Loss of longitudinal superiority marks the microarchitecture deterioration of osteoporotic cancellous bones

Osteoporosis (OP), a skeletal disease making bone mechanically deteriorate and easily fracture, is a global public health issue due to its high prevalence. It has been well recognized that besides bone loss, microarchitecture degradation plays a crucial role in the mechanical deterioration of OP bones, but the specific role of microarchitecture in OP has not been well clarified and quantified from mechanics perspective. Here, we successfully decoupled and identified the specific roles of microarchitecture, bone mass and tissue property in the failure properties of cancellous bones, through μCT-based digital modeling and finite element method simulations on bone samples from healthy and ovariectomy-induced osteoporotic mice. The results show that the microarchitecture of healthy bones exhibits longitudinal superiority in mechanical properties such as the effective stiffness, strength and toughness, which fits them well to bearing loads along their longitudinal direction. OP does not only reduce bone mass but also impair the microarchitecture topology. The former is mainly responsible for the mechanical degradation of bones in magnitude, wherever the latter accounts for the breakdown of their function-favorable anisotropy, the longitudinal superiority. Hence, we identified the microarchitecture-deterioration-induced directional mismatch between material and loading as a hazardous feature of OP and defined a longitudinal superiority index as measurement of the health status of bone microarchitecture. These findings provide useful insights and guidelines for OP diagnosis and treat assessment.