modelling of fluid flow in unconfined compression is needed. This study compared Fung's quasi-linear viscoelastic (QLV) model with a stretched-exponential model of cartilage stress relaxation and examined each of these models both alone and in combination with a fluid-flow model in unconfined compression. Cartilage explants were harvested from bovine calf patellofemoral joints and equilibrated in tissue culture for 5 days before stress-relaxation testing in unconfined compression at 5% nominal strain. The stretched exponential models fit as well as the QLV models. Furthermore, the average stretched exponential relaxation time determined by this model lies within the range of experimentally measured relaxation times for extracted proteoglycan aggregates, consistent with the hypothesis that the stretched exponential model represents polymeric mechanisms of cartilage viscoelasticity.     

In situ multi-level analysis of viscoelastic deformation mechanisms in tendon collagen

Tendon is a hydrated multi-level fibre composite, in which time-dependent behaviour is well established. Studies indicate significant stress relaxation, considered important for optimising tissue stiffness. However, whilst this behaviour is well documented, the mechanisms associated with the response are largely unknown. This study investigates the sub-structural mechanisms occurring during stress relaxation at both the macro (fibre) and nano (fibril) levels of the tendon hierarchy. Stress relaxation followed a two-stage exponential behaviour, during which structural changes were visible at the fibre and fibril levels. Fibril relaxation and fibre sliding showed a double exponential response, while fibre sliding was clearly the largest contributor to relaxation. The amount of stress relaxation and sub-structural reorganisation increased with increasing load increments, but fibre sliding was consistently the largest contributor to stress relaxation. A simple model of tendon viscoelasticity at the fibril and fibre levels has been developed, capturing this behaviour by serially coupling a Voigt element (collagen fibril), with two Maxwell elements (non-collagenous matrix between fibrils and fibres). This multi-level analysis provides a first step towards understanding how sub-structural interactions contribute to viscoelastic behaviour. It indicates that nano- and micro-scale shearing are significant dissipative mechanisms, and the kinetics of relaxation follows a two-stage exponential decay, well fitted by serially coupled viscoelastic elements.     

The apparent viscoelastic behavior of articular cartilage--the contributions from the intrinsic matrix viscoelasticity and interstitial fluid flows

Articular cartilage was modeled rheologically as a biphasic poroviscoelastic material. A specific integral-type linear viscoelastic model was used to describe the constitutive relation of the collagen-proteoglycan matrix in shear. For bulk deformation, the matrix was assumed either to be linearly elastic, or viscoelastic with an identical reduced relaxation spectrum as in shear. The interstitial fluid was considered to be incompressible and inviscid. The creep and the rate-controlled stress-relaxation experiments on articular cartilage under confined compression were analyzed using this model. Using the material data available in the literature, it was concluded that both the interstitial fluid flow and the intrinsic matrix viscoelasticity contribute significantly to the apparent viscoelastic behavior of this tissue under confined compression.     

Effect of preservation period on the viscoelastic material properties of soft tissues with implications for liver transplantation

The liver harvested from a donor must be preserved and transported to a suitable recipient immediately for a successful liver transplantation. In this process, the preservation period is the most critical, since it is the longest and most tissue damage occurs during this period due to the reduced blood supply to the harvested liver and the change in its temperature. We investigate the effect of preservation period on the dynamic material properties of bovine liver using a viscoelastic model derived from both impact and ramp and hold experiments. First, we measure the storage and loss moduli of bovine liver as a function of excitation frequency using an impact hammer. Second, its time-dependent relaxation modulus is measured separately through ramp and hold experiments performed by a compression device. Third, a Maxwell solid model that successfully imitates the frequency- and time-dependent dynamic responses of bovine liver is developed to estimate the optimum viscoelastic material coefficients by minimizing the error between the experimental data and the corresponding values generated by the model. Finally, the variation in the viscoelastic material coefficients of bovine liver are investigated as a function of preservation period for the liver samples tested 1 h, 2 h, 4 h, 8 h, 12 h, 24 h, 36 h, and 48 h after harvesting. The results of our experiments performed with three animals show that the liver tissue becomes stiffer and more viscous as it spends more time in the preservation cycle.     

Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: II--Effect of variable strain rates

This study investigated the abilities of the linear biphasic poroviscoelastic (BPVE) model and the linear biphasic poroelastic (BPE) model to simulate the effect of variable ramp strain rates on the unconfined compression stress relaxation response of articular cartilage. Curve fitting of experimental data showed that the BPVE model was able to successfully account for the ramp strain rate-dependent viscoelastic behavior of articular cartilage under unconfined compression, while the BPE model was able to account for the complete viscoelastic response at a slow strain rate, but only the long-term viscoelastic response at faster strain rates. We concluded that the short-term viscoelastic behavior of articular cartilage, when subjected to a fast ramp strain rate, is primarily governed by a fluid flow-independent (intrinsic) viscoelastic mechanism, whereas the long-term viscoelastic behavior is governed by a fluid flow-dependent (biphasic) viscoelastic mechanism. Furthermore, a linear viscoelastic representation of the solid stress was found to be a valid model assumption for the simulation of ramp strain rate-dependent relaxation behaviors of articular cartilage within the range of ramp strain rates investigated.     

