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Journal of Neurology

, Volume 257, Issue 5, pp 806–815 | Cite as

Neurocognitive dysfunction in adult moyamoya disease

  • Joanne R. FestaEmail author
  • Lauren R. Schwarz
  • Neil Pliskin
  • C. Munro Cullum
  • Laura Lacritz
  • Fady T. Charbel
  • Dana Mathews
  • Robert M. Starke
  • E. Sander Connolly
  • Randolph S. Marshall
  • Ronald M. Lazar
Original Communication

Abstract

We wanted to determine the neurocognitive profile of adult patients with moyamoya disease prior to neurosurgical intervention. The experience of three United States medical centers, Columbia University, University of Illinois at Chicago, and the University of Texas Southwestern Medical Center at Dallas, were combined. Clinical data from adult patients (N = 29) referred for neuropsychological evaluation from 1996 to 2008 were reviewed. Neurocognitive functioning was assessed using standardized neuropsychological tests and all data were converted to z-scores. Memory, attention, processing speed, verbal memory, visuo-spatial, language, and executive functions were examined. Cognitive dysfunction was defined as performance in two or more cognitive domains 1.5 standard deviations below age-corrected normative means OR one or more cognitive domains two standard deviations below age-corrected normative means. Manual strength and dexterity, as well as depressive symptoms, were also assessed. Two-thirds of patients demonstrated neurocognitive dysfunction. A large proportion of patients were found to have pronounced cognitive dysfunction (>2 SD below the mean) on tests of processing speed (29%), verbal memory (31%), verbal fluency (26%) and executive function (25%). Manual strength and dexterity were also affected in many patients, with impairment found in 36–58% of patients. Twenty-eight percent of patients reported moderate to severe depression, but depressive symptoms did not correlate with neurocognitive findings. A large proportion of adults with moyamoya disease demonstrate disruption of neurocognition in a broad range of functions, particularly those mediated by subcortical and frontal regions. The pattern of deficits suggests a mechanism of diffuse small vessel disease possibly caused by chronic hypoperfusion.

Keywords

Moyamoya Cognitive functioning Neuropsychology 

Notes

Acknowledgment

This work was supported in part by NIH:NCRR M01 RR 00645-27 Pilot Award, 2004.

Conflicts of interest statement

There are no conflicts of interests to report.

