Keywords
Acute large vessel occlusion ischemic stroke
After endovascular thrombectomy
Hemorrhagic transformation
Published : 2026-08-05
Abstract
With the intensification of population aging and the rapid development of neuroimaging, cerebral small vessel disease (CSVD) has garnered increasing attention. Endovascular thrombectomy (EVT) can significantly improve functional outcomes in patients with intracranial large vessel occlusion and has become the standard treatment for acute large vessel occlusion ischemic stroke. Numerous studies suggest that pre-existing CSVD before acute ischemic stroke may increase the risk of hemorrhagic transformation (HT) after EVT, yet results remain controversial. This article primarily discusses the impact of different subtypes of CSVD and the total burden on magnetic resonance imaging on HT after EVT in patients with acute large vessel occlusion ischemic stroke, aiming to provide a clinical reference.
References
Paul S, Candelario-Jalil E, 2021, Emerging Neuroprotective Strategies for the Treatment of Ischemic Stroke: An Overview of Clinical and Preclinical Studies. Experimental Neurology, 2021(335): 113518.
Report on Stroke Center in China Writing Group, 2024, Summary of the “China Stroke Center Report 2022”. Chinese Journal of Cerebrovascular Diseases, 21(8): 565–576.
Huo XC, Gao F, 2023, Chinese Guidelines for Endovascular Treatment of Acute Ischemic Stroke 2023. Chinese Stroke Journal, 18(6): 684–711.
Nogueira RG, Jadhav AP, Haussen DC, et al., 2018, DAWN Trial Investigators. Thrombectomy 6 to 24 Hours after Stroke with a Mismatch between Deficit and Infarct. The New England Journal of Medicine, 378(1): 11–21.
Albers GW, Marks MP, Kemp S, et al., 2018, DEFUSE 3 Investigators. Thrombectomy for Stroke at 6 to 16 Hours with Selection by Perfusion Imaging. The New England Journal of Medicine, 378(8): 708–718.
Duarte AR, Vilela P, 2020, Acute Ischemic Stroke Hemorrhagic Transformation at Angiography before Mechanical Thrombectomy: A Neurointerventional Dilemma. Clinical Neuroradiology, 2020(30): 875–878.
Li W, Xing X, Wen C, et al., 2023, Risk Factors and Functional Outcome were Associated with Hemorrhagic Transformation after Mechanical Thrombectomy for Acute Large Vessel Occlusion Stroke. Journal of Neurosurgical Sciences, 67(5): 585–590.
Hu WL, Yang L, Li XT, et al., 2021, Chinese Expert Consensus on the Diagnosis and Treatment of Cerebral Small Vessel Diseases 2021. Chinese Stroke Journal, 16(7): 716–726.
Pang J, Zhang JH, Jiang Y, 2019, Delayed Recanalization in Acute Ischemic Stroke Patients: Late is Better than Never? Journal of Cerebral Blood Flow & Metabolism, 39(12): 2536–2538.
Hooper D, Nisar T, McCane D, et al., 2021, Severe Cerebral Small Vessel Disease Burden is Associated with Poor Outcomes after Endovascular Thrombectomy in Acute Ischemic Stroke with Large Vessel Occlusion. Cureus, 13(2): e13122.
Duan YX, Zhao Y, Pei HL, et al., 2021, Cerebral Small Vessel Disease and Outcomes After Endovascular Thrombectomy in Patients with Acute Ischemic Stroke. International Journal of Cerebrovascular Diseases, 29(8): 602–607.
von Kummer R, Broderick JP, Campbell BC, et al., 2015, The Heidelberg Bleeding Classification: Classification of Bleeding Events After Ischemic Stroke and Reperfusion Therapy. Stroke, 46(10): 2981–2986.
Martins SO, Mont’Alverne F, Rebello LC, et al., 2020, Thrombectomy for Stroke in the Public Health Care System of Brazil. The New England Journal of Medicine, 382(24): 2316–2326.
