Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis

Andreas Charidimou; Toshio Imaizumi; Solene Moulin; Alexandro Biffi; Neshika Samarasekera; Yusuke Yakushiji; Andre Peeters; Yves Vandermeeren; Patrice Laloux; Jean Claude Baron; Mar Hernandez-Guillamon; Joan Montaner; Barbara Casolla; Simone M. Gregoire; Dong Wha Kang; Jong S. Kim; H. Naka; Eric E. Smith; Anand Viswanathan; Hans R. Jäger; Rustam Al-Shahi Salman; Steven M. Greenberg; Charlotte Cordonnier; David J. Werring

doi:10.1212/WNL.0000000000004259

Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis

Andreas Charidimou, Toshio Imaizumi, Solene Moulin, Alexandro Biffi, Neshika Samarasekera, Yusuke Yakushiji, Andre Peeters, Yves Vandermeeren, Patrice Laloux, Jean Claude Baron, Mar Hernandez-Guillamon, Joan Montaner, Barbara Casolla, Simone M. Gregoire, Dong Wha Kang, Jong S. Kim, H. Naka, Eric E. Smith, Anand Viswanathan, Hans R. JägerRustam Al-Shahi Salman, Steven M. Greenberg, Charlotte Cordonnier, David J. Werring

Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

Résumé

Objective: We evaluated recurrent intracerebral hemorrhage (ICH) risk in ICH survivors, stratified by the presence, distribution, and number of cerebral microbleeds (CMBs) on MRI (i.e., the presumed causal underlying small vessel disease and its severity). Methods: This was a meta-analysis of prospective cohorts following ICH, with blood-sensitive brain MRI soon after ICH. We estimated annualized recurrent symptomatic ICH rates for each study and compared pooled odds ratios (ORs) of recurrent ICH by CMB presence/absence and presumed etiology based on CMB distribution (strictly lobar CMBs related to probable or possible cerebral amyloid angiopathy [CAA] vs non-CAA) and burden (1, 2-4, 5-10, and >10 CMBs), using random effects models. Results: We pooled data from 10 studies including 1,306 patients: 325 with CAA-related and 981 CAA-unrelated ICH. The annual recurrent ICH risk was higher in CAA-related ICH vs CAA-unrelated ICH (7.4%, 95% confidence interval [CI] 3.2-12.6 vs 1.1%, 95% CI 0.5-1.7 per year, respectively; p = 0.01). In CAA-related ICH, multiple baseline CMBs (versus none) were associated with ICH recurrence during follow-up (range 1-3 years): OR 3.1 (95% CI 1.4-6.8; p = 0.006), 4.3 (95% CI 1.8-10.3; p = 0.001), and 3.4 (95% CI 1.4-8.3; p = 0.007) for 2-4, 5-10, and >10 CMBs, respectively. In CAA-unrelated ICH, only >10 CMBs (versus none) were associated with recurrent ICH (OR 5.6, 95% CI 2.1-15; p = 0.001). The presence of 1 CMB (versus none) was not associated with recurrent ICH in CAA-related or CAA-unrelated cohorts. Conclusions: CMB burden and distribution on MRI identify subgroups of ICH survivors with higher ICH recurrence risk, which may help to predict ICH prognosis with relevance for clinical practice and treatment trials.

langue originale	Anglais
Pages (de - à)	820-829
Nombre de pages	10
journal	Neurology
Volume	89
Numéro de publication	8
Les DOIs	https://doi.org/10.1212/WNL.0000000000004259
Etat de la publication	Publié - 22 août 2017
Modification externe	Oui

