Electroencephalographic features in pediatric patients with moyamoya disease in China

Jiuyi Lü1, Xia Qin1, Tuanfeng Yang1, Jun Qiang1, Xianzeng Liu1, Xun Ye2, Rong Wang2
1Department of Neurology, Peking University International Hospital, No.1 Life Park Road, Changping District, Beijing, 102206, China
2Department of Neurosurgery, Peking University International Hospital, Beijing, 102206, China

Tóm tắt

Abstract Background Moyamoya disease (MMD) is a relatively important and common disease, especially in East Asian children. There are few reports about EEG in children with MMD in China till now. This study is aimed to analyze the electroencephalographic features of MMD in pediatric patients in China preliminarily. Methods Pediatric patients with MMD who were hospitalized in Peking University International Hospital and Beijing Tiantan Hospital from January 2016 to December 2018 were collected. Clinical and electroencephalography (EEG) findings were analyzed retrospectively. Results A total of 110 pediatric patients with MMD were involved, and 17 (15.5%) cases had a history of seizure or epilepsy. Ischemic stroke was associated with a 1.62-fold relative risk of seizure. A subset of 15 patients with complete EEG data was identified. Indications for EEG in patients with MMD included limb shaking, unilateral weakness, or generalized convulsion. Abnormal EEG was seen in 14 (93.3%) cases, with the most common findings being focal slowing 12 (80.0%), followed by epileptiform discharge 10 (66.7%), and diffuse slowing 9 (60.0%). “Re-build up” phenomenon on EEG was observed in one patient. Conclusions Seizure and abnormal background activity or epileptiform discharge on EEG were common in pediatric patients with MMD. EEG may play a role in differential diagnosis among the transient neurological events in MMD such as transient ischemic attack and seizure.

Từ khóa


Tài liệu tham khảo

Kim JS. Moyamoya disease: epidemiology, clinical features, and diagnosis. J Stroke. 2016;18(1):2–11.

Fujimura M, Bang OY, Kim JS. Moyamoya disease. Front Neurol Neurosci. 2016;40:204–20.

Huang S, Guo ZN, Shi M, et al. Etiology and pathogenesis of moyamoya disease: an update on disease prevalence. Int J Stroke. 2017;12(3):246–53.

Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288–99.

Nakase H, Ohnishi H, Touho H, et al. Long-term follow-up study of “epileptic type” moyamoya disease in children. Neurol Med Chir (Tokyo). 1993;33(9):621–4.

Ma Y, Zhao M, Zhang Q, et al. Risk factors for epilepsy recurrence after revascularization in pediatric patients with moyamoya disease. J Stroke Cerebrovasc Dis. 2018;27(3):740–6.

Jin SC, Oh CW, Kwon OK, et al. Epilepsy after bypass surgery in adult moyamoya disease. Neurosurgery. 2011;68(5):1227–32 discussion 1232.

Frechette ES, Bell-Stephens TE, Steinberg GK, et al. Electroencephalographic features of moyamoya in adults. Clin Neurophysiol. 2015;126(3):481–5.

Ali S, Khan MA, Khealani B. Limb-shaking transient ischemic attacks: case report and review of literature. BMC Neurol. 2006;6:5.

Kraemer M, Diehl RR, Diesner F, et al. Differential diagnosis between cerebral ischemia, focal seizures and limb shaking TIAs in moyamoya disease. Br J Neurosurg. 2012;26(6):896–8.

Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo). 2012;52(5):245–66.

Engel J, Van Ness PC, Rasmussen TB, et al. Outcome with respect to epileptic seizures. In: Engel J, editor. Surgical treatment of the epilepsies. 2nd ed. New York: Raven Press; 1993. p. 609–21.

Rodríguez Lucci F, Alet M, Ameriso SF. Post-stroke epilepsy. Medicina (B Aires). 2018;78(2):86–90.

Benninger F, Holtkamp M. Epileptic seizures and epilepsy after a stroke: incidence, prevention and treatment. Nervenarzt. 2017;88(10):1197–207.

Mikami T, Ochi S, Houkin K, et al. Predictive factors for epilepsy in moyamoya disease. J Stroke Cerebrovasc Dis. 2015;24(1):17–23.

