Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Use of Epimacular Amniotic Membrane Graft in Cases of Recurrent Retinal Detachment Due to Failure of Myopic Macular Hole Closure

Hossam M. Moharram, MD; M. Tarek Moustafa, MD; Hassan A. Mortada, MD; Mohamed Farouk Abdelkader, MD

Abstract

BACKGROUND AND OBJECTIVE:

To study the anatomical and functional outcomes of using epimacular amniotic membrane graft (AMG) to close myopic macular holes (MMHs) in patients with recurrent retinal detachment (RD).

PATIENTS AND METHODS:

Fourteen patients with recurrent MMH-RD were enrolled in a single-arm, prospective study. Pars plana vitrectomy with peeling of any residual internal limiting membrane, preserved AMG was placed over the macular hole (MH) after air-fluid exchange, all patient left on 16% of C2F6.

RESULTS:

Fourteen patients (11 females and three males) with an average age of 58.7 years were included; follow-up was 6 months. Thirteen patients (93%) showed retinal reattachment and closure of the hole confirmed by optical coherent tomography. The mean logMAR of best-corrected visual acuity improved to 1.38 compared to 2.2 preoperatively (P < .002, paired t-test), with no serious intraoperative or postoperative complications.

CONCLUSION:

Epimacular AMG for MMH-RD is a safe and effective treatment for closure of myopic MHs.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:101–108.]

Abstract

BACKGROUND AND OBJECTIVE:

To study the anatomical and functional outcomes of using epimacular amniotic membrane graft (AMG) to close myopic macular holes (MMHs) in patients with recurrent retinal detachment (RD).

PATIENTS AND METHODS:

Fourteen patients with recurrent MMH-RD were enrolled in a single-arm, prospective study. Pars plana vitrectomy with peeling of any residual internal limiting membrane, preserved AMG was placed over the macular hole (MH) after air-fluid exchange, all patient left on 16% of C2F6.

RESULTS:

Fourteen patients (11 females and three males) with an average age of 58.7 years were included; follow-up was 6 months. Thirteen patients (93%) showed retinal reattachment and closure of the hole confirmed by optical coherent tomography. The mean logMAR of best-corrected visual acuity improved to 1.38 compared to 2.2 preoperatively (P < .002, paired t-test), with no serious intraoperative or postoperative complications.

CONCLUSION:

Epimacular AMG for MMH-RD is a safe and effective treatment for closure of myopic MHs.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:101–108.]

Introduction

Myopic macular hole (MMH) is a sight-threatening complication of high myopia,1,2 where surgical repair for MMH associated with retinal detachment (MMH-RD) remains a challenge with limited success rates.3,4 The mechanisms of developing MMH in highly myopic eyes are thought to be due to an anteroposterior and/or tangential traction of epiretinal membrane (ERM), posterior staphyloma (PS), retinal pigment epithelium (RPE) and choroidal atrophy, and stiffened internal limiting membrane (ILM).5–8

Reported surgical techniques for such cases include conventional pars plana vitrectomy (PPV) using gas or silicone oil tamponade,9,10 including ILM peeling,11,12 inverted ILM flap,13–16 macular buckle,17 scleral infoldings,18 autologous blood,19 using lens capsule over the hole,20,21 and retinal autograft.22,23

Amniotic membrane (AM) is the avascular, low immunogenic, innermost layer of the human placenta. Several factors that promote healing and act as anti-inflammatory agents have been identified in the amniotic membrane epithelium and stroma such as: elastin, collagen, hyaluronic acid, TGF-alpha, perlecan hydrated proteoglycans, and glycoproteins,24–26 thus acting as a scaffold for cell proliferation.27

The aim of this study is to determine the efficacy of using epimacular AM graft (AMG) to close macular holes (MHs) in highly myopic eyes with recurrent MMH-RD.

Patients and Methods

This is a prospective, interventional case series study done at the vitreoretinal unit of the ophthalmology department, Minia University Hospital, between February 2018 and May 2019.

