Elastic properties of microstructural components of human bone tissue as measured by nanoindentation

Rho, Jae-Young; Roy, II, Marcel E.; Tsui, Ting Y.; Pharr, George M.

Year	Entry
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2011	Novitskaya E, Chen P-Y, Lee S, Castro-Ceseña A, Hirata G, Lubarda VA, McKittrick J. Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents. Acta Biomater. August 2011;7(8):3170-3177.
2018	Wu D, Isaksson P, Ferguson SJ, Persson C. Young’s modulus of trabecular bone at the tissue level: a review. Acta Biomater. September 15, 2018;78:1.
2021	Casari D, Michler J, Zysset P, Schwiedrzik J. Microtensile properties and failure mechanisms of cortical bone at the lamellar level. Acta Biomater. January 15, 2021;120:135-145.
2021	Bonithon R, Kao AP, Fernández MP, Dunlop JN, Blunn GW, Witte F, Tozzi G. Multi-scale mechanical and morphological characterisation of sintered porous magnesium-based scaffolds for bone regeneration in critical-sized defects. Acta Biomater. June 2021;127:338-352.
2008	Yoon YJ, Cowin SC. The estimated elastic constants for a single bone osteonal lamella. Biomech Model Mechanobiol. February 2008;7(1):1-11.
1999	Rho JY, Zioupos P, Currey JD, Pharr GM. Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone. September 1999;25(3):295-300.
2002	Hengsberger S, Kulik A, Zysset P. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone. 2002;30(1):178-184.
2007	Mulder L, Koolstra JH, den Toonder JMJ, van Eijden TMGJ. Intratrabecular distribution of tissue stiffness and mineralization in developing trabecular bone. Bone. August 2007;41(2):256-265.
2009	Bevill G, Eswaran SK, Farahmand F, Keaveny TM. The influence of boundary conditions and loading mode on high-resolution finite element-computed trabecular tissue properties. Bone. April 2009;44(4):573-578.
2010	Wolfram U, Wilke H-J, Zysset PK. Rehydration of vertebral trabecular bone: influences on its anisotropy, its stiffness and the indentation work with a view to age, gender and vertebral level. Bone. February 2010;46(2):348-354.
2020	Xi L, Song Y, Wu W, Qu Z, Wen J, Liao B, Tao R, Ge J, Fang D. Investigation of bone matrix composition, architecture and mechanical properties reflect structure-function relationship of cortical bone in glucocorticoid induced osteoporosis. Bone. July 2020;136:115334.
2022	Farlay D, Falgayrac G, Ponçon C, Rizzo S, Cortet B, Chapurlat R, Penel G, Badoud I, Ammann P, Boivin G. Material and nanomechanical properties of bone structural units of cortical and trabecular iliac bone tissues from untreated postmenopausal osteoporotic women. Bone Rep. December 2022;17:101623.
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2011	Donnelly E. Methods for assessing bone quality: a review. Clin Orthop Relat Res. August 2011;469:2128-2138.
2019	Semaan M, Karam E, Baron C, Pithioux M. Estimation of the elastic modulus of child cortical bone specimens via microindentation. Connect Tissue Res. July 4, 2019;60(4):399-405.
2001	Hengsberger S, Kulik A, Zysset P. A combined atomic force microscopy and nanoindentation technique to investigate the elastic properties of bone structural units. Eur Cell Mater. January–June 2001;1:12-17.
2020	Zhou Y, Kastner MJ, Tighe TB, Du J. Elastic modulus mapping for bovine cortical bone from submillimeter- to submicron-scales using PeakForce Tapping atomic force microscopy. Extreme Mech Lett. November 1, 2020;41:101031.
2011	Mischinski S, Ural A. Finite element modeling of microcrack growth in cortical bone. J Appl Mech. July 2011;78(4):041016.
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2004	Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM. Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech. January 2004;37(1):27-35.
2004	Bourne BC, van der Meulen MCH. Finite element models predict cancellous apparent modulus when tissue modulus is scaled from specimen CT-attenuation. J Biomech. May 2004;37(5):613-621.
2004	Silva MJ, Brodt MD, Fan Z, Rho J-Y. Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6. J Biomech. November 2004;37(11):1639-1646.
2007	Rath Bonivtch A, Bonewald LF, Nicolella DP. Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech. 2007;40(10):2199-2206.
2010	Wolfram U, Wilke H-J, Zysset PK. Valid μ finite element models of vertebral trabecular bone can be obtained using tissue properties measured with nanoindentation under wet conditions. J Biomech. 2010;43(9):1731-1737.
