The bone tissue of the canine mandible is elastically isotropic

This paper reports experimental measurements which show that canine mandibular bone tissue is elastically isotropic. Earlier work has established that human, canine and bovine cortical bone tissue of the femur, tibia and skull are elastically anisotropic and therefore the reported isotropy of mandibular tissue was unexpected. The isotropic elastic moduli of the canine mandible are represented by a Young's modulus of 7.5 GPa and a Poisson's ratio of 0.4. Earlier work gave the three orthotropic Young's moduli of the cortical one of the canine femur as 12.8 GPa, 15.6 GPa and 20.1 GPa. The experimental technique employed is elastic wave propagation at ultrasonic frequencies.     

The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques

Acoustic microscopy (30-60 microm resolution) and nanoindentation (1-5 microm resolution) are techniques that can be used to evaluate the elastic properties of human bone at a microstructural level. The goals of the current study were (1) to measure and compare the Young's moduli of trabecular and cortical bone tissues from a common human donor, and (2) to compare the Young's moduli of bone tissue measured using acoustic microscopy to those measured using nanoindentation. The Young's modulus of cortical bone in the longitudinal direction was about 40% greater than (p<0.01) the Young's modulus in the transverse direction. The Young's modulus of trabecular bone tissue was slightly higher than the transverse Young's modulus of cortical bone, but substantially lower than the longitudinal Young's modulus of cortical bone. These findings were consistent for both measurement methods and suggest that elasticity of trabecular tissue is within the range of that of cortical bone tissue. The calculation of Young's modulus using nanoindentation assumes that the material is elastically isotropic. The current results, i.e., the average anisotropy ratio (E(L)/E(T)) for cortical bone determined by nanoindentation was similar to that determined by the acoustic microscope, suggest that this assumption does not limit nanoindentation as a technique for measurement of Young's modulus in anisotropic bone.     

The elastic moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus

The elastic moduli of human subchondral, trabecular, and cortical bone tissue from a proximal tibia were experimentally determined using three-point bending tests on a microstructural level. The mean modulus of subchondral specimens was 1.15 GPa, and those of trabecular and cortical specimens was 4.59 GPa and 5.44 GPa respectively. Significant differences were found in the modulus values between bone tissues, which may have mainly resulted from the differences in the microstructures of each bone tissue rather than in the mineral density. Furthermore, the size-dependency of the modulus was examined using eight different sizes of cortical specimens (heights h = 100-1000 microns). While the modulus values for relatively large specimens (h greater than 500 microns) remained fairly constant (approximately 15 GPa), the values decreased as the specimens became smaller. A significant correlation was found between the modulus and specimen size. The surface area to volume ratio proved to be a key variable to explain the size-dependency.     

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).     

Determination of mechanical properties of human femoral cortical bone by the Hopkinson bar stress technique

The Hopkinson bar stress technique and a universal testing machine (Instron 1125) have been used to investigate the dynamic and static mechanical properties of cortical bone taken from a human femur respectively. We found that the average dynamic Young's modulus value (Ed = 19.9 GPa) to be 23% higher than the average static Young's modulus value (Ed = 16.2 GPa). Furthermore, the Poisson's ratio did not exhibit any significant variation for the two different types of loading. No difference was observed between the values of the dynamic Young's modulus in tension and those found in compression. A comparison was made of the results of this study with those found by other researchers using different techniques, such as ultrasonics, and it was found that they agree well with most of the results of previous studies. Finally, the viscosity for cortical bone found in this study correlates with viscosity reported by Tennyson et al. [Expl Mech. 12, 502-507 (1972)] for ten days post mortem age specimens.     

