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PRESERVATION OF THE FOVEAL FLAP IN MACULAR HOLE SURGERY

Lee, Suhwan, MD; Kim, June-Gone, MD

doi: 10.1097/IAE.0000000000002132
Original Study
Free

Purpose: To investigate the impact of preserving the foveal flap on surgical outcomes of full-thickness macular hole (MH) with foveal flaps.

Methods: We retrospectively reviewed patients with Stages 2 and 3 idiopathic MH, who underwent pars plana vitrectomy by a single surgeon at Asan Medical Center from November 2011 to November 2016. In the study group, we included eyes with MH and a foveal flap on preoperative spectral domain optical coherence tomography and successfully preserved the flap during surgery. The control group included eyes with MH and an operculum in the posterior vitreous plane on preoperative optical coherence tomography. We compared the anatomical and functional surgical outcomes between these groups.

Results: Postoperative mean best-corrected visual acuity at the last visit was 20/25 and 20/33 in the study (9 eyes) and control (23 eyes) groups, respectively. The study group showed a significantly better postoperative best-corrected visual acuity (P < 0.05). Restoration of both the external limiting membrane and ellipsoid zone, as assessed by spectral domain optical coherence tomography, was achieved in 9 (100%) and 15 (65.2%) eyes of the study and control groups, respectively.

Conclusion: Preserving the foveal flap might improve both functional and anatomical outcomes of vitrectomy for MHs with a foveal flap.

Preservation of flaps during vitrectomy in cases of macular hole with a foveal flap might significantly affect functional and anatomical outcomes of surgery. Thus, a saved flap technique with careful induction of posterior vitreous detachment and internal limiting membrane peeling may be used to maintain foveal flaps.

Department of Ophthalmology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.

Reprint requests: June-Gone Kim, MD, Department of Ophthalmology, Asan Medical Center, 88, Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea; e-mail: junekim@amc.seoul.kr

None of the authors has any financial/conflicting interests to disclose.

Idiopathic macular holes (MHs) are full-thickness axial retinal defects in the foveal neurosensory retina and are believed to be one of the vitreoretinal interface disorders that cause central visual loss. In general, there have been two primary hypotheses regarding the pathogenesis of idiopathic full-thickness MH formation through vitreous traction: 1) anteroposterior traction of the vitreous fibers from the vitreous base and 2) tangential traction exerted by the prefoveolar cortical vitreous.1–5 Recently, high-resolution optical coherence tomography (OCT) devices have provided detailed in vivo visualization of the vitreomacular interface and intraretinal structures, leading to a better understanding of the pathogenesis of MH formation associated with vitreofoveal interactions.6–9 Several studies using OCT have suggested that anteroposterior vitreofoveal traction arising from perifoveal posterior vitreous detachment (PVD) plays a critical role in the formation of idiopathic MHs.8–13 The anteroposterior vitreofoveal traction arising from perifoveal PVD causes foveal splitting, resulting in the formation of foveal cysts and finally in that of a full-thickness MH.8–19 Then, a part of the retinal tissue that was separated during the process appears to characteristically attach to the fovea in the form of an open roof or a flap.12–21 The foveal flap accompanies posterior vitreous traction that is caused by the firm attachment of the posterior vitreous membrane. Therefore, as PVD progresses, the foveal flap is separated from the retinal tissue and detached in the form of an operculum.12–21 Histopathological observation of the operculum shows the presence of retinal tissue, implying that the operculum is a part of the retinal tissue that is detached from the foveal flap.22,23 This foveal flap is weakly attached to the upper part of the retina, and strong attachment of the vitreous makes the detachment easier on the occurrence of PVD. Also, during a surgical procedure in which PVD is induced, the foveal flap may detach from the retinal tissue to form an iatrogenic operculum. In this study, we investigated whether it is important to preserve the foveal flap during MH surgery in terms of the anatomical and functional outcomes of the surgery, and we proposed a surgical technique to preserve the foveal flap during the surgery.

