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

Thanh N Nguyen, Muhammad M Qureshi, Piers Klein, Hiroshi Yamagami, Mohamad Abdalkader, Robert Mikulik, Anvitha Sathya, Ossama Yassin Mansour, Anna Czlonkowska, Hannah Lo, Thalia S Field, Andreas Charidimou, Soma Banerjee, Shadi Yaghi, James E Siegler, Petra Sedova, Joseph Kwan, Diana Aguiar de Sousa, Jelle Demeestere, Violiza Inoa, Setareh Salehi Omran, Liqun Zhang, Patrik Michel, Davide Strambo, João Pedro Marto, Raul G Nogueira, SVIN COVID-19 Global COVID Stroke Registry, Espen Saxhaug Kristoffersen, Georgios Tsivgoulis, Virginia Pujol Lereis, Alice Ma, Christian Enzinger, Thomas Gattringer, Aminur Rahman, Thomas Bonnet, Noémie Ligot, Sylvie De Raedt, Robin Lemmens, Peter Vanacker, Fenne Vandervorst, Adriana Bastos Conforto, Raquel C T Hidalgo, Daissy Liliana Mora Cuervo, Luciana de Oliveira Neves, Isabelle Lameirinhas da Silva, Rodrigo Targa Martíns, Letícia C Rebello, Igor Bessa Santiago, Teodora Sakelarova, Rosen Kalpachki, Filip Alexiev, Elena Adela Cora, Michael E Kelly, Lissa Peeling, Aleksandra Pikula, Hui-Sheng Chen, Yimin Chen, Shuiquan Yang, Marina Roje Bedekovic, Martin Čabal, Dusan Tenora, Petr Fibrich, Pavel Dušek, Helena Hlaváčová, Emanuela Hrabanovska, Lubomír Jurák, Jana Kadlčíková, Igor Karpowicz, Lukáš Klečka, Martin Kovář, Jiří Neumann, Hana Paloušková, Martin Reiser, Vladimir Rohan, Libor Šimůnek, Ondreij Skoda, Miroslav Škorňa, Martin Šrámek, Nicolas Drenck, Khalid Sobh, Emilie Lesaine, Candice Sabben, Peggy Reiner, Francois Rouanet, Daniel Strbian, Stefan Boskamp, Joshua Mbroh, Simon Nagel, Michael Rosenkranz, Sven Poli, Götz Thomalla, Theodoros Karapanayiotides, Ioanna Koutroulou, Odysseas Kargiotis, Lina Palaiodimou, José Dominguo Barrientos Guerra, Vikram Huded, Shashank Nagendra, Chintan Prajapati, P N Sylaja, Achmad Firdaus Sani, Abdoreza Ghoreishi, Mehdi Farhoudi, Elyar Sadeghi Hokmabadi, Mazyar Hashemilar, Sergiu Ionut Sabetay, Fadi Rahal, Maurizio Acampa, Alessandro Adami, Marco Longoni, Raffaele Ornello, Leonardo Renieri, Michele Romoli, Simona Sacco, Andrea Salmaggi, Davide Sangalli, Andrea Zini, Kenichiro Sakai, Hiroki Fukuda, Kyohei Fujita, Hirotoshi Imamura, Miyake Kosuke, Manabu Sakaguchi, Kazutaka Sonoda, Yuji Matsumaru, Nobuyuki Ohara, Seigo Shindo, Yohei Takenobu, Takeshi Yoshimoto, Kazunori Toyoda, Takeshi Uwatoko, Nobuyuki Sakai, Nobuaki Yamamoto, Ryoo Yamamoto, Yukako Yazawa, Yuri Sugiura, Jang-Hyun Baek, Si Baek Lee, Kwon-Duk Seo, Sung-Il Sohn, Jin Soo Lee, Anita Ante Arsovska, Chan Yong Chieh, Wan Asyraf Wan Zaidi, Wan Nur Nafisah Wan Yahya, Fernando Gongora-Rivera, Manuel Martinez-Marino, Adrian Infante-Valenzuela, Diederik Dippel, Dianne H K van Dam-Nolen, Teddy Y Wu, Martin Punter, Tajudeen Temitayo Adebayo, Abiodun H Bello, Taofiki Ajao Sunmonu, Kolawole Wasiu Wahab, Antje Sundseth, Amal M Al Hashmi, Saima Ahmad, Umair Rashid, Liliana Rodriguez-Kadota, Miguel Ángel Vences, Patrick Matic Yalung, Jon Stewart Hao Dy, Waldemar Brola, Aleksander Dębiec, Malgorzata Dorobek, Michal Adam Karlinski, Beata M Labuz-Roszak, Anetta Lasek-Bal, Halina Sienkiewicz-Jarosz, Jacek Staszewski, Piotr Sobolewski, Marcin Wiącek, Justyna Zielinska-Turek, André Pinho Araújo, Mariana Rocha, Pedro Castro, Patricia Ferreira, Ana Paiva Nunes, Luísa Fonseca, Teresa Pinho E Melo, Miguel Rodrigues, M Luis Silva, Bogdan Ciopleias, Adela Dimitriade, Cristian Falup-Pecurariu, May Adel Hamid, Narayanaswamy