Microtensile properties and failure mechanisms of cortical bone at the lamellar level

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Casari, Daniele¹; Michler, Johann¹; Zysset, Philippe²; Schwiedrzik, Jakob¹

Microtensile properties and failure mechanisms of cortical bone at the lamellar level

Acta Biomater. January 15, 2021;120:135-145

©2020 The Authors. Published by Elsevier Ltd on behalf of Acta Materialia Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

Affiliations

¹Empa, Swiss Federal Laboratories for Materials Science and Technology, Laboratory for Mechanics of Materials and Nanostructures, Feuerwerkerstrasse 39, CH-3602 Thun, Switzerland

²ARTORG Centre for Biomedical Engineering Research, University of Bern, Freiburgstrasse 3, CH-3010 Bern, Switzerland
Abstract and keywords

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 Significance: Understanding 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.

Keywords: Bone; Microtensile strength; Lamellar level; Failure mechanisms; Composite modeling; MCF; mineralized collagen fibril; EFM; extrafibrillar matrix; ECM; extracellular matrix; FIB; focused ion beam; SEM; scanning electron microscope; STEM; scanning transmission electron microscopy; HR-SEM; high-resolution SEM; BF-STEM; bright-field STEM
Links

DOI: 10.1016/j.actbio.2020.04.030

PubMed: 32428682

WoS: 000608170400012
History

Received: 2020-01-10

Revised: 2020-04-16

Accepted: 2020-04-16

Online: 2020-05-16

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