Anatomical and Functional Outcome of Epiretinal Membrane Peeling Surgery

Background: The purpose of this study is to study the anatomical and functional outcome of epiretinal membrane peeling surgery by evaluating the visual outcomes, comparing the pre and post operative macular thickness and functional changes through electroretinogram. Methods: It is a non-randomized, open labelled, prospective study conducted in a tertiary eye care centre. The anatomical and functional outcome of epiretinal membrane peeling surgery was evaluated by comparing the preoperative BCVA, OCT and ERG with post operative results of the same, at 4 & 12 weeks after the surgery in 25 eyes. Results: There was a signicant reduction in CFT (p ≤ 0.05) with marked improvement in vision on follow ups at 4 weeks and 12 weeks after removal of ERM with signicant reduction in the macular edema. On post operative ERG, 18 (72%) patients showed global improvement in amplitudes and P1 implicit time as compared to their preoperative value while 2 (8%) patients showed global improvement in amplitude but there was still delay in P1 implicit time as similar to their preoperative value and 4 patients (16%) showed no improvement in global amplitude as well as in P1 implicit time. Conclusions: ERM peeling surgery in selected cases improves visual acuity signicantly in majority of the patients. CFT and foveal architecture signicantly improves with ERM peeling surgery which also explains the improvement in functional visual acuity. ERG interpretation goes along the improvement in best corrected visual acuity signifying improvement in functioning of macula. patients in 2 groups depending on the anatomical distortion seen on SD-OCT. Among the two groups they observed preoperative reduction in N1 and P1 amplitudes which after surgical removal of epiretinal membrane showed improvement in amplitudes of ERGs signicantly correlated with improvent in BCVA post surgery. (20) Our study also shows improvement in amplitudes in mfERG consistent with improvement in BCVA with restoration of near normal anatomical conguration of macula.


Introduction
An epiretinal membrane (ERM) is a thin sheet of brous tissue that can develop on the surface of the macular area of the retina and cause disturbance in vision. An epiretinal membrane can also be called macular pucker, premacular brosis, surface wrinkling retinopathy or cellophane maculopathy. Most commonly, macular epiretinal membrane are asymptomatic or causes mild symptoms of metamorphopsia and/or modest decrease in central visual acuity. A minority of these membranes can cause macular distortion or macular edema to induce clinicians to recommend ERM removal via pars plana vitrectomy.
Optical coherence tomography (OCT) has become the most useful, noninvasive ancillary test for the evaluation of epiretinal membranes. OCT may be predictive of visual outcomes with ERM surgery. The hyperre ective line above retinal pigment epithelium (RPE) demonstrates the inner segment/outer segment (IS/OS) junction of photoreceptors. Several studies have demonstrated that an intact continuous IS/OS junction is predictive of better visual outcome at 12 months. (1,2) OCT also helps in distinguishing macular pseudo holes from full thickness macular hole which is an exclusion criterion for this study. (1) The detection of elevated ERM via enface OCT could assist safer grasping of the ERM and indicate the potential for visual outcome improvement after PPV and ERM peeling. (3) The multifocal electroretinogram (mfERG) represents a cone generated response of localized retinal function in the central macula, which is useful in establishing the presence of macular dysfunction. (4) Multifocal electroretinography (mfERG), is a noninvasive, objective method to detect regional functional changes in the central retina by measuring electrophysiologic responses, has demonstrated macular function changes in eyes with ERM by several reports. (5,6) The biphasic rst order response of the mfERG includes an initial negative de ection [N1] followed by a positive peak [P1]. Previous studies have found that abnormalities in the P1 latency disorders might re ect dysfunctions of the inner retinal layers and Müller cells. (7) The mfERG values might be associated with numerous factors. In another study it was demonstrated that there was a signi cant correlation between P1 implicit time and CMT. MfERG abnormalities appear to demonstrate subtle macular function changes and correlate with visual acuity and central macular thickness in eyes with ERM. In rst-order mfERG responses, P1 wave changes may be a sensitive functional measurement for ERM patients.
The goal of membrane peeling is to reduce or eliminate the most common mechanisms of visual loss, including macular distortion, traction macular detachment, foveal ectopia, tissue that covers the fovea, retinal vascular leakage with macular edema, and traction induced obstruction of axoplasmic ow. In general, most patients considered for vitrectomy have signi cant visual impairment.
ERMs are found most frequently over the age of 50 and several large clinical studies have noted a clinical prevalence lying between 7% and 11.8%. (8,9) Most of these are asymptomatic, with many being extra foveal in location. There appears to be no signi cant gender predilection and 20 to 30 % are bilateral.
Other eye involvement was reported in the Blue Mountains Eye Study to occur in 13.5% of patients over a 5 years time period. (10) The majority of ERMs are globally adherent to the retinal surface, however, some appear to have focal adhesions. (11) These focal adhesions are more common in eyes with secondary ERMs.
The incidence of symptomatic ERM formation is 4-8% after repair of rhegmatogenous retinal detachment, (12,13) and 1-2 % after prophylactic treatment of peripheral retinal breaks. (14) The electroretinography (ERG) is a diagnostic test that measures the electrical activity generated by neural and non-neuronal cells in the retina in response to a light stimulus. The electrical response is a result of a retinal potential generated by light-induced changes in the ux of transretinal ions, primarily sodium and potassium. Most often, ERGs are obtained using electrodes embedded in a corneal contact lens, which measure a summation of retinal electrical activity at the corneal surface. The International Society for Clinical Electrophysiology of Vision (ISCEV) introduced minimum standards for the ERG in 1989. The ERG can provide important diagnostic information on a variety of retinal disorders. Moreover, an ERG can also be used to monitor disease progression.

