Journal List > J Korean Soc Radiol > v.80(6) > 1138850

Cho, Jung, Suh, Kim, Woo, Oh, Kim, and Lee: Neuroimaging in Acute Recent Advances Ischemic Stroke: Role and


Neuroimaging plays a key role in assessing the detection of acute hemorrhage, diagnosis of infarct core, detection of steno-occlusive arteries, mismatch between infarct core and penumbra, and collateral circulation in patients with acute cerebral ischemic stroke. The recent announcement of randomized clinical trials that demonstrated the usefulness of intra-arterial mechanical thrombectomy and the guidelines of 2018 Guidelines for the Early Management of Patients with Acute Ischemic Stroke from American Heart Association/American Stroke Association led to a larger role of neuroimaging and required new neuroimaging strategy for acute cerebral ischemic stroke. In this review, we summarize the recommendation on neuroimaging from the 2018 Guidelines, and review pros and cons between CT and MR and fast scanned stroke MR. Based on the new guidelines and recent research, we discuss the appropriate neuroimaging strategy for acute cerebral ischemic stroke patients.


1. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke.N Engl J Med. 1995; 333:1581–1587.
2. Rha JH, Saver JL. The impact of recanalization on ischemic stroke outcome: a metaanalysis.Stroke. 2007; 38:967–973.
3. Broderick JP, Palesch YY, Demchuk AM, Yeatts SD, Khatri P, Hill MD, et al. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke.N Engl J Med. 2013; 368:893–903.
4. Ciccone A, Valvassori L, Nichelatti M, Sgoifo A, Ponzio M, Sterzi R, et al. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013; 368:904–913.
5. Kidwell CS, Jahan R, Gornbein J, Alger JR, Nenov V, Ajani Z, et al. A trial of imaging selection and endovascular treatment for ischemic stroke. N Engl J Med. 2013; 368:914–923.
6. Khatri P, Hacke W, Fiehler J, Saver JL, Diener HC, Bendszus M, et al. State of acute endovascular therapy: report from the 12th thrombolysis, thrombectomy, and acute stroke therapy conference.Stroke. 2015; 46.
7. Berkhemer OA, Fransen PS, Beumer D, Van den Berg LA, Lingsma HF, Yoo AJ, et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med. 2015; 372:11–20.
8. Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection.N Engl J Med. 2015; 372:1009–1018.
9. Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke.N Engl J Med. 2015; 372:1019–1030.
10. Jovin TG, Chamorro A, Cobo E, De Miquel MA, Molina CA, Rovira A, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med. 2015; 372:2296–2306.
11. Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM, et al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke.N Engl J Med. 2015; 372:2285–2295.
12. Nogueira RG, Jadhav AP, Haussen DC, Bonafe A, Budzik RF, Bhuva P, et al. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct.N Engl J Med. 2018; 378:11–21.
13. Albers GW, Marks MP, Kemp S, Christensen S, Tsai JP, Ortega-Gutierrez S, et al. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018; 378:708–718.
14. Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, et al. 2018 guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018; 49:e46–e110.
15. Bracard S, Ducrocq X, Mas JL, Soudant M, Oppenheim C, Moulin T, et al. Mechanical thrombectomy after intravenous alteplase versus alteplase alone after stroke (THRACE): a randomised controlled trial.Lancet Neurol. 2016; 15:1138–1147.
16. Wardlaw JM, Seymour J, Cairns J, Keir S, Lewis S, Sandercock P. Immediate computed tomography scanning of acute stroke is cost-effective and improves quality of life. Stroke. 2004; 35:2477–2483.
