Cerebral microbleeds and stroke risk after ischaemic stroke or transient ischaemic attack: a pooled analysis of individual patient data from cohort studies - 14/06/19
Doi : 10.1016/S1474-4422(19)30197-8
Duncan Wilson, PhD a, b, c, Gareth Ambler, PhD d, Keon-Joo Lee, MD e, Jae-Sung Lim, MD f, Masayuki Shiozawa, MD g, Masatoshi Koga, PhD g, Linxin Li, DPhil h, Caroline Lovelock, FRACP h, Hugues Chabriat, MD i, j, Michael Hennerici, MD k, Yuen Kwun Wong, MSc l, Henry Ka Fung Mak, MD m, Luis Prats-Sánchez, MD n, Alejandro Martínez-Domeño, MD n, Shigeru Inamura, MD o, Kazuhisa Yoshifuji, PhD o, Ethem Murat Arsava, MD p, Solveig Horstmann, MD q, Jan Purrucker, MD q, Bonnie Yin Ka Lam, PhD r, Adrian Wong, PhD r, Young Dae Kim, MD s, Tae-Jin Song, PhD t, Maarten Schrooten, MD u, Robin Lemmens, PhD v, Sebastian Eppinger, MD w, Thomas Gattringer, MD w, Ender Uysal, MD x, Zeynep Tanriverdi, MD x, Natan M Bornstein, MD y, z, Einor Ben Assayag, MD y, z, Hen Hallevi, MD y, z, Jun Tanaka, MD aa, Hideo Hara, PhD aa, Shelagh B Coutts, MD ab, Lisa Hert, MD ac, Alexandros Polymeris, MD ac, David J Seiffge, MD a, b, ac, al, Philippe Lyrer, MD ac, Ale Algra, MD ad, ae, Jaap Kappelle, MD ae, Rustam Al-Shahi Salman, PhD af, Hans R Jäger, FRCR ai, Gregory Y H Lip, MD aj, ak, Heinrich P Mattle, MD al, Leonidas D Panos, MD al, Jean-Louis Mas, MD am, Laurence Legrand, MD an, Christopher Karayiannis, MD ao, Thanh Phan, MD ap, Sarah Gunkel, MD aq, Nicolas Christ, MD aq, Jill Abrigo, MD ar, Thomas Leung, MD as, Winnie Chu, MD ar, Francesca Chappell, PhD ag, ah, Stephen Makin, PhD at, Derek Hayden, MD au, David J Williams, PhD av, aw, M Eline Kooi, PhD ax, Dianne H K van Dam-Nolen, MD bp, Carmen Barbato, MD a, b, az, Simone Browning, BSc a, b, az, Kim Wiegertjes, MD ba, Anil M Tuladhar, MD ba, Noortje Maaijwee, PhD bb, Christine Guevarra, MD bc, Chathuri Yatawara, PhD bc, Anne-Marie Mendyk, MD bd, Christine Delmaire, MD bd, Sebastian Köhler, PhD be, Robert van Oostenbrugge, MD ay, Ying Zhou, PhD bf, Chao Xu, MD bf, Saima Hilal, PhD bg, Bibek Gyanwali, MD bg, Christopher Chen, FRCP bg, Min Lou, PhD bf, Julie Staals, MD ay, Régis Bordet, MD bd, Nagaendran Kandiah, FRCP bc, Frank-Erik de Leeuw, MD ba, Robert Simister, PhD a, b, az, Aad van der Lugt, MD bp, Peter J Kelly, MD au, Joanna M Wardlaw, MD ag, ah, Yannie Soo, MD as, Felix Fluri, MD aq, Velandai Srikanth, PhD ao, David Calvet, MD am, Simon Jung, MD al, Vincent I H Kwa, MD bh, Stefan T Engelter, MD ac, bi, Nils Peters, MD ac, bi, Eric E Smith, MD ab, Yusuke Yakushiji, PhD aa, Dilek Necioglu Orken, MD x, Franz Fazekas, MD w, Vincent Thijs, MD bj, bk, bl, Ji Hoe Heo, MD s, Vincent Mok, MD r, Roland Veltkamp, MD bm, bn, Hakan Ay, MD p, Toshio Imaizumi, MD o, Beatriz Gomez-Anson, PhD bo, Kui Kai Lau, PhD l, Eric Jouvent, MD i, j, Peter M Rothwell, FMedSci h, Kazunori Toyoda, MD g, Hee-Joon Bae, MD e, Joan Marti-Fabregas, PhD n, David J Werring, PhD a, ⁎ 
on behalf of the
on behalf of the
Microbleeds International Collaborative Network†
