Cilioretinal Artery Occlusion in Young Adults with Central Retinal Vein Occlusion HOWARD SCHATZ, MD,t ANDREW C. O. FONG, MD/ H. RICHARD McDONALD, MD,t ROBERT N. JOHNSON, MD,t LEONARD JOFFE, MD,3 CHARLES P. WILKINSON, MD,4 JEAN-JACQUES de LAEY, MD,5 LAWRENCE A. YANNUZZI, MD,6 ROBERT T. WENDEL, MD,7 BRIAN C. JOONDEPH, MD,8 LOUIS V. ANGIOLETTI, MD,9 TRAVIS A. MEREDITH, MD 10

Abstract: Ten patients, all younger than 50 years of age, had a temporal cilioretinal artery occlusion associated with a nonischemic central retinal vein occlusion. On fluorescein angiography, the cilioretinal artery eventually filled in all but one eye. The cilioretinal artery showed pulsations on fluorescein angiography in five eyes. The central retinal vein occlusion eventually resolved and the fundus assumed a normal appearance in all nine of the followed cases. Eight of nine eyes that underwent follow-up examination had final visual acuity of 20/30 or better. The occlusion of the central retinal vein produces an elevation of intraluminal capillary pressure because the central retinal artery continues to pump blood into the retina. Because the perfusion pressure of the cilioretinal artery is lower than the central retinal artery, it becomes relatively occluded. The prognosis for these patients is generally good unless the entire parafoveal capillary net is affected by the cilioretinal artery that is occluded. Ophthalmology 1991; 98:594-601

Originally received: October 15, 1990. Revision accepted: December 27,1990. Retina Research Fund of St. Mary's Hospital and Medical Center, San Francisco. 2 Department of Ophthalmology, University of California, San Francisco. 3 Department of Ophthalmology, University of Arizona, Tucson. 4 Dean A. McGee Eye Institute, University of Oklahoma Health Sciences Center, Oklahoma City. 5 Department of Ophthalmology, University Hospital, Ghent, Belgium. 6 Department of Ophthalmology, Manhattan Eye, Ear and Throat Hospital, New York. 7 Department of Ophthalmology. University of California, Davis, and Mercy General Hospital, Sacramento. 8 Kresge Eye Institute, Wayne State University School of Medicine, Detroit. 9 New York Medical College and New York Eye and Ear Infirmary, New York. 10 Wilmer Institute, Johns Hopkins University School of Medicine, Baltimore. 1

Presented at the American Academy of Ophthalmology Annual Meeting, Atlanta, OctjNov 1990. Reprint requests to Howard Schatz, MD, 1 Daniel Burnham Court, Suite 210, San Francisco, CA 94109.

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We report on 10 patients, all younger than 50 years of age, who had a cilioretinal artery occlusion associated with a central retinal vein occlusion. We describe the clinical findings and angiographic characteristics of this syndrome. We also propose a pathogenesis.

RESULTS Of the 10 patients on whom we report, 5 were men and 5 were women, ranging in age from 23 to 44 years. The average and median age was 36 years. Most of the patients had no systemic problems (Table 1). At initial presentation, visual acuity ranged from 20/ 20 to hand motions. The intraocular pressure was normal in all patients. Complete ocular examination including slit-lamp examination and retinal biomicroscopy of all patients showed only retinal abnormalities of the involved eye. All 10 fellow eyes were normal. The retinal examination showed a nonischemic central retinal vein occlusion in all 10 patients and a temporal cilioretinal artery

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Table 1. Patient Characteristics Case No.

Age

Race

Sex

Initial Visual Acuity

Pulsations

Follow-Up

Final Visual Acuity

1 2 3

44 40 23

W W B

F M F

CF HM 20/40

Yes Yes No

4 yrs 6 mas 2 yrs

20/20 20/20 20/20

PMB and macula (partial) Lower PMB Upper PMB

Right Left Right

4 5

30 36

W W

F M

20/25 20/200

Yes No

3 yrs 6 mas

Yes No

3 mas 2 yrs

M

20/50

Yes

None

20/50

M F

20/60 20/25

No No

1 rna 1 rna

20/30 20/30

Nasal PMB PMB and entire parafoveal capillary net Superotemporal Superotemporal (above macula) Upper PMB and inferonasal (2 ciliaretinal artery occlusions Superotemporal Superotemporal