17. Truwit CL, Barkovich AJ, Gean-Marton A, Hibri N, Norman D. Loss of the insular ribbon: another early CT sign of acute middle cerebral artery infarction.Radiology. 1990; 176:801–806.
18. Marks MP, Holmgren EB, Fox AJ, Patel S, Von Kummer R, Froehlich J. Evaluation of early computed tomographic findings in acute ischemic stroke. Stroke. 1999; 30:389–392.
19. 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.
20. Gupta AC, Schaefer PW, Chaudhry ZA, Leslie-Mazwi TM, Chandra RV, González RG, et al. Interobserver reliability of baseline noncontrast CT Alberta Stroke Program Early CT Score for intraarterial stroke treatment.
21. Bal S, Bhatia R, Menon BK, Shobha N, Puetz V, Dzialowski I, et al. Time dependence of reliability of noncontrast computed tomography in comparison to computed tomography angiography source image in acute ischemic stroke.Int J Stroke. 2015; 10:55–60.
22. Menon BK, Goyal M. Imaging paradigms in acute ischemic stroke: a pragmatic evidencebased approach. Radiology. 2015; 277:7–12.
23. Menon BK, Demchuk AM. Computed tomography angiography in the assessment of patients with stroke/TIA.Neurohospitalist. 2011; 1:187–199.
24. Menon BK, Campbell BC, Levi C, Goyal M. Role of imaging in current acute ischemic stroke workflow for en-dovascular therapy.Stroke. 2015; 46:1453–1461.
25. Nambiar V, Sohn SI, Almekhlafi MA, Chang HW, Mishra S, Qazi E, et al. CTA collateral status and response to.
26. Menon BK, D'Esterre CD, Qazi EM, Almekhlafi M, Hahn L, Demchuk AM, et al. Multiphase CT angiography: a.
27. Liebeskind DS. Collateral circulation.Stroke. 2003; 34:2279–2284.
28. Cianfoni A, Colosimo C, Basile M, Wintermark M, Bonomo L. Brain perfusion CT: principles, technique and clinical applications. Radiol Med. 2007; 112:1225–1243.
29. Hunter GJ, Silvennoinen HM, Hamberg LM, Koroshetz WJ, Buonanno FS, Schwamm LH, et al. Whole-brain CT perfusion measurement of perfused cerebral blood volume in acute ischemic stroke: probability curve for regional infarction.Radiology. 2003; 227:725–730.
30. Menon BK, O'Brien B, Bivard A, Spratt NJ, Demchuk AM, Miteff F, et al. Assessment of leptomeningeal collat-erals using dynamic CT angiography in patients with acute ischemic stroke.J Cereb Blood Flow Metab. 2013; 33:365–371.
31. Goyal M, Menon BK, Derdeyn CP. Perfusion imaging in acute ischemic stroke: let us improve the science before changing clinical practice. Radiology. 2013; 266:1621.
32. Köhrmann M, Schellinger PD. Acute stroke triage to intravenous thrombolysis and other therapies with advanced CT or MR imaging: pro MR imaging.Radiology. 2009; 251:627–633.
33. Vilela P, Rowley HA. Brain ischemia: CT and MRI techniques in acute ischemic stroke.Eur J Radiol. 2017; 96.
34. Thomalla G, Cheng B, Ebinger M, Hao Q, Tourdias T, Wu O, et al. DWI-FLAIR mismatch for the identification of patients with acute ischaemic stroke within 4·5 h of symptom onset (PRE-FLAIR): a multicentre observational study.Lancet Neurol. 2011; 10:978–986.
35. Kinoshita T, Ogawa T, Kado H, Sasaki N, Okudera T. CT angiography in the evaluation of intracranial occlusive disease with collateral circulation: comparison with MR angiography.Clin Imaging. 2005; 29:303–306.
36. Wintermark M, Maeder P, Thiran JP, Schnyder P, Meuli R. Quantitative assessment of regional cerebral blood flows by perfusion CT studies at low injection rates: a critical review of the underlying theoretical models.Eur Radiol. 2001; 11:1220–1230.
37. Wintermark M, Rowley HA, Lev MH. Acute stroke triage to intravenous thrombolysis and other therapies with advanced CT or MR imaging: pro CT.Radiology. 2009; 251:619–626.
38. Rudkin S, Cerejo R, Tayal A, Goldberg MF. Imaging of acute ischemic stroke. Emerg Radiol. 2018; 25:659–672.
