|Year : 2014 | Volume
| Issue : 1 | Page : 23-27
Evaluation of internal limiting membrane peeling for idiopathic full-thickness macular hole by optical coherence tomography and multifocal electroretinography
Kamal Enam, Amr El-Kannishy
Department of Ophthalmology, Faculty of Medicine, Mansoura Ophthalmology Center, Mansoura University, Mansoura, Egypt
|Date of Submission||01-Dec-2013|
|Date of Acceptance||19-Feb-2014|
|Date of Web Publication||21-Jun-2014|
MD, Mansoura Ophthalmic Center, EL-Gomhouria St, Mansoura University, 35516 Mansoura
Source of Support: None, Conflict of Interest: None
The aim of the study was to evaluate the anatomical and functional success of idiopathic macular hole surgery using optical coherence tomography (OCT) and multifocal electroretinography (mfERG).
The study was designed as a prospective interventional case series.
Patients and methods
Fourteen eyes with idiopathic full-thickness macular hole were treated with pars plana vitrectomy and internal limiting membrane peeling. OCT and mfERG were performed in all patients preoperatively and during a follow-up period of 6 months to elicit anatomical and functional changes of the macula.
OCT images revealed closure of macular holes in all patients after 3 months of follow-up, whereas mfERG showed improvement of retinal responses. These changes were associated with a significant improvement in visual acuity (P = 0.0001).
Pars plana vitrectomy with internal limiting membrane peeling successfully restored the normal architecture of the fovea, with improvement in retinal function.
Keywords: Internal limiting membrane peeling; macular hole; multifocal electroretinography; optical coherence tomography
|How to cite this article:|
Enam K, El-Kannishy A. Evaluation of internal limiting membrane peeling for idiopathic full-thickness macular hole by optical coherence tomography and multifocal electroretinography. J Egypt Ophthalmol Soc 2014;107:23-7
|How to cite this URL:|
Enam K, El-Kannishy A. Evaluation of internal limiting membrane peeling for idiopathic full-thickness macular hole by optical coherence tomography and multifocal electroretinography. J Egypt Ophthalmol Soc [serial online] 2014 [cited 2020 Jul 15];107:23-7. Available from: http://www.jeos.eg.net/text.asp?2014/107/1/23/134938
| Introduction|| |
Idiopathic full-thickness macular hole (FTMH) represents a defect in the fovea. If left untreated, it often leads to severe central visual loss . FTMH has an estimated incidence of 7.8 persons/100 000 population per year . Macular hole surgery, first developed by Kelly and Wendell  in 1991, represents one of the challenging procedures performed by vitreoretinal surgeons .
Four stages of idiopathic macular hole have been described . Randomized controlled clinical trials conducted in 1990 showed that macular hole surgery was effective for stages 2, 3, and 4 ,. Peeling the internal limiting membrane (ILM) of the retina was introduced as an additional maneuver in macular hole surgery to improve anatomical and functional outcomes after surgery . Several observational studies suggested a benefit of peeling the ILM ,. Furthermore, data from two studies undertaken in China and Denmark, which included 49 and 75 patients, respectively, suggested a potential beneficial effect of this operation ,.
The mechanism by which visual function improves after surgery is not understood. Visual function before and after macular hole surgery is generally assessed by visual acuity (VA) measurement ,. However, the VA level represents only a part of the impaired visual function resulting from macular hole development, which includes metamorphopsia, blurred vision, and scotoma. There have been a few methods to evaluate these subjective symptoms. Some researchers used objective methods such as multifocal electroretinography (mfERG) to evaluate macular function .
With optical coherence tomography (OCT), it has become much easier to define and understand the retinal anatomy before and after macular hole surgery. In addition to assessment of postsurgical retinal status, OCT has helped to determine the time frame of resolution to normal retinal anatomy after surgery, and has also helped to explain poor VA in cases where the retina appeared normal in the results of biomicroscopic examination ,,,,.
| Aim|| |
The aim of the study was to evaluate the anatomical and functional success of ILM peeling in eyes with idiopathic FTMH using OCT and mfERG.
| Patients and methods|| |
The present study was designed as a prospective, nonrandomized, interventional case series. The study was approved by the local institutional review board, and the research procedures used in this study followed the tenets of the Declaration of Helsinki. The nature of the procedure was explained to the participants in details, and written informed consents were given by all participants before included in the study.
