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Vitrectomy with Internal Limiting Membrane Repositioning and Autologous Blood for Macular Hole Retinal Detachment in Highly Myopic Eyes
Vitrectomy with Internal Limiting Membrane Repositioning and Autologous Blood for Macular Hole Retinal Detachment in Highly Myopic Eyes Chi-Chun Lai, MD,1,2 Yen-Po Chen, MD, PhD,1,2 Nan-Kai Wang, MD, PhD,1,2 Lan-Hsin Chuang, MD,2,3 Laura Liu, MD, PhD,1,2 Kuan-Jen Chen, MD,1,2 Yih-Shiou Hwang, MD, PhD,1,2 Wei-Chi Wu, MD, PhD,1,2 Tun-Lu Chen, MD1,2 Purpose: To investigate the surgical results of macular hole retinal detachment (MHRD) repaired using vitrectomy combined with inverted internal limiting membrane repositioning (ILMR) and autologous blood clot (ABC) in highly myopic eyes. Design: Retrospective, interventional case series. Participants: Twenty-seven cases of MHRD. Methods: Twenty-seven cases of highly myopic eyes with MHRD in 27 patients who underwent a vitrectomy combined with ILMR and ABC and were followed up over 6 months were reviewed. The anatomic outcomes of MHRD were evaluated by fundus examinations and optical coherence tomography. The preoperative and postoperative best-corrected visual acuities (BCVAs) were compared as the functional outcome. Main Outcome Measures: Retinal reattachment, macular hole (MH) closure, and BCVA before and after surgery. Results: In total, women accounted for 85% (23/27) of the MHRD patients. The mean age was 59.110.6 years. The mean axial length was 29.371.92 mm. Type 1 MHRD was present in 9 eyes, and type 2 MHRD was present in 18 eyes. After a single surgery, the retina was attached and the hole was closed in 26 eyes (96%), and 100% retinal attachment was achieved by another vitrectomy for rhegmatogenous retinal detachment that occurred 3 months after the initial surgery. A parafoveal unclosed hole was found in 1 eye (4%) during the followup period, and the patient did not undergo further treatment. Three eyes with a closed hole showed persistent subretinal fluid (SRF) after gas absorption. In 2 of these cases, the fluid absorbed completely during the follow-up period, but 1 eye exhibited persistent SRF, which was resolved progressively during the 12 months of follow-up. The surgery significantly improved the BCVAs {from 1.80.7 logarithm of the minimum angle of resolution units to 1.30.7 logarithm of the minimum angle of resolution units (P ¼ 0.001)} at 3 and 6 months and at the last visit after surgery. Seven patients underwent cataract surgery during the follow-up period. Conclusions: A vitrectomy combined with ILMR and ABC is effective for closing MHs and reattaching the retina and significantly improves the postoperative BCVA in MHRD patients. Ophthalmology 2015;-:1e10 ª 2015 by the American Academy of Ophthalmology. Supplemental video is available at www.aaojournal.org.
Macular hole (MH) retinal detachment (MHRD) is one of the most vision-threatening complications associated with highly myopic eyes, and it is highly prevalent in east Asia.1,2 The mechanisms of MHRD may be related to the tangential traction from the epimacular structure and the inverse traction from the posterior staphyloma. Choroidal and retinal pigment epithelium atrophy also may result in weakened retinal adherence to the posterior pole.3e5 According to the pathologic mechanisms, several surgical methods have been introduced to treat MHRD. They include intraocular gas tamponade, pars plana vitrectomy, macular 2015 by the American Academy of Ophthalmology Published by Elsevier Inc.
buckling, and combination approaches. Among them, vitrectomy and gasefluid exchange with internal limiting membrane (ILM) removal followed by face-down positioning was most popular for the treatment of MHRD.6e19 The retinal reattachment rate ranged from 40% to 90% after vitrectomy and gasefluid exchange, but the hole closure rate was lower; the hole could remain open even if the retina was attached.14e16,20 In addition to the unsatisfying anatomic results of MHRD, remaining in a face-down position for 1 to 2 weeks after vitrectomy and gasefluid exchange is an unpleasant experience for the patient during http://dx.doi.org/10.1016/j.ophtha.2015.05.040 ISSN 0161-6420/15
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Figure 1. The surgical procedure of macular hole retinal detachment repaired by a vitrectomy combined with inverted internal limiting membrane (ILM) repositioning and autologous blood clot in highly myopic eyes. A, B, After a vitrectomy, ILM lifting was assisted by staining with indocyanine green without intentional drainage of the subretinal fluid. The lifted ILM was not detached completely from the retina and remained attached to the edge of the macular hole. C, D, Then, the lifted ILM was inverted and placed into the macular hole. E, The inverted ILM was used to fill the macular hole. F, Then, fresh blood from the patient was injected gently to cover the macula and seal the macular hole.
recovery. Although silicone oil was introduced in the initial surgery to avoid the need for face-down positioning,21 it is necessary to remove the silicone oil afterward, and longterm retinal toxicity cannot be ignored.18,22,23 Increasing the successful rate of retinal attachment and hole closure and decreasing the duration that patients are in a prone position are the main goals of MHRD repair. Recently, an inverted ILM flap was used to close large idiopathic MHs in a small case series of MHs in highly myopic eyes with or without retinal detachment (RD).24,25 In addition, blood from the patient long has been applied in vitreoretinal surgeries, and blood components long have been used to improve the hole closure rate for MH.26e29 The purpose of this study was to determine the efficacy of a modified combination therapy, that is, a vitrectomy with inverted ILM repositioning (ILMR) combined with autologous blood clot (ABC) and gas tamponade in a prone position for 1 day, to treat MHRD in highly myopic eyes.
Methods A retrospective, consecutive chart review of all patients with MHRD who underwent a vitrectomy with ILMR combined with ABC and
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gas tamponade by a single surgeon (C.-C.L.) at Chang Gung Memorial Hospital was conducted. The institutional review board of Chang Gung Memorial Hospital, Taoyuan, Taiwan, approved this retrospective study. This study included only the patients with MHRD in a highly myopic eye (6 diopters or axial length 26.5 mm). Patients with a history of RD or proliferative vitreoretinopathy, any kind of retinal surgery, diabetic retinopathy, vitreous hemorrhage, retinal vascular occlusion, uveitis, trauma, optic atrophy, ocular tumors, glaucoma, corneal opacity, or incomplete chart records were excluded. The patient’s age, gender, ocular history, initial best-corrected visual acuity (BCVA), preoperative and postoperative clinical manifestations, subtypes of MHRD, optical coherence tomography (OCT) results, and final BCVA were collected. The classifications of MHRD were based on the extension of RD as described previously.17 Briefly, a classification of type 1 indicated RD within the macula, type 2 indicated RD beyond the macula, and type 3 indicated total RD. Optical coherence tomography was performed before and after surgery in all eyes using a commercially available spectral-domain OCT device (Spectralis HRA OCT; Heidelberg Engineering, Heidelberg, Germany) with macular volume scan acquisition protocol to detect any defect in the macular area. The BCVA in Snellen value was converted to the logarithm of the minimum angle of resolution for analysis purposes. If the BCVA was counting fingers or hand movements, it was assigned as the equivalent Snellen acuity of 20/2000 or 20/20000, respectively, based on a previous publication.30
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Table 1. Baseline Clinical Factors of Highly Myopic Patients (n ¼ 27) with Retinal Detachment Caused by a Macular Hole
equations were used to evaluate visual outcomes after the surgery for MHRD repair. P 0.05 was considered to be statistically significant.
