Characteristics of Peripapillary Staphylomas Associated with High Myopia Determined by Swept-Source Optical Coherence Tomography

Characteristics of Peripapillary Staphylomas Associated With High Myopia Determined by Swept-Source Optical Coherence Tomography

KOSEI SHINOHARA, MUKA MORIYAMA, NORIAKI SHIMADA, TAKESHI YOSHIDA, AND KYOKO OHNO-MATSUI

PURPOSE: To analyze the morphologic features of peri- POSTERIOR STAPHYLOMA IS AN IMPORTANT papillary staphylomas associated with high myopia by feature of eyes with pathologic myopia.1–5 Curtin swept-source optical coherence tomography (OCT). classified posterior staphylomas in eyes with A 1 DESIGN: Validity analysis. pathologic myopia into 10 different types. The peripapil- METHODS: Highly myopic patients (refractive error lary staphyloma (type 3) was reported to be a rare type of >8.0 diopters or axial length >26.5 mm) with a peripa- posterior staphyloma, and its incidence was approximately pillary staphyloma who had undergone swept-source 1.5% of all staphylomas. Other investigators have reported OCT were studied. The non–highly myopic fellow eyes that the incidence of a peripapillary staphyloma was 4.3%6 in patients with unilateral high myopia were also studied. and 6.9%7 of highly myopic eyes based on Curtin’s classifi- The presence of a peripapillary staphyloma was deter- cation. Curtin’s classification was made by ophthalmosco- mined by stereoscopic ophthalmoscopic examinations. pic observations and chart drawings,1 so the findings are The OCT features of the peripapillary staphylomas and considered to be relatively subjective. other peripapillary lesions were evaluated. To analyze an eye deformity caused by a staphyloma 8,9 RESULTS: Twenty-five eyes of 16 patients were stud- more objectively, Moriyama and associates performed ied. Twenty-two eyes were highly myopic and the remain- 3-dimensional magnetic resonance imaging (3D MRI). ing 3 eyes of the patients with unilateral high myopia were Later, Ohno-Matsui4 used a combination of 3D MRI and non–highly myopic. A peripapillary staphyloma was seen ultra-wide-field fundus imaging and classified posterior in the swept-source OCT images as a gently sloping exca- staphylomas into 6 different types according to their size vation around the optic disc in all 25 eyes. The posterior and location (wide macular, narrow macular, peripapillary, sclera in the area of a peripapillary staphyloma was nasal, inferior, and other). Ohno-Matsui reported that peri- observed to bow posteriorly, with the local curvature papillary staphylomas were observed in only 5 of 198 eyes steeper than the curvature of the adjacent scleral regions. (2.5%).4 However, because the outpouching of a peripapil- The sclera at the edge of a peripapillary staphyloma lary staphyloma can be slight and narrow, eyes with a peri- appeared to be elevated inward from the surrounding papillary staphyloma had a nasally distorted shape that was sclera, and the choroid at the staphyloma edge appeared different from other types of a staphyloma, and they did not to be compressed and thinned. A peripapillary intrachor- show clear outpouching of the globe in the 3D MRI images. oidal cavitation was a frequent complication and was Thus, the diagnosis of peripapillary staphylomas was found in 13 eyes with a peripapillary staphyloma mainly based on the presence of pigmentary abnormalities (52.5%). around the optic disc in the wide-field fundus images. CONCLUSIONS: Swept-source OCT can detect the slight Recent advances in optical coherence tomography (OCT) changes of the sclera and choroid in the area of a peripapil- have enabled clinicians to investigate the structure of the lary staphyloma, and we recommend its use in determining fundus in more detail.10–13 Current swept-source OCT in- the presence of a peripapillary staphyloma. (Am J struments use a longer central wavelength, generally in the Ophthalmol 2016;169:138–144. Ó 2016 Elsevier Inc. 1 mm range, which has improved their ability to penetrate All rights reserved.) deeper into tissues than the conventional spectral-domain OCT instruments. Owing to its deep penetration, swept- source OCT can obtain images of deeper tissues, such as the choroid, sclera, and optic nerve, more clearly.10,14,15 Although the scan length of currently available OCT instruments is still limited, we believed that staphylomas in Supplemental Material available at AJO.com. Accepted for publication Jun 16, 2016. a restricted area, such as peripapillary staphylomas, might From the Department of Ophthalmology and Visual Science, Tokyo be suitable for detection by swept-source OCT. Medical and Dental University, Tokyo, Japan. A PubMed search on March 2016 using the keywords Inquiries to Kyoko Ohno-Matsui, Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, 1-5-45 Yushima, ‘‘peripapillary staphyloma’’ or ‘‘type 3 staphyloma’’ and Bunkyo-ku, Tokyo 113-8510, Japan; e-mail: [email protected] ‘‘optical coherence tomography’’ detected 5 articles;

