Home Infection, inflammation and thrombosis: a review of potential mechanisms mediating arterial thrombosis associated with influenza and severe acute respiratory syndrome coronavirus 2
Article
Licensed
Unlicensed Requires Authentication

Infection, inflammation and thrombosis: a review of potential mechanisms mediating arterial thrombosis associated with influenza and severe acute respiratory syndrome coronavirus 2

  • Stefan Veizades ORCID logo , Alexandria Tso ORCID logo and Patricia K. Nguyen ORCID logo EMAIL logo
Published/Copyright: December 22, 2021

Abstract

Thrombosis has long been reported as a potentially deadly complication of respiratory viral infections and has recently received much attention during the global coronavirus disease 2019 pandemic. Increased risk of myocardial infarction has been reported during active infections with respiratory viruses, including influenza and severe acute respiratory syndrome coronavirus 2, which persists even after the virus has cleared. These clinical observations suggest an ongoing interaction between these respiratory viruses with the host’s coagulation and immune systems that is initiated at the time of infection but may continue long after the virus has been cleared. In this review, we discuss the epidemiology of viral-associated myocardial infarction, highlight recent clinical studies supporting a causal connection, and detail how the virus’ interaction with the host’s coagulation and immune systems can potentially mediate arterial thrombosis.


Corresponding author: Patricia K. Nguyen, Department of Medicine (Cardiovascular Medicine), Stanford University, Falk CVRB, 870 Quarry Ave, Stanford, CA 94305, USA, E-mail:

Funding source: American Heart Association (AHA) https://professional.heart.org/en/research-programs/application-information/transformational-project-award

Award Identifier / Grant number: 20TPA355500081

Funding source: National Institutes of Health (NIH) https://grants.nih.gov/grants/funding/r01.html

Award Identifier / Grant number: RO1 HL 134830-01

Acknowledgements

We would like to acknowledge Katlyn Alexis Carey for the preparation of the figures.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: We would like to thank the AHA (20TPA355500081) and the NIH (RO1 HL 134830-01) for funding support.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Angelillis, M., De Carlo, M., Christou, A., Marconi, M., Mocellin, D.M., Caravelli, P., De Caterina, R., and Petronio, A.S. (2021). A case report of multisite arterial thrombosis in a patient with coronavirus disease 2019 (COVID-19). Eur. Heart J. 1: ytaa339, https://doi.org/10.1093/ehjcr/ytaa339.Search in Google Scholar

Azarhani, A., Al Abdulsalam, H., Al-Sakkaf, H., and Albadr, F.B. (2021). Arterial thrombosis in an asymptomatic COVID-19 complicated by malignant middle cerebral artery syndrome: a case report and literature review. Int Case Rep. 4: 401–405.10.2147/IMCRJ.S306830Search in Google Scholar

Bakirli, I., Tomka, J., Pis, M., Bakirili, H., Bakirova, G., Osusky, M., Gazi, A., and Bakirov, I. (2021). Symptomatic carotid artery thrombosis in a patient recently recovered from a COVID-19 infection. Cureus 13: e18626, https://doi.org/10.7759/cureus.18626.Search in Google Scholar

Benagiano, M., D’Elios, M.M., Amedei, A., Azzurri, A., van der Zee, R., Ciervo, A., Rombolà, G., Romagnani, S., Cassone, A., and Del Prete, G. (2005). Human 60-kDa heat shock protein is a target autoantigen of T cells derived from atherosclerotic plaques. J. Immunol. 174: 6509–6517, https://doi.org/10.4049/jimmunol.174.10.6509.Search in Google Scholar

Boilard, E., Paré, G., Rousseau, M., Cloutier, N., Dubuc, I., Lévesque, T., Borgeat, P., and Flamand, L. (2014). Influenza virus H1N1 activates platelets through FcγRIIA signaling and thrombin generation. Blood 123: 2854–2863, https://doi.org/10.1182/blood-2013-07-515536.Search in Google Scholar

