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Subfoveal Neovascular Membrane Removal in Patients with Traumatic Choroidal Rupture
Sub£oveal N eovascular Membrane Removal in Patients with Traumatic Choroidal Rupture Jeffrey G. Gross, MD,t Lowrey P. King, MD,2 Eugene de Juan, Jr., MD,3 Timothy Powers, MD2 Purpose: To describe the clinical outcomes of patients undergoing pars plana vitrectomy to remove subretinal neovascular membranes caused by traumatic choroidal ruptures. Methods: Three patients with traumatic choroidal rupture in whom subfoveal choroidal neovascularization developed underwent pars plana vitrectomy with surgical excision of the neovascular membrane. Surgical specimens were examined histopathologically in two patients. Results: The choroidal neovascularization was removed completely in each patient. Visual results were excellent with visual acuities improving to 20/30 or better in each patient. Recurrence of choroidal neovascularization has not been observed. Fibrovascular membranes with reactive retinal pigment epithelium were observed in two specimens examined histopathologically. Conclusion: Surgical removal of subretinal neovascular membranes emanating from traumatic choroidal ruptures produced an excellent visual outcome in three patients studied. The neovascular membranes, which were removed with minor disturbance to the underlying pigment epithelium, have similar characteristics to those obtained from patients with ocular histoplasmosis syndrome. Ophthalmology 1996;103:579-585
Subretinal neovascularization arising from discrete defects in Bruch membrane may be associated with angioid streaks, myopia, ocular histoplasmosis, photocoagulation bums, and traumatic choroidal rupture. Visual acuity after choroidal rupture initially may be reduced by subretinal or subpigment epithelial hemorrhage i but usually improves as the blood is reabsorbed. Serous retinal detachOriginally received: August 25, 1995. Revision accepted: December 22, 1995. 1 Carolina Retina Center, Columbia. 2 Department of Ophthalmology, Storm Eye Center, Medical College of South Carolina, Charleston. 3 Department of Ophthalmology, Wilmer Eye Institute, Johns Hopkins University, Baltimore. Presented in part at The Vitreous Society Annual Meeting, Aspen, Colorado, August 1994. Reprint requests to Jeffrey G. Gross, MD, 3000 Northeast Medical Park, Suite 101, Columbia, SC 29223.
ment and subretinal hemorrhage from choroidal neovascularization may be responsible for delayed onset of visual loss months to years after the initial trauma. 2-4 Laser photocoagulation for extrafoveallesions is highly successful. Untreated lesions may result in disciform scarring and severe visual loss. 5 Surgical excision of subfoveal neovascular membranes has been well described in associatIon with a variety of macular diseases. 6- s Presumed ocular histoplasmosis has been the most favorable to date. 9 We present three case reports describing the successful surgical removal of subfoveal neovascularization in patients with traumatic choroidal rupture resulting in excellent visual acuity.
Case Reports Case 1. A 27-year-old white man had acute vision loss in the left eye after a horse kicked the left side of his face. Results of
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examination disclosed orbital fractures, traumatic choroidal rupture, and submacular blood. Initial visual acuity was 20/200 but improved to 20/25 6 weeks after the injury. Eight months later, the patient began to notice central visual distortion, which became progressively worse over a 4- to 6-week period. Visual acuity was 20/15 in the right eye and 20/400 in the left. Pupils were equally reactive with no afferent pupillary defect. Amsler grid testing disclosed diffuse metamorphopsia in the left eye. The anterior segment examination of both eyes and the fundus examination of the right eye were completely normal. In the left eye, acurvilinear choroidal rupture was present temporal to the macula, bridging the superior and inferiotemporal arcades. A smaller curved choroidal rupture scar was identified more posteriorly. The superior aspect of this scar connected with an apparent submacular neovascular membrane, and an even smaller rupture scar was located inferiotemporal to the optic nerve head. A total of three choroidal ruptures were present. A green-gray subretinal membrane emanated from the largest rupture scar and extended beneath the fovea. The membrane was rimmed by a thin layer of subretinal hemorrhage. A second well-defined subretinal neovascular membrane was located adjacent and temporal to the large choroidal rupture scar. There was a serous retinal detachment overlying both lesions (Fig IA). fluorescein angiography confirmed the clinical findings and demonstrated the membrane edge extending into the foveal avascular zone (Fig 1B). A three-port pars plana vitrectomy was performed by one of us (JGG) with careful removal of the posterior hyaloid. The retina superior to the membrane was cauterized lightly, and a retinotomy was performed by gentle irrigation of balanced salt solution through a 33-gauge cannula, producing a focal retinal detachment in the macula. The intraocular pressure was elevated transiently, and a 130 0 subretinal spatula was used to separate the membrane from the underlying retinal pigment epithelium. The membrane was grasped with 130 0 subretinal forceps and removed in one piece through the retinotomy. A fluid-air exchange served to pneumohydraulically reattach the retina, and the retinotomy was surrounded by light focal endolaser. The second, more inferior subretinal membrane was treated focally with endolaser. The vitreous cavity was lavaged with a 20%
