A Modified Vitrectomy Technique for Macular Hole-Related Retinal Detachment

Clinical Research

A Modified Vitrectomy Technique for Macular Hole-Related Retinal Detachment

Corresponding author: Dr. Hui Chen, Eye Institute, Affiliated Hospital of Nantong University, 20 Xisi Road, Nantong, Jiangsu, 226001, China, Tel: +86-13809082586; Fax: +86-513-85519820; E-mail: chenhuieye@126.com

Abstract
 
Purpose: To report the use of the dye brilliant blue G (BBG) and perfluorocarbon liquid (PFCL) in peeling of the internal limiting membrane (ILM) during macular hole-related retinal detachment (MHRD) surgery.
Methods: This study involved 18 eyes from 18 consecutive patients with MHRD who were peeled ILM underwent BBG and PFCLassisted and followed up 6 months or more. In these cases, 0.2% BBG solution injected onto the surface of macula and cleaned, for a while. Then, PFCL (0.5–1 mL) was gently injected onto the posterior retina. This technique enables peeling ILM easy and surgery perfectly by improving visualization of the ILM. The closed macular holes were categorised into two patterns based on optical coherence tomography (OCT), type 1 closure and type 2 closure.
Results: There were 6 eyes with silicone oil tamponade and 12 eyes with gas tamponade. Postoperative visual acuity improved in 18 eyes (100%), 13 out of 18 eyes (72.2%) were classified into the type 1 closure and 5 eyes (27.8%) into the type 2 closure. No adverse effect was observed postoperatively.
Conclusions: It is a simple, safe, effective and comfortable surgical technique of peeling internal limiting membrane under PFCL with BBG dye guided in MH-RD surgery.
Keywords: Brilliant Blue G (BBG); Internal Limiting Membrane (ILM) Peeling; Macular Hole-Related Retinal Detachment (MHRD); Perfluorocarbon Liquids (PFCL) 
List of Abbreviations
ILM: Internal Limiting Membrane;
BBG: Brilliant Blue G Dye;
PFCL: Perfluorocarbon Liquid;
MHRD: Macular Hole-Related Retinal Detachment;
OCT: Optical Coherence Tomography;
BSS: Balanced Salt Solution;
ICG: Indocyanine Green;
TA: Triamcinolone Acetonide;
TB: Trypan Blue;
PHACO: Phacoemulsification–Aspiration;
PVC: Posterior Vitreous Cortex;
ERM: Epiretinal Membranes;
LP: Laser photocoagulation
Introduction
Macular hole-related retinal detachment (MHRD) is a special type of rhegmatogenous retinal detachment (RRD) [1] and a common entity in highly myopic eyes [2]. The pathogenesis is considered to be the result of tangential traction from an epiretinal membrane or the inverse traction of the retina unable to expand with the posterior staphyloma [2,3].
Numerous strategies for surgical management of MHRD have been described from the initial pars plana vitrectomy and gas tamponade [4] to various adjunctive procedures, including epiretinal membrane peeling [5,6], internal limiting membrane (ILM) peeling [7], and silicone oil tamponade [8]. However, these surgical procedures do not always result in favorable outcomes.
It has been reported that ILM can be peeled by the intraocular pics forceps under balanced salt solution (BSS) with staining agent. Because ILM is thin and transparent, the poor visibility makes it hard to identify the border and range of ILM peeling  under BSS in PPV by naked eyesand lead to incomplete peeling. A variety of specially applied staining agents, such as, indocyanine green (ICG), triamcinolone acetonide (TA), trypan blue (TB) and brilliant blue G (BBG) have been used to facilitate the identification of ILM peeling in previous studies [9] by increasing the contrast between ILM and the surrounding tissue. Clinical and experimental reports have suggested that intravitreal injections of ICG [10] and TB [11] can cause retinal damage, such as high rate of postoperative RPE atrophic changes [12], decreasing mitochondrial enzyme activity [13], and retinal damage [14].
A report concluded that BBG is a good candidate dye for ILM peeling since it has low toxicity, high staining ability, and ease of handling [15]. BBG does not affect the retinal structure and function [15-17], and has neuroprotective properties against photoreceptor cell death[18]. Therefore, most retinal surgeons prefer BBG for vital staining [19,20].
BBG-assisted ILM peeling provides excellent anatomic and visual results in surgery compared with other stain dyes [21]. BBG can provide marked enhancement of contrast at vitreoretinal interface due to its superior staining properties [22].However, even stained by BBG, it’s difficult to grasp the ILM effectively with the intraocular tweezers due to the movement of the detached retina in the macular; and it’s hard to peel the ILM by sheet despite the ILM is grasped. Consequently, repeated peeling of ILM would cause high risk for the damage of the nerve fibers in the macular area.
The application of perfluorocarbon liquids (PFCL) has been well acclaimed in vitreoretinal surgery. Its unique physical properties make it an ideal intraoperative tool to improve the efficiency and safety of surgical procedures in complicated cases. The main functions of PFCL in vitreoretinal surgery include relocating and fixing the detached retina, displacing the subretinal and subchoroidal to fluid anteriorly [23], revealing proliferative vitreous retinopathy (PVR) for further maneuvers [24], protecting the macula from exposure to chemicals with potential toxicity [25-27], assisting the removal of foreign body [28], and perfluorocarbon-perfused vitrectomy [29].
In order to control the movement of the detached retina, and make it to the original anatomical position, we modified the procedure by taking advantage of the gravity of PFCL to fix and relocate the detached retina, thus improved the efficacy and shortened the time of the ILM sheet. Here, we described in details a novel technique to demonstrate the applicability of using PFCL- and BBG-assisted technique for peeling of ILM during vitrectomy in eyes with MHRD.
Patients and Methods
Ethics Statement
This study was approved by the institutional review board (IRB) of Affiliated Hospital of Nantong University, Nantong, China. And the methods were carried out in accordance with the approved guidelines. Informed consent was obtained from all patients.

