Influenza in asthmatics: For better or for worse?

Frontiers in Immunology

Volumn 9, Issue AUG, 2018, Pages

  Veerapandian, Raja ^a,b   Snyder, John D ^a,b   Samarasinghe, Amali E ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

Author keywords

Allergic asthma; Co morbidity; Eosinophils; Mouse; Pandemic influenza

Indexed keywords

HISTAMINE; IMMUNOGLOBULIN E; LEUKOTRIENE; PROSTAGLANDIN; REACTIVE OXYGEN METABOLITE;

ALLERGIC REACTION; ASTHMA; BACTERIAL INFECTION; CELLULAR IMMUNITY; COMORBIDITY; EOSINOPHILIA; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INFLUENZA; INFLUENZA VIRUS; LEUKOCYTE; MUSCLE FIBER CONTRACTION; NONHUMAN; RESPIRATORY TRACT DISEASE; REVIEW; RISK FACTOR; VASODILATATION; WOUND HEALING; ANIMAL; DISEASE MODEL; HOSPITALIZATION; HOST PATHOGEN INTERACTION; HYPERSENSITIVITY; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); MOUSE; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; UNITED STATES;

ANIMALS; ASTHMA; COMORBIDITY; DISEASE MODELS, ANIMAL; HOSPITALIZATION; HOST-PATHOGEN INTERACTIONS; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MICE; ORTHOMYXOVIRIDAE INFECTIONS; UNITED STATES;

EID: 85054932330     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.01843     Document Type: Review

References (175)

1. WHO. Asthma. Asthma Fact Sheet. WHO Media Centre, WHO (2011). Available from: http://www.who.int/en/news-room/fact-sheets/detail/asthma
2. American Lung Association. Asthma and Children Fact Sheet. (2012). Available from: http://www.lung.org/lung-health-and-diseases/lung-disease-lookup/asthma/learn-about-asthma/asthma-children-facts-sheet.html
3. CDC. Asthma in the US. Statistics on Asthma in the US. (2011). Available from: https://www.cdc.gov/vitalsigns/asthma/index.html
4. Monto AS. Epidemiology of viral respiratory infections. Am J Med (2002) 112(Suppl 6A):4S-12S. doi:10.1016/S0002-9343(01)01058-0
5. Sigurs N, Gustafsson PM, Bjarnason R, Lundberg F, Schmidt S, Sigurbergsson F, et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med (2005) 171:137-41. doi:10.1164/rccm.200406-730OC
6. Wu P, Dupont WD, Griffin MR, Carroll KN, Mitchel EF, Gebretsadik T, et al. Evidence of a causal role of winter virus infection during infancy in early childhood asthma. Am J Respir Crit Care Med (2008) 178:1123-9. doi:10.1164/rccm.200804-579OC
7. Gern JE. How rhinovirus infections cause exacerbations of asthma. Clin Exp Allergy (2015) 45:32-42. doi:10.1111/cea.12428
8. Gern JE, Busse WW. Association of rhinovirus infections with asthma. Clin Microbiol Rev (1999) 12:9-18
9. Adamko DJ, Friesen M. Why does respiratory syncytial virus appear to cause asthma? J Allergy Clin Immunol (2012) 130:101-2. doi:10.1016/j.jaci.2012.05.024
10. Kuehni CE, Spycher BD, Silverman M. Causal links between RSV infection and asthma: no clear answers to an old question. Am J Respir Crit Care Med (2009) 179:1079-80. doi:10.1164/rccm.200904-0567ED
11. Saavedra-Delgado AM, Cohen SG. Huang-Ti, the Yellow Emperor and the Nei Ching: antiquity's earliest reference to asthma. Allergy Proc (1991) 12:197-8. doi:10.2500/108854191778879395
12. Keeney EL. The history of asthma from hippocrates to meltzer. J Allergy (1964) 35:215-26. doi:10.1016/0021-8707(64)90004-8
13. Marketos SG, Ballas CN. Bronchial asthma in the medical literature of Greek antiquity. J Asthma (1982) 19:263-9. doi:10.3109/02770908209104771
14. Sakula A. A history of asthma. The FitzPatrick lecture 1987. J R Coll Physicians Lond (1988) 22:36-44
15. Walter MJ, Holtzman MJ. A centennial history of research on asthma pathogenesis. Am J Respir Cell Mol Biol (2005) 32:483-9. doi:10.1165/rcmb. F300
16. Hohlfeld JM. The role of surfactant in asthma. Respir Res (2002) 3:4. doi:10.1186/rr176
17. WHO. Asthma. Bronchial Asthma Fact Sheet. WHO Media Centre, WHO (2017). N206 p. Available from: http://www.who.int/mediacentre/factsheets/fs206/en/
18. Maslan J, Mims JW. What is asthma? Pathophysiology, demographics, and health care costs. Otolaryngol Clin North Am (2014) 47:13-22. doi:10.1016/j.otc.2013.09.010
19. Barnett SB, Nurmagambetov TA. Costs of asthma in the United States: 2002-2007. J Allergy Clin Immunol (2011) 127:145-52. doi:10.1016/j.jaci.2010.10.020
20. Simpson JL, Scott R, Boyle MJ, Gibson PG. Inflammatory subtypes in asthma: assessment and identification using induced sputum. Respirology (2006) 11:54-61. doi:10.1111/j.1440-1843.2006.00784.x
