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Published in: Neurocritical Care 1/2024

26-12-2023 | Edema | Original work

Association Between Hypoperfusion Intensity Ratio and Postthrombectomy Malignant Brain Edema for Acute Ischemic Stroke

Authors: Wang Chen, Xianjun Wang, Ji Liu, Mengen Wang, Shuna Yang, Lei Yang, Zixiang Gong, Wenli Hu

Published in: Neurocritical Care | Issue 1/2024

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Abstract

Background

Malignant brain edema (MBE) is a life-threatening complication that can occur after mechanical thrombectomy (MT) for acute ischemic stroke. The hypoperfusion intensity ratio (HIR) reflects the tissue-level perfusion status within the ischemic territory. This study investigated the association between HIR and MBE occurrence after MT in patients with anterior circulation large artery occlusion.

Methods

We conducted a retrospective cohort study of patients who received MT at a comprehensive stroke center from February 2020 to June 2022. Using computed tomography perfusion, the HIR was derived from the ratio of tissue volume with a time to maximum (Tmax) > 10 s to that with a Tmax > 6 s. We dichotomized patients based on the occurrence of MBE following MT. The primary outcome, assessed using a multivariable logistic regression model, was the MBE occurrence post MT. The secondary outcome focused on favorable outcomes, defined as achieving a modified Rankin Scale score of 0–2 at 90 days.

Results

Of the 603 included patients, 90 (14.9%) developed MBE after MT. The median HIR exhibited a significantly higher value in the MBE group compared with the non-MBE group (0.5 vs. 0.3; P < 0.001). Multivariable logistic regression analysis indicated that a higher HIR (adjusted odds ratio [aOR] 8.98; 95% confidence interval [CI] 2.85–28.25; P < 0.001), baseline large infarction (Alberta Stroke Program Early Computed Tomography Score < 6; aOR 1.77; 95% CI 1.04–3.01; P = 0.035), internal carotid artery occlusion (aOR 1.80; 95% CI 1.07–3.01; P = 0.028), and unsuccessful recanalization (aOR 8.45; 95% CI 4.75–15.03; P < 0.001) were independently associated with MBE post MT. Among those with successful recanalization, a higher HIR (P = 0.017) and baseline large infarction (P = 0.032) remained as predictors of MBE occurrence. Furthermore, a higher HIR (P = 0.001) and the occurrence of MBE (P < 0.001) both correlated with reduced odds of achieving favorable outcomes.