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Materials and Methods

Study Design and Patient Selection

A retrospective consecutive chart review of all patients with Stages 2 and 3 full-thickness MHs who underwent pars plana vitrectomy by a single surgeon (J.-G.K.) at Asan Medical Center, Seoul, Korea, from November 2011 to November 2016 was conducted. Among them, the study group included eyes with MH in which the foveal flap was strongly adherent to the posterior hyaloid membrane in preoperative OCT scans and was successfully preserved using the saved foveal flap technique, and the control group included eyes with MH in which the operculum was observed in the posterior vitreous plane in preoperative OCT scans (Figure 1). Patients with a history of retinal detachment, proliferative retinopathy, vitreous hemorrhage, retinal vascular occlusions, uveitis, trauma, optic atrophy, glaucoma, or corneal opacity were excluded from the study. We also excluded all patients with incomplete chart records and an inadequate follow-up period of <12 months. The data collected from patient records included details of patients' age, sex, axial length, preoperative best-corrected visual acuity (BCVA), preoperative minimum diameter of MH, follow-up period, postoperative spectral domain (SD)-OCT findings, and postoperative final BCVA. Later visual outcome after yttrium aluminum garnet laser capsulotomy was included as the final visual outcome when it was decreased from posterior capsular opacity. Optical coherence tomography was performed before and after surgery for all eyes using a commercially available SD-OCT device (Spectralis HRA OCT; Heidelberg Engineering, Heidelberg, Germany), with a macular volume scan acquisition protocol to detect any defect of discontinuity in the macular area and also to assess restoration of the photoreceptor layer integrity in the postoperative period. Best-corrected visual acuity in Snellen values was converted to the logarithm of the minimum angle of resolution (logMAR) for statistical analysis. Patients who were only able to count fingers and detect hand motions were assigned logMAR values of 2.0 and 2.3, respectively. This study was approved by the Institutional Review Board of the Asan Medical Center (2017-0780) and adhered to the tenets of the Declaration of Helsinki. The need for informed consent was waived by the board.

Fig. 1

Fig. 1

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Surgical Technique

In both groups, hybrid 23 to 25-gauge pars plana vitrectomy, internal limiting membrane (ILM) peeling, and endotamponade using perfluoropropane (C3F8) were conducted under general anesthesia. Cataract operation was performed for all phakic eyes.

Fig. 2

Fig. 2

Fig. 3

Fig. 3

To preserve the foveal flap in the study group, we used the saved foveal flap technique, which comprises the following steps (Figures 2 and 3).

  1. The surgery was performed under general anesthesia in all patients using a hybrid 23 to 25-gauge pars plana vitrectomy. The hybrid 23 to 25-gauge vitrectomy system comprises two 23-gauge ports for illumination and cutter and one 25-gauge port for infusion.
  2. After core vitrectomy, the posterior vitreous cortex and posterior hyaloid face were identified using 20% diluted triamcinolone acetonide.
  3. Posterior vitreous detachment was induced using the suction power of a 23-gauge vitrectomy cutter in the optic disk area. The macular area was spared.
  4. Using the same 23-gauge cutter, the posterior hyaloid membrane was cut while sparing and isolating the posterior hyaloid in the macular area.
  5. After staining the posterior pole with indocyanine green, the ILM was grasped with an ILM forceps and peeled off in a circular manner for approximately two disk diameters around the MH. Internal limiting membrane was carefully removed along the tangential plane of the foveal flap together with the isolated posterior hyaloid membrane.
  6. Air–fluid exchange followed by endotamponade was performed.

During the procedure, the foveal flap was observed under the microscope as a tissue with the shape of a crescent or half moon. The surgeon examined the foveal flap under the microscope during the procedure and judged it to be preserved when the original shape was retained without conversion to operculum.

