Skip to main content
Top
Published in: BMC Neurology 1/2023

Open Access 01-12-2023 | Cerebral Small Vessel Disease | Research

Effect of leukoaraiosis on collateral circulation in acute ischemic stroke treated with endovascular therapy: a meta-analysis

Authors: Wang Chen, Yijie Qin, Shuna Yang, Lei Yang, Yutong Hou, Wenli Hu

Published in: BMC Neurology | Issue 1/2023

Login to get access

Abstract

Background and objective

The recruitment of collateral circulation correlates with a balance of the microvasculature. Uncertainty remains to be made about the association of leukoaraiosis with leptomeningeal collaterals. To explore the effect of leukoaraiosis on leptomeningeal collaterals in patients treated with endovascular therapy.

Methods

Observational studies exploring the correlation between leukoaraiosis and leptomeningeal collaterals in large vessel occlusion treated with endovascular therapy were searched from PubMed, EMBASE, and Cochrane Libraries databases. Two independent reviewers retrieved eligible literature, extracted purpose-related data, and utilized the Newcastle–Ottawa Scale to evaluate the risk of bias. A Mantel–Haenszel method was used to calculate the odds ratio (OR). Meta-regression and subgroup analyses were conducted to clarify heterogeneity.

Results

Data from 10 studies with 1606 patients were extracted for pooled analysis. Compared to non-severe leukoaraiosis, patients with severe leukoaraiosis showed significant relevance to poor leptomeningeal collaterals (OR, 2.13; 95% confidence interval [1.27–3.57]; P = 0.004). Meta-regression indicated that sample size (coefficient = -0.007299, P = 0.035) and the number of female patients (coefficient = -0.0174709, P = 0.020) were sources of heterogeneity. Furthermore, all of the countries (USA versus France versus China, Q = 3.67, P = 0.159), various assessment scales of leukoaraiosis (the Fazekas scale versus Non-Fazekas scales, Q = 0.77, P = 0.379), and different imaging methods of leukoaraiosis (computed tomography versus magnetic resonance imaging, Q = 2.12, P = 0.146) and leptomeningeal collaterals (computed tomography angiography versus digital subtraction angiography, Q = 1.21, P = 0.271) showed no contribution to the effect size.

