Observations of Vascular Structures within and Posterior to Sclera in Eyes with Pathologic Myopia by Swept-Source Optical Coherence Tomography

Abstract

Purpose.: We examined the intrascleral and retrobulbar blood vessels in highly myopic eyes by swept-source optical coherence tomography (swept-source OCT).

Methods.: We included in the study 662 of 357 patients with pathologic myopia (spherical equivalent of myopic refractive error ≥ 8.00 diopters or axial length > 26.5 mm). A swept-source OCT system that uses a wavelength sweeping laser with A-scan repetition rate of 100,000 Hz and 1 μm wavelength was used. Radial scans along 12 meridians of 12 mm scan length centered on the fovea were made. Indocyanine green angiography (ICGA) also was performed to identify the intrascleral and retrobulbar vessels that were observed by swept-source OCT.

Results.: Intrascleral and retrobulbar blood vessels were observed in the macular area of the highly myopic eyes. Linear hyporeflective structures running in the sclera were observed in 474 of the 662 myopic eyes, and ICGA confirmed that these structures were the long posterior ciliary arteries (LPCAs) or the short posterior ciliary arteries (SPCAs) whose entry sites into the eye were displaced toward the temporal edge of the posterior staphyloma in 50 eyes. In 36 of the 662 eyes (5.4%), cross sections of the blood vessels were seen coursing through the scleral layer. In 177 of these 443 eyes, the retrobulbar posterior ciliary arteries (PCAs) also were observed as a cluster of circular or curved hyporeflectant structures just posterior to the sclera.

Conclusions.: Swept-source OCT is a high-quality method to detect intrascleral and retroscleral blood vessels in the eyes with pathologic myopia. These findings and longitudinal studies of these vessels will help in investigating how they are altered in pathologic myopia, and how such alterations are related to the complications in the retina–choroid and optic nerve.

Introduction

Earlier indocyanine green angiographic (ICGA) studies by Quaranta et al. ¹ and our laboratory ² showed that it was possible to observe the retrobulbar arteries and veins in highly myopic eyes with thin choroid and sclera. These findings indicated that these vessels were extraocular because they moved independently of the choroidal and retinal vessels during eye movements in the ICG angiograms. ^1,2 The results of these ICGA studies indicated that the spatial distribution of the retrobulbar and intrascleral vasculature was altered in highly myopic eyes with posterior staphylomas. We showed that the entry sites of the retrobulbar short posterior ciliary arteries (SPCAs) into the choroid were displaced to the midperiphery close to the edge of a posterior staphyloma in highly myopic eyes, ³ whereas the SPCAs entered the eye in the peripapillary and macular regions in non-myopic control eyes. We also found that in approximately one-fourth of the highly myopic eyes, the vortex veins were present in the posterior fundus around the optic disc or macula, and these macular vortex veins appeared to exit the eye in the posterior fundus. ⁴ We suggested that the severe stretching and deformity of the posterior sclera by a posterior staphyloma would displace the entry or exit of the posterior ciliary arteries (PCAs), which supply and the vortex veins that drain the choroidal blood. However, because ICGA is a two dimensional (2D) examination, the retrobulbar and intrascleral existence of these vessels was not shown in a topographic relationship. 

Most studies of the retrobulbar or intrascleral vasculature have been made on histologic sections or vascular castings with methylmethacrylate of human cadaver eyes. ^2,5,6 However, in such histologic examinations, the number of eyes was limited and no information of the refractive status of the eyes was presented. 