A novel in vivo mouse model for mechanically stimulated bone adaptation--a combined experimental and computational validation study

To facilitate the investigation of bone formation, in vivo, in response to mechanical loading a caudal vertebra axial compression device (CVAD) has been developed to deliver precise mechanical loads to the fifth caudal vertebra (C5) of the C57BL/6 female mouse. A combined experimental and computational approach was used to quantify the micro-mechanical strain induced in trabecular and cortical components following static and dynamic loading using the CVAD. Cortical bone strains were recorded using micro-strain gages. Finite element (FE) models based on micro-computed tomography were constructed for all C5 vertebrae. Both theoretical and experimental cortical strains correlated extremely well (R(2)>0.96) for a Young's modulus of 14.8 GPa, thus validating the FE model. In this study, we have successfully applied mechanical loads to the C5 murine vertebrae, demonstrating the potential of this model to be used for in vivo loading studies aimed at stimulating both trabecular and cortical bone adaptation.     

How is the indentation modulus of bone tissue related to its macroscopic elastic response? A validation study

This work consists of the validation of a novel approach to estimate the local anisotropic elastic constants of the bone extracellular matrix using nanoindentation. For this purpose, nanoindentation on two planes of material symmetry were analyzed and the resulting longitudinal elastic moduli compared to the moduli measured with a macroscopic tensile test. A combined lathe and tensile system was designed that allows machining and testing of cylindrical microspecimens of approximately 4mm in length and 300 microm in diameter. Three bovine specimens were tested in tension and their outer geometry and porosity assessed by synchrotron radiation microtomography. Based on the results of the traction test and the precise outer geometry, an apparent longitudinal Young's modulus was calculated. Results between 20.3 and 27.6 GPa were found that match with previously reported values for bovine compact bone. The same specimens were then characterized by nanoindentation on a transverse and longitudinal plane. A longitudinal Young's modulus for the bone matrix was then derived using the numerical scheme proposed by Swadener and Pharr and the fabric-elasticity relationship by Zysset and Curnier. Based on the matrix modulus and a power law effective volume fraction, an apparent longitudinal Young's modulus was predicted for each microspecimen. This alternative approach provided values between 19.9 and 30.0 GPa, demonstrating differences between 2% and 13% to the values provided by the initial tensile test. This study therefore raises confidence in our nanoindentation protocol of the bone extracellular matrix and supports the underlying hypotheses used to extract the anisotropic elastic constants.     

Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue

The ability to determine trabecular bone tissue elastic and failure properties has biological and clinical importance. To date, trabecular tissue yield strains remain unknown due to experimental difficulties, and elastic moduli studies have reported controversial results. We hypothesized that the elastic and tensile and compressive yield properties of trabecular tissue are similar to those of cortical tissue. Effective tissue modulus and yield strains were calibrated for cadaveric human femoral neck specimens taken from 11 donors, using a combination of apparent-level mechanical testing and specimen-specific, high-resolution, nonlinear finite element modeling. The trabecular tissue properties were then compared to measured elastic modulus and tensile yield strain of human femoral diaphyseal cortical bone specimens obtained from a similar cohort of 34 donors. Cortical tissue properties were obtained by statistically eliminating the effects of vascular porosity. Results indicated that mean elastic modulus was 10% lower (p<0.05) for the trabecular tissue (18.0+/-2.8 GPa) than for the cortical tissue (19.9+/-1.8 GPa), and the 0.2% offset tensile yield strain was 15% lower for the trabecular tissue (0.62+/-0.04% vs. 0.73+/-0.05%, p<0.001). The tensile-compressive yield strength asymmetry for the trabecular tissue, 0.62 on average, was similar to values reported in the literature for cortical bone. We conclude that while the elastic modulus and yield strains for trabecular tissue are just slightly lower than those of cortical tissue, because of the cumulative effect of these differences, tissue strength is about 25% greater for cortical bone.     

Validation of a voxel-based FE method for prediction of the uniaxial apparent modulus of human trabecular bone using macroscopic mechanical tests and nanoindentation

