The link between bronchiolitis and asthma

Tuomas Jartti, Mika J Mäkelä, Timo Vanto, Olli Ruuskanen, Tuomas Jartti, Mika J Mäkelä, Timo Vanto, Olli Ruuskanen

Abstract

Bronchiolitis and asthma are common wheezing illnesses of childhood. Respiratory syncytial virus is the main causative agent of Bronchiolitis. Rhinovirus is the most common trigger of exacerbations of asthma, but also has been detected increasingly in doing children with Bronchiolitis. Reportedly, childhood asthma develops in 40% of children with a history of Bronchiolitis. No convincing link has been reported between Bronchiolitis and development of atopy, although atopy generally is regarded as the main risk factor for chronic asthma. This article focuses on the association between bronchiolitis and the development of asthma. The authors address the question how respiratory syncytial virus and rhinovirus infections in young children, together with genetics and immunologic immaturity, may contribute to the development of asthma.

Figures

Fig. 1
Fig. 1
Multifactorial influences on the development of asthma. BHR, bronchial hyperreactivity. (From Openshaw PJ, Yamaguchi Y, Tregoning JS. Childhood infections, the developing immune system, and the origins of asthma. J Allergy Clin Immunol 2004;114:1276; with permission.)

References

    1. Ruuskanen O., Ogra P.L. Respiratory syncytial virus. Curr Probl Pediatr. 1993;23:50–79.
    1. National Asthma Education and Prevention Program Expert Panel Report Guidelines for the diagnosis and management of asthma: update on selected topics—2002. J Allergy Clin Immunol. 2002;110:S141–S219.
    1. Shay D.K., Holman R.C., Newman R.D., Liu L.L., Stout J.W., Anderson L.J. Bronchiolitis-associated hospitalizations among US children, 1980–1996. JAMA. 1999;282:1440–1446.
    1. Langley J.M., LeBlanc J.C., Smith B., Wang E.E. Increasing incidence of hospitalization for bronchiolitis among Canadian children, 1980–2000. J Infect Dis. 2003;188:1764–1767.
    1. Akinbami L.J., Schoendorf K.C. Trends in childhood asthma: prevalence, health care utilization, and mortality. Pediatrics. 2002;110:315–322.
    1. Forster J., Tacke U., Krebs H. Respiratory syncytial virus infection: its role in aeroallergen sensitization during the first two years of life. Pediatr Allergy Immunol. 1996;7:55–60.
    1. Stein R.T., Sherrill D., Morgan W.J. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet. 1999;354:541–545.
    1. Sigurs N., Gustafsson P.M., Bjarnason R. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med. 2005;171:137–141.
    1. Kotaniemi-Syrjänen A., Vainionpää R., Reijonen T.M., Waris M., Korhonen K., Korppi M. Rhinovirus-induced wheezing in infancy—the first sign of childhood asthma? J Allergy Clin Immunol. 2003;111:66–71.
    1. Rakes G.P., Arruda E., Ingram J.M. Rhinovirus and respiratory syncytial virus in wheezing children requiring emergency care: IgE and eosinophil analyses. Am J Respir Crit Care Med. 1999;159:785–790.
    1. Andreoletti L., Lesay M., Deschildre A., Lambert V., Dewilde A., Wattre P. Differential detection of rhinoviruses and enteroviruses RNA sequences associated with classical immunofluorescence assay detection of respiratory virus antigens in nasopharyngeal swabs from infants with bronchiolitis. J Med Virol. 2000;61:341–346.
    1. Papadopoulos N.G., Moustaki M., Tsolia M. Association of rhinovirus infection with increased disease severity in acute bronchiolitis. Am J Respir Crit Care Med. 2002;165:1285–1289.
    1. Jartti T., Lehtinen P., Vuorinen T., Koskenvuo M., Ruuskanen O. Persistence of rhinovirus and enterovirus RNA after acute respiratory illness in children. J Med Virol. 2004;72:695–699.
    1. Jartti T., Lehtinen P., Vuorinen T. Respiratory picornaviruses and respiratory syncytial virus as causative agents of acute expiratory wheezing in children. Emerg Infect Dis. 2004;10:1095–1101.
    1. Johnston S.L., Pattemore P.K., Sanderson G. Community study of role of viral infections in exacerbations of asthma in 9–11 year old children. BMJ. 1995;310:1225–1229.
    1. Freymuth F., Vabret A., Brouard J. Detection of viral, Chlamydia pneumoniae and Mycoplasma pneumoniae infections in exacerbations of asthma in children. J Clin Virol. 1999;13:131–139.
