Epidemiology, pathogenesis, and management of coronavirus disease 2019-associated stroke

Abstract

The coronavirus disease 2019 (COVID-19) epidemic has triggered a huge impact on healthcare, socioeconomics, and other aspects of the world over the past three years. An increasing number of studies have identified a complex relationship between COVID-19 and stroke, although active measures are being implemented to prevent disease transmission. Severe COVID-19 may be associated with an increased risk of stroke and increase the rates of disability and mortality, posing a serious challenge to acute stroke diagnosis, treatment, and care. This review aims to provide an update on the influence of COVID-19 itself or vaccines on stroke, including arterial stroke (ischemic stroke and hemorrhagic stroke) and venous stroke (cerebral venous thrombosis). Additionally, the neurovascular mechanisms involved in SARS-CoV-2 infection and the clinical characteristics of stroke in the COVID-19 setting are presented. Evidence on vaccinations, potential therapeutic approaches, and effective strategies for stroke management has been highlighted.

Keywords

SARS-CoV-2 / ischemic stroke / stroke / hemorrhagic stroke / cerebral venous thrombosis / vaccination

Lu Liu et al.

参考文献

[1] Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Peñaranda S, Bankamp B, Maher K, Chen MH, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TC, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, Günther S, Osterhaus AD, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 2003; 300(5624): 1394–1399

[2] Saad M, Omrani AS, Baig K, Bahloul A, Elzein F, Matin MA, Selim MA, Al Mutairi M, Al Nakhli D, Al Aidaroos AY, Al Sherbeeni N, Al-Khashan HI, Memish ZA, Albarrak AM. Clinical aspects and outcomes of 70 patients with Middle East respiratory syndrome coronavirus infection: a single-center experience in Saudi Arabia. Int J Infect Dis 2014; 29: 301–306

[3] Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579(7798): 270–273

[4] Katsanos AH, Palaiodimou L, Zand R, Yaghi S, Kamel H, Navi BB, Turc G, Romoli M, Sharma VK, Mavridis D, Shahjouei S, Catanese L, Shoamanesh A, Vadikolias K, Tsioufis K, Lagiou P, Alexandrov AV, Tsiodras S, Tsivgoulis G. The impact of SARS-CoV-2 on stroke epidemiology and care: a meta-analysis. Ann Neurol 2021; 89(2): 380–388

[5] Merkler AE, Parikh NS, Mir S, Gupta A, Kamel H, Lin E, Lantos J, Schenck EJ, Goyal P, Bruce SS, Kahan J, Lansdale KN, LeMoss NM, Murthy SB, Stieg PE, Fink ME, Iadecola C, Segal AZ, Cusick M, Campion TR Jr, Diaz I, Zhang C, Navi BB. Risk of ischemic stroke in patients with coronavirus disease 2019 (COVID-19) vs patients with influenza. JAMA Neurol 2020; 77(11): 1366–1372

[6] Zhou Y, Jiang H, Wei H, Liu L, Zhou C, Ji X. Venous stroke—a stroke subtype that should not be ignored. Front Neurol 2022; 13: 1019671

[7] Kalekar T, Thakker V, Bansal A. Role of neuroimaging in COVID 19 infection—a retrospective study. J Radiol Nurs 2021; 40(4): 370–376

[8] Chiew YR, Kong Y. Encephalopathy as the only manifestation in simultaneous arterial infarct and cerebral venous sinus thrombosis in recent COVID-19 infection. Am J Case Rep 2022; 23: e938571

[9] Chen Z, Peng Y, Wu X, Pang B, Yang F, Zheng W, Liu C, Zhang J. Comorbidities and complications of COVID-19 associated with disease severity, progression, and mortality in China with centralized isolation and hospitalization: a systematic review and meta-analysis. Front Public Health 2022; 10: 923485

[10] Cagnazzo F, Arquizan C, Derraz I, Dargazanli C, Lefevre PH, Riquelme C, Gaillard N, Mourand I, Gascou G, Bonafe A, Costalat V. Neurological manifestations of patients infected with the SARS-CoV-2: a systematic review of the literature. J Neurol 2021; 268(8): 2656–2665

[11] Kurian C, Mayer S, Kaur G, Sahni R, Feldstein E, Samaan M, Viswanathan D, Sami T, Ali SF, Al-Shammari H, Bloomfield J, Bravo M, Nuoman R, Gulko E, Gandhi CD, Al-Mufti F. Bihemispheric ischemic strokes in patients with COVID-19. Brain Circ 2022; 8(1): 10–16

[12] Samim MM, Dhar D, Arshad F, Anudeep DDS, Patel VG, Neeharika SR, Dhamija K, Ravindranath CM, Yadav R, Raja P, Netravathi M, Menon D, Holla VV, Kamble NL, Pal PK, Nalini A, Vengalil S. Co-VAN study: COVID-19 vaccine associated neurological diseases—an experience from an apex neurosciences centre and review of the literature. J Clin Neurosci 2023; 108: 37–75

[13] Ho FK, Man KKC, Toshner M, Church C, Celis-Morales C, Wong ICK, Berry C, Sattar N, Pell JP. Thromboembolic risk in hospitalized and nonhospitalized COVID-19 patients: a self-controlled case series analysis of a nationwide cohort. Mayo Clin Proc 2021; 96(10): 2587–2597

[14] Lund LC, Hallas J, Nielsen H, Koch A, Mogensen SH, Brun NC, Christiansen CF, Thomsen RW, Pottegård A. Post-acute effects of SARS-CoV-2 infection in individuals not requiring hospital admission: a Danish population-based cohort study. Lancet Infect Dis 2021; 21(10): 1373–1382

[15] Piazza G, Campia U, Hurwitz S, Snyder JE, Rizzo SM, Pfeferman MB, Morrison RB, Leiva O, Fanikos J, Nauffal V, Almarzooq Z, Goldhaber SZ. Registry of arterial and venous thromboembolic complications in patients with COVID-19. J Am Coll Cardiol 2020; 76(18): 2060–2072

[16] Vogrig A, Gigli GL, Bnà C, Morassi M. Stroke in patients with COVID-19: clinical and neuroimaging characteristics. Neurosci Lett 2021; 743: 135564

[17] Syahrul S, Maliga HA, Ilmawan M, Fahriani M, Mamada SS, Fajar JK, Frediansyah A, Syahrul FN, Imran I, Haris S, Rambe AS, Emran TB, Rabaan AA, Tiwari R, Dhama K, Nainu F, Mutiawati E, Harapan H. Hemorrhagic and ischemic stroke in patients with coronavirus disease 2019: incidence, risk factors, and pathogenesis—a systematic review and meta-analysis. F1000 Res 2021; 10: 34

[18] Bhatia R, Pedapati R, Komakula S, Srivastava MVP, Vishnubhatla S, Khurana D. Stroke in coronavirus disease 2019: a systematic review. J Stroke 2020; 22(3): 324–335

[19] Lee KW, Yusof Khan AHK, Ching SM, Chia PK, Loh WC, Abdul Rashid AM, Baharin J, Inche Mat LN, Wan Sulaiman WA, Devaraj NK, Sivaratnam D, Basri H, Hoo FK. Stroke and novel coronavirus infection in humans: a systematic review and meta-analysis. Front Neurol 2020; 11: 579070

[20] Siow I, Lee KS, Zhang JJY, Saffari SE, Ng A, Young B. Stroke as a neurological complication of COVID-19: a systematic review and meta-analysis of incidence, outcomes and predictors. J Stroke Cerebrovasc Dis 2021; 30(3): 105549

[21] Nannoni S, de Groot R, Bell S, Markus HS. Stroke in COVID-19: a systematic review and meta-analysis. Int J Stroke 2021; 16(2): 137–149

[22] Silvis SM, de Sousa DA, Ferro JM, Coutinho JM. Cerebral venous thrombosis. Nat Rev Neurol 2017; 13(9): 555–565

[23] Otite FO, Patel S, Sharma R, Khandwala P, Desai D, Latorre JG, Akano EO, Anikpezie N, Izzy S, Malik AM, Yavagal D, Khandelwal P, Chaturvedi S. Trends in incidence and epidemiologic characteristics of cerebral venous thrombosis in the United States. Neurology 2020; 95(16): e2200–e2213

[24] Devasagayam S, Wyatt B, Leyden J, Kleinig T. Cerebral venous sinus thrombosis incidence is higher than previously thought: a retrospective population-based study. Stroke 2016; 47(9): 2180–2182

[25] Koh JS, De Silva DA, Quek AML, Chiew HJ, Tu TM, Seet CYH, Hoe RHM, Saini M, Hui AC, Angon J, Ker JR, Yong MH, Goh Y, Yu WY, Lim TCC, Tan BYQ, Ng KWP, Yeo LLL, Pang YZ, Prakash KM, Ahmad A, Thomas T, Lye DCB, Tan K, Umapathi T. Neurology of COVID-19 in Singapore. J Neurol Sci 2020; 418: 117118

