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ORIGINAL ARTICLE
Year : 2020  |  Volume : 7  |  Issue : 1  |  Page : 13-18

Comparative study of success of various techniques of internal limiting membrane peel in the management of rhegmatogenous retinal detachment with proliferative vitreoretinopathy with concomitant macular hole


1 Consultant Vitreo-Retina, Sarakshi Netralaya, Nagpur, Maharashtra, India
2 Head, Data Analysis Group MDS BioAnalytics Pvt. Ltd, Nagpur, Maharashtra, India

Date of Submission09-Jun-2020
Date of Acceptance04-Aug-2020
Date of Web Publication11-Dec-2020

Correspondence Address:
Dr. Shilpi H Narnaware
Consultant Vitreo-Retina, Sarakshi Netralaya, 19, Rajiv Nagar, Wardha Road, Nagpur - 440 025 Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/erj.erj_7_20

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  Abstract 


Purpose: To assess the anatomical and functional success in patients with rhegmatogenous retinal detachment (RRD) with proliferative vitreoretinopathy (PVR) ≥ C1 with coexisting macular holes (MHs) using different management strategies. Materials and Methods: It is a prospective, nonrandomized, observational study in 23 eyes of 23 patients (male: female = 15:8) diagnosed with RRD with PVR ≥ C1 with MH. Patients were divided into three groups according to the technique: Group 1: Pars plana vitrectomy (PPV) without internal limiting membrane (ILM) peel, Group 2: PPV with ILM peel, and Group 3: PPV with inverted ILM peel technique. Results: The closure of MH was confirmed on SD-OCT. Of the total 23 eyes, 19 patients had attached retina with closed MH during a follow-up period of 6 months. Out of four cases of recurrent retinal detachment (RD), three patients belonged to the no peel group and one to the ILM peel group. In no peel group, two patients had recurrence with re-opening of MH, and out of these two cases, one patient had additional break in the periphery. However, two other cases, each from no peel and ILM peel group, had recurrence due to PVR changes in the periphery. Visual acuity (VA) improvement to LogMar ≤ 1 is seen in 50%, 70%, and 85.7% in the no peel, ILM peel, and inverted flap technique, respectively. Conclusion: The results suggest that ILM flap technique without encirclage band can be effectively applied to the treatment of MH with RD with more severe PVR changes and that the hole closure results in improved postoperative best-corrected VA.

Keywords: Internal limiting membrane peel, inverted internal limiting membrane peel, macular hole, retinal detachment


How to cite this article:
Narnaware SH, Bawankule PK, Raje D. Comparative study of success of various techniques of internal limiting membrane peel in the management of rhegmatogenous retinal detachment with proliferative vitreoretinopathy with concomitant macular hole. Egypt Retina J 2020;7:13-8

How to cite this URL:
Narnaware SH, Bawankule PK, Raje D. Comparative study of success of various techniques of internal limiting membrane peel in the management of rhegmatogenous retinal detachment with proliferative vitreoretinopathy with concomitant macular hole. Egypt Retina J [serial online] 2020 [cited 2021 Jan 21];7:13-8. Available from: https://www.egyptretinaj.com/text.asp?2020/7/1/13/302997




  Introduction Top


About 2.5%–4% of cases of rhegmatogenous retinal detachment (RRD) have coexistent macular hole (MH),[1] and according to different studies, 53%–67%[1],[2] of cases have associated proliferative vitreoretinopathy (PVR) at presentation. RRD with concomitant MH can typically occur in two scenarios. First, MH acts as a hole and leads to retinal detachment (RD) which is typically posterior but in rare cases can extend anteriorly. This scenario is usually seen in the pathological myopia cases[3] and is not associated with breaks in the periphery.[3]

In the second scenario, RD typically starts with break in the periphery and progresses posteriorly. Because of spreading of thesubretinal fluid under fovea, it may cause stretching of retinal tissue, leading to MH formation.

The pathogenesis behind RRD with peripheral breaks with concomitant MH is not fully understood. There are various theories behind pathophysiology of RRD with MH. One theory is that posterior vitreous detachment (PVD) can put traction on central macula causing MH[1] (mechanism similar to that causes peripheral break). Another theory is similar to PVR process, i.e., peripheral break releases retinal pigment epithelial (RPE) cells, which attach to macular surface and contracts, leading to tangential traction and thereby MH formation.[2]

The principle to manage RRD with PVR is similar, i.e., relief of traction (by membrane peeling/retinotomy/relaxing retinectomy), closure of break(s), and tamponade. However, associated MH management is a point of debate. Although the principle of management of MH with RRD is similar to typical MH without concurrent RRD, challenges to repair hole in RRD are different. First challenge is fear of dye (used for staining internal limiting membrane [ILM]) gaining access to the subretinal space in a detached retina and so its potential toxicity. Another challenge is to peel ILM in the detached mobile retina. Various studies[4] have demonstrated the use of Per Fluoro Carbon Liquid (PFCL) to flatten retina to aid in the ILM peel in such cases. However, in spite of all the maneuvers, every time, it is not possible to achieve ILM peel in such cases.