138 © 2016 ELSEVIER INC.ALL RIGHTS RESERVED. 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2016.06.033 however, 4 articles were analyses of congenital peripapil- The OCT features of peripapillary staphylomas were lary changes,16–19 and only 1 article was a report about a analyzed, and other peripapillary lesions such as intrachor- peripapillary staphyloma associated with high myopia.20 oidal cavitations (ICCs) were also evaluated. In addition, the OCT features of peripapillary staphylomas have not been examined in detail in any of the earlier studies. Therefore, reports about the morphologic characteristics of a peripapillary staphyloma associated with RESULTS high myopia are limited. CLINICAL AND FUNDUS FEATURES OF PATIENTS WITH The purpose of this study was to determine the morpho- PERIPAPILLARY STAPHYLOMA: Thirty-four eyes of 21 logic characteristics, especially the sclera and choroid, of patients were diagnosed ophthalmoscopically as having a peripapillary staphylomas in the swept-source OCT images. peripapillary staphyloma. Among them, 9 eyes (5 patients) were excluded: 8 eyes (4 patients) owing to a lack of OCT images centered on the optic disc and 1 eye (1 patient) owing to a history of vitreoretinal surgery. There were no METHODS patients who were suspected to have a congenital staphyloma. In the end, 25 eyes of 16 patients were enrolled THE PROCEDURES USED IN THIS STUDY ADHERED TO THE TE- and the swept-source OCT images of these cases were nets of the Declaration of Helsinki, and they were approved examined in more detail. There were 2 men and 14 women by the Ethics Committee of Tokyo Medical and Dental with a mean age of 68.3 6 6.6 years and a range of 55–78 University. An informed consent was obtained from years. In the stereoscopic fundus examinations, a peripapil- each of the subjects to perform all of the examination lary staphyloma was observed as a slight excavation around procedures. the optic disc, and the edge of the excavation had pigmen- Highly myopic patients who visited the High Myopia tary abnormalities (Figure 1) as reported.4 In all cases, the Clinic at Tokyo Medical and Dental University between peripapillary staphyloma extended beyond the margin of February 2, 2015 and September 25, 2015 were analyzed the peripapillary conus; thus it differed from the excavation for the presence of a peripapillary staphyloma. High myopia of the peripapillary gamma zone (Figure 1).21 The mean was deﬁned as a myopic refractive error (spherical equiva- refractive error (spherical equivalent), except for the pseu- lent) greater than 8.0 diopters (D) or an axial length dophakic eyes, was 9.0 6 3.3 D with a range of 1.5 >26.5 mm. For the patients with unilateral high myopia, to 13.0 D. The mean axial length was 27.6 6 1.6 mm the non–highly myopic fellow eyes were also studied in with a range of 22.5–30.5 mm. the same way. The diagnosis of a peripapillary staphyloma Among the 16 patients, 9 had a peripapillary staphyloma was based on the detection of an excavation and edge bilaterally and 7 had a peripapillary staphyloma unilater- around the optic disc by stereoscopic fundus examination ally. Of the 9 patients who had a peripapillary staphyloma with agreement of 2 of the authors (K.S. and K.O.