Pathogenetic and clinical aspects of the development of acute coronary syndrome in influenza and COVID-19: vaccination issues

Highlights. The new coronavirus infection necessitates mandatory vaccination of patients at high cardiovascular risk (in particular after myocardial infarction), including both COVID-19 vaccine and influenza vaccine, which represent an important condition for reducing mortality. At the same time, vaccination coverage among the population is still low, thus requiring a detailed analysis of clinical and pathogenetic components of this problem. The doctor's understanding of the most complex aspects of the problem will help achieve positive outcome in the treatment of patients who suffered from myocardial infarction, even before acquiring the data of specially planned studies.

Abstract. This review contains current data on the relationship of viral infections with an increase in the incidence of cardiovascular diseases, as well as on the role of vaccination in improving the prognosis after myocardial infarction. The literature search was carried out by using the websites of cardiological societies, as well as the PubMed, EMBASE, eLibrary databases using the following keywords: flu, influenza, new coronavirus infection, SARS-CoV2, COVID-19, vaccination, acute coronary syndrome. The pandemic of COVID-19 (COronaVIrus Disease 2019) dictates the need for urgent vaccination against COVID-19 and influenza in patients with cardiovascular diseases. The importance of this measure, as a clear condition in preventing further increase in mortality from cardiovascular diseases, should not be doubted. At the same time, the still remaining low percentage of vaccinations is one of the causal factors of high rates of morbidity and mortality from cardiovascular pathology.

1. Tsang F.H., Chan W.C.C., Cho W.C.S., Yu A.C.S., Yim A.K.Y., Chan A.K.C., Ng L.P.W., Wong Y.K.E., Pei X.M., Li M.J.W., Wong S.C. An update on COVID-19 pandemic: the epidemiology, pathogenesis, prevention and treatment strategies. Expert Rev Anti Infect Ther. 2021;19(7):877-88. doi:10.1080/14787210.2021.1863146.

2. Russian Statistical Yearbook 2021. Мoscow; 2021. 692 p. (In Russian)

3. Boytsov S. COVID-19 is a serious risk factor for the heart. [Available at: https://cardioweb.ru/news/item/3201-akademik-ran-sergej-bojtsov-covid-19-sereznyj-faktor-riska-dlya-serdtsa (accessed 12.05.2022) (In Russian)

4. Disease Burden of Flu. Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases (NCIRD). Available at: https://www.cdc.gov/flu/about/burden/index.html (accessed 14.12.2021).

5. Nguyen J.L., Yang W., Ito K., Matte T.D., Shaman J., Kinney P.L. Seasonal influenza infections and cardiovascular disease mortality. JAMA Cardiol. 2016;1:274-81. doi:10.1001/jamacardio.2016.0433

6. Arora A., Rout A., Satya K. Cardiovascular disease burden of influenza syndrome: national trends and outcomes from a United States population study from 2011 to 2014. J Am Coll Cardiol. 2019;73:1794. doi:10.1016/S0735-1097(19)32400-3.

7. Caldeira D., Rodrigues B., David C., Costa J., Pinto F.J., Ferreira J.J. The association of influenza infection and vaccine with myocardial infarction: systematic review and meta-analysis of self-controlled case series. Expert Rev Vaccines. 2019;18(11):1211-17. doi:10.1080/14760584.2019.1690459.

8. Chow E.J., Rolfes M.A., O’Halloran A., Anderson E.J., Bennett N.M., Billing L., Chai S., Dufort E., Herlihy R., Kim S., Lynfield R., McMullen C., Monroe M.L., Schaffner W., Spencer M., Talbot H.K., Thomas A., Yousey-Hindes K., Reed C., Garg S. Acute cardiovascular events associated with influenza in hospitalized adults. Ann Intern Med. 2020;173:605–613. doi: 10.7326/M20-1509.

9. Iuliano A.D., Roguski K.M., Chang H.H., Muscatello D.J., Palekar R., Tempia S., Cohen C., Gran J.M., Schanzer D., Cowling B.J., Wu P., Kyncl J., Ang L.W., Park M., Redlberger-Fritz M., Yu H., Espenhain L., Krishnan A., Emukule G., van Asten L., Pereira da Silva S., Aungkulanon S., Buchholz U., Widdowson M.A., Bresee J.S.; Global Seasonal Influenza-associated Mortality Collaborator Network. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2018;391:1285– 1300. doi: 10.1016/S0140-6736(17)33293-2.