Because of the advances in the optical coherence tomography (OCT) technology, for example, swept-source OCT ^7–13 and enhanced depth imaging (EDI)-OCT, ¹⁴ it has become possible to observe the deeper tissues, such as the choroid and sclera, of the eye. Swept-source OCT is a relatively new technique that uses a wavelength-sweeping laser as the light source ¹⁵ and has less sensitivity roll-off with tissue depth than conventional spectral domain OCTs. The current swept-source OCT instruments use a longer central wavelength, generally in the 1 μm range, which has improved their ability to penetrate deeper into tissues than the conventional spectral domain OCT instruments. A PubMed search extracted only two articles that studied the intrascleral parts of the SPCAs and long posterior ciliary arteries (LPCAs) by OCT. ^7,16 These studies reported on the intrascleral course of the SPCAs and LPCAs in situ; however, only part of the SPCAs and LPCAs near the choroidal-scleral border was visible in nonhighly myopic eyes. 

Thus, as a first step of our projects to analyze the alteration of intrascleral and retrobulbar course of the PCAs and the vortex veins in eyes with pathologic myopia, we investigated the characteristics of the blood vessels that are situated in the posterior part of the sclera in a large population of highly myopic patients by swept-source OCT. 

Methods

The procedures used in our study adhered to the tenets of the Declaration of Helsinki, and they were approved by the Ethics Committee of Tokyo Medical and Dental University. A written informed consent was obtained from all participants for the procedures used in the examinations. 

We studied 357 consecutive patients with pathologic myopia who were examined by swept-source OCT in the High Myopia Clinic at Tokyo Medical and Dental University between May 6, 2011 and February 24, 2012. The definition of pathologic myopia was a myopic refractive error (spherical equivalent) of ≥8.0 diopters (D) or an axial length >26.5 mm. All participants had comprehensive ocular examinations, including measurements of the refractive errors, axial length measurements using IOL master (Carl-Zeiss, Tubingen, Germany), detailed ophthalmoscopic examinations, and OCT. ICGA was performed using an infrared fundus camera (TRC 50 IA; Topcon, Tokyo, Japan). Only the early phase of the ICG angiograms, within 1 minute after dye injection, were examined to identify the intrascleral and retrobulbar blood vessels that had been observed by swept-source OCT. As we have reported, ² the retrobulbar blood vessels could be identified by their movements during eye movements in the ICG angiograms. Also, the intrascleral blood vessels were identified as the segments between the moving retrobulbar blood vessels and their entry into the choroid. The color fundus photographs and fluorescein fundus angiograms were used to study the same location in the fundus for comparisons of the ICGA and OCT images. 

Swept-Source OCT

All eyes were examined with a swept-source OCT prototype instrument manufactured by Topcon Corp. This OCT system has an A-scan repetition rate of 100,000 Hz, and its light source operates in the 1 μm wavelength region. The light source is a wavelength tunable laser centered at 1050 nm with a 100 nm tuning range. The axial resolution was measured to be 8 μm, the lateral resolution was 20 μm, and the imaging depth was 2.3 mm in tissue. Radial scans consisting of 12 equal meridian scans (scan length 12 mm) centered on the fovea were performed. In some cases, 7-line raster scans (scan length 6 or 12 mm) also were performed. One of the authors (MM) who was masked to the refractive status read and measured the OCT images. 

Results

We studied 714 eyes of 357 consecutive patients who were examined in our High Myopia Clinic and had undergone swept-source OCT. From these 714 eyes, 52 eyes were excluded because of poor fixation during the OCT examination due to a large macular atrophy (31 eyes), low quality OCT images due to dense cataracts (5 eyes), and history of vitreoretinal surgery (6 eyes). The remaining 10 eyes were not highly myopic due to unilateral high myopia. In the end, 662 eyes of 357 highly myopic patients were studied and their demographics are shown in the Table. The early angiographic phase, within 1 minute after injection of the ICG dye, was obtained from 177 of these eyes from 177 patients with pathologic myopia. 

Table. 

 

Patients Demographics in Groups with Pathologic Myopia

	Pathologic Myopia
Sex, N persons (eyes)
Men	181 (99)
Women	481 (258)
Age, y, mean ± SD	58.6 ± 14.2
Refractive error, D, mean ± SD	−12.6 ± 3.9
Axial length, mm, mean ± SD	29.6 ± 2.3

 N/A, not available.

