SARS-CoV-2 and Stroke Characteristics: A Report From the Multinational COVID-19 Stroke Study Group

Shima Shahjouei; Georgios Tsivgoulis; Ghasem Farahmand; Eric Koza; Ashkan Mowla; Alireza Vafaei Sadr; Arash Kia; Alaleh Vaghefi Far; Stefania Mondello; Achille Cernigliaro; Annemarei Ranta; Martin Punter; Faezeh Khodadadi; Soheil Naderi; Mirna Sabra; Mahtab Ramezani; Ali Amini Harandi; Oluwaseyi Olulana; Durgesh Chaudhary; Aicha Lyoubi; Bruce C V Campbell; Juan F Arenillas; Daniel Bock; Joan Montaner; Saeideh Aghayari Sheikh Neshin; Diana Aguiar de Sousa; Matthew S Tenser; Ana Aires; Mercedes de Lera Alfonso; Orkhan Alizada; Elsa Azevedo; Nitin Goyal; Zabihollah Babaeepour; Gelareh Banihashemi; Leo H Bonati; Carlo W Cereda; Jason J Chang; Miljenko Crnjakovic; Gian Marco De Marchis; Massimo Del Sette; Seyed Amir Ebrahimzadeh; Mehdi Farhoudi; Ilaria Gandoglia; Bruno Gonçalves; Christoph J Griessenauer; Mehmet Murat Hanci; Aristeidis H Katsanos; Christos Krogias; Ronen R Leker; Lev Lotman; Jeffrey Mai; Shailesh Male; Konark Malhotra; Branko Malojcic; Teresa Mesquita; Asadollah Mir Ghasemi; Hany Mohamed Aref; Zeinab Mohseni Afshar; Jusun Moon; Mika Niemelä; Behnam Rezai Jahromi; Lawrence Nolan; Abhi Pandhi; Jong-Ho Park; João Pedro Marto; Francisco Purroy; Sakineh Ranji-Burachaloo; Nuno Reis Carreira; Manuel Requena; Marta Rubiera; Seyed Aidin Sajedi; João Sargento-Freitas; Vijay K Sharma; Thorsten Steiner; Kristi Tempro; Guillaume Turc; Yasaman Ahmadzadeh; Mostafa Almasi-Dooghaee; Farhad Assarzadegan; Arefeh Babazadeh; Humain Baharvahdat; Fabricio Buchadid Cardoso; Apoorva Dev; Mohammad Ghorbani; Ava Hamidi; Zeynab Sadat Hasheminejad; Sahar Hojjat-Anasri Komachali; Fariborz Khorvash; Firas Kobeissy; Hamidreza Mirkarimi; Elahe Mohammadi-Vosough; Debdipto Misra; Ali Reza Noorian; Peyman Nowrouzi-Sohrabi; Sepideh Paybast; Leila Poorsaadat; Mehrdad Roozbeh; Behnam Sabayan; Saeideh Salehizadeh; Alia Saberi; Mercedeh Sepehrnia; Fahimeh Vahabizad; Thomas Alexandre Yasuda; Mojdeh Ghabaee; Nasrin Rahimian; Mohammad Hossein Harirchian; Afshin Borhani-Haghighi; Mahmoud Reza Azarpazhooh; Rohan Arora; Saeed Ansari; Venkatesh Avula; Jiang Li; Vida Abedi; Ramin Zand

doi:10.1161/STROKEAHA.120.032927

SARS-CoV-2 and Stroke Characteristics: A Report From the Multinational COVID-19 Stroke Study Group

Stroke. 2021 May;52(5):e117-e130. doi: 10.1161/STROKEAHA.120.032927. Epub 2021 Apr 21.