concentration of sulfur hexafluoride, and the sclerotomies and conjunctiva were closed with absorbable suture. Visual acuity improved to 20/60 at 1 week and 20/20 by 2 months postoperatively. fluorescein angiography performed I week and then 2 months after surgery demonstrated no evidence of subretinal neovascularization (Fig 2). The intact retinal pigment epithelium was mottled lightly beneath the temporal macula and fovea and at the laser sites. Six months after surgery, uncorrected distance visual acuity returned to 20/15 with near vision to Jaeger I + and was maintained at this level at the last follow-up examination 18 months after surgery. The lens has remained clear. There has been no recurrence of choroidal neovascularization. Case 2. A 56-year-old African-American man had decreased vision in the left eye after being kicked in the face during an altercation. Initial visual acuity was 20/400. Pupils were minimally reactive without afferent pupillary defect. Anterior segment examination disclosed a confluent subconjunctival hemorrhage and mild anterior segment cellular reaction. The lens was clear. Fundus findings included commotia retinae postequatorial in every meridian. A small hemorrhagic pigment epithelial detachment was present just nasal to the optic disc. A curvilinear choroidal rupture was noted inferotemporal to the central macula with an associated serous and hemorrhagic detachment of the neurosensory retina occupying approximately seven to eight disc areas within the posterior pole. There was no hemorrhage directly underlying the foveola. The patient was treated conservatively, and visual acuity improved to 20/20 6 weeks later. There was complete resolution of the serous and hemorrhagic macular detachment. Vision remained stable until almost precisely I year later, at which time he reported a sudden decline in vision associated with a central scotoma and metamorphopsia. Visual acuity was 20/200. A focal serous detachment of the sensory retina extended into the edge of the fovea associated with a rim of subretinal hemorrhage under the foveola. fluorescein angiography demonstrated a well-defined choroidal neovascular membrane in conjunction with subretinal hemorrhage arising from the choroidal rupture scar and extending into the foveal avascular zone.
Figure 1. A, preoperatively, three choroidal ruptures spare the fovea with choroidal neovascularization emanating from the choroidal rupture temporal to the fovea. The neovascular membrane (arrowheads) extends into the fovea and is associated with subretinal hemorrhage. B, fluorescein angiography demonstrates two contiguous well-defined choroidal neovascular membranes (large arrows) and a smaller isolated membrane (small arrow).
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Figure 2 . Postoperative photograph (A) and fluorescein angiogram (B) demonstrate mild mottling of the retinal pigment epithelium beneath the macula. A, the retinotomy (large arrow) is bordered by a laser scar, and the contiguous neovascular membrane is replaced by a dry laser scar (small arrow). There is no recurrence of choroidal neovascularization.
Surgical removal of the choroidal neovascular membrane was recommended, but shortly before surgery the patient had further visual loss to 20/400 associated with more extensive subretinal hemorrhage beneath the macula (Fig 3). A pars plana vitrectomy was performed by one of us (LPK) with removal ofthe posterior hyaloid. Intraoperatively, the subretinal hemorrhage was found to be diffuse with less than 1 mm of associated elevation. The hemorrhage was nearly completely aspirated through the retinotomy site. Using standard methods and instrumentation for submacular surgery, the neovascular complex was extracted, and gas-fluid exchange was performed with 20% sulfur hexafluoride. The retinotomy site was not treated. Distance visual acuity improved to 20/30 3 weeks after sur-
gery. A confluent area of retinal pigment epithelial depigmentation corresponded to the position of the extracted choroidal neovascular complex. Four months later, there was minimal subfoveal pigment epithelial disturbance with no evidence of persistent neovascularization clinically or angiographically (Fig 4). When last examined, 8 months after surgery, visual acuity remained at 20/30 and there was no evidence of recurrent neovascularization. Results of histopathologic examination by light microscopy showed a fibrovascular membrane lined on two surfaces by multilayered retinal pigment epithelial cells (Fig 5). A photoreceptor fragment was present. Case 3. A 12-year-old white boy was hit in the left eye with an ice ball. Initially, visual acuity was markedly reduced but
Figure 3. Fluorescein angiography demonstrates choroidal neovascularization at the superior end of a choroidal rupture. Subretinal hemorrhage extends beneath the fovea.
Figure 4 . Fluorescein angiography at 4 months after surgery discloses no recurrence of choroidal neovascularization. The retinal pigment epithelium is mottled corresponding to the extracted membrane and retinotomy site.