Patients with idiopathic FTMH were enrolled in this study. Inclusion criteria were stages 2, 3, or 4 macular hole (according to the Gass  classification), symptoms duration of 12 months or less, VA of at least 34 letters using Early Treatment Diabetic Retinopathy Study (ETDRS) VA chart, and intraocular pressure of 22 mmHg or less. Exclusion criteria were aphakia, pseudophakia, apparent cataract (≥stage 2 nuclear and cortical or ≥stage 1 posterior subcapsular; according to the LOCS 3 classification), other posterior segment disease or surgery, and general systemic diseases that could affect vision, such as history of bleeding disorders, cardiovascular accidents, pulmonary embolus, deep venous thrombosis, myocardial infarction, uncompensated coronary artery disease within the past 6 months, major surgery within the past 6 weeks, diabetes mellitus, and uncontrolled hypertension.
Complete ophthalmic examination was performed in all patients. Best-corrected VA was measured using ETDRS VA chart . A thorough slit-lamp examination using a three-mirror contact lens and/or a 90-diopter lens was undertaken. OCT and mfERG were performed for each patient before surgery.
Optical coherence tomography
OCT was performed using Topcon (Topcon Corporation, 75-1, Hasunuma-cho, Itabashi-ku, Tokyo 174-8580 Japan) 3D OCT-1000 Mark II. It scans a cube of 6.0 × 6.0 mm length at a resolution of 512 × 128 with the fixation on the macula. The print out includes the foveal central thickness (FCT) and the thickness map, which is a circle with a diameter of 6 mm centered on the foveola. The map divides the macula into nine ETDRS regions. The cross-sectional scan showed morphological changes before and after treatment. Scans with image quality of at least 55 were used for analysis. Low-quality scans were reacquired.
RETIscan21 Multifocal ERG (version 07/01; Roland Instrument, Dipl.Ing.M.-Willy-Str.11, D-65197 Wiesbaden, Germany.) was used for mfERG recording. The stimulus consisted of 61 hexagons; hexagon number 31 was used for fixation placed centric. The instrument used in the study gives us the opportunity to use many forms of targets. For example, we can use a spot, a cross, rings, and lines. We used two lines; each extended diagonally from one angle of the screen to the opposite one. They crossed at the center of the screen. The advantage of this fixation target is the large size, which is helpful for patients with poor vision to maintain fixation during examination. Each hexagon was stimulated by alternating white and black stimulus on gray background. M-sequence was 1024 elements/reversal. The M-sequence was controlled by 58 binary pseudorandom sequences derived from a family of sequences called Kasami sequences. High stimulus luminance of 120 cd/m 2 was used, which displayed on Cathode Ray Tube (CRT) color monitor 20" size. Eye to screen distance was nearly 310 mm, the field of view was 27°, stimulation consisted of eight cycles, and each cycle lasted for 38.0 s, with total test time of about 5 min. Alteration between black and white stimulation was performed at frame frequency of 60 Hz/s. Distortion factor for hexagons was 4.0, starting at the central hexagon (number 31). The recording procedure was repeated if percentage of artifacts was more than 10.
The pupils of the patient were dilated using tropicamide 0.5% and phenylepherine 10%. Eyes were optically corrected for near vision. Signals picking up were performed through electrodes placed in specific regions of patient's head. The electrodes were active HK-loop electrode, reference, and ground silver-EEG-electrodes. The first one was attached to the lower lid with its thread (loop) touching the globe just below the cornea; the other electrodes were attached to the patient's head (forehead and temple) after cleaning the skin and placing conductive plast (TEN20, Bio-Medical Instruments, Inc. 2387 East 8 Mile Road, Warren, MI 48091-2486, Detroit, USA). The mfERG stimuli location and anatomic areas corresponded roughly as follows: ring 1 to the fovea (R1 = Central 2°), ring 2 to the parafovea (R1 = Central 2-5°), ring 3 to the perifovea (R1 = Central 5-10°), ring 4 to the near periphery (R1=central 10-15°), and ring 5 to the middle periphery (R1 > 15°). The study recorded the mfERG amplitude in the central two rings.
