Osteocyte-lacuna shape and canaliculi architecture dictate fluid flow around osteocyte, and strain of cell and bone matrix: implications for cell mechanobiology and bone fragility

Abstract

Osteocytes, the most abundant cells in bone, play a critical role in maintaining bone quality by sensing mechanical loads and orchestrating bone modeling and remodeling. These cells are housed in lacunae and connected by a complex network of canaliculi, through which interstitial fluid flows in response to mechanical loading. Osteocyte-lacuna shape can vary from elongated in healthy lamellar bones subjected to directional loading to more spherical shapes, often seen in flat bones, or in aging and diseases. Additionally, canaliculi can be star-shaped or run perpendicular to the lacunar major axis. The morphology of the osteocyte-lacunar-canalicular system is believed to impact fluid flow and mechanical strain on cell influencing osteocyte signaling, and strains on bone affecting bone fragility. However, the mechanical implications of these geometrical variations are not yet fully understood. This study uses fluid-structure interaction (FSI) models of osteocytes within bone blocks to investigate how changes in lacunar shape, canalicular orientation and number influence bone strain, interstitial fluid velocity and cell deformation caused by mechanical loading-induced convection-driven fluid flow. Our results demonstrate that spherical lacunae, and canaliculi oriented perpendicular to the lacunar major axis result in high bone strain concentrations but low osteocyte strain, increasing bone fragility and impairing cell mechanosensation. In contrast, elongated lacunae, and many and/or star-shaped canaliculi result in low bone strain and high interstitial fluid flow and osteocyte strain, fostering a more anabolic mechanical environment and nutrient transport. Our findings offer new insights into how osteocyte-lacuna morphology and canalicular arrangement affect bone fragility and cell mechanobiology, particularly in aging and diseases.