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Review Article

Multiscale Contribution of Bone Tissue Material Property Heterogeneity to Trabecular Bone Mechanical Behavior

[+] Author and Article Information
Ashley A. Lloyd

Department of Materials Science
and Engineering,
Cornell University,
B60 Bard Hall,
Ithaca, NY 14853
e-mail: aal99@cornell.edu

Zhen Xiang Wang

Department of Materials Science
and Engineering,
Cornell University,
B60 Bard Hall,
Ithaca, NY 14853
e-mail: zw55@cornell.edu

Eve Donnelly

Assistant Professor
Department of Materials Science
and Engineering,
Cornell University,
227 Bard Hall,
Ithaca, NY 14853
Hospital for Special Surgery,
535 E. 70th Street,
New York, NY 10021
e-mail: eve.donnelly@cornell.edu

1Corresponding author.

Manuscript received June 11, 2014; final manuscript received November 5, 2014; accepted manuscript posted November 12, 2014; published online December 10, 2014. Assoc. Editor: Blaine Christiansen.

J Biomech Eng 137(1), 010801 (Jan 01, 2015) (8 pages) Paper No: BIO-14-1256; doi: 10.1115/1.4029046 History: Received June 11, 2014; Revised November 05, 2014; Accepted November 12, 2014; Online December 10, 2014

Heterogeneity of material properties is an important potential contributor to bone fracture resistance because of its putative contribution to toughness, but establishing the contribution of heterogeneity to fracture risk is still in an incipient stage. Experimental studies have demonstrated changes in distributions of compositional and nanomechanical properties with fragility fracture history, disease, and pharmacologic treatment. Computational studies have demonstrated that models with heterogeneous material properties predict apparent stiffness moderately better than homogeneous models and show greater energy dissipation. Collectively, these results suggest that microscale material heterogeneity affects not only microscale mechanics but also structural performance at larger length scales.