Methods
The possible advantages and risks of the treatment were explained to all patients before surgery, and written informed consent was obtained from the patients.
All surgeries were performed by the same experienced surgeon (Dr. H. C.). Patients were identified by searching the surgical records in the Medical Record Department, Affiliated Hospital of Nantong University, from September 2011 to October 2012. Inclusion criteria included MHRD with high myopia, but without choroidal detachment or trauma. In this study, 18 consecutive patients who had been treated by the novel technique for ILM peeling with BBG- and PFCL-assisted vitreoretinal surgery for MHRD were followed up at least 6 months. All of them had RD at the posterior pole or even the total, owing to MH, including found at preoperative or intraoperative. It included 1 man and 17 women, with 8 right eyes and 10 left eyes.
Mean age at the time of surgery was 59.9 years (range, 46–77 years), mean duration of the disease was 3.48 months (range, 3 days–1 years). Patients were followed up for a mean of 7.6 months (range, 6–11 months) (Table).
Each patient underwent measurement of best-corrected visual acuity with Snellen chart. Patients were assessed at 1 day, 1 week, and half month after vitreoretinal surgery and every month thereafter, follow-up visit if discomfort. At each visit, a complete eye examination was performed, including best-corrected visual acuity, slitlamp retinal examination, intraocular pressure measurement, and optical coherence tomography (OCT) if necessary. Main outcomes included changes in best-corrected visual acuity, retinal reattachment, and the status of the macular hole. All data were tabulated and analyzed with Microsoft Excel (Microsoft, Inc., Redmond, WA).
Surgical Technique
Before the vitreous surgery, lens surgery either lensectomy through the pars plana or phacoemulsification–aspiration (PHACO) was performed on all the phakic eyes (injected sodium hyaluronate into the anterior chamber and capsular bag of the eyes after PHACO, to ensure visual field clear during the next procedure).
Surgery consisted of three-port pars plana vitrectomy with induction of a posterior vitreous detachment by suction with a vitrectomy cutter injected triamcinolone acetonide (Shanghai General Pharmaceutical Co., LTD, Shanghai, China) as required. This procedure could perfectly accomplish the artificial posterior detachment of vitreous. An artificial posterior vitreous detachment was initiated in the eyes of macular hole with limited shallow retinal detachment except for the cases with extensive or complete detachment of the retina. If there existed macular retinal stiffness or
 that indicate residual vitreous cortex and/or premacular membranes present on the surface, posterior vitreous cortex (PVC) and/ or macular epiretinal membranes were removed. In the cases that macular epiretinal membrane was hard to identify, 10 ul of 0.2% BBG (Wells Pharmacy, Florida) in 50% glucose were spread onto the surface of macula (Figure. A) to stain it for 20- 30 seconds and cleaned the dye before removing the macular epiretinal membranes. Additional 10 ul of BBG was added to ILM, so called “sandwich staining”. Before peeling the ILM, residual BBG on the retina surface and under subretina and subretinal fluid with a drainage canula through MH was cleaned as completely as possible. Immediately, PFCL (0.5-1 mL) was gently placed onto the posterior retina to relocate and fix the detached retina, and displace the subretinal fluid anteriorly (Figure.B). Subsequently, the ILM around the macular hole was removed from an area within the major temporal vascular arcades using a vitreous pics forceps (Figure C). After peeling the ILM, we performed an fluid-air exchange with simultaneous removal of PFCL and subretinal fluid through the macular hole. To avoid retinal damage, gentle drainage of the