Susceptibility to Rhinovirus-induced Early Wheezing as a Risk Factor for Subsequent Asthma Development

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Abstract

Rhinovirus is one of the two most common viral agents that cause bronchiolitis in young children. During the first 12 months, it is second to the respiratory syncytial virus, but after 12 months, it begins dominating the statistics. Wheezing and dry cough are typical clinical symptoms indicative of rhinovirus-induced bronchiolitis, although overlap of symptoms with other virus infections is common. Several studies have shown that atopic predisposition and reduced interferon responses increase susceptibility to rhinovirus-induced wheezing. More recent studies have found that certain genetic variations at strong asthma loci also increase susceptibility. Rhinovirus-induced wheezing in the early years of life is known to increase the risk of subsequent asthma development and may be associated with airway remodeling. This risk is increased by aeroallergen sensitization. Currently, there are no clinically approved preventive treatments for asthma. However, studies show promising results indicating that children with rhinovirus-affected first-time wheezing respond to bronchodilators in terms of less short-term symptoms and that controlling airway inflammatory responses with anti-inflammatory medication may markedly decrease asthma development. Also, enhancing resistance to respiratory viruses has been a topic of discussion. Primary and secondary prevention strategies are being developed with the aim of decreasing the incidence of asthma. Here, we review the current knowledge on rhinovirus-induced early wheezing as a risk factor for subsequent asthma development and related asthma-prevention strategies.

Keywords: Asthma, rhinovirus, polymorphism, corticosteroid, bronchiolitis, tachypnea.

Graphical Abstract

[1]
Masoli M, Fabian D, Holt S, Beasley R. Global Initiative for Asthma (GINA) Program. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 2004; 59(5): 469-78.
[http://dx.doi.org/10.1111/j.1398-9995.2004.00526.x] [PMID: 15080825]
[2]
Stein MM, Hrusch CL, Gozdz J, et al. Innate immunity and asthma risk in amish and hutterite farm children. N Engl J Med 2016; 375(5): 411-21.
[http://dx.doi.org/10.1056/NEJMoa1508749] [PMID: 27518660]
[3]
Tiotiu AI, Novakova P, Nedeva D, et al. Impact of air pollution on asthma outcomes. Int J Environ Res Public Health 2020; 17(17): 6212.
[http://dx.doi.org/10.3390/ijerph17176212] [PMID: 32867076]
[4]
Rubner FJ, Jackson DJ, Evans MD, et al. Early life rhinovirus wheezing, allergic sensitization, and asthma risk at adolescence. J Allergy Clin Immunol 2017; 139(2): 501-7.
[http://dx.doi.org/10.1016/j.jaci.2016.03.049] [PMID: 27312820]
[5]
Jartti T, Gern JE. Role of viral infections in the development and exacerbation of asthma in children. J Allergy Clin Immunol 2017; 140(4): 895-906.
[http://dx.doi.org/10.1016/j.jaci.2017.08.003] [PMID: 28987219]
[6]
Calışkan M, Bochkov YA, Kreiner-Møller E, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med 2013; 368(15): 1398-407.
[http://dx.doi.org/10.1056/NEJMoa1211592] [PMID: 23534543]
[7]
Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 2008; 178(7): 667-72.
[http://dx.doi.org/10.1164/rccm.200802-309OC] [PMID: 18565953]
[8]
Wark PA, Johnston SL, Bucchieri F, et al. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med 2005; 201(6): 937-47.
[http://dx.doi.org/10.1084/jem.20041901] [PMID: 15781584]
[9]
Lehtinen P, Ruohola A, Vanto T, Vuorinen T, Ruuskanen O, Jartti T. Prednisolone reduces recurrent wheezing after a first wheezing episode associated with rhinovirus infection or eczema. J Allergy Clin Immunol 2007; 119(3): 570-5.
[http://dx.doi.org/10.1016/j.jaci.2006.11.003] [PMID: 17196244]
[10]
Lukkarinen M, Lukkarinen H, Lehtinen P, Vuorinen T, Ruuskanen O, Jartti T. Prednisolone reduces recurrent wheezing after first rhinovirus wheeze: a 7-year follow-up. Pediatr Allergy Immunol 2013; 24(3): 237-43.
