Abstract

Bone features a remarkable combination of toughness and strength which originates from its complex hierarchical structure and motivates its investigation on multiple length scales. Here, in situ microtensile experiments were performed on dry ovine osteonal bone for the first time at the length scale of a single lamella. The micromechanical response was brittle and revealed larger ultimate tensile strength compared to the macroscale (factor of 2.3). Ultimate tensile strength for axial and transverse specimens was 0.35 ± 0.05 GPa and 0.13 ± 0.02 GPa, respectively. A significantly greater strength anisotropy relative to compression was observed (axial to transverse strength ratio of 2.7:1 for tension, 1.3:1 for compression). Fracture surface and transmission electron microscopic analysis suggested that this may be rationalized by a change in failure mode from fibril-matrix interfacial shearing for axial specimens to fibril-matrix debonding in the transverse direction. An improved version of the classic Hashin's composite failure model was applied to describe lamellar bone strength as a function of fibril orientation. Together with our experimental observations, the model suggests that cortical bone strength at the lamellar level is remarkably tolerant to variations of fibrils orientation of about ±30°. This study highlights the importance of investigating bone's hierarchical organization at several length scales for gaining a deeper understanding of its macroscopic fracture behavior. Statement of SignificanceUnderstanding bone deformation and failure behavior at different length scales of its hierarchical structure is fundamental for the improvement of bone fracture prevention, as well as for the development of multifunctional bio-inspired materials combining toughness and strength. The experiments reported in this study shed light on the microtensile properties of dry primary osteonal bone and establish a baseline from which to start further investigations in more physiological conditions. Microtensile specimens were stronger than their macroscopic counterparts by a factor of 2.3. Lamellar bone strength seems remarkably tolerant to variations of the sub-lamellar fibril orientation with respect to the loading direction (±30°). This study underlines the importance of studying bone on all length scales for improving our understanding of bone's macroscopic mechanical response.

Highlights

  • The tensile properties of ovine lamellar bone were characterized at the length scale of a single lamella under uniaxial loading using a microtensile setup inside an scanning electron microscope (SEM)

  • Microtensile testing was combined with post-test scanning transmission electron microscopy (STEM) observation to analyze deformation and failure mechanisms, as well as to define a composite failure model able to predict strength and failure mode as a function of the main mineralized collagen fibril (MCF) orientation

  • To what was observed at the macroscale, strength anisotropy was considerably greater for tension than for compression. This discrepancy between the two loading modes may be attributed to a change in failure mode from fibril-matrix interfacial shearing for axial specimens to fibrilmatrix debonding for transverse specimens

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Summary

Introduction

R Part of the Special Issue on Biomineralization: From Cells to Biomaterials, associated with the BIOMIN XV: 15th International Symposium on Biomineralization, held at the Ludwig Maximilian University, Sept 9-13, 2019, organized by Wolfgang Schmahl and Erika Griesshaber. Bone is a hierarchically structured connective tissue with remarkable mechanical properties. Its primary functions are structural support, locomotion, organ protection, mineral storage and strasse 39, 3602 Thun, Switzerland.

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