Factor Male/female (no.) Age (yrs) Eye (right/left) Preoperative BCVA (logMAR) Axial length (mm) Foveoschisis Staphyloma Follow-up (months) Lens status Phakic Pseudophakic Subtype of RD Type 1* Type 2y
4/23 59.110.6 13/14 1.80.7 29.371.92 (range, 26.5e33.8) 22 25 12.45.3 19 8 9 18
BCVA ¼ best-corrected visual acuity; logMAR ¼ logarithm of minimum angle of resolution; RD ¼ retinal detachment. *Within the vascular arcades. y Beyond the vascular arcades without total RD.
The standard surgical procedures for MHRD repair in this study included a standard 3-port vitrectomy with ILMR combined with ABC and gas tamponade (Video 1, available at www.aaojournal.org). The surgery was undertaken using retrobulbar anesthesia in all patients, with a 23-gauge vitrectomy (Constellation; Alcon, Fort Worth, TX). Briefly, after the core vitrectomy, the posterior vitreous cortex was identified with 20% diluted triamcinolone acetonide (40 mg/ml; Kenalog [Bristol-Myers Squibb, Princeton, NJ]), and the vitreous cortex was lifted by a diamond-dusted membrane scraper (Synergetics, Inc., O’Fallon, MO). Then, ILM peeling was facilitated by staining with indocyanine green (ICG; Daiichi, Tokyo, Japan). The concentration of ICG was 0.125 mg/ml diluted in 5% glucose water, and the exposure time was approximately 30 seconds. No intentional drainage of the subretinal fluid (SRF) was performed during the ILM peeling. During the circumferential ILM peeling of approximately 4 disc diameters, the ILM was not removed completely from the retina, but remained attached to the edge of the MH. The ILM at the margin of the hole was connected as previously described.24,25 After the ILM was lifted, the ILM flap was inverted and used to fill the entire MH by forceps. In a previously published study, the investigator used only a layer of the ILM flap to cover the MH. In this study, we repositioned the inverted ILM to fill the MH. Then, fresh blood obtained from the patient’s antecubital vein was injected gently to cover the macula (Fig 1). The fresh blood soon became a clot on the surface of the macula, and the ILMR and ABC mixture became a macular plug that sealed the hole in minutes. Then, the remaining ILM in the macular area was removed as far as the vascular arcade and the optic nerve head in all patients. The peripheral vitreous was removed as much as possible, and the peripheral retina was checked circumferentially to detect any retinal tears or lattice. Laser photocoagulation was applied to these retinal tears or lattice during the surgery to prevent RD afterward. Airefluid exchange was performed with gas tamponade by 15% perfluoropropane (C3F8) at the end of surgery. The SRF was maintained without intentional drainage. The patients were asked to remain in a prone position for 1 day and to avoid the supine position afterward during the follow-up period until the gas was absorbed. SPSS software version 17.0 (SPSS, Inc., Chicago, IL) was used to perform statistical analyses of the data. Generalized estimating
Results Twenty-seven cases of highly myopic eyes with MHRD in 27 patients were recruited for this study. According to the fundus examination, 9 and 18 eyes were classified as having type 1 and 2 MHRD, respectively, and no type 3 cases were included in this study. The average axial length was 29.371.92 mm. Twenty-five eyes had staphyloma. In addition, the examination of the OCT results showed 22 eyes with foveoschisis. The patient population consisted of 23 women (85%) and 4 men with a mean age of 59.110.6 years. The mean follow-up period was 12.45.3 months. The baseline clinical characteristics of patients are shown in Table 1. In terms of the anatomic outcomes after the surgery, the retina was attached the next day in most cases, and the blood clot could be observed through the gas approximately 14 days after surgery (Fig 2). Retina attachment was achieved in 26 eyes (96%) by a single surgery and in 27 eyes (100%) after a secondary surgery. The initial surgery resulted in a reattached retina in all 27 eyes after complete gas absorption. Unfortunately, rhegmatogenous RD developed in 1 patient 3 months after the surgery. In this case, the MH was closed, but a retinal break located at the nasal upper quadrant of the retina was found. Another vitrectomy with laser photocoagulation of the retinal break and gas tamponade was performed to reattach the retina in this case. The MH was closed in 26 eyes (96%) after the initial surgery. Most of the ILMR could be observed during the follow-up period in these patients after the MH was closed (Fig 3). However, an open parafoveal hole was observed clearly by OCT in 1 patient. In this particular case, the ILMR could not be found in the hole area. Fortunately, this open hole was located in the parafoveal area, and visual acuity was improved in this patient after the surgery (Fig 4). We postulated that the ILMR may dislocate, and in this case, a parafoveal hole was present before surgery. Because the hole was not located at the central fovea and vision improved progressively, we did not perform a secondary procedure for this particular case. Persistent SRF was noted in 3 MH closure cases after the gas was absorbed. The SRF absorbed after surgery in 1 patient after 2.5 months and in another patient after 4 months. The third patient exhibited persistent SRF at the last follow-up examination 12 months after the surgery, but the fluid level was decreasing and visual acuity was improved (Fig 5). With respect to the functional outcomes, the BCVA was improved in 18 eyes (67%), stable in 7 eyes (26%), and worse in 2 eyes (7%) at the final follow-up examination (Table 2). One patient with reduced vision demonstrated RD and underwent secondary surgery. The other patient underwent successful surgery but still had decreased vision because of cataract formation. The mean preoperative and postoperative last visit BCVAs were 1.80.7 and 1.30.7 logarithm of the minimum angle of resolution units, respectively (P ¼ 0.001). In general, there was a significant improvement in BCVA after the surgery at 3 and 6 months and at the last visit, but not during the first month. We observed 8 pseudophakic and 19 phakic eyes before the surgery. Phacoemulsification with intraocular lens implantation was performed in 7 eyes because of the development of cataracts that hindered visual improvement after the vitrectomy surgery. At the end of the follow-up period, with the exception of the 15 pseudophakic eyes, the other 12 phakic cases showed some degree of cataract formation.
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Figure 2. In most cases, the retina was attached 1 day after surgery, and the blood clot persisted approximately 14 days after surgery, which was observed through the gas. A, Case of type 2 macular hole retinal detachment before the surgery. Visual acuity was determined by counting fingers at 50 cm. B, One day after the surgery, the retina was well attached, which was confirmed by optical coherence tomography (OCT). C, Fourteen days after surgery, the blood clot remained. D, Eight months after surgery, the retina was attached and the hole was closed. The visual acuity improved to 0.05. The arrows in (AeD) indicate the location of the macular hole, and the OCT images were acquired in the horizontal view.
Discussion The results of this MHRD case series demonstrated the efficacy of a novel surgical approach using a vitrectomy and ILMR combined with ABC and gas tamponade with 1 day in the prone position for the treatment of MHRD. Retinal attachment and MH closure were achieved in 26 eyes (96%) by a single surgery, and 100% retinal attachment was achieved by the last visit after a secondary surgery was performed for a delayed rhegmatogenous RD that occurred 3 months after the initial surgery. The only open hole was located parafoveally and did not affect central vision. No further vitrectomy was performed in this case. The process of retinal reattachment with MH closure is illustrated in Figure 6. Clinically, anatomic success of both retinal reattachment and MH closure are pivotal in determining the final visual outcome of MHRD. Therefore, in this study, the high anatomic success rate also resulted in postoperative functional recovery, and vision was improved in 18 eyes (67%) by the end of the follow-up period.