[http://dx.doi.org/10.1111/pai.12046] [PMID: 23373881]
[11]
Beale J, Jayaraman A, Jackson DJ, et al. Rhinovirus-induced IL-25 in asthma exacerbation drives type 2 immunity and allergic pulmonary inflammation. Sci Transl Med 2014; 6(256): 256ra134.
[http://dx.doi.org/10.1126/scitranslmed.3009124] [PMID: 25273095]
[12]
Kennedy JL, Koziol-White CJ, Jeffus S, et al. Effects of rhinovirus 39 infection on airway hyperresponsiveness to carbachol in human airways precision cut lung slices. J Allergy Clin Immunol 2018; 141(5): 1887-1890.e1.
[http://dx.doi.org/10.1016/j.jaci.2017.11.041] [PMID: 29317243]
[13]
Jartti T, Smits HH, Bønnelykke K, et al. Bronchiolitis needs a revisit: distinguishing between virus entities and their treatments. Allergy 2019; 74(1): 40-52.
[http://dx.doi.org/10.1111/all.13624] [PMID: 30276826]
[14]
Ralston SL, Lieberthal AS, Meissner HC, et al. Clinical practice guideline: the diagnosis, management, and prevention of bronchiolitis. Pediatrics 2014; 134(5): e1474-502.
[http://dx.doi.org/10.1542/peds.2014-2742] [PMID: 25349312]
[15]
Meissner HC. Viral bronchiolitis in children. N Engl J Med 2016; 374(1): 62-72.
[http://dx.doi.org/10.1056/NEJMra1413456] [PMID: 26735994]
[16]
National Asthma Education and Prevention Program. US Department of Health and Human Services; Bethesda: 2007. National Heart, Lung, and Blood Institute, National Institutes of Health. Expert panel report 3: guidelines for the diagnosis and management of asthma. 2007.
[17]
Bush A, Saglani S. Medical algorithm: diagnosis and treatment of preschool asthma. Allergy 2020; 75(10): 2711-2.
[http://dx.doi.org/10.1111/all.14172] [PMID: 31898808]
[18]
Johansson SG, Hourihane JO, Bousquet J, et al. A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 2001; 56(9): 813-24.
[http://dx.doi.org/10.1034/j.1398-9995.2001.t01-1-00001.x] [PMID: 11551246]
[19]
Heinzerling LM, Burbach GJ, Edenharter G, et al. GA(2)LEN skin test study I: GA(2)LEN harmonization of skin prick testing: novel sensitization patterns for inhalant allergens in Europe. Allergy 2009; 64(10): 1498-506.
[http://dx.doi.org/10.1111/j.1398-9995.2009.02093.x] [PMID: 19772515]
[20]
Serebrisky D, Wiznia A. Pediatric asthma: a global epidemic. Ann Glob Health 2019; 85(1): 6.
[http://dx.doi.org/10.5334/aogh.2416] [PMID: 30741507]
[21]
Taussig LM, Wright AL, Holberg CJ, Halonen M, Morgan WJ, Martinez FD. Tucson children’s respiratory study: 1980 to present. J Allergy Clin Immunol 2003; 111(4): 661-75.
[http://dx.doi.org/10.1067/mai.2003.162] [PMID: 12704342]
[22]
Lai CK, Beasley R, Crane J, Foliaki S, Shah J, Weiland S. Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 2009; 64(6): 476-83.
[http://dx.doi.org/10.1136/thx.2008.106609] [PMID: 19237391]
[23]
Turunen R, Koistinen A, Vuorinen T, et al. The first wheezing episode: respiratory virus etiology, atopic characteristics, and illness severity. Pediatr Allergy Immunol 2014; 25(8): 796-803.
[http://dx.doi.org/10.1111/pai.12318] [PMID: 25444257]
[24]
Bochkov YA, Grindle K, Vang F, Evans MD, Gern JE. Improved molecular typing assay for rhinovirus species A, B, and C. J Clin Microbiol 2014; 52(7): 2461-71.
[http://dx.doi.org/10.1128/JCM.00075-14] [PMID: 24789198]
[25]
McIntyre CL, Knowles NJ, Simmonds P. Proposals for the classification of human rhinovirus species A, B and C into genotypically assigned types. J Gen Virol 2013; 94(Pt 8): 1791-806.