Colocalization of abnormalities was performed objectively by superimposing option in mfERG, where the resulting mfERG figure with the stimulus pattern is overlaid on the central fundus. We divided the posterior segment into five rings.
The patients were arranged to undergo standard pars plana vitrectomy. Central core vitrectomy was performed followed by detachment of the posterior hyaloid using high vacuum of the vitrectomy probe and assisted by intravitreal triamcinolone injection. The peripheral vitreous was then removed with careful inspection of the periphery of the retina. Air-fluid exchange was performed and the macular area was stained with brilliant blue G (Brilliant Peel, Geuder AG, Hertzstrasse 4, 69126 Heidelberg, Germany). Fluid-air exchange and ILM maculorhexis were carried out covering an area of about 2 disc diameters using Eckardt forceps. Two rows of laser were performed 360° at retinal periphery to guard against the occurrence of postoperative retinal detachment. Nonexpansile concentration of sulfur hexafluoride 20% was used to fill the vitreous cavity at the end of the procedure. After surgery, the patients were instructed to keep facedown position for at least 10 h/day for 10 days.
Patients were examined on the first postoperative day for signs of ocular inflammation, changes of intraocular pressure, and retinal stability. Thereafter, they were scheduled for follow-up examination at 1 month interval during the first 3 months and at the end of the sixth month. At these visits, best-corrected VA, complete ophthalmic examination, OCT, and mfERG were performed.
The statistical analysis of the data was performed using Excel program on office 2003 software and statistical package for the social science program (version 16; SPSS Inc., Chicago, Illinois, USA) on Windows 2003.
| Results|| |
Fourteen patients (14 eyes) with stages 2, 3, or 4 FTMH were enrolled. Stage 2 macular hole was present in four (28.6%) patients, whereas stage 3 was present in six (42.9%) patients, and stage 4 in four (28.6%) patients. Thereafter, mean reported macular hole symptoms duration was 7.9 ± 1.7 months (range 5-11 months). In all, 57.1% of the patients were female individuals and 42.9% were male individuals. The average axial length of eyes was 23.1 ± 0.4 mm. Successful macular holes closure was achieved in 70% of eyes at 1 month of the follow-up period. At 3 months of follow-up, all macular holes were closed.
[Figure 1] provides the VA for all patients preoperatively and at 6 months of follow-up. The mean preoperative VA was 53.7 ± 7.3 ETDRS score, whereas the mean VA at the end of follow-up was 76.2 ± 3.8 ETDRS score (P = 0.0001).
Retinal optical coherence tomography
The mean preoperative maximum aperture diameter was 445 ± 45.6 μm, and the mean preoperative maximum base diameter was 892.8 ± 72.5 μm. Twenty percent of macular holes had vitreoretinal traction and 7% had subretinal fluid and intraretinal cysts. Seventy percent of holes achieved closure by 1 month of follow-up and all holes were closed by 3 months of follow-up. [Figure 2] provides the mean FCT for all patients during 6 months of follow-up. There was no statistically significant correlation between the FCT and the VA measurements preoperatively and during follow-up period.