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Although spontaneous retinal attachment and hole closure have occurred in sporadic cases of MHRD, surgical intervention is still vital for MHRD.31 Gas injection, vitrectomy, macular buckling, or combination approaches have been applied for the treatment of MHRD.6,7,15,20,21 Among these approaches, vitrectomy for MHRD plus intraocular gas or silicone oil tamponade and ILM peeling are the most popular procedures for MHRD.12,15,16,21 Theoretically, there is no macular defect in the center of the fovea before MHRD occurs. The MHRD may occur when the traction force or other mechanisms overcome a so-called point of no return in normal retinal tissue. These factors exert traction to detach the retina, which can be relieved by vitrectomy and ILM peeling.32 Furthermore, ILM peeling also may remove the scaffold for cellular proliferation or any other traction components affecting the rigidity of retina. Thus, the flexibility of the retina will increase to facilitate the closure of the MH through the proliferation of glial cells after ILM peeling.33e35 These results may support the hypothesis that proliferation of glial cells generates a microenvironment
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Figure 3. Internal limiting membrane repositioning (ILMR) could be found during the follow-up examinations in hole closure cases. A, Color fundus photograph of a type 2 macular hole retinal detachment before the surgery. The visual acuity was determined by counting fingers at 60 cm. B, Color fundus photograph obtained 12 months after surgery. Note that the retina is well attached. Visual acuity was improved to 0.1 after cataract extraction 9 months after the initial vitrectomy. C, Optical coherence tomography (OCT) image obtained before the surgery. Note the macular hole and epiretinal membrane. D, Optical coherence tomography image obtained 6 months after surgery. Note the ILMR around the macular hole. E, Optical coherence tomography image obtained 12 months after surgery showing that the size of the ILMR decreased. Arrows in (D) and (E) indicate the location of the ILMR in the macular hole, and the OCT images were acquired in the horizontal view.
conducive to the repositioning of photoreceptors in the direct proximity of the fovea. However, the limitations of this popular technique include remaining in a face-down position for approximately 2 weeks after surgery, and the hole closure rate is lower than 50% in previous studies.21,23 Opportunities still exist to improve the surgical outcomes by other means. To improve the closure rate of large MH without RD, Michalewska et al24 introduced the inverted ILM flap technique. This inverted ILM flap could facilitate the proliferation of glial cells that fill MHs, thereby improving the MH closure rate and postoperative BCVA in patients with idiopathic chronic MH. This technique also has been applied in a case series of highly myopic eyes to repair an MH with or without RD.25 However, blood components have been use to facilitate the hole closure in MH surgery for a long period.26e29 Apart from the cell components such as platelets, various factors in the serum have been demonstrated to facilitate the wound-healing process in the human body. Therefore, the combination of these 2 procedures of
inverted ILM and blood application may be more effective for hole closure in MHRD. In this study, inverted ILM and blood application were combined, along with some modifications to facilitate hole closure, to reduce the duration that patients must remain in a prone position after MHRD surgery. Other than applying blood as adjuvant, the major modification in this study consisted of repositioning ILM to fill the hole instead of an inverted ILM flap to cover the surface of hole. The ILMR could provide more ILM tissue to fill the MH. The main advantages of this combined technique were as follows. First, the inverted ILMR could fill almost the entire hole and may provide a stronger bridge for the proliferation of glial cells for retinal tissue. Second, the blood clot can seal the hole after application, and the components and growth factors of the blood also could facilitate healing. Furthermore, complete detachment of the inverted ILM may occur after the surgery and can result in failure to close the MH.25 This technique of combined ILMR with ABC may decrease the risk of losing the inverted ILM completely after the vitrectomy, and thus
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Figure 4. An unclosed parafoveal macular hole after an initial vitrectomy in a case of type 2 macular hole retinal detachment. A, Color fundus photograph obtained before surgery. Visual acuity was determined by counting fingers at 30 cm. B, Color fundus photograph obtained 6 months after surgery. Note that the retina is well attached, and it is difficult to identify the macular hole in the color fundus C, Color fundus photograph obtained 12 months after surgery. The retina is well attached, and visual acuity has improved to 0.05. D, Optical coherence tomography image obtained before surgery. Note the macular hole and epiretinal membrane. E, Optical coherence tomography image obtained 1 month after surgery. Note that no repositioned internal limiting membrane was found, and a parafoveal macular hole around the macula is present. FeI, Optical coherence tomography images obtained 3, 6, 9, and 12 months after surgery. Note that the parafoveal hole remained open, and the foveal depression is recovering progressively. Optical coherence tomography images were acquired in the horizontal view.
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Figure 5. A type 2 macular hole retinal detachment with persistent subretinal fluid (SRF) 12 months after surgery. A, Color fundus photograph obtained before surgery. The visual acuity was 0.05. B, Color fundus photograph obtained 6 months after surgery. Note that the retina is well attached, and in the color fundus photograph, it is difficult to identify the SRF. The visual acuity was improved to 0.1. C, Color fundus photograph obtained 12 months after surgery. Note that the retina is well attached, and the visual acuity was improved to 0.2. D, Optical coherence tomography images obtained before the surgery. Note the macular hole and epiretinal membrane. E, Optical coherence tomography image obtained 1 month after surgery. Note that the hole is closed with repositioned internal limiting membrane, but persistent SRF was noted. FeI, Optical coherence tomography images obtained 3, 6, 9, and 12 months after surgery. Note that the SRF level decreased progressively, and vision was improving. Optical coherence tomography images were acquired in a horizontal view.
improve the successful rate of closing the MH and reattach the retina. Theoretically, the hole is completely sealed after blood clot formation, and the complex of the ILMR and ABC formed a macular plug to seal the hole. Communication between the
vitreous and subretinal space was secluded, and the SRF was removed progressively by the retinal pigment epithelium afterward. In our series, some patients’ retinas were attached 1 day after surgery. Therefore, remaining in a prone position
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Ophthalmology Volume -, Number -, Month 2015 Table 2. Surgical Results among All Cases (n ¼ 27) Factor Retinal attachment (no.) Single/final MH closed (no.) Postoperative BCVA (logMAR) 1 mo 3 mos 6 mos Last visit BCVA at last visit, no. (%) Improved No change Worse Complication (no.) RRD Cataract surgery Persistent subretinal fluid
26/27 26 2.00.6 1.50.6* 1.40.7* 1.30.7* 18 (67%) 7 (26%) 2 (7%) 1 7 3
BCVA ¼ best-corrected visual acuity; logMAR ¼ logarithm of the minimum angle of resolution; MH ¼ macular hole; RRD ¼ rhegmatogenous retinal detachment. *P < 0.05.
