Abstract
Ageing societies suffer from an increasing incidence of bone fractures. Bone strength depends on the amount of mineral measured by clinical densitometry, but also on the micromechanical properties of the hierarchical organization of bone. Here, we investigate the mechanical response under monotonic and cyclic compression of both single osteonal lamellae and macroscopic samples containing numerous osteons. Micropillar compression tests in a scanning electron microscope, microindentation and macroscopic compression tests were performed on dry ovine bone to identify the elastic modulus, yield stress, plastic deformation, damage accumulation and failure mechanisms. We found that isolated lamellae exhibit a plastic behaviour, with higher yield stress and ductility but no damage. In agreement with a proposed rheological model, these experiments illustrate a transition from a ductile mechanical behaviour of bone at the microscale to a quasi-brittle response driven by the growth of cracks along interfaces or in the vicinity of pores at the macroscale.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
In situ micropillar compression of an anisotropic metal-organic framework single crystal
Communications Chemistry Open Access 04 April 2023
-
Multiscale mechanical consequences of ocean acidification for cold-water corals
Scientific Reports Open Access 16 May 2022
-
Aggravated stress fluctuation and mechanical size effects of nanoscale lamellar bone pillars
NPG Asia Materials Open Access 03 September 2021
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout





References
Fratzl, P. & Weinkamer, R. Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).
Weiner, S., Traub, W. & Wagner, H. Lamellar bone: structure–function relations. J. Struct. Biol. 126, 241–255 (1999).
Currey, J. D. Bones: Structure and Mechanics (Princeton Univ. Press, 2002).
Currey, J. D. The relationship between the stiffness and the mineral content of bone. J. Biomech. 2, 477–480 (1969).
Lees, S., Tao, N-J. & Lindsay, S. Studies of compact hard tissues and collagen by means of Brillouin light scattering. Connect. Tissue Res. 24, 187–205 (1990).
Giraud-Guille, M. M. Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcified Tissue Int. 42, 167–180 (1988).
Weiner, S., Arad, T., Sabanay, I. & Traub, W. Rotated plywood structure of primary lamellar bone in the rat: Orientations of the collagen fibril arrays. Bone 20, 509–514 (1997).
Martin, R. B. Porosity and specific surface of bone. Crit. Rev. Biomed. Eng. 10, 179–222 (1984).
Cowin, S. C. Bone Mechanics Handbook (CRC Press, 2001).
Kutz, M. Standard Handbook of Biomedical Engineering and Design Ch. 8 (McGraw Hill, 2003).
Gruber, P. et al. Biomimetics-Materials, Structures and Processes Ch. 5 (Springer, 2011).
Rho, J-Y, Kuhn-Spearing, L. & Zioupos, P. Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92–102 (1998).
O’Brien, F. J., Taylor, D. & Lee, T. C. An improved labelling technique for monitoring microcrack growth in compact bone. J. Biomech. 35, 523–526 (2002).
Sun, X., Jeon, J. H., Blendell, J. & Akkus, O. Visualization of a phantom post-yield deformation process in cortical bone. J. Biomech. 43, 1989–1996 (2010).
Zioupos, P., Hansen, U. & Currey, J. D. Microcracking damage and the fracture process in relation to strain rate in human cortical bone tensile failure. J. Biomech. 41, 2932–2939 (2008).
Gupta, H. et al. Fibrillar level fracture in bone beyond the yield point. Int. J. Fracture 139, 425–436 (2006).
Oliver, W. C. & Pharr, G. M. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564–1583 (1992).
Lewis, G. & Nyman, J. S. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state of the art review. J. Biomed. Mater. Res. B 87, 286–301 (2008).
Zysset, P. K., Guo, X. E., Hoffler, C. E., Moore, K. E. & Goldstein, S. A. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J. Biomech. 32, 1005–1012 (1999).
