The mechanical behavior of bone

Abstract Bone functions as the main load-bearing component of the musculoskeletal system, making it a classic subject for the study of biomechanics. Bone has a hierarchical structure and all levels play a role in its overall behavior and function. There are multiple factors that affect bone’s mechanical behavior, such as tissue material properties and bone geometry and structure. These factors, which undergo numerous changes with age, contribute to whole bone’s structural behavior. This chapter provides a review of classic bone biomechanics, the role of bone’s structure and composition on its mechanical properties, the mechanical behavior of whole bone, and age-related changes in bone that contribute to fracture.

[1]  W. Hayes,et al.  Bone compressive strength: the influence of density and strain rate. , 1976, Science.

[2]  Bruce Martin,et al.  Aging and strength of bone as a structural material , 2005, Calcified Tissue International.

[3]  D. Vashishth.  Hierarchy of Bone Microdamage at Multiple Length Scales. , 2007, International journal of fatigue.

[4]  W C Hayes,et al.  Computed tomography‐based finite element analysis predicts failure loads and fracture patterns for vertebral sections , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[5]  D. Vashishth,et al.  Effects of Bone Matrix Proteins on Fracture and Fragility in Osteoporosis , 2012, Current Osteoporosis Reports.

[6]  T J Sims,et al.  Mechanical Properties of Adult Vertebral Cancellous Bone: Correlation With Collagen Intermolecular Cross‐Links , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[7]  D. Vashishth,et al.  Non-enzymatic glycation alters microdamage formation in human cancellous bone. , 2010, Bone.

[8]  B. Hasegawa,et al.  Effect of bone distribution on vertebral strength: assessment with patient-specific nonlinear finite element analysis. , 1991, Radiology.

[9]  Guo X. Edward,et al.  Is Trabecular Bone Tissue Different from Cortical Bone Tissue , 1998 .

[10]  A Rohlmann,et al.  An instrumented implant for in vivo measurement of contact forces and contact moments in the shoulder joint. , 2009, Medical engineering & physics.

[11]  S. Kikuchi,et al.  In vivo intradiscal pressure measurement in healthy individuals and in patients with ongoing back problems. , 1999, Spine.

[12]  R. Martin,et al.  Age and sex-related changes in the structure and strength of the human femoral shaft. , 1977, Journal of biomechanics.

[13]  J A McGeough,et al.  Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. , 1993, The Journal of bone and joint surgery. American volume.

[14]  D R Carter,et al.  Bone creep-fatigue damage accumulation. , 1989, Journal of biomechanics.

[15]  Steven A. Goldstein,et al.  Measurement and significance of three-dimensional architecture to the mechanical integrity of trabecular bone , 2005, Calcified Tissue International.

[16]  R. Ritchie,et al.  Mechanistic fracture criteria for the failure of human cortical bone , 2003, Nature materials.

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

[18]  A. Burstein,et al.  The elastic modulus for bone. , 1974, Journal of biomechanics.

[19]  Peter Zioupos,et al.  Fatigue strength of human cortical bone: age, physical, and material heterogeneity effects. , 2008, Journal of biomedical materials research. Part A.

[20]  K. Khaw,et al.  Effects of gender, anthropometric variables, and aging on the evolution of hip strength in men and women aged over 65. , 2003, Bone.

[21]  J. M. Guralnik,et al.  Aging bone in men and women: beyond changes in bone mineral density , 2003, Osteoporosis International.

[22]  D. Vashishth,et al.  Influence of nonenzymatic glycation on biomechanical properties of cortical bone. , 2001, Bone.

[23]  S. Robinovitch,et al.  Prediction of upper extremity impact forces during falls on the outstretched hand. , 1998, Journal of biomechanics.

[24]  W. Ambrosius,et al.  Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. , 1997, Bone.

[25]  Justin W. Fernandez,et al.  Evaluation of predicted knee‐joint muscle forces during gait using an instrumented knee implant , 2008, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[26]  A J van den Bogert,et al.  An analysis of hip joint loading during walking, running, and skiing. , 1999, Medicine and science in sports and exercise.

