DOI QR코드

DOI QR Code

Cerebrovascular Reservoir and Arterial Transit Time Changes Assessed by Acetazolamide-Challenged Multi-Phase Arterial Spin Labeling Perfusion MRI in Chronic Cerebrovascular Steno-Occlusive Disease

만성 뇌혈관 협착폐색증에서 아세타졸아미드 부하 다상 동맥스핀표지 자기공명관류영상으로 평가한 뇌혈류 예비능과 동맥 통과 시간의 변화

  • Inpyeong Hwang (Department of Radiology, Seoul National University Hospital) ;
  • Chul-Ho Sohn (Department of Radiology, Seoul National University Hospital) ;
  • Keun-Hwa Jung (Department of Neurology, Seoul National University Hospital) ;
  • Eung Koo Yeon (Department of Radiology, Seoul National University Hospital) ;
  • Ji Ye Lee (Department of Radiology, Seoul National University Hospital) ;
  • Roh-Eul Yoo (Department of Radiology, Seoul National University Hospital) ;
  • Koung Mi Kang (Department of Radiology, Seoul National University Hospital) ;
  • Tae Jin Yun (Department of Radiology, Seoul National University Hospital) ;
  • Seung Hong Choi (Department of Radiology, Seoul National University Hospital) ;
  • Ji-hoon Kim (Department of Radiology, Seoul National University Hospital)
  • 황인평 (서울대학교병원 영상의학과) ;
  • 손철호 (서울대학교병원 영상의학과) ;
  • 정근화 (서울대학교병원 신경과) ;
  • 연응구 (서울대학교병원 영상의학과) ;
  • 이지예 (서울대학교병원 영상의학과) ;
  • 유노을 (서울대학교병원 영상의학과) ;
  • 강경미 (서울대학교병원 영상의학과) ;
  • 윤태진 (서울대학교병원 영상의학과) ;
  • 최승홍 (서울대학교병원 영상의학과) ;
  • 김지훈 (서울대학교병원 영상의학과)
  • Received : 2020.12.08
  • Accepted : 2020.12.31
  • Published : 2021.05.01

Abstract

Purpose To explore cerebrovascular reservoir (CVR) and arterial transit time (ATT) changes using acetazolamide-challenged multi-phase arterial spin labeling (MP-ASL) perfusion-weighted MRI in chronic cerebrovascular steno-occlusive disease. Materials and Methods This retrospective study enrolled patients with chronic steno-occlusion who underwent acetazolamide-challenged MP-ASL between June 2019 and October 2020. Cerebral blood flow, CVR, basal ATT, and ATT changes associated with severe stenosis, total occlusion, and chronic infarction lesions were compared. Results There were 32 patients (5 with bilateral steno-occlusion) in our study sample. The CVR was significantly reduced during total occlusion compared with severe stenosis (26.2% ± 28.8% vs. 41.4% ± 34.1%, respectively, p = 0.004). The ATT changes were not significantly different (p = 0.717). The CVR was marginally lower in patients with chronic infarction (29.6% ± 39.1% vs. 38.9% ± 28.7%, respectively, p = 0.076). However, the ATT was less shortened in patients with chronic infarction (-54 ± 135 vs. -117 ± 128 ms, respectively, p = 0.013). Conclusion Acetazolamide-challenged MP-ASL provides an MRI-based CVR evaluation tool for chronic steno-occlusive disease.

목적 만성 뇌동맥 협착-폐색증에서 아세타졸아미드 부하 다상 동맥 스핀 표지(multi-phase arterial spin labeling; 이하 MP-ASL) 자기공명관류영상을 이용하여 뇌혈류 예비능(cerebrovascular reservoir; 이하 CVR)과 동맥 통과 시간(arterial transit time; 이하 ATT)의 변화를 탐색하였다. 대상과 방법 2019년 6월부터 2020년 10월까지 새롭게 만성 협착-폐색증으로 진단되어 아세타졸아미드 부하 MP-ASL을 시행한 환자를 후향적으로 모집하였다. 부하 전후의 뇌혈류(cerebral blood flow), CVR, 부하전 ATT 및 부하 전후의 ATT 변화량을 중증 협착과 완전 폐색간, 만성 뇌경색 병변의 유무에 따라 비교하였다. 결과 5명의 양측성 협착-폐색을 포함하여 총 32명의 환자가 본 연구에 포함되었다. CVR은 완전 폐색에서 중증 협착보다 유의하게 낮았다(26.2% ± 28.8% vs. 41.4% ± 34.1%, p = 0.004). ATT의 변화는 두 군간 유의한 차이는 없었다(p = 0.717). 만성 뇌경색 병변의 유무에 따른 CVR의 통계적 차이는 미미하였다(29.6% ± 39.1% vs. 38.9% ± 28.7%, p = 0.076). 하지만, 만성 뇌경색 병변이 있는 환자에서 ATT의 단축 정도는 유의하게 작았다(-54 ± 135 vs. -117 ± 128 ms, p = 0.013). 결론 만성 협착-폐색증에서 아세타졸아미드 부하 MP-ASL 검사는 MRI 기반의 CVR 평가 도구로 사용될 수 있다.

