Internal Limiting Membrane Peeling in Primary Rhegmatogenous Retinal Detachment: Functional and Morphologic Results

Abstract

Purpose The aim of this study was to evaluate the influence of internal limiting membrane (ILM) peeling on the repair of proliferative vitreoretinopathy grade B (PVR B) primary rhegmatogenous retinal detachment (RRD).

Methods Thirteen consecutive eyes that underwent pars plana vitrectomy (ppV) with ILM peeling for PVR B (group 1) were matched to a cohort of 13 eyes with primary RRD without PVR and without ILM peeling (group 2). Minimum follow-up was 6 months, and all eyes were operated by the same surgeon. Preoperative characteristics (age, lens status, macula-ON/OFF) were similar in the two groups (p ≥ 0.113).

Results At the end of follow-up, reattachment rates were comparable, with 92.3% in group 1 and 92.3% in group 2 (p = 1.0). Postoperative epiretinal membrane formation based on OCT was significantly reduced by ILM peeling (p = 0.04). Visual acuity was also comparable (group 1: 0.26 ± 0.29, group 2: 0.15 ± 0.17 logMAR; p = 0.125).

Conclusion This study suggests that intraoperative removal of the ILM in PVR B RRD can improve functional and morphological outcomes to levels obtained in uncomplicated RRD without PVR. ILM peeling does not appear to negatively affect postoperative visual acuity. Studies with longer follow-up are warranted to gauge a potential positive impact.

Zusammenfassung

Hintergrund Ziel dieser retrospektiven Kohortenstudie war es, das funktionelle und morphologische Ergebnis nach primärer rhegmatogener Netzhautablösung zwischen Patienten mit und ohne intraoperatives Peeling der internen limitierenden Membran (ILM) zu vergleichen.

Methoden Die morphologische Datenbank der Augenklinik wurde auf Patienten untersucht, die im Zeitraum von 2020 bis 2023 an einer primär rhegmatogenen Netzhautablösung operiert wurden (Single Surgeon) und ein verfügbares Follow-up von mindestens 6 Monaten aufwiesen. Eingeschlossen wurden 13 Augen, die sich einer Pars-plana-Vitrektomie (ppV) mit ILM-Peeling bei PVR B (Gruppe 1) unterzogen, sowie 13 Augen ohne PVR und ohne ILM-Peeling (Gruppe 2). Alle Patienten wurden primär ausgewertet hinsichtlich des bestkorrigierten prä- und postoperativen Visus und der primären Netzhautanlagerate. Als sekundäre Zielvariablen wurden definiert: Endotamponande, Nachweis von PVR, intra- und postoperative OCT-Biomarker (Integrität der äußeren Netzhautschichten, Nachweis intraretinaler Flüssigkeit).

Ergebnisse Beide Gruppen unterschieden sich nicht signifikant bez. Durchschnittsalter, Vorhandensein eines Linsenimplantats und dem intraoperativen Status der Makula (Makula on vs. off) (p ≥ 0,05). Die primäre Anlagerate war mit 92,3% in Gruppe 1 und 92,3% in Gruppe 2 vergleichbar (p = 1,0). Postoperativ zeigte sich in Gruppe 1 signifikant seltener eine postoperative epiretinale Membran (p = 0.04). Hinsichtlich der postoperativen Visusveränderung zeigte sich kein signifikanter Unterschied (Gruppe 1: 0,26 ± 0,29, Gruppe 2: 0,15 ± 0,17 logMAR; p = 0,125).

Schlussfolgerung Unsere Ergebnisse deuten darauf hin, dass die intraoperative Entfernung der ILM bei rhegmatogener Netzhautablösung die Wahrscheinlichkeit des Auftretens einer postoperativen PVR-Reaktion reduzieren kann und keinen negativen Einfluss auf den postoperativen Visus zu nehmen scheint. Zusätzliche Studien mit größerer Kohorte sind zu empfehlen.

Keywords

retina - vitreous - retinal detachment - epiretinal membrane

Schlüsselwörter

Retina - Netzhautablösung - epiretinale Membran - Vitrektomie

Introduction

Pars plana vitrectomy (ppV) currently represents the most popular and successful surgical approach to rhegmatogenous retinal detachment (RRD) [1]. While its use and technical aspects are standardized internationally, a multitude of procedural subtleties based on the individual surgeonʼs discretion have been described. These include, for example, the use of 23-, 25-, or 27-gauge trocars [2], the use of air or gas tamponades [3], or the addition of macular surgery.

