42 STROKE VOL 9, No 1, JANUARY-FEBRUARY 1978

contraceptives and increased risk of cerebral ischemia or thrombosis. NEngl J Med. 288: 871-878, 1973

20. Masi AT, Dugdale M: Cerebrovascular diseases associated with the useof oral contraceptives, Ann Intern Med 72: 111-120, 1970

21. Schoenberg BS, Whisnant JP, Taylor WF, Kempers RD: Strokes inwomen of childbearing age. A population study. Neurology (Minneap)20: 181-189, 1970

22. Ford AB, Katz S: Prognosis after strokes, Part I, critical review.Medicine 45: 223-246, 1966

23. David NJ, Heyman A: Factors influencing the prognosis of cerebralthrombosis and infarction due to atherosclerosis. J Chron Dis 11:394^03, 1960

24. Lindgren SO: Course and prognosis in spontaneous occlusions of cerebralarteries. Acta Psychiatr Scand 33: 343-358, 1958

25. Pincock JG: Natural history of cerebral thrombosis, Ann Intern Med 46:925-929, 1957

26. Carter AB: Treatment of cerebrovascular disease. Practitioner 192:49-61, 1964

Dilated Episcleral Arteries — A SignificantPhysical Finding in Assessment of Patients

With Cerebrovascular Insufficiency

ROGER W. COUNTEE, M.D., A GNANADEV, M.D.,

AND PAMELA CHAVIS, M.D.

SUMMARY Dilated episcleral vessels associated with ipsilateralinternal carotid artery occlusions have been previously reportedthough not widely appreciated. These ocular changes have beenpresumed to be manifestations of ocular ischemia. The authors haverecently encountered this sign in seven patients and in none was thereevidence of ocular ischemia. In addition to an ipsilateral internalcarotid artery occlusion, arteriograms demonstrated that the majorsource of blood supply to the homolateral cerebral hemisphere was by

retrograde flow through markedly enlarged ophthalmic arteries filledin retrograde fashion from dilated external carotid collateralchannels in the orbit. This association of dilated episcleral arteries asa sign of increased orbital blood flow and the major source ofcollateral blood supply to the homolateral cerebral hemisphere hasnot been previously reported. We reemphasize the importance of acareful examination of the episcleral vessels in patients suspected ofhaving internal carotid artery occlusions.

A GREAT VARIETY of ocular signs have been describedin patients with cerebrovascular occlusive disease. Amongthese, dilated episcleral vessels associated with ipsilateralcarotid artery occlusion, presumably a sign of ocularischemia, have been previously reported.1'2 This associa-tion, however, has not been widely appreciated. The authorshave recently encountered seven instances of internal carotidartery occlusion associated with ipsilateral dilated episcleralarteries in six patients in whom no signs of ocular ischemiawere present. In addition, however, angiograms revealedthat the major source of blood to the affected hemisphereswas by way of markedly dilated ophthalmic arteries fillingretrograde from external carotid orbital collateral channels.This ocular sign, we believe, may imply increased orbitalblood flow and, therefore, carries additional physiologicalsignificance for the clinician in that it emphasizes the impor-tance of maintaining a patent external carotid artery.

Two representative cases are described.

Case Reports

Case I (H.L.)

A 57 year old, right-handed, hypertensive, white male wasadmitted to the Neurology Service of the East Orange, New

From the College of Medicine and Dentistry of New Jersey, New JerseyMedical School, Newark, NJ, and East Orange Veterans AdministrationHospital, East Orange, NJ.

Reprint requests to Dr. Countee, College of Medicine and Dentistry of NJ,NJ Medical School, Martland Hospital, 65 Bergen St., Newark, NJ 07107.

Jersey, Vetejans Administration Hospital in January, 1977,with a history of several episodes of transient weakness ofhis left side for three months prior to his admission. Fre-quently the episodes were accompanied by fleeting sensa-tions of giddiness and on one occasion with a complete lossof consciousness reported to have lasted 24 hours. The left-sided weakness on this occasion is said to have lasted about48 hours. However, the subsequent attacks lasted no morethan a "few minutes" to 2 to 3 hours. The patient was aknown hypertensive who had had two previous admissionsfor uncontrolled blood pressure elevations.