[http://dx.doi.org/10.1099/vir.0.053686-0] [PMID: 23677786]
[26]
Simmonds P, McIntyre C, Savolainen-Kopra C, Tapparel C, Mackay IM, Hovi T. Proposals for the classification of human rhinovirus species C into genotypically assigned types. J Gen Virol 2010; 91(Pt 10): 2409-19.
[http://dx.doi.org/10.1099/vir.0.023994-0] [PMID: 20610666]
[27]
Turunen R, Jartti T, Bochkov YA, Gern JE, Vuorinen T. Rhinovirus species and clinical characteristics in the first wheezing episode in children. J Med Virol 2016; 88(12): 2059-68.
[http://dx.doi.org/10.1002/jmv.24587] [PMID: 27232888]
[28]
Erkkola R, Turunen R, Räisänen K, et al. Rhinovirus C is associated with severe wheezing and febrile respiratory illness in young children. Pediatr Infect Dis J 2020; 39(4): 283-6.
[http://dx.doi.org/10.1097/INF.0000000000002570] [PMID: 31876616]
[29]
Zhang N, Wang L, Deng X, et al. Recent advances in the detection of respiratory virus infection in humans. J Med Virol 2020; 92(4): 408-17.
[http://dx.doi.org/10.1002/jmv.25674] [PMID: 31944312]
[30]
Arden KE, McErlean P, Nissen MD, Sloots TP, Mackay IM. Frequent detection of human rhinoviruses, paramyxoviruses, coronaviruses, and bocavirus during acute respiratory tract infections. J Med Virol 2006; 78(9): 1232-40.
[http://dx.doi.org/10.1002/jmv.20689] [PMID: 16847968]
[31]
Do DH, Laus S, Leber A, et al. A one-step, real-time PCR assay for rapid detection of rhinovirus. J Mol Diagn 2010; 12(1): 102-8.
[http://dx.doi.org/10.2353/jmoldx.2010.090071] [PMID: 19948820]
[32]
Bochkov YA, Palmenberg AC, Lee WM, et al. Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus C. Nat Med 2011; 17(5): 627-32.
[http://dx.doi.org/10.1038/nm.2358] [PMID: 21483405]
[33]
Chen JHK, Lam HY, Yip CCY, et al. Clinical evaluation of the new high-throughput luminex NxTAG respiratory pathogen panel assay for multiplex respiratory pathogen detection. J Clin Microbiol 2016; 54(7): 1820-5.
[http://dx.doi.org/10.1128/JCM.00517-16] [PMID: 27122380]
[34]
Feng ZS, Zhao L, Wang J, et al. A multiplex one-tube nested real time RT-PCR assay for simultaneous detection of respiratory syncytial virus, human rhinovirus and human metapneumovirus. Virol J 2018; 15(1): 167.
[http://dx.doi.org/10.1186/s12985-018-1061-0] [PMID: 30376870]
[35]
Sam SS, Caliendo AM, Ingersoll J, Abdul-Ali D, Hill CE, Kraft CS. Evaluation of performance characteristics of panther fusion assays for detection of respiratory viruses from nasopharyngeal and lower respiratory tract specimens. J Clin Microbiol 2018; 56(8): e00787-18.
[http://dx.doi.org/10.1128/JCM.00787-18] [PMID: 29793965]
[36]
Han M, Chung Y, Young Hong J, et al. Toll-like receptor 2-expressing macrophages are required and sufficient for rhinovirus-induced airway inflammation. J Allergy Clin Immunol 2016; 138(6): 1619-30.
[http://dx.doi.org/10.1016/j.jaci.2016.01.037] [PMID: 27084403]
[37]
Slater L, Bartlett NW, Haas JJ, et al. Co-ordinated role of TLR3, RIG-I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog 2010; 6(11): e1001178.
[http://dx.doi.org/10.1371/journal.ppat.1001178] [PMID: 21079690]
[38]
Bochkov YA, Watters K, Ashraf S, et al. Cadherin-related family member 3, a childhood asthma susceptibility gene product, mediates rhinovirus C binding and replication. Proc Natl Acad Sci USA 2015; 112(17): 5485-90.
[http://dx.doi.org/10.1073/pnas.1421178112] [PMID: 25848009]
[39]
Contoli M, Message SD, Laza-Stanca V, et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 2006; 12(9): 1023-6.
