STEREOPSIS AND OPTICAL COHERENCE TOMOGRAPHY FINDINGS AFTER EPIRETINAL MEMBRANE SURGERY FUMIKI OKAMOTO, MD, YOSHIMI SUGIURA, MD, YOSHIFUMI OKAMOTO, MD, TAKAHIRO HIRAOKA, MD, TETSURO OSHIKA, MD Purpose: To evaluate stereopsis in patients undergoing vitrectomy for epiretinal membrane and to investigate the relationship between stereopsis and foveal microstructures. Methods: This study included 55 eyes of 55 patients who underwent vitrectomy for unilateral epiretinal membrane and 27 age-matched normal subjects. We examined stereopsis using the Titmus Stereo Test, TNO stereotest, and, optical coherence tomography before surgery and 6 months after surgery. Central foveal thickness, central retinal thickness at the parafovea (CRT-3 mm), macular volume, and retinal layer thickness were measured with the optical coherence tomography software and an image-processing program. Results: Epiretinal membrane surgery significantly improved stereopsis in Titmus Stereo Test and in TNO. Stereopsis after surgery was significantly worse than in normal subjects. In stepwise multiple regression analysis, preoperative stereopsis showed a significant association with preoperative CRT-3 mm. Postoperative stereopsis was significantly correlated with postoperative inner nuclear layer thickness. Postoperative Titmus Stereo Test and TNO were significantly related to preoperative CRT-3 mm and preoperative macular volume and inner nuclear layer thickness, respectively. Conclusion: Vitrectomy for epiretinal membrane improved stereopsis, albeit not to a normal level. Titmus Stereo Test, a stereotest with a smaller index, was related to CRT-3 mm, whereas TNO with a larger index was correlated with retinal volume of the entire posterior pole and mean inner nuclear layer thickness. RETINA 35:1415–1421, 2015
E
cases. Stereopsis is the ability to perceive the depth of field based on the disparity of the images formed by two eyes. Asaria et al3 evaluated binocular visual function after vitrectomy for ERM and found that stereopsis deteriorated by a unilateral ERM, with some recovery observed after vitrectomy, although not to a normal level. With the introduction of optical coherence tomography (OCT), clinicians now can evaluate the microstructural changes of the macula region both qualitatively and quantitatively.4,5 Many studies have reported on visual acuity and metamorphopsia, and the relationship between these visual functions and the OCT findings in patients with ERM.6–23 However, no studies have investigated the relationship between stereopsis and the retinal microstructure in patients with ERM. The purpose of this study was to quantify stereopsis in patients undergoing vitrectomy for ERM, and to
piretinal membrane (ERM) is generally located in the macula and its ability to contract can distort the photoreceptor distribution in the fovea, frequently resulting in disturbance of visual acuity or metamorphopsia. A majority of patients with ERM (80–85%) exhibit moderate-to-severe distortion of vision, or metamorphopsia, as one of the most common symptoms.1,2 Surgery for ERM has been a common vitreoretinal procedure for many years. However, even after successful membrane peeling and improvement of visual acuity, the postoperative quality of vision, such as distortion, diplopia, and aniseikonia, may be unsatisfactory in some From the Department of Ophthalmology, Faculty of Medicine, University of Tsukuba, Ibaraki, Japan. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Fumiki Okamoto, MD, Department of Ophthalmology, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki 305-8575 Japan; e-mail: fumiki-o@ md.tsukuba.ac.jp
1415
1416 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
investigate the relationship between the stereopsis and spectral domain OCT findings. Methods We included 55 eyes of 55 patients with unilateral ERM who were undergoing pars plana vitrectomy at Tsukuba University Hospital. The subjects were 22 men and 33 women, averaging 65.8 ± 9.9 years of age (mean ± standard deviation). Twenty-seven agematched subjects served as controls (13 men and 14 women, age, 64.0 ± 6.0 years). We conducted this prospective, consecutive comparative study in accordance with the Declaration of Helsinki, and received approval from the Institutional Review Committees of University of Tsukuba Hospital. Before inclusion in the study, all patients provided informed consent after the nature of the study was explained. Epiretinal membrane was defined as macular thickening involving the center of the macular, with or without distortion, and wrinkling of the inner retinal surface on biomicroscopy and OCT. Exclusion criteria were age under 18 years, previously diagnosed anterior segment disease, glaucoma, moderate and severe cataract, any systemic disease that influenced ocular motility, and vitreoretinal disorders except ERM. Eyes with secondary ERM because of retinal vascular disease, uveitis, trauma, and retinal breaks were also excluded from the study. All patients underwent examinations including bestcorrected visual acuity (BCVA), cover test, and ocular motility before and 6 months after surgery. Bestcorrected visual acuity measured with the Landolt Chart was expressed as logarithm of the minimum angle of resolution (logMAR). A 4-diopter (D) prism test was performed to detect the presence of a central suppression scotoma or small manifest deviation and to prove bifoveal fixation. All patients had good corrected visual acuity in the fellow eye. The requirements included no shift of either eye on cover test, distance and near, normal or atypical-1 response to 4-D base-out prism test, no history of strabismus or amblyopia. Stereopsis was measured with the Titmus Stereo Test (TST) and TNO stereotest at the standard viewing distance of 40 cm with appropriate spectacle correction. To ensure that patients were not using monocular clues in TST, responses were checked by inverting the stereotarget and asking the patient if the target appeared in front of or behind the page. The results of TST and TNO were expressed as “seconds of arc.” We converted these values to logarithm for statistical evaluation. Retinal images were obtained with spectral domain OCT (Cirrus high-definition OCT; Carl Zeiss,
2015 VOLUME 35 NUMBER 7
Dublin, CA). We performed the 5-line Raster scans in a horizontal and vertical manner for each eye using the Cirrus analysis software version 3.0. Scans with signal strength of .7/10 were considered appropriate, and a representative image was selected. Based on the obtained image with OCT, the following six parameters were measured: central foveal thickness (CFT), central retinal thickness at the parafovea (CRT-3 mm), macular volume (MV), thickness of the ganglion cell layer (GCL), inner nuclear layer (INL), and outer retinal layer (outer nuclear layer and outer plexiform layer [ONL + OPL]). The Cirrus highdefinition OCT device automatically calculates CFT, CRT-3 mm, and MV. We divided the 1.0- · 1.0-mm area centered on the fovea into 9 sections at 0.25-mm intervals and quantified the preceding retinal layer thickness.6 A freely available image-processing program (ImageJ software; developed by Wayne Rasband, National Institutes of Health, Bethesda, MD; available from http://rsbweb.nih.gov/ij/index.html) was used to quantify the thickness of each retinal layer. The continuity of the external limiting membrane (ELM), the photoreceptor inner and outer segment (IS/OS) junction, and cone outer segment tips (COST) line was evaluated on OCT images at the 1.0- · 1.0-mm area centered on the fovea. A disruption of each line was diagnosed when there was a loss of each hyperreflective line. Two graders (Y.S., T.H.) measured retinal layer thickness and assessed the status of the ELM, IS/OS junction, and COST line. Both the graders were masked to the clinical findings of the patients, including their visual acuity and stereopsis. All surgeries were performed by two surgeons (F.O., Y.O.) under sub-Tenon local anesthesia. The lens was removed by phacoemulsification and intraocular lens implantation when required, followed by vitrectomy. The surgical technique used was 23-gauge or 25-gauge pars plana vitrectomy. With the aid of conventional contact lenses and a wide viewing system, posterior hyaloid separation and removal of the posterior vitreous membrane were performed. The ERM and inner limiting membrane were removed with intraocular forceps by a double staining technique.24 Peripheral retinal examination with scleral depression was performed to search for a retinal tear. Air–fluid exchange was conducted if iatrogenic retinal tear and/or rhegmatogenous retinal detachment were identified intraoperatively. The mean scores were compared, and standard deviations were calculated for each parameter of visual function and OCT measurements. A Mann–Whitney U test was performed to compare stereopsis between patients with ERM and normal subjects. The same test was also used to compare stereopsis related to the
