Idiopathic macular hole (MH) is characterized by a central neurosensory retinal defect that may cause blurred central vision, central scotoma, or metamorphopsia in symptomatic patients.1 Although idiopathic MHs are most commonly unilateral, they occur bilaterally in between 13% and 31% of patients.2–4 The presence of a unilateral MH increases the risk of MH formation in the fellow eye, especially in fellow eyes with a predisposing foveal lesion.1,5
A biomicroscopic classification, which has been described by Gass, is used most widely to evaluate MHs.6 Optical coherence tomography (OCT)-based classification has increased our understanding of the pathogenesis of MH and has led to accurate diagnosis and staging.7,8 In unilateral cases, OCT also allows detailed evaluation of the vitreomacular interface and outer retinal layers in the fellow eye for assessment of the risk of MH formation.8,9
Although there is no consensus on optimal treatment of MH, including face-down positioning after surgery, removal of the internal limiting membrane (ILM) has increased hole closure rates, reported as more than 90% in surgical studies.11–15 Improvement in visual acuity (VA) after successful repair has also been reported. This depends on preoperative and postoperative factors.16 Undoubtedly, photoreceptor restoration, shown on OCT imaging, is the main factor in the recovery of VA after MH surgery.17
In this retrospective study, we report the anatomical and functional results of patients with bilateral idiopathic MH whose surgery involved removal of the ILM without dye assistance, and with 12% to 14% perfluoropropane tamponade and face-down positioning. We also used OCT to evaluate postoperative photoreceptor restoration and compared results from the patients' first MH surgery and surgery in the fellow eye.
Patients and Methods
The medical records of patients with MH who were examined at Istanbul Retina Institute, Istanbul, Turkey, were reviewed retrospectively. Forty-two patients with no diseases limiting VA other than idiopathic bilateral MH and who underwent bilateral MH surgery between January 2007 and April 2016 were included in the present study. Informed consent was obtained from each participant prior to the surgical procedure. The study protocol was approved by the Institutional Review Board of Şişli Memorial Hospital, Istanbul. The study was in accordance with the principles of the Declaration of Helsinki.
All patients received a comprehensive ocular examination, including measurement of best-corrected VA (BCVA) with the Early Treatment Diabetic Retinopathy Study (ETDRS) chart and intraocular pressure (IOP) by applanation tonometer, detailed anterior segment, and fundus examination with slit-lamp biomicroscopy with a 90 diopter noncontact lens before surgery and 1 day, 1 week, 1 month, 3 months, 6 months, and 1 year after surgery, and yearly thereafter. OCT images were obtained using Stratus OCT 3000 (Carl Zeiss, Dublin, CA) between September 2002 and December 2007, and Spectralis HRA+OCT (Heidelberg Engineering, Heidelberg, Germany) between January 2008 and April 2016 before and after surgery, after resorption of the intraocular gas in patients who had had surgery, and at each visit.
OCT images were obtained by a single examiner experienced in performing scans. The 6 mm × 6 mm radial line scan protocol was performed using the Stratus OCT. The macula was screened by taking 49 sections (512 A-scan) at 120 μm intervals within a 20° × 20° rectangular field by Spectralis HRA+OCT. An average of nine images were obtained for each section. Two high-quality horizontal and vertical line scans centered on the fovea were obtained for each eye. One hundred frames were averaged using automatic averaging, and fundus features were saved and tracked automatically to align follow-up scans with preoperative scans. The hole base diameter was measured at the level of the retinal pigment epithelium. The manual calipers provided with the software of the device were used for the measurements. All scans were evaluated by two of the coauthors experienced in OCT interpretation.
MH staging was based on both biomicroscopic examination according to the modified Gass classification6 and OCT examination. Differences between stage 1A and B and stage 2 and 3 MHs were determined by OCT, and diagnosis of a stage 4 MH was based on visualization of a Weiss ring on biomicroscopy. A stage 4 MH of more than 1 year's duration with reduced retinal cyst formation at the edge of the hole was accepted as a chronic MH.10 Stage 1A cases were followed up for at least 1 year and progression to advanced stages was evaluated.