39. Muir KW, Buchan A, Von Kummer R, Rother J, Baron JC. Imaging of acute stroke.Lancet Neurol. 2006; 5:755–768.
40. Rai AT, Seldon AE, Boo S, Link PS, Domico JR, Tarabishy AR, et al. A population-based incidence of acute large vessel occlusions and thrombectomy eligible patients indicates significant potential for growth of en-dovascular stroke therapy in the USA.J Neuro/iinterv Surg. 2017; 9:722–726.
41. Lee JH, Han SJ, Yun YH, Choi HC, Jung S, Cho SJ, et al. Posterior circulation ischemic stroke in Korean population. Eur J Neurol. 2006; 13:742–748.
42. Kim JT, Park MS, Choi KH, Kim BJ, Han MK, Park TH, et al. Clinical outcomes of posterior versus anterior circulation infarction with low National Institutes of Health Stroke Scale Scores.Stroke. 2017; 48:55–62.
43. Pallesen LP, Lambrou D, Eskandari A, Barlinn J, Barlinn K, Reichmann H, et al. Perfusion computed tomography in posterior circulation stroke: predictors and prognostic implications of focal hypoperfusion.Eur J Neurol. 2018; 25:725–731.
44. 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; 28:1673–1687.
45. Van der Hoeven EJ, Dankbaar JW, Algra A, Vos JA, Niesten JM, Van Seeters T, et al. Additional diagnostic value of computed tomography perfusion for detection of acute ischemic stroke in the posterior circulation. .Stroke.
46. Bash S, Villablanca JP, Jahan R, Duckwiler G, Tillis M, Kidwell C, et al. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography, MR angiography, and digital subtraction angiography.AJNR Am J Neuroradiol. 2005; 26:1012–1021.
47. Campbell BC, Christensen S, Levi CR, Desmond PM, Donnan GA, Davis SM, et al. Comparison of computed tomography perfusion and magnetic resonance imaging perfusion-diffusion mismatch in ischemic stroke.
48. Wisco D, Uchino K, Saqqur M, Gebel JM, Aoki J, Alam S, et al. Addition of hyperacute MRI AIDS in patient selection, decreasing the use of endovascular stroke therapy. Stroke. 2014; 45:467–472.
49. Jauch EC, Saver JL, Adams HP Jr, Bruno A, Connors JJ, Demaerschalk BM, et al. Guidelines for the early man-agement of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013; 44:870–947.
50. Sauser K, Burke JF, Levine DA, Scott PA, Meurer WJ. Time to brain imaging in acute stroke is improving: secondary analysis of the INSTINCT trial. Stroke. 2014; 45:287–289.
51. Sauser K, Levine DA, Nickles AV, Reeves MJ. Hospital variation in thrombolysis times among patients with acute ischemic stroke: the contributions of door-to-imaging time and imaging-to-needle time.JAMA Neurol. 2014; 71:1155–1161.
52. Wang H, Thevathasan A, Dowling R, Bush S, Mitchell P, Yan B. Streamlining workflow for endovascular mechanical thrombectomy: lessons learned from a comprehensive stroke center. J Stroke Cerebrovasc Dis. 2017; 26:1655–1662.
53. Zaidi SF, Shawver J, Espinosa Morales A, Salahuddin H, Tietjen G, Lindstrom D, et al. Stroke care: initial data.
54. Shah S, Luby M, Poole K, Morella T, Keller E, Benson RT, et al. Screening with MRI for accurate and rapid stroke.
55. Li B, Li H, Dong L, Huang G. Fast carotid artery MR angiography with compressed sensing based three-dimensional time-of-flight sequence.Magn Reson Imaging. 2017; 43:129–135.
56. Wu EL, Kuo LW, Wu FH, Hsu CF, Hsieh CW, Chen JH, et al. Ultra-fast brain MR imaging using simultaneous multislice acquisition (SMA) technique. Conf Proc IEEE Eng Med Biol Soc. 2007; 2007:2618–2621.
57. Baek HJ. Two-minute MR ultra-fast neuro protocol. Available at. Published 2017. Accessed Jun 30,. 2018.
58. Nael K, Khan R, Choudhary G, Meshksar A, Villablanca P, Tay J, et al. Six-minute magnetic resonance imaging protocol for evaluation of acute ischemic stroke: pushing the boundaries.Stroke. 2014; 45:1985–1991.

