Clinical Advances in Hemorrhagic Transformation after Mechanical Thrombectomy for Acute Ischemic Stroke due to Large Vessel Occlusion

doi:10.3969/j.issn.1673-5765.2024.01.013

Abstract

Abstract: Mechanical thrombectomy is the standard treatment for acute ischemic stroke due to large vessel occlusion in the anterior circulation within 24 hours of onset, and hemorrhagic transformation is the most common and serious complication, which not only increases the length of hospital stay, but also leads to a poor prognosis and negates the benefits of mechanical thrombectomy. Therefore, it is of great importance to scientifically understand this complication. Recently, domestic and foreign scholars have carried out extensive investigations on the hemorrhagic transformation after mechanical thrombectomy. In this paper, the definition, classification, incidence, risk factors, prevention and management of hemorrhagic transformation were reviewed based on domestic and foreign literatures.

Key words: Ischemic stroke; Mechanical thrombectomy; Hemorrhagic transformation; Risk factor

摘要： 机械取栓是发病24 h内的急性前循环大血管闭塞性缺血性卒中的标准治疗，出血转化是其最常见、最严重的并发症，不仅会延长患者的住院时间，而且会导致预后不良，抵消机械取栓带来的获益。因此，有必要科学地认识这一并发症。近年来，国内外学者围绕机械取栓术后出血转化开展了广泛研究，本文结合国内外文献，从出血转化的定义、分型、发生率、危险因素、预防和管理等方面进行综述。

关键词: 缺血性卒中; 机械取栓; 出血转化; 危险因素

CLC Number:

KANG Zhiming, MEI Bin. Clinical Advances in Hemorrhagic Transformation after Mechanical Thrombectomy for Acute Ischemic Stroke due to Large Vessel Occlusion[J]. Chinese Journal of Stroke, 2024, 19(1): 94-104.

康志明, 梅斌. 急性大血管闭塞性卒中机械取栓术后出血转化的研究进展[J]. 中国卒中杂志, 2024, 19(1): 94-104.

