Skip to main content

Advertisement

Log in

Value of thrombus imaging in predicting the outcomes of patients with large-vessel occlusive strokes after endovascular therapy

  • Review Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

Acute ischemic stroke leads to serious long-term disability and high mortality, especially in patients with large-vessel occlusive strokes. Nowadays, endovascular therapy is considered as an alternative treatment for these patients. Several studies have used thrombus characteristics based on non-contrast computed tomography (NCCT) and computed tomography angiography (CTA) to predict prognosis in ischemic stroke. We conducted a systematic review to identify potential imaging predictive factors for successful recanalization and improved clinical outcome after endovascular therapy in patients with large-vessel occlusion (LVO) in anterior arterial circulation.

Methods

The PubMed databases were searched for related studies reported between September 18, 2009, and September 18, 2019.

Results

We selected 11 studies on revascularization and 12 studies on clinical outcome. Patients with thrombus of higher Hounsfield unit (HU), shorter length, higher clot burden score, and increased thrombus permeability may achieve higher recanalization and improved clinical outcome, but the matter is still under debate.

Conclusion

Imaging of thrombus can be used as an aseessment tool to predict the outcomes and it needs further studies in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Smith WS, Lev MH, English JD, Camargo EC, Chou M, Johnston SC, Gonzalez G, Schaefer PW, Dillon WP, Koroshetz WJ, Furie KL (2009) Significance of large vessel intracranial occlusion causing acute ischemic stroke and TIA. Stroke 40(12):3834–3840

    Article  PubMed  PubMed Central  Google Scholar 

  2. Zangerle A et al (2007) Recanalization after thrombolysis in stroke patients: predictors and prognostic implications. Neurology 68(1):39–44

    Article  CAS  PubMed  Google Scholar 

  3. Rha JH, Saver JL (2007) The impact of recanalization on ischemic stroke outcome: a meta-analysis. Stroke 38(3):967–973

    Article  PubMed  Google Scholar 

  4. National Institute of Neurological, D. and P.A.S.S.G. Stroke rt (1995) Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 333(24):1581–1587

    Article  Google Scholar 

  5. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, von Kummer R, Wahlgren N, Toni D, ECASS Investigators (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 359(13):1317–1329

    Article  CAS  PubMed  Google Scholar 

  6. Berkhemer OA, Fransen PS, Beumer D, van den Berg L, Lingsma HF, Yoo AJ, Schonewille WJ, Vos JA, Nederkoorn PJ, Wermer MJ, van Walderveen M, Staals J, Hofmeijer J, van Oostayen J, Lycklama à Nijeholt GJ, Boiten J, Brouwer PA, Emmer BJ, de Bruijn SF, van Dijk L, Kappelle LJ, Lo RH, van Dijk E, de Vries J, de Kort PL, van Rooij W, van den Berg J, van Hasselt B, Aerden LA, Dallinga RJ, Visser MC, Bot JC, Vroomen PC, Eshghi O, Schreuder TH, Heijboer RJ, Keizer K, Tielbeek AV, den Hertog H, Gerrits DG, van den Berg-Vos R, Karas GB, Steyerberg EW, Flach HZ, Marquering HA, Sprengers ME, Jenniskens SF, Beenen LF, van den Berg R, Koudstaal PJ, van Zwam W, Roos YB, van der Lugt A, van Oostenbrugge R, Majoie CB, Dippel DW, MR CLEAN Investigators (2015) A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med 372(1):11–20

    Article  CAS  PubMed  Google Scholar 

  7. Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, Yan B, Dowling RJ, Parsons MW, Oxley TJ, Wu TY, Brooks M, Simpson MA, Miteff F, Levi CR, Krause M, Harrington TJ, Faulder KC, Steinfort BS, Priglinger M, Ang T, Scroop R, Barber PA, McGuinness B, Wijeratne T, Phan TG, Chong W, Chandra RV, Bladin CF, Badve M, Rice H, de Villiers L, Ma H, Desmond PM, Donnan GA, Davis SM, EXTEND-IA Investigators (2015) Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med 372(11):1009–1018

