An Application of Nanoindentation Technique to Measure Bone Tissue Lamellae Properties
Abstract
Measuring the microscopic mechanical properties of bone tissue is important in support of understanding the etiology and pathogenesis of many bone diseases. Knowledge about these properties provides a context for estimating the local mechanical environment of bone related cells that coordinate the adaptation to loads experienced at the whole organ level. The objective of this study was to determine the effects of experimental testing parameters on nanoindentation measures of lamellar-level bone mechanical properties. Specifically, we examined the effect of specimen preparation condition, indentation depth, repetitive loading, time delay, and displacement rate. The nanoindentation experiments produced measures of lamellar elastic moduli for human cortical bone (average value of 17.7±4.0GPa for osteons and 19.3±4.7GPa for interstitial bone tissue). In addition, the hardness measurements produced results consistent with data in the literature (average 0.52±0.15GPa for osteons and 0.59±0.20GPa for interstitial bone tissue). Consistent modulus values can be obtained from a 500-nm-deep indent. The results also indicated that the moduli and hardnesses of the dry specimens are significantly greater (22.6% and 56.9%, respectively) than those of the wet and wet and embedded specimens. The latter two groups were not different. The moduli obtained at a 5‐nm∕s loading rate were significantly lower than the values at the 10- and 20‐nm∕s loading rates while the 10- and 20‐nm∕s rates were not significantly different. The hardness measurements showed similar rate-dependent results. The preliminary results indicated that interstitial bone tissue has significantly higher modulus and hardness than osteonal bone tissue. In addition, a significant correlation between hardness and elastic modulus was observed.
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The difference between nanoscale moduli and those at greater length scales may be due to most nanoindentation measurements on bone being conducted under dry conditions.
“Although the nanoscale moduli appear higher than those at greater length scales (Table 1), this difference may be due to the fact that most nanoindentation measurements on bone are conducted under dry conditions (38).”
From Bone Mechanical Properties in Healthy and Diseased States (2018) · cites this paper as [38]
Cites
Baltosser, W. H., & Zar, J. H. (1996) · Ecology · doi:10.2307/2265725 · Cited by 35,166 · see citing works
Oliver, W. C., & Pharr, G. M. (1992) · Journal of materials research/Pratt's guide to venture capital sources · doi:10.1557/jmr.1992.1564 · Cited by 26,941 · see citing works
Sneddon, I. N. (1965) · International Journal of Engineering Science · doi:10.1016/0020-7225(65)90019-4 · Cited by 4,407 · see citing works
A method for interpreting the data from depth-sensing indentation instruments
Doerner, M. F., & Nix, W. D. (1986) · Journal of materials research/Pratt's guide to venture capital sources · doi:10.1557/jmr.1986.0601 · Cited by 2,871 · see citing works
Pharr, G. M., Oliver, W. C., & Brotzen, F. R. (1992) · Journal of materials research/Pratt's guide to venture capital sources · doi:10.1557/jmr.1992.0613 · Cited by 1,573 · see citing works
The elastic and ultimate properties of compact bone tissue
Reilly, D. T., & Burstein, A. H. (1975) · Journal of Biomechanics · doi:10.1016/0021-9290(75)90075-5 · Cited by 1,533 · see citing works
Young's modulus of trabecular and cortical bone material: Ultrasonic and microtensile measurements
Rho, J. Y., Ashman, R. B., & Turner, C. H. (1993) · Journal of Biomechanics · doi:10.1016/0021-9290(93)90042-d · Cited by 1,283 · see citing works
Zysset, P. K., Guo, X.-D. E., Hoffler, C. E., Moore, K. E., & Goldstein, S. A. (1999) · Journal of Biomechanics · doi:10.1016/s0021-9290(99)00111-6 · Cited by 1,001 · see citing works
Self-citationElastic properties of human cortical and trabecular lamellar bone measured by nanoindentation
Rho, J.-Y., Tsui, T. Y., & Pharr, G. M. (1997) · Biomaterials · doi:10.1016/s0142-9612(97)00073-2 · Cited by 924 · see citing works
Elastic analysis of some punch problems for a layered medium
King, R. B. (1987) · International Journal of Solids and Structures · doi:10.1016/0020-7683(87)90116-8 · Cited by 903 · see citing works
Bone Compressive Strength: The Influence of Density and Strain Rate
Carter, D. R., & Hayes, W. C. (1976) · Science · doi:10.1126/science.996549 · Cited by 709 · see citing works
The Mechanical Properties of Cortical Bone
Reilly, D. T., & Burstein, A. H. (1974) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-197456050-00012 · Cited by 656 · see citing works
