Respiratory Syncytial Virus and Associations With Cardiovascular Disease in Adults

Journal of the American College of Cardiology

Volumn 71, Issue 14, 2018, Pages 1574-1583

  Ivey, Kelsey S ^a   Edwards, Kathryn M ^a   Talbot, H Keipp ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

cardiac exacerbation; hospitalizations; respiratory syncytial virus

Indexed keywords

INFLUENZA VACCINE; PALIVIZUMAB; PLACEBO; RESPIRATORY SYNCYTIAL VIRUS VACCINE;

ACUTE CORONARY SYNDROME; ADULT; ALL CAUSE MORTALITY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CHRONIC INFLAMMATION; CONGENITAL HEART DISEASE; CONGESTIVE HEART FAILURE; CORONARY ARTERY DISEASE; DISEASE BURDEN; FLU LIKE SYNDROME; HEALTH CARE UTILIZATION; HEART ARRHYTHMIA; HEART BLOCK; HEART LEFT VENTRICLE FAILURE; HEART RIGHT VENTRICLE FAILURE; HEART VENTRICLE TACHYCARDIA; HOSPITALIZATION COST; HUMAN; INFLUENZA; INFLUENZA VACCINATION; MYOCARDITIS; NONHUMAN; PERICARDIAL EFFUSION; PRIORITY JOURNAL; PROGNOSIS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; REVIEW; SUPRAVENTRICULAR TACHYCARDIA; VIRAL RESPIRATORY TRACT INFECTION; VIRUS PNEUMONIA; COMPLICATION; GLOBAL HEALTH; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INCIDENCE; VIROLOGY;

ADULT; CARDIOVASCULAR DISEASES; GLOBAL HEALTH; HUMANS; INCIDENCE; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN;

EID: 85044117539     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2018.02.013     Document Type: Review

References (90)

