Ocular Symptoms of Moyamoya Disease Sachiko Noda, M.D., Seiji Hayasaka, M.D., Tomoichi Setogawa, M.D. and Shigeo Matsumoto, M.D. We examined four patients with moyamoya disease who had ocular symptoms. The diagnosis of the disease was based on an abnormal vascular network in the cerebral basilar region, observed by carotid angiography. One patient had amaurosis fugax. A second patient demonstrated bilaterally decreased visual acuity and visual spatial agnosia. The other two patients had homonymous hemianopsia; one also had transient diplopia and the other had temporal pallor of the optic disks. We found that patients with moyamoya disease exhibited various ocular symptoms but had few abnormal intraocular findings. MOYAMOYA DISEASE is defined as an abnormal vascular network in the cerebral basilar region caused by bilaterally occluded carotid arteries at the level of siphon. 1 2 It was first described as a type of occlusive disease of the internal carotid artery by Takeuchi. 3 The Japanese word moyamoya, which means misty, foggy, or smoky, derives from the characteristic angiographic picture of the abnormal vascular network in the cerebral basilar region. Although common in the Japanese population,' ,2,4 patients with moyamoya disease also have been reported in Europe. 5 Various ophthalmic findings such as visual field defect, nystagmus, decreased vision, homonymous hemianopsia, amaurosis fugax, and transient diplopia have been described in affected patients. 1 ' 7 Most cases of this disease have been reported by neurosurgeons; only a few have been described by ophthalmologists. Accepted for publication March 23, 1987. From the Departments of Ophthalmology (Drs. Noda, Hayasaka, and Setogawa) and Neurosurgery (Dr. Matsumoto), Shimane Medical University, Izumo, Japan. Reprint requests to Sachiko Noda, M.D., Department of Ophthalmology, Shimane Medical University, Izumo, Shimane 693, Japan. 812 Subjects and Methods We examined four patients with moyamoya disease who had ocular symptoms. The diagnosis, which was based on the characteristic angiographic findings, was confirmed in all patients by the Neurosurgery Department of our institution. The condition of each patient was determined by best corrected visual acuity, intraocular pressure, visual fields, central visual fields, and fundus examination with direct and indirect ophthalmoscopy. Case Reports Case 1 A 6-year-old boy was examined for a sudden onset of weakness of the limbs and amaurosis fugax (Table). Carotid angiography disclosed the classic abnormal vasculature of moyamoya disease. The posterior cerebral and ophthalmic arteries were patent. A computed tomographic scan of the brain appeared normal. The patient's visual acuity was R.E.: 20/32 and L.E.: 20/25 without correction. Intraocular pressure was 12 mm Hg bilaterally. Results of the remainder of the examination were normal. The boy underwent bilateral encephaloduroarteriosynangiosis, and had an uneventful postoperative course. Ten months after the original examination, his visual acuity had improved to 20/16 in both eyes. The visual fields showed a concentric contraction bilaterally. All other ocular findings appeared normal. Case 2 A 28-year-old man experienced numbness and motor paresis of the extremities (Table). Carotid angiography demonstrated the abnormal vascular network in the cerebral basilar region. The paresis gradually resolved with no treatment. At age 33 years, he complained of ©AMERICAN JOURNAL OF OPHTHALMOLOGY 103:812-816, JUNE, 1987 Moyamoya Disease Vol. 103, No. 6 813 TABLE SUMMARY OF PATIENT DATA PATIENT NO., AGE AT ONSET (YBS), SEX 1,6, M 2, 28, M 3, 62, M 4, 34, M CAROTID ANGIOGRAPHY Abnormal basilar network, bilaterally occluded carotid arteries at the level of siphon Abnormal basilar network, bilaterally occluded carotid arteries at the level of siphon Abnormal basilar network, bilaterally occluded carotid arteries at the level of siphon Abnormal basilar network, bilaterally occluded carotid arteries at the level of siphon COMPUTED TOMOGRAPHY OF BRAIN SYSTEMIC OCULAR SYMPTOMS SYMPTOMS SURGERY* Bilateral encephaloduro-arteriosynangiosis Right STA-MCA anastomosis Normal Weakness of limbs Decreased vision, amaurosis fugax Low density area in right temporal, parietal, and occipital regions Low density area in right occipital region, high density area in