Energy Storage and Dissipation in the Eye: The Importance of the Biomechanical Connections between the Cornea-Limbus-Scleral Series Biomechanical Element and the Scleral-Optic Nerve-Posterior Segment Tissues in Protecting Sensitive Visual Components from Mechanical Damage

Research Article

Austin J Clin Ophthalmol. 2023; 10(6): 1162.

Energy Storage and Dissipation in the Eye: The Importance of the Biomechanical Connections between the Cornea-Limbus-Scleral Series Biomechanical Element and the Scleral-Optic Nerve-Posterior Segment Tissues in Protecting Sensitive Visual Components from Mechanical Damage

Frederick H Silver1,2*; Tanmay Deshmukh2; Dominick Benedetto3; Michael Gonzalez-Mercedes2; Jose Pulido4

1Department of Pathology and Laboratory Medicine, Robert Wood Johnson Medical School, Rutgers, the State University of New Jersey, USA

2OptoVibronex, LLC., Ben Franklin Tech Partners, Bethlehem, USA

3Center For Advanced Eye Care, Vero Beach, USA

4Vickie and Jack Farber Vision Research Center, Wills Eye Hospital, Philadelphia, USA

*Corresponding author: Frederick H Silver Department of Pathology and Laboratory Medicine, Robert Wood Johnson Medical School, Rutgers, the State University of New Jersey, USA. Email: silverfr@rutgers.edu

Received: July 18, 2023 Accepted: August 28, 2023 Published: September 04, 2023

Abstract

An understanding of ocular biomechanics is essential to appreciate the molecular structure of the anterior and posterior segments of the eye and their role in maintaning corneal shape, refractive power and visual acuity. Energy storage, transmission and dissipation are essential elements of normal mechanical homeostasis. Vibrational Optical Coherence Tomography (VOCT) was used to study the viscoelasticity of the anterior and posterior segments of the porcine eye. Our VOCT results indicate that both the cornea and retina are highly viscoelastic tissues that can dissipate large amounts of applied energy to support mechanical homeostasis of the anterior and posterior segments of the eye. We conclude that a relationship exists between the anterior cornea-limbus-scleral series biomechanical unit and the posterior sclera-retina complex that assists in energy dissipation. This relationship limits structural changes in the eye and supports delicate ocular posterior segment structures like the retina and optic nerve from acute or chronic insult

Keywords: Cornea; Sclera; Limbus; Retina; Optic nerve; Bruch’s membrane; Choroid; Lamina cribrosa; Viscoelasticity; Loss modulus; Elastic modulus; Stiffness; Collagen

Introduction

Energy storage, transmission and dissipation are important functions that prevent cornea delamination and mechanical damage to the visual components in the posterior segment of the eye [1]. Significant scleral thinning and tissue loss, particularly at the posterior pole of the eye, has been associated with ocular enlargement and myopia development [2] while the shape of the posterior sclera has been viewed as a sign of open-angle glaucoma [3]. Scleral thinning may be due to tensile stretching and creep of the sclera as a result of external and internal forces that act on the cornea-limbus-scleral biomechanical unit [1].

On earth, all ocular tissues experience gravitational forces that exceed 760 mm Hg. Gravitational and other external forces must be offset by internal forces within the eye, or the entire globe would deflate. The loss of gravity has been reported to cause the globes of astronauts to flatten and the optic nerve length to change, resulting in modification of the location of the optic nerve head [4,5]. In addition to gravity, the cornea experiences several other forces including shearing, lid pressure, surface tension associated with the tear film, extraocular muscle stress, intraocular pressure, and tension in the cornea due to internal stretching [1]. In dermal tissue the balance between internal and external stresses has been reported to modulate mechanotransduction and the balance between tissue atrophy and tissue deposition [6]. Blunt external forces acting on the cornea cause corneal deformation. The cornea must store and then transmit this energy to the anterior and posterior segments of the eye to prevent corneal delamination and tearing. If this energy is not dissipated, mechanical fatigue and structural failure of both anterior and sensitive posterior segment structures like the retina and optic nerve may result. Since the cornea does not delaminate during blunt trauma, this energy must be transmitted to other parts of the eye where it is dissipated. It has been proposed that this energy is transmitted through the attachments of the cornea and limbus to the posterior sclera [1]. It is important to understand how and where this energy is dissipated in the eye since any anatomic changes that occur to the posterior scleral connection to the optic nerve could lead to a loss of visual acuity.

