Skip to main content
Top
Published in: Child's Nervous System 6/2018

01-06-2018 | Original Paper

Neuropsychological impacts of indirect revascularization for pediatric moyamoya disease

Authors: WooHyun Kim, Eun-Young Lee, Seong-eun Park, Eun-Kyung Park, Ju-Seong Kim, Dong-Seok Kim, Kyu-Won Shim

Published in: Child's Nervous System | Issue 6/2018

Login to get access

Abstract

Purpose

Moyamoya disease (MMD) commonly leads to neurocognitive impairment. This study was carried out to show that temporal encephaloduroarteriosynangiosis (EDAS) has a positive neuropsychological impact on pediatric MMD patients.

Methods

Fifty-five participants diagnosed with MMD from 2008 to 2014 were included in this retrospective study. The mean age at the preoperative evaluation was 9.5 years and the mean age at postoperative evaluation was 10.4. The average interval of initial and follow-up test was 10 months. K-WISC-III, Rey-Kim memory test, Children’s Color Trails test (CCTT), Wisconsin Card Sorting Test (WCST), and Advanced Test of Attention (ATA) were used to evaluate patient’s neurocognitive profile.

Results

In this study, preoperative and postoperative neuropsychological fields were compared. Prior operation, pediatric MMD patients showed 54.2% deficit of inattention but only around 2.5% deficit in verbal memory recall function. There was a significant increase of performance IQ and PO score component of PIQ improved almost 10 scores after surgery. For memorial function, there was an improvement of approximately 10 scores in MQ after the surgery. This study also showed parietal activation following surgical treatment which enhanced the ability to interpret visual materials, to register and to retrieve visual information. Interestingly, despite the parietal cover surgery, there was a significant improvement of performance on WCST and CCTT measuring the prefrontal executive function. Concerning failure to maintain set, no significant postoperative improvements were made. However, simple and selective visual attention on ATA was significantly improved postoperatively.

