Symmetrically reduced stiffness and increased extensibility in compression and tension at the mineralized fibrillar level in rachitic bone

In metabolic bone diseases, the alterations in fibrillar level bone-material quality affecting macroscopic mechanical competence are not well-understood quantitatively. Here, we quantify the fibrillar level deformation in cantilever bending in a mouse model for hereditary rickets (Hpr). Microfocus in-situ synchrotron small-angle X-ray scattering (SAXS) combined with cantilever bending was used to resolve nanoscale fibril strain in tensile- and compressive tissue regions separately, with quantitative backscattered scanning electron microscopy used to measure microscale mineralization. Tissue-level flexural moduli for Hpr mice were significantly (p < 0.01) smaller compared to wild-type (~ 5 to 10-fold reduction). At the fibrillar level, the fibril moduli within the tensile and compressive zones were significantly (p < 0.05) lower by ~ 3- to 5-fold in Hpr mice compared to wild-type mice. Hpr mice have a lower mineral content (24.2 ± 2.1 Ca wt.% versus 27.4 ± 3.3 Ca wt.%) and its distribution was more heterogeneous compared to wild-type animals. However, the average effective fibril modulus did not differ significantly (p > 0.05) over ages (4, 7 and 10 weeks) between tensile and compressive zones. Our results indicate that incompletely mineralized fibrils in Hpr mice have greater deformability and lower moduli in both compression and tension, and those compressive and tensile zones have similar moduli at the fibrillar level.

► Microfocus synchrotron X-ray diffraction was used to resolve nanoscale tensile and compressive zones in a murine rachitic model.
► Significant reductions in fibril-level moduli were observed in rachitic bone in both tension and compression compared to controls.
► Tissue zones loaded in compression and tension exhibited similar moduli at fibrillar level.
► No significant difference in fibril/tissue strain ratio or orientation was found between rachitic mice and controls.