Optical Coherence Tomographic Imaging of Posterior Episclera and Tenon’S Capsule

Retina Optical Coherence Tomographic Imaging of Posterior Episclera and Tenon’s Capsule

Kyoko Ohno-Matsui,1 Yuxin Fang,1 Kei Morohoshi,1 and Jost B. Jonas2

1Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, Tokyo, Japan 2Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University of Heidelberg, Heidelberg, Germany

Correspondence: Kyoko Ohno-Mat- PURPOSE. To investigate structural features of the posterior episclera and Tenon’s capsule in sui, Department of Ophthalmology patients with high myopia. and Visual Science, Tokyo Medical and Dental University, 1-5-45 Yush- METHODS. This hospital-based observational study included highly myopic eyes (myopic ima, Bunkyo-ku, Tokyo 1138510, refractive error > 8 diopters or axial length ‡26.5 mm) in which the posterior sclera in its Japan; full thickness could be visualized on swept-source optical coherence tomography (OCT) [email protected]. images in all 12 radial scans centered on the fovea. We assessed the posterior episclera and Submitted: December 28, 2016 Tenon’s capsule. Accepted: May 29, 2017 RESULTS. The study included 278 eyes of 175 patients (mean age, 60.9 6 11.4 years; range, 32– Citation: Ohno-Matsui K, Fang Y, 89 years; axial length, 30.7 6 1.9 mm; range, 26.5–36.6 mm). The episclera was detected Morohoshi K, Jonas JB. Optical co- outside of the sclera in 164 eyes (59.0%) and appeared as a relatively uniform structure with a herence tomographic imaging of pos- reﬂectivity slightly lower than scleral reﬂectivity. In these eyes, mean scleral thickness was terior episclera and Tenon’s capsule. 197 6 73 lm in the foveal region and 164 6 64 lm and 146 6 59 lm at 1000 and 2500 lm Invest Ophthalmol Vis Sci. temporal to the fovea, respectively. The posterior episclera was visualized in the region 2017;58:3389–3394. DOI:10.1167/ temporal to the fovea. Mean episcleral thickness detected in 77 eyes was 80 6 27 lm and 82 iovs.16-21394 6 30 lm at 1000 lm and 2500 lm temporal to the fovea, respectively. Tenon’s capsule was detected in 11 of the 278 eyes (4.0%) as structurally, loosely connected tissue with a meshwork-like appearance. The measured thickness in four eyes was 60 6 32 lm. In 25 eyes with extremely thin sclera (<100 lm at 1000 lm temporal to the foveola), the mean thickness of the sclera and episclera were 87 6 11 lm and 65 6 15 lm, respectively.

CONCLUSIONS. Swept-source OCT applied to a subset of highly myopic eyes with signiﬁcant thinning of the retina and choroid allowed visualization of the posterior sclera and episclera, and in some cases, also Tenon’s capsule. Keywords: posterior episclera, Tenon’s capsule, optical coherence tomography, swept-source optical coherence tomography, pathologic myopia, high myopia

he sclera, which is the outermost coat of the eye globe, is enhanced-depth imaging mode of OCT to examine the T mostly collagenous and can be divided into three layers: the posterior sclera and was able to determine the entire scleral episclera on the outer scleral surface, the scleral stroma, and thickness in the macular region in 48 eyes with high axial the lamina fusca on the inner surface of the sclera.1 Although myopia. Using swept-source OCT as a further reﬁnement of the the episclera merges with the sclera, both tissues differ. The OCT technology, we observed the full posterior sclera in a collagen bundles in the episclera, compared to the collagen previous study of 278 eyes with high myopia.4 Although the bundles in the sclera, are thinner, more irregularly arranged, latter study brieﬂy mentioned that the tissues exterior to the and less densely packed.2 The episclera also contains more sclera were detected in the OCT images of some eyes, a detailed ground substance than the sclera.2 The Tenon’s capsule is analysis of the posterior episclera and Tenon’s capsule was not composed of collagen and overlies the episclera.1,2 Histologic performed. Thus, the purpose of the present swept-source OCT studies revealed that the Tenon’s capsule is closely connected study was to perform a further analysis of collected images, to the outer episclera by delicate lamellae in the region of the with a focus on the features of the episclera and Tenon’s insertion of the extraocular muscles and with the dura mater capsule in the posterior segment of eyes with high myopia. around the optic nerve head.2 Observations of the episclera and Tenon’s capsule posterior to the equator have so far been limited mostly to surgical METHODS situations (e.g., during scleral buckling surgery for retinal detachment or ocular enucleation). Histologic studies have This observational hospital-based case series included patients rarely been focused on the posterior episclera or Tenon’s with high myopia who had consecutively been examined by capsule. swept-source OCT (DRI-OCT Atlantis; Topcon Corp., Tokyo, The clinical introduction of optical coherence tomography Japan) in the High Myopia Clinic at the Tokyo Medical and (OCT) has made it possible to visualize the posterior ocular Dental University between May 2014 and December 2015. The segment including the sclera. Imamura et al.3 used the Ethics Committee of the Tokyo Medical and Dental University

