Exercise and physical activity exert mechanical loading on the bones enabling bone formation. However, the relationship between mechanical stress experienced by osteocytes and stimulation of bone formation and osteocyte lacunocanalicular network (LCN) morphology is not fully understood.

In this study, we assessed the effect of morphological parameters including canalicular density, lacunocanalicular space thickness, dendrite diameter, number of fluid inlets to the lacuna, and load direction on fluid flow shear stress (FFSS) and bone strains and how these might change with microstructural deterioration of the LCN that occurs with aging. Four distinct theoretical models were initially created of osteocytes with either ten or eighteen dendrites using a fluid-structure interaction (FSI) method with idealized geometries. Next, two models of young and aged osteocytes were developed from confocal images after FITC staining of the femur of a 5-month-old and 22-month-old C57BL6 mouse. Also, several simulated osteocyte models were then developed from confocal images of a 4-month-old C57BL6 mouse using a new geometry modification approach with different LCN morphologies. Shear stresses on osteocyte and dendritic membranes were estimated using a computational fluid dynamics (CFD) approach considering the average surface area and volume of each model.

The models predicted higher fluid velocity in the canaliculi versus the lacuna. Comparison of idealized models with one fluid inlet versus five fluid inlets indicated that the average shear stress increased from 0.13 Pa to 0.28 Pa and one-half of the dendrites experienced FFSS greater than 0.8 Pa with four more fluid inlets. The 3D simulations of models based on confocal images of osteocytes indicated that the velocity profile alters in the tortuous canaliculi, near canalicular branches, and canalicular junctions. Our findings indicate a higher ratio of canalicular to lacunar surface area in the young osteocyte model than the aged model and a greater average FFSS in young model than the aged model. Consequently, osteocytes experience lower shear stresses on the osteocyte body and dendritic membranes in the aged models. We also predicted that with increasing canalicular density or lacunocanalicular space thickness, FFSS experienced by osteocytes increases. Both realistic aged osteocyte model generated from the confocal images of an aged mouse and the simulated aged osteocyte model generated from confocal images of a young mouse using the geometry modification technique showed similar FFSS results. This study shows the significance of this technique in computer modeling of osteocytes. Overall, this study may explain the impaired mechano-responsiveness of the osteocytes with aging.