Clinical Findings and Outcome of Moyamoya Disease/Syndrome

Year 2024, Articles Online First, 1 - 6

Betül Diler Durgut , Beril Dilber , Tulay Kamasak , Ahmet Sarı , Ali Cansu

https://doi.org/10.12956/tchd.1517440

Abstract

Objective: Moyamoya disease is a rare progressive cerebrovascular disorder. It is characterized by progressive stenosis in the terminal branches of the internal carotid arteries, leading to the formation of an abnormal vascular network. The aim of this study was to present the clinical findings and outcomes of pediatric patients diagnosed with Moyamoya disease by analyzing our cohort to identify the common clinical presentations, diagnostic challenges, and treatment outcomes associated with this rare cerebrovascular disorder.

Material and Methods: Nine pediatric cases of Moyamoya disease admitted over a 10-year period were retrospectively reviewed. Clinical presentations, associated diseases, radiological findings, treatments, and outcomes were analyzed.

Results: The median age at diagnosis was 48 months (3-87). Presenting symptoms included hemiparesis in five patients, seizures in six patients, headache in one patient, and choreathetosis with headache in one patient. Three patients experienced symptoms triggered by fever, and one patient by exposure to hot water. Seven patients presented with ischemic symptoms, while two presented with non-ischemic symptoms. Neurofibromatosis type-1 (NF-1) was associated with the disease in four patients. Recurrent attacks occurred in two patients. Interictal electroencephalograms (EEGs) showed hemispheric/focal slowing in five cases. Cranial magnetic resonance imaging (MRI) revealed infarctions in seven patients, and MR angiography showed bilateral findings in six patients. Two patients experienced no long-term sequelae.

Conclusion: Moyamoya disease manifests with both ischemic and non-ischemic symptoms. Recognition of non-ischemic presentations requires a high index of suspicion for accurate diagnosis.

Keywords

Children, electroencephalogram, moyamoya disease, neuroimaging, stroke

Ethical Statement

Ethical approval was obtained from the Clinical Research Ethics Committee of the University of Health Sciences, Karadeniz Technical University, with approval number 2023/173.

Supporting Institution

None

Thanks

None

Moyamoya Hastalığı/Sendromu’nun Klinik Bulguları ve Sonuçları

Abstract

Amaç: Moyamoya hastalığı nadir görülen, ilerleyici bir serebrovasküler bozukluktur. İç karotid arterlerin terminal dallarında ilerleyici darlık ile karakterize olup, anormal bir vasküler ağın oluşumuna yol açar. Bu çalışmanın amacı, bu nadir serebrovasküler bozuklukla ilişkili yaygın klinik tabloları, tanısal zorlukları ve tedavi sonuçlarını belirlemek için Moyamoya hastalığı tanısı konan pediatrik hastaların klinik bulgularını ve sonuçlarını sunmaktır.

Gereç ve Yöntemler: On yıllık bir dönemde kabul edilen dokuz pediatrik Moyamoya vakası retrospektif olarak incelendi. Klinik tablolar, ilişkili hastalıklar, radyolojik bulgular, tedaviler ve sonuçlar analiz edildi.

Bulgular: Tanı anında median yaş 48 ay (3-87)’dı. Başvuru semptomları beş hastada hemiparezi, altı hastada nöbet, bir hastada baş ağrısı ve bir hastada koreoatetoz ile baş ağrısı içeriyordu. Üç hasta ateşle tetiklenen semptomlar yaşadı, bir hasta ise sıcak suya maruz kalma ile tetiklenen semptomlar yaşadı. Yedi hasta iskemik semptomlarla, iki hasta ise iskemik olmayan semptomlarla başvurdu. Dört hastada hastalık ile ilişkili olarak Nörofibromatozis tip 1 (NF-1) mevcuttu. İki hastada tekrarlayan ataklar gözlendi. İnteriktal elektroensefalogramlarda (EEG) beş vakada hemisferik/odaksalyavaşlama görüldü. Kraniyal manyetik rezonans görüntüleme (MRI) yedi hastada enfarktüsleri ortaya koydu ve MR anjiyografi altı hastada bilateral bulgular gösterdi. İki hasta uzun dönem sekelsiz kaldı.