Cameli, M., Pastore, M.C., Mandoli, G.E., D’Ascenzi, F., Focardi, M., Biagioni, G., Cameli, P., Patti, G., Franchi, F., Mondillo, S., et al.. (2021). COVID-19 and acute coronary syndromes: current data and future implications. Front. Cardiovasc. Med. 7: 369, https://doi.org/10.3389/fcvm.2020.593496.Search in Google Scholar

Campbell, G.M., Nicol, M.Q., Dransfield, I., Shaw, D.J., Nash, A.A., and Dutia, B.M. (2015). Susceptibility of bone marrow-derived macrophages to influenza virus infection is dependent on macrophage phenotype. J. Gen. Virol. 96: 2951–2960, https://doi.org/10.1099/jgv.0.000240.Search in Google Scholar

Centers for Disease Control and Prevention (2021). Selected adverse events reported after COVID-19 vaccination. Available at: https://www.cdc.gov/coronavirus/2019-ncov/vaccines/safety/adverse-events.html.Search in Google Scholar

Chen, J., Zhang, H., Chen, P., Lin, Q., Zhu, X., Zhang, L., and Xue, X. (2015). Correlation between systemic lupus erythematosus and cytomegalovirus infection detected by different methods. Clin Rheumatol. 34: 691–698, doi:https://doi.org/10.1007/s10067-015-2868-3.Search in Google Scholar

Cheruiyot, I., Kipkorir, V., Ngure, B., Misiani, M., Munguti, J., and Ogeng’o, J. (2021). Arterial thrombosis in coronavirus disease 2019 patients: a rapid systematic review. Ann. Vasc. Surg. 70: 273–281, https://doi.org/10.1016/j.avsg.2020.08.087.Search in Google Scholar

Cornillet, M., Verrouil, E., Cantagrel, A., Serre, G., and Nogueira, L. (2015). In ACPA-positive RA patients, antibodies to EBNA35-58Cit, a citrullinated peptide from the Epstein-Barr nuclear antigen-1, strongly cross-react with the peptide β60-74Cit which bears the immunodominant epitope of citrullinated fibrin. Immunol Res. 61: 117–125, doi:https://doi.org/10.1007/s12026-014-8584-2.Search in Google Scholar

Cummings, M.J., Baldwin, M.R., Abrams, D., Jacobson, S.D., Meyer, B.J., Balough, E.M., Aaron, J.G., Claassen, J., Rabbani, L.E., Hastie, J., et al.. (2020). Epidemiology, clinical course, and outcomes of critically ill adults with COVID-19 in New York City: a prospective cohort study. Lancet 395: 1763–1770, https://doi.org/10.1016/s0140-6736(20)31189-2.Search in Google Scholar

Dawood, F.S., Iuliano, A.D., Reed, C., Meltzer, M.I., Shay, D.K., Cheng, P.Y., Bandaranayake, D., Breiman, R.F., Brooks, W.A., Buchy, P., et al.. (2012). Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect. Dis. 12: 687–695, https://doi.org/10.1016/s1473-3099(12)70121-4.Search in Google Scholar

de Boer, O.J., Teeling, P., Idu, M.M., Becker, A.E., and van der Wal, A.C. (2006). Epstein Barr virus specific T-cells generated from unstable human atherosclerotic lesions: implications for plaque inflammation. Atherosclerosis 184: 322–329, https://doi.org/10.1016/j.atherosclerosis.2005.05.001.Search in Google Scholar

Dong, E., Du, H., and Gardner, L. (2020). An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect. Dis. 20: 533–534, https://doi.org/10.1016/s1473-3099(20)30120-1.Search in Google Scholar

Essers, M.A.G., Offner, S., Blanco-Bose, W.E., Waibler, Z., Kalinke, U., Duchosal, M.A., and Trumpp, A. (2009). IFNα activates dormant haematopoietic stem cells in vivo. Nature 458: 904–908, https://doi.org/10.1038/nature07815.Search in Google Scholar PubMed