    1. Rawlinson W.D., Waliuzzaman Z., Carter I.W., Belessis Y.C., Gilbert K.M., Morton J.R. Asthma exacerbations in children associated with rhinovirus but not human metapneumovirus infection. J Infect Dis. 2003;187:1314–1318.
    1. Martinez F.D., Wright A.L., Taussig L.M., Holberg C.J., Halonen M., Morgan W.J. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med. 1995;332:133–138.
    1. Young S., O'Keeffe P.T., Arnott J., Landau L.I. Lung function, airway responsiveness, and respiratory symptoms before and after bronchiolitis. Arch Dis Child. 1995;72:16–24.
    1. Hull J., Thomson A., Kwiatkowski D. Association of respiratory syncytial virus bronchiolitis with the interleukin 8 gene region in UK families. Thorax. 2000;55:1023–1027.
    1. Lahti M., Löfgren J., Marttila R. Surfactant protein D gene polymorphism associated with severe respiratory syncytial virus infection. Pediatr Res. 2002;51:696–699.
    1. Hoebee B., Rietveld E., Bont L. Association of severe respiratory syncytial virus bronchiolitis with interleukin-4 and interleukin-4 receptor alpha polymorphisms. J Infect Dis. 2003;187:2–11.
    1. Heinzmann A., Ahlert I., Kurz T., Berner R., Deichmann K.A. Association study suggests opposite effects of polymorphisms within IL8 on bronchial asthma and respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol. 2004;114:671–676.
    1. Gern J.E. Viral respiratory infection and the link to asthma. Pediatr Infect Dis J. 2004;23:S78–S86.
    1. Heidema J., Kimpen J.L.L., van Bleek G.M. Pathogenesis of respiratory syncytial virus bronchiolitis: immunology and genetics. In: Kimpen J.L.L., Ramilo O., editors. Respiratory tract infections, pathogenesis and emerging strategies for control. Horizon Bioscience; Norfolk: 2004. pp. 233–252.
    1. Tripp R.A., Moore D., Barskey A., 4th Peripheral blood mononuclear cells from infants hospitalized because of respiratory syncytial virus infection express T helper-1 and T helper-2 cytokines and CC chemokine messenger RNA. J Infect Dis. 2002;185:1388–1394.
    1. Message S.D., Johnston S.L. Host defense function of the airway epithelium in health and disease: clinical background. J Leukoc Biol. 2004;75:5–17.
    1. Ruuskanen O., Hyypiä T. Rhinovirus: is it really a relevant pathogen? In: Kimpen J.L.L., Ramilo O., editors. Respiratory tract infections, pathogenesis and emerging strategies for control. Horizon Bioscience; Norfolk: 2004. pp. 291–317.
    1. Fraenkel D.J., Bardin P.G., Sanderson G., Lampe F., Johnston S.L., Holgate S.T. Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects. Am J Respir Crit Care Med. 1995;151:879–886.
    1. Korppi M., Kotaniemi-Syrjänen A., Waris M., Vainionpää R., Reijonen T.M. Rhinovirus-associated wheezing in infancy: comparison with respiratory syncytial virus bronchiolitis. Pediatr Infect Dis J. 2004;23:995–999.
    1. Camilli A.E., Holberg C.J., Wright A.L., Taussig L.M. Parental childhood respiratory illness and respiratory illness in their infants. Group Health Medical Associates. Pediatr Pulmonol. 1993;16:275–280.
    1. Steinke J.W., Borish L., Rosenwasser L.J. Genetics of hypersensitivity. J Allergy Clin Immunol. 2003;111:S495–S501.
    1. Weiss S.T., Raby B.A. Asthma genetics 2003. Hum Mol Genet. 2004;13:R83–R89.
    1. Kere J., Laitinen T. Positionally cloned susceptibility genes in allergy and asthma. Curr Opin Immunol. 2004;16:689–694.
    1. Xu J., Meyers D.A., Ober C., Collaborative Study on the Genetics of Asthma Genomewide screen and identification of gene-gene interactions for asthma-susceptibility loci in three US populations: collaborative study on the genetics of asthma. Am J Hum Genet. 2001;68:1437–1446.
    1. Heaton T., Rowe J., Turner S. An immunoepidemiological approach to asthma: identification of in-vitro T-cell response patterns associated with different wheezing phenotypes in children. Lancet. 2005;365:142–149.
    1. Akdis C.A., Blesken T., Akdis M., Wuthrich B., Blaser K. Role of interleukin 10 in specific immunotherapy. J Clin Invest. 1998;102:98–106.