Choi, K., Kuhn, J. L., Ciarelli, M. J., & Goldstein, S. A. (1990) · Journal of Biomechanics · doi:10.1016/0021-9290(90)90003-l · Cited by 534 · see citing works
Self-citationProperties and an Anisotropic Model of Cancellous Bone From the Proximal Tibial Epiphysis
Williams, J. L., & Lewis, J. L. (1982) · Journal of Biomechanical Engineering · doi:10.1115/1.3138303 · Cited by 418 · see citing works
The compressive properties of single osteons
Ascenzi, A., & BONUCCI, E. (1968) · The Anatomical Record · doi:10.1002/ar.1091610309 · Cited by 394 · see citing works
Elastic modulus of trabecular bone material
ASHMAN, R. B., & Rho, J. Y. (1988) · Journal of Biomechanics · doi:10.1016/0021-9290(88)90167-4 · Cited by 393 · see citing works
The tensile properties of single osteons
Ascenzi, A., & BONUCCI, E. (1967) · The Anatomical Record · doi:10.1002/ar.1091580403 · Cited by 351 · see citing works
Elastic properties of microstructural components of human bone tissue as measured by nanoindentation
Rho, J. Y., Roy, M. E., Tsui, T. Y., & Pharr, G. M. (1999) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(199904)45:1 · Cited by 348 · see citing works
Rho, J. Y., Zioupos, P., Currey, J. D., & Pharr, G. M. (2002) · Journal of Biomechanics · doi:10.1016/s0021-9290(01)00199-3 · Cited by 276 · see citing works
Heterogeneity of bone lamellar-level elastic moduli
Hoffler, C. E., Moore, K. E., Kozloff, K. M., Zysset, P. K., Brown, M. B., & Goldstein, S. A. (2000) · Bone · doi:10.1016/s8756-3282(00)00268-4 · Cited by 259 · see citing works
Self-citationEffects of drying on the mechanical properties of bovine femur measured by nanoindentation
Rho, J. Y., & Pharr, G. M. (1999) · Journal of Materials Science Materials in Medicine · doi:10.1023/a:1008901109705 · Cited by 254 · see citing works
A comparison of the fatigue behavior of human trabecular and cortical bone tissue
Choi, K., & Goldstein, S. A. (1992) · Journal of Biomechanics · doi:10.1016/0021-9290(92)90051-2 · Cited by 247 · see citing works
Self-citation(2020) · Springer eBooks · doi:10.1007/978-981-15-2063-1 · Cited by 243 · see citing works
Buckling studies of single human trabeculae
Townsend, P. R., Rose, R. M., & Radin, E. L. (1975) · Journal of Biomechanics · doi:10.1016/0021-9290(75)90025-1 · Cited by 192 · see citing works
A model of vertebral trabecular bone architecture and its mechanical properties
Jensen, K. S., Mosekilde, L., & Mosekilde, L. (1990) · Bone · doi:10.1016/8756-3282(90)90137-n · Cited by 180 · see citing works
Microstructure-microhardness relations in parallel-fibered and lamellar bone
Ziv, V., Wagner, H. D., & Weiner, S. (1996) · Bone · doi:10.1016/8756-3282(96)00049-x · Cited by 180 · see citing works
Wright, T. M., & Hayes, W. C. (1976) · Medical & Biological Engineering & Computing · doi:10.1007/bf02477046 · Cited by 177 · see citing works
Mechanical properties of trabecular bone. Dependency on strain rate
Linde, F., Nørgaard, P., Hvid, I., Odgaard, A., & Søballe, K. (1991) · Journal of Biomechanics · doi:10.1016/0021-9290(91)90305-7 · Cited by 171 · see citing works
Evans, G. P., Behiri, J. C., Currey, J. D., & Bonfield, W. (1990) · Journal of Materials Science Materials in Medicine · doi:10.1007/bf00705352 · Cited by 153 · see citing works
Hardness, Young's modulus and yield stress in mammalian mineralized tissues
Currey, J. D., & Brear, K. (1990) · Journal of Materials Science Materials in Medicine · doi:10.1007/bf00705348 · Cited by 150 · see citing works
Some viscoplastic characteristics of bovine and human cortical bone
Fondrk, M. T., Bahniuk, E., Davy, D. T., & Michaels, C. (1988) · Journal of Biomechanics · doi:10.1016/0021-9290(88)90200-x · Cited by 144 · see citing works
Ginebra, M., Rilliard, A., Fern�ndez, E., Elvira, C., Rom�n, J. S., & Planell, J. A. (2001) · Journal of Biomedical Materials Research · doi:10.1002/1097-4636(200110)57:1 · Cited by 138 · see citing works
Age-related differences in post-yield damage in human cortical bone. Experiment and model
Courtney, A. C., Hayes, W. C., & Gibson, L. J. (1996) · Journal of Biomechanics · doi:10.1016/0021-9290(96)84542-8 · Cited by 131 · see citing works
Age, gender, and bone lamellae elastic moduli
Hoffler, C. E., Moore, K. E., Kozloff, K. M., Zysset, P. K., & Goldstein, S. A. (2000) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100180315 · Cited by 129 · see citing works
Self-citationHardness, an indicator of the mechanical competence of cancellous bone
Hodgskinson, R., Currey, J. D., & Evans, G. P. (1989) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100070518 · Cited by 124 · see citing works
INVESTIGATIONS ON SOME PHYSICAL PROPERTIES OF BONE TISSUE
Amprino, R. (2008) · Acta Anatomica · doi:10.1159/000141381 · Cited by 118 · see citing works
The Microscopic Hardness of Bone
