The Shape of the Sclera Using Swept-source OCT in Eyes With Pathologic Myopia

Kyoko Ohno-Matsui, MD, PhD, is an associate professor in the Department of Ophthalmology and Visual Science at Tokyo Medical and Dental University and chief of the High Myopia Clinic at Tokyo Medical and Dental University. She reports no financial interest in any products mentioned in this article. Dr. Ohno-Matsui can be reached via e-mail at k.ohno.oph@tmd.ac.jp.

Kyoko Ohno-Matsui, MD, PhD

Pathologic myopia is a major cause of visual impairments worldwide.^1-6 These visual impairments are mainly caused by different types of myopic lesions in the retina and choroid, especially in the macula and optic disc areas.^7-9

Although the mechanism that causes the development of myopic lesions is not clear, we recently analyzed the shape of the external surface of highly myopic eyes by high-resolution three-dimensional magnetic resonance imaging (3D MRI).^10,11 We found that highly myopic eyes were not simply elongated but had out-pouched areas, especially in their posterior poles.

We also found that visual field defects that were not due to myopic fundus lesions were present significantly more frequently in eyes with temporally distorted shapes than with distortions in other areas.¹⁰ These results suggest that the eye shape might be related to visual impairments in the patients with pathologic myopia.

 

 

 

Figure 1. Observations of the sclera and Tenon’s capsule in highly myopic eyes by sweptsource OCT. (A, C) The sclera is observed as the highly reflective tissue outside the very thin choroid. Less reflective tissue can be seen outside the sclera. Orbital fat tissue is also observed as grayish tissue with many dots. (B, D) Schematic drawings of (A) and (C), respectively, with the tissues labeled. The sclera is colored orange, and the tissue outside the sclera, suggestive of Tenon’s capsule and episclera, is colored brown. (E, F) The fibers (arrows) of Tenon’s capsule appear to spread and blend into the orbital fat tissue posteriorly. Crosssections of episcleral blood vessels can be seen posterior to the sclera (arrowhead, E).

IMAGING ESSENTIALS

In obtaining 3D MRI images of the eye, it is necessary to use T2-weighed images, which represent the fluid-filled chamber in the eye, to obtain high-contrast images. Thus, in a strict sense, this method does not show the contour of outer shell of the eye.

Recent advances in optical coherence tomography have enabled investigators to image the tissues deeper than the neural retina, such as the choroid and sclera.¹² Especially in eyes with pathologic myopia, the retina and choroid of which are very thin, it is possible to observe the entire thickness of the sclera. Thus, this review will show observation of the sclera and scleral vessels using sweptsource OCT.

 

 

 

Figure 2. Different curvature patterns of the inner scleral surface in emmetropic eyes. The curves of the inner scleral surface and retinal pigmented epithelium are not necessarily the same because a thick choroid exists between the RPE and sclera. (A) Horizontal scan through the central fovea shows the RPE line is almost straight and slopes toward the optic nerve. The curvature of the inner scleral surface (arrowheads) bows slightly and symmetrically around the fovea. (B) Vertical scan through the central fovea of the same eye in (A) shows the RPE line is almost straight. The curve of the inner scleral surface (arrowheads) bows slightly and symmetrically around the fovea. (C) Horizontal scan through the central fovea shows the RPE line bows slightly and the fovea is situated on the bottom of RPE curve. The curvature of the inner scleral surface (arrowheads) bows slightly and symmetrically around the fovea. (D) Vertical scan through the central fovea of the same eye in (C) shows the RPE line bows slightly. Curvature of inner scleral surface (arrowheads) bows slightly and symmetrically around the fovea.

OBSERVATION OF SCLERA, EPISCLERA, TENON’S CAPSULE, AND ORBITAL FAT BY OCT

The sclera is observed as a relatively uniform, hyperreflective structure exterior to the thin choroid on sweptsource OCT images (Figure 1).¹³ We were also able to observe the retrobulbar orbital fat beyond the sclera in eyes with pathological myopia.

 

 

 

Figure 3. Four distinct patterns of inner scleral curvature in highly myopic eyes. Due to a very thin choroid, the curvatures of the inner scleral surface and RPE are almost identical, although the RPE can be atrophied in some cases. (A) The curvature slopes toward the optic nerve: The curve of the inner scleral surface is straight, and the optic disc is at the bottom of the posterior segment. This pattern is more obvious on horizontal scans than on vertical scans. The central fovea (arrowhead) is on the wall of the slope inclined toward the optic nerve. (B) The curvature is symmetrical around the fovea: The sclera is strongly bowed posteriorly; however, the curve is symmetrical around the fovea (arrowhead), which is situated on the bottom of the posterior segment. (C) Asymmetrical curvature around the fovea: The sclera is strongly bowed posteriorly, and the most protruded point is away from the central fovea. The fovea (arrowhead) is on the slope. (D) Irregular curvature: The sclera is irregular and does not have smooth curvature. The yellow arrowhead indicates the fovea, the white arrowhead indicates the intrascleral artery (ON = optic nerve; SAS = subarachnoid space).

