Mechanical properties of porcine femoral cortical bone measured by nanoindentation

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Feng, Liang¹; Chittenden, Michael¹; Schirer, Jeffrey³; Dickinson, Michelle⁴; Jasiuk, Iwona^1,2

Mechanical properties of porcine femoral cortical bone measured by nanoindentation

J Biomech. June 26, 2012;45(10):1775-1782

©2012 Elsevier Ltd. All rights reserved.

Affiliations

¹Department of Mechanical Science and Engineering, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA

²Department of Bioengineering, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA

³Hysitron Inc., 9625 West 76th Street, Minneapolis, MN 55344, USA

⁴Department of Chemical and Materials Engineering, University of Auckland, 92019 Auckland, New Zealand
Abstract and keywords

This study uses a nanoindentation technique to examine variations in the local mechanical properties of porcine femoral cortical bone under hydrated conditions. Bone specimens from three age groups (6, 12 and 42 months), representing developing bone, ranging from young to mature animals, were tested on the longitudinal and transverse cross-sectional surfaces. Elastic modulus and hardness of individual lamellae within bone's microstructure: laminar bone, interstitial bone, and osteons, were measured. Both the elastic modulus and hardness increased with age. However, the magnitudes of these increases were different for each microstructural component. The longitudinal moduli were higher than the transverse moduli. Dehydrated samples were also tested to allow a comparison with hydrated samples and these resulted in higher moduli and hardness than the hydrated samples. Ag+++ MAain, the degree of variation was different for each microstructural component. These results indicate that the developmental changes in bone have different rates of mechanical change within each microstructural component.

Keywords: Nanoindentation; Cortical bone; Elastic moduli; Hardness; Age; Laminar bone; Interstitial lamellae; Osteons
Links

DOI: 10.1016/j.jbiomech.2012.05.001

PubMed: 22648144

WoS: 000306451800004
History

Accepted: 2012-05-1

Online: 2012-05-28

Cited Works (46)

Year	Entry
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.
1999	Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech. October 1999;32(10):1005-1012.
1993	Riggs CM, Lanyon LE, Boyde A. Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius. Anat Embryol. March 1993;187(3):231-238.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
1996	Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffins LV. Osteonal structure in the equine third metacarpus. Bone. February 1996;18(2):165-171.
2006	Gupta HS, Stachewicz U, Wagermaier W, Roschger P, Wagner HD, Fratzl P. Mechanical modulation at the lamellar level in osteonal bone. J Mater Res. August 2006;21(8):1913-1921.
2006	Bembey AK, Bushby AJ, Boyde A, Ferguson VL, Oyen ML. Hydration effects on the micro-mechanical properties of bone. J Mater Res. August 2006;21(8):1962-1968.
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.
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.
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.
1969	Currey JD. The relationship between the stiffness and the mineral content of bone. J Biomech. October 1969;2(4):477-480.
2003	Hengsberger S, Enstroem J, Peyrin F, Zysset P. How is the indentation modulus of bone tissue related to its macroscopic elastic response? a validation study. J Biomech. October 2003;36(10):1503-1509.
2011	Reisinger AG, Pahr DH, Zysset PK. Elastic anisotropy of bone lamellae as a function of fibril orientation pattern. Biomech Model Mechanobiol. February 2011;10(1):67-77.
2006	Ascenzi M-G, Lomovtsev A. Collagen orientation patterns in human secondary osteons, quantified in the radial direction by confocal microscopy. J Struct Biol. January 2006;153(1):14-30.
2010	Zhang J, Michalenko MM, Kuhl E, Ovaert TC. Characterization of indentation response and stiffness reduction of bone using a continuum damage model. J Mech Behav Biomed Mater. February 2010;3(2):189-202.
2010	Donnelly E, Boskey AL, Baker SP, van der Meulen MCH. Effects of tissue age on bone tissue material compositionand nanomechanical properties in the rat cortex. J Biomed Mater Res. March 1, 2010;A92(3):1048-1056.
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.
1994	Heřt J, Fiala P, Petrtýl M. Osteon orientation of the diaphysis of the long bones in man. Bone. May–June 1994;15(3):269-277.
1969	Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. March 1969;2(1):1-11.
1996	Petrtýl M, Heřt J, Fiala P. Spatial organization of the haversian bone in man. J Biomech. February 1996;29(2):161-169.
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.
2000	Hoffler CE, Moore KE, Kozloff K, Zysset PK, Brown MB, Goldstein SA. Heterogeneity of bone lamellar-level elastic moduli. Bone. June 2000;26(6):603-609.
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.
1999	Rho J-Y, Pharr GM. Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J Mater Sci Mater Med. 1999;10(8):485-488.
2006	Bembey AK, Oyen ML, Bushby AJ, Boyde A. Viscoelastic properties of bone as a function of hydration state determined by nanoindentation. Philos Mag. November 21–December 11, 2006;86(33-35):5691-5703.
2008	Zhang J, Niebur GL, Ovaert TC. Mechanical property determination of bone through nano- and micro-indentation testing and finite element simulation. J Biomech. 2008;41(2):267-275.
2010	Lievers WB, Poljsak AS, Waldman SD, Pilkey AK. Effects of dehydration-induced structural and material changes on the apparent modulus of cancellous bone. Med Eng Phys. 2010;32(8):921-925.
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.
2000	Hoffler CE, Moore KE, Kozloff K, Zysset PK, Goldstein SA. Age, gender, and bone lamellae elastic moduli. J Orthop Res. May 2000;18(3):432-437.
2011	Zebaze RMD, Jones AC, Pandy MG, Knackstedt MA, Seeman E. Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties. Bone. June 1, 2011;48(6):1246-1251.
2005	Ager JW III, Nalla RK, Breeden KL, Ritchie RO. Deep-ultraviolet Raman spectroscopy study of the effect of aging on human cortical bone. J Biomed Opt. May–June 2005;10(3):034012.
2010	Hamed E, Lee Y, Jasiuk I. Multiscale modeling of elastic properties of cortical bone. Acta Mech. August 2010;213(1):131-154.
2011	Willems NMBK, Mulder L, Bank RA, Grünheid T, Toonder JMJd, Zentner A, Langenbach GEJ. Determination of the relationship between collagen cross-links and the bone–tissue stiffness in the porcine mandibular condyle. J Biomech. April 7, 2011;44(6):1132-1136.
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.
2011	Feng L, Jasiuk I. Multi-scale characterization of swine femoral cortical bone. J Biomech. January 11, 2011;44(2):313-320.
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.
2006	Oyen ML. Nanoindentation hardness of mineralized tissues. J Biomech. 2006;39(14):2699-2702.
1992	Oliver WC, Pharr GM. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res. 1992;7(6):1564-1583.
2005	Gupta HS, Schratter S, Tesch W, Roschger P, Berzlanovich A, Schoeberl T, Klaushofer K, Fratzl P. Two different correlations between nanoindentation modulus and mineral content in the bone–cartilage interface. J Struct Biol. February 2005;149(2):138-148.
1971	Katz JL. Hard tissue as a composite material, I: bounds on the elastic behavior. J Biomech. October 1971;4(5):455-473.
2009	Franzoso G, Zysset PK. Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. J Biomech Eng. February 2009;131(2):021001.
1997	Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials. 1997;18(20):1325-1330.
1993	Marotti G. A new theory of bone lamellation. Calcif Tiss Int. February 1993;53(suppl 1):S47-S56.
1993	McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone: the relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg. 1993;75A(8):1193-1205.
2002	Rho JY, Zioupos P, Currey JD, Pharr GM. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J Biomech. February 2002;35(2):189-198.
1999	Rho J-Y, Roy ME II, Tsui TY, Pharr GM. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res. 1999;A45(1):48-54.