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Main Outcome Measures and Statistical Analysis

We compared the BCVA and photoreceptor layer status observed on SD-OCT images obtained in the postoperative follow-up period between the two groups. We evaluated the reconstruction of the continuous back reflection line corresponding to the ellipsoid zone (EZ) and the external limiting membrane (ELM) to assess the restoration of the photoreceptor layer (Figure 3). Analysis of the imaging was performed by two independent observers (S.L. and J.-G.K.), with a consensus used to resolve disagreements. Statistical analysis was performed using SPSS 22.0 for Windows (SPSS, Inc, Chicago, IL), and a P value ≤0.05 was considered statistically significant.

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Results

The study group included 9 eyes, and the control group included 23 eyes. Patients' characteristics at baseline are summarized in Table 1. The study group comprised 2 men and 7 women with a mean age of 67.2 ± 7.0 years, and the control group comprised 3 men and 20 women with a mean age of 66.4 ± 5.4 years. The preoperative mean visual acuity was 0.7 ± 0.34 logMAR (20/100, Snellen acuity) in the study group and 0.74 ± 0.35 logMAR (20/111, Snellen acuity) in the control group. The mean axial length was 23.7 ± 1.0 mm in the study group and 23.6 ± 1.1 in the control group. There was no eye with an axial length greater than 26.5 mm in both groups. The mean minimum MH diameter was 344.8 ± 109.6 μm in the study group and 346.9 ± 145.3 μm in the control group. The study group comprised 6 (66.7%) Stage 2 and 3 (33.3%) Stage 3 MH cases, and the control group comprised 13 (56.5%) Stage 2 and 10 (43.5%) Stage 3 MH cases. The mean follow-up period was 26.1 ± 10.9 months in the study group and 24.6 ± 13.5 months in the control group. The two groups did not differ significantly in terms of sex, age, preoperative visual acuity, axial length, MH diameter, preoperative MH stage, and mean follow-up period.

Table 1

Table 1

The main outcome results were as follows (Table 2 and 3). In the study group, all eyes showed improvement in BCVA after the surgery, but in the control group, one case did not show improvement in BCVA. Postoperative mean BCVA at the last visit was 0.10 ± 0.87 logMAR (20/25, Snellen acuity) in the study group and 0.22 ± 0.21 logMAR (20/33, Snellen acuity) in the control group. The study group exhibited significantly better BCVA at the last visit than the control group (P = 0.031). Macular hole was closed in all eyes after the surgery in both groups. Restoration of both ELM and EZ, as assessed by SD-OCT, was observed in all eyes of the study group and 15 (65.2%) eyes of the control group at the final visit. In one eyes of the control group, both ELM and EZ could not be recovered, but no such case was observed in the study group. However, this difference was not statistically significant (P = 0.124). Of the 9 and 15 eyes that recovered both ELM and EZ in the study and control groups, 7 (77.8%) and 8 (53.3%) showed recovery of ELM and EZ within 6 months after surgery, respectively.

Table 2

Table 2

Table 3

Table 3

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Discussion

This study examined the effects of preserving foveal flaps on the functional and anatomical prognosis of MH surgery and introduced a technique for preserving such flaps during surgery. To this end, a control group was selected, in which the opercula were clearly visible in the posterior vitreous plane on preoperative SD-OCT scans. We believe that our control group is able to represent the following situations: 1) spontaneous PVD progressed and the foveal flap was lost into the operculum; 2) the iatrogenic operculum formed in the process of PVD induction during macular hole surgery for MH with foveal flap. Neither the MH size nor preoperative visual acuity, which are known to have significant effects on the prognosis of MH surgery,24–26 showed any significant differences between the two groups. The group in which flaps were preserved showed better functional and anatomical results after surgery than the group in which opercula were present. Functionally, the study group exhibited a statistically significant improvement in the postoperative BCVA compared with the control group, and anatomically, the study group showed a tendency toward better and faster, although not statistically significant, restoration of the microstructure of the foveal photoreceptor, namely, ELM and EZ, which is known to be related to a good postoperative prognosis of vision on SD-OCT scans.27–29 In both groups, restoration of the foveal microstructure was observed within 12 months after surgery. In other words, if complete restoration fails within 12 months of surgery, it can be assumed that restoration is difficult to achieve. Therefore, the 12-month follow-up criterion in this study is considered to be clinically valid. This result suggests that even MH of the same size and stage may have different prognosis according to the status of the operculum and the foveal flap. In addition, preservation of the flap without forming an iatrogenic operculum during surgery may have a significant impact on prognosis.

