Exudative Retinal Detachment

Following Central and

Hemicentral Retinal Vein Occlusions David

Weinberg, MD;

Lee M.

Jampol, MD; Howard Schatz, MD; Kevin D. Brady,

\s=b\ We describe five eyes of five patients that developed an exudative retinal detachment following a central retinal vein occlusion (including one eye with a hemicentral [hemispheric] retinal vein occlusion). The time interval between the occurrence of the vein occlusion and the appearance of the retinal detachment ranged from 7 to 36 weeks in the four cases seen in the acute period. Each detachment involved the posterior retina and was associated with the development of marked retinal ischemia. Neovascular glaucoma occurred in two cases. The sub\x=req-\ retinal fluid completely or partially resorbed in the four eyes that were treated with retinal photocoagulation, but the final visual acuity was poor in all cases. Exudative retinal detachment is a potential complication of central retinal vein occlusion and in this series was associated with a poor visual prognosis.

moval. Detachments such have been referred to as

MD

these

ment that followed a central or hemicentral

nonrhegmatogenous, serous, secondary, or ex¬ udative and occur in a variety of is¬ chemie, inflammatory, neoplastic, and idiopathic conditions. Familiar clini¬ cal entities in which secondary retinal

retinal vein occlusion, with no other cause of detachment (Table). Initial evaluation included ocular and medical history, an eye examination including best corrected visual acuity and dilated examination of the fun¬ dus with direct and indirect ophthalmosco¬ py, as well as fundus photography and flu¬ orescein angiography. At least one complete examination was performed by one of us both before and af¬ ter the development of retinal detachment in four of the five cases. Fundus photo¬ graphs were performed following retinal detachment in all patients. Fluorescein an¬ giography was performed in four cases. One patient (case 1) was also studied with con¬ tact B-scan echography. Duration of followup ranged from 50 weeks to 9 years (mean, 38 months; median, 24 months).

detachments

occur

as

include central

se¬

chorioretinopathy, subretinal neovascularization, hypertensive choroidopathy, Coats' disease, Harada's disease, posterior scleritis, choroidal neoplasms, and many others. We re¬ rous

port the occurrence of exudative reti¬ nal detachment as a complication of central and hemicentral retinal vein occlusions.

PATIENTS AND METHODS Patients for this study were taken from our clinical records and were selected based on a history of exudative retinal detach-

REPORT OF CASES Case 1.—A 26-year-old woman presented with a 1-week history of reduced vision in

(Arch Ophthalmol. 1990;108:271-275) Patients With Retinal Detachment

"Tìetachment of the sensory retina in

the absence of a retinal break is a well-known clinical phenomenon. It may occur when fluid from the retinal or choroidal circulation leaks into the subretinal space and exceeds the com¬ pensatory mechanisms for fluid reAccepted for publication October 6, 1989. From the Department of Ophthalmology, Northwestern University Medical School, Chicago, Ill (Drs Weinberg and Jampol); the Retina Research Fund, St Mary's Hospital and Medical Center, and the Department of Ophthalmology, University of California, San Francisco (Dr Schatz); and the University of Colorado School of Medicine, Denver (Dr Brady). Reprint requests to Department of Ophthalmology, Northwestern University Medical School, 303 E Chicago Ave, Ward Bldg 2-186, Chicago, IL 60611 (Dr Jampol).

Patient

1/26/F

Subsequent

Time

No. /Age,

y/Sex

Following CRVO*

Associated

Eye OS

Conditions

Initial Vision

DM

to

RD,

wk

24

Initial Presentation Good

perfusion 2/56/M

OD

HTN, DM,

CF

Good

CAD

3/69/M

OS

HTN

4/72/F

OD

HTN,

perfusion Good

perfusion Uncertain

Not

seen

Course

Final

(Time, wk) Nonperfusion (28), NVD (28), NVI (28), NVG (32) Nonperfusion (52), NVD (52), NVI (78), NVG (78) Nonperfusion (27) Nonperfusion

Vision NLP

NLP

LP

AMD 5/18/M

OD

20/200

7

Good

perfusion

Nonperfusion (6), NVD (6), traction

20/200

*CRVO indicates central retinal vein occlusion; RD, retinal detachment; DM, diabetes mellitus; NVD, neovas¬ cularization of the disc; NVI, neovascularization of the iris; NVG, neovascular glaucoma; NLP, no light percep¬ tion; HTN, hypertension; CAD, coronary artery disease; CF, counting fingers; AMD, age-related macular degen¬ eration; and LP, light perception. Time to RD indicates time between onset of symptoms and first observation of retinal detachment; time in parentheses under "Subsequent Course" indicates interval from Initial examina¬ tion with good perfusion to development of nonperfusion, NVD, NVI, or NVG.

