Multiscale interstitial fluid computation modeling of cortical bone to characterize the hydromechanical stimulation of lacunar-canalicular network.

Abstract

Bone tissue is a biological composite material with a complex hierarchical structure that could continuously adjust its internal structure to adapt to the alterations in the external load environment. The fluid flow within bone is the main route of osteocyte metabolism, and the pore pressure as well as the fluid shear stress generated by it are important mechanical stimuli perceived by osteocytes. Owing to the irregular multiscale structure of bone tissue, the fluid stimulation that lacunar-canalicular network (LCN) in different regions of the tissue underwent remained unclear. In this study, we constructed a multiscale conduction model of fluid flow stimulus signals in bone tissue based on the poroelasticity theory. We analyzed the fluid flow behaviors at the macro-scale (whole bone tissue), macro-meso scale (periosteum, interstitial bone, osteon and endosteum), and micro-scale (lacunar-osteocyte-canalicular) levels. We explored how fluid stimulation at the tissue level correlated with that at the cellular level in cortical bone and characterized the distributions of the pore pressure, fluid velocity and fluid shear stress that the osteocytes experienced across the entire tissue structure. The results showed that the initial conditions of intramedullary pressure had a significant impact on the pore pressure of Haversian systems, but had a relatively small influence on the fluid velocity. The osteocyte which were located at different positions in the bone tissue received very distinct fluid stimuli. Osteocytes in the vicinity of the Haversian Canals experienced higher fluid shear stress stimulation. When the permeability of the LCN was within the range from 10^-21 m² to 10^-18 m², the distribution of pressure, fluid velocity and fluid shear stress within the osteon near the periosteum and endosteum was significantly different from that in other parts of the bone. However, when the permeability was less than 10^-22 m², such a difference did not exist. Particularly, the flow velocity at the lacunae was markedly higher than that in the canaliculi. Meanwhile, the pore pressure and fluid shear stress were conspicuously lower than those in the canaliculi. In this study, we considered the interconnections of different biofunctional units at different scales of bone tissue, construct a more complete multiscale model of bone tissue, and propose that osteocytes at different locations receive different fluid stimuli, which provides a reference for a deeper understanding of bone mechanotransduction.