21. Porsbjerg C, Lund TK, Pedersen L, Backer V. Inflammatory subtypes in asthma are related to airway hyperresponsiveness to mannitol and exhaled NO. J Asthma (2009) 46:606-12. doi:10.1080/02770900903015654
22. Report WNW. Global Strategy for Asthma Management and Prevention. Bethesda, MD: National Heart, Lung, and Blood Institute (1995)
23. Global Initiative for Asthma. 2018 GINA Report, Global Strategy for Asthma Management and Prevention. (2018). p. 1-162. Available from: https://ginasthma.org/2018-gina-report-global-strategy-for-asthma-management-and-prevention/
24. Wanner A, Salathe M, O'Riordan TG. Mucociliary clearance in the airways. Am J Respir Crit Care Med (1996) 154:1868-902. doi:10.1164/ajrccm.154.6.8970383
25. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med (2000) 161:1720-45. doi:10.1164/ajrccm.161.5.9903102
26. Islam SA, Luster AD. T cell homing to epithelial barriers in allergic disease. Nat Med (2012) 18:705-15. doi:10.1038/nm.2760
27. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med (2012) 18:673-83. doi:10.1038/nm.2731
28. Deckers J, Branco Madeira F, Hammad H. Innate immune cells in asthma. Trends Immunol (2013) 34:540-7. doi:10.1016/j.it.2013.08.004
29. DeKruyffRH, Yu S, Kim HY, Umetsu DT. Innate immunity in the lung regulates the development of asthma. Immunol Rev (2014) 260:235-48. doi:10.1111/imr.12187
30. Lloyd CM, Saglani S. Epithelial cytokines and pulmonary allergic inflammation. Curr Opin Immunol (2015) 34:52-8. doi:10.1016/j.coi.2015.02.001
31. Divakaran S, Dellaripa P, Kobzik L, Levy B, Loscalzo J. All that wheezes. N Engl J Med (2017) 377:477-84. doi:10.1056/NEJMcps1607526
32. Patterson K, Strek ME. Allergic bronchopulmonary aspergillosis. Proc Am Thorac Soc (2010) 7:237-44. doi:10.1513/pats.200908-086AL
33. Hashimoto S, Bel EH. Current treatment of severe asthma. Clin Exp Allergy (2012) 42:693-705. doi:10.1111/j.1365-2222.2011.03936.x
34. Patel PH, Sharma S. Wheezing. StatPearls. Treasure Island (FL): StatPearls Publishing (2018). Available from: https://www.ncbi.nlm.nih.gov/books/NBK482454/
35. Pasterkamp H. The highs and lows of wheezing: a review of the most popular adventitious lung sound. Pediatr Pulmonol (2018) 53:243-54. doi:10.1002/ppul.23930
36. Busse WW, Lemanske RF Jr, Gern JE. Role of viral respiratory infections in asthma and asthma exacerbations. Lancet (2010) 376:826-34. doi:10.1016/S0140-6736(10)61380-3
37. Gern JE. The ABCs of rhinoviruses, wheezing, and asthma. J Virol (2010) 84:7418-26. doi:10.1128/JVI.02290-09
38. Kim CK, Callaway Z, Gern JE. Viral infections and associated factors that promote acute exacerbations of asthma. Allergy Asthma Immunol Res (2018) 10:12-7. doi:10.4168/aair.2018.10.1.12
39. Fry J. Acute wheezy chests. Br Med J (1961) 1:227-32. doi:10.1136/bmj.1.5221.227
40. Pavord ID, Beasley R, Agusti A, Anderson GP, Bel E, Brusselle G, et al. After asthma: redefining airways diseases. Lancet (2018) 391:350-400. doi:10.1016/S0140-6736(17)30879-6
41. Bush A, Fleming L. Is asthma overdiagnosed? Arch Dis Child (2016) 101:688-9. doi:10.1136/archdischild-2015-309053
42. Aaron SD, Boulet LP, Reddel HK, Gershon A. Under-diagnosis and over-diagnosis of asthma. Am J Respir Crit Care Med (2018). doi:10.1164/rccm.201804-0682CI
43. Looijmans-van den Akker I, van Luijn K, Verheij T. Overdiagnosis of asthma in children in primary care: a retrospective analysis. Br J Gen Pract (2016) 66:e152-7. doi:10.3399/bjgp16X683965
44. Lindsay JT, Heaney LG. Nonadherence in difficult asthma-facts, myths, and a time to act. Patient Prefer Adherence (2013) 7:329-36. doi:10.2147/PPA.S38208
45. Papi A, Brightling C, Pedersen SE, Reddel HK. Asthma. Lancet (2018) 391:783-800. doi:10.1016/S0140-6736(17)33311-1
46. Loxham M, Davies DE. Phenotypic and genetic aspects of epithelial barrier function in asthmatic patients. J Allergy Clin Immunol (2017) 139:1736-51. doi:10.1016/j.jaci.2017.04.005
47. Lambrecht BN, Hammad H. The airway epithelium in asthma. Nat Med (2012) 18:684-92. doi:10.1038/nm.2737
48. Locksley RM. Asthma and allergic inflammation. Cell (2010) 140:777-83. doi:10.1016/j.cell.2010.03.004
49. Lambrecht BN, Hammad H. Biology of lung dendritic cells at the origin of asthma. Immunity (2009) 31:412-24. doi:10.1016/j.immuni.2009.08.008