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Figure 5. There is an irregular monolayer of retinal pigment epithelium along the edge of the specimen. Melanophages and chronic inflammatory cells are present in the loose fibrous connective tissue (hematoxylin-eosin; original magnification, X400).
subsequently improved to 20/20. Approximately 7 months later, visual acuity deteriorated to 20/150. Anterior segment findings disclosed a superficial corneal scar. Results of fundus examination showed a choroidal rupture in the posterior pole of the left eye extending from a point just inferior to the optic disc to the center of the macula (Fig 6A). Fluorescein angiography demonstrated classic choroidal neovascularization in the center of the macula overlying the posterior end ofthe choroidal rupture (Fig 6B). Pars plana vitrectomy was performed by one of us (EdJ). A posterior vitreous detachment was created with the vitrector in aspiration mode and the posterior hyaloid removed. A retinotomy
was created just inferior to the choroidal neovascular membrane. A similar retinotomy was made just superonasal to the choroidal neovascular membrane. The subretinal space was separated from the overlying retina. Subretinal forceps then were introduced through the superior retinotomy, and the choroidal neovascular membrane was removed. The remainder of the membrane was removed through the inferior retinotomy. A fluid-air exchange was performed. The retinotomy sites were not treated focally. The sclerotomies and conjunctiva were closed. Visual acuity improved to 20/60 I week after surgery and to 20/50 after 2 months. The macula demonstrated an area of pigment epithelial atrophy and a small area of hemorrhage along
Figure 6. Preoperative photograph (A) and fluorescein angiography (B) before surgery demonstrate a single choroidal rupture extending from the inferior margin of the optic disc to the inferionasal macula, sparing the fovea. Choroidal neovascularization is present beneath the fovea and is associated with subretinal hemorrhage.
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Figure 7. Fundus photograph (A) and fluorescein angiography (B) taken 2 months after surgery shows mottling of the retinal pigment epithelium, sparing the fovea. The retinotomy is visible along the superior arcade.
the superotemporal arcade (Fig 7A). Auorescein angiography showed no persistent neovascularization (Fig 7B). Seven months after surgery, visual acuity improved to 20/25. The specimen was examined by transmission electron microscopy, which showed a fibrovascular membrane composed of a collagenous matrix with native collagen fibers and new collagen. There were scattered collections of homogenous electrondense material (Fig 8). The membrane was lined on one surface by multiple layers of retinal pigment epithelium. External to the pigmented epithelium, a zone of finely granular material with widely spaced collagen was present (Fig 9).
Figure B. A fibrovascular membrane is composed of a collagenous matrix with native collagen fibers (12-nm diameter) and new collagen (25-nm diameter). There are scattered collections of homogenous electron-dense material (original magnification, XIB,OOO).
Discussion Traumatic choroidal rupture typically produces immediate visual loss secondary to submacular and/or vitreous hemorrhage. The hemorrhage frequently reabsorbs, and vision often returns to near normal levels unless the defect in Bruch membrane involves the fovea or otherwise causes macular distortion. Subretinal neovascularization may produce late visual loss through creation of a serous neurosensory detachment of the macula with or without fresh subretinal hemorrhage. Choroidal neovascularization complexes are a common histopathologic finding during the early healing process of choroidal ruptures. The majority of these vessels apparently regress because the incidence of reported late complications is only 25% to 30%.10,11 Neovascularization beneath the retinal pigment epithelium was observed in only 1 of 39 autopsy specimens with indirect choroidal rupture. 12 There are clinical reports of subretinal neovascularization spontaneously involuting without treatment. 2 ,1l Extrafoveal membranes have been treated successfully with laser photocoagulation. 4 However, if the neovascularization extends beneath the foveal avascular zone, the ultimate visual outcome is poor, especially if the complex is associated with new hemorrhage. 5,10 Of the other entities associated with the development of subfoveal neovascularization, presumed ocular histoplasmosis syndrome and age-related macular degeneration have been studied the most. 13 The visual results of surgery are most apparent among patients with ocular histoplasmosis. This is likely attributable to the observation that the neovascular complex may have a solitary ingrowth site through a focal abnormality in Bruch membrane and grow anterior to the retinal pigment epithelium. 8 Patients with ocular histoplasmosis are usually young, have visual symptoms early in the disease process, and typically do
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Figure 9. The membrane is lined on one surface by multiple layers of retinal pigment epithelium. External to the pigmented epithelium, a zone of finely granular material with widely spaced collagen is present (original magnification, X6480).
