Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation

Author:

Soo Yannie1ORCID,Zietz Annaelle2ORCID,Yiu Brian1,Mok Vincent C. T.13,Polymeris Alexandros A.2ORCID,Seiffge David4ORCID,Ambler Gareth5,Wilson Duncan6,Leung Thomas Wai Hong1,Tsang Suk Fung1,Chu Winnie7,Abrigo Jill7,Cheng Cyrus1,Lee Keon‐Joo8,Lim Jae‐Sung9,Shiozawa Masayuki10,Koga Masatoshi10ORCID,Chabriat Hugues11ORCID,Hennerici Michael12,Wong Yuen Kwun13,Mak Henry14,Collet Roger15,Inamura Shigeru16,Yoshifuji Kazuhisa16,Arsava Ethem Murat17,Horstmann Solveig18,Purrucker Jan18,Lam Bonnie Y. K.13,Wong Adrian3,Kim Young Dae19ORCID,Song Tae‐Jin20,Lemmens Robin212223,Eppinger Sebastian2425,Gattringer Thomas2425ORCID,Uysal Ender26,Demirelli Derya Selçuk27,Bornstein Natan M.2829,Assayag Einor Ben2829,Hallevi Hen2829,Molad Jeremy2829,Nishihara Masashi30,Tanaka Jun31,Coutts Shelagh B.32,Kappelle L. Jaap33,Al‐Shahi Salman Rustam34,Jager Rolf35,Lip Gregory Y. H.3637,Goeldlin Martina B.4ORCID,Panos Leonidas D.4,Mas Jean‐Louis38,Legrand Laurence39,Karayiannis Chris40,Phan Thanh41,Bellut Maximilian42,Chappell Francesca4344,Makin Stephen45,Hayden Derek46,Williams David47,van Dam‐Nolen Dianne H. K.48,Nederkoorn Paul J.49,Barbato Carmen50,Browning Simone5152,Wiegertjes Kim53ORCID,Tuladhar Anil Man53ORCID,Mendyk Anne‐Marie54,Köhler Sebastian55,van Oostenburgge Robert56,Zhou Ying57ORCID,Xu Chao57,Hilal Saima58,Gyanwali Bibek59,Chen Christopher59,Lou Min57,Staals Julie56,Bordet Regis54,Kandiah Nagaendran60ORCID,de Leeuw Frank‐Erik53,Simister Robert5152,Hendrikse Jeroen61,Wardlaw Joanna6263ORCID,Kelly Peter64,Fluri Felix42,Srikanth Velandai65,Calvet David38,Jung Simon4,Kwa Vincent, I. H.66,Smith Eric E.32,Hara Hideo67,Yakushiji Yusuke68,Orken Dilek Necioglu69,Fazekas Franz24,Thijs Vincent7071,Heo Ji‐Hoe19ORCID,Veltkamp Roland1872,Ay Hakan73,Imaizumi Toshio16,Lau Kui Kai1374,Jouvent Eric7576ORCID,Toyoda Kazunori10ORCID,Yoshimura Sohei10ORCID,Bae Hee‐Joon77,Martí‐Fàbregas Joan15ORCID,Prats‐Sánchez Luis15,Lyrer Philippe2,Best Jonathan5152,Werring David5152,Engelter Stefan T.278,Peters Nils27879,

Affiliation:

1. Division of Neurology, Department of Medicine and Therapeutics, Prince of Wales Hospital The Chinese University of Hong Kong Shatin Hong Kong

2. Department of Neurology and Stroke Centre University Hospital Basel and University of Basel Basel Switzerland

3. Gerald Choa Neuroscience Institute, Margaret K. L. Cheung Research Centre for Management of Parkinsonism, Therese Pei Fong Chow Research Centre for Prevention of Dementia, Lui Che Woo Institute of Innovative Medicine, Li Ka Shing Institute of Health Science, Lau Tat‐chuen Research Centre of Brain Degenerative Diseases in Chinese The Chinese University of Hong Kong Hong Kong SAR Hong Kong

4. Department of Neurology, Inselspital University Hospital Bern, University of Bern Bern Switzerland

5. Department of Statistical Science University College London London UK

6. Stroke Research Centre, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, London, UK New Zealand Brain Research Institute Christchurch New Zealand

7. Department of Imaging and Interventional Radiology, Prince of Wales Hospital The Chinese University of Hong Kong Shatin Hong Kong