Various studies have reported various success rates with and without ILM peel. A study by Ryan et al.[5] has shown increased success with ILM peel, while the study by Shukla et al.[6] reported similar anatomical success with any of the techniques and better visual gain in the no peel group. However, these studies excluded cases with PVR > C. They also placed encirclage band in all cases and used silicon oil as a tamponading agent in majority of their cases. A study by Najafi et al.[1] reported a recurrence rate of 27% in the ILM peel group while 50% in the no peel group in cases of significant PVR.

Studies have shown increased favorable surgical outcomes with inverted ILM flap technique in refractory MH[7] and MH-RD.[8],[9],[10] One study[11] has studied the success of free ILM flap or inverted ILM peel flap in cases of paracentral breaks in RD.

No study has directly compared the success rate with no peel, ILM peel, and inverted flap (IF) technique. To our knowledge, ours is the first study that compared the surgical and functional success rates in cases of RRD with concurrent MH with different strategies, i.e., no ILM peel, ILM peel, and IF ILM peel in cases of PVR ≥Grade C, and without concurrent use of encirclage band.


  Materials and Methods Top


Study design

This was a prospective, nonrandomized, observational study on 23 eyes of 23 patients of RRD with PVR ≥ C with concurrent full-thickness MH who underwent vitrectomy between July 2018 and October 2019 at a tertiary care center. All operations were performed by a single experienced vitreoretinal surgeon. The study was performed according to the ethical standards of the Declaration of Helsinki and approval from the ethics committee. Eyes were randomly distributed into three groups – Group 1: PPV with no ILM peel, Group 2: PPV with ILM peel, and Group 3: PPV with inverted ILM peel flap technique. For the purpose of the study, patients with RD secondary to MH (with no peripheral breaks), axial length >24 mm, recurrent RD, combined RD, and incomplete follow-up were excluded from the study. All patients had PVR stage ≥ C1. PVR staging was graded according to the updated classification of Retina Society Terminology Committee (1991).[12] All patients underwent thorough preoperative ophthalmological examination, including best-corrected visual acuity (BCVA), slit lamp examination, and dilated indirect ophthalmoscopy examinations. The presence of MH was confirmed either before surgery with OCT [Figure 1]a and [Figure 1]b or during surgery by direct examination [Figure 2]a and [Figure 2]b. Demographic data and lens status at the time of surgery were recorded. SD-OCT (Zeiss) [Figure 3]a, [Figure 3]b, [Figure 3]c and fundus photograph [Figure 4] were done 1 month later to document the status of MH. BCVA and retinal status were recorded at 1 month, 3 months, and 6 months after the first surgery.
Figure 1: (a and b) SD-OCT preoperatively showing retinal detachment with macular hole

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Figure 2: (a) Intraoperative fundus photograph before drainage of fluid (macular hole not seen). (b) Intraoperative fundus photograph revealing macular hole after drainage of fluid

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Figure 3: (a) SD-OCT 1-month postoperative in case of inverted internal limiting membrane peel flap. (b) SD-OCT 1-month postoperative in case of internal limiting membrane peel. (c) SD-OCT 1-month postoperative in case of no peel

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Figure 4: One-month postoperative fundus photograph with silicon oil in situ showing closed macular hole

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Surgical technique

In all cases, 23-gauge PPV with Alcon constellation was performed using a noncontact wide-angle viewing system (Oculus BIOM). Informed written consent was taken from the patients before surgery. Surgery was performed mostly under local anesthesia. Cannulae were placed 3 and 3.5 mm away from the limbus in pseudophakic and phakic patients, respectively. Core vitrectomy was done. Remaining adherent posterior hyaloid was removed by PVD induction using cutter. Membranes were peeled using peeling forceps. Base excision with scleral depression was done in all cases. No case received encircling/sclera buckle (SB). In Group 2 and 3, Internal Limting Membrane (ILM) peel was done after staining with Brilliant blue dye (0.05%) by pinch and peel technique using ILM forceps (Grieshaber, Alcon) under PFCL. ILM was peeled at the macular area in Group 2. In Group 3, IF technique was done after peeling the ILM. PFCL was used to flatten the retina followed by PFCL–air. Drainage of the fluid was predominantly done through the peripheral break after flattening retina with PFCL till edge of the posterior most peripheral break. Residual fluid through MH was drained only in Group 1 and 2 with 41-gauge tapered extrusion needle (by Pricon). Endolaser was applied around the peripheral retinal tear and 360° to the vitreous base. Tamponading with silicon oil (1000 centistokes) was done in all cases.