    Article  CAS  PubMed  Google Scholar 

  8. Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, Roy D, Jovin TG, Willinsky RA, Sapkota BL, Dowlatshahi D, Frei DF, Kamal NR, Montanera WJ, Poppe AY, Ryckborst KJ, Silver FL, Shuaib A, Tampieri D, Williams D, Bang OY, Baxter BW, Burns PA, Choe H, Heo JH, Holmstedt CA, Jankowitz B, Kelly M, Linares G, Mandzia JL, Shankar J, Sohn SI, Swartz RH, Barber PA, Coutts SB, Smith EE, Morrish WF, Weill A, Subramaniam S, Mitha AP, Wong JH, Lowerison MW, Sajobi TT, Hill MD, ESCAPE Trial Investigators (2015) Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 372(11):1019–1030

    Article  CAS  PubMed  Google Scholar 

  9. Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM, Albers GW, Cognard C, Cohen DJ, Hacke W, Jansen O, Jovin TG, Mattle HP, Nogueira RG, Siddiqui AH, Yavagal DR, Baxter BW, Devlin TG, Lopes DK, Reddy VK, du Mesnil de Rochemont R, Singer OC, Jahan R, SWIFT PRIME Investigators (2015) Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med 372(24):2285–2295

    Article  CAS  PubMed  Google Scholar 

  10. Flacke S, Urbach H, Keller E, Träber F, Hartmann A, Textor J, Gieseke J, Block W, Folkers PJ, Schild HH (2000) Middle cerebral artery (MCA) susceptibility sign at susceptibility-based perfusion MR imaging: clinical importance and comparison with hyperdense MCA sign at CT. Radiology 215(2):476–482

    Article  CAS  PubMed  Google Scholar 

  11. Lam WW et al (2003) Hyperintense middle cerebral artery sign using MRI. Clin Radiol 58(7):542–544

    Article  CAS  PubMed  Google Scholar 

  12. Naggara O, Raymond J, Domingo Ayllon M, al-Shareef F, Touzé E, Chenoufi M, Gerber S, Mellerio C, Zuber M, Meder JF, Mas JL, Oppenheim C (2013) T2* “susceptibility vessel sign” demonstrates clot location and length in acute ischemic stroke. PLoS One 8(10):e76727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Brinjikji W et al (2017) Correlation of imaging and histopathology of thrombi in acute ischemic stroke with etiology and outcome: a systematic review. J Neurointerv Surg 9(6):529–534

    Article  PubMed  Google Scholar 

  14. Kirchhof K, Welzel T, Mecke C, Zoubaa S, Sartor K (2003) Differentiation of white, mixed, and red thrombi: value of CT in estimation of the prognosis of thrombolysis phantom study. Radiology 228(1):126–130

    Article  PubMed  Google Scholar 

  15. Puetz V et al (2008) Intracranial thrombus extent predicts clinical outcome, final infarct size and hemorrhagic transformation in ischemic stroke: the clot burden score. Int J Stroke 3(4):230–236

    Article  PubMed  Google Scholar 

  16. Riedel CH, Jensen U, Rohr A, Tietke M, Alfke K, Ulmer S, Jansen O (2010) Assessment of thrombus in acute middle cerebral artery occlusion using thin-slice nonenhanced computed tomography reconstructions. Stroke 41(8):1659–1664

    Article  PubMed  Google Scholar 

  17. Riedel CH, Zoubie J, Ulmer S, Gierthmuehlen J, Jansen O (2012) Thin-slice reconstructions of nonenhanced CT images allow for detection of thrombus in acute stroke. Stroke 43(9):2319–2323

    Article  PubMed  Google Scholar 

  18. Kim EY, Lee SK, Kim DJ, Suh SH, Kim J, Heo JH, Kim DI (2005) Detection of thrombus in acute ischemic stroke: value of thin-section noncontrast-computed tomography. Stroke 36(12):2745–2747

    Article  PubMed  Google Scholar 

  19. Kaschka IN, Kloska SP, Struffert T, Engelhorn T, Gölitz P, Kurka N, Köhrmann M, Schwab S, Doerfler A (2016) Clot burden and collaterals in anterior circulation stroke: differences between single-phase CTA and multi-phase 4D-CTA. Clin Neuroradiol 26(3):309–315