The vitreoretinal unit of the ophthalmology department of Minia University is a tertiary referral center for most of cases of complicated retinal surgery in Upper Egypt. The study was approved by the Faculty of Medicine, Research Ethical Committee, Minia University. This study was registered on the Clinicaltrials.gov public registry (No. NCT03528122), with an actual study start date in February 2018. A written informed consent about the benefits and risks of surgery was obtained from all patients. The study adhered to the tenets of Declaration of Helsinki.

Preoperatively, patients' records of previous retinal surgeries were collected, and all patients were subjected to full ophthalmic examination including history taking, best-corrected visual acuity (BCVA), slit-lamp examination, intraocular pressure (IOP) by Goldmann applanation, indirect ophthalmoscopy, fundus slit-lamp biomicroscopy using a 90-diopter (D) Volk lens (Volk Optical, Mentor, OH), and B-scan. Optical coherence tomography (OCT) was done preoperatively if possible.

Fourteen eyes of 14 patients with recurrent MMH-RD after previous 23-gauge PPV with ILM peeling were enrolled in this study.

The exclusion criteria included patients with visual acuity (VA) less than hand motion with good light perception, glaucoma, and significant corneal opacities that could hinder good visualization of the posterior segment; patients with any other retinal pathology that may affect the postoperative VA, such as retinal vascular occlusions and maculopathies other than MMH; and patients with optic nerve atrophy. Patients with severe proliferative vitreoretinopathy were also excluded from the study.

B-scan (Sonomed E-Z Scan AB5500; Sonomed Escalon, New Hyde Park, NY) was performed in all patients to record staphyloma presence and measure the axial length (AL).

Surgical Technique

Twenty-three-gauge PPV was done to insure removal of any remnant of vitreous. ILM was stained by Brilliant Blue G (ILM-Blue; DORC International, Zuidland, The Netherlands), to make sure that the previously peeled ILM from previous surgeries extended to the vascular arcades. Any ERMs were peeled. Phacoemulsification with single-piece acrylic IOL was combined with vitrectomy in eyes with cataract. Surgeries were done by the same experienced surgeons (HM and MF) (See video below).

Fluid-air exchange was done through the MH until the retina was flat and a minimal amount of fluid was left over the retinal surface. The closure valve of the 23-gauge cannula of the trocar system was removed to facilitate entry of AMG, which was fashioned to be double the size of the hole. AMG was stained with Brilliant Blue G for better visualization and grasped gently using serrated forceps (Figure 1A) and placed over the fluid puddle with its epithelial side facing the vitreous cavity and stromal side resting on the edges of MH. The 23-gauge cannula was recapped by the closure valve, fluid-air exchange was then completed by passive aspiration of the backflush needle over the optic disc, and the AMG was properly positioned over the MMH by the soft-tip needle (Figures 1B and 1C). The retinal periphery was thoroughly examined helped by scleral indentation and any break was treated by diode laser photocoagulation (OcuLight 810 nm; Iridex, Mountain View, CA). All patients were left on 16% of C2F6 and were asked to maintain face-down position for 1 week.

(A) Image showing handling and introduction of amniotic membrane graft (AMG) inside the vitreous cavity. (B) Showing backflush needle completing fluid-air exchange nearby the AMG. (C) Showing the final positioning of the membrane over the macular hole.

Figure 1.

(A) Image showing handling and introduction of amniotic membrane graft (AMG) inside the vitreous cavity. (B) Showing backflush needle completing fluid-air exchange nearby the AMG. (C) Showing the final positioning of the membrane over the macular hole.

Postoperatively, all patients were examined after 1 day, 1 week, 2 weeks, 1 month, and 3 and 6 months. In each postoperative visit, all patients had a full ophthalmic examination including BCVA, slit-lamp examination, IOP assessment by Goldmann applanation, retinal examination by indirect ophthalmoscopy, and slit-lamp biomicroscopy using the 90 D Volk lens. OCT images were obtained once visualization of the macula was permitted after gas absorption using (RTVue 100; Optovue, Fremont, CA) and Spectralis (Heidelberg Engineering, Heidelberg, Germany) in the first and sixth month postoperatively.

