Abstract
Purpose
The clinical value of electroencephalography (EEG) in pediatric moyamoya disease has been underestimated, though the characteristic patterns are well known. We undertook this study to evaluate the clinical value of EEG as a diagnostic and postoperative follow-up modality in pediatric moyamoya disease.
Methods
We retrospectively reviewed the pre and postoperative EEG with effective hyperventilation in 127 pediatric moyamoya patients and compared their patterns with hemodynamic images.
Results
One hundred and two patients (80.3 %) among 127 showed abnormal EEG findings before revascularization surgery. The typical rebuild-up phenomenon was observed in 82 (64.6 %) and localized build-up in 32 (25.2 %) without any significant clinical ischemic events during and after hyperventilation. The rebuild-up was observed more frequently in younger age groups (less than 13 years) and Suzuki stages III. The location of the rebuild-up distribution and asymmetric build-up was consistent with the area showing hemodynamic abnormalities on single photon emission computed tomography and/or perfusion magnetic resonance imaging. Postoperative follow-up EEGs were performed in 41 patients. Six patients with remaining rebuild-up in postoperative follow-up EEG showed poorer postoperative clinical outcomes.
Conclusions
This study may reappraise EEG as an easy, safe, and adjunctive diagnostic and postoperative follow-up modality for evaluation of hemodynamic status and clinical outcome, especially in children with moyamoya disease.
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References
Baba T, Houkin K, Kuroda S (2008) Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79(8):900–904
Caldarelli M, Di Rocco C, Gaglini P (2001) Surgical treatment of moyamoya disease in pediatric age. J Neurosurg Sci 45(2):83
Fisch BJ (1999) Fisch and Spehlmann's EEG primer: basic principles of digital and analog EEG. Elsevier, New York
Goda M, Isono M, Ishii K, Kamida T, Abe T, Kobayashi H (2004) Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. Journal of Neurosurgery: Pediatrics 100(2):156–162
Houkin K, Aoki T, Takahashi A, Abe H (1994) Diagnosis of moyamoya disease with magnetic resonance angiography. Stroke 25(11):2159–2164
Houkin K, Kuroda S, Nakayama N (2001) Cerebral revascularization for moyamoya disease in children. Neurosurgery Clinics of North America 12(3):575
Ishikawa T, Houkin K, Kamiyama H, Abe H (1997) Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke 28(6):1170–1173
Kameyama M, Shirane R, Tsurumi Y, Takahashi A, Fujiwara S, Suzuki J, Ito M, Ido T (1986) Evaluation of cerebral blood flow and metabolism in childhood moyamoya disease: an investigation into “re-build-up” on EEG by positron CT. Child's Nervous System 2(3):130–133
Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK (2003) Encephaloduroarteriosynangiosis with bifrontal encephalogaleo (periosteal) synangiosis in the pediatric moyamoya disease: the surgical technique and its outcomes. Child's Nervous System 19(5):316–324
Kim DS, Ko TS, Ra YS, Choi CG (2006) Postoperative electroencephalogram for follow up of pediatric moyamoya disease. J Korean Med Sci 21(3):495–499
Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC (2004) Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 54(4):840
Kim SK, Wang KC, Kim DG, Paek SH, Chung HT, Hee M, Ahn Y, Cho BK (2000) Clinical feature and outcome of pediatric cerebrovascular disease: a neurosurgical series. Childs Nerv Syst 16(7):421–428
Kim SK, Wang KC, Kim IO, Lee DS, Cho BK (2002) Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery 50(1):88–96
Kim SK, Wang KC, Oh CW, Kim IO, Lee DS, Song IC, Cho BK (2003) Evaluation of cerebral hemodynamics with perfusion MRI in childhood moyamoya disease. Pediatr Neurosurg 38(2):68–75