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References

Cefalu, C. A., 2004, “Is Bone Mineral Density Predictive of Fracture Risk Reduction?,” Curr. Med. Res. Opin., 20(3), pp. 341–349. [CrossRef] [PubMed]
Moro, M., Hecker, A. T., Bouxsein, M. L., and Myers, E. R., 1995, “Failure Load of Thoracic Vertebrae Correlates With Lumbar Bone Mineral Density Measured by DXA,” Calcif. Tissue Int., 56(3), pp. 206–209. [CrossRef] [PubMed]
Oden, Z. M., Selvitelli, D. M., Hayes, W. C., and Myers, E. R., 1998, “The Effect of Trabecular Structure on DXA-Based Predictions of Bovine Bone Failure,” Calcif. Tissue Int., 63(1), pp. 67–73. [CrossRef] [PubMed]
Bjarnason, K., Hassager, C., Svendsen, O. L., Stang, H., and Christiansen, C., 1996, “Anteroposterior and Lateral Spinal Dxa for the Assessment of Vertebral Body Strength: Comparison With Hip and Forearm Measurement,” Osteoporos. Int., 6(1), pp. 37–42. [CrossRef] [PubMed]
Cheng, X. G., Nicholson, P. H., Boonen, S., Lowet, G., Brys, P., Aerssens, J., Van Der Perre, G., and Dequeker, J., 1997, “Prediction of Vertebral Strength In Vitro by Spinal Bone Densitometry and Calcaneal Ultrasound,” J. Bone Miner. Res., 12(10), pp. 1721–1728. [CrossRef] [PubMed]
Linde, F., Gothgen, C. B., Hvid, I., and Pongsoipetch, B., 1988, “Mechanical Properties of Trabecular Bone by a Non-Destructive Compression Testing Approach,” Eng. Med., 17(1), pp. 23–29. [CrossRef] [PubMed]
Lochmuller, E. M., Eckstein, F., Kaiser, D., Zeller, J. B., Landgraf, J., Putz, R., and Steldinger, R., 1998, “Prediction of Vertebral Failure Loads From Spinal and Femoral Dual-Energy X-Ray Absorptiometry, and Calcaneal Ultrasound: An In Situ Analysis With Intact Soft Tissues,” Bone, 23(5), pp. 417–424. [CrossRef] [PubMed]
Donnelly, E., Lane, J. M., and Boskey, A. L., 2014, “Research Perspectives: The 2013 AAOS/ORS Research Symposium on Bone Quality and Fracture Prevention,” J. Orthop. Res., 32(7), pp. 855–864. [CrossRef] [PubMed]
Gourion-Arsiquaud, S., Faibish, D., Myers, E., Spevak, L., Compston, J., Hodsman, A., Shane, E., Recker, R. R., Boskey, E. R., and Boskey, A. L., 2009, “Use of FTIR Spectroscopic Imaging to Identify Parameters Associated With Fragility Fracture,” J. Bone Miner. Res., 24(9), pp. 1565–1571. [CrossRef] [PubMed]
Tai, K., Dao, M., Suresh, S., Palazoglu, A., and Ortiz, C., 2007, “Nanoscale Heterogeneity Promotes Energy Dissipation in Bone,” Nat. Mater., 6(6), pp. 454–462. [CrossRef] [PubMed]
Ritchie, R. O., 2011, “The Conflicts Between Strength and Toughness,” Nat. Mater., 10(11), pp. 817–822. [CrossRef] [PubMed]
Gourion-Arsiquaud, S., Lukashova, L., Power, J., Loveridge, N., Reeve, J., and Boskey, A. L., 2013, “Fourier Transform Infrared Imaging of Femoral Neck Bone: Reduced Heterogeneity of Mineral-to-Matrix and Carbonate-to-Phosphate and More Variable Crystallinity in Treatment-Naive Fracture Cases Compared With Fracture-Free Controls,” J. Bone Miner. Res., 28(1), pp. 150–161. [CrossRef] [PubMed]
Boskey, A. L., Dicarlo, E., Paschalis, E., West, P., and Mendelsohn, R., 2005, “Comparison of Mineral Quality and Quantity in Iliac Crest Biopsies From High- and Low-Turnover Osteoporosis: An FT-IR Microspectroscopic Investigation,” Osteoporos. Int., 16(12), pp. 2031–2038. [CrossRef] [PubMed]