Retinal multifocal electroretinography (foveal and parafoveal rings)
mfERG results at the foveal and the parafoveal rings showed statistically significant changes (P = 0.0001) with respect to the P1 amplitudes at the end of follow-up period [Figure 3]. Statistical analysis demonstrated a significant correlation between mfERG values and VA measurements at the sixth month postoperatively for both foveal (P = 0.028) and parafoveal rings (P = 0.02). There was no correlation between mfERG and VA preoperatively and at 1 and 3 months postoperatively.
| Discussion|| |
ILM peeling was introduced as an additional maneuver in macular hole surgery to improve anatomical and functional outcomes . This study showed that 100% closure of idiopathic macular holes could be achieved if vitreoretinal surgery included ILM peeling. The anatomical success rate of macular hole surgery with ILM peeling in various series varied from 81 to 100% ,,,. Kwok et al.  reported a significantly low anatomical success rate (32%) in the non-ILM peeling group compared with the ILM peeling group (92.3%). In other words, ILM peeling improves the anatomical success of surgery markedly.
The mean VA of patients included in the study significantly improved after surgery. These results were comparable with previously published studies ,,,,. The mechanism by which visual function improves after surgery is not clearly understood. However, the centripetal movement of the previously displaced photoreceptors to its original site as proven by OCT images may be the simplest explanation .
The results of mfERG recorded preoperatively in the studied eyes showed marked decreases in retinal response densities that were not only limited to the fovea, but also involved the parafoveal area. Decreased retinal response densities in the perifoveal area (area 2) seems to reflect perifoveal retinoschisis. The same finding was concluded by previously published studies ,.
The improvement in the retinal response densities after surgery in the foveal area (area 1) appeared to reflect the closure of the macular holes with proliferated glial cells and centripetal displacement of surrounding photoreceptor cells. The improvement in the retinal response density in area 2 is presumably achieved by reattachment of perifoveal retinoschisis.
In this study, the improvement in the VA was not correlated to FCT, but it was correlated to the mfERG values only at 6 months postoperatively. This indicates that the anatomical recovery is not the only decisive factor for the improvement of visual function, and a residual pathology remains despite of the morphological changes.
| Conclusion|| |
This study demonstrates excellent anatomical and functional results after ILM peeling in patients with idiopathic FTMH. This supports the fact that ILM peeling is a settled treatment in patients with idiopathic FTMH.
| Acknowledgements|| |
Conflicts of interest
| References|| |
|1.||Casuso LA, Scott IU, Flynn HWJr, Gass JD, Smiddy WE, Lewis ML, Schiffman J. Long-term follow-up of un-operated macular holes. Ophthalmology 2001; 108:1150-1155. |
|2.|| McCannel CA, Ensminger JL, Diehl NN, Hodge DN. Population-based incidence of macular holes. Ophthalmology 2009; 116:1366-1369. |
|3.|| Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes: results of a pilot study. Arch Ophthalmol 1991; 109:654-659. |
|4.|| Ah-Fat FG, Sharma MC, Majid MA, McGalliard JN, Wong D. Trends in vitreoretinal surgery at a tertiary referral centre: 1987 to 1996. Br J Ophthalmol 1999; 83:385-386. |
|5.|| Gass JD. Idiopathic senile macular hole: its early stages and pathogenesis. Arch Ophthalmol 1988; 106:629-639. |
|6.|| Kim JW, Freeman WR, Azen SP, el-Haig W, Klein DJ, Bailey IL. Prospective randomized trial of vitrectomy or observation for stage 2 macular holes: Vitrectomy for Macular Hole Study Group. Am J Ophthalmol 1996; 121:605-614. |
|7.|| Freeman WR, Azen SP, Kim JW, El-Haig W, Mishell DRIII, Bailey I. Vitrectomy for the treatment of full-thickness stage 3 or 4 macular holes: results of a multicentered randomized clinical trial. The Vitrectomy for Treatment of Macular Hole Study Group. Arch Ophthalmol 1997; 115:11-21. |