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her left eye. Her ocular history was unre¬ markable. Her medical history was signif¬ icant for hypothyroidism and for insulindependent diabetes mellitus for 7 years. Best corrected visual acuity was 20/20 OD and 20/40 OS. There was no relative af¬ ferent pupillary defect. Slit-lamp examina¬ tion showed no abnormality. Examination of the right fundus showed mild back¬ ground diabetic retinopathy. Findings in the left eye included blurring of the disc margins, retinal venous dilation, extensive superficial retinal hemorrhages, and a few cotton-wool spots (Color Fig 1). Fluorescein angiography showed scattered microaneu¬ rysms and intraretinal hemorrhages in the right eye and, in the left eye, retinal vascu¬ lar abnormalities consistent with a central retinal vein occlusion with good capillary

perfusion.

Seven weeks later the vision in the left was reduced to hand motions. A left af¬ ferent pupillary defect was present. No rubeosis iridis was seen. The left fundus showed increased intraretinal hemor¬ rhages and retinal thickening (Color Fig 2). Fluorescein angiography showed mild cap¬ illary nonperfusion and macular capillary eye

leakage.

At 24 weeks, the vision in the left eye re¬ mained hand motions. The iris had no neovascularization. There was now an infe¬ rior exudative retinal detachment. No disc or retinal neovascularization was seen. At 28 weeks, for the first time, definite rubeosis iridis was seen at the left pupillary margin. Intraocular pressures were 16 and 10 mm Hg in the right and left eyes, respectively. The left fundus demonstrated massive intraretinal edema and hemor¬ rhage, as well as extensive exudative de¬ tachment involving the entire posterior pole and inferior retina (Color Fig 3). Neovascularization of the disc was present. B-scan echography demonstrated shifting subretinal fluid. There was no fractional

component.

Argon green scatter photocoagulation applied to the left retina. Despite this, the left eye developed progressive rubeosis iridis, neovascular glaucoma, and vitreous hemorrhage. Although the amount of sub¬ retinal fluid subsequently decreased signif¬ icantly, vision diminished to no light per¬ ception by 34 weeks. The subretinal fluid was

gone at 50 weeks. Case 2.—A 56-year-old man complained of blurred vision in his right eye for 3 weeks. His ocular history was unremarkable. His was

medical

history

was

significant for adult-

mellitus, hypertension, and lumbar radiculopathy. He had undergone coronary artery bypass surgery. Vision was counting fingers in the right

onset diabetes

eye and 20/20 OS. There

was no relative af¬ ferent pupillary defect. Slit-lamp examina¬ tion results were normal. Intraocular pres¬ sures were 14 mm Hg in each eye. Fundus examination showed venous dilation with extensive deep and superficial intraretinal hemorrhages, especially in the peripapil¬ lary area, consistent with a central retinal vein occlusion (Color Fig 4). The left fundus normal. Fluorescein angiography was showed blockage by the hemorrhage, but

the retinal capillary perfusion appeared well preserved (Fig 1). At 36 weeks, the vision was light percep¬ tion. A right afferent pupillary defect was present. A small exudative retinal detach¬ ment was present in the right eye. At 52 weeks, the vision was light perception. Slitlamp examination results remained nor¬ mal, with no rubeosis iridis. Fundus exam¬ ination showed extensive elevation of the posterior retina, extending to the equator, with turbid subretinal fluid and exúdate (Color Fig 5). Fluorescein angiography showed substantial nonperfusion of the el¬ evated retina in the midperiphery and probable neovascularization of the disc (Fig 2). Over the following months rubeosis iri¬ dis, neovascular glaucoma, and dense vitre¬ ous hemorrhage developed, with deteriora¬ tion of vision to no light perception. The patient has been followed up for 2 years. Dense vitreous hemorrhage has pre¬ cluded any further view of the fundus. Case 3.—A 69-year-old man complained of 3 weeks of reduced vision of the left eye. His medical history was significant only for

hypertension. Visual acuity was 20/20 OD and 20/40 OS. Slit-lamp examination results were nor¬

mal. Fundus examination showed a left central retinal vein occlusion. Fluorescein angiography demonstrated good capillary

perfusion. Ophthalmoscopy and fluorescein angiography of the right eye were normal.