Conclusion

Severe leukoaraiosis is associated with poor leptomeningeal collaterals in patients treated with endovascular therapy. Further studies may focus on whether the finding applies to different stroke subtypes.
Appendix
Available only for authorised users
Literature
1.
go back to reference Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, 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. Stroke. 2019;50(12):e344–418.CrossRefPubMed Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, 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. Stroke. 2019;50(12):e344–418.CrossRefPubMed
2.
go back to reference Warach SJ, Luby M, Albers GW, Bammer R, Bivard A, Campbell BC, et al. Acute stroke imaging research roadmap iii imaging selection and outcomes in acute stroke reperfusion clinical trials: consensus recommendations and further research priorities. Stroke. 2016;47(5):1389–98.CrossRefPubMedPubMedCentral Warach SJ, Luby M, Albers GW, Bammer R, Bivard A, Campbell BC, et al. Acute stroke imaging research roadmap iii imaging selection and outcomes in acute stroke reperfusion clinical trials: consensus recommendations and further research priorities. Stroke. 2016;47(5):1389–98.CrossRefPubMedPubMedCentral
3.
go back to reference Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P, Parsons MW. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 2009;132(Pt 8):2231–8.CrossRefPubMed Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P, Parsons MW. The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 2009;132(Pt 8):2231–8.CrossRefPubMed
4.
go back to reference Garcia-Tornel A, Ciolli L, Rubiera M, Requena M, Muchada M, Pagola J, et al. Leptomeningeal Collateral Flow Modifies Endovascular Treatment Efficacy on Large-Vessel Occlusion Strokes. Stroke. 2021;52(1):299–303.CrossRefPubMed Garcia-Tornel A, Ciolli L, Rubiera M, Requena M, Muchada M, Pagola J, et al. Leptomeningeal Collateral Flow Modifies Endovascular Treatment Efficacy on Large-Vessel Occlusion Strokes. Stroke. 2021;52(1):299–303.CrossRefPubMed
5.
go back to reference Regenhardt RW, Gonzalez RG, He J, Lev MH, Singhal AB. Symmetric CTA Collaterals Identify Patients with Slow-progressing Stroke Likely to Benefit from Late Thrombectomy. Radiology. 2022;302(2):400–7.CrossRefPubMed Regenhardt RW, Gonzalez RG, He J, Lev MH, Singhal AB. Symmetric CTA Collaterals Identify Patients with Slow-progressing Stroke Likely to Benefit from Late Thrombectomy. Radiology. 2022;302(2):400–7.CrossRefPubMed
6.
go back to reference Roman LS, Menon BK, Blasco J, Hernandez-Perez M, Davalos A, Majoie C, et al. Imaging features and safety and efficacy of endovascular stroke treatment: a meta-analysis of individual patient-level data. Lancet Neurol. 2018;17(10):895–904.CrossRefPubMed Roman LS, Menon BK, Blasco J, Hernandez-Perez M, Davalos A, Majoie C, et al. Imaging features and safety and efficacy of endovascular stroke treatment: a meta-analysis of individual patient-level data. Lancet Neurol. 2018;17(10):895–904.CrossRefPubMed
7.
go back to reference Wiegers EJA, Mulder M, Jansen IGH, Venema E, Compagne KCJ, Berkhemer OA, et al. Clinical and Imaging Determinants of Collateral Status in Patients With Acute Ischemic Stroke in MR CLEAN Trial and Registry. Stroke. 2020;51(5):1493–502.CrossRefPubMed Wiegers EJA, Mulder M, Jansen IGH, Venema E, Compagne KCJ, Berkhemer OA, et al. Clinical and Imaging Determinants of Collateral Status in Patients With Acute Ischemic Stroke in MR CLEAN Trial and Registry. Stroke. 2020;51(5):1493–502.CrossRefPubMed
8.
go back to reference Nannoni S, Sirimarco G, Cereda CW, Lambrou D, Strambo D, Eskandari A, et al. Determining factors of better leptomeningeal collaterals: a study of 857 consecutive acute ischemic stroke patients. J Neurol. 2019;266(3):582–8.CrossRefPubMed Nannoni S, Sirimarco G, Cereda CW, Lambrou D, Strambo D, Eskandari A, et al. Determining factors of better leptomeningeal collaterals: a study of 857 consecutive acute ischemic stroke patients. J Neurol. 2019;266(3):582–8.CrossRefPubMed
9.
go back to reference Fujita K, Tanaka K, Yamagami H, Ide T, Ishiyama H, Sonoda K, et al. Detrimental effect of chronic hypertension on leptomeningeal collateral flow in acute ischemic stroke. Stroke. 2019;50(7):1751–7.CrossRefPubMed Fujita K, Tanaka K, Yamagami H, Ide T, Ishiyama H, Sonoda K, et al. Detrimental effect of chronic hypertension on leptomeningeal collateral flow in acute ischemic stroke. Stroke. 2019;50(7):1751–7.CrossRefPubMed
10.