1417
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL
continuity of ELM, IS/OS junction, and COST line. A Wilcoxon signed-ranks test was performed to compare preoperative and postoperative visual function and OCT parameters. The associations between stereopsis and OCT parameters, and between preoperative and postoperative stereopsis were examined by the Spearman rank correlation test. If significant differences between stereopsis and OCT parameters were observed, we conducted a stepwise multiple regression analysis using the parameters related to stereopsis as explanatory variables. All tests of associations were considered statistically significant if P , 0.05. The analyses were carried out using StatView (version 5.0; SAS Inc, Cary, NC). Results Table 1 shows visual functions and OCT parameters of patients with ERM before and after surgery. Vitrectomy significantly improved logMAR BCVA, whereas spherical equivalent and the difference in spherical equivalent between both eyes did not change. Central foveal thickness, CRT-3 mm, MV, mean GCL, INL, and ONL + OPL thickness at 6 months after surgery were significantly lower than the baseline values. Stereopsis Before and After Surgery for ERM and Normal Subjects The results of stereopsis in the patients with ERM and normal subjects are shown in Figure 1. ERM surgery significantly improved TST values (P , 0.05) and TNO stereotest values (P , 0.0005). Titmus Stereo Test and TNO stereotest values (log) in normal subjects were 1.88 ± 0.39 and 1.71 ± 0.15, respectively. Stereopsis
values of patients with ERM before and after surgery were significantly worse than those of normal subjects. Preoperatively, 5 of 55 patients realized only the fly screening plate in depth with TST (3,000 seconds of arc), whereas 3 patients exhibited good stereopsis of 40 or 50 seconds of arc. Postoperatively, the number of patients who showed 3,000 seconds of arc came down to 3, whereas those who demonstrated good stereopsis increased to 9 (Figure 2). With the TNO stereotest, 27 of 55 patients could only appreciate the screening plates (1,980 seconds of arc) before surgery, but the number came down to 18 after surgery (Figure 3). Relationship Between Stereopsis and Visual Acuity in Patients With ERM Preoperative stereopsis showed a significant correlation with preoperative logMAR BCVA (TST: r = 0.466, P , 0.0005; TNO stereotest: r = 0.379, P , 0.005). At 6 months postoperatively, stereopsis significantly correlated with logMAR BCVA (TST: r = 0.490, P , 0.0005; TNO stereotest: r = 0.371, P , 0.01). Postoperative TST values significantly correlated with preoperative logMAR BCVA (r = 0.279, P , 0.05), whereas postoperative TNO stereotest values showed no association with preoperative logMAR BCVA (r = 0.264, P = 0.054). Postoperative logMAR BCVA was not associated with preoperative TST (r = 0.187, P = 0.179) and TNO stereotest values (r = 0.200, P = 0.151). Relationship Between Stereopsis and OCT Parameters Before and After Surgery Preoperatively, the log values of TST had a significant correlation with CFT (P , 0.001), CRT-3 mm
Table 1. Visual Function and Retinal Microstructure in Eyes After ERM Surgery
BCVA (logMAR) Spherical equivalent (D) Difference in spherical equivalent between both eyes (D) Stereopsis Titmus Stereo Test (log) TNO stereotest (log) CFT (mm) CRT-3 mm (mm) MV (mm3) Mean GCL thickness (mm) Mean INL thickness (mm) Mean ONL + OPL thickness (mm) ELM disruption no. (%) IS/OS disruption no. (%) COST disruption no. (%)
Before Surgery
6 Months After Surgery
0.33 ± 0.23 −1.2 ± 2.3 0.8 ± 1.1
0.14 ± 0.19* −1.4 ± 1.8 1.0 ± 1.0
2.35 ± 0.51 2.84 ± 0.48 423 ± 140 420 ± 73 12.0 ± 1.4 131 ± 50 96 ± 34 198 ± 22 6 (11) 7 (13) 38 (69)
2.19 ± 0.45† 2.63 ± 0.53‡ 322 ± 82* 355 ± 30* 10.8 ± 0.8* 89 ± 17* 75 ± 19* 180 ± 22* 2 (4) 6 (11) 37 (67)
Values are presented as mean ± standard deviation. Statistically significant compared with baseline (*P , 0.0001; †P , 0.05; ‡P , 0.005).
1418 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
2015 VOLUME 35 NUMBER 7
Fig. 1. Box and whisker plots with the top and bottom boundaries of the box indicating the 75th and 25th percentiles, respectively. Whiskers above and below the box indicate the 90th and 10th percentiles, respectively. A. Titmus Stereo test values of patients with ERM before and after surgery and of normal subjects. B. TNO stereotest values of patients with ERM before and after surgery and of normal subjects. *P , 0.0001; †P , 0.05; ‡P , 0.005.
(P , 0.0001), MV (P , 0.05), mean GCL thickness (P , 0.05), mean INL thickness (P , 0.005), status of ELM line (P , 0.005), and status of COST line (P , 0.05). No significant correlations were found between preoperative TST values and mean ONL + OPL thickness (P = 0.392) and status of IS/OS junction line (P = 0.266). Multiple regression analysis revealed that preoperative TST values were significantly related to the CRT-3 mm (r = 0.553, P , 0.01, F-statistic = 13.622), whereas other variables (CFT, MV, mean GCL and INL thickness, status of ELM and COST line) were not relevant. Preoperative TNO stereotest values showed a significant correlation with CFT (P , 0.0005), CRT-3 mm (P , 0.0001), MV (P , 0.0001), mean GCL thickness (P , 0.001), and mean INL thickness (P , 0.005), whereas other variables were not relevant. Central retinal thickness at the parafovea was significantly associated with preoperative TNO stereotest values by multiple regression analysis (r = 0.622, P , 0.0001, F-statistic = 27.169), but CFT, MV, mean GCL, and mean INL thickness were not associated with preoperative TNO stereotest values. At 6 months postoperatively, TST values significantly correlated with mean INL thickness (P , 0.01). TNO stereotest values showed a significant correlation
Fig. 2. Histogram of the TST values in patients with ERM before and after surgery.
with CFT (P , 0.005) and mean INL thickness (P , 0.0001), whereas other variables were not relevant. Multiple significant correlations were found between postoperative TNO stereotest values and mean INL thickness (r = 0.565, P , 0.0001, F-statistic = 20.178). Preoperative Factors of OCT Parameters Affecting Postoperative Stereopsis Titmus Stereo Test values at 6 months postoperatively significantly correlated with preoperative CFT (P , 0.005), CRT-3 mm (P , 0.001, Figure 4A), MV (P , 0.005), and mean ONL + OPL thickness (P , 0.005). Multiple regression analysis revealed that postoperative TST values were significantly related to preoperative CRT-3 mm (r = 0.480, P , 0.001, F-statistic = 12.841), whereas other variables (CFT, MV, and mean ONL + OPL thickness) were not relevant. Postoperative TNO stereotest values showed a significant correlation with preoperative CFT (P , 0.0005),
Fig. 3. Histogram of the TNO stereotest values in patients with ERM before and after surgery.
