Gradient mechanical environments modulate intra-osteonal fluid flow: a three-dimensional finite element study

Interstitial fluid flow within the osteonal lacunar-canalicular system (LCS) is crucial for osteocyte mechanotransduction and bone remodeling. This study aims to develop a three-dimensional finite element model of an osteon with gradient-varying boundary conditions to systematically investigate how mechanical loading, outer wall constraints, and pulsatile blood pressure modulate intra-osteonal fluid flow.

This study constructs a three-dimensional finite element model to systematically analyze the dynamic responses of fluid flow behavior under gradient boundary conditions. Gradient parametric analyses were performed by varying: (1) axial strain amplitudes (250-5000 με) to simulate different activity levels; (2) radial displacement constraints at the outer wall (0- 0.042 μm) to represent confinement by surrounding tissues; and (3) pulsatile blood pressure amplitudes (A = 0-2.5) at the inner wall to mimic physiological to hypertensive conditions. The resulting pore pressure, fluid velocity, and fluid shear stress (FSS) distributions were analyzed.

All parameters exhibited axisymmetric distributions. Peak pore pressure, fluid velocity, and FSS increased nearly linearly with strain magnitude, ranging from 1.7×10⁴ to 1.4×10⁵ Pa, 1.69×10^-8 to 3.50×10^-8 m/s, and 0.34 to 6.5 Pa, respectively. Relaxation of outer wall constraints from fully constrained (0 μm) to fully elastic (0.042 μm) significantly reduced all three parameters. Elevated pulsatile blood pressure markedly increased intra-osteonal pore pressure (from 2.7×10⁴ to 6.5×10⁴ Pa) but had minimal effect on velocity and FSS. A subsequent multiscale validation using an explicit LCS model showed that the macro-scale poroelastic model accurately captures global trends, while local FSS within canaliculi is amplified by a factor of 1.5-2.5.

The gradient boundary condition approach effectively quantifies the differential and synergistic effects of mechanical load, structural constraint, and vascular pressure on the osteonal fluid environment. These findings provide a quantitative framework for understanding mechanotransduction in bone and may inform clinical strategies for managing bone adaptation and disease.