Epiretinal Membrane Peeling in Eyes with Pseudophakia: Prognostic and Morphological Factors of Visual Outcomes

doi:10.21203/rs.3.rs-3718333/v1

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Epiretinal Membrane Peeling in Eyes with Pseudophakia: Prognostic and Morphological Factors of Visual Outcomes

https://doi.org/10.21203/rs.3.rs-3718333/v1

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Background

Epiretinal membrane (ERM) is a sight-threatening disorder, and diagnosis can be delayed. In this study, spectral domain optical coherence tomography (SD-OCT) was used to investigate the predictive factors of visual outcomes in patients with pseudophakic ERM following surgery.

Methods

The records of 61 patients with pseudophakic eyes (61 eyes) with ERM who underwent PPV, ERM peeling, and ILM peeling were retrospectively reviewed. OCT features such as central foveal thickness (CFT), cotton ball sign, ERM foveoschisis, ellipsoid zone (EZ) disruption, external limiting membrane (ELM) disruption, ectopic inner foveal layer (EFIL), disorganization of the retinal inner layers (DRIL), dissociated optic nerve fiber layer (DONFL), and microcystic macular edema (MME), as well as surgical factors, were compared before and after surgery. The correlations between the OCT and surgical factors and change of best-corrected visual acuity (BCVA) before and after the surgery were examined.

Results

The mean follow-up time was 6 months. The BCVA (P < 0.01) and CFT (P < 0.01) showed significant improvements after ERM removal (P < 0.01). Cotton ball sign and DRIL exhibited statistically significant improvement after ERM removal. ERM-foveoschisis (P = 0.015) and MME (P = 0.009) were significantly correlated with less improvement of visual acuity. Better visual acuity before surgery was significantly associated with better improvement of visual acuity (P < 0.001).

Conclusions

Better baseline visual acuity is correlated with better visual acuity improvement after surgery, while ERM foveoschisis and MME identified preoperatively on OCT are associated with relatively less improvement of visual acuity.

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Epiretinal membrane (ERM), also referred to as macular pucker, is a sight-threatening disorder. The formation of an ERM is related to abnormality of the vitreoretinal interface combined with posterior vitreous detachment, causing a pathological fibrocellular layer that proliferates over the internal limiting membrane. Patients may present with decreased or distorted central vision, metamorphopsia, or may be asymptomatic. An idiopathic epiretinal membrane (iERM) accounts for most cases of ERM, while ocular trauma, uveitis, or retinal detachment can result in secondary ERM. Symptomatic ERM is typically treated with pars plana vitrectomy (PPV), ERM peeling, followed by internal limiting membrane (ILM) peeling ¹. Spectral domain optical coherence tomography (SD-OCT) has become the standard method for diagnosing ERM. The method identifies microstructural abnormalities of the retinal layers to determine ERM severity before and after surgery. Recent studies have suggested that anatomical changes identified on SD-OCT may predict postoperative visual acuity.

A review of published studies found that few studies have listed cataracts as an exclusion criteria; however, we believe it is necessary to exclude patients with cataracts to avoid interference with the analysis of outcomes. In addition to confounding baseline visual acuity, the gradually progression of cataracts may affect the efficacy of ERM surgery, and the prediction of postoperative visual acuity using SD-OCT findings. Some surgeons may successively conduct ERM peeling and phacoemulsification-vitrectomy; however, when this is done it makes it difficult to determine if improvement of vision is a result of ERM removal or the pseudophakia state ².

A recent study by Kim et al. examined the correlations between individual OCT parameters and visual outcomes in pseudophakia ERM patients³. However, separate analysis of each OCT parameter without controlling for other factors and patient characteristics may not provide conclusive evidence as to which parameters are related to improved visual acuity.

