The epiretinal membrane (ERM) is a cellular avascular membrane that may cause visual disturbances due to retinal wrinkling. Although the natural history of ERM is variable and the condition may have only a mild effect on vision, many patients report significant symptoms of distortion and blurring of vision. These patients complain of impaired quality of vision, often related to metamorphopsia, without a measurable decrease in visual acuity (VA).

Amsler charts are widely used to detect metamorphopsia [1, 2]. However, fixation monitoring, precise localisation and quantification of metamorphopsia is limited with this technique. Several methods of improved assessment have been developed [4, 5, 7–9, 17]. Among the different approaches, scanning laser ophthalmoscopy (SLO) generated Amsler grid enables fixation monitoring, precise retinal localisation of metamorphopsia and its confrontation with retinal lesions [10, 16].

A previously reported method of quantification of metamorphopsia [3] is applied to assess pre- and post-operative metamorphopsia in patients scheduled for epiretinal membrane peeling.

Patients and methods

Patients

One hundred and four cases of vitrectomy and epiretinal membrane peeling by a single surgeon in 104 patients were followed over a 12-month period. The consecutive cases included in this series consisted of nonvascular-appearing membranes confined to the macula. All patients had significant visual symptoms. Eyes with concurrent ocular disorders were excluded from this study. Only patients with non-exsudative retinal pigment epithelial changes were not excluded.

Clinical evaluation

A full ophthalmic examination was performed on all eyes preoperatively, including best-corrected logMAR VA using an EDTRS chart for distant vision and a Parinaud reading chart for near vision, evaluation of metamorphopsia with an Amsler chart, slitlamp biomicroscopy, Watze–Allen slit-beam testing and optical coherence tomography (Zeiss OCT3), to exclude the existence of a full-thickness neuroretinal defect in the presence of a lamellar hole or macular pseudohole. The presence of cystoid macular oedema, a pseudohole or an epiretinal membrane in the fellow eye was also recorded. A functional assessment with a scanning laser ophthalmoscopy (SLO) was performed.

Functional assessment with scanning laser ophthalmoscopy

In order to assess the effects of surgery on functional vision, metamorphopsia was quantified with a scanning laser ophthalmoscope (Rodenstock 101, Munich, Germany) pre-operatively and 3 months after surgery. Evaluation of metamorphopsia (Fig. 1) was performed using a procedure described previously [3]. Briefly, the optico-acoustic modulation of the Helium Neon laser made it possible to generate a grid of 256 squares similar to the Amsler chart, each side of each square subtending an angular size of 1 degree. The lines of the grid subtended an angle of 3 minutes of arc. Fixation was continuously monitored, as stability and accuracy of fixation was necessary to provide reliable evaluation of metamorphopsia [3]. The difference between distortion and scotoma was explained to the patient before the beginning of the procedure. The patient was instructed to report only distortion and to ignore scotoma. First, the entire grid was presented. If a distortion was detected by the patient, then the grid was divided into four grids of 64 squares and presented separately to the patient. Each grid of 64 squares perceived as distorted was then subdivided into four grids of 16 squares. And again, each grid of 16 squares was subdivided into four smaller grids of four squares if the patient reported a distortion. Finally, adding up the different responses of the patient to each presentation made it possible to quantify the area of distortion as the sum of all the grid fragments perceived by the patient to be distorted. The procedure was repeated at a 30-minute interval. Only responses with an identical area of distortion (both the sum of the area and area pattern had to be identical) were considered as reliable. If there was difference between the two sessions, then the patient was excluded from the follow-up. The duration of the first and second procedure was monitored.

Fig. 1
figure 1

Grid exploration strategy based on scanning laser ophthalmoscopy

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Surgical technique and postoperative follow-up

A standardised three-port pars plana vitrectomy and membrane-peeling technique, using high-magnification viewing and end-gripping microforceps, was performed by one single surgeon. Patients were reviewed with a full clinical examination at 1 day, 1 week, 1 month, 3 months, and 12 months post-operatively. SLO functional assessment was performed at 12 months post-operatively. Cataract surgery was scheduled when lens opacities were judged to affect visual function.

Statistical analysis

Quantitative statistical analyses were performed on preoperative and postoperative logMAR VAs and metamorphopsia using the Analyse-It statistics package (Analyse-It Software Ltd, Leeds, UK). All comparisons were two-tailed. Means of two groups were compared using the t-test. Appropriate prognostic parameters were analysed by Pearson correlation against final postoperative acuity and change in VA.