1. Madjid, M., Naghavi, M., Litovsky, S., Casscells, S.W., Influenza and cardiovascular disease: a new opportunity for prevention and the need for further studies. Circulation 108 (2003), 2730–2736.
2. Fischer, W.A. 2nd, Gong, M., Bhagwanjee, S., Sevransky, J., Global burden of influenza as a cause of cardiopulmonary morbidity and mortality. Glob Heart 9 (2014), 325–336.
3. Warren-Gash, C., Smeeth, L., Hayward, A.C., Influenza as a trigger for acute myocardial infarction or death from cardiovascular disease: a systematic review. Lancet Infect Dis 9 (2009), 601–610.
4. Benjamin, E.J., Blaha, M.J., Chiuve, S.E., et al. Heart Disease and Stroke Statistics-2017 Update: a report from the American Heart Association. Circulation 135 (2017), e146–e603.
5. Chanock, R., Roizman, B., Myers, R., Recovery from infants with respiratory illness of a virus related to chimpanzee coryza agent (CCA). I. Isolation, properties and characterization. Am J Hyg 66 (1957), 281–290.
6. Ogra, P.L., From chimpanzee coryza to palivizumab: changing times for respiratory syncytial virus. Pediatr Infect Dis J 19 (2000), 774–779 discussion 811–3.
7. Smith, D.K., Seales, S., Budzik, C., Respiratory syncytial virus bronchiolitis in children. Am Fam Physician 95 (2017), 94–99.
8. Hall, C.B., Weinberg, G.A., Iwane, M.K., et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med 360 (2009), 588–598.
9. Hall, C.B., Respiratory syncytial virus and parainfluenza virus. N Engl J Med 344 (2001), 1917–1928.
10. Bont, L., Checchia, P.A., Fauroux, B., et al. Defining the epidemiology and burden of severe respiratory syncytial virus infection among infants and children in Western countries. Infect Dis Ther 5 (2016), 271–298.
11. Mejias, A., Garcia-Maurino, C., Rodriguez-Fernandez, R., Peeples, M.E., Ramilo, O., Development and clinical applications of novel antibodies for prevention and treatment of respiratory syncytial virus infection. Vaccine 35 (2017), 496–502.
12. Volling, C., Hassan, K., Mazzulli, T., et al. Respiratory syncytial virus infection-associated hospitalization in adults: a retrospective cohort study. BMC Infect Dis, 14, 2014, 665.
13. Falsey, A.R., Cunningham, C.K., Barker, W.H., et al. Respiratory syncytial virus and influenza A infections in the hospitalized elderly. J Infect Dis 172 (1995), 389–394.
14. Dowell, S.F., Anderson, L.J., Gary, H.E. Jr., et al. Respiratory syncytial virus is an important cause of community-acquired lower respiratory infection among hospitalized adults. J Infect Dis 174 (1996), 456–462.
15. Walsh, E.E., Peterson, D.R., Falsey, A.R., Is clinical recognition of respiratory syncytial virus infection in hospitalized elderly and high-risk adults possible?. J Infect Dis 195 (2007), 1046–1051.
16. Widmer, K., Zhu, Y., Williams, J.V., Griffin, M.R., Edwards, K.M., Talbot, H.K., Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J Infect Dis 206 (2012), 56–62.
17. Falsey, A.R., McElhaney, J.E., Beran, J., et al. Respiratory syncytial virus and other respiratory viral infections in older adults with moderate to severe influenza-like illness. J Infect Dis 209 (2014), 1873–1881.
18. Falsey, A.R., Hennessey, P.A., Formica, M.A., Cox, C., Walsh, E.E., Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352 (2005), 1749–1759.
19. Walsh, E.E., Falsey, A.R., Hennessey, P.A., Respiratory syncytial and other virus infections in persons with chronic cardiopulmonary disease. Am J Respir Crit Care Med 160 (1999), 791–795.
20. Fleming, D.M., Taylor, R.J., Lustig, R.L., et al. Modelling estimates of the burden of Respiratory Syncytial virus infection in adults and the elderly in the United Kingdom. BMC Infect Dis, 15, 2015, 443.
21. Mullooly, J.P., Bridges, C.B., Thompson, W.W., et al. Influenza- and RSV-associated hospitalizations among adults. Vaccine 25 (2007), 846–855.
22. Zhou, H., Thompson, W.W., Viboud, C.G., et al. Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993–2008. Clin Infect Dis 54 (2012), 1427–1436.
23. Checchia, P.A., Paes, B., Bont, L., et al. Defining the risk and associated morbidity and mortality of severe respiratory syncytial virus infection among infants with congenital heart disease. Infect Dis Ther 6 (2017), 37–56.