8. Department of Neurology Korea University Guro Hospital Seoul Republic of Korea

9. Department of Neurology, Asan Medical Center University of Ulsan College of Medicine Seoul Republic of Korea

10. Department of Cerebrovascular Medicine National Cerebral and Cardiovascular Centre Suita Japan

11. APHP, Lariboisière Hospital, Translational Neurovascular Centre, F‐75475 Paris, France FHU NeuroVasc, Université de Paris and INSERM U1141 Paris France

12. Department of Neurology University of Heidelberg/Mannheim Hospital Mannheim Germany

13. Division of Neurology, Department of Medicine The University of Hong Kong Hong Kong Hong Kong

14. Department of Diagnostic Radiology The University of Hong Kong Hong Kong Hong Kong

15. Department of Neurology, Hospital de la Santa Creu i Sant Pau Biomedical Research Institute Barcelona Spain

16. Department of Neurosurgery Kushiro City General Hospital Kushiro Japan

17. Departments of Neurology and Radiology, Massachusetts General Hospital Harvard Medical School Boston MA USA

18. Department of Neurology Heidelberg University Hospital Heidelberg Germany

19. Department of Neurology Yonsei University College of Medicine Seoul South Korea

20. Department of Neurology, Seoul Hospital Ewha Womans University College of Medicine Seoul South Korea

21. Experimental Neurology, Department of Neurosciences KU Leuven—University of Leuven Leuven Belgium

22. VIB Center for Brain & Disease Research Leuven Belgium

23. Department of Neurology University Hospitals Leuven Leuven Belgium

24. Department of Neurology Medical University of Graz Graz Austria

25. Division of Neuroradiology, Vascular and Interventional Radiology, Department of Radiology Medical University of Graz Graz Austria

26. Antalya Teaching and Research Hospital, Department of Radiology University of Health Sciences Turkey Antalya Turkey

27. Sisli Hamidiye Etfal Teaching and Research Hospital, Department of Neurology University of Health Sciences Turkey Antalya Turkey

28. Department of Neurology Tel‐Aviv Sourasky Medical Center Tel‐Aviv Israel

29. Sackler Faculty of Medicine Tel‐Aviv University Tel‐Aviv Israel

30. Department of Radiology Saga University Faculty of Medicine Saga Japan

31. Department of Cerebrovascular Medicine St. Mary's Hospital Kurume Japan

32. Calgary Stroke Program, Department of Clinical Neurosciences, Radiology and Community Health Sciences, Hotchkiss Brain Institute University of Calgary Calgary Canada

33. Department of Neurology and Neurosurgery University Medical Centre Utrecht and Utrecht University Utrecht The Netherlands

34. Centre for Clinical Brain Sciences, School of Clinical Sciences University of Edinburgh Edinburgh UK

35. 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

36. Liverpool Centre for Cardiovascular Science at University of Liverpool Liverpool John Moores University and Liverpool Heart & Chest Hospital Liverpool UK

37. Department of Clinical Medicine Aalborg University Aalborg Denmark

38. GHU‐Paris Psychiatrie et Neurosciences, Neurology Department and Stroke Unit, Sainte‐Anne Hospital, and Université de Paris Cité, INSERM U1266 Institute of Psychiatry and Neuroscience of Paris Paris France

39. GHU‐Paris Psychiatrie et Neurosciences, Neuroradiology Department, Sainte‐Anne Hospital, and Université Paris Cité, INSERM U1266 Institute of Psychiatry and Neuroscience of Paris Paris France

40. Peninsula Clinical School, Peninsula Health Monash University Melbourne Australia

41. Stroke and Ageing Research Group, School of Clinical Sciences at Monash Health Monash University Melbourne Australia

42. Department of Neurology University Hospital of Würzburg Würzburg Germany

43. Centre for Clinical Brain Sciences Edinburgh Imaging Edinburgh UK

44. UK Dementia Institute at the University of Edinburgh Edinburgh UK

45. Centre for Rural Health, Institute for Applied Health Sciences University of Aberdeen Aberdeen UK

46. Acute Medical Unit and Department of Age‐related Healthcare Tallaght University Hospital Dublin Ireland

47. Department of Geriatric and Stroke Medicine, RCSI University of Medicine and Health Sciences Dublin Ireland and Beaumont Hospital Dublin Dublin Ireland

48. Department of Radiology and Nuclear Medicine Erasmus University Medical Center Rotterdam Rotterdam The Netherlands

49. Department of Neurology Amsterdam University Medical Centers Amsterdam The Netherlands

50. Department of Neurology University of Florence Firenze Italy

51. Stroke Research Centre, Department of Brain Repair and Rehabilitation UCL Queen Square Institute of Neurology London UK

52. Comprehensive Stroke Service University College London Hospitals NHS Trust London UK

53. Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Centre for Medical Neuroscience Radboud University Medical Center Nijmegen The Netherlands

