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Research Papers

Biomechanics of the Posterior Eye: A Critical Role in Health and Disease

[+] Author and Article Information
Ian C. Campbell

Wallace H. Coulter Department of
Biomedical Engineering,
Georgia Institute of Technology and
Emory University,
Atlanta, GA 30332;
Rehabilitation Research and
Development Center of Excellence,
Atlanta VA Medical Center,
1670 Clairmont Road,
Decatur, GA 30032

Baptiste Coudrillier

Wallace H. Coulter Department of
Biomedical Engineering,
Georgia Institute of Technology and Emory University,
Atlanta, GA 30332

C. Ross Ethier

Wallace H. Coulter Department of
Biomedical Engineering,
Georgia Institute of Technology and Emory University,
Atlanta, GA 30332;
Rehabilitation Research and
Development Center of Excellence,
Atlanta VA Medical Center,
1670 Clairmont Road,
Decatur, GA 30032;
Department of Ophthalmology,
School of Medicine,
Emory University,
Atlanta, GA 30322;
Department of Bioengineering,
Imperial College London,
London SW7 2AZ, UK
e-mail: ross.ethier@bme.gatech.edu

1Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the Journal of Biomechanical Engineering. Manuscript received September 10, 2013; final manuscript received December 15, 2013; accepted manuscript posted December 19, 2013; published online February 5, 2014. Editor: Victor H. Barocas.

J Biomech Eng 136(2), 021005 (Feb 05, 2014) (19 pages) Paper No: BIO-13-1422; doi: 10.1115/1.4026286 History: Received September 10, 2013; Revised December 15, 2013; Accepted December 19, 2013

The posterior eye is a complex biomechanical structure. Delicate neural and vascular tissues of the retina, choroid, and optic nerve head that are critical for visual function are subjected to mechanical loading from intraocular pressure, intraocular and extraorbital muscles, and external forces on the eye. The surrounding sclera serves to counteract excessive deformation from these forces and thus to create a stable biomechanical environment for the ocular tissues. Additionally, the eye is a dynamic structure with connective tissue remodeling occurring as a result of aging and pathologies such as glaucoma and myopia. The material properties of these tissues and the distribution of stresses and strains in the posterior eye is an area of active research, relying on a combination of computational modeling, imaging, and biomechanical measurement approaches. Investigators are recognizing the increasing importance of the role of the collagen microstructure in these material properties and are undertaking microstructural measurements to drive microstructurally-informed models of ocular biomechanics. Here, we review notable findings and the consensus understanding on the biomechanics and microstructure of the posterior eye. Results from computational and numerical modeling studies and mechanical testing of ocular tissue are discussed. We conclude with some speculation as to future trends in this field.

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References

Figures

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Fig. 1

Overview of the eye, including some tissues important in glaucomatous optic neuropathy. (a) Micro-MRI image of the human eye. The typical radius of the eye is 12.5 mm. The lens is the biconvex structure in the anterior portion of the eye (left side of the panel) and is covered by the cornea on the exterior of the eye. The sclera, which appears black in this imaging modality, can be clearly distinguished from the other tissues. The contour of the retina is also visible, in light gray, attached to the innermost layer of the sclera. Some details of the optic nerve can be detected, such as the pia matter, a sheath of connective tissue enclosing the optic nerve posterior to the sclera (right side of the panel). The optic nerve exits the eye posteriorly via the scleral canal, carrying visual signals to the brain. The boxed region is the optic nerve head (ONH). (Image courtesy of Mr. Richard Norman.) (b) Histologic cross-section of the ONH showing the retina (dark gray at left), the peripapillary sclera (bright tissue at top and bottom), the lamina cribrosa (boxed in red, which spans the scleral canal like a hammock), and the columns of axon bundles in the posterior laminar region en route to the brain (middle right). (Reproduced with permission from Sigal et al. [205]. Image: ARVO.) (c) En face scanning electron micrograph of the human lamina cribrosa, showing connective tissue elements only. Axon bundles, which normally pass through the pores, have been digested away. Individual beams and pores are visible, and the typical “hourglass” organization of the pores is highlighted (dashed red line). The average LC radius is 0.85 mm. (Reproduced with permission from Quigley et al. [59]. Image: Elsevier.)

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Fig. 2

Intraocular pressure (IOP) is dynamic, fluctuating in response to external forces on the globe. Actions such as blinking, squeezing, rubbing, and moving the eye all acutely alter the IOP by significant amounts. Additionally, pulsation of systemic blood pressure results in a periodic change in the IOP, which is termed the ocular pulse. This ocular pulse magnitude is approximately 20% of the mean IOP. Based upon data from Ref. [20].

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Fig. 3

Histologic section through the ONH, showing the retina (R), the choroid (C), the peripapillary sclera (ppS), the lamina cribrosa (LC) (outlined in black), the post-laminar tissue of the optic nerve (pLC), and the vitreous chamber inside of the eye (VH) for (a) a normal ONH, and (b) a glaucomatous ONH. Note that the retina has artifactually separated from the choroid in some regions of the image in (a). Glaucoma is clinically characterized by the cupping of the ONH, which results from the loss of RGC axons and from thinning and the permanent posterior bowing of the LC. Scale bar: about 0.75 mm. (Reproduced with permission from Ref. [64]. Images: ARVO.)

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Fig. 4

Histologic sections of a normal ONH fixed at (a) 5 mm Hg, and (b) 50 mm Hg (original magnification 35×). The LC significantly bows backward at 50 mm Hg, yet its thickness is not noticeably different between the two pressures. (c) Interpretation of the deformation mechanisms of the LC. The similar deformed thickness and significant bowing together suggest that shear deformation dominates in the peripheral LC, while tensile deformation dominates in the central LC. (Reproduced with permission from Yan et al. [85]. Image: BMJ Publishing Group.)