Venketasubramanian, Georgi Krastev, Jozef Haring, Oscar Ayo-Martin, Francisco Hernandez-Fernandez, Jordi Blasco, Alejandro Rodríguez-Vázquez, Antonio Cruz-Culebras, Francisco Moniche, Joan Montaner, Soledad Perez-Sanchez, María Jesús García Sánchez, Marta Guillán Rodríguez, Gianmarco Bernava, Manuel Bolognese, Emmanuel Carrera, Anchalee Churojana, Ozlem Aykac, Atilla Özcan Özdemir, Arsida Bajrami, Songul Senadim, Syed I Hussain, Seby John, Kailash Krishnan, Robert Lenthall, Kaiz S Asif, Kristine Below, Jose Biller, Michael Chen, Alex Chebl, Marco Colasurdo, Alexandra Czap, Adam H de Havenon, Sushrut Dharmadhikari, Clifford J Eskey, Mudassir Farooqui, Steven K Feske, Nitin Goyal, Kasey B Grimmett, Amy K Guzik, Diogo C Haussen, Majesta Hovingh, Dinesh Jillela, Peter T Kan, Rakesh Khatri, Naim N Khoury, Nicole L Kiley, Murali K Kolikonda, Stephanie Lara, Grace Li, Italo Linfante, Aaron I Loochtan, Carlos D Lopez, Sarah Lycan, Shailesh S Male, Fadi Nahab, Laith Maali, Hesham E Masoud, Jiangyong Min, Santiago Orgeta-Gutierrez, Ghada A Mohamed, Mahmoud Mohammaden, Krishna Nalleballe, Yazan Radaideh, Pankajavalli Ramakrishnan, Bliss Rayo-Taranto, Diana M Rojas-Soto, Sean Ruland, Alexis N Simpkins, Sunil A Sheth, Amy K Starosciak, Nicholas E Tarlov, Robert A Taylor, Barbara Voetsch, Linda Zhang, Hai Quang Duong, Viet-Phuong Dao, Huynh Vu Le, Thong Nhu Pham, Mai Duy Ton, Anh Duc Tran, Osama O Zaidat, Paolo Machi, Elisabeth Dirren, Claudio Rodríguez Fernández, Jorge Escartín López, Jose Carlos Fernández Ferro, Niloofar Mohammadzadeh, Neil C Suryadevara, Beatriz de la Cruz Fernández, Filipe Bessa, Nina Jancar, Megan Brady, Dawn Scozzari, Thanh N Nguyen, Muhammad M Qureshi, Piers Klein, Hiroshi Yamagami, Mohamad Abdalkader, Robert Mikulik, Anvitha Sathya, Ossama Yassin Mansour, Anna Czlonkowska, Hannah Lo, Thalia S Field, Andreas Charidimou, Soma Banerjee, Shadi Yaghi, James E Siegler, Petra Sedova, Joseph Kwan, Diana Aguiar de Sousa, Jelle Demeestere, Violiza Inoa, Setareh Salehi Omran, Liqun Zhang, Patrik Michel, Davide Strambo, João Pedro Marto, Raul G Nogueira, SVIN COVID-19 Global COVID Stroke Registry, Espen Saxhaug Kristoffersen, Georgios Tsivgoulis, Virginia Pujol Lereis, Alice Ma, Christian Enzinger, Thomas Gattringer, Aminur Rahman, Thomas Bonnet, Noémie Ligot, Sylvie De Raedt, Robin Lemmens, Peter Vanacker, Fenne Vandervorst, Adriana Bastos Conforto, Raquel C T Hidalgo, Daissy Liliana Mora Cuervo, Luciana de Oliveira Neves, Isabelle Lameirinhas da Silva, Rodrigo Targa Martíns, Letícia C Rebello, Igor Bessa Santiago, Teodora Sakelarova, Rosen Kalpachki, Filip Alexiev, Elena Adela Cora, Michael E Kelly, Lissa Peeling, Aleksandra Pikula, Hui-Sheng Chen, Yimin Chen, Shuiquan Yang, Marina Roje Bedekovic, Martin Čabal, Dusan Tenora, Petr Fibrich, Pavel Dušek, Helena Hlaváčová, Emanuela Hrabanovska, Lubomír Jurák, Jana Kadlčíková, Igor Karpowicz, Lukáš Klečka, Martin Kovář, Jiří Neumann, Hana Paloušková, Martin Reiser, Vladimir Rohan, Libor Šimůnek, Ondreij Skoda, Miroslav Škorňa, Martin Šrámek, Nicolas Drenck, Khalid Sobh, Emilie Lesaine, Candice Sabben, Peggy Reiner, Francois Rouanet, Daniel Strbian, Stefan Boskamp, Joshua Mbroh, Simon Nagel, Michael Rosenkranz, Sven Poli, Götz Thomalla, Theodoros Karapanayiotides, Ioanna Koutroulou, Odysseas Kargiotis, Lina Palaiodimou, José Dominguo Barrientos Guerra, Vikram Huded, Shashank Nagendra, Chintan Prajapati, P N Sylaja, Achmad