Ten weeks later vision in the left eye was 20/100. Much more retinal hemorrhage was present. Fluorescein angiography still showed good capillary perfusion. At 27 weeks, the vision in the left eye was 3/200. An exudative detachment was observed ex¬ tending inferiorly from the inferior papillomacular bundle. Fluorescein angiography showed macular edema and nonperfusion primarily localized to the area of the de¬ tachment. At 49 weeks the vision remained 3/200 and the inferior retinal detachment persisted, now with extensive subretinal exúdate. Grid photocoagulation was ap¬ plied to the left macula and scatter photocoagulation was applied to the area of detached retina. Two months later the ret¬ ina was flat; however, the visual acuity was reduced to 1/200. Case 4.—A 72-year-old woman was re¬ ferred for evaluation of suspected subreti¬ nal neovascularization of the left macula. She had been diagnosed as having a central retinal vein occlusion in the right eye 3 years previously. Her medical history was significant for hypertension, rheumatoid arthritis, peptic ulcer disease, and chronic obstructive pulmonary disease. Vision was light perception in the right eye and 20/30 OS. Slit-lamp examination results were normal. Fundus examination showed evidence of an old ischemie, central retinal vein occlusion in the right eye with some hard exúdate, a few hemorrhages, venous tortuosity, and narrowed arteries. The macula was thickened and there was evidence of an exudative retinal detach¬ ment extending from the disc superonasally to the equator of the right eye from 12:30 to 2:30 o'clock. In the left eye a probable area of subretinal neovascularization was seen

above the macula. A fluorescein angiogram on the right showed marked widespread is¬ chemia of the entire posterior pole and midperiphery with no neovascularization. A perifoveal area of subretinal neovascu¬ larization in the left eye was identified and treated with photocoagulation. Panretinal photocoagulation including the area of detachment was applied to the right eye. Four weeks later, the extent of the retinal detachment was unchanged. Additional panretinal photocoagulation was applied. After an additional 3 weeks, the vision in the right eye remained light perception. The retina was still partially detached. Case 5.—An 18-year-old man complained of 5 days of blurred vision involving pre¬ dominantly the superior visual field of his right eye. His ocular and medical histories were negative. Visual acuity was 20/200 OD and 20/25+ OS. There was no afferent pu¬ pillary defect. Slit-lamp examination re¬ sults were normal in each eye. Intraocular pressures were 15 mm Hg in each eye. Fun¬ dus examination revealed massive nerve fiber layer hemorrhage and edema in the inferior retina, with minimal spread of hemorrhage above the horizontal raphe. Most of the major abnormalities were in the distribution of an inferior hemicentral ret¬ inal vein, with the site of the obstruction being in the disc. There was slightly in¬ creased tortuosity of the superior arteries and distention of the superior veins. The fundus of the left eye was normal. Fluores¬ cein angiography showed extensive block¬ age by the hemorrhage, staining of the in¬ ferior veins, and extensive leakage inferiorly extending into the macula. An extensive medical evaluation showed nothing abnormal. Computed tomography of the brain and orbits, with infusion, was also normal. No significant change in the examination results was noted until 6 weeks later. At that time vision in the right eye was 20/400. There was no afferent pupillary defect. There was neovascularization seen on the right disc and an inferior exudative retinal detachment approximating the distribu¬ tion of the vein occlusion. Argon photoco¬ agulation was applied to areas of attached inferior retina. Three weeks later the vision in the right eye was reduced to counting fingers. There was still no rubeosis iridis, but the neovas¬ cularization of the disc appeared worse. Additional photocoagulation was applied. After an additional 6 weeks, the vision had returned to 20/400 OD. A right afferent pupillary defect was observed. A fresh vit¬ reous hemorrhage obscured the inferior retina of his right eye. Over the next 3 weeks, the disc neovascularization contin¬ ued to progress. Scatter photocoagulation was again applied to the peripheral retina, including the superior periphery. Over the next month there was dramatic regression of the disc neovascularization, as well as reduction of the retinal edema and eleva¬ tion. Over the next several months the ne¬ ovascularization regressed to a fibrous stalk, and the exudative detachment re¬ solved.

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Color Fig 1.—Case 1. Central retinal vein occlusion at the time of pre¬ sentation with moderate hemorrhage and few cotton-wool spots.

