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Subtracted Dynamic MR Perfusion Source Images (sMRP-SI) provide Collateral Blood Flow Assessment in MCA Occlusions and Predict Tissue Fate

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

Collateral blood flow is accepted as a predictive factor of tissue fate in ischemic stroke. Thus, we aimed to evaluate a new method derived from MR perfusion source images to assess collateral flow in patients with ICA/MCA occlusions.

Methods

A total of 132 patients of the prospective 1000+ study were examined. MR perfusion source images were assessed according to Δimg_n = img_n + 1 − img_n − 1 using the five-grade Higashida collateral flow rating system. Higashida scores were correlated to mismatch (MM) volume, mismatch ratio, day 6 FLAIR lesion volumes and day 90 mRS.

Results

Patients with Higashida scores 3 and 4 had significantly lower admission NIHSS, smaller FLAIR day 6 lesion volumes (p < 0.001) and higher rates of better long-term outcome (mRS 0–2, p = 0.002). There was a linear trend for the association of Higashida grade 1 (p = 0.002) and 2 (p = 0.001) with unfavourable outcome (day 90 mRS 3–6), but no significant association was found for MM volume, MM ratio and day 90 mRS. Inter-rater agreement was 0.58 (95 % CI 0.43–0.73) on day 1, 0.70 (95 % CI 0.58–0.81) on day 2.

Conclusion

sMRP-SI Higashida score offers a non-invasive collateral vessel and tissue perfusion assessment of ischemic tissue. The predictive value of Higashida rating proved superior to MM with regard to day 90 mRS.

Key points

• Assessment of collateral flow using subtracted dynamic MR perfusion source imaging (sMRP-SI).

• sMRP-SI offers additional information about morphological characteristics of ischemic brain tissue.

• sMRP-SI collateral flow assessment proves superior to mismatch volume.

• Better collateral flow was significantly associated with better outcome (day 90 mRS).

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Abbreviations

ASITN/SIR:

American Society of Interventional and Therapeutic Neuroradiology/Society of Radiology collateral flow grading system

DWI:

diffusion weighted imaging

FLAIR:

fluid attenuated inversion recovery

HIR:

hypoperfusion intensity ratio

ICA:

internal carotid artery

iv:

intravenous

MCA:

middle cerebral artery

MM:

mismatch

ml:

millilitre

MRA:

magnetic resonance angiography

mRS:

modified Rankin scale

NIHSS:

National Institutes of Health stroke scale score

PI:

perfusion imaging

s:

seconds

sMRP-SI:

subtracted dynamic MR perfusion source imaging

TIMI:

thrombolysis in myocardial infarction

TR:

repetition time

References

  1. Hacke W, Kaste M, Bluhmki E, Investigators ECASS et al (2008) Thrombolysis with alteplase 3 to 4 · 5 hours after acute ischemic stroke. N Engl J Med 359:1317–1329

    Article  CAS  PubMed  Google Scholar 

  2. Albers GW (2013) Impact of recanalization, reperfusion, and collateral flow on clinical efficacy. Stroke 44:511–512

    Article  Google Scholar 

  3. Wardlaw JM, Murray V, Berge E et al (2012) Recombinant tissue plasminogen activator for acute ischaemic stroke: an updated systematic review and meta-analysis. Lancet 379:2364–2372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lee KY, Latour LL, Luby M, Hsia AW, Merino JG, Warach S (2009) Distal hyperintense vessels on FLAIR: an MRI marker for collateral circulation in acute stroke? Neurology 72:1134–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bang OY, Saver JL, Alger JR, Starkman S, Ovbiagele B, Liebeskind DS et al (2008) Determinants of the distribution and severity of hypoperfusion in patients with ischemic stroke. Neurology 71:1804–1811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Christoforidis GA, Mohammad Y, Kehagias D, Avutu B, Slivka AP (2005) Angiographic assessment of pial collaterals as a prognostic indicator following intra-arterial thrombolysis for acute ischemic stroke. Am J Neuroradiol 26:1789–1797

    PubMed  Google Scholar 

  7. Ciccone A, Valvassori L, Nichelatti M, for the SYNTHESIS Expansion Investigators et al (2013) Endovascular treatment for acute ischemic stroke. N Engl J Med 368:904–913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Campbell BCV, Christensen S, Tress BM, for the EPITHET Investigators et al (2013) Failure of collateral blood flow is associated with infarct growth in ischemic stroke. J Cereb Blood Flow Metab 44:3039–3043

    Google Scholar 

  9. Hotter B, Pittl S, Ebinger M et al (2009) Prospective study on the mismatch concept in acute stroke patients within the first 24 h after symptom onset – 1000Plus study. BMC Neurol. doi:10.1186/1471-2377-9-60

    PubMed  PubMed Central  Google Scholar 

  10. Higashida RT, Furlan AJ (2003) Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke 34:109–137

    Article  Google Scholar 

  11. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  12. Ringelstein EB, Biniek R, Weiller C, Ammeling B, Nolte PN, Thron A (1992) Type and extent of hemispheric brain infarctions and clinical outcome in early and delayed middle cerebral artery recanalization. Neurology 42:289–298

    Article  CAS  PubMed  Google Scholar 

  13. Lee JH, Kim YJ, Choi JW et al (2013) Multimodal CT: favorable outcome factors in acute middle cerebral artery stroke with large artery occlusion. Eur Neurol 69:266–274