50. Bousquet J, Chanez P, Lacoste JY, Barneon G, Ghavanian N, Enander I, et al. Eosinophilic inflammation in asthma. N Engl J Med (1990) 323:1033-9. doi:10.1056/NEJM199010113231505
51. Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, et al. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med (1992) 326:298-304. doi:10.1056/NEJM199201303260504
52. Sur S, Gleich GJ, Offord KP, Swanson MC, Ohnishi T, Martin LB, et al. Allergen challenge in asthma: association of eosinophils and lymphocytes with interleukin-5. Allergy (1995) 50:891-8. doi:10.1111/j.1398-9995.1995.tb02495.x
53. Weller PF, Spencer LA. Functions of tissue-resident eosinophils. Nat Rev Immunol (2017) 17:746-60. doi:10.1038/nri.2017.95
54. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM, et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science (1998) 282:2261-3. doi:10.1126/science.282.5397.2261
55. Wills-Karp M. Interleukin-13 in asthma pathogenesis. Immunol Rev (2004) 202:175-90. doi:10.1111/j.0105-2896.2004.00215.x
56. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol (2011) 12:1045-54. doi:10.1031/ni.2131
57. Hallstrand TS, Henderson WR Jr. An update on the role of leukotrienes in asthma. Curr Opin Allergy Clin Immunol (2010) 10:60-6. doi:10.1097/ACI.0b013e32833489c3
58. WoodruffPG, Khashayar R, Lazarus SC, Janson S, Avila P, Boushey HA, et al. Relationship between airway inflammation, hyperresponsiveness, and obstruction in asthma. J Allergy Clin Immunol (2001) 108:753-8. doi:10.1067/mai.2001.119411
59. Wenzel SE, Schwartz LB, Langmack EL, Halliday JL, Trudeau JB, Gibbs RL, et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med (1999) 160:1001-8. doi:10.1164/ajrccm.160.3.9812110
60. Moore WC, Hastie AT, Li X, Li H, Busse WW, Jarjour NN, et al. Sputum neutrophil counts are associated with more severe asthma phenotypes using cluster analysis. J Allergy Clin Immunol (2014) 133:1557-63.e5. doi:10.1016/j.jaci.2013.10.011
61. Sur S, Crotty TB, Kephart GM, Hyma BA, Colby TV, Reed CE, et al. Sudden-onset fatal asthma. A distinct entity with few eosinophils and relatively more neutrophils in the airway submucosa? Am Rev Respir Dis (1993) 148:713-9. doi:10.1164/ajrccm/148.3.713
62. Noda T. Native morphology of influenza virions. Front Microbiol (2011) 2:269. doi:10.3389/fmicb.2011.00269
63. Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, et al. Influenza. Nat Rev Dis Primers (2018) 4:3. doi:10.1038/s41572-018-0002-y
64. Bourouiba L, Dehandschoewercker E, Bush JWM. Violent expiratory events: on coughing and sneezing. J Fluid Mech (2014) 745:537-63. doi:10.1017/jfm.2014.88
65. McCullers JA. The role of punctuated evolution in the pathogenicity of influenza viruses. Microbiol Spectr (2016) 4. doi:10.1128/microbiolspec. EI10-0001-2015
66. Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS. Kinetics of influenza A virus infection in humans. J Virol (2006) 80:7590-9. doi:10.1128/JVI.01623-05
67. Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev (2011) 24:210-29. doi:10.1128/CMR.00014-10
68. Braciale TJ, Sun J, Kim TS. Regulating the adaptive immune response to respiratory virus infection. Nat Rev Immunol (2012) 12:295-305. doi:10.1038/nri3166
69. Herold S, Becker C, Ridge KM, Budinger GR. Influenza virus-induced lung injury: pathogenesis and implications for treatment. Eur Respir J (2015) 45:1463-78. doi:10.1183/09031936.00186214
70. Sanders CJ, Doherty PC, Thomas PG. Respiratory epithelial cells in innate immunity to influenza virus infection. Cell Tissue Res (2011) 343:13-21. doi:10.1007/s00441-010-1043-z
71. Reiss TF, Gruenert DC, Nadel JA, Jacoby DB. Infection of cultured human airway epithelial cells by influenza A virus. Life Sci (1991) 49:1173-81. doi:10.1016/0024-3205(91)90565-S
72. Doherty PC, Turner SJ, Webby RG, Thomas PG. Influenza and the challenge for immunology. Nat Immunol (2006) 7:449-55. doi:10.1038/ni1343
73. Uetani K, Hiroi M, Meguro T, Ogawa H, Kamisako T, Ohmori Y, et al. Influenza A virus abrogates IFN-gamma response in respiratory epithelial cells by disruption of the Jak/Stat pathway. Eur J Immunol (2008) 38:1559-73. doi:10.1002/eji.200737045
74. Schultz-Cherry S, Hinshaw VS. Influenza virus neuraminidase activates latent transforming growth factor beta. J Virol (1996) 70:8624-9