go back to reference Chan SL, Sweet JG, Bishop N, Cipolla MJ. Pial collateral reactivity during hypertension and aging: understanding the function of collaterals for stroke therapy. Stroke. 2016;47(6):1618–25.CrossRefPubMedPubMedCentral Chan SL, Sweet JG, Bishop N, Cipolla MJ. Pial collateral reactivity during hypertension and aging: understanding the function of collaterals for stroke therapy. Stroke. 2016;47(6):1618–25.CrossRefPubMedPubMedCentral
11.
go back to reference Fernando MS, Simpson JE, Matthews F, Brayne C, Lewis CE, Barber R, et al. White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke. 2006;37(6):1391–8.CrossRefPubMed Fernando MS, Simpson JE, Matthews F, Brayne C, Lewis CE, Barber R, et al. White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke. 2006;37(6):1391–8.CrossRefPubMed
12.
go back to reference Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjogren M, et al. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32(6):1318–22.CrossRefPubMed Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjogren M, et al. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32(6):1318–22.CrossRefPubMed
13.
go back to reference Mark I, Seyedsaadat SM, Benson JC, Kallmes DF, Rabinstein AA, Brinjikji W. Leukoaraiosis and collateral blood flow in stroke patients with anterior circulation large vessel occlusion. J Neurointerv Surg. 2020;12(10):942–5.CrossRefPubMed Mark I, Seyedsaadat SM, Benson JC, Kallmes DF, Rabinstein AA, Brinjikji W. Leukoaraiosis and collateral blood flow in stroke patients with anterior circulation large vessel occlusion. J Neurointerv Surg. 2020;12(10):942–5.CrossRefPubMed
14.
go back to reference Lin MP, Brott TG, Liebeskind DS, Meschia JF, Sam K, Gottesman RF. Collateral recruitment is impaired by cerebral small vessel disease. Stroke. 2020;51(5):1404–10.CrossRefPubMed Lin MP, Brott TG, Liebeskind DS, Meschia JF, Sam K, Gottesman RF. Collateral recruitment is impaired by cerebral small vessel disease. Stroke. 2020;51(5):1404–10.CrossRefPubMed
15.
go back to reference Zhou JY, Shi YB, Xia C, Lu CQ, Tang TY, Lu T, et al. Beyond collaterals: brain frailty additionally improves prediction of clinical outcome in acute ischemic stroke. Eur Radiol. 2022;32(10):6943–52.CrossRefPubMed Zhou JY, Shi YB, Xia C, Lu CQ, Tang TY, Lu T, et al. Beyond collaterals: brain frailty additionally improves prediction of clinical outcome in acute ischemic stroke. Eur Radiol. 2022;32(10):6943–52.CrossRefPubMed
16.
go back to reference Hashimoto T, Kunieda T, Honda T, Scalzo F, Ali L, Hinman JD, et al. Reduced Leukoaraiosis, Noncardiac Embolic Stroke Etiology, and Shorter Thrombus Length Indicate Good Leptomeningeal Collateral Flow in Embolic Large-Vessel Occlusion. AJNR Am J Neuroradiol. 2022;43(1):63–9.CrossRefPubMedPubMedCentral Hashimoto T, Kunieda T, Honda T, Scalzo F, Ali L, Hinman JD, et al. Reduced Leukoaraiosis, Noncardiac Embolic Stroke Etiology, and Shorter Thrombus Length Indicate Good Leptomeningeal Collateral Flow in Embolic Large-Vessel Occlusion. AJNR Am J Neuroradiol. 2022;43(1):63–9.CrossRefPubMedPubMedCentral
17.
go back to reference Henninger N, Lin E, Baker SP, Wakhloo AK, Takhtani D, Moonis M. Leukoaraiosis predicts poor 90-day outcome after acute large cerebral artery occlusion. Cerebrovasc Dis. 2012;33(6):525–31.CrossRefPubMed Henninger N, Lin E, Baker SP, Wakhloo AK, Takhtani D, Moonis M. Leukoaraiosis predicts poor 90-day outcome after acute large cerebral artery occlusion. Cerebrovasc Dis. 2012;33(6):525–31.CrossRefPubMed
18.
go back to reference Eker OF, Rascle L, Cho TH, Mechtouff L, Derex L, Ong E, et al. Does small vessel disease burden impact collateral circulation in ischemic stroke treated by mechanical thrombectomy? Stroke. 2019;50(6):1582–5.CrossRefPubMed Eker OF, Rascle L, Cho TH, Mechtouff L, Derex L, Ong E, et al. Does small vessel disease burden impact collateral circulation in ischemic stroke treated by mechanical thrombectomy? Stroke. 2019;50(6):1582–5.CrossRefPubMed
19.
go back to reference Mutzenbach JS, Muller-Thies-Broussalis E, Killer-Oberpfalzer M, Griessenauer CJ, Hecker C, Moscote-Salazar LR, et al. severe leukoaraiosis is associated with poor outcome after successful recanalization of M1 middle cerebral artery occlusion strokes. Cerebrovasc Dis. 2020;49(3):253–61.CrossRefPubMed Mutzenbach JS, Muller-Thies-Broussalis E, Killer-Oberpfalzer M, Griessenauer CJ, Hecker C, Moscote-Salazar LR, et al. severe leukoaraiosis is associated with poor outcome after successful recanalization of M1 middle cerebral artery occlusion strokes. Cerebrovasc Dis. 2020;49(3):253–61.CrossRefPubMed