Sonuç: Moyamoya hastalığı hem iskemik hem de iskemik olmayan semptomlarla kendini gösterir. İskemik olmayan tabloların tanınması, doğru tanı için yüksek düzeyde şüphe gerektirir.

Keywords

Çocuklar, elektroensefalogram, Moya-Moya hastalığı, nörogörüntüleme, inme

References

• Gatti JR, Sun LR. Nonischemic Presentations of Pediatric Moyamoya Arteriopathy: A Natural History Study. Stroke 2022;53:219-20.
• Kuroda S, Fujimura M, Takahashi J, Kataoka H, Ogasawara K, Iwama T, et al. Research Committee on Moyamoya Disease (Spontaneous Occlusion of Circle of Willis) of the Ministry of Health, Labor, and Welfare, Japan. Diagnostic Criteria for Moyamoya Disease - 2021 Revised Version. Neurologia Medico-Chirurgica (Tokyo) 2022;62:307-12.
• Takanashi J. Moyamoya disease in children. Brain Development 2011;33:229-34.
• Das S, Ray BK, Pandit A, Ghosh R, Diehl R, Dubey S, et al. Profile of precipitating factorwws and its implication in 160 Indian patients with Moyamoya angiopathy Journal of Neurology. 2023;270:1654-61.
• Po’ C, Nosadini M, Zedde M, Pascarella R, Mirone G, Cicala D, et al. Pediatric Moyamoya Disease and Syndrome in Italy: A Multicenter Cohort. Frontiers in Pediatrics 2022;6:892445.
• Zheng J, Yu LB, Dai KF, Zhang Y, Wang R, Zhang D, et al. Clinical Features, Surgical Treatment, and Long-Term Outcome of a Multicenter Cohort of Pediatric Moyamoya. Front Neurol 2019;22:14.
• Zhao M, Zhang D, Wang S, Zhang Y, Deng X, Zhao C, et al. The Collateral Circulation in Moyamoya Disease: A Single-Center Experience in 140 Pediatric Patients. Pediatr Neurol 2017;77:78-83.
• Hishikawa T, Sugiu K, Date I. Moyamoya Disease: A Review of Clinical Research. Acta Medica Okayama 2016;70:229-36.
• Zhang X, Xiao W, Zhang Q, Xia D, Gao PSu J, et al. Progression in Moyamoya Disease: Clinical Features, Neuroimaging Evaluation, and Treatment. Curr Neuropharmacol 2022;20:292-308.
• Graf J, Schwitalla JC, Albrecht P, Veltkamp R, Berlit P, Hartung HP et al. Misdiagnoses and delay of diagnoses in Moyamoya angiopathy-a large Caucasian case series. J Neurol 2019;266:1153-9.
• Fukui M, Kono S, Sueishi K, Ikezaki K. Moyamoya disease. Neuropathology 2000;20 Suppl:S61-4.
• Hong YH, Ahn TB, Oh CW, Jeon BS. Hemichorea as an initial manifestation of moyamoya disease: reversible striatal hypoperfusion demonstrated on single photon emission computed tomography. Mov Disord 2002;17:1380-3.
• Gonzalez-Alegre P, Ammache Z, Davis PH, Rodnitzky RL. Moyamoya-induced paroxysmal dyskinesia. Mov Disord 2003;18:1051-6.
• Jung MY, Kim YO, Yoon W, Joo SP, Woo YJ. Characteristics of brain magnetic resonance images at symptom onset in children with moyamoya disease. Brain Dev 2015;37:299-306.
• Sato Y, Kazumata K, Nakatani E, Houkin K, Kanatani Y. Characteristics of Moyamoya Disease Based on National Registry Data in Japan. Stroke 2019;50:1973-80.
• Zanoni P, Steindl K, Sticht H, Oneda B, Joset P, Ivanovski I, et al. The genetic landscape and clinical implication of pediatric Moyamoya angiopathy in an international cohort. Eur J Hum Genet 2023;31:784-92.
