Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation

Yannie Soo; Annaelle Zietz; Brian Yiu; Vincent C. T. Mok; Alexandros A. Polymeris; David Seiffge; Gareth Ambler; Duncan Wilson; Thomas Wai Hong Leung; Suk Fung Tsang; Winnie Chu; Jill Abrigo; Cyrus Cheng; Keon-Joo Lee; Jae-Sung Lim; Masayuki Shiozawa; Masatoshi Koga; Hugues Chabriat; Michael Hennerici; Yuen Kwun Wong; Henry Mak; Roger Collet; Shigeru Inamura; Kazuhisa Yoshifuji; Ethem Murat Arsava; Solveig Horstmann; Jan Purrucker; Bonnie Y. K. Lam; Adrian Wong; Young Dae Kim; Tae-Jin Song; Robin Lemmens; Sebastian Eppinger; Thomas Gattringer; Ender Uysal; Derya Selçuk Demirelli; Natan M. Bornstein; Einor Ben Assayag; Hen Hallevi; Jeremy Molad; Masashi Nishihara; Jun Tanaka; Shelagh B. Coutts; L. Jaap Kappelle; Rustam Al-Shahi Salman; Rolf Jager; Gregory Y. H. Lip; Martina B. Goeldlin; Leonidas D. Panos; Jean-Louis Mas; Laurence Legrand; Chris Karayiannis; Thanh Phan; Maximilian Bellut; Francesca Chappell; Stephen Makin; Derek Hayden; David Williams; Dianne H. K. van Dam-Nolen; Paul J. Nederkoorn; Carmen Barbato; Simone Browning; Kim Wiegertjes; Anil Man Tuladhar; Anne-Marie Mendyk; Sebastian Köhler; Robert van Oostenburgge; Ying Zhou; Chao Xu; Saima Hilal; Bibek Gyanwali; Christopher Chen; Min Lou; Julie Staals; Regis Bordet; Nagaendran Kandiah; Frank-Erik de Leeuw; Robert Simister; Jeroen Hendrikse; Joanna Wardlaw; Peter Kelly; Felix Fluri; Velandai Srikanth; David Calvet; Simon Jung; I. H. Kwa Vincent; Eric E. Smith; Hideo Hara; Yusuke Yakushiji; Dilek Necioglu Orken; Franz Fazekas; Vincent Thijs; Ji-Hoe Heo; Roland Veltkamp; Hakan Ay; Toshio Imaizumi; Kui Kai Lau; Eric Jouvent; Kazunori Toyoda; Sohei Yoshimura; Hee-Joon Bae; Joan Martí-Fàbregas; Luis Prats-Sánchez; Philippe Lyrer; Jonathan Best; David Werring; Stefan T. Engelter; Nils Peters; the Microbleeds International Collaborative Network

doi:10.1002/ana.26642

Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation

Yannie Soo, Annaelle Zietz, Brian Yiu, Vincent C. T. Mok, Alexandros A. Polymeris, David Seiffge, Gareth Ambler, Duncan Wilson, Thomas Wai Hong Leung, Suk Fung Tsang, Winnie Chu, Jill Abrigo, Cyrus Cheng, Keon-Joo Lee, Jae-Sung Lim, Masayuki Shiozawa, Masatoshi Koga, Hugues Chabriat, Michael Hennerici, Yuen Kwun WongHenry Mak, Roger Collet, Shigeru Inamura, Kazuhisa Yoshifuji, Ethem Murat Arsava, Solveig Horstmann, Jan Purrucker, Bonnie Y. K. Lam, Adrian Wong, Young Dae Kim, Tae-Jin Song, Robin Lemmens, Sebastian Eppinger, Thomas Gattringer, Ender Uysal, Derya Selçuk Demirelli, Natan M. Bornstein, Einor Ben Assayag, Hen Hallevi, Jeremy Molad, Masashi Nishihara, Jun Tanaka, Shelagh B. Coutts, L. Jaap Kappelle, Rustam Al-Shahi Salman, Rolf Jager, Gregory Y. H. Lip, Martina B. Goeldlin, Leonidas D. Panos, Jean-Louis Mas, Laurence Legrand, Chris Karayiannis, Thanh Phan, Maximilian Bellut, Francesca Chappell, Stephen Makin, Derek Hayden, David Williams, Dianne H. K. van Dam-Nolen, Paul J. Nederkoorn, Carmen Barbato, Simone Browning, Kim Wiegertjes, Anil Man Tuladhar, Anne-Marie Mendyk, Sebastian Köhler, Robert van Oostenburgge, Ying Zhou, Chao Xu, Saima Hilal, Bibek Gyanwali, Christopher Chen, Min Lou, Julie Staals, Regis Bordet, Nagaendran Kandiah, Frank-Erik de Leeuw, Robert Simister, Jeroen Hendrikse, Joanna Wardlaw, Peter Kelly, Felix Fluri, Velandai Srikanth, David Calvet, Simon Jung, I. H. Kwa Vincent, Eric E. Smith, Hideo Hara, Yusuke Yakushiji, Dilek Necioglu Orken, Franz Fazekas, Vincent Thijs, Ji-Hoe Heo, Roland Veltkamp, Hakan Ay, Toshio Imaizumi, Kui Kai Lau, Eric Jouvent, Kazunori Toyoda, Sohei Yoshimura, Hee-Joon Bae, Joan Martí-Fàbregas, Luis Prats-Sánchez, Philippe Lyrer, Jonathan Best, David Werring, Stefan T. Engelter, Nils Peters, the Microbleeds International Collaborative Network

