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Vol 30, No 2 (2024)
Review paper
Published online: 2024-08-13

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Influenza and its cardiovascular complications: a comprehensive review

Mohammad Hassan Kalantar Neyestanaki1, Majid Kalantar Neyestanaki2
Acta Angiologica 2024;30(2):69-78.

Abstract

Influenza is a respiratory illness caused by RNA viruses. These viruses can cause mild to severe illness, and can lead to pandemics and epidemics. Influenza spreads through respiratory droplets produced when an infected person coughs, sneezes, talks, or comes into contact with contaminated surfaces. In some cases, influenza can lead to more serious extrapulmonary complications, such as cardiovascular complications. During influenza virus infection, endothelial cells become activated, evidenced by increased levels of von Willebrand factor, enhanced coagulation, and necrosis. Microcirculatory dysfunction has been linked with adverse outcomes, including increased rates of organ failure and mortality. The most important cardiovascular complications can occur directly, causing myocarditis and pericarditis. They can also occur indirectly, exacerbating underlying cardiovascular conditions such as ischemic heart disease and heart failure. Vaccination and antiviral treatment for influenza can be effective in reducing the risk of these cardiovascular complications. As outlined in the preceding discussion on influenza, its identification and complications have presented a significant challenge in the healthcare domain. However, through enhanced understanding and meticulous research on this virus, we can make informed decisions that will optimize treatment strategies. This article delves into the epidemiological factors, risk factors, and clinical manifestations of influenza and association of influenza with cardiovascular manifestations.

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References

  1. Loscalzo J, Fauci AS, Kasper DL, et al. Harrison's principles of internal medicine. (No Title): 2022.
  2. Warren-Gash C, Hayward AC, Hemingway H, et al. Influenza as a trigger for acute myocardial infarction or death from cardiovascular disease: a systematic review. Lancet Infect Dis. 2009; 9(10): 601–610.
  3. Mamas MA, Fraser D, Neyses L. Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol. 2008; 130(3): 304–309.
  4. Jeyanathan T, Overgaard C, McGeer A. Cardiac complications of influenza infection in 3 adults. CMAJ. 2013; 185(7): 581–584.
  5. Berkhoff EGM, de Wit E, Geelhoed-Mieras MM, et al. Fitness costs limit escape from cytotoxic T lymphocytes by influenza A viruses. Vaccine. 2006; 24(44-46): 6594–6596.
  6. Bridges CB, Kuehnert MJ, Hall CB. Transmission of influenza: implications for control in health care settings. Clin Infect Dis. 2003; 37(8): 1094–1101.
  7. Kalil AC, Thomas PG. Influenza virus-related critical illness: pathophysiology and epidemiology. Crit Care. 2019; 23(1): 258.
  8. Warren-Gash C, Hayward AC, Hemingway H, et al. Influenza infection and risk of acute myocardial infarction in England and Wales: a CALIBER self-controlled case series study. J Infect Dis. 2012; 206(11): 1652–1659.
  9. Warren-Gash C, Bhaskaran K, Hayward A, et al. Circulating influenza virus, climatic factors, and acute myocardial infarction: a time series study in England and Wales and Hong Kong. J Infect Dis. 2011; 203(12): 1710–1718.
  10. Bennett JE, Dolin R, Blaser MJ. Mandell, Douglas, and Bennett's principles and practice of infectious diseases: Elsevier Inc. ; 2014.
  11. TREANOR J. Influenza viruses, including avian influenza and swine influenza. Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases. 2010: 2265–2288.
  12. Johanson WG, Pierce AK, Sanford JP. Pulmonary function in uncomplicated influenza. Am Rev Respir Dis. 1969; 100(2): 141–146.
  13. Kondo S, Abe K. The effects of influenza virus infection on FEV1 in asthmatic children. The time-course study. Chest. 1991; 100(5): 1235–1238.