• Malone M, Ritchie D. The Mystery of a Unilateral Headache Ultimately Diagnosed as Moyamoya Disease. Cureus 2022;14:e26816.
• Smith ER, Scott RM. Spontaneous occlusion of the circle of Willis in children: pediatric moyamoya summary with proposed evidence-based practice guidelines. A review. J Neurosurg Pediatr 2012;9:353–60.
• Gao B, Kang K, Zhang J, Zhang D, Zhao X. Clinical Characteristics and Long-Term Outcome of Headaches Associated With Moyamoya Disease in the Chinese Population-A Cohort Study. Front Neurol 2020;11:605636.
• Hao Z, Lai X. Sturge-Weber Syndrome Coexisting With Moyamoya Disease in the Fifth Decade: A Case Report and Literature Review. Neurologist 2019;24:13-6.
• Eisenmenger LB, Rivera-Rivera LA, Johnson KM, Drolet BA. Utilisation of advanced MRI techniques to understand neurovascular complications of PHACE syndrome: a case of arterial stenosis and dissection. BMJ Case Rep 2020;13:e235992.
• Pavlakis SG, Schneider S, Black K, Gould RJ. Steroid-responsive chorea in moyamoya disease. Mov Disord 1991;6:347-9.
• Sugita Y, Funaki T, Takahashi JC, Takagi Y, Fushimi Y, Kikuchi T, et al. Reversible striatal hypermetabolism in chorea associated with moyamoya disease: a report of two cases. Childs Nerv Syst 2016;32:2243-7.
• Demartini Z Jr, Teixeira BCA, Cardoso-Demartini AA. Choreoathetosis in Moyamoya Disease. World Neurosurg 2021;156:103-4.
• Maheshwari S, Anthony A, Kushwaha S, Singh S, Desai R, Madan D. Moyamoya Disease Presenting as Alternating Hemiparesis with Relapsing Remitting Hemichorea: An Unusual Manifestation. J Pediatr Neurosci 2018;13:514-6.
• Hara S, Hori M, Murata S, Ueda R, Tanaka Y, Inaji M, et al. Microstructural Damage in Normal-Appearing Brain Parenchyma and Neurocognitive Dysfunction in Adult Moyamoya Disease. Stroke 2018;49:2504-7.
• Gatti JR, Torriente AG, Sun LR. Clinical presentation and stroke incidence differ by moyamoya etiology. J Child Neurol 2021;36:272–80.
• Lu J, Xia Q, Yang T, Qiang J, Liu X, Ye X, et al. Electroencephalographic features in pediatric patients with moyamoya disease in China. Chin Neurosurg J 2020;6:3.
• M. Srinivasan HL, Hausman-Kedem M, Smith ER, Constantini S, Roth J. Current trends in pediatric moyamoya: a survey of international practitioners. Childs Nerv Syst 2021;37:2011-23.
• Kim T, Oh CW, Bang JS, Kim JE, Cho WS. Moyamoya Disease: Treatment and Outcomes. J Stroke 2016;18:21-30.
• Yamada S, Oki K, Itoh Y, Kuroda S, Houkin K, Tominaga T, et al. Research Committee on Spontaneous Occlusion of Circle of Willis (Moyamoya Disease). Effects of Surgery and Antiplatelet Therapy in Ten-Year Follow-Up from the Registry Study of Research Committee on Moyamoya Disease in Japan. J Stroke Cerebrovasc Dis 2016;25:340-9.
• Hao F, Gao G, Guo Q, Liu S, Wang M, Chang Z, et al. Risk Factors for Massive Cerebral Infarction in Pediatric Patients With Moyamoya Disease. Pediatr Neurol 2024;153:159-65.