References

[1] RENNERT R C，WALI A R，STEINBERG J A，et al. Epidemiology，natural history，and clinical presentation of large vessel ischemic stroke[J/OL]. Neurosurgery，2019，85：S4-S8[2023-03-18]. https://doi.org/10.1093/neuros/nyz042.
[2] LAKOMKIN N，DHAMOON M，CARROLL K，et al. Prevalence of large vessel occlusion in patients presenting with acute ischemic stroke：a 10-year systematic review of the literature[J]. J Neurointerv Surg，2019，11（3）：241-245.
[3] GOYAL M，MENON B K，VAN ZWAM W H，et al. Endovascular thrombectomy after large-vessel ischaemic stroke：a meta-analysis of individual patient data from five randomised trials[J]. Lancet，2016，387（100029）：1723-1731.
[4] POWERS W J，RABINSTEIN A A，ACKERSON T，et al. Guidelines for the early management of patients with acute ischemic stroke：2019 update to the 2018 guidelines for the early management of acute ischemic stroke：a guideline for healthcare professionals from the American Heart Association/American Stroke Association
[J/OL]. Stroke，2019，50（12）：e344-e418[2023-03-19].
https://doi.org/10.1161/STR.0000000000000211.
[5] 中国卒中学会，中国卒中学会神经介入分会，中华预防医学会卒中预防与控制专业委员会介入学组. 急性缺血性卒中血管内治疗中国指南2018[J]. 中国卒中杂志，2018，13（7）：706-729.
Chinese Stroke Association，Chinese Interventional Neuroradiology Society，Intervention Group of Committee of Stroke Prevention and Control of Chinese Preventive Medicine Association. Chinese guideline for endovascular treatment of acute ischemic stroke 2018[J]. Chin J Stroke，2018，13（7）：706-729.
[6] 中华医学会神经病学分会，中华医学会神经病学分会脑血管病学组. 中国急性缺血性脑卒中诊治指南2018[J]. 中华神经科杂志，2018，51（9）：666-682.
Chinese Society of Neurology，Chinese Stroke Society. Chinese guidelines for diagnosis and treatment of acute ischemic stroke 2018[J]. Chin J Neurol，2018，51（9）：666-682.
[7] VAN KRANENDONK K R，TREURNIET K M，BOERS A M M，et al. Hemorrhagic transformation is associated with poor functional outcome in patients with acute ischemic stroke due to a large vessel occlusion[J]. J Neurointerv Surg，2019，11（5）：464-468.
[8] LEE Y B，YOON W，LEE Y Y，et al. Predictors and impact of hemorrhagic transformations after endovascular thrombectomy in patients with acute large vessel occlusions[J]. J Neurointerv Surg，2019，11（5）：469-473.
[9] KAESMACHER J，KAESMACHER M，MAEGERLEIN C，et al. Hemorrhagic transformations after thrombectomy：risk factors and clinical relevance[J]. Cerebrovasc Dis，2017，43（5/6）：294-304.
[10] LI W R，XING X L，WEN C，et al. Risk factors and functional outcome were associated with hemorrhagic transformation after mechanical thrombectomy for acute large vessel occlusion stroke[J]. J Neurosurg Sci，2023，67（5）：585-590.
[11] VON KUMMER R，BRODERICK J P，CAMPBELL B C，et al. The Heidelberg bleeding classification：classification of bleeding events after ischemic stroke and reperfusion therapy[J]. Stroke，2015，46（10）：2981-2986.
[12] Intracerebral hemorrhage after intravenous t-pa therapy for ischemic stroke[J]. Stroke，1997，28（11）：2109-2118.
[13] 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）[J]. JAMA，1995，274（13）：1017-1025.
[14] HACKE W，KASTE M，BLUHMKI E，et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke[J]. N Engl J Med，2008，359（13）：1317-1329.
[15] CONSTANT D B P，PRETERRE C，DE GAALON S，et al. Prognosis and risk factors associated with asymptomatic intracranial hemorrhage after endovascular treatment of large vessel occlusion stroke：a prospective multicenter cohort study[J]. Eur J Neurol，2021，28（1）：229-237.