Silicon oil removal was done at 3 months after the surgery in patients with attached retina and earlier in patients with recurrent detachment. The cause of recurrent RD in our study was reopening of MH in two cases and peripheral PVR in two cases. Patients with recurrence due to re-opening of MH in the no peel group underwent ILM peel with tamponading during re-surgery.Patients with recurrence in No peel group underwent membrane peel with tamponade during re-surgery. No belt buckle was done even in recurrent RD cases.

Statistical methods

The baseline characteristics of the patients across three groups, i.e., ILM IF, ILM peel, and no ILM peel, were summarized according to the scale of measurement. The continuous variable such as age was expressed in terms of mean and standard deviation, and the significance of difference across groups was tested using one-way analysis of variance. The categorical variables such as gender, preoperative visual acuity (VA), and lens status were summarized as numbers and percentage, and the difference was tested using Pearson's Chi-square test. The comparison of VA before and after treatment was compared using McNemar test. Further, the comparison of VA >1 across three treatment groups was carried out using Fisher's exact test. The cumulative recurrence rates of RD were obtained as Kaplan–Meier plots [Figure 5] and were compared using log-rank test.
Figure 5: Kaplan–Meier plots showing cumulative recurrence rates of retinal detachment in three internal limiting membrane peel-treated groups

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  Results Top


The descriptive statistics for 23 cases treated with ILM IF (n = 7), ILM peel (n = 10), and no peel (n = 6) are given in [Table 1]. The difference in the mean age of the patients across groups was statistically insignificant. In addition, the gender distribution and preoperative VA status of the patients across three treatment groups was insignificantly different. However, the lens status showed significant difference across groups (P < 0.0001), with 90% of the ILM peel-treated cases as pseudophakic and aphakic. The overall comparison of VA of cases before and after treatment across three groups revealed statistically significant difference with a P value of 0.0003 using McNemar test [Table 2]. Sixteen out of 23 cases (69.5%) with preoperative VA >1 (LogMar) had postoperative VA <1 (LogMar). Overall, there was a statistically significant improvement in the VA after treatment. Further, the comparison of postoperative VA >1 across three treatment groups was carried out with the results as shown in [Table 3]. In all the three groups, the difference in the proportion of cases with VA ≤ 1 and VA > 1 was insignificantly different (P > 0.05). In addition, the difference in the proportion of cases with VA ≤ 1 across three groups was statistically insignificant (P = 0.937). The Kaplan–Meier plot shows the cumulative recurrence of RRD in three treatment groups [Table 1]. The difference of recurrence rates was statistically significant with a P value of 0.029 using log-rank test. The rate was higher in without ILM peel group as compared to ILM peel and IF groups.
Table 1: Comparison of baseline characteristics of patients across three treatment categories (n=23)

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Table 2: Overall comparison of visual acuity of patients before and after treatment

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Table 3: Comparison of visual acuity of nonmyopic patients after treatment in three groups

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  Discussion Top


Management problems which are seen in cases of RRD with coexisting MHs are successful anatomical retinal reattachment and closure of MH. In spite of anatomical success attained by various techniques, visual gain is usually poor in this subset. One cause of poor visual gain in these patients is drainage of the fluid through MH which may enlarge the hole and disrupt photoreceptors (PRs) and RPE cells.

MH surgery was first introduced by Kelly and Wendel.[13] Since then, various refinements in the techniques were explored to increase the anatomical and functional success rate in such cases. It was Yooh et al.[14] who showed the role of ILM in the pathogenesis of MH. RD with concomitant MH is not a common entity, but the need of re-operation in such cases is significantly higher compared to RD with no coexisting MH as reported by Najafi et al.[1] More chances of failure might be attributed to more chances of PVR in such cases.[1] Studies[1],[6],[7] have suggested that addition of SB and use of silicone oil can increase the success rate in cases of RRD with MH with PVR changes. Studies have also shown the importance of ILM peel in RRD with MH to increase the success rate.[10] Study by Singh[15] and Shukla et al.[6] showed no difference in anatomical success between groups receiving ILM peel or not. However, as unclosed MH can be a risk factor for re-detachment, inverted ILM flap technique can reduce this risk and need of re-surgery. Meta-analysis[10] showed increased anatomical success rate and more rate of MH closure in cases who underwent inverted ILM peel as compared to ILM peel only in MH-RD.[10] Further, studies[16],[17] have shown that MH remained close in recurrent RD cases who underwent inserted ILM tissue during primary repair.