2011	Burket J, Gourion-Arsiquaud S, Havill LM, Baker SP, Boskey AL, van der Meulen MCH. Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech. January 11, 2011;44(2):277-284.
2011	Wu Z, Baker TA, Ovaert TC, Niebur GL. The effect of holding time on nanoindentation measurements of creep in bone. J Biomech. April 7, 2011;44(6):2055-2062.
2011	Carnelli D, Lucchini R, Ponzoni M, Contro R, Vena P. Nanoindentation testing and finite element simulations of cortical bone allowing for anisotropic elastic and inelastic mechanical response. J Biomech. July 7, 2011;44(10):1852-1858.
2012	Feng L, Chittenden M, Schirer J, Dickinson M, Jasiuk I. Mechanical properties of porcine femoral cortical bone measured by nanoindentation. J Biomech. June 26, 2012;45(10):1775-1782.
2014	Yamada S, Tadano S, Fukuda S. Nanostructure and elastic modulus of single trabecula in bovine cancellous bone. J Biomech. November 7, 2014;47(14):3482-3487.
2000	Vajjhala S, Kraynik AM, Gibson LJ. A cellular solid model for modulus reduction due to resorption of trabeculae in bone. J Biomech Eng. October 2000;122(5):511-515.
2002	Makiyama AM, Vajjhala S, Gibson LJ. Analysis of crack growth in a 3D Voronoi structure: a model for fatigue in low density trabecular bone. J Biomech Eng. October 2002;124(4):512-520.
2004	Dong XN, Guo XE. Geometric determinants to cement line debonding and osteonal lamellae failure in osteon pushout tests. J Biomech Eng. June 2004;126(3):387-390.
2005	Hoffler CE, Guo XE, Zysset PK, Goldstein SA. An application of nanoindentation technique to measure bone tissue lamellae properties. J Biomech Eng. January 2005;127(7):1046-1053.
2006	Dong XN, Guo XE. Prediction of cortical bone elastic constants by a two-level micromechanical model using a generalized self-consistent method. J Biomech Eng. June 2006;128(3):309-316.
2009	Franzoso G, Zysset PK. Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. J Biomech Eng. February 2009;131(2):021001.
2010	Carnelli D, Gastaldi D, Sassi V, Contro R, Ortiz C, Vena P. A finite element model for direction-dependent mechanical response to nanoindentation of cortical bone allowing for anisotropic post-yield behavior of the tissue. J Biomech Eng. August 2010;132(8):081008.
2015	Oftadeh R, Perez-Viloria M, Villa-Camacho JC, Vaziri A, Nazarian A. Biomechanics and mechanobiology of trabecular bone: a review. J Biomech Eng. January 2015;137(1):010802.
2001	Swadener JG, Rho J, Pharr GM. Effects of anisotropy on elastic moduli measured by nanoindentation in human tibial cortical bone. J Biomed Mater Res. October 2001;57(1):108-112.
2003	Fan Z, Rho J-Y. Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone. J Biomed Mater Res. October 1, 2003;A67(1):208-214.
2003	Xu J, Rho JY, Mishra SR, Fan Z. Atomic force microscopy and nanoindentation characterization of human lamellar bone prepared by microtome sectioning and mechanical polishing technique. J Biomed Mater Res. December 1, 2003;A67(3):719-726.
2006	Donnelly E, Baker SP, Boskey AL, van der Meulen MC. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res. May 2006;A77(2):426-435.
2008	Mulder L, Koolstra JH, den Toonder JMJ, van Eijden TMGJ. Relationship between tissue stiffness and degree of mineralization of developing trabecular bone. J Biomed Mater Res. February 2008;A84(2):508-515.
2008	Lewis G, Nyman JS. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. J Biomed Mater Res. October 2008;B87(1):286-301.
2000	Kinney JH, Haupt DL, Balooch M, Ladd AJC, Ryaby JT, Lane NE. Three‐dimensional morphometry of the L6 vertebra in the ovariectomized rat model of osteoporosis: biomechanical implications. J Bone Miner Res. October 2000;15(10):1981-1991.
2001	Rho JY, Currey JD, Zioupos P, Pharr GM. The anisotropic Young's modulus of equine secondary osteones and interstitial bone determined by nanoindentation. J Exp Biol. May 2001;204(10):1775-1781.
2006	Donnelly E, Williams RM, Downs SA, Dickinson ME, Baker SP, van der Meulen MCH. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res. August 2006;21(8):2106-2117.