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL
1419
Fig. 4. Correlation between postoperative stereopsis and preoperative OCT parameters. A. Postoperative TST values versus preoperative CRT-3 mm in patients with ERM. B. Postoperative TNO stereotest values versus preoperative mean INL thickness in patients with ERM. C. Postoperative TNO stereotest values versus preoperative retinal volume at the 5.0- · 5.0-mm area centered on the fovea (MV) in patients with ERM.
CRT-3 mm (P , 0.0005), mean INL thickness (P , 0.005, Figure 4B), mean GCL thickness (P , 0.01), and MV (P , 0.0001, Figure 4C). Multiple significant correlations were found between postoperative TNO stereotest values and preoperative MV (r = 0.554, P , 0.0001, F-statistic = 19.066) and mean INL thickness (r = 0.296, P , 0.0001, F-statistic = 4.813), whereas other variables (CFT, CRT-3 mm, and mean GCL thickness) were not relevant.
Discussion This study demonstrated that stereopsis improved after ERM removal but remained inferior to the stereopsis of the controls. In addition, stereopsis was associated with various parameters of the retinal microstructure. Central retinal thickness at the parafovea is a prognostic factor for postoperative TST, whereas MV and mean INL thickness are prognostic factors for postoperative TNO stereotest in multiple regression analysis. This is the first study to report the relationship between stereopsis and OCT findings in patients with retinal disease. Epiretinal membrane surgery generally improves visual acuity. Stereopsis was also improved by surgery, albeit not to a normal level in this study. Kinoshita et al7 investigated the time course of changes in metamorphopsia after ERM surgery and found that although metamorphopsia was reduced by surgery, moderate metamorphopsia remained for up to 12 months after surgery. In addition, retinally induced aniseikonia in ERM remained after surgery longitudinally.25 Judging from the findings of previous reports and our present study, it is considered that visual prognosis of patients with ERM is good in general, whereas satisfactory results have not been obtained for other visual functions, including stereopsis, metamorphopsia, and aniseikonia. Asaria et al3 reported
that patients with ERM with a longer duration of symptoms before surgery had worse stereopsis both preoperatively and postoperatively. Longstanding surgical monovision induced by refractive surgery deteriorated stereopsis.26 Progressive reduction in stereopsis in patients with ERM may be caused by deterioration in binocular vision at the cortical level. Preoperative and postoperative stereopsis showed a significant correlation with visual acuity. Stereopsis could also be damaged in patients after successful surgery of unilateral ERM, macular hole, or retinal detachment.3,27–29 Previous reports have indicated an association between visual acuity and stereopsis in normal subjects,30–32 in patients who underwent macular hole surgery,27 and in patients after retinal detachment surgery.29,33 These results are consistent with our findings. Stereopsis was significantly associated with various OCT parameters, including CFT, CRT-3 mm, MV, each retinal layer thickness, and each outer retinal line by simple regression. Multiple regression analysis revealed that preoperative TST and TNO values were significantly correlated with preoperative CRT-3 mm that indicated central retinal thickness at the parafovea. Many studies have reported on the association between visual acuity and OCT findings in patients with ERM. Visual acuity was significantly associated with some parameters at the foveal lesion, including CFT,10–12 outer retinal thickness,13 integrity of IS/OS junction,14,15 and COST line.16 This discrepancy may arise from the different index size in visual acuity, TST, and TNO stereotest. At the standard examination distance, the TST circles subtend a visual angle of 0.7° and 1 set of 4 circles subtends 2.5°. TNO stereotest subtends a visual angle of 8.5°. In contrast, the visual angle of index in visual acuity chart was much smaller than that for stereopsis. Thus, it is considered that visual acuity with a relatively smaller index was associated with CFT, which was small in area, and each
1420 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
outer retinal line at the foveal lesion, whereas the TST and TNO stereotest with a larger index showed an association with larger parafoveal lesion. Postoperative TST and TNO values showed a significant correlation with postoperative INL thickness. The thickness of INL in patients with ERM was found to be associated with metamorphopsia.6,8,10 In addition, b-wave and oscillatory potentials measured with focal macular electroretinography were reduced in eyes with ERM, indicating that ERM damaged the neurons in the inner retinal layers.34–36 These morphologic and functional disturbances in the inner retina could have an influence on stereopsis. Prognostic factors for postoperative stereopsis in patients with ERM were CRT-3 mm in TST, and MV and mean INL thickness in TNO stereotest. Macular volume means the retinal volume at the 5.0- · 5.0-mm area centered on the fovea and is wider than the area of CRT-3 mm. As described earlier, the stimulus index of the TNO stereotest is larger than those of Titmus circles. Thus, the TNO stereotest with a relatively larger index size might have demonstrated an association with wider MV. As prognostic factors for visual acuity, CFT,8,17 photoreceptor outer segment length,19 integrity of IS/OS junction,15,20,21 and COST line at the foveal lesion22,23 have been reported. Based on these studies, it suggested that in patients with ERM, stereopsis is affected by a wider area of the retinal structure than visual acuity. Our study has several limitations. Although some other factors are known to affect stereopsis, such as eye dominance,37,38 pupil size,39,40 and accommodation,32,41 we did not take these factors into consideration in this study. Other limitations of this study include a relatively small sample size, measurements based on only five horizontal B-scan cross sections, and imaging inaccuracy in each of the retinal layers of ERM eyes by manual segmentation. In addition, our postoperative follow-up was short. We evaluated the patients at 6 months postoperatively. Previous studies reported that visual acuity in patients with ERM improved more at 1 to 3 years postoperatively than at 6 months postoperatively.42 Therefore, stereopsis may improve in a longer follow-up period. Future studies with a large sample size, longer follow-up period, and improved OCT technologies will be needed. Key words: epiretinal membrane, stereopsis, optical coherence tomography. References 1. Bouwens MD, Meurs JC. Sine Amsler Charts: a new method for the follow-up of metamorphopsia in patients undergoing
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
2015 VOLUME 35 NUMBER 7