Retinal reattachment with closure of MH by OCT was considered as anatomical success, and improvement in the BCVA by 2 lines or more of Snellen's acuity was considered as functional success.

Statistical Analysis

For statistical analysis, BCVA was converted to logarithm of the minimal angle of resolution (logMAR). Data were analyzed with paired t-test using the GraphPad Prism version 5.00 for Windows (GraphPad Software, San Diego, CA). A P value of less than .05 was considered statistically significant. Quantitative data are shown as mean ± standard deviation (SD), whereas qualitative data are shown as frequency and percentage.

Results

A total of 14 eyes of 14 patients with recurrent MMH-RD after previous 23-gauge PPV with ILM peeling were included in this study. Eleven patients were female (78.6%) and three were male (21.4%). The average age of the patients was 58.7 ± 11 years (range: 32 years to 80 years). The mean of preoperative logMAR VA was 2.2 ± 0.18 (Figure 2), whereas the mean AL measured by B-scan was 29.13 mm ± 1 mm (range: 27 mm to 31 mm). Table 1 shows the clinical data of all patients.

Scatterplot showing the best-corrected visual acuity (BCVA) in logMAR preoperatively and after 6 months in the 14 patients undergoing amniotic membrane graft for repair of myopic macular hole-associated retinal detachment.

Figure 2.

Scatterplot showing the best-corrected visual acuity (BCVA) in logMAR preoperatively and after 6 months in the 14 patients undergoing amniotic membrane graft for repair of myopic macular hole-associated retinal detachment.

Clinical Data of the Patients Undergoing AMG for MMH-RD

Table 1:

Clinical Data of the Patients Undergoing AMG for MMH-RD

A review of patients' previous records showed 12 eyes had previous 23-gauge PPV with ILM peeling and gas tamponade. Two eyes had two previous surgeries in the form of PPV with ILM peeling and gas tamponade during the first surgery and free ILM graft and silicone tamponade during the second surgery. ILM was found peeled in the previous surgery in all patients (100%). Sixteen percent C2F6 gas tamponade was used at the end of the surgery in all patients (100%).

In the sixth month, 13 out of 14 eyes (93%) had sealed MH with complete retinal reattachment. Closure of MH was noted by the end of the first month and was maintained throughout the whole follow-up period of 6 months (Figures 3A–3C and Figures 4A–4C). The mean logMAR of BCVA improved to 1.38 ± 0.5, which was statistically significant (P < .002, paired t-test) (Figure 2), whereas opened MH and recurrence of retinal detachment was seen in one patient (7%) (Table 1).

(A) Preoperative spectral-domain optical coherence tomography (SD-OCT) image showing recurrent retinal detachment (RD) with macular hole (MH). (B) One-month follow-up SD-OCT image of the macular area with sealed myopic MH-associated RD and overlying amniotic membrane graft (AMG) with good apposition to the edges of the MMH (white arrow). (C) Six-month follow-up SD-OCT image of the macular area with maintained sealed MMH and AMG starting to dissolve but still seen in place (white arrow).

Figure 3.

(A) Preoperative spectral-domain optical coherence tomography (SD-OCT) image showing recurrent retinal detachment (RD) with macular hole (MH). (B) One-month follow-up SD-OCT image of the macular area with sealed myopic MH-associated RD and overlying amniotic membrane graft (AMG) with good apposition to the edges of the MMH (white arrow). (C) Six-month follow-up SD-OCT image of the macular area with maintained sealed MMH and AMG starting to dissolve but still seen in place (white arrow).

(A) Preoperative spectral-domain optical coherence tomography (SD-OCT) image showing recurrent retinal detachment (RD) with macular hole (MH). (B) One-month follow-up SD-OCT image of the macular area with myopic MH-associated RD starting to close (black arrow) and overlying amniotic membrane graft (AMG) (white arrow). (C) Six-month follow-up SD-OCT image of the macular area with maintained sealed MMH and still seen edge of the AMG (white arrow).