Concerning the latter, peeling of the internal limiting membrane (ILM) represents the most frequently performed addendum in retinal detachment (RD) repair. Nevertheless, its potential risks and benefits are debated controversially. A large benefit of ILM peeling in RRD repair includes the prevention of postoperative fibrotic proliferation on the macular surface. The formation of epiretinal membranes (ERMs) is one of the most common postoperative complications after vitrectomy for RD. In 7 – 15% of vitrectomies for RD, an ERM forms postoperatively [4], [5], [6]. The resulting membrane can exert high tensile forces on the underlying retinal layer and alter its anatomy [7]. As a result, visual acuity (VA) gain after surgery is limited, metamorphopsia can occur, and in some cases, reoperation with peeling of the ERMs is required [8]. In the development of ERMs, vitreous cortex remnants (VCRs) play a major role by serving as a scaffold on the ILM for fibrocellular proliferation [9], [10], [11], [12]. Peeling of the ILM results in removal of the VCRs and thus a reduced proliferative stimulus [13], [14], [15], [16], [17], [18].

On the other hand, the ILM is a physiologic component of the retinal architecture. Thus, ILM removal also carries some risks. Among these are modified postoperative retinal anatomy with foveal shifting, focal retinal hemorrhage, and dissociated optic nerve fiber layer (DONFL) [19], [20], [21], [22], [23]. Functionally, paracentral scotomas and reduced central retinal sensitivity may occur [20], [24]. In addition, removal of the ILM in detached retina is surgically challenging and much more complex compared to an attached retina [5].

The aim of the present study was to compare the outcomes of ILM peeling in proliferative vitreoretinopathy (PVR) B RRD with uncomplicated RRD without ILM peeling concerning VA and retinal reattachment rates.

Methods

Patient selection

For this retrospective cohort study, the Smart Eye Database (SmEyeDat) of the University Hospital was screened for patients with primary RRD repair between January 2020 and May 2023 by a single surgeon. The study adhered to the declaration of Helsinki and local ethics committee approval was obtained. Provided written informed consent for treatment was obtained and analysis was performed after anonymization. Screening included all patients with at least a follow-up of 6 months. We included macular on and off patients. Eyes with a history of trauma, uveitis, proliferative vitreoretinopathy C, or high myopia > − 6 D were excluded. ILM peeling was performed based on the surgeonʼs discretion using Membrane Blue as dye (DORC, Zuidland, Netherlands). Patients were retrospectively divided into two groups. All patients with ILM peeling during RD surgery and PVR B reaction were included in group 1, and patients who did not undergo ILM peeling with no PVR were included in group 2. PVR B reaction was categorized intraoperative by the surgeon. Intraoperative optical coherence tomography (OCT) was performed in every patient and used for grading.

Intraoperative OCT was used to rule out a concomitant macular hole. Before and after surgery, each patient underwent a standardized examination including refraction-based VA testing, air-puff noncontact tonometry, slit lamp examination, and fundoscopy. Postoperative OCT was performed using the Heidelberg Spectralis (Heidelberg Engineeringʼs Spectralis HRA + OCT, Heidelberg, Germany) OCT. Clinical data was collected, including age, sex, date of RD surgery, best-corrected visual acuity (BCVA) at each follow-up visit, postoperative ERM formation, retinal redetachment, macular edema, and OCT parameters such as central subfield thickness (CST). Decimal VA was converted to logarithm of the minimum angle resolution (logMAR) units for analysis. Hand motion and finger counting was converted to 2.3 and 1.9 as previously described [25].

Optical coherence tomography

Imaging was performed as previously described elsewhere [26]. Spectral-domain OCT was performed using the Spectralis HRA + OCT (Heidelberg Engineering) system, including a volume scan (49 B-scans). Auto segmentation was proofed by a physician. Heidelberg Spectralis SD-OCT (Heidelberg Engineering) was used to evaluate the postoperative presence of ERMs, foveal profile, CST, presence of macular edema, and the integrity of the ellipsoid zone (EZ).

