Limitations of Global Morphometry in Predicting Trabecular Bone Failure

Efforts in finding independent measures for accurate and reliable prediction of trabecular bone failure have led to the development of a number of morphometric indices characterizing trabecular bone microstructure. Generally, these indices assume a high homogeneity within the bone specimen. However, in the present study we found that the variance in bone volume fraction (BV/TV) in a single bone specimen can be relatively large (CV = 9.07% to 28.23%). To assess the limitations of morphometric indices in the prediction of bone failure for specimens in which the assumption of homogeneity is not met, we harvested 13 cadaveric samples from a single human spine. We tested these cylindrical samples using image‐guided failure assessment (IGFA), a technique combining stepwise microcompression and time‐lapsed micro–computed tomography (µCT). Additionally, we computed morphometric indices for the entire sample as well as for 10 equal subregions along the anatomical axis. We found that ultimate strength was equally well predicted by BV/TV of the entire sample (R2 = 0.55) and BV/TV of the weakest subregion (R2 = 0.57). Investigating three‐dimensional animations of structural bone failure, we showed that two main failure mechanisms determine the competence of trabecular bone samples; in homogeneous, isotropic trabecular bone samples, competence is determined by a whole set of trabecular elements, whereas in inhomogeneous, anisotropic bone samples a single or a missing trabeculae may induce catastrophic failure. The latter failure mechanism cannot be described by conventional morphometry, indicating the need for novel morphometric indices also applicable to the prediction of failure in inhomogeneous bone samples. © 2014 American Society for Bone and Mineral Research.

[1]  P. Papadopoulos,et al.  Vertebral fragility and structural redundancy , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[2]  R. Müller,et al.  Vertebral body bone strength: the contribution of individual trabecular element morphology , 2012, Osteoporosis International.

[3]  Jan D'hooge,et al.  Fast and accurate specimen-specific simulation of trabecular bone elastic modulus using novel beam-shell finite element models. , 2011, Journal of biomechanics.

[4]  Mathieu Charlebois,et al.  The role of fabric in the large strain compressive behavior of human trabecular bone. , 2010, Journal of biomechanical engineering.

[5]  Tony M Keaveny,et al.  Heterogeneity of yield strain in low-density versus high-density human trabecular bone. , 2009, Journal of biomechanics.

[6]  B. Snyder,et al.  Bone Volume Fraction Explains the Variation in Strength and Stiffness of Cancellous Bone Affected by Metastatic Cancer and Osteoporosis , 2008, Calcified Tissue International.

[7]  Paul Sajda,et al.  Complete Volumetric Decomposition of Individual Trabecular Plates and Rods and Its Morphological Correlations With Anisotropic Elastic Moduli in Human Trabecular Bone , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[8]  X Edward Guo,et al.  Contributions of trabecular rods of various orientations in determining the elastic properties of human vertebral trabecular bone. , 2007, Bone.

[9]  G H van Lenthe,et al.  Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. , 2006, Bone.

[10]  B. Snyder,et al.  The interaction of microstructure and volume fraction in predicting failure in cancellous bone. , 2006, Bone.

[11]  Ralph Müller,et al.  Volumetric spatial decomposition of trabecular bone into rods and plates--a new method for local bone morphometry. , 2006, Bone.

[12]  Ralph Müller,et al.  Importance of Individual Rods and Plates in the Assessment of Bone Quality and Their Contribution to Bone Stiffness , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[13]  Ralph Müller,et al.  Design and implementation of a novel mechanical testing system for cellular solids. , 2005, Journal of biomedical materials research. Part B, Applied biomaterials.

[14]  Philippe K Zysset,et al.  A review of morphology-elasticity relationships in human trabecular bone: theories and experiments. , 2003, Journal of biomechanics.

[15]  R. Müller,et al.  Three-dimensional quantitation of periradicular bone destruction by micro-computed tomography. , 2003, Journal of endodontics.

[16]  Punam K Saha,et al.  Topology-based orientation analysis of trabecular bone networks. , 2003, Medical physics.

[17]  R Müller,et al.  Effects of Daily Treatment with Parathyroid Hormone on Bone Microarchitecture and Turnover in Patients with Osteoporosis: A Paired Biopsy Study * , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[18]  R. Müller,et al.  Human Parathyroid Hormone 1–34 Reverses Bone Loss in Ovariectomized Mice , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[19]  R Müller,et al.  Genetic Regulation of Cortical and Trabecular Bone Strength and Microstructure in Inbred Strains of Mice , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[20]  K. Balto,et al.  Quantification of Periapical Bone Destruction in Mice by Micro-computed Tomography , 2000, Journal of dental research.

