SARS-CoV-2 and Stroke Characteristics: A Report From the Multinational COVID-19 Stroke Study Group
Shima Shahjouei
(1)
,
Georgios Tsivgoulis
(2, 3)
,
Ghasem Farahmand
(4)
,
Eric Koza
(5)
,
Ashkan Mowla
(1, 6)
,
Alireza Vafaei Sadr
(7)
,
Arash Kia
(8)
,
Alaleh Vaghefi Far
(4)
,
Stefania Mondello
(9)
,
Achille Cernigliaro
(10)
,
Annemarei Ranta
(11)
,
Martin Punter
(11)
,
Faezeh Khodadadi
(12)
,
Soheil Naderi
(4)
,
Mirna Sabra
(13)
,
Mahtab Ramezani
(14)
,
Ali Amini Harandi
(14)
,
Oluwaseyi Olulana
(5)
,
Durgesh Chaudhary
(1)
,
Aicha Lyoubi
(15)
,
Bruce Campbell
(16)
,
Juan F Arenillas
(17)
,
Daniel Bock
(18)
,
Joan Montaner
(19)
,
Saeideh Aghayari Sheikh Neshin
(20)
,
Diana Aguiar de Sousa
(21)
,
Matthew S Tenser
(6)
,
Ana Aires
(22, 23)
,
Mercedes de Lera Alfonso
(17)
,
Orkhan Alizada
(24)
,
Elsa Azevedo
(22, 23)
,
Nitin Goyal
(25)
,
Zabihollah Babaeepour
(26)
,
Gelareh Banihashemi
(4)
,
Leo H Bonati
(27)
,
Carlo W Cereda
(28)
,
Jason Chang
(29)
,
Miljenko Crnjakovic
(30)
,
Gian Marco de Marchis
(31)
,
Massimo del Sette
(32)
,
Seyed Amir Ebrahimzadeh
(33)
,
Mehdi Farhoudi
(34)
,
Ilaria Gandoglia
(32)
,
Bruno Gonçalves
(35)
,
Christoph Griessenauer
(1)
,
Mehmet Murat Hanci
(24)
,
Aristeidis Katsanos
(36)
,
Christos Krogias
(37)
,
Ronen Leker
(38)
,
Lev Lotman
(39)
,
Jeffrey Mai
(40)
,
Shailesh Male
(41)
,
Konark Malhotra
(42)
,
Branko Malojcic
(43, 44)
,
Teresa Mesquita
(45)
,
Asadollah Mir Ghasemi
(46)
,
Hany Mohamed Aref
(47)
,
Zeinab Mohseni Afshar
(48)
,
Jusun Moon
(49)
,
Mika Niemelä
(50, 51)
,
Behnam Rezai Jahromi
(50, 51)
,
Lawrence Nolan
(39)
,
Abhi Pandhi
(25)
,
Jong-Ho Park
(52)
,
João Pedro Marto
(45)
,
Francisco Purroy
(53)
,
Sakineh Ranji-Burachaloo
(4)
,
Nuno Reis Carreira
(53, 21)
,
Manuel Requena
(54, 55)
,
Marta Rubiera
(54, 55)
,
Seyed Aidin Sajedi
(56)
,
João Sargento-Freitas
(57)
,
Vijay Sharma
(58)
,
Thorsten Steiner
(18, 59)
,
Kristi Tempro
(39)
,
Guillaume Turc
(35)
,
Yasaman Ahmadzadeh
(60)
,
Mostafa Almasi-Dooghaee
(61)
,
Farhad Assarzadegan
(62)
,
Arefeh Babazadeh
(63)
,
Humain Baharvahdat
(64)
,
Fabricio Buchadid Cardoso
(65)
,
Apoorva Dev
(12)
,
Mohammad Ghorbani
(61)
,
Ava Hamidi
(66)
,
Zeynab Sadat Hasheminejad
(14)
,
Sahar Hojjat-Anasri Komachali
(67)
,
Fariborz Khorvash
(68)
,
Firas Kobeissy
(13, 69)
,
Hamidreza Mirkarimi
(70)
,
Elahe Mohammadi-Vosough
(70)
,
Debdipto Misra
(1)
,
Ali Reza Noorian
(71)
,
Peyman Nowrouzi-Sohrabi
(72)
,
Sepideh Paybast
(73)
,
Leila Poorsaadat
(74)
,
Mehrdad Roozbeh
(14)
,
Behnam Sabayan
(75)
,
Saeideh Salehizadeh
(76)
,
Alia Saberi
(20)
,
Mercedeh Sepehrnia
(14)
,
Fahimeh Vahabizad
(4)
,
Thomas Alexandre Yasuda
(65)
,
Mojdeh Ghabaee
(4)
,
Nasrin Rahimian
(33)
,
Mohammad Hossein Harirchian
(4)
,
Afshin Borhani-Haghighi
(72)
,
Mahmoud Reza Azarpazhooh
(77)
,
Rohan Arora
(78)
,
Saeed Ansari
(25)
,
Venkatesh Avula
(1)
,
Jiang Li
(1, 79)
,
Vida Abedi
(1, 79)
,
Ramin Zand
(1)
1
Geisinger Health System [Danville, PA, USA]
2 NKUA - National and Kapodistrian University of Athens
3 “Attikon” University Hospital
4 TUMS - Tehran University of Medical Sciences
5 Geisinger Commonwealth School of Medicine [Scranton, PA, USA]
6 USC - University of Southern California
7 UNIGE - Université de Genève = University of Geneva
