DIAGNOSTIC CHALLENGE: IMAGING STRATEGY IN ACUTE ISCHEMIC STROKE
Abstract
Stroke is the third leading cause of death and the most common cause of permanent disability among the world population. Imaging plays a central role in assessing this pathology and various techniques can be used to examine brain and its vessels in acute stroke.
Angio- and perfusion computer tomography (CT) are widely used due to their high availability worldwide. However, MRI diffusion-weighted imaging (DWI) allows earlier and more accurate detection of ischemia. It is used in conjunction with other sequences, especially with susceptibility-weighted imaging (SWI), 3D-time-of-flight MR angiography (MRA), and contrast-enhanced MRA of supra-aortic arteries (CE-MRA), which allows diagnosing occluded arteries or hemorrhage and localizing thrombosis. By means of non-contrast arterial spin labeling (ASL) perfusion, which is of special interest, it is possible to diagnose ischemic penumbra and suggest prognosis in a noninvasive way.
MRI is the most accurate and the most reliable technique for diagnosing ischemic stroke and, in combination with the ASL sequence, for differentiating it from other diseases such as epilepsy and migraine aura. However, CT may be a valuable alternative in case MR is non-available or contraindicated.
References
Alsop D, Detre J, Golay X, Günther M, Hendrikse J, Hernandez-Garcia L, et al. Recommended imple-mentation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM per-fusion study group and the European consortium for ASL in dementia. Magn Reson Med 2015;73:102-16. [CrossRef] [PubMed]
Alves JE, Carneiro Â, Xavier J. Reliability of CT per-fusion in the evaluation of the ischaemic penumbra. Neuroradiol J 2014;27(1):91-5. [CrossRef] [PubMed]
Amukotuwa SA, Yu C, Zaharchuk G. 3D Pseudo-continuous arterial spin labeling in routine clinical practice: A review of clinically significant artifacts. J Magn Reson Imaging 2016;43(1):11-27. [CrossRef] [PubMed]
B Law-ye, B Geerts, D Galanaud, D Dormont, N Pyatigorskaya. Pseudo-asymmetry of cerebral blood flow in arterial spin labeling caused by unilateral fetal-type circle of Willis: Technical limitation or a way to better understanding physiological variations of cere-bral perfusion and improving arterial spin labeling acquisition? J Cereb Blood Flow Metab 2016;36(9): 1641-3. [CrossRef] [PubMed]
Barber PA, Hill MD, Eliasziw M, Demchuk AM, Pexman JH, Hudon ME, et al; ASPECTS Study Group. Imaging of the brain in acute ischaemic stroke: comparison of computed tomography and magnetic resonance dif-fusion-weighted imaging. J Neurol Neurosurg Psychia-try 2005;76(11):1528-33. [CrossRef] [PubMed]
Béjot Y, Bailly H, Durier J, Giroud M. Epidemiology of stroke in Europe and trends for the 21st century. Presse Med 2016;45(12 Pt 2): e391-e398. [CrossRef] [PubMed]
Béjot Y, Daubail B, Jacquin A, Durier J, Osseby GV, Rouaud O, et al. Trends in the incidence of ischaemic stroke in young adults between 1985 and 2011: the Dijon Stroke Registry. J Neurol Neurosurg Psychiatry 2014;85(5):509-13. [CrossRef] [PubMed]
Birenbaum D, Bancroft LW, Felsberg GJ. Imaging in acute stroke. West J Emerg Med 2011;12(1):67-76. [PubMed]
Bivard A, Krishnamurthy V, Stanwell P, Levi C, Spratt NJ, Davis S, et al. Arterial spin labeling versus bolus-tracking perfusion in hyperacute stroke. Stroke 2014; 45(1):127-33. [CrossRef] [PubMed]
Bivard A, Stanwell P, Levi C, Parsons M. Arterial spin labeling identifies tissue salvage and good clinical recovery after acute ischemic stroke. J Neuroimaging 2013;23(3):391-6. [CrossRef] [PubMed]
Chalela JA, Alsop DC, Gonzalez-Atavales JB, Maldjian JA, Kasner SE, Detre JA. Magnetic resonance per-fusion imaging in acute ischemic stroke using con-tinuous arterial spin labeling. Stroke 2000;31(3):680-7. [CrossRef] [PubMed]