macular pucker surgery. Graefes Arch Clin Exp Ophthalmol 2003;241:89–93. Wong JG, Sachder N, Beaumont PE, Chang AA. Visual outcomes following vitrectomy and peeling of epiretinal membrane. Clin Experiment Ophthalmol 2005;33:373–378. Asaria R, Garnham L, Gregor ZJ, Sloper JJ. A prospective study of binocular visual function before and after successful surgery to remove a unilateral epiretinal membrane. Ophthalmology 2008;115:1930–1937. Puliafito CA, Hee MR, Lin CP, et al. Imaging of macular diseases with optical coherence tomography. Ophthalmology 1995;102:217–229. Wilkins JR, Puliafito CA, Hee MR, et al. Characterization of epiretinal membranes using optical coherence tomography. Ophthalmology 1996;103:2142–2151. Okamoto F, Sugiura Y, Okamoto Y, et al. Associations between metamorphopsia and foveal microstructure in patients with epiretinal membrane. Invest Ophthalmol Vis Sci 2012;53: 6770–6775. Kinoshita T, Imaizumi H, Okushiba U, et al. Time course of changes in metamorphopsia, visual acuity, and OCT parameters after successful epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2012;53:3592–3597. Kim JH, Kang SW, Kong MG, Ha HS. Assessment of retinal layers and visual rehabilitation after epiretinal membrane removal. Graefes Arch Clin Exp Ophthalmol 2013;251: 1055–1064. Bae SH, Kim D, Park TK, et al. Preferential hyperacuity perimeter and prognostic factors for metamorphopsia after idiopathic epiretinal membrane surgery. Am J Ophthalmol 2013;155: 109–117. Watanabe A, Arimoto S, Nishi O. Correlation between metamorphopsia and epiretinal membrane optical coherence tomography findings. Ophthalmology 2009;116:1788–1793. Michalewski J, Michalewska Z, Cisiecki S, Nawrocki J. Morphologically functional correlations of macular pathology connected with epiretinal membrane formation in spectral optical coherence tomography (SOCT). Graefes Arch Clin Exp Ophthalmol 2007;245:1623–1631. Ooto S, Hangai M, Takayama K, et al. High-resolution imaging of the photoreceptor layer in epiretinal membrane using adaptive optics scanning laser ophthalmoscopy. Ophthalmology 2011;118:873–881. Arichika S, Hangai M, Yoshimura N. Correlation between thickening of the inner and outer retina and visual acuity in patients with epiretinal membrane. Retina 2010;30:503–508. Inoue M, Morita S, Watanabe Y, et al. Inner segment/outer segment junction assessed by spectral-domain optical coherence tomography in patients with idiopathic epiretinal membrane. Am J Ophthalmol 2010;150:834–839. Suh MH, Seo JM, Park KH, Yu HG. Associations between macular findings by optical coherence tomography and visual outcomes after epiretinal membrane removal. Am J Ophthalmol 2009;147:473–480. Watanabe K, Tsunoda K, Mizuno Y, et al. Outer retinal morphology and visual function in patients with idiopathic epiretinal membrane. JAMA Ophthalmol 2013;131:172–177. Kim J, Rhee KM, Woo SJ, et al. Long-term temporal changes of macular thickness and visual outcome after vitrectomy for idiopathic epiretinal membrane. Am J Ophthalmol 2010;150: 701–709. Falkner-Radler CI, Glittenberg C, Hagen S, et al. Spectraldomain optical coherence tomography for monitoring epiretinal membrane surgery. Ophthalmology 2010;117:798–805.
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL 19. Shiono A, Kogo J, Klose G, et al. Photoreceptor outer segment length: a prognostic factor for idiopathic epiretinal membrane surgery. Ophthalmology 2013;120:788–794. 20. Mitamura Y, Hirano K, Baba T, Yamamoto S. Correlation of visual recovery with presence of photoreceptor inner/outer segment junction in optical coherence images after epiretinal membrane surgery. Br J Ophthalmol 2009;93:171–175. 21. Inoue M, Morita S, Watanabe Y, et al. Preoperative inner segment/outer segment junction in spectral-domain optical coherence tomography as a prognostic factor in epiretinal membrane surgery. Retina 2011;31:1366–1372. 22. Shimozono M, Oishi A, Hata M, et al. The significance of cone outer segment tips as a prognostic factor in epiretinal membrane surgery. Am J Ophthalmol 2012;153:698–704. 23. Itoh Y, Inoue M, Rii T, et al. Correlation between foveal cone outer segment tips line and visual recovery after epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2013;54: 7302–7308. 24. Shimada H, Nakashizuka H, Hattori T, et al. Double staining with brilliant blue G and double peeling for epiretinal membranes. Ophthalmology 2009;11:1370–1376. 25. Rutstein RP. Retinally induced aniseikonia: a case series. Optom Vis Sci 2012;89:e50–5. 26. Fawcett SL, Herman WK, Alfieri CD, et al. Stereoacuity and foveal fusion in adults with long-standing surgical monovision. J AAPOS 2001;5:342–347. 27. Hikichi T, Onodera A, Ishiko S, et al. Stereo acuity in patients with unilateral macular hole and after unilateral macular hole surgery. Graefes Arch Clin Exp Ophthalmol 2001;239:128– 132. 28. Mireskandari K, Garnham L, Sheard R, et al. A prospective study of the effect of a unilateral macular hole on sensory and motor binocular function and recovery following successful surgery. Br J Ophthalmol 2004;88:1320–1324. 29. Watanabe H, Okamoto F, Sugiura Y, et al. Stereopsis after successful surgery for rhegmatogenous retinal detachment. Graefes Arch Clin Exp Ophthalmol 2014;252:1207–1212.
1421
30. Levy NS, Glick EB. Stereoscopic perception and Snellen visual acuity. Am J Ophthalmol 1974;78:722–724. 31. Donzis PB, Rappazzo JA, Burde RM, Gordon M. Effect of binocular variations of Snellen’s visual acuity on Titmus stereoacuity. Arch Ophthalmol 1983;101:930–932. 32. Goodwin RT, Romano PE. Stereoacuity degradation by experimental and real monocular and binocular amblyopia. Invest Ophthalmol Vis Sci 1985;26:917–923. 33. Amemiya T, Takami H, Yoshida H, Harayama K. Binocular visual function after surgery for detached retina. Graefes Arch Clin Exp Ophthalmol 1982;218:304–306. 34. Tanikawa A, Horiguchi M, Kondo M, et al. Abnormal focal macular electroretinograms in eyes with idiopathic epimacular membrane. Am J Ophthalmol 1999;127:559–564. 35. Niwa T, Terasaki H, Kondo M, et al. Function and morphology of macula before and after removal of idiopathic epiretinal membrane. Invest Ophthalmol Vis Sci 2003;44:1652–1656. 36. Hibi N, Ueno S, Ito Y, et al. Relationship between retinal layer thickness and focal macular electroretinogram components after epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2013;54:7207–7214. 37. Weinman J, Cooke V. Eye dominance and stereopsis. Perception 1982;11:207–210. 38. Erickson P, McGill EC. Role of visual acuity, stereoacuity, and ocular dominance in monovision patient success. Optom Vis Sci 1992;69:761–764. 39. Pierce DM. Comparability of two methods of estimating realdepth acuity. Ophthalmologica 1975;171:224–235. 40. Lovasik JV, Szymkiw M. Effects of aniseikonia, anisometropia, accommodation, retinal illuminance, and pupil size on stereopsis. Invest Ophthalmol Vis Sci 1985;26:741–750. 41. Kani W. Stereopsis and spatial perception in amblyopes and uncorrected ametropes. Br J Ophthalmol 1978;62:756–762. 42. Pesin SR, Olk RJ, Grand MG, et al. Vitrectomy for premacular fibroplasia: prognostic factors, long-term follow-up, and time course of visual improvement. Ophthalmology 1991;98:1109– 1114.