Kirsty Harkness, Louise Shaw, Jane Sword, Azlisham Mohd Nor, Pankaj Sharma, Deborah Kelly, Frances Harrington, Marc Randall, Matthew Smith, Karim Mahawish, Abduelbaset Elmarim, Bernard Esisi, Claire Cullen, Arumug Nallasivam, Christopher Price, Adrian Barry, Christine Roffe, John Coyle, Ahamad Hassan, Jonathan Birns, David Cohen, Lakshmanan Sekaran, Adrian Parry-Jones, Anthea Parry, David Hargroves, Harald Proschel, Prabel Datta, Khaled Darawil, Aravindakshan Manoj, Mathew Burn, Chris Patterson, Elio Giallombardo, Nigel Smyth, Syed Mansoor, Ijaz Anwar, Rachel Marsh, Sissi Ispoglou, Dinesh Chadha, Mathuri Prabhakaran, Sanjeevikumar Meenakishundaram, Janice O’Connell, Jon Scott, Vinodh Krishnamurthy, Prasanna Aghoram, Michael McCormick, Nikola Sprigg, Paul O’Mahony, Martin Cooper, Lillian Choy, Peter Wilkinson, Simon Leach, Sarah Caine, Ilse Burger, Gunaratam Gunathilagan, Paul Guyler, Hedley Emsley, Michelle Davis, Dulka Manawadu, Kath Pasco, Maam Mamun, Robert Luder, Mahmud Sajid, Ijaz Anwar, James Okwera, Elizabeth Warburton, Kari Saastamoinen, Timothy England, Janet Putterill, Enrico Flossman, Michael Power, Krishna Dani, David Mangion, Appu Suman, John Corrigan, Enas Lawrence, Djamil Vahidassr, Clare Shakeshaft, Martin Brown, Andreas Charidimou, Hannah Cohen, Gargi Banerjee, Henry Houlden, Mark White, Tarek Yousry, Kirsty Harkness, Enrico Flossmann, Nigel Smyth, Louise Shaw, Elizabeth Warburton, Keith Muir, Marwan El-Koussy, Pascal Gratz, Jeremy Molad, Amos Korczyn, Efrat Kliper, Philippe Maeder, Achim Gass, Chahin Pachai, Luc Bracoub, Marie-Yvonne Douste-Blazy, Marie Dominique Fratacci, Eric Vicaut, Shoichiro Sato, Kaori Miwa, Kyohei Fujita, Toshihiro Ide, Henry Ma, John Ly, Shahoo Singhal, Ronil Chandra, Lee-Anne Slater, Cathy Soufan, Christopher Moran, Christopher Traenka, Sebastian Thilemann, Joachim Fladt, Henrik Gensicke, Leo Bonati, Beom Joon Kim, Moon-Ku Han, Jihoon Kang, Eunbin Ko, Mi Hwa Yang, Myung Suk Jang, Sean Murphy, Fiona Carty, Layan Akijian, John Thornton, Mark Schembri, Elles Douven, Raquel Delgado-Mederos;, Rebeca Marín, Pol Camps-Renom, Daniel Guisado-Alonso, Fidel Nuñez, Santiago Medrano-Martorell, Elisa Merino, Kotaro Iida, Syuhei Ikeda, Masashi Nishihara, Hiroyuki Irie, Derya Selcuk Demirelli, Jayesh Modi Medanta, Charlotte Zerna, Maria Valdés Hernández, Paul Armitage, Anna Heye, Susana Muñoz-Maniega, Eleni Sakka, Michael Thrippleton, Martin Dennis, Ysoline Beigneux, Mauro Silva, Narayanaswamy Venketasubramanian, Shu Leung Ho, Raymond Tak Fai Cheung, Koon Ho Chan, Kay Cheong Teo, Edward Hui, Joseph Shiu Kwong Kwan, Richard Chang, Man Yu Tse, Chu Peng Hoi, Chung Yan Chan, Oi Ling Chan, Ryan Hoi Kit Cheung, Edmund Ka Ming Wong, Kam Tat Leung, Suk Fung Tsang, Hing Lung Ip, Sze Ho Ma, Karen Ma, Wing Chi Fong, Siu Hung Li, Richard Li, Ping Wing Ng, Kwok Kui Wong, Wenyan Liu, Lawrence Wong, Lino Ramos, Els De Schryver, Joost Jöbsis, Jaap van der Sande, Paul Brouwers, Yvo Roos, Jan Stam, Stef Bakker, Henk Verbiest, Wouter Schoonewille, Cisca Linn, Leopold Hertzberger, Maarten van Gemert, Paul Berntsen, Jeroen Hendrikse, Paul Nederkoorn, Werner Mess, Peter Koudstaal, Alexander Leff, Nicholas Ward, Parashkev Nachev, Richard Perry, Hatice Ozkan, John Mitchell
a Stroke Research Centre, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, London, UK
b National Hospital for Neurology and Neurosurgery, London UK
c New Zealand Brain Research Institute, Christchurch, New Zealand
d Department of Statistical Science, University College London, London, UK
e Department of Neurology, Seoul National University Bundang Hospital, Seoul National University School of Medicine, Seongnam, South Korea
f Department of Neurology, Hallym University Sacred Heart Hospital, Anyang, South Korea
g Department of Cerebrovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan
h Centre for Prevention of Stroke and Dementia, University of Oxford, Oxford, UK
i Assistance Publique Hôpitaux de Paris, Lariboisière Hospital, Department of Neurology, Paris, France