Weaver, J. K. (1966) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-196648020-00006 · Cited by 118 · see citing works
A 3D damage model for trabecular bone based on fabric tensors
Zysset, P. K., & Curnier, A. (1996) · Journal of Biomechanics · doi:10.1016/s0021-9290(96)80006-6 · Cited by 117 · see citing works
Self-citationTensile testing of rodlike trabeculae excised from bovine femoral bone
Ryan, S. D., & Williams, J. L. (1989) · Journal of Biomechanics · doi:10.1016/0021-9290(89)90049-3 · Cited by 112 · see citing works
Mechanical behavior of damaged trabecular bone
Keaveny, T. M., Wachtel, E. F., Guo, X.-D. E., & Hayes, W. C. (1994) · Journal of Biomechanics · doi:10.1016/0021-9290(94)90040-x · Cited by 110 · see citing works
Self-citationA Global Relationship Between Trabecular Bone Morphology and Homogenized Elastic Properties
Zysset, P. K., Goulet, R. W., & Hollister, S. J. (1998) · Journal of Biomechanical Engineering · doi:10.1115/1.2834756 · Cited by 105 · see citing works
Self-citationFinite Element Analysis of a Three-Dimensional Open-Celled Model for Trabecular Bone
Beaupré, G. S., & Hayes, W. C. (1985) · Journal of Biomechanical Engineering · doi:10.1115/1.3138550 · Cited by 104 · see citing works
A structural model for the mechanical behavior of trabecular bone
Pugh, J., Rose, R. M., & Radin, E. L. (1973) · Journal of Biomechanics · doi:10.1016/0021-9290(73)90022-5 · Cited by 101 · see citing works
Is there a role for bone quality in fragility fractures?
Heaney, R. P. (1993) · Calcified Tissue International · doi:10.1007/bf01673394 · Cited by 90 · see citing works
The limitations of canine trabecular bone as a model for human: A biomechanical study
Kuhn, J. L., Goldstein, S. A., Ciarelli, M. J., & Matthews, L. S. (1989) · Journal of Biomechanics · doi:10.1016/0021-9290(89)90032-8 · Cited by 88 · see citing works
Self-citationExperimental method for the measurement of the elastic modulus of trabecular bone tissue
Mente, P. L., & Lewis, J. L. (1989) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100070320 · Cited by 79 · see citing works
Is Trabecular Bone Tissue Different from Cortical Bone Tissue
Edward, G. X., & Goldstein, S. A. (1998) · Forma · Cited by 69 · see citing works
Self-citationMechanical properties of microcallus in human cancellous bone
Blackburn, J., Hodgskinson, R., Currey, J. D., & Mason, J. E. (1992) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100100211 · Cited by 67 · see citing works
The Micromechanics Versus the Macromechanics of Cortical Bone—A Comprehensive Presentation
Ascenzi, A. (1988) · Journal of Biomechanical Engineering · doi:10.1115/1.3108454 · Cited by 65 · see citing works
Experimental investigation of Poisson's ratio as a damage parameter for bone fatigue
Pidaparti, R. M., & Vogt, A. (2001) · Journal of Biomedical Materials Research · doi:10.1002/jbm.1243 · Cited by 48 · see citing works
Micro-hardness measurements on single haversian systems in bone
Carlström, D. (1954) · Cellular and Molecular Life Sciences · doi:10.1007/bf02157195 · Cited by 45 · see citing works
A study of turbulent combustion and its modeling using a diffusion reaction equation model
Girimaji, S. S. (1996) · International Journal of Engineering Science · doi:10.1016/0020-7225(95)00076-3 · Cited by 35 · see citing works
Runkle, J. C., & Pugh, J. (1975) · PubMed · Cited by 31 · see citing works
Human bone microstructure studied by collagenase etching
Mackie, I. G., Green, M., Clarke, H., & Isaac, D. (1989) · Journal of Bone and Joint Surgery - British Volume · doi:10.1302/0301-620x.71b3.2542341 · Cited by 11 · see citing works
Relationship Between Mechanical Properties and Structure in Secondary Bone
Ascenzi, A., BOYDE, A., Bianco, P., & Barbos, M. P. (1986) · Connective Tissue Research · doi:10.3109/03008208609001975 · Cited by 5 · see citing works
An investigation of the mechanical anisotropy of the alternately-structured osteons.
Ascenzi, A., & BONUCCI, E. (1977) · PubMed · Cited by 3 · see citing works
An investigation on the mechanical anisotropy of the alternatelystructured osteons
Ascenzi, A., BONUCCI, E., & Benvenuti, A. (1976) · Calcified Tissue International · doi:10.1007/bf02064158 · Cited by 3 · see citing works
Flagged first, then by citations
4 of the 61 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Bone Mechanical Properties in Healthy and Diseased States
Morgan, E. F., Unnikrisnan, G. U., & Hussein, A. I. (2018) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-062117-121139 · Cited by 1,026 · see citing works
“Although the nanoscale moduli appear higher than those at greater length scales (Table 1), this difference may be due to the fact that most nanoindentation measurements on bone are conducted under dry conditions (38).”