10. Udell J.A., Zawi R., Bhatt D.L., Keshtkar-Jahromi M., Gaughran F., Phrommintikul A., Ciszewski A., Vakili H., Hoffman E.B., Farkouh M.E., Cannon C.P. Association between influenza vaccination and cardiovascular outcomes in high-risk patients: a meta-analysis. JAMA. 2013;310:1711-20. doi:10.1001/jama.2013.279206.

11. Phrommintikul A., Kuanprasert S., Wongcharoen W., Kanjanavanit R., Chaiwarith R., Sukonthasarn A. I Influenza vaccination reduces cardiovascular events in patients with acute coronary syndrome. Eur Heart J. 2011;32:1730-1735. doi:10.1093/eurheartj/ehr004.

12. Wu H.H., Chang Y.Y., Kuo S.C., Chen Y.T. Influenza vaccination and secondary prevention of cardiovascular disease among Taiwanese elders—A propensity score-matched follow-up study. PLoS ONE. 2019;14(7): e0219172. doi: 10.1371/journal.pone.0219172.

13. Barnes M., Heywood A.E., Mahimbo A., Rahman B., Newall A.T., Macintyre C.R. Acute myocardial infarction and influenza: a meta-analysis of case–control studies. Heart. 2015;101:1738–47. doi: 10.1136/heartjnl-2015-307691.

14. Fihn S.D., Gardin J.M., Abrams J., Berra K., Blankenship J.C., Dallas A.P., Douglas P.S., Foody J.M., Gerber T.C., Hinderliter A.L., King S.B. 3rd, Kligfield P.D., Krumholz H.M., Kwong R.Y., Lim M.J., Linderbaum J.A., Mack M.J., Munger M.A., Prager R.L., Sabik J.F., Shaw L.J., Sikkema J.D., Smith C.R. Jr., Smith S.C. Jr., Spertus J.A., Williams S.V.; American College of Cardiology Foundation; American Heart Association Task Force on Practice Guidelines; American College of Physicians; American Association for Thoracic Surgery; Preventive Cardiovascular Nurses Association; Society for Cardiovascular Angiography and Interventions; Society of Thoracic Surgeons.2012 ACCF/AHA/ ACP/AATS/PCNA/SCAI/STS Guideline for the Diagnosis and Management of Patients With Stable Ischemic Heart Disease. JACC. 2012;60(24):e44–e164. doi:10.1016/j.jacc.2012.07.013.

15. Knuuti J., Wijns W., Saraste A., Capodanno D., Barbato E., Funck-Brentano C., Prescott E., Storey R.F., Deaton C., Cuisset T., Agewall S., Dickstein K., Edvardsen T., Escaned J., Gersh B.J., Svitil P., Gilard M., Hasdai D., Hatala R., Mahfoud F., Masip J., Muneretto C., Valgimigli M., Achenbach S., Bax J.J.; ESC Scientific Document Group. . 2019 ESC Guidelines for the diagnosis and management of chronic coronary syndromes The Task Force for the diagnosis and management of chronic coronary syndromes of the European Society of Cardiology (ESC). European Heart Journal. 2020;41:407-77. doi:10.1093/eurheartj/ehz425.

16. 2020 Clinical practice guidelines for Stable coronary artery disease. Russian Journal of Cardiology. 2020;25(11):4076. (In Russian) doi:10.15829/29/1560-4071-2020-4076

17. 2020 Clinical practice guidelines for Acute ST-segment elevation myocardial infarction. Russian Journal of Cardiology. 2020;25(11):4103. (In Russian) doi:10.15829/29/1560-4071-2020-4103

18. 2021 ESC Guidelines on cardiovascular disease prevention in clinical practice. European Heart Journal. 2021; 42: 32273337. doi:10.1093/eurheartj/ehab484

19. Cardiovascular prevention 2017. National guidelines. Russian Journal of Cardiology. 2018;(6):7-122. (In Russian) doi:10.15829/1560-4071-2018-6-7-122.