Thus, the purpose of this study was to identify which OCT parameters may be independent predictors of visual outcomes in pseudophakia patients with ERM who undergo surgery. Our review of the literature indicated that no prior study has combined all OCT parameters into a multivariate regression model focused on pseudophakia patients with ERM. We selected nine outer and inner retinal parameters that have been discussed in prior studies and can easily be evaluated by SD-OCT. The use of these parameters allows a simplified and efficient approach for each clinical evaluation.

Study design and patients

The records of patients who underwent successful surgery for iERM between July 2017 and July 2022 at Kaohsiung Veterans General Hospital, Taiwan, were retrospectively reviewed. ERM diagnosis and surgical procedures were performed by 2 retina surgeons. This study was approved by the hospital Review Board and Ethics Committee. Because of the retrospective nature of the study, the requirement of informed consent was waived.

Inclusion criteria for the study were: 1) Diagnosis of ERM; 2) Diagnosis of pseudophakia before ERM surgery; 3) Treated with PPV, ERM peeling, and ILM peeling; 4) Attended follow-up visits for at least 3 months after surgery. Exclusion criteria were: 1) Eyes with high myopia defined by an axial length ≥ 26 mm; 2) Lamellar or full-thickness macular hole on preoperative SD-OCT examination; 3) History of prior surgery, intravitreal or subretinal injection, or laser treatment; 4) Laser treatment during ERM surgery; 5) History of, or concomitant ophthalmological disease that affects visual acuity or causes maculopathy, including glaucoma, uveitis, optic neuropathy, ocular trauma, diabetic retinopathy, choroidal neovascularization, retinal vein occlusion, and retinal tear or detachment.

Surgical intervention

All surgeries were performed by 2 surgeons at Kaohsiung Veterans General Hospital, Taiwan. First, a 3-port 23- or 25-gauge microincision vitrectomy surgery was performed. After the vitrectomy procedure, posterior vitreous detachment (PVD) was performed in patients without PVD. ERM peeling was then performed with intraocular forceps. Following removal of the ERM, indocyanine green (0.25% diluted in a 1-to-1 ratio with 20% glucose water) was applied to identify ILM, and to then perform ILM peeling. Peeling of the ERM and the ILM was performed eccentrically starting 1.5-to-2-disc diameters from the fovea, and the membranes were gradually removed in layers. Air-fluid exchange was conducted based on surgeon’s discretion.

Statistical analysis

Descriptive statistics were summarized as mean ± standard deviation, and interquartile range (IQR). The best-corrected visual acuity BCVA was converted into the logarithm of the minimum angle of resolution (logMAR). The mean values of continuous variables were compared using the paired t-test. The McNamar test was used to compare categorical variables. Multivariate linear regression analysis was performed to identify the OCT parameters that were most associated with visual acuity. Values of P < 0.05 were regarded as statistically significant. Statistical analyses were performed using SPSS version 26.0 software (SPSS Inc., Chicago, IL, USA) and R Project for Statistical Computing version 4.3.1 for Mac.

Clinical assessment and SD-OCT imaging

Every patient underwent a thorough standard ophthalmologic examination that included measurement of intraocular pressure, slit-lamp biomicroscopy, color fundus photography, and SD-OCT (Optovue, Inc., Fremont, CA) before and after surgery. The SD-OCT scans were evaluated by a single investigator who unaware of the patient history.

Central foveal thickness (CFT) was determined by measuring the mean thickness of the retina within a circular region of 1 mm diameter around the fovea. The cotton ball sign refers to an encircled hyper-reflective lesion localized on the outer retinal layers within the fovea, and indicates traction on photoreceptors ⁴(Supplementary Fig. 1). Microcystic macular edema (MME), also known as inner nuclear layer microcysts (INLC), is defined as small hyporeflective lesions with no clear cyst wall, located in the inner nuclear layer, within or outside the perimacular rim⁵ (Supplementary Fig. 2).