Zi W, Wang H, Yang D, et al., 2017, Clinical Effectiveness and Safety Outcomes of Endovascular Treatment for Acute Anterior Circulation Ischemic Stroke in China. Cerebrovascular Disease, 44(5–6): 248–258.
vander Steen W, van der Ende NAM, Luijten SPR, et al., 2023, MR CLEAN-NO IV, MR CLEAN-MED, and CONTRAST investigators. Type of Intracranial Hemorrhage after Endovascular Stroke Treatment: Association with Functional Outcome. Journal of NeuroInterventional Surgery, 15(10): 971–976.
Jovin TG, Nogueira RG, Lansberg MG, et al., 2022, Thrombectomy for Anterior Circulation Stroke beyond 6 h from Time last Known Well (AURORA): A Systematic Review and Individual Patient Data Meta-analysis. Lancet, 399(10321): 249–258.
Neurology Branch of the Chinese Medical Association, Cerebrovascular Disease Group of the Neurology Branch of the Chinese Medical Association, 2019, Chinese Expert Consensus on the Diagnosis and Treatment of Hemorrhagic Transformation after Acute Cerebral Infarction 2019. Chinese Journal of Neurology, 52(4): 252–265.
Jurcau A, Ardelean AI, 2022, Oxidative Stress in Ischemia/Reperfusion Injuries following Acute Ischemic Stroke. Biomedicines, 10(3): 574.
Candelario-Jalil E, Dijkhuizen RM, Magnus T, 2022, Neuroinflammation, Stroke, Blood-Brain Barrier Dysfunction, and Imaging Modalities. Stroke, 53(5): 1473–1486.
Zhang X, Xie Y, Wang H, et al., 2020, Symptomatic Intracranial Hemorrhage After Mechanical Thrombectomy in Chinese Ischemic Stroke Patients: The ASIAN Score. Stroke, 51(9): 2690–2696.
Wardlaw JM, Smith C, Dichgans M, 2019, Small Vessel Disease: Mechanisms and Clinical Implications. Lancet Neurology, 18(7): 684–696.
Wardlaw JM, Smith EE, Biessels GJ, et al., 2013, Standards for Reporting Vascular Changes on Neuroimaging (STRIVE v1). Neuroimaging Standards for Research into Small Vessel Disease and its Contribution to Ageing and neurodegeneration. Lancet Neurology, 12(8): 822–838.
Duering M, Biessels GJ, Brodtmann A, et al., 2023, Neuroimaging Standards for Research into Small Vessel Disease-advances since 2013. Lancet Neurology, 22(7): 602–618.
Gao Z, Wang W, Wang Z, et al., 2014, Cerebral Microbleeds are Associated with Deep White Matter Hyperintensities, but only in Hypertensive Patients. PLoS One, 9(3): e91637.
Zhu YC, Tzourio C, Soumaré A, et al., 2010, Severity of Dilated Virchow-Robin Spaces is Associated with Age, Blood Pressure, and MRI Markers of Small Vessel Disease: A Population-based Study. Stroke, 41(11): 2483–2490.
Staals J, Makin SD, Doubal FN, et al., 2014, Stroke Subtype, Vascular Risk Factors, and Total MRI Brain Small-vessel Disease Burden. Neurology, 83(14): 1228–1234.
Debette S, Schilling S, Duperron MG, et al., 2019, Clinical Significance of Magnetic Resonance Imaging Markers of Vascular Brain Injury: A Systematic Review and Meta-analysis. JAMA Neurology, 76(1): 81–94.
Yang YY, Wang YJ, Wang YL, 2019, Research Progress on the Relationship Between Cerebral Small Vessel Disease and Intracranial Large Artery Disease. Chinese Stroke Journal, 14(11): 1135–1139.
Kwon HM, Lynn MJ, Turan TN, et al., 2016, SAMMPRIS Investigators. Frequency, Risk Factors, and Outcome of Coexistent Small Vessel Disease and Intracranial Arterial Stenosis: Results From the Stenting and Aggressive Medical Management for Preventing Recurrent Stroke in Intracranial Stenosis (SAMMPRIS) Trial. JAMA Neurology, 73(1): 36–42.