20. Fröbert О., Götberg M., Erlinge D., Akhtar Z., Christiansen E.H., MacIntyre C.R., Oldroyd K.G., Motovska Z., Erglis A., Moer R., Hlinomaz O., Jakobsen L., Engstrøm T., Jensen L.O., Fallesen C.O., Jensen S.E., Angerås O., Calais F., Kåregren A., Lauermann J., Mokhtari A., Nilsson J., Persson J., Stalby P., Islam A.K.M.M., Rahman A., Malik F., Choudhury S., Collier T., Pocock S.J., Pernow J. Influenza Vaccination After Myocardial Infarction: A Randomized, Double-Blind, Placebo-Controlled, Multicenter Trial. Circulation. 2021;144(18): 1476-84. doi:10.1161/CIRCULATIONAHA.121.057042.

21. Grandhi G.R., Mszar R., Vahidy F., Valero-Elizondo J., Blankstein R., Blaha M.J., Virani S.S., Andrieni J.D., Omer S.B., Nasir K. Sociodemographic disparities in influenza vaccination among adults with atherosclerotic cardiovascular disease in the United States. JAMA Cardiol. 2021;6:87–89. doi:10.1001/jamacardio.2020.3978.

22. Bhugra P., Grandhi G.R., Mszar R., Satish P., Singh R., Blaha M., Blankstein R., Virani S.S., Cainzos-Achirica M., Nasir K. Determinants of Influenza Vaccine Uptake in Patients With Cardiovascular Disease and Strategies for Improvement. J Am Heart Assoc. 2021;10:e019671. doi:10.1161/JAHA.120.019671.

23. Katsoularis I., Fonseca-Rodríguez O., Farrington P., Lindmark K., Fors Connolly A.M. Risk of acute myocardial infarction and ischaemic stroke following COVID-19 in Sweden: a self-controlled case series and matched cohort study. The Lancet. 2021;398(10300):599-607. doi: 10.1016/S0140-6736(21)00896-5.

24. Modin D., Claggett B., Sindet-Pedersen C., Lassen M.C.H., Skaarup K.G., Jensen J.U.S., Fralick M., Schou M., Lamberts M., Gerds T., Fosbøl E.L., Phelps M., Kragholm K.H., Andersen M.P., Køber L., Torp-Pedersen C., Solomon S.D., Gislason G., Biering-Sørensen T. Acute COVID-19 and the incidence of ischemic stroke and acute myocardial infarction. Circulation. 2020;142(21):2080– 82. doi: 10.1161/CIRCULATIONAHA.120.050809.

25. Bilaloglu S., Aphinyanaphongs Y., Jones S., Iturrate E., Hochman J., Berger J.S. Thrombosis in hospitalized patients with COVID-19 in a New York City health system. JAMA. 2020;324(8):799–801. doi: 10.1001/jama.2020.13372.

26. Lodigiani C., Iapichino G., Carenzo L., Cecconi M., Ferrazzi P., Sebastian T., Kucher N., Studt J.D., Sacco C., Bertuzzi A., Sandri M.T., Barco S.; Humanitas COVID-19 Task Force. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14. doi: 10.1016/j.thromres.2020.04.024.

27. Yau J.W., Teoh H., Verma S. Endothelial cell control of thrombosis. BMC Cardiovasc. Disord. 2015;15:130. doi: 10.1186/s12872-015-0124-z.

28. Ackermann M., Verleden S.E., Kuehnel M., Haverich A., Welte T., Laenger F., Vanstapel A., Werlein C., Stark H., Tzankov A., Li W.W., Li V.W., Mentzer S.J., Jonigk D. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N. Engl. J. Med. 2020;383:120–8. doi: 10.1056/NEJMoa2015432.

29. Wan Y., Shang J., Graham R., Baric R.S., Li F. Receptor recognition by the novel coronavirus from Wuhan: an analysis based on decade-long structural studies of SARS Coronavirus. Journal of virology. 2020;94(7):e00127-20. doi: 10.1128/JVI.00127-20.

30. Santos R.A.S., Sampaio W.O., Alzamora A.C., Motta-Santos D., Alenina N., Bader M., Campagnole-Santos M.J. The ACE2/ angiotensin-(1-7)/MAS Axis of the Renin-Angiotensin System: Focus on Angiotensin-(1-7). Physiol Rev. 2018;98(1):505-53. doi:10.1152/physrev.00023.2016.

31. Shevchenko O.P., Shevchenko А.О. Angiotensin II and myocardial infarction. Rational Pharmacother. Card. 2008;3:105-10. (In Russian)

32. Wang K., Gheblawi M., Oudit G.Y. Angiotensin converting enzyme 2: a double-edged sword. Circulation. 2020;142(5):426-428. doi:10.1161/CIRCULATIONAHA.120.047049.