Roschger, P., Rinnerthaler, S., Yates, J., Rodan, G. A., Fratzl, P., and Klaushofer, K., 2001, “Alendronate Increases Degree and Uniformity of Mineralization in Cancellous Bone and Decreases the Porosity in Cortical Bone of Osteoporotic Women,” Bone, 29(2), pp. 185–191. [CrossRef] [PubMed]
Roschger, P., Lombardi, A., Misof, B. M., Maier, G., Fratzl-Zelman, N., Fratzl, P., and Klaushofer, K., 2009, “Mineralization Density Distribution of Postmenopausal Osteoporotic Bone is Restored to Normal After Long-Term Alendronate Treatment: QBEI and SSAXS Data From the Fracture Intervention Trial Long-Term Extension (Flex),” J. Bone Miner. Res., 25(1), pp. 48–55. [CrossRef]
Van Der Linden, J. C., Birkenhager-Frenkel, D. H., Verhaar, J. A., and Weinans, H., 2001, “Trabecular Bone's Mechanical Properties Are Affected by Its Non-Uniform Mineral Distribution,” J. Biomech., 34(12), pp. 1573–1580. [CrossRef] [PubMed]
Jaasma, M. J., Bayraktar, H. H., Niebur, G. L., and Keaveny, T. M., 2002, “Biomechanical Effects of Intraspecimen Variations in Tissue Modulus for Trabecular Bone,” J. Biomech., 35(2), pp. 237–246. [CrossRef] [PubMed]
Bourne, B. C., and Van Der Meulen, M. C., 2004, “Finite Element Models Predict Cancellous Apparent Modulus When Tissue Modulus Is Scaled From Specimen CT-Attenuation,” J. Biomech., 37(5), pp. 613–621. [CrossRef] [PubMed]
Tai, K., Qi, H. J., and Ortiz, C., 2005, “Effect of Mineral Content on the Nanoindentation Properties and Nanoscale Deformation Mechanisms of Bovine Tibial Cortical Bone,” J. Mater. Sci. Mater. Med., 16(10), pp. 947–959. [CrossRef] [PubMed]
Fratzl, P., Gupta, H. S., Fischer, F. D., and Kolednik, O., 2007, “Hindered Crack Propagation in Materials With Periodically Varying Young's Modulus–Lessons From Biological Materials,” Adv. Mater., 19(18), pp. 2657–2661. [CrossRef]
Nalla, R. K., Stolken, J. S., Kinney, J. H., and Ritchie, R. O., 2005, “Fracture in Human Cortical Bone: Local Fracture Criteria and Toughening Mechanisms,” J. Biomech., 38(7), pp. 1517–1525. [CrossRef] [PubMed]
Augat, P., and Schorlemmer, S., 2006, “The Role of Cortical Bone and Its Microstructure in Bone Strength,” Age Ageing,35(Suppl 2), pp. ii27–ii31. [CrossRef]
Rho, J. Y., Kuhn-Spearing, L., and Zioupos, P., 1998, “Mechanical Properties and the Hierarchical Structure of Bone,” Med. Eng. Phys., 20(2), pp. 92–102. [CrossRef] [PubMed]
Dempster, D. W., 2000, “The Contribution of Trabecular Architecture to Cancellous Bone Quality,” J. Bone Miner. Res., 15(1), pp. 20–23. [CrossRef] [PubMed]
Keaveny, T. M., Morgan, E. F., Niebur, G. L., and Yeh, O. C., 2001, “Biomechanics of Trabecular Bone,” Annu. Rev. Biomed. Eng., 3(1), pp. 307–333. [CrossRef] [PubMed]
Zysset, P. K., 2003, “A Review of Morphology-Elasticity Relationships in Human Trabecular Bone: Theories and Experiments,” J. Biomech., 36(10), pp. 1469–1485. [CrossRef] [PubMed]
Rho, J. Y., Tsui, T. Y., and Pharr, G. M., 1997, “Elastic Properties of Human Cortical and Trabecular Lamellar Bone Measured by Nanoindentation,” Biomaterials, 18(20), pp. 1325–1330. [CrossRef] [PubMed]
Rho, J. Y., Zioupos, P., Currey, J. D., and Pharr, G. M., 1999, “Variations in the Individual Thick Lamellar Properties Within Osteons by Nanoindentation,” Bone, 25(3), pp. 295–300. [CrossRef] [PubMed]
Donnelly, E., Williams, R. W., Downs, S. A., Dickinson, M. E., Baker, S. P., and van der Meulen, M. C. H., 2006, “Quasistatic and Dynamic Nanomechanical Properties of Cancellous Bone Tissue Relate to Collagen Content and Organization,” J. Mater. Res., 21(8), pp. 2106–2117. [CrossRef]