24. Chu, P.Y., Hornik, C.P., Li, J.S., Campbell, M.J., Hill, K.D., Respiratory syncytial virus hospitalisation trends in children with haemodynamically significant heart disease, 1997–2012. Cardiol Young 27 (2017), 16–25.
25. Zhang, X.B., Liu, L.J., Qian, L.L., et al. Clinical characteristics and risk factors of severe respiratory syncytial virus-associated acute lower respiratory tract infections in hospitalized infants. World J Pediatr 10 (2014), 360–364.
26. Willson, D.F., Landrigan, C.P., Horn, S.D., Smout, R.J., Complications in infants hospitalized for bronchiolitis or respiratory syncytial virus pneumonia. J Pediatr 143 (2003), S142–S149.
27. Hall, C.B., Simoes, E.A., Anderson, L.J., Clinical and epidemiologic features of respiratory syncytial virus. Curr Top Microbiol Immunol 372 (2013), 39–57.
28. Butt, M., Symington, A., Janes, M., et al. Respiratory syncytial virus prophylaxis in children with cardiac disease: a retrospective single-centre study. Cardiol Young 24 (2014), 337–343.
29. Rodriguez, D.A., Rodriguez-Martinez, C.E., Cardenas, A.C., et al. Predictors of severity and mortality in children hospitalized with respiratory syncytial virus infection in a tropical region. Pediatr Pulmonol 49 (2014), 269–276.
30. El Kholy, A.A., Mostafa, N.A., El-Sherbini, S.A., et al. Morbidity and outcome of severe respiratory syncytial virus infection. Pediatr Int 55 (2013), 283–288.
31. Szabo, S.M., Gooch, K.L., Bibby, M.M., et al. The risk of mortality among young children hospitalized for severe respiratory syncytial virus infection. Paediatr Respir Rev 13 Suppl 2 (2013), S1–S8.
32. Thorburn, K., Pre-existing disease is associated with a significantly higher risk of death in severe respiratory syncytial virus infection. Arch Dis Child 94 (2009), 99–103.
33. Friedman, D., Wong, P.C., Risk of respiratory syncytial virus hospitalization in the first and second years of life in pediatric patients with congenital heart disease. Pediatr Cardiol 38 (2017), 1311–1312.
34. American Academy of Pediatrics Committee on Infectious Diseases, American Academy of Pediatrics Bronchiolitis Guidelines Committee. Updated guidance for palivizumab prophylaxis among infants and young children at increased risk of hospitalization for respiratory syncytial virus infection. Pediatrics 134 (2014), 415–420.
35. Feltes, T.F., Cabalka, A.K., Meissner, H.C., et al. Palivizumab prophylaxis reduces hospitalization due to respiratory syncytial virus in young children with hemodynamically significant congenital heart disease. J Pediatr 143 (2003), 532–540.
36. Loubet, P., Lenzi, N., Valette, M., et al. Clinical characteristics and outcome of respiratory syncytial virus infection among adults hospitalized with influenza-like illness in France. Clin Microbiol Infect 23 (2017), 253–259.
37. Widmer, K., Griffin, M.R., Zhu, Y., Williams, J.V., Talbot, H.K., Respiratory syncytial virus- and human metapneumovirus-associated emergency department and hospital burden in adults. Influenza Other Respir Viruses 8 (2014), 347–352.
38. Duncan, C.B., Walsh, E.E., Peterson, D.R., Lee, F.E., Falsey, A.R., Risk factors for respiratory failure associated with respiratory syncytial virus infection in adults. J Infect Dis 200 (2009), 1242–1246.
39. Walsh, E.E., Peterson, D.R., Falsey, A.R., Risk factors for severe respiratory syncytial virus infection in elderly persons. J Infect Dis 189 (2004), 233–238.
40. Sundaram, M.E., Meece, J.K., Sifakis, F., Gasser, R.A. Jr., Belongia, E.A., Medically attended respiratory syncytial virus infections in adults aged >/= 50 years: clinical characteristics and outcomes. Clin Infect Dis 58 (2014), 342–349.
41. Mehta, J., Walsh, E.E., Mahadevia, P.J., Falsey, A.R., Risk factors for respiratory syncytial virus illness among patients with chronic obstructive pulmonary disease. COPD 10 (2013), 293–299.
42. McCracken, J.P., Prill, M.M., Arvelo, W., et al. Respiratory syncytial virus infection in Guatemala, 2007–2012. J Infect Dis 208 Suppl 3 (2013), S197–S206.
43. Bainton, D., Jones, G.R., Hole, D., Influenza and ischaemic heart disease–a possible trigger for acute myocardial infarction?. Int J Epidemiol 7 (1978), 231–239.