Financement

C.C. is a member of the Institut Universitaire de France. Supported by The Greek State Scholarship Foundation, Stroke Association, and British Heart Foundation (A.C.); The Department of Health/Higher Education Funding Council for England, Stroke Association, British Heart Foundation, and Rosetrees Trust (D.J.W.); Medical Research Council senior clinical fellowship (R.A.-S.S.); and Medical Research Council/The Stroke Association clinical research training fellowship (N.S.). From the Stroke Research Centre (A.C., Y.Y., S.M.G., H.R.J., D.J.W.), Department of Brain Repair and Rehabilitation, UCL Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UK; Hemorrhagic Stroke Research Program, Department of Neurology (A.C., A.B., E.E.S., A.V., S.M.G.), Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurosurgery (T.I.), Kushiro City General Hospital, Hokkaido, Japan; Degenerative & Vascular Cognitive Disorders (S.M., B.C., C.C.), Univ Lille, Inserm, CHU Lille, France; Centre for Clinical Brain Sciences (N.S., R.A.-S.S.), University of Edinburgh, UK; Department of Neurology (A.P.), Cliniques Universitaires UCL Saint Luc; Department of Neurology (Y.V., P.L.), CHU Dinant Godinne, Université Catholique de Louvain; Institute of Neuroscience (Y.V., P.L.), Université Catholique de Louvain, Brussels, Belgium; Department of Clinical Neurosciences (J.-C.B.), University of Cambridge, Addenbrooke’s Hospital, UK; UMR 894 INSERM-Université Paris 5 (J.-C.B.), Sorbonne Paris Cité, Paris, France; Department of Neurology (M.H.-G., J.M.), Hospital Vall d’Hebron, Vall d’Hebron Research Institute, Universitat Autònoma de Barcelona, Spain; Department of Neurology (D.-W.K., J.S.K.), Asan Medical Center, University of Ulsan College of Medicine, Seoul, South Korea; Department of Neurology (H.N.), Hiroshima Prefectural Hospital, Japan; and Hotchkiss Brain Institute (E.E.S.), University of Calgary, Canada. Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article. The Article Processing Charge was funded by RCUK. This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Bailleurs de fonds	Numéro du bailleur de fonds
Department of Health and Social Care
Rosetrees Trust
Stroke Association
Higher Education Funding Council for England
British Heart Foundation
Medical Research Council/The Stroke Association
Greek State Scholarship Foundation
Research Councils UK
UK Research and Innovation
Medical Research Council	G0900428, G1002605
National Institute on Aging (NIA)	R01AG047975

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10.1212/WNL.0000000000004259

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Charidimou, A., Imaizumi, T., Moulin, S., Biffi, A., Samarasekera, N., Yakushiji, Y., Peeters, A., Vandermeeren, Y., Laloux, P., Baron, J. C., Hernandez-Guillamon, M., Montaner, J., Casolla, B., Gregoire, S. M., Kang, D. W., Kim, J. S., Naka, H., Smith, E. E., Viswanathan, A., ... Werring, D. J. (2017). Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis. Neurology, 89(8), 820-829. https://doi.org/10.1212/WNL.0000000000004259

@article{bb25fe718e0c443bb997af5da7a8c953,

title = "Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis",

abstract = "Objective: We evaluated recurrent intracerebral hemorrhage (ICH) risk in ICH survivors, stratified by the presence, distribution, and number of cerebral microbleeds (CMBs) on MRI (i.e., the presumed causal underlying small vessel disease and its severity). Methods: This was a meta-analysis of prospective cohorts following ICH, with blood-sensitive brain MRI soon after ICH. We estimated annualized recurrent symptomatic ICH rates for each study and compared pooled odds ratios (ORs) of recurrent ICH by CMB presence/absence and presumed etiology based on CMB distribution (strictly lobar CMBs related to probable or possible cerebral amyloid angiopathy [CAA] vs non-CAA) and burden (1, 2-4, 5-10, and >10 CMBs), using random effects models. Results: We pooled data from 10 studies including 1,306 patients: 325 with CAA-related and 981 CAA-unrelated ICH. The annual recurrent ICH risk was higher in CAA-related ICH vs CAA-unrelated ICH (7.4\%, 95\% confidence interval [CI] 3.2-12.6 vs 1.1\%, 95\% CI 0.5-1.7 per year, respectively; p = 0.01). In CAA-related ICH, multiple baseline CMBs (versus none) were associated with ICH recurrence during follow-up (range 1-3 years): OR 3.1 (95\% CI 1.4-6.8; p = 0.006), 4.3 (95\% CI 1.8-10.3; p = 0.001), and 3.4 (95\% CI 1.4-8.3; p = 0.007) for 2-4, 5-10, and >10 CMBs, respectively. In CAA-unrelated ICH, only >10 CMBs (versus none) were associated with recurrent ICH (OR 5.6, 95\% CI 2.1-15; p = 0.001). The presence of 1 CMB (versus none) was not associated with recurrent ICH in CAA-related or CAA-unrelated cohorts. Conclusions: CMB burden and distribution on MRI identify subgroups of ICH survivors with higher ICH recurrence risk, which may help to predict ICH prognosis with relevance for clinical practice and treatment trials.",