-M.). bilaterally, 8 patients had bilateral high myopia and 1 pa- The staphyloma was also identiﬁed by the presence of tient had unilateral high myopia. Of the 7 patients who pigmentary changes along the presumed edge of the staph- had a peripapillary staphyloma unilaterally, 4 patients 4 yloma as reported by Ohno-Matsui. The exclusion criteria had bilateral high myopia and 3 patients had unilateral included a lack of OCT images centered on the optic disc high myopia. Therefore, in the total of 25 eyes with a peri- and a history of vitreoretinal surgery. The patients with a papillary staphyloma, 22 eyes were highly myopic and the history of a reduction of the best-corrected visual acuity remaining 3 eyes were not highly myopic. The mean age (BCVA) and a history of fundus abnormalities in the papil- was 68.2 6 7.0 years with a range of 55–78 years in the lary and peripapillary region in childhood were excluded. patients with high myopia and 70.7 6 4.5 years with a All of the patients underwent comprehensive ophthal- range of 66–75 years in those without high myopia. The mologic examinations, including measurements of the mean axial length was 28.1 6 1.0 mm with a range of refractive error (spherical equivalent) and axial length 26.8–30.5 mm in the eyes with high myopia and 24.0 6 with the IOLMaster (Carl Zeiss Meditec, Jena, Germany) 1.3 with a range of 22.5–25.0 mm in the eyes without and stereoscopic fundus examination with pupillary dila- high myopia. The clinical characteristics of the eyes with tion. Swept-source OCT (DRI OCT-1; Topcon Corp, a peripapillary staphyloma are shown in the Table. Tokyo, Japan) was performed by radial scans with 12 equal meridian scans centered on the optic disc. This swept- OPTICAL COHERENCE TOMOGRAPHIC FEATURES OF source OCT system has an A-scan repetition rate of 100 PERIPAPILLARY STAPHYLOMA: In the OCT images 000 Hz, and its light source operates in the 1 mm wave- centered on the optic disc, a gently sloping excavation length region. The light source is a wavelength tunable was clearly observed around the optic disc in all 25 eyes laser centered at 1050 nm with a 100 nm tuning range. (Figures 2 and 3). This excavation was observed at least The scan line length was 6 or 9 mm, and 32 B-scan images 180 degrees around the optic disc in all 25 eyes. The poste- were averaged to improve the signal-to-noise ratio. rior sclera in the area of the peripapillary staphyloma was

