Nasopharyngeal bacterial colonization during the first wheezing episode is associated with longer duration of hospitalization and higher risk of relapse in young children

  • T. Jartti
  • S. Kuneinen
  • P. Lehtinen
  • V. Peltola
  • T. Vuorinen
  • M. Leinonen
  • O. Ruuskanen


The purpose of this study was to examine the association between bacterial colonization/infection and respiratory outcomes in children younger than 3 years old who were hospitalized for their first wheezing episode. This was an observational study. The primary outcome was hospitalization time and the secondary outcomes included relapses within 2 months and time to recurrent wheezing (i.e. three physician confirmed wheezing episodes) within 12 months. Bacterial antibody assays for Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, Mycoplasma pneumoniae and Chlamydia pneumoniae were studied as well as nasopharyngeal bacterial culture for the three former and urine pneumococcal antigen. Nasopharyngeal bacterial culture was positive in 31/52 (60%) children, serologic evidence of bacterial infection was found in 17/96 (18%) children, urine pneumococcal antigen was positive in 24/101 (24%), and any bacterial detection method was positive in 53/106 (50%) children. The children with positive nasopharyngeal bacterial culture had longer duration of hospitalization (hazard ratio 2.4) and more often relapsed within two months than those with negative culture (odds ratio 7.3). In this study, half of the first time wheezing children had bacterial colonization or symptomatic or asymptomatic bacterial infection. The bacterial colonization (i.e. positive nasopharyngeal bacterial culture) was associated with longer duration of hospitalization and higher risk of recurrent wheezing.


Conflict of interest


Addition to proofs

A recent study showed that acute wheezy episodes in young children of a high risk cohort were associated with bacterial infections similar to, but independent of the association with, virus infections. (Bisgaard H, Hermansen MN, Bønnelykke K, Stokholm J, Baty F, Skytt NL, et al (2010) Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ 4;341:c4978).