Observations of Intrascleral Course of LPCAs and SPCAs

In 474 of the 662 eyes (71.6%), linear hyporeflective structures were observed in horizontal or oblique sections at the level of the sclera between the highly reflective scleral tissue and the relatively less hyperreflective tissue outside the sclera, probably the episclera (Figs. 1, 2, and see Supplementary Material and Supplementary Figs. S1, S2). The curvature of the hyporeflective structures was smooth and ran parallel to the outer surface of the sclera. 

Figure 1. 

 

Observations of the LPCAs in a highly myopic eye in images obtained by swept-source OCT and by ICGA. (A) Fundus photograph of the left eye of a 55-year-old woman with a refractive error of −10.5 D (spherical equivalent) and axial length of 29.7 mm. A large annular conus and diffuse chorioretinal atrophy can be seen in the posterior fundus. (B) ICG angiogram 10 seconds after dye injection showing intense hyperfluorescence due to retrobulbar blood vessels (between arrows). A lateral LPCA is observed as a horizontally-oriented linear hypofluorescence (arrowheads). (C) The same ICGA image as shown in (B) is shown. Arrows indicate the scanned lines for the OCT images in (D) and (E). (D) A uniform hyporeflective structure (arrowheads) can be seen to course between the scleral stroma and a slightly less hyperreflective tissue outside the sclera, probably the episclera, along the scleral curvature in a horizontal swept-source OCT section, which is along the horizontal course of LPCA observed in the ICG angiogram. (E) An oblique OCT section shows a part of the intrascleral course of a LPCA as a uniform hyporeflective structure (arrowheads) paralleling the scleral curvature. Cross sections of retrobulbar blood vessels also are seen posterior to the sclera (arrow). Scale bars: 1 mm.

Figure 2. 

 

Observations of the SPCAs in a highly myopic eye by swept-source OCT and by ICGA. (A) Fundus photograph of the right eye of a 44-year-old woman with a refractive error of −13.0 D (spherical equivalent) and axial length of 31.8 mm. Diffuse and patchy chorioretinal atrophy can be seen in the posterior fundus. (B) ICGA at 8 seconds after dye injection showing intense hyperfluorescence due to retrobulbar blood vessels (between arrows). Two SPCAs can be seen as linear hyperfluorescent structures (arrowheads) that enter the choroid and give choroidal branches at the sites indicated by the yellow arrows. (C) ICGA at 10 seconds after dye injection showing two SPCAs as linear hyperfluorescence (arrowheads). These two SPCAs enter the choroid and give choroidal branches at the sites indicated by the yellow arrows. (D) The same ICGA image as shown in (C). Arrows indicate the scanned lines by OCT for (E) and (F). (E) A uniform hyporeflective structure (arrowheads) can be seen to course between the scleral stroma and a slightly less hyperreflective tissue outside the sclera, which probably is the episclera. The structure runs along the scleral curvature in an OCT section, which is along the course of one of the 2 SPCAs (the upper one among the 2 SPCAs shown by arrowheads in C) observed by ICGA. A direct communication between the choroid and SPCA can be seen (arrow). (F) An oblique OCT section along the course of the other SPCAs (the lower one among the 2 SPCAs shown by arrowheads in C) observed by ICGA showing a uniform hyporeflective structure (arrowheads) between the scleral stroma and a slightly less hyperreflective tissue outside the sclera, probably the episclera. The SPCA runs along the scleral curvature. Scale bars: 1 mm.