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Abstract

Objectives Cerebral 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). Methods We 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. Results A 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, 95.76–4.26) and ischemic stroke (aHR = 1.29, 95.04–1.59). 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). Interpretation Patients 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

Original language	English
Pages (from-to)	61-74
Number of pages	14
Journal	Annals of Neurology
Volume	94
Issue number	1
Early online date	17 Mar 2023
DOIs	https://doi.org/10.1002/ana.26642
Publication status	Published - Jul 2023

Bibliographical note

Acknowledgments
This study was funded by the Swiss Heart Foundation. Furthermore, the study was funded in part by Wellcome Trust (WT088134/Z/09/A) and for the purpose of openaccess, co-authors have applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission. The authors would like to thank the patients that participated in the various cohorts. Open access funding provided by Universitat Basel.

Research Funding
Swiss Heart Foundation
Wellcome [WT088134/Z/09/A]
Open access funding provided by Universitat Basel.

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© 2023 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
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Soo, Y., Zietz, A., Yiu, B., Mok, V. C. T., Polymeris, A. A., Seiffge, D., Ambler, G., Wilson, D., Leung, T. W. H., Tsang, S. F., Chu, W., Abrigo, J., Cheng, C., Lee, K.-J., Lim, J.-S., Shiozawa, M., Koga, M., Chabriat, H., Hennerici, M., ... Network, T. M. I. C. (2023). Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation. Annals of Neurology, 94(1), 61-74. https://doi.org/10.1002/ana.26642

Soo, Y, Zietz, A, Yiu, B, Mok, VCT, Polymeris, AA, Seiffge, D, Ambler, G, Wilson, D, Leung, TWH, Tsang, SF, Chu, W, Abrigo, J, Cheng, C, Lee, K-J, Lim, J-S, Shiozawa, M, Koga, M, Chabriat, H, Hennerici, M, Wong, YK, Mak, H, Collet, R, Inamura, S, Yoshifuji, K, Arsava, EM, Horstmann, S, Purrucker, J, Lam, BYK, Wong, A, Kim, YD, Song, T-J, Lemmens, R, Eppinger, S, Gattringer, T, Uysal, E, Demirelli, DS, Bornstein, NM, Assayag, EB, Hallevi, H, Molad, J, Nishihara, M, Tanaka, J, Coutts, SB, Kappelle, LJ, Al-Shahi Salman, R, Jager, R, Lip, GYH, Goeldlin, MB, Panos, LD, Mas, J-L, Legrand, L, Karayiannis, C, Phan, T, Bellut, M, Chappell, F, Makin, S, Hayden, D, Williams, D, van Dam-Nolen, DHK, Nederkoorn, PJ, Barbato, C, Browning, S, Wiegertjes, K, Tuladhar, AM, Mendyk, A-M, Köhler, S, van Oostenburgge, R, Zhou, Y, Xu, C, Hilal, S, Gyanwali, B, Chen, C, Lou, M, Staals, J, Bordet, R, Kandiah, N, de Leeuw, F-E, Simister, R, Hendrikse, J, Wardlaw, J, Kelly, P, Fluri, F, Srikanth, V, Calvet, D, Jung, S, Kwa Vincent, IH, Smith, EE, Hara, H, Yakushiji, Y, Orken, DN, Fazekas, F, Thijs, V, Heo, J-H, Veltkamp, R, Ay, H, Imaizumi, T, Lau, KK, Jouvent, E, Toyoda, K, Yoshimura, S, Bae, H-J, Martí-Fàbregas, J, Prats-Sánchez, L, Lyrer, P, Best, J, Werring, D, Engelter, ST, Peters, N & Network, TMIC 2023, 'Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation', Annals of Neurology, vol. 94, no. 1, pp. 61-74. https://doi.org/10.1002/ana.26642