Biomechanics and Mechanobiology of Trabecular Bone: A Review
Oftadeh, R., Perez‐Viloria, M., Villa‐Camacho, J. C., Vaziri, A., & Nazarian, A. (2014) · Journal of Biomechanical Engineering · doi:10.1115/1.4029176 · Cited by 554 · see citing works
Uskoković, V., & Uskokovic, D. P. (2010) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.31746 · Cited by 540 · see citing works
Nanoindentation of biological materials
Ebenstein, D. M., & Pruitt, L. A. (2006) · Nano Today · doi:10.1016/s1748-0132(06)70077-9 · Cited by 479 · see citing works
Mirzaali, M. J., Schwiedrzik, J. J., Thaiwichai, S., Best, J. P., Michler, J., Zysset, P. K., & Wolfram, U. (2016) · Bone · doi:10.1016/j.bone.2015.11.018 · Cited by 325 · see citing works
Self-citationLewis, G., & Nyman, J. S. (2008) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.31092 · Cited by 165 · see citing works
Accretion of Bone Quantity and Quality in the Developing Mouse Skeleton
Miller, L. M., Little, W. C., Schirmer, A., Sheik, F., Busa, B., & Judex, S. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.070402 · Cited by 148 · see citing works
Nanoindentation of Biological and Biomimetic Materials
Oyen, M. L. (2011) · Experimental Techniques · doi:10.1111/j.1747-1567.2011.00716.x · Cited by 141 · see citing works
Wolfram, U., Wilke, H., & Zysset, P. K. (2009) · Bone · doi:10.1016/j.bone.2009.09.035 · Cited by 126 · see citing works
Self-citationInsight into differences in nanoindentation properties of bone
Rodríguez-Flórez, N., Oyen, M. L., & Shefelbine, S. J. (2012) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2012.11.005 · Cited by 124 · see citing works
Sihota, P., Yadav, R. N., Dhaliwal, R., Bose, J. C., Dhiman, V., Neradi, D., Karn, S., Sharma, S., Aggarwal, S., Goni, V. G., et al. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab027 · Cited by 122 · see citing works
Nano Hydroxyapatite-coated Implants Improve Bone Nanomechanical Properties
Jimbo, R., Coelho, P. G., Bryington, M. S., Baldassarri, M., Tovar, N., Currie, F., Hayashi, M. K., Janal, M. N., Andersson, M., Ono, D., et al. (2012) · Journal of Dental Research · doi:10.1177/0022034512463240 · Cited by 112 · see citing works
Zhang, J., Niebur, G. L., & Ovaert, T. C. (2007) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2007.09.019 · Cited by 109 · see citing works
Wolfram, U., Wilke, H., & Zysset, P. K. (2010) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2010.02.026 · Cited by 95 · see citing works
Self-citationIndentation of bone tissue: a short review
Zysset, P. K. (2009) · Osteoporosis International · doi:10.1007/s00198-009-0854-9 · Cited by 96 · see citing works
Self-citationElastic Anisotropy of Human Cortical Bone Secondary Osteons Measured by Nanoindentation
Franzoso, G., & Zysset, P. K. (2009) · Journal of Biomechanical Engineering · doi:10.1115/1.3005162 · Cited by 89 · see citing works
Self-citationBiomechanical Characteristics and Analysis Approaches of Bone and Bone Substitute Materials
Niu, Y., Du, T., & Liu, Y. (2023) · Journal of Functional Biomaterials · doi:10.3390/jfb14040212 · Cited by 91 · see citing works
Bala, Y., Dépalle, B., Douillard, T., Meille, S., Clément, P., Follet, H., Chevalier, J., & Boivin, G. (2011) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2011.05.017 · Cited by 87 · see citing works
Forouzesh, E., Goel, A. K., Mackenzie, S. A., & Turner, J. A. (2012) · The Plant Journal · doi:10.1111/tpj.12042 · Cited by 82 · see citing works
Validation of an anatomy specific finite element model of Colles’ fracture
Varga, P., Baumbach, S. F., Pahr, D. H., & Zysset, P. K. (2009) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2009.04.017 · Cited by 80 · see citing works
Self-citationForm and functional repair of long bone using 3D‐printed bioactive scaffolds
Tovar, N., Witek, L., Atria, P. J., Sobieraj, M. C., Bowers, M. M., Lopez, C. D., Cronstein, B. N., & Coelho, P. G. (2018) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2733 · Cited by 78 · see citing works
Hunt, H. B., & Donnelly, E. L. (2016) · Clinical Reviews in Bone and Mineral Metabolism · doi:10.1007/s12018-016-9222-4 · Cited by 77 · see citing works
Tjhia, C. K., Odvina, C. V., Rao, D. S., Stover, S. M., Wang, X., & Fyhrie, D. P. (2011) · Bone · doi:10.1016/j.bone.2011.09.042 · Cited by 76 · see citing works
