Comparison of CT angiography collaterals for predicting target perfusion profile and clinical outcome in patients with acute ischemic stroke

  • Shan-shan Lu
  • Xuan Zhang
  • Xiao-quan Xu
  • Yue-zhou Cao
  • Lin bo Zhao
  • Qiang-hui Liu
  • Fei-yun Wu
  • Sheng Liu
  • Hai-bin ShiEmail author



To compare collateral status on single-phase CT angiography (sCTA) and multiphase CT angiography (mCTA) and their ability to predict a target mismatch on CT perfusion (CTP) and clinical outcome in patients with acute ischemic stroke (AIS).


Seventy-three AIS patients with stroke onset between 5 and 15 h or with unclear onset time and occlusions in the M1/M2 segment of the middle cerebral artery and/or intracranial internal carotid artery underwent head non-contrast CT and CTP. Simulated sCTA and mCTA were reconstructed from CTP data and were compared for collaterals assessment. The ability to predict target mismatch on CTP (an ischemic core < 70 ml, a mismatch ratio ≥ 1.8, and an absolute difference ≥ 15 ml) and 90-day modified Rankin Scale (mRS) score of 0–2 was compared between sCTA and mCTA by using receiver operating curve analysis.


sCTA underestimated the collateral status when compared with mCTA (p < 0.01). The ability of mCTA to predict target mismatch (AUC = 0.902, 95% confidence interval [CI] 0.809, 0.959) and clinical outcome (AUC = 0.771; 95% CI, 0.655, 0.864) was better than that of sCTA (p < 0.05 overall). A mCTA collateral score of > 3 best identified the target mismatch (sensitivity, 78.4%; specificity, 90.9%) and predicted 90-day mRS score of 0–2 (sensitivity, 84.8%; specificity, 69.4%).


The collaterals were better estimated by mCTA compared with sCTA. A mCTA collateral score of > 3 optimized the prediction of a target mismatch on CTP and a good clinical outcome in patients with AIS.

Key Points

• Collateral circulation is a key determinant of ischemic core and penumbra. Better collaterals are associated with smaller ischemic core volumes and larger mismatch ratios on CT perfusion.

• The collaterals can be better estimated by multiphase CTA compared with single-phase CTA.

• A collateral score of > 3 on multiphase CTA best identifies patients with target mismatch on CT perfusion and predicts 90-day mRS score of 0–2.


Collateral circulation Perfusion imaging CT angiography Stroke 



Arterial input function


Acute ischemic stroke


Area under the ROC curve


Cerebral blood flow


CT angiography


CT perfusion


Internal carotid artery


Interventional Management of Stroke


Middle cerebral artery (MCA)


Multiphase CT angiography


Non-contrast CT


National Institute of Health Stroke Scale


Randomized controlled trials


Receiver operating characteristic


Single-phase CT angiography


Time to maximum


Venous input function


Volume perfusion CT



We sincerely thank Mrs. Min-lin Zhou from the National Clinical Research Center of Kidney Diseases, Jinling Hospital, for her reviewing of all the statistics. We also thank Dr. Kai Qiu and Dr. Wei Wang for their kind help in collecting the clinical information.


The authors state that this work has not received any funding.

Compliance with ethical standards


The scientific guarantor of this publication is Dr. Hai-bin Shi.

Email address:

Conflict of interest

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.

Statistics and biometry

Mrs. Min-lin Zhou from national clinical research center of kidney diseases, Jinling Hospital, kindly provided statistical advice for this manuscript.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.


