Viscoelastic Modeling of Optic Nerve Head Biomechanics: Effects of Intraocular and Cerebrospinal Fluid Pressure.

Abstract

Although the optic nerve head (ONH) has demonstrated a significant viscoelastic response to changes in intraocular pressure (IOP), existing computational models of ONH biomechanics have yet to fully account for these viscoelastic properties. In this study, we introduce and evaluate a mesh-free beam-in-solid coupling algorithm to model the complex viscoelastic behavior of anisotropic collagen fibers within a viscoelastic scleral matrix. We also incorporated viscoelastic formulations for the retina, lamina cribrosa, and optic nerve to provide a more comprehensive understanding of ONH tissue mechanics. We compared the biomechanics of the ONH resulting from hyperelastic and viscoelastic scleral material formulations using an eye-specific finite element model of the posterior human eye. This model integrates the detailed 3D microstructure of the load-bearing lamina cribrosa, including interspersed laminar neural tissues, as well as the heterogeneous, anisotropic behavior of the collagenous sclera and pia. The viscoelastic material properties were validated against published experimental tensile tests of human scleral and retinal tissue samples. Simulations of ONH biomechanical responses were conducted by applying changes in IOP and cerebrospinal fluid pressure (CSFP) typical of body position transitions, such as moving from sitting to supine, over a 250 ms period. In both simulations, the ONH tissues exhibited greater stresses and strains in the supine position compared to sitting, as anticipated. The laminar surface showed posterior deformation (+6 μm) during the transition from sitting to supine when using the hyperelastic material model, whereas it deformed anteriorly (-5.7 μm) with the viscoelastic model. Furthermore, the radial scleral canal expansion at the anterior laminar insertion was significantly smaller in the viscoelastic formulation (9 μm) compared to the hyperelastic formulation (19.8 μm). All results aligned with experimental observations. While the stresses, strains, and deformations remained within physiological ranges for both models, there were substantial differences between the two formulations, particularly in terms of deformation. Improving the accuracy of material formulations in ONH models is expected to enhance our understanding of ONH biomechanics. However, further experimental validation is needed to confirm these results and strengthen their applicability.