[26] Siegler JE, Cardona P, Arenillas JF, Talavera B, Guillen AN, Chavarría-Miranda A, de Lera M, Khandelwal P, Bach I, Patel P, Singla A, Requena M, Ribo M, Jillella DV, Rangaraju S, Nogueira RG, Haussen DC, Vazquez AR, Urra X, ChamorroÁ, Román LS, Thon JM, Then R, Sanborn E, de la Ossa NP, Millàn M, Ruiz IN, Mansour OY, Megahed M, Tiu C, Terecoasa EO, Radu RA, Nguyen TN, Curiale G, Kaliaev A, Czap AL, Sebaugh J, Zha AM, Liebeskind DS, Ortega-Gutierrez S, Farooqui M, Hassan AE, Preston L, Patterson MS, Bushnaq S, Zaidat O, Jovin TG. Cerebrovascular events and outcomes in hospitalized patients with COVID-19: the SVIN COVID-19 Multinational Registry. Int J Stroke 2021; 16(4): 437–447

[27] Shahjouei S, Naderi S, Li J, Khan A, Chaudhary D, Farahmand G, Male S, Griessenauer C, Sabra M, Mondello S, Cernigliaro A, Khodadadi F, Dev A, Goyal N, Ranji-Burachaloo S, Olulana O, Avula V, Ebrahimzadeh SA, Alizada O, Hancı MM, Ghorbani A, Vaghefi Far A, Ranta A, Punter M, Ramezani M, Ostadrahimi N, Tsivgoulis G, Fragkou PC, Nowrouzi-Sohrabi P, Karofylakis E, Tsiodras S, Neshin Aghayari Sheikh S, Saberi A, Niemelä M, Rezai Jahromi B, Mowla A, Mashayekhi M, Bavarsad Shahripour R, Sajedi SA, Ghorbani M, Kia A, Rahimian N, Abedi V, Zand R. Risk of stroke in hospitalized SARS-CoV-2 infected patients: a multinational study. EBioMedicine 2020; 59: 102939

[28] Trimaille A, Curtiaud A, Marchandot B, Matsushita K, Sato C, Leonard-Lorant I, Sattler L, Grunebaum L, Ohana M, Von Hunolstein JJ, Andres E, Goichot B, Danion F, Kaeuffer C, Poindron V, Ohlmann P, Jesel L, Morel O. Venous thromboembolism in non-critically ill patients with COVID-19 infection. Thromb Res 2020; 193: 166–169

[29] Al-Mufti F, Amuluru K, Sahni R, Bekelis K, Karimi R, Ogulnick J, Cooper J, Overby P, Nuoman R, Tiwari A, Berekashvili K, Dangayach N, Liang J, Gupta G, Khandelwal P, Dominguez JF, Sursal T, Kamal H, Dakay K, Taylor B, Gulko E, El-Ghanem M, Mayer SA, Gandhi C. Cerebral venous thrombosis in COVID-19: a New York metropolitan cohort study. AJNR Am J Neuroradiol 2021; 42(7): 1196–1200

[30] Baldini T, Asioli GM, Romoli M, Carvalho Dias M, Schulte EC, Hauer L, Aguiar De Sousa D, Sellner J, Zini A. Cerebral venous thrombosis and severe acute respiratory syndrome coronavirus-2 infection: a systematic review and meta-analysis. Eur J Neurol 2021; 28(10): 3478–3490

[31] 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. Global impact of the COVID-19 pandemic on cerebral venous thrombosis and mortality. J Stroke 2022; 24(2): 256–265

[32] Taquet M, Husain M, Geddes JR, Luciano S, Harrison PJ. Cerebral venous thrombosis and portal vein thrombosis: a retrospective cohort study of 537,913 COVID-19 cases. EClinicalMedicine 2021; 39: 101061

[33] Requena M, Olivé-Gadea M, Muchada M, García-Tornel Á, Deck M, Juega J, Boned S, Rodríguez-Villatoro N, Piñana C, Pagola J, Rodríguez-Luna D, Hernández D, Rubiera M, Tomasello A, Molina CA, Ribo M. COVID-19 and stroke: incidence and etiological description in a high-volume center. J Stroke Cerebrovasc Dis 2020; 29(11): 105225

[34] Rothstein A, Oldridge O, Schwennesen H, Do D, Cucchiara BL. Acute cerebrovascular events in hospitalized COVID-19 patients. Stroke 2020; 51(9): e219–e222

[35] Oates CP, Bienstock SW, Miller M, Giustino G, Danilov T, Kukar N, Kocovic N, Sperling D, Singh R, Benhuri D, Beerkens F, Camaj A, Lerakis S, Croft L, Stein LK, Goldman ME. Using clinical and echocardiographic characteristics to characterize the risk of ischemic stroke in patients with COVID-19. J Stroke Cerebrovasc Dis 2022; 31(2): 106217

[36] Chand S, Kapoor S, Orsi D, Fazzari MJ, Tanner TG, Umeh GC, Islam M, Dicpinigaitis PV. COVID-19-associated critical illness-report of the first 300 patients admitted to intensive care units at a New York City medical center. J Intensive Care Med 2020; 35(10): 963–970

[37] Ji XY, Ma Y, Shi NN, Liang N, Chen RB, Liu SH, Shi S, Wu GH, Li JK, Chen H, Wang JW, Na H, Zhou YC, Li MQ, Wang YD, Hu XM, Hu YH, Liu Z, Xie HJ, Zhang LS, Zhang HM, Wang YP, Wang YY. Clinical characteristics and treatment outcome of COVID-19 patients with stroke in China: a multicenter retrospective study. Phytomedicine 2021; 81: 153433

[38] Siepmann T, Sedghi A, Simon E, Winzer S, Barlinn J, de With K, Mirow L, Wolz M, Gruenewald T, Schroettner P, von Bonin S, Pallesen LP, Rosengarten B, Schubert J, Lohmann T, Machetanz J, Spieth P, Koch T, Bornstein S, Reichmann H, Puetz V, Barlinn K. Increased risk of acute stroke among patients with severe COVID-19: a multicenter study and meta-analysis. Eur J Neurol 2021; 28(1): 238–247

[39] Gao Y, Chen Y, Liu M, Niu M, Song Z, Yan M, Tian J. Nervous system diseases are associated with the severity and mortality of patients with COVID-19: a systematic review and meta-analysis. Epidemiol Infect 2021; 149: e66

[40] Luo W, Liu X, Bao K, Huang C. Ischemic stroke associated with COVID-19: a systematic review and meta-analysis. J Neurol 2022; 269(4): 1731–1740

[41] Saposnik G, Barinagarrementeria F, Brown RD Jr, Bushnell CD, Cucchiara B, Cushman M, deVeber G, Ferro JM, Tsai FY; American Heart Association Stroke Council, the Council on Epidemiology. Diagnosis and management of cerebral venous thrombosis: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2011; 42(4): 1158–1192

[42] Green M, Styles T, Russell T, Sada C, Jallow E, Stewart J, Lazariashvili O, Lubomirova I, Cotlarciuc I, Sharma S, Han TS, Sharma P. Non-genetic and genetic risk factors for adult cerebral venous thrombosis. Thromb Res 2018; 169: 15–22

[43] Park DS, Moon CT, Chun YI, Koh YC, Kim HY, Roh HG. Clinical characteristics of cerebral venous thrombosis in a single center in Korea. J Korean Neurosurg Soc 2014; 56(4): 289–294

[44] Cognat E, Crassard I, Denier C, Vahedi K, Bousser MG. Cerebral venous thrombosis in inflammatory bowel diseases: eight cases and literature review. Int J Stroke 2011; 6(6): 487–492

[45] Coutinho JM, Ferro JM, Canhão P, Barinagarrementeria F, Cantú C, Bousser MG, Stam J. Cerebral venous and sinus thrombosis in women. Stroke 2009; 40(7): 2356–2361

[46] Zuurbier SM, Middeldorp S, Stam J, Coutinho JM. Sex differences in cerebral venous thrombosis: a systematic analysis of a shift over time. Int J Stroke 2016; 11(2): 164–170

[47] Portier I, Campbell RA, Denorme F. Mechanisms of immunothrombosis in COVID-19. Curr Opin Hematol 2021; 28(6): 445–453

[48] Pellicori P, Doolub G, Wong CM, Lee KS, Mangion K, Ahmad M, Berry C, Squire I, Lambiase PD, Lyon A, McConnachie A, Taylor RS, Cleland JG. COVID-19 and its cardiovascular effects: a systematic review of prevalence studies. Cochrane Database Syst Rev 2021; 3(3): CD013879

[49] Endres M, Moro MA, Nolte CH, Dames C, Buckwalter MS, Meisel A. Immune pathways in etiology, acute phase, and chronic sequelae of ischemic stroke. Circ Res 2022; 130(8): 1167–1186