Fara, M.G., Stein, L.K., Skliut, M., Morgello, S., Fifi, J.T., and Dhamoon, M.S. (2020). Macrothrombosis and stroke in patients with mild Covid-19 infection. J. Thromb. Haemostasis 18: 2031–2033, https://doi.org/10.1111/jth.14938.Search in Google Scholar PubMed PubMed Central

Guilmot, A., Maldonado Slootjes, S., Sellimi, A., Bronchain, M., Hanseeuw, B., Belkhir, L., Yombi, J.C., De Greef, J., Pothen, L., Yildiz, H., et al.. (2021). Immune-mediated neurological syndromes in SARS-CoV-2-infected patients. J. Neurol. 268: 751–757, https://doi.org/10.1007/s00415-020-10108-x.Search in Google Scholar PubMed PubMed Central

Gürtler, L., Seitz, R., and Schramm, W. (2021). Cerebral venous thrombosis after COVID-19 vaccination: is the risk of thrombosis increased by intravascular application of the vaccine? Infection 49: 1071–1074.10.1007/s15010-021-01658-xSearch in Google Scholar PubMed PubMed Central

Janegova, A., Janega, P., Rychly, B., Kuracinova, K., and Babal, P. (2015). The role of Epstein-Barr virus infection in the development of autoimmune thyroid diseases. Endokrynol Pol. 66: 132–136, doi:https://doi.org/10.5603/EP.2015.0020.Search in Google Scholar PubMed

Keller, T.T., van der Meer, J.J., Teeling, P., van der Sluijs, K., Idu, M.M., Rimmelzwaan, G.F., Levi, M., van der Wal, A.C., and de Boer, O.J. (2008). Selective expansion of influenza A virus–specific T cells in symptomatic human carotid artery atherosclerotic plaques. Stroke 39: 174–179, https://doi.org/10.1161/strokeaha.107.491282.Search in Google Scholar PubMed

Kim, J., Chang, D.-Y., Lee, H.-W., Lee, H., Kim, J.-H., Sung, P.S., Kim, K.H., Hong, S.-H., Kang, W., Lee, J., et al.. (2018). Innate-like cytotoxic function of Bystander-Activated CD8+ T Cells is associated with liver injury in Acute Hepatitis A. Immunity 48: 161–173.e5, doi:https://doi.org/10.1016/j.immuni.2017.11.025.Search in Google Scholar PubMed

Kimura, T., Kobiyama, K., Winkels, H., Tse, K., Miller, J., Vassallo, M., Wolf, D., Ryden, C., Orecchioni, M., Dileepan, T., et al.. (2018). Regulatory CD4+ T cells recognize major histocompatibility complex class II molecule–restricted peptide epitopes of apolipoprotein B. Circulation 138: 1130–1143, https://doi.org/10.1161/circulationaha.117.031420.Search in Google Scholar

Kirsebom, Freja C.M., Kausar, F., Nuriev, R., Makris, S., and Johansson, C. (2019). Neutrophil recruitment and activation are differentially dependent on MyD88/TRIF and MAVS signaling during RSV infection. Mucosal Immunol 12: 1244–1255, doi:https://doi.org/10.1038/s41385-019-0190-0.Search in Google Scholar PubMed PubMed Central

Kohlmeier, J.E., Cookenham, T., Roberts, A.D., Miller, S.C., and Woodland, D.L. (2010). Type I interferons regulate cytolytic activity of memory CD8+ T cells in the lung airways during respiratory virus challenge. Immunity 33: 96–105, https://doi.org/10.1016/j.immuni.2010.06.016.Search in Google Scholar PubMed PubMed Central

Koupenova, M., Corkrey, H.A., Vitseva, O., Manni, G., Pang, C.J., Clancy, L., Yao, C., Rade, J., Levy, D., Wang, J.P., et al.. (2019). The role of platelets in mediating a response to human influenza infection. Nat. Commun. 10: 1780, doi:https://doi.org/10.1038/s41467-019-09607-x.Search in Google Scholar PubMed PubMed Central

