Multiscale composite model of fiber-reinforced tissues with direct representation of sub-tissue properties

In many fiber-reinforced tissues, collagen fibers are embedded within a glycosaminoglycan-rich extrafibrillar matrix. Knowledge of the structure-function relationship between the sub-tissue properties and bulk tissue mechanics is important for understanding tissue failure mechanics and developing biological repair strategies. Difficulties in directly measuring sub-tissue properties led to a growing interest in employing finite element modeling approaches. However, most models are homogeneous and are therefore not sufficient for investigating multiscale tissue mechanics, such as stress distributions between sub-tissue structures. To address this limitation, we developed a structure-based model informed by the native annulus fibrosus structure, where fibers and the matrix were described as distinct materials occupying separate volumes. A multiscale framework was applied such that the model was calibrated at the sub-tissue scale using single-lamellar uniaxial mechanical test data, while validated at the bulk scale by predicting tissue multiaxial mechanics for uniaxial tension, biaxial tension, and simple shear (13 cases). Structure-based model validation results were compared to experimental observations and homogeneous models. While homogeneous models only accurately predicted bulk tissue mechanics for one case, structure-based models accurately predicted bulk tissue mechanics for 12 of 13 cases, demonstrating accuracy and robustness. Additionally, six of eight structure-based model parameters were directly linked to tissue physical properties, further broadening its future applicability. In conclusion, the structure-based model provides a powerful multiscale modeling approach for simultaneously investigating the structure-function relationship at the sub-tissue and bulk tissue scale, which is important for studying multiscale tissue mechanics with degeneration, disease, or injury.