may not be so critical after hole closure by this so-called macular plug in MHRD cases. Therefore, remaining in a strictly prone position was required for only 1 day. Third, all of the material and techniques in this study are readily available, and most retinal surgeons are familiar with them. Because of the barrier of the ILMR at the hole, the red blood cells will not enter the subretinal space and induce toxicity in the photoreceptors; therefore, the safety concern is reduced regarding the toxicity issues of red blood cells in this technique.36,37 Compared with other potential blood components for this technique, such as platelets, plasma, or serum, fresh blood is more visible and may be easier to manipulate during the application. Also, no extra procedures or instruments are needed to handle fresh blood. In addition, the components of blood also may reduce the toxic effects of ICG stains of the ILM.38
Several advantages of not intentionally draining the SRF during the surgery for MHRD via this technique can be noted. First, drainage of the SRF from the MH in MHRD is a traumatic procedure and may damage the retinal tissue around the fovea and produce an adverse effect on functional outcomes.39 Because the SRF is viscous, the hole tends to be enlarged by this maneuver. To reduce the damage, other traumatic methods such as an extramacular retinotomy have been suggested to drain SRF.40 Second, the distance between the sclerotomy site and ILM on the detached macula is shorter than an attached macula in highly myopic eyes; therefore, it was easier for the surgeon to reach the tractional membranes on the posterior pole using regular forceps. Regular forceps may not be long enough to reach the posterior pole in highly myopic eyes with staphyloma in an attached macula, and specially designed forceps may be needed in this situation.41 Third, while repositioning the ILM into the hole in a detached macula, the detached macula could prevent the instruments from touching the retinal pigment epithelium and choroid, which may cause severe damage in these venerable tissues in highly myopic eyes. However, the remaining viscous SRF may need more time to be absorbed in some cases. In this study, persistent SRF was found in 3 cases after the gas was absorbed. The SRF was absorbed in one eye at 2.5 months and in another eye at 4 months after surgery. A third case showed persistent SRF at the 12-month follow-up visit, but the fluid was decreasing and vision was improving. Regarding the complications after MHRD repair in highly myopic eyes, except for cataract formation and 7 eyes that received cataract extraction, rhegmatogenous RD developed in 1 eye (3%) after the MHRD repair 3 months after the initial vitrectomy, and the patient experienced visual field defects. A retinal break was found in the nasal upper quadrant close to the previous sclerotomy site. This rhegmatogenous RD may have resulted from peripheral retinal breaks and traction from an abnormal vitreoretinal interface.42 After further surgical interventions, the retina was reattached in this case.
Figure 6. Schematic drawings showing how the retina was reattached after vitrectomy combined with inverted internal limiting membrane (ILM) repositioning and autologous blood clot (ABC) and gas tamponade for the treatment of macular hole (MH) retinal detachment. A, Retinal detachment with an MH. B, After ILM peeling, the ILM remained attached to the edge of the MH. C, The inverted ILM was used to fill the MH. D, Fresh blood was used to cover the macula, and the ILM repositioning and ABC mixture became a macular plug that sealed the hole. E, After airefluid exchange, the vitreous cavity was filled with gas (as shown in white) and the subretinal fluid (SRF) was maintained without intentional drainage. F, The retina was reattached with a closed MH after SRF was progressively pumped out by the retinal pigment epithelium.
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There are several limitations to this study, which include its retrospective design, small case number, short follow-up period, and lack of a control group. Some patients had progressive cataracts that might have affected the analysis of visual acuity at the last follow-up visit. The ILMR may induce too much fibrosis in the center of the macula and may hinder further visual recovery. In addition, maneuvering the ILM may damage the foveal tissue. Furthermore, too much of the repositioned ILM may have been preserved in this study. The adequate amount of repositioned ILM use needs to be determined for this procedure. Both staining of the ILM with ICG and placing this ICG-stained tissue into the MH may induce toxicity in the tissue.43 In addition, although blood is a useful adjuvant for MHRD repair, the possible risks of infection associated with using this autologous product should not be ignored.44 Blood may leak into the subretinal space and cause damage to the retinal tissue.37 In conclusion, vitrectomy with ILMR combined with ABC and gas tamponade is an effective treatment for MHRD in highly myopic eyes and showed a high success rate of anatomic restoration and significant visual recovery. The mixture of ILMR and ABC formed a macular plug that sealed the MH shortly after application. This macular plug could reduce the duration that a patient must remain in a prone position and increase the MH closure rate. It is a simple, cost-effective, and high-efficacy method to treat MHRD.
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with retinal detachment in highly myopic eyes. Chang Gung Med J 2003;26:578–85. Ripandelli G, Parisi V, Friberg TR, et al. Retinal detachment associated with macular hole in high myopia: using the vitreous anatomy to optimize the surgical approach. Ophthalmology 2004;111:726–31. Theodossiadis GP, Theodossiadis PG. The macular buckling procedure in the treatment of retinal detachment in highly myopic eyes with macular hole and posterior staphyloma: mean follow-up of 15 years. Retina 2005;25:285–9. Li X, Wang W, Tang S, et al. Gas injection versus vitrectomy with gas for treating retinal detachment owing to macular hole in high myopes. Ophthalmology 2009;116:1182–7. Lim LS, Tsai A, Wong D, et al. Prognostic factor analysis of vitrectomy for retinal detachment associated with myopic macular holes. Ophthalmology 2014;121:305–10. Lam RF, Lai WW, Cheung BTO, et al. Pars plana vitrectomy and perfluoropropane (C3F8) tamponade for retinal detachment due to myopic macular hole: a prognostic factor analysis. Am J Ophthalmol 2006;142:938–44. Chen YP, Chen TL, Yang KR, et al. Treatment of retinal detachment resulting from posterior staphyloma-associated macular hole in highly myopic eyes. Retina 2006;26:25–31. Mancino R, Ciuffoletti E, Martucci A, et al. Anatomical and functional results of macular hole retinal detachment surgery in patients with high myopia and posterior staphyloma treated with perfluoropropane gas or silicone oil. Retina 2013;33:586–92. Oie Y, Emi K, Takaoka G, et al. Effect of indocyanine green staining in peeling of internal limiting membrane for retinal detachment resulting from macular hole in myopic eyes. Ophthalmology 2007;114:303–6. Ando F, Ohba N, Touura K, et al. Anatomical and visual outcomes after episcleral macular buckling compared with those after pars plana vitrectomy for retinal detachment caused by macular hole in highly myopic eyes. Retina 2007;27:37–44. Nishimura A, Kimura M, Saito Y, et al. Efficacy of primary silicone oil tamponade for the treatment of retinal detachment caused by macular hole in high myopia. Am J Ophthalmol 2011;151:148–55. Xie A, Lei J. Pars plana vitrectomy and silicone oil tamponade as a primary treatment for retinal detachment caused by macular holes in highly myopic eyes: a risk-factor analysis. Curr Eye Res 2013;38:108–13. Grzybowski A, Pieczynski J, Ascaso FJ. Neuronal complications of intravitreal silicone oil: an updated review. Acta Ophthalmol 2014;92:201–4. Michalewska Z, Michalewski J, Adelman RA, et al. Inverted internal limiting membrane flap technique for large macular holes. Ophthalmology 2010;117:2018–25. 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: 125–31. Korobelnik JF, Hannouche D, Belayachi N, et al. Autologous platelet concentrate as an adjunct in macular hole healing: a pilot study. Ophthalmology 1996;103:590–4. Liggett PE, Skolik DS, Horio B, et al. Human autologous serum for the treatment of full-thickness macular holes. A preliminary study. Ophthalmology 1995;102:1071–6. Ryan EA, Lee S, Chern S. Use of intravitreal autologous blood to identify posterior cortical vitreous in macular hole surgery. Arch Ophthalmol 1995;113:822–3. Lai CC, Hwang YS, Liu L, et al. Blood-assisted internal limiting membrane peeling for macular hole repair. Ophthalmology 2009;116:1525–30.