Results

One hundred and four cases with epiretinal membranes in 104 patients underwent surgery.

Preoperative findings

Demographic details are provided in Table 1.

Table 1 Demographics of 104 consecutive patients scheduled for epiretinal membrane peeling
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Metamorphopsia

Of 104 patients evaluated clinically and by SLO to assess pre-operative metamorphopsia, in six patients the score obtained in the two test sessions was not identical. These patients were excluded from further analysis. Thus, a reproducible quantification of metamorphopsia was able to be performed in 98 patients (94%). The mean duration of the SLO test was 5 ± 1 minutes (3–11); there was no significant difference in duration between the first and second sessions.

Of 98 patients, 28 patients (29%) spontaneously complained of metamorphopsia, and all detected distortions on both the Amsler chart and the SLO-generated grid. Seventy patients (77%) did not complain of metamorphopsia spontaneously; however, 12 detected metamorphopsia on the Amsler chart and 27 on the SLO-generated grid. Thus, both procedures made it possible to increase the detection of metamorphopsia (12% for the Amsler grid and 27% for the SLO procedure).

Overall, a total of 40 patients (41%) detected distortions on the Amsler chart, and a total of 55 patients (56%) detected distortions on the SLO-generated grid, with a mean area of distortion of 36 ± 13 square degrees (12–192). One of the 40 patients with an abnormal Amsler test was missed with the SLO procedure (2.5%), but 15 patients detected with the SLO procedure were missed with the Amsler test (28%).

No significant correlation between visual acuity and the area of metamorphopsia was found. No significant difference in visual acuity between patients presenting metamorphopsia with or without foveolar involvement was found.

Scotoma

Twelve patients spontaneously reported scotoma, which they all identified as such on the Amsler chart. Of these patients, five also reported distortions on the Amsler chart and on the SLO-generated grid. However, scotoma was not reported on the SLO procedure, as the patient was instructed to concentrate only on distortion.

Post-operative findings

In all cases, epiretinal membranes were successfully removed from the macula. Eighty-five patients (82%) completed the clinical and SLO follow-up at 12 months. Of these patients, 24 had undergone cataract surgery after 1 year of follow-up.

Visual acuity outcomes

Visual acuity improved by two or more lines of vision in 60 cases (70%), stayed the same within ±1 line in 21 cases (25%), and worsened two lines or more in six cases (5%) (Fig. 2). Mean postoperative VA was 0.34 ± 0.16. Visual acuity improved following surgery by a mean of 0.22 ± 0.12 (2 lines of vision). Twenty-three patients (27%) had a halving of their visual angle.

Fig. 2
figure 2

Preoperative versus postoperative visual acuity in 85 patients completing the follow-up of 1 year (some patients had identical preoperative and post-operative visual acuity; therefore, there are less than 85 symbols on the graph)

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Distant (t = 6.62, p < 0.0001) and near (t = 6.35, p < 0.0001) VA improved significantly, there was a significant correlation between the pre-operative and the post-operative VA, which was observed for both distant VA (r = 0.68, p < 0.0001) and near VA (r = 0.70, p < 0.0001).

In the subgroup of 24 patients who had undergone cataract surgery before completing the 1-year follow-up visit, visual acuity improved by two or more lines in 17 cases (71%), and stayed the same within ±1 line in seven cases (29%). No patient worsened in this subgroup. Nine patients (38%) had a halving of their visual angle. Mean postoperative VA was 0.51 ± 0.09. Visual acuity improved following surgery by a mean of 0.25 ± 0.08 (2.5 lines of vision). At the 1-year follow-up visit, there was no significant difference in visual outcome between the patients who had undergone cataract surgery and those who had not.

Metamorphopsia

Table 2, Fig. 3

Table 2 Metamorphopsia of 85 post-operative cases completing the follow-up of one year after epiretinal membrane peeling
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Fig. 3
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Preoperative versus postoperative distortion in 48 patients completing the follow-up of 1 year. (Some patients had an identical preoperative and post-operative area of distortion; therefore, there are less than 48 symbols on the graph)

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A significant reduction in metamorphospia was observed (t = −5,74, p < 0.0001). No significant correlation between the preoperative area of metamorphopsia and post-operative standard VA (r = −0.06, p = 0.6136) was found. However, the decrease of metamorphopsia correlated with the change in visual acuity (r = −0.460, p = 0.011).

