Vitrectomy with Inner Retinal Fenestration for Optic Disc Pit Maculopathy Sotaro Ooto, MD,1 Robert A. Mittra, MD,2 Miriam E. Ridley, MD,3 Richard F. Spaide, MD1 Objective: To evaluate the clinical outcomes after vitrectomy with inner retinal fenestrationdmaking a partial thickness retinal hole radial to the pitdfor the treatment of optic disc pit maculopathy. Design: Retrospective, interventional case series. Participants: Eighteen eyes with optic disc pit maculopathy. Intervention: Pars plana vitrectomy with creation of an inner retinal fenestration was performed in all eyes. A bent 25-gauge needle was used to make a partial thickness inner retinotomy just temporal to the optic disc pit. Main Outcome Measures: Anatomic outcomes determined by optical coherence tomography and postoperative best-corrected visual acuity (BCVA). Results: Before surgery, gross thickening of the inner and outer retinal layers with accumulation of fluid in the central macula was present in all eyes. Macular detachment was observed in 14 eyes, and outer layer hole was identified in 9 eyes. Patients were followed up for a mean of 34.626.6 months after surgery. After surgery, complete resolution of fluid in and under the fovea was achieved in 17 eyes (94%) without additional treatment. In these eyes, reduction of the inner retinal fluid was followed by a slow decrease in the outer retinal fluid and macular detachment. The macular detachment resolved in a mean of 6.13.9 months after surgery. Postoperative BCVA (mean, 0.3780.487 logarithm of the minimum angle of resolution [logMAR]; Snellen equivalent, 20/48) improved significantly compared with preoperative BCVA (mean, 0.7250.510 logMAR; Snellen equivalent, 20/ 106; P ¼ 0.006). Ten eyes (56%) had a postoperative BCVA of 20/30 or better. There was neither the recurrence of macular detachment nor an accumulation of outer retinal fluid in the central macula in any eyes. Conclusions: The introduction of a partial thickness fenestration radial to the optic disc pit was associated with retinal anatomic and functional improvement without additional treatments. These results are consistent with the hypothesis that redirection of flow to allow egress of fluid into the vitreous cavity instead of into the retina can achieve long-lasting amelioration of the pathologic findings of optic pit maculopathy. Ophthalmology 2014;:1e7 ª 2014 by the American Academy of Ophthalmology.
Optics disc pits are a congenital disc abnormality secondary to a colobomatous malformation of the optic nerve head. They typically appear as a solitary, oval, gray-white depression located in the inferotemporal segment of the optic disc. An optic disc pit commonly is associated with an arcuate scotoma or an enlarged blind spot, which is related to the optic nerve abnormality and the loss of the nerve fiber layer extending radially. Abnormalities of the nerve with absence of nerve fibers have been shown.1,2 Acquired visual acuity loss usually is the result of the development of serous detachment of the macula, with a concomitant ophthalmoscopic appearance of the inner retina mimicking retinoschisis.3 Optical coherence tomography (OCT) of the optic disc pit maculopathy has demonstrated gross thickening of the retina, particularly the nasal macula, with fluid accumulating in and under the central macula.4e6 The natural history of optic disc pit maculopathy is poor: 80% of eyes will end up with visual acuity of 20/200 or worse.7 Even if spontaneous resolution occurs, vision often remains reduced because of outer layer lamellar holes or pigment epitheliopathy, particularly when there is long-standing serous detachment.8e10 Multiple approaches for the management of optic disc pit-related maculopathy have been suggested, including 2014 by the American Academy of Ophthalmology Published by Elsevier Inc.
laser photocoagulation, intravitreal gas injection, macular buckling, and pars plana vitrectomy.11e31 The use of peripapillary laser photocoagulation often is unsuccessful, and repeated treatments are needed.11e16 The treatment strategy with peripapillary laser photocoagulation is to try to develop a wall of scar tissue around the potential area of fluid entry into the retina. Intravitreal gas injection alone can induce pneumatic displacement of the outer layer detachment18; however, this effect may be temporary.18 Several researchers have reported small case series that showed a favorable response after vitrectomy with various adjunct procedures.20e31 However, the effect of vitrectomy itself is still unclear because most patients who underwent vitrectomy underwent attempts at laser photocoagulation at time of surgery with fluidegas exchange. In addition, if macular reattachment failed with the initial vitrectomy, multiple additional treatments were tried to reattach the macula.29 Thus, to date, there is not enough evidence to recommend any specific option for primary treatment or persistence of the macular detachment after an initial intervention. The site of inflow into the retina seems to be related topographically to the optic disc pit, because the fluid invariably is seen contiguous with the pit.4e6 The distension ISSN 0161-6420/14/$ - see front matter http://dx.doi.org/10.1016/j.ophtha.2014.04.006
1
Ophthalmology Volume -, Number -, Month 2014 of the retina extending away from the optic nerve implies the fluid enters the retina under pressure. This suggests that redirection of the flow to allow egress of fluid into the vitreous cavity instead of into the retina and to allow a venting of this pressure may alleviate the accumulation of fluid in the macula. Based on this idea, one of the authors (R.F.S.) previously proposed a new technique of inner retinal fenestration, making a partial thickness fenestration adjacent to the pit, as a possible treatment approach for optic disc pit maculopathy.32 The first case was a 15-year-old boy with optic disc maculopathy, who showed rapid improvement in visual acuity and fundus appearance without any complications and recurrences during a long follow-up period.32 The purpose of this study was to evaluate the clinical outcomes of the following consecutive cases who underwent vitrectomy with creation of an inner retinal fenestration for the treatment of optic disc pit maculopathy.
Methods Consecutive eyes with optic disc maculopathy that underwent vitrectomy with inner retinal fenestration at Manhattan Eye, Ear and Throat Hospital (New York, NY), Vitreo Retinal Surgery (Minneapolis, MN), and Horizon Eye Care (Charlotte, NC) were ascertained through review of medical records. This study had institutional review board approval and complied with the Health Insurance Portability and Accountability Act of 1996. The diagnosis of optic disc pit maculopathy was based on the existence of an excavation of the optic nerve in combination with fluid within or under the macula. The patients were evaluated with a complete ophthalmologic examination, including measurement of best-corrected visual acuity (BCVA), color fundus photography, and OCT. The OCT images were obtained using Stratus OCT (Carl Zeiss Meditec, Dublin, CA), Topcon OCT (3D OCT-1000; Topcon Medical Systems, Paramus, NJ), Cirrus HD-OCT (Carl Zeiss Meditec, Dublin, CA), or Spectralis HRAþOCT (Heidelberg Engineering, Heidelberg, Germany). Surgery was performed for worsening BCVA or for the development of macular detachment. Surgeries were performed by 1 of 3 surgeons (R.A.M., M.E.R., or R.F.S.) between September 2003 and January 2012. In 9 eyes, 23-gauge vitrectomy was performed, and 25-gauge vitrectomy was performed in another 9 eyes. After core vitrectomy, a bent 25-gauge needle was used to make a partial thickness retinotomy just temporal to the optic disc pit. The cortical vitreous was removed in only 5 cases because of the lack of association of increased risk of retinal detachment in young patients not having surgically induced posterior vitreous detachments.33 Fluideair exchange was performed in 1 eye, and no eye had internal limiting membrane (ILM) peeling or peripapillary laser at the initial surgery.