Krammer, F. (2019). The human antibody response to influenza A virus infection and vaccination. Nat. Rev. Immunol. 19: 383–397, https://doi.org/10.1038/s41577-019-0143-6.Search in Google Scholar PubMed

Kwong, J.C., Schwartz, K.L., Campitelli, M.A., Chung, H., Crowcroft, N.S., Karnauchow, T., Katz, K., Ko, D.T., McGeer, A.J., McNally, D., et al.. (2018). Acute myocardial infarction after laboratory-confirmed influenza infection. N. Engl. J. Med. 378: 345–353, https://doi.org/10.1056/nejmoa1702090.Search in Google Scholar PubMed

Lecendreux, M., Libri, V., Jaussent, I., Mottez, E., Lopez, R., Lavault, S., Regnault, A., Arnulf, I., and Dauvilliers, Y. (2015). Impact of cytokine in type 1 narcolepsy: role of pandemic H1N1 vaccination? J. Autoimmun. 60: 20–31, https://doi.org/10.1016/j.jaut.2015.03.003.Search in Google Scholar PubMed

Liu, J., Yang, D., Wang, X., Zhu, Z., Wang, T., Ma, A., and Liu, P. (2019). Neutrophil extracellular traps and dsDNA predict outcomes among patients with ST-elevation myocardial infarction. Sci. Rep. 9: 11599, https://doi.org/10.1038/s41598-019-47853-7.Search in Google Scholar PubMed PubMed Central

Luo, G., Ambati, A., Lin, L., Bonvalet, M., Partinen, M., Ji, X., Maecker, H.T., and Mignot, E.J.-M. (2018). Autoimmunity to hypocretin and molecular mimicry to flu in type 1 narcolepsy. Proc. Natl. Acad. Sci. U.S.A. 115: E12323–E12332, https://doi.org/10.1073/pnas.1818150116.Search in Google Scholar PubMed PubMed Central

Madjid, M., Miller, C.C., Zarubaev, V.V., Marinich, I.G., Kiselev, O.I., Lobzin, Y.V., Filippov, A.E., and Casscells, S.W.III (2007). Influenza epidemics and acute respiratory disease activity are associated with a surge in autopsy-confirmed coronary heart disease death: results from 8 years of autopsies in 34 892 subjects. Eur. Heart J. 28: 1205–1210, https://doi.org/10.1093/eurheartj/ehm035.Search in Google Scholar PubMed PubMed Central

Malas, M.B., Naazie, I.N., Elsayed, N., Mathlouthi, A., Marmor, R., and Clary, B. (2020). Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: a systematic review and meta-analysis. EClin. Med. 29: 100639, https://doi.org/10.1016/j.eclinm.2020.100639.Search in Google Scholar PubMed PubMed Central

Mazaleuskaya, L., Veltrop, R., Ikpeze, N., Martin-Garcia, J., and Navas-Martin, S. (2012). Protective role of Toll-like receptor 3-induced type I interferon in murine coronavirus infection of macrophages. Viruses 4: 901–923, https://doi.org/10.3390/v4050901.Search in Google Scholar PubMed PubMed Central

McAlpine, C.S., Kiss, M.G., Rattik, S., He, S., Vassalli, A., Valet, C., Anzai, A., Chan, C.T., Mindur, J.E., Kahles, F., et al.. (2019). Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 566: 383–387, https://doi.org/10.1038/s41586-019-0948-2.Search in Google Scholar PubMed PubMed Central

Merkler, A.E., Parikh, N.S., Mir, S., Gupta, A., Kamel, H., Lin, E., Lantos, J., Schenck, E.J., Goyal, P., Bruce, S.S., et al.. (2020). Risk of ischemic stroke in patients with coronavirus disease 2019 (COVID-19) vs patients with influenza. JAMA Neurol. 77: 1366–1372, https://doi.org/10.1001/jamaneurol.2020.2730.Search in Google Scholar PubMed PubMed Central