[http://dx.doi.org/10.1038/nm1462] [PMID: 16906156]
[40]
Pang LL, Yuan XH, Shao CS, et al. The suppression of innate immune response by human rhinovirus C. Biochem Biophys Res Commun 2017; 490(1): 22-8.
[http://dx.doi.org/10.1016/j.bbrc.2017.05.169] [PMID: 28576493]
[41]
Licona-Limón P, Kim LK, Palm NW, Flavell RA. TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 2013; 14(6): 536-42.
[http://dx.doi.org/10.1038/ni.2617] [PMID: 23685824]
[42]
Sugita K, Steer CA, Martinez-Gonzalez I, et al. Type 2 innate lymphoid cells disrupt bronchial epithelial barrier integrity by targeting tight junctions through IL-13 in asthmatic patients. J Allergy Clin Immunol 2018; 141(1): 300-310.e11.
[http://dx.doi.org/10.1016/j.jaci.2017.02.038] [PMID: 28392332]
[43]
Celebi Sözener Z, Cevhertas L, Nadeau K, Akdis M, Akdis CA. Environmental factors in epithelial barrier dysfunction. J Allergy Clin Immunol 2020; 145(6): 1517-28.
[http://dx.doi.org/10.1016/j.jaci.2020.04.024] [PMID: 32507229]
[44]
Bønnelykke K, Coleman AT, Evans MD, et al. Cadherin-related family member 3 genetics and rhinovirus C respiratory illnesses. Am J Respir Crit Care Med 2018; 197(5): 589-94.
[http://dx.doi.org/10.1164/rccm.201705-1021OC] [PMID: 29121479]
[45]
Dumas O, Mansbach JM, Jartti T, et al. A clustering approach to identify severe bronchiolitis profiles in children. Thorax 2016; 71(8): 712-8.
[http://dx.doi.org/10.1136/thoraxjnl-2016-208535] [PMID: 27339060]
[46]
Bønnelykke K, Sleiman P, Nielsen K, et al. A genome-wide association study identifies CDHR3 as a susceptibility locus for early childhood asthma with severe exacerbations. Nat Genet 2014; 46(1): 51-5.
[http://dx.doi.org/10.1038/ng.2830] [PMID: 24241537]
[47]
Akdis CA. Does the epithelial barrier hypothesis explain the increase in allergy, autoimmunity and other chronic conditions? Nat Rev Immunol 2021; 21(11): 739-51.
[http://dx.doi.org/10.1038/s41577-021-00538-7] [PMID: 33846604]
[48]
Bisgaard H, Hermansen MN, Buchvald F, et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 2007; 357(15): 1487-95.
[http://dx.doi.org/10.1056/NEJMoa052632] [PMID: 17928596]
[49]
Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science 2016; 352(6285): 539-44.
[http://dx.doi.org/10.1126/science.aad9378] [PMID: 27126036]
[50]
Hasegawa K, Mansbach JM, Ajami NJ, et al. Association of nasopharyngeal microbiota profiles with bronchiolitis severity in infants hospitalised for bronchiolitis. Eur Respir J 2016; 48(5): 1329-39.
[http://dx.doi.org/10.1183/13993003.00152-2016] [PMID: 27799386]
[51]
Stokholm J, Chawes BL, Vissing NH, et al. Azithromycin for episodes with asthma-like symptoms in young children aged 1-3 years: a randomised, double-blind, placebo-controlled trial. Lancet Respir Med 2016; 4(1): 19-26.
[http://dx.doi.org/10.1016/S2213-2600(15)00500-7] [PMID: 26704020]
[52]
Petrarca L, Nenna R, Frassanito A, et al. Acute bronchiolitis: Influence of viral co-infection in infants hospitalized over 12 consecutive epidemic seasons. J Med Virol 2018; 90(4): 631-8.
[http://dx.doi.org/10.1002/jmv.24994] [PMID: 29226974]
[53]
Drajac C, Laubreton D, Riffault S, Descamps D. Pulmonary susceptibility of neonates to respiratory syncytial virus infection: a problem of innate immunity? J Immunol Res 2017; 2017: 8734504.
[http://dx.doi.org/10.1155/2017/8734504] [PMID: 29250560]
[54]
Jartti T, Kuusipalo H, Vuorinen T, et al. Allergic sensitization is associated with rhinovirus-, but not other virus-, induced wheezing in children. Pediatr Allergy Immunol 2010; 21(7): 1008-14.