Results Preoperative clinical characteristics of patients are summarized in Table 1. Ten of the patients were men and 8 were women, and the mean age was 48.2 years, with an interquartile range of 35.5 to 63.0 years. The mean preoperative BCVA was 0.725 logarithm of the minimum angle of resolution (logMAR; interquartile range, 0.301e1.207), which corresponds to a Snellen equivalent of 20/106. Before surgery, the presence of an accumulation of fluid in the inner intraretinal layers (sub-ILM, ganglion cell layer, inner nuclear layer) was present in 17 eyes and in the outer intraretinal layer
2
Table 1. Preoperative Characteristics of Eyes with Optic Disc Pit Maculopathy Characteristic
Value
Mean patient age (interquartile range), yrs Gender, no. (%) Men Women Mean preoperative visual acuity (interquartile range), logMAR Inner retinal fluid, no. (%) Outer retinal fluid, no. (%) Macular detachment, no. (%) Outer layer lamellar hole, no. (%)
48.2 (35.5e63.0) 10 (56) 8 (44) 0.725 (0.301e1.207) 17 18 14 9
(94) (100) (78) (50)
logMAR ¼ logarithm of the minimum angle of resolution.
(outer nuclear layer) in all eyes (Figs 1 and 2). Macular retinal detachment was observed in 14 eyes, and an outer layer lamellar hole was identified in 9 eyes (Figs 1 and 2). Spectral-domain OCT revealed a defect in the septum interpapillo-maculare34 of the vitreous in 2 of 6 eyes in which spectral-domain OCT results were available before surgery (Fig 3). The postoperative characteristics are summarized in Table 2. The patients were followed up for a mean of 34.6 months (interquartile range, 10.0e60.0 months; range, 6e83 months). After the initial surgery, complete resolution of fluid in and under the central macula was achieved in 17 eyes (94%). Of these, there were no eyes that needed additional treatments to reduce the fluid. In all eyes after reduction of the inner retinal fluid, there was a slow decrease in the outer retinal fluid and macular detachment (Figs 1 and 2). After reduction of the outer retinal fluid, the macular detachment decreased with complete absorption of fluid with a mean of 6.1 months (interquartile range, 2.0e11.0 months) after surgery. In only 1 eye did subretinal fluid persist until 18 months, although there was an improvement in BCVA and a reduction of both the intraretinal fluid and macular detachment. The mean postoperative BCVA was 0.378 logMAR (interquartile range, 0e0.559), which corresponds to a Snellen equivalent of 20/48. Postoperative BCVA improved significantly, compared with preoperative BCVA (P ¼ 0.006, t test). In 11 eyes (61%) logMAR BCVA improved more than 0.3, whereas in no eyes did it worsen more than 0.3. Each 0.3-logMAR change represented a doubling of the visual angle, that is, a change by 3 lines on the eye chart. Despite evidence of some residual intraretinal fluid and persistent macular detachment, the BCVA started to improve within a few months in most eyes. Ten eyes (56%) had a postoperative BCVA of 20/30 or better. There was neither the recurrence of macular detachment nor an accumulation of outer retinal fluid in the central macula in any eyes, although an accumulation of fluid was observed in 2 eyes outside the central macula 3 and 7 years after the surgery, respectively. One of the eyes, which underwent vitreous attachment on the ILM and sub-ILM fluid inferotemporal to the disc, underwent repeat vitrectomy with induction of vitreous detachment and ILM puncture. Three eyes, all of which had outer layer lamellar hole before surgery, demonstrated full-thickness macular hole after surgery; these eyes underwent repeat vitrectomy with ILM peeling and gas tamponade, resulting in the closure of the macular hole. These eyes did not demonstrate macular holes directly from the creation of the fenestration, but did so coincident with reabsorption of intraretinal and subretinal fluid during followup. There were no eyes in which retinal detachment developed.
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Retinal Fenestration for Pit Maculopathy
Figure 1. The left eye of a 38-year-old man with optic disc pit maculopathy and best-corrected visual acuity of 20/200. A, Preoperative fundus photograph showing optic disc pit, fluid accumulation in and under the macula, outer retinal deposits, and outer layer lamellar hole. B, Infrared reflectance image obtained 1 year after surgery. Green line indicates the directions of the scans producing the images in Figure 2.
Cataract progressed in 2 older patients (54 and 63 years of age), and cataract extractions were performed.