Assessment of the mechanical properties of trabecular bone is of major biological and clinical importance for the investigation of bone diseases, fractures and their treatments. Finite element (FE) methods are getting increasingly popular for quantifying the elastic and failure properties of trabecular bone. In particular, voxel-based FE methods have been previously used to calculate the effective elastic properties of trabecular microstructures. However, in most studies, bone tissue moduli were assumed or back-calculated to match the apparent elastic moduli from experiments, which often lead to surprisingly low values when compared to nanoindentation results. In this study, voxel-based FE analysis of trabecular bone is combined with physical measures of volume fraction, micro-CT (microCT) reconstructions, uniaxial mechanical tests and specimen-specific nanoindentation tests for proper validation of the method. Cylindrical specimens of cancellous bone were extracted from human femurs and their volume fraction determined with Archimede's method. Uniaxial apparent modulus of the specimens was measured with an improved tension-compression testing protocol that minimizes boundary artefacts. Their microCT reconstructions were segmented to match the measured bone volume fraction and used to create full-size voxel models with 30-45 microm element size. For each specimen, linear isotropic elastic material properties were defined based on specific nanoindentation measurements of its embedded bone tissue. Linear FE analyses were finally performed to simulate the uniaxial mechanical tests. Additional parametric analyses were performed to evaluate the potential errors on the predicted apparent modulus arising from variations in segmentation threshold, tissue modulus, and the use of 125-mm(3) cubic sub-regions. The results demonstrate an excellent correspondence between experimental measures and FE predictions of uniaxial apparent modulus. In conclusion, the adopted voxel-based FE approach is found to be a robust method to predict the linear elastic properties of human cancellous bone, provided segmentation of the microCT reconstructions is carefully calibrated, tissue modulus is known a priori and the entire region of interest is included in the analysis.     

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).     

Biomechanical effect of mineral heterogeneity in trabecular bone

Due to daily loading, trabecular bone is subjected to deformations (i.e., strain), which lead to stress in the bone tissue. When stress and/or strain deviate from the normal range, the remodeling process leads to adaptation of the bone architecture and its degree of mineralization to effectively withstand the sustained altered loading. As the apparent mechanical properties of bone are assumed to depend on the degree and distribution of mineralization, the goal of the present study was examine the influences of mineral heterogeneity on the biomechanical properties of trabecular bone in the human mandibular condyle. For this purpose nine right condyles from human dentate mandibles were scanned and evaluated with a microCT system. Cubic regional volumes of interest were defined, and each was transformed into two different types of finite element (FE) models, one homogeneous and one heterogeneous. In the heterogeneous models the element tissue moduli were scaled to the local degree of mineralization, which was determined using microCT. Compression and shear tests were simulated to determine the apparent elastic moduli in both model types. The incorporation of mineralization variation decreased the apparent Young's and shear moduli by maximally 21% in comparison to the homogeneous models. The heterogeneous model apparent moduli correlated significantly with bone volume fraction and degree of mineralization. It was concluded that disregarding mineral heterogeneity may lead to considerable overestimation of apparent elastic moduli in FE models.     

Elasticity of alveolar bone near dental implant-bone interfaces after one month's healing

Information is scarce about Young's modulus of healing bone surrounding an implant. The purpose of this preliminary study is to quantify elastic properties of pig alveolar bone that has healed for 1 month around titanium threaded dental implants, using the nanoindentation method. Two 2-year-old Sinclair miniswine were used for the study. Nanoindentation tests perpendicular to the bucco-lingual cross section were performed on harvested implant-bone blocks using the Hysitron TriboScope III. Nomarski differential interference contrast microscopy was used to identify pyramidal indentation measurements that were from bone. Reduced moduli, averaged for all anatomical regions, were found to start low (6.17 GPa) at the interface and gradually increase (slope=0.014) to a distance of 150 microm (7.89 GPa) from the implant surface, and then flatten to a slope of 0.001 from 150 to 1500 microm (10.13 GPa). Mean reduced modulus and its relationship to distance did not differ significantly by anatomic location (e.g., coronal, middle, and apical third; P>/=0.28 for all relevant tests) at 1 month after implantation.     

Static and dynamic finite element analyses of an idealized structural model of vertebral trabecular bone.