8 MSSM - Icahn School of Medicine at Mount Sinai [New York]
9 University of Messina
10 Regional Health Authority of Sicily [Palermo]
11 University of Otago [Dunedin, Nouvelle-Zélande]
12 PES University [Bangalore]
13 LU / ULB - الجامعة اللبنانية [بيروت] = Lebanese University [Beirut] = Université libanaise [Beyrouth]
14 SBUMS - Shahid Beheshti University of Medical Sciences [Tehran]
15 Hôpital Delafontaine
16 University of Melbourne
17 UVa - Universidad de Valladolid [Valladolid]
18 Klinikum Frankfurt Höchst
19 University Hospital Virgen Macarena [Sevilla]
20 Poursina Hospital
21 ULISBOA - Universidade de Lisboa = University of Lisbon
22 Centro Hospitalar Universitário de São João [Porto]
23 Universidade do Porto = University of Porto
24 Cerrahpasa Faculty of Medicine
25 UTC - University of Tennessee [Chattanooga]
26 Valiasr Hospital [Borujen]
27 University Hospital Basel [Basel]
28 Neurocenter of Southern Switzerland
29 MedStar Washington Hospital Center
30 CHD - Clinical Hospital Dubrava [Zagreb, Croatia]
31 Unibas - Université de Bâle = University of Basel = Basel Universität
32 Galliera Hospital [Genova, Italy]
33 YH - Yasrebi Hospital [Kashan, Iran]
34 TUOMS - Tabriz University of Medical Sciences [Tabriz, Iran]
35 IPNP - U1266 Inserm - Institut de psychiatrie et neurosciences de Paris
36 McMaster University [Hamilton, Ontario]
37 RUB - Ruhr University Bochum = Ruhr-Universität Bochum
38 Hadassah Hebrew University Medical Center [Jerusalem]
39 Albany Medical College
40 Georgetown University Medical Center
41 VMC - Vidant Medical Center [Greenville, NC, USA]
42 AHN - Allegheny Health Network [Pittsburgh, PA, USA]
43 University Hospital Centre Zagreb
44 University of Zagreb
45 Hospital De Egas Moniz [Lisbon]
46 University of Ottawa [Ottawa]
47 ASU - Ain Shams University
48 Kermanshah University of Medical Sciences
49 Asan Medical Center [Seoul]
50 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
51 HUS - Helsinki University Hospital [Finland]
52 Hanyang University College of Medicine
53 Universitat de Lleida
54 Vall d'Hebron University Hospital [Barcelona]
55 UAB - Universitat Autònoma de Barcelona = Autonomous University of Barcelona = Universidad Autónoma de Barcelona
56 Golestan University of Medical Sciences
57 Universidade de Coimbra [Coimbra]
58 NUHS - National University Health System [Singapore]
59 Heidelberg University Hospital [Heidelberg]
60 Hospital for Special Surgery
61 Iran University of Medical Sciences
62 Shahid Beheshti University
63 Babol University of Medical Sciences
64 Mashhad University of Medical Sciences
65 Centro Médico de Campinas [São Paulo]
66 Gheshm Hospital
67 Gilan University of Medical Sciences [Lahijan]
68 MUI - Isfahan University of Medical Sciences [Iran]
69 UF - University of Florida [Gainesville]
70 Modarres Hospital [Kashmar]
71 Southern California Permanente Medical Group
72 SUMS - Shiraz University of Medical Sciences [Iran]
73 Qazvin University of Medical Sciences
74 Arak University of Medical Sciences
75 HMS - Harvard Medical School [Boston]
76 Salahadin Ayubi Hospital [Baneh]
77 UWO - University of Western Ontario
78 Long Island Jewish Forest Hills [New York]
79 Biocomplexity Institute of Virginia Tech [Blacksburg]