[16] HAO Y G，LIU W H，WANG H M，et al. Prognosis of asymptomatic intracranial hemorrhage after endovascular treatment[J]. J Neurointerv Surg，2019，11（2）：123-126.
[17] JIANG F，ZHAO W B，WU C J，et al. Asymptomatic intracerebral hemorrhage may worsen clinical outcomes in acute ischemic stroke patients undergoing thrombectomy[J]. J Stroke Cerebrovasc Dis，2019，28（6）：1752-1758.
[18] DZIALOWSKI I，PEXMAN J H，BARBER P A，et al. Asymptomatic hemorrhage after thrombolysis may not be benign：prognosis by hemorrhage type in the Canadian alteplase for stroke effectiveness study registry[J]. Stroke，2007，38（1）：75-79.
[19] VAN DER STEEN W，VAN DER ENDE N A M，LUIJTEN S P R，et al. Type of intracranial hemorrhage after endovascular stroke treatment：association with functional outcome[J]. J Neurointerv Surg，2023，15（10）：971-976.
[20] FELDMAN M J，ROTH S，FUSCO M R，et al. Association of asymptomatic hemorrhage after endovascular stroke treatment with outcomes[J]. J Neurointerv Surg，2021，13（12）：1095-1098.
[21] MARTINS S O，MONT’ALVERNE F，REBELLO L C，et al. Thrombectomy for stroke in the public health care system of Brazil[J]. N Engl J Med，2020，382（24）：2316-2326.
[22] NOGUEIRA R G，JADHAV A P，HAUSSEN D C，et al. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct[J]. N Engl J Med，2018，378（1）：11-21.
[23] ALBERS G W，MARKS M P，KEMP S，et al. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging[J]. N Engl J Med，2018，378（8）：708-718.
[24] JOVIN T G，NOGUEIRA R G，LANSBERG M G，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[J]. Lancet，2022，399（10321）：249-258.
[25] ZI W J，WANG H M，YANG D，et al. Clinical effectiveness and safety outcomes of endovascular treatment for acute anterior circulation ischemic stroke in China[J]. Cerebrovasc Dis，2017，44（5/6）：248-258.
[26] CAI L X，YU X B，YU J，et al. Can tirofiban improve the outcome of patients with acute ischemic stroke：a propensity score matching analysis[J/OL]. Front Neurol，2021，12：688019[2023-03-11]. https://doi.org/10.3389/fneur.2021.688019.
[27] KINJO N，YOSHIMURA S，UCHIDA K，et al. Incidence and prognostic impact of intracranial hemorrhage after endovascular treatment for acute large vessel occlusion[J]. Cerebrovasc Dis，2020，49（5）：540-549.
[28] 中华医学会神经病学分会，中华医学会神经病学分会脑血管病学组. 中国急性脑梗死后出血转化诊治共识2019[J]. 中华神经科杂志，2019，52（4）：252-265.
Chinese Society of Neurology，Chinese Stroke Society. Consensus on diagnosis and treatment of hemorrhagic transformation after acute ischemic stroke in China 2019[J]. Chin J Neurol，2019，52（4）：252-265.
[29] YOSHIMURA S，SAKAI N，YAMAGAMI H，et al. Endovascular therapy for acute stroke with a large ischemic region[J]. N Engl J Med，2022，386（14）：1303-1313.
[30] CAPPELLARI M，MANGIAFICO S，SAIA V，et al. IER-SICH nomogram to predict symptomatic intracerebral hemorrhage after thrombectomy for stroke[J]. Stroke，2019，50（4）：909-916.
[31] SUN J C，LAM C，CHRISTIE L，et al. Risk factors of hemorrhagic transformation in acute ischaemic stroke：a systematic review and meta-analysis
[J/OL]. Front Neurol，2023，14：1079205[2023-03-11]. https://doi.org/10.3389/fneur.2023.1079205.
[32] JIANG S W，FEI A H，PENG Y，et al. Predictors of outcome and hemorrhage in patients undergoing endovascular therapy with solitaire stent for acute ischemic stroke[J/OL]. PLoS One，2015，10（12）：e144452[2023-03-11]. https://doi.org/10.1371/journal.pone.0144452.
[33] HAO Z L，YANG C S，XIANG L B，et al. Risk factors for intracranial hemorrhage after mechanical thrombectomy：a systematic review and meta-analysis[J]. Expert Rev Neurother，2019，19（10）：927-935.
