Skip to main content
Log in

Neuropsychological impacts of indirect revascularization for pediatric moyamoya disease

  • Original Paper
  • Published:
Child's Nervous System Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237

    Article  PubMed  CAS  Google Scholar 

  2. Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    Article  PubMed  CAS  Google Scholar 

  3. 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 20:302–308

    Article  PubMed  Google Scholar 

  4. Smith JL (2009) Understanding and treating moyamoya disease in children. Neurosurg Focus 26:E4

    PubMed  Google Scholar 

  5. Imaizumi C, Imaizumi T, Osawa M, Fukuyama Y, Takeshita M (1999) Serial intelligence test scores in pediatric moyamoya disease. Neuropediatrics 30:294–299

    Article  PubMed  CAS  Google Scholar 

  6. 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 54:30–37

    Article  PubMed  Google Scholar 

  7. Shim KW, Park EK, Kim JS, Kim DS (2015) Cognitive outcome of pediatric moyamoya disease. J Korean Neurosurg Soc 57:440–444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. 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 68:92–101

    Article  PubMed  Google Scholar 

  9. 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–S150

    Article  PubMed  Google Scholar 

  10. 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 6:440–443

    Article  PubMed  CAS  Google Scholar 

  11. 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–S161

    Article  PubMed  Google Scholar 

  12. 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. 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

    Google Scholar 

  14. 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 98:135–140

    Article  PubMed  CAS  Google Scholar 

  15. 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 43

    Article  PubMed  Google Scholar 

  16. Flanagan DP, Kaufman AS (2009) Essentials of Wisc-iv Assessment. Wiley, Hoboken

    Google Scholar 

  17. Kim H (2001) Assessment of memory disorders using Rey-Kim Memory Test. J Rehabil Psychol 8:29–48

    CAS  Google Scholar 

  18. McMillian SG, Rees CS, Pestel C (2013) An investigation of executive functioning, attention and working memory in compulsive hoarding. Behav Cogn Psychother 41:610–625

    Article  Google Scholar 

  19. 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. 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 41:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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 126:527–536

    Article  PubMed  Google Scholar 

  22. 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 1:274–277

    Article  PubMed  CAS  Google Scholar 

  23. Trahan LH, Stuebing KK, Fletcher JM, Hiscock M (2014) The Flynn effect: a meta-analysis. Psychol Bull 140:1332–1360

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Google Scholar 

  25. Hearne LJ, Mattingley JB, Cocchi L (2016) Functional brain networks related to individual differences in human intelligence at rest. Sci Rep 6:32328

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. 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 2009:2212–2215

    PubMed  Google Scholar 

  27. Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32:8988–8999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009) Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kyu-Won Shim.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, W., Lee, EY., Park, Se. et al. Neuropsychological impacts of indirect revascularization for pediatric moyamoya disease. Childs Nerv Syst 34, 1199–1206 (2018). https://doi.org/10.1007/s00381-018-3804-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00381-018-3804-z

Keywords

Navigation