44. Glezen, W.P., Payne, A.A., Snyder, D.N., Downs, T.D., Mortality and influenza. J Infect Dis 146 (1982), 313–321.
45. Scragg, R., Effect of influenza epidemics on Australian mortality. Med J Aust 142 (1985), 98–102.
46. Marshall, R.J., Scragg, R., Bourke, P., An analysis of the seasonal variation of coronary heart disease and respiratory disease mortality in New Zealand. Int J Epidemiol 17 (1988), 325–331.
47. Cooper, R., Tsong, Y., Hoeksema, R., Liu, K., Is the recent decline in coronary disease mortality in the United States attributable to lower rates of influenza and pneumonia?. Prev Med 9 (1980), 559–568.
48. Tillett, H.E., Smith, J.W., Gooch, C.D., Excess deaths attributable to influenza in England and Wales: age at death and certified cause. Int J Epidemiol 12 (1983), 344–352.
49. Alling, D.W., Blackwelder, W.C., Stuart-Harris, C.H., A study of excess mortality during influenza epidemics in the United States, 1968–1976. Am J Epidemiol 113 (1981), 30–43.
50. Spodick, D.H., Flessas, A.P., Johnson, M.M., Association of acute respiratory symptoms with onset of acute myocardial infarction: prospective investigation of 150 consecutive patients and matched control patients. Am J Cardiol 53 (1984), 481–482.
51. Mattila, K.J., Viral and bacterial infections in patients with acute myocardial infarction. J Intern Med 225 (1989), 293–296.
52. Meier, C.R., Jick, S.S., Derby, L.E., Vasilakis, C., Jick, H., Acute respiratory-tract infections and risk of first-time acute myocardial infarction. Lancet 351 (1998), 1467–1471.
53. Smeeth, L., Thomas, S.L., Hall, A.J., Hubbard, R., Farrington, P., Vallance, P., Risk of myocardial infarction and stroke after acute infection or vaccination. N Engl J Med 351 (2004), 2611–2618.
54. Giles, T.D., Gohd, R.S., Respiratory syncytial virus and heart disease. A report of two cases. JAMA 236 (1976), 1128–1130.
55. Huang, M., Bigos, D., Levine, M., Ventricular arrhythmia associated with respiratory syncytial viral infection. Pediatr Cardiol 19 (1998), 498–500.
56. Menchise, A., Myocarditis in the setting of RSV bronchiolitis. Fetal Pediatr Pathol 30 (2011), 64–68.
57. Thomas, J.A., Raroque, S., Scott, W.A., Toro-Figueroa, L.O., Levin, D.L., Successful treatment of severe dysrhythmias in infants with respiratory syncytial virus infections: two cases and a literature review. Crit Care Med 25 (1997), 880–886.
58. Thorburn, K., Eisenhut, M., Shauq, A., Narayanswamy, S., Burgess, M., Right ventricular function in children with severe respiratory syncytial virus (RSV) bronchiolitis. Minerva Anestesiol 77 (2011), 46–53.
59. Armstrong, D.S., Menahem, S., Cardiac arrhythmias as a manifestation of acquired heart disease in association with paediatric respiratory syncitial virus infection. J Paediatr Child Health 29 (1993), 309–311.
60. Menahem, S., Respiratory syncytial virus and supraventricular tachycardia in an infant. Int J Cardiol 32 (1991), 249–251.
61. Menahem, S., Respiratory syncytial virus and complete heart block in a child. Cardiol Young 20 (2010), 103–104.
62. Menahem, S., Uren, E.C., Respiratory syncytial virus and heart block–cause and effect?. Aust N Z J Med 15 (1985), 55–57.
63. Bairan, A.C., Cherry, J.D., Fagan, L.F., Codd, J.E. Jr, Complete heart block and respiratory syncytial virus infection. Am J Dis Child 127 (1974), 264–265.
64. Haddad, W., Agoudemous, M., Basnet, S., Prolonged sinoatrial block in an infant with respiratory syncytial viral bronchiolitis. Pediatr Cardiol 33 (2012), 1203–1205.
65. Esposito, S., Salice, P., Bosis, S., et al. Altered cardiac rhythm in infants with bronchiolitis and respiratory syncytial virus infection. BMC Infect Dis, 10, 2010, 305.
66. Guan, X.R., Jiang, L.X., Ma, X.H., Wang, L.F., Quan, H., Li, H.Y., Respiratory syncytial virus infection and risk of acute myocardial infarction. Am J Med Sci 340 (2010), 356–359.
67. Anderson, N.W., Binnicker, M.J., Harris, D.M., et al. Morbidity and mortality among patients with respiratory syncytial virus infection: a 2-year retrospective review. Diagn Microbiol Infect Dis 85 (2016), 367–371.
