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Accuracy of brain perfusion single-photon emission computed tomography for detecting misery perfusion in adult patients with symptomatic ischemic moyamoya disease

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Abstract

Objective

The purpose of the present study was to determine how accurately relative cerebral blood flow (RCBF) and relative cerebrovascular reactivity (RCVR) to acetazolamide assessed using brain perfusion single-photon emission computed tomography (SPECT) detected misery perfusion identified on positron emission tomography (PET) in adult patients with ischemic moyamoya disease (MMD).

Methods

Oxygen extraction fraction (OEF), RCBF, and RCVR were assessed using 15O gas PET and N-isopropyl-p-[123I]-iodoamphetamine SPECT without and with acetazolamide challenge, respectively, in 45 patients. Regions of interest (ROIs) were automatically placed in the five middle cerebral artery (MCA) territories in the symptomatic cerebral hemisphere and in the ipsilateral cerebellar hemisphere using a three-dimensional stereotaxic ROI template. For RCBF and RCVR to acetazolamide, the ratio of the MCA ROI to cerebellar ROI was calculated. Of the five MCA ROIs in the symptomatic cerebral hemisphere in each patient, the ROI with the highest and lowest OEF value (two ROIs per patient) was selected for analyses.

Results

A significant square or linear correlation was observed between the OEF and RCBF (correlation coefficient, 0.780) or RCVR (correlation coefficient, − 0.345), respectively. The area under the receiver operating characteristic curve for detecting misery perfusion (OEF > 51.3%) was significantly greater for the RCBF than for the RCVR (difference between areas, 0.221; p < 0.0001). Sensitivity, specificity, and positive- and negative-predictive values for the RCBF for detecting misery perfusion were 100, 91, 67, and 100%, respectively. The specificity and positive-predictive value did not differ between the combination of the RCBF and RCVR and the CBF ratio alone.

Conclusions

RCBF assessed using brain perfusion SPECT detects misery perfusion with high sensitivity, a high negative-predictive value, and a low positive-predictive value in adult patients with ischemic MMD. The accuracy of RCVR to acetazolamide assessed using brain perfusion SPECT is lower than that of RCBF.

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Abbreviations

AUC:

Area under the receiver operating characteristic curve

CBF:

Cerebral blood flow

CI:

Confidence interval

CVR:

Cerebrovascular reactivity

ICA:

Internal carotid artery

123I-IMP:

N-Isopropyl-p-[123I]-iodoamphetamine

MCA:

Middle cerebral artery

MMD:

Moyamoya disease

OEF:

Oxygen extraction fraction

PET:

Positron emission tomography

RCBF:

Relative cerebral blood flow

RCBFACZ :

Relative cerebral blood flow with acetazolamide challenge

RCBFrest :

Relative cerebral blood flow without acetazolamide challenge

RCVR:

Relative cerebrovascular reactivity to acetazolamide

ROC:

Receiver operating characteristic

ROIs:

Regions of interest

SD:

Standard deviation

SPECT:

Single-photon emission computed tomography

References

  1. Research Committee on the Pathology and treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Intractable Diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo). 2012;52:245–66.

    Article  Google Scholar 

  2. Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288–99.

    Article  CAS  Google Scholar 

  3. Fujimura M, Tominaga T. 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. 2015;236:45–53.

    Article  Google Scholar 

  4. Fujimura M, Shimizu H, Mugikura S, Tominaga T. Delayed intracerebral hemorrhage after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease: possible involvement of cerebral hyperperfusion and increased vascular permeability. Surg Neurol. 2009;71:223–7.

    Article  Google Scholar 

  5. Fushimi Y, Okada T, Takagi Y, Funaki T, Takahashi JC, Miyamoto S, et al. Voxel based analysis of surgical revascularization for moyamoya disease: pre- and postoperative SPECT studies. PLoS One 2016:11:e0148925.

  6. Grubb RL Jr, Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO, et al. Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. JAMA. 1998;280:1055–60.

