Characteristics and Outcomes in Patients With COVID-19 and Acute Ischemic Stroke: The Global COVID-19 Stroke Registry

doi:10.1161/STROKEAHA.120.031208

. 2020 Sep;51(9):e254-e258.

doi: 10.1161/STROKEAHA.120.031208. Epub 2020 Jul 9.

Characteristics and Outcomes in Patients With COVID-19 and Acute Ischemic Stroke: The Global COVID-19 Stroke Registry

George Ntaios¹, Patrik Michel², Georgios Georgiopoulos³, Yutao Guo⁴, Wencheng Li⁵, Jing Xiong⁶, Patricia Calleja⁷, Fernando Ostos⁷, Guillermo González-Ortega⁷, Blanca Fuentes⁸, María Alonso de Leciñana⁸, Exuperio Díez-Tejedor⁸, Sebastian García-Madrona⁹, Jaime Masjuan⁹, Alicia DeFelipe⁹, Guillaume Turc¹⁰, Bruno Gonçalves^{10

11}, Valerie Domigo¹⁰, Gheorghe-Andrei Dan¹², Roxana Vezeteu¹², Hanne Christensen¹³, Louisa Marguerite Christensen¹³, Per Meden¹³, Lejla Hajdarevic¹³, Angela Rodriguez-Lopez¹⁴, Fernando Díaz-Otero¹⁴, Andrés García-Pastor¹⁴, Antonio Gil-Nuñez¹⁴, Errikos Maslias², Davide Strambo², David J Werring¹⁵, Arvind Chandratheva¹⁵, Laura Benjamin¹⁵, Robert Simister¹⁵, Richard Perry¹⁵, Rahma Beyrouti¹⁵, Pascal Jabbour¹⁶, Ahmad Sweid¹⁶, Stavropoula Tjoumakaris¹⁶, Elisa Cuadrado-Godia^{17

18}, Ana Rodríguez Campello^{17

18}, Jaume Roquer^{17

18}, Tiago Moreira^{19

20}, Michael V Mazya^{19

20}, Fabio Bandini²¹, Karl Matz²², Helle K Iversen²³, Alejandra González-Duarte²⁴, Cristina Tiu^{25

26}, Julia Ferrari²⁷, Milan R Vosko²⁸, Helmut J F Salzer²⁹, Bernd Lamprecht²⁹, Martin W Dünser³⁰, Carlo W Cereda³¹, Ángel Basilio Corredor Quintero³², Eleni Korompoki³³, Eduardo Soriano-Navarro³⁴, Luis Enrique Soto-Ramírez³⁴, Paulo F Castañeda-Méndez³⁴, Daniela Bay-Sansores³⁴, Antonio Arauz³⁵, Vanessa Cano-Nigenda³⁵, Espen Saxhaug Kristoffersen^{36