An ectopic inner foveal layer (EIFL), as described by Govetto et al. ⁶, involves a continuous hyporeflective or hyperreflective band extending from the inner nuclear layer (INL) and inner plexiform layer (IPL) across the foveal region, and is visible on all OCT scans centered on the fovea ⁶. When the horizontal extent in microns for which any boundaries between the ganglion cell–inner plexiform layer complex (GCIPL), inner nuclear layer (INL), and outer plexiform layer (OPL) could not be identified, it was defined as disorganization of retinal inner layers (DRIL)⁷ .

In addition, SD-OCT scans were evaluated for external limiting membrane (ELM) disruption and ellipsoid zone (EZ) disruption, based on the presence of a continuous hyperreflective line appearing in the macular. A newly proposed consensus definition for ERM foveoschisis based on OCT (Supplementary Fig. 3) includes two mandatory criteria: a contractile ERM and foveoschisis at the level of Henle’s fiber layer. Optional criteria are the presence of microcystoid spaces in the inner nuclear layer, retinal thickening, and retinal wrinkling⁸. Few studies have included ERM foveoschisis as part of their evaluation; however, we believe it is an important characteristic to evaluate and thus included it in our study.

Additionally, a distinct post-operative appearance of dark arcuate striae along the course of the optic nerve fibers, resulting from small dimples in the regions of the retina where the ILM has been removed, was defined as a dissociated optic nerve fiber layer (DONFL) ⁹.The aforementioned characteristics were reviewed on the pre- and post-operative OCT images of all patients.

A total of 61 patients with ERM (61 pseudophakia eyes) including 29 males and 32 females with a mean age of 71 ± 3.5 years (IQR: 55-81years) were included in the study. Characteristics of the patients are summarized in Table 1. Baseline logMAR BCVA was 0.52 ± 0.2 and the mean CFT was 439 ± 57.5µm. After the surgery, the BCVA of 42 eyes improved, the BCVA of 9 eyes worsened, and the BCVA of 10 eyes remained the same.

Table 1

Demographic and Clinical Data of Epiretinal Membrane Patients with Pseudophakia
Characteristics	Summary statistics (total, median with IQR, or %)
Number of eyes (n, %) Right eyes Left eyes	n = 61 31 (50.8) 30 (59.2)
Age (years, mean ± SD [range])	71 ± 3.5 [55–91]
Gender Male Female	29(47.5) 32(52.5)
23/25 gauge PPV (n, %)
23 gauge	16 (26.2)
25 gauge	45 (73.8)
PVD history (n, %)	52(85)
DM without retinopathy (n, %)	8(13)
Gas or air tamponade (n, %)	12(20)
Duration of symptoms (months, mean ± SD [range])	6.31 ± 2.07 [4–23]
Mean follow up time (months, mean ± SD [range])	5.96 ± 3.91 [3–19]
Baseline CFT (µm, mean ± SD [range])	439 ± 57.5 [243–609]
Baseline BCVA (log MAR, mean ± SD [range])	0.49 ± 0.27 [0.05-1]
Abbreviation: SD, standard deviation; BCVA, best corrected visual acuity; DM, diabetes mellitus; PVD, posterior vitreous detachment; CFT, central foveal thickness; BCVA, best corrected visual acuity

BCVA and SD-OCT changes after ERM surgery are shown in Table 2. The CFT was significantly improved from 439 ± 57.5 µm to 358 ± 28.5 µm (P < 0.001), and the BCVA was improved from 0.52 ± 0.2 to 0.125 ± 0.22 (P < 0.001). OCT findings of cotton ball sign and DRIL were significantly decreased after surgery (both, P < 0.05).