j Département Hospitalo-Universtaire NeuroVasc, University Paris Diderot, and INSERM U1141, Paris, France
k Department of Neurology, Universitätsmedizin Mannheim, University of Heidelberg, Mannheim, Germany
l Division of Neurology, Department of Medicine, The University of Hong Kong, Hong Kong
m Department of Diagnostic Radiology, The University of Hong Kong, Hong Kong
n Department of Neurology, Hospital de la Santa Creu i Sant Pau, Biomedical Research Institute, Barcelona, Spain
o Department of Neurosurgery, Kushiro City General Hospital, Kushiro, Japan
p Departments of Neurology and Radiology, Massachusetts General Hospital, Harvard Medical School, Boston MA, USA
q Department of Neurology, Heidelberg University Hospital, Heidelberg, Germany
r Therese Pei Fong Chow Research Centre for Prevention of Dementia, Gerald Choa Neuroscience Centre, Lui Che Woo Institute of Innovative Medicine, Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong
s Department of Neurology, Yonsei University College of Medicine, Seoul, South Korea
t Department of Neurology, Ewha Womans University College of Medicine, Seoul, South Korea
u Center for Brain and Disease Research, VIB, Leuven, Belgium
v Experimental Neurology and Leuven Institute for Neuroscience and Disease, Katholieke Universiteit Leuven, University of Leuven, Laboratory of Neurobiology, Leuven, Belgium
w Department of Neurology, Medical University of Graz, Graz, Austria
x Department of Neurology, Demiroglu Bilim University, Istanbul, Turkey
y Department of Neurology, Tel-Aviv Sourasky Medical Center, Tel-Aviv, Israel
z Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel
aa Division of Neurology, Department of Internal Medicine, Saga University Faculty of Medicine, Nabeshima, Saga, Japan
ab Calgary Stroke Program, Department of Clinical Neurosciences, Radiology and Community Health Sciences, Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
ac Department of Neurology and Stroke Centre, University Hospital Basel and University of Basel, Basel, Switzerland
ad Julius Centre for Health Sciences and Primary Care, University Medical Center Utrecht and Utrecht University, Utrecht, Netherlands
ae Department of Neurology and Neurosurgery, Utrecht Stroke Centre, University Medical Center Utrecht and Utrecht University, Utrecht, Netherlands
af Centre for Clinical Brain Sciences, School of Clinical Sciences, University of Edinburgh, Edinburgh, UK
ag Edinburgh Imaging, School of Clinical Sciences, University of Edinburgh, Edinburgh, UK
ah UK Dementia Institute at the University of Edinburgh, School of Clinical Sciences, University of Edinburgh, Edinburgh, UK
ai Lysholm Department of Neuroradiology and the Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, UCL Institute of Neurology and the National Hospital for Neurology and Neurosurgery, London, UK
aj Liverpool Centre for Cardiovascular Science, University of Liverpool and Liverpool Heart and Chest Hospital, Liverpool, UK
ak Aalborg Thrombosis Research Unit, Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
al Department of Diagnostic and Interventional Neuroradiology and Department of Neurology Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland
am Department of Neurology, Sainte-Anne Hospital, Paris Descartes University, INSERM U1266, Paris, France
an Department of Neuroradiology, Sainte-Anne Hospital, Paris Descartes University, INSERM U1266, Paris, France
ao Peninsula Clinical School, Peninsula Health, Monash University, Melbourne, VIC, Australia
