Original Article| Volume 23, ISSUE 6, P1344-1350, July 2014

Coexisting Diseases of Moyamoya Vasculopathy


      Several coexisting diseases have been reported in patients with moyamoya vasculopathy (MMV), but studies of quasi-moyamoya disease (quasi-MMD) are rare. This study aims to investigate the frequency of known coexisting diseases in patients with quasi-MMD and to compare quasi-MMD with moyamoya disease (MMD).


      Between 2000 and 2011, we retrospectively screened patients with International Classification of Diseases, Ninth Revision, code of 4375 (MMD) in the Health Information System of our hospital. The vascular images of each patient were confirmed by 2 neurologists and 1 neuroradiologist based on the diagnostic criteria of Japan Ministry of Health and Welfare. We excluded the patients with missing images and erroneous diagnosis. Demographics, coexisting diseases, laboratory data, treatment, and recurrent strokes were recorded. The eligible patients were divided into quasi-MMD and MMD groups according to the presence or absence of coexisting diseases.


      MMV was found in 90 patients including 37 (41.1%) quasi-MMD and 53 (58.9%) MMD. Atherosclerosis (32.4%) and thyroid disease (29.7%) were the leading coexisting diseases in quasi-MMD. Patients with MMD became symptomatic in a bimodal age distribution, whereas patients with quasi-MMD became symptomatic in a single-peak distribution. The prognosis of recurrent strokes was similar between quasi-MMD and MMD based on Kaplan–Meier analysis.