Color Fig 2.—Case 1. Seven weeks later, worsening of retinal hemor¬ rhage and edema are seen. Color Fig 3. Case 1. Markedly elevated exudative retinal detachment is seen.

Color Fig 4.—Case 2. Central retinal vein occlusion with extensive hemorrhage.

—

Color Fig 5.—Case 2. Extensive subretinal fluid and exúdate involving the entire posterior pole.

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Fig 1.—Case 2. Early venous phase of fluorescein angiogram demon¬ strating blockage by hemorrhage, but good capillary perfusion.

The patient has now been followed up for 9 years. His vision has stabilized at 20/200 OD, with a residual small peripapillary traction retinal detachment and a macular fold. RESULTS

The Table summarizes the clinical data on these five patients. All patients were white and ranged in age from 18 to 72 years (mean, 48 years). Three pa¬ tients were male and two were female. The right eye was affected in three pa¬ tients and the left in two. Two of the patients were diabetic. Three had a history of hypertension; one of these had undergone previous coronary ar¬

tery bypass

surgery.

One patient had age-related macu¬ lar degeneration with subretinal neo¬ vascularization in the fellow eye. There was no evidence of subretinal neovascularization in the eye with the central retinal vein occlusion at any time during the study. None of the pa¬ tients had a history of glaucoma, ele¬ vated intraocular pressure, or evidence of glaucomatous optic nerve damage before the development of the vein oc¬ clusion. Two patients with central retinal vein occlusion presented with 20/40 vision and two with counting fingers or worse. The patient with the hemicentral (hemispheric) retinal vein occlu¬ sion presented with 20/200 vision. The time interval between onset of symp¬ toms and detection of retinal detach¬ ment ranged from 7 to 36 weeks. Pa¬ tient 4 was not seen until 3 years after the vein occlusion, so the time of de¬ velopment of the detachment was un¬ certain. The central retinal vein occlusion was associated initially with good cap¬ illary perfusion in all four cases seen

Fig 2.—Case 2. Late phase of fluorescein angiogram demonstrating marked capillary nonperfusion of the elevated retina. Hyperfluorescent area represents probable disc neovascularization.

during the early phase of their disease. There was a progression to ischemia in these four cases, the time interval be¬ ing 6 to 52 weeks. Patient 4 was is¬ chemie when first seen 3 years after the vein occlusion. In three eyes neovascularization de¬ veloped on the disc 6 to 28 weeks after the vein occlusion and about the same time or slightly after the retinal de¬ tachment was noted. Two of these pa¬ tients were diabetic, and in both rube¬ osis and neovascular glaucoma devel¬ oped. Neither of these patients demonstrated proliferative diabetic retinopathy or rubeosis iridis in their fellow eye. In all four eyes in which photocoag¬ ulation was performed, there was a decrease in the amount of subretinal fluid. In no case did the subretinal fluid resorb spontaneously, but this might have occurred had we not intervened. Final visual acuity was 20/200 in the eye with the hemicentral retinal vein occlusion, 1/200 in the one case, and light perception or worse in the others. COMMENT

The most common, visually signifi¬ complications of central retinal vein occlusion include retinal hemor¬ rhage, macular edema, retinal is¬ chemia, rubeosis iridis leading to neo¬ vascular glaucoma,^ and, less fre¬ quently, neovascularization of the disc or retina.1 Metzler and associates2 described 7 of 35 patients with central or branch retinal vein occlusions who also had retinal detachment. However, these detachments were peripheral and re¬ sembled retinoschisis, in contrast to our patients, whose detachments were predominantly posterior and exuda¬ tive. cant

Rhegmatogenous retinal detach¬

ments have been described in associa¬

tion with branch retinal vein occlusion34 and central retinal vein occlusion.3 Retinal breaks were not found in any of our patients. Fujino and associates5 made brief reference to a "localized detachment inferior to the disc" observed 2 hours following ex¬ perimental occlusion of the central retinal vein by neoprene inj ection in an owl monkey. Schatz and associates6'7 described localized exudative retinal detach¬ ment following branch retinal vein oc¬ clusion in eight patients. These detach¬ ments occurred in the quadrant af¬ fected by the vein occlusion and were proportional in size to the area of non¬ perfusion. No neovascularization was seen in any of the eyes. There was complete resolution of subretinal fluid in all six eyes treated in the quadrant of detachment with photocoagulation. A similar case mimicking Coats' dis¬ ease has also been described.8 Vascular leakage following central retinal vein occlusion has been shown to be a common initial finding by flu¬ orescein angiography9 and by vitreous fluorophotometry.'011 This leakage tends to be transient, and persistence of leakage months later is associated with a poorer visual prognosis.'"0 It is uncertain which factor or fac¬ tors caused the extensive collection of subretinal fluid in our patients. Severe damage to the retinal capillary bed with nonperfusion was present in all 5 cases. It is possible that these patients represent the extreme end of the con¬ tinuum of vascular damage and incom¬ petence of retinal vessels. Extreme fluid leakage leads to collection of fluid under the retina. Impaired retinal pig¬ ment epithelial and retinal capillary