VOL. 169 CHARACTERISTICS OF PERIPAPILLARY STAPHYLOMAS BY OCT 139 FIGURE 1. Fundus photographs of eyes with a peripapillary staphyloma. (Top, Bottom left, Bottom center) Color fundus photographs of eyes with a peripapillary staphyloma. The edge of the staphyloma can be seen to have pigmentary abnormalities (black arrowheads). (Bottom right) Fundus autoﬂuorescence image of the eye shown at bottom center. The edge of the staphyloma is seen to be hyperautoﬂuorescent.

choroid at the site of the staphyloma edge appeared to be TABLE. Clinical Characteristics of the Eyes With Peripapillary compressed and thinned (Figures 2 and 3). Staphyloma A peripapillary ICC was a frequent complication in eyes with a peripapillary staphyloma and was found by OCT Eyes With Peripapillary Staphyloma in 13 eyes (52.0%; Supplemental Figure, available at Not Highly Myopic AJO.com): 12 of the 22 highly myopic eyes (54.5%) and ¼ ¼ Characteristic Highly Myopic (N 22) (N 3) 1 of the 3 non–highly myopic eyes (33.3%). Refractive error, 10.0 6 2.0 3.5 6 2.8 mean 6 SD (5.75 to 13.0) (1.5, IOL, (range) 5.5) Axial length, 28.1 6 1.0 24.0 6 1.3 DISCUSSION mean 6 SD (26.8–30.5) (22.5, 24.4, 25.0) (range) THE SWEPT-SOURCE OCT IMAGES SHOWED A CHANGE OF ICC, n (%) 12 (54.5%) 1 (33.3%) the scleral curvature to a gentle slope in the area of peri- Type of myopic 21 (95.5%) 2 (66.7%) papillary staphyloma in all of the eyes. This suggests that conus Annular 8 (36.4%) 2 (66.7%) although currently available OCT instrument has a lim- Temporal 10 (45.5%) 0 itation in the scan length, swept-source OCT can be used Inferior 3 (13.6%) 0 to examine a restricted area of a staphyloma, such as a peripapillary staphyloma. In our earlier studies, we ICC ¼ intrachoroidal cavitation; IOL ¼ intraocular lens. analyzed the shape of a staphyloma by using 3D MRI,4,8,9 and the results showed that it was a useful technique to detect a posterior staphyloma as an seen to bow posteriorly, with the local curvature steeper outpouching of the globe. However, probably because than that of the adjacent scleral regions. Similar changes the outpouching is milder and the change in the of the scleral curvature have been reported in the area of curvature is not as rapid in a peripapillary staphyloma a peripapillary ICC by Spaide and associates.22 However, compared with the other types of staphylomas, it is the curvature of the sclera at the edge of the peripapillary difﬁcult to detect peripapillary staphylomas by 3D staphyloma appeared to be elevated inwardly, and the MRI because of the limited resolution.4 Thus, OCT

140 AMERICAN JOURNAL OF OPHTHALMOLOGY SEPTEMBER 2016 FIGURE 2. Highly myopic right eye of a 71-year-old woman with bilateral high myopia with a peripapillary staphyloma. The refractive error was L10.5 diopters and axial length was 28.7 mm. (Top) Fundus photograph of eye with a peripapillary staphyloma. The white lines are the scanned lines of the swept-source optical coherence tomography (OCT) images shown in the middle and bottom rows. The border of the peripapillary staphyloma has pigmentary abnormalities (arrowheads). (Middle and Bottom) B-scan swept- source OCT image of the scanned line shown in the top row (Middle: horizontal scan image; Bottom: vertical scan image). The OCT images centered on the disc show that the posterior sclera in the area of peripapillary staphyloma bows posteriorly, with the local curvature steeper than that of the adjacent sclera. There is also a change of curvature of the sclera at the site corresponding to the pigmentary abnormalities in stereoscopic fundus image (white arrows). The sclera at the edge of the staphyloma is elevated inward from the surrounding sclera, and the choroid at the site of the staphyloma edge appears to be compressed and thin (white arrows).

VOL. 169 CHARACTERISTICS OF PERIPAPILLARY STAPHYLOMAS BY OCT 141 FIGURE 3. An emmetropic left eye of a 71-year-old woman with unilateral high myopia and a peripapillary staphyloma. The axial length was 24.4 mm. (Top) Fundus photograph of eye with a peripapillary staphyloma. The white lines are the scanned lines of the swept-source optical coherence tomography (OCT) images shown in the middle and the bottom row. The edge of the peripapillary staphyloma has pigmentary abnormalities (arrowheads). (Middle and Bottom) B-scan swept-source OCT image of the scanned line shown in the top row (Middle: horizontal scan image; Bottom: vertical scan image). The OCT images centered on the disc show that the posterior sclera in the area of a peripapillary staphyloma bows posteriorly, with the local curvature steeper than that of the adjacent scleral regions. There is also a change of curvature of the sclera at the site corresponding to the pigmentary abnormalities in stereoscopic fundus photographs (white arrows). The sclera at the edge of a staphyloma appears to be elevated inward from the surrounding sclera, and the choroid at the site of the staphyloma edge is compressed and thin (white arrows). These characteristics are the same as in highly myopic eyes with a peripapillary staphyloma.