Data analysis and statistics

Data management was performed with Microsoft Excel Version 16.72 (Microsoft Corp., Redmond, WA, USA) for Mac. For statistical analyses, IBM SPSS Statistics 28 (IBM Germany GmbH, Ehningen, Deutschland) was used. As the data was not normally distributed, nonparametric tests were applied. The differences between the groups were assessed using the Mann-Whitney U test for nominal scaled data and non-normally distributed variables. Continuous variables are expressed as the mean ± standard deviation and categorial variables as frequencies. The significance level was set at p < 0.05.

Results

Baseline demographics

In total, 26 patients with 26 eyes were included in our study. All patients with ILM peeling during RD surgery and PVR B reaction were included in group 1 (13 patients), and patients who did not undergo ILM peeling with no PVR were included in group 2 (13 patients). The mean age was similar in group 1 (62.38 ± 8.61 years) and group 2 (63.77 ± 7.98) (p = 0.65). Characteristics of groups 1 and 2, including sex, age, baseline VA, preoperative lens status, and foveal involvement, did not differ significantly within the two groups and are summarized in [Table 1]. Preoperative PVR B features are also listed in [Table 1].

Table 1 Baseline clinical characteristics of groups 1 and 2. Bold: statistically significant differences between the two groups. ^aMann-Whitney U test.

	Group 1	Group 2	p value
n	13	13
Age (years)	62.38 ± 8.61	63.77 ± 7.98	0.65a
Baseline: visual acuity	1.03 ± 0.96	0.84 ± 0.97	0.39a
Pseudophakic	5	3	0.84a
Foveal involvement Macular on/off	4/9	7/6	0.34a
PVR B: ERMs preoperative	7	0	< 0.02a
PVR B: Surface wrinkling	13	0	< 0.01a
PVR B: Retinal stiffness	2	0	0.51a
PVR B: Decreased mobility of vitreous	3	0	0.34 a

Surgical outcomes

All eyes underwent RD surgery with vitrectomy including intraocular tamponade. Primary success rates were 92.3% in groups 1 and 2 (12/13) (p = 1.0). The distribution of intraocular tamponades did not differ significantly between groups and is listed in [Table 2] (p = 0.96).

Table 2 Distribution of intraocular tamponade during vitrectomy in groups 1 and 2.

Tamponade	Group 1	Group 2
C2F6	9	9
6F6	0	1
Silicone oil	2	1
Air	2	2

In group 1, five patients had a combined phakovitrectomy surgery, and in group 2, three patients (p = 0.84). All phakic patients received combined phakovitrectomy, except for one 51-year old patient in group 2 who only underwent vitrectomy. Postoperatively, this patient had a slight posterior subcapsular cataract, which, however, was visually insignificant, with a VA of 0.1 logMAR postoperatively. There were no severe intraoperative complications. Mean follow-up period was 555.08 ± 376.62 days in group 1 and 808.31 ± 402.12 days in group 2 in total and did not significantly vary in the two groups (p = 0.13).

OCT outcomes

Postoperative ERM formation based on OCT was significantly reduced by ILM peeling (p = 0.04). Postoperative ERM formation was found in one patient in group 1 and six patients in group 2. Two patients in group 2 had the need for a second ERM peeling surgery. [Fig. 1] shows exemplary postoperative OCT scans. The mean CST in group 1 was 339.08 ± 50.14 µm and in group 2 315.62 ± 33.53 µm; there was no significant difference (p = 0.06). A postoperative cystoid macular edema was found in five patients in group 1 and in two patients in group 2 (p = 0.34). Treatment was needed in most patients and included Nevanac eye drops (Novartis AG, Basel, Switzerland), one patient additionally needed peribulbar triamcinolone, and one patient received a dexamethasone implant (Ozurdex, Abbvie, North Chicago, IL, USA). To evaluate the outer retina, the integrity of the EZ was analyzed. In group 1, two patients and in group 2, three patients showed an EZ defect in the OCT scan; there was no significant difference (p = 0.76). OCT outcome parameters are shown in [Table 3].

Fig. 1 a Group 1 patient (with intraoperative internal limiting membrane peeling) with asymptomatic mild postoperative epiretinal membrane that required no treatment at that stage. b Group 2 patient (without intraoperative internal limiting membrane peeling) with symptomatic postoperative epiretinal membrane that required further treatment.

