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Hemodynamic stress distribution identified by SPECT reflects ischemic symptoms of Moyamoya disease patients

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Abstract

This study aimed to validate the hypothesis that the ratio of cerebral blood flow (CBF) at rest in the lenticular nucleus (LN) territory to that in the middle cerebral artery (MCA) territory is higher in symptomatic Moyamoya disease (MMD) patients than in asymptomatic MMD patients. This was a retrospective observational study of adult patients with documented MMD who underwent single-photon emission computed tomography (SPECT) and had been examined at the Department of Neurosurgery of Keio University Hospital during a 10-year period (2006–2016). The diagnosis was made on the basis of typical imaging findings. We classified unoperated MMD patients into three groups: class I, no evidence of stenosis or occlusion hemispheres and without symptoms in unilateral MMD patients; class II, hemispheres with stenosis or occlusion but without ischemic symptoms; and class III, hemispheres with evidence of stenosis or occlusion associated with ischemic symptoms. Hemodynamic stress distribution (hdSD) was defined as the ratio of CBF in one LN to the CBF in the peripheral MCA; this was obtained by SPECT at rest. We compared the values of CBF and hdSD among the groups. A total of 173 adult patients were diagnosed with MMD from January 1, 2006, to January 1, 2016. Among them, 85 MMD patients underwent SPECT studies. After excluding inappropriate cases, 144 hemispheres were included in our analysis. hdSD was significantly higher (p < 0.001) in hemispheres with ischemic symptoms (class III, mean hdSD = 1.1; 36 sides) than in those without symptoms (class II, mean hdSD = 1.03; 82 sides). However, CBF at rest in the MCA or LN was not significantly associated with ischemic symptoms. The optimal threshold for hdSD to have ischemic symptoms was 1.040 (area under the curve; 74% sensitivity 91.7% and specificity 54.9%). We used SPECT to investigate cerebral blood from MMD patients and found that high hdSD values were predictive of ischemic symptom development in these patients.

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References

  1. Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research committee on spontaneous occlusion of the circle of Willis (Moyamoya disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 99:S238–S240

    PubMed  Google Scholar 

  2. Ogawa A, Yoshimoto T, Suzuki J, Sakurai Y (1990) Cerebral blood flow in moyamoya disease. Part 1: correlation with age and regional distribution. Acta Neurochir 105:30–34

    CAS  PubMed  Google Scholar 

  3. Baba T, Houkin K, Kuroda S (2008) Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79:900–904

    CAS  PubMed  Google Scholar 

  4. Nariai T, Suzuki R, Matsushima Y, Ishimura K, Hirakawa K, Ishii K et al (1994) Surgically induced angiogenesis to compensate for hemodynamic cerebral ischemia. Stroke 24:1014–1021

    Google Scholar 

  5. Pandey P, Steinberg GK (2011) Neurosurgical advances in the treatment of moyamoya disease. Stroke 42:3304–3310

    PubMed  Google Scholar 

  6. Czabanka M, Peña-Tapia P, Scharf J, Schubert GA, Münch E, Horn P, Schmiedek P, Vajkoczy P (2011) Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis 32:361–369

    CAS  PubMed  Google Scholar 

  7. Schmiedek P, Piepgras A, Leinsinger G, Kirsch CM, Einhüpl K (1994) Improvement of cerebrovascular reserve capacity by EC-IC arterial bypass surgery in patients with ICA occlusion and hemodynamic cerebral ischemia. J Neurosurg 81:236–244

    CAS  PubMed  Google Scholar 

  8. Zimmermann S, Achenbach S, Wolf M, Janka R, Marwan M, Mahler V (2014) Recurrent shock and pulmonary edema due to acetazolamide medication after cataract surgery. Heart Lung 43:124–126

    CAS  PubMed  Google Scholar 

  9. Takahashi S, Tanizaki Y, Kimura H, Akaji K, Nakazawa M, Yoshida K, Mihara B (2015) Hemodynamic stress distribution reflects ischemic clinical symptoms of patients with moyamoya disease. Clin Neurol Neurosurg 138:104–110

