Abstract
Nanoindentation is a sophisticated technique that has been used to characterize a wide selection of materials, including bone. Given the complex and hierarchical nature of bone, nanoindentation allows for assessment of composite material properties at the nano-range of bone tissue. These nanoindentation-based measures can provide important baseline information to aid in understanding the overall mechanical behavior, the pathologic changes of disease, and the pharmaceutical response of bone. In this review, the challenges and limitations of our current knowledge related to nanoindentation are presented as well as the future directions for its application to bone biology.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, New York, p 79
Carter DR, Beaupre GS (2001) Skeletal function and form: mechanobiology of skeletal development, aging, and regeneration. Cambridge University Press, Cambridge
Seeman E (2003) Pathogenesis of osteoporosis. J Appl Physiol 95:2142–2151
Keaveny TM, Morgan EF, Niebur GL, Yeh OC (2001) Biomechanics of trabecular bone. Annu Rev Biomed Eng 3:307–333
Kopperdahl DL, Keaveny TM (1998) Yield strain behavior of trabecular bone. J Biomech 31:601–608
McCreadie BR, Goldstein SA (2000) Biomechanics of fracture: is bone mineral density sufficient to assess risk? J Bone Miner Res 15:2305–2308
Heaney RP (2003) Is the paradigm shifting? Bone 33:457–465
Seeman E, Delmas PD (2006) Bone quality – the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261
Hernandez CJ, Keaveny TM (2006) A biomechanical perspective on bone quality. Bone 39:1173–1181
Renders GA, Mulder L, van Ruijven LJ, van Eijden TM (2006) Degree and distribution of mineralization in the human mandibular condyle. Calcif Tissue Int 79:190–196
Seeman E (2003) Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos Int 14(Suppl 3):S2–S8
Boonrungsiman S, Gentleman E, Carzaniga R, Evans ND, McComb DW, Porter AE, Stevens MM (2012) The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc Natl Acad Sci USA 109:14170–14175
Roschger P, Paschalis EP, Fratzl P, Klaushofer K (2008) Bone mineralization density distribution in health and disease. Bone 42:456–466
Ruppel M, Miller L, Burr D (2008) The effect of the microscopic and nanoscale structure on bone fragility. Osteoporos Int 19:1251–1265
Boivin G, Meunier PJ (2003) Methodological considerations in measurement of bone mineral content. Osteoporosis Int 14(Suppl 5):S22–S27; discussion S27–28
Yao W, Cheng Z, Koester KJ, Ager JW, Balooch M, Pham A, Chefo S, Busse C, Ritchie RO, Lane NE (2007) The degree of bone mineralization is maintained with single intravenous bisphosphonates in aged estrogen-deficient rats and is a strong predictor of bone strength. Bone 41:804–812
Roschger P, Gupta HS, Berzlanovich A, Ittner G, Dempster DW, Fratzl P, Cosman F, Parisien M, Lindsay R, Nieves JW, Klaushofer K (2003) Constant mineralization density distribution in cancellous human bone. Bone 32:316–323
Busse B, Hahn M, Soltau M, Zustin J, Puschel K, Duda GN, Amling M (2009) Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone 45:1034–1043
Gilmore RS, Katz JL (1982) Elastic properties of apatites. J Mater Sci 17:1131–1141
Grant CA, Brockwell DJ, Radford SE, Thomson NH (2009) Tuning the elastic modulus of hydrated collagen fibrils. Biophys J 97:2985–2992
Burr DB (2002) The contribution of the organic matrix to bone’s material properties. Bone 31:8–11
Donnelly E (2011) Methods for assessing bone quality: a review. Clin Orthop Relat Res 469:2128–2138
Oliver WC, Pharr GM (1992) An improved technique for determining hardness and elastic modulus using load and displacement-sensing indentation systems. J Mater Res 7:1564–1583
Hoffler CE, Guo XE, Zysset PK, Goldstein SA (2005) An application of nanoindentation technique to measure bone tissue Lamellae properties. J Biomech Eng 127:1046–1053
Roy ME, Rho JY, Tsui TY, Evans ND, Pharr GM (1999) Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J Biomed Mater Res 44:191–197
Oliver WC, Pharr GM (2004) Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology. J Mater Res 19:3–20