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standardized regression coefficient b, the nonstandardized regression coefficient b and its 95% confidence intervals (CI). Additionally, we carried out a 1-way ANOVA to compare the measurements obtained at different locations in the same eye. All P-values were two-sided and considered to be statistically significant if their value was lower than 0.05.

RESULTS Out of 488 highly myopic eyes, which had undergone swept- FIGURE 1. Methods used to measure the thickness of the sclera, source OCT examination in the study period, the entire sclera episclera, and Tenon’s capsule. The thickness was measured along the was visualized in all 12 radial foveal scans in 278 eyes (57.0%) perpendicular axis to the curvature of the retinal pigment epithelium. of 175 patients.4 The mean age of these 175 patients was 60.9 Double-headed red arrow: sclera. Blue bar: episclera. Yellow bar: Tenon’s capsule. Note: Cross-section of an intrascleral blood vessel 6 11.4 years (32–89 years) and the mean axial length of the surrounded by loose tissue. The sclera appears thickened in that 278 eyes was 30.7 6 1.9 mm (26.5–36.6 mm). Among the 278 region. The choroid is barely detectable except for a few large vessels. eyes, the episclera and/or Tenon’s capsule were detected in 164 eyes (59.0%; or 33.6% of the original 488 eyes) of 117 patients (mean age: 59.4 6 11.4 years; mean axial length: 30.9 approved the investigation and confirmed that the methods 6 1.8 mm). The episclera appeared as a relatively uniform used in our study conformed to the tenets of the Declaration of structure with a reflectivity that was slightly lower than the Helsinki. The ethics committee waived informed consent, scleral reflectivity (Fig. 2). The episclera was closely attached since this study involved a reevaluation of images collected in to the outer surface of the sclera in most areas; although in our previously approved study, and since the previously some regions, especially in the macular area, the episclera was collected data were deidentified. High myopia was defined as clearly separated from the outer surface of the sclera (Figs. 3, a myopic refractive error (spherical equivalent) of > 8 4). The latter finding suggested that the episclera represented a diopters or an axial length ‡26.5 mm. Exclusion criteria were a different tissue, distinct from the sclera proper. The border lack of clear OCT images, and a history of previous vitreoretinal between the sclera and episclera was relatively clear in most surgery, since it could have affected the scleral curvature. eyes due to differences in reflectivity between these tissues. All patients underwent a comprehensive ophthalmologic Eyes with detectable episclera compared to eyes in which the examination including refraction, ocular biometry for mea- episclera was not visible had a significantly longer axial length surement of axial length (IOLMaster; Carl Zeiss Meditec Co., (P ¼ 0.003); thinner central retinal thickness (P ¼ 0.01); and Jena, Germany); color fundus photography; fundus autofluo- thinner subfoveal scleral thickness (P < 0.001). There were no rescence; and swept-source OCT. The optical coherence significant differences in age between these groups (P ¼ 0.66). tomography examination was carried out using a prototype Because the subfoveal choroid was too thin to be measured in of a swept-source OCT device (Topcon Corp.). This device had most eyes included in our study, choroidal thickness was not an A-scan repetition rate of 100,000 Hz. The light source used included in the list of outcome parameters. was a wavelength-sweeping laser centered at 1050 nm with a Overlying the episclera, the tissue considered to be Tenon’s bandwidth of approximately 100 nm. The effective bandwidth capsule was detected in 11 of the 278 eyes (4.0%). Tenon’s was roughly 60 nm due to water absorption. The axial capsule appeared as loosely arranged tissue. In some eyes, a resolution in the tissue was estimated to be 8 lm while the thin space was observed between the episclera and Tenon’s lateral resolution was estimated as 20 lm. The imaging depth capsule (similar to the slit shown in Fig. 2A, although slightly in the tissue was 2.6 mm, and the lateral scan length was wider than that shown in Fig. 2C). adjustable. Our scanning protocol included a pattern of 12-mm Blood vessels located in the sclera were surrounded by long radial scans along 12 meridians centered on the fovea. A fibrous tissue within a rhomboid space (Fig. 2C). A cluster of single image was made up of 1024 A-line scans acquired in 10 blood vessels was observed in the subfoveal area between the ms. Each scan consisted of 32 B-scan images which were sclera and episclera (Fig. 2E). In contrast to the intrascleral recorded and averaged by postprocessing to yield a des- blood vessels, the blood vessels between the sclera and peckled, high-quality B-scan image. The thickness of the sclera, episclera did not appear to be ensheathed. Due to the episclera, and Tenon’s capsule were measured with the presence of these blood vessels between the episclera and ‘‘caliper function’’ of the built-in software of the OCT. The sclera, the outer border of the episclera was located outside of scleral thickness was determined in the foveal region and at the imaging range of the OCT in these eyes. The region with eight locations at 1000 lm and at 2500 lm superior, inferior, the posterior episclera visible on the horizontal OCT images temporal, and nasal to the fovea, respectively. Since the scleral was located in these eyes temporal to the fovea. In three eyes, shape was bent, the scleral thickness was measured along an the outer surface of the sclera was folded inwardly and a axis orientated perpendicularly to the eye surface (Fig. 1). cluster of blood vessels was located between the inwardly The statistical analysis was carried out using a commercially folded sclera and the episclera (Fig. 4). available statistical software program (SPSS version 22.0; IBM- In the 164 eyes in which the episclera could be visualized in SPSS, Chicago, IL, USA). The measured values of the outcome the OCT images, the mean scleral thickness in the foveal region parameters were presented as mean 6 standard deviations. was 197 6 73 lm (range, 64–482 lm; Table 1). In univariate Since the parameters were not normally distributed, as shown analysis, scleral thickness decreased in conjunction with the by the Kolmogorov-Smirnov test, the statistical significance of longer axial length in the subfoveal region (P ¼ 0.008; b: 0.22) the differences between the two groups of eyes was assessed and at 1000 lm(P ¼ 0.02; b: 0.20) and at 2500 lm(P ¼ 0.01; by the Mann-Whitney U test for unpaired samples. The dif- b: 0.21) temporal to the fovea. The scleral thickness was ferences in measurements between two locations within the significantly (P < 0.0001) thicker in the foveal region than at same eye were examined by the Wilcoxon-test for paired the region that was located 1000 lm temporal to the fovea. samples. Associations between two linear parameters were The scleral thickness at this point was thicker (P < 0.0001) assessed by a linear regression analysis with calculation of the than that found at 2500 lm temporal to the fovea (Table 2).

