Tough Lessons From Bone: Extreme Mechanical Anisotropy at the Mesoscale

Authors


  • We would like to thank the European Synchrotron Radiation Facility (ESRF) for provision of synchrotron radiation facilities and Elodie Boller for assistance at beamline ID19. We thank Annemarie Martins for assistance in sample preparation, Gunthard Benecke for development of essential image analysis software, and Petra Leibner for technical assistance with the micromechanical setup. John Dunlop, Wolfgang Wagermaier, and Richard Weinkamer are greatly appreciated for their discussions and thoughtful comments. H. S. G., H. D. W., and P. F. acknowledge that funding for this work is provided through the German-Israeli Foundation for Scientific Research and Development and the Max Planck Society. J. S. is supported by EU Marie Curie EST Fellowship on Biomimetic Systems, MEST-CT-2004-504465. Supporting Information is available online from Wiley InterScience or from the authors.

Abstract

Bone is mechanically and structurally anisotropic with oriented collagen fibrils and nanometer-sized mineral particles aggregating into lamellar or woven bone.[1] Direct measurements of anisotropic mechanical properties of sublamellar tissue constituents are complicated by the existence of an intrinsic hierarchical architecture. Methods such as nanoindentation provide insight into effective modulus values; however, bulk material properties cannot sufficiently be characterized since such measurements represent properties of near-surface volumes and are partially averaged over fibril orientations.[2–5] In this study, we focus on the material properties of bone at one single level of hierarchy. By measuring properties of individual parallel-fibered units of fibrollamellar bone under tension under controlled humidity conditions, an unusually high anisotropy is found. Here, we clearly demonstrate ratios as large as 1:20 in elastic modulus and 1:15 in tensile strength between orientations perpendicular and parallel to the main collagen fiber orientation in native wet bone; these ratios reduce to 1:8 and 1:7, respectively, under dry conditions. This extreme anisotropy appears to be caused by the existence of periodic, weak interfaces at the mesoscopic length scale. These interfaces are thought to be relevant to the proper mechanical and physiological performance of bone.

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