Left Left

20/20 20/100

20/20 20/ 200 20/20 20/20

6 7

39 33

W W

F M

8

42

W

9 10

31 38

W W

Systemic Disease and Drug Therapy Hypothyroid, estrogen Sickle cell, .hypertension, oral contraceptives Oral contraceptives Hypertension

Location Cilioretinal Artery Occlusion

Eye

Left Right Right Right Left

CF = counting fi ngers; PMB = papillomacular bundle; HM = hand motions.

occlusion, which was the onl y ischemic component. In one eye, there was an additional cilioretinal artery occlusion, nasall y (case 8). In seven patients, the vein occlusion was mild to moderate with few retinal hemorrhages. The vein occlusion was extremely hemorrhagic in three eyes. The ophthalmoscopic findings for cilioretinal artery occlusion included an apparently infarcted retina with cloudy swelling in th e area of th e cilioretinal artery. The location ofeach cilio retinal artery is listed in Table I. In one eye only (case 5), the entire foveal capillary net was fed by the occluded cilioretinal artery. Fluorescein angiography showed a typical central retinal vein occlusion with delayed filling and emptying of the central retinal vein, as well as dilation and tortuosity of the retinal veins. In all 10 eyes, there was some retinal vascular leakage. The capillaries filled (Fig I, case 2) in all but one case (case 5). In three eyes, the capillaries filled in a retrograde fashion. The cilioretinal artery eventually filled in all but one eye (case 5). Of the nine cases in which the cilioretinal artery filled on fluorescein angiography, pulsation occurred in five. These pulsations were characterized as follows: one frame of the fluorescein angiogram would show no filling of the cilioretinal artery; the next frame, taken within a few seconds, showed some filling of the cilioretinal artery; a subsequent frame would show emptying (no filling) of the cilioretinal artery (Fig 2, case 6). This sequ ence of events was repeated numerous times in those eyes where pulsations were seen. It appeared that systolic flow was sufficient to cause fluoresc ein to be seen in th e cilioretinal artery, but with d iastol e, the flow reversed . This indicated that there was no specific focal area of arterial obstruction (such as by a thrombus or embolus) but an intravascular resistance to flow with back and forth mo vem ents in response to systole and dia stol e. In two cases, filling was seen to be apparently steady but very sluggish. In one eye, the retina was pale in the area of the cilioretinal artery, suggesting that the ciliore-

tinal artery was occluded, but angiography showed that the cilio retinal artery filled normally. Presumably, th is eye had a partial or relative occlusion of the cilioretinal artery but subsequently reopened, perhaps as venous collaterals formed (Fig 3, case 10). All but one patient (case 8) were seen on at least one follow-up visit. This patient not seen in follow-up had a visual acuity of20/50 and the cilioretina l artery occlusion did not include the fovea. Eight of the nine patients who underwent follow-up examination did well ; final visual acu ity was 20/30 or better in all eight patients. Furthermore, the central retinal vein occlusion eventually resolved , and the fundus assumed a normal appearance in all nine of the followed cases. The cilioretinal artery reperfused in all nine cases. In one eye (case 6), the vein occlusion worsened with in I week and almost obscured the cilioretinal artery occlusion. The retina in the area of the cilioretinal artery occlusion remained pale, but fluoresc ein angiography showed that the cilioretinal artery had reopened. Five weeks later, the central retinal vein occlusion resolved with resolution of dilated and tortuous veins, and most of the hemorrhage and retinal edema. The cilioretinal artery appeared patent although narrowed. In the on e case in which visual acu ity did not improve (case 5), visual acuity remained at 20/200 throughout the follow-up period. This was due to the severe ischemia of the papillomacular bundle and entire parafoveal capillary net caused by the cilioretinal artery occlu sion. However, the central retinal vein occlusion did resol ve in this case.

DISCUSSION The central retinal vein occlusions in all 10 cases were typical cases of central retinal vein occlusion in young people (called papillophlebitisj.H In five cases, the vision 595

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Fig l. Top left , lop right, not ice the inferotemporal cilioretinal artery occlusion and the central retin al vein occlusion. Th e veins are dilated and tortuous and retinal hemorrh ages are present. Th e retina is pale and infarcted along the inferotemporal cilioretinal artery , Second row left. early arterial filling phase of the fluorescein angiogram. T he inferotemporal cilioreti nal artery shows on ly part ial filling. Second rowright, midarteriovenous phase fluorescein angiogram. The occluded cilioretinal artery shows onl y slightly more filling. Bottom , later arteriovenous phase angiogram . The cilioretinal artery shows still mor e filling.