An idealized three-dimensional finite element model of a rodlike trabecular bone structure was developed to study its static and dynamic responses under compressive loading, considering the effects of bone marrow and apparent density. Static analysis of the model predicted hydraulic stiffening of trabecular bone due to the presence of bone marrow. The predicted power equation relating trabecular bone apparent elastic modulus to its apparent density was in good agreement with those of the reported experimental investigations. The ratio of the maximum stress in the trabecular bone tissue to its apparent stress had a high value, decreasing with increasing bone apparent density. Frequency analyses of the model predicted higher natural frequencies for the bone without marrow than those for the bone with marrow. Adding a mass relatively large compared to that of bone rendered a single-degree-of-freedom response. In this case, the resonant frequency was higher for the bone with marrow than that for the bone without marrow. The predicted vibrational measurement of apparent modulus was in good agreement with that of the static measurement, suggesting vibrational testing as a method for nondestructive measurement of trabecular bone elastic moduli.     

On the dependence of the elasticity and strength of cancellous bone on apparent density

This paper presents a statistical analysis of the pooled data from a number of previous experiments concerning the dependence of the Young's moduli and strength of cancellous bone tissue upon apparent density. The results show that both the Young's moduli and the strength are proportional to the square of apparent density of the tissue and are therefore proportional to one another. It is shown that the coefficient of proportionality is different for human and bovine tissue. It is concluded that the suggestion of Wolff (Das Gesetz der Transformation der Knochen, Hirschwald, Berlin, 1892) that compact bone tissue is simply more dense cancellous bone tissue is not an accurate statement when only the mechanical properties of these two tissues are considered. It is noted that estimates for the elastic modulus of the individual trabecula of human cancellous bone vary from 1 to 20 GPa and it is suggested that this question needs further study.     

The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone

The Young's modulus of elasticity, the calcium content and the volume fraction (1-porosity) of 23 tension specimens and 80 bending specimens, taken from compact bone of 18 species of mammal, bird and reptile, were determined. There was a strong positive relationship between Young's modulus and both calcium content and volume fraction. A power law model fits the data better than a linear model. Young's modulus has a roughly cubic relationship with both calcium content and volume fraction. Over 80% of the total variation in Young's modulus in this data set is explained by these two variables.     

Effects of thresholding techniques on microCT-based finite element models of trabecular bone

Microimaging based finite element analysis is widely used to predict the mechanical properties of trabecular bone. The choice of thresholding technique, a necessary step in converting grayscale images to finite element models, can significantly influence the predicted bone volume fraction and mechanical properties. Therefore, we investigated the effects of thresholding techniques on microcomputed tomography (micro-CT) based finite element models of trabecular bone. Three types of thresholding techniques were applied to 16-bit micro-CT images of trabecular bone to create three different models per specimen. Bone volume fractions and apparent moduli were predicted and compared to experimental results. In addition, trabecular tissue mechanical parameters and morphological parameters were compared among different models. Our findings suggest that predictions of apparent mechanical properties and structural properties agree well with experimental measurements regardless of the choice of thresholding methods or the format of micro-CT images.     

The effects of bone and pore volume fraction on the mechanical properties of PMMA/bone biopsies extracted from augmented vertebrae

Vertebroplasty forms a porous PMMA/bone composite which was shown to be weaker and less stiff than pure PMMA. It is not known what determines the mechanical properties of such composites in detail. This study investigated the effects of bone volume fraction (BV/TV), cement porosity (PV/(TV-BV), PV…pore volume) and cement stiffness. Nine human vertebral bodies were augmented with either standard or low-modulus PMMA cement and scanned with a HR-pQCT system before and after augmentation. Fourteen cylindrical PMMA/bone biopsies were extracted from the augmented region, scanned with a micro-CT system and tested in compression until failure. Micro-finite element (FE) models of the complete biopsies, of the trabecular bone alone as well as of the porous cement alone were generated from CT images to gain more insight into the role of bone and pores. PV/(TV-BV) and experimental moduli of standard/low-modulus cement (R(2)=0.91/0.98) as well as PV/(TV-BV) and yield stresses (R(2)=0.92/0.83) were highly correlated. No correlation between BV/TV (ranging from 0.057 to 0.138) and elastic moduli was observed (R(2)< 0.05). Interestingly, the micro-FE models of the porous cement alone reproduced the experimental elastic moduli of the standard/low-modulus cement biopsies (R(2)=0.75/0.76) more accurately than the models with bone (R(2)=0.58/0.31). In conclusion, the mechanical properties of the biopsies were mainly determined by the cement porosity and the cement material properties. The study showed that bone tissue inside the biopsies was mechanically "switched off" such that load was carried essentially by the porous PMMA.     