Authors

Shima Shahjouei¹, Georgios Tsivgoulis², Ghasem Farahmand^{3

4}, Eric Koza⁵, Ashkan Mowla^{1

6}, Alireza Vafaei Sadr⁷, Arash Kia⁸, Alaleh Vaghefi Far⁴, Stefania Mondello⁹, Achille Cernigliaro¹⁰, Annemarei Ranta¹¹, Martin Punter¹¹, Faezeh Khodadadi¹², Soheil Naderi¹³, Mirna Sabra¹⁴, Mahtab Ramezani¹⁵, Ali Amini Harandi¹⁵, Oluwaseyi Olulana⁵, Durgesh Chaudhary¹, Aicha Lyoubi¹⁶, Bruce C V Campbell¹⁷, Juan F Arenillas¹⁸, Daniel Bock¹⁹, Joan Montaner²⁰, Saeideh Aghayari Sheikh Neshin²¹, Diana Aguiar de Sousa^{22

23}, Matthew S Tenser⁶, Ana Aires^{24

25}, Mercedes de Lera Alfonso¹⁸, Orkhan Alizada²⁶, Elsa Azevedo^{24

25}, Nitin Goyal²⁷, Zabihollah Babaeepour²⁸, Gelareh Banihashemi²⁹, Leo H Bonati³⁰, Carlo W Cereda³¹, Jason J Chang³², Miljenko Crnjakovic³³, Gian Marco De Marchis³⁴, Massimo Del Sette³⁵, Seyed Amir Ebrahimzadeh³⁶, Mehdi Farhoudi³⁷, Ilaria Gandoglia³⁵, Bruno Gonçalves³⁸, Christoph J Griessenauer¹, Mehmet Murat Hanci²⁶, Aristeidis H Katsanos^{2

39}, Christos Krogias⁴⁰, Ronen R Leker⁴¹, Lev Lotman⁴², Jeffrey Mai⁴³, Shailesh Male⁴⁴, Konark Malhotra⁴⁵, Branko Malojcic⁴⁶, Teresa Mesquita⁴⁷, Asadollah Mir Ghasemi⁴⁸, Hany Mohamed Aref⁴⁹, Zeinab Mohseni Afshar⁵⁰, Jusun Moon⁵¹, Mika Niemelä⁵², Behnam Rezai Jahromi⁵², Lawrence Nolan⁴², Abhi Pandhi²⁷, Jong-Ho Park⁵³, João Pedro Marto⁴⁷, Francisco Purroy⁵⁴, Sakineh Ranji-Burachaloo³, Nuno Reis Carreira^{55

54}, Manuel Requena^{56

57}, Marta Rubiera^{56

57}, Seyed Aidin Sajedi⁵⁸, João Sargento-Freitas⁵⁹, Vijay K Sharma⁶⁰, Thorsten Steiner^{61

62}, Kristi Tempro⁴², Guillaume Turc³⁸, Yasaman Ahmadzadeh⁶³, Mostafa Almasi-Dooghaee^{64

65

66

67}, Farhad Assarzadegan, Arefeh Babazadeh⁶⁸, Humain Baharvahdat⁶⁹, Fabricio Buchadid Cardoso⁷⁰, Apoorva Dev¹², Mohammad Ghorbani⁶⁴, Ava Hamidi⁷¹, Zeynab Sadat Hasheminejad⁷², Sahar Hojjat-Anasri Komachali⁷³, Fariborz Khorvash⁷⁴, Firas Kobeissy^{14

75}, Hamidreza Mirkarimi⁷⁶, Elahe Mohammadi-Vosough⁷⁶, Debdipto Misra⁷⁷, Ali Reza Noorian⁷⁸, Peyman Nowrouzi-Sohrabi⁷⁹, Sepideh Paybast⁸⁰, Leila Poorsaadat⁸¹, Mehrdad Roozbeh⁸², Behnam Sabayan⁸³, Saeideh Salehizadeh⁸⁴, Alia Saberi²¹, Mercedeh Sepehrnia⁷², Fahimeh Vahabizad²⁹, Thomas Alexandre Yasuda⁷⁰, Mojdeh Ghabaee^{3