Lucchini, R. et al. Role of damage mechanics in nanoindentation of lamellar bone at multiple sizes: experiments and numerical modelling. J. Mech. Behav. Biomed. 4, 1852–1863 (2011).
Zhang, J., Michalenko, M. M., Kuhl, E. & Ovaert, T. C. Characterization of indentation response and stiffness reduction of bone using a continuum damage model. J. Mech. Behav. Biomed. 3, 189–202 (2010).
Chen, X., Ogasawara, N., Zhao, M. & Chiba, N. On the uniqueness of measuring elastoplastic properties from indentation: the indistinguishable mystical materials. J. Mech. Phys. Solids 55, 1618–1660 (2007).
Howie, P. R., Korte, S. & Clegg, W. J. Fracture modes in micropillar compression of brittle crystals. J. Mater. Res. 27, 141–151 (2012).
Michler, J., Wasmer, K., Meier, S., Ostlund, F. & Leifer, K. Plastic deformation of gallium arsenide micropillars under uniaxial compression at room temperature. Appl. Phys. Lett. 90, 043123–043123-3 (2007).
Bažant, Z. Scaling theory for quasibrittle structural failure. Proc. Natl Acad. Sci. USA 101, 13400–13407 (2004).
Östlund, F. et al. Brittle-to-ductile transition in uniaxial compression of silicon pillars at room temperature. Adv. Funct. Mater. 19, 2439–2444 (2009).
Östlund, F. et al. Ductile–brittle transition in micropillar compression of GaAs at room temperature. Phil. Mag. 91, 1190–1199 (2011).
Griffith, A. A. The phenomena of flow and rupture in solids. Phil. Trans. R. Soc. A 221, 163–198 (1921).
Hengsberger, S., Kulik, A. & Zysset, P. K. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30, 178–184 (2002).
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. 44, 1852–1858 (2011).
Reisinger, A. G., Pahr, D. H. & Zysset, P. K. Principal stiffness orientation and degree of anisotropy of human osteons based on nanoindentation in three distinct planes. J. Mech. Behav. Biomed. 4, 2113–2127 (2011).
Franzoso, G. & Zysset, P. K. Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. J. Biomech. Eng. 131, 117001 (2009).
Chamay, A. Mechanical and morphological aspects of experimental overload and fatigue in bone. J. Biomech. 3, 263–270 (1970).
Krajcinovic, D., Trafimow, J. & Sumarac, D. Simple constitutive model for a cortical bone. J. Biomech. 20, 779–784 (1987).
Pearce, A. I., Richards, R. G., Milz, S., Schneider, E. & Pearce, S. G. Animal models for implant biomaterial research in bone: a review. Eur. Cells Mater. 13, 1–10 (2007).
Ravaglioli, A. et al. Mineral evolution of bone. Biomaterials 17, 617–622 (1996).
Reilly, D. T. & Burstein, A. H. The elastic and ultimate properties of compact bone tissue. J. Biomech. 8, 393–405 (1975).
Zhang, H., Schuster, B. E., Wei, Q. & Ramesh, K. T. The design of accurate micro-compression experiments. Scr. Mater. 54, 181–186 (2006).
Fantner, G. E. et al. Hierarchical interconnections in the nano-composite material bone: Fibrillar cross-links resist fracture on several length scales. Compos. Sci. Technol. 66, 1205–1211 (2006).
Koester, K. J., Ager, J. W. & Ritchie, R. O. The true toughness of human cortical bone measured with realistically short cracks. Nature Mater. 7, 672–677 (2008).
Peterlik, H., Roschger, P., Klaushofer, K. & Fratzl, P. From brittle to ductile fracture of bone. Nature Mater. 5, 52–55 (2006).
Poundarik, A. A. et al. Dilatational band formation in bone. Proc. Natl Acad. Sci. USA 109, 19178–19183 (2012).
Tai, K., Ulm, F-J. & Ortiz, C. Nanogranular origins of the strength of bone. Nano Lett. 6, 2520–2525 (2006).
