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. 2022 May;24(2):256-265.
doi: 10.5853/jos.2022.00752. Epub 2022 May 31.

Global Impact of the COVID-19 Pandemic on Cerebral Venous Thrombosis and Mortality

Thanh N Nguyen  1   2 , Muhammad M Qureshi  2   3 , Piers Klein  1   2 , Hiroshi Yamagami  4 , Mohamad Abdalkader  2 , Robert Mikulik  5 , Anvitha Sathya  1   2 , Ossama Yassin Mansour  6 , Anna Czlonkowska  7 , Hannah Lo  1   2 , Thalia S Field  8 , Andreas Charidimou  1 , Soma Banerjee  9 , Shadi Yaghi  10 , James E Siegler  11 , Petra Sedova  5 , Joseph Kwan  9 , Diana Aguiar de Sousa  12 , Jelle Demeestere  13 , Violiza Inoa  14 , Setareh Salehi Omran  15 , Liqun Zhang  16 , Patrik Michel  17 , Davide Strambo  17 , João Pedro Marto  18 , Raul G Nogueira  19 ; SVIN COVID-19 Global COVID Stroke Registry; Espen Saxhaug Kristoffersen  20   21 , Georgios Tsivgoulis  22 , Virginia Pujol Lereis  23 , Alice Ma  24 , Christian Enzinger  25 , Thomas Gattringer  26 , Aminur Rahman  27 , Thomas Bonnet  28 , Noémie Ligot  28 , Sylvie De Raedt  29 , Robin Lemmens  13 , Peter Vanacker  30   31 , Fenne Vandervorst  29 , Adriana Bastos Conforto  32 , Raquel C T Hidalgo  33 , Daissy Liliana Mora Cuervo  34 , Luciana de Oliveira Neves  35 , Isabelle Lameirinhas da Silva  32 , Rodrigo Targa Martíns  36 , Letícia C Rebello  37 , Igor Bessa Santiago  35 , Teodora Sakelarova  38 , Rosen Kalpachki  38 , Filip Alexiev  38 , Elena Adela Cora  39 , Michael E Kelly  40 , Lissa Peeling  40 , Aleksandra Pikula  41 , Hui-Sheng Chen  42 , Yimin Chen  43 , Shuiquan Yang  43 , Marina Roje Bedekovic  44 , Martin Čabal  45 , Dusan Tenora  46 , Petr Fibrich  47 , Pavel Dušek  48 , Helena Hlaváčová  49 , Emanuela Hrabanovska  50 , Lubomír Jurák  51 , Jana Kadlčíková  52 , Igor Karpowicz  53 , Lukáš Klečka  54 , Martin Kovář  55 , Jiří Neumann  56 , Hana Paloušková  57 , Martin Reiser  58 , Vladimir Rohan  59 , Libor Šimůnek  60 , Ondreij Skoda  61 , Miroslav Škorňa  62 , Martin Šrámek  63 , Nicolas Drenck  64 , Khalid Sobh  65 , Emilie Lesaine  66 , Candice Sabben  67 , Peggy Reiner  68 , Francois Rouanet  69 , Daniel Strbian  70 , Stefan Boskamp  71 , Joshua Mbroh  72   73 , Simon Nagel  74   75 , Michael Rosenkranz  71 , Sven Poli  72   73 , Götz Thomalla  76 , Theodoros Karapanayiotides  77 , Ioanna Koutroulou  77 , Odysseas Kargiotis  78 , Lina Palaiodimou  22 , José Dominguo Barrientos Guerra  79 , Vikram Huded  80 , Shashank Nagendra  81 , Chintan Prajapati  80 , P N Sylaja  82 , Achmad Firdaus Sani  83 , Abdoreza Ghoreishi  84 , Mehdi Farhoudi  85 , Elyar Sadeghi Hokmabadi  85 , Mazyar Hashemilar  86 , Sergiu Ionut Sabetay  87 , Fadi Rahal  88 , Maurizio Acampa  89 , Alessandro Adami  90 , Marco Longoni  91 , Raffaele Ornello  92 , Leonardo Renieri  93 , Michele Romoli  94 , Simona Sacco  92 , Andrea Salmaggi  95 , Davide Sangalli  95 , Andrea Zini  96 , Kenichiro Sakai  97 , Hiroki Fukuda  98 , Kyohei Fujita  99 , Hirotoshi Imamura  100 , Miyake Kosuke  101 , Manabu Sakaguchi  102 , Kazutaka Sonoda  103 , Yuji Matsumaru  104 , Nobuyuki Ohara  105 , Seigo Shindo  106 , Yohei Takenobu  107 , Takeshi Yoshimoto  108 , Kazunori Toyoda  109 , Takeshi Uwatoko  110 , Nobuyuki Sakai  100 , Nobuaki Yamamoto  111 , Ryoo Yamamoto  112 , Yukako Yazawa  113 , Yuri Sugiura  114 , Jang-Hyun Baek  115 , Si Baek Lee  116 , Kwon-Duk Seo  117 , Sung-Il Sohn  118 , Jin Soo Lee  119 , Anita Ante Arsovska  120 , Chan Yong Chieh  121 , Wan Asyraf Wan Zaidi  122 , Wan Nur Nafisah Wan Yahya  