[34] JIMENEZ-CONDE J，BIFFI A，RAHMAN R，et al. Hyperlipidemia and reduced white matter hyperintensity volume in patients with ischemic stroke[J]. Stroke，2010，41（3）：437-442.
[35] D’AMELIO M，TERRUSO V，FAMOSO G，et al. Cholesterol levels and risk of hemorrhagic transformation after acute ischemic stroke[J]. Cerebrovasc Dis，2011，32（3）：234-238.
[36] YERAMANENI S，KLEINDORFER D O，SUCHAREW H，et al. Hyperlipidemia is associated with lower risk of poststroke mortality independent of statin use：a population-based study[J]. Int J Stroke，2017，12（2）：152-160.
[37] SUGIURA Y，YAMAGAMI H，SAKAI N，et al. Predictors of symptomatic intracranial hemorrhage after endovascular therapy in acute ischemic stroke with large vessel occlusion[J]. J Stroke Cerebrovasc Dis，2017，26（4）：766-771.
[38] VENDITTI L，CHASSIN O，ANCELET C，et al. Pre-procedural predictive factors of symptomatic intracranial hemorrhage after thrombectomy in stroke[J]. J Neurol，2021，268（5）：1867-1875.
[39] GOYAL N，TSIVGOULIS G，PANDHI A，et al. Admission hyperglycemia and outcomes in large vessel occlusion strokes treated with mechanical thrombectomy[J]. J Neurointerv Surg，2018，10（2）：112-117.
[40] ZANG L，ZHANG D，YAO Y Y，et al. Symptomatic intracranial hemorrhage in patients with admission hyperglycemia and diabetes after mechanical thrombectomy：a systematic review and meta-analysis
[J/OL]. Am J Emerg Med，2021，45：23-28[2023-03-11]. https://doi.org/10.1016/j.ajem.2021.02.032.
[41] CHIU C D，CHEN C C，SHEN C C，et al. Hyperglycemia exacerbates intracerebral hemorrhage via the downregulation of aquaporin-4：temporal assessment with magnetic resonance imaging[J]. Stroke，2013，44（6）：1682-1689.
[42] DIETRICH W D，ALONSO O，BUSTO R. Moderate hyperglycemia worsens acute blood-brain barrier injury after forebrain ischemia in rats[J]. Stroke，1993，24（1）：111-116.
[43] BARBER P A，DEMCHUK A M，ZHANG J，et al. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy[J]. Lancet，2000，355（9216）：1670-1674.
[44] HAO Y G，YANG D，WANG H M，et al. Predictors for symptomatic intracranial hemorrhage after endovascular treatment of acute ischemic stroke[J]. Stroke，2017，48（5）：1203-1209.
[45] DEMEESTERE J，GARCIA-ESPERON C，GARCIA-BERMEJO P，et al. Evaluation of hyperacute infarct volume using ASPECTS and brain CT perfusion core volume[J]. Neurology，2017，88（24）：2248-2253.
[46] BANG O Y，SAVER J L，KIM S J，et al. Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke[J]. Stroke，2011，42（8）：2235-2239.
[47] QIAN J C，FAN L，ZHANG W Q，et al. A meta-analysis of collateral status and outcomes of mechanical thrombectomy[J]. Acta Neurol Scand，2020，142（3）：191-199.
[48] PUETZ V，DZIALOWSKI I，HILL M D，et al. Intracranial thrombus extent predicts clinical outcome，final infarct size and hemorrhagic transformation in ischemic stroke：the clot burden score[J]. Int J Stroke，2008，3（4）：230-236.
[49] YOGENDRAKUMAR V，AL-AJLAN F，NAJM M，et al. Clot burden score and early ischemia predict intracranial hemorrhage following endovascular therapy[J]. AJNR Am J Neuroradiol，2019，40（4）：655-660.
[50] MAIR G，BOYD E V，CHAPPELL F M，et al. Sensitivity and specificity of the hyperdense artery sign for arterial obstruction in acute ischemic stroke[J]. Stroke，2015，46（1）：102-107.
[51] KANG Z M，WU L S，SUN D，et al. Proximal hyperdense middle cerebral artery sign is associated with increased risk of asymptomatic hemorrhagic transformation after endovascular thrombectomy：a multicenter retrospective study[J]. J Neurol，2023，270（3）：1587-1599.