    1. Borish L., Aarons A., Rumbyrt J., Cvietusa P., Negri J., Wenzel S. Interleukin-10 regulation in normal subjects and patients with asthma. J Allergy Clin Immunol. 1996;97:1288–1296.
    1. Arkwright P.D., Chase J.M., Babbage S., Pravica V., David T.J., Hutchinson I.V. Atopic dermatitis is associated with a low-producer transforming growth factor beta(1) cytokine genotype. J Allergy Clin Immunol. 2001;108:281–284.
    1. Karjalainen J., Hulkkonen J., Pessi T. The IL1A genotype associates with atopy in nonasthmatic adults. J Allergy Clin Immunol. 2002;110:429–434.
    1. Colavita A.M., Hastie A.T., Musani A.I. Kinetics of IL-10 production after segmental antigen challenge of atopic asthmatic subjects. J Allergy Clin Immunol. 2000;106:880–886.
    1. Papadopoulos N.G., Stanciu L.A., Papi A., Holgate S.T., Johnston S.L. A defective type 1 response to rhinovirus in atopic asthma. Thorax. 2002;57:328–332.
    1. van Benten I.J., van Drunen C.M., Koevoet J.L. Reduced nasal IL-10 and enhanced TNFalpha responses during rhinovirus and RSV induced upper respiratory tract infection in atopic and non-atopic infants. J Med Virol. 2005;75:348–357.
    1. Hansen G., Berry G., DeKruyff R.H., Umetsu D.T. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J Clin Invest. 1999;103:175–183.
    1. Umetsu D.T. Revising the immunological theories of asthma and allergy. Lancet. 2005;365:98–100.
    1. Strachan D.P. Hay fever, hygiene, and household size. BMJ. 1989;299:1259–1260.
    1. Rautava S., Ruuskanen O., Ouwehand A., Salminen S., Isolauri E. The hygiene hypothesis of atopic disease—an extended version. J Pediatr Gastroenterol Nutr. 2004;38:378–388.
    1. Sigurs N., Bjarnason R., Sigurbergsson F., Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med. 2000;161:1501–1507.
    1. Wenzel S.E., Gibbs R.L., Lehr M.V., Simoes E.A. Respiratory outcomes in high-risk children 7 to 10 years after prophylaxis with respiratory syncytial virus immune globulin. Am J Med. 2002;112:627–633.
    1. Pala P., Bjarnason R., Sigurbergsson F., Metcalfe C., Sigurs N., Openshaw P.J. Enhanced IL-4 responses in children with a history of respiratory syncytial virus bronchiolitis in infancy. Eur Respir J. 2002;20:376–382.
    1. Sporik R., Holgate S.T., Platts-Mills T.A., Cogswell J.J. Exposure to house-dust mite allergen (Der p I) and the development of asthma in childhood: a prospective study. N Engl J Med. 1990;323:502–507.
    1. Arshad S.H., Bateman B., Matthews S.M. Primary prevention of asthma and atopy during childhood by allergen avoidance in infancy: a randomised controlled study. Thorax. 2003;58:489–493.
    1. Sporik R., Ingram J.M., Price W., Sussman J.H., Honsinger R.W., Platts-Mills T.A. Association of asthma with serum IgE and skin test reactivity to allergens among children living at high altitude: tickling the dragon's breath. Am J Respir Crit Care Med. 1995;151:1388–1392.
    1. Platts-Mills T.A., Rakes G., Heymann P.W. The relevance of allergen exposure to the development of asthma in childhood. J Allergy Clin Immunol. 2000;105:S503–S508.
    1. Green R.M., Custovic A., Sanderson G., Hunter J., Johnston S.L., Woodcock A. Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study. BMJ. 2002;324:763.
    1. Carlsen K.H., Orstavik I., Leegaard J., Hoeg H. Respiratory virus infections and aeroallergens in acute bronchial asthma. Arch Dis Child. 1984;59:310–315.
    1. Steinmann G.G. Changes in the human thymus during aging. Curr Top Pathol. 1986;75:43–88.
    1. Comans-Bitter W.M., de Groot R., van den Beemd R. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr. 1997;130:388–393.
    1. Crespo I., Paiva A., Couceiro A., Pimentel P., Orfao A., Regateiro F. Immunophenotypic and functional characterization of cord blood dendritic cells. Stem Cells Dev. 2004;13:63–70.
    1. Langrish C.L., Buddle J.C., Thrasher A.J., Goldblatt D. Neonatal dendritic cells are intrinsically biased against Th-1 immune responses. Clin Exp Immunol. 2002;128:118–123.