75. Denney L, Branchett W, Gregory LG, Oliver RA, Lloyd CM. Epithelial-derived TGF-beta1 acts as a pro-viral factor in the lung during influenza A infection. Mucosal Immunol (2018) 11:523-35. doi:10.1038/mi.2017.77
76. van der Sluijs KF, van Elden LJ, Nijhuis M, Schuurman R, Pater JM, Florquin S, et al. IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J Immunol (2004) 172:7603-9. doi:10.4049/jimmunol.172.12.7603
77. Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN, Smith DE, et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol (2011) 12:631-8. doi:10.1038/ni.2045
78. Iwasaki A, Pillai PS. Innate immunity to influenza virus infection. Nat Rev Immunol (2014) 14:315-28. doi:10.1038/nri3665
79. Liu Q, Zhou YH, Yang ZQ. The cytokine storm of severe influenza and development of immunomodulatory therapy. Cell Mol Immunol (2016) 13:3-10. doi:10.1038/cmi.2015.74
80. Waithman J, Mintern JD. Dendritic cells and influenza A virus infection. Virulence (2012) 3:603-8. doi:10.4161/viru.21864
81. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol (2013) 191:1250-9. doi:10.4049/jimmunol.1300014
82. Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med (2008) 14:558-64. doi:10.1038/nm1765
83. Tate MD, Deng YM, Jones JE, Anderson GP, Brooks AG, Reading PC. Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J Immunol (2009) 183:7441-50. doi:10.4049/jimmunol.0902497
84. Thomas PG, Keating R, Hulse-Post DJ, Doherty PC. Cell-mediated protection in influenza infection. Emerg Infect Dis (2006) 12:48-54. doi:10.3201/eid1201.051237
85. Hufford MM, Kim TS, Sun J, Braciale TJ. The effector T cell response to influenza infection. Curr Top Microbiol Immunol (2015) 386:423-55. doi:10.1007/82_2014_397
86. Schultz-Cherry S. Role of NK cells in influenza infection. Curr Top Microbiol Immunol (2015) 386:109-20. doi:10.1007/82_2014_403
87. Centers for Disease Control and Prevention (CDC). Swine influenza A (H1N1) infection in two children-Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep (2009) 58:400-2
88. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature (2009) 459:1122-5. doi:10.1038/nature08182
89. Puzelli S, Facchini M, De Marco MA, Palmieri A, Spagnolo D, Boros S, et al. Molecular surveillance of pandemic influenza A(H1N1) viruses circulating in Italy from May 2009 to February 2010: association between haemagglutinin mutations and clinical outcome. Euro Surveill (2010) 15
90. Hurt AC, Chotpitayasunondh T, Cox NJ, Daniels R, Fry AM, Gubareva LV, et al. Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lancet Infect Dis (2012) 12:240-8. doi:10.1016/S1473-3099(11)70318-8
91. Karageorgopoulos DE, Vouloumanou EK, Korbila IP, Kapaskelis A, Falagas ME. Age distribution of cases of 2009 (H1N1) pandemic influenza in comparison with seasonal influenza. PLoS One (2011) 6:e21690. doi:10.1371/journal.pone.0021690
92. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med (2009) 361:1945-52. doi:10.1056/NEJMoa0906453
93. Van Kerkhove MD, Hirve S, Koukounari A, Mounts AW; H1N1pdm Serology Working Group. Estimating age-specific cumulative incidence for the 2009 influenza pandemic: a meta-analysis of A(H1N1)pdm09 serological studies from 19 countries. Influenza Other Respi Viruses (2013) 7:872-86. doi:10.1111/irv.12074
94. WHO. Weekly Epidemiological Record. (2009). Available from: http://www.who.int/wer/2009/en/
95. CDC. Clinical Signs and Symptoms of Influenza. (2009). Available from: https://www.cdc.gov/flu/pastseasons/0910season.htm
96. Reed C, Chaves SS, Perez A, D'Mello T, Daily Kirley P, Aragon D, et al. Complications among adults hospitalized with influenza: a comparison of seasonal influenza and the 2009 H1N1 pandemic. Clin Infect Dis (2014) 59:166-74. doi:10.1093/cid/ciu285
97. Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM, Kroneman M, et al. Global mortality estimates for the 2009 Influenza Pandemic from the GLaMOR project: a modeling study. PLoS Med (2013) 10:e1001558. doi:10.1371/journal.pmed.1001558
98. Fowlkes AL, Arguin P, BiggerstaffMS, Gindler J, Blau D, Jain S, et al. Epidemiology of 2009 pandemic influenza A (H1N1) deaths in the United States, April-July 2009. Clin Infect Dis (2011) 52(Suppl 1):S60-8. doi:10.1093/cid/ciq022