author = "Andreas Charidimou and Toshio Imaizumi and Solene Moulin and Alexandro Biffi and Neshika Samarasekera and Yusuke Yakushiji and Andre Peeters and Yves Vandermeeren and Patrice Laloux and Baron, \{Jean Claude\} and Mar Hernandez-Guillamon and Joan Montaner and Barbara Casolla and Gregoire, \{Simone M.\} and Kang, \{Dong Wha\} and Kim, \{Jong S.\} and H. Naka and Smith, \{Eric E.\} and Anand Viswanathan and J{\"a}ger, \{Hans R.\} and \{Al-Shahi Salman\}, Rustam and Greenberg, \{Steven M.\} and Charlotte Cordonnier and Werring, \{David J.\}",

note = "Publisher Copyright: Copyright {\textcopyright} 2017 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.",

year = "2017",

month = aug,

day = "22",

doi = "10.1212/WNL.0000000000004259",

language = "English",

volume = "89",

pages = "820--829",

journal = "Neurology",

issn = "0028-3878",

publisher = "Lippincott Williams and Wilkins",

number = "8",

}

Charidimou, A, Imaizumi, T, Moulin, S, Biffi, A, Samarasekera, N, Yakushiji, Y, Peeters, A, Vandermeeren, Y , Laloux, P, Baron, JC, Hernandez-Guillamon, M, Montaner, J, Casolla, B, Gregoire, SM, Kang, DW, Kim, JS, Naka, H, Smith, EE, Viswanathan, A, Jäger, HR, Al-Shahi Salman, R, Greenberg, SM, Cordonnier, C & Werring, DJ 2017, 'Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis', Neurology, VOL. 89, Numéro 8, p. 820-829. https://doi.org/10.1212/WNL.0000000000004259

TY - JOUR

T1 - Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds

T2 - A meta-analysis

AU - Charidimou, Andreas

AU - Imaizumi, Toshio

AU - Moulin, Solene

AU - Biffi, Alexandro

AU - Samarasekera, Neshika

AU - Yakushiji, Yusuke

AU - Peeters, Andre

AU - Vandermeeren, Yves

AU - Laloux, Patrice

AU - Baron, Jean Claude

AU - Hernandez-Guillamon, Mar

AU - Montaner, Joan

AU - Casolla, Barbara

AU - Gregoire, Simone M.

AU - Kang, Dong Wha

AU - Kim, Jong S.

AU - Naka, H.

AU - Smith, Eric E.

AU - Viswanathan, Anand

AU - Jäger, Hans R.

AU - Al-Shahi Salman, Rustam

AU - Greenberg, Steven M.

AU - Cordonnier, Charlotte

AU - Werring, David J.