  14. Qian M-M, Wu W. Dong K-X. Clinical features and TCM syndromes of infectious AECOPD caused by influenza virus. Journal of Hainan Medical College. 2021; 27(24).
  15. Levandowski RA, Gerrity TR, Garrard CS. Modifications of lung clearance mechanisms by acute influenza A infection. J Lab Clin Med. 1985; 106(4): 428–432.
  16. Pittet LA, Hall-Stoodley L, Rutkowski MR, et al. Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Respir Cell Mol Biol. 2010; 42(4): 450–460.
  17. van der Sluijs KF, van Elden LJR, Nijhuis M, et al. IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J Immunol. 2004; 172(12): 7603–7609.
  18. Sun K, Metzger DW. Influenza infection suppresses NADPH oxidase-dependent phagocytic bacterial clearance and enhances susceptibility to secondary methicillin-resistant Staphylococcus aureus infection. J Immunol. 2014; 192(7): 3301–3307.
  19. Small CL, Shaler CR, McCormick S, et al. Influenza infection leads to increased susceptibility to subsequent bacterial superinfection by impairing NK cell responses in the lung. J Immunol. 2010; 184(4): 2048–2056.
  20. Hayden FG, Fritz R, Lobo MC, et al. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Invest. 1998; 101(3): 643–649.
  21. Marsden PA. Inflammation and coagulation in the cardiovascular system: the contribution of influenza. Circ Res. 2006; 99(11): 1152–1153.
  22. Smeeth L, Cook C, Thomas S, et al. Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting. Lancet. 2006; 367(9516): 1075–1079.
  23. Keller TT, van der Sluijs KF, de Kruif MD, et al. Effects on coagulation and fibrinolysis induced by influenza in mice with a reduced capacity to generate activated protein C and a deficiency in plasminogen activator inhibitor type 1. Circ Res. 2006; 99(11): 1261–1269.
  24. Muramoto Y, Ozaki H, Takada A, et al. Highly pathogenic H5N1 influenza virus causes coagulopathy in chickens. Microbiol Immunol. 2006; 50(1): 73–81.
  25. Szretter KJ, Gangappa S, Belser JA, et al. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol. 2007; 81(6): 2736–2744.
  26. Di Stefano R, Di Bello V, Barsotti MC, et al. Inflammatory markers and cardiac function in acute coronary syndrome: difference in ST-segment elevation myocardial infarction (STEMI) and in non-STEMI models. Biomed Pharmacother. 2009; 63(10): 773–780.
  27. Stanek A, Fazeli B, Bartuś S, et al. The role of endothelium in physiological and pathological states: new data. Biomed Res Int. 2018; 2018: 1098039.
  28. Goeijenbier M, van Gorp ECM, Van den Brand JMA, et al. Activation of coagulation and tissue fibrin deposition in experimental influenza in ferrets. BMC Microbiol. 2014; 14: 134.
  29. Short KR, Kasper J, van der Aa S, et al. Influenza virus damages the alveolar barrier by disrupting epithelial cell tight junctions. Eur Respir J. 2016; 47(3): 954–966.
  30. Ashar HK, Mueller NC, Rudd JM, et al. The Role of Extracellular Histones in Influenza Virus Pathogenesis. Am J Pathol. 2018; 188(1): 135–148.
  31. Chan LLY, Hui KPY, Kuok DIT, et al. Risk assessment of the tropism and pathogenesis of the highly pathogenic avian influenza A/H7N9 virus using ex vivo and in vitro cultures of human respiratory tract. J Infect Dis. 2019; 220(4): 578–588.
  32. Short K, Kroeze EV, Reperant L, et al. Influenza virus and endothelial cells: a species specific relationship. Frontiers in Microbiology. 2014; 5.
  33. Short KR, Kuiken T, Van Riel D. Role of endothelial cells in the pathogenesis of influenza in humans. J Infect Dis. 2019; 220(11): 1859–1860.
  34. Perisetti A, Goyal H, Gajendran M, et al. Prevalence, mechanisms, and implications of gastrointestinal symptoms in COVID-19. Front Med (Lausanne). 2020; 7: 588711.