Mercer, C., He, M. Y., Wang, R. & Evans, A. G. Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone. Acta Biomater. 2, 59–68 (2006).
Gupta, H. et al. Intrafibrillar plasticity through mineral/collagen sliding is the dominant mechanism for the extreme toughness of antler bone. J. Mech. Behav. Biomed. 28, 366–382 (2013).
Hayes, W. C. & Carter, D. R. Postyield behavior of subchondral trabecular bone. J. Biomed. Mater. Res. 10, 537–544 (1976).
Schaffler, M. B., Choi, K. & Milgrom, C. Aging and matrix microdamage accumulation in human compact bone. Bone 17, 521–525 (1995).
Carter, D. R. & Hayes, W. C. Compact bone fatigue damage: A microscopic examination. Clin. Orthop. Relat. R. 127, 265–274 (1977).
Martin, R. B. & Burr, D. B. Structure, Function, and Adaptation of Compact Bone (Raven Press, 1989).
Currey, J. D. Stress concentrations in bone. Q. J. Microsc. Sci. 103, 111–133 (1962).
Zysset, P. K. A Constitutive Law for Trabecular Bone PhD thesis, Ecole Polytechnique Federale de Lausanne (1994)
Fischer-Cripps, A. C. Nanoindentation (Springer, 2002).
Nyman, J. S. et al. The influence of water removal on the strength and toughness of cortical bone. J. Biomech. 39, 931–938 (2006).
Wolfram, U., Wilke, H-J. & Zysset, P. K. 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 46, 348–354 (2010).
Ziegler, J. F. & Biersack, J. P. The Stopping and Range of Ions in Matter (Springer, 1985).
Nalla, R. et al. Ultrastructural examination of dentin using focused ion-beam cross-sectioning and transmission electron microscopy. Micron 36, 672–680 (2005).
Rabe, R. et al. Observation of fracture and plastic deformation during indentation and scratching inside the scanning electron microscope. Thin Solid Films 469, 206–213 (2004).
Ashby, M. & Jones, D. Engineering Materials (Pergamon, 1980).
R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2008).
Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).
Acknowledgements
The authors would like to thank M. Mirzaali for help with the specimen preparation, I. Utke for the discussions about ion–matter interactions and SRIM, C. Schwiedrzik for valuable comments on the manuscript, and D. Frey and G. Buerki for technical assistance with the in situ indenter and FIB milling.
Author information
Authors and Affiliations
Contributions
The initial planning of the study was done by J.S., R.R., J.M. and P.Z. The FIB was operated by R.R. Micropillar compressions and SEM imaging were performed by J.S. and R.R., Raman measurements and interpretation were performed by V.L. Monte Carlo simulations and microindentations were performed by J.S. Macroscopic tests were performed by J.S., U.W. and A.B. Data analysis was performed by J.S. and R.R. with the assistance of U.W., and interpreted in cooperation with J.M. and P.Z. Modelling was performed by J.S. and P.Z. The manuscript was written by J.S. with contributions from all the authors.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Information (PDF 2027 kb)
Rights and permissions
About this article
Cite this article
Schwiedrzik, J., Raghavan, R., Bürki, A. et al. In situ micropillar compression reveals superior strength and ductility but an absence of damage in lamellar bone. Nature Mater 13, 740–747 (2014). https://doi.org/10.1038/nmat3959
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nmat3959
This article is cited by
-
In situ micropillar compression of an anisotropic metal-organic framework single crystal
Communications Chemistry (2023)
-
Multiscale mechanical consequences of ocean acidification for cold-water corals
Scientific Reports (2022)
-
Bone architecture, bone material properties, and bone turnover in non-osteoporotic post-menopausal women with fragility fracture
Osteoporosis International (2022)
-
Aggravated stress fluctuation and mechanical size effects of nanoscale lamellar bone pillars
NPG Asia Materials (2021)
-
Heat impact during laser ablation extraction of mineralised tissue micropillars
Scientific Reports (2021)