An in-vivo measurement and analysis of viscoelastic properties of the spinal cord of cats

An in-vivo experimental technique was employed to determine the linear and nonlinear characteristics of viscoelastic properties of the spinal cord of anesthetized cats. The stress relaxation and recovery curves were reproducible in a group of cat experiments. The data of linear viscoelastic properties were used to develop a power law model with Boltzmann's convolution integral. The model was capable of predicting a prolonged stress relaxation and recovery curve. For larger deformation, the results were quantified using a nonlinear analysis of viscoelastic response of the spinal cord under the uniaxial experiment.     

Analysis of several biomechanical models for the simulation of lamb liver behaviour using similarity coefficients from medical image

In this study, six biomechanical models for simulating lamb liver behaviour are presented. They are validated using similarity coefficients from Medical Image on reconstructed volumes from computerised tomography images. In particular, the Jaccard and Hausdorff coefficients are used. Loads of 20 and 40 g are applied to the livers and their deformation is simulated by means of the finite element method. The models used are a linear elastic model, a neo-Hookean model, a Mooney–Rivlin model, an Ogden model, a linear viscoelastic model and a viscohyperelastic model. The model that provided a behaviour that is closest to reality was the viscohyperelastic model, where the hyperelastic part was modelled with an Ogden model.     

Large deformation shear properties of liver tissue

Characterization of the mechanical properties of soft biological tissues is important for establishing the mechanical tolerances of the tissues, and for input to computational models. In this work, the viscoelastic properties of bovine liver tissue in shear loading have been measured using relaxation and constant shear rate loading. The tissue is nonlinearly viscoelastic for strains greater than 0.2%, has a yield strain of approximately 10, and shows moderate strain-rate sensitivity. The response can be modelled using a nonlinear viscoelastic differential model previously developed for brain tissue.     

Systematic investigation of degradation effects on spin-spin relaxation times in mouse-liver by low resolution NMR

Despite numerous work on spin-lattice (T1) relaxation in vitro, not much attention has been paid on spin-spin (T2) relaxation until now. In this study we are presenting spin-spin relaxation time measurements of mouse liver tissue in order to estimate the time-after-excision effects. The post mortem behaviour of excised tissue was investigated up to four hours in intervals of about nine minutes. The time course of liver T2 was determined for different temperatures (4 degrees - 40 degrees C) for female mice. In order to describe the similar behaviour of T2 and pH changes in mouse liver after excision, we are suggesting an empirical model to correlate this data. In contrast to T1 results published recently, we found no significant differences in liver T2 time course after excision due to different physiological states like sex, starvation or circadian rhythm. T1/T2-behaviour after tissue excision is discussed in an attempt to separate various relaxation mechanisms.     

Linear viscoelasticity - bone volume fraction relationships of bovine trabecular bone

Trabecular bone has been previously recognized as time-dependent (viscoelastic) material, but the relationships of its viscoelastic behaviour with bone volume fraction (BV/TV) have not been investigated so far. Therefore, the aim of the present study was to quantify the time-dependent viscoelastic behaviour of trabecular bone and relate it to BV/TV. Uniaxial compressive creep experiments were performed on cylindrical bovine trabecular bone samples (\(\textit{n}\,{=}\,13\)) at loads corresponding to physiological strain level of 2000 \({\upmu }{\upvarepsilon }\). We assumed that the bone behaves in a linear viscoelastic manner at this low strain level and the corresponding linear viscoelastic parameters were estimated by fitting a generalized Kelvin–Voigt rheological model to the experimental creep strain response. Strong and significant power law relationships (\(r^2\,{=}\,0.73,\ p\,{<}\,0.001\)) were found between time-dependent creep compliance function and BV/TV of the bone. These BV/TV-based material properties can be used in finite element models involving trabecular bone to predict time-dependent response. For users’ convenience, the creep compliance functions were also converted to relaxation functions by using numerical interconversion methods and similar power law relationships were reported between time-dependent relaxation modulus function and BV/TV.     

Stress relaxation behaviour of trabecular bone specimens

The present study defines several conditions under which stress relaxation tests can be performed and investigates the viscoelastic behaviour of trabecular bone in compression through a series of stress relaxation tests at three strain levels and in three loading directions of each cubic specimen. A visoelastic model is proposed to characterize the behaviour of trabecular bone and a spectrum of relaxation times is determined. Trabecular bone from the femoral head is non-linearly viscoelastic and displays anisotropic behaviour, which cannot be more symmetric elastically than orthotropic.