[27]  A. Boskey,et al.  Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. , 1998, Bone.

[28]  King H. Yang,et al.  Load Sharing Within a Human Lumbar Vertebral Body Using the Finite Element Method , 2001, Spine.

[29]  C. M. Agrawal,et al.  Age-related changes in the collagen network and toughness of bone. , 2002, Bone.

[30]  E. F. Morgan,et al.  The effect of intravertebral heterogeneity in microstructure on vertebral strength and failure patterns , 2013, Osteoporosis International.

[31]  D. Vashishth.  Small animal bone biomechanics. , 2008, Bone.

[32]  Mehdi Balooch,et al.  Role of microstructure in the aging-related deterioration of the toughness of human cortical bone , 2006 .

[33]  D. Burr,et al.  Three Years of Alendronate Treatment Results in Similar Levels of Vertebral Microdamage as After One Year of Treatment , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[34]  F. Linde,et al.  Tensile and compressive properties of cancellous bone. , 1991, Journal of biomechanics.

[35]  W. C. Hayes,et al.  Tensile and compressive properties of vertebral trabecular bone , 1983 .

[36]  L. Mosekilde.  Iliac crest trabecular bone volume as predictor for vertebral compressive strength, ash density and trabecular bone volume in normal individuals. , 1988, Bone.

[37]  Michael A. Adams,et al.  Biomechanics of vertebral compression fractures and clinical application , 2011, Archives of Orthopaedic and Trauma Surgery.

[38]  L. Twomey,et al.  Age changes in the bone density and structure of the lumbar vertebral column. , 1983, Journal of anatomy.

[39]  W. C. Hayes,et al.  Role of trabecular morphology in the etiology of age-related vertebral fractures , 2005, Calcified Tissue International.

[40]  Deepak Vashishth,et al.  Morphology, localization and accumulation of in vivo microdamage in human cortical bone. , 2007, Bone.

[41]  H Weinans,et al.  Osteoporosis Changes the Amount of Vertebral Trabecular Bone at Risk of Fracture but Not the Vertebral Load Distribution , 2001, Spine.

[42]  David Mitton,et al.  Prediction of the Vertebral Strength Using a Finite Element Model Derived From Low-Dose Biplanar Imaging: Benefits of Subject-Specific Material Properties , 2012, Spine.

[43]  V. Bousson,et al.  Anatomical distribution of the degree of mineralization of bone tissue in human femoral neck: impact on biomechanical properties. , 2012, Bone.

[44]  F. Reinholt,et al.  Osteopontin--a possible anchor of osteoclasts to bone. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[45]  R. G. Paul,et al.  Mechanisms of maturation and ageing of collagen , 1998, Mechanisms of Ageing and Development.

[46]  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.

[47]  S. Majumdar,et al.  In Vivo Assessment of Architecture and Micro-Finite Element Analysis Derived Indices of Mechanical Properties of Trabecular Bone in the Radius , 2002, Osteoporosis International.

[48]  J. Currey,et al.  Changes in the impact energy absorption of bone with age. , 1979, Journal of biomechanics.

[49]  W. C. Hayes,et al.  Stress distributions within the proximal femur during gait and falls: Implications for osteoporotic fracture , 2005, Osteoporosis International.

[50]  W. Hayes,et al.  Prediction of vertebral body compressive fracture using quantitative computed tomography. , 1985, The Journal of bone and joint surgery. American volume.

[51]  D Vashishth,et al.  Crack growth resistance in cortical bone: concept of microcrack toughening. , 1997, Journal of biomechanics.

[52]  A Viidik,et al.  Correlation between the compressive strength of iliac and vertebral trabecular bone in normal individuals. , 1985, Bone.

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

[54]  Ego Seeman,et al.  The structural and biomechanical basis of the gain and loss of bone strength in women and men. , 2003, Endocrinology and metabolism clinics of North America.

[55]  Allan Bradley,et al.  Increased bone formation in osteocalcin-deficient mice , 1996, Nature.