Fig. 1.
Acute ischemic hyperintensity on fast and conventional FLAIR. Acute ischemic hyperintensity (left column, arrows) in a diffusion-restricted area is well demonstrated in both conventional FLAIR (middle column, scan time: 128 s) and fast FLAIR [right column: (EPI-FLAIR, top, scan time: 45 s), (ETL-FLAIR, middle row, scan time: 74 s), and (TR-FLAIR, bottom, scan time: 79 s)]. DWI = diffusion-weighted imaging, EPI = echo planar imaging, ETL = echo train length, FLAIR = fluid-attenuated inversion recovery imaging, TR = repetition time
Fig. 2.
Fast and conventional GRE. A microbleed in the right thalmus (arrows) is well-demonstrated on both conventional GRE (right, scan time: 141 s) and fast GRE [EPI-GRE (middle, scan time: 29 s) and parallel-GRE (left, scan time: 54 s)]. EPI = echo planar imaging, GRE = Gradient echo
Fig. 3.
Fast CE-MRA and TOF-MRA. Both TOF-MRA (left, scan time: 274 s) and fast CE-MRA (right, scan time: 39 s) demonstrate an occlusion in the right middle cerebral artery (arrows). CE = contrast-enhanced, MRA = magnetic resonance angiography, TOF = time-of-flight
Table 1.
AHA/ASA 2018 Recommendation of Imaging Protocols
뇌 영상 가이드라인 권고 수준 COR 근거 수준 LOE 개정 상태
1. 허혈성 뇌 경색이 의심돼 내원한 모든 환자는 도착과 동시에 뇌 영상 검사를 시행해야 한다. 대부분의 경우, I B-NR†† 2013권고안으로
비 조영 증강 CT (noncontrast CT) 가 초기 치료 결정에 필요한 정보를 제공할 것이다.     부터 개정됨
2. 정맥 내 혈전 용해술(IV alteplase) 또는 동맥 내 재개통술(mechanical thrombectomy)의 대상이 될 수 있는 환자의 적어도 50%가 응급실 내원 후 20분 안에 뇌 영상 검사를 할 수 있도록 시스템을 갖추어야 한다. I B-NR†† 새 권고 사항
3. 정맥 내 혈전 용해술(IV alteplase)의 치료반응에 영향을 줄 수 있는 급성 CT 저음영(acute CT hypoattenuation)의 정도와 크기에 대한 특정한 역치값에 대한 증거는 여전히 불충분하다. 따라서 급성초기 허혈성 저음영을 제외하면 정맥 내 혈전 용해술 치료 대상인 환자에 대해서 급성 초기 허혈성 저음영초기 허혈성 저음영을 제외하면 정맥 내 혈전 용해술 치료 대상인 환자에 대해서 급성 초기 허혈성 저음영 (CT hypoattenuation or early ischemic change)의 정도와 크기를 치료를 유보하는 기준으로 삼아서는 안된다. III: No Benefit§ B-R∗∗ 2015 권고안으로 부터 개정됨
4. CT 동맥 고음영 소견(CT hyperdense MCA sign)을 제외하면 치료 대상인 환자에 대해서 CT 동맥 고음영소견을 정맥 내 혈전 용해술(IV alteplase) 치료를 유보하는 기준으로 삼아서는 안된다. III: No Benefit§ B-R∗∗ 새 권고 사항
5. 정맥 내 혈전 용해술(IV alteplase) 치료 전에 뇌 미세출혈(cerebral microbleeds)을 배제하려는 목적으로 시행하는 정례적인 MR (routine MR)은 권고되지 않는다. III: No Benefit§ B-NR†† 새 권고 사항
6. 증상발생시점이 불명확하거나 기상 시 발견된 뇌졸중(awoke with stroke) 환자에서 정맥 내 혈전 용해술 (IV alteplase) 치료 결정을 위해 뇌영상의 기준(imaging criteria)을 적용하는 것은 임상시험외에는 III: No Benefit§ B-NR†† 2015 권고안과차이 없음.
7. 관류 영상을 포함한 다중기법의 CT, MR (multimodal CT and MR) 검사로 인해 정맥 내 혈전 용해술(IV alteplase) 치료가 지연되어서는 안된다. III: Harm B-NR†† 새 권고 사항
8. 동맥 내 재개통술 적응증에 해당하는 환자들에게 초기 영상학적 검사 중 비 침습적 혈관 조영술(CTA 및MRA)이 권장되지만, 정맥 내 혈전 용해술(IV alteplase) 치료를 지연시켜서는 안된다. 전문적인 의료 그룹(professional medical societies)의 가이드라인을 따라 정맥 내 혈전 용해술(IV alteplase) 치료 대상이되는 환자들에서 초기 영상학적 검사 중에 비 침습적 혈관 조영술이 시행되지 않았다면 그 검사 전에정맥 내 혈전 용해술(IV alteplase) 치료를 먼저 시행하는 것이 권고된다. 그리고 비 침습적 혈관 조영술은가능한 빨리 시행해야 한다. I A 2015 권고안으로 부터 명료한부터 명료한 표현으로 수정됨
9. 동맥 내 재개통술 대상인 환자에서 큰 뇌 혈관 폐색 (large vessel occlusion)이 의심된다면 혈중 크레아티닌 검사를 하지 않았을 경우라도 이전에 신장 기능 장애의 기왕력이 없다면 CT 혈관 조영술을 시행하는 것이 합리적이다. IIa B-NR†† 새 권고 사항
10. 동맥 내 재개통술의 잠재적 후보 환자들에서 뇌 혈관뿐 아니라 두개 외경동맥(extracranial carotid artery) 과 척추동맥에 대한 영상 검사는 치료 환자 선별과 계획에 유용한 정보를 줄 수 있으므로 합리적이다. IIa C-EO§§ 새 권고 사항
11. CT 그리고 CTA, 또는 MR 그리고 MRA 검사 외 관류영상과 같은 추가적인 영상은 6시간 이내 환자에서는 동맥 내 재개통술 대상자 선정을 위한 검사로 권고되지 않는다. III: No Benefit§ B-R∗∗ 새 권고 사항
12. 증상 발생 추정 시점부터 6시간부터 24시간 사이의 환자가 전방 순환의 큰 뇌혈관 폐색이 확인되었다면동맥 내 재개통술 대상자 선정을 위해 관류 CT, 확산 강조 MR, 혹은 관류 MR 검사를 추천한다. 하지만동맥 내 재개통술을 위한 환자 선정은 DAWN과 DEFUSE-3 임상 시험에서 동맥 내 재개통술이 이득을보였던 뇌 영상을 포함한 기준 범위 내에서 엄격히 적용돼야 한다. I A 새 권고 사항
13. 동맥 내 재개통술의 대상자 선정을 위해 측부 순환 상태를 임상적 결정에 포함시키는 것은 합리적일 수 있다. IIb C-LD‡‡ 2015 권고안으로 부터 개정됨