Conclusions

The presence of a higher HIR on pretreatment perfusion imaging serves as a robust predictor for MBE occurrence after MT, irrespective of successful recanalization.
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Literature
1.
go back to reference Goyal M, Menon BK, van Zwam WH, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723–31.CrossRefPubMed Goyal M, Menon BK, van Zwam WH, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723–31.CrossRefPubMed
2.
go back to reference Jovin TG, Nogueira RG, Lansberg MG, et al. Thrombectomy for anterior circulation stroke beyond 6 h from time last known well (AURORA): a systematic review and individual patient data meta-analysis. Lancet. 2022;399(10321):249–58.CrossRefPubMed Jovin TG, Nogueira RG, Lansberg MG, et al. Thrombectomy for anterior circulation stroke beyond 6 h from time last known well (AURORA): a systematic review and individual patient data meta-analysis. Lancet. 2022;399(10321):249–58.CrossRefPubMed
3.
go back to reference Huo X, Ma G, Tong X, et al. Trial of endovascular therapy for acute ischemic stroke with large infarct. N Engl J Med. 2023;388(14):1272–83.CrossRefPubMed Huo X, Ma G, Tong X, et al. Trial of endovascular therapy for acute ischemic stroke with large infarct. N Engl J Med. 2023;388(14):1272–83.CrossRefPubMed
4.
go back to reference Yoshimura S, Sakai N, Yamagami H, et al. Endovascular therapy for acute stroke with a large ischemic region. N Engl J Med. 2022;386(14):1303–13.CrossRefPubMed Yoshimura S, Sakai N, Yamagami H, et al. Endovascular therapy for acute stroke with a large ischemic region. N Engl J Med. 2022;386(14):1303–13.CrossRefPubMed
5.
go back to reference Sarraj A, Hassan AE, Abraham MG, et al. Trial of endovascular thrombectomy for large ischemic strokes. N Engl J Med. 2023;388(14):1259–71.CrossRefPubMed Sarraj A, Hassan AE, Abraham MG, et al. Trial of endovascular thrombectomy for large ischemic strokes. N Engl J Med. 2023;388(14):1259–71.CrossRefPubMed
6.
go back to reference Vahedi K, Hofmeijer J, Juettler E, et al. Early decompressive surgery in malignant infarction of the middle cerebral artery: a pooled analysis of three randomised controlled trials. Lancet Neurol. 2007;6(3):215–22.CrossRefPubMed Vahedi K, Hofmeijer J, Juettler E, et al. Early decompressive surgery in malignant infarction of the middle cerebral artery: a pooled analysis of three randomised controlled trials. Lancet Neurol. 2007;6(3):215–22.CrossRefPubMed
7.
go back to reference Huang X, Chen C, Wang H, Cai Q, Li Z, Xu J, Yuan L, Xu X, Yang Q, Zhou Z, Liu X. The ACORNS grading scale: a novel tool for the prediction of malignant brain edema after endovascular thrombectomy. J Neurointerventional Surg. 2023;15(e2):e190–7.CrossRef Huang X, Chen C, Wang H, Cai Q, Li Z, Xu J, Yuan L, Xu X, Yang Q, Zhou Z, Liu X. The ACORNS grading scale: a novel tool for the prediction of malignant brain edema after endovascular thrombectomy. J Neurointerventional Surg. 2023;15(e2):e190–7.CrossRef
8.
go back to reference Guo W, Xu J, Zhao W, et al. A nomogram for predicting malignant cerebral artery infarction in the modern thrombectomy era. Front Neurol. 2022;13:934051.CrossRefPubMedPubMedCentral Guo W, Xu J, Zhao W, et al. A nomogram for predicting malignant cerebral artery infarction in the modern thrombectomy era. Front Neurol. 2022;13:934051.CrossRefPubMedPubMedCentral
9.
go back to reference Bernsen MLE, Kauw F, Martens JM, et al. Malignant infarction after endovascular treatment: Incidence and prediction. Int J Stroke. 2022;17(2):198–206.CrossRefPubMed Bernsen MLE, Kauw F, Martens JM, et al. Malignant infarction after endovascular treatment: Incidence and prediction. Int J Stroke. 2022;17(2):198–206.CrossRefPubMed
10.
go back to reference Kimberly WT, Dutra BG, Boers AMM, et al. Association of reperfusion with brain edema in patients with acute ischemic stroke: a secondary analysis of the MR CLEAN trial. JAMA Neurol. 2018;75(4):453–61.CrossRefPubMedPubMedCentral Kimberly WT, Dutra BG, Boers AMM, et al. Association of reperfusion with brain edema in patients with acute ischemic stroke: a secondary analysis of the MR CLEAN trial. JAMA Neurol. 2018;75(4):453–61.CrossRefPubMedPubMedCentral
11.
go back to reference Maier IL, Behme D, Schnieder M, et al. Early computed tomography-based scores to predict decompressive hemicraniectomy after endovascular therapy in acute ischemic stroke. PLoS ONE. 2017;12(3):e0173737.CrossRefPubMedPubMedCentral Maier IL, Behme D, Schnieder M, et al. Early computed tomography-based scores to predict decompressive hemicraniectomy after endovascular therapy in acute ischemic stroke. PLoS ONE. 2017;12(3):e0173737.CrossRefPubMedPubMedCentral
12.