The majority of the patients, 12 months after surgery, did not detect any distortions (Fig. 4a,b). Among the patients detecting distortions post-operatively on both Amsler chart and SLO grid, in each case the area of distortion had decreased. In one patient, the distortion had shifted post-operatively from the pericentral area to the centre, following a pre-operative central scotoma (Fig. 5a,b).

Fig. 4
figure 4

(Left) Preoperative area of distortion in a patient with marked retinal wrinkling. The fragments of the grid represent the area of distortion. The patient had reported no scotoma on the Amsler grid. (Right) Post-operative evaluation with no residual distortion detected by the patient when the complete grid was presented

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Fig. 5
figure 5

(Left) A patient presenting with a preoperative central scotoma, identified as such on the Amsler grid and pericentral distortion (the scotoma does not appear on the SLO procedure, as the patients were instructed to ignore scotomata). (Right) In the same eye post-operatively, no pericentral distortions were detected and the patient perceived distortions in the central area of preoperative scotoma

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Among the patients with no preoperative distortions, two presented with asymptomatic distortions post-operatively detected with the SLO grid. In both cases, a recurring epiretinal membrane was observed.

Discussion

Vitrectomy and membrane peeling has become an effective procedure in patients, with visual improvement reported in a majority of cases following surgery for visually significant epiretinal membranes. [6, 11, 12, 14, 15]. In many of these studies, surgical indications and outcome measures have been based solely on VA parameters. Many patients who undergo surgery complain of significant symptoms other than blurred vision, especially distortion, which may be inadequately reflected by assessment of VA alone. Although metamorphopsia is spontaneously reported by many patients, it is generally admitted that the use of the Amsler grid may enhance the detection of visual distortion, which was also shown in this study.

It also appears that visual distortion may be underestimated when its evaluation is solely based on the Amsler grid. In this study, the SLO procedure performed after the Amsler grid detected a greater rate of metamorphopsia. However, a possible learning effect cannot be excluded, as the patient was not re-examined with the Amsler grid after the SLO procedure was performed. Several authors have validated the quantification of visual distortion in patients with retinal diseases [4, 5, 8, 17]. Shinoda [17] analysed the drawings performed by the patient. Bouwens and van Meurs [5] presented different charts in which the central grid was replaced by sinusoid lines of increasing amplitude. The patient was asked to identify with the non-affected eye the chart representing the magnitude of distortion perceived with the affected eye. The method presented in this study makes it possible to quantify distortion even if both eyes are affected, and does not require any drawing skills. It appears reproducible in evaluating the area of visual distortion in patients with visually significant epiretinal membranes; however, the magnitude of distortion (as in the test presented by Bouwens and van Meurs) was not possible. The fragmented presentation of the grid possibly simplifies the patient’s task of analysing distortion. In addition, SLO-generated stimulation enables fixation monitoring, and the retinal image obtained is less blurred by media opacities. However, it remains to be evaluated if a computer screen-based test, using the same method, could not also provide reliable results. This would considerably simplify the procedure, and thus provide an easily available tool for preoperative surgical planning and monitoring of postoperative outcomes in membrane-peeling surgery. A comparison of the SLO procedure and a LCD screen procedure is currently undertaken.

As in other studies [6, 11, 12, 14, 15], in our series, preoperative VA correlated with post-operative visual outcome. However, no relationship between the preoperative score of metamorphopsia (area of distortion) and either preoperative visual function or post-operative visual outcome could be demonstrated in this study [5]; the results were identical when patients with foveolar involvement of distortion were analysed separately. Thus, preoperative metamorphopsia (area of distortion) evaluated with the SLO did not provide a prognostic factor for postoperative visual outcome. This could be linked to the fact that metamorphopsia is not necessarily an indicator of the severity of visual impairment, although the reduction of distortion correlated with the increase of VA. The presence of cystoid macular oedema, thicker membranes or leakage of fluorescein on angiography does not necessarily result in more visual distortion [5, 17], although worse visual outcomes have been observed in these cases [13, 18]. It is probable that poor vision with central scotoma alters the perception of distortion, although the architecture of the retina—and in particular photoreceptor alignment—has been severely impaired by retinal wrinkling (Fig. 4).

In conclusion, this study suggests that vitrectomy and membrane peeling is beneficial in successfully reducing metamorphopsia, which is consistent with the improving visual symptoms in the majority of patients with significant preoperative symptoms from epiretinal membranes [5]. It suggests that automated monitoring of visual distortion in patients with epiretinal membranes may provide an additional tool to assess deterioration in vision, and improve surgical planning and case selection.