Orthotropic properties of cancellous bone modelled as parameterized cellular material

Analysis of stresses and strains in bone tissues and simulation of their adaptive remodelling require exhaustive information about distribution of constitutive properties of cancellous bone and their relationships to microstructural parameters. Homogenization of “equivalent” trabecular microstructures appears to be an advantageous tool for this task. In this study, parameterized orthotropic constitutive models of cancellous bone are derived from finite element analysis of repeatable microstructure cells. The models, based on a space-filling dodecahedron, are fully three-dimensional and are parameterized with four shape parameters. Variation of the parameters allows to imitate most of typical microstructure patterns observed in real bones, along with a variety of intermediate geometries. Finite element models of cells are generated by a special-purpose structured mesh generator for any arbitrary set of shape parameter values. Static numerical tests are performed for an exhaustive number of parameter value sets (microstructure instances). Coefficients of elastic orthotropic stiffness matrix are determined as tabularized functions of elastic constants versus the shape parameters. Additionally, they are correlated to apparent density and principal fabric tensor values. Comparison of the results with micro-FE data obtained for a large set of cancellous bone specimens proves a good agreement.     

Elastic properties of cancellous bone derived from finite element models of parameterized microstructure cells

Evaluation of constitutive properties of cancellous bone and their relationships to microstructural parameters is a crucial issue in analysis of stresses and strains in bone tissues and simulation of their remodelling. Known limitations of experimental methods as well as of the micro-FE techniques make the analysis and homogenization of 'equivalent' trabecular microstructures an advantageous tool for this task. In this study, parameterized orthotropic constitutive models of cancellous bone are derived from finite element analysis of repeatable microstructure cells. Two cell types are analysed: cube- and prism-based. The models are fully three-dimensional, have realistic curvilinear shapes and are parameterized with three shape parameters. Variation of the parameters allows to imitate most of the typical microstructure patterns observed in real bones, along with variety of intermediate geometries. Finite element models of cells are generated by a special-purpose structured mesh generator for any arbitrary set of shape parameter values. Six static numerical tests are performed for an exhaustive number of parameter value sets (microstructure instances). Multi-point boundary conditions imposed on the models ensure mutual fitting of deformed neighbouring cells. Values of computed stresses allow to determine all coefficients of elastic orthotropic stiffness matrix. Results have a form of tabularized functions of elastic constants versus the shape parameters. Comparison of the results with micro-FE data obtained for a large set of cancellous bone specimens proves a good agreement, though evidently better in the case of the prism-based cell model.     

Mimetization of the elastic properties of cancellous bone via a parameterized cellular material

Bone tissue mechanical properties and trabecular microarchitecture are the main factors that determine the biomechanical properties of cancellous bone. Artificial cancellous microstructures, typically described by a reduced number of geometrical parameters, can be designed to obtain a mechanical behavior mimicking that of natural bone. In this work, we assess the ability of the parameterized microstructure introduced by Kowalczyk (Comput Methods Biomech Biomed Eng 9:135–147, 2006. doi: 10.1080/10255840600751473) to mimic the elastic response of cancellous bone. Artificial microstructures are compared with actual bone samples in terms of elasticity matrices and their symmetry classes. The capability of the parameterized microstructure to combine the dominant isotropic, hexagonal, tetragonal and orthorhombic symmetry classes in the proportions present in the cancellous bone is shown. Based on this finding, two optimization approaches are devised to find the geometrical parameters of the artificial microstructure that better mimics the elastic response of a target natural bone specimen: a Sequential Quadratic Programming algorithm that minimizes the norm of the difference between the elasticity matrices, and a Pattern Search algorithm that minimizes the difference between the symmetry class decompositions. The pattern search approach is found to produce the best results. The performance of the method is demonstrated via analyses for 146 bone samples.     