[50] Sagris D, Papanikolaou A, Kvernland A, Korompoki E, Frontera JA, Troxel AB, Gavriatopoulou M, Milionis H, Lip GYH, Michel P, Yaghi S, Ntaios G. COVID-19 and ischemic stroke. Eur J Neurol 2021; 28(11): 3826–3836

[51] Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, Cheng Z, Yu T, Xia J, Wei Y, Wu W, Xie X, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J, Wang G, Jiang R, Gao Z, Jin Q, Wang J, Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223): 497–506

[52] Tang N, Bai H, Chen X, Gong J, Li D, Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost 2020; 18(5): 1094–1099

[53] Hu B, Huang S, Yin L. The cytokine storm and COVID-19. J Med Virol 2021; 93(1): 250–256

[54] Bautista LE, Vera LM, Arenas IA, Gamarra G. Independent association between inflammatory markers (C-reactive protein, interleukin-6, and TNF-α) and essential hypertension. J Hum Hypertens 2005; 19(2): 149–154

[55] Mackman N, Antoniak S, Wolberg AS, Kasthuri R, Key NS. Coagulation abnormalities and thrombosis in patients infected with SARS-CoV-2 and other pandemic viruses. Arterioscler Thromb Vasc Biol 2020; 40(9): 2033–2044

[56] Koupenova M. Potential role of platelets in COVID-19: implications for thrombosis. Res Pract Thromb Haemost 2020; 4(5): 737–740

[57] Beristain-Covarrubias N, Perez-Toledo M, Thomas MR, Henderson IR, Watson SP, Cunningham AF. Understanding infection-induced thrombosis: lessons learned from animal models. Front Immunol 2019; 10: 2569

[58] Bautista-Vargas M, Bonilla-Abadía F, Cañas CA. Potential role for tissue factor in the pathogenesis of hypercoagulability associated with in COVID-19. J Thromb Thrombolysis 2020; 50(3): 479–483

[59] McGonagle D, O’Donnell JS, Sharif K, Emery P, Bridgewood C. Immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia. Lancet Rheumatol 2020; 2(7): e437–e445

[60] van der Poll T, van de Veerdonk FL, Scicluna BP, Netea MG. The immunopathology of sepsis and potential therapeutic targets. Nat Rev Immunol 2017; 17(7): 407–420

[61] Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, Wang B, Xiang H, Cheng Z, Xiong Y, Zhao Y, Li Y, Wang X, Peng Z. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020; 323(11): 1061–1069

[62] Shahjouei S, Tsivgoulis G, Farahmand G, Koza E, Mowla A, Vafaei Sadr A, Kia A, Vaghefi Far A, Mondello S, Cernigliaro A, Ranta A, Punter M, Khodadadi F, Naderi S, Sabra M, Ramezani M, Amini Harandi A, Olulana O, Chaudhary D, Lyoubi A, Campbell BCV, Arenillas JF, Bock D, Montaner J, Aghayari Sheikh Neshin S, Aguiar de Sousa D, Tenser MS, Aires A, Alfonso ML, Alizada O, Azevedo E, Goyal N, Babaeepour Z, Banihashemi G, Bonati LH, Cereda CW, Chang JJ, Crnjakovic M, De Marchis GM, Del Sette M, Ebrahimzadeh SA, Farhoudi M, Gandoglia I, Gonçalves B, Griessenauer CJ, Murat Hanci M, Katsanos AH, Krogias C, Leker RR, Lotman L, Mai J, Male S, Malhotra K, Malojcic B, Mesquita T, Mir Ghasemi A, Mohamed Aref H, Mohseni Afshar Z, Moon J, Niemelä M, Rezai Jahromi B, Nolan L, Pandhi A, Park JH, Marto JP, Purroy F, Ranji-Burachaloo S, Carreira NR, Requena M, Rubiera M, Sajedi SA, Sargento-Freitas J, Sharma VK, Steiner T, Tempro K, Turc G, Ahmadzadeh Y, Almasi-Dooghaee M, Assarzadegan F, Babazadeh A, Baharvahdat H, Cardoso FB, Dev A, Ghorbani M, Hamidi A, Hasheminejad ZS, Hojjat-Anasri Komachali S, Khorvash F, Kobeissy F, Mirkarimi H, Mohammadi-Vosough E, Misra D, Noorian AR, Nowrouzi-Sohrabi P, Paybast S, Poorsaadat L, Roozbeh M, Sabayan B, Salehizadeh S, Saberi A, Sepehrnia M, Vahabizad F, Yasuda TA, Ghabaee M, Rahimian N, Harirchian MH, Borhani-Haghighi A, Azarpazhooh MR, Arora R, Ansari S, Avula V, Li J, Abedi V, Zand R. SARS-CoV-2 and stroke characteristics: a report from the multinational COVID-19 stroke study group. Stroke 2021; 52(5): e117–e130

[63] Guo L, Rondina MT. The era of thromboinflammation: platelets are dynamic sensors and effector cells during infectious diseases. Front Immunol 2019; 10: 2204

[64] Gaertner F, Massberg S. Blood coagulation in immunothrombosis—at the frontline of intravascular immunity. Semin Immunol 2016; 28(6): 561–569

[65] Becker RC. COVID-19 update: Covid-19-associated coagulopathy. J Thromb Thrombolysis 2020; 50(1): 54–67

[66] Barnes BJ, Adrover JM, Baxter-Stoltzfus A, Borczuk A, Cools-Lartigue J, Crawford JM, Daßler-Plenker J, Guerci P, Huynh C, Knight JS, Loda M, Looney MR, McAllister F, Rayes R, Renaud S, Rousseau S, Salvatore S, Schwartz RE, Spicer JD, Yost CC, Weber A, Zuo Y, Egeblad M. Targeting potential drivers of COVID-19: neutrophil extracellular traps. J Exp Med 2020; 217(6): e20200652

[67] Skendros P, Mitsios A, Chrysanthopoulou A, Mastellos DC, Metallidis S, Rafailidis P, Ntinopoulou M, Sertaridou E, Tsironidou V, Tsigalou C, Tektonidou M, Konstantinidis T, Papagoras C, Mitroulis I, Germanidis G, Lambris JD, Ritis K. Complement and tissue factor-enriched neutrophil extracellular traps are key drivers in COVID-19 immunothrombosis. J Clin Invest 2020; 130(11): 6151–6157

[68] Nicolai L, Leunig A, Brambs S, Kaiser R, Joppich M, Hoffknecht ML, Gold C, Engel A, Polewka V, Muenchhoff M, Hellmuth JC, Ruhle A, Ledderose S, Weinberger T, Schulz H, Scherer C, Rudelius M, Zoller M, Keppler OT, Zwißler B, von Bergwelt-Baildon M, Kääb S, Zimmer R, Bülow RD, von Stillfried S, Boor P, Massberg S, Pekayvaz K, Stark K. Vascular neutrophilic inflammation and immunothrombosis distinguish severe COVID-19 from influenza pneumonia. J Thromb Haemost 2021; 19(2): 574–581

[69] Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A, Müller MA, Drosten C, Pöhlmann S. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181(2): 271–280.e8

[70] Labò N, Ohnuki H, Tosato G. Vasculopathy and coagulopathy associated with SARS-CoV-2 infection. Cells 2020; 9(7): 1583

[71] Henry BM, Vikse J, Benoit S, Favaloro EJ, Lippi G. Hyperinflammation and derangement of renin-angiotensin-aldosterone system in COVID-19: a novel hypothesis for clinically suspected hypercoagulopathy and microvascular immunothrombosis. Clin Chim Acta 2020; 507: 167–173

[72] Liu Y, Yang Y, Zhang C, Huang F, Wang F, Yuan J, Wang Z, Li J, Li J, Feng C, Zhang Z, Wang L, Peng L, Chen L, Qin Y, Zhao D, Tan S, Yin L, Xu J, Zhou C, Jiang C, Liu L. Clinical and biochemical indexes from 2019-nCoV infected patients linked to viral loads and lung injury. Sci China Life Sci 2020; 63(3): 364–374

[73] Genchi A, Semerano A, Schwarz G, Dell’Acqua B, Gullotta GS, Sampaolo M, Boeri E, Quattrini A, Sanvito F, Diamanti S, Bergamaschi A, Grassi S, Podini P, Panni P, Michelozzi C, Simionato F, Scomazzoni F, Remida P, Valvassori L, Falini A, Ferrarese C, Michel P, Saliou G, Hajdu S, Beretta S, Roveri L, Filippi M, Strambo D, Martino G, Bacigaluppi M. Neutrophils predominate the immune signature of cerebral thrombi in COVID-19 stroke patients. Acta Neuropathol Commun 2022; 10(1): 14