      A bimodal distribution of onset age was noted in MMD, whereas a single-peak distribution was found in quasi-MMD. Coexisting diseases were usually underevaluated but were more common than expected in patients with MMV. Atherosclerosis and thyroid diseases were the leading coexisting diseases in different preferential age.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Journal of Stroke and Cerebrovascular Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Suzuki J.
        • Kodama N.
        Moyamoya disease—a review.
        Stroke. 1983; 14: 104-109
        • Fukui M.
        Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis ('moyamoya' disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan.
        Clin Neurol Neurosurg. 1997; 99: S238-S240
        • Scott R.M.
        • Smith E.R.
        Moyamoya disease and moyamoya syndrome.
        N Engl J Med. 2009; 360: 1226-1237
        • Tanaka M.
        • Sakaguchi M.
        • Kitagawa K.
        Mechanism of moyamoya vessels secondary to intracranial atherosclerotic disease: angiographic findings in patients with middle cerebral artery occlusion.
        J Stroke Cerebrovasc Dis. 2012; 21: 373-378
        • Kim S.J.
        • Heo K.G.
        • Shin H.Y.
        • et al.
        Association of thyroid autoantibodies with moyamoya-type cerebrovascular disease: a prospective study.
        Stroke. 2010; 41: 173-176
        • Li H.
        • Zhang Z.S.
        • Dong Z.N.
        • et al.
        Increased thyroid function and elevated thyroid autoantibodies in pediatric patients with moyamoya disease: a case-control study.
        Stroke. 2011; 42: 1138-1139
        • Ohba S.
        • Nakagawa T.
        • Murakami H.
        Concurrent Graves' disease and intracranial arterial stenosis/occlusion: special considerations regarding the state of thyroid function, etiology, and treatment.
        Neurosurg Rev. 2011; 34: 297-304
        • Cramer S.C.
        • Robertson R.L.
        • Dooling E.C.
        • et al.
        Moyamoya and Down syndrome. Clinical and radiological features.
        Stroke. 1996; 27: 2131-2135
        • van Diemen-Steenvoorde R.
        • van Nieuwenhuizen O.
        • de Klerk J.B.
        • et al.
        Quasi-moyamoya disease and heterozygosity for homocystinuria in a five-year-old girl.
        Neuropediatrics. 1990; 21: 110-112
        • Pilz P.
        • Hartjes H.J.
        Fibromuscular dysplasia and multiple dissecting aneurysms of intracranial arteries. A further cause of Moyamoya syndrome.
        Stroke. 1976; 7: 393-398
        • Ghosh P.S.
        • Rothner A.D.
        • Emch T.M.
        • et al.
        Cerebral vasculopathy in children with neurofibromatosis type 1.
        J Child Neurol. 2013; 28: 95-101
        • Pracyk J.B.
        • Massey J.M.
        Moyamoya disease associate with polycystic kidney disease and eosinophilic granuloma.
        Stroke. 1989; 20: 1092-1094
        • Terada T.
        • Yokote H.
        • Tsuura M.
        • et al.
        Marfan syndrome associated with moyamoya phenomenon and aortic dissection.
        Acta Neurochir (Wien). 1999; 141: 663-665
        • Dobson S.R.
        • Holden K.R.
        • Nietert P.J.
        • et al.
        Moyamoya syndrome in childhood sickle cell disease: a predictive factor for recurrent cerebrovascular events.
        Blood. 2002; 99: 3144-3150
        • Peerless S.J.
        Risk factors of moyamoya disease in Canada and the USA.
        Clin Neurol Neurosurg. 1997; 99: S45-S48
        • Meena S.S.
        • Ramkumar T.V.
        • Sharma S.
        • et al.
        Moyamoya syndrome associated with severe iron deficiency anemia in a young child.
        Pediatr Hematol Oncol. 2012; 29: 368-371
        • Akgun D.
        • YiLmaz S.
        • Senbil N.
        • et al.
        Moyamoya syndrome with protein S deficiency.
        Eur J Paediatr Neurol. 2000; 4: 185-188
        • Andeejani A.M.
        • Salih M.A.
        • Kolawole T.
        • et al.
        Moyamoya syndrome with unusual angiographic findings and protein C deficiency: review of the literature.
        J Neurol Sci. 1998; 159: 11-16
        • Cerrato P.
        • Grasso M.
        • Lentini A.
        • et al.
        Atherosclerotic adult moyamoya disease in a patient with hyperhomocysteinaemia.
        Neurol Sci. 2007; 28: 45-47
        • Booth F.
        • Yanofsky R.
        • Ross I.B.
        • et al.
        Primary antiphospholipid syndrome with moyamoya-like vascular changes.
        Pediatr Neurosurg. 1999; 31: 45-48
        • Tsuda H.
        • Hattori S.
        • Tanabe S.
        • et al.
        Thrombophilia found in patients with Moyamoya disease.
        Clin Neurol Neurosur. 1997; 99: S229-S233
        • Jeong H.C.
        • Kim Y.J.
        • Yoon W.
        • et al.
        Moyamoya syndrome associated with systemic lupus erythematosus.
        Lupus. 2008; 17: 679-682
        • Czartoski T.
        • Hallam D.
        • Lacy J.M.
        • et al.
        Postinfectious vasculopathy with evolution to moyamoya syndrome.
        J Neurol Neurosurg Psychiatry. 2005; 76: 256-259
        • Ullrich N.J.
        • Robertson R.
        • Kinnamon D.D.
        • et al.
        Moyamoya following cranial irradiation for primary brain tumors in children.
        Neurology. 2007; 68: 932-938
        • Levine S.R.
        • Knake J.E.
        • Young A.B.
        Atypical progressive stroke syndrome associated with oral contraceptives and cigarette use.
        Stroke. 1987; 18: 519-523
        • Drees J.C.
        • Stone J.A.
        • Wu A.H.
        Morbidity involving the hallucinogenic designer amines MDA and 2C-I.
        J Forensic Sci. 2009; 54: 1485-1487
        • Storen E.C.
        • Wijdicks E.F.
        • Crum B.A.
        • et al.
        Moyamoya-like vasculopathy from cocaine dependency.
        AJNR Am J Neuroradiol. 2000; 21: 1008-1010
        • Hayashi K.
        • Horie N.
        • Suyama K.
        • et al.
        An epidemiological survey of moyamoya disease, unilateral moyamoya disease and quasi-moyamoya disease in Japan.
        Clin Neurol Neurosurg. 2013; 115: 930-933
        • Kleinloog R.
        • Regli L.
        • Rinkel G.J.
        • et al.
        Regional differences in incidence and patient characteristics of moyamoya disease: a systematic review.
        J Neurol Neurosurg Psychiatry. 2012; 83: 531-536
        • Baba T.
        • Houkin K.
        • Kuroda S.
        Novel epidemiological features of moyamoya disease.
        J Neurol Neurosurg Psychiatry. 2008; 79: 900-904
        • Hung C.C.
        • Tu Y.K.
        • Su C.F.
        • et al.
        Epidemiological study of moyamoya disease in Taiwan.
        Clin Neurol Neurosurg. 1997; 99: S23-S25
        • Houkin K.
        • Nakayama N.
        • Kuroda S.
        • et al.
        Novel magnetic resonance angiography stage grading for moyamoya disease.
        Cerebrovasc Dis. 2005; 20: 347-354
        • Zhang J.
        • Wang J.
        • Geng D.
        • et al.
        Whole-brain CT perfusion and CT angiography assessment of moyamoya disease before and after surgical revascularization: preliminary study with 256-slice CT.
        PLoS One. 2013; 8: e57595
        • Hochberg M.C.
        Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus.
        Arthritis Rheum. 1997; 40: 1725
        • Kuriyama S.
        • Kusaka Y.
        • Fujimura M.
        • et al.
        Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey.
        Stroke. 2008; 39: 42-47
        • Han D.H.
        • Kwon O.K.
        • Byun B.J.
        • et al.
        A co-operative study: clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976-1994). The Korean Society for Cerebrovascular Disease.
        Acta Neurochir (Wien). 2000; 142 (discussion 73-74): 1263-1273
        • Miao W.
        • Zhao P.L.
        • Zhang Y.S.
        • et al.
        Epidemiological and clinical features of moyamoya disease in Nanjing, China.
        Clin Neurol Neurosurg. 2010; 112: 199-203
        • Uchino K.
        • Johnston S.C.
        • Becker K.J.
        • et al.
        Moyamoya disease in Washington State and California.
        Neurology. 2005; 65: 956-958
        • Natori Y.
        • Ikezaki K.
        • Matsushima T.
        • et al.
        'Angiographic moyamoya' its definition, classification, and therapy.
        Clin Neurol Neurosurg. 1997; 99: S168-S172
        • Horn P.
        • Pfister S.
        • Bueltmann E.
        • et al.
        Moyamoya-like vasculopathy (moyamoya syndrome) in children.
        Childs Nerv Syst. 2004; 20: 382-391
        • Bower R.S.
        • Mallory G.W.
        • Nwojo M.
        • et al.
        Moyamoya disease in a primarily white, midwestern US population: increased prevalence of autoimmune disease.
        Stroke. 2013; 44: 1997-1999
        • Lee T.H.
        • Hsu W.C.
        • Chen C.J.
        • et al.
        Etiologic study of young ischemic stroke in Taiwan.
        Stroke. 2002; 33: 1950-1955
        • Squizzato A.
        • Gerdes V.E.
        • Brandjes D.P.
        • et al.
        Thyroid diseases and cerebrovascular disease.
        Stroke. 2005; 36: 2302-2310