Journal of Neuro-Ophthalmology, June 1981, Volume 1, Issue 2

Moyamoya disease with central retinal vein occlusion. Case report.

1. Clin. NeuW-llphth.llnlll/. 1: 123-127. l0tll. Moyamoya Disease with Central Retinal Vein Occlusion Case Report THOMAS L. SlAMOVITS, M.D. TERENCE G. KlINGELE. M.D. RONALD M. BURDE, M.D. MOKHTAR H. GADO, M.D. Abstract A -15-year-old woman who was seen for symptoms of blurr;d vision in the left eye due to central retinal vein occlusion, was found to have a left homonymous hemianopia; carotid angiography demonstrated moya­moya disease. Movamova disease is characterized by progres­sive o~c1usi~n of intracranial arteries, usually at the level of the carotid syphon. Seizures, headaches. and visual disturbances are common presenting symptoms. Recently we saw a patient with visual complaints related to hemorrhagic retinopathy. In­vestigation led to a diagnosis of moyamoya disease. Case Report A 45-year-old white woman was referred for ophthalmologic evaluation because of blurred vi­sion in the left eye. About 2 weeks earlier she experienced a bilateral blackout of vision associ­ated with headache and nausea, which lasted sev­eral hours. Following this, there was progressive resolution of symptoms except for persistence of blurred vision in the left eye. Medical history was positive for rheumatic fever and subsequent rheumatic fever heart disease, with mitral stenosis necessitating a mitral commissuro­tomy at age 30. After the procedure the patient was in a coma for several days. This was attributl.'d to cerebral hypoperfusion. Following this she began to have grand mal seizures, which were controlled by diphenylhydantoin. Review of systems revealed a possible episode of transient left hemiparesis in From the Departments of Ophthalmolol'Y (TLS. TGK. RMB). Neurology (RMB). Neurological Surl'('ry (RMB). and Radll,logy (MHGj, Washington University School of M('dicin('. St. LouIS. Missouri. June 1981 May of 1977. In addition, she had had headaches associated with an aura of perioral dyesthesia di­agnosed as migraine. The patient denied recollec­tion or awareness of tachycardia or arrhythmia. She was on no medication other than diphenyl­hydantoin. Cardiac examination revealed regular rhythm. a loud S, sound and a soft diastolic rum­ble. No bruits were heard. Carotid upstroke was normal. and no jugular venous distension was seen. Ophthalmologic examination revealed a visual acuity of 20/25 in the right eye and 20/200 in the left eye. External examination was normal. Ap­planation tensions were 20 mm Hg in each eye. The right fundus was normal. In the left fundus, there was hemorrhagic retinopathy with a dilated and tortuous venous ci rculation and numerous blot-dot and nerve fiber layer hemorrhages (Fig. 1). There was also cystoid macular edema. Ophthal­modynamometry was done with diastolic readings of 45 g, right eye, and 40 g, left eye. Kinetic visual fields showed a congruous left homonymous quad­rantanopia (Fig. 2) as well as a central scotoma in the left eye. Follow-up examinations over 15 months showed no changes except for variabll.' visual acuities in the left eyl.' ranging between 2.0/70 and finger counting and commensurate with varying degrees t)f cystoid macular edema. Workup included a CT sc.m which showed increase in the size of the lateral and third ventricles. A recent right occipital cortex infarct was also seen. Cerebral angiogr,lms rl.'vealed char­acteristic findings of moyamoy.l. On the right side, the internal carotid artery was l1Ccluded distal to the origin of the ophthalmic artery (Fig. 3). The right ophthalmic artery supplied orbital ,masto­motic vessels that take part in the vascularization of the inferior surface of the right frontal lobe. On the left side, the internal carotid ,utery was occluded at its origin in the neck as shown by an arch injection. Thl.' vertebral artery injection (Fig. 