GAG content, fiber stiffness, and fiber angle affect swelling-based residual stress in the intact annulus fibrosus

Biological tissues with a high glycosaminoglycan (GAG) content have an excellent ability to swell by absorbing water molecules from the surrounding environment. Our recent work showed that anisotropy in tissue swelling depends on the fiber-network architecture, including fiber angle, fiber stiffness, and lamellae structure. However, that work did not evaluate the effect of in situ boundary conditions, such as the kidney-bean shape of the annulus fibrosus (AF), on swelling behavior. The biochemical composition of intact AF is inhomogeneous with respect to GAG composition, collagen fiber angle, and fiber stiffness. Moreover, the GAG content in the inner AF decreases significantly with degeneration. In this study, we investigated the role of GAG content, fiber angle, and fiber stiffness in AF swelling and residual strain development using a finite element model based on a human lumbar disk. Our results showed that the annular ring structure had a great impact on swelling by developing region-dependent compressive stress/stretch in the inner layers and tensile stress/stretch in the outer AF. Swelling-based residual stretch was comparable to experimentally measured values, suggesting an important role of tissue swelling in maintaining residual stresses. Moreover, GAG loss in the inner AF, as observed with degeneration, decreased circumferential-direction stress by over 65%. Homogeneous distributions of fiber angle and stiffness overestimated or underestimated AF swelling behavior, such as swelling ratio, circumferential/axial stretch, and fiber stretch/reorientation. These findings demonstrate the need to include native fiber architecture in finite element models, to accurately predict tissue failure, as well as to cultivate engineered disks.