99. Viboud C, Miller M, Olson D, Osterholm M, Simonsen L. Preliminary estimates of mortality and years of life lost associated with the 2009 A/H1N1 pandemic in the US and comparison with past influenza seasons. PLoS Curr (2010) 2:RRN1153. doi:10.1371/currents. RRN1153
100. Vaillant L, La Ruche G, Tarantola A, Barboza P; V. S. Epidemic Intelligence Team. Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009. Euro Surveill (2009) 14. doi:10.2807/ese.14.33.19309-en
101. Writing Committee of the WHO Consultation on Clinical Aspects of Pandemic (H1N1) 2009 Influenza, Bautista T, Chotpitayasunondh Z, Gao S, Harper A, Shaw M, et al. Clinical aspects of pandemic 2009 influenza A (H1N1) virus infection. N Engl J Med (2010) 362:1708-19. doi:10.1056/NEJMra1000449
102. Van Kerkhove MD, Vandemaele KA, Shinde V, Jaramillo-Gutierrez G, Koukounari A, Donnelly CA, et al. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis. PLoS Med (2011) 8:e1001053. doi:10.1371/journal.pmed.1001053
103. Rothberg MB, Haessler SD. Complications of seasonal and pandemic influenza. Crit Care Med (2010) 38:e91-7. doi:10.1097/CCM.0b013e3181c92eeb
104. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, et al. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med (2009) 361:1935-44. doi:10.1056/NEJMoa0906695
105. Bramley AM, Dasgupta S, Skarbinski J, Kamimoto L, Fry AM, Finelli L, et al. Intensive care unit patients with 2009 pandemic influenza A (H1N1pdm09) virus infection-United States, 2009. Influenza Other Respi Viruses (2012) 6:e134-42. doi:10.1111/j.1750-2659.2012.00385.x
106. Diaz E, Rodriguez A, Martin-Loeches I, Lorente L, Del Mar Martin M, Pozo JC, et al. Impact of obesity in patients infected with 2009 influenza A(H1N1). Chest (2011) 139:382-6. doi:10.1378/chest.10-1160
107. Cullen G, Martin J, O'Donnell J, Boland M, Canny M, Keane E, et al. Surveillance of the first 205 confirmed hospitalised cases of pandemic H1N1 influenza in Ireland, 28 April-3 October 2009. Euro Surveill (2009) 14
108. Park YB, Kim C, Hwang YI, Lee CL, Lee WY, Park HY, et al. Asthma and severity of the 2009 novel H1N1 influenza: a case-control study. J Asthma (2014) 51:69-74. doi:10.3109/02770903.2013.838257
109. Szabo SM, Levy AR, Gooch KL, Bradt P, Wijaya H, Mitchell I. Elevated risk of asthma after hospitalization for respiratory syncytial virus infection in infancy. Paediatr Respir Rev (2013) 13(Suppl 2):S9-15. doi:10.1016/S1526-0542(12)70161-6
110. Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med (2008) 178:667-72. doi:10.1164/rccm.200802-309OC
111. Bergman H, Livornese LL Jr, Sambhara S, Santoro J, Dessain SK. Patients hospitalized with pH1N1 influenza in an Academic Community Medical Center. Open Respir Med J (2011) 5:19-23. doi:10.2174/1874306401105010019
112. Tran D, Vaudry W, Moore DL, Bettinger JA, Halperin SA, Scheifele DW, et al. Comparison of children hospitalized with seasonal versus pandemic influenza A, 2004-2009. Pediatrics (2012) 130:397-406. doi:10.1542/peds.2011-3216
113. Louie JK, Acosta M, Samuel MC, Schechter R, Vugia DJ, Harriman K, et al. A novel risk factor for a novel virus: obesity and 2009 pandemic influenza A (H1N1). Clin Infect Dis (2011) 52:301-12. doi:10.1093/cid/ciq152
114. Skarbinski J, Jain S, Bramley A, Lee EJ, Huang J, Kirschke D, et al. Hospitalized patients with 2009 pandemic influenza A (H1N1) virus infection in the United States-September-October 2009. Clin Infect Dis (2011) 52(Suppl 1):S50-9. doi:10.1093/cid/ciq021
115. Eriksson CO, Graham DA, Uyeki TM, Randolph AG. Risk factors for mechanical ventilation in U.S. children hospitalized with seasonal influenza and 2009 pandemic influenza A*. Pediatr Crit Care Med (2012) 13:625-31. doi:10.1097/PCC.0b013e318260114e
116. Jouvet P, Hutchison J, Pinto R, Menon K, Rodin R, Choong K, et al. Critical illness in children with influenza A/pH1N1 2009 infection in Canada. Pediatr Crit Care Med (2010) 11:603-9. doi:10.1097/PCC.0b013e3181d9c80b
117. O'Riordan S, Barton M, Yau Y, Read SE, Allen U. Risk factors and outcomes among children admitted to hospital with pandemic H1N1 influenza. Can Med Assoc J (2010) 182:39-44. doi:10.1503/cmaj.091724
118. Song X, DeBiasi RL, Campos JM, Fagbuyi DB, Jacobs BR, Singh N. Comparison of pandemic and seasonal influenza A infections in pediatric patients: were they different? Influenza Other Respi Viruses (2012) 6:25-7. doi:10.1111/j.1750-2659.2011.00258.x