The dependence of the elastic properties of osteoporotic cancellous bone on volume fraction and fabric

Osteoporosis is a progressive systemic skeletal condition characterized by low bone mass and microarchitectural deterioration, with a consequent increase in susceptibility to fracture. Hence, osteoporosis would be best diagnosed by in vivo measurements of bone strength. As this is not clinically feasible, our goal is to estimate bone strength through the assessment of elastic properties, which are highly correlated to strength. Previously established relations between morphological parameters (volume fraction and fabric) and elastic constants could be applied to estimate cancellous bone stiffness in vivo. However, these relations were determined for normal cancellous bone. Cancellous bone from osteoporotic patients may require different relations. In this study we set out to answer two questions. First, can the elastic properties of osteoporotic cancellous bone be estimated from morphological parameters? Second, do the relations between morphological parameters and elastic constants, determined for normal bone, apply to osteoporotic bone as well? To answer these questions we used cancellous bone cubes from femoral heads of patients with (n=26) and without (n=32) hip fractures. The elastic properties of the cubes were determined using micro-finite element analysis, assuming equal tissue moduli for all specimens. The morphological parameters were determined using microcomputed tomography. Our results showed that, for equal tissue properties, the elastic properties of cancellous bone from fracture patients could indeed be estimated from morphological parameters. The morphology-based relations used to estimate the elastic properties of cancellous bone are not different for women with or without fractures.     

Errors induced by off-axis measurement of the elastic properties of bone

Misalignment between the axes of measurement and the material symmetry axes of bone causes error in anisotropic elastic property measurements. Measurements of Poisson's ratio were strongly affected by misalignment errors. The mean errors in the measured Young's moduli were 9.5 and 1.3 percent for cancellous and cortical bone, respectively, at a misalignment angle of 10 degrees. Mean errors of 1.1 and 5.0 percent in the measured shear moduli for cancellous and cortical bone, respectively, were found at a misalignment angle of 10 degrees. Although, cancellous bone tissue was assumed to have orthotropic elastic symmetry, the possibility of the greater symmetry of transverse isotropy was investigated. When the nine orthotropic elastic constants were forced to approximate the five transverse isotropic elastic constants, errors of over 60 percent were introduced. Therefore, it was concluded that cancellous bone is truly orthotropic and not transversely isotropic. A similar but less strong result for cortical bone tissue was obtained.     

Estimation of the effective transversely isotropic elastic constants of a material from known values of the material's orthotropic elastic constants

A method is illustrated for determining the effective transversely isotropic (or isotropic) elastic constants from measured orthotropic elastic constants. This method consists of constructing upper and lower bounds on the effective transversely isotropic (or isotropic) elastic constants using the known orthotropic values. This method is illustrated using three sets of elastic constants for bone. Fortunately, the upper and lower bounds are very close. Thus very good approximations for the effective transversely isotropic (or isotropic) elastic constants for cortical and cancellous bone are obtained from previously published data on the orthotropic elastic constants for those tissue types. This work is undertaken to build a greater database for the transversely isotropic elastic constants of bone with the intention of employing them in a transversely isotropic model of bone poroelasticity. An interesting aspect of the present result is that the Voigt and Reuss bounds are very tight for these anisotropic materials. This is not always the case for these bounds. Received: 14 November 2001 / Accepted: 25 February 2002     

Mineral heterogeneity has a minor influence on the apparent elastic properties of human cancellous bone: a SRμCT-based finite element study

At the tissue level, the local material properties of human cancellous bone are heterogeneous due to constant remodelling. Since standard high-resolution computed tomography scanning methods are unable to capture this heterogeneity in detail, local differences in mineralisation are normally not incorporated in computational models. To investigate the effects of heterogeneous mineral distribution on the apparent elastic properties, 40 cancellous bone samples from the human femoral neck were scanned by means of synchrotron radiation microcomputed tomography (SRμCT). SRμCT-based micromechanical finite element models that accounted for mineral heterogeneity were compared with homogeneous models. Evaluation of the apparent stiffness tensor of both model types revealed that homogeneous models led to a minor but significant (p < 0.05) overestimation of the elastic properties of heterogeneous models by 2.18 ± 1.89%. Variation of modelling parameters did not affect the overestimation to a great extent. It was concluded that the heterogeneous mineralisation has only a minor influence on the apparent elastic properties of human cancellous bone.     