Discussion In this study, the introduction of a partial thickness fenestration near the optic disc pit was associated with both resolution of fluid and visual improvement. Optical coherence tomography revealed a reduction in the inner retinal fluid in the early postoperative period. After reduction of the inner retinal fluid, there was a slow decrease in the outer retinal fluid and macular detachment. This pattern of improvement was similar in part to what was reported in previous treatments of vitrectomy with induction of posterior vitreous detachment,29 but the mechanism of fluid resolution was different. Importantly, additional treatments were unnecessary to reduce or prevent the fluid accumulation. Several types of treatments have been proposed for optic disc pit maculopathy. In 1969, Gass11 used xenon photocoagulation along the temporal disc margin in 2 patients to create a chorioretinal adhesion and scar at the disc edge that minimized fluid movement from the pit to the subretinal space. In 1972, Mustonen and Varonen12 reported the use of argon laser photocoagulation to treat 3 patients, and later Brockhurst13 reported the results of argon laser photocoagulation along the disc margin in the area of the retinal detachment in 6 patients. The goal of treatment was to create a sufficient scar along the disc margin to prevent ingress of fluid into and under the retina. However, the use of peripapillary laser therapy often was unsuccessful, and repeat treatments were necessary.11e16 A possible explanation is that laser energy is absorbed principally by pigment in the retinal pigment epithelium and choroid, whereas some of the earliest and most pronounced changes in optic disc maculopathy usually occur in the inner retina adjacent to the nerve. Other proposed therapeutic methods include intravitreal gas tamponade with or without laser photocoagulation.18,19
The buoyancy of an air bubble compresses the retina temporally and may alter fluid flow coming from the vitreous cavity (if that indeed happens)35; however, later flow into the retina may cause recurrent accumulation of the intraretinal and subretinal fluid. Theodossiadis17 proposed a technique that used macular buckling surgery as primary treatment for serous macular detachment. In this technique, a scleral sponge was placed on the area corresponding to the macula, with no application of additional gas or laser photocoagulation. This method is technically difficult because of poor visualization and required monitoring of the implant position during surgery by ultrasonography and after surgery using magnetic resonance imaging.17 In recent years, several investigators have performed vitrectomy with various adjunct procedures.20e31 However, because most reports of surgical combinations seem to converge on a maximum approach combining vitrectomy, laser photocoagulation, and gas tamponade to optimize surgical outcomes, the effect of vitrectomy itself is still unclear. Hirakata et al29 reported a small case series in which most eyes had a favorable response after vitrectomy with induction of posterior vitreous detachment without gas tamponade or laser photocoagulation. Eyes with successful outcomes required almost 1 year to reach complete reattachment after vitrectomy. However, in 1 of the 8 patients, macular reattachment failed with the initial vitrectomy, and multiple treatments including repeat vitrectomy with intraocular gas and laser were necessary to reattach the macula.29 Considering the mechanism of continuous flow into the retina, induction of posterior vitreous detachment seems to be insufficient to prevent reaccumulation of the fluid, at least in some cases with optic disc pit maculopathy; every patient whose surgery involving laser or gas was unsuccessful also had a concurrent vitrectomy. In our series, the largest ever reported, complete resolution of fluid in and under the central macula was found relatively early after surgery. Most importantly, complete resolution of fluid was achieved without additional
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Figure 2. Horizontal line scan spectral-domain optical coherence tomography images thorough the center of the fovea. A, Image obtained before surgery showing gross thickening of the inner and outer retinal layers with accumulation of fluid in the central macula, macular detachment, and an outer layer lamellar hole. B, Image obtained 2 months after surgery showing that inner retinal fluid is absent and fluid accumulation in the outer retina is reduced at the nasal side of the fovea. C, Image obtained 6 months after surgery showing that fluid accumulation in the outer retina is reduced at the temporal side of the fovea. D, Image obtained 12 months after surgery showing minimal outer retinal fluid, disappearance of macular detachment, and recovery of the inner segment ellipsoid line. Best-corrected visual acuity improved to 20/30.
treatments during a long follow-up period. The high degree of success noted in this series suggests that fluid can egress by introducing inner retinal fenestration. Although some accumulation of fluid was observed in 2 eyes outside the central macula, there was no accumulation of outer retinal fluid in the central macula in any eye. The absence of recurrence suggests that a long-lasting modification of the ocular physiology was achieved by this surgical method.
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The surgical procedure presented here offers a promising alternative to those used previously. Inner retinal fenestration seemed to result in the redirection of the flow to allow egress of fluid into the vitreous cavity instead of into the retina, and thus interruption of the continuous flow into the subretinal space. After the inner retinal fluid disappeared, the subretinal fluid was resorbed. It is possible that the inner retinal fenestration will close spontaneously; however,
Ooto et al
Retinal Fenestration for Pit Maculopathy
Figure 3. Vitreous findings of eyes with optic disc pit maculopathy. Preoperative horizontal line scan spectral-domain optical coherence tomography images of (A) the same patient in Figures 1 and 2 and (B) a 49-year-old man with optic disc pit maculopathy. There is a defect in the septum interpapillo-maculare.
continued flow of fluid would be expected to keep the fenestration open. Redirection of flow seems to offer a rational alternative to the surgical procedure of forming a wall or dam of scar tissue to block the passage of fluid, because the wall of scar tissue necessarily involves critical retinal tissue adjacent to the nerve. Although several researchers considered that vitreous traction may be an important factor in the pathogenesis of optic pit maculopathy,29 others suggested that an abnormality in the vitreous interface is responsible for its development.34 Johnson and Johnson34 proposed a hypothesis that a pocket of liquefied vitreous may exist over the abnormally developed optic disc, and a tear in this diaphanous tissue may allow liquefied vitreous to dissect under and into the retina. The preoperative spectral-domain OCT images from the current study revealed a defect in the septum interpapillo-maculare,35 but we have observed this abnormality in otherwise normal eyes. Fine defects in the optic nerve surface have been Table 2. Postoperative Characteristics of Eyes with Optic Disc Pit Maculopathy Characteristic
Value
Mean follow-up after surgery (interquartile range), mos Mean postoperative visual acuity (interquartile range), logMAR Complete resolution of fluid in and under the fovea, no. (%) Mean time to resolution of fluid in and under the central macula (interquartile range), mos Development of full-thickness macular hole after surgery, no. (%)
34.6 (10.0e60.0)
logMAR ¼ logarithm of minimal angle of resolution.
0.378 (0e0.559) 7 (94) 51 (2.0e8.0) 3 (17)
seen on histologic evaluation.2 Considering the embryology of the vitreous, it is likely that eyes with optic disc pit would have abnormalities of the vitreous in the region of Martegiani’s area, which has discontinuities in the hyaloid membranes even in normal eyes.36,37 Thus, a defect visualized in the vitreous could be an association with the development of a pit or even aging and not necessarily a cause of the maculopathy. In any case, inner retinal fenestration would obviate any hypothetical pumping or 1-way valve effects of the abnormal vitreous. Vitrectomy for optic disc pit maculopathy and outer retinal dehiscence may cause full-thickness macular hole. Shukla et al31 reported the outcomes of vitrectomy with ILM peeling, barrage laser photocoagulation, and gas tamponade for optic disc pit maculopathy with central outer retinal dehiscence. In their series, 4 of 7 eyes demonstrated full-thickness macular hole after surgery, and gas tamponade was repeated in 2 patients with large macular holes. In our series, outer layer lamellar hole was observed in 9 eyes, and 3 of them demonstrated fullthickness macular hole after surgery. After surgery, the inner retinal fluid on the nasal side of the detachment resolved quickly, which seemed to cause the outer retinal defect in the central macula to enlarge somewhat, as seen in Figure 2. This implies an increase in the amount of tensile strain on the central macula and may increase the risk of hole development. For these patients, vitrectomy with ILM peeling and gas tamponade was performed, and the macular hole was closed successfully. At the last visit, BCVA improved in 3 of 4 eyes in the study by Shukla et al and in 2 of 3 eyes of our series (1 case; 20/20). Judging from these results and OCT images, it seems that the marked thinning area of the fovea in eyes with outer lamellar hole represents a separation of photoreceptors. If the thinning separates the photoreceptors, then hole development in the thinned area may not cause the loss of
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Ophthalmology Volume -, Number -, Month 2014 foveal photoreceptors directly. Thus, even if full-thickness macular hole occurs after surgery, macular hole repair should be recommended to improve vision in patients with optic disc pit maculopathy. Our study has several limitations. In addition to its retrospective nature and lack of controls, it is possible that this procedure may not be useful for all types of pit maculopathy, just for the more typical forms. Although the fenestration procedure was useful for eyes with a clear entry of fluid through the inner retina, there are some patients in whom fluid entry seems to be more posterior.5,6 Despite these limitations, we present encouraging surgical outcomes with vitrectomy with creation of an inner retinal fenestration for optic disc maculopathy. This study suggests that the introduction of a partial thickness fenestration near the optic disc pit is associated with both retinal anatomic and functional improvement without additional treatments. The durable results seen in this series are consistent with the hypothesis that redirection of flow to allow egress of fluid into the vitreous cavity can rectify pathologic processes induced in optic pit maculopathy.