119. von der Beck D, Seeger W, Herold S, Gunther A, Loh B. Characteristics and outcomes of a cohort hospitalized for pandemic and seasonal influenza in Germany based on nationwide inpatient data. PLoS One (2017) 12:e0180920. doi:10.1371/journal.pone.0180920
120. Dawood FS, Kamimoto L, D'Mello TA, Reingold A, Gershman K, Meek J, et al. Children with asthma hospitalized with seasonal or pandemic influenza, 2003-2009. Pediatrics (2011) 128:e27-32. doi:10.1542/peds.2010-3343
121. Santillan Salas CF, Mehra S, Pardo Crespo MR, Juhn YJ. Asthma and severity of 2009 novel H1N1 influenza: a population-based case-control study. J Asthma (2013) 50:1069-76. doi:10.3109/02770903.2013.834505
122. Garten R, Blanton L, Elal AIA, Alabi N, Barnes J, BiggerstaffM, et al. Update: influenza activity in the United States during the 2017-18 season and composition of the 2018-19 influenza vaccine. MMWR Morb Mortal Wkly Rep (2018) 67:634-42. doi:10.15585/mmwr.mm6722a4
123. Santa-Olalla P, Cortes-Garcia M, Vicente-Herrero M, Castrillo-Villamandos C, Arias-Bohigas P, Pachon-del Amo I, et al. Risk factors for disease severity among hospitalised patients with 2009 pandemic influenza A (H1N1) in Spain, April-December 2009. Euro Surveill (2010) 15(38):19667
124. Gilca R, De Serres G, Boulianne N, Ouhoummane N, Papenburg J, Douville-Fradet M, et al. Risk factors for hospitalization and severe outcomes of 2009 pandemic H1N1 influenza in Quebec, Canada. Influenza Other Respi Viruses (2011) 5:247-55. doi:10.1111/j.1750-2659.2011.00204.x
125. Torres SF, Iolster T, Schnitzler EJ, Farias JA, Bordogna AC, Rufach D, et al. High mortality in patients with influenza A pH1N1 2009 admitted to a pediatric intensive care unit: a predictive model of mortality. Pediatr Crit Care Med (2012) 13:e78-83. doi:10.1097/PCC.0b013e318219266b
126. Koshio N, Hasegawa T, Suzuki K, Tanabe Y, Koya T, Sakagami T, et al. Analysis of the influenza A (H1N1) 2009 pandemic infection in Japanese asthmatic patients: using a questionnaire-based survey. Allergol Int (2014) 63:67-74. doi:10.2332/allergolint.13-OA-0609
127. Thomson NC, Chaudhuri R, Livingston E. Asthma and cigarette smoking. Eur Respir J (2004) 24:822-33. doi:10.1183/09031936.04.00039004
128. Kang MJ, Lee CG, Lee JY, Dela Cruz CS, Chen ZJ, Enelow R, et al. Cigarette smoke selectively enhances viral PAMP-and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest (2008) 118:2771-84. doi:10.1172/JCI32709
129. Louie JK, Gavali S, Acosta M, Samuel MC, Winter K, Jean C, et al. Children hospitalized with 2009 novel influenza A(H1N1) in California. Arch Pediatr Adolesc Med (2010) 164:1023-31. doi:10.1001/archpediatrics.2010.203
130. Myles P, Nguyen-Van-Tam JS, Semple MG, Brett SJ, Bannister B, Read RC, et al. Differences between asthmatics and nonasthmatics hospitalised with influenza A infection. Eur Respir J (2013) 41:824-31. doi:10.1183/09031936.00015512
131. Sutherland TJT, Cowan JO, Young S, Goulding A, Grant AM, Williamson A, et al. The association between obesity and asthma-interactions between systemic and airway inflammation. Am J Respir Crit Care Med (2008) 178:469-75. doi:10.1164/rccm.200802-301OC
132. Heinonen MT, Laine AP, Soderhall C, Gruzieva O, Rautio S, Melen E, et al. GIMAP GTPase family genes: potential modifiers in autoimmune diabetes, asthma, and allergy. J Immunol (2015) 194:5885-94. doi:10.4049/jimmunol.1500016
133. Appleton SL, Ruffin RE, Wilson DH, Taylor AW, Adams RJ; T. North West Adelaide Cohort Health Study. Cardiovascular disease risk associated with asthma and respiratory morbidity might be mediated by short-acting beta2-agonists. J Allergy Clin Immunol (2009) 123:124-30.e1. doi:10.1016/j.jaci.2008.10.032
134. Kloepfer KM, Olenec JP, Lee WM, Liu G, Vrtis RF, Roberg KA, et al. Increased H1N1 infection rate in children with asthma. Am J Respir Crit Care Med (2012) 185:1275-9. doi:10.1164/rccm.201109-1635OC
135. Hasegawa S, Hirano R, Hashimoto K, Haneda Y, Shirabe K, Ichiyama T. Characteristics of atopic children with pandemic H1N1 influenza viral infection: pandemic H1N1 influenza reveals 'occult' asthma of childhood. Pediatr Allergy Immunol (2011) 22:e119-23. doi:10.1111/j.1399-3038.2010.01090.x