References

  1. 1.
    Beck A, Steer R, Brown G (1996) Beck depression inventory, 2nd edn. The Psychological Corporation, San AntonioGoogle Scholar
  2. 2.
    Benton A, Hamsher K (1989) Multilingual aphasia examination. AJA Associates, Iowa CityGoogle Scholar
  3. 3.
    Bornstein RA (1985) Neuropsychological performance in Moya Moya disease: a case study. Int J Neurosci 26:39–46CrossRefPubMedGoogle Scholar
  4. 4.
    Brandt J, Benedict R (2001) Hopkins verbal learning test-revised. Psychological Assessment Resources, OdessaGoogle Scholar
  5. 5.
    Chiu D, Shedden P, Bratina P, Grotta JC (1998) Clinical features of moyamoya disease in the United States. Stroke 29:1347–1351PubMedGoogle Scholar
  6. 6.
    Chmayssani M, Festa JR, Marshall RS (2007) Chronic ischemia and neurocognition. Neuroimaging Clin N Am 17:313–324CrossRefPubMedGoogle Scholar
  7. 7.
    Choi JU, Kim DS, Kim EY, Lee KC (1997) Natural history of moyamoya disease: comparison of activity of daily living in surgery and non surgery groups. Clin Neurol Neurosurg 99(suppl 2):S11–S18CrossRefPubMedGoogle Scholar
  8. 8.
    Delis D, Kramer J, Kaplan E, Ober B (1994) California verbal learning test, 2nd edn. Adult Version. The Pyschological Corporation, San AntonioGoogle Scholar
  9. 9.
    Hachinski V, Iadecola C, Petersen RC, Breteler MM, Nyenhuis DL, Black SE, Powers WJ, DeCarli C, Merino JG, Kalaria RN, Vinters HV, Holtzman DM, Rosenberg GA, Wallin A, Dichgans M, Marler JR, Leblanc GG (2006) National Institute of Neurological Disorders and Stroke-Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke 37:2220–2241 (see comment) [erratum appears in Stroke. 2007 Mar;38(3):1118 Note: Wallin, Anders (added)]Google Scholar
  10. 10.
    Hallemeier CL, Rich KM, Grubb RL Jr, Chicoine MR, Moran CJ, Cross DT III, Zipfel GJ, Dacey RG Jr, Derdeyn CP (2006) Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37:1490–1496CrossRefPubMedGoogle Scholar
  11. 11.
    Heaton R, Chelune G, Talley J, Kay G, Curtiss G (1993) Wisconsin card sorting test manual revised and expanded. Psychological Assessment Resources, OdessaGoogle Scholar
  12. 12.
    Ikezaki K, Han DH, Kawano T, Kinukawa N, Fukui M (1997) A clinical comparison of definite moyamoya disease between South Korea and Japan. Stroke 28:2513–2517PubMedGoogle Scholar
  13. 13.
    Jefferson AL, Glosser G, Detre JA, Sinson G, Liebeskind DS (2006) Neuropsychological and perfusion MR imaging correlates of revascularization in a case of moyamoya syndrome. AJNR Am J Neuroradiol 27:98–100PubMedGoogle Scholar
  14. 14.
    Kaplan E, Goodglass H, Weintraub S (1983) The Boston naming test, 2nd edn. Lea and Feinberg, PhiladelphiaGoogle Scholar
  15. 15.
    Karzmark P, Zeifert PD, Tan S, Dorfman LJ, Bell-Stephens TE, Steinberg GK (2008) Effect of moyamoya disease on neuropsychological functioning in adults. Neurosurgery 62:1048–1051 (discussion 1051–1042)CrossRefPubMedGoogle Scholar
  16. 16.
    Kim JM, Lee SH, Roh JK (2009) Changing ischaemic lesion patterns in adult moyamoya disease. J Neurol Neurosurg Psychiatry 80:36–40CrossRefPubMedGoogle Scholar
  17. 17.
    Kraemer M, Heienbrok W, Berlit P (2008) Moyamoya disease in Europeans. Stroke 39:3193–3200CrossRefPubMedGoogle Scholar
  18. 18.
    Lezak M, Howieson D, Loring D, Hannay H, Fischer J (2004) Neuropsychological assessment, 4th edn. Oxford University Press, New YorkGoogle Scholar
  19. 19.
    Matthews C, Klove K (1964) Instruction manual for the adult neuropsychological test battery. University of Wisconsin Medical School, MadisonGoogle Scholar
  20. 20.
    Mula M, Trimble MR, Mula M, Trimble MR (2009) Antiepileptic drug-induced cognitive adverse effects: potential mechanisms and contributing factors. CNS Drugs 23:121–137CrossRefPubMedGoogle Scholar
  21. 21.
