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.     

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.     

Effects of damage on the orthotropic material symmetry of bovine tibial trabecular bone

The macroscopic mechanical properties of trabecular bone can be predicted by its architecture using theoretical relationships between the elastic and architectural properties. Microdamage caused by overloading or fatigue decreases the apparent elastic moduli of trabecular bone requiring these relationships to be modified to predict the damaged elastic properties. In the case of isotropic damage, the apparent level elastic properties could be determined by multiplying all of the elastic constants by a single scalar factor. If the damage is anisotropic, the elastic constants may change by differing factors and the material coordinate system could become misaligned with the fabric coordinate system. High-resolution finite element models were used to simulate damage overloading on seven trabecular bone specimens subjected to pure shear strain in two planes. Comparison of the apparent elastic moduli of the specimens before and after damage showed that the reduction of the elastic moduli was anisotropic. This suggests that the microdamage within the specimens was inhomogeneous. However, after damage the specimens exhibited nearly orthotropic material symmetry as they did before damage. Changes in the orientation of the orthotropic material coordinate system were also small and occurred primarily in the transverse plane. Thus, while damage in trabecular bone is anisotropic, the material coordinate system remains aligned with the fabric tensor.     

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.     

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.     

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.     

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.     

Direct mechanics assessment of elastic symmetries and properties of trabecular bone architecture

A method is presented to find orthotropic elastic symmetries and constants directly from the elastic coefficients in the overall stiffness matrix of trabecular bone test specimens. Contrary to earlier developed techniques, this method does not require pure orthotropic behavior or additional fabric measurements. The method uses high-resolution computer reconstructions of trabecular bone specimens as input for large-scale FE-analyses to determine all the 21 elastic coefficients in the overall stiffness matrix of the specimen, using a direct mechanics approach. An optimization procedure is then used to find the coordinate transformation that yields the best orthotropic representation of this matrix. The method is illustrated here relative to two trabecular bone specimens. The techniques developed here can be used to obtain a complete characterization of the mechanical properties of trabecular architecture. With the development of in vivo reconstruction techniques, even in vivo measurements will be possible.     

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     

A global relationship between trabecular bone morphology and homogenized elastic properties.

An alternative concept of the relationship between morphological and elastic properties of trabecular bone is presented and applied to human tissue from several anatomical locations using a digital approach. The three-dimensional morphology of trabecular bone was assessed with a microcomputed tomography system and the method of directed secants as well as the star volume procedure were used to compute mean intercept length (MIL) and average bone length (ABL) of 4 mm cubic specimens. Assuming isotropic elastic properties for the trabecular tissue, the general elastic tensors of the bone specimens were determined using the homogenization method and the closest orthotropic tensors were calculated with an optimization algorithm. The assumption of orthotropy for trabecular bone was found to improve with specimen size and hold within 6.1 percent for a 4 mm cube size. A strong global relationship (r2 = 0.95) was obtained between fabric and the orthotropic elastic tensor with a minimal set of five constants. Mean intercept length and average bone length provided an equivalent power of prediction. These results support the hypothesis that the elastic properties of human trabecular bone from an arbitrary anatomical location can be estimated from an approximation of the anisotropic morphology and a prior knowledge of tissue properties.     

Elastic modulus of trabecular bone material

An ultrasonic technique was used to measure both the elastic modulus (Young's modulus) of trabecular bone material and the elastic modulus of the cancellous structure. The average trabecular modulus, measured on specimens obtained from three human and one bovine distal femora, was 13.0 GPa (S.D. 1.47) and 10.9 GPa (S.D. 1.57), respectively. On human specimens the structural elastic modulus was found to be related to the structural (apparent) density raised to the 1.88 power. The elastic modulus from the bovine specimens showed a more linear relationship with the density of the cancellous structure (density raised to the 1.57 power).     

On Wolff's law of trabecular architecture.

Several studies suggest that the yield strain in cancellous bone may be uniformly distributed and isotropic. Yield strain was reported to be independent of textural anisotropy in bovine cancellous bone [Turner, J. biomech. Engng 111, 1-5 (1989)] and it is plausible that yield strain is isotropic in human cancellous bone as well. In this paper, it is hypothesized that uniform, isotropic strain represents a goal of cancellous bone adaptation, i.e. cancellous bone alters its structure to maintain uniform, isotropic peak strains. Therefore, textural anisotropy must exactly cancel the anisotropy of the peak principal stresses imposed upon cancellous bone. When evaluating the relationships between mechanical properties of cancellous bone and trabecular architecture, it was found that over 90% of the variance of yield strength can be explained by one term--rho 2H3 (where rho is apparent density and H is the normalized anisotropy (fabric) constant). Furthermore, this single term explains 70-78% of the variance in Young's modulus of cancellous bone. Based upon these findings, it was postulated that fabric adaptation goes as Hi/Hj = [ sigma i/sigma j[, where Hi and Hj are fabric eigenvalues in the i- and the j-direction and sigma i and sigma j are peak principal stresses.     