4}, Nasrin Rahimian⁸⁵, Mohammad Hossein Harirchian³, Afshin Borhani-Haghighi⁸⁶, Mahmoud Reza Azarpazhooh⁸⁷, Rohan Arora⁸⁸, Saeed Ansari²⁷, Venkatesh Avula⁸⁹, Jiang Li^{89

90}, Vida Abedi^{89

90}, Ramin Zand¹

Affiliations

¹ Neurology Department, Neuroscience Institute, Geisinger Health System, PA (S. Shahjouei, A. Mowla, D.C., C.J.G., R.Z.).
² Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, "Attikon" University Hospital, Greece (G. Tsivgoulis, A.H.K.).
³ Iranian Center of Neurological Research, Neuroscience Institute (G.F., S.R.-B., M. Ghabaee, M.H.H.), Tehran University of Medical Sciences, Iran.
⁴ Neurology Department (G.F., A.V.F., M. Ghabaee), Tehran University of Medical Sciences, Iran.
⁵ Geisinger Commonwealth School of Medicine, Scranton, PA (E.K., O.O.).
⁶ Division of Stroke and Endovascular Neurosurgery, Department of Neurological Surgery, Keck School of Medicine, University of Southern California, CA (A. Mowla, M.S.T.).
⁷ Department de Physique Theorique and Center for Astroparticle Physics, University Geneva, Switzerland (A.V.S.).
⁸ Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, Institute for Healthcare Delivery Science, New York City, NY (A.K.).
⁹ Department of Biomedical and Dental Sciences and Morphofunctional Imaging, University of Messina, Italy (S. Mondello).
¹⁰ Regional Health Authority of Sicily, Palermo, Italy (A.C.).
¹¹ Department of Neurology, Wellington Hospital, New Zealand and Department of Medicine, University of Otago, New Zealand (A.R., M.P.).
¹² PES University, Bangaluru, Karnataka, India (F. Khodadadi, A.D.).
¹³ Department of Neurosurgery (S.N.), Tehran University of Medical Sciences, Iran.
¹⁴ Neurosciences Research Center, Lebanese University/Medical School, Beirut, Lebanon (M. Sabra, F. Kobeissy).
¹⁵ Neurology Department, Shahid Beheshti University of Medical Sciences, Tehran, Iran (M. Ramezani, A.A.H.).
¹⁶ Neurology Department, Delafontaine Hospital, Saint-Denis, France (A.L.).
¹⁷ Department of Medicine and Neurology, Melbourne Brain Centre at the Royal Melbourne Hospital, University of Melbourne, Parkville, Australia (B.C.V.C.).
¹⁸ Department of Neurology, University of Valladolid, Spain (J.F.A., M.D.L.A.).
¹⁹ Department of Cardiology, Klinikum Frankfurt Höchst, Germany (D.B.).
²⁰ Department of Neurology, Hospital Universitario Virgen Macarena, Sevilla, Spain (J. Montaner).
²¹ Neurology Department, Poursina Hospital, Rasht, Guilan, Iran (S.A.S.N., A.S.).
²² Department of Neurology (D.A.d.S.), Hospital de Santa Maria, University of Lisbon, Portugal.
²³ Department of Neurology, Hospital de Santa Maria, University of Lisbon, Portugal (D.A.d.S.).
²⁴ Department of Neurology, Centro Hospitalar Universitário de São João, Porto, Portugal (A.A., E.A.).
²⁵ Department of Medicine, University of Porto, Portugal (A.A., E.A.).
²⁶ Neurosurgery Department, Istanbul University-Cerrahpasa, Cerrahpasa Medical Faculty, Turkey (O.A., M.M.H.).
²⁷ Department of Neurology, University of Tennessee (N.G., A.P., S.A.).
²⁸ Neurology Ward, Valiasr Hospital, Borujen, Iran (Z.B.).
²⁹ Imam Khomeini Hospital, and Neurology Department, Sina Hospital (G.B., F.V.), Tehran University of Medical Sciences, Iran.