Upon hospital admission he was found to be generallyhealthy but aesthenic with normal blood pressure, mild left-sided weakness, and a right carotid bruit. Ophthalmologicexamination revealed markedly dilated and tortuous epi-scleral vessels in both eyes, which on slit lamp examinationproved to be dilated arteries (fig. 1). Fundoscopic and formalfield examinations were normal and vision was correctableto 20/20 bilaterally. Intraocular pressures were normal.Ophthalmodynamometry pressures were 40/20 in both eyes.

While in the hospital, the patient experienced several fleet-ing episodes of transient right upper extremity weaknesswhich often seemed to be related to postural changes.However, he reported no frank syncope or giddiness. Aorticarch angiography with selective catheterization of both com-mon carotids and the left vertebral arteries demonstratedcomplete occlusions of both internal carotid arteries and theright vertebral artery. There was modest stenosis at theorigins of both external carotid arteries which weremarkedly dilated and filled in retrograde fashion the

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DILATED EPISCLERAL ARTERIES/Counta? el al. 43

FIGURE 1. Dilated episcleral arteries in Case I.Though present in both eyes, the vascular patternsare not symmetrical.

ophthalmic arteries, distal intracranial internal carotidarteries, and their respective distributions on both sides. Theleft vertebral artery filled the vertebro-basilar circulationand there was some retrograde filling of both distal anteriorcerebral arteries via the posterior pericallosal artery on theleft.

CaseII(E.T.)

A 60-year-old, hypertensive, right-handed, white malewas admitted to the Neurology Service of the East OrangeVeterans Administration Hospital in June, 1976, one weekafter the sudden onset of a mild right-sided weakness. Dur-ing the 48 hours prior to admission, the patient reportedprogressive worsening of his right-sided weakness anddifficulty with his speech.

Examination on admission revealed a hypertensive withmild expressive aphasia, a moderately dense right hemi-paresis, and a mild right cortical sensory loss. A left carotidbruit was audible. A Tc 99m-technetium pertechnetate staticand dynamic brain scan showed evidence of a moderatelysized left fronto-parietal infarction and marked reduction inflow in the left middle cerebral artery distribution. His sub-sequent course of improvement was punctuated by a suddencomplete loss of vision in the left eye and worsening of hisaphasia and right hemiparesis on the 1 lth day after admis-sion. The previously noted left carotid bruit was no longeraudible. His aphasia and right hemiparesis improvedsomewhat after several hours although his visual lossremained unchanged. His fundoscopic examination was con-sistent with a central retinal artery occlusion presumed to bethe result of emboli from his diseased left cervical carotidartery.

After repeat brain scan revealed no change and a cerebro-spinal fluid analysis was normal, the patient was given an-ticoagulant therapy. After improvement in his aphasia andhemiparesis he was discharged. He remained amaurotic inthe left eye.

Four months later the patient was readmitted to theNeurology Service for revaluation. Though hisneurological deficit had impressively improved and his an-

ticoagulant therapy had been well controlled, bilateralcarotid bruits were noted on a recent clinic visit.Ophthalmologic examination revealed dilated episcleralarteries in the left eye, especially when compared to the right(fig. 2). Visual acuity was 20/20 in the right eye and 20/800in the left with a small residual island of vision in the tem-poral field. Fundoscopic examination was consistent with anold central retinal artery occlusion and ophthalmody-namometry was 30/10 L.E. and 100/40 R.E. Intraocularpressures were normal.

Selective arteriography showed occlusion of the left inter-nal carotid artery at its origin and modest stenosis of theorigin of the left external carotid artery which was dilatedand filled the intracranial left internal carotid artery and itsdistribution by retrograde filling of the greatly enlarged leftophthalmic artery. There was no evidence of collateral flowfrom the opposite carotid which was widely patent, or fromthe posterior circulation.

Discussion

Pavlou and Wolff1 first described dilated episcleral ves-sels in eyes ipsilateral to an internal carotid artery occlu-sion. They demonstrated by slip lamp examination dilata-tion of the arteries, arterioles, veins, and venules in 7patients: 4 patients had arteriograms documenting internalcarotid occlusions; in one patient an internal carotid arteryocclusion was presumed; two patients had known occlusionsof the homolateral common carotid arteries. No mentionwas made as to the status of the external carotid orophthalmic arteries. Reference was made to various visualsymptoms, including transient monocular blindness;however, details of the visual status in their patients were notreported. They concluded that the vessel changes weremanifestations of chronic ocular ischemia and hypoxia.