Zhang, J., Michalenko, M. M., Ellen Kuhl, A., & Ovaert, T. C. (2009) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2009.08.001 · Cited by 74 · see citing works
Measuring the dynamic mechanical response of hydrated mouse bone by nanoindentation
Pathak, S., Swadener, J. G., Kalidindi, S. R., Courtland, H., Jepsen, K. J., & Goldman, H. M. (2010) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2010.09.002 · Cited by 72 · see citing works
Mechanical properties of porcine femoral cortical bone measured by nanoindentation
Feng, L., Chittenden, M., Schirer, J. P., Dickinson, M., & Jasiuk, I. (2012) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2012.05.001 · Cited by 69 · see citing works
Reisinger, A., Pahr, D. H., & Zysset, P. K. (2011) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2011.07.010 · Cited by 68 · see citing works
Self-citationBaldassarri, M., Bonfante, E. A., Suzuki, M., Marin, C., Granato, R., Tovar, N., & Coelho, P. G. (2012) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.32786 · Cited by 66 · see citing works
Granke, M., Coulmier, A., Uppuganti, S., Gaddy, J. A., Does, M. D., & Nyman, J. S. (2014) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2014.05.016 · Cited by 63 · see citing works
Milovanovic, P. D., Potočnik, J., Djonić, D., Nikolić, S., Živković, V., Djuric, M. P., & Rakočević, Z. L. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2011.11.011 · Cited by 63 · see citing works
Microtensile properties and failure mechanisms of cortical bone at the lamellar level
Casari, D., Michler, J., Zysset, P. K., & Schwiedrzik, J. J. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.04.030 · Cited by 61 · see citing works
Self-citationPradeep, N. B., Hegde, M. M. R., Shashanka, R., & Surendranathan, A. O. (2022) · Powder Technology · doi:10.1016/j.powtec.2022.117715 · Cited by 61 · see citing works
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Wang, X., Nyman, J. S., Dong, X., Leng, H., & Reyes, M. (2010) · Synthesis lectures on tissue engineering · doi:10.1007/978-3-031-02579-2 · Cited by 89 · see citing works
Multifunctional Calcium Phosphate Nanostructured Materials and Biomedical Applications
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A novel sample preparation method to avoid influence of embedding medium during nano-indentation
Meng, Y., Wang, S., Cai, Z., Young, T. M., Du, G., & Li, Y. (2012) · Applied Physics A · doi:10.1007/s00339-012-7123-z · Cited by 59 · see citing works
Chen, F., Huang, P., Qi, C., Lu, B., Zhao, X., Li, C., Wu, J. L., Cui, D., & Zhu, Y. (2014) · Journal of Materials Chemistry B · doi:10.1039/c4tb01193g · Cited by 58 · see citing works
Freitas, G. P., Lopes, H. B., Souza, A. T. P., de Oliveira, P. G. F. P., Almeida, A. L. G., de Souza, L. E. B., Coelho, P. G., Beloti, M. M., & Rosa, A. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-50067-6 · Cited by 59 · see citing works
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Direct comparison of nanoindentation and macroscopic measurements of bone viscoelasticity
Shepherd, T. N., Zhang, J., Ovaert, T. C., Roeder, R. K., & Niebur, G. L. (2011) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2011.07.004 · Cited by 56 · see citing works
Zhou, R., Xu, W. L., Chen, F., Qi, C., Lu, B., Zhang, H., Wu, J. L., Qian, Q., & Zhu, Y. (2014) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2014.09.021 · Cited by 51 · see citing works
Fundamental Biomechanics in Bone Tissue Engineering
Wang, X., Nyman, J. S., Dong, X., Leng, H., & Reyes, M. (2010) · Synthesis lectures on tissue engineering · doi:10.2200/s00246ed1v01y200912tis004 · Cited by 51 · see citing works
Finite Element Modeling of Microcrack Growth in Cortical Bone
Mischinski, S., & Ural, A. (2011) · Journal of Applied Mechanics · doi:10.1115/1.4003754 · Cited by 51 · see citing works
Caeiro, J. R., González, P., & Guede, D. (2013) · Revista de Osteoporosis y Metabolismo Mineral · doi:10.4321/s1889-836x2013000200007 · Cited by 50 · see citing works
Coelho, P. G., Takayama, T., Yoo, D. Y., Jimbo, R., Karunagaran, S., Tovar, N., Janal, M. N., & Yamano, S. (2014) · Bone · doi:10.1016/j.bone.2014.05.004 · Cited by 49 · see citing works
Co-administration of Antiresorptive and Anabolic Agents: A Missed Opportunity
Seeman, E., & Martin, T. J. (2015) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2496 · Cited by 48 · see citing works
Bone properties by nanoindentation in mild and severe osteogenesis imperfecta