In our study, all cases were of PVR > C1, ILM peel was done without using PFCL, all cases received silicone oil as a tamponading agent, and none received encirclage band. 50% (3/6) cases had re-detachment in the no peel group, and out of those three cases, two (66.6%) were because of re-opening of MH and one was because of PVR changes in the periphery. In ILM peel group, one recurrence was seen due to PVR changes in the periphery. In our study, no recurrence was seen in the IF group. All the patients had attached retina after re-surgery in cases of re-detachment.

The study by Nazafi et al.[1] reported 50% success rate in no ILM peel group, and similar are the findings of our study. The study by Shukla et al.[6] had 100% anatomical success rate in their case series even in no peel group. However, their study included cases with PVR grade B only. In addition, in their series, all cases received encirclage band and majority of patients received silicone oil as a tamponading agent even in grade B PVR cases. In our study, one case was posttrauma and two were postendophthalmitis cases in the no peel group, and out of three cases with recurrent detachment in no peel group, one was posttrauma and one postendophthalmitis RD. Studies have shown moderate success rate in this subgroup of detachment.[18],[19]

Better anatomical success in the IF technique can be attributed to ILM which acts as a scaffold for glial cell proliferation, compensating for retinal shortening,[20] and thereby helps in MH closure and retinal attachment.[7],[8]

Various studies have reported variable functional success with different techniques. Although the anatomical success rate has been achieved in nearly 100% of cases, still the visual gain is not as promising as in other subset of RRD without MHs. In the study by Singh,[15] visual gain was poor in the no peel group compared to the ILM peel group. However, Shukla et al.[6] reported better visual results in the no peel group. In meta-analysis by Yuan et al.,[10] there was no significance in postoperative gain in VA with any of the technique.

The overall visual improvement to LogMar ≤1 was seen in 69.5% of cases in our study. In the present study, 85.7%, 70%, and 50% of the patients achieved final VA of LogMar ≤1 in the IF, ILM peel, and no peel group, respectively. The visual gain was seen more in the IF technique compared to no peel, but it was not statistically significant. More amount of vision gain in the IF technique can be attributed to no fluid drainage through MH, thus preventing more iatrogenic damage to photoreceptor cells. Also, inverted flap can cause proliferation of glial cell causing photoreceptors to assume new position in direct proximity to fovea.[7]

Although various modifications in the surgical techniques can achieve attached retina with closed MH in this subset, MH surgery is very demanding in the presence of detached retina. ILM peel can be facilitated with the use of dyes and PFCL, but one should be aware that ILM behaves differently under PFCL. ILM under PFCL has more elastic recoil, and it also eliminates the need of counter pressure to ensure atraumatic peel. Still, peeling an ILM is not free of complications which ranges from trauma to macular PR cells,[21] iatrogenic paramacular breaks, and dye-related photo-toxicity which can have long-term effect on macular function.


  Conclusion Top


  1. Better MH closure and attachment rates can be achieved with inverted ILM flap technique without the use of encirclage band/SB in cases of RRD with concomitant MH with significant PVR changes
  2. Visual gain is seen more in inverted ILM peel group compared to no peel group
  3. Although challenging and not free of complications, inverted ILM peel can be considered as procedure of choice in these cases.


Limitations

The study has a small sample group. Large, randomized studies needed to confirm the better results with inverted ILM flap technique in this subset of RRD.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Najafi M, Brown JS, Rosenberg KI. Increased reoperation rate in surgical treatment of rhegmatogenous retinal detachment with coexistent macular hole. Ophthalmol Retina 2018;2:187-91.  Back to cited text no. 1
    
2.
Cunningham MA, Tarantola RM, Folk JC, Sohn EH, Boldt HC, Graff JA, et al. Proliferative vitreoretinopathy may be a risk factor in combined macular hole retinal detachment cases. Retina 2013;33:579-85.  Back to cited text no. 2
    
3.
Atchison EA, Rezaei KA. Managing the macular hole with concurrent retinal detachment. Retina Today 2018;1:26-27.  Back to cited text no. 3
    