Materials And Methods
This is a non randomized, open labelled, prospective study conducted in a tertiary eye care centre. In this study 25 eyes are included as per the inclusion and exclusion criteria mentioned below.
In this study a detailed history and clinical examination were performed with necessary investigations as and when required. Pre-operatively patients were evaluated for Best Corrected Visual Acuity (BCVA), metamorphopsia, fundus examination with indirect ophthalmoscopy and slit lamp biomicroscopy, fundus photographs were taken of all patients. Optical Coherence Tomography (OCT) was performed preoperatively to assess the macular anatomy and to measure Central Foveal Thickness (CFT). Multifocal Electroretinogram (mfERG) was performed in all patients for preoperative evaluation of electrophysioloigc response of central retina. Patients in this study then underwent pars plana vitrectomy with epiretinal membrane peeling. BCVA was assessed at post-operative day 1 and post operative 1 week, 4 weeks and 12 weeks with focus also on improvement in the quality of the vision and reduction in metamorphopsia. OCT was performed at 4weeks and 12 weeks to evaluate the change in macular anatomy and central foveal thickness after epiretinal membrane peeling surgery. ERG was performed in all patients 12 weeks after surgery to evaluate the electrophysiologic response of central retina post surgery. Thus in this study anatomical and functional outcome of epiretinal membrane peeling surgery was evaluated by comparing the preoperative BCVA, OCT and ERG with post operative results of the same, 12 weeks after the surgery.
The Ethical approval for the study was taken from the local Institutional Ethical Committee.
None of the authors have any nancial/con icting interests to disclose.

Inclusion criteria:
Patients between the ages of 20 to 80 years. Intraocular pressure < 21mmHg. Normal pupillary shape, size and reaction.
Preoperative OCT presence of ERM on macular area covering central fovea with or without macular edema.
Clearance of media for preoperative mfERG and OCT.
Poor xation for OCT examination.
Patients with pre-existing macular hole, optic atrophy, vitreomacular traction, choroidal neovascular membrane, macular ischemia from previous retinal vascular occlusion or any other pre existing macular disorder.
Patients with rubeosis iridis or glaucoma.
Only eyed patient.

AGE
Of 25 patients, 1 patient was of 40 years of age, 2 were in 40-50 age group, 7 in 50-60 age group, 14 were in 60-70 age group, and 1 was above 70years of age.

RELATION BETWEEN CFT AND BCVA IN LOG MAR
The below scatter graph shows association between central foveal thickness pre-operative and after removal of ERM at 4 weeks and 12 weeks follow-up. It shows signi cant relation between BCVA and CFT and also shows marked improvement in vision with reduction in CFT after removal of ERM as the traction at the fovea is released as well as signi cant reduction in the macular edema.