subretinal fluid was conducted with a soft-tipped needle or downgrade infusion pressure. Endophotocoagulation was performed if the macular hole was larger than 1000μm in diameter or peripheral retinal hole. Simultaneous cataract surgery was performed by PHACO (10 eyes) or lensectomy (8 eyes) through the pars plana. Intraocular lenses were inserted before air-fluid exchange in the cases with C3F8 as the extended tamponade. The surgery was concluded by air/fluid exchange and the replacement of intraocular gas with 12% C3F8 or silicone oil. Each patient was asked to maintain a face-down position at least two weeks postoperatively.
Silicone oil was removed at 3 to 6 months after surgery if the retina was totally reattached and the macular hole was reattached by OCT examined. Silicone oil was removed from all operated eyes before the last follow-up visit. The process of membrane removal with BBG- and PFCL-assisted was recorded by video in the surgery (Video).
Figures 
Intraoperative photographs of BBG dye guided ILM peeling under PFCL in MH-RD surgery.
Figure A, BBG was spread onto the surface of macula to stain it. Figure B, PFCL (arrow) was placed onto the posterior retina to relocate and fix the detached retina, and displace the subretinal fluid anteriorly. Figure C, ILM (arrow) around the macular hole was removed from an areausing a vitreous pics forceps.
Results
The surgical outcomes and other clinical characteristics including diagnosis, preoperative and postoperative visual acuity at final visit are listed in Table. All eyes showed high myopia and MHRD with incomplete posterior vitreous detachment, and 1 eye had peripheral retinal break.
Postoperative visual acuity was improved in 18 eyes (100%). Postoperative OCT scanning showed that 13 out of 18 eyes (72.2%) were classified into the type 1 closure group and 5 eyes (27.8%) into the type 2 closure group. All patients were satisfied with the postoperative visual acuity. Recurrent retinal detachment in 1 eye because of not maintain a facedown position after surgery strictly, the retina and macular reattached after second operation at the last follow-up. No patients have developed phthisis bulbi or undue inflammation.
Three cases had complications of iatrogenic peripheral retinal breaks, which were treated by endolaser intraoperatively. Two of the iatrogenic retinal breaks were located anterior to the equator, and one was located posterior to the equator. All of the iatrogenic retinal breaks were very small. Three eyes with artificial retinal breaks to strip the subretinal membranes. Two cases had high intraocular pressure after 2 months, and treated with travoprost 0.004% (Alcon Laboratories, INC. Fort Worth, TX 76134 USA) (Table). No eye experienced subretinal PFCL passage. Any acute toxicity induced by BBG injection, such as corneal edema, severe retinal edema, and severe intraocular inflammation, was not observed.
Discussion
The macular and retina would fail to reattach after removing the silicone oil if ILM, posterior vitreous cortex and/or macular epiretinal membranes (ERM) are not sufficiently peeled, in vitrectomy for MHRD [8,30,31]. Several investigators have confirmed the efficacy of PPV with removal of the ERM as a treatment for MHRD, based on a hypothesis that tangential traction exerted by the ILM and/or ERM contributes to MH related to detachment [32,33]. The retinal reattachment rate in MHRD was significantly higher when ERM removal was complete than when there was residual ERM (P = 0.005) [34]. Incomplete removal of ERM was considered the most likely factor of the low success rate and the reopened MH [35,36]. Several studies have described the efficacy of surgical technique consisting of PPV combined with ILM peeling for the initial treatment of MHRD and reported a success rate ranging was between 69% and 93.8% [37-39].