4.
Hussain N, Hussain A, Natarajan S. PFCL and ILM peeling in macular hole with retinal detachment. Int J Ophthalmol 2008;1:66-9.  Back to cited text no. 4
    
5.
Ryan EH Jr., Bramante CT, Mittra RA, Dev S, Bennett SR, Williams DF, et al. Management of rhegmatogenous retinal detachment with coexistent macular hole in the era of internal limiting membrane peeling. Am J Ophthalmol 2011;152:815-9.e1.  Back to cited text no. 5
    
6.
Shukla D, Kalliath J, Srinivasan K, Neelakantan N, Rajendran A, Naresh KB, et al. Management of rhegmatogenous retinal detachment with coexisting macular hole: A comparison of vitrectomy with and without internal limiting membrane peeling. Retina 2013;33:571-8.  Back to cited text no. 6
    
7.
Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology 2010;117:2018-25.  Back to cited text no. 7
    
8.
Kuriyama S, Hayashi H, Jingami Y, Kuramoto N, Akita J, Matsumoto M. Efficacy of inverted internal limiting membrane flap technique for the treatment of macular hole in high myopia. Am J Ophthalmol 2013;156:125-31.e1.  Back to cited text no. 8
    
9.
Chen SN, Yang CM. Inverted internal limiting membrane insertion for macular hole-associated retinal detachment in high myopia. Am J Ophthalmol 2016;162:99-106.e1.  Back to cited text no. 9
    
10.
Yuan J, Zhang LL, Lu YJ, Han MY, Yu AH, Cai XJ. Vitrectomy with internal limiting membrane peeling versus inverted internal limiting membrane flap technique for macular hole-induced retinal detachment: A systematic review of literature and meta-analysis. BMC Ophthalmol 2017;17:219.  Back to cited text no. 10
    
11.
Chen YC, Yang CM, Chen SN. Internal limiting membrane flap in the management of retinal detachment due to paracentral retinal breaks. J Ophthalmol 2019;2019:4303056.  Back to cited text no. 11
    
12.
Machemer R, Aaberg TM, Freeman HM, Irvine AR, Lean JS, Michels RM. An updated classification of retinal detachment with proliferative vitreoretinopathy. Am J Ophthalmol 1991;112:159-65.  Back to cited text no. 12
    
13.
Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes. Results of a pilot study. Arch Ophthalmol 1991;109:654-9.  Back to cited text no. 13
    
14.
Yooh HS, Brooks HL Jr., Capone A Jr, L'Hernault NL, Grossniklaus HE. Ultrastructural features of tissue removed during idiopathic macular hole surgery. Am J Ophthalmol 1996;122:67-75.  Back to cited text no. 14
    
15.
Singh AJ. Combined or sequential surgery for management of rhegmatogenous retinal detachment with macular holes. Retina 2009;29:1106-10.  Back to cited text no. 15
    
16.
Hainsworth DP, Johnson MW, Jaffe GJ. Sustained closure of surgically repaired macular holes after retinal detachment with submacular fluid. Am J Ophthalmol 1997;123:364-9.  Back to cited text no. 16
    
17.
Herring JH, Chen CJ, Chen LL. Confirmation of persistent closure of surgically repaired macular hole in subsequent retinal detachment by optical coherence tomography. Ophthalmic Surg Lasers 2000;31:243-4.  Back to cited text no. 17
    
18.
Dave VP, Pathengay A, Relhan N, Sharma P, Jalali S, Pappuru RR, et al. Endophthalmitis and concurrent or delayed-onset rhegmatogenous retinal detachment managed with pars plana vitrectomy, intravitreal antibiotics, and silicone oil. Ophthalmic Surg Lasers Imaging Retina 2017;48:546-51.  Back to cited text no. 18
    
19.
Lai WY, Wu TT. Successful management in a case of traumatic retinal detachment due to open globe injury using microincisional vitrectomy. Case Rep Ophthalmol 2016;7:198-202.  Back to cited text no. 19
    
20.
Madreperla SA, Geiger GL, Funata M, de la Cruz Z, Green WR. Clinicopathologic correlation of a macular hole treated by cortical vitreous peeling and gas tamponade. Ophthalmology 1994;101:682-6.  Back to cited text no. 20
    
21.
Hayashi H, Kuriyama S. Foveal microstructure in macular holes surgically closed by inverted internal limiting membrane flap technique. Retina 2014;34:2444-50.  Back to cited text no. 21
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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