    1. Marodi L. Down-regulation of Th1 responses in human neonates. Clin Exp Immunol. 2002;128:1–2.
    1. Ribeiro-do-Couto L.M., Boeije L.C., Kroon J.S. High IL-13 production by human neonatal T cells: neonate immune system regulator? Eur J Immunol. 2001;31:3394–3402.
    1. Kotiranta-Ainamo A., Rautonen J., Rautonen N. Imbalanced cytokine secretion in newborns. Biol Neonate. 2004;85:55–60.
    1. Yu H.R., Chang J.C., Chen R.F. Different antigens trigger different Th1/Th2 reactions in neonatal mononuclear cells (MNCs) relating to T-bet/GATA-3 expression. J Leukoc Biol. 2003;74:952–958.
    1. Mäkelä P.H., Sibakov M., Herva E. Pneumococcal vaccine and otitis media. Lancet. 1980;2:547–551.
    1. Timens W., Boes A., Rozeboom-Uiterwijk T., Poppema S. Immaturity of the human splenic marginal zone in infancy: possible contribution to the deficient infant immune response. J Immunol. 1989;143:3200–3206.
    1. Rijkers G.T., Sanders E.A., Breukels M.A., Zegers B.J. Infant B cell responses to polysaccharide determinants. Vaccine. 1998;16:1396–1400.
    1. De Rosa S.C., Andrus J.P., Perfetto S.P. Ontogeny of gamma delta T cells in humans. J Immunol. 2004;172:1637–1645.
    1. Gleeson M., Cripps A.W. Development of mucosal immunity in the first year of life and relationship to sudden infant death syndrome. FEMS Immunol Med Microbiol. 2004;42:21–33.
    1. van Benten I.J., van Drunen C.M., Koopman L.P. Age- and infection-related maturation of the nasal immune response in 0–2-year-old children. Allergy. 2005;60:226–232.
    1. Martinez F.D., Holt P.G. Role of microbial burden in aetiology of allergy and asthma. Lancet. 1999;354:SII12–SII15.
    1. Culley F.J., Pollott J., Openshaw P.J. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J Exp Med. 2002;196:1381–1386.
    1. Schwarze J., O'Donnell D.R., Rohwedder A., Openshaw P.J.M. Latency and persistence of respiratory syncytial virus despite T cell immunity. Am J Respir Crit Care Med. 2004;169:801–805.
    1. Sims D.G., Downham M.A., Gardner P.S., Webb J.K., Weightman D. Study of 8-year-old children with a history of respiratory syncytial virus bronchiolitis in infancy. BMJ. 1978;1:11–14.
    1. Pullan C.R., Hey E.N. Wheezing, asthma, and pulmonary dysfunction 10 years after infection with respiratory syncytial virus in infancy. BMJ. 1982;284:1665–1669.
    1. Mok J.Y., Simpson H. Outcome of acute lower respiratory tract infection in infants: preliminary report of seven-year follow-up study. BMJ. 1982;285:333–337.
    1. McConnochie K.M., Roghmann K.J. Bronchiolitis as a possible cause of wheezing in childhood: new evidence. Pediatrics. 1984;74:1–10.
    1. McConnochie K.M., Mark J.D., McBride J.T. Normal pulmonary function measurements and airway reactivity in childhood after mild bronchiolitis. J Pediatr. 1985;107:54–58.
    1. McConnochie K.M., Roghmann K.J. Wheezing at 8 and 13 years: changing importance of bronchiolitis and passive smoking. Pediatr Pulmonol. 1989;6:138–146.
    1. Carlsen K.H., Larsen S., Bjerve O., Leegaard J. Acute bronchiolitis: predisposing factors and characterization of infants at risk. Pediatr Pulmonol. 1987;3:153–160.
    1. Osundwa V.M., Dawod S.T., Ehlayel M. Recurrent wheezing in children with respiratory syncytial virus (RSV) bronchiolitis in Qatar. Eur J Pediatr. 1993;152:1001–1003.
    1. Noble V., Murray M., Webb M.S., Alexander J., Swarbrick A.S., Milner A.D. Respiratory status and allergy nine to 10 years after acute bronchiolitis. Arch Dis Child. 1997;76:315–319.
    1. Weber M.W., Milligan P., Giadom B. Respiratory illness after severe respiratory syncytial virus disease in infancy in The Gambia. J Pediatr. 1999;135:683–688.