Figure 4.

(A) Preoperative spectral-domain optical coherence tomography (SD-OCT) image showing recurrent retinal detachment (RD) with macular hole (MH). (B) One-month follow-up SD-OCT image of the macular area with myopic MH-associated RD starting to close (black arrow) and overlying amniotic membrane graft (AMG) (white arrow). (C) Six-month follow-up SD-OCT image of the macular area with maintained sealed MMH and still seen edge of the AMG (white arrow).

No serious intraoperative or postoperative complications occurred in any of the patients. Transient increase of the IOP occurred in three out of 14 patients (21.4%), which was well controlled by antiglaucoma drops of a combination of timolol and dorzolamide (Cosopt; Merk, Kenilworth, NJ) without any further intervention.

Discussion

Surgery for MMH-RD remains a surgical challenge due to multifactorial causes including degenerative macular changes, loss of contrast, long anteroposterior diameter, and presence of PS.3,4 For idiopathic full-thickness MH, the rate of MH reopening was about 7% and was less in patients who received ILM peeling.28 MMH reopening is common,10–12,29,30 even with ILM inverted flap technique.13–16

Many techniques have been used in order to increase the closure rate in refractory and recurrent MMH including: using free ILM patch,31–33 ILM repositioning and autologous blood,19 and retinal autograft.22,23 The idea behind using such techniques was to seal the hole, to prevent abnormal fluid currency at the area of the hole,34 and to allow tissue proliferation to close it.

In this report, we are presenting the first-ever case series using epimacular human preserved AMG to facilitate closure of MMH in recurrent MMH-RD patients. The complete retinal reattachment and MMH closure was seen in 13 out of 14 patients (93%). In order to seal MHs in highly myopic eyes, different kinds of tissues have been used to cover the MH with variable success rates.

Peng et al. showed a 90% closure rate in their case series after using the lens capsule (LC) and autologous blood for persistent MMH-RD,20 which was comparable to our results. Also, our case series showed almost the same improvement in VA (mean logMAR of 1.34 vs. 1.38 in our study); however, we started with less preoperative VA. Using AMG has some advantages over using LC including that amniotic membrane is readily available in the operating room; it is thicker, so it is much easier to handle and position; and there is no need to perform simultaneous phacoemulsification in all patients. As a result, it can be used with pseudophakic and aphakic patients, as well as in young patients with clear crystalline lens.

Chen et al. showed that using multiple free ILM graft insertions resulted in 100% success rates.33 However, in our series, we used only one AMG.

Lai et al. showed 96% closure rate with their technique of ILM repositioning and autologous blood,19 which was comparable to our results, but they did not work on recurrent cases.

Using retinal autograft achieved 66.7% closure rate and the retinal graft was buried under the edge of the MH,23 which was inferior to our results.

In the present study, all patients had a very long AL (29.13 mm ± 1 mm) with PS. Failure of MMH closure and recurrence of RD was seen in one patient who had undergone two previous surgeries, and the AL was 30.2 mm by B-scan. In this patient, AMG was displaced and disappeared from the macular area in the early postoperative period because he was not compliant with the face-down position in the first week, which may suggest the importance of the face-down position to allow good apposition of the epimacular AMG to the edges of the MH.

Still, AMG positioning was quite easy in most of the patients intraoperatively with the help of the highly concave surface of the posterior pole due to the presence of PS, as well as placing the AMG over a small puddle of fluid using the adhesive property of the fluid to attract the AMG out from the forceps. Additionally, the AMG is much thicker than ILM graft, so epimacular AMG is easier in handling and positioning and is resistant to aspiration through the soft-tip needle.