Keywords

Acknowledgement

This research was supported by the Bio & Medical Technology Development Program of the National Research Foundation (NRF) funded by the Korean government (MSIT) (No. 2018M3C7A1056884 and 2018M3C7A1056888).

References

  1. North American Symptomatic Carotid Endarterectomy Trial Collaborators, Barnett HJM, Taylor DW, Haynes RB, Sackett DL, Peerless SJ, et al. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 1991;325:445-453 https://doi.org/10.1056/NEJM199108153250701
  2. Brott TG, Hobson RW 2nd, Howard G, Roubin GS, Clark WM, Brooks W, et al. Stenting versus endarterectomy for treatment of carotid-artery stenosis. N Engl J Med 2010;363:11-23 https://doi.org/10.1056/NEJMoa0912321
  3. Derdeyn CP. Hemodynamics and oxygen extraction in chronic large artery steno-occlusive disease: clinical applications for predicting stroke risk. J Cereb Blood Flow Metab 2018;38:1584-1597 https://doi.org/10.1177/0271678X17732884
  4. Bang OY, Goyal M, Liebeskind DS. Collateral circulation in ischemic stroke: assessment tools and therapeutic strategies. Stroke 2015;46:3302-3309 https://doi.org/10.1161/STROKEAHA.115.010508
  5. Fisher JA, Venkatraghavan L, Mikulis DJ. Magnetic resonance imaging-based cerebrovascular reactivity and hemodynamic reserve. Stroke 2018;49:2011-2018 https://doi.org/10.1161/STROKEAHA.118.021012
  6. Reinhard M, Schwarzer G, Briel M, Altamura C, Palazzo P, King A, et al. Cerebrovascular reactivity predicts stroke in high-grade carotid artery disease. Neurology 2014;83:1424-1431 https://doi.org/10.1212/WNL.0000000000000888
  7. Haller S, Zaharchuk G, Thomas DL, Lovblad KO, Barkhof F, Golay X. Arterial spin labeling perfusion of the brain: emerging clinical applications. Radiology 2016;281:337-356 https://doi.org/10.1148/radiol.2016150789
  8. Yun TJ, Paeng JC, Sohn CH, Kim JE, Kang HS, Yoon BW, et al. Monitoring cerebrovascular reactivity through the use of arterial spin labeling in patients with Moyamoya disease. Radiology 2016;278:205-213 https://doi.org/10.1148/radiol.2015141865
  9. Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke 2011;42:2485-2491 https://doi.org/10.1161/STROKEAHA.111.616466
  10. Dai W, Shankaranarayanan A, Alsop DC. Volumetric measurement of perfusion and arterial transit delay using hadamard encoded continuous arterial spin labeling. Magn Reson Med 2013;69:1014-1022 https://doi.org/10.1002/mrm.24335
  11. Fan AP, Khalighi MM, Guo J, Ishii Y, Rosenberg J, Wardak M, et al. Identifying hypoperfusion in moyamoya disease with arterial spin labeling and an [15O]-water positron emission tomography/magnetic resonance imaging normative database. Stroke 2019;50:373-380 https://doi.org/10.1161/STROKEAHA.118.023426
  12. Samuels OB, Joseph GJ, Lynn MJ, Smith HA, Chimowitz MI. A standardized method for measuring intracranial arterial stenosis. AJNR Am J Neuroradiol 2000;21:643-646
  13. Dai W, Robson PM, Shankaranarayanan A, Alsop DC. Reduced resolution transit delay prescan for quantitative continuous arterial spin labeling perfusion imaging. Magn Reson Med 2012;67:1252-1265 https://doi.org/10.1002/mrm.23103
  14. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002;17:143-155 https://doi.org/10.1002/hbm.10062
  15. Greve DN, Fischl B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage 2009;48:63-72 https://doi.org/10.1016/j.neuroimage.2009.06.060
  16. Datta S, Satten GA. A signed-rank test for clustered data. Biometrics 2008;64:501-507 https://doi.org/10.1111/j.1541-0420.2007.00923.x