123 , Fernando Gongora-Rivera  124 , Manuel Martinez-Marino  125 , Adrian Infante-Valenzuela  124 , Diederik Dippel  126 , Dianne H K van Dam-Nolen  127 , Teddy Y Wu  128 , Martin Punter  129   130 , Tajudeen Temitayo Adebayo  131 , Abiodun H Bello  132 , Taofiki Ajao Sunmonu  133 , Kolawole Wasiu Wahab  132 , Antje Sundseth  20 , Amal M Al Hashmi  134 , Saima Ahmad  135 , Umair Rashid  135 , Liliana Rodriguez-Kadota  136 , Miguel Ángel Vences  136 , Patrick Matic Yalung  137 , Jon Stewart Hao Dy  137 , Waldemar Brola  138 , Aleksander Dębiec  139 , Malgorzata Dorobek  140 , Michal Adam Karlinski  7 , Beata M Labuz-Roszak  141 , Anetta Lasek-Bal  142 , Halina Sienkiewicz-Jarosz  143 , Jacek Staszewski  144 , Piotr Sobolewski  145 , Marcin Wiącek  146 , Justyna Zielinska-Turek  140   147 , André Pinho Araújo  148 , Mariana Rocha  149 , Pedro Castro  150 , Patricia Ferreira  151 , Ana Paiva Nunes  151 , Luísa Fonseca  152 , Teresa Pinho E Melo  153 , Miguel Rodrigues  154 , M Luis Silva  155 , Bogdan Ciopleias  156 , Adela Dimitriade  157 , Cristian Falup-Pecurariu  158 , May Adel Hamid  159 , Narayanaswamy Venketasubramanian  160 , Georgi Krastev  161   162   163 , Jozef Haring  161   162 , Oscar Ayo-Martin  164 , Francisco Hernandez-Fernandez  164 , Jordi Blasco  165 , Alejandro Rodríguez-Vázquez  166 , Antonio Cruz-Culebras  167 , Francisco Moniche  168 , Joan Montaner  169   170 , Soledad Perez-Sanchez  169   170 , María Jesús García Sánchez  171 , Marta Guillán Rodríguez  172 , Gianmarco Bernava  173 , Manuel Bolognese  174 , Emmanuel Carrera  175 , Anchalee Churojana  176 , Ozlem Aykac  177 , Atilla Özcan Özdemir  177 , Arsida Bajrami  178 , Songul Senadim  178 , Syed I Hussain  179 , Seby John  179 , Kailash Krishnan  180 , Robert Lenthall  181 , Kaiz S Asif  182 , Kristine Below  183 , Jose Biller  184 , Michael Chen  185 , Alex Chebl  186 , Marco Colasurdo  187 , Alexandra Czap  188 , Adam H de Havenon  189 , Sushrut Dharmadhikari  190 , Clifford J Eskey  191 , Mudassir Farooqui  192 , Steven K Feske  193 , Nitin Goyal  14 , Kasey B Grimmett  190 , Amy K Guzik  194 , Diogo C Haussen  195 , Majesta Hovingh  196 , Dinesh Jillela  195 , Peter T Kan  197 , Rakesh Khatri  198 , Naim N Khoury  199 , Nicole L Kiley  2 , Murali K Kolikonda  200 , Stephanie Lara  201 , Grace Li  202 , Italo Linfante  203 , Aaron I Loochtan  204 , Carlos D Lopez  205 , Sarah Lycan  194 , Shailesh S Male  206 , Fadi Nahab  207 , Laith Maali  208 , Hesham E Masoud  209 , Jiangyong Min  196 , Santiago Orgeta-Gutierrez  210 , Ghada A Mohamed  186 , Mahmoud Mohammaden  211 , Krishna Nalleballe  212 , Yazan Radaideh  185 , Pankajavalli Ramakrishnan  213 , Bliss Rayo-Taranto  214 , Diana M Rojas-Soto  191 , Sean Ruland  184 , Alexis N Simpkins  215 , Sunil A Sheth  188 , Amy K Starosciak  216 , Nicholas E Tarlov  201 , Robert A Taylor  214 , Barbara Voetsch  217 , Linda Zhang  218 , Hai Quang Duong  219 , Viet-Phuong Dao  220 , Huynh Vu Le  221 , Thong Nhu Pham  219 , Mai Duy Ton  220 , Anh Duc Tran  221 , Osama O Zaidat  183 , Paolo Machi  222 , Elisabeth Dirren  222 , Claudio Rodríguez Fernández  171 , Jorge Escartín López  171 , Jose Carlos Fernández Ferro  171 , Niloofar Mohammadzadeh  223 , Neil C Suryadevara  224 , Beatriz de la Cruz Fernández  225 , Filipe Bessa  226 , Nina Jancar  226 , Megan Brady  227 , Dawn Scozzari  227
Affiliations

Global Impact of the COVID-19 Pandemic on Cerebral Venous Thrombosis and Mortality

Thanh N Nguyen et al. J Stroke. 2022 May.

