Role of Trabecular Microarchitecture and Its Heterogeneity Parameters in the Mechanical Behavior of Ex Vivo Human L3 Vertebrae

Low bone mineral density (BMD) is a strong risk factor for vertebral fracture risk in osteoporosis. However, many fractures occur in people with moderately decreased or normal BMD. Our aim was to assess the contributions of trabecular microarchitecture and its heterogeneity to the mechanical behavior of human lumbar vertebrae. Twenty‐one human L3 vertebrae were analyzed for BMD by dual‐energy X‐ray absorptiometry (DXA) and microarchitecture by high‐resolution peripheral quantitative computed tomography (HR‐pQCT) and then tested in axial compression. Microarchitecture heterogeneity was assessed using two vertically oriented virtual biopsies—one anterior (Ant) and one posterior (Post)—each divided into three zones (superior, middle, and inferior) and using the whole vertebral trabecular volume for the intraindividual distribution of trabecular separation (Tb.Sp*SD). Heterogeneity parameters were defined as (1) ratios of anterior to posterior microarchitectural parameters and (2) the coefficient of variation of microarchitectural parameters from the superior, middle, and inferior zones. BMD alone explained up to 44% of the variability in vertebral mechanical behavior, bone volume fraction (BV/TV) up to 53%, and trabecular architecture up to 66%. Importantly, bone mass (BMD or BV/TV) in combination with microarchitecture and its heterogeneity improved the prediction of vertebral mechanical behavior, together explaining up to 86% of the variability in vertebral failure load. In conclusion, our data indicate that regional variation of microarchitecture assessment expressed by heterogeneity parameters may enhance prediction of vertebral fracture risk. © 2010 American Society for Bone and Mineral Research.

[1]  Harry K Genant,et al.  Bone mass and architecture determination: state of the art. , 2008, Best practice & research. Clinical endocrinology & metabolism.

[2]  S. Majumdar,et al.  Impact of spatial resolution on the prediction of trabecular architecture parameters. , 1998, Bone.

[3]  N. Sharkey,et al.  Mechanical effects of postmortem changes, preservation, and allograft bone treatments , 2001 .

[4]  H Follet,et al.  The degree of mineralization is a determinant of bone strength: a study on human calcanei. , 2004, Bone.

[5]  M. Bouxsein,et al.  Structural Determinants of Vertebral Fracture Risk , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[6]  Sharmila Majumdar,et al.  A Local Adaptive Threshold Strategy for High Resolution Peripheral Quantitative Computed Tomography of Trabecular Bone , 2007, Annals of Biomedical Engineering.

[7]  P Rüegsegger,et al.  Resolution dependency of microstructural properties of cancellous bone based on three-dimensional mu-tomography. , 1996, Technology and health care : official journal of the European Society for Engineering and Medicine.

[8]  P. Rüegsegger,et al.  The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. , 1999, Bone.

[9]  S. Goldstein,et al.  Variations in Three‐Dimensional Cancellous Bone Architecture of the Proximal Femur in Female Hip Fractures and in Controls , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[10]  Tony M Keaveny,et al.  Role of Trabecular Microarchitecture in Whole‐Vertebral Body Biomechanical Behavior , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[11]  S. Majumdar,et al.  Title Assessment of trabecular bone structure using MDCT : comparison of 64-and 320-slice CT using HR-pQCT as the reference standard Permalink , 2010 .

[12]  P. Rüegsegger,et al.  Ridge number density: a new parameter for in vivo bone structure analysis. , 1997, Bone.

[13]  P. Delmas,et al.  Bone quality--the material and structural basis of bone strength and fragility. , 2006, The New England journal of medicine.

[14]  J. Buckley,et al.  Comparison of quantitative computed tomography-based measures in predicting vertebral compressive strength. , 2007, Bone.

[15]  P. M. Donnell,et al.  Vertebral Osteoporosis and Trabecular Bone Quality , 2007, Annals of Biomedical Engineering.

[16]  Laurence Vico,et al.  High‐Resolution pQCT Analysis at the Distal Radius and Tibia Discriminates Patients With Recent Wrist and Femoral Neck Fractures , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[17]  Olivier Guyen,et al.  Contribution of Trabecular and Cortical Components to Biomechanical Behavior of Human Vertebrae: An Ex Vivo Study , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[18]  L. Mosekilde Age-related changes in vertebral trabecular bone architecture--assessed by a new method. , 1988, Bone.

[19]  M. Bouxsein,et al.  In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. , 2005, The Journal of clinical endocrinology and metabolism.

[20]  Christian Rey,et al.  Mineral maturity and crystallinity index are distinct characteristics of bone mineral , 2010, Journal of Bone and Mineral Metabolism.

[21]  Paul Sajda,et al.  Accuracy of high‐resolution in vivo micro magnetic resonance imaging for measurements of microstructural and mechanical properties of human distal tibial bone , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  J S Thomsen,et al.  Lumbar vertebral body compressive strength evaluated by dual-energy X-ray absorptiometry, quantitative computed tomography, and ashing. , 1999, Bone.

[23]  R. Recker,et al.  Use of FTIR Spectroscopic Imaging to Identify Parameters Associated With Fragility Fracture , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[24]  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.

[25]  J S Thomsen,et al.  Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. , 2002, Bone.

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

[27]  F Eckstein,et al.  The osteoporotic vertebral structure is well adapted to the loads of daily life, but not to infrequent "error" loads. , 2004, Bone.

[28]  M. Grynpas,et al.  Inhomogeneity of human vertebral cancellous bone: systematic density and structure patterns inside the vertebral body. , 2001, Bone.

[29]  Liang Yu,et al.  Structure Analysis of the Was , 2002 .

[30]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[31]  X. Guo,et al.  High-Resolution Peripheral Quantitative Computed Tomography Can Assess Microstructural and Mechanical Properties of Human Distal Tibial Bone , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[32]  Patrik Rogalla,et al.  Trabecular Bone Structure Analysis in the Osteoporotic Spine Using a Clinical In Vivo Setup for 64‐Slice MDCT Imaging: Comparison to μCT Imaging and μFE Modeling , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[33]  M. Grynpas,et al.  Patient-specific microarchitecture of vertebral cancellous bone: a peripheral quantitative computed tomographic and histological study. , 2002, Bone.

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

[35]  P. Delmas,et al.  Alterations of Cortical and Trabecular Architecture Are Associated With Fractures in Postmenopausal Women, Partially Independent of Decreased BMD Measured by DXA: The OFELY Study , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  L. Qin,et al.  Regional variations in microstructural properties of vertebral trabeculae with aging , 2004, Journal of Bone and Mineral Metabolism.

[37]  S. Majumdar,et al.  New Model-Independent Measures of Trabecular Bone Structure Applied to In Vivo High-Resolution MR Images , 2002, Osteoporosis International.

[38]  C. Turner,et al.  The Biomechanical Basis of Vertebral Body Fragility in Men and Women , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[39]  Ling Qin,et al.  Regional Variations in Microstructural Properties of Vertebral Trabeculae With Structural Groups , 2006, Spine.

[40]  J. Kellgren,et al.  Radiological Assessment of Osteo-Arthrosis , 1957, Annals of the rheumatic diseases.

[41]  S J Ferguson,et al.  Regional variation in vertebral bone morphology and its contribution to vertebral fracture strength. , 2007, Bone.

[42]  D. Mitton,et al.  High-Resolution Computed Tomography for Architectural Characterization of Human Lumbar Cancellous Bone: Relationships with Histomorphometry and Biomechanics , 1999, Osteoporosis International.