Chng SM, Petersen ET, Zimine I, Sitoh YY, Lim CC, Golay X. Territorial arterial spin labeling in the assess-ment of collateral circulation: comparison with digital subtraction angiography. Stroke 2008;39(12):3248-54. [CrossRef] [PubMed]
Copenhaver BR, Shin J, Warach S, Butman JA, Saver JL, Kidwell CS. Gradient echo MRI: implementation of a training tutorial for intracranial hemorrhage diag-nosis. Neurology 2009;72(18):1576-81. [CrossRef] [PubMed]
Corso G, Bottacchi E, Giardini G, De la Pierre F, Meloni T, Pesenti Campagnoni M, et al. Community-based study of stroke incidence in the Valley of Aosta, Italy. CARe-cerebrovascular Aosta Registry: years 2004-2005. Neuroepidemiology 2009;32(3):186-95. [CrossRef] [PubMed]
Danière F, Edjlali-Goujon M, Mellerio C, Turc G, Naggara O, Tselikas L, et al. MR screening of candidates for thrombolysis: How to identify stroke mimics? J Neuroradiol 2014;41(5):283-95. [CrossRef] [PubMed]
Dawson A, Cloud GC, Pereira AC, Moynihan BJ. Stroke mimic diagnoses presenting to a hyperacute stroke unit. Clin Med (Lond) 2016;16(5):423-6. [CrossRef] [PubMed]
de Lucas EM, Sánchez E, Gutiérrez A, Mandly AG, Ruiz E, Flórez AF, et al. CT protocol for acute stroke: tips and tricks for general radiologists. Radiographics 2008;28(6):1673-87. [CrossRef] [PubMed]
Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA. Arterial spin-labeling in routine clinical practice, part 2: hypoperfusion patterns. AJNR Am J Neuroradiol 2008;29(7):1235-41. [CrossRef] [PubMed]
Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA. Arterial spin-labeling in routine clinical practice, part 3: hyperperfusion patterns. AJNR Am J Neuroradiol 2008;29(8):1428-35. [CrossRef] [PubMed]
Eastwood JD, Lev MH, Wintermark M, Fitzek C, Barboriak DP, Delong DM, et al. Correlation of early dynamic CT perfusion imaging with whole-brain MR diffusion and perfusion imaging in acute hemispheric stroke. AJNR Am J Neuroradiol 2003;24(9):1869-75. [PubMed]
Feigin VL, Forouzanfar MH, Krishnamurthi R, Mensah GA, Connor M, Bennett DA, et al; Global Burden of Diseases, Injuries, and Risk Factors Study 2010 (GBD 2010) and the GBD Stroke Experts Group. Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet 2014;383(9913):245-54. [CrossRef] [PubMed]
Ferré JC, Raoult H, Breil S, Carsin-Nicol B, Ronzière T, Gauvrit JY. Supra-aortic arteries: three-dimensional time-resolved k-t BLAST contrast-enhanced MRA using a nondedicated body coil at 3 tesla in acute ischemic stroke. J Magn Reson Imaging 2014; 40(5): 1056-63. [CrossRef] [PubMed]
Golay X, Petersen ET. Arterial spin labeling: benefits and pitfalls of high magnetic field. Neuroimaging Clin N Am. 2006;16(2):259-68, x. [CrossRef] [PubMed]
Goyal M, Menon BK, Derdeyn CP. Perfusion imaging in acute ischemic stroke: let us improve the science before changing clinical practice. Radiology 2013; 266(1):16-21. [CrossRef] [PubMed]
Grade M, Hernandez Tamames JA, Pizzini FB, Achten E, Golay X, Smits M. A neuroradiologist's guide to arterial spin labeling MRI in clinical practice. Neuro-radiology 2015;57(12):1181-1202. [CrossRef] [PubMed]
Grandin CB. Assessment of brain perfusion with MRI: methodology and application to acute stroke. Neuro-radiology 2003;45(11):755-66. [CrossRef] [PubMed]
Hacke W, Donnan G, Fieschi C, Kaste M, von Kummer R, Broderick JP, et al. Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet 2004; 363:768-74. [CrossRef] [PubMed]
Hilmarsson A., Kjartansson O, Olafsson E. Incidence of first stroke: a population study in Iceland. Stroke. 2013;44(6):1714-16. [CrossRef] [PubMed]
Hwang DY, Silva GS, Furie KL, Greer DM. Comparative sensitivity of computed tomography vs. magnetic resonance imaging for detecting acute posterior fossa infarct. J Emerg Med 2012;42(5):559-65. [CrossRef] [PubMed]