Conclusions

The results from neuropsychological field comparison testifies the effectiveness of temporal EDAS in pediatric MMD patients. The surgery not only enhances the blood flow in operative regions, but it also improves the broad cerebral function including frontoparietal domains. Such alteration leads to overall advancement in cognitive function which are impaired due to MMD.
Literature
1.
2.
go back to reference Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299CrossRefPubMed Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299CrossRefPubMed
3.
go back to reference Kuroda S, Houkin K, Ishikawa T, Nakayama N, Ikeda J, Ishii N, Kamiyama H, Iwasaki Y (2004) Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis. Childs Nerv Syst 20:302–308CrossRefPubMed Kuroda S, Houkin K, Ishikawa T, Nakayama N, Ikeda J, Ishii N, Kamiyama H, Iwasaki Y (2004) Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis. Childs Nerv Syst 20:302–308CrossRefPubMed
4.
go back to reference Smith JL (2009) Understanding and treating moyamoya disease in children. Neurosurg Focus 26:E4PubMed Smith JL (2009) Understanding and treating moyamoya disease in children. Neurosurg Focus 26:E4PubMed
5.
go back to reference Imaizumi C, Imaizumi T, Osawa M, Fukuyama Y, Takeshita M (1999) Serial intelligence test scores in pediatric moyamoya disease. Neuropediatrics 30:294–299CrossRefPubMed Imaizumi C, Imaizumi T, Osawa M, Fukuyama Y, Takeshita M (1999) Serial intelligence test scores in pediatric moyamoya disease. Neuropediatrics 30:294–299CrossRefPubMed
6.
go back to reference Williams TS, Westmacott R, Dlamini N, Granite L, Dirks P, Askalan R, Macgregor D, Moharir M, Deveber G (2012) Intellectual ability and executive function in pediatric moyamoya vasculopathy. Dev Med Child Neurol 54:30–37CrossRefPubMed Williams TS, Westmacott R, Dlamini N, Granite L, Dirks P, Askalan R, Macgregor D, Moharir M, Deveber G (2012) Intellectual ability and executive function in pediatric moyamoya vasculopathy. Dev Med Child Neurol 54:30–37CrossRefPubMed
8.
go back to reference Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, Hwang YS, Kim IO, Lee DS, Lee J, Wang KC (2010) Pediatric moyamoya disease: an analysis of 410 consecutive cases. Ann Neurol 68:92–101CrossRefPubMed Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, Hwang YS, Kim IO, Lee DS, Lee J, Wang KC (2010) Pediatric moyamoya disease: an analysis of 410 consecutive cases. Ann Neurol 68:92–101CrossRefPubMed
9.
go back to reference Matsushima Y, Aoyagi M, Nariai T, Takada Y, Hirakawa K (1997) Long-term intelligence outcome of post-encephalo-duro-arterio-synangiosis childhood moyamoya patients. Clin Neurol Neurosurg 99(Suppl 2):S147–S150CrossRefPubMed Matsushima Y, Aoyagi M, Nariai T, Takada Y, Hirakawa K (1997) Long-term intelligence outcome of post-encephalo-duro-arterio-synangiosis childhood moyamoya patients. Clin Neurol Neurosurg 99(Suppl 2):S147–S150CrossRefPubMed
10.
go back to reference Matsushima Y, Aoyagi M, Masaoka H, Suzuki R, Ohno K (1990) Mental outcome following encephaloduroarteriosynangiosis in children with moyamoya disease with the onset earlier than 5 years of age. Childs Nerv Syst 6:440–443CrossRefPubMed Matsushima Y, Aoyagi M, Masaoka H, Suzuki R, Ohno K (1990) Mental outcome following encephaloduroarteriosynangiosis in children with moyamoya disease with the onset earlier than 5 years of age. Childs Nerv Syst 6:440–443CrossRefPubMed
11.
go back to reference Nakashima H, Meguro T, Kawada S, Hirotsune N, Ohmoto T (1997) Long-term results of surgically treated moyamoya disease. Clin Neurol Neurosurg 99(Suppl 2):S156–S161CrossRefPubMed Nakashima H, Meguro T, Kawada S, Hirotsune N, Ohmoto T (1997) Long-term results of surgically treated moyamoya disease. Clin Neurol Neurosurg 99(Suppl 2):S156–S161CrossRefPubMed
12.
go back to reference Park SE, Kim JS, Park EK, Shim KW, Kim DS (2017) Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg:1–10 Park SE, Kim JS, Park EK, Shim KW, Kim DS (2017) Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg:1–10
13.
go back to reference Gonzalez N, Dusick J, Connolly M, Bounni F, Martin N, Van de Wiele B, Liebeskind D, Saver J (2015) Encephaloduroarteriosynangiosis for adult intracranial arterial steno-occlusive disease: long-term single-center experience with 107 operations. J Neurosurg 12:1–8 Gonzalez N, Dusick J, Connolly M, Bounni F, Martin N, Van de Wiele B, Liebeskind D, Saver J (2015) Encephaloduroarteriosynangiosis for adult intracranial arterial steno-occlusive disease: long-term single-center experience with 107 operations. J Neurosurg 12:1–8
14.