E
cases. Stereopsis is the ability to perceive the depth of field based on the disparity of the images formed by two eyes. Asaria et al3 evaluated binocular visual function after vitrectomy for ERM and found that stereopsis deteriorated by a unilateral ERM, with some recovery observed after vitrectomy, although not to a normal level. With the introduction of optical coherence tomography (OCT), clinicians now can evaluate the microstructural changes of the macula region both qualitatively and quantitatively.4,5 Many studies have reported on visual acuity and metamorphopsia, and the relationship between these visual functions and the OCT findings in patients with ERM.6–23 However, no studies have investigated the relationship between stereopsis and the retinal microstructure in patients with ERM. The purpose of this study was to quantify stereopsis in patients undergoing vitrectomy for ERM, and to
piretinal membrane (ERM) is generally located in the macula and its ability to contract can distort the photoreceptor distribution in the fovea, frequently resulting in disturbance of visual acuity or metamorphopsia. A majority of patients with ERM (80–85%) exhibit moderate-to-severe distortion of vision, or metamorphopsia, as one of the most common symptoms.1,2 Surgery for ERM has been a common vitreoretinal procedure for many years. However, even after successful membrane peeling and improvement of visual acuity, the postoperative quality of vision, such as distortion, diplopia, and aniseikonia, may be unsatisfactory in some From the Department of Ophthalmology, Faculty of Medicine, University of Tsukuba, Ibaraki, Japan. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Fumiki Okamoto, MD, Department of Ophthalmology, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki 305-8575 Japan; e-mail: fumiki-o@ md.tsukuba.ac.jp
1415
1416 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
investigate the relationship between the stereopsis and spectral domain OCT findings. Methods We included 55 eyes of 55 patients with unilateral ERM who were undergoing pars plana vitrectomy at Tsukuba University Hospital. The subjects were 22 men and 33 women, averaging 65.8 ± 9.9 years of age (mean ± standard deviation). Twenty-seven agematched subjects served as controls (13 men and 14 women, age, 64.0 ± 6.0 years). We conducted this prospective, consecutive comparative study in accordance with the Declaration of Helsinki, and received approval from the Institutional Review Committees of University of Tsukuba Hospital. Before inclusion in the study, all patients provided informed consent after the nature of the study was explained. Epiretinal membrane was defined as macular thickening involving the center of the macular, with or without distortion, and wrinkling of the inner retinal surface on biomicroscopy and OCT. Exclusion criteria were age under 18 years, previously diagnosed anterior segment disease, glaucoma, moderate and severe cataract, any systemic disease that influenced ocular motility, and vitreoretinal disorders except ERM. Eyes with secondary ERM because of retinal vascular disease, uveitis, trauma, and retinal breaks were also excluded from the study. All patients underwent examinations including bestcorrected visual acuity (BCVA), cover test, and ocular motility before and 6 months after surgery. Bestcorrected visual acuity measured with the Landolt Chart was expressed as logarithm of the minimum angle of resolution (logMAR). A 4-diopter (D) prism test was performed to detect the presence of a central suppression scotoma or small manifest deviation and to prove bifoveal fixation. All patients had good corrected visual acuity in the fellow eye. The requirements included no shift of either eye on cover test, distance and near, normal or atypical-1 response to 4-D base-out prism test, no history of strabismus or amblyopia. Stereopsis was measured with the Titmus Stereo Test (TST) and TNO stereotest at the standard viewing distance of 40 cm with appropriate spectacle correction. To ensure that patients were not using monocular clues in TST, responses were checked by inverting the stereotarget and asking the patient if the target appeared in front of or behind the page. The results of TST and TNO were expressed as “seconds of arc.” We converted these values to logarithm for statistical evaluation. Retinal images were obtained with spectral domain OCT (Cirrus high-definition OCT; Carl Zeiss,
2015 VOLUME 35 NUMBER 7
Dublin, CA). We performed the 5-line Raster scans in a horizontal and vertical manner for each eye using the Cirrus analysis software version 3.0. Scans with signal strength of .7/10 were considered appropriate, and a representative image was selected. Based on the obtained image with OCT, the following six parameters were measured: central foveal thickness (CFT), central retinal thickness at the parafovea (CRT-3 mm), macular volume (MV), thickness of the ganglion cell layer (GCL), inner nuclear layer (INL), and outer retinal layer (outer nuclear layer and outer plexiform layer [ONL + OPL]). The Cirrus highdefinition OCT device automatically calculates CFT, CRT-3 mm, and MV. We divided the 1.0- · 1.0-mm area centered on the fovea into 9 sections at 0.25-mm intervals and quantified the preceding retinal layer thickness.6 A freely available image-processing program (ImageJ software; developed by Wayne Rasband, National Institutes of Health, Bethesda, MD; available from http://rsbweb.nih.gov/ij/index.html) was used to quantify the thickness of each retinal layer. The continuity of the external limiting membrane (ELM), the photoreceptor inner and outer segment (IS/OS) junction, and cone outer segment tips (COST) line was evaluated on OCT images at the 1.0- · 1.0-mm area centered on the fovea. A disruption of each line was diagnosed when there was a loss of each hyperreflective line. Two graders (Y.S., T.H.) measured retinal layer thickness and assessed the status of the ELM, IS/OS junction, and COST line. Both the graders were masked to the clinical findings of the patients, including their visual acuity and stereopsis. All surgeries were performed by two surgeons (F.O., Y.O.) under sub-Tenon local anesthesia. The lens was removed by phacoemulsification and intraocular lens implantation when required, followed by vitrectomy. The surgical technique used was 23-gauge or 25-gauge pars plana vitrectomy. With the aid of conventional contact lenses and a wide viewing system, posterior hyaloid separation and removal of the posterior vitreous membrane were performed. The ERM and inner limiting membrane were removed with intraocular forceps by a double staining technique.24 Peripheral retinal examination with scleral depression was performed to search for a retinal tear. Air–fluid exchange was conducted if iatrogenic retinal tear and/or rhegmatogenous retinal detachment were identified intraoperatively. The mean scores were compared, and standard deviations were calculated for each parameter of visual function and OCT measurements. A Mann–Whitney U test was performed to compare stereopsis between patients with ERM and normal subjects. The same test was also used to compare stereopsis related to the