ap Stroke and Ageing Research Group, School of Clinical Sciences at Monash Health, Monash University, Melbourne, VIC, Australia
aq Department of Neurology, University Hospital of Würzburg, Josef-Schneider Strasse 11, Würzburg, Germany
ar Department of Imaging and Interventional Radiology, Prince of Wales Hospital, The Chinese University of Hong Kong, Ma Liu Shui, Hong Kong
as Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Ma Liu Shui, Hong Kong
at Institute of Cardiovascular and Medical Science, University of Glasgow, Glasgow, UK
au The Neurovascular Research Unit and Health Research Board, Stroke Clinical Trials Network Ireland, University College Dublin, Dublin, Ireland
av Department of Geriatric and Stroke Medicine, Royal College of Surgeons in Ireland, Dublin, Ireland
aw Beaumont Hospital Dublin, Ireland
ax Department of Radiology and Nuclear Medicine, Maastricht University Medical Centre, Maastricht, Netherlands
ay Department of Neurology, CARIM School for Cardiovascular Diseases, Maastricht University Medical Centre, Maastricht, Netherlands
az Comprehensive Stroke Service, University College London Hospitals NHS Trust, London, UK
ba Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Centre for Medical Neuroscience, Radboud University Medical Center, Nijmegen, Netherlands
bb Lucerne State Hospital; Switzerland Center for Neurology and Neurorehabilitation, Luzern, Switzerland
bc Department of Neurology, National Neuroscience Institute, Singapore, Singapore
bd University of Lille, Inserm, CHU de Lille, Degenerative and vascular cognitive disorders U1171, Lille, France
be Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands
bf Department of Neurology, The 2nd Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China
bg Memory Aging and Cognition Centre, National University Health System, Singapore, Singapore
bh Department of Neurology, Onze Lieve Vrouwe Gasthuis, Amsterdam, Netherlands
bi Neurology and Neurorehabilitation, University Department of Geriatric Medicine Felix Platter, University of Basel, Basel, Switzerland
bj Stroke Division, Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, VIC, Australia
bk Department of Neurology, Austin Health, Melbourne, VIC, Australia
bl Department of Neurosciences, University Hospitals Leuven, Belgium
bm Department of Stroke Medicine, Imperial College London, London, UK
bn Department of Neurology, Heidelberg University Hospital, Heidelberg, Germany
bo Unit of Neuroradiology, Hospital Santa Creu i Sant Pau, Universitat Autonoma, Barcelona, Spain
bp Department of Radiology and Nuclear Medicine, Erasmus Medical Centre, University Medical Centre, Rotterdam, Netherlands
*Correspondence to: Prof David J Werring, Stroke Research Centre, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, London WC1B 5EH, UKStroke Research CentreDepartment of Brain Repair and RehabilitationUCL Queen Square Institute of NeurologyLondonWC1B 5EHUK
Summary |
Background |
Cerebral microbleeds are a neuroimaging biomarker of stroke risk. A crucial clinical question is whether cerebral microbleeds indicate patients with recent ischaemic stroke or transient ischaemic attack in whom the rate of future intracranial haemorrhage is likely to exceed that of recurrent ischaemic stroke when treated with antithrombotic drugs. We therefore aimed to establish whether a large burden of cerebral microbleeds or particular anatomical patterns of cerebral microbleeds can identify ischaemic stroke or transient ischaemic attack patients at higher absolute risk of intracranial haemorrhage than ischaemic stroke.