Larsson et al26 studied the prognosis of MH surgery depending on the presence of opercula and reported that the presence of opercula did not have a significant effect on postoperative prognosis. They believed that the very small amount of photoreceptors in the operculum could be the reason. However, that study differs from the present study in terms of research methodology. It compared groups with and without opercula and focused on the operculum; therefore, groups without opercula may have a wider spectrum of MH than our study group. However, the present study compared groups with flaps and opercula based on the preservation of the flap. This might explain the different outcomes between these studies.

The saved foveal flap technique, which we proposed, is considered to be an effective method for improving the success rate of flap preservation. This method preserves the flap by conducting vitrectomy, with minimal traction on the flap and with ILM peeling in the tangential direction of the flap. Currently, we have continued to apply the above technique to all operations of cases with MHs with foveal flaps since the initial attempt (November 2011). We consider that the learning curve would not be steep when the principle of the technique is understood. However, flap preservation using this technique failed in two cases, in which PVD progressed and the operculum was made on the initiation of core vitrectomy. Thereafter, the procedure was progressed as carefully as possible, with lowering of the vacuum parameter to about half to prevent flap loss. In addition, all operations in this study were performed under general anesthesia. When performing the operation under local anesthesia, gentler anesthetic techniques may be needed to prevent losing the flap from an increase in intraocular pressure, deformation of the globe, and possible acute PVD. Therefore, when the flap tissue is weakly attached to the retina and receives stronger traction, more caution is necessary while administering anesthesia and in the early phase of operation.

To facilitate the closure of MHs, various surgical techniques have recently been proposed.30–34 One such example is the inverted ILM flap technique, in which instead of completely removing ILM, MH is covered with an inverted ILM flap to facilitate the healing process.30–32 Through this technique, it is assumed that the inverted ILM facilitates gliosis and functions as a scaffold for tissue proliferation, assisting in the closure of MHs. If the ILM can help in the closure of MHs, we can assume that preserving foveal flaps, which are believed to include more retinal tissues such as Muller cells and cone photoreceptors, and using them to cover the sites of MHs may have important implications in prognosis after MH surgery. Because the preserved foveal flaps can more quickly cover-up defects in the inner retina and function as a scaffold for tissue proliferation, they are believed to be helpful in the faster closure of MHs. During this study, OCT scans of the 9 eyes in the study group were obtained on Day 1 after surgery. Although it was unclear owing to the filled gas, OCT images appeared to show complete restoration of the inner retina integrity. When examining OCT images taken between 1 week and 1 month after the procedure; a tissue with a signal intensity distinct from the surroundings, which seemed to be the saved flap, was found covering the top of the fovea and was observed as a shape linking both sides of the retinal tissue as a bridge (Figure 3). The fast closure of MHs might produce an environment for the photoreceptors to assume new positions in direct proximity to the fovea. Furthermore, it is believed that if some cone photoreceptors considered to remain in the study group are preserved, they can also be helpful for the prognosis of vision. Therefore, this study concludes that in cases with a greater size or amount of foveal flaps, the preservation of flaps may have a greater significance. Future studies should be conducted on methods for quantitatively measuring flap sizes and effects of their preservation on prognosis. In addition, combining the inverted ILM flap technique and preserving the flap might help in obtaining the best anatomical and functional outcomes in case of a large MH with a flap.