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FIGURE 2. Swept-source OCT images of the posterior sclera, episclera, and Tenon’s capsule. (A, C, E) A horizontal OCT section across the fovea. (B, D, F) Schematic illustration of corresponding OCT images. Sclera is observed as uniform hyperfluorescent tissue. The episclera appears as a relatively uniform structure with a reflectivity slightly lower than the scleral reflectivity. Tenon’s capsule appears as a structurally loosely connected tissue with meshwork appearance and splitting fibers. Red circle shows a cross-section of blood vessels; intrascleral blood vessel in Figure 1D and orbital vessels in Figure 1F. The intrascleral blood vessel is surrounded by relatively hyporeflective tissue (shown in pink, Fig. 1D). In Figure 1E, although the choroid is observed temporal to the fovea, the choroid is extremely thin and barely visible in Figures 1A or 1C.

The same results were found when all of the measurements for lm). The thickness of Tenon’s capsule was measurable in 4 all of the locations were included in the statistical analysis and eyes at this location. However, the outer surface of Tenon’s subsequent ANOVA. capsule could not be detected in any of the other eyes. The In the horizontal OCT sections of the 164 eyes with mean thickness of Tenon’s capsule in these four eyes was 60 6 detectable episclera, the mean thickness of the sclera at 1000 32 lm (range, 19–93 lm). At a location of 2500 lm temporal to lm temporal to the fovea was 164 6 64 lm (range, 54–412 the fovea, the mean scleral thickness was 146 6 59 lm (range, lm). The full thickness of the episclera was detectable in 77 58–561 lm) in the 164 eyes that underwent episcleral imaging. eyes with a mean thickness of 80 6 27 lm (range, 30–135 At this location, the thickness of the posterior episclera that

FIGURE 3. Swept-source OCT image of the posterior fundus of an eye with dome-shaped macula. Note: cluster of blood vessels (shown in red ovals) between the sclera and episclera.