Linear poroelastic cancellous bone anisotropy: trabecular solid elastic and fluid transport properties

The mechanical performance of cancellous bone is characterized using experiments which apply linear poroelasticity theory. It is hypothesized that the anisotropic organization of the solid and pore volumes of cancellous bone can be physically characterized separately (no deformable boundary interactive effects) within the same bone sample. Due to its spongy construction, the in vivo mechanical function of cancellous or trabecular bone is dependent upon fluid and solid materials which may interact in a hydraulic, convective fashion during functional loading. This project provides insight into the organization of the tissue, ie., the trabecular connectivity, by defining the separate nature of this biphasic performance. Previous fluid flow experiments [Kohles et al., 2001, Journal of Biomechanics, 34(11), pp. 1197-1202] describe the pore space via orthotropic permeability. Ultrasonic wave propagation through the trabecular network is used to describe the solid component via orthotropic elastic moduli and material stiffness coefficients. The linear poroelastic nature of the tissue is further described by relating transport (fluid flow) and elasticity (trabecular load transmission) during regression analysis. In addition, an empirical relationship between permeability and porosity is applied to the collected data. Mean parameters in the superior-inferior (SI) orientation of cubic samples (n=20) harvested from a single bovine distal femur were the largest (p<0.05) in comparison to medial-lateral (ML) and anterior-posterior (AP) orientations: Apparent elastic modulus (2,139 MPa), permeability (4.65x10(-10) m2), and material stiffness coefficient (13.6 GPa). A negative correlation between permeability as a predictor of structural elastic modulus supported a parametric relationship in the ML (R2=0.4793), AP (R2=0.3018), and SI (R2=0.6445) directions (p<0.05).     

Tensile properties of rat femoral bone as functions of bone volume fraction, apparent density and volumetric bone mineral density

Mechanical testing has been regarded as the gold standard to investigate the effects of pathologies on the structure-function properties of the skeleton. Tensile properties of cancellous and cortical bone have been reported previously; however, no relationships describing these properties for rat bone as a function of volumetric bone mineral density (ρ(MIN)), apparent density or bone volume fraction (BV/TV) have been reported in the literature. We have shown that at macro level, compression and torsion properties of rat cortical and cancellous bone can be well described as a function of BV/TV, apparent density or ρ(MIN) using non-destructive micro-computed tomographic imaging and mechanical testing to failure. Therefore, the aim of this study is to derive a relationship expressing the tensile properties of rat cortical bone as a function of BV/TV, apparent density or ρ(MIN) over a range of normal and pathologic bones. We used bones from normal, ovariectomized and osteomalacic animals. All specimens underwent micro-computed tomographic imaging to assess bone morphometric and densitometric indices and uniaxial tension to failure. We obtained univariate relationships describing 74-77% of the tensile properties of rat cortical bone as a function of BV/TV, apparent density or ρ(MIN) over a range of density and common skeletal pathologies. The relationships reported in this study can be used in the structural rigidity to provide a non-invasive method to assess the tensile behavior of bones affected by pathology and/or treatment options.     

The cancellous bone multiscale morphology-elasticity relationship

The cancellous bone effective properties relations are analysed on multiscale across two aspects; properties of representative volume element on micro scale and statistical measure of trabecular trajectory orientation on mesoscale. Anisotropy of the microstructure is described across fabric tensor measure with trajectory orientation tensor as bridging scale connection. The scatter measured data (elastic modulus, trajectory orientation, apparent density) from compression test are fitted by stochastic interpolation procedure. The engineering constants of the elasticity tensor are estimated by last square fitt procedure in multidimensional space by Nelder-Mead simplex. The multiaxial failure surface in strain space is constructed and interpolated by modified super-ellipsoid.     

A novel approach to estimate trabecular bone anisotropy using a database approach

Continuum finite element (FE) models of bones have become a standard pre-clinical tool to estimate bone strength. These models are usually based on clinical CT scans and material properties assigned are chosen as isotropic based only on the density distribution. It has been shown, however, that trabecular bone elastic behavior is best described as orthotropic. Unfortunately, the use of orthotropic models in FE analysis derived from CT scans is hampered by the fact that the measurement of a trabecular orientation (fabric) is not possible from clinical CT images due to the low resolution of such images. In this study, we explore the concept of using a database (DB) of high-resolution bone models to derive the fabric information that is missing in clinical images. The goal of this study was to investigate if models with fabric derived from a relatively small database can already produce more accurate results than isotropic models.     