temporal region Low density area in right temporal, parietal, and occipital regions Numbness and motor paresis in the extremities, unsteady speech Left hemiparesis Decreased vision, central scotoma, visual agnosia Numbness in left hand Transient diplopia, left homonymous hemianopsia Evacuation of hematoma Left homonymous hemianopsia, temporal pallor of optic disks Right STA-MCA anastomosis S STA-MCA, superficial temporal artery-middle cerebral artery. wavering speech and decreased vision. He also suffered from visual spatial agnosia. Bilateral carotid angiography disclosed the characteristic vascular findings of moyamoya disease and an enlarged right ophthalmic artery. Computed tomography showed a low density area in the right temporal, parietal, and occipital regions of the brain. His visual acuity in both eyes was 20/100 corrected for myopic astigmatism (sphere -1.75 D, cylinder -1.25 D, axis 180 degrees). The peripheral visual fields were full, but both eyes had a relative central scotoma. A left homonymous hemianopsia was not detected. All other ocular findings appeared normal. The right superficial temporal artery and the middle cerebral artery were anastomosed surgically, and the postoperative course was uneventful. At age 34 years, the patient still had visual disturbances. His corrected visual acuity had increased to 20/50 in both eyes. All other ophthalmologic findings were normal. Case 3 A 62-year-old man was examined for the sudden onset of a visual field defect and transient diplopia (Table). Moyamoya disease was diagnosed based on the characteristic angiographic pattern. Six years later the patient was referred to our institution because of left hemi- paresis. Carotid angiography demonstrated an abnormal cerebrovascular network in the basilar region and bilaterally occluded carotid arteries at the level of siphon. Vertebral angiography showed a proximally occluded right posterior cerebral artery. Computed tomography disclosed a low density area in the right occipital region of the brain and a high density area in the right temporal region. A hematoma was surgically removed from that area. His visual acuity in both eyes was 20/20 corrected for myopic astigmatism (cylinder — 1.5 D, axis 90 degrees). Intraocular pressure was 14 mm Hg bilaterally. Visual field examination showed a left homonymous hemianopsia (Fig. 1). Cortical wheel-like opacities were noted in both lenses. All other ophthalmic findings appeared to be normal. Case 4 A 34-year-old man whose father (Patient 3) had moyamoya disease suffered from transient numbness in the left hand (Table). One year later he again experienced numbness and weakness in the same hand. Carotid angiography showed the classic findings of moyamoya disease (Fig. 2). The posterior cerebral arteries and ophthalmic arteries were patent. No abnormalities were detected on computed tomography of the brain. At age 36 years, the patient HO 105 90 73 60 120 103 90 75 60 '345 240 255 270 285 300 LEFT RIGHT Fig. 1 (Noda and associates). Patient 3. Visual field showing left homonymous hemianopsia. Fig. 2 (Noda and associates). Patient 4. Carotid angiography shows stenosis at the level of the siphon of the internal carotid arteries (long arrow) and abnormal vascular networks (short arrows). Top left, Anteroposterior projection and top right, lateral projection of right carotid angiography. Bottom left, Anteroposterior projection and bottom right, lateral projection of left carotid angiography. Vol. 103, No. 6 815 Moyamoya Disease 130 105 240 259 90 75 60 120 103 270 3B5 300 ~240 255 LEFT 90 75 60 270 285 300" RIGHT Fig. 3 (Noda and associates). Patient 4. Visual field of left homonymous hemianopsia. noticed a visual field defect. Computed tomography showed a low density area in the right temporal, parietal, and occipital regions of the brain. His visual acuity was 20/20 bilaterally with myopic correction (—6 D). The intraocular pressure was 15 mm Hg bilaterally. A visual field examination showed a left homonymous hemianopsia (Fig. 3). Both optic disks demonstrated a temporal pallor ophthalmoscopically. All other ocular findings appeared to be normal. He underwent right superficial temporal artery-middle cerebral artery anastomosis. The postoperative course was uneventful. Six months after surgery his visual field enlarged, with only a left lower homonymous quadrantanopsia remaining. Discussion Although our four patients were men, sexual prevalence has not been noted previously in moyamoya disease. 