1417
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL
continuity of ELM, IS/OS junction, and COST line. A Wilcoxon signed-ranks test was performed to compare preoperative and postoperative visual function and OCT parameters. The associations between stereopsis and OCT parameters, and between preoperative and postoperative stereopsis were examined by the Spearman rank correlation test. If significant differences between stereopsis and OCT parameters were observed, we conducted a stepwise multiple regression analysis using the parameters related to stereopsis as explanatory variables. All tests of associations were considered statistically significant if P , 0.05. The analyses were carried out using StatView (version 5.0; SAS Inc, Cary, NC). Results Table 1 shows visual functions and OCT parameters of patients with ERM before and after surgery. Vitrectomy significantly improved logMAR BCVA, whereas spherical equivalent and the difference in spherical equivalent between both eyes did not change. Central foveal thickness, CRT-3 mm, MV, mean GCL, INL, and ONL + OPL thickness at 6 months after surgery were significantly lower than the baseline values. Stereopsis Before and After Surgery for ERM and Normal Subjects The results of stereopsis in the patients with ERM and normal subjects are shown in Figure 1. ERM surgery significantly improved TST values (P , 0.05) and TNO stereotest values (P , 0.0005). Titmus Stereo Test and TNO stereotest values (log) in normal subjects were 1.88 ± 0.39 and 1.71 ± 0.15, respectively. Stereopsis
values of patients with ERM before and after surgery were significantly worse than those of normal subjects. Preoperatively, 5 of 55 patients realized only the fly screening plate in depth with TST (3,000 seconds of arc), whereas 3 patients exhibited good stereopsis of 40 or 50 seconds of arc. Postoperatively, the number of patients who showed 3,000 seconds of arc came down to 3, whereas those who demonstrated good stereopsis increased to 9 (Figure 2). With the TNO stereotest, 27 of 55 patients could only appreciate the screening plates (1,980 seconds of arc) before surgery, but the number came down to 18 after surgery (Figure 3). Relationship Between Stereopsis and Visual Acuity in Patients With ERM Preoperative stereopsis showed a significant correlation with preoperative logMAR BCVA (TST: r = 0.466, P , 0.0005; TNO stereotest: r = 0.379, P , 0.005). At 6 months postoperatively, stereopsis significantly correlated with logMAR BCVA (TST: r = 0.490, P , 0.0005; TNO stereotest: r = 0.371, P , 0.01). Postoperative TST values significantly correlated with preoperative logMAR BCVA (r = 0.279, P , 0.05), whereas postoperative TNO stereotest values showed no association with preoperative logMAR BCVA (r = 0.264, P = 0.054). Postoperative logMAR BCVA was not associated with preoperative TST (r = 0.187, P = 0.179) and TNO stereotest values (r = 0.200, P = 0.151). Relationship Between Stereopsis and OCT Parameters Before and After Surgery Preoperatively, the log values of TST had a significant correlation with CFT (P , 0.001), CRT-3 mm
Table 1. Visual Function and Retinal Microstructure in Eyes After ERM Surgery
BCVA (logMAR) Spherical equivalent (D) Difference in spherical equivalent between both eyes (D) Stereopsis Titmus Stereo Test (log) TNO stereotest (log) CFT (mm) CRT-3 mm (mm) MV (mm3) Mean GCL thickness (mm) Mean INL thickness (mm) Mean ONL + OPL thickness (mm) ELM disruption no. (%) IS/OS disruption no. (%) COST disruption no. (%)
Before Surgery
6 Months After Surgery
0.33 ± 0.23 −1.2 ± 2.3 0.8 ± 1.1
0.14 ± 0.19* −1.4 ± 1.8 1.0 ± 1.0
2.35 ± 0.51 2.84 ± 0.48 423 ± 140 420 ± 73 12.0 ± 1.4 131 ± 50 96 ± 34 198 ± 22 6 (11) 7 (13) 38 (69)
2.19 ± 0.45† 2.63 ± 0.53‡ 322 ± 82* 355 ± 30* 10.8 ± 0.8* 89 ± 17* 75 ± 19* 180 ± 22* 2 (4) 6 (11) 37 (67)
Values are presented as mean ± standard deviation. Statistically significant compared with baseline (*P , 0.0001; †P , 0.05; ‡P , 0.005).
1418 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
2015 VOLUME 35 NUMBER 7
Fig. 1. Box and whisker plots with the top and bottom boundaries of the box indicating the 75th and 25th percentiles, respectively. Whiskers above and below the box indicate the 90th and 10th percentiles, respectively. A. Titmus Stereo test values of patients with ERM before and after surgery and of normal subjects. B. TNO stereotest values of patients with ERM before and after surgery and of normal subjects. *P , 0.0001; †P , 0.05; ‡P , 0.005.
(P , 0.0001), MV (P , 0.05), mean GCL thickness (P , 0.05), mean INL thickness (P , 0.005), status of ELM line (P , 0.005), and status of COST line (P , 0.05). No significant correlations were found between preoperative TST values and mean ONL + OPL thickness (P = 0.392) and status of IS/OS junction line (P = 0.266). Multiple regression analysis revealed that preoperative TST values were significantly related to the CRT-3 mm (r = 0.553, P , 0.01, F-statistic = 13.622), whereas other variables (CFT, MV, mean GCL and INL thickness, status of ELM and COST line) were not relevant. Preoperative TNO stereotest values showed a significant correlation with CFT (P , 0.0005), CRT-3 mm (P , 0.0001), MV (P , 0.0001), mean GCL thickness (P , 0.001), and mean INL thickness (P , 0.005), whereas other variables were not relevant. Central retinal thickness at the parafovea was significantly associated with preoperative TNO stereotest values by multiple regression analysis (r = 0.622, P , 0.0001, F-statistic = 27.169), but CFT, MV, mean GCL, and mean INL thickness were not associated with preoperative TNO stereotest values. At 6 months postoperatively, TST values significantly correlated with mean INL thickness (P , 0.01). TNO stereotest values showed a significant correlation
Fig. 2. Histogram of the TST values in patients with ERM before and after surgery.
with CFT (P , 0.005) and mean INL thickness (P , 0.0001), whereas other variables were not relevant. Multiple significant correlations were found between postoperative TNO stereotest values and mean INL thickness (r = 0.565, P , 0.0001, F-statistic = 20.178). Preoperative Factors of OCT Parameters Affecting Postoperative Stereopsis Titmus Stereo Test values at 6 months postoperatively significantly correlated with preoperative CFT (P , 0.005), CRT-3 mm (P , 0.001, Figure 4A), MV (P , 0.005), and mean ONL + OPL thickness (P , 0.005). Multiple regression analysis revealed that postoperative TST values were significantly related to preoperative CRT-3 mm (r = 0.480, P , 0.001, F-statistic = 12.841), whereas other variables (CFT, MV, and mean ONL + OPL thickness) were not relevant. Postoperative TNO stereotest values showed a significant correlation with preoperative CFT (P , 0.0005),
Fig. 3. Histogram of the TNO stereotest values in patients with ERM before and after surgery.
