Beyond Respiratory Syncytial Virus and Rhinovirus in the Pathogenesis and Exacerbation of Asthma: The Role of Metapneumovirus, Bocavirus and Influenza Virus

Immunology and Allergy Clinics of North America

Volumn 39, Issue 3, 2019, Pages 391-401

  Coverstone, Andrea M ^a   Wang, Leyao ^a   Sumino, Kaharu ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Asthma; Bocavirus; Human metapneumovirus; Influenza virus; Wheezing

Indexed keywords

CD8 ANTIGEN; CYTOKINE; INACTIVATED VACCINE; INFLUENZA VACCINE; INTERLEUKIN 13; INTERLEUKIN 33; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC ASTHMA; ASTHMA; BOCAPARVOVIRUS; CD8+ T LYMPHOCYTE; CLINICAL TRIAL (TOPIC); CYTOKINE RESPONSE; DISEASE ASSOCIATION; DISEASE EXACERBATION; HUMAN; HUMAN BOCAVIRUS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INFECTION RISK; INFLUENZA VIRUS; LYMPHOID CELL; METAPNEUMOVIRUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHINOVIRUS; SYSTEMATIC REVIEW (TOPIC); TH1 CELL; TH2 CELL; VIRAL BRONCHIOLITIS; VIRUS DETECTION; VIRUS IDENTIFICATION; WHEEZING; ABNORMAL RESPIRATORY SOUND; COMPLICATION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MORTALITY; ODDS RATIO; ORTHOMYXOVIRIDAE; PNEUMOVIRUS; VIROLOGY; VIRUS INFECTION;

ASTHMA; BOCAVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; METAPNEUMOVIRUS; ODDS RATIO; ORTHOMYXOVIRIDAE; RESPIRATORY SOUNDS; RESPIRATORY SYNCYTIAL VIRUSES; RHINOVIRUS; VIRUS DISEASES;

EID: 85065558332     PISSN: 08898561     EISSN: 15578607     Source Type: Journal    
DOI: 10.1016/j.iac.2019.03.007     Document Type: Review

References (73)