Li XD, Bhushan B (2002) A review of nanoindentation continuous stiffness measurement technique and its applications. Mater Charact 48:11–36
Rho JY, Tsui TY, Pharr GM (1997) Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 18:1325–1330
Mittra E, Akella S, Qin YX (2006) The effects of embedding material, loading rate and magnitude, and penetration depth in nanoindentation of trabecular bone. J Biomed Mater Res A 79:86–93
Fan Z, Rho JY (2003) Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone. J Biomed Mater Res 67A:208–214
Kim DG, Huja SS, Navalgund A, D’Atri A, Tee B, Reeder S, Ri Lee H (2013) Effect of estrogen deficiency on regional variation of a viscoelastic tissue property of bone. J Biomech 46:110–115
Kim DG, Huja SS (2008) Nanoindentation viscosity of osteonal bone matrix is associated with degree of mineralization. Trans Orthop Res Soc 33:297
Kim DG, Huja SS, Lee HR, Tee BC, Hueni S (2010) Relationships of viscosity with contact hardness and modulus of bone matrix measured by nanoindentation. J Biomech Eng 132:024502
Huja SS, Beck FM, Thurman DT (2006) Indentation properties of young and old osteons. Calcif Tissue Int 78:392–397
Rho JY, Pharr GM (1999) Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J Mater Sci Mater Med 10:485–488
Zhang J, Niebur GL, Ovaert TC (2008) Mechanical property determination of bone through nano- and micro-indentation testing and finite element simulation. J Biomech 41:267–275
Wu Z, Ovaert TC, Niebur GL (2012) Viscoelastic properties of human cortical bone tissue depend on gender and elastic modulus. J Orthop Res 30:693–699
Reilly DT, Burstein AH (1974) Review article. The mechanical properties of cortical bone. J Bone Joint Surg Am 56:1001–1022
Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA (1999) Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech 32:1005–1012
Johnson WM, Rapoff AJ (2007) Microindentation in bone: hardness variation with five independent variables. J Mater Sci Mater Med 18:591–597
Mulder L, Koolstra JH, den Toonder JM, van Eijden TM (2008) Relationship between tissue stiffness and degree of mineralization of developing trabecular bone. J Biomed Mater Res A 84:508–515
Carter DR, Hayes WC (1977) The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg 59-A:954–962
Isaksson H, Nagao S, Malkiewicz M, Julkunen P, Nowak R, Jurvelin JS (2010) Precision of nanoindentation protocols for measurement of viscoelasticity in cortical and trabecular bone. J Biomech 43:2410–2417
Rho JY, Roy ME 2nd, Tsui TY, Pharr GM (1999) Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res 45:48–54
Donnelly E, Baker SP, Boskey AL, van der Meulen MC (2006) Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res A 77:426–435
Kim DG, Hueni S, Tee BC, Lee H, Huja SS (2009) Effect of nanoindentation holding periods on correlation between viscosity and modulus of bone matrix. BMES Fall meeting, Pittsburgh, p 1256
van der Meulen MCH, Huiskes R (2002) Why mechanobiology?: a survey article. J Biomech 35:401–414
Novitskaya E, Chen PY, Lee S, Castro-Cesena A, Hirata G, Lubarda VA, McKittrick J (2011) Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents. Acta Biomater 7:3170–3177
Hoffler CE, Moore KE, Kozloff K, Zysset PK, Brown MB, Goldstein SA (2000) Heterogeneity of bone lamellar-level elastic moduli. Bone 26:603–609
Hoffler CE, Moore KE, Kozloff K, Zysset PK, Goldstein SA (2000) Age, gender, and bone lamellae elastic moduli. J Orthop Res 18:432–437
Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP (2011) Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone 49:1279–1289
Mulder L, Koolstra JH, den Toonder JMJ, van Eijden TMGJ (2007) Intratrabecular distribution of tissues stiffness and mineralization in developing trabecular bone. Bone 41:256–265
Oyen ML, Cook RF (2003) Load–displacement behavior during sharp indentation of viscous-elastic–plastic materials. J Mater Res 18:139–150
Oyen ML, Ko CC (2007) Examination of local variations in viscous, elastic, and plastic indentation responses in healing bone. J Mater Sci Mater Med 18:623–628
Oyen ML (2006) Nanoindentation hardness of mineralized tissues. J Biomech 39:2699–2702