Inoue M, Mlynash M, Christensen S, Wheeler HM, Straka M, Tipirneni A, et al; DEFUSE 2 Investigators. Early diffusion-weighted imaging reversal after endovascular reperfusion is typically transient in pa-tients imaged 3 to 6 hours after onset. Stroke 2014; 45(4):1024-8. [CrossRef] [PubMed]
Ishimaru H, Ochi M, Morikawa M, Takahata H, Matsuoka Y, Koshiishi T, et al. Accuracy of pre- and postcontrast 3D time-of-flight MR angiography in patients with acute ischemic stroke: correlation with catheter angiography. AJNR Am J Neuroradiol 2007; 28(5):923-6. [PubMed]
Jia B, Scalzo F, Agbayani E, Woolf GW, Liu L, Miao Z, et al. Multimodal CT techniques for cerebrovascular and hemodynamic evaluation of ischemic stroke: occlusion, collaterals, and perfusion. Expert Rev Neurother 2016;16(5):515-25. [CrossRef] [PubMed]
Kamran S, Bates V, Bakshi R, Wright P, Kinkel W, Miletich R. Significance of hyperintense vessels on FLAIR MRI in acute stroke. Neurology 2000;55(2): 265-9. [CrossRef] [PubMed]
Kloska SP, Nabavi DG, Gaus C, Nam EM, Klotz E, Ringelstein EB, et al. Acute stroke assessment with CT: do we need multimodal evaluation? Radiology 2004;233(1): 79-86. [CrossRef] [PubMed]
Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann PU. Epidemiology of ischemic stroke subtypes according to TOAST criteria: Incidence, recurrence, and long-term survival in is-chemic stroke subtypes: a population-based study. Stroke 2001;32(12):2735-40. [CrossRef] [PubMed]
Lansberg MG, Albers GW, Beaulieu C, Marks MP. Comparison of diffusion-weighted MRI and CT in acute stroke. Neurology 2000;54(8):1557-61. [CrossRef] [PubMed]
Lansberg MG, Lee J, Christensen S, Straka M, De Silva DA, Mlynash M, et al. RAPID automated patient selection for reperfusion therapy: a pooled analysis of the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET) and the Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution (DEFUSE) Study. Stroke 2011;42(6):1608-14. [CrossRef] [PubMed]
Lev MH. Perfusion imaging of acute stroke: its role in current and future clinical practice. Radiology 2013; 266(1):22-7. [CrossRef] [PubMed]
Mair G, Wardlaw JM. Imaging of acute stroke prior to treatment: current practice and evolving techniques. Br J Radiol 2014;87(1040):20140216. [CrossRef] [PubMed]
Majer M, Mejdoubi M, Schertz M, Colombani S, Arrigo A. Raw arterial spin labeling data can help identify arterial occlusion in acute ischemic stroke. Stroke 2015;46(6):e141-144. [CrossRef] [PubMed]
Medin J, Nordlund A, Ekberg K; Swedish Hospital Discharge Register. Increasing stroke incidence in Sweden between 1989 and 2000 among persons aged 30 to 65 years: evidence from the Swedish Hospital Discharge Register. Stroke 2004;35(5):1047-51. [CrossRef] [PubMed]
Meshksar A, Villablanca P.J, Khan R, Carmody R, Coull B, Nael K. Role of EPI-FLAIR in Patients with Acute Stroke: A Comparative Analysis with FLAIR. AJNR Am J Neuroradiol 2014;35(5):878-83. [CrossRef] [PubMed]
Mullins ME, Schaefer PW, Sorensen AG, Halpern EF, Ay H, He J, et al. CT and conventional and diffusion-weighted MR imaging in acute stroke: study in 691 patients at presentation to the emergency depart-ment. Radiology 2002;224(2):353-60. [CrossRef] [PubMed]
Ojaghihaghighi S, Vahdati SS, Mikaeilpour A, Ramouz A. Comparison of neurological clinical manifestation in patients with hemorrhagic and ischemic stroke. World J Emerg Med 2017;8(1):34-8. [CrossRef] [PubMed]
Okorie CK, Ogbole GI, Owolabi MO, Ogun O, Adeyinka A, Ogunniyi A. Role of Diffusion-weighted Imaging in Acute Stroke Management using Low-field Magnetic Resonance Imaging in Resource-limited Settings. West Afr J Radiol 2015;22(2):61-6. [CrossRef] [PubMed]
Olivot JM, Mosimann PJ, Labreuche J, Inoue M, Meseguer E, Desilles JP, et al. Impact of diffusion-weighted imaging lesion volume on the success of endovascular reperfusion therapy. Stroke 2013;44(8): 2205-11. [CrossRef] [PubMed]
Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gyldensted C, Rosen BR. High resolution measure-ment of cerebral blood flow using intravascular tracer bolus passages. Part II: Experimental comparison and preliminary results. Magn Reson Med 1996;36(5): 726-36. [CrossRef] [PubMed]
Roldan-Valadez E, Lopez-Mejia M. Current concepts on magnetic resonance imaging (MRI) perfusion-diffusion assessment in acute ischaemic stroke: a review & an update for the clinicians. Indian J Med Res 2014; 140(6):717-28. [PubMed]
Saini M, Butcher K. Advanced imaging in acute stroke management-Part II: Magnetic resonance imaging. Neurol India 2009;57(5):550-8. [CrossRef] [PubMed]
Sims J, Schwamm LH. The evolving role of acute stroke imaging in intravenous thrombolytic therapy: patient selection and outcomes assessment. Neuro-imaging Clin N A 2005;15(2):421-40, xii. [CrossRef] [PubMed]
Straka M, Albers GW, Bammer R. Real-time diffusion-perfusion mismatch analysis in acute stroke. J Magn Reson Imaging 2010;32(5):1024-37. [CrossRef] [PubMed]
Thomalla G, Rossbach P, Rosenkranz M, Siemonsen S, Krützelmann A, Fiehler J, et al. Negative fluid-atte-nuated inversion recovery imaging identifies acute ischemic stroke at 3 hours or less. Ann Neurol 2009; 65(6):724-32. [CrossRef] [PubMed]
Tong E, Komlosi P, Wintermarkb M. One-stop-shop stroke imaging with functional CT. Eur J Radiol 2015; 84(12):2425-31. [CrossRef] [PubMed]
Verclytte S, Fisch O, Colas L, Vanaerde O, Toledano M, Budzik JF. ASL and susceptibility-weighted imaging contribution to the management of acute ischaemic stroke. Insights Imaging 2017;8(1):91-100. [CrossRef] [PubMed]
Vidorreta M, Balteau E, Wang Z, De Vita E, Pastor MA, Thomas DL, et al. Evaluation of segmented 3D acquisition schemes for whole-brain high-resolution arterial spin labeling at 3 T. NMR Biomed 2014; 27 (11):1387-96. [CrossRef] [PubMed]
Vilela P. Acute stroke differential diagnosis: Stroke mimics. Eur J Radiol 2017;96:133-44. [CrossRef] [PubMed]
Wang DJ, Alger JR, Qiao JX, Hao Q, Hou S, Fiaz R, et al; UCLA Stroke Investigators. The value of arterial spin-labeled perfusion imaging in acute ischemic stroke: comparison with dynamic susceptibility con-trast-enhanced MRI. Stroke 2012;43(4):1018-24. [CrossRef] [PubMed]
Wardlaw JM, Keir SL, Dennis MS. The impact of delays in computed tomography of the brain on the accuracy of diagnosis and subsequent management in patients with minor stroke. J Neurol Neurosurg Psychiatry 2003;74(1):77-81. [CrossRef] [PubMed]
Wardlaw JM, Mielke O. Early signs of brain infarction at CT: observer reliability and outcome after thrombolytic treatment--systematic review. Radiology 2005;235(2):444-53. [CrossRef] [PubMed]
Wintermark M, Albers GW, Alexandrov AV, Alger JR, Bammer R, Baron JC, at al. Acute stroke imaging research roadmap. AJNR Am J Neuroradiol 2008; 29(5):e23-30. [CrossRef] [PubMed]
Wintermark M. Brain perfusion-CT in acute stroke patients. Eur Radiol 2005; 15(suppl 4):D28–D31. [CrossRef] [PubMed]
Wolf RL, Detre JA. Clinical neuroimaging using arterial spin-labeled perfusion magnetic resonance imaging. Neurotherapeutics 2007;4(3):346-59. [CrossRef] [PubMed]
Wright VL, Olan W, Dick B, Yu H, Alberts-Grill N, Latour LL, et al. Assessment of CE-MRA for the rapid detection of supra-aortic vascular disease. Neurology 2005;65(1):27-32. [CrossRef] [PubMed]
Yoo RE, Yun TJ, Rhim JH, Yoon BW, Kang KM, Choi SH, et al. Bright vessel appearance on arterial spin labeling MRI for localizing arterial occlusion in acute ischemic stroke. Stroke 2015;46(2):564-7. [CrossRef] [PubMed]
Zaharchuk G, Bammer R, Straka M, Shankaranarayan A, Alsop DC, Fischbein NJ, et al. Arterial spin-label imaging in patients with normal bolus perfusion-weighted MR imaging findings: pilot identification of the borderzone sign. Radiology 2009;252(3):797-807. [CrossRef] [PubMed]