Muhammad, S., Haasbach, E., Kotchourko, M., Strigli, A., Krenz, A., Ridder, D.A., Vogel, A.B., Marti, H.H., Al-Abed, Y., Planz, O., et al.. (2011). Influenza virus infection aggravates stroke outcome. Stroke 42: 783–791, https://doi.org/10.1161/strokeaha.110.596783.Search in Google Scholar PubMed

Muscente, F. and De Caterina, R. (2020). Causal relationship between influenza infection and risk of acute myocardial infarction: pathophysiological hypothesis and clinical implications. Eur. Heart J. 22: E68–E72, https://doi.org/10.1093/eurheartj/suaa064.Search in Google Scholar PubMed PubMed Central

Muthukumar, A., Narasimhan, M., Li, Q.-Z., Mahimainathan, L., Hitto, I., Fuda, F., Batra, K., Jiang, X., Zhu, C., Schoggins, J., et al.. In depth evaluation of a case of presumed myocarditis following the second dose of COVID-19 mRNA vaccine. Circulation 144: 487–498, https://doi.org/10.1161/CIRCULATIONAHA.121.056038.Search in Google Scholar PubMed PubMed Central

Nagata, K., Kumata, K., Nakayama, Y., Satoh, Y., Sugihara, H., Hara, S., Matsushita, M., Kuwamoto, S., Kato, M., Murakami, I., et al.. (2017). Epstein-Barr virus lytic reactivation activates B cells polyclonally and induces activation-induced cytidine deaminase expression: a mechanism underlying autoimmunity and its contribution to Graves’ disease. Viral Immunol. 30: 240–249, doi:https://doi.org/10.1089/vim.2016.0179.Search in Google Scholar PubMed PubMed Central

Naghavi, M., Wyde, P., Litovsky, S., Madjid, M., Akhtar, A., Naguib, S., Siadaty, M.S., Sanati, S., and Casscells, W. (2003). Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E-deficient mice. Circulation 107: 762–768, https://doi.org/10.1161/01.cir.0000048190.68071.2b.Search in Google Scholar PubMed

Pacheco, Y., Acosta-Ampudia, Y., Monsalve, D.M., Chang, C., Gershwin, M.E., and Anaya, J.M. (2019). Bystander activation and autoimmunity. J. Autoimmun. 103: 102301, https://doi.org/10.1016/j.jaut.2019.06.012.Search in Google Scholar PubMed

Partinen, M., Saarenpää-Heikkilä, O., Ilveskoski, I., Hublin, C., Linna, M., Olsén, P., Nokelainen, P., Alén, R., Wallden, T., Espo, M., et al.. (2012). Increased incidence and clinical picture of childhood narcolepsy following the 2009 H1N1 pandemic vaccination campaign in Finland. PLoS One 7: e33723, https://doi.org/10.1371/journal.pone.0033723.Search in Google Scholar PubMed PubMed Central

Pascutti, M.F., Erkelens, M.N., and Nolte, M.A. (2016). Impact of viral infections on hematopoiesis: from beneficial to detrimental effects on bone marrow output. Front. Immunol. 7: 364, https://doi.org/10.3389/fimmu.2016.00364.Search in Google Scholar PubMed PubMed Central

Petrilli, C.M., Jones, S.A., Yang, J., Rajagopalan, H., O’Donnell, L., Chernyak, Y., Tobin, K.A., Cerfolio, R.J., Francois, F., and Horwitz, L.I. (2020). Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. Br. Med. J. 369: m1966, https://doi.org/10.1136/bmj.m1966.Search in Google Scholar PubMed PubMed Central