A finite element study of invariant-based orthotropic constitutive equations in the context of myocardial material parameter estimation

A previous study investigated a number of invariant-based orthotropic and transversely isotropic constitutive equations for their suitability to fit three-dimensional simple shear mechanics data of passive myocardial tissue. The study was based on the assumption of a homogeneous deformation. Here, we extend the previous study by performing an inverse finite element material parameter estimation. This ensures a more realistic deformation state and material parameter estimates. The constitutive relations were compared on the basis of (i) ‘goodness of fit’: how well they fit a set of six shear deformation tests and (ii) ‘variability’: how well determined the material parameters are over the range of experiments. These criteria were utilised to discuss the advantages and disadvantages of the constitutive relations. It was found that a specific form of the polyconvex type as well as the exponential Fung-type equations were most suitable for modelling the orthotropic behaviour of myocardium under simple shear.     

显微CT分辨率对松质骨微观结构及生物力学测量的影响

目的:探究不同分辨率对显微CT测量腰椎松质骨显微结构及显微有限元分析松质骨生物力学参数精确性的影响。方法:以人腰椎L5椎体标本为对象,通过显微CT扫描得到松质骨显微CT数据,扫描分辨率为14μm,通过对合并像素点将分辨率降低至28μm~224μm等,分别测量不同分辨率下,松质骨标本的结构参数;利用不同分辨率下的显微CT数据建立显微有限元模型,计算各正交异性的弹性模量,应用统计学分析比较结构参数和力学参数的在不同分辨率下的差异。结果:各参数与分辨率间相关性不尽相同,BV/TV(骨体积分数)和Tb.Th(平均骨小梁厚度)的数值大小随着分辨率的降低呈增高趋势,Conn.D(骨小梁连接度),BS/BV(骨表面积体积比),Tb.N(平均骨小梁密度)和Tb.Sp(平均骨小梁间距)随着分辨率的降低呈降低趋势。分辨率的改变对SMI(结构模型指数)和DA(骨小梁各向异性度)没有显著影响。在三个轴向上,弹性模量均随着分辨率的降低呈增高趋势,当分辨率大于126μm时,该分辨率下的弹性模量和对照组存在显著性差异(P<0.05)。结论:该实验证实了不同分辨率对显微CT测量腰椎松质骨显微结构和生物力学参数有显著影响。提示在研究腰椎松质骨显微结构和生物力学参数时,采用126μm以上分辨率,可以在不降低准确度的情况下提高运算效率。     

Myocardial material parameter estimation

The passive material properties of myocardium play a major role in diastolic performance of the heart. In particular, the shear behaviour is thought to play an important mechanical role due to the laminar architecture of myocardium. We have previously compared a number of myocardial constitutive relations with the aim to extract their suitability for inverse material parameter estimation. The previous study assumed a homogeneous deformation. In the present study we relaxed the homogeneous assumption by implementing these laws into a finite element environment in order to obtain more realistic measures for the suitability of these laws in both their ability to fit a given set of experimental data, as well as their stability in the finite element environment. In particular, we examined five constitutive laws and compare them on the basis of (i) "goodness of fit": how well they fit a set of six shear deformation tests, (ii) "determinability": how well determined the objective function is at the optimal parameter fit, and (iii) "variability": how well determined the material parameters are over the range of experiments. Furthermore, we compared the FE results with those from the previous study.It was found that the same material law as in the previous study, the orthotropic Fung-type "Costa-Law", was the most suitable for inverse material parameter estimation for myocardium in simple shear.     

The fabric dependence of the orthotropic elastic constants of cancellous bone

It has been proposed that the orthotropic elastic constants of cancellous bone depend upon a tensorial measure of anisotropy called fabric as well as the tissue's structural density. Cowin (1985, Mechanics Mater, 4, 137-147; 1986, J. biomech. Engng 108, 83-88) developed explicit relationships for the elastic constant, structural density and fabric relationship. In this study the orthotropic elastic moduli, structural density, and fabric components were measured for 11 cancellous bone specimens from five bovine femora and for 75 specimens from three human proximal tibiae and fitted to these relationships using a least squares analysis. The relationships explained between 72 and 94% of the variance in the elastic constants. The relationships between the elastic constants and squared or cubed power functions of structural density had better predictive value over the entire distribution of the data than did expressions with linear functions of structural density.     

