Journal of Neuro-Ophthalmology, March 1984, Volume 4, Issue 1

Retinal artery occlusion due to moyamoya disease.

Ophthalmic complications from moyamoya disease, or multiple progressive intracranial arterial occlusion syndrome, have rarely been reported. This case report describes a patient with this syndrome who developed acute retinal artery occlusion.

J. Clin. Neuro-opththalmol. 4: 31-34, 1984. Retinal Artery Occlusion Due to Moyamoya Disease RICHARD CHACE, M.D. THOMAS R. HEDGES, III, M.D. Abstract Ophthalmic complications from moyamoya disease, or multiple progressive intracranial arterial occlu­sion syndrome, have rarely been reported. This case report describes a patient with this syndrome who developed acute retinal artery occlusion. Introduction Moyamoya disease, or multiple progressive in­tracranial arterial occlusion syndrome, is charac­terized by stenosis of the arteries in and around the circle of Willis in association with a telangiec­tatic network of collateral vessels emanating from the base of the brain. Despite the proximity of this vascular occlusive process to the ophthalmic artery, retinal vascular abnormalities have been described only on rare occasions. 1.2 We observed a patient with moyamoya disease who suddenly developed retinal artery occlusion. Case Reports A 13-year-old white boy was admitted to the New England Medical Center with acute loss of vision, ophthalmoplegia, and pain involving the right eye. Ten days earlier, he awoke in the mid­dle of the night with right eye and right-sided head pain. He was able to go back to sleep, but the pain continued to be present in the morning. His parents noted the right upper eyelid to droop, and when it was elevated, the patient noted vision in the right eye to be diminished. His pediatrician noted orbital swelling and treated him with an­tibiotics suspecting orbital cellulitis. The pain sub­sided, but the poor vision in the right eye per­sisted. He saw an ophthalmologist who noted right third nerve dysfunction and retinal abnor­malities. The patient was referred to us for further evaluation. Previous examinations showed vision of 20/40 in the right eye and 20/200 in the left with From the Departments of Ophthalmology (RC,TRH) and Neu­rology (TRH), New England Medical Center, Tufts University School of Medicine, Boston, Massachusetts. March 1984 hyperopic astigmatism and left exotropia. He also had a history of seizures and at least one episode of transient hemiparesis. He had multiple con­genital abnormalities including symmetric reduc­tion defects of the limbs, flexion contractures of various joints, syndactyly, mild mental retarda­tion, and silvery hair. This constellation of abnor­malities has been labelled the "pseudothalidom­ide" or "SC-syndrome" (SC from the first initials of the surnames of the involved families).3 When we examined him, vision was counting fingers at 4 ft. in the right eye and 20/200 in the left. There was complete ptosis of the right upper lid, marked mydriasis with no light reaction in the right pupiL and severe dysfunction of all the extraocular muscles served by the third cranial nerve. The right fundus showed signs of retinal ischemia, including pallor in the macular area, scattered flame and dot hemorrhages, nerve fiber layer infarcts, and aneurysmal dilatations at sev­eral arteriolar bifurcations (Fig. 1). Both right and left optic nerve heads were anomalous, with situs inversus of the blood vessels and cupping. The right visual field was full to hand movement, and the left visual field showed no abnormalities with Goldmann perimetry. There were no cardiac, hematologic, or other systemic findings other than those described above. Routine blood studies including a com­plete blood count, blood sugar, and prothrombin and partial thromboplastin times were normal. Lumbar puncture showed clear, colorless fluid with 60 mg% glucose (normal 50-70 mg%), and 97 mg% protein (normal 15-45 mg%). Computerized tomography of the head showed a contrast enhancing mass lateral to the dorsum sella extending along the course of the right third cranial nerve. Cerebral angiography showed nar­rowing of the left carotid artery, occlusion of the left middle cerebral artery, narrowing of the bas­ilar artery, and occlusion of the M1 segment of the right internal carotid artery. There was a network of mutiple telangiectatic collateral arter­ies, supplied through various intracranial and extracranial routes, including the right ophthalmic artery (Fig. 2). The large vessel occlu­sions and the "puff of smoke" appearance of the anastomotic vessels are typical of moyamoya dis- 31 