Breitweg I, Stülpnagel CV, Pieper T, et al. Early seizures predict the development of epilepsy in children and adolescents with stroke. Eur J Paediatr Neurol. 2017;21(3):465–7.

Fox CK, Glass HC, Sidney S, et al. Acute seizures predict epilepsy after childhood stroke. Ann Neurol. 2013;74(2):249–56.

Kim HY, Chung CS, Lee J, et al. Hyperventilation-induced limb shaking TIA in moyamoya disease. Neurology. 2003;60(1):137–9.

Kodama N, Aoki Y, Hiraga H, et al. Electroencephalographic findings in children with moyamoya disease. Arch Neurol. 1979;36(1):16–9.

Amzica F, Lopes da Silva FH. Cellular substrates of brain rhythms. In: Niedermeyer E, Schomer DL, Lopes da Silva FH, editors. Niedermeyer’s Electroencephalography: Basic Principles, Clinical Applications, and Related Fields. 6th ed. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2010. p. 33–64.

Evans BM. Patterns of arousal in comatose patients. J Neurol Neurosurg Psychiatry. 1976;39(4):392–402.

Foreman B, Claassen J. Quantitative EEG for the detection of brain ischemia. Crit Care. 2012;16(2):216.

Sharbrough FW, Messick JM Jr, Sundt TM Jr. Correlation of continuous electroencephalograms with cerebral blood flow measurements during carotid endarterectomy. Stroke. 1973;4(4):674–83.

Rogers JM, Bechara J, Middleton S, et al. Acute EEG patterns associated with transient ischemic attack. Clin EEG Neurosci. 2019;50(3):196–204.

Cho A, Chae JH, Kim HM, et al. Electroencephalography in pediatric moyamoya disease: reappraisal of clinical value. Childs Nerv Syst. 2014;30(3):449–59.

Kuroda S, Kamiyama H, Isobe M, et al. Cerebral hemodynamics and “re-build-up” phenomenon on electroencephalogram in children with moyamoya disease. Childs Nerv Syst. 1995;11(4):214–9.

Kameyama M, Shirane R, Tsurumi Y, et al. Evaluation of cerebral blood flow and metabolism in childhood moyamoya disease: an investigation into “re-build-up” on EEG by positron CT. Childs Nerv Syst. 1986;2(3):130–3.

Konishi T. The standardization of hyperventilation on EEG recording in childhood II. The quantitative analysis of build-up. Brain Dev. 1987;9(1):21–5.

Kuwabara Y, Ichiya Y, Sasaki M, et al. Response to hypercapnia in moyamoya disease. Cerebrovascular response to hypercapnia in pediatric and adult patients with moyamoya disease. Stroke. 1997;28(4):701–7.

Lin Y, Yoshiko K, Negoro T, et al. Cerebral oxygenation state in childhood moyamoya disease: a near-infrared spectroscopy study. Pediatr Neurol. 2000;22(5):365–9.

Kazumata K, Kuroda S, Houkin K, et al. Regional cerebral hemodynamics during re-build-up phenomenon in childhood moyamoya disease. An analysis using 99mTc-HMPAO SPECT. Childs Nerv Syst. 1996;12(3):161–5.

Qiao F, Kuroda S, Kamada K, et al. Source localization of the re-build up phenomenon in pediatric moyamoya disease-a dipole distribution analysis using MEG and SPECT. Childs Nerv Syst. 2003;19(10-11):760–4.

Touho H, Karasawa J, Shishido H, et al. Mechanism of the re-buildup phenomenon in moyamoya disease--analysis of local cerebral hemodynamics with intra-arterial digital subtraction angiography. Neurol Med Chir (Tokyo). 1990;30(10):721–6.

Kim DS, Ko TS, Ra YS, et al. Postoperative electroencephalogram for follow up of pediatric moyamoya disease. J Korean Med Sci. 2006;21(3):495–9.

Boulos MI, Lena S, Han J, et al. Novel EEG pattern associated with impaired cerebrovascular reserve in moyamoya disease. Clin Neurophysiol. 2014;125(2):422–5.

Garson SR, Monteith SJ, Smith SD, et al. Down syndrome associated moyamoya may worsen epilepsy control and can benefit from surgical revascularization. Epilepsy Behav Case Rep. 2018;11:14–7.