2 NKUA - National and Kapodistrian University of Athens
3 “Attikon” University Hospital
4 TUMS - Tehran University of Medical Sciences
5 Geisinger Commonwealth School of Medicine [Scranton, PA, USA]
6 USC - University of Southern California
7 UNIGE - Université de Genève = University of Geneva
8 MSSM - Icahn School of Medicine at Mount Sinai [New York]
9 University of Messina
10 Regional Health Authority of Sicily [Palermo]
11 University of Otago [Dunedin, Nouvelle-Zélande]
12 PES University [Bangalore]
13 LU / ULB - الجامعة اللبنانية [بيروت] = Lebanese University [Beirut] = Université libanaise [Beyrouth]
14 SBUMS - Shahid Beheshti University of Medical Sciences [Tehran]
15 Hôpital Delafontaine
16 University of Melbourne
17 UVa - Universidad de Valladolid [Valladolid]
18 Klinikum Frankfurt Höchst
19 University Hospital Virgen Macarena [Sevilla]
20 Poursina Hospital
21 ULISBOA - Universidade de Lisboa = University of Lisbon
22 Centro Hospitalar Universitário de São João [Porto]
23 Universidade do Porto = University of Porto
24 Cerrahpasa Faculty of Medicine
25 UTC - University of Tennessee [Chattanooga]
26 Valiasr Hospital [Borujen]
27 University Hospital Basel [Basel]
28 Neurocenter of Southern Switzerland
29 MedStar Washington Hospital Center
30 CHD - Clinical Hospital Dubrava [Zagreb, Croatia]
31 Unibas - Université de Bâle = University of Basel = Basel Universität
32 Galliera Hospital [Genova, Italy]
33 YH - Yasrebi Hospital [Kashan, Iran]
34 TUOMS - Tabriz University of Medical Sciences [Tabriz, Iran]
35 IPNP - U1266 Inserm - Institut de psychiatrie et neurosciences de Paris
36 McMaster University [Hamilton, Ontario]
37 RUB - Ruhr University Bochum = Ruhr-Universität Bochum
38 Hadassah Hebrew University Medical Center [Jerusalem]
39 Albany Medical College
40 Georgetown University Medical Center
41 VMC - Vidant Medical Center [Greenville, NC, USA]
42 AHN - Allegheny Health Network [Pittsburgh, PA, USA]
43 University Hospital Centre Zagreb
44 University of Zagreb
45 Hospital De Egas Moniz [Lisbon]
46 University of Ottawa [Ottawa]
47 ASU - Ain Shams University
48 Kermanshah University of Medical Sciences
49 Asan Medical Center [Seoul]
50 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
51 HUS - Helsinki University Hospital [Finland]
52 Hanyang University College of Medicine
53 Universitat de Lleida
54 Vall d'Hebron University Hospital [Barcelona]
55 UAB - Universitat Autònoma de Barcelona = Autonomous University of Barcelona = Universidad Autónoma de Barcelona
56 Golestan University of Medical Sciences
57 Universidade de Coimbra [Coimbra]
58 NUHS - National University Health System [Singapore]
59 Heidelberg University Hospital [Heidelberg]
60 Hospital for Special Surgery
61 Iran University of Medical Sciences
62 Shahid Beheshti University
63 Babol University of Medical Sciences
64 Mashhad University of Medical Sciences
65 Centro Médico de Campinas [São Paulo]
66 Gheshm Hospital
67 Gilan University of Medical Sciences [Lahijan]
68 MUI - Isfahan University of Medical Sciences [Iran]
69 UF - University of Florida [Gainesville]
70 Modarres Hospital [Kashmar]
71 Southern California Permanente Medical Group
72 SUMS - Shiraz University of Medical Sciences [Iran]
73 Qazvin University of Medical Sciences