Cited By (17)

Year	Entry
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.
2022	Rux CJ, Vahidi G, Darabi A, Cox LM, Heveran CM. Perilacunar bone tissue exhibits sub-micrometer modulus gradation which depends on the recency of osteocyte bone formation in both young adult and early-old-age female C57Bl/6 mice. Bone. April 2022;157:116327.
2015	Granke M, Does MD, Nyman JS. The role of water compartments in the material properties of cortical bone. Calcif Tiss Int. September 2015;97(3):292-307.
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.
2014	Faingold A, Cohen SR, Shahar R, Weiner S, Rapoport L, Wagner HD. The effect of hydration on mechanical anisotropy, topography and fibril organization of the osteonal lamellae. J Biomech. January 22, 2014;47(2):367-372.
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.
2015	Chittenden M, Najafi AR, Li J, Jasiuk I. Nanoindentation and ash content study of age dependent changes in porcine cortical bone. J Mech Med Biol. October 2015;15(5):1550074.
2017	Costa MC, Tozzi G, Cristofolini L, Danesi V, Viceconti M, Dall’Ara E. Micro finite element models of the vertebral body: validation of local displacement predictions. PLoS One. July 11, 2017;12(7):e0180151.
2017	Bakalova LP. Relating Cortical Bone Mechanics to Intracortical Pore Morphology, Distribution and Remodeling History Within the Fibula Diaphysis [Master's thesis]. Urbana, IL: University of Illinois at Urbana-Champaign; 2017.
2015	Rodriguez-Florez N. Mechanics of Cortical Bone: Exploring the Micro- and Nano-Scale [PhD thesis]. Imperial College London; January 2015.
2020	Bennison MBL. The Role of Cancellous Bone Architecture in Misalignment and Side Effect Errors [Master's thesis]. Sudbury, ON: Laurentian University; 2020.
2022	Cook TH. A Mechanical and Finite Element Analysis of Bone Screw Thread Design [Master's thesis]. Mississippi State University; August 2022.
2018	Costa MC. Prediction of the Risk of Vertebral Fracture in Patients With Metastatic Bone Lesions as a Tool for More Effective Patients’ Management [PhD thesis]. University of Sheffield; November 2018.
2021	Muraro P. Biomechanical Characterization of Fibrolamellar Bone Using Nano-Scale Modulus Mapping [Master's thesis]. Liège, Belgique: Université de Liège; 2021.
2020	Singleton RC. A Study of Aging in Male Cortical Bone Using Nanoindentation [PhD thesis]. Knoxville, University of Tennessee; August 2020.
2017	Tilak K. Finite Element Simulation of Nanoindentation in Lamellar Bone Composites [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; May 2017.
2013	Faingold A. Bone Elementary Units: Mechanical Properties and Structure [PhD thesis]. Weizmann Institute of Science; February 2013.