@article{988f90bf195a415b91f116d2c08bb47f,

title = "Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation",

abstract = "Objectives Cerebral 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). Methods We 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. Results A 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, 95.76–4.26) and ischemic stroke (aHR = 1.29, 95.04–1.59). 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). Interpretation Patients 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",

author = "Yannie Soo and Annaelle Zietz and Brian Yiu and Mok, {Vincent C. T.} and Polymeris, {Alexandros A.} and David Seiffge and Gareth Ambler and Duncan Wilson and Leung, {Thomas Wai Hong} and Tsang, {Suk Fung} and Winnie Chu and Jill Abrigo and Cyrus Cheng and Keon-Joo Lee and Jae-Sung Lim and Masayuki Shiozawa and Masatoshi Koga and Hugues Chabriat and Michael Hennerici and Wong, {Yuen Kwun} and Henry Mak and Roger Collet and Shigeru Inamura and Kazuhisa Yoshifuji and Arsava, {Ethem Murat} and Solveig Horstmann and Jan Purrucker and Lam, {Bonnie Y. K.} and Adrian Wong and Kim, {Young Dae} and Tae-Jin Song and Robin Lemmens and Sebastian Eppinger and Thomas Gattringer and Ender Uysal and Demirelli, {Derya Sel{\c c}uk} and Bornstein, {Natan M.} and Assayag, {Einor Ben} and Hen Hallevi and Jeremy Molad and Masashi Nishihara and Jun Tanaka and Coutts, {Shelagh B.} and Kappelle, {L. Jaap} and {Al-Shahi Salman}, Rustam and Rolf Jager and Lip, {Gregory Y. H.} and Goeldlin, {Martina B.} and Panos, {Leonidas D.} and Jean-Louis Mas and Laurence Legrand and Chris Karayiannis and Thanh Phan and Maximilian Bellut and Francesca Chappell and Stephen Makin and Derek Hayden and David Williams and {van Dam-Nolen}, {Dianne H. K.} and Nederkoorn, {Paul J.} and Carmen Barbato and Simone Browning and Kim Wiegertjes and Tuladhar, {Anil Man} and Anne-Marie Mendyk and Sebastian K{\"o}hler and {van Oostenburgge}, Robert and Ying Zhou and Chao Xu and Saima Hilal and Bibek Gyanwali and Christopher Chen and Min Lou and Julie Staals and Regis Bordet and Nagaendran Kandiah and {de Leeuw}, Frank-Erik and Robert Simister and Jeroen Hendrikse and Joanna Wardlaw and Peter Kelly and Felix Fluri and Velandai Srikanth and David Calvet and Simon Jung and {Kwa Vincent}, {I. H.} and Smith, {Eric E.} and Hideo Hara and Yusuke Yakushiji and Orken, {Dilek Necioglu} and Franz Fazekas and Vincent Thijs and Ji-Hoe Heo and Roland Veltkamp and Hakan Ay and Toshio Imaizumi and Lau, {Kui Kai} and Eric Jouvent and Kazunori Toyoda and Sohei Yoshimura and Hee-Joon Bae and Joan Mart{\'i}-F{\`a}bregas and Luis Prats-S{\'a}nchez and Philippe Lyrer and Jonathan Best and David Werring and Engelter, {Stefan T.} and Nils Peters and Network, {the Microbleeds International Collaborative}",

note = "Acknowledgments This study was funded by the Swiss Heart Foundation. Furthermore, the study was funded in part by Wellcome Trust (WT088134/Z/09/A) and for the purpose of openaccess, co-authors have applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission. The authors would like to thank the patients that participated in the various cohorts. Open access funding provided by Universitat Basel. Research Funding Swiss Heart Foundation Wellcome [WT088134/Z/09/A] Open access funding provided by Universitat Basel.",

year = "2023",

month = jul,

doi = "10.1002/ana.26642",

language = "English",

volume = "94",

pages = "61--74",

journal = "Annals of Neurology",

issn = "0364-5134",

publisher = "John Wiley and Sons Inc.",

number = "1",

}

TY - JOUR

T1 - Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation

AU - Soo, Yannie

AU - Zietz, Annaelle

AU - Yiu, Brian

AU - Mok, Vincent C. T.

AU - Polymeris, Alexandros A.