2005	Tai K, Qi HJ, Ortiz C. Effect of mineral content on the nanoindentation properties and nanoscale deformation mechanisms of bovine tibial cortical bone. J Mater Sci Mater Med. October 2005;16(10):947-959.
2009	Espinoza Orías AA, Deuerling JM, Landrigan MD, Renaud JE, Roeder RK. Anatomic variation in the elastic anisotropy of cortical bone tissue in the human femur. J Mech Behav Biomed Mater. July 2009;2(3):255-263.
2011	Jungmann R, Szabo ME, Schitter G, Tang RY-S, Vashishth D, Hansma PK, Thurner PJ. Local strain and damage mapping in single trabeculae during three-point bending tests. J Mech Behav Biomed Mater. May 2011;4(4):523-534.
2011	Shepherd TN, Zhang J, Ovaert TC, Roeder RK, Niebur GL. Direct comparison of nanoindentation and macroscopic measurements of bone viscoelasticity. J Mech Behav Biomed Mater. November 2011;4(8):2055-2062.
2012	Vaughan TJ, McCarthy CT, McNamara LM. A three-scale finite element investigation into the effects of tissue mineralisation and lamellar organisation in human cortical and trabecular bone. J Mech Behav Biomed Mater. August 2012;12:50-62.
2013	Carretta R, Stüssi E, Müller R, Lorenzetti S. Within subject heterogeneity in tissue-level post-yield mechanical and material properties in human trabecular bone. J Mech Behav Biomed Mater. August 2013;24:64-73.
2018	Frank M, Marx D, Nedelkovski V, Fischer J-T, Pahr DH, Thurner PJ. Dehydration of individual bovine trabeculae causes transition from ductile to quasi-brittle failure mode. J Mech Behav Biomed Mater. November 2018;87:296-305.
2019	Asgari M, Abi-Rafeh J, Hendy GN, Pasini D. Material anisotropy and elasticity of cortical and trabecular bone in the adult mouse femur via AFM indentation. J Mech Behav Biomed Mater. May 2019;93:81-92.
2020	Remache D, Semaan M, Rossi JM, Pithioux M, Milan J. Application of the Johnson-Cook plasticity model in the finite element simulations of the nanoindentation of the cortical bone. J Mech Behav Biomed Mater. January 2020;101:103426.
2002	Fan Z, Swadener JG, Rho JY, Roy ME, Pharr GM. Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res. July 2002;20(4):806-810.
2004	Day JS, Ding M, Bednarz P, van der Linden JC, Mashiba T, Hirano T, Johnston CC, Burr DB, Hvid I, Sumner DR, Weinans H. Bisphosphonate treatment affects trabecular bone apparent modulus through micro-architecture rather than matrix properties. J Orthop Res. May 2004;22(3):465-471.
2020	Collins CJ, Kozyrev M, Frank M, Andriotis OG, Byrne RA, Kiener HP, Pretterklieber ML, Thurner PJ. The impact of age, mineralization, and collagen orientation on the mechanics of individual osteons from human femurs. Materialia. March 2020;9:100573.
2007	Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater. June 2007;6(6):454-462.
2008	Ruppel ME, Miller LM, Burr DB. The effect of the microscopic and nanoscale structure on bone fragility. Osteoporos Int. September 2008;19(9):1251-1265.
2020	Ogurkowska MB, Błaszczyk A. Distribution of Young's modulus at various sampling points in a human lumbar spine vertebral body. Spine J. November 2020;20(11):1861-1875.
2016	Guang Y. Characterization of Bone and Bone Marrow Lesions in the Osteoarthritic Hip [Master's thesis]. Boston University; 2016.
2026	Gutiérrez Marty AF. Modeling the Contributions of Mechanical Heterogeneity to the Mechanical Behavior of Bone [PhD thesis]. Boston University; 2026.
2010	Campbell SE. Nanoindentation of Bio- and Geo-Mineralized Composites: Contribution of Microstructure and Composition [PhD thesis]. University of Colorado; 2010.
2013	Abraham AC. From Meniscus to Bone: Structure and Function of Human Meniscal Entheses and Deleterious Effects of Osteoarthritis [PhD thesis]. Colorado State University; 2013.
2002	Dong X. Micromechanics of Osteonal Cortical Bone [PhD thesis]. Columbia University; 2002.
2007	Cole JH. The Role of Architecture and Tissue Properties in the Structural Integrity of Human Vertebral Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2007.