[http://dx.doi.org/10.1111/j.1399-3038.2010.01059.x] [PMID: 20977499]
[55]
Mansbach JM, Clark S, Teach SJ, et al. Children hospitalized with rhinovirus bronchiolitis have asthma-like characteristics. J Pediatr 2016; 172: 202-4.
[http://dx.doi.org/10.1016/j.jpeds.2016.01.041] [PMID: 26875009]
[56]
Turunen R, Vuorinen T, Bochkov Y, Gern J, Jartti T. Clinical and virus surveillance after the first wheezing episode: special reference to rhinovirus A and C species. Pediatr Infect Dis J 2017; 36(6): 539-44.
[http://dx.doi.org/10.1097/INF.0000000000001495] [PMID: 28027280]
[57]
Spycher BD, Silverman M, Pescatore AM, Beardsmore CS, Kuehni CE. Comparison of phenotypes of childhood wheeze and cough in 2 independent cohorts. J Allergy Clin Immunol 2013; 132(5): 1058-67.
[http://dx.doi.org/10.1016/j.jaci.2013.08.002] [PMID: 24075230]
[58]
Jartti T, Lee WM, Pappas T, Evans M, Lemanske RF Jr, Gern JE. Serial viral infections in infants with recurrent respiratory illnesses. Eur Respir J 2008; 32(2): 314-20.
[http://dx.doi.org/10.1183/09031936.00161907] [PMID: 18448489]
[59]
Copenhaver CC, Gern JE, Li Z, et al. Cytokine response patterns, exposure to viruses, and respiratory infections in the first year of life. Am J Respir Crit Care Med 2004; 170(2): 175-80.
[http://dx.doi.org/10.1164/rccm.200312-1647OC] [PMID: 15087299]
[60]
Bergauer A, Sopel N, Kroß B, et al. IFN-α/IFN-λ responses to respiratory viruses in paediatric asthma. Eur Respir J 2017; 49(2): 1600969.
[http://dx.doi.org/10.1183/13993003.00969-2016] [PMID: 27836955]
[61]
Jayaraman A, Jackson DJ, Message SD, et al. IL-15 complexes induce NK- and T-cell responses independent of type I IFN signaling during rhinovirus infection. Mucosal Immunol 2014; 7(5): 1151-64.
[http://dx.doi.org/10.1038/mi.2014.2] [PMID: 24472849]
[62]
Guilbert TW, Singh AM, Danov Z, Evans MD, Jackson DJ, Burton R. Decreased lung function after preschool wheezing rhinovirus illnesses in children at risk to develop asthma. J Allergy Clin Immunol 2011; 128(3): 532-8-10.
[http://dx.doi.org/10.1016/j.jaci.2011.06.037]
[63]
Loss GJ, Depner M, Hose AJ, et al. The early development of wheeze. environmental determinants and genetic susceptibility at 17q21. Am J Respir Crit Care Med 2016; 193(8): 889-97.
[http://dx.doi.org/10.1164/rccm.201507-1493OC] [PMID: 26575599]
[64]
Stokholm J, Blaser MJ, Thorsen J, et al. Maturation of the gut microbiome and risk of asthma in childhood. Nat Commun 2018; 9(1): 141.
[http://dx.doi.org/10.1038/s41467-017-02573-2] [PMID: 29321519]
[65]
Koistinen A, Lukkarinen M, Turunen R, et al. Prednisolone for the first rhinovirus-induced wheezing and 4-year asthma risk: a randomized trial. Pediatr Allergy Immunol 2017; 28(6): 557-63.
[http://dx.doi.org/10.1111/pai.12749] [PMID: 28660720]
[66]
Del Giacco SR, Bakirtas A, Bel E, et al. Allergy in severe asthma. Allergy 2017; 72(2): 207-20.
[http://dx.doi.org/10.1111/all.13072] [PMID: 27775836]
[67]
Bergroth E, Aakula M, Elenius V, et al. Rhinovirus type in severe bronchiolitis and the development of asthma. J Allergy Clin Immunol Pract 2020; 8(2): 588-95.