54. University of Lille, Inserm, CHU de Lille. Lille Neuroscience & Cognition Lille France

55. Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience (MHeNs) Maastricht University Maastricht The Netherlands

56. Department of Neurology, Cardiovascular Research Institute Maastricht (CARIM) Maastricht University Medical Centre Maastricht The Netherlands

57. Department of Neurology The Second Affiliated Hospital of Zhejiang University, School of Medicine Hangzhou China

58. Saw Swee Hock School of Public Health National University of Singapore and National University Health System Singapore Singapore

59. Memory Aging & Cognition Centre, Yong Loo Lin School of Medicine National University of Singapore Singapore Singapore

60. Dementia Research Centre (Singapore) Lee Kong Chian School of Medicine Singapore Singapore

61. Department of Radiology and Nuclear Medicine University Medical Center Utrecht Utrecht The Netherlands

62. Division of Neuroimaging Sciences Edinburgh Imaging Edinburgh UK

63. UK Dementia Research Institute University of Edinburgh and NHS Lothian Edinburgh UK

64. The Neurovascular Research Unit and Health Research Board, Stroke Clinical Trials Network Ireland University College Dublin Dublin Ireland

65. Peninsula Clinical School, Peninsula Health, Monash University, Melbourne, Australia National Centre for Healthy Ageing Melbourne Australia

66. Department of Neurology OLVG Amsterdam The Netherlands

67. Division of Neurology, Department of Internal Medicine Saga University Faculty of Medicine Saga Japan

68. Department of Neurology Kansai Medical University Hirakata Japan

69. Department of Neurology Istanbul Arel University Istanbul Turkey

70. Stroke Division, Florey Institute of Neuroscience and Mental Health University of Melbourne Heidelberg Australia

71. A.A. Martinos Center for Biomedical Imaging, Departments of Neurology and Radiology, Massachusetts General Hospital Harvard Medical School Boston MA USA

72. Department of Neurology Austin Health Heidelberg Australia

73. Department of Brain Sciences Imperial College London London UK

74. State Key Laboratory of Brain and Cognitive Sciences The University of Hong Kong Shatin Hong Kong

75. Université de Paris—Assistance Publique Hôpitaux de Paris Paris France

76. Département de Neurologie Hôpital Lariboisière, FHU NeuroVasc, INSERM NeuroDiderot U1141 Paris France

77. Department of Neurology Seoul National University Bundang Hospital, Seoul National University College of Medicine Seongnam Republic of Korea

78. Neurology and Neurorehabilitation University Department of Geriatric Medicine FELIX PLATTER, University of Basel Basel Switzerland

79. Stroke Center, Klinik Hirslanden Zürich Switzerland

Abstract

ObjectivesCerebral microbleeds are associated with the risks of ischemic stroke and intracranial hemorrhage, causing clinical dilemmas for antithrombotic treatment decisions. We aimed to evaluate the risks of intracranial hemorrhage and ischemic stroke associated with microbleeds in patients with atrial fibrillation treated with vitamin K antagonists, direct oral anticoagulants, antiplatelets, and combination therapy (i.e. concurrent oral anticoagulant and antiplatelet).MethodsWe included patients with documented atrial fibrillation from the pooled individual patient data analysis by the Microbleeds International Collaborative Network. Risks of subsequent intracranial hemorrhage and ischemic stroke were compared between patients with and without microbleeds, stratified by antithrombotic use.ResultsA total of 7,839 patients were included. The presence of microbleeds was associated with an increased relative risk of intracranial hemorrhage (adjusted hazard ratio [aHR] = 2.74, 95% confidence interval = 1.76–4.26) and ischemic stroke (aHR = 1.29, 95% confidence interval = 1.04–1.59). For the entire cohort, the absolute incidence of ischemic stroke was higher than intracranial hemorrhage regardless of microbleed burden. However, for the subgroup of patients taking combination of anticoagulant and antiplatelet therapy, the absolute risk of intracranial hemorrhage exceeded that of ischemic stroke in those with 2 to 4 microbleeds (25 vs 12 per 1,000 patient‐years) and ≥ 11 microbleeds (94 vs 48 per 1,000 patient‐years).InterpretationPatients with atrial fibrillation and high burden of microbleeds receiving combination therapy have a tendency of higher rate of intracranial hemorrhage than ischemic stroke, with potential for net harm. Further studies are needed to help optimize stroke preventive strategies in this high‐risk group. ANN NEUROL 2023;94:61–74

Funder

Schweizerische Herzstiftung

Publisher

Wiley

Subject

Neurology (clinical),Neurology

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