[74] Iba T, Connors JM, Levy JH. The coagulopathy, endotheliopathy, and vasculitis of COVID-19. Inflamm Res 2020; 69(12): 1181–1189

[75] Ojo AS, Balogun SA, Idowu AO. Acute ischemic stroke in COVID-19: putative mechanisms, clinical characteristics, and management. Neurol Res Int 2020; 2020: 7397480

[76] Fifi JT, Mocco J. COVID-19 related stroke in young individuals. Lancet Neurol 2020; 19(9): 713–715

[77] Benger M, Williams O, Siddiqui J, Sztriha L. Intracerebral haemorrhage and COVID-19: clinical characteristics from a case series. Brain Behav Immun 2020; 88: 940–944

[78] Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, Mehra MR, Schuepbach RA, Ruschitzka F, Moch H. Endothelial cell infection and endotheliitis in COVID-19. Lancet 2020; 395(10234): 1417–1418

[79] Song P, Li W, Xie J, Hou Y, You C. Cytokine storm induced by SARS-CoV-2. Clin Chim Acta 2020; 509: 280–287

[80] Buzhdygan TP, DeOre BJ, Baldwin-Leclair A, Bullock TA, McGary HM, Khan JA, Razmpour R, Hale JF, Galie PA, Potula R, Andrews AM, Ramirez SH. The SARS-CoV-2 spike protein alters barrier function in 2D static and 3D microfluidic in-vitro models of the human blood-brain barrier. Neurobiol Dis 2020; 146: 105131

[81] Yang C, Hawkins KE, Doré S, Candelario-Jalil E. Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am J Physiol Cell Physiol 2019; 316(2): C135–C153

[82] Hernández-Fernández F, Sandoval Valencia H, Barbella-Aponte RA, Collado-Jiménez R, Ayo-MartínÓ, Barrena C, Molina-Nuevo JD, García-García J, Lozano-Setién E, Alcahut-Rodriguez C, Martínez-MartínÁ, Sánchez-López A, Segura T. Cerebrovascular disease in patients with COVID-19: neuroimaging, histological and clinical description. Brain 2020; 143(10): 3089–3103

[83] Franceschi AM, Ahmed O, Giliberto L, Castillo M. Hemorrhagic posterior reversible encephalopathy syndrome as a manifestation of COVID-19 infection. AJNR Am J Neuroradiol 2020; 41(7): 1173–1176

[84] Hess DC, Eldahshan W, Rutkowski E. COVID-19-related stroke. Transl Stroke Res 2020; 11(3): 322–325

[85] Valderrama EV, Humbert K, Lord A, Frontera J, Yaghi S. Severe acute respiratory syndrome coronavirus 2 infection and ischemic stroke. Stroke 2020; 51(7): e124–e127

[86] Berkman SA, Tapson VF. COVID-19 and its implications for thrombosis and anticoagulation. Semin Respir Crit Care Med 2021; 42(2): 316–326

[87] Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, Endeman H. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res 2020; 191: 145–147

[88] Levi M. COVID-19 coagulopathy vs disseminated intravascular coagulation. Blood Adv 2020; 4(12): 2850

[89] Szegedi I, Orbán-Kálmándi R, Csiba L, Bagoly Z. Stroke as a potential complication of COVID-19-associated coagulopathy: a narrative and systematic review of the literature. J Clin Med 2020; 9(10): 3137

[90] Zhang Y, Cao W, Jiang W, Xiao M, Li Y, Tang N, Liu Z, Yan X, Zhao Y, Li T, Zhu T. Profile of natural anticoagulant, coagulant factor and anti-phospholipid antibody in critically ill COVID-19 patients. J Thromb Thrombolysis 2020; 50(3): 580–586

[91] Bowles L, Platton S, Yartey N, Dave M, Lee K, Hart DP, MacDonald V, Green L, Sivapalaratnam S, Pasi KJ, MacCallum P. Lupus anticoagulant and abnormal coagulation tests in patients with Covid-19. N Engl J Med 2020; 383(3): 288–290

[92] Guo T, Fan Y, Chen M, Wu X, Zhang L, He T, Wang H, Wan J, Wang X, Lu Z. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA Cardiol 2020; 5(7): 811–818

[93] Faghy MA, Yates J, Hills AP, Jayasinghe S, da Luz Goulart C, Arena R, Laddu D, Gururaj R, Veluswamy SK, Dixit S, Ashton REM. Cardiovascular disease prevention and management in the COVID-19 era and beyond: an international perspective. Prog Cardiovasc Dis 2023; 76: 102–111

[94] Yaghi S, Ishida K, Torres J, Mac Grory B, Raz E, Humbert K, Henninger N, Trivedi T, Lillemoe K, Alam S, Sanger M, Kim S, Scher E, Dehkharghani S, Wachs M, Tanweer O, Volpicelli F, Bosworth B, Lord A, Frontera J. SARS-CoV-2 and stroke in a New York healthcare system. Stroke 2020; 51(7): 2002–2011

[95] Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, Endeman H. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: an updated analysis. Thromb Res 2020; 191: 148–150

[96] Spence JD, de Freitas GR, Pettigrew LC, Ay H, Liebeskind DS, Kase CS, Del Brutto OH, Hankey GJ, Venketasubramanian N. Mechanisms of stroke in COVID-19. Cerebrovasc Dis 2020; 49(4): 451–458

[97] Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. JAMA 2020; 323(13): 1239–1242

[98] Solomon IH, Normandin E, Bhattacharyya S, Mukerji SS, Keller K, Ali AS, Adams G, Hornick JL, Padera RF Jr, Sabeti P. Neuropathological features of Covid-19. N Engl J Med 2020; 383(10): 989–992

[99] Co COC, Yu JRT, Laxamana LC, David-Ona DIA. Intravenous thrombolysis for stroke in a COVID-19 positive Filipino patient, a case report. J Clin Neurosci 2020; 77: 234–236

[100] Helms J, Kremer S, Merdji H, Clere-Jehl R, Schenck M, Kummerlen C, Collange O, Boulay C, Fafi-Kremer S, Ohana M, Anheim M, Meziani F. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med 2020; 382(23): 2268–2270

[101] Williams OH, Mohideen S, Sen A, Martinovic O, Hart J, Brex PA, Sztriha LK. Multiple internal border zone infarcts in a patient with COVID-19 and CADASIL. J Neurol Sci 2020; 416: 116980

[102] Schulman S. Coronavirus disease 2019, prothrombotic factors, and venous thromboembolism. Semin Thromb Hemost 2020; 46(7): 772–776

[103] Helms J, Tacquard C, Severac F, Leonard-Lorant I, Ohana M, Delabranche X, Merdji H, Clere-Jehl R, Schenck M, Fagot Gandet F, Fafi-Kremer S, Castelain V, Schneider F, Grunebaum L, Anglés-Cano E, Sattler L, Mertes PM, Meziani F; CRICS TRIGGERSEP Group (Clinical Research in Intensive Care, Sepsis Trial Group for Global Evaluation, Research in Sepsis). High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med 2020; 46(6): 1089–1098

[104] Ghosh R, Roy D, Mandal A, Pal SK, Chandra Swaika B, Naga D, Pandit A, Ray BK, Benito-León J. Cerebral venous thrombosis in COVID-19. Diabetes Metab Syndr 2021; 15(3): 1039–1045

[105] Yamakawa M, Kuno T, Mikami T, Takagi H, Gronseth G. Clinical characteristics of stroke with COVID-19: a systematic review and meta-analysis. J Stroke Cerebrovasc Dis 2020; 29(12): 105288

[106] Lisabeth LD, Brown DL, Hughes R, Majersik JJ, Morgenstern LB. Acute stroke symptoms: comparing women and men. Stroke 2009; 40(6): 2031–2036

[107] Majidi S, Fifi JT, Ladner TR, Lara-Reyna J, Yaeger KA, Yim B, Dangayach N, Oxley TJ, Shigematsu T, Kummer BR, Stein LK, Weinberger J, Fara MG, De Leacy R, Dhamoon MS, Tuhrim S, Mocco J. Emergent large vessel occlusion stroke during New York City’s COVID-19 outbreak: clinical characteristics and paraclinical findings. Stroke 2020; 51(9): 2656–2663

[108] Wang A, Mandigo GK, Yim PD, Meyers PM, Lavine SD. Stroke and mechanical thrombectomy in patients with COVID-19: technical observations and patient characteristics. J Neurointerv Surg 2020; 12(7): 648–653

[109] Perry RJ, Smith CJ, Roffe C, Simister R, Narayanamoorthi S, Marigold R, Willmot M, Dixit A, Hassan A, Quinn TJ, Ankolekar S, Zhang L, Banerjee S, Ahmed U, Padmanabhan N, Ferdinand P, McGrane F, Banaras A, Marks IH, Werring DJ; SETICOS collaborators. Characteristics and outcomes of COVID-19 associated stroke: a UK multicentre case-control study. J Neurol Neurosurg Psychiatry 2021; 92(3): 242–248