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL
1419
Fig. 4. Correlation between postoperative stereopsis and preoperative OCT parameters. A. Postoperative TST values versus preoperative CRT-3 mm in patients with ERM. B. Postoperative TNO stereotest values versus preoperative mean INL thickness in patients with ERM. C. Postoperative TNO stereotest values versus preoperative retinal volume at the 5.0- · 5.0-mm area centered on the fovea (MV) in patients with ERM.
CRT-3 mm (P , 0.0005), mean INL thickness (P , 0.005, Figure 4B), mean GCL thickness (P , 0.01), and MV (P , 0.0001, Figure 4C). Multiple significant correlations were found between postoperative TNO stereotest values and preoperative MV (r = 0.554, P , 0.0001, F-statistic = 19.066) and mean INL thickness (r = 0.296, P , 0.0001, F-statistic = 4.813), whereas other variables (CFT, CRT-3 mm, and mean GCL thickness) were not relevant.
Discussion This study demonstrated that stereopsis improved after ERM removal but remained inferior to the stereopsis of the controls. In addition, stereopsis was associated with various parameters of the retinal microstructure. Central retinal thickness at the parafovea is a prognostic factor for postoperative TST, whereas MV and mean INL thickness are prognostic factors for postoperative TNO stereotest in multiple regression analysis. This is the first study to report the relationship between stereopsis and OCT findings in patients with retinal disease. Epiretinal membrane surgery generally improves visual acuity. Stereopsis was also improved by surgery, albeit not to a normal level in this study. Kinoshita et al7 investigated the time course of changes in metamorphopsia after ERM surgery and found that although metamorphopsia was reduced by surgery, moderate metamorphopsia remained for up to 12 months after surgery. In addition, retinally induced aniseikonia in ERM remained after surgery longitudinally.25 Judging from the findings of previous reports and our present study, it is considered that visual prognosis of patients with ERM is good in general, whereas satisfactory results have not been obtained for other visual functions, including stereopsis, metamorphopsia, and aniseikonia. Asaria et al3 reported
that patients with ERM with a longer duration of symptoms before surgery had worse stereopsis both preoperatively and postoperatively. Longstanding surgical monovision induced by refractive surgery deteriorated stereopsis.26 Progressive reduction in stereopsis in patients with ERM may be caused by deterioration in binocular vision at the cortical level. Preoperative and postoperative stereopsis showed a significant correlation with visual acuity. Stereopsis could also be damaged in patients after successful surgery of unilateral ERM, macular hole, or retinal detachment.3,27–29 Previous reports have indicated an association between visual acuity and stereopsis in normal subjects,30–32 in patients who underwent macular hole surgery,27 and in patients after retinal detachment surgery.29,33 These results are consistent with our findings. Stereopsis was significantly associated with various OCT parameters, including CFT, CRT-3 mm, MV, each retinal layer thickness, and each outer retinal line by simple regression. Multiple regression analysis revealed that preoperative TST and TNO values were significantly correlated with preoperative CRT-3 mm that indicated central retinal thickness at the parafovea. Many studies have reported on the association between visual acuity and OCT findings in patients with ERM. Visual acuity was significantly associated with some parameters at the foveal lesion, including CFT,10–12 outer retinal thickness,13 integrity of IS/OS junction,14,15 and COST line.16 This discrepancy may arise from the different index size in visual acuity, TST, and TNO stereotest. At the standard examination distance, the TST circles subtend a visual angle of 0.7° and 1 set of 4 circles subtends 2.5°. TNO stereotest subtends a visual angle of 8.5°. In contrast, the visual angle of index in visual acuity chart was much smaller than that for stereopsis. Thus, it is considered that visual acuity with a relatively smaller index was associated with CFT, which was small in area, and each
1420 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
outer retinal line at the foveal lesion, whereas the TST and TNO stereotest with a larger index showed an association with larger parafoveal lesion. Postoperative TST and TNO values showed a significant correlation with postoperative INL thickness. The thickness of INL in patients with ERM was found to be associated with metamorphopsia.6,8,10 In addition, b-wave and oscillatory potentials measured with focal macular electroretinography were reduced in eyes with ERM, indicating that ERM damaged the neurons in the inner retinal layers.34–36 These morphologic and functional disturbances in the inner retina could have an influence on stereopsis. Prognostic factors for postoperative stereopsis in patients with ERM were CRT-3 mm in TST, and MV and mean INL thickness in TNO stereotest. Macular volume means the retinal volume at the 5.0- · 5.0-mm area centered on the fovea and is wider than the area of CRT-3 mm. As described earlier, the stimulus index of the TNO stereotest is larger than those of Titmus circles. Thus, the TNO stereotest with a relatively larger index size might have demonstrated an association with wider MV. As prognostic factors for visual acuity, CFT,8,17 photoreceptor outer segment length,19 integrity of IS/OS junction,15,20,21 and COST line at the foveal lesion22,23 have been reported. Based on these studies, it suggested that in patients with ERM, stereopsis is affected by a wider area of the retinal structure than visual acuity. Our study has several limitations. Although some other factors are known to affect stereopsis, such as eye dominance,37,38 pupil size,39,40 and accommodation,32,41 we did not take these factors into consideration in this study. Other limitations of this study include a relatively small sample size, measurements based on only five horizontal B-scan cross sections, and imaging inaccuracy in each of the retinal layers of ERM eyes by manual segmentation. In addition, our postoperative follow-up was short. We evaluated the patients at 6 months postoperatively. Previous studies reported that visual acuity in patients with ERM improved more at 1 to 3 years postoperatively than at 6 months postoperatively.42 Therefore, stereopsis may improve in a longer follow-up period. Future studies with a large sample size, longer follow-up period, and improved OCT technologies will be needed. Key words: epiretinal membrane, stereopsis, optical coherence tomography. References 1. Bouwens MD, Meurs JC. Sine Amsler Charts: a new method for the follow-up of metamorphopsia in patients undergoing
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
2015 VOLUME 35 NUMBER 7