All the surgical procedures were performed under general anesthesia by the same surgeon (MK), and patients underwent standard three-port 20-gauge or 23-gauge pars plana vitrectomy using the Associate 2500 vitrectomy system (DORC, Zuidland, The Netherlands). After removal of the core vitreous, 0.2 mL to 0.3 mL triamcinolone acetonide aqueous suspension (40 mg/mL) was injected into the midvitreous cavity, for visualization of the residual vitreous and the posterior hyaloid membrane if necessary. Induction of posterior vitreous detachment was attempted by active aspiration with a vitreous cutter just anterior to the peripapillary retina if still attached. Subtotal vitrectomy was performed. In cases with coexisting epiretinal membrane (ERM), the ERM was removed.
Then, the ILM was carefully elevated with end-gripping intraocular forceps and peeled in a circumferential manner around the hole. Peeling was started from the parafoveal region, where the ILM was thicker than the other areas. After ILM peeling, 360° of the peripheral retina was examined with scleral depression to confirm the absence of iatrogenic retinal breaks. Complete air-fluid exchange was performed and then gas-air exchange was completed with 12% to 14% perfluoropropane (C3F8). All patients were asked to position face down for about 5 days.
After the surgery, restoration of the photoreceptor layers was defined as reconstruction of the continuous back-reflection line corresponding to the interdigitation zone, ellipsoid zone, and external limiting membrane (ELM) on OCT along two high-quality horizontal and vertical scans centered on the fovea.
Data on sex, age, duration of symptoms, refractive error, IOP, lens status, hole base diameter, dissociated optic nerve fiber layer appearance, interdigitation zone, ellipsoid zone, and ELM impairment, details of surgery, duration of follow-up, and complications were collected from medical records, and data for all 84 eyes were used for statistical analysis. Descriptive statistical methods (mean, standard deviation) were used for characteristics such as age, sex, and BCVA. Measurement values of the groups were compared using the independent-sample t-test or the paired-samples t-test. The McNemar test, Pearson chi-square test, and Fisher's exact test were used for categorical data. Statistical analyses used SPSS version 20.0 (SPSS, Chicago, IL). A P value of less than .05 was considered statistically significant.
Forty-two patients who underwent bilateral MH surgery with a follow-up duration at least 12 months were assessed. Thirty-one patients were female (74%) and 11 were male (26%). In 14 fellow eyes (33%) the MH was detected as an asymptomatic finding during the first eye's examination. Thirty patients (71.4%) had bilateral MH at presentation. Upon initial diagnosis of MH in the first eye, 12 patients had asymptomatic vitreomacular adhesion diagnosed by OCT in the fellow eye. The vitreomacular adhesions progressed to a MH after a mean of 31 months ± 29.7 months (range: 4 months to 99 months). There was a statistically significant difference between the first and fellow eyes in mean symptom duration (P < .001), preoperative VA (P <0 .001), hole stage (P < .001), and hole base diameter (P = .001). Detailed clinical characteristics shown in Table 1. A patient with stage-2 MH in one eye at the initial visit, and stage 1-B MH developed in the fellow eye during the observational period was demonstrated in the Figures 1 and 2.
Preoperative Demographic and Clinical Characteristics of Patients Who UnderwentBilateral Macular Hole Surgery
Spectral-domain optical coherence tomography image from an eye with stage 2 macular hole (A). One month after the surgery, ellipsoid zone and interdigitation zone disruption, as well as external limiting membrane restoration are seen (B). Three months after the surgery, the ellipsoid zone restoration is clearly seen (C). Six months after the surgery, a decrease in interdigitation defect length is demonstrated (D).
Spectral-domain optical coherence tomography (SD-OCT) scan of the patient's fellow eye shows a partial posterior vitreous detachment, vitreofoveal adhesion, and an intraretinal split at the initial visit (A). One month after the first visit, a subtle perpendicular line and an interdigitation zone disruption beneath the fovea are seen (B). Three months after the first visit, a SD-OCT image demonstrates the development of a stage 1B hole (C). One month after the surgery, the interdigitation zone disruption is demonstrated with restoration of the external limiting membrane and ellipsoid zone (D).