The speed of sound through trabecular bone predicted by Biot theory

Cancellous bone is a highly porous material filled with fluid. The mechanical properties of cancellous bone determine whether the bone is normal or osteoporotic. Wave propagation can be used to measure the elastic constants of cancellous bone. Recently, poroelasticity theory has been used to predict the elastic constants of cancellous bone from the wave velocities. In this study, it is shown that the fast wave, predicted by the Biot theory, corresponds to the wave penetrating the trabeculae, while the slow wave is determined by the interaction between the trabeculae and the fluid. The trabecular shape does not affect the wave velocity significantly when using the variable, which is determined by the microstructure, and the slow wave velocity decreases after the porosity reaches 80%.     

Anatomical variation of orthotropic elastic moduli of the proximal human tibia

The anatomical variation of orthotropic elastic moduli of the cancellous bone from three human proximal tibiae was investigated using an ultrasonic technique. With this technique, it was possible to measure three orthogonal elastic moduli and three shear moduli from cubic specimens of cancellous bone as small as 8 mm per side. Correlation with mechanical tensile testing has shown this technique to offer a precise measure of cancellous modulus (Eten = 0.94Eult + 144.6 MPa, r2 = 0.96, n = 34). The cancellous bone of the proximal tibia was found to be very inhomogeneous, with the axial modulus ranging between 340 and 3350 MPa. A course map is presented, showing measured Young's moduli as a function of anatomical position. The anisotropy of the cancellous bone, determined by the relative differences between the three orthogonal moduli, was shown to be relatively constant over the entire range of cancellous densities tested. The relationship between the axial elastic modulus and the apparent density was found to be approximately linear, as reported by others for proximal tibial cancellous bone.     

Robust optimization of total joint replacements incorporating environmental variables.

Direct search techniques for the optimal design of biomechanical devices are computationally intensive requiring many iterations before converging to a global solution. This, along with the incorporation of environmental variables such as multiple loading conditions and bone properties, makes direct search techniques infeasible. In this study, we introduced new methods that are based on the statistical design and analysis of computer experiments to account efficiently for environmental variables. Using data collected at a relatively small set of training sites, the method employs a computationally inexpensive predictor of the structural response that is statistically motivated. By using this predictor in place of the simulator (e.g., finite element model), a sufficient number of iterations can be performed to facilitate the optimization of the complex system. The applicability of these methods was demonstrated through the design of a femoral component for total hip arthroplasty incorporating variations in joint force orientation and cancellous bone properties. Beams on elastic foundation (BOEF) finite element models were developed to simulate the structural response. These simple models were chosen for their short computation time. This allowed us to represent the actual structural response surface by an exhaustive enumeration of the design and environmental variable space, and provided a means by which to validate the statistical predictor. We were able to predict the structural response and the optimal design accurately using only 16 runs of the computer code. The general trends predicted by the BOEF models were in agreement with previous three-dimensional finite element computer simulations, and experimental and clinical results, which demonstrated that the important features of intramedullary fixation systems were captured. These results indicate that the statistically based optimization methods are appropriate for optimization studies using computationally demanding models.     

A model for the nonlinear elastic response of large arteries

The nonlinear elastic response of large arteries subjected to finite deformations due to action of biaxial principal stresses, is described by simple constitutive equations. Generalized measures of strain and stress are introduced to account for material nonlinearity. This also ensures the existence of a strain energy density function. The orthotropic elastic response is described via quasi-linear relations between strains and stresses. One nonlinear parameter which defines the measures of strain and stress, and three elastic moduli are assumed to be constants. The lateral strain parameters (equivalent to Poisson's ratios in infinitesimal deformations) are deformation dependent. This dependence is defined by empirical relations developed via the incompressibility condition, and by the introduction of a fifth material parameter. The resulting constitutive model compares well with biaxial experimental data of canine carotid arteries.     

