August 22, 2017; 89 (8) ArticleOpen Access
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
First published July 26, 2017, DOI: https://doi.org/10.1212/WNL.0000000000004259
Andreas Charidimou
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.
Toshio Imaizumi
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.
Solene Moulin
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.
Alexandro Biffi
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.
Neshika Samarasekera
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.
Yusuke Yakushiji
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.
Andre Peeters
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.
Yves Vandermeeren
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.
Patrice Laloux
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.
Jean-Claude Baron
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.
Mar Hernandez-Guillamon
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.
Joan Montaner
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.
Barbara Casolla
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.
Simone M. Gregoire
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.
Dong-Wha Kang
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.
Jong S. Kim
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.
H. Naka
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.
Eric E. Smith
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.
Anand Viswanathan
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.
Hans R. Jäger
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.
Rustam Al-Shahi Salman
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.
Steven M. Greenberg
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.
Charlotte Cordonnier
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.
David J. Werring
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.
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
Neurology Aug 2017, 89 (8) 820-829; DOI: 10.1212/WNL.0000000000004259
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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.
GLOSSARY
- CAA=
- cerebral amyloid angiopathy;
- CI=
- confidence interval;
- CMB=
- cerebral microbleed;
- GRE=
- gradient-recalled echo;
- ICH=
- intracerebral hemorrhage;
- OR=
- odds ratio
Footnotes
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.
Supplemental data at Neurology.org
- Received October 11, 2016.
- Accepted in final form May 24, 2017.
- Copyright © 2017 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.
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.
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