Early phase of ICGA was obtained from 128 of the 474 eyes. The LPCAs were observed as horizontally-oriented hyperfluorescent vessels that were filled immediately after the filling of the retrobulbar parts of the PCAs (Fig. 1 and see Supplementary Material and Supplementary Fig. S1). Earlier, we reported that the entry sites of the SPCAs into the choroid were dislocated toward the edge of posterior staphyloma in highly myopic eyes.³ In the present study, we were able to observe the intrascleral course of SPCAs before their entry into the choroid as horizontally- or obliquely-oriented linear hyperfluorescence in the ICG angiograms (Fig. 2 and see Supplementary Material and Supplementary Fig. S2). Because the entry sites into the choroid by the SPCAs were dislocated more peripherally in highly myopic eyes, the subsequent long course within the sclera of the SPCAs tended to cause them to be misdiagnosed as LPCAs. The differentiation between LPCAs and SPCAs was done mainly by the presence of branching of the SPCAs in the posterior choroid, although earlier studies have reported variations in the branching patterns.¹⁷ Thus, when PCAs gave off branches to the choroid at or within the area of the posterior staphyloma, the vessels were taken to be SPCAs and not LPCAs. By this definition, and a comparison of the OCT and ICGA findings, the linear hyporeflective structures observed by OCT were concluded to be the LPCAs. They were seen in 78 eyes (Fig. 1 and see Supplementary Material and Supplementary Fig. S1) and SPCAs were seen in the remaining 50 eyes (Fig. 2 and see Supplementary Material and Supplementary Fig. S2). 

The entry sites of the LPCAs into the sclera were identified by OCT in 58 eyes (see Supplementary Material and Supplementary Fig. S1). In these 58 eyes, the average distance of the entry site from the outer border of the optic nerve sheath was measured with the built-in software of the swept-source OCT to be 4276 ± 1291 μm, with a range of 2034 to 5771 μm. 

Cross Sections of Blood Vessels in Sclera

In 36 of the 662 eyes (5.4%), the blood vessels coursing in the sclera were seen in cross section (Figs. 3, 4, and see Supplementary Material and Supplementary Fig. S3). All of these 36 eyes had macular chorioretinal atrophy, and the cross sections of the intrascleral blood vessels were observed only within the area of the atrophy. These cross sections were detected non-systematically in horizontal, vertical, and oblique sections. In the areas where cross sections were observed, the surrounding scleral fibrous tissue was pushed outward by the blood vessels and the sclera was split into a rhomboid–shape (Figs. 3, 4G, and see Supplementary Material and Supplementary Figs. S3G, S3H). Within this space, the tissue was slightly more hyporeflective than the adjacent scleral tissue surrounding the cross sections of the blood vessels (Figs. 3G, 4G). In some eyes, multiple cross sections of blood vessels were seen side-by-side at approximately the same depth in the scleral stroma, that is middle to relatively more posterior stroma (see Supplementary Material and Supplementary Figs. S3G, S3H). 

Figure 3. 

 

Cross sections of intrascleral blood vessels in a highly myopic eye by swept-source OCT. (A) Fundus photograph of the right eye of a 66-year-old woman with a refractive error of −18.0 D (spherical equivalent) and axial length of 31.0 mm. Macular chorioretinal atrophy can be seen. A large blood vessel is observed in the area of the macular atrophy (arrowheads). (B) ICGA at 13 seconds after dye injection showing intense hyperfluorescence due to the retrobulbar blood vessels (arrow). A horizontally-oriented PCA (arrowheads) can be seen to course parallel to the inferotemporal retinal artery. (C) The same ICGA image as shown in (B). Arrows indicate the scanned lines by OCT for (D) to (G). (D–G) Cross sections of intrascleral blood vessels are observed as circular hyporeflective structures (arrowheads) within the scleral stroma. The scleral stroma appears to be split into a rhomboid-shaped space by the blood vessels. Within this space, slightly hyporeflective tissue compared to the surrounding scleral tissue surrounds the cross sections of the blood vessels to fill the space. Scale bars: 1 mm.

Figure 4. 

