Multiscale Meniscus Mechanics under Unconfined Compression: Composite Fibril-Reinforced Biphasic Modeling across Infinitesimal to Physiological Cumulative Strain Regimes.

To investigate the mechanical roles of proteoglycan aggregates, interstitial fluid, and the collagen fibrillar network in meniscal mechanics, we developed and experimentally validated a composite fibril-reinforced biphasic (CFRB) model based on a heterogeneous and anisotropic structural description of the meniscus and tested whether shear wave elastography (SWE) could independently reflect matrix‑dominated and fibril‑engaged behavior. Focusing on the pars intermedia, 21+12+(6 × 5) disc specimens underwent unconfined compression across cumulative strains extending into the nonlinear regime to identify model parameters and evaluate strain-rate effects, pressurization, and interstitial fluid transport. Within classical fibril-reinforced poroelastic (FRB) theory, the equally distributed collagen fibrillar network across three orthogonal directions corresponded to linear progressive fibrillar recruitment, while dynamic stiffness amplitude exhibited heterogeneous yet systematically evolving behavior consistent with interstitial fluid transport and pressurization. With nonlinear fibrillar reinforcement, the FRB model showed substantial errors in fibril modulus, whereas the CFRB framework, incorporating frequency-time circular poroelastic analysis, identified lateral strain, biphasic parameters, and mechanical-regime thresholds, and captured the experimental curves and strain heterogeneity. These findings were supported by inverse analysis, finite element methods, meniscal tensile mechanics, and SWE measurements in the plane perpendicular to loading. Increasing strain rate increased the elastic fraction and enabled derivation of pressurization convergence equations, whereas the equilibrium modulus showed no significant rate dependence, consistent with matrix-deformation estimates from the normalized threshold curve and corresponding SWE measurements; this range is proposed as a mechanical regime suitable for evaluation of matrix-related degeneration and elastographic assessment. This framework stratifies cumulative strain, decodes elastography into matrix versus fibril responses, and advances meniscal constitutive modeling toward clinical translation. STATEMENT OF SIGNIFICANCE: Quantifying solid-phase moduli, lateral strain evolution, nonlinear fibril-recruitment thresholds, and permeability parameters can provide insights into the mechanics of porous menisci. Here, Hashemi S.S. et al. introduce a composite fibril-reinforced biphasic (CFRB) framework with poroelastic transformation equations that quantitatively resolves matrix- and fibril-dominated mechanical regimes across cumulative compressive strains from infinitesimal to physiological levels. The framework quantitatively resolved matrix and fibrillar contributions within the matrix-dominated regime, revealing that fibrillar reinforcement also modulated the matrix-deformation response, potentially contributing to anisotropic behavior. The low-strain regime provides a mechanically meaningful range for small-spatial-scale elastographic measurements, whereas the strain range approaching the nonlinear fibril-recruitment threshold provides a basis for evaluating matrix-dominated mechanics. Overall, this systematic implementation of cumulative-strain mechanics quantitatively resolves matrix-fibril mechanics and their coupling with interstitial fluid transport, providing a mechanistic basis for nondestructive assessment, tissue engineering, and clinical translation.