Knox, in 1965,2 reported five patients in whom dilatedepiscleral vessels were associated with occlusions of thecarotid arteries. In his patients, however, visual loss, diffuseepiscleral vascular congestion, rubeosis, retinal changes, andother signs of a fulminant ocular inflammation were promi-nent. All of his patients had either diffuse and severe aortic

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STROKE VOL 9, No 1, JANUARY-FEBRUARY 1978

FIGURE 2. (Case II). Dilatation of theepiscleral arteries of the left eye aredemonstrated.

arch occlusive disease and/or multiple small vessel occlusivedisease from diabetes. He concluded that the visual loss andinflammatory ocular changes were indeed due to ischemiaand hypoxia associated with multiple large vessel occlusionsand/or severe oligemia in the distribution of the ciliaryarteries as well as the central retinal artery.

In none of our 7 patients was there evidence of ocular in-flammation. Nor was there evidence of ongoing ocularischemia. Of the 7 patients whose carotid arteries werestudied, in only 1 was there any visual deficit. In this patientthe visual loss was of sudden onset, clearly the result of acentral retinal artery occlusion, and appeared fromarteriography to be from an embolus because theophthalmic artery and its collaterals were widely patent andthere was no evidence of propagated thrombus from the in-ternal carotid artery. The dilated episcleral arteriesdeveloped over the course of several months and wereassociated with the insidious recurrence of a carotid bruit

which appeared to represent increased flow through a dilatedexternal carotid artery.

Although ophthalmic artery pressures were significantlyreduced, on the affected side of all of our 7 patients, theophthalmic artery on arteriograms in each were not only pa-tent but markedly enlarged. This was associated with tor-tuously dilated arterial channels in the orbit which filled theophthalmic artery as well as the intracranial internal carotidartery and its distribution in a retrograde fashion. Loweredophthalmic artery pressures are probably necessary tofacilitate retrograde flow. In patients without signs of ocularischemia, visibly dilated episcleral arteries are evidence ofprominent collateral retrograde flow through enlarged or-bital collateral channels similar to the situation that Fisherhas pointed out with anastomotic channels about the orbitalrim.3

Dilated episcleral vessels may be an important physicalfinding in patients suspected of having an ipsilateral internal

FIGURE 3. Right common carotid arteriogramin Case I. The internal carotid is occluded at itsorigin in the neck. Dilated orbital arteries (a), areseen to fill retrograde the much enlargedophthalmic artery (b). which in turn fills the intra-cranial internal carotid artery (c) and its distribu-tion.

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DILATED EPISCLERAL ARTERIES/Cow/Hee et al. 45

carotid artery occlusion. Dilated episcleral arteries, par-ticularly in the absence of other stigmata of ocular ischemia,strongly suggest that the external carotid artery is the majorsource of blood supply to the homolateral cerebralhemisphere. Consequently, maintaining patency of the ex-ternal carotid artery in these situations is important.

References

1. Pavlou AT, Wolff HG: The bulbar conjunctival vessels in occlusion of theinternal carotid artery. Arch Int Med 104: 53-60, 1959

2. Knox DL: Ischemic ocular inflammation. Amer J Ophthal 60: 995-1001,1965

3. Fisher CM: Facial pulses in internal carotid artery occlusion. Neurology20: 476-478, 1970

Cerebrovascular Disease in Sickle Cell Anemia: A Clinical,Pathological and Radiological Correlation

KURT H. H. MERKEL, M.D., PAUL L. GINSBERG, M.D.,

JOSEPH C. PARKER, JR., M.D., AND M. JUDITH DONOVAN POST, M.D.