    Article  Google Scholar 

  14. Lima FO, Furie KL, Silva GS et al (2010) The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke 41:2316–2322

    Article  PubMed  Google Scholar 

  15. Liebeskind DS, Tomsick TA, Foster LD et al (2014) Collaterals at angiography and outcomes in the Interventional Management of Stroke (IMS) III Trial. Stroke 45:759–764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P, Parsons MW (2009) The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain 132:2231–2238

    Article  PubMed  Google Scholar 

  17. Menon BK, Smith EE, Modi J et al (2011) Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. Am J Neuroradiol 32:1640–1645

    Article  CAS  PubMed  Google Scholar 

  18. Tan IYL, Demchuk AM, Hopyan J et al (2009) CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. Am J Neuroradiol 30:525–531

    Article  CAS  PubMed  Google Scholar 

  19. Beyer SE, von Baumgarten L, Thierfelder KM et al (2014) Predictive value of the velocity of collateral filling in patients with acute ischemic stroke. J Cereb Blood Flow Metab 35:206–212

    Article  PubMed  PubMed Central  Google Scholar 

  20. Smit EJ, Vonken E-J, van Seeters T et al (2013) Timing-invariant imaging of collateral vessels in acute ischemic stroke. Stroke 44:2194–2199

    Article  CAS  PubMed  Google Scholar 

  21. Calleja AI, Cortijo E, García-Bermejo P et al (2013) Collateral circulation on perfusion-computed tomography-source images predicts the response to stroke intravenous thrombolysis. Euro J Neurol 20:795–802

    Article  CAS  Google Scholar 

  22. Menon BK, d’Esterre CD, Qazi EM et al (2015) Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology 275:510–520

    Article  PubMed  Google Scholar 

  23. Kim SJ, Son JP, Ryoo S et al (2014) Approach to collateral flow imaging in ischemic stroke. Ann Neurol 76:356–369

    Article  PubMed  Google Scholar 

  24. Berkhemer OA, Beumer FD, van den Berg LA, for the MR CLEAN investigators et al (2015) A randomized trail of intraarterial treatment for acute ischemic stroke. N Engl J Med 372:11–20

    Article  PubMed  Google Scholar 

  25. Goyal M, Demchuk AM, Menon BK, for the ESCAPE Trial Investigators et al (2015) Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 12:1019–1030

    Article  Google Scholar 

  26. Menon BK, Almekhlafi MA, Pereira VM et al; STAR Study Investigators (2014) Optimal workflow and process-based performance measures for endovascular therapy in acute ischemic stroke: analysis of the Solitaire FR thrombectomy for acute revasculatization study. Stroke 45:2024–2029

    Article  Google Scholar 

  27. Khatri P, Yeatts SD, Mazighi M, Trialists IMSIII et al (2014) Time to angiographic reperfusion and clinical outcome after acute ischaemic stroke: an analysis of data from the Interventional Management of Stroke (IMS III) phase 3 trial. Lancet Neurol 13:567–574

    Article  PubMed  PubMed Central  Google Scholar 

  28. Campbell BCV, Mitchell PJ, Kleinig TJ, for the EXTEND-IA Investigators et al (2015) Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med 372:1009–1018

    Article  CAS  PubMed  Google Scholar 

  29. Bang OY, Saver JL, Buck BH et al [on behalf of the UCLA Collateral Investigators] (2009) Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry 79:625–629

    Google Scholar 

  30. Bang OY, Saver JL, Kim SJ et al (2011) Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke 42:693–699

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Anna Kufner for critical language revision of the manuscript. The scientific guarantor of this publication is PD Dr. Jochen Fiebach. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. Jochen B. Fiebach reports receiving consulting, lecture and advisory board fees from BMS, Siemens, Perceptive, Synarc, BioImaging Technologies, Novartis, Wyeth, Pfizer, Boehringer Ingelheim, Lundbeck and Sygnis

This study received funding from the Federal Ministry of Education and Research via the grant Center for Stroke Research Berlin (01EO0801 and 01EO01301). Dr. Ulrike Grittner kindly provided statistical advice for this manuscript. Institutional review board approval was obtained (EA4/026/08). Written informed consent was obtained from all subjects (patients) in this study. Some study subjects or cohorts have been previously presented at the International Stroke Conference, San Diego, 2014 as an oral presentation. Methodology: prospective, retrospective, observational, performed at one institution.

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Authors and Affiliations

  1. Academic Neuroradiology, Center for Stroke Research (CSB), Charité-Universitätsmedizin, Campus Benjamin Franklin, Hindenburgdamm 30, 12200, Berlin, Germany

    Kersten Villringer, Rafael Serrano-Sandoval, Ivana Galinovic, Ann-Christin Ostwaldt, Peter Brunecker & Jochen B. Fiebach

  2. Center for Stroke Research, Charité, Universitätsmedizin Berlin, Berlin, Germany

    Ulrike Grittner & Alice Schneider

  3. Department of Neurology and Center for Stroke Research, Charité, Berlin, Germany

    Andrea Rocco

  4. Department for Biostatistics and Clinical Epidemiology, Charité, Berlin, Germany

    Ulrike Grittner

Authors
  1. Kersten Villringer
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  2. Rafael Serrano-Sandoval
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  9. Jochen B. Fiebach
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Correspondence to Kersten Villringer.

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Villringer, K., Serrano-Sandoval, R., Grittner, U. et al. Subtracted Dynamic MR Perfusion Source Images (sMRP-SI) provide Collateral Blood Flow Assessment in MCA Occlusions and Predict Tissue Fate. Eur Radiol 26, 1396–1403 (2016). https://doi.org/10.1007/s00330-015-3927-5

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  • DOI: https://doi.org/10.1007/s00330-015-3927-5

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