    Article  CAS  PubMed  Google Scholar 

  20. Yan S, Chen Q, Xu M, Sun J, Liebeskind DS, Lou M (2016) Thrombus length estimation on delayed gadolinium-enhanced T1. Stroke 47(3):756–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mokin M, Morr S, Natarajan SK, Lin N, Snyder KV, Hopkins LN, Siddiqui AH, Levy EI (2015) Thrombus density predicts successful recanalization with solitaire stent retriever thrombectomy in acute ischemic stroke. J Neurointerv Surg 7(2):104–107

    Article  PubMed  Google Scholar 

  22. Spiotta AM et al (2014) Hounsfield unit value and clot length in the acutely occluded vessel and time required to achieve thrombectomy, complications and outcome. J Neurointerv Surg 6(6):423–427

    Article  PubMed  Google Scholar 

  23. Dutra BG, Tolhuisen ML, Alves HCBR, Treurniet KM, Kappelhof M, Yoo AJ, Jansen IGH, Dippel DWJ, van Zwam W, van Oostenbrugge R, da Rocha AJ, Lingsma HF, van der Lugt A, Roos YBWEM, Marquering HA, Majoie CBLM, MR CLEAN Registry Investigators† (2019) Thrombus imaging characteristics and outcomes in acute ischemic stroke patients undergoing endovascular treatment. Stroke 50(8):2057–2064

    Article  PubMed  Google Scholar 

  24. Yilmaz U et al (2013) Thrombus attenuation does not predict angiographic results of mechanical thrombectomy with stent retrievers. AJNR Am J Neuroradiol 34(11):2184–2186

    Article  CAS  PubMed  Google Scholar 

  25. Jagani M, Kallmes DF, Brinjikji W (2017) Correlation between clot density and recanalization success or stroke etiology in acute ischemic stroke patients. Interv Neuroradiol 23(3):274–278

    Article  PubMed  PubMed Central  Google Scholar 

  26. Shobha N, Bal S, Boyko M, Kroshus E, Menon BK, Bhatia R, Sohn SI, Kumarpillai G, Kosior J, Hill MD, Demchuk AM (2014) Measurement of length of hyperdense MCA sign in acute ischemic stroke predicts disappearance after IV tPA. J Neuroimaging 24(1):7–10

    Article  PubMed  Google Scholar 

  27. Yoo AJ, Khatri P, Mocco J, Zaidat OO, Gupta R, Frei D, Lopes D, Shownkeen H, Berkhemer OA, Meyer D, Hak SS, Kuo SS, Buell H, Bose A, Sit SP, von Kummer R, THERAPY Trial Investigators (2017) Impact of thrombus length on outcomes after intra-arterial aspiration thrombectomy in the THERAPY trial. Stroke 48(7):1895–1900

    Article  PubMed  Google Scholar 

  28. Mokin M et al (2017) Association of clot burden score with radiographic and clinical outcomes following solitaire stent retriever thrombectomy: analysis of the SWIFT PRIME trial. J Neurointerv Surg 9(10):929–932

    Article  PubMed  Google Scholar 

  29. Angermaier A, Michel P, Khaw AV, Kirsch M, Kessler C, Langner S (2016) Intravenous thrombolysis and passes of thrombectomy as predictors for endovascular revascularization in ischemic stroke. J Stroke Cerebrovasc Dis 25(10):2488–2495

    Article  PubMed  Google Scholar 

  30. Treurniet KM et al (2016) Clot burden score on baseline computerized tomographic angiography and intra-arterial treatment effect in acute ischemic stroke. Stroke 47(12):2972–2978

    Article  PubMed  Google Scholar 

  31. Santos EM et al (2016) Thrombus permeability is associated with improved functional outcome and recanalization in patients with ischemic stroke. Stroke 47(3):732–741

    Article  CAS  PubMed  Google Scholar 

  32. Songsaeng D, Kaeowirun T, Sakarunchai I, Cheunsuchon P, Weankhanan J, Suwanbundit A, Krings T (2019) Efficacy of thrombus density on noninvasive computed tomography neuroimaging for predicting thrombus pathology and patient outcome after mechanical thrombectomy in acute ischemic stroke. Asian J Neurosurg 14(3):795–800

    Article  PubMed  PubMed Central  Google Scholar 

  33. Guzzardi G et al (2018) Mechanical thrombectomy by a direct aspiration first pass technique (ADAPT) in ischemic stroke: results of monocentric study based on multimodal CT patient selection. Stroke Res Treat 2018:6192483