While energy storage, transmission and dissipation have been addressed in tissues including skin, tendon, muscle, blood vessels and cartilage [6-12], very little attention has been paid to how energy is stored, transmitted, and dissipated in the eye. While the cornea is the major tissue that protects the visual components in the anterior and posterior segments of the eye from mechanical damage, it is in series mechanically with the limbus and sclera [1]. Recently it was pointed out that the corneal-limbus-scleral biomechanical unit and the integration of the circumferential and collagen fibrillar networks in the cornea are important in preventing corneal delamination [1]. This mechanism of energy dissipation was further hypothesized to protect the cornea from changes in shape, curvature, and therefore, refractive power. Ultimately, energy dissipation of both external and internal forces acting on the globe and the mechanical connection between the anterior and posterior segments may lead to thinning of the sclera and be associated with several ocular diseases [13].

Energy storage, transmission and dissipation by mammalian tissues has been elucidated by x-ray diffraction and biomechanical studies on both tendon, skin and cartilage [14-18]. These properties are a consequence of the viscoelasticity of the macromolecular components found in extracellular matrices [19]. They are related to the ability of extracellular matrices to undergo reversible stretching of the collagen triple helix (energy storage), reversible stretching of collagen molecules and crosslinks, and sliding of the quarter-staggered collagen molecules [14-18]. These deformation mechanisms increase the D period (energy storage and transmission), and result in energy dissipation through sliding and rearrangement of both water and proteoglycans surrounding collagen fibrils [14-20].

Previous pilot studies on both human and porcine eyes indicate that they have similar mechanovibrational peaks and moduli; however they do differ in the resonant frequency peak amplitudes at 80, 120, 150 and 250 Hz [1,21]. The resonant frequencies of cellular, fibrillar collagen, blood vessels, and fibrotic collagen are related to their elastic moduli (stiffness) [1] and changes in resonant frequency and modulus may be used as markers of skin and other tissue pathologies [22,23]. While It is known that the stroma of porcine cornea is much thicker than that of human corneas, the porcine eye has been used as a good model of the anatomy and mechanical behavior of the human eye. The similarity between the resonant frequency peaks near 80, 120, 150 and 250 Hz of human and porcine corneas, sclera and limbus, suggest that the anatomically described layers in these tissues are connected in a single biomechanical unit that can store external mechanical energy with transmission to the posterior segment of the eye for dissipation [1].

In this publication, we compare the viscoelasticity of both the anterior and posterior segments of porcine eyes in order to determine which parts of the eye are able to dissipate large amounts of energy as a result of external and internal mechanical loading. In addition, the resonant frequency and elastic modulus of excised components of porcine eyes are measured to further characterize the biomechanical properties of individual components of the eye.

Materials and Methods

Resonant Frequency and Elastic Modulus Measurements

Vibrational Optical Coherence Tomography (VOCT) is a technique that uses infrared light that is reflected to a detector from different depths in a tissue to create an image. By applying an acoustic force and measuring the change in displacement of the tissue components, it is possible to calculate the component tissue stiffnesses [1,20-23]. The experimental setup for VOCT is shown in Figure 1. A stiffer component will have a larger displacement than a softer component under a fixed load. The weighted displacement of a tissue is obtained after correction for the displacement of the speaker, background noise, and out-of-phase vibrations (viscoelasticity) as a function of frequency to isolate the elastic response. The normalized weighted displacement is a unitless number and is the ratio of the displacement of the sample divided by the displacement in the absence of the sample. Mechanovibrational VOCT spectra were collected on porcine whole globes and excised components of the porcine eyes in vitro. 30 fresh porcine eyes were obtained from Spear products (Coopersburg, PA USA) and kept on ice during transport for testing. The pigs weighed 220 to 280 lbs. and were 6 to 12 months old. Porcine eyes were studied using VOCT within 4 hours of harvesting at Ben Franklin Tech Ventures (Bethlehem, PA, USA). It was noted that the excised corneal thickness increased after excision even when kept on ice. The porcine eyes were studied intact after removal of the extraocular muscles and conjunctiva, as well as after the cornea, and parts of the cornea and posterior segment were removed by dissection.