Close observation of the deeper tissues showed a relatively hyporeflective layer outlining the sclera (Figure 1). This hyporeflective layer was in close contact with the outer surface of the sclera and appeared to break up into smaller bundles and blend into the orbital fat tissue posteriorly. From these morphological features, the hyporeflective layer was considered to be the episclera and Tenon’s capsule.

The mean subfoveal scleral thickness was 227.9 ±82.0 μm, with a range of 80 to 546 μm in the 246 eyes we observed with pathologic myopia (mean axial length: 30.7 mm; mean age; 60.9 years old).¹³

Curtin⁷ used histological studies to show that the scleral thickness at the posterior pole of normal eyes with axial lengths between 22 and 24 mm was 660 μm, whereas it was 233 μm in myopic eyes with an axial length of 27.8 mm. Thus, the data obtained using swept-source OCT are compatible with the data in human cadaver eyes.

In highly myopic eyes, the subfoveal scleral thickness was significantly greater than that at 3 mm temporal to the fovea, than that at 3 mm upper to the fovea, and than that at 3 mm lower to the fovea. The cases with domeshaped maculas or with tilted disc syndrome were excluded from the analyses.

 

 

 

Figure 4. Different patterns of scleral curvature in eyes classified as having irregular curvature. (A) The sclera nasal to the most protruded point is extremely thin, and the scleral curvature is not spherical. The central fovea is on the slope (arrowhead). (B) The scleral curvature is bent at the site of the central fovea (arrowhead). (C) The scleral curvature is similar to that in (A); however, the curvature is more linear, and the transition of the change in curvature is more acute. The central fovea is on the slope (arrowhead). (D) The scleral thickness is irregular, and the sclera is acutely displaced posteriorly beside the central fovea, indicated by the arrowhead. (E)The sclerais extremely thin, and the scleral curvature is entirely irregular. The central fovea (arrowhead) is almost centered in the irregular curvature.

SHAPE OF THE POSTERIOR SCLERAL SURFACE IN EMMETROPIC EYES

In emmetropic eyes, the curvature of Bruch’s membrane was not similar to the curvature of the inner scleral surface, mainly because the choroid was thick and the choroidal thickness affected the scleral curvature.

The curvature of the retinal pigment epithelium and Bruch’s membrane in emmetropic eyes had two patterns; the contour was straight and sloped toward the optic disc (Figures 2A and 2B) or had a roughly symmetrical curvature centered on the fovea (Figures 2C and 2D).

Despite the different patterns of curvature of the RPE and Bruch’s membrane, the curvature of the inner scleral surface was always symmetrical and mainly centered on the fovea.

 

 

 

Figure 5. Classification of ocular shape based on 3D MRI viewed from the inferior. (A) Nasally distorted type: The nasal and temporal halves of the posterior segment are asymmetrical; the nasal half protrudes more posteriorly than temporally. (B) Temporally distorted type: The nasal and temporal halves of the posterior segment are asymmetrical, and the temporal half protrudes more than the nasal half. (C) Cylindrical type: The nasal and temporal halves of the posterior segment are symmetrical, and the radii of the curvatures of both halves are steeper than a circle. (D) Barrel type: The nasal and temporal halves of the posterior segment are symmetrical, and the radii of the curvatures of the both halves are flatter than a circle.

VARIATIONS OF SCLERAL SHAPE IN EYES WITH PATHOLOGIC MYOPIA

Contrary to emmetropic eyes, the contour of the inner scleral surface in eyes with pathologic myopia had four distinct patterns (Figure 3). The first pattern was one in which the curvature sloped toward the optic disc and the optic disc was at the bottom of the curvature (Figure 3A).

In the second pattern, the curvature of the inner scleral surface was symmetrically centered on the fovea, and the fovea was situated in the center and at the bottom of the curvature (Figure 3B).

The first two patterns appeared to be similar to the contour of the RPE and Bruch’s membrane in emmetropic eyes, although the degree of curvature was greater in the highly myopic eyes. These findings suggested the possibility that the symmetrical shape around the fovea and sloping toward the optic disc might be an exaggeration of the normal curvature of the RPE and Bruch’s membrane seen in emmetropic eyes.

In highly myopic eyes with very thin choroids, the scleral curvature was almost identical to the RPE curve. We suggest that when an eye elongates without forming a staphyloma, the patterns may be the same as those seen in emmetropic eyes but more exaggerated in highly myopic eyes.

