Fluid flow-induced biomechanical origin of collagen architecture in articular cartilage

The zonal collagen architecture of articular cartilage (AC) is essential for its mechanical function and long-term homeostasis. While its structure is well characterized, the mechanistic basis for its emergence and maintenance remains unresolved. Here, we propose a fluid flow-driven mechanism for the evolution of collagen fibre orientation in AC, using both a continuum orientation field model and a discrete three-dimensional fibre network model. Joint movements-shear-dominated during embryogenesis and combined shear-compression post-natally-induce synovial fluid flow, which guides collagen alignment via preferential fibre deposition. Our models reproduce the characteristic Benninghoff architecture of mature AC and are validated against experimental data across multiple species, joint types and developmental stages. We show that joint- and organism-specific loading patterns generate distinct collagen arrangements and zonal organization. By varying shear and compressive loading durations to mimic different physical activities, we demonstrate that collagen architecture, mechanical stiffness and effective synovial fluid viscosity adapt in an activity-dependent manner. Finally, we simulate osteoarthritic remodelling as a localized disruption to fluid flow and show its role in progressive collagen disorganization. These findings provide a unifying biomechanical framework for AC development, function and degeneration, with implications for tissue engineering and rehabilitation.