    Article  Google Scholar 

  7. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. J Neurosurg. 2009;111:927–35.

    Article  Google Scholar 

  8. Miyoshi K, Chida K, Kobayashi M, Kubo Y, Yoshida K, Terasaki K, et al. Two-year clinical, cerebral hemodynamic and cognitive outcomes of adult patients undergoing medication alone for symptomatically ischemic moyamoya disease without cerebral misery perfusion: a prospective cohort study. Neurosurgery 2018.https://doi.org/10.1093/neuros/nyy234.

  9. Baron JC, Bousser MG, Rey A, Guillard A, Comar D, Castaigne P. Reversal of focal “misery-perfusion syndrome” by extra-intracranial arterial bypass in hemodynamic cerebral ischemia: a case study with 15O positron emission tomography. Stroke 1981;12:454–59.

    Article  CAS  Google Scholar 

  10. Nemoto EM, Yonas H, Kuwabara H, Pindzola RR, Sashin D, Meltzer CC, et al. Identification of hemodynamic compromise by cerebrovascular reserve and oxygen extraction fraction in occlusive vascular disease. J Cereb Blood Flow Metab. 2004;24:1081–9.

    Article  Google Scholar 

  11. Yamauchi H, Okazawa H, Kishibe Y, Sugimoto K, Takahashi M. Oxygen extraction fraction and acetazolamide reactivity in symptomatic carotid artery disease. J Neurol Neurosurg Psychiatry. 2004;75:33–7.

    Article  CAS  Google Scholar 

  12. Kuroda H, Ogasawara K, Suzuki T, Chida K, Aso K, Kobayashi M, et al. Accuracy of central benzodiazepine receptor binding potential/cerebral blood flow SPECT imaging for detecting misery perfusion in patients with unilateral major cerebral artery occlusive diseases: comparison with cerebrovascular reactivity to acetazolamide and cerebral blood flow SPECT imaging. Clin Nucl Med. 2012;37:235–40.

    Article  Google Scholar 

  13. Imaizumi M, Kitagawa K, Hashikawa K, Oku N, Teratani T, Takasawa M, et al. Detection of misery perfusion with split-dose 123I-iodoamphetamine single-photon emission computed tomography in patients with carotid occlusive diseases. Stroke. 2002;33:2217–23.

    Article  CAS  Google Scholar 

  14. Kuroda S, Shiga T, Houkin K, Ishikawa T, Katoh C, Tamaki N, et al. Cerebral oxygen metabolism and neuronal integrity in patients with impaired vasoreactivity attributable to occlusive carotid artery disease. Stroke. 2006;37:393–8.

    Article  CAS  Google Scholar 

  15. Hokari M, Kuroda S, Shiga T, Nakayama N, Tamaki N, Iwasaki Y. Combination of a mean transit time measurement with an acetazolamide test increases predictive power to identify elevated oxygen extraction fraction in occlusive carotid artery diseases. J Nucl Med. 2008;49:1922–7.

    Article  Google Scholar 

  16. Ibaraki M, Miura S, Shimosegawa E, Sugawara S, Mizuta T, Ishikawa A, et al. Quantification of cerebral blood flow and oxygen metabolism with 3-dimensional PET and 15O: validation by comparison with 2-dimensional PET. J Nucl Med. 2008;49:50–9.

    Article  Google Scholar 

  17. Frackowiak RS, Lenzi GL, Jones T, Heather JD. Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 15O and positron emission tomography: theory, procedure, and normal values. J Comput Assist Tomogr. 1980;4:727–36.

    Article  CAS  Google Scholar 

  18. Nishimiya M, Matsuda H, Imabayashi E, Kuji I, Sato N. Comparison of SPM and NEUROSTAT in voxelwise statistical analysis of brain SPECT and MRI at the early stage of Alzheimer’s disease. Ann Nucl Med. 2008;22:921–7.