Zysset, P. K., Guo, X. E., Hoffler, C. E., Moore, K. E., and Goldstein, S. A., 1999, “Elastic Modulus and Hardness of Cortical and Trabecular Bone Lamellae Measured by Nanoindentation of the Human Femur,” J. Biomech., 32, pp. 1005–1012. [CrossRef] [PubMed]
Jepsen, K. J., and Schlecht, S. H., 2014, “Biomechanical Mechanisms: Resolving the Apparent Conundrum of Why Individuals With Type II Diabetes Show Increased Fracture Incidence Despite Having Normal Bmd,” J. Bone Miner. Res., 29(4), pp. 784–786. [CrossRef] [PubMed]
Hansma, P., Turner, P., Drake, B., Yurtsev, E., Proctor, A., Mathews, P., Lulejian, J., Randall, C., Adams, J., Jungmann, R., Garza-De-Leon, F., Fantner, G., Mkrtchyan, H., Pontin, M., Weaver, A., Brown, M. B., Sahar, N., Rossello, R., and Kohn, D., 2008, “The Bone Diagnostic Instrument II: Indentation Distance Increase,” Rev. Sci. Instrum., 79(6), p. 064303. [CrossRef] [PubMed]
Choi, K., Kuhn, J. L., Ciarelli, M. J., and Goldstein, S. A., 1990, “The Elastic Moduli of Human Subchondral, Trabecular, and Cortical Bone Tissue and the Size-Dependency of Cortical Bone Modulus,” J. Biomech., 23(11), pp. 1103–1113. [CrossRef] [PubMed]
Kuhn, L. T., Grynpas, M. D., Rey, C. C., Wu, Y., Ackerman, J. L., and Glimcher, M. J., 2008, “A Comparison of the Physical and Chemical Differences Between Cancellous and Cortical Bovine Bone Mineral at Two Ages,” Calcif. Tissue Int., 83(2), pp. 146–154. [CrossRef] [PubMed]
Tseng, K. F., Bonadio, J. F., Stewart, T. A., Baker, A. R., and Goldstein, S. A., 1996, “Local Expression of Human Growth Hormone in Bone Results in Impaired Mechanical Integrity in the Skeletal Tissue of Transgenic Mice,” J. Orthop. Res., 14(4), pp. 598–604. [CrossRef] [PubMed]
Morgan, E. F., and Keaveny, T. M., 2001, “Dependence of Yield Strain of Human Trabecular Bone on Anatomic Site,” J. Biomech., 34(5), pp. 569–577. [CrossRef] [PubMed]
Boskey, A., and Mendelsohn, R., 2005, “Infrared Analysis of Bone in Health and Disease,” J. Biomed. Opt., 10(3), p. 031102. [CrossRef] [PubMed]
Carden, A., and Morris, M. D., 2000, “Application of Vibrational Spectroscopy to the Study of Mineralized Tissues (Review),” J. Biomed. Opt., 5(3), pp. 259–268. [CrossRef] [PubMed]
Judex, S., Boyd, S., Qin, Y. X., Miller, L., Muller, R., and Rubin, C., 2003, “Combining High-Resolution Micro-Computed Tomography With Material Composition to Define the Quality of Bone Tissue,” Curr. Osteoporos Rep., 1(1), pp. 11–19. [CrossRef] [PubMed]
Donnelly, E., 2011, “Methods for Assessing Bone Quality: A Review,” Clin. Orthop. Relat. Res., 469(8), pp. 2128–2138. [CrossRef] [PubMed]
Ciarelli, T. E., Tjhia, C., Rao, D. S., Qiu, S., Parfitt, A. M., and Fyhrie, D. P., 2009, “Trabecular Packet-Level Lamellar Density Patterns Differ by Fracture Status and Bone Formation Rate in White Females,” Bone, 45(5), pp. 903–908. [CrossRef] [PubMed]
Wang, Z. X., and Donnelly, E., “Altered Heterogeneity of Tissue Mineral and Collagen Properties in Perimenopausal Women With Fragility Fractures,” (in review).
Bousson, V., Bergot, C., Wu, Y., Jolivet, E., Zhou, L. Q., and Laredo, J. D., 2011, “Greater Tissue Mineralization Heterogeneity in Femoral Neck Cortex From Hip-Fractured Females Than Controls. A Microradiographic Study,” Bone, 48(6), pp. 1252–1259. [CrossRef] [PubMed]