In contrast, the other two patterns were observed only in highly myopic eyes. The third pattern was one in which the contour of the inner scleral surface was curved posteriorly, with the curvature asymmetrical around the central fovea. The fovea was not situated at the bottom of the curvature but on the slope of the wall (Figure 3C).

 

 

 

Figure 6. Relationship between highly myopic eyes with the scleral curvature sloped toward the optic nerve, by OCT, and a nasally distorted eye, by 3D MRI. (A) The left fundus of a 71-year-old woman with a myopic refractive error of ·9.50 D and axial length of 26.6 mm. Photograph shows a ring conus around the optic disc and mild chorioretinal atrophy in the macula. Yellow line shows OCT scan line used in (B). (B) Horizontal OCT scan shows RPE and curvature of the inner scleral surface are almost straight and slope toward the optic nerve (scale bar = 1 mm). (C) Inferior view of 3D MRI image shows globe elongated slightly nasally and the optic nerve (arrow) attached at the most protruded part of the globe. (D) Posterior view of 3D MRI image shows optic nerve (arrow) is attached at the center of the globe protrusion.

In the eyes with asymmetrical curvature around the central fovea, the most protruded point was almost always present inferiorly, including temporally and nasally inferior to the fovea. The foveas in these eyes were located on the superior slope of the curvature.

These findings indicate that the inferior sclera expands more in highly myopic eyes. The sclera in the lower half of the eye is where embryonic ocular fissure closes. Thus, it might be possible that this part of the sclera is structurally weaker than other areas. It is also suggestive of some similarities between pathologic myopia and tilted disc syndrome.

During staphyloma development, the greater expansion of the inferior sclera, compared to other parts of the sclera, can cause a shift of the most protruded part from the subfovea to the inferior fundus. In turn, the fovea can shift onto the upper slope of the sclera.

The final pattern was the type in which the contour of the inner scleral surface was irregular and did not form a smooth circular arc (Figure 3D). In extreme cases, the curvature of the posterior eye segment was totally irregular (Figure 4).

 

 

 

Figure 7. OCT image of a highly myopic eye with irregular curvature of the sclera, and 3D MRI image showing temporally distorted eye. (A) Photograph of the left fundus of a 74-year-old woman with an axial length of 32.4 mm (intraocular lens-implanted eye) showing severe chorioretinal atrophy in the macula. Yellow lines indicated scanned lines by OCT in (B), (C), and (D). (B) Horizontal OCT image showing that the sclera is thin and not spherical. The orbital fat tissue is clearly seen posterior to the sclera. Macular retinoschisis is seen around the central fovea (arrowhead). Scale bar = 1 mm. (C, D) OCT image from a vertical scan (C) and image from an oblique scan (D). The scleral contour is not spherical, and the most protruded point is located inferior to the central fovea (arrowhead). Macular retinoschisis can also be seen. Scale bars = 1 mm. (E) Inferior view of a 3D MRI image of the eye shows that the posterior segment of the globe is temporally dislocated. The optic nerve (arrow) is attached nasally to the protrusion (arrowheads) of the globe. (F) Posterior view of 3D MRI image of the eye shows that the optic nerve (arrow) is attached nasally to the protrusion (surrounded by arrowheads).

CLINICAL CHARACTERISTICS OF EYES WITH DIFFERENT SCLERAL SHAPES

Statistical analyses have shown that patients with irregular curvature were significantly older and significantly more myopic with significantly longer axial lengths than those who showed the other patterns. The subfoveal sclera was thinnest in the eyes with irregular curvature, followed by the eyes with symmetrical curvature, those with asymmetrical curvature, and those with curvature sloping toward the optic disc.

We suggest that when the sclera is stretched and becomes extremely thin, it can no longer maintain its normal curvature. This would contribute to the development of myopic fundus lesions. Thus, irregular curvature might be the most severe and advanced form of pathologic myopia.

Chorioretinal atrophy, patchy atrophy or macular atrophy, and myopic choroidal neovascularization were observed significantly more frequently in eyes with irregular curvature than in any other group. Myopic traction maculopathy was observed most frequently in eyes with irregular curvatures, followed by those with asymmetrical curvatures, symmetrical curvatures, and curvatures sloping toward the optic disc, respectively.

CORRELATION BETWEEN GLOBE SHAPE DETERMINED BY 3D MRI AND INNER SCLERAL SURFACE CONTOUR DETERMINED BY OCT

Using 3D MRI, we showed that the shape of highly myopic eyes had four distinct patterns of distortion: nasal, temporal, cylindrical, and barrel-type (Figure 5).¹⁰ Thus, we observed that the eyes with different scleral shapes on swept-source OCT were those in which 3D MRI determined their shapes.