    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–S161PubMedGoogle Scholar
  22. 22.
    Nelson H, Willison J (1991) National adult reading test (NART): test manual, 2nd edn. NFER Nelson Windsor, UKGoogle Scholar
  23. 23.
    Numaguchi Y, Gonzalez CF, Davis PC, Monajati A, Afshani E, Chang J, Sutton CL, Lee RR, Shibata DK (1997) Moyamoya disease in the United States. Clin Neurol Neurosurg 99(suppl 2):S26–S30CrossRefPubMedGoogle Scholar
  24. 24.
    Ogasawara K, Komoribayashi N, Kobayashi M, Fukuda T, Inoue T, Yamadate K, Ogawa A (2005) Neural damage caused by cerebral hyperperfusion after arterial bypass surgery in a patient with moyamoya disease: case report. Neurosurgery 56:E1380 (discussion E1380)CrossRefPubMedGoogle Scholar
  25. 25.
    Radloff L (1977) The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas 1:385–401CrossRefGoogle Scholar
  26. 26.
    Reitan R, Wolfson D (1985) The Halstead Reitan neuropsychological test battery. Neuropsychological Press, TucsonGoogle Scholar
  27. 27.
    Reitan R, Wolfson D (1993) The Halstead Reitan neuropsychological test battery: theory and clinical applications, 2nd edn. Neuropsychological Press, TucsonGoogle Scholar
  28. 28.
    Starke RM, Komotar RJ, Hickman SL, Paz YE, Pugliese AG, Otten ML, Garrett MC, Elkind MSV, Marshall RS, Festa JR, Meyers PM, Connolly ES (2009) Clinical features, surgical treatment, and long-term outcome of adult moyamoya patients. J Neurosurg 111:936–942CrossRefPubMedGoogle Scholar
  29. 29.
    Takeuchi K, Shimizu K (1957) Hypogenesis of bilateral internal carotid arteries. No To Shinkei 9:37–43Google Scholar
  30. 30.
    Wechsler D (1990) Wechsler abbreviated intelligence scale. The Psychological Corporation, San AntonioGoogle Scholar
  31. 32.
    Wechsler D (1991) Wechsler test of adult reading. The Psychological Corporation, San AntonioGoogle Scholar
  32. 31.
    Wechsler D (1997) Wechsler adult intelligence scale, 3rd edn. The Psychological Corporation, San AntonioGoogle Scholar
  33. 33.
    White J, Hopkins RO, Glissmeyer EW, Kitterman N, Elliott CG (2006) Cognitive, emotional, and quality of life outcomes in patients with pulmonary arterial hypertension. Resp Res 7:55CrossRefGoogle Scholar
  34. 34.
    Wityk RJ, Hillis A, Beauchamp N, Barker PB, Rigamonti D (2002) Perfusion-weighted magnetic resonance imaging in adult moyamoya syndrome: characteristic patterns and change after surgical intervention: case report. Neurosurgery 51:1499–1505 (discussion 1506)CrossRefPubMedGoogle Scholar
  35. 35.
    Wright CB, Festa JR, Paik MC, Schmiedigen A, Brown TR, Yoshita M, DeCarli C, Sacco R, Stern Y (2008) White matter hyperintensities and subclinical infarction: associations with psychomotor speed and cognitive flexibility. Stroke 39:800–805CrossRefPubMedGoogle Scholar
  36. 36.
    Yilmaz EY, Pritz MB, Bruno A, Lopez-Yunez A, Biller J (2001) Moyamoya: Indiana University Medical Center experience. Arch Neurol 58:1274–1278CrossRefPubMedGoogle Scholar
  37. 37.
    Yonekawa Y, Ogata N, Kaku Y, Taub E, Imhof HG (1997) Moyamoya disease in Europe, past and present status. Clin Neurol Neurosurg 99(suppl 2):S58–S60CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Joanne R. Festa
    • 1
    Email author
  • Lauren R. Schwarz
    • 2
  • Neil Pliskin
    • 2
  • C. Munro Cullum
    • 3
  • Laura Lacritz
    • 3
  • Fady T. Charbel
    • 2
  • Dana Mathews
    • 3
  • Robert M. Starke
    • 1
  • E. Sander Connolly
    • 1
  • Randolph S. Marshall
    • 1
  • Ronald M. Lazar
    • 1
  1. 1.College of Physicians and Surgeons, Neurological InstituteColumbia UniversityNew YorkUSA
  2. 2.University of Illinois College of MedicineChicagoUSA
  3. 3.University of Texas Southwestern Medical Center at DallasDallasUSA

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