[21]  P. Rüegsegger,et al.  Direct Three‐Dimensional Morphometric Analysis of Human Cancellous Bone: Microstructural Data from Spine, Femur, Iliac Crest, and Calcaneus , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  R. Coatney,et al.  Applications of micro-CT and MR microscopy to study pre-clinical models of osteoporosis and osteoarthritis. , 1998, Technology and health care : official journal of the European Society for Engineering and Medicine.

[23]  W C Hayes,et al.  Micro-compression: a novel technique for the nondestructive assessment of local bone failure. , 1998, Technology and health care : official journal of the European Society for Engineering and Medicine.

[24]  P. Rüegsegger,et al.  Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. , 1998, Bone.

[25]  L. Gibson,et al.  Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. , 1997, Bone.

[26]  A Odgaard,et al.  Three-dimensional methods for quantification of cancellous bone architecture. , 1997, Bone.

[27]  T. Keaveny,et al.  Systematic and random errors in compression testing of trabecular bone , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[28]  P. Rüegsegger,et al.  A new method for the model‐independent assessment of thickness in three‐dimensional images , 1997 .

[29]  L. Melton,et al.  The worldwide problem of osteoporosis: insights afforded by epidemiology. , 1995, Bone.

[30]  T. Keller Predicting the compressive mechanical behavior of bone. , 1994, Journal of biomechanics.

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

[32]  T. McMahon,et al.  Trabecular bone exhibits fully linear elastic behavior and yields at low strains. , 1994, Journal of biomechanics.

[33]  S A Goldstein,et al.  The relationship between the structural and orthogonal compressive properties of trabecular bone. , 1994, Journal of biomechanics.

[34]  W C Hayes,et al.  Trabecular bone modulus and strength can depend on specimen geometry. , 1993, Journal of biomechanics.

[35]  C H Turner,et al.  Basic biomechanical measurements of bone: a tutorial. , 1993, Bone.

[36]  Harry K. Genant,et al.  Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. , 1993, The American journal of medicine.

[37]  W. Hayes,et al.  Theoretical analysis of the experimental artifact in trabecular bone compressive modulus. , 1993, Journal of biomechanics.

[38]  H. Gundersen,et al.  Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. , 1993, Bone.

[39]  M Vogel,et al.  Trabecular bone pattern factor--a new parameter for simple quantification of bone microarchitecture. , 1992, Bone.

[40]  Frank Linde,et al.  The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. , 1992, Journal of biomechanics.

[41]  William E. Lorensen,et al.  Marching cubes: A high resolution 3D surface construction algorithm , 1987, SIGGRAPH.

[42]  W. Hayes,et al.  The compressive behavior of bone as a two-phase porous structure. , 1977, The Journal of bone and joint surgery. American volume.

[43]  M Viceconti,et al.  Dependence of mechanical compressive strength on local variations in microarchitecture in cancellous bone of proximal human femur. , 2008, Journal of biomechanics.

[44]  P. Rüegsegger,et al.  A microtomographic system for the nondestructive evaluation of bone architecture , 2006, Calcified Tissue International.

[45]  R. Müller,et al.  Time-lapsed microstructural imaging of bone failure behavior. , 2004, Journal of biomechanics.

[46]  Ralph Müller,et al.  Microarchitectural aspects of quality and competence of bone , 2004 .

[47]  Stefan Judex,et al.  Combining high-resolution micro-computed tomography with material composition to define the quality of bone tissue , 2003, Current osteoporosis reports.

[48]  H. Jinnai,et al.  Surface curvatures of trabecular bone microarchitecture. , 2002, Bone.

[49]  P Rüegsegger,et al.  Micro-tomographic imaging for the nondestructive evaluation of trabecular bone architecture. , 1997, Studies in health technology and informatics.

[50]  TOR Hildebrand,et al.  Quantification of Bone Microarchitecture with the Structure Model Index. , 1997, Computer methods in biomechanics and biomedical engineering.

[51]  P Rüegsegger,et al.  Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. , 1994, Physics in medicine and biology.

[52]  F. Linde,et al.  The underestimation of Young's modulus in compressive testing of cancellous bone specimens. , 1991, Journal of biomechanics.

[53]  S. Cowin,et al.  On the dependence of the elasticity and strength of cancellous bone on apparent density. , 1988, Journal of biomechanics.