2013	Burket JC. Alterations in Tissue Composition and Nanomechanical Properties With Ageing, Osteoporosis, and Treatment [PhD thesis]. Ithaca, NY: Cornell University; January 2013.
2013	Kim G. The Effects of Mineralization and Crystallinity on the Mechanical Behavior of Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2013.
2005	Cook RB. Non-Invasively Assessed Skeletal Bone Status and Its Relationship to the Biomechanical Properties and Condition of Cancellous Bone [PhD thesis]. Cranfield, UK: Cranfield University; December 18, 2005.
2005	Yoon YJ. Estimates of Bone Elastic Constants At Sequential Hierarchical Levels [PhD thesis]. New York, NY: The City University of New York; 2005.
2012	Sharma D. Effects of Estrogen Deficiency on the Osteocyte Lacunar-Canalicular Network [PhD thesis]. New York, NY: The City University of New York; 2012.
2002	Hengsberger S. Mechanical Characterization of Bone from the Tissue Down to the Lamellar Level by Means of Nanoindentation [PhD thesis]. Lausanne, Switzerland: École Polytechnique Fédérale de Lausanne; 2002.
2006	Garcia D. Elastic Plastic Damage Laws for Cortical Bone [PhD thesis]. Lausanne, Switzerland: École Polytechnique Fédérale de Lausanne; 2006.
2005	Day JS. Bone Quality: The Mechanical Effects of Microarchitecture and Matrix Properties [PhD thesis]. Erasmus University Rotterdam; 2005.
2014	Carretta R. Post-Yield Mechanics and Material Composition of Single Trabeculae: A Combined Experimental and Modelling Approach [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2014.
2010	Feng L. Multi-Scale Characterization of Swine Femoral Cortical Bone and Long Bone Defect Repair by Regeneration [PhD thesis]. University of Illinois at Urbana-Champaign; 2010.
2012	Hamed E. Multiscale Modeling of Elastic Moduli and Strength of Bone [PhD thesis]. University of Illinois at Urbana-Champaign; 2012.
2017	Bakalova LP. Relating Cortical Bone Mechanics to Intracortical Pore Morphology, Distribution and Remodeling History Within the Fibula Diaphysis [Master's thesis]. University of Illinois at Urbana-Champaign; 2017.
2020	Bennison MBL. The Role of Cancellous Bone Architecture in Misalignment and Side Effect Errors [Master's thesis]. Sudbury, ON: Laurentian University; 2020.
2022	Rahovich P. Effects of Bone Structural Unit (BSU) Geometry and Material Properties on Crack Growth Through Idealized Trabecular Microstructures [Master's thesis]. Sudbury, ON: Laurentian University; 2022.
2007	Akhtar R. Micromechanical Behaviour of Bone [PhD thesis]. University of Manchester; 2007.
2007	Tai K. Nanomechanics and Ultrastructural Studies of Cortical Bone: Fundamental Insights Regarding Structure-Function, Mineral-Organic Force Mechanics Interactions, and Heterogeneity [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; June 2007.
2024	Cox JM. Tissue Material Heterogeneity and Structural Organization in Trabecular Bone: New Insights Into Tissue Mechanics and Development [PhD thesis]. North Carolina State University; 2024.
2015	Oftadeh R. Hierarchical Analysis and Multiscale Modelling of Cellular Structures: From Meta Materials to Bone Structure [PhD thesis]. Northeastern University; December 2015.
2012	Deymier-Black AC. Study of the Elasto-Plastic Properties of Mineralized Biomaterials Via Synchrotron High-Energy X-Ray Diffraction [PhD thesis]. Evanston, IL: Northwestern University; June 2012.
2005	Espinoza Orias AA. The Relationship Between the Mechanical Anisotropy of Human Cortical Bone Tissue and Its Microstructure [PhD thesis]. University of Notre Dame; April 2005.
2010	Deuerling JM. Effects of Ultrastructural Organization on the Mechanical Properties and Anisotropy of Human Cortical Bone [PhD thesis]. University of Notre Dame; December 2010.
2010	Shi X. Effects of Architecture on Microdamage Susceptibility in Trabecular Bone [PhD thesis]. University of Notre Dame; April 2010.
2011	Wu Z. Measures of Bone Quality and Their Relationship to Bone Mechanical Properties [PhD thesis]. University of Notre Dame; December 2011.
2020	Karali A. Multi-Scale Evaluation of Bone Combining Indentation, in Situ XCT Mechanics and Digital Volume Correlation [PhD thesis]. Portsmouth, England: University of Portsmouth; 2020.