[56]  S. Goldstein,et al.  Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[57]  Failure of trabecular bone with simulated lytic defects can be predicted non‐invasively by structural analysis , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[58]  Deepak Vashishth,et al.  Microarchitecture Influences Microdamage Accumulation in Human Vertebral Trabecular Bone , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  Eric Lespessailles,et al.  Evaluation of macrostructural bone biomechanics. , 2007, Joint, bone, spine : revue du rhumatisme.

[60]  P. Fratzl,et al.  Constant mineralization density distribution in cancellous human bone. , 2003, Bone.

[61]  S. Yerby,et al.  Measurement of strain distributions within vertebral body sections by texture correlation. , 1999, Spine.

[62]  W. Bonfield,et al.  Advances in the fracture mechanics of cortical bone. , 1987, Journal of biomechanics.

[63]  O Lindahl,et al.  Cortical bone in man. II. Variation in tensile strength with age and sex. , 1967, Acta orthopaedica Scandinavica.

[64]  L. Mosekilde,et al.  Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. , 1990, Bone.

[65]  A. Burstein,et al.  The elastic and ultimate properties of compact bone tissue. , 1975, Journal of biomechanics.

[66]  G Bergmann,et al.  Direct comparison of calculated hip joint contact forces with those measured using instrumented implants. An evaluation of a three-dimensional mathematical model of the lower limb. , 2003, Journal of biomechanics.

[67]  Ego Seeman,et al.  Bone Fragility: Failure of Periosteal Apposition to Compensate for Increased Endocortical Resorption in Postmenopausal Women , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[68]  W C Hayes,et al.  Compact bone fatigue damage--I. Residual strength and stiffness. , 1977, Journal of biomechanics.

[69]  M. He,et al.  Cortical bone atrophy and osteoporosis as a manifestation of aging. , 1963 .

[70]  Ming Ding,et al.  Age variations in the properties of human tibial trabecular bone. , 1997, The Journal of bone and joint surgery. British volume.

[71]  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.

[72]  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.

[73]  Deepak Vashishth,et al.  Heterogeneous Glycation of Cancellous Bone and Its Association with Bone Quality and Fragility , 2012, PloS one.

[74]  D. Burr,et al.  Effects of suppressed bone turnover by bisphosphonates on microdamage accumulation and biomechanical properties in clinically relevant skeletal sites in beagles. , 2001, Bone.

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

[76]  Felix Eckstein,et al.  The role of fabric in the quasi-static compressive mechanical properties of human trabecular bone from various anatomical locations , 2008, Biomechanics and modeling in mechanobiology.

[77]  T. Keaveny,et al.  Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. , 2003, Bone.

[78]  D. Burr,et al.  Suppressed Bone Turnover by Bisphosphonates Increases Microdamage Accumulation and Reduces Some Biomechanical Properties in Dog Rib , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[79]  J. Klaksvik,et al.  Biomechanical femoral neck fracture experiments--a narrative review. , 2012, Injury.

[80]  L. Mosekilde,et al.  Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. , 1987, Bone.

[81]  T. Keaveny,et al.  Quantitative computed tomography estimates of the mechanical properties of human vertebral trabecular bone , 2002, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[82]  G. H. Bell,et al.  Variations in strength of vertebrae with age and their relation to osteoporosis , 2005, Calcified Tissue Research.

[83]  Robert O. Ritchie,et al.  Invited Article , 2004 .

[84]  W. Hayes,et al.  Sex differences in age‐related remodeling of the femur and tibia , 1988, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[85]  R O Ritchie,et al.  Effect of aging on the toughness of human cortical bone: evaluation by R-curves. , 2004, Bone.

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

[87]  R. Ritchie,et al.  Measurement of the toughness of bone: a tutorial with special reference to small animal studies. , 2008, Bone.

[88]  P Rüegsegger,et al.  Mechanical analysis of bone and its microarchitecture based on in vivo voxel images. , 1998, Technology and health care : official journal of the European Society for Engineering and Medicine.

[89]  A. Boskey,et al.  Contribution of Mineral to Bone Structural Behavior and Tissue Mechanical Properties , 2010, Calcified Tissue International.