Albert, C., Jameson, J., Toth, J. M., Smith, P. A., & Harris, G. E. (2012) · Clinical Biomechanics · doi:10.1016/j.clinbiomech.2012.10.003 · Cited by 48 · see citing works
Compositional and mechanical properties of growing cortical bone tissue: a study of the human fibula
Lefèvre, E., Farlay, D., Bala, Y., Subtil, F., Wolfram, U., Rizzo, S., Baron, C., Zysset, P. K., Pithioux, M., & Follet, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-54016-1 · Cited by 49 · see citing works
Self-citationBaron, C., Talmant, M., & Laugier, P. (2007) · The Journal of the Acoustical Society of America · doi:10.1121/1.2759165 · Cited by 48 · see citing works
Paietta, R. C., Campbell, S. E., & Ferguson, V. L. (2010) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2010.10.008 · Cited by 47 · see citing works
Shahnazari, M., Yao, W., Dai, W., Wang, B., Ionova-Martin, S. S., Ritchie, R. O., Heeren, D., Burghardt, A. J., Nicolella, D. P., Kimiecik, M. G., et al. (2010) · Bone · doi:10.1016/j.bone.2009.11.019 · Cited by 46 · see citing works
Remache, D., Semaan, M., Rossi, J.-M., Pithioux, M., & Milan, J. (2019) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2019.103426 · Cited by 46 · see citing works
Chen, F., Zhu, Y., Zhao, X., Lu, B., & Wu, J. L. (2013) · CrystEngComm · doi:10.1039/c3ce40115d · Cited by 45 · see citing works
Bone properties surrounding hydroxyapatite‐coated custom osseous integrated dental implants
Baker, M. I., Eberhardt, A. W., Martin, D. M., McGwin, G., & Lemons, J. E. (2010) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.31693 · Cited by 45 · see citing works
Nanoindentation of the insertional zones of human meniscal attachments into underlying bone
Hauch, K., Oyen, M. L., Odegard, G. M., & Donahue, T. L. H. (2008) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2008.10.005 · Cited by 45 · see citing works
Multi-level femoral morphology and mechanical properties of rats of different ages
Zhang, R., Gong, H., Zhu, D., Ma, R., Fang, J., & Fan, Y. (2015) · Bone · doi:10.1016/j.bone.2015.03.022 · Cited by 43 · see citing works
Nanostructured Calcium Phosphates: Preparation and Their Application in Biomedicine
Chen, F., Zhu, Y., Wu, J. L., Huang, P., & Cui, D. (2012) · Nano Biomedicine and Engineering · doi:10.5101/nbe.v4i1.p41-49 · Cited by 41 · see citing works
Kim, D., Huja, S. S., Lee, H. R., Tee, B. C., & Hueni, S. E. (2010) · Journal of Biomechanical Engineering · doi:10.1115/1.4000936 · Cited by 41 · see citing works
Chavassieux, P., & Chapurlat, R. D. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.907914 · Cited by 45 · see citing works
Reduced tissue hardness of trabecular bone is associated with severe osteoarthritis
Dall’Ara, E., Öhman‐Mägi, C., Baleani, M., & Viceconti, M. (2011) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2010.12.022 · Cited by 40 · see citing works
Evolution of load transfer between hydroxyapatite and collagen during creep deformation of bone
Deymier-Black, A. C., Yuan, F., Singhal, A., Almer, J., Brinson, L. C., & Dunand, D. C. (2011) · Acta Biomaterialia · doi:10.1016/j.actbio.2011.08.014 · Cited by 40 · see citing works
Nanoindentation analysis of the micromechanical anisotropy in mouse cortical bone
Casanova, M., Balmelli, A., Carnelli, D., Courty, D., Schneider, P., & Müller, R. (2017) · Royal Society Open Science · doi:10.1098/rsos.160971 · Cited by 40 · see citing works
Albert, C. I., Jameson, J., & Harris, G. F. (2012) · Proceedings of the Institution of Mechanical Engineers Part H Journal of Engineering in Medicine · doi:10.1177/0954411912463868 · Cited by 40 · see citing works
Albert, C., Jameson, J., Smith, P. A., & Harris, G. E. (2014) · Bone · doi:10.1016/j.bone.2014.05.022 · Cited by 39 · see citing works
Mechanical Property Assessment of Bone Healing around a Titanium–Zirconium Alloy Dental Implant
Anchieta, R. B., Baldassarri, M., Guastaldi, F. P. S., Tovar, N., Janal, M. N., Gottlow, J., Dard, M. M., Jimbo, R., & Coelho, P. G. (2013) · Clinical Implant Dentistry and Related Research · doi:10.1111/cid.12061 · Cited by 38 · see citing works
Ferguson, V. L. (2009) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2009.01.004 · Cited by 38 · see citing works
Pathak, S., Vachhani, S. J., Jepsen, K. J., Goldman, H. M., & Kalidindi, S. R. (2012) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2012.03.018 · Cited by 38 · see citing works