1. Allander, T., Jartti, T., Gupta, S., et al. Human bocavirus and acute wheezing in children. Clin Infect Dis 44:7 (2007), 904–910.
2. Heymann, P.W., Carper, H.T., Murphy, D.D., et al. Viral infections in relation to age, atopy, and season of admission among children hospitalized for wheezing. J Allergy Clin Immunol 114:2 (2004), 239–247.
3. Kusel, M.M., Kebadze, T., Johnston, S.L., et al. Febrile respiratory illnesses in infancy and atopy are risk factors for persistent asthma and wheeze. Eur Respir J 39:4 (2012), 876–882.
4. Zheng, X.Y., Xu, Y.J., Guan, W.J., et al. Regional, age and respiratory-secretion-specific prevalence of respiratory viruses associated with asthma exacerbation: a literature review. Arch Virol 163:4 (2018), 845–853.
5. Tan, W.C., Viruses in asthma exacerbations. Curr Opin Pulm Med 11:1 (2005), 21–26.
6. Rubner, F.J., Jackson, D.J., Evans, M.D., et al. Early life rhinovirus wheezing, allergic sensitization, and asthma risk at adolescence. J Allergy Clin Immunol 139:2 (2017), 501–507.
7. Jackson, D.J., Gangnon, R.E., Evans, M.D., et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 178:7 (2008), 667–672.
8. Anderson, H.M., Lemanske, R.F. Jr., Evans, M.D., et al. Assessment of wheezing frequency and viral etiology on childhood and adolescent asthma risk. J Allergy Clin Immunol 139:2 (2017), 692–694.
9. Bacharier, L.B., Cohen, R., Schweiger, T., et al. Determinants of asthma after severe respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 130:1 (2012), 91–100 e103.
10. Sigurs, N., Aljassim, F., Kjellman, B., et al. Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax 65:12 (2010), 1045–1052.
11. Kusel, M.M., de Klerk, N.H., Kebadze, T., et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 119:5 (2007), 1105–1110.
12. Turunen, R., Koistinen, A., Vuorinen, T., et al. The first wheezing episode: respiratory virus etiology, atopic characteristics, and illness severity. Pediatr Allergy Immunol 25:8 (2014), 796–803.
13. Coverstone, A.M., Wilson, B., Burgdorf, D., et al. Recurrent wheezing in children following human metapneumovirus infection. J Allergy Clin Immunol 142:1 (2018), 297–301.e2.
14. Bonnelykke, K., Vissing, N.H., Sevelsted, A., et al. Association between respiratory infections in early life and later asthma is independent of virus type. J Allergy Clin Immunol 136:1 (2015), 81–86.e4.
15. van den Hoogen, B.G., de Jong, J.C., Groen, J., et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med 7:6 (2001), 719–724.
16. Williams, J.V., Harris, P.A., Tollefson, S.J., et al. Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med 350:5 (2004), 443–450.
17. Jartti, T., van den Hoogen, B., Garofalo, R.P., et al. Metapneumovirus and acute wheezing in children. Lancet 360:9343 (2002), 1393–1394.
18. Boivin, G., De Serres, G., Cote, S., et al. Human metapneumovirus infections in hospitalized children. Emerg Infect Dis 9:6 (2003), 634–640.
19. Agapov, E., Sumino, K.C., Gaudreault-Keener, M., et al. Genetic variability of human metapneumovirus infection: evidence of a shift in viral genotype without a change in illness. J Infect Dis 193:3 (2006), 396–403.
20. Wei, H.Y., Tsao, K.C., Huang, C.G., et al. Clinical features of different genotypes/genogroups of human metapneumovirus in hospitalized children. J Microbiol Immunol 46:5 (2013), 352–357.
21. Zhang, L., Liu, W., Liu, D., et al. Epidemiological and clinical features of human metapneumovirus in hospitalised paediatric patients with acute respiratory illness: a cross-sectional study in Southern China, from 2013 to 2016. BMJ Open, 8(2), 2018, e019308.
22. Gu, W., Wang, Y., Hao, C., et al. Elevated serum levels of thymic stromal lymphopoietin in wheezing children infected with human metapneumovirus. Jpn J Infect Dis 70:2 (2017), 161–166.
23. Edwards, K.M., Zhu, Y., Griffin, M.R., et al. Burden of human metapneumovirus infection in young children. N Engl J Med 368:7 (2013), 633–643.
24. Garcia-Garcia, M.L., Calvo, C., Rey, C., et al. Human metapnuemovirus infections in hospitalized children and comparison with other respiratory viruses. 2005-2014 prospective study. PLoS One, 12(3), 2017, e0173504.
25. Pancham, K., Sami, I., Perez, G.F., et al. Human metapneumovirus infection is associated with severe respiratory disease in preschool children with history of prematurity. Pediatr Neonatol 57:1 (2016), 27–34.