136. McKenna JJ, Bramley AM, Skarbinski J, Fry AM, Finelli L, Jain S, et al. Asthma in patients hospitalized with pandemic influenza A(H1N1)pdm09 virus infection-United States, 2009. BMC Infect Dis (2013) 13:57. doi:10.1186/1471-2334-13-57
137. Kloepfer KM, Gern JE. Virus/allergen interactions and exacerbations of asthma. Immunol Allergy Clin North Am (2010) 30:553-563,vii. doi:10.1016/j.iac.2010.08.002
138. Poulakou G, Souto J, Balcells J, Perez M, Laborda C, Roca O, et al. First influenza season after the 2009 pandemic influenza: characteristics of intensive care unit admissions in adults and children in Vall d'Hebron Hospital. Clin Microbiol Infect (2012) 18:374-80. doi:10.1111/j.1469-0691.2011.03617.x
139. Samarasinghe AE, Woolard SN, Boyd KL, Hoselton SA, Schuh JM, McCullers JA. The immune profile associated with acute allergic asthma accelerates clearance of influenza virus. Immunol Cell Biol (2014) 92:449-59. doi:10.1038/icb.2013.113
140. Kusznierz G, Uboldi A, Sosa G, Torales S, Colombo J, Moyano C, et al. Clinical features of the hospitalized patients with 2009 pandemic influenza A (H1N1) in Santa Fe, Argentina. Influenza Other Respir Viruses (2013) 7:410-7. doi:10.1111/j.1750-2659.2012.00405.x
141. Louie JK, Acosta M, Winter K, Jean C, Gavali S, Schechter R, et al. Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA (2009) 302:1896-902. doi:10.1001/jama.2009.1583
142. Nguyen-Van-Tam JS, Openshaw PJ, Hashim A, Gadd EM, Lim WS, Semple MG, et al. Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May-September 2009). Thorax (2010) 65:645-51. doi:10.1136/thx.2010.135210
143. Myles PR, Semple MG, Lim WS, Openshaw PJ, Gadd EM, Read RC, 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 (2012) 67:709-17. doi:10.1136/thoraxjnl-2011-200266
144. Brun-Buisson C, Richard JC, Mercat A, Thiebaut AC, Brochard L; REVA-SRLF A/H1N1v 2009 Registry Group. Early corticosteroids in severe influenza A/H1N1 pneumonia and acute respiratory distress syndrome. Am J Respir Crit Care Med (2011) 183:1200-6. doi:10.1164/rccm.201101-0135OC
145. Yang JW, Fan LC, Miao XY, Mao B, Li MH, Lu HW, et al. Corticosteroids for the treatment of human infection with influenza virus: a systematic review and meta-analysis. Clin Microbiol Infect (2015) 21:956-63. doi:10.1016/j.cmi.2015.06.022
146. Zhang Y, Sun WJ, Svendsen ER, Tang S, MacIntyre RC, Yang P, et al. Do corticosteroids reduce the mortality of influenza A (H1N1) infection? A meta-analysis. Crit Care (2015) 19:46. doi:10.1186/s13054-015-0764-5
147. Zarychanski R, Stuart TL, Kumar A, Doucette S, Elliott L, Kettner J, et al. Correlates of severe disease in patients with 2009 pandemic influenza (H1N1) virus infection. CMAJ (2010) 182:257-64. doi:10.1503/cmaj.091884
148. CDC. FluVaxView Interactive. CDC. Available from: https://www.cdc.gov/flu/fluvaxview/reportshtml/trends/index.html
149. Atkins CY, Patel A, Taylor TH, BiggerstaffM, Merlin TL, Dulin SM, et al. Estimating effect of antiviral drug use during pandemic (H1N1) 2009 outbreak, United States. Emerg Infect Dis (2011) 17:1591-8. doi:10.3201/eid1709.110295
150. Oshansky CM, Gartland AJ, Wong SS, Jeevan T, Wang D, Roddam PL, et al. Mucosal immune responses predict clinical outcomes during influenza infection independently of age and viral load. Am J Respir Crit Care Med (2014) 189:449-62. doi:10.1164/rccm.201309-1616OC
151. Obuchi M, Adachi Y, Takizawa T, Sata T. Influenza A(H1N1)pdm09 virus and asthma. Front Microbiol (2013) 4:307. doi:10.3389/fmicb.2013.00307
152. Takano T, Tajiri H, Kashiwagi Y, Kimura S, Kawashima H. Cytokine and chemokine response in children with the 2009 pandemic influenza A (H1N1) virus infection. Eur J Clin Microbiol Infect Dis (2011) 30:117-20. doi:10.1007/s10096-010-1041-9
153. Zarnegar B, Mendez-Enriquez E, Westin A, Soderberg C, Dahlin JS, Gronvik KO, et al. Influenza infection in mice induces accumulation of lung mast cells through the recruitment and maturation of mast cell progenitors. Front Immunol (2017) 8:310. doi:10.3389/fimmu.2017.00310
154. Terai M, Honda T, Yamamoto S, Yoshida M, Tsuchiya N, Moriyama Y, et al. Early induction of interleukin-5 and peripheral eosinophilia in acute pneumonia in Japanese children infected by pandemic 2009 influenza A in the Tokyo area. Microbiol Immunol (2011) 55:341-6. doi:10.1111/j.1348-0421.2011.00320.x