not have a diffuse dystrophy of the choriocapillaris-Bruch membrane complex. 14,15 Gass 16 recently has described histopathologic findings in five patients with ocular histoplasmosis syndrome. The subretinal vessels were found to grow in the subsensory retinal space and to be engulfed partially by proliferating retinal epithelium. In particular, the duplicated retinal pigment epithelium was identified on the posterior surface ofthe new vessels. This may confuse histopathologic interpretation because excised tissue from surgical cases may give the erroneous impression that the neovascular membrane was removed from the subpigment epithelial space. 16,17 Gass 16 believes certain factors may predict whether a neovascular membrane will be located in the subsensory retinal space. These include age younger than 50· years, subretinal pigmented halo or plaque around the origin of neovascularization, sharply defined neovascular borders, absence of elevated pigment epithelium beyond the neovascular complex, and normal fellow eye. These are important because surgical excision may be less complicated and should yield better results with greater potential visual acuity in patients with the above characteristics. Although the neovascular complex technically can be removed in age-related macular degeneration, the visual results are not as good as in ocular histoplasmosis. In agerelated macular degeneration, unlike cases of presumed ocular histoplasmosis syndrome and other causes offocal choroiditis, active growth of choroidal neovascularization occurs primarily in the sUbpigment epithelial space rather than in the subretinal space. The neovascular complex in age-related macular degeneration develops a degree of attachment to the retinal pigment epithelium anteriorly, which is removed during surgery, thus destroying the function of the overlying retina. 16
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Elimination or reduction of the exudative retinal detachment produced by a choroidal neovascular membrane may allow for some improvement in vision, even iffoveal retinal pigment epithelium is absent. Recurrences occur within 5 to 8 months in at least one third of patients with either age-related macular degeneration or ocular histoplasmosis. 9 The natural history of exudative age-related macular degeneration is poor. Only a controlled study will resolve which patients will benefit the most. The submacular surgery trial, which has been funded by the National Institutes of Health, may clarify these issues. Subretinal neovascular membranes emanating from choroidal ruptures appear to behave similarly to those arising in the maculae of patients with ocular histoplasmosis. Patients are usually young and have focal defects in Bruch membrane with healthy surrounding retinal pigment epithelium. In addition, the choroidal neovascularization appears to grow anterior to the pigment epithelium in the subneurosensory retinal space. One patient in our series was older than 50 years of age but had no other retinal disease or dystrophy. The specimen from this patient had an irregular monolayer of retinal pigment epithelium covering both surfaces of the membrane similar to the findings described in ocular histoplasmosis. Because (1) most trauma-induced neovascular membranes regress spontaneously and (2) extrafoveal lesions often respond favorably to laser treatment, it is unlikely that many patients will present with subfoveal disease. To our knowledge, this is the first report of surgical excision of subfoveal neovascularization related to choroidal rupture. The membranes generally were separated easily from the underlying retinal pigment epithelium. Postoperative angiography demonstrated mottled transmission defects. There has been no neovascular recurrence after 1 year in
Gross et al . Subfoveal Neovascular Membrane Removal two patients, and recovery of excellent visual acuity was obtained in all three patients.
References 1. Gross JG, Freeman WR. Post traumatic yellow maculopathy. Retina 1990;10:37-41. 2. Smith RE, Kelly JS, Harbin TS. Late macular complications of choroidal ruptures. Am J Ophthalmol 1974;77:650-8. 3. Pearlstone AD. Delayed loss of central vision following multiple posterior segment trauma. Ann Ophthalmol 1980;12:409-11. 4. Fuller B, Gitter KA. Traumatic choroidal rupture with late serous detachment of macula: Report of successful argon laser treatment. Arch Ophthalmol 1973;89:354-5. 5. Luxenberg MN. Subretinal neovascularization associated with rupture of the choroid. Arch Ophthalmol 1986; 104: 1233. 6. deJuan E Jr, Machemer R. Vitreous surgery for hemorrhagic and fibrous complications of age-related macular degeneration. Am J Ophthalmol 1988;105:25-9. 7. Thomas MA, Kaplan HJ. Surgical removal of subfoveal neovascularization in the presumed ocular histoplasmosis syndrome. Am J Ophthalmol 1991; III : 1-7. 8. Thomas MA, Grand MG, Williams OF, et al. Surgical management of subfoveal choroidal neovascularization. Ophthalmology 1992;99:952-76.
9. Thomas MA, Dickinson JD, Melberg NS, et al. Visual results after surgical removal of subfoveal choroidal neovascular membranes. Ophthalmology 1994; 101: 1384-96. 10. Wyszynski RE, Grossniklaus HE, Frank KE. Indirect choroidal rupture secondary to blunt ocular trauma. A review of eight eyes. Retina 1988;8:237-43. 11. Hart JCD, Natsikos VE, Raistrick ER, Doran RML.Indirect choroidal tears at the posterior pole: a fluorescein angiographic and perimetric study. Br J Opthalmol 1980;64:5967. 12. Aguilar JP, Green WR.Choroidal rupture. A histopathologic study of 47 cases. Retina 1984;4:269-75. 13. Grossniklaus HE, Hutchinson AK, Capone A Jr, et al. Clinicopathologic features of surgically excised choroidal neovascular membranes. Ophthalmology 1994; 10 1: 1099-111. 14. Berger AS, Kaplan HJ. Clinical experience with the surgical removal of subfoveal neovascular membranes. Short-term postoperative results. Ophthalmology 1992;99:969-76. 15. Gass JDM. Pathogenesis of disciform detachment of the neuorepithelium. V. Disciform macular degeneration secondary to focal choroiditis. Am J OphthalmoI1967;63:66187. 16. Gass JDM. Biomicroscopic and histopathologic considerations regarding the feasibility of surgical excision of subfoveal neovascular membranes. Am J Ophthalmology 1994; 118:285-98. 17. Saxe SJ, Grossniklaus HE, Lopez PF, et al. Ultrastructural features of surgically excised subretinal neovascular membranes in the ocular histoplasmosis syndrome. Arch Ophthalmology 1993; 111 :88-95.