References 1. Meyer CH, Rodrigues EB, Schmidt JC. Congenital optic nerve head pit associated with reduced retinal nerve fibre thickness at the papillomacular bundle. Br J Ophthalmol 2003;87:1300–1. 2. Christoforidis JB, Terrell W, Davidorf FH. Histopathology of optic nerve pit-associated maculopathy. Clin Ophthalmol 2012;6:1169–74. 3. Lincoff H, Lopez R, Kreissig I, et al. Retinoschisis associated with optic nerve pits. Arch Ophthalmol 1988;106:61–7. 4. Lincoff H, Schiff W, Krivoy D, Ritch R. Optic coherence tomography of optic disk pit maculopathy. Am J Ophthalmol 1996;122:264–6. 5. Moon SJ, Kim JE, Spaide RF. Optic pit maculopathy without inner retinal schisis cavity. Retina 2006;26:113–6. 6. Imamura Y, Zweifel SA, Fujiwara T, et al. High-resolution optical coherence tomography findings in optic pit maculopathy. Retina 2010;30:1104–12. 7. Apple DJ, Rabb MF, Walsh PM. Congenital anomalies of the optic disc. Surv Ophthalmol 1982;27:3–41. 8. Georgalas I, Ladas I, Georgopoulos G, Petrou P. Optic disc pit: a review. Graefes Arch Clin Exp Ophthalmol 2011;249:1113–22. 9. Sugar HS. An explanation for the acquired macular pathology associated with congenital pits of the optic disc. Am J Ophthalmol 1964;57:833–5. 10. Sugar HS. Congenital pits of the optic disc and their equivalents (congenital colobomas and colobomalike excavations) associated with submacular fluid. Am J Ophthalmol 1967;63:298–307. 11. Gass JD. Serous detachment of the macula: secondary to congenital pit of the optic nervehead. Am J Ophthalmol 1969;67:821–41. 12. Mustonen E, Varonen T. Congenital pit of the optic nerve head associated with serous detachment of the macula. Acta Ophthalmol 1972;50:689–98. 13. Brockhurst RJ. Optic pits and posterior retinal detachment. Trans Am Ophthalmol Soc 1975;73:264–91. 14. Gass JD. Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment. 3rd ed. vol II. St. Louis, MO: Mosby; 1987: 728–33.
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15. Cox MS, Witherspoon CD, Morris RE, Flynn HW. Evolving techniques in the treatment of macular detachment caused by optic nerve pits. Ophthalmology 1988;95:889–96. 16. Postel EA, Pulido JS, McNamara JA, Johnson MW. The etiology and treatment of macular detachment associated with optic nerve pits and related anomalies. Trans Am Ophthalmol Soc 1998;96:73–88. 17. Theodossiadis GP. Treatment of maculopathy associated with optic disk pit by sponge explant. Am J Ophthalmol 1996;121: 630–7. 18. Lincoff H, Yannuzzi L, Singerman L, et al. Improvement in visual function after displacement of the retinal elevations emanating from optic pits. Arch Ophthalmol 1993;111: 1071–9. 19. Lincoff H, Kreissig I. Optical coherence tomography of pneumatic displacement of optic disc pit maculopathy. Br J Ophthalmol 1998;82:367–72. 20. Snead MP, James N, Jacobs PM. Vitrectomy, argon laser, and gas tamponade for serous retinal detachment associated with an optic disc pit: a case report. Br J Ophthalmol 1991;75: 381–2. 21. Dai S, Polkinghorne P. Peeling the internal limiting membrane in serous macular detachment associated with congenital optic disc pit. Clin Exp Ophthalmol 2003;31:272–5. 22. Poulson AV, Snead DR, Jacobs PM, et al. Intraocular surgery for optic nerve disorders. Eye (Lond) 2004;18:1056–65. 23. Hirakata A, Okada AA, Hida T. Long-term results of vitrectomy without laser treatment for macular detachment associated with an optic disc pit. Ophthalmology 2005;112:1430–5. 24. Hirakata A, Hida T, Wakabayashi T, Fukuda M. Unusual posterior hyaloid strand in a young child with optic disc pit maculopathy: intraoperative and histopathological findings. Jpn J Ophthalmol 2005;49:264–6. 25. Ishikawa K, Terasaki H, Mori M, et al. Optical coherence tomography before and after vitrectomy with internal limiting membrane removal in a child maculopathy. Jpn J Ophthalmol 2005;49:411–3. 26. Schaal KB, Wrede J, Dithmar S. Internal drainage in optic pit maculopathy. Br J Ophthalmol 2007;91:1093. 27. Ghosh YK, Banerjee S, Konstantinidis A, et al. Surgical management of optic disc pit associated maculopathy. Eur J Ophthalmol 2008;18:142–6. 28. Georgalas I, Petrou P, Koutsandrea C, et al. Optic disc pit maculopathy treated with vitrectomy, internal limiting membrane peeling, and gas tamponade: a report of two cases. Eur J Ophthalmol 2009;19:324–6. 29. Hirakata A, Inoue M, Hiraoka T, McCuen BW II. Vitrectomy without laser treatment or gas tamponade for macular detachment associated with an optic disc pit. Ophthalmology 2012;119:810–8. 30. Theodossiadis GP, Grigoropoulos VG, Liarakos VS, et al. Restoration of the photoreceptor layer and improvement of visual acuity in successfully treated optic disc pit maculopathy: a long follow-up study by optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2012;250:971–9. 31. Shukla D, Kalliath J, Tandon M, Vijayakumar B. Vitrectomy for optic disk pit with macular schisis and outer retinal dehiscence. Retina 2012;32:1337–42. 32. Spaide RF, Fisher Y, Ober M, Stoller G. Surgical hypothesis: inner retinal fenestration as a treatment for optic disc pit maculopathy. Retina 2006;26:89–91. 33. Lit ES, Kim RY, Damico DJ. Surgical removal of subfoveal choroidal neovascularization without removal of posterior hyaloid: a consecutive series in younger patients. Retina 2001;21:317–23.