155. Shiraishi Y, Asano K, Niimi K, Fukunaga K, Wakaki M, Kagyo J, et al. Cyclooxygenase-2/prostaglandin D2/CRTH2 pathway mediates double-stranded RNA-induced enhancement of allergic airway inflammation. J Immunol (2008) 180:541-9. doi:10.4049/jimmunol.180.1.541
156. Torres D, Dieudonne A, Ryffel B, Vilain E, Si-Tahar M, Pichavant M, et al. Double-stranded RNA exacerbates pulmonary allergic reaction through TLR3: implication of airway epithelium and dendritic cells. J Immunol (2010) 185:451-9. doi:10.4049/jimmunol.0902833
157. Takayama S, Tamoaoka M, Takayama K, Okayasu K, Tsuchiya K, Miyazaki Y, et al. Synthetic double-stranded RNA enhances airway inflammation and remodeling in a rat model of asthma. Immunology (2011) 134:140-50. doi:10.1111/j.1365-2567.2011.03473.x
158. Furuya Y, Roberts S, Hurteau GJ, Sanfilippo AM, Racine R, Metzger DW. Asthma increases susceptibility to heterologous but not homologous secondary influenza. J Virol (2014) 88:9166-81. doi:10.1128/JVI.00265-14
159. Kim HS, Lee H, Kim HS, Won S, Lee EK, Bang K, et al. Effect of influenza virus infection in a murine model of asthma. Iran J Allergy Asthma Immunol (2015) 14:392-401
160. Lee DCP, Tay NQ, Thian M, Prabhu N, Furuhashi K, Kemeny DM. Prior exposure to inhaled allergen enhances anti-viral immunity and T cell priming by dendritic cells. PLoS One (2018) 13:e0190063. doi:10.1371/journal.pone.0190063
161. Ishikawa H, Sasaki H, Fukui T, Fujita K, Kutsukake E, Matsumoto T. 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 (2012) 32:256-67. doi:10.1007/s10875-011-9619-2
162. Kawaguchi A, Suzuki T, Ohara Y, Takahashi K, Sato Y, Ainai A, et al. Impacts of allergic airway inflammation on lung pathology in a mouse model of influenza A virus infection. PLoS One (2017) 12:e0173008. doi:10.1371/journal.pone.0173008
163. Furuya Y, Furuya AK, Roberts S, Sanfilippo AM, Salmon SL, Metzger DW. Prevention of influenza virus-induced immunopathology by TGF-beta produced during allergic asthma. PLoS Pathog (2015) 11:e1005180. doi:10.1371/journal.ppat.1005180
164. Makinde T, Murphy RF, Agrawal DK. The regulatory role of TGF-beta in airway remodeling in asthma. Immunol Cell Biol (2007) 85:348-56. doi:10.1038/sj.icb.7100044
165. Wang SM, Tsai MH, Lei HY, Wang JR, Liu CC. The regulatory T cells in anti-influenza antibody response post influenza vaccination. Hum Vaccin Immunother (2012) 8:1243-9. doi:10.4161/hv.21117
166. Leon B, Bradley JE, Lund FE, Randall TD, Ballesteros-Tato A. FoxP3+ regulatory T cells promote influenza-specific Tfh responses by controlling IL-2 availability. Nat Commun (2014) 5:3495. doi:10.1038/ncomms4495
167. Samarasinghe AE, Melo RC, Duan S, LeMessurier KS, Liedmann S, Surman SL, et al. Eosinophils promote antiviral immunity in mice infected with influenza A virus. J Immunol (2017) 198:3214-26. doi:10.4049/jimmunol.1600787
168. Lim K, Hyun YM, Lambert-Emo K, Capece T, Bae S, Miller R, et al. Neutrophil trails guide influenza-specific CD8(+) T cells in the airways. Science (2015) 349:aaa4352. doi:10.1126/science.aaa4352
169. Lloyd CM, Hessel EM. Functions of T cells in asthma: more than just T(H)2 cells. Nat Rev Immunol (2010) 10:838-48. doi:10.1038/nri2870
170. Doorley LA, LeMessurier KS, Iverson AR, Palipane M, Samarasinghe AE. Humoral immune responses during asthma and influenza co-morbidity in mice. Immunobiology (2017) 222(12):1064-73. doi:10.1016/j.imbio.2017.08.002
171. Lloyd CM. Building better mouse models of asthma. Curr Allergy Asthma Rep (2007) 7:231-6. doi:10.1007/s11882-007-0077-0
172. Caliskan M, Bochkov YA, Kreiner-Moller E, Bonnelykke K, Stein MM, Du G, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med (2013) 368:1398-407. doi:10.1056/NEJMoa1211592
173. Song DJ, Miller M, Beppu A, Rosenthal P, Das S, Karta M, et al. Rhinovirus infection of ORMDL3 transgenic mice is associated with reduced rhinovirus viral load and airway inflammation. J Immunol (2017) 199:2215-24. doi:10.4049/jimmunol.1601412
174. Kelly JT, Busse WW. Host immune responses to rhinovirus: mechanisms in asthma. J Allergy Clin Immunol (2008) 122:671-682; quiz 683-674. doi:10.1016/j.jaci.2008.08.013
175. Varner AE. The increase in allergic respiratory diseases: survival of the fittest? Chest (2002) 121:1308-16. doi:10.1378/chest.121.4.1308