Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents

Novitskaya, Ekaterina; Chen, Po-Yu; Lee, Steve; Castro-Ceseña, Ana; Hirata, Gustavo; Lubarda, Vlado A.; McKittrick, Joanna

Affiliations

¹Materials Science and Engineering Program, University of California, San Diegoa, La Jolla, CA 92093, USA

²Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada, Mexico

³Centro de Nanociencias y Nanotecnologia, UNAM, Ensenada, Mexico

⁴Department of Mechanical and Aerospace Engineering, University of California, San Diegoa, La Jolla, CA 92093, USA

Abstract and keywords

The mechanical properties of fully demineralized, fully deproteinized and untreated cortical bovine femur bone were investigated by compression testing in three anatomical directions (longitudinal, radial and transverse). The weighted sum of the stress–strain curves of the treated bones was far lower than that of the untreated bone, indicating a strong molecular and/or mechanical interaction between the collagen matrix and the mineral phase. Demineralization and deproteinization of the bone demonstrated that contiguous, stand-alone structures result, showing that bone can be considered an interpenetrating composite material. Structural features of the samples from all groups were studied by optical and scanning electron microscopy. Anisotropic mechanical properties were observed: the radial direction was found to be the strongest for untreated bone, while the longitudinal one was found to be the strongest for deproteinized and demineralized bones. A possible explanation for this phenomenon is the difference in bone microstructure in the radial and longitudinal directions.

Keywords: Anisotropy; Cortical bone; Compression; Demineralization; Deproteinization

Links

DOI: 10.1016/j.actbio.2011.04.025

PubMed: 21571104

WoS: 000293259500018

History

Received: 2011-02-10

Revised: 2011-04-26

Accepted: 2011-04-26

Online: 2011-04-30

Cited Works (25)

Year	Entry
1976	Wainwright SA, Biggs WD, Currey JD, Gosline JM. Mechanical Design in Organisms. London, UK: Edward Arnold; 1976.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
1996	Landis WJ, Hodgens KJ, Arena J, Song MJ, McEwen BF. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc Res Tech. 1996;33(2):192-202.
1996	Martin RB, Lau ST, Mathews PV, Gibson VA, Stover SM. Collagen fiber organization is related to mechanical properties and remodeling in equine bone: a comparsion of two methods. J Biomech. December 1996;29(12):1515-1521.
2011	Chen P-Y, Toroian D, Price PA, McKittrick J. Minerals form a continuum phase in mature cancellous bone. Calcif Tiss Int. May 2011;88(5):351-361.
2011	Chen P-Y, McKittrick J. Compressive mechanical properties of demineralized and deproteinized cancellous bone. J Mech Behav Biomed Mater. October 2011;4(7):961-973.
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.
1977	Bonfield W, Grynpas MD. Anisotropy of the Young's modulus of bone. Nature. December 1, 1977;270:453-454.
2004	Iyo T, Maki Y, Sasaki N, Nakata M. Anisotropic viscoelastic properties of cortical bone. J Biomech. September 2004;37(9):1433-1437.
1995	Broz JJ, Simske SJ, Greenberg AR. Material and compositional properties of selectively demineralized cortical bone. J Biomech. November 1995;28(11):1357-1368.
1973	Piekarski K. Analysis of bone as a composite material. Int J Eng Sci. June 1973;11(6):557-565.
2009	Currey J. Measurement of the mechanical properties of bone: a recent history. Clin Orthop Relat Res. August 2009;467(8):1948-1954.
1974	Reilly DT, Burstein AH. The mechanical properties of cortical bone. J Bone Joint Surg. 1974;56A(5):1001-1022.
1993	Martin RB, Boardman DL. The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J Biomech. September 1993;26(9):1047-1054.
1975	Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech. 1975;8(6):393-405.
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.
2002	Benezra Rosen V, Hobbs LW, Spector M. The ultrastructure of anorganic bovine bone and selected synthetic hyroxyapatites used as bone graft substitute materials. Biomaterials. February 2002;23(3):921-928.
2007	Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, Douglas EP, Gower LB. Bone structure and formation: a new perspective. Mater Sci Eng R Rep. November 28, 2007;58(3-5):77-116.
1994	Hasegawa K, Turner CH, Burr DB. Contribution of collagen and mineral to the elastic anisotropy of bone. Calcif Tiss Int. November 1994;55(5):381-386.
1996	Rho J-Y. An ultrasonic method for measuring the elastic properties of human tibial cortical and cancellous bone. Ultrasonics. December 1996;34(8):777-783.
1975	Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg. October 1975;57A(7):956-961.
1970	Currey JD. The mechanical properties of bone. Clin Orthop Relat Res. November–December 1970;73:210-231.
1951	Weibull W. A statistical distribution function of wide applicability. J Appl Mech. 1951;18(3):293-297.
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.
1998	Rho J-Y, Kuhn-Spearing L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998;20(2):92-102.