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Fig 2. Top left. left fundus. Notice the pale retina in the area of the cilioretinal artery superotemporal to the disc and above the macula. Top right, very early filling phase of fluorescein angiogram. The cilioretinal artery shows no filling. Center left. a few seconds later, the cilioretinal artery superotemporal to the disc shows partial filling. Center right. a few seconds later, the cilioretinal artery shows no filling. Bottom left. a few seconds later, the cilioretinal artery shows partial filling. Bottom right. a few seconds later, the cilioretinal artery shows no filling.

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Fig 2 (continued) . Top left . a few seconds later, the cilioretinal artery shows partial filling. Top right. later arteriovenous fluorescein angiogram. Th e cilioretinal arte ry shows filling. Much of its capillary bed is not filled, although the parafoveal capillary net is filled. Center left . later phase fluorescein angiogram shows comp lete filling of the cilioretinal artery and its capillary bed. Note the dilated , tortu ous veins as part of central retinal vein occlusion. Center right. one week later, it appears the vein occlusion has worsened ; there are more hemorrhages and more dilation and tortu osity of the vein. The area ofcilioret inal artery occlusion is still pale, but it is not so apparent because of the retinal edema . Bottom left. midarteriov enous phase fluorescein angiogram shows complete filling of the cilioretinal artery . Notice the markedly dilated and tortuous retinal veins and hemorrhages. Bottom right. five weeks later, there appears to be resolution of the central retinal vein occlusion with much less vascular dilation and tortuosity. There is only one small retinal hemorrhage superotemporal to the fovea and below the disc. The area of infarction (white retina) has resolved.

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Fig 2 (continued). Arteriovenous phase fluorescein angiogram shows normal filIing of retinal arteries and veins.

was initially affected mostly by the presence of macular (foveal) hemorrhage or edema. On the clearing of the hemorrhage or edema, or both, vision improved. In all but one of the nine patients followed, there was no demonstrable focal area of obstruction, such as by thrombus or embolus. The cilioretinal artery occlusions were relative; five showed pulsations on fluorescein angiography and four showed gradual filling of the cilioretinal artery. Generally, the prognosis for this condition is quite good. McLeod and Ring" reported on four patients younger than 50 years of age with central retinal vein occlusion and cilioretinal artery occlusion. In all four patients, visual acuity recovered to 20/40 or better. Brown et al" reported three such cases in which two patients regained a visual acuity of 20/20 and one regained a visual acuity of 20/ 50. It appears that, because the cilioretinal artery occlusion is reversible, relative, and partial, the prognosis is good unless the cilioretinal artery involves all the parafoveal net and remains nonperfused (case 5).4 Although evidence of retinal infarction is present because of the presence of white (pale) retina in the area of the cilioretinal artery, it appears that visual function can improve. In all cases in which the fovea was partially involved by the occlusion, a visual acuity of 20/20 was eventually recovered. Brown et al 4 also demonstrated visual field improvement in their cases. With the exception of one ofour cases, initial visual reduction occurred from foveal hemorrhage and edema, but as the vein occlusion resolved , the hemorrhage and edema resorbed and visual acuity improved. The cause of central retinal vein occlusion in young people is not known, although a small number of patients do have systemic vascular disease . In those cases, the prognosis is often poor. 5 When no systemic vascular disease is present, the prognosis generally tends to be good, although it is not universally good. In a series of 103 young patients with central retinal vein occlusion who were followed for 6 months or more, 54 (52%) had no systemic