[52] RENÚ A，LAREDO C，TUDELA R，et al. Brain hemorrhage after endovascular reperfusion therapy of ischemic stroke：a threshold-finding whole-brain perfusion CT study[J]. J Cereb Blood Flow Metab，2017，37（1）：153-165.
[53] KAMEDA K，UNO J，OTSUJI R，et al. Optimal thresholds for ischemic penumbra predicted by computed tomography perfusion in patients with acute ischemic stroke treated with mechanical thrombectomy[J]. J Neurointerv Surg，2018，10（3）：279-284.
[54] JIANG L，ZHOU L L，ZHANG H，et al. MRI predictors of intracranial hemorrhage in acute ischemic stroke after endovascular thrombectomy therapy[J]. Am J Transl Res，2020，12（8）：4532-4541.
[55] EMBERSON J，LEES K R，LYDEN P，et al. Effect of treatment delay，age，and stroke severity on the effects of intravenous thrombolysis with alteplase for acute ischaemic stroke：a meta-analysis of individual patient data from randomised trials[J]. Lancet，2014，384（9958）：1929-1935.
[56] SUMII T，LO E H. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats[J]. Stroke，2002，33（3）：831-836.
[57] LAKHAN S E，KIRCHGESSNER A，TEPPER D，et al. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke[J/OL]. Front Neurol，2013，4：32[2023-03-11]. https://doi.org/10.3389/fneur.2013.00032.
[58] PODLASEK A，DHILLON P S，BUTT W，et al. Direct mechanical thrombectomy without intravenous thrombolysis versus bridging therapy for acute ischemic stroke：a meta-analysis of randomized controlled trials[J]. Int J Stroke，2021，16（6）：621-631.
[59] ZHENG M L，LI L，CHEN L Z，et al. Mechanical thrombectomy combined with intravenous thrombolysis for acute ischemic stroke：a systematic review and meta-analyses[J/OL]. Sci Rep，2023，13（1）：8597[2023-03-11]. https://doi.org/10.1038/s41598-023-35532-7.
[60] COUTURE M，MARNAT G，GRIFFIER R，et al. Antiplatelet therapy increases symptomatic ICH risk after thrombolysis and thrombectomy[J]. Acta Neurol Scand，2021，144（5）：500-508.
[61] VAN DE GRAAF R A，ZINKSTOK S M，CHALOS V，et al. Prior antiplatelet therapy in patients undergoing endovascular treatment for acute ischemic stroke：results from the MR CLEAN registry[J]. Int J Stroke，2020，16（4）：476-485.
[62] MEINEL T R，KNIEPERT J U，SEIFFGE D J，et al. Endovascular stroke treatment and risk of intracranial hemorrhage in anticoagulated patients[J]. Stroke，2020，51（3）：892-898.
[63] RAMOS-ARAQUE M E，CHAVARRÍA-MIRANDA A，GÓMEZ-VICENTE B，et al. Oral anticoagulation and risk of symptomatic hemorrhagic transformation in stroke patients treated with mechanical thrombectomy：data from the Nordictus registry
[J/OL]. Front Neurol，2020，11：594251[2023-03-11]. https://doi.org/10.3389/fneur.2020.594251.
[64] L’ALLINEC V，ERNST M，SEVIN-ALLOUET M，et al. Safety and efficacy of mechanical thrombectomy in acute ischemic stroke of anticoagulated patients[J/OL]. J Neurointerv Surg，2018，10（12）：e29[2023-03-11]. https://doi.org/10.1136/neurintsurg-2017-013714.
[65] PURRUCKER J C，WOLF M，HAAS K，et al. Safety of endovascular thrombectomy in patients receiving non-vitamin K antagonist oral anticoagulants[J]. Stroke，2016，47（4）：1127-1130.
[66] GOLDHOORN R B，VAN DE GRAAF R A，VAN REES J M，et al. Endovascular treatment for acute ischemic stroke in patients on oral anticoagulants：results from the MR CLEAN registry[J]. Stroke，2020，51（6）：1781-1789.
[67] LAPERGUE B，BLANC R，GORY B，et al. Effect of endovascular contact aspiration vs. stent retriever on revascularization in patients with acute ischemic stroke and large vessel occlusion：the ASTER randomized clinical trial[J]. JAMA，2017，318（5）：443-452.
