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 structural organization is well established, the mechanistic basis for the emergence and maintenance of this architecture remains unresolved. In this study, we propose a fluid flow-driven mechanism for the evolution of collagen fiber orientation in AC, using both a continuum orientation field model and a discrete three-dimensional fiber network model. Joint movements, shear-dominated during embryogenesis and combined shear-compression postnatally, induce synovial fluid flow, which guides collagen alignment through preferential fiber deposition. Our models reproduce the characteristic Benninghoff architecture observed in mature AC and are validated against experimental data across multiple species, joint types, and developmental stages. We demonstrate how joint- and organism-specific mechanical loading leads to diverse collagen arrangements and zonal organization. Further, by systematically varying shear and compressive loading durations to mimic different physical activities, we show that the collagen architecture, mechanical stiffness, and effective synovial fluid viscosity of AC adapt in an activity-dependent manner. Finally, we simulate osteoarthritic remodeling as a localized disruption to fluid flow and show how it leads to progressive collagen disorganization. These findings offer a unifying biomechanical framework for AC development, function, and degeneration, with implications for tissue engineering and rehabilitation strategies.