  17. Donner A, Klar N. Statistical considerations in the design and analysis of community intervention trials. J Clin Epidemiol 1996;49:435-439 https://doi.org/10.1016/0895-4356(95)00511-0
  18. Federau C, Christensen S, Zun Z, Park SW, Ni W, Moseley M, et al. Cerebral blood flow, transit time, and apparent diffusion coefficient in moyamoya disease before and after acetazolamide. Neuroradiology 2017;59:5-12 https://doi.org/10.1007/s00234-016-1766-y
  19. Gupta A, Chazen JL, Hartman M, Delgado D, Anumula N, Shao H, et al. Cerebrovascular reserve and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. Stroke 2012;43:2884-2891 https://doi.org/10.1161/STROKEAHA.112.663716
  20. Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Rossini PM, et al. Effect of collateral blood flow and cerebral vasomotor reactivity on the outcome of carotid artery occlusion. Stroke 2001;32:1552-1558 https://doi.org/10.1161/01.STR.32.7.1552
  21. Choi HJ, Sohn CH, You SH, Yoo RE, Kang KM, Yun TJ, et al. Can arterial spin-labeling with multiple postalbeling delays predict cerebrovascular reserve? AJNR Am J Neuroradiol 2018;39:84-90 https://doi.org/10.3174/ajnr.A5439
  22. Chen A, Shyr MH, Chen TY, Lai HY, Lin CC, Yen PS. Dynamic CT perfusion imaging with acetazolamide challenge for evaluation of patients with unilateral cerebrovascular steno-occlusive disease. AJNR Am J Neuroradiol 2006;27:1876-1881
  23. Ma J, Mehrkens JH, Holtmannspoetter M, Linke R, Schmid-Elsaesser R, Steiger HJ, et al. Perfusion MRI before and after acetazolamide administration for assessment of cerebrovascular reserve capacity in patients with symptomatic internal carotid artery (ICA) occlusion: comparison with 99mTc-ECD SPECT. Neuroradiology 2007;49:317-326 https://doi.org/10.1007/s00234-006-0193-x
  24. Wang R, Yu S, Alger JR, Zuo Z, Chen J, Wang R, et al. Multi-delay arterial spin labeling perfusion MRI in moyamoya disease--comparison with CT perfusion imaging. Eur Radiol 2014;24:1135-1144 https://doi.org/10.1007/s00330-014-3098-9
  25. Konstas AA, Goldmakher GV, Lee TY, Lev MH. Theoretic basis and technical implementations of CT perfusion in acute ischemic stroke, part 1: theoretic basis. AJNR Am J Neuroradiol 2009;30:662-668 https://doi.org/10.3174/ajnr.A1487
  26. Cohen AD, Agarwal M, Jagra AS, Nencka AS, Meier TB, Lebel RM, et al. Longitudinal reproducibility of MR perfusion using 3D pseudocontinuous arterial spin labeling with Hadamard-encoded multiple postlabeling delays. J Magn Reson Imaging 2020;51:1846-1853 https://doi.org/10.1002/jmri.27007
  27. Burt RW, Witt RM, Cikrit DF, Reddy RV. Carotid artery disease: evaluation with acetazolamide-enhanced Tc99m HMPAO SPECT. Radiology 1992;182:461-466 https://doi.org/10.1148/radiology.182.2.1732965
  28. Vagal AS, Leach JL, Fernandez-Ulloa M, Zuccarello M. The acetazolamide challenge: techniques and applications in the evaluation of chronic cerebral ischemia. AJNR Am J Neuroradiol 2009;30:876-884 https://doi.org/10.3174/ajnr.A1538
  29. Kapucu OL, Nobili F, Varrone A, Booij J, Vander Borght T, Nagren K, et al. EANM procedure guideline for brain perfusion SPECT using 99mTc-labelled radiopharmaceuticals, version 2. Eur J Nucl Med Mol Imaging 2009;36:2093-2102 https://doi.org/10.1007/s00259-009-1266-y
  30. Inoue Y, Tanaka Y, Hata H, Hara T. Arterial spin-labeling evaluation of cerebrovascular reactivity to acetazolamide in healthy subjects. AJNR Am J Neuroradiol 2014;35:1111-1116 https://doi.org/10.3174/ajnr.A3815
  31. Barber PA, Demchuk AM, Zhang J, Buchan AM. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group. Alberta Stroke Programme Early CT Score. Lancet 2000;355:1670-1674 https://doi.org/10.1016/S0140-6736(00)02237-6