Discussion
In the study conducted by James G Wong MMed, Nitin Sachdev PhD, Paul E Beaumont FRANZCO, Andrew A Chang FRANZCO of "Visual outcomes following vitrectomy and peeling of epiretinal membrane" in 125 eyes of 123 patients with visually signi cant macular epiretinal membranes showed Visual acuity improved by a mean of 0.31 Â± 0.21 logMAR (three lines of vision). (15) Whereas our study which showed improvement by mean of 0.72 (± 0.45) logMAR. As mentioned in the study, we observed that epiretinal membrane peeling improves vision in the majority of patients with signi cant symptoms, even if preoperative visual acuity is not substantially reduced. Surgery improves functional vision including metamorphopsia not measurable by visual acuity, and thus assessment of functional vision should be included in surgical case planning.
In a similar study conducted by Ionas Miliatos1 and Gun Lindgren2 of Epiretinal membrane surgery evaluated by subjective outcome in 239 eyes of 231 patients with idiopathic ERM showed that the preoperative visual acuity was mean 0.58 logMAR which improved to post operative visual acuity of mean 0.36 logMAR which was very signi cant with p value < 0.05. (16) Where as our study showed improvement in visual acuity from mean 1.04 logMAR pre-operratively to visual acuity of mean 0.72 logMAR which is also signi cant with p value of 0.001.
In a study conducted by Parisi V, Coppe AM, Gallinaro G, Strip M of "Assessment of macular function by focal electroretinogram and pattern electroretinogram before and after epimacular membrane surgery assessment of macular volume" were evaluated for 22 eyes of 22 patients (mean age +/-SD, 63.20 +/-10.0 years) with ERM preoperatively (baseline) and 6 months after surgical peeling. Preoperative visual acuity and fERG and pERG amplitudes observed in ERM eyes were compared with those in 15 agematched control eyes. It was observed that, at the postoperative evaluation, ERM eyes had a correlated signi cant (P < 0.01) increase in visual acuity, fERG amplitude, and pERG amplitude with respect to the preoperative values. All ERM eyes had a signi cant (P < 0.01) reduction in macular volume, and retinal microanatomy was restored to normal conditions. Hence the decrease in visual acuity is related to dysfunction of both preganglionic (abnormal fERG) and ganglionic (abnormal pERG) macular elements.
Surgical removal of ERM may induce improvement of the function of both outer and innermost macular retinal layers, leading to a related increase in visual acuity. (17) In our study we performed preoperative and post operative multifocal ERGs in 25 eyes of 25 patients which showed improvement in global and P wave amplitudes as well improvement in delay in P1 implicit time post ERM peeling surgery correlated with improvement in visual acuity.
In a study conducted by Liu Z, Ye J, Chen Y, Dong F of "Clinical study of vitrectomy with epiretinal membrane peeling for idiopathic macular membrane" Clinical data of 51 patients (51 eyes) who underwent vitrectomy with ERM peeling were retrospectively investigated. All the patients were examined by visual acuity, slit lamp, fundus under mydriasis, optical coherence tomography (OCT) before and after the surgery. The 3-18 months follow-up were included. There was a negative correlation between visual acuity and mean foveomacular thickness (r=-0.452, P = 0.001), and it was obvious postoperatively (r=-0.602, P = 0.000). The increase of visual acuity was strongly correlated with the decline of mean foveomacular thickness (r = 0.382, P = 0.006). It was concluded that Vitrectomy with ERM peeling can improve visual acuity and ease macular edema. And it is a safe and effective therapy to treat patients. (18) In our study as mentioned in the scatter graph we observed the signi cant negative correlation between visual acuity and central foveal thickness both preoperatively and postoperatively at the end of 3 months.
In another study conducted by Soon II Kwon, Sung Jo Ko and In-Won Park of " The Clinical Course of the Idiopathic Epiretinal Membrane After Surgery" in 30 eyes of 30 patients and followed for a period of 7 months after surgery it was observed that there was signi cant improvement in the visual acuity with upto 2 or more lines of improvement and the mean foveal thickness which was 409.7+/-107.9 micron before surgery was improved to 288.6+/-66.1 micron seven months after surgery. Thus the Foveal thickness and visual acuity improved until seven months after the vitrectomy in patients with idiopathic ERM. Preoperative visual acuity, foveal thickness, and nal foveal thickness had a signi cant correlation with the nal visual acuity. (19) Whereas in our study the preoperative mean central foveal thickness 388mm (± 88.16) was reduced to 308.48mm (± 61.54) correlating with the improvement in visual acuity.
A study conducted by Jong-uk Hwang, Joonhong Sohn, Byung Gil Moon, Soo Geun Joe, Joo Yong Lee, June-Gone Kim, and Young Hee Yoon of "Assessment of Macular Function for Idiopathic Epiretinal Membranes Classi ed by Spectral-Domain Optical Coherence Tomography" showed that multifocal electroretinography can be used to investigate the pathophysiology of ERM and to evaluate the degree of functional demise in the fovea on SD-OCT. On the basis of Spectral Domain OCT they classi ed the patients in 2 groups depending on the anatomical distortion seen on SD-OCT. Among the two groups they observed preoperative reduction in N1 and P1 amplitudes which after surgical removal of epiretinal membrane showed improvement in amplitudes of ERGs signi cantly correlated with improvent in BCVA post surgery. (20) Our study also shows improvement in amplitudes in mfERG consistent with improvement in BCVA with restoration of near normal anatomical con guration of macula.

Conclusion
1. ERM peeling surgery in selected cases improves visual acuity signi cantly in majority of the patients.
2. CFT and foveal architecture signi cantly improves with ERM peeling surgery which also explains the improvement in functional visual acuity .
3. ERG interpretation goes along the improvement in best corrected visual acuity signifying improvement in functioning of macula. surgical complications