The first use of AM in ophthalmology literature was reported in 1940,35 where the modern preservation methods insured off the shelf and ready-to-use AM obtained after Cesarean section and still retained the original biological properties36,37 with no immunological rejection.38 AM was successfully used in cases with persistent corneal epithelial defects, acute chemical burns, and corneal limbal stem cell deficiency.39,40

In this study, we used preserved AMG fashioned to have a size that is twice the diameter of the hole, as was previously advised with ILM free graft.41 Our hypothesis was inspired by the use of AMG in patients with resistant corneal ulcer, so we considered the MMH as “macular ulcer” and dealt with it the same way we usually deal with persistent corneal ulcer. Placing the AMG over the macular ulcer with its epithelial side facing the vitreous cavity could promote the healing of the underlying ulcer mechanically by acting as a lid to prevent fluid influx into the hole, or physiologically, by direct diffusion of the growth promotion factors which are abundant in the AM stroma.24

Recently, Rizzo et al.42 studied the use of human AM (hAM) as a plug to close MHs and retinal breaks. They reached 100% success rate in their case series, in which only one case was recurrent MMH. The hAM was insinuated under the retinal surface, whereas we used the AMG over the retinal surface and could use only one hand instead of the bimanual technique they used. The loss of contrast in highly myopic eyes with posterior staphyloma and extensive myopic macular chorioretinal atrophy makes it easier and safer for AMG to be inserted over rather than under the retina. Also, any future assumed complications of the maneuver could be corrected and easily accessed.

MH closure is usually associated with postoperative visual recovery.19,20,31–33 In this case series, all patients with successful MMH closure experienced improvement of their BCVA.

Limitations for this study include small sample size, relatively short follow-up period, and a lack of a control group. This is the first case series using epimacular AMG for treatment of recurrent MMH-RD where a larger, randomized, controlled study with longer follow-up period is needed to validate this technique and to better evaluate its safety and effectiveness in different types of MH.

In conclusion, epimacular AMG for MMH-RD is a safe, relatively simple and effective treatment for recurrent cases. It provides high anatomical closure rate and significant VA recovery.

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Clinical Data of the Patients Undergoing AMG for MMH-RD

No. Age/Sex/Eye Axial Length by B-Scan No. of Previous Surgeries Lens Status Preoperative VA Snellen`s (logMAR) Postoperative BCVA at 6 Months Snellen's (logMAR) MH Status at 6 Months by OCT
1 80/F/L 28.4 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
2 57/M/L 29.2 mm 2 Pseudophakia 20/4000 (2.3) 20/100 (0.7) Closed
3 60/M/L 29.7 mm 1 Pseudophakia 20/4000 (2.3) 20/200 (1) Closed
4 65/F/R 27 mm 1 Cataract 20/4000 (2.3) 20/1500 (1.8) Closed
5 60/F/L 28.1 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
6 58/F/R 29.3 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
7 60/F/R 28.2 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
8 55/F/R 30.1 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
9 32/F/L 29 mm 1 Clear phakic 20/4000 (2.3) 20/4000 (2.3) Closed
10 66/F/R 30.2 mm 2 Pseudophakia 20/4000 (2.3) 20/4000 (2.3) Opened; Recurrent RD
11 64/M/L 29 mm 1 Cataract 20/4000 (2.3) 20/1500 (1.8) Closed
12 67/F/L 31 mm 1 Pseudophakia 20/4000 (2.3) 20/400 (1.3) Closed
13 53/F/L 30.4 mm 1 Pseudophakia 20/1500 (1.8) 20/100 (0.7) Closed
14 45/F/L 28.2 mm 1 Clear phakic 20/1500 (1.8) 20/200 (1) Closed
Authors

From Ophthalmology Department, Minia University, Minia, Egypt (HMM, MFA, MTM); and Ophthalmology Department, Cairo University, Giza, Egypt (HAM).

The authors report no relevant financial disclosures.

Address correspondence to M. Tarek Moustafa, MD, Minia University Hospital, Ophthalmology Department, Cournich El Nil, Minia, Egypt; email: mohamedtarek@mu.edu.eg.

Received: July 08, 2019
Accepted: September 10, 2019

10.3928/23258160-20200129-06

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