 

Cross sections of intrascleral blood vessels and observation of retrobulbar blood vessels in a highly myopic eye by swept-source OCT. (A) Fundus photograph of the right eye of a 65-year-old woman with a refractive error of −20.0 D (spherical equivalent) and axial length of 30.3 mm. A large patchy chorioretinal atrophy can be seen inferior to the macula. A large blood vessel (arrowheads) can be observed in the area of chorioretinal atrophy after its entry into the sclera (arrow). (B) ICGA at 8 seconds after dye injection showing the intense hyperfluorescence due to retrobulbar blood vessels (between arrow). Intrascleral course of two SPCAs can be seen (yellow arrowheads). These SPCAs enter the choroid and give choroidal branches at the sites indicated by blue arrows. The red arrowheads show the same blood vessel that is observed within the macular atrophy in (A). (C) The same ICGA image as shown in (B). Arrows indicate the scanned lines by OCT for (D) through (G). (D) Two cross sections of retrobulbar blood vessels (arrows) are observed side-by-side posterior to the sclera within the orbital fat tissue. The spreading fibers of the episclera (yellow arrows) also are observed around the retrobulbar blood vessels. A part of the intrascleral course of SPCAs is observed as a uniform hyporeflectivity (arrowheads). (E) A slightly longer section of the retrobulbar vessels can be seen as curved hyporeflective structures (arrow). A part of the intrascleral course of SPCAs is observed as a uniform hyporeflectivity (arrowheads). (F) In an oblique OCT scan across the two SPCAs, the cross sections of two SPCAs are observed (arrow and arrowhead). The cross section of the upper one of 2 SPCAs (seen in B) is observed between the sclera and episclera (arrow) and the cross section of the lower one of the 2 SPCAs in (B) is observed intrasclerally (arrowhead). (G) In a more oblique OCT scan, the cross sections of both SPCAs are observed within the scleral stroma (arrow and arrowhead). The scleral stroma appears to be split into a rhomboid-shaped space by the blood vessels. Scale bars: 1 mm.

ICGA was obtained from 29 of 36 eyes. ICGA showed that the cross sections observed by OCT were cross sections of the intrascleral segments of the SPCAs and/or LPCAs in all of the 29 eyes (Figs. 3, 4, and see Supplementary Material and Supplementary Fig. S3). 

Observations of Retrobulbar Blood Vessels

In 177 of 662 eyes (26.7%), blood vessels were observed posterior to the sclera (Figs. 4–6 and see Supplementary Material and Supplementary Fig. S3). These retrobulbar blood vessels were seen in cross sections as a cluster of circles (Fig. 5 and see Supplementary Material and Supplementary Fig. S3). Occasionally, a longitudinal section of a retrobulbar blood vessel was seen as a curved hyporeflectivity structure (Figs. 4E, 5, 6K). Most of these blood vessels were detected between the sclera and episcleral fibrous tissue, which blended into the orbital fat tissue. 

Figure 5. 

 

