Dr. Kshitiz Kumar, K13309, Dr. Pallavi Raj
Lamellar macular hole (LMH) was first described by Gass1 in 1975 as an abortive process of full thickness macular hole formation that resulted from cystoid macular edema. In contrast, macular pseudoholes (MPHs) were attributable to centripetal contraction of the epiretinal membrane (ERM).2 Michalewski et al3 used SD-OCT to demonstrate that MPH may progress to LMH, and because it is an advanced stage of the same non–full-thickness macular disorder, progression of ERM may be the cause of both MPH and LMH. Chen et al4 hypothesized that both entities may be different manifestations of the same disease. The ERM has been shown to coexist in most of cases with LMH.5
Currently, vitrectomy for LMH remains controversial.6–10 Although the natural prognosis for idiopathic LMH is usually good,11 some patients exhibit a visual acuity decrease that may be amenable to surgical treatment. Because LMH is usually accompanied by typical
ERM, surgical treatment regularly includes ERM removal and internal limiting membrane (ILM) peeling with or without gas tamponade which we term as “Double Membrane Peeling” technique.
LMH is frequently accompanied by ERM containing macular pigment, and the ERM appearing to originate from inside the LMH. Because the degree of this migration is on a case-by-case basis, a dehiscence of inner from outer retina is accompanied by a translucent ERM (posterior hyaloid membrane) alone, but not an ERM with macular pigment, in some cases with LMH. DMP technique can be routinely performed for cases containing translucent ERM. Shiraga et.al12 described a modified technique which we labelled as “Inverted ERM” technique for LMH cases with ERM having macular pigments. The aim of the current study was to compare “Inverted ERM” technique for LMH with ERM containing macular pigments with the routine DMP technique for cases of LMH with translucent ERM.
Materials & Methods
This was a retrospective, interventional case series study. Between July 2013 and November 2016, we examined 12 eyes of consecutive patients with LMH and ERM. All subjects had noted visual acuity loss and/or distorted vision and agreed to undergo 23-gauge microincision vitrectomy. Before the surgery, all patients received an explanation of the purpose of the study and the surgical procedure, including the possibility of the use of a new surgical technique, after which they provided written informed consent. This study was approved by the Institutional Review Board
In all patients, before the surgery, we used SD-OCT to determine if there was splitting of the inner and outer foveal layers, the absence of a full thickness defect, and the presence of irregular foveal contour which is the currently established definition for LMH.13
If epiretinal tissue containing macular pigment was detected during the removal of the posterior hyaloid, we then performed Inverted ERM procedure, else routine DMP procedure was performed.
Best-corrected visual acuity (BCVA) measurement, OCT examination using SD-OCT (Cirrus; Carl Zeiss Meditec, Inc., Dublin, CA) and slit-lamp fundus examinations using a 90-diopter lens were performed before and at 1, 2, 4, and 12 weeks, and then every 3 months after the initial surgery. The SD-OCT reader (K.K) evaluated the inner segment/outer segment (IS/OS) junction line as reconstructed or restored when continuity of the IS/OS line was observed at the fovea after surgery. Moreover, the SD-OCT reader also classified the foveal contour into three categories (regular, irregular, and lamellar defect).
Double Membrane Peeling surgical technique
All cases underwent 23-gauge, transconjunctival, sutureless microincision vitrectomy. All surgeries were performed by a single surgeon (KK). Cataract surgery was performed simultaneously in patients older than 50 years. After core vitrectomy, triamcinolone acetonide (TA) was injected into the vitreous cavity to determine if posterior vitreous detachment had occurred. For cases without posterior vitreous detachment, vitreous cutter switched to the vacuum mode was used to induce posterior vitreous detachment. The residual TA particles would stain the vitreoretinal interface along with ERM on the macula. This ensured complete identification and peeling of ERM with 23G ILM forceps (Grieshaber Revolution DSP). After ERM removal, the ILM was stained using Brilliant Blue G (BBG), 0.2 mL with a concentration of 0.25 mg/mL, 0.025% (Brilliant Peel; Geuder, Heidelberg, Germany) on the macula under air conditions for 2 minutes. ILM was peeled easily and safely for about two disc diameter size in the same fashion. Peripheral retinal indentation was done to check for any retinal breaks.