[110] Simpkins AN, Lekoubou A. Risk of acute ischemic stroke in patients 65 and older is early after COVID-19 diagnosis. Neurology. 2022; 98(8): 301–302

[111] Li Y, Li M, Wang M, Zhou Y, Chang J, Xian Y, Wang D, Mao L, Jin H, Hu B. Acute cerebrovascular disease following COVID-19: a single center, retrospective, observational study. Stroke Vasc Neurol 2020; 5(3): 279–284

[112] Fridman S, Bres Bullrich M, Jimenez-Ruiz A, Costantini P, Shah P, Just C, Vela-Duarte D, Linfante I, Sharifi-Razavi A, Karimi N, Bagur R, Debicki DB, Gofton TE, Steven DA, Sposato LA. Stroke risk, phenotypes, and death in COVID-19: systematic review and newly reported cases. Neurology 2020; 95(24): e3373–e3385

[113] Escalard S, Chalumeau V, Escalard C, Redjem H, Delvoye F, Hébert S, Smajda S, Ciccio G, Desilles JP, Mazighi M, Blanc R, Maïer B, Piotin M. Early brain imaging shows increased severity of acute ischemic strokes with large vessel occlusion in COVID-19 patients. Stroke 2020; 51(11): 3366–3370

[114] John S, Hussain SI, Piechowski-Jozwiak B, Dibu J, Kesav P, Bayrlee A, Elkambergy H, John TLS, Roser F, Mifsud VA. Clinical characteristics and admission patterns of stroke patients during the COVID 19 pandemic: a single center retrospective, observational study from the Abu Dhabi, United Arab Emirates. Clin Neurol Neurosurg 2020; 199: 106227

[115] Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, De Leacy RA, Shigematsu T, Ladner TR, Yaeger KA, Skliut M, Weinberger J, Dangayach NS, Bederson JB, Tuhrim S, Fifi JT. Large-vessel stroke as a presenting feature of Covid-19 in the young. N Engl J Med 2020; 382(20): e60

[116] Tan YK, Goh C, Leow AST, Tambyah PA, Ang A, Yap ES, Tu TM, Sharma VK, Yeo LLL, Chan BPL, Tan BYQ. COVID-19 and ischemic stroke: a systematic review and meta-summary of the literature. J Thromb Thrombolysis 2020; 50(3): 587–595

[117] Siegler JE, Heslin ME, Thau L, Smith A, Jovin TG. Falling stroke rates during COVID-19 pandemic at a comprehensive stroke center. J Stroke Cerebrovasc Dis 2020; 29(8): 104953

[118] Jain R. Evolving neuroimaging findings during COVID-19. AJNR Am J Neuroradiol 2020; 41(8): 1355–1356

[119] Sweid A, Hammoud B, Ramesh S, Wong D, Alexander TD, Weinberg JH, Deprince M, Dougherty J, Maamari DJ, Tjoumakaris S, Zarzour H, Gooch MR, Herial N, Romo V, Hasan DM, Rosenwasser RH, Jabbour P. Acute ischaemic stroke interventions: large vessel occlusion and beyond. Stroke Vasc Neurol 2020; 5(1): 80–85

[120] Malhotra K, Gornbein J, Saver JL. Ischemic strokes due to large-vessel occlusions contribute disproportionately to stroke-related dependence and death: a review. Front Neurol 2017; 8: 651

[121] Ornello R, Degan D, Tiseo C, Di Carmine C, Perciballi L, Pistoia F, Carolei A, Sacco S. Distribution and temporal trends from 1993 to 2015 of ischemic stroke subtypes: a systematic review and meta-analysis. Stroke 2018; 49(4): 814–819

[122] Lin E, Lantos JE, Strauss SB, Phillips CD, Campion TR Jr, Navi BB, Parikh NS, Merkler AE, Mir S, Zhang C, Kamel H, Cusick M, Goyal P, Gupta A. Brain imaging of patients with COVID-19: findings at an academic institution during the height of the outbreak in New York City. AJNR Am J Neuroradiol 2020; 41(11): 2001–2008

[123] Tsivgoulis G, Katsanos AH, Ornello R, Sacco S. Ischemic stroke epidemiology during the COVID-19 pandemic: navigating uncharted waters with changing tides. Stroke 2020; 51(7): 1924–1926

[124] Trifan G, Goldenberg FD, Caprio FZ, Biller J, Schneck M, Khaja A, Terna T, Brorson J, Lazaridis C, Bulwa Z, Alvarado Dyer R, Saleh Velez FG, Prabhakaran S, Liotta EM, Batra A, Reish NJ, Ruland S, Teitcher M, Taylor W, De la Pena P, Conners JJ, Grewal PK, Pinna P, Dafer RM, Osteraas ND, DaSilva I, Hall JP, John S, Shafi N, Miller K, Moustafa B, Vargas A, Gorelick PB, Testai FD. Characteristics of a diverse cohort of stroke patients with SARS-CoV-2 and outcome by sex. J Stroke Cerebrovasc Dis 2020; 29(11): 105314

[125] Ramos-Araque ME, Siegler JE, Ribo M, Requena M, López C, de Lera M, Arenillas JF, Pérez IH, Gómez-Vicente B, Talavera B, Portela PC, Guillen AN, Urra X, Llull L, Renú A, Nguyen TN, Jillella D, Nahab F, Nogueira R, Haussen D, Then R, Thon JM, Esparragoza LR, Hernández-Pérez M, Bustamante A, Mansour OY, Megahed M, Hassan T, Liebeskind DS, Hassan A, Bushnaq S, Osman M, Vazquez AR; SVIN Multinational Registry, Task Force. Stroke etiologies in patients with COVID-19: the SVIN COVID-19 multinational registry. BMC Neurol 2021; 21(1): 43

[126] Saver JL. Cryptogenic stroke. N Engl J Med 2016; 375(11): e26

[127] Arboix A, Blanco-Rojas L, Martí-Vilalta JL. Advancements in understanding the mechanisms of symptomatic lacunar ischemic stroke: translation of knowledge to prevention strategies. Expert Rev Neurother 2014; 14(3): 261–276

[128] Arboix A, Blanco-Rojas L, Martí-Vilalta JL. Advancements in understanding the mechanisms of symptomatic lacunar ischemic stroke: translation of knowledge to prevention strategies. Expert Rev Neurother 2014; 14(3): 261–276

[129] Dogra S, Jain R, Cao M, Bilaloglu S, Zagzag D, Hochman S, Lewis A, Melmed K, Hochman K, Horwitz L, Galetta S, Berger J. Hemorrhagic stroke and anticoagulation in COVID-19. J Stroke Cerebrovasc Dis 2020; 29(8): 104984

[130] Chen Y, Xia F, Li Y, Li H, Ma L, Hu X, You C. Changes in characteristics, treatment and outcome in patients with hemorrhagic stroke during COVID-19. J Stroke Cerebrovasc Dis 2021; 30(3): 105536

[131] Parra-Romero G, Navarro-Olvera JL, Beltrán-Mendoza JQ, Ruiz-Sandoval JL, Mar-Álvarez A, Aguado-Carrillo G, Teyes-Calva N, Rodríguez-Morales J, Martínez-Luna AA, Hernández-Valencia AF, Carrillo-Ruiz JD. Primary spontaneous intracerebral hemorrhage in COVID-19 patients: differences among presentation patterns—a systematic review. Cir Cir 2022; 90(6): 734–741

[132] Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, Osteraas ND, Pellack DR, Asthana A, Fegan K, Patel V, Conners JJ, John S, Silva ID. Neurological manifestations and COVID-19: experiences from a tertiary care center at the frontline. J Neurol Sci 2020; 415: 116969

[133] Kvernland A, Kumar A, Yaghi S, Raz E, Frontera J, Lewis A, Czeisler B, Kahn DE, Zhou T, Ishida K, Torres J, Riina HA, Shapiro M, Nossek E, Nelson PK, Tanweer O, Gordon D, Jain R, Dehkharghani S, Henninger N, de Havenon A, Grory BM, Lord A, Melmed K. Anticoagulation use and hemorrhagic stroke in SARS-CoV-2 patients treated at a New York healthcare system. Neurocrit Care 2021; 34(3): 748–759

[134] Gunes HN, Cokal BG, Guler SK, Yoldas TK, Malkan UY, Demircan CS, Yon MI, Yoldas Z, Gunes G, Haznedaroglu IC. Clinical associations, biological risk factors and outcomes of cerebral venous sinus thrombosis. J Int Med Res 2016; 44(6): 1454–1461

[135] Coutinho JM, Zuurbier SM, Aramideh M, Stam J. The incidence of cerebral venous thrombosis: a cross-sectional study. Stroke 2012; 43(12): 3375–3377