Observations of a retrobulbar blood vessels in a highly myopic eye by swept-source OCT. (A) Fundus photograph of the right eye of a 62-year-old man with a refractive error of −15.0 D (spherical equivalent) and axial length of 29.0 mm. Patchy chorioretinal atrophy can be seen inferior to the macula. The inferotemporal retinal vein is indicated by arrowheads for a comparison of the same location in (A) and (B). (B) ICGA at 10 seconds after dye injection showing intense hyperfluorescence due to retrobulbar blood vessels (between arrows). Curved course of a SPCA (red arrowhead) also can be seen before giving off choroidal branches. The inferotemporal retinal vein is indicated by arrowheads for a detection of the same location in (A) and (B). (C) The same ICGA image as shown in (B). Arrow indicates the scanned line by OCT for (G). (D) Left fundus of the same patient with a refractive error of −15.0 D (spherical equivalent) and axial length of 28.7 mm. Patchy chorioretinal atrophy can be seen inferior to the macula. For an indication of location matching between (D) and (E), pigmentation along the upper edge of patchy atrophy is indicated by a white arrow and a curved narrow choroidal artery is indicated by an arrowhead. A vertically-oriented blood vessel is observed within the area of patchy atrophy (black arrow). (E) ICGA at 1 minute after dye injection showing intense fluorescence by the retrobulbar arteries (between yellow arrows). The curved course of a thin choroidal artery (arrowhead) and the pigmentation (white arrow) are indicated to clarify the location in the fundus. The long course of a vertically-oriented blood vessel is observed in the ICG angiogram (black arrows). (F) The same ICGA image as shown in (E). Long arrows indicate the scanned lines by OCT for (H) and (I). The crossing points between the horizontal scanned line and two vertically-oriented blood vessels are indicated by arrows. (G) Vertical OCT image along the scanned line in (D) shows a cross section of a SPCA (arrowhead) posterior to the sclera within the orbital fat tissue. (H) Horizontal OCT scan along the scanned line in (F) showing a cluster of cross sections of retrobulbar vessels (arrowheads) and the cross sections of two retrobulbar blood vessels (arrows; also indicated as arrows in F). (I) An oblique OCT scan showing cross sections (arrowheads) and a slightly longer curved course (red arrows) of retrobulbar blood vessels posterior to the sclera. A cross section of an intrascleral vessel can also be seen (black arrow).

Figure 6. 

 

Observations of retrobulbar blood vessels in two highly myopic eyes by swept-source OCT. (A) Fundus photograph of the left eye of a 61-year-old man with intraocular lens implanted eye and axial length of 32.4 mm. The pigmentation at the periconus choroidal neovascularization (CNV) is indicated by an arrow to match the location for (A) and (B). (B) ICGA at 8 seconds after dye injection showing intense hyperfluorescence due to the retrobulbar blood vessels (between arrowheads). The pigmentation of the CNV is indicated by an arrow. (C) The same ICGA image as shown in (B). Arrow indicates the scanned line by OCT for (D). (D) Many cross sections are seen side-by-side posterior to the sclera (arrowheads). (E) Left fundus of 56-year-old woman with intraocular lens implanted eye with an axial length of 29.7 mm showing a large annular conus and macular chorioretinal atrophy. The arrow indicates the branching point of V-shaped blood vessels as a marker to match the location in (E) through (H). (F) Fundus fluorescein angiogram at 7 seconds after dye injection showing many large arteries within the area of the macular atrophy. (G) ICGA at 6 seconds after dye injection showing intense fluorescence of retrobulbar arteries (between arrowheads). (H) ICGA at 20 seconds after dye injection showing intense fluorescence of retrobulbar arteries (between arrowheads). (I) The same ICGA image as shown in (H). Arrows indicate the scanned lines by OCT for (J) and (K). (J) and (K) OCTs show a cluster of cross sections of retrobulbar arteries (arrowheads) as well as a little long curved course of the vessels (arrows). Scale bars: 1 mm.

ICGA was performed on all 177 eyes. In the ICG angiograms of the eyes with pathologic myopia, the retrobulbar segments of the PCAs were observed as intensely hyperfluorescent curved structures that moved in unison with eye movements and some showed pulsations as we reported. ² A comparison of the ICGA and OCT images showed that the retrobulbar vascular structures observed by OCT were retrobulbar PCAs by ICGA in 154 of the 177 eyes. In the other 23 eyes, the hyperfluorescence of the retrobulbar PCAs in the ICG angiograms was too intense, and it was difficult to follow the intricate course of the retrobulbar PCAs by ICGA. 

Macular Vortex Veins and Their Exit from Sclera.

Amalric ¹⁸ used fluorescein angiography to show posterior routes of choroidal blood outflow around the optic disc. In our ICGA study, we found the posterior routes of choroidal blood outflow in 23.9% of the highly myopic eyes. ⁴ However, it was not certain if these vessels penetrated and exited the sclera in the macular region by examining only the ICG angiographic images because of a lack of topographic landmarks. Unfortunately, ICGA was not performed routinely on all patients, and thus the exact percentage of eyes in which the macular vortex veins was detectable could not be determined. Swept-source OCT examinations clearly showed that the macular vortex vein exited the sclera in the macular area (Fig. 7) in four of 12 cases. 