    PubMed  Google Scholar 

  10. Okamoto K, Ushijima Y, Okuyama C, Nakamura T, Nishimura T (2002) Measurement of cerebral blood flow using graph plot analysis and I-123 iodoamphetamine. Clin Nucl Med 27:191–196

    PubMed  Google Scholar 

  11. Ishikawa M, Saito H, Yamaguro T, Ikoda M, Ebihara A, Kusaka G, Tanaka Y (2016) Cognitive impairment and neurovascular function in patients with severe steno-occlusive disease of a main cerebral artery. J Neurol Sci 361:43–48

    PubMed  Google Scholar 

  12. Ogura T, Hida K, Masuzuka T, Saito H, Minoshima S, Nishikawa K (2009) An automated ROI setting method using NEUROSTAT on cerebral blood flow SPECT images. Ann Nucl Med 23:33–41

    PubMed  Google Scholar 

  13. Suzuki J, Takaku A (1969 Mar) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20(3):288–299

    CAS  PubMed  Google Scholar 

  14. Kashiwagi S, Yamashita T, Katoh S, Kitahara T, Nakashima K, Yasuhara S, Ito H (1996) Regression of moyamoya vessels and hemodynamic changes after successful revascularization in childhood moyamoya disease. Acta Neurol Scand Suppl 166:85–88

    CAS  PubMed  Google Scholar 

  15. Schubert GA, Czabanka M, Seiz M, Horn P, Vajkoczy P, Thomé C (2014) Perfusion characteristics of Moyamoya disease: an anatomically and clinically oriented analysis and comparison. Stroke 45:101–106

    PubMed  Google Scholar 

  16. Yonas H, Smith HA, Durham SR, Pentheny SL, Johnson DW (1993) Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 79:483–489

    CAS  PubMed  Google Scholar 

  17. Gupta A, Chazen JL, Hartman M, Delgado D, Anumula N, Shao H, Mazumdar M, Segal AZ, Kamel H, Leifer D, Sanelli PC (2012) Cerebrovascular reserve and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. Stroke. 43:2884–2891

    PubMed  PubMed Central  Google Scholar 

  18. Fujimura M, Tominaga T (2015 May) Current status of revascularization surgery for Moyamoya disease: special consideration for its ‘internal carotid-external carotid (IC-EC) conversion’ as the physiological reorganization system. Tohoku J Exp Med 236(1):45–53

    PubMed  Google Scholar 

  19. Acker G, Lange C, Schatka I, Pfeifer A, Czabanka MA, Vajkoczy P, Buchert R (2018 Feb) Brain perfusion imaging under acetazolamide challenge for detection of impaired cerebrovascular reserve capacity: positive findings with 15O-water PET in patients with negative 99mTc-HMPAO SPECT findings. J Nucl Med 59(2):294–298

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgery, Keio University School of Medicine, 35 Shinanomachi, Shinjukuku, Tokyo, Japan

    Nobuhiko Arai, Takashi Horiguchi, Satoshi Takahashi, Takenori Akiyama & Kazunari Yoshida

  2. Department of Radiology, Keio University School of Medicine, Tokyo, Japan

    Tadaki Nakahara & Masahiro Jinzaki

Authors
  1. Nobuhiko Arai
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  2. Takashi Horiguchi
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  3. Satoshi Takahashi
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  4. Tadaki Nakahara
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  5. Takenori Akiyama
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  6. Masahiro Jinzaki
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  7. Kazunari Yoshida
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Correspondence to Nobuhiko Arai.

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All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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This is retrospective observational study. Keio University Ethical Committee approved the study and waived the necessity of individual patients included in the study.

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Arai, N., Horiguchi, T., Takahashi, S. et al. Hemodynamic stress distribution identified by SPECT reflects ischemic symptoms of Moyamoya disease patients. Neurosurg Rev 43, 1323–1329 (2020). https://doi.org/10.1007/s10143-019-01145-w

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  • DOI: https://doi.org/10.1007/s10143-019-01145-w

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