Tamminen, I. S., Misof, B. M., Roschger, P., Mayranpaa, M. K., Turunen, M. J., Isaksson, H., Kroger, H., Makitie, O., and Klaushofer, K., 2014, “Increased Heterogeneity of Bone Matrix Mineralization in Pediatric Patients Prone to Fractures: A Biopsy Study,” J. Bone Miner. Res., 29(5), pp. 1110–1117. [CrossRef] [PubMed]
Fratzl-Zelman, N., Roschger, P., Misof, B. M., Pfeffer, S., Glorieux, F. H., Klaushofer, K., and Rauch, F., 2009, “Normative Data on Mineralization Density Distribution in Iliac Bone Biopsies of Children, Adolescents and Young Adults,” Bone, 44(6), pp. 1043–1048. [CrossRef] [PubMed]
Paschalis, E. P., Betts, F., Dicarlo, E., Mendelsohn, R., and Boskey, A. L., 1997, “FTIR Microspectroscopic Analysis of Human Iliac Crest Biopsies From Untreated Osteoporotic Bone,” Calcif. Tissue Int., 61(6), pp. 487–492. [CrossRef] [PubMed]
Boskey, A. L., and Mendelsohn, R., 2005, “Infrared Spectroscopic Characterization of Mineralized Tissues,” Vib. Spectrosc., 38(1–2), pp. 107–114. [CrossRef] [PubMed]
Tjhia, C. K., Odvina, C. V., Rao, D. S., Stover, S. M., Wang, X., and Fyhrie, D. P., 2011, “Mechanical Property and Tissue Mineral Density Differences Among Severely Suppressed Bone Turnover (Ssbt) Patients, Osteoporotic Patients, and Normal Subjects,” Bone, 49(6), pp. 1279–1289. [CrossRef] [PubMed]
Busse, B., Hahn, M., Soltau, M., Zustin, J., Puschel, K., Duda, G. N., and Amling, M., 2009, “Increased Calcium Content and Inhomogeneity of Mineralization Render Bone Toughness in Osteoporosis: Mineralization, Morphology and Biomechanics of Human Single Trabeculae,” Bone, 45(6), pp. 1034–1043. [CrossRef] [PubMed]
Nyman, J. S., Roy, A., Shen, X., Acuna, R. L., Tyler, J. H., and Wang, X., 2006, “The Influence of Water Removal on the Strength and Toughness of Cortical Bone,” J. Biomech., 39(5), pp. 931–938. [CrossRef] [PubMed]
Sedlin, E. D., and Hirsch, C., 1966, “Factors Affecting the Determination of the Physical Properties of Femoral Cortical Bone,” Acta. Orthop. Scand., 37(1), pp. 29–48. [CrossRef] [PubMed]
Gourion-Arsiquaud, S., Allen, M. R., Burr, D. B., Vashishth, D., Tang, S. Y., and Boskey, A. L., 2010, “Bisphosphonate Treatment Modifies Canine Bone Mineral and Matrix Properties and Their Heterogeneity,” Bone, 46(3), pp. 666–672. [CrossRef] [PubMed]
Donnelly, E., Meredith, D. S., Nguyen, J. T., Gladnick, B. P., Rebolledo, B. J., Shaffer, A. D., Lorich, D. G., Lane, J. M., and Boskey, A. L., 2012, “Reduced Cortical Bone Compositional Heterogeneity With Bisphosphonate Treatment in Postmenopausal Women With Intertrochanteric and Subtrochanteric Fractures,” J. Bone Miner. Res., 27(3), pp. 672–678. [CrossRef] [PubMed]
Launey, M. E., Buehler, M. J., and Ritchie, R. O., 2010, “On the Mechanistic Origins of Toughness in Bone,” Annu. Rev. Mater. Res., 40(1), pp. 25–53. [CrossRef]
Wang, X., and Puram, S., 2004, “The Toughness of Cortical Bone and Its Relationship With Age,” Ann. Biomed. Eng., 32(1), pp. 123–135. [CrossRef] [PubMed]
Ciarelli, T. E., Fyhrie, D. P., and Parfitt, A. M., 2003, “Effects of Vertebral Bone Fragility and Bone Formation Rate on the Mineralization Levels of Cancellous Bone From White Females,” Bone, 32(3), pp. 311–315. [CrossRef] [PubMed]
Renders, G. A., Mulder, L., Van Ruijven, L. J., and Van Eijden, T. M., 2006, “Degree and Distribution of Mineralization in the Human Mandibular Condyle,” Calcif. Tissue Int., 79(3), pp. 190–196. [CrossRef] [PubMed]