[http://dx.doi.org/10.1016/j.jaip.2019.08.043] [PMID: 31520837]
[68]
Lukkarinen M, Koistinen A, Turunen R, Lehtinen P, Vuorinen T, Jartti T. Rhinovirus-induced first wheezing episode predicts atopic but not nonatopic asthma at school age. J Allergy Clin Immunol 2017; 140(4): 988-95.
[http://dx.doi.org/10.1016/j.jaci.2016.12.991] [PMID: 28347734]
[69]
Florin TA, Plint AC, Zorc JJ. Viral bronchiolitis. Lancet 2017; 389(10065): 211-24.
[http://dx.doi.org/10.1016/S0140-6736(16)30951-5] [PMID: 27549684]
[70]
Franklin D, Babl FE, Schlapbach LJ, et al. A randomized trial of high-flow oxygen therapy in infants with bronchiolitis. N Engl J Med 2018; 378(12): 1121-31.
[http://dx.doi.org/10.1056/NEJMoa1714855] [PMID: 29562151]
[71]
Jartti T, Bønnelykke K, Elenius V, Feleszko W. Role of viruses in asthma. Semin Immunopathol 2020; 42(1): 61-74.
[http://dx.doi.org/10.1007/s00281-020-00781-5] [PMID: 31989228]
[72]
Jartti T, Nieminen R, Vuorinen T, et al. Short- and long-term efficacy of prednisolone for first acute rhinovirus-induced wheezing episode. J Allergy Clin Immunol 2015; 135(3): 691-8.
[http://dx.doi.org/10.1016/j.jaci.2014.07.001] [PMID: 25129681]
[73]
Leino A, Lukkarinen M, Turunen R, et al. Pulmonary function and bronchial reactivity 4 years after the first virus-induced wheezing. Allergy 2019; 74(3): 518-26.
[http://dx.doi.org/10.1111/all.13593] [PMID: 30144084]
[74]
Skevaki CL, Christodoulou I, Spyridaki IS, et al. Budesonide and formoterol inhibit inflammatory mediator production by bronchial epithelial cells infected with rhinovirus. Clin Exp Allergy 2009; 39(11): 1700-10.
[http://dx.doi.org/10.1111/j.1365-2222.2009.03307.x] [PMID: 19549024]
[75]
Farr BM, Gwaltney JM Jr, Hendley JO, et al. A randomized controlled trial of glucocorticoid prophylaxis against experimental rhinovirus infection. J Infect Dis 1990; 162(5): 1173-7.
[http://dx.doi.org/10.1093/infdis/162.5.1173] [PMID: 2172395]
[76]
Papi A, Papadopoulos NG, Degitz K, Holgate ST, Johnston SL. Corticosteroids inhibit rhinovirus-induced intercellular adhesion molecule-1 up-regulation and promoter activation on respiratory epithelial cells. J Allergy Clin Immunol 2000; 105(2 Pt 1): 318-26.
[http://dx.doi.org/10.1016/S0091-6749(00)90082-4] [PMID: 10669853]
[77]
Bakel LA, Hamid J, Ewusie J, et al. International variation in asthma and bronchiolitis guidelines. Pediatrics 2017; 140(5): e20170092.
[http://dx.doi.org/10.1542/peds.2017-0092] [PMID: 29070533]
[78]
Kirolos A, Manti S, Blacow R, et al. A systematic review of clinical practice guidelines for the diagnosis and management of bronchiolitis. J Infect Dis 2020; 222(Suppl. 7): S672-9.
[http://dx.doi.org/10.1093/infdis/jiz240] [PMID: 31541233]
[79]
Edwards MR, Johnson MW, Johnston SL. Combination therapy: Synergistic suppression of virus-induced chemokines in airway epithelial cells. Am J Respir Cell Mol Biol 2006; 34(5): 616-24.
[http://dx.doi.org/10.1165/rcmb.2005-0385OC] [PMID: 16424382]
[80]
Volonaki E, Psarras S, Xepapadaki P, Psomali D, Gourgiotis D, Papadopoulos NG. Synergistic effects of fluticasone propionate and salmeterol on inhibiting rhinovirus-induced epithelial production of remodelling-associated growth factors. Clin Exp Allergy 2006; 36(10): 1268-73.
[http://dx.doi.org/10.1111/j.1365-2222.2006.02566.x] [PMID: 17014435]
[81]
Hurme P, Homil K, Lehtinen P, et al. Efficacy of inhaled salbutamol with and without prednisolone for first acute rhinovirus-induced wheezing episode. Clin Exp Allergy 2021; 51(9): 1121-32.