Inverted ERM Technique
All the initial steps were similar to the above procedure till removal of posterior hyaloid. Residual TA particles were removed to identify ERM with macular pigments. After that, ERM with macular pigment was centripetally peeled off from the retina using a microforceps,
with the ERM then left attached to the edge of the LMH. In some cases, a peripheral lucent part of the peeled ERM, which did not contain any macular pigment, was trimmed using the vitreous cutter. As a consequence, only ERM tissues that contained macular pigment remained and surrounded the LMH. The ERM tissues were gently massaged centripetally over the LMH using a back flush instrument with a brush needle so that the LMH was covered with the inverted ERM pieces. Next, brilliant blue–assisted ILM peeling was performed around the LMH in a circumferential manner. During the ILM peeling, the ERM tissues over the LMH were left untouched. At the end of surgery, air–fluid exchange was performed. After surgery, patients maintained a facedown position for 24 hours to 48 hours.
Data Analysis
Continuous variables are represented as mean ± SD. Paired t test/ Wilcoxon signed rank test was used to compare the pre operative and post operative values of visual acuity and central retinal thickness in the same group. Comparision between groups was done using independent t test/Mann-Whitney U test. All statistical analyses were performed using SPSS for Windows, Version 17.0 (SPSS, Inc., Chicago, IL). P≤0.05 was considered to be statistically significant.
Results
In the Inverted ERM surgery group, mean patient age at the time of surgery was 63.33±3.01 years with 1:1 sex ratio. The mean follow-up period was 7.08±0.74 months.
In the DMP surgery group, mean patient age at the time of surgery was 62.33± 2.16 years with 1:2 (M:F) sex ratio. The mean follow-up duration was 6.17±0.73 months.
Functional Results
The mean BCVA improved significantly from 0.62± 0.05 logMAR preoperatively to 0.13± 0.08 logMAR with Inverted ERM peeling technique (p<0.001; Wilcoxon test) and in DMP group from 0.63 ± 0.36 logMAR preoperatively to 0.51± 0.33 postoperatively logMAR (p=0.02; Wilcoxon test). Visual recovery gain was more in Group A compared to Group B (p=0.02; Mann-Whitney U test).
Microstructural Results
The mean central retinal thickness (CRT) recovered from 105.83±22.27 μm before surgery to 227.22 ±42.38 at the final visit after surgery (P<0.001; paired t-test) in the Inverted ERM surgery group. Whereas in the DMP surgery group, the mean central retinal thickness (CRT) changed from 91.66 ± 38.46 μm before surgery to 160.83±79.68 μm (p=0.03; paired t-test). There was no significant difference in post – operative CRT between the groups (p=0.4364; Mann-Whitney U test).
Regular recovery of the foveal contour occurred in 6 out of six eyes (100%) operated by Inverted ERM technique, whereas the recovery was regular in 2 eyes (33.33%), irregular in 3 eyes (50%) and persistent lamellar defect was seen in 1out of 6 eyes (16.66%) operated by DMP technique.
Early after surgery, OCT showed a hyper-reflective tissue infilling of the dehiscence space that had been seen before the surgery between the inner and outer retina by the Inverted ERM technique. Subsequently, the foveal configuration seemed to be recovering to the normal state once again. No such morphological sequence was observed in the DMP group.