[90]  D. Vashishth.  The role of the collagen matrix in skeletal fragility , 2007, Current Osteoporosis Reports.

[91]  T. Norman,et al.  Microdamage of human cortical bone: incidence and morphology in long bones. , 1997, Bone.

[92]  E. Seeman,et al.  Pathogenesis : Structural Features During Aging , Men Lose Less Bone Than Women Because They Gain More Periosteal Bone , Not Because They Resorb Less Endosteal Bone , 2001 .

[93]  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.

[94]  Ivan Hvid,et al.  Energy absorptive properties of human trabecular bone specimens during axial compression , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

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

[96]  D. Burr,et al.  Bone Microdamage and Skeletal Fragility in Osteoporotic and Stress Fractures , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[97]  M. Bouxsein,et al.  Age-related differences in cross-sectional geometry of the forearm bones in healthy women , 1994, Calcified Tissue International.

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

[99]  F. G. Evans,et al.  Strength of biological materials , 1970 .

[100]  Y. Akiyama,et al.  Influence of bone osteocalcin levels on bone loss induced by ovariectomy in rats , 2007, Journal of Bone and Mineral Metabolism.

[101]  W C Hayes,et al.  Prediction of femoral impact forces in falls on the hip. , 1991, Journal of biomechanical engineering.

[102]  Masataka Uetani,et al.  Age-related changes in bone density, geometry and biomechanical properties of the proximal femur: CT-based 3D hip structure analysis in normal postmenopausal women. , 2011, Bone.

[103]  Vilmundur Gudnason,et al.  Increasing sex difference in bone strength in old age: The Age, Gene/Environment Susceptibility-Reykjavik study (AGES-REYKJAVIK). , 2006, Bone.

[104]  L. S. Matthews,et al.  The limitations of canine trabecular bone as a model for human: a biomechanical study. , 1989, Journal of biomechanics.

[105]  R. Martin,et al.  The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. , 1989, Journal of biomechanics.

[106]  L. Claes,et al.  New in vivo measurements of pressures in the intervertebral disc in daily life. , 1999, Spine.

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

[108]  J. Currey,et al.  The mechanical properties of bone tissue in children. , 1975, The Journal of bone and joint surgery. American volume.

[109]  W C Hayes,et al.  Subperiosteal expansion and cortical remodeling of the human femur and tibia with aging. , 1982, Science.

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

[111]  W. C. Hayes,et al.  Impact direction from a fall influences the failure load of the proximal femur as much as age-related bone loss , 1996, Calcified Tissue International.

[112]  P Brinckmann,et al.  Prediction of the compressive strength of human lumbar vertebrae. , 1989, Clinical biomechanics.

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

[114]  P. Delmas,et al.  Microcrack Frequency and Bone Remodeling in Postmenopausal Osteoporotic Women on Long‐Term Bisphosphonates: A Bone Biopsy Study , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[115]  M. Hahn,et al.  Heterogeneity of the skeleton: Comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus , 1996, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[116]  C. Ruff,et al.  Age-related changes in female femoral neck geometry: Implications for bone strength , 1993, Calcified Tissue International.

[117]  G. Beaupré,et al.  Improved method for analysis of whole bone torsion tests , 1994, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[118]  Antonius Rohlmann,et al.  An instrumented implant for vertebral body replacement that measures loads in the anterior spinal column. , 2007, Medical engineering & physics.

[119]  E. Seeman.  From Density to Structure: Growing Up and Growing Old on the Surfaces of Bone , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[120]  S. Khosla,et al.  Sex- and Age-Related Differences in Bone Microarchitecture in Men Relative to Women Assessed by High-Resolution Peripheral Quantitative Computed Tomography , 2012, Journal of osteoporosis.

[121]  G. Bergmann,et al.  Hip contact forces and gait patterns from routine activities. , 2001, Journal of biomechanics.

[122]  R. Müller,et al.  Age-related changes in trabecular bone microstructures: global and local morphometry , 2005, Osteoporosis International.

[123]  D A Smith,et al.  Relations between age, mineral density and mechanical properties of human femoral compacta. , 1976, Acta orthopaedica Scandinavica.