³⁰ Department of Neurology and Stroke Unit, University Hospital Basel, Switzerland (L.H.B.).
³¹ Stroke Center, Neurocenter of Southern Switzerland, Lugano (C.W.C.).
³² Department of Critical Care Medicine, MedStar Washington Hospital Center, Washington, DC (J.J.C.).
³³ Intensive Care Unit, Department of Neurology, Clinical Hospital Dubrava, Zagreb, Croatia (M.C.).
³⁴ Neurorehabilitation Unit, University Center for Medicine of Aging and Rehabilitation Basel, Felix Platter Hospital, University of Basel, Switzerland (G.D.M.).
³⁵ Neurology Unit, Galliera Hospital, Genova, Italy (M.D.S., I.G.).
³⁶ Department of Radiology, Yasrebi Hospital, Kashan, Iran (S.A.E.).
³⁷ Neurosciences Research Center, Tabriz University of Medical Sciences, Iran (M.F.).
³⁸ Department of Neurology, GHU Paris Psychiatrie et Neurosciences, Université de Paris, INSERM U1266, France (B.G., G. Turc).
³⁹ Division of Neurology, McMaster University/Population Health Research Institute, Hamilton, ON, Canada (A.H.K.).
⁴⁰ Department of Neurology, St. Josef-Hospital, Ruhr University Bochum, Germany (C.K.).
⁴¹ Department of Neurology, Hadassah-Hebrew University Medical Center, Jerusalem, Israel (R.R.L.).
⁴² Department of Neurology, Albany Medical Center, NY (L.L., L.N., K.T.).
⁴³ Department of Neurosurgery, Georgetown University and MedStar Washington Hospital Center, DC (J. Mai).
⁴⁴ Department of Neurosurgery, Vidant Medical Center, Greenville, NC (S. Male).
⁴⁵ Department of Neurology, Allegheny Health Network, Pittsburgh, PA (K.M.).
⁴⁶ Department of Neurology, TIA Clinic, University Hospital Centre Zagreb, Zagreb School of Medicine, University of Zagreb, Croatia (B.M.).
⁴⁷ Department of Neurology, Hospital de Egas Moniz, Centro Hospitalar Lisboa Ocidental, Lisbon, Portugal (T.M., J.P.M.).
⁴⁸ Department of Anesthesiology, University of Ottawa, Canada (A.M.G.).
⁴⁹ Department of Neurology, Ain Shams University, Cairo, Egypt (H.M.A.).
⁵⁰ Infection Disease Research Center, Kermanshah University of Medical Sciences, Iran (Z.M.A.).
⁵¹ Department of Neurology, National Medical Center, Seoul, South Korea (J. Moon).
⁵² Department of Neurosurgery, Helsinki University and Helsinki University Hospital, Finland (M.N., B.R.J.).
⁵³ Department of Neurology, Myongji Hospital, Hanyang University College of Medicine, South Korea (J.-H.P.).
⁵⁴ Department of Neurology, Hospital Arnau de Vilanova, Institut de Recerca Biomèdica de Lleida, Universitat de Lleida, Spain (F.P., N.R.C.).
⁵⁵ Department of Internal Medicine (N.E.C.), Hospital de Santa Maria, University of Lisbon, Portugal.
⁵⁶ Stroke Unit, Department of Neurology, Hospital Vall d'Hebron Barcelona, Spain (M. Requena, M. Rubiera).
⁵⁷ Department de Medicina, Universitat Autònoma de Barcelona, Spain (M. Requena, M. Rubiera).
⁵⁸ Department of Neurology, Neuroscience Research Center, Golestan University of Medical Sciences, Iran (S.A.S.).
⁵⁹ Department of Neurology, Centro Hospitalar e Universitário de Coimbra, Coimbra, Portugal (J.S.-F.).
⁶⁰ Division of Neurology, University Medicine Cluster, National University Health System, Singapore (V.K.S.).
⁶¹ Department of Neurology, Klinikum Frankfurt Höchst, Germany (T.S.).
⁶² Department of Neurology, Heidelberg University Hospital, Germany (T.S.).