This study has the following limitations. It was a retrospective study and involved a small number of cases, which limited the statistical strength of the analysis. And selection bias may have occurred while recruiting the control group. Therefore, prospective comparative studies with a larger cohort of patients will be necessary to assess the importance of preserving the foveal flap. Although preservation of the flap could be identified by the surgeon under the microscope during the procedure, the use of intraoperative OCT in the future may be helpful for making more objective assessments during the entire operation.

In conclusion, preservation of the flap might improve both the functional and anatomical outcomes of vitrectomy for Stage 2 or 3 MHs with foveal flap. Therefore, to improve the prognosis in cases of MHs that present with a foveal flap on OCT scans and are associated with anteroposterior traction arising from perifoveal PVD, we could consider early surgery before the flap becomes detached as an operculum along with PVD. In this hospital, we are attempting to perform the operation for MH with a flap as soon as possible. There had been no case in which the flap was lost as operculum when the operation was performed within 1 to 2 weeks of the diagnosis. The progression from flap to operculum might be affected by several factors, and additional studies on the optimal time of operation will be needed. Also, the saved foveal flap technique was useful for avoiding the formation of iatrogenic operculum during surgery.

Our conclusion suggests that the prevention of additional foveal tissue defects is one of the important factors for achieving the best anatomical and functional outcomes after MH repair.