[124]  T. Einhorn,et al.  The Bone Organ System: Form and Function , 2001 .

[125]  T. Diab,et al.  Effects of damage morphology on cortical bone fragility. , 2005, Bone.

[126]  Joshua A. Gargac,et al.  Shear strength and toughness of trabecular bone are more sensitive to density than damage. , 2011, Journal of biomechanics.

[127]  Wilson C. Hayes,et al.  Geometric variables from DXA of the radius predict forearm fracture load in vitro , 1993, Calcified Tissue International.

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

[129]  S A Goldstein,et al.  A comparison of the fatigue behavior of human trabecular and cortical bone tissue. , 1992, Journal of biomechanics.

[130]  W. Hayes,et al.  Mechanical properties of trabecular bone from the proximal femur: a quantitative CT study. , 1990, Journal of computer assisted tomography.

[131]  P Zioupos,et al.  Changes in the stiffness, strength, and toughness of human cortical bone with age. , 1998, Bone.

[132]  H. Skinner,et al.  Prediction of femoral fracture load using automated finite element modeling. , 1997, Journal of biomechanics.

[133]  D. Vashishth,et al.  Effects of non-enzymatic glycation on cancellous bone fragility. , 2007, Bone.

[134]  J. Currey.  Physical characteristics affecting the tensile failure properties of compact bone. , 1990, Journal of biomechanics.

[135]  J. Currey.  The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. , 1988, Journal of biomechanics.

[136]  B. L. Riggs,et al.  Relationship of age to bone microstructure independent of areal bone mineral density , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[137]  N L Fazzalari,et al.  Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. , 1998, Bone.

[138]  M Martens,et al.  Aging of bone tissue: mechanical properties. , 1976, The Journal of bone and joint surgery. American volume.

[139]  Hwj Rik Huiskes,et al.  Trabecular Bone Tissue Strains in the Healthy and Osteoporotic Human Femur , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[140]  C. Whyne,et al.  Quantification of the effect of osteolytic metastases on bone strain within whole vertebrae using image registration , 2012, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[141]  Richmond W. Smith,et al.  Femoral Expansion in Aging Women: Implications for Osteoporosis and Fractures , 1964, Science.

[142]  S. Rockoff,et al.  The relative contribution of trabecular and cortical bone to the strength of human lumbar vertebrae , 2005, Calcified Tissue Research.

[143]  A. Bailey,et al.  Age-related changes in collagen: the identification of reducible lysine-carbohydrate condensation products. , 1972, Biochemical and biophysical research communications.

[144]  Ego Seeman,et al.  Pathogenesis of bone fragility in women and men , 2002, The Lancet.

[145]  C. Turner,et al.  Sexual Dimorphism in Vertebral Fragility Is More the Result of Gender Differences in Age‐Related Bone Gain Than Bone Loss , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[146]  M. Bouxsein,et al.  Biomechanics of Age-Related Fractures , 2001 .

[147]  Michael R Hardisty,et al.  Whole bone strain quantification by image registration: a validation study. , 2009, Journal of biomechanical engineering.

[148]  D. Cody,et al.  Decrease in canine proximal femoral ultimate strength and stiffness due to fatigue damage. , 1997, Journal of biomechanics.

[149]  J G Clement,et al.  Age‐related changes in cortical porosity of the midshaft of the human femur , 1997, Journal of anatomy.

[150]  Ann L Oberg,et al.  Effects of Sex and Age on Bone Microstructure at the Ultradistal Radius: A Population‐Based Noninvasive In Vivo Assessment , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[151]  S. Goldstein,et al.  Femoral strength is better predicted by finite element models than QCT and DXA. , 1999, Journal of biomechanics.

[152]  D. Cody,et al.  Correlations Between Vertebral Regional Bone Mineral Density (rBMD) and Whole Bone Fracture Load , 1991, Spine.

[153]  G. Niebur,et al.  Biomechanics of trabecular bone. , 2001, Annual review of biomedical engineering.