disease, and , of these, 11 (20%) had a visual acuity of 20/ 100 or worse on follow-up (Fong et ai, unpublished data) . In all 10 of our cases, the vein occlusion was nonischemic. All but one case resolved and did well visually. In three cases, the central retinal vein occlusion was seen and documented angiographically and photographically before the development of the cilioretinal artery occlusion. Therefore, it appears that cilioretinal artery occlusion occurs subsequent and probably secondary to central retinal vein occlusion. The question is, why would the cilioretinal artery become occluded, even partially so, after a central retinal vein occlusion? One theory proposes that the central retinal vein occlusion causes edema of the optic nerve and that the swelling causes occlusion of the cilioretinal artery. The optic nerve was not clinically edematous in six of our cases. Also, retinal artery occlusion is rare in patients who have papilledema. It appears that optic nerve edema and inflammation may possibly cause venous, but not arterial, occlusion." The occlusion is not thrombotic or embolic. The cilioretinal artery appears to be patent, but the flow is either extremely sluggish or even shows pulsation with systole. A more likely explanation relates to the perfusion pressure in the cilioretinal artery and the resistance to perfusion created by the central retinal vein occlusion. The occlusion ofthe central retinal vein produces an elevation of intraluminal capillary pressure because the central retinal artery continues to pump blood into the retina. However, the perfusion pressure of the central retinal artery is usually slightly higher than the perfusion pressure of the posterior ciliary artery circulation (which controls the perfusion pressure of the cilioretinal artery)." Therefore, the cilioretinal artery, with its lower perfusion pressure, cannot perfuse into the retinal capillary bed or does so only sluggishly or only with systole (this is the cause of the presence of systolic pulsation as seen on angiography within the cilioretinal artery). Therefore, the cilioretinal artery becomes relatively occluded; the occlusion is not embolic. This resistance to perfusion and relative closure of the cilioretinal artery appears to be temporary. This may be because the central retinal vein begins to establish collaterals within the optic nerve head causing the intraluminal pressure within the retinal capillaries to decrease, thereby allowing perfusion of the cilioretinal artery. Central or branch retinal artery occlusion or cilioretinal artery occlusion IS a rare phenomenon in young patients. It can be seen in association with systemic vascular diseases, such as diabetes and collagen vascular diseases (none of our patients); embolic diseases, such as with atrial myxoma; subacute bacterial endocarditis and other causes of emboli (none of our patients); inflammation, such as multifocal retinitis and other causes of retinitis (none of our patients); and with optic nerve tumors," It may be possible that cilioretinal artery occlusion associated with central retinal vein occlusion is more common than appreciated. It is interesting to note that only one of our patients had a fairly severe central retinal vein occlusion with ischemia of the papillomacular bundle related to the cilioretinal artery occlusion and no return of 599

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Fig 3. Top left. left fundus shows central retinal vein occlusion and an area of cilioretinal artery occlusion superotemporal and above the macula. Notice the pale, infarcted retina in this area. Top right, early arterial phase fluorescein angiogram . Notice that the cilioretinal artery is filled. The veins are dilated and tortuous . Center left , arteriovenous phase fluorescein angiogram shows normal filling of retinal capillaries. Center right. late arterio venous phase fluorescein angiogram shows delayed venous empt ying. Bot/om left, late phase fluorescein angiogram. Notice the disc leakage and scattered area of retinal vascular staining. Bottom right. one month later, notice that the central retinal vein occlusion appears to have resolved,

and the retina is no longer pale in the area of the cilioretinal artery occlusion.

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vision. It is possible that in more severe cases of central retinal vein occlusion, a cilioretinal artery occlusion may simply not be appreciated if there is a great deal of hemorrhage and retinal infarction. This may well be the case, especially since the presence of a cilioretinal artery occlusion is quite common." In our cases, in which only a relatively mild central retinal vein occlusion was present, the cilioretinal artery occlusion was more readily apparent than it might have been in a severe central retinal vein occlusion.

REFERENCES 1. Hunter CP, Thompson HS. Papillophlebitis. In: Blodi FC, ed. Current Concepts in Ophthalmology. Vol. IV St. Louis, MO: CV Mosby, 1974; 353-61.

2. Hayreh SS. Optic disc vasculitis. Br J Ophthalmol1972; 56:652-70. 3. McLeod 0, Ring CP. Cilio-retinal infarction after retinal vein occlusion. Br J Ophthalmol1976; 60:419-27. 4. Brown GC, Moffat K, Cruess A, et al. Cilioretinal artery obstruction. Retina 1983; 3:182-7. 5. Priluck lA, Robertson OM, Hollenhorst RW. Long-term follow-up of occlusion of the central retinal vein in young adults. Am J Ophthalmol 1980; 90:190-202. 6. Duker JS, Sergott RC, Savino PJ, Bosley TM. Optic neuritis with secondary retinal venous stasis. Ophthalmology 1989; 96:475-80. 7. Blumenthal M, Best M, Galin M, Gitter KA. Ocular circulation: analysis of the effect of induced ocular hypertension on retinal and choroidal blood flow in man. Am J Ophthalmol 1971; 71:819-25. 8. Hovland KR, Ellis PP. Hemorrhagic glaucoma with optic nerve glioma. Arch Ophthalmol 1966; 75:806-9. 9. Justice J Jr, Lehmann RP. Cilioretinal arteries: a study based on review of stereo fundus photographs and fluorescein angiographic findings. Arch Ophthalmol1976; 94:1355-8.