Mulder, L., Koolstra, J. H., De Jonge, H. W., and Van Eijden, T. M., 2006, “Architecture and Mineralization of Developing Cortical and Trabecular Bone of the Mandible,” Anat. Embryol. (Berl), 211(1), pp. 71–78. [CrossRef] [PubMed]
Smith, L. J., Schirer, J. P., and Fazzalari, N. L., 2010, “The Role of Mineral Content in Determining the Micromechanical Properties of Discrete Trabecular Bone Remodeling Packets,” J. Biomech., 43(16), pp. 3144–3149. [CrossRef] [PubMed]
Paschalis, E. P., Betts, F., Dicarlo, E., Mendelsohn, R., and Boskey, A. L., 1997, “FTIR Microspectroscopic Analysis of Normal Human Cortical and Trabecular Bone,” Calcif. Tissue Int., 61(6), pp. 480–486. [CrossRef] [PubMed]
Fyhrie, D. P., and Schaffler, M. B., 1994, “Failure Mechanisms in Human Vertebral Cancellous Bone,” Bone, 15(1), pp. 105–109. [CrossRef] [PubMed]
Mulder, L., Koolstra, J. H., Den Toonder, J. M., and Van Eijden, T. M., 2007, “Intratrabecular Distribution of Tissue Stiffness and Mineralization in Developing Trabecular Bone,” Bone, 41(2), pp. 256–265. [CrossRef] [PubMed]
Skedros, J. G., Knight, A. N., Farnsworth, R. W., and Bloebaum, R. D., 2012, “Do Regional Modifications in Tissue Mineral Content and Microscopic Mineralization Heterogeneity Adapt Trabecular Bone Tracts for Habitual Bending? Analysis in the Context of Trabecular Architecture of Deer Calcanei,” J. Anat., 220(3), pp. 242–255. [CrossRef] [PubMed]
Lotz, J. C., Cheal, E. J., and Hayes, W. C., 1995, “Stress Distributions Within the Proximal Femur During Gait and Falls: Implications for Osteoporotic Fracture,” Osteoporos. Int., 5(4), pp. 252–261. [CrossRef] [PubMed]
Gao, H., Ji, B., Jager, I. L., Arzt, E., and Fratzl, P., 2003, “Materials Become Insensitive to Flaws at Nanoscale: Lessons From Nature,” Proc. Natl. Acad. Sci. U.S.A., 100(10), pp. 5597–5600. [CrossRef] [PubMed]
Bonderer, L. J., Studart, A. R., and Gauckler, L. J., 2008, “Bioinspired Design and Assembly of Platelet Reinforced Polymer Films,” Science, 319(5866), pp. 1069–1073. [CrossRef] [PubMed]
Yao, H. M., Dao, M., Carnelli, D., Tai, K. S., and Ortiz, C., 2011, “Size-Dependent Heterogeneity Benefits the Mechanical Performance of Bone,” J. Mech. Phys. Solids, 59(1), pp. 64–74. [CrossRef]
Wang, X., Zauel, R. R., Rao, D. S., and Fyhrie, D. P., 2008, “Cancellous Bone Lamellae Strongly Affect Microcrack Propagation and Apparent Mechanical Properties: Separation of Patients With Osteoporotic Fracture From Normal Controls Using a 2D Nonlinear Finite Element Method (Biomechanical Stereology),” Bone, 42(6), pp. 1184–1192. [CrossRef] [PubMed]
Mcnamara, L. M., Van Der Linden, J. C., Weinans, H., and Prendergast, P. J., 2006, “Stress-Concentrating Effect of Resorption Lacunae in Trabecular Bone,” J. Biomech., 39(4), pp. 734–741. [CrossRef] [PubMed]
Smit, T. H., and Burger, E. H., 2000, “Is BMU-Coupling a Strain-Regulated Phenomenon? A Finite Element Analysis,” J. Bone Miner. Res., 15(2), pp. 301–307. [CrossRef] [PubMed]
Slyfield, C. R., Tkachenko, E. V., Fischer, S. E., Ehlert, K. M., Yi, I. H., Jekir, M. G., O'brien, R. G., Keaveny, T. M., and Hernandez, C. J., 2012, “Mechanical Failure Begins Preferentially Near Resorption Cavities in Human Vertebral Cancellous Bone Under Compression,” Bone, 50(6), pp. 1281–1287. [CrossRef] [PubMed]
Hernandez, C. J., Gupta, A., and Keaveny, T. M., 2006, “A Biomechanical Analysis of the Effects of Resorption Cavities on Cancellous Bone Strength,” J. Bone Miner. Res., 21(8), pp. 1248–1255. [CrossRef] [PubMed]