[154]  T M Keaveny,et al.  Biomechanical consequences of an isolated overload on the human vertebral body , 2000, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[155]  Sharmila Majumdar,et al.  Age- and Gender-Related Differences in the Geometric Properties and Biomechanical Significance of Intracortical Porosity in the Distal Radius and Tibia , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[156]  Sundeep Khosla,et al.  Population‐Based Study of Age and Sex Differences in Bone Volumetric Density, Size, Geometry, and Structure at Different Skeletal Sites , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[157]  M. Dalstra,et al.  Age variations in the properties of human tibial trabecular bone and cartilage , 1997, Acta orthopaedica Scandinavica. Supplementum.

[158]  T M Keaveny,et al.  Nonlinear behavior of trabecular bone at small strains. , 2001, Journal of biomechanical engineering.

[159]  Craig R. Slyfield,et al.  Quantitative Computed Tomography-Based Predictions of Vertebral Strength in Anterior Bending , 2007, Spine.

[160]  B. van Rietbergen,et al.  Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT , 2009, Osteoporosis International.

[161]  Luigi Ferrucci,et al.  Longitudinal Changes in BMD and Bone Geometry in a Population‐Based Study , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[162]  L. Mosekilde,et al.  Sex differences in age-related loss of vertebral trabecular bone mass and structure--biomechanical consequences. , 1989, Bone.

[163]  N Yoganandan,et al.  Functional biomechanics of the thoracolumbar vertebral cortex. , 1988, Clinical biomechanics.

[164]  Jacqueline A. Cutroni,et al.  Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture , 2005, Nature materials.

[165]  D. Burr,et al.  Stiffness of compact bone: effects of porosity and density. , 1988, Journal of biomechanics.

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

[167]  H. Spjut,et al.  Clomiphene protects against osteoporosis in the mature ovariectomized rat , 2006, Calcified Tissue International.

[168]  F. G. Evans,et al.  Relations of the compressive properties of human cortical bone to histological structure and calcification. , 1974, Journal of biomechanics.

[169]  Paul E Barbone,et al.  Digital Volume Correlation for Study of the Mechanics of Whole Bones. , 2012, Procedia IUTAM.

[170]  S. Majumdar,et al.  High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. , 1998, Bone.

[171]  L. Mosekilde,et al.  Normal vertebral body size and compressive strength: relations to age and to vertebral and iliac trabecular bone compressive strength. , 1986, Bone.

[172]  D. Vashishth,et al.  Biochemical Characterization of Major Bone-Matrix Proteins Using Nanoscale-Size Bone Samples and Proteomics Methodology* , 2011, Molecular & Cellular Proteomics.

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

[174]  M H Bartley,et al.  Skeletal Changes in Aging and Disease , 1966, Clinical orthopaedics and related research.

[175]  P Zioupos,et al.  The accumulation of fatigue microdamage in human cortical bone of two different ages in vitro. , 1996, Clinical biomechanics.

[176]  W C Hayes,et al.  Age-related differences in post-yield damage in human cortical bone. Experiment and model. , 1996, Journal of biomechanics.

[177]  S. Garn,et al.  Continuing bone growth throughout life: a general phenomenon. , 1967, American journal of physical anthropology.

[178]  M. Bouxsein,et al.  Predicting the failure load of the distal radius , 2003, Osteoporosis International.

[179]  M. Schaffler,et al.  Examination of compact bone microdamage using back-scattered electron microscopy. , 1994, Bone.

[180]  M. J. Drews,et al.  The effect of boundary conditions on experimentally measured trabecular strain in the thoracic spine. , 1998, Journal of biomechanics.

[181]  G. Beaupré,et al.  The influence of bone volume fraction and ash fraction on bone strength and modulus. , 2001, Bone.

[182]  A. Mann,et al.  Effect of osteocalcin deficiency on the nanomechanics and chemistry of mouse bones. , 2009, Journal of the mechanical behavior of biomedical materials.

[183]  A. Nachemson,et al.  IN VIVO MEASUREMENTS OF INTRADISCAL PRESSURE. DISCOMETRY, A METHOD FOR THE DETERMINATION OF PRESSURE IN THE LOWER LUMBAR DISCS. , 1964, The Journal of bone and joint surgery. American volume.

