Potential of in vivo MRI-based nonlinear finite-element analysis for the assessment of trabecular bone post-yield properties.

PURPOSE Bone strength is the key factor impacting fracture risk. Assessment of bone strength from high-resolution (HR) images have largely relied on linear micro-finite element analysis (μFEA) even though failure always occurs beyond the yield point, which is outside the linear regime. Nonlinear μFEA may therefore be more informative in predicting failure behavior. However, existing nonlinear models applied to trabecular bone (TB) have largely been confined to micro-computed tomography (μCT) and, more recently, HR peripheral quantitative computed tomography (HR-pQCT) images, and typically have ignored evaluation of the post-yield behavior. The primary purpose of this work was threefold: (1) to provide an improved algorithm and program to assess TB yield as well as post-yield properties; (2) to explore the potential benefits of nonlinear μFEA beyond its linear counterpart; and (3) to assess the feasibility and practicality of performing nonlinear analysis on desktop computers on the basis of micro-magnetic resonance (μMR) images obtained in vivo in patients. METHODS A method for nonlinear μFE modeling of TB yield as well as post-yield behavior has been designed where material nonlinearity is captured by adjusting the tissue modulus iteratively according to the tissue-level effective strain obtained from linear analysis using a computationally optimized algorithm. The software allows for images at in vivo μMRI resolution as input with retention of grayscale information. Associations between axial stiffness estimated from linear analysis and yield as well as post-yield parameters from nonlinear analysis were investigated from in vivo μMR images of the distal tibia (N = 20; ages: 58-84) and radius (N = 20; ages: 50-75). RESULTS All simulations were completed in 1 h or less for 61 strain levels using a desktop computer (dual quad-core Xeon 3.16 GHz CPUs equipped with 40 GB of RAM). Although yield stress and ultimate stress correlated strongly (R(2) > 0.95, p < 0.001) with axial stiffness, toughness correlated moderately at the distal tibia (R(2) = 0.81, p < 0.001) and only weakly at the distal radius (R(2) = 0.34, p = 0.007). Further, toughness was found to vary by up to 16% for bone of very similar axial stiffness (<2%). CONCLUSIONS The work demonstrates the practicality of nonlinear μFE simulations at in vivo μMRI resolution, as well as its potential for providing additional information beyond that obtainable from linear analysis. The data suggest that a direct assessment of toughness may provide information not captured by stiffness.

[1]  Steven K Boyd,et al.  Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. , 2008, Bone.

[2]  A. Wright,et al.  Quantitative MRI for the assessment of bone structure and function , 2006, NMR in biomedicine.

[3]  R Huiskes,et al.  The role of an effective isotropic tissue modulus in the elastic properties of cancellous bone. , 1999, Journal of biomechanics.

[4]  Bert Van Rietbergen,et al.  Finite Element Analysis Based on In Vivo HR‐pQCT Images of the Distal Radius Is Associated With Wrist Fracture in Postmenopausal Women , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[5]  J. Macneil,et al.  Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. , 2007, Medical engineering & physics.

[6]  P Rüegsegger,et al.  The quality of trabecular bone evaluated with micro-computed tomography, FEA and mechanical testing. , 1997, Studies in health technology and informatics.

[7]  David Christen,et al.  Multiscale modelling and nonlinear finite element analysis as clinical tools for the assessment of fracture risk , 2010, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[8]  S. Goldstein,et al.  Finite‐element modeling of trabecular bone: Comparison with mechanical testing and determination of tissue modulus , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[9]  T. Keaveny,et al.  Yield strain behavior of trabecular bone. , 1998, Journal of biomechanics.

[10]  T. Keaveny,et al.  Mechanisms of uniformity of yield strains for trabecular bone. , 2004, Journal of biomechanics.

[11]  G. Niebur,et al.  Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. , 2004, Journal of biomechanics.

[12]  Ning Zhang,et al.  Computationally-Optimized Bone Mechanical Modeling from High-Resolution Structural Images , 2012, PloS one.

[13]  Ming Zhang,et al.  Relationships Between Femoral Strength Evaluated by Nonlinear Finite Element Analysis and BMD, Material Distribution and Geometric Morphology , 2012, Annals of Biomedical Engineering.

[14]  R. Huiskes,et al.  Please Scroll down for Article Computer Methods in Biomechanics and Biomedical Engineering Micro-finite Element Simulation of Trabecular-bone Post-yield Behaviour -effects of Material Model, Element Size and Type Micro-finite Element Simulation of Trabecular-bone Post-yield Behaviour – Effects of Ma , 2022 .

[15]  Harry K. Genant,et al.  Appendicular Bone Density and Age Predict Hip Fracture in Women , 1990 .

[16]  Felix W Wehrli,et al.  In Vivo μMRI‐Based Finite Element and Morphological Analyses of Tibial Trabecular Bone in Eugonadal and Hypogonadal Men Before and After Testosterone Treatment , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[17]  T. Keaveny,et al.  Trabecular bone strength predictions using finite element analysis of micro-scale images at limited spatial resolution. , 2009, Bone.

[18]  J. Kinney,et al.  On the importance of geometric nonlinearity in finite-element simulations of trabecular bone failure. , 2003, Bone.

[19]  Ralph Müller,et al.  Long-term prediction of three-dimensional bone architecture in simulations of pre-, peri- and post-menopausal microstructural bone remodeling , 2005, Osteoporosis International.

[20]  F. Wehrli,et al.  Structural and mechanical parameters of trabecular bone estimated from in vivo high‐resolution magnetic resonance images at 3 tesla field strength , 2010, Journal of magnetic resonance imaging : JMRI.