Hori S, Hori E, Shibata T, et al., 2019, Correlation Between Cerebral Microbleeds and Vulnerable Plaque in Patients with Severe Carotid Artery Stenosis; Comparative Magnetic Resonance Imaging Study. Journal of Stroke and Cerebrovascular Diseases, 28(10): 104300.
Lu T, Liang J, Wei N, et al., Extracranial Artery Stenosis is Associated with Total MRI Burden of Cerebral Small Vessel Disease in Ischemic Stroke Patients of Suspected Small or Large Artery Origins. Frontiers in Neurology, 2019(10): 243.
Sun Z, Gao C, Gao D, et al., 2021, Reduction in Pericyte Coverage Leads to Blood-brain Barrier Dysfunction via Endothelial Transcytosis Following Chronic Cerebral Hypoperfusion. Fluids and Barriers of the CNS, 18(1): 21.
Kerkhofs D, Wong SM, Zhang E, et al., 2021, Blood-brain Barrier Leakage at Baseline and Cognitive Decline in Cerebral Small Vessel Disease: A 2-Year Follow-Up Study. Geroscience, 43(4): 1643–1652.
Huo YC, Li Q, Zhang WY, et al., 2019, Total Small Vessel Disease Burden Predicts Functional Outcome in Patients with Acute Ischemic Stroke. Frontiers in Neurology, 2019(10): 808.
Zhang J, Puri AS, Khan MA, et al., 2014, Leukoaraiosis Predicts a Poor 90-day Outcome after Endovascular Stroke Therapy. American Journal of Neuroradiology, 35(11): 2070–2075.
Fladt J, Kronlage C, De Marchis GM, 2018, Cerebral White Matter Hyperintensities and Microbleeds in Acute Ischemic Stroke: Impact on Recanalization Therapies. A Review of the Literature. Neuroscience Letters, 2018(687): 55–64.
Eilaghi A, Brooks J, d’Esterre C, et al., 2013, Reperfusion is a Stronger Predictor of Good Clinical Outcome Than Recanalization in Ischemic Stroke. Radiology, 269(1): 240–248.
Kumral E, Güllüoğlu H, Alakbarova N, et al., 2015, Cognitive Decline in Patients with Leukoaraiosis within 5 Years after Initial Stroke. Journal of Stroke and Cerebrovascular Diseases, 24(10): 2338–2347.
Deng G, Xiao J, Yu H, et al., 2022, Predictors of Futile Recanalization after Endovascular Treatment in Acute Ischemic Stroke: A Meta-analysis. Journal of NeuroInterventional Surgery, 14(9): 881–885.
Demchuk AM, Khan F, Hill MD, et al., 2008, Importance of Leukoaraiosis on CT for Tissue Plasminogen Activator Decision Making: Evaluation of the NINDS rt-PA Stroke Study. Cerebrovascular Disease, 26(2): 120–125.
Kongbunkiat K, Wilson D, Kasemsap N, et al., 2017, Leukoaraiosis, Intracerebral Hemorrhage, and Functional Outcomes after Thrombolysis for Acute Stroke. Neurology, 88(7): 638–645.
Uniken Venema SM, Postma AA, van den Wijngaard IR, et al., 2021, White Matter Lesions and Outcomes after Endovascular Treatment for Acute Ischemic Stroke: Results from the MR CLEAN Registry. Stroke, 52(9): 2849–2857.
Xu T, Wang Y, Yuan J, et al., 2021, The Burden of Small Vessel Disease and Outcomes of Mechanical Thrombectomy in Ischemic Stroke: A Systematic Review and Meta-analysis. Frontiers in Neurology, 2021(12): 602037.
Neumann-Haefelin T, Hoelig S, Berkefeld J, et al., 2006, Leukoaraiosis is a Risk Factor for Symptomatic Intracerebral Hemorrhage after Thrombolysis for Acute Stroke. Stroke, 37(10): 2463–2466.
Guo Y, Zhang S, Li M, et al., 2020, Leukoaraiosis and Early Neurological Outcomes after Mechanical Thrombectomy in Acute Ischemic Stroke. Journal of Neuroradiology, 47(6): 428–432.