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Ophthalmology Volume -, Number -, Month 2015 30. Holladay JT. Proper method for calculating average visual acuity. J Refract Surg 1997;13:388–91. 31. Yu J, Jiang C, Xu G. Spontaneous closure of a myopic macular hole with retinal reattachment in an eye with high myopia and staphyloma: a case report. BMC Ophthalmol 2014;14:111. 32. Spaide RF, Fisher Y. Removal of adherent cortical vitreous plaques without removing the internal limiting membrane in the repair of macular detachments in highly myopic eyes. Retina 2005;25:290–5. 33. Almony A, Nudleman E, Shah GK, et al. Techniques, rationale, and outcomes of internal limiting membrane peeling. Retina 2012;32:877–91. 34. Funata M, Wendel RT, de la Cruz Z, et al. Clinicopathologic study of bilateral macular holes treated with pars plana vitrectomy and gas tamponade. Retina 1992;12:289–98. 35. Madreperla SA, Geiger GL, Funata M, et al. Clinicopathologic correlation of a macular hole treated by cortical vitreous peeling and gas tamponade. Ophthalmology 1994;101:682–6. 36. Glatt H, Machemer R. Experimental subretinal hemorrhage in rabbits. Am J Ophthalmol 1982;94:762–73. 37. Benner JD, Hay A, Landers MB, et al. Fibrinolytic-assisted removal of experimental subretinal hemorrhage within seven days
38. 39. 40. 41. 42.
43. 44.
reduces outer retinal degeneration. Ophthalmology 1994;101: 672–81. Nakamura H, Hayakawa K, Sawaguchi S, et al. Removal of retinal indocyanine green dye by autologous serum irrigation in macular hole surgery. Retina 2005;25:736–41. Charles S. Retinal pigment epithelial abnormalities after macular hole surgery. Retina 1993;13:176. Jeon HS, Byon IS, Park SW, et al. Extramacular drainage of subretinal fluid during vitrectomy for macular hole retinal detachment in high myopia. Retina 2014;34:1096–102. Gao X, Ikuno Y, Nishida K. Long-shaft forceps for membrane peeling in highly myopic eyes. Retina 2013;33:1475–6. Ripandelli G, Rossi T, Scarinci F, et al. Macular vitreoretinal interface abnormalities in highly myopic eyes with posterior staphyloma: 5-year follow-up. Retina 2012;32: 1531–8. Gandorfer A, Haritoglou C, Kampik A. Toxicity of indocyanine green in vitreoretinal surgery. Dev Ophthalmol 2008;42:69–81. Blumenkranz MS, Ohana E, Shaikh S, et al. Adjuvant methods in macular hole surgery: intraoperative plasma-thrombin mixture and postoperative fluid-gas exchange. Ophthalmic Surg Lasers 2001;32:198–207.
Footnotes and Financial Disclosures Originally received: January 12, 2015. Final revision: May 19, 2015. Accepted: May 23, 2015. Available online: ---.
Author Contributions: Conception and design: Lai, Y-P Chen, Chuang, Hwang, Wu, T-L Chen Manuscript no. 2015-18.
1
Department of Ophthalmology, Chang-Gung Memorial Hospital, Taoyuan, Taiwan.
2
Chang Gung University College of Medicine, Taoyuan, Taiwan.
Analysis and interpretation: Lai, Y-P Chen, Wang, Chuang, Liu, K-J Chen Data collection: Lai, Wang, Liu, K-J Chen Obtained funding: Lai Overall responsibility: Lai, Y-P Chen, Hwang, Wu, T-L Chen
Department of Ophthalmology, Chang-Gung Memorial Hospital, Keelung, Taiwan. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article.
Abbreviations and Acronyms: ABC ¼ autologous blood clot; BCVA ¼ best-corrected visual acuity; ICG ¼ indocyanine green; ILM ¼ internal limiting membrane; ILMR ¼ internal limiting membrane repositioning; MH ¼ macular hole; MHRD ¼ macular hole retinal detachment; OCT ¼ optical coherence tomography; RD ¼ retinal detachment; SRF ¼ subretinal fluid.
Supported by the National Science Council Taipei, Taiwan (grant no.: 1022314-B-182-042); and Chang-Gung Memorial Hospital Research Project, Taoyuan, Taiwan (grant no.: G3D0811). The funding organizations had no role in the design or conduct of this research.
Correspondence: Chi-Chun Lai, MD, Department of Ophthalmology, Chang Gung Memorial Hospital, 5, Fu-Hsin Kwei-Shan, 333 Taoyuan, Taiwan. E-mail: chichun. [email protected].
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Macular hole (MH) retinal detachment (MHRD) is one of the most vision-threatening complications associated with highly myopic eyes, and it is highly prevalent in east Asia.1,2 The mechanisms of MHRD may be related to the tangential traction from the epimacular structure and the inverse traction from the posterior staphyloma. Choroidal and retinal pigment epithelium atrophy also may result in weakened retinal adherence to the posterior pole.3e5 According to the pathologic mechanisms, several surgical methods have been introduced to treat MHRD. They include intraocular gas tamponade, pars plana vitrectomy, macular 2015 by the American Academy of Ophthalmology Published by Elsevier Inc.
buckling, and combination approaches. Among them, vitrectomy and gasefluid exchange with internal limiting membrane (ILM) removal followed by face-down positioning was most popular for the treatment of MHRD.6e19 The retinal reattachment rate ranged from 40% to 90% after vitrectomy and gasefluid exchange, but the hole closure rate was lower; the hole could remain open even if the retina was attached.14e16,20 In addition to the unsatisfying anatomic results of MHRD, remaining in a face-down position for 1 to 2 weeks after vitrectomy and gasefluid exchange is an unpleasant experience for the patient during http://dx.doi.org/10.1016/j.ophtha.2015.05.040 ISSN 0161-6420/15
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Figure 1. The surgical procedure of macular hole retinal detachment repaired by a vitrectomy combined with inverted internal limiting membrane (ILM) repositioning and autologous blood clot in highly myopic eyes. A, B, After a vitrectomy, ILM lifting was assisted by staining with indocyanine green without intentional drainage of the subretinal fluid. The lifted ILM was not detached completely from the retina and remained attached to the edge of the macular hole. C, D, Then, the lifted ILM was inverted and placed into the macular hole. E, The inverted ILM was used to fill the macular hole. F, Then, fresh blood from the patient was injected gently to cover the macula and seal the macular hole.
recovery. Although silicone oil was introduced in the initial surgery to avoid the need for face-down positioning,21 it is necessary to remove the silicone oil afterward, and longterm retinal toxicity cannot be ignored.18,22,23 Increasing the successful rate of retinal attachment and hole closure and decreasing the duration that patients are in a prone position are the main goals of MHRD repair. Recently, an inverted ILM flap was used to close large idiopathic MHs in a small case series of MHs in highly myopic eyes with or without retinal detachment (RD).24,25 In addition, blood from the patient long has been applied in vitreoretinal surgeries, and blood components long have been used to improve the hole closure rate for MH.26e29 The purpose of this study was to determine the efficacy of a modified combination therapy, that is, a vitrectomy with inverted ILM repositioning (ILMR) combined with autologous blood clot (ABC) and gas tamponade in a prone position for 1 day, to treat MHRD in highly myopic eyes.