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Subretinal neovascularization arising from discrete defects in Bruch membrane may be associated with angioid streaks, myopia, ocular histoplasmosis, photocoagulation bums, and traumatic choroidal rupture. Visual acuity after choroidal rupture initially may be reduced by subretinal or subpigment epithelial hemorrhage i but usually improves as the blood is reabsorbed. Serous retinal detachOriginally received: August 25, 1995. Revision accepted: December 22, 1995. 1 Carolina Retina Center, Columbia. 2 Department of Ophthalmology, Storm Eye Center, Medical College of South Carolina, Charleston. 3 Department of Ophthalmology, Wilmer Eye Institute, Johns Hopkins University, Baltimore. Presented in part at The Vitreous Society Annual Meeting, Aspen, Colorado, August 1994. Reprint requests to Jeffrey G. Gross, MD, 3000 Northeast Medical Park, Suite 101, Columbia, SC 29223.
ment and subretinal hemorrhage from choroidal neovascularization may be responsible for delayed onset of visual loss months to years after the initial trauma. 2-4 Laser photocoagulation for extrafoveallesions is highly successful. Untreated lesions may result in disciform scarring and severe visual loss. 5 Surgical excision of subfoveal neovascular membranes has been well described in associatIon with a variety of macular diseases. 6- s Presumed ocular histoplasmosis has been the most favorable to date. 9 We present three case reports describing the successful surgical removal of subfoveal neovascularization in patients with traumatic choroidal rupture resulting in excellent visual acuity.
Case Reports Case 1. A 27-year-old white man had acute vision loss in the left eye after a horse kicked the left side of his face. Results of
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examination disclosed orbital fractures, traumatic choroidal rupture, and submacular blood. Initial visual acuity was 20/200 but improved to 20/25 6 weeks after the injury. Eight months later, the patient began to notice central visual distortion, which became progressively worse over a 4- to 6-week period. Visual acuity was 20/15 in the right eye and 20/400 in the left. Pupils were equally reactive with no afferent pupillary defect. Amsler grid testing disclosed diffuse metamorphopsia in the left eye. The anterior segment examination of both eyes and the fundus examination of the right eye were completely normal. In the left eye, acurvilinear choroidal rupture was present temporal to the macula, bridging the superior and inferiotemporal arcades. A smaller curved choroidal rupture scar was identified more posteriorly. The superior aspect of this scar connected with an apparent submacular neovascular membrane, and an even smaller rupture scar was located inferiotemporal to the optic nerve head. A total of three choroidal ruptures were present. A green-gray subretinal membrane emanated from the largest rupture scar and extended beneath the fovea. The membrane was rimmed by a thin layer of subretinal hemorrhage. A second well-defined subretinal neovascular membrane was located adjacent and temporal to the large choroidal rupture scar. There was a serous retinal detachment overlying both lesions (Fig IA). fluorescein angiography confirmed the clinical findings and demonstrated the membrane edge extending into the foveal avascular zone (Fig 1B). A three-port pars plana vitrectomy was performed by one of us (JGG) with careful removal of the posterior hyaloid. The retina superior to the membrane was cauterized lightly, and a retinotomy was performed by gentle irrigation of balanced salt solution through a 33-gauge cannula, producing a focal retinal detachment in the macula. The intraocular pressure was elevated transiently, and a 130 0 subretinal spatula was used to separate the membrane from the underlying retinal pigment epithelium. The membrane was grasped with 130 0 subretinal forceps and removed in one piece through the retinotomy. A fluid-air exchange served to pneumohydraulically reattach the retina, and the retinotomy was surrounded by light focal endolaser. The second, more inferior subretinal membrane was treated focally with endolaser. The vitreous cavity was lavaged with a 20%