Table 3 Optical coherence tomography parameters during the follow-up period. Bold: statistically significant differences between the two groups. ^aMann-Whitney U test. ERM = epiretinal membrane; CME = cystoid macular edema; DONFL = dissociated optic nerve fiber layer.

	Group 1	Group 2	p value
n	13	13
ERM formation	1	6	0.04a
Redetachment	1	1	1.0a
Central retinal thickness	339.08 ± 50.14 µm	315.62 ± 33.53 µm	0.06a
CME	5	2	0.34a
Treatment für CME	4	2	0.52a
Ellipsoid zone defect	2	3	0.76a
DONFL	5	0	< 0.01a

Visual acuity

VA was tested at every visit. The baseline VA was 1.03 ± 0.96 in group 1 and 0.84 ± 0.97 logMAR in group 2; there was no significant difference (p = 0.39). We analyzed VA postoperatively, as well as the VA gain between baseline and postoperative visit ([Table 4], [Fig. 2], and [Fig. 3]). Postoperative VA was 0.26 ± 0.29 in group 1 and 0.15 ± 0.17 in group 2 (p = 0.125). The VA gain between the baseline visit and postoperative follow-up visit in group 1 was − 0.77 ± 0.97 compared to − 0.7 ± 0.89 in group 2 (p = 0.920).

Table 4 Visual acuity follow-up in groups 1 and 2. Bold: statistically significant differences between the two groups. ^aMann-Whitney U test. VA = visual acuity; logMAR = logarithm of the minimum angle of resolution

	Group 1	Group 2	p value
logMAR VA
Postoperative follow-up	0.26 ± 0.29	0.15 ± 0.17	0.125a
logMAR VA Change
Difference baseline – follow-up visit	− 0.77 ± 0.97	− 0.7 ± 0.89	0.92a

Fig. 2 Representation of the preoperative visual acuity (logMAR) in both groups using a boxplot. ILM = internal limiting membrane; VA = visual acuity.

Fig. 3 Representation of the postoperative visual acuity (logMAR) in both groups using a boxplot. ILM = internal limiting membrane; VA = visual acuity.

Discussion

Our study shows that, in skilled hands, additional ILM peeling in RRD with PVR B does not negatively influence VA outcomes or anatomical success, while it dramatically reduces the postoperative formation of ERMs, which, in the long term, reduces the burden of reoperation and VA decline in patients with successful RD repair. Moreover, no negative impact on ILM peeling on OCT biomarkers demonstrating a healthy retinal architecture was found, except DONFL, which was seen in 38.5% of patients in group 1; however, VA did not significantly differ between our groups.

Concerning clinical decision-making, our study adds evidence supporting ILM peeling in cases with primary RD with PVR B reaction. It seems to dramatically reduce the redetachment rate. While redetachment in PVR B cases has been described to be up to 34% [13], we only found a redetachment in 7.7% of our ILM peeled PVR B cases. We thereby could achieve a reduction of the redetachment rate to the levels of uncomplicated RDs. As our data suggest, this benefit is not outweighed by potential anatomical damage, for example, foveal shifting, focal retinal hemorrhage, and DONFL [19], [20], [21], [22], [23]. Concerning foveal shifting, the retina itself is already displaced due to the RD, which probably renders this effect secondary to ILM peeling less important. Many retinal surgeons even advocate performing ILM peeling in patients with foveal splitting, a special anatomical configuration where the demarcation line of the RD goes directly through the fovea and can cause severe postoperative metamorphopsia [27]. Besides, potential negative effects of ILM peeling, such as paracentral scotomas and reduced central retinal sensitivity, may also be caused by the RD itself [20], [24].

The efficacy of simultaneous ILM peeling with removal of the ERM to prevent recurrence has been demonstrated in a number of studies in recent years. However, most of these studies refer to idiopathic and not secondary ERMs [28]. Currently, there is controversy regarding the potential beneficial effects of ILM peeling during RD surgery other than ERM recurrence reduction [24]. Based on recent literature, many authors recommend ILM peeling only for patients with complicated RD [17], [29].

As a limitation, our study provides primary outcomes at follow-ups of 6 months.

Although our follow-up is relatively short, most ERM formations are detected within the first 3 months postoperatively [4], [15], [18], [30]. So with a mean follow-up of 681.69 ± 389.94 days, we should have detected most of the ERM formations. Metamorphopsia was, unfortunately, not recorded in all patients, so it was omitted from the analysis. However, a large percentage of ERMs remain asymptomatic and OCT imaging provides a sensitive diagnosis [8], [31].