PY - 2017/8/22

Y1 - 2017/8/22

N2 - Objective: We evaluated recurrent intracerebral hemorrhage (ICH) risk in ICH survivors, stratified by the presence, distribution, and number of cerebral microbleeds (CMBs) on MRI (i.e., the presumed causal underlying small vessel disease and its severity). Methods: This was a meta-analysis of prospective cohorts following ICH, with blood-sensitive brain MRI soon after ICH. We estimated annualized recurrent symptomatic ICH rates for each study and compared pooled odds ratios (ORs) of recurrent ICH by CMB presence/absence and presumed etiology based on CMB distribution (strictly lobar CMBs related to probable or possible cerebral amyloid angiopathy [CAA] vs non-CAA) and burden (1, 2-4, 5-10, and >10 CMBs), using random effects models. Results: We pooled data from 10 studies including 1,306 patients: 325 with CAA-related and 981 CAA-unrelated ICH. The annual recurrent ICH risk was higher in CAA-related ICH vs CAA-unrelated ICH (7.4%, 95% confidence interval [CI] 3.2-12.6 vs 1.1%, 95% CI 0.5-1.7 per year, respectively; p = 0.01). In CAA-related ICH, multiple baseline CMBs (versus none) were associated with ICH recurrence during follow-up (range 1-3 years): OR 3.1 (95% CI 1.4-6.8; p = 0.006), 4.3 (95% CI 1.8-10.3; p = 0.001), and 3.4 (95% CI 1.4-8.3; p = 0.007) for 2-4, 5-10, and >10 CMBs, respectively. In CAA-unrelated ICH, only >10 CMBs (versus none) were associated with recurrent ICH (OR 5.6, 95% CI 2.1-15; p = 0.001). The presence of 1 CMB (versus none) was not associated with recurrent ICH in CAA-related or CAA-unrelated cohorts. Conclusions: CMB burden and distribution on MRI identify subgroups of ICH survivors with higher ICH recurrence risk, which may help to predict ICH prognosis with relevance for clinical practice and treatment trials.

AB - Objective: We evaluated recurrent intracerebral hemorrhage (ICH) risk in ICH survivors, stratified by the presence, distribution, and number of cerebral microbleeds (CMBs) on MRI (i.e., the presumed causal underlying small vessel disease and its severity). Methods: This was a meta-analysis of prospective cohorts following ICH, with blood-sensitive brain MRI soon after ICH. We estimated annualized recurrent symptomatic ICH rates for each study and compared pooled odds ratios (ORs) of recurrent ICH by CMB presence/absence and presumed etiology based on CMB distribution (strictly lobar CMBs related to probable or possible cerebral amyloid angiopathy [CAA] vs non-CAA) and burden (1, 2-4, 5-10, and >10 CMBs), using random effects models. Results: We pooled data from 10 studies including 1,306 patients: 325 with CAA-related and 981 CAA-unrelated ICH. The annual recurrent ICH risk was higher in CAA-related ICH vs CAA-unrelated ICH (7.4%, 95% confidence interval [CI] 3.2-12.6 vs 1.1%, 95% CI 0.5-1.7 per year, respectively; p = 0.01). In CAA-related ICH, multiple baseline CMBs (versus none) were associated with ICH recurrence during follow-up (range 1-3 years): OR 3.1 (95% CI 1.4-6.8; p = 0.006), 4.3 (95% CI 1.8-10.3; p = 0.001), and 3.4 (95% CI 1.4-8.3; p = 0.007) for 2-4, 5-10, and >10 CMBs, respectively. In CAA-unrelated ICH, only >10 CMBs (versus none) were associated with recurrent ICH (OR 5.6, 95% CI 2.1-15; p = 0.001). The presence of 1 CMB (versus none) was not associated with recurrent ICH in CAA-related or CAA-unrelated cohorts. Conclusions: CMB burden and distribution on MRI identify subgroups of ICH survivors with higher ICH recurrence risk, which may help to predict ICH prognosis with relevance for clinical practice and treatment trials.

UR - https://www.scopus.com/pages/publications/85027836709

U2 - 10.1212/WNL.0000000000004259

DO - 10.1212/WNL.0000000000004259

M3 - Article

C2 - 28747441

AN - SCOPUS:85027836709

SN - 0028-3878

VL - 89

SP - 820

EP - 829

JO - Neurology

JF - Neurology

IS - 8

ER -

Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis

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