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Predictors and Prognostic Implications of Hemorrhagic Transformation Following Cerebral Endovascular Thrombectomy in Acute Ischemic Stroke: A Multicenter Analysis

  • Clinical Investigation
  • Stroke/Neurointerventions
  • Published:
CardioVascular and Interventional Radiology Aims and scope Submit manuscript

Abstract

Purpose

Hemorrhagic transformation (HT) following cerebral endovascular thrombectomy (EVT) for large vessel occlusion (LVO) in acute ischemic stroke is associated with poor outcome. Recent studies have shown that EVT can be efficacious in imaging-selected patients as late as 6–24 h from onset (late time window; LTW). We sought to determine predictors and prognostic implications of HT following EVT in LTW.

Methods

Consecutive patients undergoing EVT for LVO were recruited into a prospective multicenter database. HT was divided into petechial hemorrhagic-infarction and parenchymal hematoma (PH) type 1 or 2 defined as confluent hemorrhage covering < or > than 1/3 of the infarct volume, respectively. Multivariate analyses were performed to determine variables associated with HT subtypes.

Results

Among 611 patients included (mean age 70.5 ± 12.5 years; median NIHSS 16), 115 (18.8%) had HT and 33 of them (5.4%) had PH2. Independent PH2 predictors included failed recanalization (OR 7.0, 95% CI 2.3–21.6), longer time from symptom onset to admission (OR 1.002 per minute 95% CI 1.001–1.003) and hyperlipidemia (OR 3.12; 95%CI 1.12–8.7). HT was not associated with outcome. In contrast, PH2 patients had lower favorable outcome rates (14.3 vs 41.6%, p = 0.004) and higher mortality rates (39 vs 17%, p = 0.001). Patients who underwent EVT in the late versus early window had similar PH2 rates (4.5 vs 6.7%, p = 0.27). In multivariate models, PH2 tripled the odds of both 90-day poor outcome (OR 3.1, 95% CI 1.01–9.5) and 90-day mortality (OR 3.2, 95% CI 1.4–7.3).

Conclusions

PH2 following EVT is associated with increased mortality and unfavorable outcome rates. Rates of PH2 are not different between LTW patients and those treated < 6 h from symptom onset.

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References

  1. van Kranendonk KR, Treurniet KM, Boers AMM, et al. Hemorrhagic transformation is associated with poor functional outcome in patients with acute ischemic stroke due to a large vessel occlusion. J Neurointervent Surg. 2019;11(5):464–8.

    Article  Google Scholar 

  2. Albers GW, Marks MP, Kemp S, et al. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018;378(8):708–18.

    Article  Google Scholar 

  3. Nogueira RG, Jadhav AP, Haussen DC, et al. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med. 2018;378(1):11–21.

    Article  Google Scholar 

  4. Powers WJ, Rabinstein AA, Ackerson T, 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(3):e46–110.

    Article  Google Scholar 

  5. Saver JL, Chapot R, Agid R, et al. Thrombectomy for distal, medium vessel occlusions: a consensus statement on present knowledge and promising directions. Stroke. 2020;51(9):2872–84.

    Article  Google Scholar 

  6. Brott T, Adams HP Jr, Olinger CP, et al. Measurements of acute cerebral infarction: a clinical examination scale. Stroke. 1989;20(7):864–70.

    Article  CAS  Google Scholar 

  7. Adams HP Jr, Bendixen BH, Kappelle LJ, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke. 1993;24(1):35–41.

    Article  Google Scholar 

  8. Hill MD, Demchuk AM, Goyal M, et al. Alberta Stroke Program early computed tomography score to select patients for endovascular treatment: interventional management of stroke (IMS)-III Trial. Stroke. 2014;45(2):444–9.

    Article  Google Scholar 

  9. Menon BK, d’Esterre CD, Qazi EM, et al. Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology. 2015;275(2):510–20.

    Article  Google Scholar 

  10. Higashida RT, Furlan AJ, Roberts H, et al. Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke. 2003;34(8):e109-137.

    Article  Google Scholar 

  11. Hacke W, Kaste M, Fieschi C, et al. Randomised double-blind placebo-controlled trial of thrombolytic therapy with intravenous alteplase in acute ischaemic stroke (ECASS II). Second European-Australasian acute stroke study investigators. Lancet. 1998;352(9136):1245–51.

    Article  CAS  Google Scholar 

  12. Hacke W, Kaste M, Fieschi C, et al. Intravenous thrombolysis with recombinant tissue plasminogen activator for acute hemispheric stroke. The European Cooperative Acute Stroke Study (ECASS). JAMA. 1995;274(13):1017–25.