AU - Seiffge, David

AU - Ambler, Gareth

AU - Wilson, Duncan

AU - Leung, Thomas Wai Hong

AU - Tsang, Suk Fung

AU - Chu, Winnie

AU - Abrigo, Jill

AU - Cheng, Cyrus

AU - Lee, Keon-Joo

AU - Lim, Jae-Sung

AU - Shiozawa, Masayuki

AU - Koga, Masatoshi

AU - Chabriat, Hugues

AU - Hennerici, Michael

AU - Wong, Yuen Kwun

AU - Mak, Henry

AU - Collet, Roger

AU - Inamura, Shigeru

AU - Yoshifuji, Kazuhisa

AU - Arsava, Ethem Murat

AU - Horstmann, Solveig

AU - Purrucker, Jan

AU - Lam, Bonnie Y. K.

AU - Wong, Adrian

AU - Kim, Young Dae

AU - Song, Tae-Jin

AU - Lemmens, Robin

AU - Eppinger, Sebastian

AU - Gattringer, Thomas

AU - Uysal, Ender

AU - Demirelli, Derya Selçuk

AU - Bornstein, Natan M.

AU - Assayag, Einor Ben

AU - Hallevi, Hen

AU - Molad, Jeremy

AU - Nishihara, Masashi

AU - Tanaka, Jun

AU - Coutts, Shelagh B.

AU - Kappelle, L. Jaap

AU - Al-Shahi Salman, Rustam

AU - Jager, Rolf

AU - Lip, Gregory Y. H.

AU - Goeldlin, Martina B.

AU - Panos, Leonidas D.

AU - Mas, Jean-Louis

AU - Legrand, Laurence

AU - Karayiannis, Chris

AU - Phan, Thanh

AU - Bellut, Maximilian

AU - Chappell, Francesca

AU - Makin, Stephen

AU - Hayden, Derek

AU - Williams, David

AU - van Dam-Nolen, Dianne H. K.

AU - Nederkoorn, Paul J.

AU - Barbato, Carmen

AU - Browning, Simone

AU - Wiegertjes, Kim

AU - Tuladhar, Anil Man

AU - Mendyk, Anne-Marie

AU - Köhler, Sebastian

AU - van Oostenburgge, Robert

AU - Zhou, Ying

AU - Xu, Chao

AU - Hilal, Saima

AU - Gyanwali, Bibek

AU - Chen, Christopher

AU - Lou, Min

AU - Staals, Julie

AU - Bordet, Regis

AU - Kandiah, Nagaendran

AU - de Leeuw, Frank-Erik

AU - Simister, Robert

AU - Hendrikse, Jeroen

AU - Wardlaw, Joanna

AU - Kelly, Peter

AU - Fluri, Felix

AU - Srikanth, Velandai

AU - Calvet, David

AU - Jung, Simon

AU - Kwa Vincent, I. H.

AU - Smith, Eric E.

AU - Hara, Hideo

AU - Yakushiji, Yusuke

AU - Orken, Dilek Necioglu

AU - Fazekas, Franz

AU - Thijs, Vincent

AU - Heo, Ji-Hoe

AU - Veltkamp, Roland

AU - Ay, Hakan

AU - Imaizumi, Toshio

AU - Lau, Kui Kai

AU - Jouvent, Eric

AU - Toyoda, Kazunori

AU - Yoshimura, Sohei

AU - Bae, Hee-Joon

AU - Martí-Fàbregas, Joan

AU - Prats-Sánchez, Luis

AU - Lyrer, Philippe

AU - Best, Jonathan

AU - Werring, David

AU - Engelter, Stefan T.

AU - Peters, Nils

AU - Network, the Microbleeds International Collaborative

N1 - Acknowledgments This study was funded by the Swiss Heart Foundation. Furthermore, the study was funded in part by Wellcome Trust (WT088134/Z/09/A) and for the purpose of openaccess, co-authors have applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission. The authors would like to thank the patients that participated in the various cohorts. Open access funding provided by Universitat Basel. Research Funding Swiss Heart Foundation Wellcome [WT088134/Z/09/A] Open access funding provided by Universitat Basel.

PY - 2023/7

Y1 - 2023/7

N2 - Objectives Cerebral 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). Methods We 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. Results A 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, 95.76–4.26) and ischemic stroke (aHR = 1.29, 95.04–1.59). 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). Interpretation Patients 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

AB - Objectives Cerebral 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). Methods We 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. Results A 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, 95.76–4.26) and ischemic stroke (aHR = 1.29, 95.04–1.59). 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). Interpretation Patients 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

U2 - 10.1002/ana.26642

DO - 10.1002/ana.26642

M3 - Article

SN - 0364-5134

VL - 94

SP - 61

EP - 74

JO - Annals of Neurology

JF - Annals of Neurology

IS - 1

ER -

Impact of Cerebral Microbleeds in Stroke Patients with Atrial Fibrillation

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