A methodological framework for nanomechanical characterization of soft biomaterials and polymers
Arevalo, S. E., Ebenstein, D. M., & Pruitt, L. A. (2022) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2022.105384 · Cited by 37 · see citing works
Effect of guided bone regeneration on bone quality surrounding dental implants
Johnson, T. B., Siderits, B., Nye, S., Jeong, Y., Han, S., Rhyu, I.-C., Han, J., Deguchi, T., Beck, F. M., & Kim, D. (2018) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2018.08.011 · Cited by 37 · see citing works
Shang, H.-B., Chen, F., Wu, J. L., Qi, C., Lu, B., Chen, X., & Zhu, Y. (2014) · RSC Advances · doi:10.1039/c4ra09902h · Cited by 36 · see citing works
Wang, X., Rao, D. S., Ajdelsztajn, L., Ciarelli, T. E., Lavernia, E. J., & Fyhrie, D. P. (2007) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.30918 · Cited by 36 · see citing works
Jimbo, R., Anchieta, R. B., Baldassarri, M., Granato, R., Marin, C., Teixeira, H. S., Tovar, N., Vandeweghe, S., Janal, M. N., & Coelho, P. G. (2013) · Implant Dentistry · doi:10.1097/id.0b013e31829f1f4b · Cited by 35 · see citing works
Wang, X., Allen, M. R., Burr, D. B., Lavernia, E. J., Jeremić, B., & Fyhrie, D. P. (2008) · Bone · doi:10.1016/j.bone.2008.05.023 · Cited by 35 · see citing works
Tjhia, C. K., Stover, S. M., Rao, D. S., Odvina, C. V., & Fyhrie, D. P. (2012) · Bone · doi:10.1016/j.bone.2012.04.010 · Cited by 34 · see citing works
Lekkala, S., Sacher, S. E., Taylor, E. A., Williams, R. M., Moseley, K. F., & Donnelly, E. L. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4757 · Cited by 34 · see citing works
Bertinetti, L., Hangen, U. D., Eder, M., Leibner, P., Fratzl, P., & Zlotnikov, I. (2014) · The Philosophical Magazine A Journal of Theoretical Experimental and Applied Physics · doi:10.1080/14786435.2014.920544 · Cited by 34 · see citing works
Vennin, S., Desyatova, A. S., Turner, J. A., Watson, P. A., Lappe, J. M., Recker, R. R., & Akhter, M. P. (2017) · Bone · doi:10.1016/j.bone.2017.01.031 · Cited by 33 · see citing works
Lievers, W. B., Poljsak, A. S., Waldman, S. D., & Pilkey, A. K. (2010) · Medical Engineering & Physics · doi:10.1016/j.medengphy.2010.06.001 · Cited by 32 · see citing works
Ciarelli, T. E., Tjhia, C. K., Rao, D. S., Qiu, S., PARFITT, A. M., & Fyhrie, D. P. (2009) · Bone · doi:10.1016/j.bone.2009.07.002 · Cited by 31 · see citing works
Influence of SEM vacuum on bone micromechanics using in situ AFM
Jiménez‐Palomar, I., Shipov, A., Shahar, R., & Barber, A. H. (2011) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2011.08.018 · Cited by 30 · see citing works
Galloway, K. A., & Porter, M. E. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.197905 · Cited by 29 · see citing works
Methods and interpretation of performance studies for dental implants
Dard, M. M. (2012) · Elsevier eBooks · doi:10.1533/9780857096456.3.308 · Cited by 27 · see citing works
Measurement of mechanical properties of multilayer waterborne coatings on wood by nanoindentation
Wu, Y., Wu, J., Wang, S., Feng, X., Chen, H., Tang, Q., & Zhang, H. (2019) · Holzforschung · doi:10.1515/hf-2018-0193 · Cited by 26 · see citing works
The in vivo effect of P‐15 coating on early osseointegration
Coelho, P. G., Teixeira, H. S., Marin, C., Witek, L., Tovar, N., Janal, M. N., & Jimbo, R. (2013) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33020 · Cited by 26 · see citing works
An experimentally validated micromechanical model of a rat vertebra under compressive loading
Tsafnat, N., & Wroe, S. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01289.x · Cited by 26 · see citing works
Hierarchically Structured Vanadium Pentoxide–Polymer Hybrid Materials
Tritschler, U., Zlotnikov, I., Zaslansky, P., Fratzl, P., Schlaad, H., & Cölfen, H. (2014) · ACS Nano · doi:10.1021/nn501153u · Cited by 25 · see citing works
Nanoindentation characterization of the cement lines in ovine and bovine femurs
Montalbano, T. J., & Feng, G. (2011) · Journal of materials research/Pratt's guide to venture capital sources · doi:10.1557/jmr.2011.46 · Cited by 25 · see citing works
Lievers, W. B., Lee, V., Arsenault, S. M., Waldman, S. D., & Pilkey, A. K. (2006) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2006.09.002 · Cited by 25 · see citing works
Spines of the porcupine fish: Structure, composition, and mechanical properties