[136] Ostovan VR, Foroughi R, Rostami M, Almasi-Dooghaee M, Esmaili M, Bidaki AA, Behzadi Z, Farzadfard F, Marbooti H, Rahimi-Jaberi A, Poursadeghfard M, Fadakar N, Bayat M, Owjfard M, Salehi MS, Zafarmand SS, Mardi F, Safari A, Shahjouei S, Mowla A, Azarpazhooh MR, Zand R, Hooshmandi E, Borhani-Haghighi A. Cerebral venous sinus thrombosis associated with COVID-19: a case series and literature review. J Neurol 2021; 268(10): 3549–3560

[137] Bousser MG, Ferro JM. Cerebral venous thrombosis: an update. Lancet Neurol 2007; 6(2): 162–170

[138] Benussi A, Pilotto A, Premi E, Libri I, Giunta M, Agosti C, Alberici A, Baldelli E, Benini M, Bonacina S, Brambilla L, Caratozzolo S, Cortinovis M, Costa A, Cotti Piccinelli S, Cottini E, Cristillo V, Delrio I, Filosto M, Gamba M, Gazzina S, Gilberti N, Gipponi S, Imarisio A, Invernizzi P, Leggio U, Leonardi M, Liberini P, Locatelli M, Masciocchi S, Poli L, Rao R, Risi B, Rozzini L, Scalvini A, Schiano di Cola F, Spezi R, Vergani V, Volonghi I, Zoppi N, Borroni B, Magoni M, Pezzini A, Padovani A. Clinical characteristics and outcomes of inpatients with neurologic disease and COVID-19 in Brescia, Lombardy, Italy. Neurology 2020; 95(7): e910–e920

[139] Beyrouti R, Adams ME, Benjamin L, Cohen H, Farmer SF, Goh YY, Humphries F, Jäger HR, Losseff NA, Perry RJ, Shah S, Simister RJ, Turner D, Chandratheva A, Werring DJ. Characteristics of ischaemic stroke associated with COVID-19. J Neurol Neurosurg Psychiatry 2020; 91(8): 889–891

[140] Barrios-López JM, Rego-García I, Muñoz Martínez C, Romero-Fábrega JC, Rivero Rodríguez M, Ruiz Giménez JA, Escamilla-Sevilla F, Mínguez-Castellanos A, Fernández Pérez MD. Ischaemic stroke and SARS-CoV-2 infection: a causal or incidental association?. Neurología (Engl Ed) 2020; 35(5): 295–302

[141] Katz JM, Libman RB, Wang JJ, Filippi CG, Sanelli P, Zlochower A, Gribko M, Pacia SV, Kuzniecky RI, Najjar S, Azhar S. COVID-19 severity and stroke: correlation of imaging and laboratory markers. AJNR Am J Neuroradiol. 2021; 42(2): 257–261

[142] Koralnik IJ, Tyler KL. COVID-19: a global threat to the nervous system. Ann Neurol 2020; 88(1): 1–11

[143] Reddy ST, Garg T, Shah C, Nascimento FA, Imran R, Kan P, Bowry R, Gonzales N, Barreto A, Kumar A, Volpi J, Misra V, Chiu D, Gadhia R, Savitz SI. Cerebrovascular disease in patients with COVID-19: a review of the literature and case series. Case Rep Neurol 2020; 12(2): 199–209

[144] Fara MG, Stein LK, Skliut M, Morgello S, Fifi JT, Dhamoon MS. Macrothrombosis and stroke in patients with mild Covid-19 infection. J Thromb Haemost 2020; 18(8): 2031–2033

[145] Morassi M, Bagatto D, Cobelli M, D’Agostini S, Gigli GL, Bnà C, Vogrig A. Stroke in patients with SARS-CoV-2 infection: case series. J Neurol 2020; 267(8): 2185–2192

[146] Gupta NA, Lien C, Iv M. Critical illness-associated cerebral microbleeds in severe COVID-19 infection. Clin Imaging 2020; 68: 239–241

[147] Dixon L, McNamara C, Gaur P, Mallon D, Coughlan C, Tona F, Jan W, Wilson M, Jones B. Cerebral microhaemorrhage in COVID-19: a critical illness related phenomenon?. Stroke Vasc Neurol 2020; 5(4): 315–322

[148] Mazzacane F, Zito A, Magno S, Persico A, Mazzoleni V, Asteggiano C, Rognone E, Pichiecchio A, Padovani A, Cavallini A, Morotti A. Vessel wall magnetic resonance imaging in COVID-19-associated cryptogenic ischemic stroke. Eur J Neurol 2022; 29(2): 615–619

[149] Ferro JM, Canhão P, Stam J, Bousser MG, Barinagarrementeria F; ISCVT Investigators. Prognosis of cerebral vein and dural sinus thrombosis: results of the International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT). Stroke 2004; 35(3): 664–670

[150] John S, Kesav P, Mifsud VA, Piechowski-Jozwiak B, Dibu J, Bayrlee A, Elkambergy H, Roser F, Elhammady MS, Zahra K, Hussain SI. Characteristics of large-vessel occlusion associated with COVID-19 and ischemic stroke. AJNR Am J Neuroradiol 2020; 41(12): 2263–2268

[151] Scutelnic A, Krzywicka K, Mbroh J, van de Munckhof A, van Kammen MS, de Sousa DA, Lindgren E, Jood K, Günther A, Hiltunen S, Putaala J, Tiede A, Maier F, Kern R, Bartsch T, Althaus K, Ciccone A, Wiedmann M, Skjelland M, Medina A, Cuadrado-Godia E, Cox T, Aujayeb A, Raposo N, Garambois K, Payen JF, Vuillier F, Franchineau G, Timsit S, Bougon D, Dubois MC, Tawa A, Tracol C, De Maistre E, Bonneville F, Vayne C, Mengel A, Michalski D, Pelz J, Wittstock M, Bode F, Zimmermann J, Schouten J, Buture A, Murphy S, Palma V, Negro A, Gutschalk A, Nagel S, Schoenenberger S, Frisullo G, Zanferrari C, Grillo F, Giammello F, Martin MM, Cervera A, Burrow J, Esperon CG, Chew BLA, Kleinig TJ, Soriano C, Zimatore DS, Petruzzellis M, Elkady A, Miranda MS, Fernandes J, VogelÅH, Johansson E, Philip AP, Coutts SB, Bal S, Buck B, Legault C, Blacquiere D, Katzberg HD, Field TS, Dizonno V, Gattringer T, Jacobi C, Devroye A, Lemmens R, Kristoffersen ES, di Poggio MB, Ghiasian M, Karapanayiotides T, Chatterton S, Wronski M, Ng K, Kahnis R, Geeraerts T, Reiner P, Cordonnier C, Middeldorp S, Levi M, van Gorp ECM, van de Beek D, Brodard J, Kremer Hovinga JA, Kruip MJHA, Tatlisumak T, Ferro JM, Coutinho JM, Arnold M, Poli S, Heldner MR. Management of cerebral venous thrombosis due to adenoviral COVID-19 vaccination. Ann Neurol 2022; 92(4): 562–573

[152] de Simone G, Stranges S, Gentile I. Incidence of cerebral venous thrombosis and COVID-19 vaccination: possible causal effect or just chance?. Eur Heart J Cardiovasc Pharmacother 2021; 7(4): e77–e78

[153] Elfil M, Aladawi M, Balian D, Fahad I, Zhou DJ, Villafuerte-Trisolini B, Diesing TS. Cerebral venous sinus thrombosis after COVID-19 vaccination: a case report and literature review. Oxf Med Case Rep 2023; 2023(1): omac154

[154] Schultz NH, Søraas AVL, Sørvoll IH, AkkökÇA, Vetlesen A, Bhamra JS, Ahlen MT, Holme PA, Aamodt AH, Skagen K, Skattør TH, Skjelland M, Wiedmann MK. Vaccine associated benign headache and cutaneous hemorrhage after ChAdOx1 nCoV-19 vaccine: a cohort study. J Stroke Cerebrovasc Dis 2023; 32(1): 106860

[155] Kakovan M, Ghorbani Shirkouhi S, Zarei M, Andalib S. Stroke associated with COVID-19 vaccines. J Stroke Cerebrovasc Dis 2022; 31(6): 106440

[156] Ferraù L, Cotroneo M, Dell'Aera C, Giammello F, Grillo F, Brizzi T, Pitrone A, Vinci SL, Musolino RF, La Spina P. Carotid free-floating thrombus during COVID-19 vaccine era: causality or not?. Neurol Sci 2022; 43(11): 6179–6183

[157] Sadoff J, Davis K, Douoguih M. Thrombotic thrombocytopenia after Ad26.COV2.S vaccination—response from the manufacturer. N Engl J Med 2021; 384(20): 1965–1966

[158] Muir KL, Kallam A, Koepsell SA, Gundabolu K. Thrombotic thrombocytopenia after Ad26.COV2.S vaccination. N Engl J Med 2021; 384(20): 1964–1965

