Abstract
Bone has a sophisticated architecture characterized by a hierarchical organization, starting at the sub-micrometre level. Thus, the analysis of the mechanical and structural properties of bone at this scale is essential to understand the relationship between its physiology, physical properties and chemical composition. Here, we unveil the potential of Brillouin–Raman microspectroscopy (BRaMS), an emerging correlative optical approach that can simultaneously assess bone mechanics and chemistry with micrometric resolution. Correlative hyperspectral imaging, performed on a human diaphyseal ring, reveals a complex microarchitecture that is reflected in extremely rich and informative spectra. An innovative method for mechanical properties analysis is proposed, mapping the intermixing of soft and hard tissue areas and revealing the coexistence of regions involved in remodelling processes, nutrient transportation and structural support. The mineralized regions appear elastically inhomogeneous, resembling the pattern of the osteons' lamellae, while Raman and energy-dispersive X-ray images through scanning electron microscopy show an overall uniform distribution of the mineral content, suggesting that other structural factors are responsible for lamellar micromechanical heterogeneity. These results, besides giving an important insight into cortical bone tissue properties, highlight the potential of BRaMS to access the origin of anisotropic mechanical properties, which are almost ubiquitous in other biological tissues.
Highlights
Human lamellar bone is a highly specialized type of tissue, characterized by a complex hierarchical structure with several levels of organization, from the macroscopic scale, i.e. long, short and irregular bone; down to the mesoscale, i.e. cortical and trabecular bone; the microscale, i.e. lamellae, lacunae and the Haversian system; and the nanoscale, i.e. collagen type I and hydroxyapatite nanocrystals [1]
Local mechanical and chemical heterogeneities revealed by single Brillouin–Raman microspectroscopy spectra
The boundary of each osteon is defined by optically dense structures, called cement lines, and the space between different Haversian systems is filled with interstitial lamellae, i.e. the residues of old osteons partially degraded by bone remodelling processes
Summary
Human lamellar bone is a highly specialized type of tissue, characterized by a complex hierarchical structure with several levels of organization, from the macroscopic scale, i.e. long, short and irregular bone; down to the mesoscale, i.e. cortical and trabecular bone; the microscale, i.e. lamellae, lacunae and the Haversian system; and the nanoscale, i.e. collagen type I and hydroxyapatite nanocrystals [1]. Cortical bone tissue is mostly located in the outer layer of the long bones and constitutes approximately 80% of the total skeletal mass It is organized in regular and concentric patterns of lamellae, wrapped around a Haversian channel [2]. An impairment in just one single component at the nano-, sub-micro- or microscale can affect the biomechanics of the entire bone material [6,7]. For this reason, considering the lamellar organization at each length scale is fundamental both for understanding its complex mechanical properties and for modelling prostheses and bioinspired materials [8,9]. Knowledge of bone tissue physiology can be crucial to detecting micro-alterations in the structure that can be early manifestations of orthopaedic diseases [10]
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