Anatomical success was achieved in all patients after a single operation, and no reopening of an initially closed MH was observed during the follow-up period. The mean improvement in VA in the first eye was 4 lines ± 2 lines (range: –3 lines to 8 lines) and in the fellow eye was 2 lines ± 2 lines (range: –1 lines to 6 lines). There was a statistically significant difference between the first and fellow eyes in mean postoperative logMAR VA (P = .048) and line improvement (P = .001). We did not observe any complication, such as retinal detachment or persistent intraocular pressure elevation, except for cataract progression. The detailed postoperative outcomes of patients are shown in Table 2.
Surgical Details and Postoperative Outcomes of Patients
The differences between preoperative VA and postoperative VA at 3 months, 6 months, 1 year, 2 years, 3 years, 4 years, and last follow-up were statistically significant in both groups (all P < .001).There was a statistically significant difference in postoperative VA in the first-operated eyes between 1 month and 3 months (P = .008) and between 1 year and 2 years (P < .001), and in postoperative VA between 6 months and 1 year in the fellow eyes (P = .02). The mean logMAR VA of patients different times, and comparison between groups, is shown in Figure 3.
The mean logMAR best-corrected visual acuity at different postoperative times in first-operated and fellow eyes before and after surgery.
Interpretable OCT images were obtained from only 21 eyes in the first-eye group and 23 eyes in the fellow-eye group at 1 month postoperatively, and thereafter follow-up data were obtained from all examined eyes. There was no statistically significant difference in dissociated optic nerve fiber layer (DONFL) appearance between 3 months postoperatively and 6 months after surgery in either group, and no statistically significant difference was observed during the following visits. No DONFL was detected during 1 year of follow-up in one first and in one fellow eye, and no new DONFL was found 6 months after surgery in any of the eyes.
Restoration of the interdigitation zone was seen in only two eyes in the first-eye group and 11 in the fellow-eye group at 1 postoperative year. There was no statistically significant difference in interdigitation zone disruption between 6 months and 1 year after surgery in the first-eye group (P = .50). No statistically significant difference was found in interdigitation zone disruption in the fellow eyes between 3 months and 6 months after surgery (P = .50) and between 6 months and 1 year after surgery (P = .06). No restoration of the interdigitation zone was seen in any eyes 2 years after surgery. The interdigitation zone disruption rates and comparison between groups is shown in Figure 4.
The rate of interdigitation zone disruption at different postoperative times in first-operated and fellow eyes after surgery.
In the first-eye group, there was a statistically significant difference in ellipsoid zone disruption between 3 months and 6 months after surgery (P = .03), and between 6 months and 1 year after surgery (P = .002), but no statistically significant difference was seen at subsequent visits (all P > .99). In the fellow eyes, a statistically significant difference in ellipsoid zone disruption was found between 3 months and 6 months after surgery (P = .004), no difference was seen at subsequent visits (all P > .99). No restoration of the ellipsoid zone was detected 1 year after surgery in any eyes of either group. The ellipsoid zone disruption rates and comparison between groups is shown in Figure 5.
The rate of ellipsoid zone disruption at different postoperative times in first-operated and fellow eyes after surgery.
An ELM impairment was seen in five of 42 (%) eyes in the first-eye group 3 months after surgery, and restoration of the ELM was detected in three eyes of those eyes 6 months after surgery. In the remainder, the ELM was not restored across 1 year of follow-up. ELM impairment was not detected in any fellow eyes.
Lewis et al. reported that a full-thickness MH (FTMH) developed in 14% of fellow eyes without posterior vitreous detachment and a 17.5-month interval between holes in the first and fellow eyes.2 In another study, a rate of 22.6% asymptomatic vitreomacular adhesion syndrome diagnosed by OCT in the fellow eye was reported, and progression to FTMH in those eyes occurred after a mean of 19.4 months.4 In our study, progression to impending or FTMH was seen in 12 (28.6%) patients' fellow eyes, all of which had an abnormal vitreofoveal interface, similar to previous studies. However, our mean 31-month interval between holes in the first and fellow eyes was longer than in previous studies.