Huo L, Chen P, Wang Z, et al., The Impact of Leukoaraiosis Severity on the Outcomes of Mechanical Thrombectomy for Acute Ischemic Stroke: A Systematic Review and Meta-analysis. Journal of Neuroradiology, 268(11): 4108–4116.
Henninger N, Lin E, Haussen DC, et al., 2013, Leukoaraiosis and Sex Predict the Hyperacute Ischemic Core Volume. Stroke, 44(1): 61–67.
Xu H, Stamova B, Jickling G, et al., 2010, Distinctive RNA Expression Profiles in Blood Associated with White Matter Hyperintensities in the Brain. Stroke, 41(12): 2744–2749.
Warach S, Latour LL, 2004, Evidence of Reperfusion Injury, Exacerbated by Thrombolytic Therapy, in Human Focal Brain Ischemia using a Novel Imaging Marker of Early Blood-brain Barrier Disruption. Stroke, 35(11 Suppl 1): 2659–2661.
Chen B, Friedman B, Cheng Q, et al., 2009, Severe Blood-Brain Barrier Disruption and Surrounding Tissue Injury. Stroke, 40(12): e666–e674.
Shi ZS, Loh Y, Liebeskind DS, et al., 2012, Leukoaraiosis Predicts Parenchymal Hematoma after Mechanical Thrombectomy in Acute Ischemic Stroke. Stroke, 43(7): 1806–1811.
Choi KH, Kim JH, Kang KW, et al., 2019, Impact of Microbleeds on Outcomes Following Recanalization in Patients with Acute Ischemic Stroke. Stroke, 50(1): 127–134.
Charidimou A, Kakar P, Fox Z, et al., 2013, Cerebral Microbleeds and Recurrent Stroke Risk: A Systematic Review and Meta-Analysis of Prospective Ischemic Stroke and Transient Ischemic Attack Cohorts. Stroke, 44(4): 995–1001.
Graff-Radford J, Simino J, Kantarci K, et al., 2017, Neuroimaging Correlates of Cerebral Microbleeds: The ARIC Study (Atherosclerosis Risk in Communities). Stroke, 48(11): 2964–2972.
Romero JR, Preis SR, Beiser A, et al., Risk Factors, Stroke Prevention Treatments, and Prevalence of Cerebral Microbleeds in the Framingham Heart Study. Stroke, 45(5): 1492–1494.
Cordonnier C, Al-Shahi Salman R, Wardlaw J, 2007, Spontaneous Brain Microbleeds: Systematic Review, Subgroup Analyses, and Standards for Study Design and Reporting. Brain, 130(Pt 8): 1988–2003.
Greenberg SM, Vernooij MW, Cordonnier C, et al., 2009, Cerebral microbleeds: A Guide to Detection and Interpretation. Lancet Neurology, 8(2): 165–174.
Shoamanesh A, Kwok CS, Lim PA, et al., 2013, Risk of Postthrombolysis Intracranial Hemorrhage in Acute Stroke Patients with Cerebral Microbleeds: A Systematic Review and Meta-analysis. International Journal of Stroke, 8(5): 348–356.
Shi ZS, Duckwiler GR, Jahan R, et al., 2016, Mechanical Thrombectomy for Acute Ischemic Stroke with Cerebral Microbleeds. Journal of NeuroInterventional Surgery, 8(6): 563–567.
Brown R, Benveniste H, Black SE, et al., 2018, Understanding the Role of the Perivascular Space in Cerebral Small Vessel Disease. Cardiovascular Research, 114(11): 1462–1473.
Chen X, Wang J, Shan Y, et al., 2019, Cerebral Small Vessel Disease: Neuroimaging Markers and Clinical Implications. Journal of Neurology, 266(10): 2347–2362.
Jungreis CA, Kanal E, Hirsch WL, et al., 1988, Normal Perivascular Spaces Mimicking Lacunar Infarction: MR Imaging. Radiology, 169(1): 101–104.
Wang X, Feng H, Wang Y, et al., 2019, Enlarged Perivascular Spaces and Cerebral Small Vessel Disease in Patients with Spontaneous Intracerebral Hemorrhage. Frontiers in Neurology, 14(10): 881.