Methods |
We did a pooled analysis of individual patient data from cohort studies in adults with recent ischaemic stroke or transient ischaemic attack. Cohorts were eligible for inclusion if they prospectively recruited adult participants with ischaemic stroke or transient ischaemic attack; included at least 50 participants; collected data on stroke events over at least 3 months follow-up; used an appropriate MRI sequence that is sensitive to magnetic susceptibility; and documented the number and anatomical distribution of cerebral microbleeds reliably using consensus criteria and validated scales. Our prespecified primary outcomes were a composite of any symptomatic intracranial haemorrhage or ischaemic stroke, symptomatic intracranial haemorrhage, and symptomatic ischaemic stroke. We registered this study with the PROSPERO international prospective register of systematic reviews, number CRD42016036602.
Findings |
Between Jan 1, 1996, and Dec 1, 2018, we identified 344 studies. After exclusions for ineligibility or declined requests for inclusion, 20 322 patients from 38 cohorts (over 35 225 patient-years of follow-up; median 1·34 years [IQR 0·19–2·44]) were included in our analyses. The adjusted hazard ratio [aHR] comparing patients with cerebral microbleeds to those without was 1·35 (95% CI 1·20–1·50) for the composite outcome of intracranial haemorrhage and ischaemic stroke; 2·45 (1·82–3·29) for intracranial haemorrhage and 1·23 (1·08–1·40) for ischaemic stroke. The aHR increased with increasing cerebral microbleed burden for intracranial haemorrhage but this effect was less marked for ischaemic stroke (for five or more cerebral microbleeds, aHR 4·55 [95% CI 3·08–6·72] for intracranial haemorrhage vs 1·47 [1·19–1·80] for ischaemic stroke; for ten or more cerebral microbleeds, aHR 5·52 [3·36–9·05] vs 1·43 [1·07–1·91]; and for ≥20 cerebral microbleeds, aHR 8·61 [4·69–15·81] vs 1·86 [1·23–2·82]). However, irrespective of cerebral microbleed anatomical distribution or burden, the rate of ischaemic stroke exceeded that of intracranial haemorrhage (for ten or more cerebral microbleeds, 64 ischaemic strokes [95% CI 48–84] per 1000 patient-years vs 27 intracranial haemorrhages [17–41] per 1000 patient-years; and for ≥20 cerebral microbleeds, 73 ischaemic strokes [46–108] per 1000 patient-years vs 39 intracranial haemorrhages [21–67] per 1000 patient-years).
Interpretation |
In patients with recent ischaemic stroke or transient ischaemic attack, cerebral microbleeds are associated with a greater relative hazard (aHR) for subsequent intracranial haemorrhage than for ischaemic stroke, but the absolute risk of ischaemic stroke is higher than that of intracranial haemorrhage, regardless of cerebral microbleed presence, antomical distribution, or burden.
Funding |
British Heart Foundation and UK Stroke Association.
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© 2019
The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Publié par Elsevier Masson SAS. Tous droits réservés.
Vol 18 - N° 7
P. 653-665 - juillet 2019 Retour au numéro
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