go back to reference Huang X, Yang Q, Shi X, et al. Predictors of malignant brain edema after mechanical thrombectomy for acute ischemic stroke. J Neurointerv Surg. 2019;11(10):994–8.CrossRefPubMed Huang X, Yang Q, Shi X, et al. Predictors of malignant brain edema after mechanical thrombectomy for acute ischemic stroke. J Neurointerv Surg. 2019;11(10):994–8.CrossRefPubMed
13.
go back to reference Olivot JM, Mlynash M, Inoue M, et al. Hypoperfusion intensity ratio predicts infarct progression and functional outcome in the DEFUSE 2 Cohort. Stroke. 2014;45(4):1018–23.CrossRefPubMedPubMedCentral Olivot JM, Mlynash M, Inoue M, et al. Hypoperfusion intensity ratio predicts infarct progression and functional outcome in the DEFUSE 2 Cohort. Stroke. 2014;45(4):1018–23.CrossRefPubMedPubMedCentral
14.
go back to reference Guenego A, Fahed R, Albers GW, et al. Hypoperfusion intensity ratio correlates with angiographic collaterals in acute ischaemic stroke with M1 occlusion. Eur J Neurol. 2020;27(5):864–70.CrossRefPubMed Guenego A, Fahed R, Albers GW, et al. Hypoperfusion intensity ratio correlates with angiographic collaterals in acute ischaemic stroke with M1 occlusion. Eur J Neurol. 2020;27(5):864–70.CrossRefPubMed
15.
go back to reference de Havenon A, Mlynash M, Kim-Tenser MA, et al. Results from DEFUSE 3: good collaterals are associated with reduced ischemic core growth but not neurologic outcome. Stroke. 2019;50(3):632–8.CrossRefPubMedPubMedCentral de Havenon A, Mlynash M, Kim-Tenser MA, et al. Results from DEFUSE 3: good collaterals are associated with reduced ischemic core growth but not neurologic outcome. Stroke. 2019;50(3):632–8.CrossRefPubMedPubMedCentral
16.
go back to reference Faizy TD, Kabiri R, Christensen S, et al. Perfusion imaging-based tissue-level collaterals predict ischemic lesion net water uptake in patients with acute ischemic stroke and large vessel occlusion. J Cereb Blood Flow Metab. 2021;41(8):2067–75.CrossRefPubMedPubMedCentral Faizy TD, Kabiri R, Christensen S, et al. Perfusion imaging-based tissue-level collaterals predict ischemic lesion net water uptake in patients with acute ischemic stroke and large vessel occlusion. J Cereb Blood Flow Metab. 2021;41(8):2067–75.CrossRefPubMedPubMedCentral
17.
go back to reference Murray NM, Culbertson CJ, Wolman DN, Mlynash M, Lansberg MG. Hypoperfusion intensity ratio predicts malignant edema and functional outcome in large-vessel occlusive stroke with poor revascularization. Neurocrit Care. 2021;35(1):79–86.CrossRefPubMed Murray NM, Culbertson CJ, Wolman DN, Mlynash M, Lansberg MG. Hypoperfusion intensity ratio predicts malignant edema and functional outcome in large-vessel occlusive stroke with poor revascularization. Neurocrit Care. 2021;35(1):79–86.CrossRefPubMed
18.
go back to reference Sarraj A, Kleinig TJ, Hassan AE, et al. Association of endovascular thrombectomy vs medical management with functional and safety outcomes in patients treated beyond 24 hours of last known well: The select late study. JAMA Neurol. 2023;80(2):172–82.CrossRefPubMed Sarraj A, Kleinig TJ, Hassan AE, et al. Association of endovascular thrombectomy vs medical management with functional and safety outcomes in patients treated beyond 24 hours of last known well: The select late study. JAMA Neurol. 2023;80(2):172–82.CrossRefPubMed
19.
go back to reference von Elm E, Altman DG, Egger M, et al. Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ. 2007;335(7624):806–8.CrossRef von Elm E, Altman DG, Egger M, et al. Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ. 2007;335(7624):806–8.CrossRef
20.
go back to reference von Kummer R, Broderick JP, Campbell BC, et al. The heidelberg bleeding classification: classification of bleeding events after ischemic stroke and reperfusion therapy. Stroke. 2015;46(10):2981–6.CrossRef von Kummer R, Broderick JP, Campbell BC, et al. The heidelberg bleeding classification: classification of bleeding events after ischemic stroke and reperfusion therapy. Stroke. 2015;46(10):2981–6.CrossRef
21.
go back to reference 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):e109–37.CrossRefPubMed 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):e109–37.CrossRefPubMed
22.
go back to reference Yang P, Zhang Y, Zhang L, et al. Endovascular thrombectomy with or without intravenous Alteplase in acute stroke. N Engl J Med. 2020;382(21):1981–93.CrossRefPubMed Yang P, Zhang Y, Zhang L, et al. Endovascular thrombectomy with or without intravenous Alteplase in acute stroke. N Engl J Med. 2020;382(21):1981–93.CrossRefPubMed
23.
go back to reference Wardlaw JM, Sellar R. A simple practical classification of cerebral infarcts on CT and its interobserver reliability. AJNR Am J Neuroradiol. 1994;15(10):1933–9.PubMedPubMedCentral Wardlaw JM, Sellar R. A simple practical classification of cerebral infarcts on CT and its interobserver reliability. AJNR Am J Neuroradiol. 1994;15(10):1933–9.PubMedPubMedCentral