    Article  Google Scholar 

  19. Takeuchi R, Matsuda H, Yoshioka K, Yonekura Y. Cerebral blood flow SPET in transient global amnesia with automated ROI analysis by 3DSRT. Eur J Nucl Med Mol Imaging. 2004;31:578–89.

    Article  Google Scholar 

  20. Pepe MS, Longton G. Standardizing diagnostic markers to evaluate and compare their performance. Epidemiology. 2005;16:598–603.

    Article  Google Scholar 

  21. Kuroda S, Kamiyama H, Abe H, Houkin K, Isobe M, Mitsumori K. Acetazolamide test in detecting reduced cerebral perfusion reserve and predicting long-term prognosis in patients with internal carotid artery occlusion. Neurosurgery. 1993;32:912–8.

    Article  CAS  Google Scholar 

  22. Okazawa H, Tsuchida T, Kobayashi M, Arai Y, Pagani M, Isozaki M, et al. Can the detection of misery perfusion in chronic cerebrovascular disease be based on reductions in baseline CBF and vasoreactivity? Eur J Nucl Med Mol Imaging. 2007;34:121–9.

    Article  Google Scholar 

  23. Derdeyn CP, Zipfel GJ, Zazulia AR, Davis PH, Prabhakaran S, Ivan CS, et al. Baseline hemodynamic impairment and future stroke risk in adult idiopathic moyamoya phenomenon: results of a prospective natural history study. Stroke. 2017;48:894–9.

    Article  Google Scholar 

  24. Saito N, Nakagawara J, Nakamura H, Teramoto A. Assessment of cerebral hemodynamics in childhood moyamoya disease using a quantitative and a semiquantitative IMP-SPECT study. Ann Nucl Med. 2004;18:323–31.

    Article  Google Scholar 

  25. Ibaraki M, Shimosegawa E, Miura S, Takahashi K, Ito H, Kanno I, et al. PET measurements of CBF, OEF, and CMRO2 without arterial sampling in hyperacute ischemic stroke: Method and error analysis. Ann Nucl Med. 2004;18:35–44.

    Article  Google Scholar 

  26. Kume N, Hayashida K, Iwama T, Cho I, Matsunaga N. Use of 123I-IMP brain SPET to predict outcome following STA-MCA bypass surgery: cerebral blood flow but not vasoreactivity is a predictive parameter. Eur J Nucl Med. 1998;25:1637–42.

    Article  CAS  Google Scholar 

  27. Ito H, Kanno I, Shimosegawa E, Tamura H, Okane K, Hatazawa J. Hemodynamic changes during neural deactivation in human brain: a positron emission tomography study of crossed cerebellar diaschisis. Ann Nucl Med. 2002;16:249.

    Article  Google Scholar 

  28. Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N. Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke. 2012;43:2610–6.

    Article  Google Scholar 

  29. Kuroda S, Kashiwazaki D, Hirata K, Shiga T, Houkin K, Tamaki N. Effects of surgical revascularization on cerebral oxygen metabolism in patients with moyamoya disease: An 15O-gas positron emission tomographic study. Stroke. 2014;45:2717–21.

    Article  CAS  Google Scholar 

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Funding

This work was partly supported by Grants-in-Aid for Strategic Medical Science Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (S1491001); and for Scientific Research from the Japan Society for the Promotion of Science (JP18K09002).

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Correspondence to Kuniaki Ogasawara.

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The author (Kuniaki Ogasawara) declared the following potential conflict of interest with respect to the research, authorship, and/or publication of this article: Consigned research funds from Nihon Medi-Physics Co., Ltd.

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Setta, K., Kojima, D., Shimada, Y. et al. Accuracy of brain perfusion single-photon emission computed tomography for detecting misery perfusion in adult patients with symptomatic ischemic moyamoya disease. Ann Nucl Med 32, 611–619 (2018). https://doi.org/10.1007/s12149-018-1283-7

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  • DOI: https://doi.org/10.1007/s12149-018-1283-7

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