2009	Lievers WB. Effects of Geometric and Material Property Changes on the Apparent Elastic Properties of Cancellous Bone [PhD thesis]. Queen's University; April 2009.
2001	Kim DG. Micromechanical Analysis of Bone At a Bone-Implant Interface [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; April 2001.
2009	Ferreri SL. Anti-Catabolic Role of Ultrasonic Mechanical Perturbation in Prevention of Bone Loss and Turnover in OVX Rat Model: A Combined Empirical, Nanomechanical and Micro-Numerical Simulation Approach [PhD thesis]. Stony Brook, NY: Stony Brook University; August 2009.
2006	Gleeson JP. Composition and Mechanical Properties of Osteoarthritic Subchondral Trabecular Tibial Bone [PhD thesis]. Trinity College Dublin; November 2006.
2021	Frank M. Mechanical Characterization of Individual Trabeculae [PhD thesis]. Vienna University of Technology; February 2021.
2006	Soares Silva LDM. Nanoindentation Study and Quantitative Backscattered Electron Imaging of Human Cortical Bone [Master's thesis]. Vancouver, BC: University of British Columbia; 2006.
2008	Tang A. Nanoindentation of Peri-Implant Bone and Dentin [Master's thesis]. Vancouver, BC: University of British Columbia; March 2008.
2003	Bayraktar HH. Multiaxial Strength and Micromechanics of Human Bone [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2003.
2004	Kazakia GJ. Development, Analysis, and Imaging of a Tissue Engineered Trabecular Bone Substitute [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2004.
2008	Bevill GR. Micromechanical Modeling of Failure in Trabecular Bone [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2008.
2019	Sadoughi S. Micromechanics of Human Bone: Role of Architecture and Tissue Material Properties [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2019.
2012	Evdokimenko E. Investigation Into Mechanical Properties of Bone and Its Main Constituents [PhD thesis]. San Diego (UCSD), University of California; 2012.
2016	Jones DA. Reference Point Indentation of Human Trabecular Bone Treated With Bisphosphonates for Varying Durations [Master's thesis]. University of Kentucky; 2016.
2005	Oyen ML. Ultrastructural Characterization of Time-Dependent, Inhomogeneous Materials and Tissues [PhD thesis]. Minneapolis, MN: University of Minnesota; June 2005.
2006	Seong W-J. Relationships Between the Physical Properties of Human Jawbone and the Initial Stability of Dental Implant, and Their Dependency on Anatomical Regions of Jawbone [PhD thesis]. University of Minnesota; April 2006.
2023	Kochetkova T. Quantifying Bone Extracellular Matrix Properties for Improved Clinical Fracture Risk Prediction [PhD thesis]. Universität Bern; 2023.
2025	Simon M. Multi-Scale Bone Morphology-Mechanical Property Relations in Ageing and Disease [PhD thesis]. Universität Bern; 2025.
2002	Raum K. Quantitative Akustische Rastermikroskopiemethoden zur Charakterisierung der elastischen Eigenschaften von Knochengewebe [PhD thesis]. Martin Luther University Halle-Wittenberg; 2002.
2011	Wolfram U. Mechanical Multiscale Characterisation of Vertebral Trabecular Bone for the Prediction of Vertebral Fracture Risk [PhD thesis]. University of Ulm; 2011.
2021	Atthapreyangkul A. Multi-Scale Finite Element Modelling of Human Cortical Bone: An Analysis of the Mechanical Properties and Microdamage Onset of Cortical Bone [PhD thesis]. University of New South Wales; April 2021.
2015	Lin C-L. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2015.
2016	Lin C-l. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2016.
2020	Singleton RC. A Study of Aging in Male Cortical Bone Using Nanoindentation [PhD thesis]. Knoxville, University of Tennessee; August 2020.
2009	Nakade R. Influence of Interfacial Properties and Inhomogeneity on Formation of Microdamage in Bone [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; December 2009.
2009	Potter RS. Age Effects on the Material and Mechanical Properties of Bone At the Osteocyte Lacuna [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; December 2009.
2013	Shome C. 3D Orientation Distribution & Deformation of Mineral Crystals in Human Cortical Bone [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; December 2013.
2014	Makowski AJ. Evaluation of Raman Spectroscopy for Fracture Resistance Assessment [PhD thesis]. Nashville, TN: Vanderbilt University; December 2014.
2009	Rath AL. The Effects of Strain and Perilacunar Environment on the Mechanotransduction of Osteocytes [PhD thesis]. Winston-Salem, NC: Wake Forest University; May 2009.

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