Mineralization-driven bone tissue evolution follows from fluid-to-solid phase transformations in closed thermodynamic systems

The fundamental mechanisms that govern bone mineralization have been fairly well evidenced by means of experimental research. However, rules for the evolution of the volume and composition of the bone tissue compartments (such as the mineralized collagen fibrils and the extrafibrillar space in between) have not been provided yet. As an original contribution to this open question, we here test whether mineralizing bone tissue can be represented as a thermodynamically closed system, where crystals precipitate from an ionic solution, while the masses of the fibrillar and extrafibrillar bone tissue compartments are preserved. When translating, based on various experimental and theoretical findings, this mass conservation proposition into diffraction–mass density relations, the latter are remarkably well confirmed by independent experimental data from various sources. Resulting shrinkage and composition rules are deemed beneficial for further progress in bone materials science and biomedical engineering. •Extracellular bone tissue mineralizes under closed thermodynamic conditions.•Fibrillar and extrafibrillar masses are preserved during mineralization.•Precipitation of mineral ions leads to volume shrinkage of mineralizing bone tissue.•Neutron diffraction data provide experimental access to fibrillar volume shrinkage.