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34. Johnson TM, Johnson MW. Pathogenic implications of subretinal gas migration through pits and atypical colobomas of the optic nerve. Arch Ophthalmol 2004;122: 1793–800. 35. Worst JG. The bursa intravitrealis premacularis. Doc Ophthalmol Proc Ser 1976;7:275–9.
36. Roth AM, Foos RY. Surface structure of the optic nerve head. 1. Epipapillary membranes. Am J Ophthalmol 1972;74: 977–85. 37. Foos RY, Roth AM. Surface structure of the optic nerve head. 2. Vitreopapillary attachments and posterior vitreous detachment. Am J Ophthalmol 1973;76:662–71.
Footnotes and Financial Disclosures Originally received: November 6, 2013. Final revision: March 26, 2014. Accepted: April 8, 2014. Available online: ---.
Richard F. Spaide: ConsultantdTopcon, Inc, Bausch & Lomb, Inc; RoyaltiesdTopcon, Inc. Supported by the LuEsther T. Mertz Retinal Research Foundation. Manuscript no. 2013-1854.
1
Vitreous Retina Macula Consultants of New York, and the LuEsther T. Mertz Retinal Research Center, Manhattan Eye, Ear and Throat Hospital, New York, New York.
2
Vitreo Retinal Surgery, Minneapolis, Minnesota.
3
Horizon Eye Care, Charlotte, North Carolina.
Financial Disclosure(s): The author(s) have made the following disclosure(s):
Abbreviations and Acronyms: BCVA ¼ best-corrected visual acuity; ILM ¼ internal limiting membrane; logMAR ¼ logarithm of the minimum angle of resolution; OCT ¼ optical coherence tomography. Correspondence: Richard F. Spaide, MD, Vitreous Retina Macula Consultants of New York, 460 Park Avenue, 5th Floor, New York, NY 10022. E-mail: rick.spaide@ gmail.com.
Sotaro Ooto: Financial supportdAlcon Japan Ltd.
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Optics disc pits are a congenital disc abnormality secondary to a colobomatous malformation of the optic nerve head. They typically appear as a solitary, oval, gray-white depression located in the inferotemporal segment of the optic disc. An optic disc pit commonly is associated with an arcuate scotoma or an enlarged blind spot, which is related to the optic nerve abnormality and the loss of the nerve fiber layer extending radially. Abnormalities of the nerve with absence of nerve fibers have been shown.1,2 Acquired visual acuity loss usually is the result of the development of serous detachment of the macula, with a concomitant ophthalmoscopic appearance of the inner retina mimicking retinoschisis.3 Optical coherence tomography (OCT) of the optic disc pit maculopathy has demonstrated gross thickening of the retina, particularly the nasal macula, with fluid accumulating in and under the central macula.4e6 The natural history of optic disc pit maculopathy is poor: 80% of eyes will end up with visual acuity of 20/200 or worse.7 Even if spontaneous resolution occurs, vision often remains reduced because of outer layer lamellar holes or pigment epitheliopathy, particularly when there is long-standing serous detachment.8e10 Multiple approaches for the management of optic disc pit-related maculopathy have been suggested, including 2014 by the American Academy of Ophthalmology Published by Elsevier Inc.
laser photocoagulation, intravitreal gas injection, macular buckling, and pars plana vitrectomy.11e31 The use of peripapillary laser photocoagulation often is unsuccessful, and repeated treatments are needed.11e16 The treatment strategy with peripapillary laser photocoagulation is to try to develop a wall of scar tissue around the potential area of fluid entry into the retina. Intravitreal gas injection alone can induce pneumatic displacement of the outer layer detachment18; however, this effect may be temporary.18 Several researchers have reported small case series that showed a favorable response after vitrectomy with various adjunct procedures.20e31 However, the effect of vitrectomy itself is still unclear because most patients who underwent vitrectomy underwent attempts at laser photocoagulation at time of surgery with fluidegas exchange. In addition, if macular reattachment failed with the initial vitrectomy, multiple additional treatments were tried to reattach the macula.29 Thus, to date, there is not enough evidence to recommend any specific option for primary treatment or persistence of the macular detachment after an initial intervention. The site of inflow into the retina seems to be related topographically to the optic disc pit, because the fluid invariably is seen contiguous with the pit.4e6 The distension ISSN 0161-6420/14/$ - see front matter http://dx.doi.org/10.1016/j.ophtha.2014.04.006
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Ophthalmology Volume -, Number -, Month 2014 of the retina extending away from the optic nerve implies the fluid enters the retina under pressure. This suggests that redirection of the flow to allow egress of fluid into the vitreous cavity instead of into the retina and to allow a venting of this pressure may alleviate the accumulation of fluid in the macula. Based on this idea, one of the authors (R.F.S.) previously proposed a new technique of inner retinal fenestration, making a partial thickness fenestration adjacent to the pit, as a possible treatment approach for optic disc pit maculopathy.32 The first case was a 15-year-old boy with optic disc maculopathy, who showed rapid improvement in visual acuity and fundus appearance without any complications and recurrences during a long follow-up period.32 The purpose of this study was to evaluate the clinical outcomes of the following consecutive cases who underwent vitrectomy with creation of an inner retinal fenestration for the treatment of optic disc pit maculopathy.
Methods Consecutive eyes with optic disc maculopathy that underwent vitrectomy with inner retinal fenestration at Manhattan Eye, Ear and Throat Hospital (New York, NY), Vitreo Retinal Surgery (Minneapolis, MN), and Horizon Eye Care (Charlotte, NC) were ascertained through review of medical records. This study had institutional review board approval and complied with the Health Insurance Portability and Accountability Act of 1996. The diagnosis of optic disc pit maculopathy was based on the existence of an excavation of the optic nerve in combination with fluid within or under the macula. The patients were evaluated with a complete ophthalmologic examination, including measurement of best-corrected visual acuity (BCVA), color fundus photography, and OCT. The OCT images were obtained using Stratus OCT (Carl Zeiss Meditec, Dublin, CA), Topcon OCT (3D OCT-1000; Topcon Medical Systems, Paramus, NJ), Cirrus HD-OCT (Carl Zeiss Meditec, Dublin, CA), or Spectralis HRAþOCT (Heidelberg Engineering, Heidelberg, Germany). Surgery was performed for worsening BCVA or for the development of macular detachment. Surgeries were performed by 1 of 3 surgeons (R.A.M., M.E.R., or R.F.S.) between September 2003 and January 2012. In 9 eyes, 23-gauge vitrectomy was performed, and 25-gauge vitrectomy was performed in another 9 eyes. After core vitrectomy, a bent 25-gauge needle was used to make a partial thickness retinotomy just temporal to the optic disc pit. The cortical vitreous was removed in only 5 cases because of the lack of association of increased risk of retinal detachment in young patients not having surgically induced posterior vitreous detachments.33 Fluideair exchange was performed in 1 eye, and no eye had internal limiting membrane (ILM) peeling or peripapillary laser at the initial surgery.