Table 2

Summary of OCT characteristics before and after epiretinal membrane (ERM) peeling
Characteristics	Summary statistics		p value
	Pre-operative	Post-operative
Cotton-ball sign (n, %)	13(21%)	3(5%)	0.002*
DRIL (n, %)	31(51%)	3(5%)	< 0.001*
EIFL (n, %)	30(49%)	31(51%)	1
ELM disruption (n, %)	11(18%)	5(8%)	0.109
EZ disruption (n, %)	6(10%)	3(5%)	0.25
ERM foveoschisis (n, %)	6(10%)	0(0%)	0.063
MME (n, %)	9(15%)	11(18%)	0.815
Mean CFT (µm)	439	358	< 0.01*
Mean BCVA (logMAR)	0.52	0.125	< 0.01*
*Statistically significant value (p value < 0.05) Abbreviation: DRIL, disorganization of retinal inner layers; EFIL, ectopic inner foveal layer; ELM, external limiting membrane; EZ, ellipsoid zone; ERM, epiretinal membrane; MME, microcystic macular edema; CFT, central foveal thickness; BCVA, best corrected visual acuity

The results of the multivariate analyses are shown in Table 3, and the predictive values of the OCT parameters for improvement of BCVA are shown in Fig. 1. Controlling for other variables, eyes with ERM-foveoschisis and eyes with MME before the surgery showed an improvement in BCVA after surgery, but this improvement was relatively less compared to eyes without these conditions (regression estimate = -0.181 logMAR, 95% confidence interval [CI]: -0.38 – -0.04, P = 0.015; regression estimate = -0.183 logMAR, 95% CI: -0.48–0.17, P = 0.009, respectively). On the other hand, patients who had better baseline visual acuity tended to have more improvement in visual outcomes (regression estimate = 0.835 logMAR, 95% CI: 0.93–1.25, P < 0.001).

Table 3

Results of multivariable analysis of factors associated with the longitudinal change in best-corrected visual acuity (BCVA) after epiretinal membrane (ERM) removal in affected eyes.
Variables	BCVA change
	Regression coefficient	P value
	(95% CI)
Patient characteristics
Age	-0.105 (-0.01 to 0.001)	0.106
ERM eye	0.087 (-0.03 to 0.15)	0.185
Gender	-0.043 (-0.13 to 0.07)	0.556
High myopia	-0.027 (-0.35 to 0.26)	0.777
Metamorphopsia	0.02 (-0.1 to -0.13)	0.797
Diabetes	0.001 (-0.12 to 0.12)	0.987
Followed-up time	0.006 (-0.01 to 0.01)	0.922
Duration if symptoms	0.032 (-0.18 to 0.04)	0.683
Visual acuity at baseline	0.835 (0.93 to 1.25)	< 0.01*
Surgery characteristics
PVD history	-0.053 (-0.19 to 0.09)	0.451
Air fluid exchange	-0.12 ( -0.26 to 0.05)	0.165
OCT characteristics before ERM removal
ERM-Foveoschisis	-0.181 (-0.38 to -0.04)	0.015*
MME	-0.183 (-0.48 to 0.17)	0.009*
DRIL	-0.029 (-0.11 to 0.12)	0.767
EIFL	-0.08 (-0.12 to 0.12)	0.336
CFT	0.058 (-0.001 to 0.001)	0.567
Cotton ball sign	0.024 (-0.09 to 0.13)	0.722
EZ disruption	0.014 (-0.22 to 0.25)	0.89
ELM disruption	-0.006 (-0.23 to 0.35)	0.949
OCT characteristics after ERM removal
ERM-Foveoschisis	0.132 (-0.05 to 0.77)	0.081
MME	-0.085 (-0.45 to 0.17)	0.377
DRIL	0.105 (-0.11 to 0.45)	0.223
EIFL	< 0.001 (-0.12 to 0.12)	0.998
CFT	-0.057 (-0.002 to 0.001)	0.578
Cotton ball sign	0.095 (-0.09 to 0.40)	0.221
EZ disruption	-0.092 (-0.71 to 0.42)	0.6
ELM disruption	0.047 (-0.17 to 0.06)	0.679
DONFL	0.009 (-0.25 to 0.28)	0.889
*Statistically significant value (p value < 0.05)
Abbreviation: PVD, posterior vitreous detachment; ILM, inner limiting membrane;
DRIL, disorganization of the retinal inner layers; DRIL, disorganization of retinal inner
layers; DONFL, dissociated optic nerve fiber layer; CFT, central foveal thickness;
EFIL, ectopic inner foveal layer; ELM, external limiting membrane; EZ, ellipsoid zone;
ERM, epiretinal membrane; MME, microcystic macular edema