20.
go back to reference Mikati AG, Mandelbaum M, Sapnar S, Puri AS, Silver B, Goddeau RP Jr, et al. Impact of leukoaraiosis severity on the association of time to successful reperfusion with 90-day functional outcome after large vessel occlusion stroke. Transl Stroke Res. 2020;11(1):39–49.CrossRefPubMed Mikati AG, Mandelbaum M, Sapnar S, Puri AS, Silver B, Goddeau RP Jr, et al. Impact of leukoaraiosis severity on the association of time to successful reperfusion with 90-day functional outcome after large vessel occlusion stroke. Transl Stroke Res. 2020;11(1):39–49.CrossRefPubMed
21.
go back to reference Mechtouff L, Nighoghossian N, Amaz C, Buisson M, Berthezène Y, Derex L, et al. White matter burden does not influence the outcome of mechanical thrombectomy. J Neurol. 2020;267(3):618–24.CrossRefPubMed Mechtouff L, Nighoghossian N, Amaz C, Buisson M, Berthezène Y, Derex L, et al. White matter burden does not influence the outcome of mechanical thrombectomy. J Neurol. 2020;267(3):618–24.CrossRefPubMed
22.
go back to reference Forestier G, Agbonon R, Bricout N, Benhassen W, Turc G, Bretzner M, et al. Small vessel disease and collaterals in ischemic stroke patients treated with thrombectomy. J Neurol. 2022;269(9):4708–16.CrossRefPubMed Forestier G, Agbonon R, Bricout N, Benhassen W, Turc G, Bretzner M, et al. Small vessel disease and collaterals in ischemic stroke patients treated with thrombectomy. J Neurol. 2022;269(9):4708–16.CrossRefPubMed
23.
go back to reference Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372: n71.CrossRefPubMedPubMedCentral Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372: n71.CrossRefPubMedPubMedCentral
25.
go back to reference Raz L. Estrogen and cerebrovascular regulation in menopause. Mol Cell Endocrinol. 2014;389(1–2):22–30.CrossRefPubMed Raz L. Estrogen and cerebrovascular regulation in menopause. Mol Cell Endocrinol. 2014;389(1–2):22–30.CrossRefPubMed
26.
go back to reference Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57(2):173–85.CrossRefPubMed Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57(2):173–85.CrossRefPubMed
27.
go back to reference Xu M, Guo W, Rascle L, Mechtouff L, Nighoghossian N, Eker O, et al. Leukoaraiosis distribution and cerebral collaterals: a systematic review and meta-analysis. Front Neurol. 2022;13:869329.CrossRefPubMedPubMedCentral Xu M, Guo W, Rascle L, Mechtouff L, Nighoghossian N, Eker O, et al. Leukoaraiosis distribution and cerebral collaterals: a systematic review and meta-analysis. Front Neurol. 2022;13:869329.CrossRefPubMedPubMedCentral
28.
go back to reference Wang Y, Zhao X, Liu L, Soo YO, Pu Y, Pan Y, et al. Prevalence and outcomes of symptomatic intracranial large artery stenoses and occlusions in China: the Chinese Intracranial Atherosclerosis (CICAS) Study. Stroke. 2014;45(3):663–9.CrossRefPubMed Wang Y, Zhao X, Liu L, Soo YO, Pu Y, Pan Y, et al. Prevalence and outcomes of symptomatic intracranial large artery stenoses and occlusions in China: the Chinese Intracranial Atherosclerosis (CICAS) Study. Stroke. 2014;45(3):663–9.CrossRefPubMed
29.
go back to reference Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM, 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, Dippel DW, Mitchell PJ, Demchuk AM, 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
30.
go back to reference Rebello LC, Bouslama M, Haussen DC, Grossberg JA, Dehkharghani S, Anderson A, et al. Stroke etiology and collaterals: atheroembolic strokes have greater collateral recruitment than cardioembolic strokes. Eur J Neurol. 2017;24(6):762–7.CrossRefPubMed Rebello LC, Bouslama M, Haussen DC, Grossberg JA, Dehkharghani S, Anderson A, et al. Stroke etiology and collaterals: atheroembolic strokes have greater collateral recruitment than cardioembolic strokes. Eur J Neurol. 2017;24(6):762–7.CrossRefPubMed
31.
go back to reference Hassler E, Kneihsl M, Deutschmann H, Hinteregger N, Magyar M, Wiesspeiner U, et al. Relationship between stroke etiology and collateral status in anterior circulation large vessel occlusion. J Neurol. 2020;267(11):3362–70.CrossRefPubMedPubMedCentral Hassler E, Kneihsl M, Deutschmann H, Hinteregger N, Magyar M, Wiesspeiner U, et al. Relationship between stroke etiology and collateral status in anterior circulation large vessel occlusion. J Neurol. 2020;267(11):3362–70.CrossRefPubMedPubMedCentral
32.
go back to reference Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6.CrossRefPubMed Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6.CrossRefPubMed