68. Lee, N., Lui, G.C., Wong, K.T., et al. High morbidity and mortality in adults hospitalized for respiratory syncytial virus infections. Clin Infect Dis 57 (2013), 1069–1077.
69. 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 101 (2015), 1738–1747.
70. Kwok, C.S., Aslam, S., Kontopantelis, E., et al. Influenza, influenza-like symptoms and their association with cardiovascular risks: a systematic review and meta-analysis of observational studies. Int J Clin Pract 69 (2015), 928–937.
71. Zambon, M.C., Stockton, J.D., Clewley, J.P., Fleming, D.M., Contribution of influenza and respiratory syncytial virus to community cases of influenza-like illness: an observational study. Lancet 358 (2001), 1410–1416.
72. Johnson, J.E., Gonzales, R.A., Olson, S.J., Wright, P.F., Graham, B.S., The histopathology of fatal untreated human respiratory syncytial virus infection. Mod Pathol 20 (2007), 108–119.
73. Thorburn, K., Hart, C.A., Think outside the box: extrapulmonary manifestations of severe respiratory syncytial virus infection. Crit Care, 10, 2006, 159.
74. Eisenhut, M., Extrapulmonary manifestations of severe respiratory syncytial virus infection–a systematic review. Crit Care, 10, 2006, R107.
75. Fishaut, M., Tubergen, D., McIntosh, K., Cellular response to respiratory viruses with particular reference to children with disorders of cell-mediated immunity. J Pediatr 96 (1980), 179–186.
76. Bowles, N.E., Ni, J., Kearney, D.L., et al. Detection of viruses in myocardial tissues by polymerase chain reaction. evidence of adenovirus as a common cause of myocarditis in children and adults. J Am Coll Cardiol 42 (2003), 466–472.
77. Mattila, K.J., Valtonen, V.V., Nieminen, M.S., Asikainen, S., Role of infection as a risk factor for atherosclerosis, myocardial infarction, and stroke. Clin Infect Dis 26 (1998), 719–734.
78. Naghavi, M., Wyde, P., Litovsky, S., et al. Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E-deficient mice. Circulation 107 (2003), 762–768.
79. Udell, J.A., Farkouh, M.E., Solomon, S.D., Vardeny, O., Does influenza vaccination influence cardiovascular complications?. Expert Rev Cardiovasc Ther 13 (2015), 593–596.
80. Corrales-Medina, V.F., Madjid, M., Musher, D.M., Role of acute infection in triggering acute coronary syndromes. Lancet Infect Dis 10 (2010), 83–92.
81. Chang, T.Y., Chao, T.F., Liu, C.J., et al. The association between influenza infection, vaccination, and atrial fibrillation: A nationwide case-control study. Heart Rhythm 13 (2016), 1189–1194.
82. Goritzka, M., Durant, L.R., Pereira, C., Salek-Ardakani, S., Openshaw, P.J., Johansson, C., Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J Virol 88 (2014), 6128–6136.
83. Kakimoto, Y., Seto, Y., Ochiai, E., Satoh, F., Osawa, M., Cytokine elevation in sudden death with respiratory syncytial virus: a case report of 2 children. Pediatrics, 138, 2016, e20161293.
84. Udell, J.A., Zawi, R., Bhatt, D.L., et al. Association between influenza vaccination and cardiovascular outcomes in high-risk patients: a meta-analysis. JAMA 310 (2013), 1711–1720.
85. Clar, C., Oseni, Z., Flowers, N., Keshtkar-Jahromi, M., Rees, K., Influenza vaccines for preventing cardiovascular disease. Cochrane Database Syst Rev(5), 2015 CD005050.
86. Vardeny, O., Claggett, B., Udell, J.A., et al. Influenza vaccination in patients with chronic heart failure: the PARADIGM-HF trial. J Am Coll Cardiol HF 4 (2016), 152–158.
87. Meijboom, M.J., Pouwels, K.B., Luytjes, W., Postma, M.J., Hak, E., RSV vaccine in development: assessing the potential cost-effectiveness in the Dutch elderly population. Vaccine 31 (2013), 6254–6260.
88. Higgins, D., Trujillo, C., Keech, C., Advances in RSV vaccine research and development - A global agenda. Vaccine 34 (2016), 2870–2875.
89. Falloon J. A phase 2b randomized, double-blind study to evaluate the efficacy of MEDI7510 for the prevention of acute respiratory syncytial virus-associated respiratory illness in older adults. 2016. Available at: https://clinicaltrials.gov/ct2/show/results/NCT02508194?sect=X70156. Accessed January 18, 2018.
90. Graham, B.S., Vaccines against respiratory syncytial virus: The time has finally come. Vaccine 34 (2016), 3535–3541.