concentration of sulfur hexafluoride, and the sclerotomies and conjunctiva were closed with absorbable suture. Visual acuity improved to 20/60 at 1 week and 20/20 by 2 months postoperatively. fluorescein angiography performed I week and then 2 months after surgery demonstrated no evidence of subretinal neovascularization (Fig 2). The intact retinal pigment epithelium was mottled lightly beneath the temporal macula and fovea and at the laser sites. Six months after surgery, uncorrected distance visual acuity returned to 20/15 with near vision to Jaeger I + and was maintained at this level at the last follow-up examination 18 months after surgery. The lens has remained clear. There has been no recurrence of choroidal neovascularization. Case 2. A 56-year-old African-American man had decreased vision in the left eye after being kicked in the face during an altercation. Initial visual acuity was 20/400. Pupils were minimally reactive without afferent pupillary defect. Anterior segment examination disclosed a confluent subconjunctival hemorrhage and mild anterior segment cellular reaction. The lens was clear. Fundus findings included commotia retinae postequatorial in every meridian. A small hemorrhagic pigment epithelial detachment was present just nasal to the optic disc. A curvilinear choroidal rupture was noted inferotemporal to the central macula with an associated serous and hemorrhagic detachment of the neurosensory retina occupying approximately seven to eight disc areas within the posterior pole. There was no hemorrhage directly underlying the foveola. The patient was treated conservatively, and visual acuity improved to 20/20 6 weeks later. There was complete resolution of the serous and hemorrhagic macular detachment. Vision remained stable until almost precisely I year later, at which time he reported a sudden decline in vision associated with a central scotoma and metamorphopsia. Visual acuity was 20/200. A focal serous detachment of the sensory retina extended into the edge of the fovea associated with a rim of subretinal hemorrhage under the foveola. fluorescein angiography demonstrated a well-defined choroidal neovascular membrane in conjunction with subretinal hemorrhage arising from the choroidal rupture scar and extending into the foveal avascular zone.
Figure 1. A, preoperatively, three choroidal ruptures spare the fovea with choroidal neovascularization emanating from the choroidal rupture temporal to the fovea. The neovascular membrane (arrowheads) extends into the fovea and is associated with subretinal hemorrhage. B, fluorescein angiography demonstrates two contiguous well-defined choroidal neovascular membranes (large arrows) and a smaller isolated membrane (small arrow).
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Figure 2 . Postoperative photograph (A) and fluorescein angiogram (B) demonstrate mild mottling of the retinal pigment epithelium beneath the macula. A, the retinotomy (large arrow) is bordered by a laser scar, and the contiguous neovascular membrane is replaced by a dry laser scar (small arrow). There is no recurrence of choroidal neovascularization.
Surgical removal of the choroidal neovascular membrane was recommended, but shortly before surgery the patient had further visual loss to 20/400 associated with more extensive subretinal hemorrhage beneath the macula (Fig 3). A pars plana vitrectomy was performed by one of us (LPK) with removal ofthe posterior hyaloid. Intraoperatively, the subretinal hemorrhage was found to be diffuse with less than 1 mm of associated elevation. The hemorrhage was nearly completely aspirated through the retinotomy site. Using standard methods and instrumentation for submacular surgery, the neovascular complex was extracted, and gas-fluid exchange was performed with 20% sulfur hexafluoride. The retinotomy site was not treated. Distance visual acuity improved to 20/30 3 weeks after sur-
gery. A confluent area of retinal pigment epithelial depigmentation corresponded to the position of the extracted choroidal neovascular complex. Four months later, there was minimal subfoveal pigment epithelial disturbance with no evidence of persistent neovascularization clinically or angiographically (Fig 4). When last examined, 8 months after surgery, visual acuity remained at 20/30 and there was no evidence of recurrent neovascularization. Results of histopathologic examination by light microscopy showed a fibrovascular membrane lined on two surfaces by multilayered retinal pigment epithelial cells (Fig 5). A photoreceptor fragment was present. Case 3. A 12-year-old white boy was hit in the left eye with an ice ball. Initially, visual acuity was markedly reduced but
Figure 3. Fluorescein angiography demonstrates choroidal neovascularization at the superior end of a choroidal rupture. Subretinal hemorrhage extends beneath the fovea.
Figure 4 . Fluorescein angiography at 4 months after surgery discloses no recurrence of choroidal neovascularization. The retinal pigment epithelium is mottled corresponding to the extracted membrane and retinotomy site.
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Figure 5. There is an irregular monolayer of retinal pigment epithelium along the edge of the specimen. Melanophages and chronic inflammatory cells are present in the loose fibrous connective tissue (hematoxylin-eosin; original magnification, X400).