Results Preoperative clinical characteristics of patients are summarized in Table 1. Ten of the patients were men and 8 were women, and the mean age was 48.2 years, with an interquartile range of 35.5 to 63.0 years. The mean preoperative BCVA was 0.725 logarithm of the minimum angle of resolution (logMAR; interquartile range, 0.301e1.207), which corresponds to a Snellen equivalent of 20/106. Before surgery, the presence of an accumulation of fluid in the inner intraretinal layers (sub-ILM, ganglion cell layer, inner nuclear layer) was present in 17 eyes and in the outer intraretinal layer
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Table 1. Preoperative Characteristics of Eyes with Optic Disc Pit Maculopathy Characteristic
Value
Mean patient age (interquartile range), yrs Gender, no. (%) Men Women Mean preoperative visual acuity (interquartile range), logMAR Inner retinal fluid, no. (%) Outer retinal fluid, no. (%) Macular detachment, no. (%) Outer layer lamellar hole, no. (%)
48.2 (35.5e63.0) 10 (56) 8 (44) 0.725 (0.301e1.207) 17 18 14 9
(94) (100) (78) (50)
logMAR ¼ logarithm of the minimum angle of resolution.
(outer nuclear layer) in all eyes (Figs 1 and 2). Macular retinal detachment was observed in 14 eyes, and an outer layer lamellar hole was identified in 9 eyes (Figs 1 and 2). Spectral-domain OCT revealed a defect in the septum interpapillo-maculare34 of the vitreous in 2 of 6 eyes in which spectral-domain OCT results were available before surgery (Fig 3). The postoperative characteristics are summarized in Table 2. The patients were followed up for a mean of 34.6 months (interquartile range, 10.0e60.0 months; range, 6e83 months). After the initial surgery, complete resolution of fluid in and under the central macula was achieved in 17 eyes (94%). Of these, there were no eyes that needed additional treatments to reduce the fluid. In all eyes after reduction of the inner retinal fluid, there was a slow decrease in the outer retinal fluid and macular detachment (Figs 1 and 2). After reduction of the outer retinal fluid, the macular detachment decreased with complete absorption of fluid with a mean of 6.1 months (interquartile range, 2.0e11.0 months) after surgery. In only 1 eye did subretinal fluid persist until 18 months, although there was an improvement in BCVA and a reduction of both the intraretinal fluid and macular detachment. The mean postoperative BCVA was 0.378 logMAR (interquartile range, 0e0.559), which corresponds to a Snellen equivalent of 20/48. Postoperative BCVA improved significantly, compared with preoperative BCVA (P ¼ 0.006, t test). In 11 eyes (61%) logMAR BCVA improved more than 0.3, whereas in no eyes did it worsen more than 0.3. Each 0.3-logMAR change represented a doubling of the visual angle, that is, a change by 3 lines on the eye chart. Despite evidence of some residual intraretinal fluid and persistent macular detachment, the BCVA started to improve within a few months in most eyes. Ten eyes (56%) had a postoperative BCVA of 20/30 or better. There was neither the recurrence of macular detachment nor an accumulation of outer retinal fluid in the central macula in any eyes, although an accumulation of fluid was observed in 2 eyes outside the central macula 3 and 7 years after the surgery, respectively. One of the eyes, which underwent vitreous attachment on the ILM and sub-ILM fluid inferotemporal to the disc, underwent repeat vitrectomy with induction of vitreous detachment and ILM puncture. Three eyes, all of which had outer layer lamellar hole before surgery, demonstrated full-thickness macular hole after surgery; these eyes underwent repeat vitrectomy with ILM peeling and gas tamponade, resulting in the closure of the macular hole. These eyes did not demonstrate macular holes directly from the creation of the fenestration, but did so coincident with reabsorption of intraretinal and subretinal fluid during followup. There were no eyes in which retinal detachment developed.
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Figure 1. The left eye of a 38-year-old man with optic disc pit maculopathy and best-corrected visual acuity of 20/200. A, Preoperative fundus photograph showing optic disc pit, fluid accumulation in and under the macula, outer retinal deposits, and outer layer lamellar hole. B, Infrared reflectance image obtained 1 year after surgery. Green line indicates the directions of the scans producing the images in Figure 2.
Cataract progressed in 2 older patients (54 and 63 years of age), and cataract extractions were performed.