4) showed that the basilar artery and its posterior cerebral branches werl.' responsible for filling of 123 Mlly,lllllly,l Dis{',lSl' t<'1 the entire territories of both middle and .mterior cerebral arteries in both cerebral hemispheres. No filling of the ophthalmic artery was furnished by the intracranial circulation. Furthermore, the right internal carotid injection did not show in the fron­tal view (not included here) evidence of filling of the left ophth.llmic artery via interophthJlmic In­astomoses across the midline. Discussion MoyamoYJ disease, .llso known JS multiple pro­!!, re.,sivp intrJCf.lnidl Mteri.ll occlusion syndrome, j., Ji,lgnospd by c('fl'brdl angiography dnd is ch.lr- Figure J. la) Elevated left optic nerve head with relatively dilated veins and diffuse hemorrhagIC activity. (b) Hemorrhagic ad,vity temporal to the macula. Icl :-':onnal right fundus. .lcterized by intrdcr.lniJI vdscul.lr occlusions, most typic.llly involving the internal .lrteries bilaterally, usudlly .it the level of the c.lrotid syphon. There is also a vilscular anastomotic network .lt the base of the brJin. The Japanese expression "moyamoya" loosely transl.lted me.lns "puff of smoke" and refers to the Jndstomotic vessels. l .z This condition most often is detected in children and young adults. It was first seen .lmong Japanese. Though most common in that population, it has been reported, .lmong others, from Korea, India, England, France, Scandinavia ana the United States (in both black Jnd white patients). The etiology of the disease is unknown, but it is Journal of Clinical Neuro-ophthalmology Slamovits, Klingele, Burde, Gado LEFT RIGHT Figure 2. Kinetic visual fields demonstrating a relative left inferior quadrantic defect (congruous). The absence of response to the I,e test object in the left eye is indicative of the presence of a central scotoma. Figure 3. Common carotid arteriogram. Later arterial phase. The right internal carotid artery is occluded distal to the ophthalmic artery. The cdrotid artery proximal to the occlusion is contracted. The ophthalmic artery fills antegrade and supplies numerous rete. not thought to be associated with vasculitis or coagulopathy. Both congenital and acquired cases have been demonstrated.'·~ Familial cases in the Japanese famill and in identical twins in India4 and Japan~ have been reported. Moyamoya disease has been found in association with cerebral atrophy and with cerebral aneurysms by Adams and co­workers, 6 Kowada and associates,7 Debrun and Lacour,8 and several others. Moyamoya disease in conjunction with sickle cell disease has been re­ported. 9- 11 Coakham and co-workersl~ have re­ported association of moyamoya with progressive June 1981 neuropathy. Tuberous sclerosis has been seen in conjunction with moyamoya. 1 : 1 Moyamoya disease has been found in patients with neurofibromato­sis!" as well as neurofibromatosis with optic glioma. ,r,One report H ; describes three patients with gliomas who had angiograms before and after ra­diation therapy and who developed the radiologic features of moyamoya after radiation. Symptoms and signs of moyamoya disease are varied and may include headaches, seizures, sub­normal intelligence, subarachnoid hemorrhage, hemiparesis or hemiplegia, and cranial nerve pal- 12.5 Moy.1moy.1 Oi5C,15C Figure 4. Left vertebral artl'riogram. Latl' Jrterial phasl'. Thl' vl'rtebral basIlar circulation provides collateral flow via leptomeningeal anastomosl'S into all the tl'rritorles of the mIddle and anterior cerebral arteries bilaterally. No flow in the ophthalmic arteries is Sl'l'n sies. Ocular involvement is alluded to in one report as "eye symptoms" with no breakdown more spe­cific than "visual disturbance" and "nystagmus."1 Frequently found ocular manifestations of moya­moya disease are hemianopias, 12.17. 