Kodama N, Aoki Y, Hiraga H, Wada T, Suzuki J (1979) Electroencephalographic findings in children with moyamoya disease. Arch Neurol 36(1):16
Kurlemann G, Fahrendorf G, Krings W, Sciuk J, Palm D (1992) Characteristic EEG findings in childhood moyamoya syndrome. Neurosurg Rev 15(1):57–60
Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7(11):1056–1066
Kuroda S, Kamiyama H, Isobe M, Houkin K, Abe H, Mitsumori K (1995) Cerebral hemodynamics and “re-build-up” phenomenon on electroencephalogram in children with moyamoya disease. Child's Nervous System 11(4):214–219
Mesiwala AH, Sviri G, Fatemi N, Britz GW, Newell DW (2008) Long-term outcome of superficial temporal artery–middle cerebral artery bypass for patients with moyamoya disease in the US. Neurosurg Focus 24(2):E15
Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360(12):1226–1237
So Y, Lee HY, Kim SK, Lee JS, Wang KC, Cho BK, Kang E, Lee DS (2005) Prediction of the clinical outcome of pediatric moyamoya disease with postoperative basal/acetazolamide stress brain perfusion SPECT after revascularization surgery. Stroke 36(7):1485–1489
Sunder T, Erwin C, Dubois P (1980) Hyperventilation induced abnormalities in the electroencephalogram of children with moyamoya disease. Electroencephalogr Clin Neurophysiol 49(3):414–420
Suzuki J, Takaku A (1969) Cerebrovascular "moyamoya" disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol 20(3):288
Togao O, Mihara F, Yoshiura T, Tanaka A, Noguchi T, Kuwabara Y, Kaneko K, Matsushima T, Honda H (2006) Cerebral hemodynamics in moyamoya disease: correlation between perfusion-weighted MR imaging and cerebral angiography. Am J Neuroradiol 27(2):391–397
Touho H, Karasawa J, Ohnishi H (1996) Preoperative and postoperative evaluation of cerebral perfusion and vasodilatory capacity with 99mTc-HMPAO SPECT and acetazolamide in childhood moyamoya disease. Stroke 27(2):282–289
Touho H, Karasawa J, Shishido H, Morisako T, Yamada K, Nagai S, Shibamoto K (1990) Mechanism of the re-buildup phenomenon in moyamoya disease—analysis of local cerebral hemodynamics with intra-arterial digital subtraction angiography. Neurol Med Chir 30(10):721
Vendrame M, Kalelyias J, Loddenkemper T, Smith E, Rockoff M, Manganaro S, McKenzie B, Gao L, Scott M, Bourgeois B, Kothare S (2011) Encephalogram monitoring during intracranial surgery for moyamoya disease. Pediatr Neurol 44:427–432
Wakai K, Tamakoshi A, Ikezaki K, Fukui M, Kawamura T, Aoki R, Kojima M, Lin Y, Ohno Y (1997) Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg 99:S1–S5
Yamada I, Suzuki S, Matsushima Y (1995) Moyamoya disease: diagnostic accuracy of MRI. Neuroradiology 37(5):356–361
Yamatani M, Konishi T, Murakami M, Okuda T (1994) Hyperventilation activation on EEG recording in childhood. Epilepsia 35(6):1199–1203
Yun TJ, Cheon JE, Na DG, Kim WS, Kim IO, Chang KH, Yeon KM, Song IC, Wang KC (2009) Childhood moyamoya disease: quantitative evaluation of perfusion MR imaging—correlation with clinical outcome after revascularization surgery1. Radiology 251(1):216–223
Acknowledgments
This study was supported by a grant of the Korean Health Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (A120099).
We would like to thank Jae So Cho for English revision of this article.
Conflict of interest
The authors declared no potential conflicts of interests with respect to the authorship and/or publication of this article.
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Jong-Hee Chae: Equally contributed and first author of the study.
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Cho, A., Chae, JH., Kim, H.M. et al. Electroencephalography in pediatric moyamoya disease: reappraisal of clinical value. Childs Nerv Syst 30, 449–459 (2014). https://doi.org/10.1007/s00381-013-2215-4
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DOI: https://doi.org/10.1007/s00381-013-2215-4