Epiretinal membrane surgery is widely regarded as one of the most frequently conducted procedures by retinal surgeons; however, a prevailing challenge for surgeons is identifying the right time for surgical intervention. Even with successful ERM removal, the visual outcome is not always satisfactory. Currently, SD-OCT is the gold standard for evaluating macular pathology and considerable research has been dedicated to the prediction of surgical and anatomical outcomes following ERM surgery based on SD-OCT findings.

Attention was initially focused on outer retinal findings in ERM due to deterioration of the outer retinal layers, and it was suggested that persistent impairment of photoreceptors thereby was correlated with an unfavorable visual prognosis¹⁰. However, since traction on the inner retinal layer has been shown to be associated with electrophysiological dysfunction and structural changes in patients with ERM, more attention has been given to inner retinal findings¹¹. Due to a lack of consensus, outer and inner retina layer SD-OCT findings are currently used for evaluation before ERM surgery and to predict outcomes¹².

Our findings showed a significant improvement in CFT and BCVA following ERM removal. The result is likely because early membrane removal prevents further progression of photoreceptor damage in patients with ERM¹³. Other studies have examined the relation between the CFT and visual outcomes in patients with ERM; however, results are inconsistent. Some studies have shown a correlation between a postoperative decrease in CFT and an increase in BCVA ^13,14. On the other hand, 2 multivariate analyses conducted by Hosoda et al.¹⁵ and Kim et al.¹⁶ found that CFT was not a reliable predictor for visual outcome after ERM surgery. In our multivariate linear regression model, no significant association between the degree of BCVA improvement and the degree of CFT resolution was found. The varying results may indicate that CFT is just one of several variables affecting visual acuity, and the relations are not fully understood¹⁵.

Our results showed that DRIL was significantly reduced after surgery, and similar results were reported in prior studies^17,18. Prior research has indicated that severe DRIL at baseline, defined as GCIPL, INL, and OPL all being indistinguishable, is correlated with limited improvement in visual acuity after surgery^12,18. Though some study has shown that severe DRIL is related to poor visual outcomes after surgery¹⁹, the study by Karasavvidou et al.¹² in which a linear regression model was developed did not find a correlation between mild DRIL and BCVA outcome after surgery; a finding that is consistent with our results. The reason may be that our patients had a lower baseline severity of DRIL.

Our results showed a significant decrease in the cotton ball sign after ERM removal. The cotton-ball sign is a round or diffuse highly reflective region at the center of the fovea caused by continuous inward traction from the ERM²⁰. Our findings are consistent with those of Tsunoda et al.²⁰, which showed the release of inward traction on the retinal layer after ERM removal. González-Saldivar et al.⁴ considered the cotton ball sign to be a prognostic factor of poor visual acuity after ERM surgery; however, their analysis did not a statistically significant association between the cotton ball sign and postoperative visual acuity. Our multivariable analysis did not find a significant relation between the cotton ball sign and an improvement in BCVA after ERM surgery. These results suggest that the disappearance of the cotton ball sign does not correlate with an improvement in BCVA after ERM surgery. Notably, a retrospective study showed that the cotton ball sign can be observed in patients with good vision²⁰. A possible speculation is that traction forces from the ERM to the outer retinal layers are present in the early stages of ERM development; however, these changes are transient and are reversible after ERM removal. Tsunoda et al. ²⁰ pointed out that the disappearance of the cotton ball sign after ERM surgery does not necessarily indicate an increase or decrease in visual acuity after surgery. The authors concluded that the cotton ball sign may only be used as a predictor of visual impairment if there is longstanding inward traction at the fovea causing irreversible retinal damage ²⁰. Notably, our results showed that ERM foveoschisis and MME identified on OCT preoperatively were significantly associated with postoperative visual improvement.