subsequently improved to 20/20. Approximately 7 months later, visual acuity deteriorated to 20/150. Anterior segment findings disclosed a superficial corneal scar. Results of fundus examination showed a choroidal rupture in the posterior pole of the left eye extending from a point just inferior to the optic disc to the center of the macula (Fig 6A). Fluorescein angiography demonstrated classic choroidal neovascularization in the center of the macula overlying the posterior end ofthe choroidal rupture (Fig 6B). Pars plana vitrectomy was performed by one of us (EdJ). A posterior vitreous detachment was created with the vitrector in aspiration mode and the posterior hyaloid removed. A retinotomy
was created just inferior to the choroidal neovascular membrane. A similar retinotomy was made just superonasal to the choroidal neovascular membrane. The subretinal space was separated from the overlying retina. Subretinal forceps then were introduced through the superior retinotomy, and the choroidal neovascular membrane was removed. The remainder of the membrane was removed through the inferior retinotomy. A fluid-air exchange was performed. The retinotomy sites were not treated focally. The sclerotomies and conjunctiva were closed. Visual acuity improved to 20/60 I week after surgery and to 20/50 after 2 months. The macula demonstrated an area of pigment epithelial atrophy and a small area of hemorrhage along
Figure 6. Preoperative photograph (A) and fluorescein angiography (B) before surgery demonstrate a single choroidal rupture extending from the inferior margin of the optic disc to the inferionasal macula, sparing the fovea. Choroidal neovascularization is present beneath the fovea and is associated with subretinal hemorrhage.
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Figure 7. Fundus photograph (A) and fluorescein angiography (B) taken 2 months after surgery shows mottling of the retinal pigment epithelium, sparing the fovea. The retinotomy is visible along the superior arcade.
the superotemporal arcade (Fig 7A). Auorescein angiography showed no persistent neovascularization (Fig 7B). Seven months after surgery, visual acuity improved to 20/25. The specimen was examined by transmission electron microscopy, which showed a fibrovascular membrane composed of a collagenous matrix with native collagen fibers and new collagen. There were scattered collections of homogenous electrondense material (Fig 8). The membrane was lined on one surface by multiple layers of retinal pigment epithelium. External to the pigmented epithelium, a zone of finely granular material with widely spaced collagen was present (Fig 9).
Figure B. A fibrovascular membrane is composed of a collagenous matrix with native collagen fibers (12-nm diameter) and new collagen (25-nm diameter). There are scattered collections of homogenous electron-dense material (original magnification, XIB,OOO).
Discussion Traumatic choroidal rupture typically produces immediate visual loss secondary to submacular and/or vitreous hemorrhage. The hemorrhage frequently reabsorbs, and vision often returns to near normal levels unless the defect in Bruch membrane involves the fovea or otherwise causes macular distortion. Subretinal neovascularization may produce late visual loss through creation of a serous neurosensory detachment of the macula with or without fresh subretinal hemorrhage. Choroidal neovascularization complexes are a common histopathologic finding during the early healing process of choroidal ruptures. The majority of these vessels apparently regress because the incidence of reported late complications is only 25% to 30%.10,11 Neovascularization beneath the retinal pigment epithelium was observed in only 1 of 39 autopsy specimens with indirect choroidal rupture. 12 There are clinical reports of subretinal neovascularization spontaneously involuting without treatment. 2 ,1l Extrafoveal membranes have been treated successfully with laser photocoagulation. 4 However, if the neovascularization extends beneath the foveal avascular zone, the ultimate visual outcome is poor, especially if the complex is associated with new hemorrhage. 5,10 Of the other entities associated with the development of subfoveal neovascularization, presumed ocular histoplasmosis syndrome and age-related macular degeneration have been studied the most. 13 The visual results of surgery are most apparent among patients with ocular histoplasmosis. This is likely attributable to the observation that the neovascular complex may have a solitary ingrowth site through a focal abnormality in Bruch membrane and grow anterior to the retinal pigment epithelium. 8 Patients with ocular histoplasmosis are usually young, have visual symptoms early in the disease process, and typically do
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Volume 103, Number 4, April 1996
Figure 9. The membrane is lined on one surface by multiple layers of retinal pigment epithelium. External to the pigmented epithelium, a zone of finely granular material with widely spaced collagen is present (original magnification, X6480).