  35. Rahban M, Stanek A, Hooshmand A, et al. Infection of human cells by SARS-CoV-2 and molecular overview of gastrointestinal, neurological, and hepatic problems in COVID-19 patients. J Clin Med. 2021; 10(21).
  36. Buzhdygan TP, DeOre BJ, Baldwin-Leclair A, et al. 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.
  37. Javanian M, Barary M, Ghebrehewet S, et al. A brief review of influenza virus infection. J Med Virol. 2021; 93(8): 4638–4646.
  38. Liu WD, Yeh CY, Shih MC, et al. Clinical manifestations and risk factors for mortality of patients with severe influenza during the 2016-2018 season. Int J Infect Dis. 2020; 95: 347–351.
  39. Daoud A, Laktineh A, Macrander C, et al. Pulmonary complications of influenza infection: a targeted narrative review. Postgrad Med. 2019; 131(5): 299–308.
  40. Radovanovic M, Petrovic M, Barsoum MK, et al. Influenza myopericarditis and pericarditis: a literature review. J Clin Med. 2022; 11(14).
  41. Kietaibl AT, Fangmeyer-Binder M, Göndör G, et al. Acute viral myositis: profound rhabdomyolysis without acute kidney injury. Wien Klin Wochenschr. 2021; 133(15-16): 847–850.
  42. Robinson CP, Busl KM. Neurologic manifestations of severe respiratory viral contagions. Crit Care Explor. 2020; 2(4): e0107.
  43. Hwang JH, You YS, Yeom SW, et al. Influenza viral infection is a risk factor for severe illness in COVID-19 patients: a nationwide population-based cohort study. Emerg Microbes Infect. 2023; 12(1): 2164215.
  44. Corrales-Medina VF, Madjid M, Musher DM. Role of acute infection in triggering acute coronary syndromes. Lancet Infect Dis. 2010; 10(2): 83–92.
  45. Lichenstein R, Magder LS, King RE, et al. The relationship between influenza outbreaks and acute ischemic heart disease in Maryland residents over a 7-year period. J Infect Dis. 2012; 206(6): 821–827.
  46. Nicholson KG, Webster RG, Hay AJ. Textbook of influenza: Blackwell Science Ltd. ; 1998.
  47. Kodama M. Influenza myocarditis. Circ J. 2010; 74(10): 2060–2061.
  48. Chotpitayasunondh T, Ungchusak K, Hanshaoworakul W, et al. Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis. 2005; 11(2): 201–209.
  49. Onitsuka H, Imamura T, Miyamoto N, et al. Clinical manifestations of influenza a myocarditis during the influenza epidemic of winter 1998-1999. J Cardiol. 2001; 37(6): 315–323.
  50. Erden I, Erden EC, Ozhan H, et al. Echocardiographic manifestations of pandemic 2009 (H1N1) influenza a virus infection. J Infect. 2010; 61(1): 60–65.
  51. Verel D, Warrack AJ, Potter CW, et al. Observations on the A2 England influenza epidemic: a clinicopathological study. Am Heart J. 1976; 92(3): 290–296.
  52. Zanettini MT, Zanettini JO, Zanettini JP. Pericarditis. Series of 84 consecutive cases. Arq Bras Cardiol. 2004; 82(4): 360–369.
  53. Estabragh ZR, Mamas MA. The cardiovascular manifestations of influenza: a systematic review. Int J Cardiol. 2013; 167(6): 2397–2403.
  54. Sellers SA, Hagan RS, Hayden FG, et al. The hidden burden of influenza: A review of the extra-pulmonary complications of influenza infection. Influenza Other Respir Viruses. 2017; 11(5): 372–393.
  55. Gokhroo R, Barjaty H, Bhawna K. Cardiac conduction system affection in a case of swine flu. J Assoc Physicians India. 2011; 59: 51–2.