macular pucker surgery. Graefes Arch Clin Exp Ophthalmol 2003;241:89–93. Wong JG, Sachder N, Beaumont PE, Chang AA. Visual outcomes following vitrectomy and peeling of epiretinal membrane. Clin Experiment Ophthalmol 2005;33:373–378. Asaria R, Garnham L, Gregor ZJ, Sloper JJ. A prospective study of binocular visual function before and after successful surgery to remove a unilateral epiretinal membrane. Ophthalmology 2008;115:1930–1937. Puliafito CA, Hee MR, Lin CP, et al. Imaging of macular diseases with optical coherence tomography. Ophthalmology 1995;102:217–229. Wilkins JR, Puliafito CA, Hee MR, et al. Characterization of epiretinal membranes using optical coherence tomography. Ophthalmology 1996;103:2142–2151. Okamoto F, Sugiura Y, Okamoto Y, et al. Associations between metamorphopsia and foveal microstructure in patients with epiretinal membrane. Invest Ophthalmol Vis Sci 2012;53: 6770–6775. Kinoshita T, Imaizumi H, Okushiba U, et al. Time course of changes in metamorphopsia, visual acuity, and OCT parameters after successful epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2012;53:3592–3597. Kim JH, Kang SW, Kong MG, Ha HS. Assessment of retinal layers and visual rehabilitation after epiretinal membrane removal. Graefes Arch Clin Exp Ophthalmol 2013;251: 1055–1064. Bae SH, Kim D, Park TK, et al. Preferential hyperacuity perimeter and prognostic factors for metamorphopsia after idiopathic epiretinal membrane surgery. Am J Ophthalmol 2013;155: 109–117. Watanabe A, Arimoto S, Nishi O. Correlation between metamorphopsia and epiretinal membrane optical coherence tomography findings. Ophthalmology 2009;116:1788–1793. Michalewski J, Michalewska Z, Cisiecki S, Nawrocki J. Morphologically functional correlations of macular pathology connected with epiretinal membrane formation in spectral optical coherence tomography (SOCT). Graefes Arch Clin Exp Ophthalmol 2007;245:1623–1631. Ooto S, Hangai M, Takayama K, et al. High-resolution imaging of the photoreceptor layer in epiretinal membrane using adaptive optics scanning laser ophthalmoscopy. Ophthalmology 2011;118:873–881. Arichika S, Hangai M, Yoshimura N. Correlation between thickening of the inner and outer retina and visual acuity in patients with epiretinal membrane. Retina 2010;30:503–508. Inoue M, Morita S, Watanabe Y, et al. Inner segment/outer segment junction assessed by spectral-domain optical coherence tomography in patients with idiopathic epiretinal membrane. Am J Ophthalmol 2010;150:834–839. Suh MH, Seo JM, Park KH, Yu HG. Associations between macular findings by optical coherence tomography and visual outcomes after epiretinal membrane removal. Am J Ophthalmol 2009;147:473–480. Watanabe K, Tsunoda K, Mizuno Y, et al. Outer retinal morphology and visual function in patients with idiopathic epiretinal membrane. JAMA Ophthalmol 2013;131:172–177. Kim J, Rhee KM, Woo SJ, et al. Long-term temporal changes of macular thickness and visual outcome after vitrectomy for idiopathic epiretinal membrane. Am J Ophthalmol 2010;150: 701–709. Falkner-Radler CI, Glittenberg C, Hagen S, et al. Spectraldomain optical coherence tomography for monitoring epiretinal membrane surgery. Ophthalmology 2010;117:798–805.
STEREOPSIS AND OCT AFTER ERM SURGERY OKAMOTO ET AL 19. Shiono A, Kogo J, Klose G, et al. Photoreceptor outer segment length: a prognostic factor for idiopathic epiretinal membrane surgery. Ophthalmology 2013;120:788–794. 20. Mitamura Y, Hirano K, Baba T, Yamamoto S. Correlation of visual recovery with presence of photoreceptor inner/outer segment junction in optical coherence images after epiretinal membrane surgery. Br J Ophthalmol 2009;93:171–175. 21. Inoue M, Morita S, Watanabe Y, et al. Preoperative inner segment/outer segment junction in spectral-domain optical coherence tomography as a prognostic factor in epiretinal membrane surgery. Retina 2011;31:1366–1372. 22. Shimozono M, Oishi A, Hata M, et al. The significance of cone outer segment tips as a prognostic factor in epiretinal membrane surgery. Am J Ophthalmol 2012;153:698–704. 23. Itoh Y, Inoue M, Rii T, et al. Correlation between foveal cone outer segment tips line and visual recovery after epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2013;54: 7302–7308. 24. Shimada H, Nakashizuka H, Hattori T, et al. Double staining with brilliant blue G and double peeling for epiretinal membranes. Ophthalmology 2009;11:1370–1376. 25. Rutstein RP. Retinally induced aniseikonia: a case series. Optom Vis Sci 2012;89:e50–5. 26. Fawcett SL, Herman WK, Alfieri CD, et al. Stereoacuity and foveal fusion in adults with long-standing surgical monovision. J AAPOS 2001;5:342–347. 27. Hikichi T, Onodera A, Ishiko S, et al. Stereo acuity in patients with unilateral macular hole and after unilateral macular hole surgery. Graefes Arch Clin Exp Ophthalmol 2001;239:128– 132. 28. Mireskandari K, Garnham L, Sheard R, et al. A prospective study of the effect of a unilateral macular hole on sensory and motor binocular function and recovery following successful surgery. Br J Ophthalmol 2004;88:1320–1324. 29. Watanabe H, Okamoto F, Sugiura Y, et al. Stereopsis after successful surgery for rhegmatogenous retinal detachment. Graefes Arch Clin Exp Ophthalmol 2014;252:1207–1212.
1421
30. Levy NS, Glick EB. Stereoscopic perception and Snellen visual acuity. Am J Ophthalmol 1974;78:722–724. 31. Donzis PB, Rappazzo JA, Burde RM, Gordon M. Effect of binocular variations of Snellen’s visual acuity on Titmus stereoacuity. Arch Ophthalmol 1983;101:930–932. 32. Goodwin RT, Romano PE. Stereoacuity degradation by experimental and real monocular and binocular amblyopia. Invest Ophthalmol Vis Sci 1985;26:917–923. 33. Amemiya T, Takami H, Yoshida H, Harayama K. Binocular visual function after surgery for detached retina. Graefes Arch Clin Exp Ophthalmol 1982;218:304–306. 34. Tanikawa A, Horiguchi M, Kondo M, et al. Abnormal focal macular electroretinograms in eyes with idiopathic epimacular membrane. Am J Ophthalmol 1999;127:559–564. 35. Niwa T, Terasaki H, Kondo M, et al. Function and morphology of macula before and after removal of idiopathic epiretinal membrane. Invest Ophthalmol Vis Sci 2003;44:1652–1656. 36. Hibi N, Ueno S, Ito Y, et al. Relationship between retinal layer thickness and focal macular electroretinogram components after epiretinal membrane surgery. Invest Ophthalmol Vis Sci 2013;54:7207–7214. 37. Weinman J, Cooke V. Eye dominance and stereopsis. Perception 1982;11:207–210. 38. Erickson P, McGill EC. Role of visual acuity, stereoacuity, and ocular dominance in monovision patient success. Optom Vis Sci 1992;69:761–764. 39. Pierce DM. Comparability of two methods of estimating realdepth acuity. Ophthalmologica 1975;171:224–235. 40. Lovasik JV, Szymkiw M. Effects of aniseikonia, anisometropia, accommodation, retinal illuminance, and pupil size on stereopsis. Invest Ophthalmol Vis Sci 1985;26:741–750. 41. Kani W. Stereopsis and spatial perception in amblyopes and uncorrected ametropes. Br J Ophthalmol 1978;62:756–762. 42. Pesin SR, Olk RJ, Grand MG, et al. Vitrectomy for premacular fibroplasia: prognostic factors, long-term follow-up, and time course of visual improvement. Ophthalmology 1991;98:1109– 1114.