    PubMed  PubMed Central  Google Scholar 

  34. Borst J, Berkhemer OA, Santos EMM, Yoo AJ, den Blanken M, Roos YBWEM, van Bavel E, van Zwam W, van Oostenbrugge R, Lingsma HF, van der Lugt A, Dippel DWJ, Marquering HA, Majoie CBLM, MR CLEAN investigators (2017) Value of thrombus CT characteristics in patients with acute ischemic stroke. AJNR Am J Neuroradiol 38(9):1758–1764

    Article  CAS  PubMed  Google Scholar 

  35. Jadhav AP, Diener HC, Bonafe A, Pereira VM, Levy EI, Baxter BW, Jovin TG, Nogueira RG, Yavagal DR, Cognard C, Purcell DD, Menon BK, Jahan R, Saver JL, Goyal M, SWIFT PRIME investigators (2017) Correlation between clinical outcomes and baseline CT and CT angiographic findings in the SWIFT PRIME trial. AJNR Am J Neuroradiol 38(12):2270–2276

    Article  CAS  PubMed  Google Scholar 

  36. Lobsien D, Gawlitza M, Schaudinn A, Schob S, Hobohm C, Fritzsch D, Quäschling U, Hoffmann KT, Friedrich B (2016) Mechanical thrombectomy versus systemic thrombolysis in MCA stroke: a distance to thrombus-based outcome analysis. J Neurointerv Surg 8(9):878–882

    Article  PubMed  Google Scholar 

  37. Park JS, Kwak HS, Chung GH, Hwang S (2018) The prognostic value of CT-angiographic parameters after reperfusion therapy in acute ischemic stroke patients with internal carotid artery terminus occlusion: leptomeningeal collateral status and clot burden score. J Stroke Cerebrovasc Dis 27(10):2797–2803

    Article  PubMed  Google Scholar 

  38. Cerase A, Grazzini I (2015) Early relapsing calcified cerebral embolism. J Stroke Cerebrovasc Dis 24(5):e125–e126

    Article  PubMed  Google Scholar 

  39. Koh E, Kwak HS, Chung GH (2017) Manual aspiration thrombectomy in patients with acute stroke-related calcified cerebral emboli. J Stroke Cerebrovasc Dis 26(10):2050–2054

    Article  PubMed  Google Scholar 

  40. Dobrocky T, Piechowiak E, Cianfoni A, Zibold F, Roccatagliata L, Mosimann P, Jung S, Fischer U, Mordasini P, Gralla J (2018) Thrombectomy of calcified emboli in stroke. Does histology of thrombi influence the effectiveness of thrombectomy? J Neurointerv Surg 10(4):345–350

    Article  PubMed  Google Scholar 

  41. Walker BS, Shah LM, Osborn AG (2014) Calcified cerebral emboli, a “do not miss” imaging diagnosis: 22 new cases and review of the literature. AJNR Am J Neuroradiol 35(8):1515–1519

    Article  CAS  PubMed  Google Scholar 

  42. Raghib MF, Mutzenbach JS, Rösler C, Otto F, Coy MM, Müller-Thies-Broussalis E, Pikija S (2018) Acute treatment of stroke due to spontaneous calcified cerebral emboli causing large vessel occlusion. J Clin Neurosci 47:56–61

    Article  PubMed  Google Scholar 

  43. Uneda A, Kanda T, Suzuki K, Hirashita K, Yunoki M, Yoshino K (2017) Acute cerebral artery occlusion by a calcified embolus with false patency sign on computed tomographic angiography. J Stroke Cerebrovasc Dis 26(1):e5–e7

    Article  PubMed  Google Scholar 

  44. Yogendrakumar V, Patro S, Dowlatshahi D, Stotts G, Iancu D (2017) Calcified embolus mimics patent middle cerebral artery on CT angiogram. Pract Neurol 17(4):307–309

    Article  PubMed  Google Scholar 

  45. Salinas P et al (2013) Neurovascular rescue for thrombus-related embolic stroke during transcatheter aortic valve implantation. JACC Cardiovasc Interv 6(9):981–982