⁶³ Hospital for Special Surgery, New York City, NY (Y.A.).
⁶⁴ Divisions of Vascular and Endovascular Neurosurgery (M.A.-D., M. Ghorbani), Firoozgar Hospital, Iran University of Medical Sciences, Tehran.
⁶⁵ Neurology (M.A.-D.), Firoozgar Hospital, Iran University of Medical Sciences, Tehran.
⁶⁶ Divisions of Vascular and Endovascular Neurosurgery (M.A.-D.), Rasoul-Akram Hospital, Iran University of Medical Sciences, Tehran.
⁶⁷ Neurology (M.A.-D.), Rasoul-Akram Hospital, Iran University of Medical Sciences, Tehran.
⁶⁸ Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Iran (A.B.).
⁶⁹ Neurosurgical Department, Ghaem Hospital, Mashhad University of Medical Sciences, Iran (H.B.).
⁷⁰ Neurology Department, Centro Médico de Campinas, São Paulo, Brazil (F.B.C., T.A.Y.).
⁷¹ Neurology Ward, Gheshm Hospital, Iran (A.H.).
⁷² Department of Neurology, Imam Hosein Hospital, Shahid Beheshti Medical University, Tehran, Iran (Z.S.H., M. Sepehrnia).
⁷³ Department of Neurology, Pirooz Hospital, Gilan University of Medical Sciences, Lahijan, Iran (S.H.-A.K.).
⁷⁴ Neurology Department, Isfahan University of Medical Sciences, Iran (F. Khorvash).
⁷⁵ Program of Neurotrauma, Neuroproteomics and Biomarker Research, University of Florida (F. Kobeissy).
⁷⁶ Neurology Department, Modarres Hospital, Kashmar, Iran (H.M., E.M.-V.).
⁷⁷ Steele Institute of Health and Innovation, Geisinger Health System, PA (D.M.).
⁷⁸ Department of Neurology, Southern California Permanente Medical Group, Irvine, CA (A.R.N.).
⁷⁹ Student Research Committee (P.N.-S.), Shiraz University of Medical Sciences, Iran.
⁸⁰ Department of Neurology, Bou Ali Hospital, Qazvin University of Medical Sciences, Iran (S.P.).
⁸¹ Department of Neurology, Arak University of Medical Sciences, Iran (L.P.).
⁸² Brain Mapping Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran (M. Roozbeh).
⁸³ Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston (B.S.).
⁸⁴ Neurology Department, Salahadin Ayubi Hospital, Baneh, Iran (S. Salehizadeh).
⁸⁵ Department of Neurology, Yasrebi Hospital, Kashan, Iran (N.R.).
⁸⁶ Clinical Neurology Research Center (A.B.-H.), Shiraz University of Medical Sciences, Iran.
⁸⁷ Neurology Department, Western University, Canada (M.R.A.).
⁸⁸ Department of Neurology, Long Island Jewish Forest Hills, Queens, NY (R.A.).
⁸⁹ Department of Molecular and Functional Genomics, Geisinger Health System, Danville, PA (V. Avula, V. Abedi, J.L.).
⁹⁰ Biocomplexity Institute, Virginia Tech, Blacksburg, VA (J.L., V. Abedi).

Abstract

[Figure: see text].

Keywords: cerebrovascular disorders; intracranial hemorrhages; neuroimaging; stroke; venous thrombosis.

Publication types

Multicenter Study
Observational Study

MeSH terms

Adult
Aged
COVID-19 / complications*
COVID-19 / epidemiology
Female
Geography
Health Expenditures
Humans
International Cooperation
Intracranial Hemorrhages / complications*
Intracranial Hemorrhages / epidemiology
Ischemic Stroke / complications*
Ischemic Stroke / epidemiology
Male
Middle Aged
Prospective Studies
Risk
Sinus Thrombosis, Intracranial / complications*
Sinus Thrombosis, Intracranial / epidemiology
Treatment Outcome
Venous Thrombosis / complications*
Venous Thrombosis / epidemiology
Young Adult