26. Garcia-Garcia, M.L., Calvo, C., Casas, I., et al. Human metapneumovirus bronchiolitis in infancy is an important risk factor for asthma at age 5. Pediatr Pulmonol 42:5 (2007), 458–464.
27. Olenec, J.P., Kim, W.K., Lee, W.M., et al. Weekly monitoring of children with asthma for infections and illness during common cold seasons. J Allergy Clin Immunol 125:5 (2010), 1001–1006.e1.
28. Kantor, D.B., Stenquist, N., McDonald, M.C., et al. Rhinovirus and serum IgE are associated with acute asthma exacerbation severity in children. J Allergy Clin Immunol 138:5 (2016), 1467–1471.e9.
29. Broughton, S., Sylvester, K.P., Fox, G., et al. Lung function in prematurely born infants after viral lower respiratory tract infections. Pediatr Infect Dis J 26:11 (2007), 1019–1024.
30. Hamelin, M.E., Prince, G.A., Gomez, A.M., et al. Human metapneumovirus infection induces long-term pulmonary inflammation associated with airway obstruction and hyperresponsiveness in mice. J Infect Dis 193:12 (2006), 1634–1642.
31. Kolli, D., Gupta, M.R., Sbrana, E., et al. Alveolar macrophages contribute to the pathogenesis of human metapneumovirus infection while protecting against respiratory syncytial virus infection. Am J Respir Cell Mol Biol 51:4 (2014), 502–515.
32. Chauhan, A., Singh, M., Agarwal, A., et al. Correlation of TSLP, IL-33, and CD4 + CD25 + FOXP3 + T regulatory (Treg) in pediatric asthma. J Asthma 52:9 (2015), 868–872.
33. Siracusa, M.C., Saenz, S.A., Hill, D.A., et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 477:7363 (2011), 229–233.
34. Lay, M.K., Cespedes, P.F., Palavecino, C.E., et al. Human metapneumovirus infection activates the TSLP pathway that drives excessive pulmonary inflammation and viral replication in mice. Eur J Immunol 45:6 (2015), 1680–1695.
35. Allander, T., Tammi, M.T., Eriksson, M., et al. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci U S A 102:36 (2005), 12891–12896.
36. Christensen, A., Nordbo, S.A., Krokstad, S., et al. Human bocavirus in children: mono-detection, high viral load and viraemia are associated with respiratory tract infection. J Clin Virol 49:3 (2010), 158–162.
37. Byington, C.L., Ampofo, K., Stockmann, C., et al. Community surveillance of respiratory viruses among families in the Utah better identification of germs-longitudinal viral epidemiology (BIG-LoVE) study. Clin Infect Dis 61:8 (2015), 1217–1224.
38. Martin, E.T., Kuypers, J., McRoberts, J.P., et al. Human bocavirus 1 primary infection and shedding in infants. J Infect Dis 212:4 (2015), 516–524.
39. Jartti, T., Hedman, K., Jartti, L., et al. Human bocavirus-the first 5 years. Rev Med Virol 22:1 (2012), 46–64.
40. Schildgen, O., Muller, A., Allander, T., et al. Human bocavirus: passenger or pathogen in acute respiratory tract infections?. Clin Microbiol Rev 21:2 (2008), 291–304 table of contents.
41. Guido, M., Tumolo, M.R., Verri, T., et al. Human bocavirus: current knowledge and future challenges. World J Gastroenterol 22:39 (2016), 8684–8697.
42. Lukkarinen, H., Soderlund-Venermo, M., Vuorinen, T., et al. Human bocavirus 1 may suppress rhinovirus-associated immune response in wheezing children. J Allergy Clin Immunol 133:1 (2014), 256–258.e1-4.
43. Del Rosal, T., Garcia-Garcia, M.L., Calvo, C., et al. Recurrent wheezing and asthma after bocavirus bronchiolitis. Allergol Immunopathol (Madr) 44:5 (2016), 410–414.
44. Molinari, N.A., Ortega-Sanchez, I.R., Messonnier, M.L., et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:27 (2007), 5086–5096.
45. Khetsuriani, N., Kazerouni, N.N., Erdman, D.D., et al. Prevalence of viral respiratory tract infections in children with asthma. J Allergy Clin Immunol 119:2 (2007), 314–321.
46. Tan, W.C., Xiang, X., Qiu, D., et al. Epidemiology of respiratory viruses in patients hospitalized with near-fatal asthma, acute exacerbations of asthma, or chronic obstructive pulmonary disease. Am J Med 115:4 (2003), 272–277.
47. Teichtahl, H., Buckmaster, N., Pertnikovs, E., The incidence of respiratory tract infection in adults requiring hospitalization for asthma. Chest 112:3 (1997), 591–596.
48. Shim, D.H., Park, Y.A., Kim, M.J., et al. Pandemic influenza virus, pH1N1, induces asthmatic symptoms via activation of innate lymphoid cells. Pediatr Allergy Immunol 26:8 (2015), 780–788.