Su, F. Y., Bushong, E. A., Deerinck, T. J., Seo, K., Herrera, S. A., Graeve, O. A., Kisailus, D., Lubarda, V. A., & McKittrick, J. M. (2017) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2017.02.029 · Cited by 24 · see citing works
Schwiedrzik, J. J., & Zysset, P. K. (2013) · Computer Methods in Biomechanics & Biomedical Engineering · doi:10.1080/10255842.2013.818665 · Cited by 23 · see citing works
Self-citationPawlikowski, M., Skalski, K., Bańczerowski, J., Makuch, A., & Jankowski, K. (2017) · Journal of Applied Biomedicine · doi:10.1016/j.bbe.2017.01.002 · Cited by 23 · see citing works
Bordin, D., Coelho, P. G., Bergamo, E. T. P., Bonfante, E. A., Witek, L., & Cury, A. A. D. B. (2018) · Dental Materials · doi:10.1016/j.dental.2018.03.005 · Cited by 22 · see citing works
Evaluating Anisotropic Properties in the Porcine Temporomandibular Joint Disc Using Nanoindentation
Yuya, P. A., Amborn, E. K., Beatty, M. W., & Turner, J. A. (2010) · Annals of Biomedical Engineering · doi:10.1007/s10439-010-9967-8 · Cited by 22 · see citing works
Freitas, G. P., Lopes, H. B., Souza, A. T. P., de Oliveira, P. G. F. P., Almeida, A. L. G., Coelho, P. G., Ferreira, F. U., Covas, D. T., Beloti, M. M., & Rosa, A. L. (2019) · Regenerative Medicine · doi:10.2217/rme-2019-0036 · Cited by 22 · see citing works
Determination of Bone's Mechanical Matrix Properties by Nanoindentation
Özçivici, E., Ferreri, S. L., Qin, Y., & Judex, S. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-104-8_22 · Cited by 22 · see citing works
(2022) · Biointerface Research in Applied Chemistry · doi:10.33263/briac132.118 · Cited by 21 · see citing works
Granke, M., Grimal, Q., Parnell, W. J., Raum, K., Gerisch, A., Peyrin, F., Saı̈ed, A., & Laugier, P. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.10.011 · Cited by 21 · see citing works
Moghaddam, A. O., Arshee, M. R., Lin, Z., Sivaguru, M., Phillips, H., McFarlin, B. L., Toussaint, K. C., & Johnson, A. J. W. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2023.01.005 · Cited by 20 · see citing works
Kim, D., Kwon, H.-J., Jeong, Y.-H., Kosel, E., Lee, D. J., Han, J., Kim, D., & Kim, D. (2016) · Clinical Oral Investigations · doi:10.1007/s00784-016-1734-2 · Cited by 20 · see citing works
Numerical modeling of bone as a multiscale poroelastic material by the homogenization technique
Perrin, E., Bou‐Saïd, B., & Massi, F. (2018) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2018.12.015 · Cited by 20 · see citing works
DeMitchell-Rodriguez, E. M., Shen, C., Nayak, V. V., Tovar, N., Witek, L., Torroni, A., Yarholar, L. M., Cronstein, B. N., Flores, R. L., & Coelho, P. G. (2023) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000010258 · Cited by 19 · see citing works
- Authors
- Hoffler, C. E., Guo, X. E., Zysset, P. K., & Goldstein, S. A.
- Affiliations
- University of Michigan (US)
- Orthopaedic Research Laboratories, Orthopaedic Surgery, The University of Michigan, Ann Arbor, MI 48109-0486
- Venue
- Journal of Biomechanical Engineering
- Publisher
- ASME International
- Published
- 2005-08-01
- Volume
- 127
- Issue
- 7
- Pages
- 1046-1053
- ISSN
- 0148-0731 (ISSN-L)
- 1528-8951
- OpenAlex
- W1999426010
- Cited by
- 222
- References
- 61
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 7 · 2023: 11 · 2022: 11 · 2021: 4 · 2020: 12 · 2019: 15 · 2018: 12 · 2017: 9 · 2016: 12 · 2015: 8 · 2014: 15 · 2013: 15 · 2012: 15
- FWCI
- 11.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Biomechanical Engineering (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ar034399-12, 1f32ar008338-01a1)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR34399, AR08338)
- Topics
- Physical Sciences › Engineering › Mechanics of Materials › Metal and Thin Film Mechanics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- nanoindentation, bone lamellae, cortical bone, elastic modulus, hardness, osteons, specimen preparation, indentation depth, loading rate, bone mechanical properties
- MeSH terms
- Aged, Aged, 80 and over, Bone and Bones, Cadaver, Elasticity, Female, Hardness, Hardness Tests, Humans, Male, Middle Aged, Physical Stimulation, Sensitivity and Specificity, Stress, Mechanical, Reproducibility of Results, Weight-Bearing, Anisotropy, Compressive Strength, Nanotechnology, In Vitro Techniques
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