Moyamoya Disease Figure 1. Photograph of the right fundus showing diffuse macular ischemia, nerve fiber layer infarction, and areas of hemorrhage. (The fovea is in the upper center on the left. and to the left of the anomalous nerve head on the right). Figure 2. Cerebral angiogram showing complete occlusion of the M, segment of the internal carotid artery and the "puff of smoke" appearance of the collateral vessels supplying the brain beyond the site of occlusion. ease or multiple intracranial artery occlusion syn­drome. The mass seen on CT scan was removed neu­rosurgically and shown histopathologically to be a cavernous hemangioma within the right third nerve with evidence of intraneural hemorrhage. The specific patholoiYof this is the subject of a separate publication. Six weeks following admis­sion to the hospital, vision in the right eye re­mained counting fingers at 4 ft. The retinal edema had resolved, but there were several residual aneurysmal dilatations of the arterioles. Six months later the findings were unchanged. Discussion Moyamoya disease was first described by Jap­anese authors,S, 6 but has become more frequently recognized in the west.7 - IO This disease is char­acterized by narrowing or occlusion of both in- Journal of Clinical Neuro-ophthalmology ternal carotid arteries at the level of the carotid siphon, nonfilling of the circle of Willis, and development of a telangiectatic network of col­lateral blood vessels at the base of the brain. The term "moyamoya" is derived from the Japanese expression meaning "something hazy like a puff of smoke." Although the specific etiology of this is unknown, several investigators have suggested that the formation of the telangiectatic vessels is secondary to the more proximal cerebral vascular occlusions. 7 ,8 It has been theorized that at least some forms of this are due to an arteriosclerotic process involving the intracranial portion of the carotid artery and its branches. 12 In some cases it may be related to radionecrosis. 13 The occurrence of familial cases, 14,15 the association of other pe­ripheral vascular occlusive abnormalities,16 and the findings of biochemical abnormalities of con­nective tissue in some cases17 implies that moya­moya disease may be due to a metabolic abnor­mality which affects the walls of blood vessels with a predilection for those at the base of the brain. Others have observed that the pathology of this process is similar to that seen following severe vasospasm, and may represent dysfunc­tion of the arteries which secondarily leads to structural arterial abnormalities. 18 The "pseudothalidomide," or "S-C syndrome" is a rare, autosomally recessive, hereditary disease characterized by symmetric reductive defects of the limbs, flexion contractures of various joints, hypoplastic ear and nose cartilage, micrognathia, scanty silvery-blond hair, growth retardation, and, in some cases, mental retardation.)' 19 The feature of the syndrome which may be related to our patient's intracranial vascular abnormalities is the fairly frequent observation of large, nevus flammeus-like, capillary hemangiomas usually found in the mid face, but also in other extracran­ial areas, This vascular abnormality may be re­lated to the intracranial vascular occlusions caus­ing the moyamoya phenomenon in our patient as well as the vascular malformation affecting his third nerve. However, in cases of "pseudothali­domide" or "S-C syndrome" so far reported, including several autopsied patients, intracranial vascular occlusion has not been observed. Whether our patient's moyamoya syndrome is related to his other physical problems remains speculative. Because moyamoya disease is an abnormality primarily affecting the carotid artery in the area of the ophthalmic artery bifurcation, it is some­what surprising that there are only a few reports in which retinal vascular abnormalities have been observed. Tortuous, dilated retinal veins have been described, 1 and recently a case of acquired moyamoya disease has been reported in which hemorrhagic retinal vein occlusion occurred. 