Methods A retrospective, consecutive chart review of all patients with MHRD who underwent a vitrectomy with ILMR combined with ABC and
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gas tamponade by a single surgeon (C.-C.L.) at Chang Gung Memorial Hospital was conducted. The institutional review board of Chang Gung Memorial Hospital, Taoyuan, Taiwan, approved this retrospective study. This study included only the patients with MHRD in a highly myopic eye (6 diopters or axial length 26.5 mm). Patients with a history of RD or proliferative vitreoretinopathy, any kind of retinal surgery, diabetic retinopathy, vitreous hemorrhage, retinal vascular occlusion, uveitis, trauma, optic atrophy, ocular tumors, glaucoma, corneal opacity, or incomplete chart records were excluded. The patient’s age, gender, ocular history, initial best-corrected visual acuity (BCVA), preoperative and postoperative clinical manifestations, subtypes of MHRD, optical coherence tomography (OCT) results, and final BCVA were collected. The classifications of MHRD were based on the extension of RD as described previously.17 Briefly, a classification of type 1 indicated RD within the macula, type 2 indicated RD beyond the macula, and type 3 indicated total RD. Optical coherence tomography was performed before and after surgery in all eyes using a commercially available spectral-domain OCT device (Spectralis HRA OCT; Heidelberg Engineering, Heidelberg, Germany) with macular volume scan acquisition protocol to detect any defect in the macular area. The BCVA in Snellen value was converted to the logarithm of the minimum angle of resolution for analysis purposes. If the BCVA was counting fingers or hand movements, it was assigned as the equivalent Snellen acuity of 20/2000 or 20/20000, respectively, based on a previous publication.30
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Table 1. Baseline Clinical Factors of Highly Myopic Patients (n ¼ 27) with Retinal Detachment Caused by a Macular Hole
equations were used to evaluate visual outcomes after the surgery for MHRD repair. P 0.05 was considered to be statistically significant.
Factor Male/female (no.) Age (yrs) Eye (right/left) Preoperative BCVA (logMAR) Axial length (mm) Foveoschisis Staphyloma Follow-up (months) Lens status Phakic Pseudophakic Subtype of RD Type 1* Type 2y
4/23 59.110.6 13/14 1.80.7 29.371.92 (range, 26.5e33.8) 22 25 12.45.3 19 8 9 18
BCVA ¼ best-corrected visual acuity; logMAR ¼ logarithm of minimum angle of resolution; RD ¼ retinal detachment. *Within the vascular arcades. y Beyond the vascular arcades without total RD.
The standard surgical procedures for MHRD repair in this study included a standard 3-port vitrectomy with ILMR combined with ABC and gas tamponade (Video 1, available at www.aaojournal.org). The surgery was undertaken using retrobulbar anesthesia in all patients, with a 23-gauge vitrectomy (Constellation; Alcon, Fort Worth, TX). Briefly, after the core vitrectomy, the posterior vitreous cortex was identified with 20% diluted triamcinolone acetonide (40 mg/ml; Kenalog [Bristol-Myers Squibb, Princeton, NJ]), and the vitreous cortex was lifted by a diamond-dusted membrane scraper (Synergetics, Inc., O’Fallon, MO). Then, ILM peeling was facilitated by staining with indocyanine green (ICG; Daiichi, Tokyo, Japan). The concentration of ICG was 0.125 mg/ml diluted in 5% glucose water, and the exposure time was approximately 30 seconds. No intentional drainage of the subretinal fluid (SRF) was performed during the ILM peeling. During the circumferential ILM peeling of approximately 4 disc diameters, the ILM was not removed completely from the retina, but remained attached to the edge of the MH. The ILM at the margin of the hole was connected as previously described.24,25 After the ILM was lifted, the ILM flap was inverted and used to fill the entire MH by forceps. In a previously published study, the investigator used only a layer of the ILM flap to cover the MH. In this study, we repositioned the inverted ILM to fill the MH. Then, fresh blood obtained from the patient’s antecubital vein was injected gently to cover the macula (Fig 1). The fresh blood soon became a clot on the surface of the macula, and the ILMR and ABC mixture became a macular plug that sealed the hole in minutes. Then, the remaining ILM in the macular area was removed as far as the vascular arcade and the optic nerve head in all patients. The peripheral vitreous was removed as much as possible, and the peripheral retina was checked circumferentially to detect any retinal tears or lattice. Laser photocoagulation was applied to these retinal tears or lattice during the surgery to prevent RD afterward. Airefluid exchange was performed with gas tamponade by 15% perfluoropropane (C3F8) at the end of surgery. The SRF was maintained without intentional drainage. The patients were asked to remain in a prone position for 1 day and to avoid the supine position afterward during the follow-up period until the gas was absorbed. SPSS software version 17.0 (SPSS, Inc., Chicago, IL) was used to perform statistical analyses of the data. Generalized estimating
Results Twenty-seven cases of highly myopic eyes with MHRD in 27 patients were recruited for this study. According to the fundus examination, 9 and 18 eyes were classified as having type 1 and 2 MHRD, respectively, and no type 3 cases were included in this study. The average axial length was 29.371.92 mm. Twenty-five eyes had staphyloma. In addition, the examination of the OCT results showed 22 eyes with foveoschisis. The patient population consisted of 23 women (85%) and 4 men with a mean age of 59.110.6 years. The mean follow-up period was 12.45.3 months. The baseline clinical characteristics of patients are shown in Table 1. In terms of the anatomic outcomes after the surgery, the retina was attached the next day in most cases, and the blood clot could be observed through the gas approximately 14 days after surgery (Fig 2). Retina attachment was achieved in 26 eyes (96%) by a single surgery and in 27 eyes (100%) after a secondary surgery. The initial surgery resulted in a reattached retina in all 27 eyes after complete gas absorption. Unfortunately, rhegmatogenous RD developed in 1 patient 3 months after the surgery. In this case, the MH was closed, but a retinal break located at the nasal upper quadrant of the retina was found. Another vitrectomy with laser photocoagulation of the retinal break and gas tamponade was performed to reattach the retina in this case. The MH was closed in 26 eyes (96%) after the initial surgery. Most of the ILMR could be observed during the follow-up period in these patients after the MH was closed (Fig 3). However, an open parafoveal hole was observed clearly by OCT in 1 patient. In this particular case, the ILMR could not be found in the hole area. Fortunately, this open hole was located in the parafoveal area, and visual acuity was improved in this patient after the surgery (Fig 4). We postulated that the ILMR may dislocate, and in this case, a parafoveal hole was present before surgery. Because the hole was not located at the central fovea and vision improved progressively, we did not perform a secondary procedure for this particular case. Persistent SRF was noted in 3 MH closure cases after the gas was absorbed. The SRF absorbed after surgery in 1 patient after 2.5 months and in another patient after 4 months. The third patient exhibited persistent SRF at the last follow-up examination 12 months after the surgery, but the fluid level was decreasing and visual acuity was improved (Fig 5). With respect to the functional outcomes, the BCVA was improved in 18 eyes (67%), stable in 7 eyes (26%), and worse in 2 eyes (7%) at the final follow-up examination (Table 2). One patient with reduced vision demonstrated RD and underwent secondary surgery. The other patient underwent successful surgery but still had decreased vision because of cataract formation. The mean preoperative and postoperative last visit BCVAs were 1.80.7 and 1.30.7 logarithm of the minimum angle of resolution units, respectively (P ¼ 0.001). In general, there was a significant improvement in BCVA after the surgery at 3 and 6 months and at the last visit, but not during the first month. We observed 8 pseudophakic and 19 phakic eyes before the surgery. Phacoemulsification with intraocular lens implantation was performed in 7 eyes because of the development of cataracts that hindered visual improvement after the vitrectomy surgery. At the end of the follow-up period, with the exception of the 15 pseudophakic eyes, the other 12 phakic cases showed some degree of cataract formation.