Finite element models predict cancellous apparent modulus when tissue modulus is scaled from specimen CT-attenuation

High-resolution architecture-based finite element models are commonly used for characterizing the mechanical behavior of cancellous bone. The vast majority of studies use homogeneous material properties to model trabecular tissue. The objectives of this study were to demonstrate that inhomogeneous finite element models that account for microcomputed tomography-measured tissue modulus variability more accurately predict the apparent stiffness of cancellous bone than homogeneous models, and to examine the sensitivity of an inhomogeneous model to the degree of tissue property variability. We tested five different material cases in finite element models of ten cancellous cubes in simulated uniaxial compression. Three of these cases were inhomogeneous and two were homogeneous. Four of these cases were unique to each specimen, and the remaining case had the same tissue modulus for all specimens. Results from all simulations were compared with measured elastic moduli from previous experiments. Tissue modulus variability for the most accurate of the three inhomogeneous models was then artificially increased to simulate the effects of non-linear CT-attenuation-modulus relationships. Uniqueness of individual models was more critical for model accuracy than level of inhomogeneity. Both homogeneous and inhomogeneous models that were unique to each specimen had at least 8% greater explanatory power for apparent modulus than models that applied the same material properties to all specimens. The explanatory power for apparent modulus of models with a tissue modulus coefficient of variation (COV) range of 21-31% was 13% greater than homogeneous models (COV=0). The results of this study indicate that inhomogenous finite element models that have tissue moduli unique to each specimen more accurately predict the elastic behavior of cancellous cubic specimens than models that have common tissue moduli between all specimens.     

Wolff's law of trabecular architecture at remodeling equilibrium

An elastic constitutive relation for cancellous bone tissue is developed. This relationship involves the stress tensor T, the strain tensor E and the fabric tensor H for cancellous bone. The fabric tensor is a symmetric second rank tensor that is a quantitative stereological measure of the microstructural arrangement of trabeculae and pores in the cancellous bone tissue. The constitutive relation obtained is part of an algebraic formulation of Wolff's law of trabecular architecture in remodeling equilibrium. In particular, with the general constitutive relationship between T, H and E, the statement of Wolff's law at remodeling equilibrium is simply the requirement of the commutativity of the matrix multiplication of the stress tensor and the fabric tensor at remodeling equilibrium, T*H* = H*T*. The asterisk on the stress and fabric tensor indicates their values in remodeling equilibrium. It is shown that the constitutive relation also requires that E*H* = H*E*. Thus, the principal axes of the stress, strain and fabric tensors all coincide at remodeling equilibrium.     

Determination of orthotropic bone elastic constants using FEA and modal analysis

Finite element models have been widely employed in an effort to quantify the stress and strain distribution around implanted prostheses and to explore the influence of these distributions on their long-term stability. In order to provide meaningful predictions, such models must contain an appropriate reflection of mechanical properties. Detailed geometrical and density information is now readily available from CT scanning. However, despite the use of phantoms, a method of determining mechanical properties (or elastic constants) from bone density has yet to be made available in a usable form.In this study, a cadaveric bone was CT scanned and its natural frequencies were measured using modal analysis. Using the geometry obtained from the CT scan data, a finite element mesh was created with the distribution of density established by matching the mass of the FE bone model with the mass of the cadaveric bone. The maximum values of the orthotropic elastic constants were then established by matching the predictions from FE modal analyses to the experimental natural frequencies, giving a maximum error of 7.8% over 4 modes of vibration. Finally, the elastic constants of the bone derived from the analyses were compared with those measured using ultrasound techniques. This produced a difference of <1% for both the maximum density and axial Young's Modulus. This study has thereby produced an orthotropic finite element model of a human femur. More importantly, however, is the implication that it is possible to create a valid FE model by simply comparing the FE results with the measured resonant frequency of the CT scanned bone.