Cited By (18)

Year	Entry
2018	Xie S, Wallace RJ, Callanan A, Pankaj P. From tension to compression: asymmetric mechanical behaviour of trabecular bone’s organic phase. Ann Biomed Eng. June 2018;46(6):801-809.
2014	Li S, Abdel-Wahab A, Demirci E, Silberschmidt VV. Penetration of cutting tool into cortical bone: experimental and numerical investigation of anisotropic mechanical behaviour. J Biomech. March 21, 2014;47(5):1117-1126.
2013	Li S, Demirci E, Silberschmidt VV. Variability and anisotropy of mechanical behavior of cortical bone in tension and compression. J Mech Behav Biomed Mater. May 2013;21:109-120.
2020	Xie S, Wallace RJ, Pankaj P. Time-dependent behaviour of demineralised trabecular bone: experimental investigation and development of a constitutive model. J Mech Behav Biomed Mater. September 2020;109:103751.
2020	Lovrenić-Jugović M, Tonković Z, Skozrit I. Experimental and numerical investigation of cyclic creep and recovery behavior of bovine cortical bone. Mech Mater. July 2020;146:103407.
2019	Yassine RA, Hamade RF. Transversely isotropic and isotropic material considerations in determining the mechanical response of geometrically accurate bovine tibia bone. Med Biol Eng Comput. October 2019;57(10):2159-2178.
2019	Tertuliano OA. Small-Scale Deformation and Fracture of Hard Biomaterials [PhD thesis]. Pasadena, CA: California Institute of Technology; 2019.
2018	Xie S. Characterisation of Time-Dependent Mechanical Behaviour of Trabecular Bone and Its Constituents [PhD thesis]. Edinburgh, Scotland: University of Edinburgh; 2018.
2015	Allen AB. Modulation of Stem Cell Delivery Strategy by Platelet Lysate Utilization and Cell Aggregation for Enhanced Bone Regeneration [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2015.
2012	Hamed E. Multiscale Modeling of Elastic Moduli and Strength of Bone [PhD thesis]. University of Illinois at Urbana-Champaign; 2012.
2013	Li S. Cutting of Cortical Bone Tissue: Analysis of Deformation and Fracture Process [PhD thesis]. Loughborough University; June 2013.
2019	Persons AK. Finite Element Analysis of the Mechanisms of Impact Mitigation Inherent to the North American Bison (Bison Bison) Skull [Master's thesis]. Mississippi State University; December 2019.
2020	Lamprecht A. Effect of Osmotic Pressure on the Viscoelastic Properties of Cortical Bone [Master's thesis]. Vienna University of Technology; 2020.
2012	Evdokimenko E. Investigation Into Mechanical Properties of Bone and Its Main Constituents [PhD thesis]. San Diego (UCSD), University of California; 2012.
2019	Jung J-Y. Learning from Nature: An Investigation of an Impact-Resistant System on the Woodpecker Head as a Non-Traumatic Brain Injury Animal Model [PhD thesis]. San Siego, CA: University of California San Diego; 2019.
2021	Muraro P. Biomechanical Characterization of Fibrolamellar Bone Using Nano-Scale Modulus Mapping [Master's thesis]. Liège, Belgique: Université de Liège; 2021.
2024	Qalaj P. Finite Element Analysis of Nanoindentation Across Bone Interfaces and Effects on the Measured Mechanical Properties [Master's thesis]. Liège, Belgique: Université de Liège; 2024.
2020	Amromanoh OA. An Experimental Study of the Effect of Bone Inorganic-Organic Composition on the Mechanical Properties [Master's thesis]. Winnipeg, MB: University of Manitoba; April 2020.