The SD-OCT results showed that the defect of the IS/OS junction line before surgery was found in one eye in the Inverted ERM group with restoration of continuity after surgery, whereas 3 eyes had disrupted IS/OS in the DMP group which did not restore in continuity by the time of the final visit after the surgery. Also in DMP technique group one eye with pre op continuous IS/OS showed paradoxical disruption post – surgery at six months. No intraoperative or postoperative complication was observed in the present study. In addition, neither retinal detachment nor macular hole was observed after the surgery.
Discussion
In past reports on visual outcomes of regular vitrectomy, which included ILM peeling alone without embedding ERM into defect, LMH eyes, visual improvement was observed in most of the patients. Michalewska et al6 reported finding visual improvement of 2 or more Snellen lines in 92% of the patients examined. Garretson et al10 also reported visual improvement in 93% of the patients. Whereas in our study using DMP technique visual gain was not statistically significant.
The visual acuity improvement in the Inverted ERM group was similar to the study by Shiraga12 et.al although numbers in our study was small compared to them.
Regarding the anatomical results, Eagler et al9 reported that 2 of 10 patients had total foveal recovery, whereas 4 had irregular recovery and 4 had a persistent lamellar defect. Michalewska et al6 presented details on the postoperative foveal morphology and reported complete normalization in 50% of the patients, whereas 21% had an irregular contour, 15% had a defect similar to MPH, and 8% exhibited a lamellar defect. In the DMP group of our study, 50%(3 eyes) had irregular foveal morphology and one eye showed persistent lamellar defect.
In the Inverted ERM group, restoration of normal foveal morphology was seen in all 6 eyes operated by this technique. In the study by Shiraga et.al12 using this modified techniquefound that 75% of the patients had a regular contour, whereas 20% had an irregular contour and 5% had a lamellar defect. This foveal contour recovery may be due to the embedding of the epiretinal tissues containing macular pigment in the patients with LMH as proposed by them.
Michalewska et.al.6 reported that IS/OS defects recovered in 6 of 8 eyes using conventional technique. In our study using DMP technique, 3 eyes which had disrupted IS/OS line, restoration of line was not achieved. As they mentioned in their study, the regeneration of the IS/OS junction that is seen in SD-OCT may be caused by gliosis. It has been reported that swelling of the glial cells may possibly move the photoreceptors, with these new positions then making it possible to recover visual function.14 In the inverted ERM group, one patient which had disrupted IS/OS full restoration was seen following surgery. In the study by Shiraga et.al,12 7 of 8 eyes in which SD-OCT showed photoreceptor defects before the surgery, the IS/OS junction lines recovered.
Michalewska et al6 concluded that intraocular gas tamponade was not a crucial step in achieving morphologic and visual success in patients with LMH. However, intraocular gas tamponade and face-down positioning for 24 hours to 48 hours after surgery may be necessary to ensure the placement of the inverted epiretinal tissue with the macular pigment inside the LMH.
In the modified technique described by Shiraga et al.6 which we termed Inverted ERM technique, the following theory was proposed by them for advantages inserting ERM tissue into the defect. The epiretinal tissues embedded inside LMH may contain not only macular pigment but also glial cells. Shortly after the surgery in our study patients, OCT demonstrated that there was a hyperreflective mass in the inner retina , with this macular configuration tending to recover the regular foveal contour over time. Therefore, glial cells may play a role in this morphologic normalization, which seems to have a similar mechanism to that seen for the occlusion process in full thickness macular holes. Macular pigment may be able to protect against age related macular degeneration because of its capacity to absorb blue light and scavenge free radicals.15 For this reason, surgeries in which the macular pigment is placed back inside the LMH may be suitable for relatively older aged patients.
In conclusion, although our study was limited by the small number of patients, the short follow-up periods, and the lack of comparisons with regular vitreous surgery patients, new surgical procedure (Inverted ERM technique) may be an effective method. However, a large randomized comparative study will need to be undertaken to definitively determine whether this new surgical technique is functionally and morphologically superior to the regular surgery methodology that includes ERM and ILM peeling (DMP technique) in the LMH eyes with ERM containing macular pigment.
References
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