[184]  Antonius Rohlmann,et al.  Material properties of femoral cancellous bone in axial loading , 1980, Archives of orthopaedic and traumatic surgery. Archiv fur orthopadische und Unfall-Chirurgie.

[185]  A. M. Parfitt,et al.  Age-related structural changes in trabecular and cortical bone: Cellular mechanisms and biomechanical consequences , 2006, Calcified Tissue International.

[186]  D Vashishth,et al.  Effect of groove on bone fracture toughness. , 1991, Journal of biomechanics.

[187]  Marco Viceconti,et al.  In vitro replication of spontaneous fractures of the proximal human femur. , 2007, Journal of biomechanics.

[188]  M. Davie,et al.  Mechanical properties of bone from iliac crest and relationship to L5 vertebral bone. , 1990, Bone.

[189]  W. Hayes,et al.  The effect of impact direction on the structural capacity of the proximal femur during falls , 1996, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[190]  W. Hayes,et al.  Cross-sectional geometry of Pecos Pueblo femora and tibiae--a biomechanical investigation: I. Method and general patterns of variation. , 1983, American journal of physical anthropology.

[191]  C Milgrom,et al.  Aging and matrix microdamage accumulation in human compact bone. , 1995, Bone.

[192]  D. Burr,et al.  Microdamage and bone strength , 2003, Osteoporosis International.

[193]  J. Currey,et al.  The mechanical consequences of variation in the mineral content of bone. , 1969, Journal of biomechanics.

[194]  E. Radin,et al.  Mechanical and morphological effects of strain rate on fatigue of compact bone. , 1989, Bone.

[195]  W C Hayes,et al.  Load Sharing Between the Shell and Centrum in the Lumbar Vertebral Body , 1997, Spine.

[196]  P. Fratzl,et al.  Bone mineralization density distribution in health and disease. , 2008, Bone.

[197]  D Vashishth,et al.  In vivo diffuse damage in human vertebral trabecular bone. , 2000, Bone.

[198]  G. Holzer,et al.  Hip Fractures and the Contribution of Cortical Versus Trabecular Bone to Femoral Neck Strength , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[199]  M. C. H. Meulen,et al.  Whole Bone Mechanics and Bone Quality , 2011, Clinical orthopaedics and related research.

[200]  M. Grynpas,et al.  Age and disease-related changes in the mineral of bone , 2005, Calcified Tissue International.

[201]  Deepak Vashishth,et al.  Age-related change in the damage morphology of human cortical bone and its role in bone fragility. , 2006, Bone.

[202]  W. Hayes,et al.  Fracture prediction for the proximal femur using finite element models: Part I--Linear analysis. , 1991, Journal of biomechanical engineering.

[203]  Heather M. Macdonald,et al.  Age‐related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: A population‐based HR‐pQCT study , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[204]  D. Vashishth,et al.  Effects of intracortical porosity on fracture toughness in aging human bone: a microCT-based cohesive finite element study. , 2007, Journal of biomechanical engineering.

[205]  T. Keaveny,et al.  Cortical and Trabecular Load Sharing in the Human Vertebral Body , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[206]  J. Compston,et al.  Connectivity of cancellous bone: assessment and mechanical implications. , 1994, Bone.

[207]  J. Lian,et al.  A role for osteocalcin in osteoclast differentiation , 1991, Journal of cellular biochemistry.

[208]  T. Keaveny,et al.  Dependence of trabecular damage on mechanical strain , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[209]  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.

[210]  Dennis M Black,et al.  Femoral Bone Strength and Its Relation to Cortical and Trabecular Changes After Treatment With PTH, Alendronate, and Their Combination as Assessed by Finite Element Analysis of Quantitative CT Scans , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[211]  D P Fyhrie,et al.  In vivo trabecular microcracks in human vertebral bone. , 1996, Bone.

[212]  W. C. Hayes,et al.  Multiaxial Structure-Property Relations in Trabecular Bone , 1990 .