Figure 7. 

 

Observations of the intrascleral course of macular a vortex vein and its exit from the sclera by swept-source OCT. (A) Photograph of the right fundus of 54-year-old woman (axial length 32.0 mm) shows many dilated branches of macular vortex vein. Arrow shows an ampulla of macular vortex vein. White long arrows show scanned OCT lines in (C) and (D). (B) Indocyanine green angiogram shows the macular vortex vein. Arrow shows an ampulla of macular vortex vein. (C and D) Horizontal OCT scan shows intrascleral course (arrows) of a macular vortex vein and its exit from the sclera (arrowhead). (E) Left fundus of a 48-year-old woman (axial length 30.0 mm) shows that the choroidal veins run toward the macula, that is a macular vortex vein. Arrow shows the ampulla of the macular vortex vein. White long arrow shows scanned line by OCT for (F). (F) The entire course of a macular vortex vein from the choroid, intrascleral part (arrow), and the exit from the eye (arrowhead) can be seen.

Detection of Intrascleral Branches to and from Posterior Choroid.

In 443 of the 662 eyes (66.9%), blood vessels were observed to penetrate into the sclera in the foveal area (see Supplementary Material and Supplementary Figs. S4, S5). The branches of these vessels were seen to continue into the choroid. ICGA was performed in 165 of the 443 eyes; however, it was difficult to observe the intrascleral course of these vessels mainly because the intrascleral course of these branches was short. In addition, the intense hyperfluorescence of the retrobulbar vessels was overlapped, which obscured the fluorescence of these vessels. 

Discussion

Examinations of highly myopic eyes by swept-source OCT showed different diameter blood vessels within and posterior to the sclera, and ICGA confirmed that these vessels were the lateral LPCA, the SPCAs, and the retrobulbar blood vessels. The OCT images also showed the exit of the macular vortex veins from the sclera. 

Earlier histologic studies showed that the lateral LPCAs entered the sclera 3.9 mm temporal to the optic nerve, ¹⁷ and Siam et al. ⁶ recently reported that the mean distance between the intrascleral entry of temporal LPCA and the optic nerve sheath was 3.0 mm in 12 human cadaver eyes. The average distance in our study was 4.28 ± 1.29 mm, which is greater than that reported. ^6,17 However, our measurements were possible in only 58 eyes whose intrascleral entry of LPCAs and optic nerve sheath were detected clearly in the same OCT scan. To analyze the spatial relationship between the intrascleral entry of the LPCA and optic nerve, we needed to examine 3D images and reconstruct the images to show clearly the spatial relationship between the entry site of the LPCAs and optic nerve sheath in the same section. This project is under way. 

A cluster of cross sections of blood vessels also was observed between the scleral stroma and the spreading fibers of the episclera in the macular area (Figs. 4, 5, and see Supplementary Material and Supplementary Fig. S3). A comparison of the ICG angiograms and the OCT images showed that the retrobulbar blood vessels observed by OCT were the retrobulbar segments of the SPCAs and/or the LPCAs (Figs. 4, 5, and see Supplementary Material and Supplementary Fig. S3). 

The drainage of the choroidal veins mainly is through the vortex vein system, which is present in the equatorial region of the four quadrants in normal eyes. After forming the ampulla of the vortex vein, the choroidal venous blood exits the sclera at the equatorial region. However, Amalric reported a case whose choroidal blood is drained around the optic disc by fluorescein angiography, ¹⁸ and we found that the choroidal venous blood drained around the optic nerve or around the macula in 61 of 255 (23.9%) highly myopic eyes by ICG angiography. We have called these macular vortex veins. ^4,19  

To confirm that the drainage from the eye exists in the macular area, we performed CT angiography. ¹⁹ However, the image quality of CT angiograms was not high enough, and because CT angiography depicts only the retrobulbar parts of the blood vessels, the precise site of exit out of the sclera could not be determined. 