|8.|| Eckardt C, Eckardt U, Groos S, Luciano L, Reale E. Removal of the internal limiting membrane in macular holes: clinical and morphological findings (in German). Ophthalmologe 1997; 94:545-551. |
|9.|| Abdelkader E, Lois N. Internal limiting membrane peeling in vitreo-retinal surgery. Surv Ophthalmol 2008; 53:368-396. |
|10.||1Bellerive C, Cinq-Mars B, Louis M, Tardif Y, Giasson M, Francis K, Hébert M. Retinal function assessment of trypan blue versus indocyanine green assisted internal limiting membrane peeling during macular hole surgery. Can J Ophthalmol 2013; 48:104-109. |
|11.||1Kwok AK, Lai TY, Wong VW. Idiopathic macular hole surgery in Chinese patients: a randomized study to compare indocyanine green-assisted internal limiting membrane peeling with no internal limiting membrane peeling. Hong Kong Med J 2005; 11:259-266. |
|12.||1Christensen UC, Krøyer K, Sander B, Larsen M, Henning V, Villumsen J, la Cour M. Value of internal limiting membrane peeling in surgery for idiopathic macular hole stage 2 and 3: a randomised clinical trial. Br J Ophthalmol 2009; 93:1005-1015. |
|13.||1Sjaarda RN, Frank DA, Glaser BM, Thompson JT, Murphy RP. Resolution of an absolute scotoma and improvement of relative scotoma after successful macular hole surgery. Am J Ophthalmol 1993; 116:129-139. |
|14.||1Smiddy WE, Thomley ML, Knighton RW, Feuer WJ. Use of the potential acuity meter and laser interferometer to predict visual acuity after macular hole surgery. Retina 1994; 14:205-209. |
|15.||1Acosta F, Lashkari K, Reynaud X, Jalkh AE, Van de Velde F, Chedid N. Characterization of functional changes in macular holes and cysts. Ophthalmology 1991; 98:1820-1823. |
|16.||1Jumper JM, Gallemore RP, McCuen BWII, Toth CA. Features of macular hole closure in the early postoperative period using optical coherence tomography. Retina 2000; 20:232-237. |
|17.||1Uemoto R, Yamamoto S, Aoki T, Tsukahara I, Yamamoto T, Takeuchi S. Macular configuration determined by optical coherence tomography after idiopathic macular hole surgery with or without internal limiting membrane peeling. Br J Ophthalmol 2002; 86:1240-1242. |
|18.||1Apostolopoulos MN, Koutsandrea CN, Moschos MN, Alonistiotis DA, Papaspyrou AE, Mallias JA, et al. Evaluation of successful macular hole surgery by optical coherence tomography and multifocal electroretinography. Am J Ophthalmol 2002; 134:667-674. |
|19.||1Kitaya N, Hikichi T, Kagokawa H, Takamiya A, Takahashi A, Yoshida A. Irregularity of photoreceptor layer after successful macular hole surgery prevents visual acuity improvement. Am J Ophthalmol 2004; 138:308-310. |
|20.||2Villate N, Lee JE, Venkatraman A, Smiddy WE. Photoreceptor layer features in eyes with closed macular holes: optical coherence tomography findings and correlation with visual outcomes. Am J Ophthalmol 2005; 139:280-289. |
|21.||2Gass JD. Reappraisal of biomicroscopic classification of stages of development of a macular hole. Am J Ophthalmol 1995; 119:752-759. |
|22.||2Vanden Bosch ME, Wall M. Visual acuity scored by the letter-by-letter or probit methods has lower retest variability than the line assignment method. Eye 1997; 11:411-417. |
|23.||2Kwok AK, Li WW, Pang CP, Lai TY, Yam GH, Chan NR, Lam DS. Indocyanine green staining and removal of internal limiting membrane in macular hole surgery: histology and outcome. Am J Ophthalmol 2001; 132:178-183. |
|24.||2Da Mata AP, Burk SE, Riemann CD, Rosa RH Jr, Snyder ME, Petersen MR, Foster RE. Indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for macular hole repair. Ophthalmology 2001; 108:1187-1192. |
|25.||2Slaughter K, Lee IL. Macular hole surgery with and without indocyanine green assistance. Eye 2004; 18:376-378. |
|26.||2Da Mata AP, Burk SE, Foster RE, Riemann CD, Petersen MR, Nehemy Má, Augsburger JJ. Long-term follow-up of indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for idiopathic macular hole repair. Ophthalmology 2004; 111:2246-2253. |
[Figure 1], [Figure 2], [Figure 3]