Among the eyes with scleral curvatures inclined toward the optic disc, none were horizontally symmetrical, and all were the nasally distorted type (Figure 6). Among the eyes with symmetrical curvatures, all were horizontally symmetrical, and 75% were sagittally symmetrical as well. Among the eyes with asymmetric curvature, most of the eyes had the inferiorly distorted shape. Among eyes with irregular curvature, most of the eyes had the temporally distorted type (Figure 7).

 

 

 

Figure 8. Schematic illustration of our hypothesis on how eye deformities on the horizontal plane progress in pathologic myopia, based on 3D MRI imaging and results obtained by sweptsource OCT. Top row: In emmetropic eyes, two different curvature patterns of the RPE and Bruch’s membrane (shown as blue line) are evident: Straight sloping of the sclera toward the optic nerve and mildly bowed centered on the fovea. However, the curvature of the inner scleral surface (red line) bows mildly posteriorly and always symmetrical around the fovea. This is due to the thick choroid affecting the curvature of the inner scleral surface in emmetropic eyes.

 

 

 

Middle row, left: In the symmetrically elongated highly myopic eye, when the eye elongates around the fovea, the symmetric curve of sclera seen in emmetropic eyes is exaggerated. The central fovea is on the most protruded point of the sclera. Right: In the nasally dislocated eye in high myopia, when the eye elongates toward the optic nerve, the curvature of the inner scleral surface has an exaggeration of the RPE and Bruch’s membrane slope, as seen in the top row, right figure. The curvature of the inner scleral surface is almost straight and slopes toward the optic nerve.

 

 

 

Bottom row: In the temporally dislocated eye in high myopia, when the sclera thins and expands further, the very thin sclera can no longer maintain the curvature, and an irregular curvature results, as seen in the OCT image. The area temporal to the central fovea appears to expand more and shows a temporally dislocated type on 3D MRI of the globe. The curvature of the inner scleral surface is shown as a red line, and the central fovea is indicated by an arrowhead in each image. (ON = optic nerve; SAS = subarachnoid space.)

When the results of 3D MRI analyses and OCT findings are combined, the temporally dislocated eyes might have represented a condition in which the sclera is extremely thinned and becomes irregular in contour at an advanced stage of pathologic myopia with a deep staphyloma.

Schematic illustrations of our hypothesis of how eye deformities progress in pathologic myopia, based on the 3D MRI findings in our earlier study^10,11 and the swept-source OCT results in this study, are shown in Figures 8 and 9.

Despite the two different curvatures of the RPE and Bruch’s membrane in emmetropic eyes, the curvature of the inner scleral surface was mildly bowed posteriorly and consistently symmetrical around the fovea (Figure 8, top row).

When the eye simply elongates around the fovea or elongates toward the optic nerve, the curvature of the inner scleral surface, as well as the curvature of Bruch’s membrane in highly myopic eyes, had an exaggeration of the patterns of the RPE and of Bruch’s membrane curvature seen in emmetropic eyes (Figure 8, middle row).

When a posterior staphyloma develops in later life, the posterior sclera tends to expand in a nonuniform fashion, and, specifically, the lower sclera tends to expand more than other parts of the sclera (Figure 9, right). This causes a shift of the most protruded point from the subfovea to the inferior fundus, and the fovea tends to move onto the superior slope.

When the sclera thins and expands further in extremely myopic eyes, the very thin sclera can no longer maintain the curvature, and this results in an irregular curvature (Figure 8, bottom row). A long-term study on the course of deformation of eyes with pathologic myopia is necessary to support our hypothesis.

 

 

 

Figure 9. Schematic illustrations of our hypothesis on how eye deformities on the sagittal plane progress in pathologic myopia based on 3D MRI and swept-source OCT vertical scans. Left: In an emmetropic eye, the globe is spherical by 3D MRI, and the vertical OCT scan shows the curvature of the inner scleral surface bows mildly and symmetrically around the central fovea. Middle: When a symmetrically elongated highly myopic eye simply elongates along the central axis, the symmetrical curvature of the sclera, seen in emmetropic eyes, is exaggerated. The scleral curvature bows more posteriorly, and the central fovea is on the most protruded point of the sclera. Right: In the inferiorly distorted eye with high myopia, when a posterior staphyloma develops in later life, the posterior sclera expands nonuniformly, and the lower sclera tends to expand more than other parts of the sclera. This causes a shift of the most protruded point, from the subfovea to the lower fundus, and the fovea tends to move onto the upper slope. The red line represents the curvature of the inner scleral surface, and the arrowhead depicts the central fovea.

CONCLUSION

Thanks to recent advancements in OCT, the scleral shape has now been observed in detail in in situ human eyes, and the associations between the changes in scleral shape and the vision-impairing complications of pathologic myopia have been clarified.

This information, obtained by ocular imaging, is considered critically important in the establishment of new treatment strategies targeting the sclera, which is the most affected site in pathologic myopia. RP

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