33. Patel V.B., Zhong J.C., Grant M.B., Oudit G.Y. Role of the ACE2/Angiotensin 1-7 axis of the renin-angiotensin system in heart failure. Circ Res. 2016;118:1313–26. doi:10.1161/CIRCRESAHA.116.307708.

34. Drapkina O.M., Vasilyeva L.E. Debatable points of using angiotensin-converting enzyme inhibitors and angiotensin receptor antagonists in patients with COVID-19. Cardiovascular Therapy and Prevention. 2020;19(3):2580. (In Russian) doi:10.15829/1728-8800-2020-2580

35. Libby P. Targeting Inflammatory Pathways in Cardiovascular Disease: The Inflammasome, Interleukin-1. Interleukin-6 and Beyond. Cells. 2021;10:951. doi:10.3390/cells10040951.

36. Dhama K., Patel S.K., Pathak M., Yatoo M.I., Tiwari R., Malik Y.S., Singh R., Sah R., Rabaan A.A., Bonilla-Aldana D.K., Rodriguez-Morales A.J. An update on SARS-CoV-2/COVID-19 with particular reference to its clinical pathology, pathogenesis, immunopathology and mitigation strategies. Travel Med. Infect. Dis. 2020;37:101-755. doi: 10.1016/j.tmaid.2020.101755

37. Bolevich S.B., Bolevich S.S. Complex mechanism of COVID-19 development. Sechenov medical journal. 2020;11(2): 50-61. (In Russian) doi:10.47093/2218-7332.2020.11.2.50-61

38. Olbei M., Hautefort I., Modos D., Treveil A., Poletti M., Gul L., Shannon-Lowe C.D., Korcsmaros T. SARS-CoV-2 causes a different cytokine response compared to other cytokine storm-causing respiratory viruses in severely ill patients. Front. Immunol. 2021;1;12:629193. doi: 10.3389/fimmu.2021.629193.

39. Dua D., Yadav M., Jetley P., Dua R. Covid-19: Immunological lessons from bats, pangolins and old coronaviruses; and how we can apply them in a timely way for a better outcome. Preprints 2020, 2020040071. doi:10.20944/preprints202004.0071.v1.

40. Golota A.S., Kamilova Т.А., Shneider О.V., Vologzhanin D.A., Sherbak S.G. Pathogenesis of the Initial Stages of Severe COVID-19. Journal of Clinical Practice. 2021;12(2):83-102. (In Russian) doi:10.17816/clinpract71351

41. Zhang S., Liu Y., Wang X., Yang L., Li H., Wang Y., Liu M., Zhao X., Xie Y., Yang Y., Zhang S., Fan Z., Dong J., Yuan Z., Ding Z., Zhang Y., Hu L. SARS-CoV-2 binds platelet ACE2 to enhance thrombosis in COVID-19. J Hematol Oncol. 2020;13(1):120. doi:10.1186/s13045-020-00954-7.

42. Golebiewska E.M., Poole A.W. Platelet secretion: From haemostasis to wound healing and beyond. Blood Rev. 2015;29(3):153-62. doi: 10.1016/j.blre.2014.10.003.

43. Nakamura S., Nakamura I., Ma L., Vaughan D.E., Fogo A.B. Plasminogen activator inhibitor-1 expression is regulated by the angiotensin type 1 receptor in vivo. Kidney Int. 2000;58:251-259. doi: 10.1046/j.1523-1755.2000.00160.x

44. Theofilis P., Sagris M., Oikonomou E., Antonopoulos A.S., Siasos G., Tsioufis C., Tousoulis D. Inflammatory mechanisms contributing to endothelial dysfunction. Biomedicines. 2021;9(7):781. doi:10.3390/biomedicines9070781.

45. McCormack J.J., Silva M.L., Ferraro F., Patella F., Cutler D.F. Weibel-Palade bodies at a glance. J Cell Sci. 2017;130(21):3611-17. doi: 10.1242/jcs.208033.

46. Anastasiou G., Gialeraki A., Merkouri E., Politou M., Travlou A. Thrombomodulin as a regulator of the anticoagulant pathway: Implication in the development of thrombosis. Blood Coagul. Fibrinolysis. 2012;23(1):1-10. doi: 10.1097/MBC.0b013e32834cb271.