As reported in prior publications, our results showed that better baseline visual acuity was predictive of a better improvement in postoperative BCVA^11,21. The possible reason is that most of our patients ERM was present for a relatively short period of time, causing less functional disturbance.

Recently, a new OCT-based definition of idiopathic epiretinal membrane foveoschisis (ERM-foveoschisis) was proposed by an international panel of vitreoretinal experts⁸. In our study, although not statistically significant, ERM-foveoschisis was shown to be resolved postoperatively (P = 0.063) (Supplementary Fig. 2), which is consistent with the results of previous studies^22,23. In addition, our results were similar to those of other studies in those patients with ERM-foveoschisis had had an improvement in vision after surgery^22,23. A possible reason is that the release of traction allows the axons of Müller cells to return to their original morphology²⁴, which restores their function in the visual transmission pathway. However, a persistence of intraretinal hyporeflective spaces in the foveal region was noted by Figueroa et al.²⁴ in the early postoperative period, although they gradually subsided during follow-up period. The delayed healing progress observed in patients with ERM-foveoschisis might indicate chronic inflammation and damage. This could explain our findings, which revealed that patients with preoperative ERM-foveoschisis showed comparatively less visual improvement after surgery than those without it.

Another OCT finding, MME which was first described in multiple sclerosis and neuromyelitis optica, has recently been studied as a predictor of postoperative visual acuity after ERM surgery^25,26. Lee et al.²⁵noted less improvement in BCVA after ERM surgery in patients with preoperative MME during a follow-up of 3 months²⁵. Yang et al.²⁶ observed similar results in a study with a follow-up period of 24 months. Our results showed that the postoperative improvement of BCVA was less in patients with preoperative MME than in those without it. Müller cell damage and retrograde trans-synaptic degeneration to bipolar cells are the two most prevalent hypotheses for this finding, and it is speculated that breakdown of the integrity of the blood–retinal barrier and dysfunction of bipolar cells affect intraretinal fluid hemostasis and visual pathway transmission^25,26,27. These findings suggest that MME might be associated with chronic inflammation, leading to challenges in achieving greater visual improvement after surgery.

The limitations of our study include its retrospective nature, the relatively small sample size, and the relatively short follow-up period. In addition, we did not account for the severity of DRIL and EIFL because there is a lack of qualitative grading of these parameters. However, there are a number of strengths of our study. First, eyes included in the study were pseudophakia, which eliminated interference of the functional assessment due to postoperative lenticular changes. Additionally, ERM-foveoschisis and MME are relatively newly defined OCT parameters. To the best of our knowledge, this is the first multivariable analysis that suggests these two parameters are indicators of limited visual outcomes in patients with ERM and pseudophakia.

In conclusions, in this study we determined prognostic factors for visual outcomes of ERM surgery by eliminating confounding factors such as BCVA improvement following combined cataract surgery or BCVA deterioration due to cataract progression. ERM- foveoschisis and MME identified preoperatively are correlated with visual improvement after surgery, but the degree of improvement is less compared to patients without these conditions. Better baseline visual acuity is correlated with better visual improvement after surgery. The precise nature of how ERM-foveoschisis and MME result in less improvement of BCVA improvement remains to be determined.

Conflict of interest

All authors certify that they have no conflict of interest.

Funding

No funding was received for conducting this study.

Acknowledgement

We would like to acknowledge and express our thanks to all staff of the Department of Ophthalmology at Kaohsiung Veterans General Hospital, who have devoted themselves to conducting, recording examinations, and caring for patients with all their hearts.

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Epiretinal Membrane Peeling in Eyes with Pseudophakia: Prognostic and Morphological Factors of Visual Outcomes

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Clinical assessment and SD-OCT imaging

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