Discussion In this study, the introduction of a partial thickness fenestration near the optic disc pit was associated with both resolution of fluid and visual improvement. Optical coherence tomography revealed a reduction in the inner retinal fluid in the early postoperative period. After reduction of the inner retinal fluid, there was a slow decrease in the outer retinal fluid and macular detachment. This pattern of improvement was similar in part to what was reported in previous treatments of vitrectomy with induction of posterior vitreous detachment,29 but the mechanism of fluid resolution was different. Importantly, additional treatments were unnecessary to reduce or prevent the fluid accumulation. Several types of treatments have been proposed for optic disc pit maculopathy. In 1969, Gass11 used xenon photocoagulation along the temporal disc margin in 2 patients to create a chorioretinal adhesion and scar at the disc edge that minimized fluid movement from the pit to the subretinal space. In 1972, Mustonen and Varonen12 reported the use of argon laser photocoagulation to treat 3 patients, and later Brockhurst13 reported the results of argon laser photocoagulation along the disc margin in the area of the retinal detachment in 6 patients. The goal of treatment was to create a sufficient scar along the disc margin to prevent ingress of fluid into and under the retina. However, the use of peripapillary laser therapy often was unsuccessful, and repeat treatments were necessary.11e16 A possible explanation is that laser energy is absorbed principally by pigment in the retinal pigment epithelium and choroid, whereas some of the earliest and most pronounced changes in optic disc maculopathy usually occur in the inner retina adjacent to the nerve. Other proposed therapeutic methods include intravitreal gas tamponade with or without laser photocoagulation.18,19
The buoyancy of an air bubble compresses the retina temporally and may alter fluid flow coming from the vitreous cavity (if that indeed happens)35; however, later flow into the retina may cause recurrent accumulation of the intraretinal and subretinal fluid. Theodossiadis17 proposed a technique that used macular buckling surgery as primary treatment for serous macular detachment. In this technique, a scleral sponge was placed on the area corresponding to the macula, with no application of additional gas or laser photocoagulation. This method is technically difficult because of poor visualization and required monitoring of the implant position during surgery by ultrasonography and after surgery using magnetic resonance imaging.17 In recent years, several investigators have performed vitrectomy with various adjunct procedures.20e31 However, because most reports of surgical combinations seem to converge on a maximum approach combining vitrectomy, laser photocoagulation, and gas tamponade to optimize surgical outcomes, the effect of vitrectomy itself is still unclear. Hirakata et al29 reported a small case series in which most eyes had a favorable response after vitrectomy with induction of posterior vitreous detachment without gas tamponade or laser photocoagulation. Eyes with successful outcomes required almost 1 year to reach complete reattachment after vitrectomy. However, in 1 of the 8 patients, macular reattachment failed with the initial vitrectomy, and multiple treatments including repeat vitrectomy with intraocular gas and laser were necessary to reattach the macula.29 Considering the mechanism of continuous flow into the retina, induction of posterior vitreous detachment seems to be insufficient to prevent reaccumulation of the fluid, at least in some cases with optic disc pit maculopathy; every patient whose surgery involving laser or gas was unsuccessful also had a concurrent vitrectomy. In our series, the largest ever reported, complete resolution of fluid in and under the central macula was found relatively early after surgery. Most importantly, complete resolution of fluid was achieved without additional
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Figure 2. Horizontal line scan spectral-domain optical coherence tomography images thorough the center of the fovea. A, Image obtained before surgery showing gross thickening of the inner and outer retinal layers with accumulation of fluid in the central macula, macular detachment, and an outer layer lamellar hole. B, Image obtained 2 months after surgery showing that inner retinal fluid is absent and fluid accumulation in the outer retina is reduced at the nasal side of the fovea. C, Image obtained 6 months after surgery showing that fluid accumulation in the outer retina is reduced at the temporal side of the fovea. D, Image obtained 12 months after surgery showing minimal outer retinal fluid, disappearance of macular detachment, and recovery of the inner segment ellipsoid line. Best-corrected visual acuity improved to 20/30.
treatments during a long follow-up period. The high degree of success noted in this series suggests that fluid can egress by introducing inner retinal fenestration. Although some accumulation of fluid was observed in 2 eyes outside the central macula, there was no accumulation of outer retinal fluid in the central macula in any eye. The absence of recurrence suggests that a long-lasting modification of the ocular physiology was achieved by this surgical method.
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The surgical procedure presented here offers a promising alternative to those used previously. Inner retinal fenestration seemed to result in the redirection of the flow to allow egress of fluid into the vitreous cavity instead of into the retina, and thus interruption of the continuous flow into the subretinal space. After the inner retinal fluid disappeared, the subretinal fluid was resorbed. It is possible that the inner retinal fenestration will close spontaneously; however,
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Figure 3. Vitreous findings of eyes with optic disc pit maculopathy. Preoperative horizontal line scan spectral-domain optical coherence tomography images of (A) the same patient in Figures 1 and 2 and (B) a 49-year-old man with optic disc pit maculopathy. There is a defect in the septum interpapillo-maculare.
continued flow of fluid would be expected to keep the fenestration open. Redirection of flow seems to offer a rational alternative to the surgical procedure of forming a wall or dam of scar tissue to block the passage of fluid, because the wall of scar tissue necessarily involves critical retinal tissue adjacent to the nerve. Although several researchers considered that vitreous traction may be an important factor in the pathogenesis of optic pit maculopathy,29 others suggested that an abnormality in the vitreous interface is responsible for its development.34 Johnson and Johnson34 proposed a hypothesis that a pocket of liquefied vitreous may exist over the abnormally developed optic disc, and a tear in this diaphanous tissue may allow liquefied vitreous to dissect under and into the retina. The preoperative spectral-domain OCT images from the current study revealed a defect in the septum interpapillo-maculare,35 but we have observed this abnormality in otherwise normal eyes. Fine defects in the optic nerve surface have been Table 2. Postoperative Characteristics of Eyes with Optic Disc Pit Maculopathy Characteristic
Value
Mean follow-up after surgery (interquartile range), mos Mean postoperative visual acuity (interquartile range), logMAR Complete resolution of fluid in and under the fovea, no. (%) Mean time to resolution of fluid in and under the central macula (interquartile range), mos Development of full-thickness macular hole after surgery, no. (%)
34.6 (10.0e60.0)
logMAR ¼ logarithm of minimal angle of resolution.
0.378 (0e0.559) 7 (94) 51 (2.0e8.0) 3 (17)
seen on histologic evaluation.2 Considering the embryology of the vitreous, it is likely that eyes with optic disc pit would have abnormalities of the vitreous in the region of Martegiani’s area, which has discontinuities in the hyaloid membranes even in normal eyes.36,37 Thus, a defect visualized in the vitreous could be an association with the development of a pit or even aging and not necessarily a cause of the maculopathy. In any case, inner retinal fenestration would obviate any hypothetical pumping or 1-way valve effects of the abnormal vitreous. Vitrectomy for optic disc pit maculopathy and outer retinal dehiscence may cause full-thickness macular hole. Shukla et al31 reported the outcomes of vitrectomy with ILM peeling, barrage laser photocoagulation, and gas tamponade for optic disc pit maculopathy with central outer retinal dehiscence. In their series, 4 of 7 eyes demonstrated full-thickness macular hole after surgery, and gas tamponade was repeated in 2 patients with large macular holes. In our series, outer layer lamellar hole was observed in 9 eyes, and 3 of them demonstrated fullthickness macular hole after surgery. After surgery, the inner retinal fluid on the nasal side of the detachment resolved quickly, which seemed to cause the outer retinal defect in the central macula to enlarge somewhat, as seen in Figure 2. This implies an increase in the amount of tensile strain on the central macula and may increase the risk of hole development. For these patients, vitrectomy with ILM peeling and gas tamponade was performed, and the macular hole was closed successfully. At the last visit, BCVA improved in 3 of 4 eyes in the study by Shukla et al and in 2 of 3 eyes of our series (1 case; 20/20). Judging from these results and OCT images, it seems that the marked thinning area of the fovea in eyes with outer lamellar hole represents a separation of photoreceptors. If the thinning separates the photoreceptors, then hole development in the thinned area may not cause the loss of
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Ophthalmology Volume -, Number -, Month 2014 foveal photoreceptors directly. Thus, even if full-thickness macular hole occurs after surgery, macular hole repair should be recommended to improve vision in patients with optic disc pit maculopathy. Our study has several limitations. In addition to its retrospective nature and lack of controls, it is possible that this procedure may not be useful for all types of pit maculopathy, just for the more typical forms. Although the fenestration procedure was useful for eyes with a clear entry of fluid through the inner retina, there are some patients in whom fluid entry seems to be more posterior.5,6 Despite these limitations, we present encouraging surgical outcomes with vitrectomy with creation of an inner retinal fenestration for optic disc maculopathy. This study suggests that the introduction of a partial thickness fenestration near the optic disc pit is associated with both retinal anatomic and functional improvement without additional treatments. The durable results seen in this series are consistent with the hypothesis that redirection of flow to allow egress of fluid into the vitreous cavity can rectify pathologic processes induced in optic pit maculopathy.