[21]  Yinxiao Liu,et al.  Performance of the MRI-based virtual bone biopsy in the distal radius: serial reproducibility and reliability of structural and mechanical parameters in women representative of osteoporosis study populations. , 2011, Bone.

[22]  F W Wehrli,et al.  Spin‐echo micro‐MRI of trabecular bone using improved 3D fast large‐angle spin‐echo (FLASE) , 2009, Magnetic resonance in medicine.

[23]  Jeremy F Magland,et al.  Computational biomechanics of the distal tibia from high-resolution MR and micro-CT images. , 2010, Bone.

[24]  F. Eckstein,et al.  Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. , 2002, Bone.

[25]  Ralph Müller,et al.  Prediction of failure load using micro-finite element analysis models: Toward in vivo strength assessment. , 2006, Drug discovery today. Technologies.

[26]  H. Song,et al.  In vivo micro‐imaging using alternating navigator echoes with applications to cancellous bone structural analysis , 1999, Magnetic resonance in medicine.

[27]  Claus Christiansen,et al.  Diagnosis of Osteoporosis , 1992, Southern medical journal.

[28]  D. Fyhrie,et al.  The dependence between the strength and stiffness of cancellous and cortical bone tissue for tension and compression: extension of a unifying principle. , 2004, Bio-medical materials and engineering.

[29]  H. Song,et al.  Fast 3D large‐angle spin‐echo imaging (3D FLASE) , 1996, Magnetic resonance in medicine.

[30]  C. Turner,et al.  Better discrimination of hip fracture using bone density, geometry and architecture , 1995, Osteoporosis International.

[31]  D P Fyhrie,et al.  Failure mechanisms in human vertebral cancellous bone. , 1994, Bone.

[32]  J. Keyak Improved prediction of proximal femoral fracture load using nonlinear finite element models. , 2001, Medical engineering & physics.

[33]  Jeremy F Magland,et al.  Mechanical Implications of Estrogen Supplementation in Early Postmenopausal Women , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[34]  Sharmila Majumdar,et al.  Magnetic Resonance Imaging of Trabecular Bone Structure , 2002, Topics in magnetic resonance imaging : TMRI.

[35]  D. Drinkwater,et al.  Regional and total body bone mineral content, bone mineral density, and total body tissue composition in children 8–16 years of age , 1993, Calcified Tissue International.

[36]  S. Ott When bone mass fails to predict bone failure , 2005, Calcified Tissue International.

[37]  J. Crisco,et al.  Rotational Head Kinematics in Football Impacts: An Injury Risk Function for Concussion , 2011, Annals of Biomedical Engineering.

[38]  Felix Eckstein,et al.  Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. , 2011, Bone.

[39]  X. Guo,et al.  Mechanical consequence of trabecular bone loss and its treatment: a three-dimensional model simulation. , 2002, Bone.

[40]  P. Papadopoulos,et al.  Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. , 2006, Bone.

[41]  Yifei Dai,et al.  Robust QCT/FEA Models of Proximal Femur Stiffness and Fracture Load During a Sideways Fall on the Hip , 2011, Annals of Biomedical Engineering.

[42]  R Huiskes,et al.  Indirect determination of trabecular bone effective tissue failure properties using micro-finite element simulations. , 2008, Journal of biomechanics.

[43]  C. Slemenda,et al.  Age and bone mass as predictors of fracture in a prospective study. , 1988, The Journal of clinical investigation.

[44]  G. A. Ladinsky,et al.  Image metric‐based correction (autofocusing) of motion artifacts in high‐resolution trabecular bone imaging , 2007, Journal of magnetic resonance imaging : JMRI.

[45]  T. Keaveny,et al.  Dependence of yield strain of human trabecular bone on anatomic site. , 2001, Journal of biomechanics.

[46]  Jeremy F Magland,et al.  Micro-MR imaging-based computational biomechanics demonstrates reduction in cortical and trabecular bone strength after renal transplantation. , 2012, Radiology.

[47]  Ralph Müller,et al.  Mechanical and Architectural Bone Adaptation in Early Stage Experimental Osteoarthritis , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[48]  Thomas J. R. Hughes,et al.  LARGE-SCALE VECTORIZED IMPLICIT CALCULATIONS IN SOLID MECHANICS ON A CRAY X-MP/48 UTILIZING EBE PRECONDITIONED CONJUGATE GRADIENTS. , 1986 .

[49]  M Y He,et al.  Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone. , 2006, Acta biomaterialia.

[50]  E. Schneider,et al.  Radius Bone Strength in Bending, Compression, and Falling and Its Correlation With Clinical Densitometry at Multiple Sites , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[51]  W C Hayes,et al.  Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. , 1994, Journal of biomechanics.

[52]  R. Huiskes,et al.  A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. , 1995, Journal of biomechanics.

[53]  R. Heaney,et al.  Is the paradigm shifting? , 2003, Bone.

[54]  O Johnell,et al.  Femoral neck geometry and radiographic signs of osteoporosis as predictors of hip fracture. , 1996, Bone.

[55]  G. Niebur,et al.  High-resolution finite element models with tissue strength asymmetry accurately predict failure of trabecular bone. , 2000, Journal of biomechanics.

[56]  Mechanical behavior of human trabecular bone after overloading , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[57]  Felix W. Wehrli,et al.  A novel local thresholding algorithm for trabecular bone volume fraction mapping in the limited spatial resolution regime of in vivo MRI , 2005, IEEE Transactions on Medical Imaging.