The Effects of Negative Periocular Pressure on Biomechanics of the Optic Nerve Head and Cornea: A Computational Modeling Study

Abstract

Purpose: The purpose of this study was to evaluate the effects of negative periocular pressure (NPP), and concomitant intraocular pressure (IOP) lowering, on the biomechanics of the optic nerve head (ONH) and cornea.

Methods: We developed a validated finite element (FE) model of the eye to compute tissue biomechanical strains induced in response to NPP delivered using the Multi-Pressure Dial (MPD) system. The model was informed by clinical measurements of IOP lowering and was based on published tissue properties. We also conducted sensitivity analyses by changing pressure loads and tissue properties.

Results: Application of -7.9 mmHg NPP decreased strain magnitudes in the ONH by c. 50% whereas increasing corneal strain magnitudes by c. 25%. Comparatively, a similar increase in corneal strain was predicted to occur due to an increase in IOP of 4 mmHg. Sensitivity studies indicated that NPP lowers strain in the ONH by reducing IOP and that these effects persisted over a range of tissue stiffnesses and spatial distributions of NPP.

Conclusions: NPP is predicted to considerably decrease ONH strain magnitudes. It also increases corneal strain but to an extent expected to be clinically insignificant. Thus, using NPP to lower IOP and hence decrease ONH mechanical strain is likely biomechanically beneficial for patients with glaucoma.

Translational relevance: This study provides the first description of how NPP affects ONH biomechanics and explains the underlying mechanism of ONH strain reduction. It complements current empirical knowledge about the MPD system and guides future studies of NPP as a treatment for glaucoma.

Figure 1.

The finite element model used in this study, including the corneoscleral shell and ONH (ppSC = peripapillary sclera and LC = lamina cribrosa). The extraocular rectus muscle attachment is also shown, which is modeled as a rigid body free to move along the y-axis. The figure also schematically represents the loads, namely intraocular pressure (IOP), negative periocular pressure (NPP), and retrolaminar tissue pressure (RTLP).

Figure 2.

(A-L) Maps of the first principal Lagrangian strain (E_I), a measure of tissue stretching, in the LC, PLT, limbus, and at the corneal apex for tissue stiffnesses defined by the Baseline tissue parameter set. Each of the top four rows correspond to one case (i.e., Normotensive [A-C], Goggle [D-F], Hypertensive [G-I], and IOP fixed [J-L]). The bottom row (M) provides a summary of E_I values (violin plots [Bechtold, Bastian, 2016. Violin Plots for Matlab, Github Project, https://github.com/bastibe/Violinplot-Matlab, doi:10.5281/zenodo.4559847], with median shown by “+”) in each region. D_Goldmann = 3.06 mm is the diameter of the applanated region during Goldmann tonometry, which is a clinically familiar region that we used to define the corneal apex region.

Figure 3.

(A-L) Maps of the third principal Lagrangian strain (E_III), and (M) summary of E_III values for tissue stiffnesses defined by the Baseline tissue parameter set. For a detailed description of each panel see the caption of Figure 2.

Figure 4.

Changes in first (E_I) and third (E_III) principal strains due to varying corneoscleral shell stiffness. Calculations were carried out for both the Normotensive and Goggle cases, using the Baseline, Soft Shell, and Stiff Shell tissue parameter sets (Table 2). Each panel depicts the strain values in the Normotensive and Goggle cases in different tissues (lamina cribrosa [LC; A and E], prelaminar tissue [PLT; B and F], limbus [C and G], and corneal apex [D and H]). Changing corneoscleral shell stiffness did not change the effect of NPP in decreasing strain magnitudes in the lamina cribrosa (LC; A and E) and prelaminar tissue (PLT; B and F); however, softening (stiffening) corneoscleral shell stiffness increased (decreased) E_I and E_III magnitudes at the limbus (C and H) and corneal apex (D and H). Data is shown using violin plots, with the median shown by “+.”

Figure 5.

The effects of changing LC stiffness on strains (E_I and E_III) in the lamina cribrosa [LC; A and C] and prelaminar tissue [PLT; B and D]) using Baseline, Soft LC, and Stiff LC tissue parameter sets (Table 2). The magnitudes of E_I and E_III increased in both the LC (A and B) and the PLT (C and D) when using Soft LC tissue parameter set relative to the values computed when using the Baseline tissue parameter set. Conversely, when using the Stiff LC tissue parameter set, they decreased. However, despite these changes, for both the Soft and Stiff LC tissue parameter sets, the magnitudes of E_I and E_III decreased in the Goggle case relative to the Normotensive case. Data is shown using violin plots and the median is marked with “+.”