Prieto-Pérez, L., Fortes, J., Soto, C., Vidal-González, Á., Alonso-Riaño, M., Lafarga, M., Cortti, M.J., Lazaro-Garcia, A., Pérez-Tanoira, R., Trascasa, Á., et al.. (2020). Histiocytic hyperplasia with hemophagocytosis and acute alveolar damage in COVID-19 infection. Mod. Pathol. 33: 2139–2146.10.1038/s41379-020-0613-1Search in Google Scholar PubMed PubMed Central

Putot, A., Chague, F., Manckoundia, P., Cottin, Y., and Zeller, M. (2019). Post-infectious myocardial infarction: new insights for improved screening. J. Clin. Med. 8: 827, https://doi.org/10.3390/jcm8060827.Search in Google Scholar PubMed PubMed Central

Rommel, M.E.G., Walz, L., Kohlscheen, S., Schenk, F., Krebs, Y., Wittwer, K., von Messling, V., and Modlich, U. (2019). Acute influenza A virus infection affects cell cycle and lineage output of hematopoietic stem cells. Blood 134: 2467, https://doi.org/10.1182/blood-2019-126482.Search in Google Scholar

Sa Ribero, M., Jouvenet, N., Dreux, M., and Nisole, S. (2020). Interplay between SARS-CoV-2 and the type I interferon response. PLoS Pathog. 16: e1008737, https://doi.org/10.1371/journal.ppat.1008737.Search in Google Scholar PubMed PubMed Central

Saigusa, R., Winkels, H., and Ley, K. (2020). T cell subsets and functions in atherosclerosis. Nat. Rev. Cardiol. 17: 387–401, https://doi.org/10.1038/s41569-020-0352-5.Search in Google Scholar PubMed PubMed Central

Sandalova, E., Laccabue, D., Boni, C., Tan, A.T., Fink, K., Ooi, E.E., Chua, R., Shafaeddin Schreve, B., Ferrari, C., and Bertoletti, A. (2010). Contribution of herpesvirus specific CD8 T cells to anti-viral T cell response in humans. PLoS Pathog. 6: e1001051, https://doi.org/10.1371/journal.ppat.1001051.Search in Google Scholar PubMed PubMed Central

Sanderson, Nicholas S.R., Zimmermann, M., Eilinger, L., Gubser, C., Schaeren-Wiemers, N., Lindberg, Raija L.P., Dougan, S.K., Ploegh, H.L., Kappos, L., and Derfuss, T. (2017). Cocapture of cognate and bystander antigens can activate autoreactive B cells. Proc. Natl. Acad. Sci. U.S.A 114: 734–739, doi:https://doi.org/10.1073/pnas.1614472114.Search in Google Scholar PubMed PubMed Central

Sarkanen, T.O., Alakuijala, A.P.E., Dauvilliers, Y.A., and Partinen, M.M. (2018). Incidence of narcolepsy after H1N1 influenza and vaccinations: systematic review and meta-analysis. Sleep Med. Rev. 38: 177–186, https://doi.org/10.1016/j.smrv.2017.06.006.Search in Google Scholar PubMed

Sato, T., Onai, N., Yoshihara, H., Arai, F., Suda, T., and Ohteki, T. (2009). Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 15: 696–700, https://doi.org/10.1038/nm.1973.Search in Google Scholar PubMed

Schultze, J.L. and Aschenbrenner, A.C. (2021). COVID-19 and the human innate immune system. Cell 184: 1671–1692, https://doi.org/10.1016/j.cell.2021.02.029.Search in Google Scholar PubMed PubMed Central

Scully, M., Singh, D., Lown, R., Poles, A., Solomon, T., Levi, M., Goldblatt, D., Kotoucek, P., Thomas, W., and Lester, W. (2021). Pathologic antibodies to platelet factor 4 after ChAdOx1 nCoV-19 vaccination. N. Engl. J. Med. 384: 2202–2211, https://doi.org/10.1056/nejmoa2105385.Search in Google Scholar

Shrock, E., Fujimura, E., Kula, T., Timms, R.T., Lee, I.H., Leng, Y., Robinson, M.L., Sie, B.M., Li, M.Z., Chen, Y., et al.. (2020). Viral epitope profiling of COVID-19 patients reveals cross-reactivity and correlates of severity. Science 370: eabd4250, https://doi.org/10.1126/science.abd4250.Search in Google Scholar PubMed PubMed Central