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References

1. Avila MP, Jalkh AE, Murakami K, et al. Biomicroscopic study of the vitreous in macular breaks. Ophthalmology 1983;90:1277–1283.
2. Kakehashi A, Schepens CL, Trempe CL. Vitreomacular observations. II. Data on the pathogenesis of idiopathic macular breaks. Graefes Arch Clin Exp Ophthalmol 1996;234:425–433.
3. Gass JD. Idiopathic senile macular hole. Its early stages and pathogenesis. Arch Ophthalmol 1988;106:629–639.
4. Gass JD. Reappraisal of biomicroscopic classification of stages of development of a macular hole. Am J Ophthalmol 1995;119:752–759.
5. Johnson RN, Gass JD. Idiopathic macular holes. Observations, stages of formation, and implications for surgical intervention. Ophthalmology 1988;95:917–924.
6. Altaweel M, Ip M. Macular hole: improved understanding of pathogenesis, staging, and management based on optical coherence tomography. Semin Ophthalmol 2003;18:58–66.
7. Ko TH, Fujimoto JG, Duker JS, et al. Comparison of ultrahigh- and standard-resolution optical coherence tomography for imaging macular hole pathology and repair. Ophthalmology 2004;111:2033–2043.
8. Gaudric A, Haouchine B, Massin P, et al. Macular hole formation: new data provided by optical coherence tomography. Arch Ophthalmol 1999;117:744–751.
9. Tanner V, Chauhan DS, Jackson TL, Williamson TH. Optical coherence tomography of the vitreoretinal interface in macular hole formation. Br J Ophthalmol 2001;85:1092–1097.
10. Chauhan DS, Antcliff RJ, Rai PA, et al. Papillofoveal traction in macular hole formation: the role of optical coherence tomography. Arch Ophthalmol 2000;118:32–38.
11. Johnson MW, Van Newkirk MR, Meyer KA. Perifoveal vitreous detachment is the primary pathogenic event in idiopathic macular hole formation. Arch Ophthalmol 2001;119:215–222.
12. Kishi S, Takahashi H. Three-dimensional observations of developing macular holes. Am J Ophthalmol 2000;130:65–75.
13. Haouchine B, Massin P, Gaudric A. Foveal pseudocyst as the first step in macular hole formation: a prospective study by optical coherence tomography. Ophthalmology 2001;108:15–22.
14. Michalewska Z, Michalewski J, Sikorski BL, et al. A study of macular hole formation by serial spectral optical coherence tomography. Clin Exp Ophthalmol 2009;37:373–383.
15. Takahashi A, Nagaoka T, Ishiko S, et al. Foveal anatomic changes in a progressing stage 1 macular hole documented by spectral-domain optical coherence tomography. Ophthalmology 2010;117:806–810.
16. Takahashi A, Yoshida A, Nagaoka T, et al. Macular hole formation in fellow eyes with a perifoveal posterior vitreous detachment of patients with a unilateral macular hole. Am J Ophthalmol 2011;151:981–989.e984.
17. Takezawa M, Toyoda F, Kambara C, et al. Clarifying the mechanism of idiopathic macular hole development in fellow eyes using spectral-domain optical coherence tomography. Clin Ophthalmol 2011;5:101–108.
18. Takahashi A, Yoshida A, Nagaoka T, et al. Idiopathic full-thickness macular holes and the vitreomacular interface: a high-resolution spectral-domain optical coherence tomography study. Am J Ophthalmol 2012;154:881–892.e882.
19. Takahashi A, Nagaoka T, Yoshida A. Enhanced vitreous imaging optical coherence tomography in primary macular holes. Int Ophthalmol 2016;36:355–363.
20. Mizushima T, Uemura A, Sakamoto T. Prefoveolar membrane in macular hole opercula formation. Jpn J Ophthalmol 2004;48:478–485.
21. Hangai M, Ojima Y, Gotoh N, et al. Three-dimensional imaging of macular holes with high-speed optical coherence tomography. Ophthalmology 2007;114:763–773.
22. Ezra E, Munro PM, Charteris DG, et al. Macular hole opercula. Ultrastructural features and clinicopathological correlation. Arch Ophthalmol 1997;115:1381–1387.
23. Ezra E, Fariss RN, Possin DE, et al. Immunocytochemical characterization of macular hole opercula. Arch Ophthalmol 2001;119:223–231.
24. Salter AB, Folgar FA, Weissbrot J, Wald KJ. Macular hole surgery prognostic success rates based on macular hole size. Ophthalmic Surg Lasers Imaging 2012;43:184–189.
25. Kusuhara S, Negi A. Predicting visual outcome following surgery for idiopathic macular holes. Ophthalmologica 2014;231:125–132.
26. Larsson J, Holm K, Lovestam-Adrian M. The presence of an operculum verified by optical coherence tomography and other prognostic factors in macular hole surgery. Acta Ophthalmol Scand 2006;84:301–304.
27. Wakabayashi T, Fujiwara M, Sakaguchi H, et al. Foveal microstructure and visual acuity in surgically closed macular holes: spectral-domain optical coherence tomographic analysis. Ophthalmology 2010;117:1815–1824.
28. Ooka E, Mitamura Y, Baba T, et al. Foveal microstructure on spectral-domain optical coherence tomographic images and visual function after macular hole surgery. Am J Ophthalmol 2011;152:283–290.e281.
29. Itoh Y, Inoue M, Rii T, et al. Significant correlation between visual acuity and recovery of foveal cone microstructures after macular hole surgery. Am J Ophthalmol 2012;153:111–119.e111.
30. Michalewska Z, Michalewski J, Adelman RA, Nawrocki J. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology 2010;117:2018–2025.
31. Kuriyama S, Hayashi H, Jingami Y, et al. Efficacy of inverted internal limiting membrane flap technique for the treatment of macular hole in high myopia. Am J Ophthalmol 2013;156:125–131.e121.
32. Lai CC, Chen YP, Wang NK, et al. Vitrectomy with internal limiting membrane repositioning and autologous blood for macular hole retinal detachment in highly myopic eyes. Ophthalmology 2015;122:1889–1898.
33. Chen SN, Yang CM. Lens capsular flap transplantation in the management of refractory macular hole from multiple etiologies. Retina 2016;36:163–170.
34. Reis R, Ferreira N, Meireles A. Management of stage IV macular holes: when standard surgery fails. Case Rep Ophthalmol 2012;3:240–250.
Keywords:

foveal flap; macular hole; operculum; optical coherence tomography; vitrectomy

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