37}, Marjaana Tiainen³⁸, Daniel Strbian³⁸, Jukka Putaala³⁸, Gregory Y H Lip^{39

40}

Affiliations

¹ Department of Internal Medicine, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa, Greece (G.N.).
² Stroke Center, Neurology Service, Department of Clinical Neurosciences, Lausanne University Hospital, Switzerland (P.M., E.M., D. Strambo).
³ School of Biomedical Engineering and Imaging Sciences, King's College, London, United Kingdom (G.G.).
⁴ Department of Cardiology, Chinese PLA General Hospital, Beijing, China (Y.G.).
⁵ Department of Urology (W.L.), Union Hospital, Tongji Medical College, Huazhong University of Science & Technology, China.
⁶ Department of Nephrology (J.X.), Union Hospital, Tongji Medical College, Huazhong University of Science & Technology, China.
⁷ Department of Neurology and Stroke Center, Doce de Octubre University Hospital, Instituto de Investigación Hospital 12 de Octubre (i+12), Madrid, Spain (P.C., F.O., G.G.-O.).
⁸ Department of Neurology and Stroke Center, La Paz University Hospital, IdiPAZ Health Research Institute, Madrid, Spain (B.F., M.A.d.L., E.D.-T.).
⁹ Department of Neurology and Stroke Centre, Ramón y Cajal University Hospital, IRYCIS Health Research Institute, Madrid, Spain (S.G.-M., J.M., A.D.).
¹⁰ Department of Neurology, GHU Paris Psychiatrie et Neurosciences, Université de Paris, INSERM U1266, and FHU Neurovasc, France (G.T., B.G., V.D.).
¹¹ Intensive Care Unit, Paulo Niemeyer State Brain Institute, Rio de Janeiro, Brazil (B.G.).
¹² Colentina University Hospital, Medicine Faculty, University of Medicine "Carol Davila"-Bucharest, Romania (G.-A.D., R.V.).
¹³ Bispebjerg Hospital & University of Copenhagen, Denmark (H.C., L.M.C., P.M., L.H.).
¹⁴ Vascular Neurology Section - Stroke Center, Hospital General Universitario Gregorio Marañón, Madrid, Spain (A.R.L., F.D.O., A.G.P., A.G.-N.).
¹⁵ Stroke Research Centre, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, London, United Kingdom (D.J.W., A.C., L.B., R.S., R.P., R.B.).
¹⁶ Department of Neurological Surgery, Thomas Jefferson University Hospital, Philadelphia, PA (P.J., A.S., S.T.).
¹⁷ Stroke Unit, Department of Neurology, Hospital del Mar (E.C.-G., A.R.C., J.R.).
¹⁸ Neurovascular Research Group, IMIM-Hospital del Mar (Institut Hospital del Mar d'Investigacions Mèdiques), Universitat Autònoma de Barcelona/DCEXS-Universitat Pompeu Fabra, Barcelona, Spain (E.C.-G., A.R.C., J.R.).
¹⁹ Department of Clinical Neuroscience (T.M., M.V.M.), Karolinska Institutet, Stockholm, Sweden.
²⁰ Department of Neurology (T.M., M.V.M.), Karolinska Institutet, Stockholm, Sweden.
²¹ Department of Neurology, San Paolo Hospital, Savona, Italy (F.B.).
²² Landesklinikum Mödling, Neurologische Abteilung und Donau-Universität Krems, Zentrum für Vaskuläre Prävention, Krems, Austria (K.M.).
²³ Stroke Centre Rigshospitalet, Department of Neurology, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark (H.K.I.).
²⁴ Department of Neurology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, a COVID Center, Mexico City (A.G.-D.).
²⁵ Carol Davila University of Medicine and Pharmacy, Bucharest, Romania (C.T.).
²⁶ University Emergency Hospital, Bucharest, Romania (C.T.).
²⁷ Department of Neurology, Krankenhaus Barmherzige Brüder, Vienna, Austria (J.F.).
²⁸ Department of Neurology 2 (M.R.V.), Kepler University Hospital, Linz, Austria.
²⁹ Department of Pulmonary Medicine (H.J.F.S., B.L.), Kepler University Hospital, Linz, Austria.
³⁰ Department of Anesthesiology and Intensive Care Medicine, Johannes Kepler University, Linz, Austria (M.W.D.).
³¹ Stroke Center EOC, Neurocenter of Southern Switzerland, Lugano (C.W.C.).
³² Department of Neurology, Hospital Departamental Universitario del Quindío San Juan de DiosArmenia, Colombia (Á.B.C.Q.).
³³ Department of Clinical Therapeutics, National and Kapodistrian University of Athens, Alexandra Hospital, Greece (E.K.).
³⁴ Internal Medicine, Fundación Clínica Médica Sur, Mexico City (E.S.-N., L.E.S.-R., P.F.C.-M., D.B.-S.).
³⁵ Stroke Clinic, Instituto Nacional de Neurologia y Neurocirugia Manuel Velasco Suarez, Mexico City (A.A., V.C.-N.).
³⁶ Department of Neurology, Akershus University Hospital, Norway (E.S.K.).
³⁷ Department of General Practice, HELSAM, University of Oslo (E.S.K.).
³⁸ Department of Neurology, Helsinki University Hospital, Finland (M.T., D. Strbian, J.P.).
³⁹ Liverpool Centre for Cardiovascular Science, University of Liverpool and Liverpool Heart & Chest Hospital, United Kingdom (G.Y.H.L.).
⁴⁰ Aalborg Thrombosis Research Unit, Department of Clinical Medicine, Aalborg University, Denmark (G.Y.H.L.).

PMID: 32787707
PMCID: PMC7359900
DOI: 10.1161/STROKEAHA.120.031208

Characteristics and Outcomes in Patients With COVID-19 and Acute Ischemic Stroke: The Global COVID-19 Stroke Registry

George Ntaios et al. Stroke. 2020 Sep.