Van Rietbergen, B., Weinans, H., Huiskes, R., and Odgaard, A., 1995, “A New Method to Determine Trabecular Bone Elastic Properties and Loading Using Micromechanical Finite-Element Models,” J. Biomech., 28(1), pp. 69–81. [CrossRef] [PubMed]
Gross, T., Pahr, D. H., Peyrin, F., and Zysset, P. K., 2012, “Mineral Heterogeneity Has a Minor Influence on the Apparent Elastic Properties of Human Cancellous Bone: A SRμCT-Based Finite Element Study,” Comput. Methods Biomech. Biomed. Eng., 15(11), pp. 1137–1144. [CrossRef]
Renders, G. A., Mulder, L., Langenbach, G. E., Van Ruijven, L. J., and Van Eijden, T. M., 2008, “Biomechanical Effect of Mineral Heterogeneity in Trabecular Bone,” J. Biomech., 41(13), pp. 2793–2798. [CrossRef] [PubMed]
Renders, G. A., Mulder, L., Van Ruijven, L. J., Langenbach, G. E., and Van Eijden, T. M., 2011, “Mineral Heterogeneity Affects Predictions of Intratrabecular Stress and Strain,” J. Biomech., 44(3), pp. 402–407. [CrossRef] [PubMed]
Chevalier, Y., Pahr, D., Allmer, H., Charlebois, M., and Zysset, P., 2007, “Validation of a Voxel-Based Fe Method for Prediction of the Uniaxial Apparent Modulus of Human Trabecular Bone Using Macroscopic Mechanical Tests and Nanoindentation,” J. Biomech., 40(15), pp. 3333–3340. [CrossRef] [PubMed]
Currey, J. D., 2003, “How Well Are Bones Designed to Resist Fracture?,” J. Bone Miner. Res., 18(4), pp. 591–598. [CrossRef] [PubMed]
Yang, Q. D., Cox, B. N., Nalla, R. K., and Ritchie, R. O., 2006, “Fracture Length Scales in Human Cortical Bone: The Necessity of Nonlinear Fracture Models,” Biomaterials, 27(9), pp. 2095–2113. [CrossRef] [PubMed]
Buchanan, D., and Ural, A., 2010, “Finite Element Modeling of the Influence of Hand Position and Bone Properties on the Colles' Fracture Load During a Fall,” ASME J. Biomech. Eng., 132(8), p. 081007. [CrossRef]
Ural, A., and Vashishth, D., 2006, “Cohesive Finite Element Modeling of Age-Related Toughness Loss in Human Cortical Bone,” J. Biomech., 39(16), pp. 2974–2982. [CrossRef] [PubMed]
Ural, A., 2009, “Prediction of Colles' Fracture Load in Human Radius Using Cohesive Finite Element Modeling,” J. Biomech., 42(1), pp. 22–28. [CrossRef] [PubMed]
Ural, A., and Mischinski, S., 2013, “Multiscale Modeling of Bone Fracture Using Cohesive Finite Elements,” Eng. Fract. Mech., 103(1), pp. 141–152. [CrossRef]
Bruno, P., Waldron, J., and Ural, A., 2014, “Influence of Reduced Compositional Heterogeneity on Fracture Resistance in Cortical Bone,” Trans. Orthop. Res. Soc., 39, p. 1496.

Figures

Grahic Jump Location
Fig. 1

Diagram of the physiologically relevant length scales at which to measure heterogeneity in trabecular bone. This review focuses on heterogeneity at the millimeter-scale (bulk tissue), the mesoscale (single trabeculae), and the microscale. Techniques that can be used to assess both mechanical and compositional properties of bone are included, along with the length scale at which they are relevant. Adapted with permission from Ref. [8], License No. 3480580167028.

Grahic Jump Location
Fig. 2

Representative FTIR images and pixel histograms of collagen maturity in trabeculae from perimenopausal women without history of fragility fracture (−Fx) and with history of fragility fracture (+Fx). The mean and the full width at half maximum values of the Gaussian fits to the distributions are indicated on each histogram.

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