  1. 1.
    Heymann PW, Carper HT, Murphy DD, Platts-Mills TA, Patrie J, McLaughlin AP et al (2004) Viral infections in relation to age, atopy, and season of admission among children hospitalized for wheezing. J Allergy Clin Immunol 114(2):239–247CrossRefPubMedGoogle Scholar
  2. 2.
    Allander T, Jartti T, Gupta S, Niesters H, Lehtinen P, Österback R et al (2007) Human bocavirus and acute wheezing in children. Clin Infect Dis 44(7):904–910CrossRefPubMedGoogle Scholar
  3. 3.
    Bruder D, Srikiatkhachorn A, Enelow RI (2006) Cellular immunity and lung injury in respiratory virus infection. Viral Immunol 19(2):147–155CrossRefPubMedGoogle Scholar
  4. 4.
    Esposito S, Blasi F, Arosio C, Fioravanti L, Fagetti L, Droghetti R et al (2000) Importance of acute Mycoplasma pneumoniae and Chlamydia pneumoniae infections in children with wheezing. Eur Respir J 16(6):1142–1146CrossRefPubMedGoogle Scholar
  5. 5.
    Normann E, Gnarpe J, Wettergren B, Janson C, Wickman M, Nordvall L (2006) Association between Chlamydia pneumoniae antibodies and wheezing in young children and the influence of sex. Thorax 61(12):1054–1058CrossRefPubMedGoogle Scholar
  6. 6.
    Nagayama Y, Tsubaki T, Nakayama S, Sawada K, Taguchi K, Toba T et al (2007) Bacterial colonization in respiratory secretions from acute and recurrent wheezing infants and children. Pediatr Allergy Immunol 18(2):110–117CrossRefPubMedGoogle Scholar
  7. 7.
    Lehtinen P, Jartti T, Virkki R, Vuorinen T, Leinonen M, Peltola V et al (2006) Bacterial coinfections in children with viral wheezing. Eur J Clin Microbiol Infect Dis 25(7):463–469CrossRefPubMedGoogle Scholar
  8. 8.
    Yu D, Wei L, Zhengxiu L, Jian L, Lijia W, Wei L, et al. Impact of bacterial colonization on the severity and airway inflammation of children with virus induced wheezing. Clin Microbiol Infect 2009. [Epub ahead of print]Google Scholar
  9. 9.
    Kotaniemi-Syrjänen A, Vainionpää R, Reijonen TM, Waris M, Korhonen K, Korppi M (2003) Rhinovirus-induced wheezing in infancy—the first sign of childhood asthma? J Allergy Clin Immunol 111(1):66–71CrossRefPubMedGoogle Scholar
  10. 10.
    Lemanske RF, Jackson DJ, Gangnon RE, Evans MD, Li Z, Shult PA et al (2005) Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol 116(3):571–577CrossRefPubMedGoogle Scholar
  11. 11.
    Lehtinen P, Ruohola A, Vuorinen T, Vanto T, Ruuskanen O, Jartti T (2007) Prednisolone reduces recurrent wheezing after a first wheezing episode associated with rhinovirus infection or eczema. J Allergy Clin Immunol 119(3):570–575CrossRefPubMedGoogle Scholar
  12. 12.
    Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL et al (2007) Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 119(5):1105–1110CrossRefPubMedGoogle Scholar
  13. 13.
    Bisgaard H, Hermansen MN, Buchvald F, Loland L, Halkjaer LB, Bønnelykke K et al (2007) Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 357(15):1487–1495CrossRefPubMedGoogle Scholar
  14. 14.
    Talbot TR, Hartert TV, Mitchel E, Halasa NB, Arbogast PG, Poehling KA et al (2005) Asthma as a risk factor for invasive pneumococcal disease. N Engl J Med 352(20):2082–2090CrossRefPubMedGoogle Scholar
  15. 15.
    Juhn YJ, Kita H, Yawn BP, Boyce TG, Yoo KH, McGree ME et al (2008) Increased risk of serious pneumococcal disease in patients with asthma. J Allergy Clin Immunol 122(4):719–723CrossRefPubMedGoogle Scholar
  16. 16.
    Jartti T, Lehtinen P, Vanto T, Hartiala J, Vuorinen T, Mäkelä MJ et al (2006) The efficacy of prednisolone in early wheezing induced by rhinovirus or respiratory syncytial virus. Pediatr Infect Dis J 25(6):482–488CrossRefPubMedGoogle Scholar
  17. 17.
    Jartti T, Lehtinen P, Vanto T, Vuorinen T, Hartiala J, Hiekkanen H et al (2007) Efficacy of prednisolone in children hospitalized for recurrent wheezing. Pediatr Allergy Immunol 18(4):326–334CrossRefPubMedGoogle Scholar
  18. 18.
    Jartti T, Lehtinen P, Vuorinen T, Österback R, van den Hoogen B, Osterhaus AD et al (2004) Respiratory picornaviruses and respiratory syncytial virus as causative agents of acute expiratory wheezing in children. Emerg Infect Dis 10(6):1095–1101PubMedGoogle Scholar
  19. 19.
    Mertsola J, Ziegler T, Ruuskanen O, Vanto T, Koivikko A, Halonen P (1991) Recurrent wheezy bronchitis and viral respiratory infections. Arch Dis Child 66(1):124–129CrossRefPubMedGoogle Scholar
  20. 20.
    Korppi M, Leinonen M, Koskela M, Mäkelä PH, Saikku P, Launiala K (1991) Bacterial infection in under school age children with expiratory difficulty. Pediatr Pulmonol 10(4):254–259CrossRefPubMedGoogle Scholar
  21. 21.
    García-Rodríguez JA, Fresnadillo Martínez MJ (2002) Dynamics of nasopharyngeal colonization by potential respiratory pathogens. J Antimicrob Chemother 50(Suppl S2):59–73CrossRefPubMedGoogle Scholar
  22. 22.
    Ong BH, Gao Q, Phoon MC, Chow VT, Tan WC, Van Bever HP (2007) Identification of human metapneumovirus and Chlamydophila pneumoniae in children with asthma and wheeze in Singapore. Singapore Med J 48(4):291–293PubMedGoogle Scholar
  23. 23.