47. Sardu C., Gambardella J., Morelli M.B., Wang X., Marfella R., Santulli G. Hypertension, thrombosis, kidney failure, and diabetes: Is COVID-19 an endothelial disease? A comprehensive evaluation of clinical and basic evidence. J Clin Med. 2020;9(5):1417. doi:10.3390/jcm9051417.

48. Shagdarsuren E., Wellner M., Braesen J.H., Park J.K., Fiebeler A., Henke N., Dechend R., Gratze P., Luft F.C., Muller DN. Complement activation in angiotensin II-induced organ damage. Circ Res. 2005;97:716-24. doi: https://doi.org/10.1161/01.RES.0000182677.89816.38

49. Rawish E., Sauter M., Sauter R. Complement, inflammation and thrombosis. J Pharmacol. 2021;178:2892-904. doi: 10.1111/bph.15476.

50. McFadyen J.D., Stevens H., Peter K. The emerging threat of (micro)thrombosis in COVID-19 and its therapeutic implications. Circ. Res. 2020;127(4):571–87. doi: 10.1161/CIRCRESAHA.120.317447.

51. Guagliumi G., Sonzogni A., Pescetelli I., Pellegrini D., Finn A.V. Microthrombi and ST-Segment Elevation Myocardial Infarction in COVID-19. Circulation 2020;142:804–9. doi: 10.1161/CIRCULATIONAHA.120.049294.

52. Cao W., Li T. COVID-19: towards understanding of pathogenesis. Cell Res. 2020;30(5):367–369. doi:10.1038/s41422-020-0327-4.

53. Guzik T., Mohiddin S.A., Dimarco A., Patel V., Savvatis K., Marelli-Berg F.M., Madhur M.S., Tomaszewski M., Maffia P., D'Acquisto F., Nicklin S.A., Marian A.J., Nosalski R., Murray E.C., Guzik B., Berry C., Touyz R.M., Kreutz R., Wang D.W., Bhella D., Sagliocco O., Crea F., Thomson E.C., McInnes I.B. COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc. Res. 2020;116 (10):1666–87. doi:10.1093/cvr/cvaa106.

54. Xiong T.Y., Redwood S., Prendergast B., Chen M. Coronaviruses and the cardiovascular system: acute and long-term implications. Eur. Heart J. 2020;41(19):1798–1800. doi:10.1093/eurheartj/ehaa231.

55. Arutyunov G.P., Tarlovskaya E.I., Arutyunov A.G. on behalf of coauthors. Clinical features of post-COVID-19 period. Results of the international register “Dynamic analysis of comorbidities in SARS-CoV-2 survivors (AKTIV SARS-CoV-2)”. Data from 6-month follow-up. Russian Journal of Cardiology. 2021;26(10):4708. (In Russian) doi:10.15829/1560-4071-2021-4708

56. Interim guidelines for the prevention, diagnosis and treatment of new coronavirus infection (COVID-19). Version 13.1 from 11/17/2021. Available at: https://medvestnik.ru/content/documents/14-ot-27-12-2021.html (accessed 14/07/2021) (In Russian)

57. Clar C., Oseni Z., Flowers N., Keshtkar-Jahromi M., Rees K. Influenza vaccines for preventing cardiovascular disease. Cochrane Database Syst Rev. 2015;5:CD005050. doi:10.1002/14651858.CD005050.pub3.

58. Aye Y.N., Mai A.S., Zhang A., Lim O.Z.H., Lin N., Ng C.H., Chan M.Y., Yip J., Loh P.H., Chew N.W.S. Acute Myocardial Infarction and Myocarditis following COVID-19 Vaccination. QJM. 2021;hcab252. doi: 10.1093/qjmed/hcab252.

59. Almas Т., Rehman S., Mansour E., Khedro T., Alansari A., Malik J., Alshareef N., Nagarajan V.R., Al-Awaid A.H., Alsufyani R., Alsufyani M., Rifai A., Alzahrani A., Nagarajan D.R., Abdullatif T., Gunasaegaram V., Alzadjali E., Subramanian A., Rahman A., Sattar Y., Galo J., Virk H.U.H., Alraies M.C. Epidemiology, clinical ramifications, and cellular pathogenesis of COVID-19 mRNA-vaccination-induced adverse cardiovascular outcomes: A state-of-the-heart review. Biomedicine & Pharmacotherapy. 2022;149:112843. doi: 10.1016/j.biopha.2022.112843