  56. Wiegand JA, Torgersen C, Bloechlinger S, et al. Influenza A(H1N1) infection and severe cardiac dysfunction in adults: A case series. Wien Klin Wochenschr. 2011; 123(3-4): 120–123.
  57. Machiedo GW, Zaets SB, Berezina TL, et al. Trauma-hemorrhagic shock-induced red blood cell damage leads to decreased microcirculatory blood flow. Crit Care Med. 2009;37(3):1000-10. doi: 10.1097/CCM.0b013e3181962d39. PubMed PMID. ; 19237910.
  58. Trzeciak S, McCoy JV, Phillip Dellinger R, et al. Microcirculatory Alterations in Resuscitation and Shock (MARS) investigators. Early increases in microcirculatory perfusion during protocol-directed resuscitation are associated with reduced multi-organ failure at 24 h in patients with sepsis. Intensive Care Med. 2008; 34(12): 2210–2217.
  59. Granger DN, Rodrigues SF, Yildirim A, et al. Microvascular responses to cardiovascular risk factors. Microcirculation. 2010; 17(3): 192–205.
  60. Feletou M, Tang EHC, Vanhoutte PM. Nitric oxide the gatekeeper of endothelial vasomotor control. Front Biosci. 2008; 13: 4198–4217.
  61. Rello J, Rodríguez A, Ibañez P, et al. Intensive care adult patients with severe respiratory failure caused by Influenza A (H1N1)v in Spain. Critical Care. 2009; 13(5): R148.
  62. Ueki H, Wang IH, Fukuyama S, et al. In vivo imaging of the pathophysiological changes and neutrophil dynamics in influenza virus-infected mouse lungs. Proc Natl Acad Sci U S A. 2018; 115(28): E6622–E6629.
  63. Salgado DR, Ortiz JA, Favory R, et al. Microcirculatory abnormalities in patients with severe influenza A (H1N1) infection. Can J Anaesth. 2010; 57(10): 940–946.
  64. Kaminski TW, Brzoska T, Li X, et al. Lung microvascular occlusion by platelet-rich neutrophil-platelet aggregates promotes cigarette smoke-induced severe flu. JCI Insight. 2024; 9(2).
  65. Brydak LB, Romanowska M, Nowak I, et al. Influenza vaccination in secondary prevention from coronary ischaemic events in coronary artery disease: FLUCAD study. Eur Heart J. 2008; 29(11): 1350–1358.
  66. Holmes EC, Hurt AC, Dobbie Z, et al. Understanding the impact of resistance to influenza antivirals. Clin Microbiol Rev. 2021; 34(2).
  67. Heneghan CJ, Onakpoya I, Jones MA, et al. Neuraminidase inhibitors for influenza: a systematic review and meta-analysis of regulatory and mortality data. Health Technol Assess. 2016; 20(42): 1–242.
  68. Casscells SW, Granger E, Kress AM, et al. Use of oseltamivir after influenza infection is associated with reduced incidence of recurrent adverse cardiovascular outcomes among military health system beneficiaries with prior cardiovascular diseases. Circ Cardiovasc Qual Outcomes. 2009; 2(2): 108–115.
  69. de Jong MD, Simmons CP, Thanh TT, et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med. 2006; 12(10): 1203–1207.
  70. Rothberg MB, Haessler SD. Complications of seasonal and pandemic influenza. Crit Care Med. 2010; 38(4 Suppl): e91–e97.
  71. Fedson DS. Confronting the next influenza pandemic with anti-inflammatory and immunomodulatory agents: why they are needed and how they might work. Influenza Other Respir Viruses. 2009; 3(4): 129–142.
  72. Short KR, Kuiken T, Van Riel D. Role of endothelial cells in the pathogenesis of influenza in humans. J Infect Dis. 2019; 220(11): 1859–1860.
  73. Gopal R, Marinelli MA, Alcorn JF. Immune Mechanisms in Cardiovascular Diseases Associated With Viral Infection. Front Immunol. 2020; 11: 570681.