. 2020 Sep;51(9):e254-e258.

doi: 10.1161/STROKEAHA.120.031208. Epub 2020 Jul 9.

Authors

Affiliations

¹ Department of Internal Medicine, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa, Greece (G.N.).
² Stroke Center, Neurology Service, Department of Clinical Neurosciences, Lausanne University Hospital, Switzerland (P.M., E.M., D. Strambo).
³ School of Biomedical Engineering and Imaging Sciences, King's College, London, United Kingdom (G.G.).
⁴ Department of Cardiology, Chinese PLA General Hospital, Beijing, China (Y.G.).
⁵ Department of Urology (W.L.), Union Hospital, Tongji Medical College, Huazhong University of Science & Technology, China.
⁶ Department of Nephrology (J.X.), Union Hospital, Tongji Medical College, Huazhong University of Science & Technology, China.
⁷ Department of Neurology and Stroke Center, Doce de Octubre University Hospital, Instituto de Investigación Hospital 12 de Octubre (i+12), Madrid, Spain (P.C., F.O., G.G.-O.).
⁸ Department of Neurology and Stroke Center, La Paz University Hospital, IdiPAZ Health Research Institute, Madrid, Spain (B.F., M.A.d.L., E.D.-T.).
⁹ Department of Neurology and Stroke Centre, Ramón y Cajal University Hospital, IRYCIS Health Research Institute, Madrid, Spain (S.G.-M., J.M., A.D.).
¹⁰ Department of Neurology, GHU Paris Psychiatrie et Neurosciences, Université de Paris, INSERM U1266, and FHU Neurovasc, France (G.T., B.G., V.D.).
¹¹ Intensive Care Unit, Paulo Niemeyer State Brain Institute, Rio de Janeiro, Brazil (B.G.).
¹² Colentina University Hospital, Medicine Faculty, University of Medicine "Carol Davila"-Bucharest, Romania (G.-A.D., R.V.).
¹³ Bispebjerg Hospital & University of Copenhagen, Denmark (H.C., L.M.C., P.M., L.H.).
¹⁴ Vascular Neurology Section - Stroke Center, Hospital General Universitario Gregorio Marañón, Madrid, Spain (A.R.L., F.D.O., A.G.P., A.G.-N.).
¹⁵ Stroke Research Centre, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, London, United Kingdom (D.J.W., A.C., L.B., R.S., R.P., R.B.).
¹⁶ Department of Neurological Surgery, Thomas Jefferson University Hospital, Philadelphia, PA (P.J., A.S., S.T.).
¹⁷ Stroke Unit, Department of Neurology, Hospital del Mar (E.C.-G., A.R.C., J.R.).
¹⁸ Neurovascular Research Group, IMIM-Hospital del Mar (Institut Hospital del Mar d'Investigacions Mèdiques), Universitat Autònoma de Barcelona/DCEXS-Universitat Pompeu Fabra, Barcelona, Spain (E.C.-G., A.R.C., J.R.).
¹⁹ Department of Clinical Neuroscience (T.M., M.V.M.), Karolinska Institutet, Stockholm, Sweden.
²⁰ Department of Neurology (T.M., M.V.M.), Karolinska Institutet, Stockholm, Sweden.
²¹ Department of Neurology, San Paolo Hospital, Savona, Italy (F.B.).
²² Landesklinikum Mödling, Neurologische Abteilung und Donau-Universität Krems, Zentrum für Vaskuläre Prävention, Krems, Austria (K.M.).
²³ Stroke Centre Rigshospitalet, Department of Neurology, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark (H.K.I.).
²⁴ Department of Neurology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, a COVID Center, Mexico City (A.G.-D.).
²⁵ Carol Davila University of Medicine and Pharmacy, Bucharest, Romania (C.T.).
²⁶ University Emergency Hospital, Bucharest, Romania (C.T.).
²⁷ Department of Neurology, Krankenhaus Barmherzige Brüder, Vienna, Austria (J.F.).
²⁸ Department of Neurology 2 (M.R.V.), Kepler University Hospital, Linz, Austria.
²⁹ Department of Pulmonary Medicine (H.J.F.S., B.L.), Kepler University Hospital, Linz, Austria.
³⁰ Department of Anesthesiology and Intensive Care Medicine, Johannes Kepler University, Linz, Austria (M.W.D.).
³¹ Stroke Center EOC, Neurocenter of Southern Switzerland, Lugano (C.W.C.).
³² Department of Neurology, Hospital Departamental Universitario del Quindío San Juan de DiosArmenia, Colombia (Á.B.C.Q.).
³³ Department of Clinical Therapeutics, National and Kapodistrian University of Athens, Alexandra Hospital, Greece (E.K.).
³⁴ Internal Medicine, Fundación Clínica Médica Sur, Mexico City (E.S.-N., L.E.S.-R., P.F.C.-M., D.B.-S.).
³⁵ Stroke Clinic, Instituto Nacional de Neurologia y Neurocirugia Manuel Velasco Suarez, Mexico City (A.A., V.C.-N.).
³⁶ Department of Neurology, Akershus University Hospital, Norway (E.S.K.).
³⁷ Department of General Practice, HELSAM, University of Oslo (E.S.K.).
³⁸ Department of Neurology, Helsinki University Hospital, Finland (M.T., D. Strbian, J.P.).
³⁹ Liverpool Centre for Cardiovascular Science, University of Liverpool and Liverpool Heart & Chest Hospital, United Kingdom (G.Y.H.L.).
⁴⁰ Aalborg Thrombosis Research Unit, Department of Clinical Medicine, Aalborg University, Denmark (G.Y.H.L.).