[159] Scully M, Singh D, Lown R, Poles A, Solomon T, Levi M, Goldblatt D, Kotoucek P, Thomas W, Lester W. Pathologic antibodies to platelet factor 4 after ChAdOx1 nCoV-19 vaccination. N Engl J Med 2021; 384(23): 2202–2211

[160] Kowarz E, Krutzke L, Külp M, Streb P, Larghero P, Reis J, Bracharz S, Engler T, Kochanek S, Marschalek R. Vaccine-induced COVID-19 mimicry syndrome. eLife 2022; 11: e74974

[161] Chen WP, Chen MH, Shang ST, Kao YH, Wu KA, Chiang WF, Chan JS, Shyu HY, Hsiao PJ. Investigation of neurological complications after COVID-19 vaccination: report of the clinical scenarios and review of the literature. Vaccines (Basel) 2023; 11(2): 425

[162] Tu TM, Yi SJ, Koh JS, Saffari SE, Hoe RHM, Chen GJ, Chiew HJ, Tham CH, Seet CYH, Yong MH, Yong KP, Hui AC, Fan BE, Tan BY, Quek AML, Seet RCS, Yeo LLL, Tan K, Thirugnanam UN. Incidence of cerebral venous thrombosis following SARS-CoV-2 infection vs mRNA SARS-CoV-2 vaccination in Singapore. JAMA Netw Open 2022; 5(3): e222940

[163] Kim AY, Woo W, Yon DK, Lee SW, Yang JW, Kim JH, Park S, Koyanagi A, Kim MS, Lee S, Shin JI, Smith L. Thrombosis patterns and clinical outcome of COVID-19 vaccine-induced immune thrombotic thrombocytopenia: a systematic review and meta-analysis. Int J Infect Dis 2022; 119: 130–139

[164] Hovi P, Palmu AA, Nieminen TA, Artama M, Jokinen J, Ruokokoski E, Lassila R, Nohynek H, Kilpi T. Incidence of sinus thrombosis with thrombocytopenia—a nation-wide register study. PLoS One 2023; 18(2): e0282226

[165] Perry RJ, Tamborska A, Singh B, Craven B, Marigold R, Arthur-Farraj P, Yeo JM, Zhang L, Hassan-Smith G, Jones M, Hutchcroft C, Hobson E, Warcel D, White D, Ferdinand P, Webb A, Solomon T, Scully M, Werring DJ, Roffe C; CVT After Immunisation Against COVID-19 (CAIAC) collaborators. Cerebral venous thrombosis after vaccination against COVID-19 in the UK: a multicentre cohort study. Lancet 2021; 398(10306): 1147–1156

[166] Wittstock M, Walter U, Volmer E, Storch A, Weber MA, Großmann A. Cerebral venous sinus thrombosis after adenovirus-vectored COVID-19 vaccination: review of the neurological-neuroradiological procedure. Neuroradiology 2022; 64(5): 865–874

[167] Kadam N, Ramavathu KV, Kamath N, Min KK. Imaging findings in a patient with suspected vaccine induced immune thrombotic thrombocytopenia. BJR Case Rep 2022; 8(1): 20210138

[168] Tiede A, Sachs UJ, Czwalinna A, Werwitzke S, Bikker R, Krauss JK, Donnerstag F, Weißenborn K, Höglinger G, Maasoumy B, Wedemeyer H, Ganser A. Prothrombotic immune thrombocytopenia after COVID-19 vaccination. Blood 2021; 138(4): 350–353

[169] Favaloro EJ. Laboratory testing for suspected COVID-19 vaccine-induced (immune) thrombotic thrombocytopenia. Int J Lab Hematol 2021; 43(4): 559–570

[170] Tu TM, Goh C, Tan YK, Leow AS, Pang YZ, Chien J, Shafi H, Chan BP, Hui A, Koh J, Tan BY, Umapathi NT, Yeo LL. Cerebral venous thrombosis in patients with COVID-19 infection: a case series and systematic review. J Stroke Cerebrovasc Dis 2020; 29(12): 105379

[171] Cheruiyot I, Sehmi P, Ominde B, Bundi P, Mislani M, Ngure B, Olabu B, Ogeng'o JA. Intracranial hemorrhage in coronavirus disease 2019 (COVID-19) patients. Neurol Sci 2021; 42(1): 25–33

[172] Katz JM, Libman RB, Wang JJ, Sanelli P, Filippi CG, Gribko M, Pacia SV, Kuzniecky RI, Najjar S, Azhar S. Cerebrovascular complications of COVID-19. Stroke 2020; 51(9): e227–e231

[173] Baud D, Qi X, Nielsen-Saines K, Musso D, Pomar L, Favre G. Real estimates of mortality following COVID-19 infection. Lancet Infect Dis 2020; 20(7): 773

[174] Bousser MG, Ferro JM. Cerebral venous thrombosis: an update. Lancet Neurol 2007; 6(2): 162–170

[175] Cappellari M, Zini A, Sangalli D, Cavallini A, Reggiani M, Sepe FN, Rifino N, Giussani G, Guidetti D, Zedde M, Marcheselli S, Longoni M, Beretta S, Sidoti V, Papurello DM, Giossi A, Nencini P, Plocco M, Balestrino M, Rota E, Toni D. Thrombolysis and bridging therapy in patients with acute ischaemic stroke and Covid-19. Eur J Neurol 2020; 27(12): 2641–2645

[176] Lazzaroni MG, Piantoni S, Masneri S, Garrafa E, Martini G, Tincani A, Andreoli L, Franceschini F. Coagulation dysfunction in COVID-19: the interplay between inflammation, viral infection and the coagulation system. Blood Rev 2021; 46: 100745

[177] Vidale S. Risk factors, and clinical and etiological characteristics of ischemic strokes in COVID-19-infected patients: a systematic review of literature. Cerebrovasc Dis 2021; 50(4): 371–374

[178] Zhao J, Rudd A, Liu R. Challenges and potential solutions of stroke care during the coronavirus disease 2019 (COVID-19) outbreak. Stroke 2020; 51(5): 1356–1357

[179] Hu Q, Hu Y, Gu Y, Song X, Shen Y, Lu H, Zhang L, Liu P, Wang G, Guo C, Fang K, Wang Q. Impact of the COVID-19 pandemic on acute stroke care: an analysis of the 24-month data from a comprehensive stroke center in Shanghai, China. CNS Neurosci Ther 2023; 29(7): 1898–1906

[180] Nawabi NLA, Duey AH, Kilgallon JL, Jessurun C, Doucette J, Mekary RA, Aziz-Sultan MA. Effects of the COVID-19 pandemic on stroke response times: a systematic review and meta-analysis. J Neurointerv Surg 2022; 14(7): 642–649

[181] Paliwal PR, Tan BYQ, Leow AST, Sibi S, Chor DWP, Chin AXY, Yau YW, Cross GB, Wong LYH, Chia MLJ, Quak Z, Chua CYK, Tang DKK, Zune ET, Hung J, Goh Y, Jing M, Gopinathan A, Yang C, Ahmad A, Khoo DXL, Lee CM, Seet RCS, Sharma VK, Teoh HL, Yeo LLL, Chan BPL. Impact of the COVID-19 pandemic on hyperacute stroke treatment: experience from a comprehensive stroke centre in Singapore. J Thromb Thrombolysis 2020; 50(3): 596–603

[182] Saban M, Reznik A, Shachar T, Wilf-Miron R, Sivan-Hoffmann R. The effect of the COVID-19 pandemic on ED referrals and care for stroke patients: a four-year comparative study. J Crit Care 2021; 62: 230–234

[183] Gabet A, Grave C, Tuppin P, Chatignoux E, Béjot Y, Olié V. Impact of the COVID-19 pandemic and a national lockdown on hospitalizations for stroke and related 30-day mortality in France: a nationwide observational study. Eur J Neurol 2021; 28(10): 3279–3288

[184] Tu WJ, Xu Y, Chen H, Li J, Du J. Impact of the COVID-19 pandemic lockdown on hospitalizations for cerebrovascular disease and related in-hospital mortality in China: a nationwide observational study. Arch Gerontol Geriatr 2023; 104: 104832

[185] Kansagra AP, Goyal MS, Hamilton S, Albers GW. Collateral effect of Covid-19 on stroke evaluation in the United States. N Engl J Med 2020; 383(4): 400–401

[186] Gu S, Dai Z, Shen H, Bai Y, Zhang X, Liu X, Xu G. Delayed stroke treatment during COVID-19 pandemic in China. Cerebrovasc Dis 2021; 50(6): 715–721

[187] Xu X, Xiao Y, Li J, Chen L, Lin G, Dong L, Lin Y, Zhan L, He J, Luan X. Decrease in intravenous thrombolysis and poor short-term functional prognosis for acute ischemic stroke during the COVID-19 pandemic. J Neurol 2022; 269(2): 597–602