[68] LAPERGUE B，BLANC R，COSTALAT V，et al. Effect of thrombectomy with combined contact aspiration and stent retriever vs. stent retriever alone on revascularization in patients with acute ischemic stroke and large vessel occlusion：the ASTER2 randomized clinical trial[J]. JAMA，2021，326（12）：1158-1169.
[69] MOHAMMADEN M H，HAUSSEN D C，PISANI L，et al. Stent-retriever alone vs. aspiration and stent-retriever combination in large vessel occlusion stroke：a matched analysis[J]. Int J Stroke，2022，17（4）：465-473.
[70] BRODERICK J P，PALESCH Y Y，DEMCHUK A M，et al. Endovascular therapy after intravenous t-PA versus t-PA alone for stroke[J]. N Engl J Med，2013，368（10）：893-903.
[71] ZHAO W B，CHE R W，SHANG S Y，et al. Low-dose tirofiban improves functional outcome in acute ischemic stroke patients treated with endovascular thrombectomy[J]. Stroke，2017，48（12）：3289-3294.
[72] PAN X，ZHENG D，ZHENG Y，et al. Safety and efficacy of tirofiban combined with endovascular treatment in acute ischaemic stroke[J]. Eur J Neurol，2019，26（8）：1105-1110.
[73] CHANG Y，KIM B M，BANG O Y，et al. Rescue stenting for failed mechanical thrombectomy in acute ischemic stroke：a multicenter experience[J]. Stroke，2018，49（4）：958-964.
[74] MOHAMMADEN M H，HAUSSEN D C，AL-BAYATI A R，et al. Stenting and angioplasty in neurothrombectomy：matched analysis of rescue intracranial stenting versus failed thrombectomy[J]. Stroke，2022，53（9）：2779-2788.
[75] MONTALVO M，MISTRY E，CHANG A D，et al. Predicting symptomatic intracranial haemorrhage after mechanical thrombectomy：the TAG score[J]. J Neurol Neurosurg Psychiatry，2019，90（12）：1370-1374.
[76] MISTRY E A，MISTRY A M，NAKAWAH M O，et al. Systolic blood pressure within 24 hours after thrombectomy for acute ischemic stroke correlates with outcome
[J/OL]. J Am Heart Assoc，2017，6（5）：e006167[2023-
03-11]. https://doi.org/10.1161/JAHA.117.006167.
[77] ANADANI M，ORABI M Y，ALAWIEH A，et al. Blood pressure and outcome after mechanical thrombectomy with successful revascularization[J]. Stroke，2019，50（9）：2448-2454.
[78] KATSANOS A H，MALHOTRA K，AHMED N，et al. Blood pressure after endovascular thrombectomy and outcomes in patients with acute ischemic stroke：an individual patient data meta-analysis[J/OL]. Neurology，2022，98（3）：e291-e301[2023-03-11]. https://doi.org/10.1212/WNL.0000000000013049.
[79] PETERSEN N H，KODALI S，MENG C，et al. Blood pressure trajectory groups and outcome after endovascular thrombectomy：a multicenter study[J]. Stroke，2022，53（4）：1216-1225.
[80] ANADANI M，ARTHUR A S，TSIVGOULIS G，et al. Blood pressure goals and clinical outcomes after successful endovascular therapy：a multicenter study[J]. Ann Neurol，2020，87（6）：830-839.
[81] MAZIGHI M，RICHARD S，LAPERGUE B，et al. Safety and efficacy of intensive blood pressure lowering after successful endovascular therapy in acute ischaemic stroke（BP-TARGET）：a multicentre，open-label，randomised controlled trial[J]. Lancet Neurol，2021，20（4）：265-274.
[82] YANG P F，SONG L L，ZHANG Y W，et al. Intensive blood pressure control after endovascular thrombectomy for acute ischaemic stroke（ENCHANTED2/MT）：a multicentre，open-label，blinded-endpoint，randomised controlled trial[J]. Lancet，2022，400（10367）：1585-1596.
[83] ZHANG X H，XIE Y，WANG H M，et al. Symptomatic intracranial hemorrhage after mechanical thrombectomy in Chinese ischemic stroke patients：the ASIAN score[J]. Stroke，2020，51（9）：2690-2696.