Liang Y, Chan YL, Deng M, et al., 2018, Enlarged Perivascular Spaces in the Centrum Semiovale are Associated with Poststroke Depression: A 3-month Prospective study. Journal of Affective Disorders, 2018(228): 166–172.
Liang Y, Deng M, Chen YK, et al., 2017, Enlarged Perivascular Spaces are Associated with Health-related Quality of Life in Patients with Acute Ischemic Stroke. CNS Neuroscience & Therapeutics, 23(12): 973–979.
Best JG, Barbato C, Ambler G, et al., 2020, Association of Enlarged Perivascular Spaces and Anticoagulant-related Intracranial Hemorrhage. Neurology, 95(16) :e2192–e2199.
Lau KK, Li L, Lovelock CE, et al., 2017, Clinical Correlates, Ethnic Differences, and Prognostic Implications of Perivascular Spaces in Transient Ischemic Attack and Ischemic Stroke. Stroke, 48(6): 1470–1477.
Charidimou A, Boulouis G, Pasi M, et al., 2017, MRI-visible Perivascular Spaces in Cerebral Amyloid Angiopathy and Hypertensive Arteriopathy. Neurology, 88(12): 1157–1164.
Song Q, Cheng Y, Wang Y, et al., 2021, Enlarged Perivascular Spaces and Hemorrhagic Transformation after Acute Ischemic Stroke. Annals of Translational Medicine, 9(14): 1126.
Ding J, Sigurðsson S, Jónsson PV, et al., 2017, Large Perivascular Spaces Visible on Magnetic Resonance Imaging, Progression of Cerebral Small Vessel Disease, and Risk of Dementia: The Age, Gene/Environment Susceptibility-Reykjavik Study. JAMA Neurology, 74(9): 1105–1112.
ST-3 Collaborative Group, 2015, Association between Brain Imaging Signs, Early and Late Outcomes, and Response to Intravenous Alteplase after Acute Ischaemic Stroke in the Third International Stroke Trial (IST-3): Secondary Analysis of a Randomised Controlled Trial. Lancet Neurology, 14(5): 485–496.
Sillanpää N, Pienimäki JP, Protto S, et al., 2018, Chronic Infarcts Predict Poor Clinical Outcomes in Mechanical Thrombectomy for Patients Aged Sixty and above. Journal of Stroke and Cerebrovascular Diseases, 27(7): 1789–1795.
Arba F, Testa GD, Limbucci N, et al., 2019, Small Vessel Disease and Clinical Outcomes after Endovascular Treatment in Acute Ischemic Stroke. Neurological Sciences, 40(6): 1227–1235.
Wang Y, Yan X, Zhan J, et al., 2021, Neuroimaging Markers of Cerebral Small Vessel Disease and their Impact on Hemorrhagic Transformation and Functional Outcomes after Intravenous Thrombolysis in Patients with Acute Ischemic Stroke: A Systematic Review and Meta-analysis. Frontiers in Aging Neuroscience, 2021(13): 692942.
Sohn JH, Kim Y, Kim C, et al., 2023, Effect of Cerebral Small Vessel Disease Burden on Infarct Growth Rate and Stroke Outcomes in Large Vessel Occlusion Stroke Receiving Endovascular Treatment. Biomedicines, 11(11): 3102.
Ter Telgte A, van Leijsen EMC, Wiegertjes K, et al., 2018, Cerebral Small Vessel Disease: From A Focal to a Global Perspective. Nature Reviews Neurology, 14(7): 387–398.
Backhouse EV, McHutchison CA, et al., 2017, Early Life Risk Factors for Cerebrovascular Disease: A Systematic Review and Meta-analysis. Neurology, 88(10): 976–984.
Wu X, Yan J, Ye H, et al., 2020, Pre-treatment Cerebral Microbleeds and Intracranial Hemorrhage in Patients with Ischemic Stroke Receiving Endovascular Therapy: A Systematic Review and Meta-analysis. Journal of Neurology, 267(5): 1227–1232.