    1. Kneyber M.C.J., Steyerberg E.W., de Groot R., Moll H.A. Long-term effects of respiratory syncytial virus (RSV) bronchiolitis in infants and young children: a quantitative review. Acta Pediatr. 2000;89:654–660.
    1. Piippo-Savolainen E., Remes S., Kannisto S., Korhonen K., Korppi M. Asthma and lung function 20 years after wheezing in infancy: results from a prospective follow-up study. Arch Pediatr Adolesc Med. 2004;158:1070–1076.
    1. Sigurs N., Bjarnason R., Sigurbergsson F., Kjellman B., Bjorksten B. Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics. 1995;95:500–505.
    1. Lehtinen P, Ruohola A, Vuorinen T, Vanto T, Jartti T, Ruuskanen O. Development of asthma after first time viral bronchiolitis [Abstract]. Presented at Frontiers in Neonatal and Infant Immunity. Madrid, Spain, March 18–20, 2005.
    1. Martinez F.D., Stern D.A., Wright A.L., Taussig L.M., Halonen M. Differential immune responses to acute lower respiratory illness in early life and subsequent development of persistent wheezing and asthma. J Allergy Clin Immunol. 1998;102:915–920.
    1. Ehlenfield D.R., Cameron K., Welliver R.C. Eosinophilia at the time of respiratory syncytial virus bronchiolitis predicts childhood reactive airway disease. Pediatrics. 2000;105:79–83.
    1. Lowe L., Murray C.S., Martin L. Reported versus confirmed wheeze and lung function in early life. Arch Dis Child. 2004;89:540–543.
    1. Devulapalli C.S., Haaland G., Pettersen M., Carlsen K.H., Lodrup Carlsen K.C. Effect of inhaled steroids on lung function in young children: a cohort study. Eur Respir J. 2004;23:869–875.
    1. Zambrano J.C., Carper H.T., Rakes G.P. Experimental rhinovirus challenges in adults with mild asthma: response to infection in relation to IgE. J Allergy Clin Immunol. 2003;111:1008–1016.
    1. Gern J.E., Calhoun W., Swenson C., Shen G., Busse W.W. Rhinovirus infection preferentially increases lower airway responsiveness in allergic subjects. Am J Respir Crit Care Med. 1997;155:1872–1876.
    1. Papi A., Johnston S.L. Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-kappaB-mediated transcription. J Biol Chem. 1999;274:9707–9720.
    1. Bianco A., Sethi S.K., Allen J.T., Knight R.A., Spiteri M.A. Th2 cytokines exert a dominant influence on epithelial cell expression of the major group human rhinovirus receptor, ICAM-1. Eur Respir J. 1998;12:619–626.
    1. Grunberg K., Timmers M.C., Smits H.H. Effect of experimental rhinovirus 16 colds on airway hyperresponsiveness to histamine and interleukin-8 in nasal lavage in asthmatic subjects in vivo. Clin Exp Allergy. 1997;27:36–45.
    1. Parry D.E., Busse W.W., Sukow K.A., Dick C.R., Swenson C., Gern J.E. Rhinovirus-induced PBMC responses and outcome of experimental infection in allergic subjects. J Allergy Clin Immunol. 2000;105:692–698.
    1. Gern J.E., Vrtis R., Grindle K.A., Swenson C., Busse W.W. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. Am J Respir Crit Care Med. 2000;162:2226–2231.
    1. Brooks G.D., Buchta K.A., Swenson C.A., Gern J.E., Busse W.W. Rhinovirus-induced interferon-gamma and airway responsiveness in asthma. Am J Respir Crit Care Med. 2003;168:1091–1094.
    1. Schwarze J., Mäkelä M., Cieslewicz G. Transfer of the enhancing effect of respiratory syncytial virus infection on subsequent allergic airway sensitization by T lymphocytes. J Immunol. 1999;163:5729–5734.
    1. Schwarze J., Cieslewicz G., Joetham A. Critical roles for interleukin-4 and interleukin-5 during respiratory syncytial virus infection in the development of airway hyperresponsiveness after airway sensitization. Am J Respir Crit Care Med. 2000;162:380–386.
    1. Mäkelä M.J., Kanehiro A., Dakhama A. The failure of interleukin-10-deficient mice to develop airway hyperresponsiveness is overcome by respiratory syncytial virus infection in allergen-sensitized/challenged mice. Am J Respir Crit Care Med. 2002;165:824–831.
    1. Schwarze J., Gelfand E.W. Respiratory viral infections as promoters of allergic sensitization and asthma in animal models. Eur Respir J. 2002;19:341–349.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe