Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Macular Choroidal Thickness Changes in Development, Progression, and Spontaneous Resolution of Epiretinal Membrane

Eun Young Choi, MD; Jongwook Han, MD; Sung Chul Lee, MD, PhD; Christopher Seungkyu Lee, MD, PhD

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the association between macular choroidal thickness and the development, progression, and resolution of epiretinal membrane (ERM).

PATIENTS AND METHODS:

The patients (n = 38) with unilateral ERM eyes with definitive changes on optical coherence tomography (OCT) and healthy fellow eyes were observed retrospectively. ERM eyes were divided into three groups: Development/new-onset group (n = 14), progression group (n = 13), and resolution group (n = 11). In each group, the average changes of macular choroidal thickness over time in ERM eyes were compared with those in the fellow eyes

RESULTS:

Choroidal thickness significantly decreased from 174.0 μm at baseline to 132.3 μm at event time (P = .001) in the development group, and from 140.0 μm ± 30.0 μm to 120.5 μm (P = .002) in the progression group. Conversely, a significant increase in choroidal thickness was observed in the resolution group (from 205.2 μm to 222.6 μm; P = .004). The fellow eyes showed no significant changes in choroidal thickness in all three groups.

CONCLUSION:

Choroidal thinning in newly developed or significantly progressed ERM eyes and choroidal thickening in spontaneously resolved ERM eyes suggest a clinical implication of choroidal changes in ERM.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:627–634.]

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the association between macular choroidal thickness and the development, progression, and resolution of epiretinal membrane (ERM).

PATIENTS AND METHODS:

The patients (n = 38) with unilateral ERM eyes with definitive changes on optical coherence tomography (OCT) and healthy fellow eyes were observed retrospectively. ERM eyes were divided into three groups: Development/new-onset group (n = 14), progression group (n = 13), and resolution group (n = 11). In each group, the average changes of macular choroidal thickness over time in ERM eyes were compared with those in the fellow eyes

RESULTS:

Choroidal thickness significantly decreased from 174.0 μm at baseline to 132.3 μm at event time (P = .001) in the development group, and from 140.0 μm ± 30.0 μm to 120.5 μm (P = .002) in the progression group. Conversely, a significant increase in choroidal thickness was observed in the resolution group (from 205.2 μm to 222.6 μm; P = .004). The fellow eyes showed no significant changes in choroidal thickness in all three groups.

CONCLUSION:

Choroidal thinning in newly developed or significantly progressed ERM eyes and choroidal thickening in spontaneously resolved ERM eyes suggest a clinical implication of choroidal changes in ERM.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:627–634.]

Introduction

Epiretinal membrane (ERM) is a vitreomacular interface disease characterized by avascular fibro-cellular proliferation on the inner retinal surface. It induces wrinkles and deformation of the retina either directly or indirectly, thereby gradually deteriorating macular function while causing visual loss.1–3 Most ERMs are idiopathic, although they may occur in association with various ocular diseases.4,5

The choroid, the posterior part of the uvea, is primarily a vascular structure supplying the outer retina.6 The quantitative measurement of choroidal thickness became possible by using enhanced depth optical coherence tomography (EDI-OCT). Using EDI-OCT, numerous studies have shown that structural changes of the choroid are significantly associated with various chorioretinal diseases including central serous chorioretinopathy,7,8 age-related macular degeneration (AMD),9–11 polypoidal choroidal vasculopathy,12–14 high myopia-related chorioretinopathly,15,16 and Vogt-Koyanagi-Harada disease.17,18 A growing interest in choroidal measurements using OCT has led to the examination of choroidal thickness in vitreoretinal interface disorders such as ERM and macular hole (MH). Currently, however, the association between choroidal thickness profile and ERM/MH remains unclear despite several relevant studies. Compared to normal control eyes, eyes with idiopathic hole and unaffected fellow eyes showed choroidal thinning.19,20 The choroidal thickness in ERM has been studied primarily in ERM patients undergoing surgery. Michalewska et al. first found that choroidal thickness in ERM patients decreased 3 months after surgery.21 The group later reported a prospective cases series where choroidal thickness in ERM decreased 6 months after surgery and remained stable until 12 months postoperatively.22 Similarly, Casini et al. reported a decrease in choroidal thickness 6 months after surgery.23 However, Ahn et al. found that choroidal thickness temporarily increased 1 week after surgery and subsequently normalized to the baseline value.24 Kang et al. found that ERM with vitreomacular traction showed increased choroidal thickness compared to ERM without traction, and that choroidal thickness decreased after surgery only in ERM with traction.25 The choroidal thickness in ERM eyes does not seem to significantly differ from that in unaffected fellow eyes, suggesting that choroidal thickness may not influence or not be influenced by the development of ERM.21,23 These results, however, are not enough to conclude whether the choroidal thickness changes are implicated in the pathophysiology of ERM development. This is mainly because no previous study has examined temporal changes of choroidal thickness in eyes along with the development of ERM. Furthermore, surgery has been a crucial bias in previous studies when investigating the effects of ERM resolution on the choroidal thickness.

In this study, we studied changes in choroidal thickness before and after de novo development or significant progression of ERM in patients using their unaffected fellow eyes as a control group. In addition, choroidal thicknesses before and after spontaneous resolution of ERM were evaluated in order to examine the effect of ERM resolution on choroidal thickness.

Patients and Methods

Study Design and Participants

We retrospectively reviewed the medical records of all patients diagnosed with ERM at the Department of Ophthalmology, Yonsei University Medical Center, Seoul, South Korea, from November 1, 2005, to March 22, 2017. This study was approved by the institutional review board at Gangnam Severance Hospital (IRB approval number: 3-2017-0132). The study has complied with the guidelines of the Declaration of Helsinki. Informed consent was not obtained from the subjects since only anonymous clinical data were used.

Examination results collected both at baseline and at event time were used for the analysis. Event time is the point when the change was observed for the first time during the follow-up period. Baseline is the time point when the ophthalmic examination (including OCT) was performed just before the event. When ERM appeared first on the next follow-up OCT, the case was included in the development (new-onset) group. Progressed ERM (progression group) included eyes that first had a cellophane-like thin membrane without visible retinal folds at baseline, which then changed to a thick fibrous membrane with at least 15% of increase in central macular thickness or the appearance of retinal folds. Resolution of ERM (resolution group) was defined as (1) the ERM disappearing spontaneously or (2) a thick, fibrous membrane becoming thinner with retinal folds or thicknesses decreasing to more than 10% of the baseline. Patients with any of the following conditions were excluded: high myopia, past or concomitant chorioretinal diseases (eg, diabetic retinopathy, AMD, central serous retinal and chorioretinopathy, retinal vascular occlusion diseases, and others), previous intravitreal injection, laser photocoagulation, and vitrectomy surgery in the study eyes with ERM. When the fellow eyes without ERM met the exclusion criteria, they were not included in paired-eye analysis. In this study, three fellow eyes were actually excluded: two fellow eyes that previously underwent vitrectomy from the progression group, and one fellow eye that showed dry AMD from the resolution group.

In addition to demographic data (eg, age, sex, and past medical history), we recorded systolic and diastolic blood pressures, and ophthalmologic basic clinical characteristics such as laterality, follow-up period, corrected distance visual acuity (CDVA), and spherical equivalent of all involved eyes. We also calculated mean arterial pressure (MAP) by adding diastolic blood pressure to one-third of pulse pressure. The CDVAs at baseline and event time were recorded with logMAR notation.

Examination and Measurement of Macular Choroidal Thickness

All eyes involved were imaged by the Heidelberg Spectralis OCT instrument (Heidelberg Engineering, Heidelberg, Germany) that uses EDI-OCT technique. The contralateral eyes were routinely scanned and used as references. During image acquisition, the OCT instrument was pushed close enough to the eye to obtain an inverted image.26 Each scan was obtained with the eye-tracking feature enabled and represented the average of 100 individual scans. The horizontal section passing through the foveal center was used for all analyses. The resultant images were viewed and measured with built-in Heidelberg Eye Explorer software (version 6.7; Heidelberg Engineering, Heidelberg, Germany). Macular choroidal thickness was defined as the distance between the outer surface of the retinal pigment epithelium line and the inner surface of the observed sclera. The choroid was measured from the outer portion of the hyperreflective line corresponding to the retinal pigment epithelium to the inner surface of the sclera. Measurements were made in the macular choroid at a total of 15 points with 500 μm intervals from the fovea to 3.5 mm nasal and 3.5 mm temporal to the center of the fovea.27 The thickness of the central macula (CMT) was measured automatically using Heidelberg software. All tests and measurements were performed by two masked observers (EYC, JH). The measurements were averaged for analysis.

Statistical Analysis

All data were presented as mean ± standard deviation. Statistical analysis was performed using SPSS version 21.0 (SPSS Inc., Chicago, IL). To compare the baseline characteristics of the three groups, a Chi square test was conducted for categorized parameters, and one-way analysis of variance was used for continuous variables. A paired t-test was conducted to compare continuous variables between ERM eyes and the fellow eyes within each group and to analyze the changes in choroidal thickness between the two time points. To examine the relationship between the changes in macular choroidal thickness in the ERM eyes and the baseline parameters, the Pearson correlation test was performed. A P value less than .05 was considered statistically significant.

Results

Thirty-eight patients in total were included in the analysis (Figure 1). There were 14 patients in the development group, 13 in the progression group, and 11 in the resolution group. None of the enrolled patients had uncontrolled hypertension or diabetes, or were taking medications (eg, sildenafil citrate, acetazolamide [Diamox Sequels; Nostrum Laboratories, Kansas City, MO]) that might affect the thickness of the choroidal layer. There were no significant differences in age, sex, MAP, eye laterality, follow-up period, CDVA, and spherical equivalent among the three groups for both the ERM eyes and the fellow eyes (Table 1). However, baseline CMT in the resolution group was significantly thicker than that in the development group (P = .01), and choroidal thickness in the resolution group was significantly thicker than that in the progression group (P = .02). CMT significantly increased by 44.4%, from 224.1 μm ± 47.0 μm to 323.5 μm ± 62.8 μm (P = .003), in the ERM eyes of the development group, and by 20.5%, from 285.2 μm ± 63.8 μm to 343.7 μm ± 66.3 μm (P = .005), in the ERM eyes of the progression group. The CMT of the ERM eyes in the resolution group significantly decreased by 16.5%, from 293.9 μm ± 56.3 μm at baseline to 245.5 µm ± 40.1 μm (P = .003).

Flowchart describing the study participants.

Figure 1.

Flowchart describing the study participants.

Clinical Characteristics of ERM Patients With Development (New-Onset), Progression, and Resolution

Table 1:

Clinical Characteristics of ERM Patients With Development (New-Onset), Progression, and Resolution

Macular choroidal thickness significantly decreased as ERM developed or progressed (Figures 2 and 3), though it increased upon ERM resolution (Figures 2 and 4). Choroidal thickness significantly decreased by 23.9%, from 174.0 μm ± 65.6 μm to 132.3 μm ± 41.9 μm (P = .001), in the ERM eyes in the development group, and by 13.9%, from 134.0 μm ± 30.0 μm to 120.5 μm ± 39.3 μm (P = .002), in the ERM eyes in the progression group. It increased, however, by 8.5%, from 205.2 µm ± 56.0 μm to 222.6 μm ± 60.4 μm (P = .004), in the ERM eyes in the resolution group. On the other hand, it did not significantly change in unaffected fellow eyes in any of the three groups.

Comparison of macular choroidal thickness between epiretinal membrane (ERM) and the fellow eyes in the development (new-onset), progression, and resolution groups. The dot and square symbols represent the average value of the groups. Standard deviations are expressed by line bars above and below the symbols. Analysis was conducted using a paired t-test to compare two time-points within a group, and P values are represented as decimal numbers on the figure. Asterisks indicate statistically significant changes, established as P values less than .05.

Figure 2.

Comparison of macular choroidal thickness between epiretinal membrane (ERM) and the fellow eyes in the development (new-onset), progression, and resolution groups. The dot and square symbols represent the average value of the groups. Standard deviations are expressed by line bars above and below the symbols. Analysis was conducted using a paired t-test to compare two time-points within a group, and P values are represented as decimal numbers on the figure. Asterisks indicate statistically significant changes, established as P values less than .05.

Changes of macular choroidal thickness in the patients with epiretinal membrane (ERM) development (new-onset) and progression by optical coherence tomography (OCT). Combination images of an en face infrared section and a horizontal enhanced depth B-scan of OCT. The average macular choroidal thickness was measured at 15 points with 500 μm intervals from the horizontal scan. (A) A 59-year-old female patient with new-onset and progression of ERM in the left eye. The macular choroidal thickness was 250.0 μm at baseline and decreased significantly to 124.6 μm after 34 months. The choroid-scleral boundary was indicated by the dotted line in the uppermost image. (B) A 65-year-old female patient with marked progression of ERM in the left eye. During the 39-month follow-up period, choroidal thickness was significantly reduced, to approximately 30.4% of the baseline. Scale bar 200 µm.

Figure 3.

Changes of macular choroidal thickness in the patients with epiretinal membrane (ERM) development (new-onset) and progression by optical coherence tomography (OCT). Combination images of an en face infrared section and a horizontal enhanced depth B-scan of OCT. The average macular choroidal thickness was measured at 15 points with 500 μm intervals from the horizontal scan. (A) A 59-year-old female patient with new-onset and progression of ERM in the left eye. The macular choroidal thickness was 250.0 μm at baseline and decreased significantly to 124.6 μm after 34 months. The choroid-scleral boundary was indicated by the dotted line in the uppermost image. (B) A 65-year-old female patient with marked progression of ERM in the left eye. During the 39-month follow-up period, choroidal thickness was significantly reduced, to approximately 30.4% of the baseline. Scale bar 200 µm.

Changes of macular choroidal thickness in the patients with epiretinal membrane (ERM) resolution by optical coherence tomography (OCT). (A) A 57-year-old male patient with spontaneous ERM regression in the left eye. During the 48-month follow-up period, choroidal thickness increased significantly to approximately 20.4% of the baseline. (B) A 57-year-old female patient with nearly complete resolution of macular pucker in the left eye. Macular choroidal thickness after 48 months (329.5 μm) was almost similar to baseline choroidal thickness (329.3 μm), thicker than that of the fellow eye (214.9 μm). Scale bar 200 μm.

Figure 4.

Changes of macular choroidal thickness in the patients with epiretinal membrane (ERM) resolution by optical coherence tomography (OCT). (A) A 57-year-old male patient with spontaneous ERM regression in the left eye. During the 48-month follow-up period, choroidal thickness increased significantly to approximately 20.4% of the baseline. (B) A 57-year-old female patient with nearly complete resolution of macular pucker in the left eye. Macular choroidal thickness after 48 months (329.5 μm) was almost similar to baseline choroidal thickness (329.3 μm), thicker than that of the fellow eye (214.9 μm). Scale bar 200 μm.

Correlation analysis using Pearson test revealed that there was no significant relationship between the changes of macular choroidal thickness and the baseline parameters (eg, age, follow-up period, CDVA, spherical equivalent, and choroidal/macular thickness) (data not shown).

Discussion

We have demonstrated here that changes in macular choroidal thickness were significantly associated with those of ERM. Specifically, ERM development and progression were associated with 23.7% and 20.7% of decrease in macular choroidal thickness respectively, whereas ERM resolution was associated with 8.9% of increase in macular choroidal thickness. Choroidal thickness is known to decrease with aging,27 but the aging was not causative in the present study as the choroidal thickness of unaffected fellow eyes did not show such changes. In contrast to our findings, the choroidal thickness in ERM eyes did not significantly differ from that in healthy fellow eyes at baseline analysis in previous studies on ERM and the choroid.21,23 One simple explanation would be the sampling bias. In fact, even in the present study, there was no difference in choroidal thickness between ERM eyes and the fellow eyes in the progression group, both before and after the event. The difference was noted in the development and resolution groups (Table 1). Another explanation could be methodological limitations of the studies, since other studies measured choroidal thickness only at the center of the fovea or at a few points apart from it. In a previous study, the choroid morphology of ERM eyes tended to be more irregular than that of normal eyes.21 We also observed the similar findings as shown in Figure A. Thus, the choroidal thickness changes, if there are any, may have not been noted properly since the actual point where the changes took place could have been overlooked. In fact, the irregular shape of the choroidal morphology in ERM eyes suggests the association between ERM and choroidal changes. We measured choroidal thickness at 15 evenly divided points semi-automatically in the macula and averaged it to obtain a representative value, which would better reflect irregular choroidal thickness and provide more accurate measurements. Another possible reason could be the presence of compensation mechanism. Even if it is true that the choroidal layer is affected by ERM development, significant changes of choroidal thickness may not be evident for a certain period of time after the development of ERM, possibly because microcirculation of the choroidal layer is compensated by other mechanisms. There has been no evidence that this type of compensatory mechanism takes place in ERM eyes over time. In the cases of progression from mild ERM progression in the present study, choroidal thickness continued to decrease.

Choroidal thickness map thickness map showing a topographical association between the presence of hyperreflective epiretinal membrane (ERM) and a decrease in choroidal thickness in the corresponding region. Combination images of an en face infrared section and a horizontal enhanced depth B-scan of spectral-domain optical coherence tomography (OCT). The macular choroidal thickness was automatically measured at each each point from the horizontal scan. A 68-year-old female patient (A) and a 72-year-old male patient (B) with ERM in their right eyes demonstrated irregular choroid/sclera boundaries. The choroidal thickness of the region, where thick hyperreflective ERM is seen on OCT image (designated by the vertical lines), appears to be relatively thinner than other regions without hyperreflective ERM. The basement membrane and choroid-scleral boundary were indicated by the upper and lower red lines in the image, respectively. Horizontal scale bar 200 µm.

Figure A.

Choroidal thickness map thickness map showing a topographical association between the presence of hyperreflective epiretinal membrane (ERM) and a decrease in choroidal thickness in the corresponding region. Combination images of an en face infrared section and a horizontal enhanced depth B-scan of spectral-domain optical coherence tomography (OCT). The macular choroidal thickness was automatically measured at each each point from the horizontal scan. A 68-year-old female patient (A) and a 72-year-old male patient (B) with ERM in their right eyes demonstrated irregular choroid/sclera boundaries. The choroidal thickness of the region, where thick hyperreflective ERM is seen on OCT image (designated by the vertical lines), appears to be relatively thinner than other regions without hyperreflective ERM. The basement membrane and choroid-scleral boundary were indicated by the upper and lower red lines in the image, respectively. Horizontal scale bar 200 µm.

A few studies have shown reduced choroidal thickness after ERM surgery,21,23 which seems to contradict our findings. Although this could be a “normalization” of thinned choroid due to ERM development and progression, the extent of choroidal thinning with ERM development and progression was greater than that of choroidal thickening with ERM resolution during a similar period of observation. The results of previous studies should be interpreted differently from ours since vitrectomy surgery is a major confounding factor. Removal of oxygen-consuming vitreous means that the posterior ocular tissues are more oxygenated.28 Contraction of choroidal blood flow in the context of increased oxygen tension29,30 may lead to a decrease in choroidal thickness. The fluctuation of intraocular pressure during and after a routine vitrectomy31,32 may be another factor affecting the thickness of the choroid, an elastic tissue.

Although it is not clear why and how choroidal thickness changes in association with ERM development, progression, and resolution, choroidal blood flow alterations may be involved in the process. Experimental studies, especially those involving chicken eyes with deprivation myopia,33,34 have shown a direct relationship between choroidal thickness and choroidal blood flow. Idiopathic MH, another vitreomacular interface disease, was found to be associated with reduced choroidal blood flow,35 which may explain the reduced choroidal thickness often found in these eyes.19,20 This relationship has also been found in other ocular diseases; choroidal blood flow and thickness were observed to decrease following intravitreal anti-vascular endothelial growth factor injection in central serous chorioretinopathy36 and branch retinal vein occlusion.37 Similarly, panretinal photocoagulation in diabetic retinopathy resulted in reduced choroidal thickness and circulation.38 We could not find a published study that had examined the relationship between choroidal blood flow and choroidal thickness in ERM. Further investigations on that would help in better understanding choroidal thickness changes in ERM.

The question remains as to whether choroidal thinning occurs secondary to ERM development or if ERM develops secondary to choroidal thinning. The former seems to be more plausible for the following reasons. First, the changes in choroidal thickness reversed after ERM resolution. The choroidal thinning could be in fact the primary change that induces secondary ERM development and progression, possibly via ischemia-associated mediators due to reduced choroidal blood flow. It is true that it is hard to imagine that the mechanical release of ERM could be induced by the thickening of the choroidal structure. However, each phase of ERM development, progression, and resolution could be governed by different mechanisms involving choroidal changes. Second, no significant change in choroidal thickness was noted until the onset of ERM development. Since most patients were not followed up on a regular basis in this study, we did not have enough data to definitively determine serial choroidal thickness changes. However, in a few cases where serial OCT images obtained prior to ERM development were available, no significant changes appeared before ERM development. Still, if choroidal thickness change did occur just prior to ERM development, this change would not have been reflected in our retrospective study. Third, the thinnest part of the irregular choroid/scleral boundary21 in some ERM eyes in this study appears to be topographically associated with the presence of ERM (Figure A), and the region where thick and hyperreflective ERM are present on OCT had a relatively thinner choroid compared to other region. Nonetheless, the finding that strengthens a correlation between ERM and choroidal thinning does not prove causality. Based on the findings of our study, it seems to be more plausible that the development and progression of ERM promote choroidal thinning, whereas the resolution of ERM induces choroidal thickening.

The weaknesses of our study include the retrospective nature of the study and the small sample size due to the scarcity of the enrollment criteria. We were not able to find enough cases that can demonstrate continuous changes of ERM, from the development to the resolution of ERM, in a single individual. A study with a more standardized and regular follow-up schedule, such as an epidemiology study using serial OCT examinations, is required to confirm our findings and to address the unanswered questions of the study. Future research involving the quantitative measurement of foveolar choroidal blood flow would be helpful in elucidating this point.

Studies on whether choroidal thickness change is associated with ERM have been inconclusive. We retrospectively evaluated the association between macular choroidal thickness and the development, progression and resolution phases of ERM, using unaffected fellow eyes as control. The significance of this study might lie in the fact that the study first demonstrated a decrease in choroidal thickness in newly developed or significantly progressed ERM eyes, whereas choroidal thickening was observed in the eyes with spontaneously resolved ERM.

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Clinical Characteristics of ERM Patients With Development (New-Onset), Progression, and Resolution

Group P Value

Development Progression Resolution

Age (Years) 62.8 ± 5.7 (56–73) 68.0 ± 5.3 (58–70) 62.5 ± 11.1 (49–76) .91*

Female/Male (N) 6/6 5/7 4/5 .93

Mean Arterial Pressure (mm Hg) 97.3 ± 8.4 105.8 ± 15.8 96.7 ± 12.3 .17*

Involved Eye, Right/Left (N) 14/8 7/5 4/5 .86

Follow-Up Period (Months) 43.6 ± 32.2 (11–84) 42.3 ± 31.7 (12–80) 43.0 ± 16.9 (13–65) .88*

CDVA (logMAR)
  ERM eye 0.08 ± 0.08 0.08 ± 0.16 0.10 ± 0.17 .87*
  Fellow eye 0.04 ± 0.10 0.03 ± 0.10 0.02 ± 0.03 .85*
   P value .70 .69 .50

Spherical Equivalent (Diopters)
  ERM eye −0.70 ± 1.17 −0.34 ± 1.15 −0.54 ± 0.94 .64*
  Fellow eye 0.07 ± 1.07 −0.64 ± 0.75 −0.37 ± 0.44 .73*
   P value .50 .67 .69

Central Macular Thickness (μm)
  ERM eye, baseline 224.1 ± 47.0 285.2 ± 63.8 293.9 ± 56.3 .03*
  Fellow eye, baseline 239.2 ± 54.0 225.1 ± 62.5 216.6 ± 36.9 .64*
   P value .88 .17 .001
  ERM eye, event time 323.5 ± 62.8 343.7 ± 66.3 245.5 ± 40.1 .01*
  Fellow eye, event time 235.8 ± 51.8 232.3 ± 63.4 213.6 ± 23.3 .53*
   P value .02 .01 .03

Macular Choroidal Thickness (μm)
  ERM eye, baseline 174.0 ± 65.6 134.0 ± 30.0 205.2 ± 60.0 .03*
  Fellow eye, baseline 179.5 ± 59.7 134.4 ± 45.5 223.9 ± 65.7 .004*
   P value .56 .62 .03
  ERM eye, event time 132.3 ± 41.9 120.5 ± 39.3 222.6 ± 60.4 <.0001*
  Fellow eye, event time 175.5 ± 49.7 135.2 ± 57.9 224.0 ± 59.0 .003*
   P value .03 .13 .87
Authors

From the Department of Ophthalmology, The Institute of Vision Research, Gangnam Severance Hospital, Yonsei University College of Medicine, Eonjuro, Gangnam-gu, Seoul, Korea (EYC, JH, CSL); and the Department of Ophthalmology, The Institute of Vision Research, Severance Hospital, Yonsei University College of Medicine, Yonseiro, Seodaemun-gu, Seoul, Korea (SCL, CSL).

Paper presented at the 2017 Korean Retina Society Annual Meeting.

Supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF-2016R1D1A1A02937349). The funding organization had no role in the design or conduct of this research.

The authors report no relevant financial disclosures.

Address correspondence to Christopher Seungkyu Lee, MD, PhD, Department of Ophthalmology, Gangnam Severance Hospital, Yonsei University College of Medicine, 211, Eonjuro, Gangnam-gu, Seoul, Korea; email: sklee219@yuhs.ac.

Received: September 12, 2018
Accepted: March 11, 2019

10.3928/23258160-20191009-05

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