As a caveat, longer-term retinal changes secondary to any intervention involving the ILM might only be obvious after many months or years. For example, Klaas et al. recently suggested that structural changes, e.g., foveal asymmetry secondary to posterior vitreous detachment, can cause a domino effect that can cause lamellar or full-thickness macular holes after a long period of 6 – 27 months [32]. This can also apply to ILM removal, which may cause substantial histologic damage to the Mueller cells within the ILM. The mechanical stress of the basal lamina caused by peeling can be transmitted to deeper retinal layers and lead to modifications of retinal structures [33]. Lamas-Francis et al. performed a meta-analysis in 2023 examining studies with ILM peeling in RD surgery, finding no significant difference in terms of VA outcome depending on the peeling condition. However, in terms of redetachment rate, a significant reduction was found in patients with ILM peeling [4]. Several other studies also demonstrated a reduction in ERM formation with ILM peeling but found no significant difference in postoperative VA [14], [15], [27]. Obata et al. even observed poorer VA in patients with ILM peeling and macula-OFF RD [16]. Eissa et al. found a worse postoperative VA and macular sensitivity in patients with ILM removal. Additionally, they described retinal pits in all patients with ILM peeling, which they explained by more mechanical trauma during surgery. Nevertheless, there was no correlation of dimples with the VA or macular sensitivity [17]. However, there are further studies that demonstrated a better visual outcome after ILM peeling [5], [18]. Nam and Kim described a better postoperative VA in macula-ON patients when ILM peeling was performed. They attribute this to the prevention of ERM formation, which could reduce VA postoperatively [18]. Although ILM peeling might not lead to a better postoperative VA, it can lead to better anatomical success and macular compliance by decreasing the contraction forces in PVR retinal redetachment [13]. Consistent with the studies mentioned above, postoperative VA was not significantly worse in patients who underwent ILM peeling than in patients without peeling in our study. Regarding the redetachment rate, we could not find any difference between the two groups.

Additionally, our study is limited by the retrospective design, the relatively small sample size, and the surgeonʼs bias of selecting patients for ILM Peeling.

In summary, we found that ILM peeling in primary rhegmatogenous ablatio with PVR B can significantly reduce the risk of ERMs in high-risk patients and improve their prognosis comparable to uncomplicated RRD. No negative effects on functional outcome were detected. Further studies with larger cohorts, longer follow-up, and additional functional testing (e.g., microperimetry) are needed to investigate the long-term impact of ILM peeling on visual function and retinal redetachment.

Conclusion

Already known:

• The formation of ERMs is one of the most common postoperative complications after vitrectomy for RD.

• The benefits of ILM peeling for maculopathies such as a macular hole or advanced macular pucker.

Newly described:

• This study suggests that intraoperative removal of the ILM in PVR B RRD can improve functional and morphological outcomes to levels obtained in uncomplicated RRD without PVR.

• ILM peeling does not appear to negatively affect postoperative VA.

Conflict of Interest

No authors reported any financial interest related to this study. However, Jakob Siedlecki received previous speaker fees and travel expenses from Novartis Pharma GmbH, Carl Zeiss Meditec AG, Roche AG, Apellis Pharmaceuticals, Allergan GmbH, Abbvie, and Heidelberg Engineering GmbH. Jakob Siedlecki received personal consultation fees from Roche AG, Bayer AG, Novartis Pharma GmbH, Allergan GmbH, Abbvie, and Apellis Pharmaceuticals. Julian Klaas received previous speaker fees and travel expenses from Norvartis GmbH. Benedikt Schworm received previous speaker fees and travel expenses from Norvatis Pharma GmbH and Topcon Corporation. Thomas Kreutzer received previous speaker fees from DORC Int. and Bausch + Lomb/Lomb Int. Leonie Keidel receives honoraria income as speeker fees from Recordati Pharma GmbH. Siegfried Priglinger received previous speaker fees and travel expenses from Norvartis Pharma GmbH, Oertli AG, Bayer AG, Alcon Pharm GmbH, and Allergan GmbH. Denise Vogt and Franziska Eckardt declare no financial disclosures.

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Publication History

Received: 11 August 2024

Accepted: 16 September 2024

Article published online:
13 February 2025