Discussion by David H. Orth, MD Schatz and co-authors present a series often patients with the clinical findings of cilioretinal artery occlusion associated with a central retinal vein occlusion in young adults. Regarding central retinal vein occlusion in young adults, in 1961, Lyle and Wybar' described seven cases of this disorder and termed it retinal vasculitis. Other terms have been used to describe this clinical entity, including papillo-phlebitis, mild retinal and papillary vasculitis, benign retinal vasculitis, and optic disc vasculitis.i? In 1980, Priluck and co-workers" performed a long-term follow-up study of patients 40 years of age and younger who were diagnosed as having occlusions of the central retinal vein. It appears that the prognosis was not as good in this group of young patients as previously described in the literature. Of the 42 patients studied, the visual acuity improved in 38%, worsened in 21%, and remained unchanged in 21%. There was no follow-up in 12%, and 7% underwent enucleation. There was also a 12% mortality rate by the end of the study. The second retinal vascular obstructive disorder described by Schatz et al is a cilioretinal artery occlusion. Cilioretinal artery obstructions usually fall into three distinct groups: I) isolated cilioretinal artery obstructions; 2) cilioretinal artery obstruction in conjunction with ischemic optic neuropathy; and 3) cilioretinal artery obstruction associated with a central retinal vein occlusion. McLeod and Ring 7 from Moorfie1ds Hospital, as well as Brown and co-authors" from Wills Eye Hospital, have described a series of patients similar to the report by Schatz et al. The theory on the pathogenesis of the cilioretinal artery occlusion presented by Schatz et al is similar to what has been presented by McLeod and Ring.? However, Schatz et al are the first to describe the pulsation characteristics within the cilioretinal artery in association with a central retinal vein occlusion in young adults. Schatz et al's hypothesis can be extrapolated to explain why cilioretinal artery occlusion in older patients with a central retinal vein obFrom the Irwin Retina Center, Ingalls Memorial Hospital, Harvey, and the Department of Ophthalmology, Rush-Presbyterian-St. Luke's Medical Center, Chicago.

struction is uncommon. These older patients frequently have arteriosclerotic disease involving the central retinal artery. This aging process within the walls of the central retinal artery may cause the perfusion pressure to approximate the lower pressure within the cilioretinal artery, and, thus, the capillary bed pressure is reduced and does not impede cilioretinal artery perfusion. The cases presented by Schatz and co-authors, as well as previous reports in the literature, demonstrate several important points, including: I) the extent of foveal involvement from the ischemic retinal whitening should be evaluated; 2) pulsatile characteristics within the cilioretinal artery can be demonstrated by fluorescein angiography when associated with a central retinal vein obstruction in young patients; 3) the venous occlusive component of this combined vascular disorder can be progressive; 4) the prognosis for final visual acuity may not be as good as previously described; 5) a medical work-up should be considered for patients presenting with this combined retinal vascular occlusive disorder. References 1. Lyle TK, Wybar K. Retinal vasculitis. Br J Ophthalmol1961; 45:77888. 2. Lonn L1, Hoyt WF. Papillophlebitis: A cause of protracted yet benign optic disc edema. Ey'e, Ear, Nose & Throat Monthly 1966; 45(10):628. 3. Cogan DG. In: Cant JS, ed. "William Mackenzie Centenary Symposium on the Ocular Circulation in Health and Disease," 1969;249-70. 4. Hart CD, Sanders MD, Miller SJH. Benign retinal vasculitis: clinical and fluorescein angiographic study. Br J Ophthalmol 1971; 55:72133. 5. Hayreh SS. Optic disc vasculitis. Br J Ophthalmol1972; 56:652-70. 6. Priluck lA, Robertson OM, Hollenhorst RW. Long-term follow-up of occlusion of the central retinal vein in young adults. Am J Ophthalmol 1980; 90:190-202. 7. McLeod 0, Ring CP. Cilio-retinal infarction after retinal vein occlusion. Br J Ophthalmol 1976; 60:419-27. 8. Brown GC, Moffat K, Cruess A, et al. Cilioretinal artery obstruction. Retina 1983; 3:182-7.

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