Fabric dependence of wave propagation in anisotropic porous media

Current diagnosis of bone loss and osteoporosis is based on the measurement of the bone mineral density (BMD) or the apparent mass density. Unfortunately, in most clinical ultrasound densitometers: 1) measurements are often performed in a single anatomical direction, 2) only the first wave arriving to the ultrasound probe is characterized, and 3) the analysis of bone status is based on empirical relationships between measurable quantities such as speed of sound (SOS) and broadband ultrasound attenuation (BUA) and the density of the porous medium. However, the existence of a second wave in cancellous bone has been reported, which is an unequivocal signature of poroelastic media, as predicted by Biot’s poroelastic wave propagation theory. In this paper, the governing equations for wave motion in the linear theory of anisotropic poroelastic materials are developed and extended to include the dependence of the constitutive relations upon fabric—a quantitative stereological measure of the degree of structural anisotropy in the pore architecture of a porous medium. This fabric-dependent anisotropic poroelastic approach is a theoretical framework to describe the microarchitectural-dependent relationship between measurable wave properties and the elastic constants of trabecular bone, and thus represents an alternative for bone quality assessment beyond BMD alone.     

A theoretical model to predict distribution of the fabric tensor and apparent density in cancellous bone

 The adaptation of cancellous bone to mechanical forces is well recognized. Theoretical models for predicting cancellous bone architecture have been developed and have mainly focused on the distribution of trabecular mass or the apparent density. The purpose of this study was to develop a theoretical model which can simultaneously predict the distribution of trabecular orthotropy/orientation, as represented by the fabric tensor, along with apparent density. Two sets of equations were derived under the assumption that cancellous bone is a biological self-optimizing material which tends to minimize strain energy. The first set of equations provide the relationship between the fabric tensor and stress tensor, and have been verified to be consistent with Wolff’s law of trabecular architecture, that is, the principal directions of the fabric tensor coincide with the principal stress trajectories. The second set of equations yield the apparent density from the stress tensor, which was shown to be identical to those obtained based on local optimization with strain energy density of true bone tissue as the objective function. These two sets of equations, together with elasticity field equations, provide a complete mathematical formulation for the adaptation of cancellous bone. Received: 25 February 1997/Revised version: 23 September 1997     

How morphology predicts mechanical properties of trabecular structures depends on intra-specimen trabecular thickness variations

Two observations underlie this work. First, that the architecture of trabecular bone can accurately predict the mechanical stiffness characteristics of bone specimens when considering the combination of volume fraction and fabric, which is a measure of architectural anisotropy. Second, that the same morphological measures could not accurately predict the mechanical properties of porous structures in general. We hypothesize that this discrepancy can be explained by the special nature of trabecular bone as a structure in remodeling equilibrium relative to the external loads. We tested this hypothesis using a generic model of trabecular bone. Five series of 153 different architectures were created with this model. Each architecture was subjected to morphological analysis, and four different fabric measures were calculated to evaluate their effectiveness in characterizing the architecture. Relationships were determined relating morphology to the elastic constants. The quality of these relationships was tested by correlating the predicted elastic constants with those determined from finite element analysis. We found that the four fabric measures used could estimate the mechanical properties almost equally well. So the suggestion that fabric measures based on trabecular bone volume better represent the architecture than mean intercept length could not be affirmed. We conclude that for structures with equally sized elliptical voids the mechanical properties can be predicted well only if trabecular thickness variations within each structure are limited. These structures closely resemble previously developed models of trabecular bone. Furthermore, they are stiff in the principal fabric direction, hence, according to Cowin (J. Biomech. Eng. (108) (1986) 83), they are in remodeling equilibrium. These structures are also stiff over a large range of loading orientations, hence, are relatively insensitive to deviations in direction of loading.     

Yield behavior of bovine cancellous bone

The compressive yield strain was measured for 61 specimens of bovine cancellous bone from three distal femora. There was no significant relationship (p = 0.08, R2 = 0.051) between yield strain and the degree of trabecular orientation. There was a significant positive correlation (p less than 0.00001, R2 = 0.319) between yield strain and structural (apparent) density and significant negative correlation (p less than 0.0025, R2 = 0.145) between yield strain and bone density. Yield strain correlated best with bone solid volume fraction Vv (epsilon y = 0.592 +2- 1.446vv, R2 = 0.337). The quantity, yield strain, is highly dependent on specific definitions of the yield point and the point of zero strain. For this study the yield point was defined by a 0.0003 offset criterion, and the point of zero strain was defined as the point where the tangent at 15 percent of yield crosses zero. The results using these definitions were compared with results using yield strain values determined by other definitions of the yield point and zero strain. The correlations between yield strain and trabecular orientation, structural density and bone density changed very little for differing definitions of yield. The results suggest that yield strain in cancellous bone is isotropic or independent of textural anisotropy, so the yield behaviour may be characterized by a maximum strain yield criterion. The results also suggest that the primary mode of yield in cancellous bone is buckling of the trabeculae.