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FIGURE 4. Separation of the episclera from the outer surface of the sclera. Inner and outer surface of the episclera is outlined by arrowheads. In the macular area, the episclera (outlined by arrowheads) is separated from the sclera and is located in a direction that is more to the center of the orbit (Fig. 4A).

was measured in 112 eyes was 82 6 30 lm (range, 29–174 In the optical coherence tomography images analyzed in lm). The thickness of Tenon’s capsule that was measurable in the current study, although Tenon’s capsule and the episclera seven eyes at this location was 55 6 13 lm (range, 30–70 lm). showed similar reflectances, the fibers appeared to be more Among the 77 eyes in which the full thickness of the loosely arranged and to be more split up in Tenon’s capsule episclera was observed, 25 eyes exhibited an extremely thin (Fig. 2). The border between the episclera and Tenon’s capsule posterior sclera with a thickness of less than 100 lm at 1000 appeared as a cleft in some eyes (Figs. 2A, 2C, 2E). Using high- lm temporal to the fovea (mean, 87 6 11 lm; range, 65–98 speed anterior segment OCT, Kumar et al.5 examined the lm; Fig. 5). In a subset of 15 eyes that had a detectable outer anterior Tenon’s capsule in 12 eyes which received a drug border of the episclera at this location, the mean episcleral injection into the posterior sub-Tenon space for the therapy of thickness was 65 6 15 lm (range, 39–94 lm). In the entire uveitis. The mean thickness of the anterior Tenon’s capsule in group of eyes in which the full thickness of the episclera was this previous study was 0.21 6 0.07 mm. In Figure 2 of the visible, the episcleral thickness measured at 1000 lm temporal Kumar et al.5 study, Tenon’s capsule showed a similar to the fovea was significantly correlated (univariate analysis) reflectance with splitting fibers similar to the findings for the with scleral thickness at the same location (P ¼ 0.03; regression Tenon’s capsule in the posterior segment in our current study. coefficient r: 0.25), but not with the axial length (P ¼ 0.12). In We observed vessels at the interface between the episclera multivariate analysis that used episcleral thickness as the and Tenon’s capsule (Figs. 2E, 3A). According to anatomic dependent variable, episcleral thickness was marginally studies, branches of the short posterior ciliary arteries 1 associated with scleral thickness (P ¼ 0.06; b 0.24; B: 0.11; perforate the sclera in the peripapillary region. Previous 95% CI: 0.01, 0.22), but not with the axial length (P ¼ 0.27). studies suggested that some of these branches run in the sclera Episcleral thickness measured at 2500 lm temporal to the toward the equator and anastomose with branches of the long fovea was significantly correlated (univariate analysis) with posterior ciliary arteries to supply the posterior episclera in the 2 axial length (P ¼ 0.02), but not with scleral thickness at the form of a thin episcleral vessel plexus. Furthermore, we same location (P ¼ 0.55). Similar results were obtained for the detected a cluster of blood vessels between the posterior sclera multivariate analysis. and the episclera, but not within the episclera. These vessels either might have been part of the so-called ‘‘posterior episcleral plexus’’ or might have been the long posterior DISCUSSION ciliary arteries. The relatively large blood vessels between the posterior In the present study, swept-source OCT applied to a subset of sclera and episclera may give rise to an inward bulging of the highly myopic eyes with significant thinning of the retinal and sclera in the macular region, similar to that observed in three of choroidal layers allowed visualization of the posterior sclera the eyes in our study population (Fig. 4). One might and episclera, and in some cases, also Tenon’s capsule. Eyes hypothesize that these types of vessels running along the with detectable episclera compared to eyes without detectable outer surface of the posterior sclera may partially resist an episclera had significantly longer axial length and thinner expansion of the sclera in eyes with pathologic myopia, and central retinal thickness. may cause a local indentation of the posterior sclera.

TABLE 1. Comparison of Clinical Characteristics (mean 6 SD; range) Between Highly Myopic Eyes With Visible Episclera or Without Visible Episclera

Characteristics Visible Episclera Episclera Not Visible P Value

Number of eyes (No. of persons) 164 (117) 17 (12) Age, y 59.1 6 12.3 (32–89) 58.3 6 8.6 (40–74) 0.66* Axial length, mm 30.9 6 1.9 (25.5–36.2) 29.9 6 1.8 (25.5–33.4) 0.03* Subfoveal sclera thickness, lm 197 6 73 (64–482) 310 6 83 (168–477) <0.001* Central retinal thickness, lm 134 6 33 (62–216) 160 6 35 (98–216) 0.02* * Mann-Whitney U tests.

