The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach

Abstract

The biomechanics of the optic nerve head is assumed to play an important role in ganglion cell loss in glaucoma. Organized collagen fibrils form complex networks that introduce strong anisotropic and nonlinear attributes into the constitutive response of the peripapillary sclera (PPS) and lamina cribrosa (LC) dominating the biomechanics of the optic nerve head. The recently presented computational remodeling approach (Grytz and Meschke in Biomech Model Mechanobiol 9:225-235, 2010) was used to predict the micro-architecture in the LC and PPS, and to investigate its impact on intraocular pressure-related deformations. The mechanical properties of the LC and PPS were derived from a microstructure-oriented constitutive model that included the stretch-dependent stiffening and the statistically distributed orientations of the collagen fibrils. Biomechanically induced adaptation of the local micro-architecture was captured by allowing collagen fibrils to be reoriented in response to the intraocular pressure-related loading conditions. In agreement with experimental observations, the remodeling algorithm predicted the existence of an annulus of fibrils around the scleral canal in the PPS, and a predominant radial orientation of fibrils in the periphery of the LC. The peripapillary annulus significantly reduced the intraocular pressure-related expansion of the scleral canal and shielded the LC from high tensile stresses. The radial oriented fibrils in the LC periphery reinforced the LC against transversal shear stresses and reduced LC bending deformations. The numerical approach presents a novel and reasonable biomechanical explanation of the spatial orientation of fibrillar collagen in the optic nerve head.

The Optic Nerve Head as a Robust Biomechanical System

“…The predictions of this study are in good agreement with the measurements (Kankipati L, et al IOVS 2011;ARVO EAbstract 6255) 3,7,9-11 and predictions 14,19,23,29 of acute effects of IOP on the human ONH. Agoumi and colleagues 9 reported that for increases in IOP of about 12 mm Hg they observed LCD (with respect to Bruch's membrane) between -8 and 8 lm.…”

Polarization microscopy for characterizing fiber orientation of ocular tissues

“…Hence, to preserve vision, it is important to characterize two elements central to connective tissues, namely the orientation and organization of the collagen fibers that form them [5,6]. Several techniques have been developed for measuring collagen fiber orientation and organization, including small angle light scattering [7,8], x-ray scattering [9][10][11][12], non-linear microscopy [7,13,14] and magnetic resonance imaging [15,16], or for estimating them using inverse numerical methods [17,18]. The complexity of the eye calls for a technique that provides data at multiple scales, including high resolution (micron-scale) and broad field of view (several mm to cm) [19].…”

A wide-angle X-ray fibre diffraction method for quantifying collagen orientation across large tissue areas: application to the human eyeball coat

“…Specifically, inferiorsuperior and temporal-nasal preferential collagen orientation in the central cornea is possibly designed to resist the pulling forces of the extraocular recti muscles during eye movement and image fixation (Daxer & Fratzl, 1997;Boote et al, 2005), while circumferential collagen at the limbus may be required to withstand the increased stress brought about by the change in tissue curvature at the corneo-scleral border (Maurice, 1988;Boote et al, 2009). At the posterior pole, the existence of a collagen annulus in the peripapillary sclera (Pijanka et al, 2012) is structurally optimal for preventing excessive scleral canal expansion under elevated intraocular pressure and hence may provide a neuroprotective function for the optic nerve axons (Grytz et al, 2011).…”