[http://dx.doi.org/10.1111/cea.13960] [PMID: 34062027]
[82]
McGregor MC, Krings JG, Nair P, Castro M. Role of biologics in asthma. Am J Respir Crit Care Med 2019; 199(4): 433-45.
[http://dx.doi.org/10.1164/rccm.201810-1944CI] [PMID: 30525902]
[83]
Esquivel A, Busse WW, Calatroni A, et al. Effects of omalizumab on rhinovirus infections, illnesses, and exacerbations of asthma. Am J Respir Crit Care Med 2017; 196(8): 985-92.
[http://dx.doi.org/10.1164/rccm.201701-0120OC] [PMID: 28608756]
[84]
Teach SJ, Gill MA, Togias A, et al. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. J Allergy Clin Immunol 2015; 136(6): 1476-85.
[http://dx.doi.org/10.1016/j.jaci.2015.09.008] [PMID: 26518090]
[85]
Haahtela T. Allergy is rare where butterflies flourish in a biodiverse environment. Allergy 2009; 64(12): 1799-803.
[http://dx.doi.org/10.1111/j.1398-9995.2009.02246.x] [PMID: 19895627]
[86]
Lynch SV, Wood RA, Boushey H, et al. Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children. J Allergy Clin Immunol 2014; 134(3): 593-601.e12.
[http://dx.doi.org/10.1016/j.jaci.2014.04.018] [PMID: 24908147]
[87]
Tanno LK, Haahtela T, Calderon MA, Cruz A, Demoly P. Implementation gaps for asthma prevention and control. Respir Med 2017; 130: 13-9.
[http://dx.doi.org/10.1016/j.rmed.2017.07.006] [PMID: 29206628]
[88]
Bisgaard H, Stokholm J, Chawes BL, et al. Fish oil-derived fatty acids in pregnancy and wheeze and asthma in offspring. N Engl J Med 2016; 375(26): 2530-9.
[http://dx.doi.org/10.1056/NEJMoa1503734] [PMID: 28029926]
[89]
Lee-Sarwar K, Litonjua AA. As you eat it: Effects of prenatal nutrition on asthma. J Allergy Clin Immunol Pract 2018; 6(3): 711-8.
[http://dx.doi.org/10.1016/j.jaip.2018.01.026] [PMID: 29412180]
[90]
Edwards MR, Walton RP, Jackson DJ, et al. The potential of anti-infectives and immunomodulators as therapies for asthma and asthma exacerbations. Allergy 2018; 73(1): 50-63.
[http://dx.doi.org/10.1111/all.13257] [PMID: 28722755]
[91]
Esposito S, Soto-Martinez ME, Feleszko W, Jones MH, Shen KL, Schaad UB. Nonspecific immunomodulators for recurrent respiratory tract infections, wheezing and asthma in children: a systematic review of mechanistic and clinical evidence. Curr Opin Allergy Clin Immunol 2018; 18(3): 198-209.
[http://dx.doi.org/10.1097/ACI.0000000000000433] [PMID: 29561355]
[92]
Glanville N, McLean GR, Guy B, et al. Cross-serotype immunity induced by immunization with a conserved rhinovirus capsid protein. PLoS Pathog 2013; 9(9): e1003669.
[http://dx.doi.org/10.1371/journal.ppat.1003669] [PMID: 24086140]
[93]
Lee S, Nguyen MT, Currier MG, et al. A polyvalent inactivated rhinovirus vaccine is broadly immunogenic in rhesus macaques. Nat Commun 2016; 7: 12838.
[http://dx.doi.org/10.1038/ncomms12838] [PMID: 27653379]
[94]
Williams GR, Kubajewska I, Glanville N, Johnston SL, Mclean GR. The potential for a protective vaccine for rhinovirus infections. Expert Rev Vaccines 2016; 15(5): 569-71.
[http://dx.doi.org/10.1586/14760584.2016.1142375] [PMID: 26766290]
[95]
Elenius V, Jartti T. Vaccines: could asthma in young children be a preventable disease?. Pediatr. Allergy Immunol. 2016; 27(7): 682-6.
[http://dx.doi.org/10.1111/pai.12598] [PMID: 27171908]