Smatti, M.K., Cyprian, F.S., Nasrallah, G.K., Al Thani, A.A., Almishal, R.O., and Yassine, H.M. (2019). Viruses and autoimmunity: a review on the potential interaction and molecular mechanisms. Viruses 11: 762, https://doi.org/10.3390/v11080762.Search in Google Scholar PubMed PubMed Central

Smeeth, L., Thomas, S.L., Hall, A.J., Hubbard, R., Farrington, P., and Vallance, P. (2004). Risk of myocardial infarction and stroke after acute infection or vaccination. N. Engl. J. Med. 351: 2611–2618, https://doi.org/10.1056/nejmoa041747.Search in Google Scholar PubMed

Stern, M.P. and Gaskill, S.P. (1978). Secular trends in ischemic heart disease and stroke mortality from 1970 to 1976 in Spanish-surnamed and other white individuals in Bexar County, Texas. Circulation 58: 537–543, https://doi.org/10.1161/01.cir.58.3.537.Search in Google Scholar PubMed

Sung, J.G., Sobieszczyk, P.S., and Bhatt, D.L. (2021). Acute myocardial infarction within 24 hours after COVID-19 vaccination. Am. J. Cardiol. 156: 129–131, https://doi.org/10.1016/j.amjcard.2021.06.047.Search in Google Scholar PubMed PubMed Central

Tajstra, M., Jaroszewicz, J., and Gąsior, M. (2021). Acute coronary tree thrombosis after vaccination for COVID-19. Cardiovasc. Intervent. 14: e103–e104, https://doi.org/10.1016/j.jcin.2021.03.003.Search in Google Scholar PubMed PubMed Central

Talanas, G., Dossi, F., and Parodi, G. (2021). Type 2 myocardial infarction in patients with coronavirus disease 2019. J. Cardiovasc. Med. 22: 603–605.10.2459/JCM.0000000000001136Search in Google Scholar PubMed

Tan, B.K., Mainbourg, S., Friggeri, A., Bertoletti, L., Douplat, M., Dargaud, Y., Grange, C., Lobbes, H., Provencher, S., and Lega, J.-C. (2021). Arterial and venous thromboembolism in COVID-19: a study-level meta-analysis. Thorax 76: 970, https://doi.org/10.1136/thoraxjnl-2020-215383.Search in Google Scholar PubMed PubMed Central

Tengvall, K., Huang, J., Hellström, C., Kammer, P., Biström, M., Ayoglu, B., Lima Bomfim, I., Stridh, P., Butt, J., Brenner, N., et al.. (2019). Molecular mimicry between Anoctamin 2 and Epstein-Barr virus nuclear antigen 1 associates with multiple sclerosis risk. Proc. Natl. Acad. Sci. U.S.A 116: 16955–16960, doi:https://doi.org/10.1073/pnas.1902623116.Search in Google Scholar PubMed PubMed Central

Tokars, J.I., Olsen, S.J., and Reed, C. (2017). Seasonal incidence of symptomatic influenza in the United States. Clin. Infect. Dis. 66: 1511–1518, https://doi.org/10.1093/cid/cix1060.Search in Google Scholar PubMed PubMed Central

Vanderlugt, C.L. and Miller, S.D. (2002). Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat. Rev. Immunol. 2: 85–95, https://doi.org/10.1038/nri724.Search in Google Scholar PubMed

Vanheusden, M., Stinissen, P., ‘t Hart, B.A., and Hellings, N. (2015). Cytomegalovirus: a culprit or protector in multiple sclerosis? Trends Mol. Med. 21: 16–23, https://doi.org/10.1016/j.molmed.2014.11.002.Search in Google Scholar PubMed