[188] Wang X, Ouyang M, Carcel C, Chen C, Sun L, Yang J, Zhang Y, Chen G, You S, Cao Y, Ma L, Hu X, Sui Y, Anderson C, Song L, Wang Y, Wang D. Impact of COVID-2019 on stroke services in China: survey from the Chinese Stroke Association. Stroke Vasc Neurol 2020; 5(4): 323–330

[189] Commission Expert Committee of Stroke Prevention, Treatment Project of National Health. Expert consensus on green channel management of stroke in novel coronavirus pneumonia. J Capital Med Univ (Shou Du Yi Ke Da Xue Xue Bao) 2020; 41(2): 293–297

[190] Commission Expert Committee of Stroke Prevention, Treatment Project of National Health. Expert consensus on green channel management of stroke in novel coronavirus pneumonia (2022 edition). Chin J Cerebrovasc Dis (Zhongguo Nao Xue Guan Bing Za Zhi) 2022; 19(11): 797–801

[191] Sharrief AZ, Guzik AK, Jones E, Okpala M, Love MF, Ranasinghe TIJ, Bushnell C. Telehealth trials to address health equity in stroke survivors. Stroke 2023; 54(2): 396–406

[192] Chen N, Wu X, Zhou M, Yang R, Chen D, Liao M, Deng Y, Hong Z, Zhou D, He L. Telestroke for the treatment of ischemic stroke in Western China during the COVID-19 pandemic: a multicenter observational study. Front Neurol 2022; 12: 822342

[193] Pan X, Ma S, Sui X, Xie L, Li F, Cheng Z, Cui L, Zhao H. The effects of the coronavirus disease pandemic on intravenous thrombolytic therapy among patients with acute ischemic stroke in Dalian, China. BMC Neurol 2023; 23(1): 10

[194] Jurkevičienė J, Vaišvilas M, Masiliūnas R, Matijošaitis V, Vaitkus A, Geštautaitė D, Taroza S, Puzinas P, Galvanauskaitė E, Jatužis D, Vilionskis A. Reperfusion therapies for acute ischemic stroke in COVID-19 patients: a nationwide multi-center study. J Clin Med 2022; 11(11): 3004

[195] de Havenon A, Yaghi S, Mistry EA, Delic A, Hohmann S, Shippey E, Stulberg E, Tirschwell D, Frontera JA, Petersen NH, Anadani M. Endovascular thrombectomy in acute ischemic stroke patients with COVID-19: prevalence, demographics, and outcomes. J Neurointerv Surg 2020; 12(11): 1045–1048

[196] El-Qushayri AE, Reda A, Dahy A, Azzam AY, Ghozy S. The impact of COVID 19 on the outcomes of thrombectomy in stroke patients: a systematic review and meta-analysis. Rev Med Virol 2023; 33(1): e2379

[197] Dietrich F, Polymeris AA, Verbeek M, Engelter ST, Hersberger KE, Schaedelin S, Arnet I, Lyrer PA. Impact of the COVID-19 lockdown on the adherence of stroke patients to direct oral anticoagulants: a secondary analysis from the MAAESTRO study. J Neurol 2022; 269(1): 19–25

[198] Kollias A, Kyriakoulis KG, Syrigos NK, Stergiou GS. Anticoagulation therapy in COVID-19: is there a dose-dependent benefit?. Thromb Res 2021; 199: 19–20

[199] Qureshi AI, Abd-Allah F, Al-Senani F, Aytac E, Borhani-Haghighi A, Ciccone A, Gomez CR, Gurkas E, Hsu CY, Jani V, Jiao L, Kobayashi A, Lee J, Liaqat J, Mazighi M, Parthasarathy R, Steiner T, Suri MFK, Toyoda K, Ribo M, Gongora-Rivera F, Oliveira-Filho J, Uzun G, Wang Y. Management of acute ischemic stroke in patients with COVID-19 infection: report of an international panel. Int J Stroke 2020; 15(5): 540–554

[200] Ospel JM, Goyal M. Endovascular stroke treatment during the COVID-19 pandemic. Nat Rev Neurol 2020; 16(7): 351–352

[201] Xu Y, Chen Y, Tang X. Guidelines for the diagnosis and treatment of coronavirus disease 2019 (COVID-19) in China. Glob Health Med 2020; 2(2): 66–72

[202] COVID-19 Treatment Guidelines Panel. Coronavirus Disease 2019 (COVID-19) Treatment Guidelines. Bethesda (MD): National Institutes of Health (US), 2021 Apr 21–2023 Nov 2

[203] Greinacher A, Thiele T, Warkentin TE, Weisser K, Kyrle PA, Eichinger S. Thrombotic thrombocytopenia after ChAdOx1 nCov-19 vaccination. N Engl J Med 2021; 384(22): 2092–2101

[204] Norouzi-Barough L, Asgari Khosroshahi A, Gorji A, Zafari F, Shahverdi Shahraki M, Shirian S. COVID-19-induced stroke and the potential of using mesenchymal stem cells-derived extracellular vesicles in the regulation of neuroinflammation. Cell Mol Neurobiol 2023; 43(1): 37–46

[205] McAlpine LS, Zubair AS, Maran I, Chojecka P, Lleva P, Jasne AS, Navaratnam D, Matouk C, Schindler J, Sheth KN, Chun H, Lee AI, Spudich S, Sharma R, Sansing LH. Ischemic stroke, inflammation, and endotheliopathy in COVID-19 patients. Stroke 2021; 52(6): e233–e238

[206] Moriarty PM, Gorby LK, Stroes ES, Kastelein JP, Davidson M, Tsimikas S. Lipoprotein(a) and its potential association with thrombosis and inflammation in COVID-19: a testable hypothesis. Curr Atheroscler Rep 2020; 22(9): 48

[207] Lee MH, Perl DP, Steiner J, Pasternack N, Li W, Maric D, Safavi F, Horkayne-Szakaly I, Jones R, Stram MN, Moncur JT, Hefti M, Folkerth RD, Nath A. Neurovascular injury with complement activation and inflammation in COVID-19. Brain 2022; 145(7): 2555–2568

[208] Chatterjee K, Buchanan A, Cottrell K, Hughes S, Day TW, John NW. Immersive virtual reality for the cognitive rehabilitation of stroke survivors. IEEE Trans Neural Syst Rehabil Eng 2022; 30: 719–728

[209] Akhtar N, Abid F, Singh R, Kamran S, Imam Y, Al Jerdi S, Salameh S, Al Attar R, Yasir M, Shabir H, Morgan D, Joseph S, AlMaslamani M, Shuaib A. Characteristics and comparisons of acute stroke in “recovered” to “active COVID-19” and “pre-pandemic” in Qatar database. J Thromb Thrombolysis 2022; 53(4): 824–828

[210] Campbell BCV, De Silva DA, Macleod MR, Coutts SB, Schwamm LH, Davis SM, Donnan GA. Ischaemic stroke. Nat Rev Dis Primers 2019; 5(1): 70

[211] Bendixen BH, Posner J, Lango R. Stroke in young adults and children. Curr Neurol Neurosci Rep 2001; 1(1): 54–66

[212] Cho SM, White N, Premraj L, Battaglini D, Fanning J, Suen J, Bassi GL, Fraser J, Robba C, Griffee M, Singh B, Citarella BW, Merson L, Solomon T, Thomson D; ISARIC Clinical Characterisation Group. Neurological manifestations of COVID-19 in adults and children. Brain 2023; 146(4): 1648–1661

[213] Mastrangelo M, Giordo L, Ricciardi G, De Michele M, Toni D, Leuzzi V. Acute ischemic stroke in childhood: a comprehensive review. Eur J Pediatr 2022; 181(1): 45–58

[214] Gabet A, Grave C, Chatignoux E, Tuppin P, Béjot Y, Olié V. Characteristics, management, and case-fatality of patients hospitalized for stroke with a diagnosis of COVID-19 in France. Neuroepidemiology 2021; 55(4): 323–330

Acknowledgements

This study was supported by the National Natural Science Foundation of China (No. 82027802), Pharmaceutical Collaboration Project of the Beijing Science and Technology Commission (No. Z181100001918026), and Talents Gathering Project of Xuanwu Hospital, Capital Medical University.

Parts of the Fig.1 and Fig.2 were drawn by using pictures from Servier Medical Art, licensed under a Creative Commons Attribution 3.0 Unported License (https://creativecommons.org/licenses/by/3.0/).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11684-023-1041-7 and is accessible for authorized users.

Compliance with ethics guidelines

Conflicts of Interest Lu Liu, Chenxia Zhou, Huimin Jiang, Huimin Wei, Yifan Zhou, Chen Zhou, and Xunming Ji declare that they have no conflict of interest.

This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

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