Erratum in

  • Global Impact of the COVID-19 Pandemic on Cerebral Venous Thrombosis and Mortality.
    Nguyen TN, Qureshi MM, Klein P, Yamagami H, Abdalkader M, Mikulik R, Sathya A, Mansour OY, Czlonkowska A, Lo H, Field TS, Charidimou A, Banerjee S, Yaghi S, Siegler JE, Sedova P, Kwan J, de Sousa DA, Demeestere J, Inoa V, Omran SS, Zhang L, Michel P, Strambo D, Marto JP, Nogueira RG; SVIN COVID-19 Global COVID Stroke Registry. Nguyen TN, et al. J Stroke. 2024 Jan;26(1):129. doi: 10.5853/jos.2022.00752.e1. Epub 2024 Jan 30. J Stroke. 2024. PMID: 38326711 Free PMC article. No abstract available.

Abstract

Background and purpose: Recent studies suggested an increased incidence of cerebral venous thrombosis (CVT) during the coronavirus disease 2019 (COVID-19) pandemic. We evaluated the volume of CVT hospitalization and in-hospital mortality during the 1st year of the COVID-19 pandemic compared to the preceding year.

Methods: We conducted a cross-sectional retrospective study of 171 stroke centers from 49 countries. We recorded COVID-19 admission volumes, CVT hospitalization, and CVT in-hospital mortality from January 1, 2019, to May 31, 2021. CVT diagnoses were identified by International Classification of Disease-10 (ICD-10) codes or stroke databases. We additionally sought to compare the same metrics in the first 5 months of 2021 compared to the corresponding months in 2019 and 2020 (ClinicalTrials.gov Identifier: NCT04934020).

Results: There were 2,313 CVT admissions across the 1-year pre-pandemic (2019) and pandemic year (2020); no differences in CVT volume or CVT mortality were observed. During the first 5 months of 2021, there was an increase in CVT volumes compared to 2019 (27.5%; 95% confidence interval [CI], 24.2 to 32.0; P<0.0001) and 2020 (41.4%; 95% CI, 37.0 to 46.0; P<0.0001). A COVID-19 diagnosis was present in 7.6% (132/1,738) of CVT hospitalizations. CVT was present in 0.04% (103/292,080) of COVID-19 hospitalizations. During the first pandemic year, CVT mortality was higher in patients who were COVID positive compared to COVID negative patients (8/53 [15.0%] vs. 41/910 [4.5%], P=0.004). There was an increase in CVT mortality during the first 5 months of pandemic years 2020 and 2021 compared to the first 5 months of the pre-pandemic year 2019 (2019 vs. 2020: 2.26% vs. 4.74%, P=0.05; 2019 vs. 2021: 2.26% vs. 4.99%, P=0.03). In the first 5 months of 2021, there were 26 cases of vaccine-induced immune thrombotic thrombocytopenia (VITT), resulting in six deaths.

Conclusions: During the 1st year of the COVID-19 pandemic, CVT hospitalization volume and CVT in-hospital mortality did not change compared to the prior year. COVID-19 diagnosis was associated with higher CVT in-hospital mortality. During the first 5 months of 2021, there was an increase in CVT hospitalization volume and increase in CVT-related mortality, partially attributable to VITT.

Keywords: COVID-19; Cerebral venous thrombosis; Mortality; SARS-CoV-2; Stroke; Vaccine-induced immune thrombotic thrombocytopenia.

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Figures

Figure 1.
Figure 1.
Study flow chart. CVT, cerebral venous thrombosis; SAH, subarachnoid hemorrhage; COVID-19, coronavirus disease 2019.
Figure 2.
Figure 2.
Cerebral venous thrombosis (CVT), CVT mortality, and coronavirus disease 2019 (COVID-19) admissions. CVT admissions are based on data submitted from 171 centers. COVID-19 admissions are based on data submitted from 154/171 centers.
Figure 3.
Figure 3.
Cerebral venous thrombosis (CVT) in-hospital mortality rate during the first 5 months of three different year (2019, 2020, 2021) comparisons in 138 hospitals with complete CVT mortality and CVT admission data. CVT in-hospital mortality 2019 vs. 2020: 2.26% vs. 4.74%, P=0.05; CVT in-hospital mortality 2019 vs. 2021: 2.26% vs. 4.99%, P=0.03; CVT in-hospital mortality 2020 vs. 2021, no difference. *Twenty-six vaccine-induced immune thrombotic thrombocytopenia (VITT) probable or confirmed cases were identified in 2021, resulting in six deaths. Excluding cases of confirmed or probable VITT, the case fatality rate of CVT during the first 5 months of 2021 drops from 4.99% to 4.04% (20/495 CVT cases) (P=0.1).
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