Firdaus Sani, Abdoreza Ghoreishi, Mehdi Farhoudi, Elyar Sadeghi Hokmabadi, Mazyar Hashemilar, Sergiu Ionut Sabetay, Fadi Rahal, Maurizio Acampa, Alessandro Adami, Marco Longoni, Raffaele Ornello, Leonardo Renieri, Michele Romoli, Simona Sacco, Andrea Salmaggi, Davide Sangalli, Andrea Zini, Kenichiro Sakai, Hiroki Fukuda, Kyohei Fujita, Hirotoshi Imamura, Miyake Kosuke, Manabu Sakaguchi, Kazutaka Sonoda, Yuji Matsumaru, Nobuyuki Ohara, Seigo Shindo, Yohei Takenobu, Takeshi Yoshimoto, Kazunori Toyoda, Takeshi Uwatoko, Nobuyuki Sakai, Nobuaki Yamamoto, Ryoo Yamamoto, Yukako Yazawa, Yuri Sugiura, Jang-Hyun Baek, Si Baek Lee, Kwon-Duk Seo, Sung-Il Sohn, Jin Soo Lee, Anita Ante Arsovska, Chan Yong Chieh, Wan Asyraf Wan Zaidi, Wan Nur Nafisah Wan Yahya, Fernando Gongora-Rivera, Manuel Martinez-Marino, Adrian Infante-Valenzuela, Diederik Dippel, Dianne H K van Dam-Nolen, Teddy Y Wu, Martin Punter, Tajudeen Temitayo Adebayo, Abiodun H Bello, Taofiki Ajao Sunmonu, Kolawole Wasiu Wahab, Antje Sundseth, Amal M Al Hashmi, Saima Ahmad, Umair Rashid, Liliana Rodriguez-Kadota, Miguel Ángel Vences, Patrick Matic Yalung, Jon Stewart Hao Dy, Waldemar Brola, Aleksander Dębiec, Malgorzata Dorobek, Michal Adam Karlinski, Beata M Labuz-Roszak, Anetta Lasek-Bal, Halina Sienkiewicz-Jarosz, Jacek Staszewski, Piotr Sobolewski, Marcin Wiącek, Justyna Zielinska-Turek, André Pinho Araújo, Mariana Rocha, Pedro Castro, Patricia Ferreira, Ana Paiva Nunes, Luísa Fonseca, Teresa Pinho E Melo, Miguel Rodrigues, M Luis Silva, Bogdan Ciopleias, Adela Dimitriade, Cristian Falup-Pecurariu, May Adel Hamid, Narayanaswamy Venketasubramanian, Georgi Krastev, Jozef Haring, Oscar Ayo-Martin, Francisco Hernandez-Fernandez, Jordi Blasco, Alejandro Rodríguez-Vázquez, Antonio Cruz-Culebras, Francisco Moniche, Joan Montaner, Soledad Perez-Sanchez, María Jesús García Sánchez, Marta Guillán Rodríguez, Gianmarco Bernava, Manuel Bolognese, Emmanuel Carrera, Anchalee Churojana, Ozlem Aykac, Atilla Özcan Özdemir, Arsida Bajrami, Songul Senadim, Syed I Hussain, Seby John, Kailash Krishnan, Robert Lenthall, Kaiz S Asif, Kristine Below, Jose Biller, Michael Chen, Alex Chebl, Marco Colasurdo, Alexandra Czap, Adam H de Havenon, Sushrut Dharmadhikari, Clifford J Eskey, Mudassir Farooqui, Steven K Feske, Nitin Goyal, Kasey B Grimmett, Amy K Guzik, Diogo C Haussen, Majesta Hovingh, Dinesh Jillela, Peter T Kan, Rakesh Khatri, Naim N Khoury, Nicole L Kiley, Murali K Kolikonda, Stephanie Lara, Grace Li, Italo Linfante, Aaron I Loochtan, Carlos D Lopez, Sarah Lycan, Shailesh S Male, Fadi Nahab, Laith Maali, Hesham E Masoud, Jiangyong Min, Santiago Orgeta-Gutierrez, Ghada A Mohamed, Mahmoud Mohammaden, Krishna Nalleballe, Yazan Radaideh, Pankajavalli Ramakrishnan, Bliss Rayo-Taranto, Diana M Rojas-Soto, Sean Ruland, Alexis N Simpkins, Sunil A Sheth, Amy K Starosciak, Nicholas E Tarlov, Robert A Taylor, Barbara Voetsch, Linda Zhang, Hai Quang Duong, Viet-Phuong Dao, Huynh Vu Le, Thong Nhu Pham, Mai Duy Ton, Anh Duc Tran, Osama O Zaidat, Paolo Machi, Elisabeth Dirren, Claudio Rodríguez Fernández, Jorge Escartín López, Jose Carlos Fernández Ferro, Niloofar Mohammadzadeh, Neil C Suryadevara, Beatriz de la Cruz Fernández, Filipe Bessa, Nina Jancar, Megan Brady, Dawn Scozzari

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.

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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