    Watson K, Carville K, Bowman J, Jacoby P, Riley TV, Leach AJ et al (2006) Upper respiratory tract bacterial carriage in Aboriginal and non-Aboriginal children in a semi-arid area of Western Australia. Pediatr Infect Dis J 25(9):782–790CrossRefPubMedGoogle Scholar
  24. 24.
    Harrison LM, Morris JA, Telford DR, Brown SM, Jones K (1999) The nasopharyngeal bacterial flora in infancy: effects of age, gender, season, viral upper respiratory tract infection and sleeping position. FEMS Immunol Med Microbiol 25(1–2):19–28CrossRefPubMedGoogle Scholar
  25. 25.
    Cardozo DM, Nascimento-Carvalho CM, Andrade AL, Silvany-Neto AM, Daltro CH, Brandão MA et al (2008) Prevalence and risk factors for nasopharyngeal carriage of Streptococcus pneumoniae among adolescents. J Med Microbiol 57(Pt 2):185–189CrossRefPubMedGoogle Scholar
  26. 26.
    Ghaffar F, Friedland IR, McCracken GH Jr (1999) Dynamics of nasopharyngeal colonization by Streptococcus pneumoniae. Pediatr Infect Dis J 18(7):638–646CrossRefPubMedGoogle Scholar
  27. 27.
    Borer A, Meirson H, Peled N, Porat N, Dagan R, Fraser D et al (2001) Antibiotic-resistant pneumococci carried by young children do not appear to disseminate to adult members of a closed community. Clin Infect Dis 33(4):436–444CrossRefPubMedGoogle Scholar
  28. 28.
    St Sauver J, Marrs CF, Foxman B, Somsel P, Madera R, Gilsdorf JR (2000) Risk factors for otitis media and carriage of multiple strains of Haemophilus influenzae and Streptococcus pneumoniae. Emerg Infect Dis 6(6):622–630CrossRefPubMedGoogle Scholar
  29. 29.
    Faden H, Duffy L, Williams A, Krystofik DA, Wolf J (1995) Epidemiology of nasopharyngeal colonization with nontypeable Haemophilus influenzae in the first 2 years of life. J Infect Dis 172(1):132–135PubMedGoogle Scholar
  30. 30.
    Hartert TV (2008) Are persons with asthma at increased risk of pneumococcal infections, and can we prevent them? J Allergy Clin Immunol 122(4):724–725CrossRefPubMedGoogle Scholar
  31. 31.
    Johnston SL (2007) Innate immunity in the pathogenesis of virus-induced asthma exacerbations. Proc Am Thorac Soc 4(3):267–270CrossRefPubMedGoogle Scholar
  32. 32.
    Holt PG, Upham JW, Sly PD (2005) Contemporaneous maturation of immunologic and respiratory functions during early childhood: implications for development of asthma prevention strategies. J Allergy Clin Immunol 116(1):16–24CrossRefPubMedGoogle Scholar
  33. 33.
    Peltola VT, McCullers JA (2004) Respiratory viruses predisposing to bacterial infections: role of neuramidase. Pediatr Infect Dis J 23(1 Suppl):S87–S97PubMedGoogle Scholar
  34. 34.
    Kusel MM, de Klerk N, Holt PG, Sly PD (2008) Antibiotic use in the first year of life and risk of atopic disease in early childhood. Clin Exp Allergy 38(12):1921–1928CrossRefPubMedGoogle Scholar
  35. 35.
    Jartti T, Vanto T, Heikkinen T, Ruuskanen O (2002) Systemic glucocorticoids in childhood expiratory wheezing: relation between age and viral etiology with efficacy. Pediatr Infect Dis J 21:873–878CrossRefPubMedGoogle Scholar
  36. 36.
    Marguet C, Jouen-Boedes F, Dean TP, Warner JO (1999) Bronchoalveolar cell profiles in children with asthma infantile wheeze, chronic cough, or cystic fibrosis. Am J Respir Crit Care Med 159(5 Pt 1):1533–1540PubMedGoogle Scholar
  37. 37.
    Fayon M, Just J, Thien HV, Pascual L, Sandouk G, Grimfeld A (1999) Bacterial flora of the lower respiratory tract in children with bronchial asthma. Acta Paediatr 88(11):1216–1222CrossRefPubMedGoogle Scholar
  38. 38.
    Krawiec ME, Westcott JY, Chu HW, Balzar S, Trudeau JB, Schwartz LB et al (2001) Persistent wheezing in very young children is associated with lower respiratory inflammation. Am J Respir Crit Care Med 163(6):1338–1343PubMedGoogle Scholar
  39. 39.
    Le Bourgeois M, Goncalves M, Le Clainche L, Benoist MR, Fournet JC, Scheinmann P et al (2002) Bronchoalveolar cells in children <3 years old with severe recurrent wheezing. Chest 122(3):791–797CrossRefPubMedGoogle Scholar
  40. 40.
    National Heart, Lung and Blood Institute (2007) Expert panel report 3 (EPR3): Guidelines for the diagnosis and management of asthma. Accessed 05 October 2010
  41. 41.
    Illi S, von Mutius E, Lau S, Niggemann B, Grüber C, Wahn U et al (2006) Perennial allergen sensitisation early in life and chronic asthma in children: a birth cohort study. Lancet 368(9537):763–770CrossRefPubMedGoogle Scholar
  42. 42.
    Jartti T, Lehtinen P, Vuorinen T, Ruuskanen O (2009) Bronchiolitis: age and previous wheezing episodes are linked to viral etiology and atopic characteristics. Pediatr Infect Dis J 28(4):311–317CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • T. Jartti
    • 1
  • S. Kuneinen
    • 1
  • P. Lehtinen
    • 1
  • V. Peltola
    • 1
  • T. Vuorinen
    • 2
  • M. Leinonen
    • 3
  • O. Ruuskanen
    • 1
  1. 1.Department of PediatricsTurku University HospitalTurkuFinland
  2. 2.Department of VirologyUniversity of TurkuTurkuFinland
  3. 3.National Institute of Health and WelfareOuluFinland

Personalised recommendations