The elasto-plastic nano- and microscale compressive behaviour of rehydrated mineralised collagen fibres.

Groetsch, Alexander; Gourrier, Aurélien; Casari, Daniele; Schwiedrzik, Jakob; Shephard, Jonathan D; Michler, Johann; Zysset, Philippe K; Wolfram, Uwe (2023). The elasto-plastic nano- and microscale compressive behaviour of rehydrated mineralised collagen fibres. Acta biomaterialia, 164, pp. 332-345. Elsevier 10.1016/j.actbio.2023.03.041

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The hierarchical design of bio-based nanostructured materials such as bone enables them to combine unique structure-mechanical properties. As one of its main components, water plays an important role in bone's material multiscale mechanical interplay. However, its influence has not been quantified at the length-scale of a mineralised collagen fibre. Here, we couple in situ micropillar compression, and simultaneous synchrotron small angle X-ray scattering (SAXS) and X-ray diffraction (XRD) with a statistical constitutive model. Since the synchrotron data contain statistical information on the nanostructure, we establish a direct connection between experiment and model to identify the rehydrated elasto-plastic micro- and nanomechanical fibre behaviour. Rehydration led to a decrease of 65%-75% in fibre yield stress and compressive strength, and 70% in stiffness with a 3x higher effect on stresses than strains. While in agreement with bone extracellular matrix, the decrease is 1.5-3x higher compared to micro-indentation and macro-compression. Hydration influences mineral more than fibril strain with the highest difference to the macroscale when comparing mineral and tissue levels. The effect of hydration seems to be strongly mediated by ultrastructural interfaces while results provide insights towards mechanical consequences of reported water-mediated structuring of bone apatite. The missing reinforcing capacity of surrounding tissue for an excised fibril array is more pronounced in wet than dry conditions, mainly related to fibril swelling. Differences leading to higher compressive strength between mineralised tissues seem not to depend on rehydration while the lack of kink bands supports the role of water as an elastic embedding influencing energy-absorption mechanisms. STATEMENT OF SIGNIFICANCE: Characterising structure-property-function relationships in hierarchical biological materials helps us to elucidate mechanisms that enable their unique properties. Experimental and computational methods can advance our understanding of their complex behaviour with the potential to inform bio-inspired material development. In this study, we close a gap for bone's fundamental mechanical building block at micro- and nanometre length scales. We establish a direct connection between experiments and simulations by coupling in situ synchrotron tests with a statistical model and quantify the behaviour of rehydrated single mineralised collagen fibres. Results suggest a high influence of hydration on structural interfaces, and the role of water as an elastic embedding by outlining important differences between wet and dry elasto-plastic properties of mineral nanocrystals, fibrils and fibres.

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