2 Additionally, no familial tendency has been reported, 2 even though two of our patients were father and son. The exact cause of the disease is still obscure. 2 Various ocular symptoms have been described in patients with moyamoya disease, 1 7 including visual field defects, nystagmus, de- creased vision, homonymous hemianopsia, amaurosis fugax, and transient diplopia. These signs are thought to originate from a circulatory disturbance of the ophthalmic or posterior cerebral artery. No circulatory disturbance of either cerebral artery was detected in our patients by carotid angiography, although one patient (Patient 3) had a proximal occlusion of the right posterior cerebral artery. The concentrically contracted visual fields noted in Patient 1 may be an artifact. Despite full peripheral fields Patient 2 had visual spatial agnosia, possibly caused by an occipital lesion. Left homonymous hemianopsia found in Patients 3 and 4 may have been associated with the occipital lesion detected by computed tomography. To our knowledge, the pallor of the optic disks observed in Patient 4 has not been previously described in moyamoya disease. The optic pallor may be caused by descending atrophy or postedematous atrophy. None of our patients had nystagmus or choked disks, which have been described in other patients with moyamoya disease. ',2'5 Rubeosis iridis, neovascular glaucoma, midperipheral intraretinal hemorrhages, narrowed retinal arteries, a cherry-red spot in the fundus, neovascularization of the disk or retina, retinal telangiectasia, and macular edema have been described after ipsilateral occlusion of the common carotid artery or severe bilateral ob- 816 AMERICAN JOURNAL OF OPHTHALMOLOGY s t r u c t i o n of the internal carotid arteries. ! M 0 Various ocular s y m p t o m s also h a v e b e e n n o t e d in aortic arch s y n d r o m e . " T h e i n t r a o c u l a r findings in m o y a m o y a d i s e a s e h a v e b e e n scarce. C o m m o n or internal carotid a r t e r y obs t r u c t i o n , aortic arch s y n d r o m e , a n d moyamoya d i s e a s e e v e n t u a l l y m a y be differentiated by the site of occlusion or s t e n o s i s . We found t h a t p a t i e n t s with m o y a m o y a d i s e a s e d e m o n strate v a r i o u s ocular s y m p t o m s b u t few intraocular findings. References 1. Suzuki, J., and Takaku, A.: Cerebrovascular "Moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch. Neurol. 20:288, 1969. 2. Nishimoto, A., and Takeuchi, S.: Moyamoya disease. Abnormal cerebrovascular network in the cerebral basal region. In Vinken, P. J., and Bruyn, G. W. (eds.): Handbook of Clinical Neurology, Vol. 12. Amsterdam, North-Holland Publishing Company, 1972, p. 352. 3. Takeuchi, K.: Occlusive diseases of the carotid artery (in Japanese). Shinkei Shimpo 5:511, 1961. 4. Karasawa, J., Kikuchi, H., Furuse, S., Sakaki, June, 1987 T., Yamagata, S., Nagata, I., Tanaka, H., and Kawamura, J.: Visual disturbance in moyamoya disease (in Japanese). Jpn. Rev. Clin. Ophthalmol. 72:540, 1978. 5. Valvo, A., Fiorillo, M., Lombardi, M., Muscella, R., and Pescosolido, E.: Ophthalmological manifestations in the Moya-Moya syndrome. In Francois, J., and Maione, M. (eds.): Paediatric Ophthalmology. London, John Wiley and Sons Publishing Co., 1982, p. 77. 6. Yoshida, T., Sakai, T., Ikeda, N., Abe, H., and Ichikawa, A.: Impairment of visual function in moyamoya disease (in Japanese). Neuro-ophthalmol. Jpn. 3:163, 1986. 7. Miyamoto, S., Kikuchi, H., Karasawa, J., Nagata, 1., Ihara, I., and Yamagata, S.: Study of the posterior circulation in moyamoya disease. Part 2. Visual disturbances and surgical treatment. J. Neurosurg. 65:454, 1986. 8. Brown, G. C , Magargal, L. E., Simeone, F. A., Goldberg, R. E., Federman, J. L., and Benson, W. E.: Arterial obstruction and ocular neovascularization. Ophthalmology 89:139, 1982. 9. Campo, R. V., and Reeser, F. H.: Retinal telangiectasia secondary to bilateral carotid artery occlusion. Arch. Ophthalmol. 101:1211, 1983. 10. Brown, G. C : Macular edema in association with severe carotid artery obstruction. Am. J. Ophthalmol. 102:442, 1986. 11. Hedges, T. R.: The aortic arch syndromes. Arch. Ophthalmol. 71:62, 1964.