Adapted from Power et al. Stroke 2018;49:e46-e110 (14). Only Korean translated table is permitted from the American Heart Association.

Class I (strong recommendation), Benefit >>> Risk.

Class IIa (moderate recommendation), Benefit >> Risk.

Class IIb (weak recommendation), Benefit ≥ Risk.

§ Class III: no Benefit (moderate recommendation), Benefit = Risk,

Class III: harm (moderate recommendation), Benefit = Risk.

Level A, high quality evidence.

∗∗ Level B-R, moderated quality evidence, randomized.

†† Level B-NR, moderated quality evidence, nonrandomized.

‡‡ Level C-LD, limited data.

§§ Level C-EO, consensus of expert opinion based on clinical experience. AHA/ASA = American Heart Association/American Stroke Association, COR = class of recommendation, CTA = CT angiography, CTP = CT perfu sion, DW = diffusion-weighted, EVT = endovascular treatment, LOE = level of evidence, MCA = middle cranial artery, MRP = MRI perfusion

Table 2.
Comparison between CT and MRI in Acute Ischemic Stroke
Accessibility High Low
Examination time Short Relatively long
Information (amount and characters) Limited, sensitive to hemorrhage and calcification Various
Radiation exposure High No
Usage of contrast agent Essential in angiography in angiography Possible without contrast agent
Standardization of examination Easy Complex
Dependency by the technician Low High
Sensitivity on early detection of hemorrhage Within 24 hours: 57–71% Within 6 hours: 95–100%
Sensitivity on early detection of hemorrhage Inter-reader agreement about infarct core Within 24 hours: 57–71% Low Within 6 hours: 95–100% High
Sensitivity on diagnosis of lesions of posterior circulation Low High
Sensitivity on localization of involved vessel Low High
Interfering factors for image interpretation False-positive high attenuated lesion, artifact (movement, beam hardening, etc) Artifact (movement, metal, etc), clastrophobia
Relative advantages of angiography Less movement artifact, less blood flow dependency, high sensitivity than MRI Less artifact for aortic arch or extracranial vessel than CT
Table 3.
Examples of Scan Parameters for 1.5 Tesla Fast MR
Conventional EPI ETL TR Conventional EPI Parallel Conventional CE-MRA Fast CE-MRA
TR/TE 9000/109 9000/101 9000/102 5560/109 690/16 2260/48 765/26 3.67/1.31 3.37/1.2
Inversion time 2500 2000 2500 1930          
Flip angle 150 90 150 150 15 90 20 30 25
Matrix 256 × 218 128 × 128 192 × 192 256 ×256 256 × 205 192 × 192 192 × 163 320 × 320 448 × 367
Field of view 210 × 184 230 × 230 210 × 184 210 ×184 210 × 210 230 × 230 220 × 220 320 × 240 340 × 276
Field of view Slice thickness (mm) 210 × 184 5 230 × 230 5 210 × 184 5 210 ×184 5 210 × 210 5 230 × 230 5 220 × 220 5 320 × 240 0.5 340 × 276 0.8
ETL 21 128 (EPI) 32 21   192 (EPI)      
GRAPPA 2 2 2 2   2 3 2 3
NAV 1 2 1 1 1 10 1 1 1
Scan time (second) 128 45 74 79 141 29 54 74 39

Scan time (second) 128 45 74 79 141 29 54 74 39 CE-MRA = contrast-enhanced MR angiography, EPI = echo planar imaging, ETL = echo train length, FLAIR = fluid attenuated inversion recovery, GRAPPA = generalized autocalibrating partial parallel acquisition, GRE = Gradient echo, NAV = number of signal averaging, TE = echo time, TR = repetition time

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