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Figure 2. In most cases, the retina was attached 1 day after surgery, and the blood clot persisted approximately 14 days after surgery, which was observed through the gas. A, Case of type 2 macular hole retinal detachment before the surgery. Visual acuity was determined by counting fingers at 50 cm. B, One day after the surgery, the retina was well attached, which was confirmed by optical coherence tomography (OCT). C, Fourteen days after surgery, the blood clot remained. D, Eight months after surgery, the retina was attached and the hole was closed. The visual acuity improved to 0.05. The arrows in (AeD) indicate the location of the macular hole, and the OCT images were acquired in the horizontal view.
Discussion The results of this MHRD case series demonstrated the efficacy of a novel surgical approach using a vitrectomy and ILMR combined with ABC and gas tamponade with 1 day in the prone position for the treatment of MHRD. Retinal attachment and MH closure were achieved in 26 eyes (96%) by a single surgery, and 100% retinal attachment was achieved by the last visit after a secondary surgery was performed for a delayed rhegmatogenous RD that occurred 3 months after the initial surgery. The only open hole was located parafoveally and did not affect central vision. No further vitrectomy was performed in this case. The process of retinal reattachment with MH closure is illustrated in Figure 6. Clinically, anatomic success of both retinal reattachment and MH closure are pivotal in determining the final visual outcome of MHRD. Therefore, in this study, the high anatomic success rate also resulted in postoperative functional recovery, and vision was improved in 18 eyes (67%) by the end of the follow-up period.
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Although spontaneous retinal attachment and hole closure have occurred in sporadic cases of MHRD, surgical intervention is still vital for MHRD.31 Gas injection, vitrectomy, macular buckling, or combination approaches have been applied for the treatment of MHRD.6,7,15,20,21 Among these approaches, vitrectomy for MHRD plus intraocular gas or silicone oil tamponade and ILM peeling are the most popular procedures for MHRD.12,15,16,21 Theoretically, there is no macular defect in the center of the fovea before MHRD occurs. The MHRD may occur when the traction force or other mechanisms overcome a so-called point of no return in normal retinal tissue. These factors exert traction to detach the retina, which can be relieved by vitrectomy and ILM peeling.32 Furthermore, ILM peeling also may remove the scaffold for cellular proliferation or any other traction components affecting the rigidity of retina. Thus, the flexibility of the retina will increase to facilitate the closure of the MH through the proliferation of glial cells after ILM peeling.33e35 These results may support the hypothesis that proliferation of glial cells generates a microenvironment
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Figure 3. Internal limiting membrane repositioning (ILMR) could be found during the follow-up examinations in hole closure cases. A, Color fundus photograph of a type 2 macular hole retinal detachment before the surgery. The visual acuity was determined by counting fingers at 60 cm. B, Color fundus photograph obtained 12 months after surgery. Note that the retina is well attached. Visual acuity was improved to 0.1 after cataract extraction 9 months after the initial vitrectomy. C, Optical coherence tomography (OCT) image obtained before the surgery. Note the macular hole and epiretinal membrane. D, Optical coherence tomography image obtained 6 months after surgery. Note the ILMR around the macular hole. E, Optical coherence tomography image obtained 12 months after surgery showing that the size of the ILMR decreased. Arrows in (D) and (E) indicate the location of the ILMR in the macular hole, and the OCT images were acquired in the horizontal view.
conducive to the repositioning of photoreceptors in the direct proximity of the fovea. However, the limitations of this popular technique include remaining in a face-down position for approximately 2 weeks after surgery, and the hole closure rate is lower than 50% in previous studies.21,23 Opportunities still exist to improve the surgical outcomes by other means. To improve the closure rate of large MH without RD, Michalewska et al24 introduced the inverted ILM flap technique. This inverted ILM flap could facilitate the proliferation of glial cells that fill MHs, thereby improving the MH closure rate and postoperative BCVA in patients with idiopathic chronic MH. This technique also has been applied in a case series of highly myopic eyes to repair an MH with or without RD.25 However, blood components have been use to facilitate the hole closure in MH surgery for a long period.26e29 Apart from the cell components such as platelets, various factors in the serum have been demonstrated to facilitate the wound-healing process in the human body. Therefore, the combination of these 2 procedures of
inverted ILM and blood application may be more effective for hole closure in MHRD. In this study, inverted ILM and blood application were combined, along with some modifications to facilitate hole closure, to reduce the duration that patients must remain in a prone position after MHRD surgery. Other than applying blood as adjuvant, the major modification in this study consisted of repositioning ILM to fill the hole instead of an inverted ILM flap to cover the surface of hole. The ILMR could provide more ILM tissue to fill the MH. The main advantages of this combined technique were as follows. First, the inverted ILMR could fill almost the entire hole and may provide a stronger bridge for the proliferation of glial cells for retinal tissue. Second, the blood clot can seal the hole after application, and the components and growth factors of the blood also could facilitate healing. Furthermore, complete detachment of the inverted ILM may occur after the surgery and can result in failure to close the MH.25 This technique of combined ILMR with ABC may decrease the risk of losing the inverted ILM completely after the vitrectomy, and thus
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Figure 4. An unclosed parafoveal macular hole after an initial vitrectomy in a case of type 2 macular hole retinal detachment. A, Color fundus photograph obtained before surgery. Visual acuity was determined by counting fingers at 30 cm. B, Color fundus photograph obtained 6 months after surgery. Note that the retina is well attached, and it is difficult to identify the macular hole in the color fundus C, Color fundus photograph obtained 12 months after surgery. The retina is well attached, and visual acuity has improved to 0.05. D, Optical coherence tomography image obtained before surgery. Note the macular hole and epiretinal membrane. E, Optical coherence tomography image obtained 1 month after surgery. Note that no repositioned internal limiting membrane was found, and a parafoveal macular hole around the macula is present. FeI, Optical coherence tomography images obtained 3, 6, 9, and 12 months after surgery. Note that the parafoveal hole remained open, and the foveal depression is recovering progressively. Optical coherence tomography images were acquired in the horizontal view.