2 March 1984 Chace, Hedges However, there are several possible reasons why the occurrence of retinal vascular abnormalities may be unusual. The disease process is progres­sive, and may evolve slowly enough to allow for collateral circulation to the eye to develop via the external carotid circulation. The disease primarily affects young people whose vasculature has a greater ability to make the necessary hemody­namic adjustments to prevent the complications of arterial occlusion seen in older people. Fur­thermore, in most cases of moyamoya disease, the occlusive process occurs distal to the bifurca­tion of the ophthalmic artery and may spare circulation to the eye entirely. In our patient, cerebral angiography showed that the anastomotic network of vessels supplying the cerebral hemispheres was fed in part by the right ophthalmic artery. It is possible that this led to a steal phenomenon whereby blood normally supplying the eye was diverted intracranially leading to retinal infarction. The possibility of emboli from thrombus formed in the area of the carotid occlusion may have caused retinal infarc­tion. However, we observed no evidence of em­boli. Alternatively, if vasospasm is indeed the cause of this disorder, temporary occlusion of the carotid artery in the region of the ophthalmic bifurcation could explain the retinal infarction as well as the apparent hemorrhagic infarction which occurred within the tumor involving the patient's third nerve on the same side. Physicians involved in the care of patients with moyamoya disease should be aware of the retinal vascular complications of the disease. In addition, because it is being recognized more frequently, moyamoya disease should be considered in the differential diagnosis of retinal vascular occlu­sion, especially in young people. References 1. Slamovits, T, L, Klingele, T. G., Burde, R. M., and Gado, M. H.: Moyamoya disease with central ret­inal artery occlusion. f. Clill. Neuro-ophthalmol. 1: 123-127,1981. 2. Schoenberg, B. S., Mellinger, J. F" Schoenberg, D. G" and Barringer, F, S,: Moyamoya disease pre­senting as a seizure disorder. A case report. Arch. Neurol. 34: 511-512,1977. 3. Hermann, J., Feingold, M., Tuffli, G. A., and Opitz, J. M.: A familial dysmorphogenic syndrome of limb deformities, characteristic facial appearance and associated anomalies in the "pseudothalidomide" or "SC-Syndrome." Birth Defects 5: 81-89,1969, 4. Scott, R. M.: Third nerve palsy in a 14-year-old boy due to cavernous hemangioma of the third nerve. Concept. Pediatr. Neurosurg. 3: 100-107, 1983. 5. Nishimoto, A. and Takeuchi, S.: Abnormal cere­brovascular network related to the internal carotid arteries, J. Neurosurg. 29: 255-260, 1968. 33 Moyamoya Disease 6. Kudo, T.: Spontaneous occlusion of the Circle of Willis. A disease apparently confined to the Japa­nese. Neurology 18: 485-496, 1968. 7. Taveras, 1- M.: Multiple progressive intracranial arterial occlusions: A syndrome of children and young adults. Am. J. Roentgenol. 160: 235-268, 1969. 8. Coakham, H. B., Duchen, L. W., and Scaravilli, F.: Moyamoya disease: Clinical and pathological re­port of a case with associated myopathy. /. Neurol. Neurosurg. Psychiatry 42: 289-297, 1979. 9. Meriwether, R. P., Barnett, H. G., and Echols, D. H.: Moyamoya disease as a cause of subarachnoid hemorrhage in a negro patient. J. Neurosurg. 44: 620-622, 1976. 10. Godoth, N., and Hirsch, M.: Primary and acquired forms of moyamoya syndrome. Israel J. Med. Sci. 16: 370-377, 1980. 11. Leeds, N. E., and Abbott, K. H.: Collateral circu­lation in cerebrovascular disease in childhood via Rete Mirabile and perforating branches of anterior choroidal and posterior cerebral arteries. Radiology 85: 628-634, 1965. 12. Poor, G. Y., and Gacs, G. Y.: The so-called "moy­amoya disease." J. Neural. Neurosurg. Psychiatry 37: 370-377,1974. 13. Rajakulasingam, K., Cerrullo, L. J., and Raimondi, A. J.: Childhood moyamoya syndrome. Postradia­tion pathogenesis. Childs Brain 5: 467-475, 1979. 14. Kitahara, T., Argia, N., Yamaura, A., Makino, H., and Maki, Y.: Familial occurrence of moyamoya disease: Report of three Japanese families. J. Neurol. Neurosurg. Psychiatry 42: 208-214, 1979. 15. Yamada, H., Nakamura, S., and Kageyama, N.: Moyamoya disease in monovular twins: case re­port. /. Neurosurg. 53: 109-112, 1980. 16. Goldberg, H. J.: Moyamoya associated with pe­ripheral vascular occlusive disease. Arch. Dis. Child 49:964-966,1974. 17. Richman, D. T., Watts, H. D., Parsons, D., Schmid, K., and Glimcher, N. J.: Familial moyamoya asso­ciated with biochemical abnormalities of connec­tive tissue. Neurology 27: 382, 1977. 18. Carlson, C. B., Harvey, F. H., and Loop, J.: Pro­gressive alternating hemiplegia in early childhood with basel arterial stenosis and telangiectasia (moy­amoya syndrome). Neurology 23: 734-744, 1973. 19. Hall, B. D., and Greenberg, M. H.: Hypomelia­hypotrichosis- facial hemangioma syndrome. Am. /. Dis. Child. 123: 602-604, 1972. Write for reprints to: Thomas R. Hedges, III, M.D., Department of Ophthalmology, Tufts University School of Medicine, Boston, Massachusetts 02111. Journal of Clinical Neuro-ophthalmology