33.
go back to reference van Swieten JC, Hijdra A, Koudstaal PJ, van Gijn J. Grading white matter lesions on CT and MRI: a simple scale. J Neurol Neurosurg Psychiatry. 1990;53(12):1080–3.CrossRefPubMedPubMedCentral van Swieten JC, Hijdra A, Koudstaal PJ, van Gijn J. Grading white matter lesions on CT and MRI: a simple scale. J Neurol Neurosurg Psychiatry. 1990;53(12):1080–3.CrossRefPubMedPubMedCentral
34.
go back to reference Fazekas F, Barkhof F, Wahlund LO, Pantoni L, Erkinjuntti T, Scheltens P, et al. CT and MRI rating of white matter lesions. Cerebrovasc Dis. 2002;13(Suppl 2):31–6.CrossRefPubMed Fazekas F, Barkhof F, Wahlund LO, Pantoni L, Erkinjuntti T, Scheltens P, et al. CT and MRI rating of white matter lesions. Cerebrovasc Dis. 2002;13(Suppl 2):31–6.CrossRefPubMed
35.
go back to reference Kapeller P, Barber R, Vermeulen RJ, Ader H, Scheltens P, Freidl W, et al. Visual rating of age-related white matter changes on magnetic resonance imaging: scale comparison, interrater agreement, and correlations with quantitative measurements. Stroke. 2003;34(2):441–5.CrossRefPubMed Kapeller P, Barber R, Vermeulen RJ, Ader H, Scheltens P, Freidl W, et al. Visual rating of age-related white matter changes on magnetic resonance imaging: scale comparison, interrater agreement, and correlations with quantitative measurements. Stroke. 2003;34(2):441–5.CrossRefPubMed
36.
go back to reference Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.CrossRefPubMed Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.CrossRefPubMed
37.
go back to reference Ma Y, Song A, Viswanathan A, Blacker D, Vernooij MW, Hofman A, et al. Blood Pressure Variability and Cerebral Small Vessel Disease: A Systematic Review and Meta-Analysis of Population-Based Cohorts. Stroke. 2020;51(1):82–9.CrossRefPubMed Ma Y, Song A, Viswanathan A, Blacker D, Vernooij MW, Hofman A, et al. Blood Pressure Variability and Cerebral Small Vessel Disease: A Systematic Review and Meta-Analysis of Population-Based Cohorts. Stroke. 2020;51(1):82–9.CrossRefPubMed
38.
go back to reference van Harten B, Oosterman JM, Potter van Loon BJ, Scheltens P, Weinstein HC. Brain lesions on MRI in elderly patients with type 2 diabetes mellitus. Eur Neurol. 2007;57(2):70–4.CrossRefPubMed van Harten B, Oosterman JM, Potter van Loon BJ, Scheltens P, Weinstein HC. Brain lesions on MRI in elderly patients with type 2 diabetes mellitus. Eur Neurol. 2007;57(2):70–4.CrossRefPubMed
39.
go back to reference Arntz RM, van den Broek SM, van Uden IW, Ghafoorian M, Platel B, Rutten-Jacobs LC, et al. Accelerated development of cerebral small vessel disease in young stroke patients. Neurology. 2016;87(12):1212–9.CrossRefPubMedPubMedCentral Arntz RM, van den Broek SM, van Uden IW, Ghafoorian M, Platel B, Rutten-Jacobs LC, et al. Accelerated development of cerebral small vessel disease in young stroke patients. Neurology. 2016;87(12):1212–9.CrossRefPubMedPubMedCentral
40.
go back to reference Chen D, Yin Y, Shi J, Yang F, Wang K, Zhao F, et al. DL-3-n-butylphthalide improves cerebral hypoperfusion in patients with large cerebral atherosclerotic stenosis: a single-center, randomized, double-blind, placebo-controlled study. BMC Neurol. 2020;20(1):212.CrossRefPubMedPubMedCentral Chen D, Yin Y, Shi J, Yang F, Wang K, Zhao F, et al. DL-3-n-butylphthalide improves cerebral hypoperfusion in patients with large cerebral atherosclerotic stenosis: a single-center, randomized, double-blind, placebo-controlled study. BMC Neurol. 2020;20(1):212.CrossRefPubMedPubMedCentral
41.
go back to reference Han QY, Zhang H, Zhang X, He DS, Wang SW, Cao X, et al. dl-3-n-butylphthalide preserves white matter integrity and alleviates cognitive impairment in mice with chronic cerebral hypoperfusion. CNS Neurosci Ther. 2019;25(9):1042–53.CrossRefPubMedPubMedCentral Han QY, Zhang H, Zhang X, He DS, Wang SW, Cao X, et al. dl-3-n-butylphthalide preserves white matter integrity and alleviates cognitive impairment in mice with chronic cerebral hypoperfusion. CNS Neurosci Ther. 2019;25(9):1042–53.CrossRefPubMedPubMedCentral
Metadata
Title
Effect of leukoaraiosis on collateral circulation in acute ischemic stroke treated with endovascular therapy: a meta-analysis
Authors
Wang Chen
Yijie Qin
Shuna Yang
Lei Yang
Yutong Hou
Wenli Hu
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2023
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-023-03266-8

Other articles of this Issue 1/2023

BMC Neurology 1/2023 Go to the issue