    Article  PubMed  Google Scholar 

  46. Fassa AA, Mazighi M, Himbert D, Deschamps L, Ducrocq G, Cheong AP, Depoix JP, Dilly MP, Alkhoder S, Mourvillier B, Vahanian A (2014) Successful endovascular stroke rescue with retrieval of an embolized calcium fragment after transcatheter aortic valve replacement. Circ Cardiovasc Interv 7(1):125–126

    Article  PubMed  Google Scholar 

  47. Kirchhof K, Welzel T, Zoubaa S, Lichy C, Sikinger M, de Ruiz HL, Sartor K (2002) New method of embolus preparation for standardized embolic stroke in rabbits. Stroke 33(9):2329–2333

    Article  CAS  PubMed  Google Scholar 

  48. Overgaard K (1994) Thrombolytic therapy in experimental embolic stroke. Cerebrovasc Brain Metab Rev 6(3):257–286

    CAS  PubMed  Google Scholar 

  49. Nam HS, Kim EY, Kim SH, Kim YD, Kim J, Lee HS, Nam CM, Heo JH (2012) Prediction of thrombus resolution after intravenous thrombolysis assessed by CT-based thrombus imaging. Thromb Haemost 107(4):786–794

    Article  CAS  PubMed  Google Scholar 

  50. Niesten JM, van der Schaaf I, van der Graaf Y, Kappelle LJ, Biessels GJ, Horsch AD, Dankbaar JW, Luitse MJ, van Seeters T, Smit EJ, Mali WP, Velthuis BK (2014) Predictive value of thrombus attenuation on thin-slice non-contrast CT for persistent occlusion after intravenous thrombolysis. Cerebrovasc Dis 37(2):116–122

    Article  CAS  PubMed  Google Scholar 

  51. Puig J, Pedraza S, Demchuk A, Daunis-I-Estadella J, Termes H, Blasco G, Soria G, Boada I, Remollo S, Baños J, Serena J, Castellanos M (2012) Quantification of thrombus Hounsfield units on noncontrast CT predicts stroke subtype and early recanalization after intravenous recombinant tissue plasminogen activator. AJNR Am J Neuroradiol 33(1):90–96

    Article  CAS  PubMed  Google Scholar 

  52. Riedel CH, Zimmermann P, Jensen-Kondering U, Stingele R, Deuschl G, Jansen O (2011) The importance of size: successful recanalization by intravenous thrombolysis in acute anterior stroke depends on thrombus length. Stroke 42(6):1775–1777

    Article  PubMed  Google Scholar 

  53. Rohan V, Baxa J, Tupy R, Cerna L, Sevcik P, Friesl M, Polivka J Jr, Polivka J, Ferda J (2014) Length of occlusion predicts recanalization and outcome after intravenous thrombolysis in middle cerebral artery stroke. Stroke 45(7):2010–2017

  54. Behrens L, Möhlenbruch M, Stampfl S, Ringleb PA, Hametner C, Kellert L, Pham M, Herweh C, Bendszus M, Rohde S (2014) Effect of thrombus size on recanalization by bridging intravenous thrombolysis. Eur J Neurol 21(11):1406–1410

    Article  CAS  PubMed  Google Scholar 

  55. Tan IY, Demchuk AM, Hopyan J, Zhang L, Gladstone D, Wong K, Martin M, Symons SP, Fox AJ, Aviv RI (2009) CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol 30(3):525–531

    Article  CAS  PubMed  Google Scholar 

  56. Demchuk AM, Goyal M, Yeatts SD, Carrozzella J, Foster LD, Qazi E, Hill MD, Jovin TG, Ribo M, Yan B, Zaidat OO, Frei D, von Kummer R, Cockroft KM, Khatri P, Liebeskind DS, Tomsick TA, Palesch YY, Broderick JP, IMS III Investigators (2014) Recanalization and clinical outcome of occlusion sites at baseline CT angiography in the Interventional Management of Stroke III trial. Radiology 273(1):202–210

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiu-ying Cai, Zhuan Xu or Yan Kong.

Ethics declarations

Informed consent

Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, Sj., Diao, Ss., Lu, Y. et al. Value of thrombus imaging in predicting the outcomes of patients with large-vessel occlusive strokes after endovascular therapy. Neurol Sci 41, 1451–1458 (2020). https://doi.org/10.1007/s10072-020-04296-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-020-04296-7

Keywords

Navigation