SUMMARY An opportunity to study cerebrovascular changes insickle cell anemia (SCA) presented itself when a black child with thisdisorder died of bihemispheric strokes. Angiography demonstratedsevere occlusive vascular disease involving primarily the circle ofWillis and major bifurcations of both internal carotid arteries.Collateral circulation to the distal branches of the internal carotidarteries occurred through transdural anastomoses from the externalcarotid system and via the leptomeningeal route. Perfusion of thebasal ganglia was accomplished by vessels arising from the proximal

internal carotid arteries. These changes resembled those ofMoyamoya disease. Autopsy showed old and recent cerebral infarcts.Two vascular processes were responsible for the arterial occlusions:(1) exuberant intimal hyperplasia, and (2) old and recent thrombiwith partial recanalization. The former has been described only oncebefore in SCA. Small vessels in the basal ganglia were exceptionallynumerous and dilated. We conclude that intimal hyperplasia withinlarge cerebral arteries may be responsible for infarction and smallvessel proliferation in basal ganglia in patients with SCA.

OVER 50 YEARS AGO, Sydensticker1 established thatsickle cell anemia (SCA) could have prominent neurologicmanifestations. A recent review of 89 cases of SCA, provenby electrophoresis to be homozygous for hemoglobin (SS),showed that 29% of the patients had developed neurologicalcomplications, and that 17% had had strokes.2 The patientwith SCA we studied arrived in coma as the result ofbilateral carotid artery occlusion. Angiography revealed apattern which is consistent with Moyamoya disease. Anautopsy showed thrombosis of major intracranial vesselswhile intimal hyperplasia, unusual in SCA, was also present.

Clinical Features

A 7-year-old black boy was admitted to JacksonMemorial Hospital with an acute alteration of con-sciousness. The patient was originally diagnosed as havingsickle cell anemia at the age of 7 months. Originally he hadedema of both hands and feet, was anemic, and had apositive sickle cell preparation. Subsequently, he had severalhemolytic crises. Seven months before this last admission,the child developed a right hemiparesis with hemianesthesia

From the University of Miami School of Medicine, Miami, FL 33152.Dr. Merkel is Resident in Neuropathology, Department of Pathology; Dr.

Parker is Professor of Pathology and Neurological Surgery and Director,Section of Neuropathology; Dr. Ginsberg is a neurologist in Hollywood, FL,and a member of the Department of Neurology; and Dr. Post is AssistantProfessor of Radiology.

Presented in part at the 53rd Annual Meeting of the American Associationof Neuropathologists Inc., June 17, 1977, Chicago, IL.

Reprint requests to Dr. Parker, Dept. of Pathology, Jackson MemorialHospital, U. of Miami School of Medicine, Miami, FL 33152.

and Broca's aphasia. This was accompanied by focal myo-clonic seizures involving his right arm and the right side ofhis face. He was given phenytoin and improved, but 4months later he suffered a similar episode, which left himwith moderately severe expressive aphasia. A Tc99(Technetium) brain scan was diagnostic for occlusion of theleft middle cerebral artery. His hemoglobin ranged between6-8 gm/dl, and his reticulocyte count between 10-40%.Prior to his last admission he had been irritable and waslater found comatose. In the emergency room, he wasstuporous, and had right spastic hemiparesis, a right gazepreference and right-beating jerk nystagmus. Hishemoglobin was 6.9 gm/dl, with a white cell count of 17,400per mm3 and 16% reticulocytes. The cerebrospinal fluid con-tained 11 white blood cells per mm,8 (45% granulocytes). Hewas treated with phenobarbital and diazepam and becamemore alert. Subsequently, an EEG revealed bilateral slow-ing, more marked on the left. Three days later, he becamefebrile (102.4°F) and more lethargic. Examination revealednuchal rigidity and a positive Brudzinski sign. A secondspinal tap showed 6850 red cells and 340 white cells per mm3

with 55% granulocytes and a protein of 322 mg/dl; CSFglucose levels were normal. Cultures of spinal fluid, bloodand urine were all negative. A brain scan (Tc99) showedanother area of increased uptake in the posterior righthemisphere. The child was treated with penicillin and atransfusion of 1000 ml packed cells after which he improvedslightly. Hemoglobin electrophoresis showed onlyhemoglobin A and S. Three days later he became comatosewith bilateral hyperreflexia, Babinski signs, a right gazepreference with nystagmus, bilateral decerebrate posturing

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R W Countee, A Gnanadev and P Chaviscerebrovascular insufficiency.

Dilated episcleral arteries--a significant physical finding in assessment of patients with

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 1978 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/01.STR.9.1.42

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