In previous studies of bilateral MH, an initial closure rate between 74% and 94%, depending on different surgical techniques, has been reported.4,18,19 In the present study, primary anatomical closure was achieved in all cases. The higher surgical closure rate may be associated with procedures being done by the same experienced surgeon, using the same surgical procedure in a single center. It is also known that chronic MH has limited anatomical success and functional gain.10,16,20 In our study, there was no case of chronic MH, which may also account its high anatomical success rate. Gupta et al. reported 6% recurrence after cataract surgery,19 and in the study by Chang et al., no patient had a recurrent hole within 3 months after cataract surgery.4 Similar to previous studies, in our study no reopening was observed during follow-up after the initial vitrectomy or after cataract surgery.4,21
Although it was reported that advanced MHs had a worse visual outcome,16 Chang et al. concluded that the stage of the hole (excluding holes with symptoms for more than 1 year) did not seem to affect visual outcome.4 In the present study, the differences between preoperative and postoperative VA were statistically significant in both eyes, similar to a previous study.4 There was a statistically significant difference in mean postoperative logMAR VA between the first and fellow eyes, which is different from the previous study.4 As more than 70% of the eyes in the first-eye group had stage 3 and 4 MH, and the rate of stage 1 and 2 macular hole was more than 70% in the fellow eyes, the difference in postoperative VA may be associated with the difference in hole stage between eyes. In the previous study, all patients with surgical closure gained more than 2 lines of VA,4 whereas in our study, there was a loss of visual acuity in two first eyes and two fellow eyes and no change three first eyes and nine fellow eyes, due to cataract progression.
The relationship between the restoration of the photoreceptor layer and the improvement in VA after successful closure of a MH has been reported in studies using OCT.17,22 It was demonstrated that the retinal layer became restored first at the ELM, followed by the ellipsoid zone and then the interdigitation zone, and a distinct interdigitation zone was first seen 6 months after surgery.17,23 Ellipsoid zone reconstruction was also considered to be a good prognostic factor for visual rehabilitation after MH surgery.22 Furthermore, it was suggested that the MH minimal diameter correlated with ELM restoration and macular hole base diameter with ellipsoid zone restoration.22 We evaluated photoreceptor layers at different postoperative times and compared results between first and fellow eyes, which has never been done in patients with bilateral MH. Similar to previous studies, we demonstrated gradual photoreceptor restoration on OCT images. None of the eyes had a complete restoration of the ellipsoid zone without a complete restoration of the ELM or a complete recovery of the interdigitation zone without a complete recovery of the ellipsoid zone. As no restoration of the ellipsoid zone was detected 1 year after surgery in any eyes, the number of eyes with interdigitation zone impairment decreased through the 2-year follow-up. However, a distinct interdigitation zone was not seen in any first eyes 6 months after surgery, but approximately 10% of the fellow eyes had interdigitation zone restoration 3 months after surgery, which is different from previous studies. Besides better postoperative VA in fellow eyes, no fellow eyes had ELM disruption at any time after the surgery, and the ellipsoid zone and interdigitation zone disruption rates of fellow eyes were lower than in the first eyes. As a result, it can be concluded that the outcomes of MH surgery in fellow eyes are better than in first eyes, perhaps because of a lower photoreceptor impairment rate related to a smaller base diameter and an earlier-stage hole. For this reason, surgical intervention can be recommended in patients with stage 1B hole, especially those whose contralateral eye reveals advanced stage MH.
This study has several strengths. A single surgeon performed the same procedure. The report showed that early detection of the second macular hole leads to fewer OCT changes and better vision. The comparison of visual acuity and restoration of the photoreceptor layers by detailed OCT tracking between the first eyes and the second eyes following MH surgery at baseline and then at subsequent visits after surgery is perhaps the worthiest feature of this study.
In conclusion, as fellow eyes have a higher risk for MH development, careful assessment of fellow eyes may allow detection of an earlier-stage MH with a smaller base diameter and shorter duration of symptoms than the first-operated eye. Although anatomical success can be achieved in both eyes after successful surgery, early detection and treatment of fellow eyes is associated with better postoperative VA related to higher rates of photoreceptor restoration.