1M high ophthal­modynamometry (ODM) values,19 nystagmus, I and papilledema.20 Miotic pupils" and eye devia­tion to one side" have also been reported; these were in conjunction with coma and hemiparesis. A child with Down's syndrome was thought to have cortical blindness due to moyamoya disease. 21 Our patient has a number of findings previously associated with moyamoya disease: a history of seizure disorders, vascular-type headaches, previ­ous hemiparesis, cerebral atrophy, and a homo­nymous hemianopia with a corresponding occipit,ll infarct. Though we cannot be absolutely certain that her occipital lesion is not due to her rheum,ltic heart disease, we assume the latter to be unlik.ely. The onset of her visual field defect was recent, and her subsequent cardiologic evaluation did not re­veal significant valvular stenosis, and we feel that the patient was not experiencing cardiac valvul,lf emboli. In addition to the field defect, the p,ltient had hemorrhage retinopathy in the left eye. We are not aware of any previously reported ,1SStlCi,1­tion of retinal disease with moyamoy,l dise,lse although one report described "tortuolls ,md di­lated retinal vesseI5."22 There are two alternative explanations for hem­orrhagic retinopathy in this patient's left eye. Ve­nous stasis retinopathy, as described by Kearns and Hollenhorsl,2:j has been associated with occlu­sion of the carotid circulation. Our patient has angiographic evidence for occlusion of the left internal carotid artery at its origin, while the right internal carotid is occluded distal to the origin of the ophthalmic artery. In view of the other angio­graphic findings described above, the most likely source for filling of the left ophthalmic artery was the left external carotid artery, although this was not demonstrated radiologically. Venous stasis in the left retina could be explained by inadequacy of anastomotic channels from the left external carotid to the left ophthalmic artery and left globe. How­ever. venous stasis retinopathy caused by chronic ischemia appears unlikely because of the relatively nt)rm.ll retinal artery pressure and applanation ten­sion in the left eye. Furthermore, dilated retinal veins with nerve fiber l.1yer hemorrhages and cys­toid m,lCular edem,l all point toward central retinal vein occlusion as the mechanism of hemorrhagic retinop,lthy in this patient. We believe that this p,ltient experienced transient, relatively severe, hy­potension in the left ophthalmic circulation during an episode of cerebral ischemia occurring at the time of onset of visual symptoms. Stasis of flow ,lnd thrombotic occlusion of the left retinal venous circul,ltion followed. We believe that this ischemic episode was caused by progression of the occlusive process affecting the circle of Willis and other vessels in this patient and is thus directly related to the confusing entity known as moyamoya dis­ease. A final consideration, the coincidental 3SS0- Journal of Clinical Neuro-ophthalmology ciation of iditlp.lthit- centr.l( retin.ll vein tKdusitlll in this normotensive 4S-ye.H-I)ld white WOIll.ln, seems quite unli\...ely. References I. :--;ishtOhlt,). A...1Ild T.I!..l'lIlhi. S.: M"y,lOll,y,l di~",ls,': Abn,)rlll.11 l .. rebr")',lsluI.H nl'tw,'r!.. in thl' ll'rl'br.11 b.1S.ll rq~i,)n. In H,wd!>",,/.. ,,( CII/H,',II .'\'l'Urlll.'l'l·. \',,/ 12. p.lrt II. I'. I. \'lIl!.. ..n .1Ild C. \V. Hruyn. [,k :\"rth-H"II.lIld ['ublt"hin~ C"lllp,lIl),. 1')72. Am"t"r­d. Hn. I v 72. pp J52-.'~J. , T,wer,ls. f t\ I. ,lIld \\"",.1. l. H.. Pi,l~n",tll' Nl'urll­r, ld".I"p· \"'/:: (2nd ...1.1 \Vdli,llll' & Wd!..in". B,llt'Ill,'rl'. Iv71:'. pp. v02-vOv . J K,t.)h,H,I. T Ar~I,I. N. 't ,)m,lUr,l. A.. M,lkin", H., .1Ild t\l.lkl. 't.' f.lmdi,11 """Urrt'nle "f m"y.lm"y,1 dls...lse: Rep,'rt "f thre(' l.lp.lIlese f,lOlilies. , Neul'll/. .\·'·UI'l'Sllrl'. T',n·hi.ltr)' ~!: 20~-21-l, I v7v . -l Snnl\·,lS. K. :\.H,I\'.lIl.lIl. M.. G,'p.ll, 5., .1Ild 1.1~,ln­n, lth.ln K. C~r,'t,d ,lrteri~1 "l.