Fischer-Cripps AC (2004) A simple phenomenological approach to nanoindentation creep. Mater Sci Eng A-Struct Mater Prop Microstruct Process 385:74–82
Kim DG, Kwon HJ, Han JS, Kim D, Lee B, Park C (2013) Change of viscoelastic property at bone-implant interface in healing. IADR #3736
Kim D-G, Huja SS, Hueni S, Tee BC, Lee H (2010) Relationship between elastic modulus and viscosity of bone matrix is strong independent of species, anatomical sites, and types of bone. Trans Ortho Res Soc 56:645
Donnelly E, Williams RM, Downs SA, Dickinson ME, Baker SP, van der Meulen MCH (2006) Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res 21:2106–2117
Pathak S, Swadener JG, Kalidindi SR, Courtland HW, Jepsen KJ, Goldman HM (2011) Measuring the dynamic mechanical response of hydrated mouse bone by nanoindentation. J Mech Behav Biomed Mater 4:34–43
Raghavan M, Sahar ND, Kohn DH, Morris MD (2012) Age-specific profiles of tissue-level composition and mechanical properties in murine cortical bone. Bone 50:942–953
Tai K, Qi HJ, 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 16:947–959
Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C (2007) Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater 6:454–462
Morris MD, Mandair GS (2011) Raman assessment of bone quality. Clin Orthop Relat Res 469:2160–2169
Hofstetter B, Gamsjaeger S, Phipps RJ, Recker RR, Ebetino FH, Klaushofer K, Paschalis EP (2012) Effects of alendronate and risedronate on bone material properties in actively forming trabecular bone surfaces. J Bone Miner Res 27:995–1003
Tzaphlidou M (2008) Bone architecture: collagen structure and calcium/phosphorus maps. J Biol Phys 34:39–49
Donnelly E, Boskey AL, Baker SP, van der Meulen MC (2010) Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A 92:1048–1056
Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L (1999) Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int 65:203–210
Kourkoumelis N, Balatsoukas I, Tzaphlidou M (2012) Ca/P concentration ratio at different sites of normal and osteoporotic rabbit bones evaluated by Auger and energy dispersive X-ray spectroscopy. J Biol Phys 38:279–291
Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, Chapurlat R, Chevalier J, Boivin G (2012) Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res 27:825–834
Donnelly E, Meredith DS, Nguyen JT, Gladnick BP, Rebolledo BJ, Shaffer AD, Lorich DG, Lane JM, Boskey AL (2012) Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J Bone Miner Res 27:672–678
Garetto LP, Chen J, Parr JA, Roberts WE (1995) Remodeling dynamics of bone supporting rigidly fixed titanium implants: a histomorphometric comparison in four species including humans. Implant Dent 4:235–243
Brunski JB (1999) In vivo bone response to biomechanical loading at the bone/dental-implant interface. Adv Dent Res 13:99–119
Kallai I, Mizrahi O, Tawackoli W, Gazit Z, Pelled G, Gazit D (2011) Microcomputed tomography-based structural analysis of various bone tissue regeneration models. Nat Protoc 6:105–110
Pellegrini G, Seol YJ, Gruber R, Giannobile WV (2009) Pre-clinical models for oral and periodontal reconstructive therapies. J Dent Res 88:1065–1076
Rios HF, Lin Z, Oh B, Park CH, Giannobile WV (2011) Cell- and gene-based therapeutic strategies for periodontal regenerative medicine. J Periodontol 82:1223–1237
Boivin G, Meunier PJ (2002) The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tissue Int 70:503–511
Asefa T, Yoshina-Ishii C, MacLachlan MJ, Ozin GA (2000) New nanocomposites: putting organic function “inside” the channel walls of periodic mesoporous silica. J Mater Chem 10:1751–1755
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Kim, DG., Elias, K.L. (2014). Elastic, Viscoelastic, and Fracture Properties of Bone Tissue Measured by Nanoindentation. In: Bhushan, B., Luo, D., Schricker, S., Sigmund, W., Zauscher, S. (eds) Handbook of Nanomaterials Properties. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-31107-9_46
Download citation
DOI: https://doi.org/10.1007/978-3-642-31107-9_46
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-31106-2
Online ISBN: 978-3-642-31107-9
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)