Previous stripping ILM and/or ERM were difficult in the presence of a detached retina. ILM and ERM are thin, translucent, so that it was very difficult to identify. It became relative easy when dyes stained, but hard to peel the ILM or ERM by sheet and time-consuming owing to active detached retina. However, PFCL can flatten the movement of the detached retina, make its restore to the original anatomical position, with the help of the gravity of the PFCL to fix and relocate the detached retina. We can peel the ILM and/or ERM effectively and completely. Therefore, this study selected BBG-and PFCLassisted technique for peeling of ILM during vitrectomy in eyes with MHRD.
BBG emerged as an optimum dye which selectively stains the ILM. Studies on rats [36] and monkeys [15] demonstrated that BBG was less toxic to the retina [15,17], although high concentrations or long exposures to BBG can damage the RGCs in vitro [40]. No adverse effects were observed postoperatively in the study on the patients [16]. In the present study, we used a low dose of BBG(0.2%) to selectively stain the ILM safely and easily. What’s more, BBG has been reported to be cytoprotective to retinal neuronal cells [18].
It is controversial that the laser photocoagulation (LP) in the management strategy for the repair of MHRD. Posterior staphyloma and atrophy of the RPE are often considered as the causes of reducing adherence of the retina to the choroid and failure to close or reopening of the MH [35]. Studies have reported that laser treatment helps seal off the MH [41,42]. However, it is uncertain whether LP improves the success rate of the operation in MHRD. The potential side effects are destruction of viable retinal tissue and subsequent enlargement of the laser scar. Scholda et al. [43] remarked that LP destroys photoreceptors around the MH even if applied with low energy. Kwok et al. [44]observed that the LP might not necessarily affect anatomy and visual outcome and reported no statistically significant difference was found in terms of visual ( P = 0.15) or anatomical outcomes between the group treated with PPV, gas tamponade, and laser (contiguous argon green endolaser over the retinal edge of the MH) and the group treated with PPV and gas tamponade alone. We don’t use LP around the macula hole intraoperatively, unless the hole is too large or failed primary vitrectomy with ILM and/or ERM peeling.
The type of vitreous substitute (silicone oil or gas) for endotamponade is still controversial. The advantages of silicone oil over gas are that the tamponade can be extended long beyond the duration of gas tamponade, which may lead to better retinal reattachment and faster rehabilitation. We insisted on injecting gas in the eyes of MHRD with fresh, small hole and well activity of the retina after ILM peeling. As for the long duration of MHRD, thin and extension of the retina, excessive axial elongation of the globe (30mm or more), or the one-eyed, we selected silicone oil as the vitreous substitute.
Important limitations in our study were difficulty reaching a general conclusion due to a small sample of patients. Since late recurrence is a trait common to retinal detachment due to macular hole, relatively short follow-up of the patients may be  another limitation. Despite all these limitations, a quite favorable result was procured from this small pilot study. The results suggest that the approach of BBG stained under the PFCL to peel the ILM could be an option in treating retinal detachment due to macular hole. It may allow the surgeon to peel the ILM and ERM more comfortably and completely, especially to beginning retinal surgeons who still are not comfortable peeling the ILM on a detached retina.
Disclosures
Financial support: No financial support was received for this submission.
Conflict of interest: None of the authors has conflict of interest with this submission.

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