Venkatakrishnan, A.J., Kayal, N., Anand, P., Badley, A.D., Church, G.M., and Soundararajan, V. (2020). Benchmarking evolutionary tinkering underlying human–viral molecular mimicry shows multiple host pulmonary–arterial peptides mimicked by SARS-CoV-2. Cell Death Dis. 6: 96, https://doi.org/10.1038/s41420-020-00321-y.Search in Google Scholar PubMed PubMed Central

Vuorela, A., Freitag, T.L., Leskinen, K., Pessa, H., Härkönen, T., Stracenski, I., Kirjavainen, T., Olsen, P., Saarenpää-Heikkilä, O., Ilonen, J., et al.. (2021). Enhanced influenza A H1N1 T cell epitope recognition and cross-reactivity to protein-O-mannosyltransferase 1 in Pandemrix-associated narcolepsy type 1. Nat. Commun. 12: 2283, https://doi.org/10.1038/s41467-021-22637-8.Search in Google Scholar PubMed PubMed Central

World Health Organization (2021). Guidance for clinical case management of thrombosis with thrombocytopenia syndrome (TTS) following vaccination to prevent coronavirus disease (COVID-19): interim guidance, Available at: <https://www.who.int/publications/i/item/WHO-2019-nCoV-TTS-2021.1>.Search in Google Scholar

World Health Organization (2021). Global influenza surveillance and response team, Available at: <https://www.who.int/initiatives/global-influenza-surveillance-and-response-system>.Search in Google Scholar

Wolf, D., Gerhardt, T., Winkels, H., Michel, N.A., Pramod, A.B., Ghosheh, Y., Brunel, S., Buscher, K., Miller, J., McArdle, S., et al.. (2020). Pathogenic autoimmunity in atherosclerosis evolves from initially protective apolipoprotein B Reactive CD4 T-Regulatory Cells. Circulation 142: 1279–1293, https://doi.org/10.1161/circulationaha.119.042863.Search in Google Scholar PubMed PubMed Central

Young, H.A., Klinman, D.M., Reynolds, D.A., Grzegorzewski, K.J., Nii, A., Ward, J.M., Winkler-Pickett, R.T., Ortaldo, J.R., Kenny, J.J., and Komschlies, K.L. (1997). Bone marrow and thymus expression of interferon-gamma results in severe B-cell lineage reduction, T-cell lineage alterations, and hematopoietic progenitor deficiencies. Blood 89: 583–595, https://doi.org/10.1182/blood.v89.2.583.Search in Google Scholar

Zdrenghea, M.T., Telcian, A.G., Laza-Stanca, V., Bellettato, C.M., Edwards, M.R., Nikonova, A., Khaitov, M.R., Azimi, N., Groh, V., Mallia, P., et al.. (2012). RSV infection modulates IL-15 production and MICA levels in respiratory epithelial cells. Eur Respir J. 39: 712–20, doi:https://doi.org/10.1183/09031936.00099811.Search in Google Scholar PubMed

Zhang, S., Liu, Y., Wang, X., Yang, L., Li, H., Wang, Y., Liu, M., Zhao, X., Xie, Y., Yang, Y., et al.. (2020). SARS-CoV-2 binds platelet ACE2 to enhance thrombosis in COVID-19. J. Hematol. Oncol. 13: 120, https://doi.org/10.1186/s13045-020-00954-7.Search in Google Scholar PubMed PubMed Central

Zhou, J., Ghoroghi, S., Benito-Martin, A., Wu, H., Unachukwu, U.J., Einbond, L.S., Guariglia, S., Peinado, H., and Redenti, S. (2016). Characterization of induced pluripotent stem cell microvesicle genesis, morphology and pluripotent content. Sci. Rep. 6: 19743, https://doi.org/10.1038/srep19743.Search in Google Scholar PubMed PubMed Central

Received: 2021-08-19
Accepted: 2021-12-07
Published Online: 2021-12-22
Published in Print: 2022-01-27

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 1.12.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2021-0348/html
Scroll to top button