Stochastic multi-scale prediction on the apparent elastic moduli of trabecular bone considering uncertainties of biological apatite (BAp) crystallite orientation and image-based modelling

An assessment of the mechanical properties of trabecular bone is important in determining the fracture risk of human bones. Many uncertainty factors contribute to the dispersion of the estimated mechanical properties of trabecular bone. This study was undertaken in order to propose a computational scheme that will be able to predict the effective apparent elastic moduli of trabecular bone considering the uncertainties that are primarily caused by image-based modelling and trabecular stiffness orientation. The effect of image-based modelling which focused on the connectivity was also investigated. A stochastic multi-scale method using a first-order perturbation-based and asymptotic homogenisation theory was applied to formulate the stochastically apparent elastic properties of trabecular bone. The effective apparent elastic modulus was predicted with the introduction of a coefficient factor to represent the variation of bone characteristics due to inter-individual differences. The mean value of the predicted effective apparent Young's modulus in principal axis was found at approximately 460 MPa for respective 15.24% of bone volume fraction, and this is in good agreement with other experimental results. The proposed method may provide a reference for the reliable evaluation of the prediction of the apparent elastic properties of trabecular bone.     

Micromechanical response of mineral and collagen phases in bone

We report the first simultaneous quantification of Young's modulus in the separate material phases of bone: collagen and carbonated hydroxyapatite. High-energy X-ray scattering and in situ loading revealed macroscopic, mineral, and collagen Young's moduli (90% confidence limit) for a canine fibula equaled 24.7(0.2) GPa, 38.2(0.5) GPa {for 00.4 and 43.6(1.4) GPa for 22.2}, and 18(1.2) GPa, respectively. The mineral contained compressive residual stresses on the order of -60 to -80 MPa before loading and had a stress enhancement (ratio of internal to applied stress) between 2.0 and 2.3. The diffraction peak width increased with increasing applied stress, mainly along the bone's longitudinal direction, and peak widths returned to pre-deformation values when load was removed. In a second fibula section from the same animal, the mineral's internal stress changed from -50 MPa (22.2 reflection) to -75 MPa (00.4) just after removal from formalin to -10 MPa after eight hours immersion in phosphate-buffered saline; the corresponding change in collagen D-spacing DeltaD/D equaled 4.2x10(-3).     

The role of an effective isotropic tissue modulus in the elastic properties of cancellous bone.

Conceptually, the elastic characteristics of cancellous bone could be predicted directly from the trabecular morphology--or architecture--and by the elastic properties of the tissue itself. Although hardly any experimental evidence exists, it is often implicitly assumed that tissue anisotropy has a negligible effect on the apparent elastic properties of cancellous bone. The question addressed in this paper is whether this is actually true. If it is, then micromechanical finite element analysis (micro-FEA) models, representing trabecular architecture, using an 'effective isotropic tissue modulus' should be able to predict apparent elastic properties of cancellous bone. To test this, accurate multi-axial compressive mechanical tests of 29 whale bone specimens were simulated with specimen-specific micro-FEA computer models built from true three-dimensional reconstructions. By scaling the micro-FEA predictions by a constant tissue modulus, 92% of the variation of Young's moduli determined experimentally could be explained. The correlation even increased to 95% when the micro-FEA moduli were scaled to the isotropic tissue moduli of individual specimens. Excellent agreement was also found in the elastic symmetry axes and anisotropy ratios. The prediction of Poisson's ratios was somewhat less precise at 85% correlation. The results support the hypothesis; for practical purposes, the concept of an 'effective isotropic tissue modulus' concept is a viable one. They also suggest that the value of such a modulus for individual cases might be inferred from the average tissue density, hence the degree of mineralization. Future studies must clarify how specific the tissue modulus should be for different types of bone if adequate predictions of elastic behavior are to be made in this way.