74 Arak University of Medical Sciences
75 HMS - Harvard Medical School [Boston]
76 Salahadin Ayubi Hospital [Baneh]
77 UWO - University of Western Ontario
78 Long Island Jewish Forest Hills [New York]
79 Biocomplexity Institute of Virginia Tech [Blacksburg]
Georgios Tsivgoulis
- Fonction : Auteur
- PersonId : 776614
- ORCID : 0000-0001-5059-4095
- IdRef : 098880470
Gian Marco de Marchis
- Fonction : Auteur
- PersonId : 808012
- ORCID : 0000-0002-0342-9780
Bruno Gonçalves
- Fonction : Auteur
- PersonId : 773121
- ORCID : 0000-0001-7046-0123
Thorsten Steiner
- Fonction : Auteur
- PersonId : 763297
- ORCID : 0000-0003-0651-1939
Guillaume Turc
- Fonction : Auteur
- PersonId : 776614
- ORCID : 0000-0001-5059-4095
- IdRef : 098880470
Humain Baharvahdat
- Fonction : Auteur
- PersonId : 808013
- ORCID : 0000-0002-1154-8843
Résumé
Background and Purpose: Stroke is reported as a consequence of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection in several reports. However, data are sparse regarding the details of these patients in a multinational and large scale. Methods: We conducted a multinational observational study on features of consecutive acute ischemic stroke, intracranial hemorrhage, and cerebral venous or sinus thrombosis among SARS-CoV-2–infected patients. We further investigated the risk of large vessel occlusion, stroke severity as measured by the National Institutes of Health Stroke Scale, and stroke subtype as measured by the TOAST (Trial of ORG 10172 in Acute Stroke Treatment) criteria among patients with acute ischemic stroke. In addition, we explored the neuroimaging findings, features of patients who were asymptomatic for SARS-CoV-2 infection at stroke onset, and the impact of geographic regions and countries’ health expenditure on outcomes. Results: Among the 136 tertiary centers of 32 countries who participated in this study, 71 centers from 17 countries had at least 1 eligible stroke patient. Of 432 patients included, 323 (74.8%) had acute ischemic stroke, 91 (21.1%) intracranial hemorrhage, and 18 (4.2%) cerebral venous or sinus thrombosis. A total of 183 (42.4%) patients were women, 104 (24.1%) patients were <55 years of age, and 105 (24.4%) patients had no identifiable vascular risk factors. Among acute ischemic stroke patients, 44.5% (126 of 283 patients) had large vessel occlusion; 10% had small artery occlusion according to the TOAST criteria. We observed a lower median National Institutes of Health Stroke Scale (8 [3–17] versus 11 [5–17]; P =0.02) and higher rate of mechanical thrombectomy (12.4% versus 2%; P <0.001) in countries with middle-to-high health expenditure when compared with countries with lower health expenditure. Among 380 patients who had known interval onset of the SARS-CoV-2 and stroke, 144 (37.8%) were asymptomatic at the time of admission for SARS-CoV-2 infection. Conclusions: We observed a considerably higher rate of large vessel occlusions, a much lower rate of small vessel occlusion and lacunar infarction, and a considerable number of young stroke when compared with the population studies before the pandemic. The rate of mechanical thrombectomy was significantly lower in countries with lower health expenditures.