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TABLE 2. Thickness of the Sclera, Episclera, and Tenon’s Capsule at Different Locations in the Posterior Fundus

Location Thickness of Sclera Thickness of Episclera Thickness of Tenon’s Capsule

Subfovea 197 6 73 (64–482; 164 eyes) 1000 lm temporal to the fovea 164 6 64 lm (164 eyes) 80 6 27 lm (77 eyes) 60 6 32 lm (4 eyes) 2500 lm temporal to the fovea 146 6 59 lm (164 eyes) 82 6 30 lm (112 eyes) 55 6 13 lm (7 eyes)

The thickness of the posterior sclera in the eyes included in results are applicable to other ethnic groups. Fourth, the our study was significantly thinner at the locations 1000 lm observation of the episclera and Tenon’s capsule was possible and 2500 lm temporal to the fovea compared to that observed only in eyes with high myopia. Thus, the mean scleral and in the foveal region (Table 1). The thinning of the sclera episcleral thickness values do not appear to represent the preferentially in the parafoveal versus the foveal region may be thickness of these tissues in general population. Fifth, a of importance, as this could explain the development of posterior scleral thickness of approximately 100 lm appears parafoveal staphylomas as local backward outpouchings of the to be very low, thereby leading to doubts about the validity of sclera. Also of potential interest is the development and such data. However, histomorphometric examinations of progression of a dome-shaped macula, which consists of a local markedly elongated eyes revealed similar thickness values as thickening and inward folding of the foveal sclera.3,6-9 low as 0.1 mm for the posterior sclera.10,11 Furthermore, it Unfortunately, since the measurement of the thickness of the needs to be taken into consideration that histologic specimens posterior episclera could only be obtained in a few eyes, it was undergo postmortem tissue swelling and tissue shrinkage due not possible to perform a comparison of the posterior to the histologic processing. Sixth, if both eyes fulfilled the episcleral thickness between the various regions. inclusion criteria, both eyes of the participant were included At 1000 lm temporal to the fovea, the sclera was thinner into our analysis. In general, studies performed on a paired, than at 100 lm in 25 eyes of our study population. In 15 of normally and mostly symmetrical organ such as the eyes should these 25 eyes, the mean episcleral thickness could be include only one randomly chosen eye for the statistical measured and was shown to be 65 lm. Thus, in eyes with analysis. This is particularly true if there are associations an extremely thin posterior sclera, the episclera appears to be a between these symmetrical organs and systemic parameters major part of the outer wall of the globe (Fig. 3A). The that are quantitatively examined, such as the blood pressure. coverage of the posterior thinned sclera by the posterior However, in our study of highly myopic individuals, both eyes episclera in highly myopic eyes may explain why none of of the same individual were relatively asymmetrical, as out of approximately 4000 highly myopic patients in the High Myopia the 164 eyes of 117 individuals, only 47 individuals had both Clinic at the Tokyo Medical and Dental University showed a eyes included, while 70 individuals had only one eye included. spontaneous rupture of the posterior globe despite the The present study showed that in highly myopic eyes, extremely thinned sclera (and episclera). However, this swept-source OCT allowed the visualization of the posterior thinning did allow ophthalmoscopic visualization of the orbital episclera and Tenon’s capsule. An increase in the tissue depth fat tissue in some of these eyes. penetration of the OCT technology may further increase the Potential limitations of our study should be discussed. First, number of eyes with detectable episclera or Tenon’s capsule as the study participants were recruited by a specialized upon OCT. Additional studies with OCT will allow further tertiary center for high myopia, it is unclear whether our investigation of the changes in the episclera and Tenon’s findings will also apply to highly myopic eyes within the capsule in pathologic myopia and their role in related general population. In particular, the study population may pathology. have consisted of a disproportionately large number of patients with pathologic myopia. Thus, our current findings may be Acknowledgments more typical for eyes with pathologic myopia than for highly myopic eyes in general. Second, the number of eyes with Supported by grants from the Japanese Society for Promotion of detectable episclera or detectable Tenon’s capsule was Science (no. 15H04993, 15K15629). relatively small. Third, the study population was composed Disclosure: K. Ohno-Matsui, None; Y. Fang, None; K. Moro- of Japanese patients, and therefore it is unclear whether these hoshi, None; J.B. Jonas, Mundipharma Co. (C), P

FIGURE 5. Swept-source OCT image of the posterior fundus of an eye (72-year-old patient; axial length: 31.0 mm) with very thin sclera (84 lmat 2500 lm temporal to the fovea) and an episcleral thickness of 74 lm. The choroid is not visible on either sides of the fovea. A cross-section of an orbital vessel that is located between the sclera and episclera (shown in red oval in Fig. 5B).

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