24.
go back to reference Ong CJ, Gluckstein J, Laurido-Soto O, Yan Y, Dhar R, Lee JM. Enhanced detection of Edema in malignant anterior circulation stroke (EDEMA) score: a risk prediction tool. Stroke. 2017;48(7):1969–72.CrossRefPubMedPubMedCentral Ong CJ, Gluckstein J, Laurido-Soto O, Yan Y, Dhar R, Lee JM. Enhanced detection of Edema in malignant anterior circulation stroke (EDEMA) score: a risk prediction tool. Stroke. 2017;48(7):1969–72.CrossRefPubMedPubMedCentral
25.
go back to reference Investigators RBT, Qiu Z, Li F, et al. Effect of Intravenous Tirofiban vs Placebo before endovascular Thrombectomy on functional outcomes in large vessel occlusion stroke: The RESCUE BT randomized clinical trial. JAMA. 2022;328(6):543–53.CrossRef Investigators RBT, Qiu Z, Li F, et al. Effect of Intravenous Tirofiban vs Placebo before endovascular Thrombectomy on functional outcomes in large vessel occlusion stroke: The RESCUE BT randomized clinical trial. JAMA. 2022;328(6):543–53.CrossRef
26.
go back to reference Haggenmüller B, Kreiser K, Sollmann N, Huber M, Vogele D, Schmidt SA, Beer M, Schmitz B, Ozpeynirci Y, Rosskopf J, Kloth C. Pictorial review on imaging findings in cerebral CTP in patients with acute stroke and its mimics: a primer for general radiologists. Diagnostics. 2023;13(3):447.CrossRefPubMedPubMedCentral Haggenmüller B, Kreiser K, Sollmann N, Huber M, Vogele D, Schmidt SA, Beer M, Schmitz B, Ozpeynirci Y, Rosskopf J, Kloth C. Pictorial review on imaging findings in cerebral CTP in patients with acute stroke and its mimics: a primer for general radiologists. Diagnostics. 2023;13(3):447.CrossRefPubMedPubMedCentral
27.
go back to reference van Horn N, Broocks G, Kabiri R, Kraemer MC, Christensen S, Mlynash M, Meyer L, Lansberg MG, Albers GW, Sporns P, Guenego A. Cerebral hypoperfusion intensity ratio is linked to progressive early edema formation. J Clin Med. 2022;11(9):2373.CrossRefPubMedPubMedCentral van Horn N, Broocks G, Kabiri R, Kraemer MC, Christensen S, Mlynash M, Meyer L, Lansberg MG, Albers GW, Sporns P, Guenego A. Cerebral hypoperfusion intensity ratio is linked to progressive early edema formation. J Clin Med. 2022;11(9):2373.CrossRefPubMedPubMedCentral
28.
go back to reference Winkelmeier L, Heit JJ, Adusumilli G, et al. Hypoperfusion intensity ratio is correlated with the risk of parenchymal hematoma after endovascular stroke treatment. Stroke. 2023;54(1):135–43.CrossRefPubMed Winkelmeier L, Heit JJ, Adusumilli G, et al. Hypoperfusion intensity ratio is correlated with the risk of parenchymal hematoma after endovascular stroke treatment. Stroke. 2023;54(1):135–43.CrossRefPubMed
29.
go back to reference Guenego A, Mlynash M, Christensen S, et al. Hypoperfusion ratio predicts infarct growth during transfer for thrombectomy. Ann Neurol. 2018;84(4):616–20.CrossRefPubMed Guenego A, Mlynash M, Christensen S, et al. Hypoperfusion ratio predicts infarct growth during transfer for thrombectomy. Ann Neurol. 2018;84(4):616–20.CrossRefPubMed
30.
go back to reference Faizy TD, Mlynash M, Kabiri R, Christensen S, Kuraitis G, Meyer L, Bechstein M, Van Horn N, Lansberg MG, Albers G, Fiehler J. Favourable arterial, tissue-level and venous collaterals correlate with early neurological improvement after successful thrombectomy treatment of acute ischaemic stroke. J Neurol Neurosurg Psychiatr. 2022;93(7):701–6.CrossRef Faizy TD, Mlynash M, Kabiri R, Christensen S, Kuraitis G, Meyer L, Bechstein M, Van Horn N, Lansberg MG, Albers G, Fiehler J. Favourable arterial, tissue-level and venous collaterals correlate with early neurological improvement after successful thrombectomy treatment of acute ischaemic stroke. J Neurol Neurosurg Psychiatr. 2022;93(7):701–6.CrossRef
31.
go back to reference Maslias E, Nannoni S, Bartolini B, et al. Early-versus-Late endovascular stroke treatment: similar frequencies of Nonrevascularization and Postprocedural cerebrovascular complications in a large single-center cohort study. AJNR Am J Neuroradiol. 2023;44(6):687–92.CrossRefPubMed Maslias E, Nannoni S, Bartolini B, et al. Early-versus-Late endovascular stroke treatment: similar frequencies of Nonrevascularization and Postprocedural cerebrovascular complications in a large single-center cohort study. AJNR Am J Neuroradiol. 2023;44(6):687–92.CrossRefPubMed
32.
Metadata
Title
Association Between Hypoperfusion Intensity Ratio and Postthrombectomy Malignant Brain Edema for Acute Ischemic Stroke
Authors
Wang Chen
Xianjun Wang
Ji Liu
Mengen Wang
Shuna Yang
Lei Yang
Zixiang Gong
Wenli Hu
Publication date
26-12-2023
Publisher
Springer US
Published in
Neurocritical Care / Issue 1/2024
Print ISSN: 1541-6933
Electronic ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-023-01900-4

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