• Retrospective

• Case-control study

• Performed at one institution


  1. 1.
    Berkhemer OA, Fransen PS, Beumer D et al (2015) A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med 372:11–20CrossRefGoogle Scholar
  2. 2.
    Campbell BC, Mitchell PJ, Kleinig TJ et al (2015) Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med 372:1009–1018CrossRefGoogle Scholar
  3. 3.
    Goyal M, Demchuk AM, Menon BK et al (2015) Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 372:1019–1030CrossRefGoogle Scholar
  4. 4.
    Jovin TG, Chamorro A, Cobo E et al (2015) Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med 372:2296–2306CrossRefGoogle Scholar
  5. 5.
    Saver JL, Goyal M, Bonafe A et al (2015) Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med 372:2285–2295CrossRefGoogle Scholar
  6. 6.
    Goyal M, Menon BK, Derdeyn CP (2013) Perfusion imaging in acute ischemic stroke: let us improve the science before changing clinical practice. Radiology 266:16–21CrossRefGoogle Scholar
  7. 7.
    Kudo K, Sasaki M, Yamada K et al (2010) Differences in CT perfusion maps generated by different commercial software: quantitative analysis by using identical source data of acute stroke patients. Radiology 254:200–209CrossRefGoogle Scholar
  8. 8.
    Bivard A, Levi C, Spratt N, Parsons M (2013) Perfusion CT in acute stroke: a comprehensive analysis of infarct and penumbra. Radiology 267:543–550CrossRefGoogle Scholar
  9. 9.
    Liebeskind DS (2003) Collateral circulation. Stroke 34:2279–2284CrossRefGoogle Scholar
  10. 10.
    Menon BK, Qazi E, Nambiar V et al (2015) Differential effect of baseline computed tomographic angiography collaterals on clinical outcome in patients enrolled in the Interventional Management of Stroke III trial. Stroke 46:1239–1244CrossRefPubMedCentralGoogle Scholar
  11. 11.
    Berkhemer OA, Jansen IG, Beumer D et al (2016) Collateral status on baseline computed tomographic angiography and intra-arterial treatment effect in patients with proximal anterior circulation stroke. Stroke 47:768–776CrossRefGoogle Scholar
  12. 12.
    Dehkharghani S, Bammer R, Straka M et al (2016) Performance of CT ASPECTS and collateral score in risk stratification: can target perfusion profiles be predicted without perfusion imaging? AJNR Am J Neuroradiol 37:1399–1404CrossRefGoogle Scholar
  13. 13.
    Vagal A, Menon BK, Foster LD et al (2016) Association between CT angiogram collaterals and CT perfusion in the Interventional Management of Stroke III trial. Stroke 47:535–538CrossRefGoogle Scholar
  14. 14.
    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 275:510–520CrossRefGoogle Scholar
  15. 15.
    Frolich AM, Psychogios MN, Klotz E, Schramm R, Knauth M, Schramm P (2012) Angiographic reconstructions from whole-brain perfusion CT for the detection of large vessel occlusion in acute stroke. Stroke 43:97–102CrossRefGoogle Scholar
  16. 16.
    Campbell BC, Christensen S, Levi CR et al (2011) Cerebral blood flow is the optimal CT perfusion parameter for assessing infarct core. Stroke 42:3435–3440CrossRefGoogle Scholar
  17. 17.
    Calamante F, Christensen S, Desmond PM, Ostergaard L, Davis SM, Connelly A (2010) The physiological significance of the time-to-maximum (Tmax) parameter in perfusion MRI. Stroke 41:1169–1174CrossRefGoogle Scholar
  18. 18.
    Olivot JM, Mlynash M, Thijs VN et al (2009) Optimal Tmax threshold for predicting penumbral tissue in acute stroke. Stroke 40:469–475CrossRefGoogle Scholar
  19. 19.
    Albers GW, Marks MP, Kemp S et al (2018) Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med 378:708–718CrossRefGoogle Scholar
  20. 20.
    Saver JL, Jahan R, Levy EI et al (2012) Solitaire flow restoration device versus the merci retriever in patients with acute ischaemic stroke (SWIFT): a randomised, parallel-group, non-inferiority trial. Lancet 380:1241–1249CrossRefGoogle Scholar
  21. 21.
    Boers AM, Jansen IG, Berkhemer OA et al (2017) Collateral status and tissue outcome after intra-arterial therapy for patients with acute ischemic stroke. J Cereb Blood Flow Metab 37:3589–3598CrossRefGoogle Scholar
  22. 22.
    Kim EY, Shin DH, Noh Y, Goh BH, Lee YB (2016) Comparison of imaging selection criteria for intra-arterial thrombectomy in acute ischemic stroke with advanced CT. Eur Radiol 26:2974–2981CrossRefGoogle Scholar
  23. 23.
    Powers WJ, Rabinstein AA, Ackerson T et al (2018) 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 49:e46–e110CrossRefGoogle Scholar
  24. 24.
    Yang CY, Chen YF, Lee CW et al (2008) Multiphase CT angiography versus single-phase CT angiography: comparison of image quality and radiation dose. AJNR Am J Neuroradiol 29:1288–1295CrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  1. 1.Department of RadiologyThe First Affiliated Hospital of Nanjing Medical UniversityNanjingChina
  2. 2.Department of Interventional RadiologyThe First Affiliated Hospital of Nanjing Medical UniversityNanjingChina
  3. 3.Department of EmergencyThe First Affiliated Hospital of Nanjing Medical UniversityNanjingChina

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