We were able to observe the entire course of a macular vortex vein from the choroid until its exit from the sclera (Fig. 7). This confirmed that there was a vortex vein that exited the eye in the macular area from the complete topographic image obtained by swept-source OCT. 

We also observed cross sections of blood vessels coursing in the scleral stroma. These cross sections were observed in multiple adjacent sections in some cases. A comparison of the ICGA and OCT images showed that these cross sections in the OCT images were the cross sections of the intrascleral parts of the SPCAs and LPCAs (Figs. 4, 5, and see Supplementary Material and Supplementary Fig. S3). A relatively hyporeflective tissue surrounded the cross sections of these blood vessels, which is compatible with the fact that the emissary canals, or passageways of blood vessels or nerves are separated from the sclera by a thin layer of loose connective tissue. ²⁰  

We also observed that the retrobulbar blood vessels that pierced the sclera around the central fovea and were continuous to the posterior choroid (see Supplementary Material and Supplementary Figs. S4, S5). Approximately 20 SPCAs have been reported to pass perpendicularly through the sclera around the optic nerve and macula area in human and monkey eyes.^20–23 After piercing the sclera, the SPCAs were reported to join the choroid at the same spot without any oblique intrascleral course.^21,22 These findings suggest that the observed vessels that entered the sclera around the fovea and were continuous to the posterior choroid most likely were the SPCAs and their branches. However, it was difficult to identify each of these vessels with a short intrascleral course even by ICGA, thus no conclusive evidence was obtained in our study. 

There are several limitations in our study. This study was conducted on patients in the High Myopia Clinic at our university. Thus, the results might not reflect the tendency in the general myopic population. Although we used ICGA to identify the intrascleral and retrobulbar blood vessels observed by swept-source OCT, a point-to-point comparison of the precise location between ICGA and OCT might not be accurate, unlike the simultaneous EDI-OCT and ICGA with the Spectralis HRA/OCT system. Also, the differentiation between LPCAs and SPCAs was done mainly by a presence of branching to the posterior choroid. However, congenital anomalies could be present in the PCAs, and we cannot completely rule out the possibility that LPCAs also give off small branches to the posterior choroid as was reported in monkeys by Hayreh. ¹⁷ In addition, the distribution may be altered significantly in the eyes with pathologic myopia together with thinning and expansion of the sclera. This would make it difficult to identify the origin of observed blood vessels that had been done based on the findings in nonhighly myopic eyes. Furthermore, the deeper structures, such as the retrobulbar blood vessels, were visible only in eyes with macular chorioretinal atrophy even by using swept-source OCT. A grid scan or 3D scan might be better than 12 radial scans to detect the entire course of the intrascleral or retrobulbar blood vessels, and to match the spatial orientation between OCT images and fundus photographs. 

Despite all of these limitations, we believe that our results clearly showed that the long course of blood vessels within and posterior to the sclera can be studied by swept-source OCT. Further studies to analyze quantitatively the entry and distribution patterns of SPCAs, LPCAs, and vortex veins in a large population of highly myopic eyes are ongoing in our clinic. We are attempting to determine in longitudinal studies how alterations of intrascleral vascular structures are related to the development of chorioretinal complications or optic nerve damages in patients with pathologic myopia. 

Supplementary Materials

pdf S1 

pdf S2 

pdf S3 

pdf S4 

pdf S5 

Acknowledgments

Duco Hamasaki provided critical discussion and final manuscript revision. 

Footnotes

 Disclosure: K. Ohno-Matsui, None; M. Akiba, Topcon Corporation (E); T. Ishibashi, None; M. Moriyama, None

Footnotes

 Supported by Japanese Society for Promotion of Science Grant 22390322.