PMID: 32787707
PMCID: PMC7359900
DOI: 10.1161/STROKEAHA.120.031208

Abstract

Recent case-series of small size implied a pathophysiological association between coronavirus disease 2019 (COVID-19) and severe large-vessel acute ischemic stroke. Given that severe strokes are typically associated with poor prognosis and can be very efficiently treated with recanalization techniques, confirmation of this putative association is urgently warranted in a large representative patient cohort to alert stroke clinicians, and inform pre- and in-hospital acute stroke patient pathways. We pooled all consecutive patients hospitalized with laboratory-confirmed COVID-19 and acute ischemic stroke in 28 sites from 16 countries. To assess whether stroke severity and outcomes (assessed at discharge or at the latest assessment for those patients still hospitalized) in patients with acute ischemic stroke are different between patients with COVID-19 and non-COVID-19, we performed 1:1 propensity score matching analyses of our COVID-19 patients with non-COVID-19 patients registered in the Acute Stroke Registry and Analysis of Lausanne Registry between 2003 and 2019. Between January 27, 2020, and May 19, 2020, 174 patients (median age 71.2 years; 37.9% females) with COVID-19 and acute ischemic stroke were hospitalized (median of 12 patients per site). The median National Institutes of Health Stroke Scale was 10 (interquartile range [IQR], 4-18). In the 1:1 matched sample of 336 patients with COVID-19 and non-COVID-19, the median National Institutes of Health Stroke Scale was higher in patients with COVID-19 (10 [IQR, 4-18] versus 6 [IQR, 3-14]), P=0.03; (odds ratio, 1.69 [95% CI, 1.08-2.65] for higher National Institutes of Health Stroke Scale score). There were 48 (27.6%) deaths, of which 22 were attributed to COVID-19 and 26 to stroke. Among 96 survivors with available information about disability status, 49 (51%) had severe disability at discharge. In the propensity score-matched population (n=330), patients with COVID-19 had higher risk for severe disability (median mRS 4 [IQR, 2-6] versus 2 [IQR, 1-4], P<0.001) and death (odds ratio, 4.3 [95% CI, 2.22-8.30]) compared with patients without COVID-19. Our findings suggest that COVID-19 associated ischemic strokes are more severe with worse functional outcome and higher mortality than non-COVID-19 ischemic strokes.

Keywords: COVID-19; coronavirus; prognosis; propensity score; survivors.

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References

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1. Beyrouti R, Adams ME, Benjamin L, Cohen H, Farmer SF, Goh YY, Humphries F, Jager HR, Losseff NA, Perry RJ, et al. Characteristics of ischaemic stroke associated with covid-19. J Neurol Neurosurg Psychiatry. 2020doi: 10.1136/jnnp-2020-323586 - PMC - PubMed
1. Yaghi S, Ishida K, Torres J, Mac Grory B, Raz E, Humbert K, Henninger N, Trivedi T, Lillemoe K, Alam S, et al. SARS-CoV-2 and stroke in a New York healthcare system. Stroke. 2020; 51:2002–2011. doi: 10.1161/STROKEAHA.120.030335 - PMC - PubMed
1. Michel P, Odier C, Rutgers M, Reichhart M, Maeder P, Meuli R, Wintermark M, Maghraoui A, Faouzi M, Croquelois A, et al. The Acute STroke Registry and Analysis of Lausanne (ASTRAL): design and baseline analysis of an ischemic stroke registry including acute multimodal imaging. Stroke. 2010; 41:2491–2498. doi: 10.1161/STROKEAHA.110.596189 - PubMed