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15. Cox MS, Witherspoon CD, Morris RE, Flynn HW. Evolving techniques in the treatment of macular detachment caused by optic nerve pits. Ophthalmology 1988;95:889–96. 16. Postel EA, Pulido JS, McNamara JA, Johnson MW. The etiology and treatment of macular detachment associated with optic nerve pits and related anomalies. Trans Am Ophthalmol Soc 1998;96:73–88. 17. Theodossiadis GP. Treatment of maculopathy associated with optic disk pit by sponge explant. Am J Ophthalmol 1996;121: 630–7. 18. Lincoff H, Yannuzzi L, Singerman L, et al. Improvement in visual function after displacement of the retinal elevations emanating from optic pits. Arch Ophthalmol 1993;111: 1071–9. 19. Lincoff H, Kreissig I. Optical coherence tomography of pneumatic displacement of optic disc pit maculopathy. Br J Ophthalmol 1998;82:367–72. 20. Snead MP, James N, Jacobs PM. Vitrectomy, argon laser, and gas tamponade for serous retinal detachment associated with an optic disc pit: a case report. Br J Ophthalmol 1991;75: 381–2. 21. Dai S, Polkinghorne P. Peeling the internal limiting membrane in serous macular detachment associated with congenital optic disc pit. Clin Exp Ophthalmol 2003;31:272–5. 22. Poulson AV, Snead DR, Jacobs PM, et al. Intraocular surgery for optic nerve disorders. Eye (Lond) 2004;18:1056–65. 23. Hirakata A, Okada AA, Hida T. Long-term results of vitrectomy without laser treatment for macular detachment associated with an optic disc pit. Ophthalmology 2005;112:1430–5. 24. Hirakata A, Hida T, Wakabayashi T, Fukuda M. Unusual posterior hyaloid strand in a young child with optic disc pit maculopathy: intraoperative and histopathological findings. Jpn J Ophthalmol 2005;49:264–6. 25. Ishikawa K, Terasaki H, Mori M, et al. Optical coherence tomography before and after vitrectomy with internal limiting membrane removal in a child maculopathy. Jpn J Ophthalmol 2005;49:411–3. 26. Schaal KB, Wrede J, Dithmar S. Internal drainage in optic pit maculopathy. Br J Ophthalmol 2007;91:1093. 27. Ghosh YK, Banerjee S, Konstantinidis A, et al. Surgical management of optic disc pit associated maculopathy. Eur J Ophthalmol 2008;18:142–6. 28. Georgalas I, Petrou P, Koutsandrea C, et al. Optic disc pit maculopathy treated with vitrectomy, internal limiting membrane peeling, and gas tamponade: a report of two cases. Eur J Ophthalmol 2009;19:324–6. 29. Hirakata A, Inoue M, Hiraoka T, McCuen BW II. Vitrectomy without laser treatment or gas tamponade for macular detachment associated with an optic disc pit. Ophthalmology 2012;119:810–8. 30. Theodossiadis GP, Grigoropoulos VG, Liarakos VS, et al. Restoration of the photoreceptor layer and improvement of visual acuity in successfully treated optic disc pit maculopathy: a long follow-up study by optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2012;250:971–9. 31. Shukla D, Kalliath J, Tandon M, Vijayakumar B. Vitrectomy for optic disk pit with macular schisis and outer retinal dehiscence. Retina 2012;32:1337–42. 32. Spaide RF, Fisher Y, Ober M, Stoller G. Surgical hypothesis: inner retinal fenestration as a treatment for optic disc pit maculopathy. Retina 2006;26:89–91. 33. Lit ES, Kim RY, Damico DJ. Surgical removal of subfoveal choroidal neovascularization without removal of posterior hyaloid: a consecutive series in younger patients. Retina 2001;21:317–23.
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34. Johnson TM, Johnson MW. Pathogenic implications of subretinal gas migration through pits and atypical colobomas of the optic nerve. Arch Ophthalmol 2004;122: 1793–800. 35. Worst JG. The bursa intravitrealis premacularis. Doc Ophthalmol Proc Ser 1976;7:275–9.
36. Roth AM, Foos RY. Surface structure of the optic nerve head. 1. Epipapillary membranes. Am J Ophthalmol 1972;74: 977–85. 37. Foos RY, Roth AM. Surface structure of the optic nerve head. 2. Vitreopapillary attachments and posterior vitreous detachment. Am J Ophthalmol 1973;76:662–71.
Footnotes and Financial Disclosures Originally received: November 6, 2013. Final revision: March 26, 2014. Accepted: April 8, 2014. Available online: ---.
Richard F. Spaide: ConsultantdTopcon, Inc, Bausch & Lomb, Inc; RoyaltiesdTopcon, Inc. Supported by the LuEsther T. Mertz Retinal Research Foundation. Manuscript no. 2013-1854.
1
Vitreous Retina Macula Consultants of New York, and the LuEsther T. Mertz Retinal Research Center, Manhattan Eye, Ear and Throat Hospital, New York, New York.
2
Vitreo Retinal Surgery, Minneapolis, Minnesota.
3
Horizon Eye Care, Charlotte, North Carolina.
Financial Disclosure(s): The author(s) have made the following disclosure(s):
Abbreviations and Acronyms: BCVA ¼ best-corrected visual acuity; ILM ¼ internal limiting membrane; logMAR ¼ logarithm of the minimum angle of resolution; OCT ¼ optical coherence tomography. Correspondence: Richard F. Spaide, MD, Vitreous Retina Macula Consultants of New York, 460 Park Avenue, 5th Floor, New York, NY 10022. E-mail: rick.spaide@ gmail.com.
Sotaro Ooto: Financial supportdAlcon Japan Ltd.
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