49. Ravanetti, L., Dijkhuis, A., Dekker, T., et al. IL-33 drives influenza-induced asthma exacerbations by halting innate and adaptive antiviral immunity. J Allergy Clin Immunol 143:4 (2019), 1355–1370.
50. Ravanetti, L., Dijkhuis, A., Sabogal Pineros, Y.S., et al. An early innate response underlies severe influenza-induced exacerbations of asthma in a novel steroid-insensitive and anti-IL-5-responsive mouse model. Allergy 72:5 (2017), 737–753.
51. Lund, S., Walford, H.H., Doherty, T.A., Type 2 innate lymphoid cells in allergic disease. Curr Immunol Rev 9:4 (2013), 214–221.
52. Chang, Y.J., Kim, H.Y., Albacker, L.A., et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 12:7 (2011), 631–638.
53. Contoli, M., Message, S.D., Laza-Stanca, V., et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 12:9 (2006), 1023–1026.
54. Forbes, R.L., Gibson, P.G., Murphy, V.E., et al. Impaired type I and III interferon response to rhinovirus infection during pregnancy and asthma. Thorax 67:3 (2012), 209–214.
55. Sykes, A., Macintyre, J., Edwards, M.R., et al. Rhinovirus-induced interferon production is not deficient in well controlled asthma. Thorax 69:3 (2014), 240–246.
56. Patel, D.A., You, Y., Huang, G., et al. Interferon response and respiratory virus control are preserved in bronchial epithelial cells in asthma. J Allergy Clin Immunol 134:6 (2014), 1402–1412.e7.
57. Kloepfer, K.M., Olenec, J.P., Lee, W.M., et al. Increased H1N1 infection rate in children with asthma. Am J Respir Crit Care Med 185:12 (2012), 1275–1279.
58. Grohskopf, L.A., Sokolow, L.Z., Broder, K.R., et al. Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices-United States, 2018-19 influenza season. MMWR Recomm Rep 67:3 (2018), 1–20.
59. Cullen, G., Martin, J., O'Donnell, J., et al. Surveillance of the first 205 confirmed hospitalised cases of pandemic H1N1 influenza in Ireland, 28 April - 3 October 2009. Euro Surveill, 14(44), 2009 [pii:19389].
60. Santillan Salas, C.F., Mehra, S., Pardo Crespo, M.R., et al. Asthma and severity of 2009 novel H1N1 influenza: a population-based case-control study. J Asthma 50:10 (2013), 1069–1076.
61. Veerapandian, R., Snyder, J.D., Samarasinghe, A.E., Influenza in asthmatics: for better or for worse?. Front Immunol, 9, 2018, 1843.
62. Van Kerkhove, M.D., Vandemaele, K.A., Shinde, V., et al. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis. PLoS Med, 8(7), 2011, e1001053.
63. Louie, J.K., Acosta, M., Winter, K., et al. Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA 302:17 (2009), 1896–1902.
64. Myles, P.R., Semple, M.G., Lim, W.S., et al. Predictors of clinical outcome in a national hospitalised cohort across both waves of the influenza A/H1N1 pandemic 2009-2010 in the UK. Thorax 67:8 (2012), 709–717.
65. Myles, P., Nguyen-Van-Tam, J.S., Semple, M.G., et al. Differences between asthmatics and nonasthmatics hospitalised with influenza A infection. Eur Respir J 41:4 (2013), 824–831.
66. Samarasinghe, A.E., Melo, R.C., Duan, S., et al. Eosinophils promote antiviral immunity in mice infected with influenza A virus. J Immunol 198:8 (2017), 3214–3226.
67. An, S., Jeon, Y.J., Jo, A., et al. Initial influenza virus replication can be limited in allergic asthma through rapid induction of type III interferons in respiratory epithelium. Front Immunol, 9, 2018, 986.
68. Ishikawa, H., Sasaki, H., Fukui, T., et al. Mice with asthma are more resistant to influenza virus infection and NK cells activated by the induction of asthma have potentially protective effects. J Clin Immunol 32:2 (2012), 256–267.
69. Cates, C.J., Rowe, B.H., Vaccines for preventing influenza in people with asthma. Cochrane Database Syst Rev(2), 2013 CD000364.
70. Nicholson, K.G., Nguyen-Van-Tam, J.S., Ahmed, A.H., et al. Randomised placebo-controlled crossover trial on effect of inactivated influenza vaccine on pulmonary function in asthma. Lancet 351:9099 (1998), 326–331.
71. Bueving, H.J., Bernsen, R.M., de Jongste, J.C., et al. Does influenza vaccination exacerbate asthma in children?. Vaccine 23:1 (2004), 91–96.
72. The American Lung Association Asthma Clinical Research Centers, The safety of inactivated influenza vaccine in adults and children with asthma. N Engl J Med 345:21 (2001), 1529–1536.
73. Turner, P.J., Southern, J., Andrews, N.J., et al. Safety of live attenuated influenza vaccine in atopic children with egg allergy. J Allergy Clin Immunol 136:2 (2015), 376–381.