go back to reference Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kitamura K, Hasuo K (1989) Surgical treatment for paediatric patients with moyamoya disease by indirect revascularisation procedures (EDAS, EMS, EMAS). Acta Neurochir 98:135–140CrossRefPubMed Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kitamura K, Hasuo K (1989) Surgical treatment for paediatric patients with moyamoya disease by indirect revascularisation procedures (EDAS, EMS, EMAS). Acta Neurochir 98:135–140CrossRefPubMed
15.
go back to reference Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43; discussion 43CrossRefPubMed Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43; discussion 43CrossRefPubMed
16.
go back to reference Flanagan DP, Kaufman AS (2009) Essentials of Wisc-iv Assessment. Wiley, Hoboken Flanagan DP, Kaufman AS (2009) Essentials of Wisc-iv Assessment. Wiley, Hoboken
17.
go back to reference Kim H (2001) Assessment of memory disorders using Rey-Kim Memory Test. J Rehabil Psychol 8:29–48 Kim H (2001) Assessment of memory disorders using Rey-Kim Memory Test. J Rehabil Psychol 8:29–48
18.
go back to reference McMillian SG, Rees CS, Pestel C (2013) An investigation of executive functioning, attention and working memory in compulsive hoarding. Behav Cogn Psychother 41:610–625CrossRef McMillian SG, Rees CS, Pestel C (2013) An investigation of executive functioning, attention and working memory in compulsive hoarding. Behav Cogn Psychother 41:610–625CrossRef
19.
go back to reference Figueroa IJ, Youmans RJ (2013) Failure to maintain set: a measure of distractibility or cognitive flexibility?. Proceedings Of The Human Factors And Ergonomics Society 57th Annual Meeting Figueroa IJ, Youmans RJ (2013) Failure to maintain set: a measure of distractibility or cognitive flexibility?. Proceedings Of The Human Factors And Ergonomics Society 57th Annual Meeting
20.
go back to reference Kang CG, Chun MH, Kang JA, Do KH, Choi SJ (2017) Neurocognitive dysfunction according to hypoperfusion territory in patients with moyamoya disease. Ann Rehabil Med 41:1–8CrossRefPubMedPubMedCentral Kang CG, Chun MH, Kang JA, Do KH, Choi SJ (2017) Neurocognitive dysfunction according to hypoperfusion territory in patients with moyamoya disease. Ann Rehabil Med 41:1–8CrossRefPubMedPubMedCentral
21.
go back to reference Lei Y, Li YJ, Guo QH, Liu XD, Liu Z, Ni W, Su JB, Yang H, Jiang HQ, Xu B, Gu YX, Mao Y (2017) Postoperative executive function in adult moyamoya disease: a preliminary study of its functional anatomy and behavioral correlates. J Neurosurg 126:527–536CrossRefPubMed Lei Y, Li YJ, Guo QH, Liu XD, Liu Z, Ni W, Su JB, Yang H, Jiang HQ, Xu B, Gu YX, Mao Y (2017) Postoperative executive function in adult moyamoya disease: a preliminary study of its functional anatomy and behavioral correlates. J Neurosurg 126:527–536CrossRefPubMed
22.
go back to reference Kurokawa T, Tomita S, Ueda K, Narazaki O, Hanai T, Hasuo K, Matsushima T, Kitamura K (1985) Prognosis of occlusive disease of the circle of Willis (moyamoya disease) in children. Pediatr Neurol 1:274–277CrossRefPubMed Kurokawa T, Tomita S, Ueda K, Narazaki O, Hanai T, Hasuo K, Matsushima T, Kitamura K (1985) Prognosis of occlusive disease of the circle of Willis (moyamoya disease) in children. Pediatr Neurol 1:274–277CrossRefPubMed
24.
go back to reference Jones-Gotman M, Smith M, Zatorre R (1993) Neuropsychological testing for localizing and lateralizing the epileptogenic region. In: Engel J Jr (ed) Surgical treatment of epilepsies. Raven Press, New York, pp 245–261 Jones-Gotman M, Smith M, Zatorre R (1993) Neuropsychological testing for localizing and lateralizing the epileptogenic region. In: Engel J Jr (ed) Surgical treatment of epilepsies. Raven Press, New York, pp 245–261
25.
26.
go back to reference Song M, Liu Y, Zhou Y, Wang K, Yu C, Jiang T (2009) Default network and intelligence difference. Conf Proc IEEE Eng Med Biol Soc 2009:2212–2215PubMed Song M, Liu Y, Zhou Y, Wang K, Yu C, Jiang T (2009) Default network and intelligence difference. Conf Proc IEEE Eng Med Biol Soc 2009:2212–2215PubMed
27.
go back to reference Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32:8988–8999CrossRefPubMedPubMedCentral Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32:8988–8999CrossRefPubMedPubMedCentral
28.
go back to reference van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009) Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624CrossRefPubMed van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009) Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624CrossRefPubMed
Metadata
Title
Neuropsychological impacts of indirect revascularization for pediatric moyamoya disease
Authors
WooHyun Kim
Eun-Young Lee
Seong-eun Park
Eun-Kyung Park
Ju-Seong Kim
Dong-Seok Kim
Kyu-Won Shim
Publication date
01-06-2018
Publisher
Springer Berlin Heidelberg
Published in
Child's Nervous System / Issue 6/2018
Print ISSN: 0256-7040
Electronic ISSN: 1433-0350
DOI
https://doi.org/10.1007/s00381-018-3804-z

Other articles of this Issue 6/2018

Child's Nervous System 6/2018 Go to the issue