not have a diffuse dystrophy of the choriocapillaris-Bruch membrane complex. 14,15 Gass 16 recently has described histopathologic findings in five patients with ocular histoplasmosis syndrome. The subretinal vessels were found to grow in the subsensory retinal space and to be engulfed partially by proliferating retinal epithelium. In particular, the duplicated retinal pigment epithelium was identified on the posterior surface ofthe new vessels. This may confuse histopathologic interpretation because excised tissue from surgical cases may give the erroneous impression that the neovascular membrane was removed from the subpigment epithelial space. 16,17 Gass 16 believes certain factors may predict whether a neovascular membrane will be located in the subsensory retinal space. These include age younger than 50· years, subretinal pigmented halo or plaque around the origin of neovascularization, sharply defined neovascular borders, absence of elevated pigment epithelium beyond the neovascular complex, and normal fellow eye. These are important because surgical excision may be less complicated and should yield better results with greater potential visual acuity in patients with the above characteristics. Although the neovascular complex technically can be removed in age-related macular degeneration, the visual results are not as good as in ocular histoplasmosis. In agerelated macular degeneration, unlike cases of presumed ocular histoplasmosis syndrome and other causes offocal choroiditis, active growth of choroidal neovascularization occurs primarily in the sUbpigment epithelial space rather than in the subretinal space. The neovascular complex in age-related macular degeneration develops a degree of attachment to the retinal pigment epithelium anteriorly, which is removed during surgery, thus destroying the function of the overlying retina. 16
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Elimination or reduction of the exudative retinal detachment produced by a choroidal neovascular membrane may allow for some improvement in vision, even iffoveal retinal pigment epithelium is absent. Recurrences occur within 5 to 8 months in at least one third of patients with either age-related macular degeneration or ocular histoplasmosis. 9 The natural history of exudative age-related macular degeneration is poor. Only a controlled study will resolve which patients will benefit the most. The submacular surgery trial, which has been funded by the National Institutes of Health, may clarify these issues. Subretinal neovascular membranes emanating from choroidal ruptures appear to behave similarly to those arising in the maculae of patients with ocular histoplasmosis. Patients are usually young and have focal defects in Bruch membrane with healthy surrounding retinal pigment epithelium. In addition, the choroidal neovascularization appears to grow anterior to the pigment epithelium in the subneurosensory retinal space. One patient in our series was older than 50 years of age but had no other retinal disease or dystrophy. The specimen from this patient had an irregular monolayer of retinal pigment epithelium covering both surfaces of the membrane similar to the findings described in ocular histoplasmosis. Because (1) most trauma-induced neovascular membranes regress spontaneously and (2) extrafoveal lesions often respond favorably to laser treatment, it is unlikely that many patients will present with subfoveal disease. To our knowledge, this is the first report of surgical excision of subfoveal neovascularization related to choroidal rupture. The membranes generally were separated easily from the underlying retinal pigment epithelium. Postoperative angiography demonstrated mottled transmission defects. There has been no neovascular recurrence after 1 year in
Gross et al . Subfoveal Neovascular Membrane Removal two patients, and recovery of excellent visual acuity was obtained in all three patients.
References 1. Gross JG, Freeman WR. Post traumatic yellow maculopathy. Retina 1990;10:37-41. 2. Smith RE, Kelly JS, Harbin TS. Late macular complications of choroidal ruptures. Am J Ophthalmol 1974;77:650-8. 3. Pearlstone AD. Delayed loss of central vision following multiple posterior segment trauma. Ann Ophthalmol 1980;12:409-11. 4. Fuller B, Gitter KA. Traumatic choroidal rupture with late serous detachment of macula: Report of successful argon laser treatment. Arch Ophthalmol 1973;89:354-5. 5. Luxenberg MN. Subretinal neovascularization associated with rupture of the choroid. Arch Ophthalmol 1986; 104: 1233. 6. deJuan E Jr, Machemer R. Vitreous surgery for hemorrhagic and fibrous complications of age-related macular degeneration. Am J Ophthalmol 1988;105:25-9. 7. Thomas MA, Kaplan HJ. Surgical removal of subfoveal neovascularization in the presumed ocular histoplasmosis syndrome. Am J Ophthalmol 1991; III : 1-7. 8. Thomas MA, Grand MG, Williams OF, et al. Surgical management of subfoveal choroidal neovascularization. Ophthalmology 1992;99:952-76.
9. Thomas MA, Dickinson JD, Melberg NS, et al. Visual results after surgical removal of subfoveal choroidal neovascular membranes. Ophthalmology 1994; 101: 1384-96. 10. Wyszynski RE, Grossniklaus HE, Frank KE. Indirect choroidal rupture secondary to blunt ocular trauma. A review of eight eyes. Retina 1988;8:237-43. 11. Hart JCD, Natsikos VE, Raistrick ER, Doran RML.Indirect choroidal tears at the posterior pole: a fluorescein angiographic and perimetric study. Br J Opthalmol 1980;64:5967. 12. Aguilar JP, Green WR.Choroidal rupture. A histopathologic study of 47 cases. Retina 1984;4:269-75. 13. Grossniklaus HE, Hutchinson AK, Capone A Jr, et al. Clinicopathologic features of surgically excised choroidal neovascular membranes. Ophthalmology 1994; 10 1: 1099-111. 14. Berger AS, Kaplan HJ. Clinical experience with the surgical removal of subfoveal neovascular membranes. Short-term postoperative results. Ophthalmology 1992;99:969-76. 15. Gass JDM. Pathogenesis of disciform detachment of the neuorepithelium. V. Disciform macular degeneration secondary to focal choroiditis. Am J OphthalmoI1967;63:66187. 16. Gass JDM. Biomicroscopic and histopathologic considerations regarding the feasibility of surgical excision of subfoveal neovascular membranes. Am J Ophthalmology 1994; 118:285-98. 17. Saxe SJ, Grossniklaus HE, Lopez PF, et al. Ultrastructural features of surgically excised subretinal neovascular membranes in the ocular histoplasmosis syndrome. Arch Ophthalmology 1993; 111 :88-95.
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