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- Lewis ML, Cohen SM, Smiddy WE, Gass JD. Bilaterality of idiopathic macular holes. Graefes Arch Clin Exp Ophthalmol. 1996;234(4):241–245. doi:10.1007/BF00430416 [CrossRef]
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- Gass JD. Reappraisal of biomicroscopic classification of stages of development of a macular hole. Am J Ophthalmol. 1995;119(6):752–759. doi:10.1016/S0002-9394(14)72781-3 [CrossRef]
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- Duker J, Kaiser PK, Binder S, et al. The International Vitreomacular Traction Study Group classification of vitreomacular adhesion, traction, and macular hole. Ophthalmology. 2013;120(12):2611–2619. doi:10.1016/j.ophtha.2013.07.042 [CrossRef]
- Takahashi A, Nagaoka T, Yoshida A. Stage 1-A macular hole: A prospective spectral-domain optical coherence tomography study. Retina. 2011;31(1):127–147. doi:10.1097/IAE.0b013e3181e7997b [CrossRef]
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- Ozdemir H, Karacorlu M, Senturk F, Karacorlu SA, Uysal O. Retinal sensitivity and fixation changes 1 year after triamcinolone acetonide assisted internal limiting membrane peeling for macular hole surgery – a MP-1 microperimetry study. Acta Ophthalmol. 2010;88(6):222–227. doi:10.1111/j.1755-3768.2010.01898.x [CrossRef]
- Hu Z, Xie P, Ding Y, Zheng X, Yuan D, Liu Q. Face-down or no face-down posturing following macular hole surgery: A meta analysis. Acta Ophthalmol. 2016;94(4):326–333. doi:10.1111/aos.12844 [CrossRef]
- Iezzi R, Kapoor KG. No face-down positioning and broad internal limiting membrane peeling in the surgical repair of idiopathic macular holes. Ophthalmology. 2013;120(10):1998–2003. doi:10.1016/j.ophtha.2013.06.001 [CrossRef]
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Preoperative Demographic and Clinical Characteristics of Patients Who UnderwentBilateral Macular Hole Surgery
|First Eye*||Fellow Eye||P Value|
|Age Range (Years)||64.3 ± 6.3 (48 to 76)||66 ± 6 (51 to 80)||.20|
|Symptom Duration (Weeks)||15.4 ± 17.3 (1 to 52)||3.8 ± 8.2 (0 to 48)||< .001|
|BCVA (logMAR)||0.6 ± 0.2 (1.2 to 0.2)||0.4 ± 0.2 (0.8 to 0.1)||< .001|
|BCVA (Snellen)||20/80 (20/320-20/32)||20/50 (20/125-20/25)|
|Refractive Error (Diopter)||0.3 ± 1.3 (−2 to +3)||0.4 ± 1.2 (−1.5 to 3)||.74|
|Intraocular Pressure (mm Hg)||15 + 2.2 (10 to 19)||15.4 + 2.1 (9 to 19)||.34|
|Phakic Lens (%)||38 (90.5%)||38 (90.5%)||> .99|
|Hole Stage (%)**||< .001|
| 1B||-||12 (28.6%)|
| 2||11 (26.2%)||19 (45.2%)|
| 3||24 (57.1%)||10 (23.8%)|
| 4||7 (16.7%)||1 (2.4%)|
|Hole Base Diameter (μm)||642.9 + 282.3 (258 to 1,458)||380.6 + 218.6 (75 to 1,082)||.001|
Surgical Details and Postoperative Outcomes of Patients
|First Eye*||Fellow Eye||P Value|
|Vitrectomy||36 (85.7%)||39 (92.9%)|
|Combined**||6 (14.3%)||3 (7.1%)|
|Follow-Up (Months)||44 ± 30.3 (12 to 111)||29.4 ± 19 (12 to 84)||.10|
|Final BCVA (logMAR)||0.3 ± 0.2 (0.8 to 0.1)||0.2 ± 0.1 (0.6 to 0)||.048|
|Final BCVA (Snellen)||20/40 (20/126-20/25)||20/32 (20/80-20/20)|
|Improvement of BCVA (%)||.001|
| 0 line||3 (7.1%)||9 (21.4%)|
| 1 line||1 (2.4%)||8 (19%)|
| ≥ 2 lines||37 (88.1%)||24 (57.1%)|
|Cataract Surgery (Months)||16 ± 8.8 (5 to 40)||14.4 ± 9.7 (5 to 40)||.55|
|Final Phakic Lens (%)||9 (21.4%)||14 (33.3%)||.22|