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[1] Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, Nigoghossian C, Ageno W, Madjid M, Guo Y, et al. ; Global COVID-19 Thrombosis Collaborative Group, Endorsed by the ISTH, NATF, ESVM, and the IUA, Supported by the ESC Working Group on Pulmonary Circulation and Right Ventricular Function. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. J Am Coll Cardiol. 2020; 75:2950–2973. doi: 10.1016/j.jacc.2020.04.031 - PMC - PubMed

[2] Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, Nigoghossian C, Ageno W, Madjid M, Guo Y, et al. ; Global COVID-19 Thrombosis Collaborative Group, Endorsed by the ISTH, NATF, ESVM, and the IUA, Supported by the ESC Working Group on Pulmonary Circulation and Right Ventricular Function. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. J Am Coll Cardiol. 2020; 75:2950–2973. doi: 10.1016/j.jacc.2020.04.031 - PMC - PubMed

[3] Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, De Leacy RA, Shigematsu T, Ladner TR, Yaeger KA, et al. Large-vessel stroke as a presenting feature of Covid-19 in the young. N Engl J Med. 2020; 382:e60.doi: 10.1056/NEJMc2009787 - PMC - PubMed

[4] Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, De Leacy RA, Shigematsu T, Ladner TR, Yaeger KA, et al. Large-vessel stroke as a presenting feature of Covid-19 in the young. N Engl J Med. 2020; 382:e60.doi: 10.1056/NEJMc2009787 - PMC - PubMed

[5] Beyrouti R, Adams ME, Benjamin L, Cohen H, Farmer SF, Goh YY, Humphries F, Jager HR, Losseff NA, Perry RJ, et al. Characteristics of ischaemic stroke associated with covid-19. J Neurol Neurosurg Psychiatry. 2020doi: 10.1136/jnnp-2020-323586 - PMC - PubMed

[6] Beyrouti R, Adams ME, Benjamin L, Cohen H, Farmer SF, Goh YY, Humphries F, Jager HR, Losseff NA, Perry RJ, et al. Characteristics of ischaemic stroke associated with covid-19. J Neurol Neurosurg Psychiatry. 2020doi: 10.1136/jnnp-2020-323586 - PMC - PubMed

[7] Yaghi S, Ishida K, Torres J, Mac Grory B, Raz E, Humbert K, Henninger N, Trivedi T, Lillemoe K, Alam S, et al. SARS-CoV-2 and stroke in a New York healthcare system. Stroke. 2020; 51:2002–2011. doi: 10.1161/STROKEAHA.120.030335 - PMC - PubMed

[8] Yaghi S, Ishida K, Torres J, Mac Grory B, Raz E, Humbert K, Henninger N, Trivedi T, Lillemoe K, Alam S, et al. SARS-CoV-2 and stroke in a New York healthcare system. Stroke. 2020; 51:2002–2011. doi: 10.1161/STROKEAHA.120.030335 - PMC - PubMed

[9] Michel P, Odier C, Rutgers M, Reichhart M, Maeder P, Meuli R, Wintermark M, Maghraoui A, Faouzi M, Croquelois A, et al. The Acute STroke Registry and Analysis of Lausanne (ASTRAL): design and baseline analysis of an ischemic stroke registry including acute multimodal imaging. Stroke. 2010; 41:2491–2498. doi: 10.1161/STROKEAHA.110.596189 - PubMed

[10] Michel P, Odier C, Rutgers M, Reichhart M, Maeder P, Meuli R, Wintermark M, Maghraoui A, Faouzi M, Croquelois A, et al. The Acute STroke Registry and Analysis of Lausanne (ASTRAL): design and baseline analysis of an ischemic stroke registry including acute multimodal imaging. Stroke. 2010; 41:2491–2498. doi: 10.1161/STROKEAHA.110.596189 - PubMed

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Characteristics and Outcomes in Patients With COVID-19 and Acute Ischemic Stroke: The Global COVID-19 Stroke Registry

Affiliations

Characteristics and Outcomes in Patients With COVID-19 and Acute Ischemic Stroke: The Global COVID-19 Stroke Registry

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