-!u5i,'n in identil.ll twins \\'Ith m"y,lIlhl\',1 Arch ,\leul'll/. 36: 253-25-l, Iv7v :; 't ~m~d.1. H. :\.lk~mur.l. 5...1Ild K~~ey.mu. N.: '1c'Y.lm,')'~ dls('~se to m,'n,'\·uI.H twins: C.1S(' report. , .\·pur,'sur,.; 53: IOv-112. Iv80 C' :\d.lm,;. H. r. II'. K~,;,;pl. :\. F, Wisoff. H. 5.. ~nd Dr~l..e. C G [ntr~rr.lIll~1 5~llul~r ~neurv,;m .lIld m(1)'~m,'y.1 d"'(,~5e. Stl'l'l.(' 10: 17-l- 170. 1070. - K,,\\~d~. \1 . M,'mm~. F. ~nd Kll..uchi. K.: Intr~crd­n', ll ~neurvsm ~ssoll~ted with cerebroVdSCuldr m,'V~moY~ ·dlse~se. Rept,rt of d case dnd review of 13 c~ses Br I R.ldll,l. 5!: 23b-237, 1070. 8. Debrun. C .. and Lolcour. r.: A new Cdse of m"Yd­mova disedse olSSt1CI~ted with severdl introlcolvernl)U5 ~neurysms..'\'eul'l,roldil,I"j{v 7: 277-282, 1074. ° Seeler. A.. ROYdl. J. E. rowe, L. dnd Coldbdr~, H. R.: MOYdmOYd in chddren with sicle cell dnemid olnd cerebrovdsculM occlusion. J Pedioltr 93: 808-810, 1978 10 Stockmdn, / A. :\,~ro. M. A. Mishkin, M. M, ~nd Oskl. F. A Occlu'lon of 1.H~e cerebr~1 vp<,spls In sickle cell dnemlol .'\' [ng/ I Med. 287: 114b-II-lO, 1972. 11. Crosley, C. '.: Chddhoud mt'Vdm,'y~ pre~enting ol<' subdrdchnoid hemorrhdgp. Arch. ,,"'eul'll/. 36: 511-5°. 1979. 12. COdkhdm, H. B., Duchen, L W., dnd SCMolvdli. F: MOyolmoyd disedse: Clinicoll olnd piltholo~ic.:tl rep,'rt of d Cilse with il<,socldted my"pdthy. I Neuro/. Neu­rosurj{. PsychiJtry 42: 2110-207. 1070. June 1981 Sl~movits, Klingele, Hurdt·, C~do 13. Inl.lizumi, M., Nuk.ldol, T., Yoned.l, 5., Tol k.J no, T., M,I~pg,lw.l, K., .lIld Abp, H.: Tubpn>us srlpn>si<, With nlllv.lnllly.1 dist'.lse. C~sP report. MeJ. /. ()s,lk.J Univ. 28(3-4): 345-353, 1978. 14. LIIlI.1S, L Lob.lto, ({.D., C~bl'lIo, A.. .Hld Ab~d, / M.: Multipll' intr,H"r.lni,11 .lrtl'ri.11 o"lusions (moyol­nllly, l disl',\<'e) ill p.ltienh with Jl('urofibrom~tosi~. Ad,l Neuro,·hir. 45: 133-145, 19711. 15 HiI.ll. S. K., Solonllln, G. L., Cold, A. 1', ,lnd (.:trtl'r, S.: I'rilll,lry cerebr~1 .:tr!pry uttlu~ivl' dis(',lSe in chil­dren. 1',Ht II. NpUrl'cut.:tnt'ou<, <,yndroml's. Neuror.J­diu/ u~y 99: 117-94, 1071. II:'. ({,lj.ll..ul,lsillg.:tm, K., Cerullo, L. J., .lIld R.\lmundi, A. f: Childhood moy~moY,1 ~yndrom('. I'ostr~di~ti"n p,ltho~ene",<,. Child's Br.Jin 5: 4b7-475, 1070 17. Arit.:t, M., T.:tk.:tkurol, ,., Num~no, F, and M~ez~wd, H.: A lase of intrdcrani~1 rete mlr~bile V~sculdnty ,I,;soci.lted with ~mnestic aphd,;i.l ~nd ri~ht Infenur ht)mtlllymous qu.:tdrdntdnopsiol. NIppon .\ldil...:t CJ/..­/... Ii Z,lsshi 66: 821-829, 1077. III. HI'Jre, A. M., .:tnd Keo~h, A. J.: CerebrovdsculJr mt'y.lmoyd disedse. Br. Med. f. 1: -l30--l32, 1074. 10 Zappi,l, R. J, Winkelmdn, / Z., Roberson, C H, Rosenb.lum, H. E., dnd CdY, A. J.: rrogessive intrd­cr. lIlioll .:trierioll occlusion syndrome. Report of d Cdse with unusudlly high ophthdlmodyn.lmometry IODM) vdlues. Arch. OphthJ/mo/. 86: 455-458, 1971. 20. Schoenber~, B. S., Mellinger, J. F, ~nd Schoenberg, D. G.: Moyamoya di5edse III children. Suuth Med. /. 71: 237-241, 1978. 21. Slhrd~N, CO., Cohen, S J.. olnd Vigmoln. M. P.. Acute hemiplegid olnd Cllrtic~1 blindness due tt' mOV.lmoy~ disedse: Report of ~ C~5e in .1 lhild with Dl'~n's ;yndrome. T'ediiltrics 60: 33-37. 1077. 22 Schoenber~, B. S., Mellin~er. I. F. 5chl'l'Ilberg. D. G., dnd BJrringer, F. S.: Moy~mov~ dise~se present­in~ olS a seizure disorder. A C.lse report. Arch..'\·eu­ro/. 34: 511-512, 1077. 23. Ke~rns, T. r., ~nd Hollenhor5t. R. W.: Ven,)us 5t.lsis retinop.lthy l,f occlusive dise.:tse l,f the c.lrt'tid .lrterv M.IY" Clin. T'roc 38: 304-312, 10t>3 Acknowledgments Thi" wor!.. W.I~ supported in p.Ht bv ,I ~r,lnt In'lll ({ese.Ht h to I'revl'nt Blindness. Inc.. Np\V 't ,'rk. Nt'w Y"rl.. ([)pp.Htment of Uphth.llml,lll~V). Write {(II' reprints t,': Rllll.lld M. Burde. M.D.. De­p.: trtment of Ophth.1Imolt'gy-BI''\ ~00l:'. N'O S,'uth Eu­did Avenu(', St. LOUIS, MisSt)uri 1:'3110. 127