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Figure 5. A type 2 macular hole retinal detachment with persistent subretinal fluid (SRF) 12 months after surgery. A, Color fundus photograph obtained before surgery. The visual acuity was 0.05. B, Color fundus photograph obtained 6 months after surgery. Note that the retina is well attached, and in the color fundus photograph, it is difficult to identify the SRF. The visual acuity was improved to 0.1. C, Color fundus photograph obtained 12 months after surgery. Note that the retina is well attached, and the visual acuity was improved to 0.2. D, Optical coherence tomography images obtained before the surgery. Note the macular hole and epiretinal membrane. E, Optical coherence tomography image obtained 1 month after surgery. Note that the hole is closed with repositioned internal limiting membrane, but persistent SRF was noted. FeI, Optical coherence tomography images obtained 3, 6, 9, and 12 months after surgery. Note that the SRF level decreased progressively, and vision was improving. Optical coherence tomography images were acquired in a horizontal view.
improve the successful rate of closing the MH and reattach the retina. Theoretically, the hole is completely sealed after blood clot formation, and the complex of the ILMR and ABC formed a macular plug to seal the hole. Communication between the
vitreous and subretinal space was secluded, and the SRF was removed progressively by the retinal pigment epithelium afterward. In our series, some patients’ retinas were attached 1 day after surgery. Therefore, remaining in a prone position
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Ophthalmology Volume -, Number -, Month 2015 Table 2. Surgical Results among All Cases (n ¼ 27) Factor Retinal attachment (no.) Single/final MH closed (no.) Postoperative BCVA (logMAR) 1 mo 3 mos 6 mos Last visit BCVA at last visit, no. (%) Improved No change Worse Complication (no.) RRD Cataract surgery Persistent subretinal fluid
26/27 26 2.00.6 1.50.6* 1.40.7* 1.30.7* 18 (67%) 7 (26%) 2 (7%) 1 7 3
BCVA ¼ best-corrected visual acuity; logMAR ¼ logarithm of the minimum angle of resolution; MH ¼ macular hole; RRD ¼ rhegmatogenous retinal detachment. *P < 0.05.
may not be so critical after hole closure by this so-called macular plug in MHRD cases. Therefore, remaining in a strictly prone position was required for only 1 day. Third, all of the material and techniques in this study are readily available, and most retinal surgeons are familiar with them. Because of the barrier of the ILMR at the hole, the red blood cells will not enter the subretinal space and induce toxicity in the photoreceptors; therefore, the safety concern is reduced regarding the toxicity issues of red blood cells in this technique.36,37 Compared with other potential blood components for this technique, such as platelets, plasma, or serum, fresh blood is more visible and may be easier to manipulate during the application. Also, no extra procedures or instruments are needed to handle fresh blood. In addition, the components of blood also may reduce the toxic effects of ICG stains of the ILM.38
Several advantages of not intentionally draining the SRF during the surgery for MHRD via this technique can be noted. First, drainage of the SRF from the MH in MHRD is a traumatic procedure and may damage the retinal tissue around the fovea and produce an adverse effect on functional outcomes.39 Because the SRF is viscous, the hole tends to be enlarged by this maneuver. To reduce the damage, other traumatic methods such as an extramacular retinotomy have been suggested to drain SRF.40 Second, the distance between the sclerotomy site and ILM on the detached macula is shorter than an attached macula in highly myopic eyes; therefore, it was easier for the surgeon to reach the tractional membranes on the posterior pole using regular forceps. Regular forceps may not be long enough to reach the posterior pole in highly myopic eyes with staphyloma in an attached macula, and specially designed forceps may be needed in this situation.41 Third, while repositioning the ILM into the hole in a detached macula, the detached macula could prevent the instruments from touching the retinal pigment epithelium and choroid, which may cause severe damage in these venerable tissues in highly myopic eyes. However, the remaining viscous SRF may need more time to be absorbed in some cases. In this study, persistent SRF was found in 3 cases after the gas was absorbed. The SRF was absorbed in one eye at 2.5 months and in another eye at 4 months after surgery. A third case showed persistent SRF at the 12-month follow-up visit, but the fluid was decreasing and vision was improving. Regarding the complications after MHRD repair in highly myopic eyes, except for cataract formation and 7 eyes that received cataract extraction, rhegmatogenous RD developed in 1 eye (3%) after the MHRD repair 3 months after the initial vitrectomy, and the patient experienced visual field defects. A retinal break was found in the nasal upper quadrant close to the previous sclerotomy site. This rhegmatogenous RD may have resulted from peripheral retinal breaks and traction from an abnormal vitreoretinal interface.42 After further surgical interventions, the retina was reattached in this case.
Figure 6. Schematic drawings showing how the retina was reattached after vitrectomy combined with inverted internal limiting membrane (ILM) repositioning and autologous blood clot (ABC) and gas tamponade for the treatment of macular hole (MH) retinal detachment. A, Retinal detachment with an MH. B, After ILM peeling, the ILM remained attached to the edge of the MH. C, The inverted ILM was used to fill the MH. D, Fresh blood was used to cover the macula, and the ILM repositioning and ABC mixture became a macular plug that sealed the hole. E, After airefluid exchange, the vitreous cavity was filled with gas (as shown in white) and the subretinal fluid (SRF) was maintained without intentional drainage. F, The retina was reattached with a closed MH after SRF was progressively pumped out by the retinal pigment epithelium.
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MHRD Repaired by ILM Repositioning and Blood
There are several limitations to this study, which include its retrospective design, small case number, short follow-up period, and lack of a control group. Some patients had progressive cataracts that might have affected the analysis of visual acuity at the last follow-up visit. The ILMR may induce too much fibrosis in the center of the macula and may hinder further visual recovery. In addition, maneuvering the ILM may damage the foveal tissue. Furthermore, too much of the repositioned ILM may have been preserved in this study. The adequate amount of repositioned ILM use needs to be determined for this procedure. Both staining of the ILM with ICG and placing this ICG-stained tissue into the MH may induce toxicity in the tissue.43 In addition, although blood is a useful adjuvant for MHRD repair, the possible risks of infection associated with using this autologous product should not be ignored.44 Blood may leak into the subretinal space and cause damage to the retinal tissue.37 In conclusion, vitrectomy with ILMR combined with ABC and gas tamponade is an effective treatment for MHRD in highly myopic eyes and showed a high success rate of anatomic restoration and significant visual recovery. The mixture of ILMR and ABC formed a macular plug that sealed the MH shortly after application. This macular plug could reduce the duration that a patient must remain in a prone position and increase the MH closure rate. It is a simple, cost-effective, and high-efficacy method to treat MHRD.
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Footnotes and Financial Disclosures Originally received: January 12, 2015. Final revision: May 19, 2015. Accepted: May 23, 2015. Available online: ---.
Author Contributions: Conception and design: Lai, Y-P Chen, Chuang, Hwang, Wu, T-L Chen Manuscript no. 2015-18.
1
Department of Ophthalmology, Chang-Gung Memorial Hospital, Taoyuan, Taiwan.
2
Chang Gung University College of Medicine, Taoyuan, Taiwan.
Analysis and interpretation: Lai, Y-P Chen, Wang, Chuang, Liu, K-J Chen Data collection: Lai, Wang, Liu, K-J Chen Obtained funding: Lai Overall responsibility: Lai, Y-P Chen, Hwang, Wu, T-L Chen
Department of Ophthalmology, Chang-Gung Memorial Hospital, Keelung, Taiwan. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article.
Abbreviations and Acronyms: ABC ¼ autologous blood clot; BCVA ¼ best-corrected visual acuity; ICG ¼ indocyanine green; ILM ¼ internal limiting membrane; ILMR ¼ internal limiting membrane repositioning; MH ¼ macular hole; MHRD ¼ macular hole retinal detachment; OCT ¼ optical coherence tomography; RD ¼ retinal detachment; SRF ¼ subretinal fluid.
Supported by the National Science Council Taipei, Taiwan (grant no.: 1022314-B-182-042); and Chang-Gung Memorial Hospital Research Project, Taoyuan, Taiwan (grant no.: G3D0811). The funding organizations had no role in the design or conduct of this research.
Correspondence: Chi-Chun Lai, MD, Department of Ophthalmology, Chang Gung Memorial Hospital, 5, Fu-Hsin Kwei-Shan, 333 Taoyuan, Taiwan. E-mail: chichun. [email protected].
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