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Fig. 5

(a) Enhanced depth imaging SD-OCT image showing a cross-section through a normal monkey ONH (top). The bottom panel shows the same image with delineations: (green) anterior surface of the retina, (blue) posterior surface of the retinal nerve fiber layer (RGC axons), (orange) posterior layer of retina/Bruch's membrane complex, (yellow) posterior layer of the sclera, (red) neural canal (also called the scleral canal) opening, (purple dots) anterior limit of the LC, and (yellow dots) posterior limit of the LC. (Reproduced with permission from Yang et al. [94].) (b) Adaptive optics scanning laser ophthalmoscope image of the primate ONH, as viewed en face. Individual LC pores and beams are visible. Scale bar = 0.2 mm. (Reproduced with permission from Ivers et al. [95]. Images: ARVO.)

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Fig. 6

(a) (top left) Cross-section of a specimen-specific finite element model of the ONH region, constructed from serial histology images (superimposed), (top right) 3-dimensional finite element model, (bottom) cross-sections of the finite element model at low IOP (5 mm Hg) compared to the cross-section of the model at elevated IOP (50 mm Hg). This model demonstrated a rotation of the sclera, elongation and thinning of the LC and neural tissue, and a posterior bowing of the LC. (Reproduced with permission from Sigal et al. [206,207]. Images: Elsevier.) (b) Multiscale model of the LC microarchitecture. Micro-scale modeling of the LC beam deformations was informed from the results obtained from the macro-scale. This method predicted that the stresses and strains in the beams were considerably larger than those obtained by modeling the LC as a homogeneous tissue. (Reproduced with permission from Downs et al. [109]. Image: IEEE.)

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Fig. 7

Imaging of the sclera microstructure at multiple length-scales. (a) Transmission electron micrograph of two rabbit scleral collagen fibrils. The characteristic D-period of the collagen fibril is clearly visible. The black filaments bridging between two adjacent fibrils are proteoglycans. (Adapted with permission from Young et al. [208]. Image: Company of Biologists.) (b) Transmission electron micrograph showing a transverse section of collagen lamellae in the outer, mid, and inner sclera of the normal tree shrew. Note the large variations in collagen diameters and spacing within and between each region. (Reproduced with permission from McBrien et al. [187]. Image: ARVO.) (c) Electron micrograph image of the human sclera showing six superimposed lamellae. Within each lamella, collagen fibrils run in the same direction. Large angle variations are observed between adjacent lamellae, and fibroblasts occupy the interlamellar space. (Reproduced with permission from Fig. 7.55 in Wolff [209]. Image: Chapman & Hall Medical.) (d) Scanning electron micrograph of the collagen bundles in the outer sclera of the human eye. (Reproduced with permission from Komai et al. [118]. Image: ARVO.) (e) Montage of 15 × 15 second harmonic generation multiphoton images of the human peripapillary sclera showing that in this region, collagen lamellae are preferentially oriented in the circumferential direction. (f) A composite polar plot showing the preferred orientations of aligned collagen fibers for a human sclera. The color scale conveys the degree of fiber alignment. (Figures 4(e) and 4(f) are reproduced with permission from Pijanka et al. [119]. Images: ARVO.)

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Fig. 8

Fibroblasts are abundant in rat scleral tissue. In this maximum intensity projection (140 slices stacked, each 1 μm thick) of rat sclera stained with the dye Draq5, red dots represent individual nuclei in the sclera. Here, the posterior sclera of an enucleated rat eye was mounted flat on a glass slide, and cellular layers of the inner eye such as the choroid and retina were removed by scrubbing with a cotton swab. Remaining nuclei are attributed to scleral fibroblasts.

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Fig. 9

Multiple mechanical interrogation modalities have been employed to derive the material properties of scleral tissue. (a) Uniaxial tensile testing of scleral strips immersed in a tissue bath yields estimates of the scleral modulus, although sample preparation may alter the collagen structure, and the imposed load may not be physiological. (Image used with permission from Geraghty et al. [135]. Image: Elsevier.) (b) Biaxial testing of samples requires a more complex testing setup but is more likely to reproduce physiological loading conditions. Here, BioRakes (tungsten wires) are used to anchor the specimen for simultaneous loading in two directions, and optical tracking of black dots on the surface is used to spatially resolve strain. (Image courtesy of Dr. Armin Eilaghi [152].) (c) Inflation testing was developed to reduce tissue preparation and impose physiological loading conditions. At left, schematic of the inflation protocol from Ref. [160]; the posterior scleral shell is glued into a plastic holder and anchored in a chamber capable of controlling both humidity and pressure. At right, a photo of a transilluminated human sclera mounted in the chamber and speckled with graphite powder for optical tracking by CCD cameras during DIC (see Ref. [160]; image: ARVO, used with permission). Other inflation protocols use similar setups with notable differences in the image acquisition technique, such as a laser for ESPI [163] or an ultrasound probe [169,170].

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Fig. 10

Micro-magnetic resonance imaging (MRI) images of the human eye segmented to produce a 3D rendering of the globe annotated with wall thickness. Here, letters denote the orientation of the eye: S, superior; I, inferior; N, nasal; T, temporal; P, posterior; and A, anterior. Thickness varies regionally, with the temporal quadrant of the posterior sclera being significantly thicker than that in the nasal quadrant. The sclera is thinnest around the equator, becomes thicker posteriorly, and then becomes thin again in the peripapillary region immediately adjacent to the optic nerve head. (Adapted with permission from Norman et al. [178]. Image: Elsevier.)

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