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endothelial pumping function may also play a role. It is also possible that in these pa¬ tients the fluid that leaks from the vessels is somehow abnormal or con¬ tains abnormal substances that con¬ tribute to impaired résorption. A higher than expected incidence of ab¬ normalities of plasma lipoproteins, immunoglobulins, and viscosity has been demonstrated in patients with retinal venous occlusive disease.1214

In addition to vasculopathy, in¬ creased hydrostatic pressure undoubt¬ edly contributes to leakage following vascular occlusion. Venous collaterals frequently develop at the disc follow¬ ing central retinal vein occlusion or within the retina following branch retinal vein occlusion15 and serve to bypass the occluded outflow channels. An absence of retinal venous collater¬ als was observed in eyes that developed retinal detachments after branch ret-

inai vein occlusion.7 The presence of disc collaterals was observed to be as¬ sociated with improvement in visual acuity following complete central ret¬ inal vein occlusion in young adults.16 Interestingly, venous collaterals were not observed in any of our patients. This failure to develop collaterals also may have contributed to the develop¬ ment of a detachment.

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neovascularization with retinal vein occlusion.

Ophthalmology. 1983;90:488-506. 2. Metzler U, Holmann R, Kaskel D. Netzhautablosungen bei verschlussen der Zentralvene oder ihrer Aste. Klin Monatsbl Augenheilkd. 1974;164:251-254.

3. Zauberman H. Retinopathy of retinal detachment after major vascular occlusions. Br J

Ophthalmol. 1968;52:117-121. 4. Lembach RG, Davidorf FH.

Acute onset of central retinal vein occlusion and retinal detachment. Ann Ophthalmol. 1975;7:983-984. 5. Fujino T, Curtin VT, Norton WD. Experimental central vein occlusion. Arch Ophthalmol.

1969;81:395-406. 6. Schatz H, Yannuzzi L, Stransky TJ. Retinal

detachment secondary to branch vein occlusion, I. Ann Ophthalmol. 1976;8:1437-1452. 7. Schatz H, Yannuzzi L, Stransky TJ. Retinal detachment secondary to branch vein occlusion, II. Ann Ophthalmol. 1976;8:1461-1471. 8. Scimeca G, Magargal LE, Augsburger JJ. Chronic exudative ischemic superior temporal\x=req-\ branch retinal-vein obstruction simulating Coat's disease. Ann Ophthalmol. 1986;18:118-120. 9. Laatikainen L, Kohner EM. Fluorescein angiography and its prognostic significance in central retinal vein occlusion. Br J Ophthalmol.

1976;60:411-418.

10. Chahal P, Fallon TJ, Chowienczyk PJ, Kohner EM. Quantitative changes in blood-retinal barrier function in central retinal vein occlusion. Trans Ophthalmol Soc UK. 1985;104:861-863. 11. Chahal PS, Fallon TJ, Kohner EM. Measurement of blood-retinal barrier function in

central retinal vein occlusion. Arch Ophthalmol. 1986;104:554-557. 12. Zegarra H, Gutman FA, Conforto J. The natural course of central retinal vein occlusion.

Ophthalmology. 1979;86:1931-1939. 13. Dodson PM, Galton DJ, Hamilton AM,

Black RK. Retinal vein occlusion and the prevalence of lipoprotein abnormalities. Br J Ophthalmol. 1982;66:161-164. 14. McGrath MA, Wechsler F, Hunyor ABL, Penny R. Systemic factors contributory to retinal vein occlusion. Arch Intern Med. 1978;138:216-220. 15. Henkind P, Wise GN. Retinal neovascularization, collaterals, and vascular shunts. Br J

Ophthalmol. 1974;58:413-422.

16. Priluck IA, Robertson DM, Hollenhorst RW. Long-term follow-up of occlusion of the central retinal vein in young adults. Am J Ophthal-

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