142 AMERICAN JOURNAL OF OPHTHALMOLOGY SEPTEMBER 2016 examinations and especially swept-source OCT, which coexistence of a peripapillary ICC in the eyes with a peri- has an advantage of being able to view the sclera, are a papillary staphyloma. However, mechanical stretching and useful tool for detecting a peripapillary staphyloma with expansion is considered to be high in the area of a peripa- a slight degree of outpouching. pillary staphyloma, and this could facilitate the develop- In the swept-source OCT images, the posterior sclera in ment of an ICC. Another possibility is that the the area of a peripapillary staphyloma was seen to bow development of an ICC may facilitate the subsequent for- posteriorly, with the local curvature steeper than that of mation of a peripapillary staphyloma. Scleral bowing in the adjacent sclera. This posterior bowing of the sclera the area of an ICC might cause scleral displacement in a was similar to that observed in the ICCs.22 However, this wider area, which might become a peripapillary staphy- posterior bowing of the sclera has also been seen in eyes loma. Owing to a lack of prospective follow-up studies, it without a peripapillary ICC (Figures 2 and 3). In addition, is not clear which one develops first in the eyes with both different from a peripapillary ICC, the scleral curvature an ICC and a peripapillary staphyloma. This should be appeared to be elevated inwardly at the border of a peripa- investigated in the future. pillary staphyloma (Figures 2 and 3). Together with the Peripapillary ICCs have been reported to be present in inward elevation of the sclera, the choroid appeared to be non–highly myopic eyes and even in hyperopic eyes.25,26 compressed and thinned. This combination of scleral In this study, a peripapillary staphyloma was also found in elevation and thinning of the choroid at the edge of a non–highly myopic fellow eyes of the patients with staphyloma was reported in eyes with an inferior staphy- unilateral high myopia. Because the refractive status or loma owing to tilted disc syndrome.23 Thus, this might be axial length is determined by the location of the fovea, a common phenomenon at the edge of a staphyloma peripapillary changes might be independent of the degree regardless of the types of staphyloma. of myopia. A peripapillary ICC was frequently found in eyes with a This study has several limitations. First, because a peripa- peripapillary staphyloma: in 52% of all eyes, in 54.5% of pillary staphyloma was not a frequent type of staphyloma, the highly myopic eyes, and in 33.3% of non–highly the number of patients was not high. Second, this study myopic eyes. Through careful observations by enhanced was not a prospective follow-up study; thus, it was not clear depth imaging OCT and swept-source OCT, Spaide and as- how peripapillary staphyloma was formed and then sociates22 showed that an ICC resulted from a posterior progressed. Swept-source OCT has a great advantage in displacement of the sclera. They also reported the presence observing the details of scleral curvature; thus it would be of a full-thickness retinal defect at the edge of a peripapil- a good method to analyze how a peripapillary staphyloma lary ICC, which supports the high prevalence of glaucoma- develops and progresses. like visual field defects in these eyes, as reported by In conclusion, we have detected the morphologic char- Shimada and associates.24 Shimada and associates reported acteristics of peripapillary staphylomas by swept-source that the peripapillary ICC was found in 14 of the 127 highly OCT. Because the deformation of an eye with a peripapil- myopic eyes (11%) examined by spectral-domain OCT. lary staphyloma is occasionally difficult to recognize by 3D Thus, a rate of 52.5% of ICCs in the present study is very MRI, the diagnosis of a peripapillary staphyloma should be high. We have not determined the reason for the frequent done by swept-source OCT.

FUNDING/SUPPORT: SUPPORTED IN PART BY RESEARCH GRANT 15H04993 AND 15K15629 FROM THE JAPAN SOCIETY FOR THE Promotion of Science, Tokyo, Japan. Financial disclosures: The following authors have no ﬁnancial disclosures: Kosei Shinohara, Muka Moriyama, Noriaki Shimada, Takeshi Yoshida, and Kyoko Ohno-Matsui. All authors attest that they meet the current ICMJE criteria for authorship. The authors thank Prof. Duco Hamasaki (Bascom Palmer Eye Institute, Miami) for his critical discussion and ﬁnal manuscript revision.

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