    Article  CAS  Google Scholar 

  13. Hacke W, Kaste M, Bluhmki E, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 2008;359(13):1317–29.

    Article  CAS  Google Scholar 

  14. Rankin J. Cerebral vascular accidents in patients over the age of 60. II. prognosis. Scott Med J. 1957;2(5):200–15.

    Article  CAS  Google Scholar 

  15. Kaesmacher J, Kaesmacher M, Maegerlein C, et al. Hemorrhagic transformations after thrombectomy: risk factors and clinical relevance. Cerebrovasc Dis. 2017;43(5–6):294–304.

    Article  CAS  Google Scholar 

  16. Lee YB, Yoon W, Lee YY, et al. Predictors and impact of hemorrhagic transformations after endovascular thrombectomy in patients with acute large vessel occlusions. J Neurointervent Surg. 2019;11(5):469–73.

    Article  Google Scholar 

  17. Desai SM, Tonetti DA, Morrison AA, et al. Relationship between reperfusion and intracranial hemorrhage after thrombectomy. J Neurointervent Surg. 2020;12(5):448–53.

    Article  Google Scholar 

  18. Nogueira RG, Gupta R, Jovin TG, et al. Predictors and clinical relevance of hemorrhagic transformation after endovascular therapy for anterior circulation large vessel occlusion strokes: a multicenter retrospective analysis of 1122 patients. J Neurointervent Surg. 2015;7(1):16–21.

    Article  Google Scholar 

  19. Goldstein LB, Amarenco P, Szarek M, et al. Hemorrhagic stroke in the stroke prevention by aggressive reduction in cholesterol levels study. Neurology. 2008;70(24 Pt 2):2364–70.

    Article  CAS  Google Scholar 

  20. Hassan AE, Kotta H, Shariff U, Preston L, Tekle W, Qureshi A. There is no association between the number of stent retriever passes and the incidence of hemorrhagic transformation for patients undergoing mechanical thrombectomy. Front Neurol. 2019;10:818.

    Article  Google Scholar 

  21. Casetta I, Pracucci G, Saletti A, et al. Combined intravenous and endovascular treatment versus primary mechanical thrombectomy. The Italian registry of endovascular treatment in acute stroke. Int J Stroke Off J Int Stroke Soc. 2019;14(9):898–907.

    Article  Google Scholar 

  22. Maros ME, Brekenfeld C, Broocks G, et al. Number of retrieval attempts rather than procedure time is associated with risk of symptomatic intracranial hemorrhage. Stroke. 2021;52(5):1580–8.

    Article  Google Scholar 

  23. Bourcier R, Saleme S, Labreuche J, et al. More than three passes of stent retriever is an independent predictor of parenchymal hematoma in acute ischemic stroke. J Neurointerv Surg. 2019;11(7):625–9.

    Article  Google Scholar 

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Funding

This study was not supported by any funding.

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Authors and Affiliations

  1. Departments of Neurology, Hadassah-Hebrew University Medical Center, P.O. Box 12000, 91120, Jerusalem, Israel

    A. Honig, N. Simaan, T. Sacagiu, A. Figolio & R. R. Leker

  2. Department of Stroke and Neurology, Tel-Aviv Sourasky Medical Center, Tel-Aviv, Israel

    J. Molad, H. Hallevi, E. Seyman & O. Rotschild

  3. Department of Neurology, Soroka- University Medical Center, Beer-Sheva, Israel

    A. Horev, F. Alguayn & M. J. Star

  4. Department of Radiology, Tel-Aviv Sourasky Medical Center, Tel-Aviv, Israel

    J. M. Gomori

  5. Departments of Radiology, Hadassah-Hebrew University Medical Center, Jerusalem, Israel

    T. Jonas-Kimchi & U. Sadeh

  6. Departments of Neurosurgery, Hadassah-Hebrew University Medical Center, Jerusalem, Israel

    J. E. Cohen

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  1. A. Honig
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  2. J. Molad
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  3. A. Horev
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  4. N. Simaan
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  5. T. Sacagiu
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  6. A. Figolio
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  7. J. M. Gomori
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  8. H. Hallevi
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  9. E. Seyman
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  10. O. Rotschild
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  12. M. J. Star
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  13. T. Jonas-Kimchi
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  14. U. Sadeh
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  15. J. E. Cohen
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  16. R. R. Leker
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Correspondence to A. Honig.

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Honig, A., Molad, J., Horev, A. et al. Predictors and Prognostic Implications of Hemorrhagic Transformation Following Cerebral Endovascular Thrombectomy in Acute Ischemic Stroke: A Multicenter Analysis. Cardiovasc Intervent Radiol 45, 826–833 (2022). https://doi.org/10.1007/s00270-022-03115-0

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  • DOI: https://doi.org/10.1007/s00270-022-03115-0

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