Bacterial coinfections in children with viral wheezing

  • P. Lehtinen
  • T. Jartti
  • R. Virkki
  • T. Vuorinen
  • M. Leinonen
  • V. Peltola
  • A. Ruohola
  • O. RuuskanenEmail author


Bacterial coinfections occur in respiratory viral infections, but the attack rates and the clinical profile are not clear. The aim of this study was to determine bacterial coinfections in children hospitalized for acute expiratory wheezing with defined viral etiology. A total of 220 children aged 3 months to 16 years were investigated. The viral etiology of wheezing was confirmed by viral culture, antigen detection, serologic investigation, and/or PCR. Specific antibodies to common respiratory bacteria were measured from acute and convalescent serum samples. All children were examined clinically for acute otitis media, and subgroups of children were examined radiologically for sinusitis and pneumonia. Rhinovirus (32%), respiratory syncytial virus (31%), and enteroviruses (31%) were the most common causative viruses. Serologic evidence of bacterial coinfection was found in 18% of the children. Streptococcus pneumoniae (8%) and Mycoplasma pneumoniae (5%) were the most common causative bacteria. Acute otitis media was diagnosed in 44% of the children. Chest radiographs showed alveolar infiltrates in 10%, and paranasal radiographs and clinical signs showed sinusitis in 17% of the older children studied. Leukocyte counts and serum C-reactive protein levels were low in a great majority of patients. Viral lower respiratory tract infection in children is often associated with bacterial-type upper respiratory tract infections. However, coexisting bacterial lower respiratory tract infections that induce systemic inflammatory response are seldom detected.


Respiratory Syncytial Virus Sinusitis Acute Otitis Medium Respiratory Syncytial Virus Infection Serologic Evidence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was supported by the Pediatric Research Foundation, Finland, and the Academy of Finland.


  1. 1.
    Rawlinson WD, Waliuzzaman Z, Carter IW, Belessis YC, Gilbert KM, Morton JR (2003) Asthma exacerbations in children associated with rhinovirus but not human metapneumovirus infection. J Infect Dis 187:1314–1318PubMedCrossRefGoogle Scholar
  2. 2.
    Ruuskanen O, Arola M, Putto-Laurila A, Mertsola J, Meurman O, Viljanen MK, Halonen P (1989) Acute otitis media and respiratory virus infections. Pediatr Infect Dis J 8:94–99PubMedGoogle Scholar
  3. 3.
    Vesa S, Kleemola M, Blomqvist S, Takala A, Kilpi T, Hovi T (2001) Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age. Pediatr Infect Dis J 20:574–581PubMedCrossRefGoogle Scholar
  4. 4.
    Jartti T, Lehtinen P, Vuorinen T, Österback R, van den Hoogen B, Osterhaus AD, Ruuskanen O (2004) Respiratory picornaviruses and respiratory syncytial virus as causative agents of acute expiratory wheezing in children. Emerg Infect Dis 10:1095–1101PubMedGoogle Scholar
  5. 5.
    National Asthma Education and Prevention Program (2002) Expert panel report: guidelines for the diagnosis and management of asthma: update on selected topics 2002. J Allergy Clin Immunol 110:S141–S219CrossRefGoogle Scholar
  6. 6.
    Jalonen E, Paton JC, Koskela M, Kerttula Y, Leinonen M (1989) Measurement of antibody responses to pneumolysin—a promising method for the presumptive aetiological diagnosis of pneumococcal pneumonia. J Infect 19:127–134PubMedCrossRefGoogle Scholar
  7. 7.
    Burman LA, Leinonen M, Trollfors B (1994) Use of serology to diagnose pneumonia caused by nonencapsulated Haemophilus influenzae and Moraxella catarrhalis. J Infect Dis 170:220–222PubMedGoogle Scholar
  8. 8.
    Waris ME, Toikka P, Saarinen T, Nikkari S, Meurman O, Vainionpää R, Mertsola J, Ruuskanen O (1998) Diagnosis of Mycoplasma pneumoniae pneumonia in children. J Clin Microbiol 36:3155–3159PubMedGoogle Scholar
  9. 9.
    Dowell SF, Peeling RW, Boman J, Carlone GM, Fields BS, Guarner J, Hammerschlag MR, Jackson LA, Kuo C, Maass M, Messmer TO, Talkington DF, Tondella ML, Zaki SR, and the C. pneumoniae Workshop Participants (2001) Standardizing Chlamydia pneumoniae assays: recommendations from the Centers for Disease Control and Prevention (USA) and the Laboratory Centre for Disease Control (Canada). Clin Infect Dis 33:492–503PubMedCrossRefGoogle Scholar
  10. 10.
    Virkki R, Juven T, Rikalainen H, Svedström E, Mertsola J, Ruuskanen O (2002) Differentiation of bacterial and viral pneumonia in children. Thorax 57:438–441PubMedCrossRefGoogle Scholar
  11. 11.
    Wald ER, Milmoe GJ, Bowen A, Ledesma-Medina J, Salamon N, Bluestone CD (1981) Acute maxillary sinusitis in children. N Engl J Med 304:749–754PubMedCrossRefGoogle Scholar
  12. 12.
    Ueda D, Yoto Y (1996) The ten-day mark as a practical diagnostic approach for acute paranasal sinusitis in children. Pediatr Infect Dis J 15:576–579PubMedCrossRefGoogle Scholar
  13. 13.
    Del Beccaro MA, Mendelman PM, Inglis AF, Richardson MA, Duncan NO, Clausen CR, Stull TL (1992) Bacteriology of acute otitis media: a new perspective. J Pediatr 120:81–84PubMedCrossRefGoogle Scholar
  14. 14.
    Heikkinen T, Ruuskanen O (1994) Temporal development of acute otitis media during upper respiratory tract infection. Pediatr Infect Dis J 13:659–661PubMedGoogle Scholar
  15. 15.
    Ruohola A, Heikkinen T, Waris ME, Puhakka T, Ruuskanen O (2000) Intranasal fluticasone propionate does not prevent acute otitis media during viral upper respiratory infection in children. J Allergy Clin Immunol 106:467–471PubMedCrossRefGoogle Scholar
  16. 16.
    Puhakka T, Mäkelä MJ, Alanen A, Kallio T, Korsoff L, Arstila P, Leinonen M, Pulkkinen M, Suonpää J, Mertsola J, Ruuskanen O (1998) Sinusitis in the common cold. J Allergy Clin Immunol 102:403–408PubMedCrossRefGoogle Scholar
  17. 17.
    Walsh-Kelly CM, Hennes HM (2002) Do clinical variables predict pathologic radiographs in the first episode of wheezing? Pediatr Emerg Care 18:8–11PubMedCrossRefGoogle Scholar
  18. 18.
    Wainwright C, Altamirano L, Cheney M, Cheney J, Barber S, Price D, Moloney S, Kimberley A, Woolfield N, Cadzow S, Fiumara F, Wilson P, Mego S, VandeVelde D, Sanders S, O’Rourke P, Francis P (2003) A multicenter, randomized, double-blind, controlled trial of nebulized epinephrine in infants with acute bronchiolitis. N Engl J Med 349:27–35PubMedCrossRefGoogle Scholar
  19. 19.
    Syrjälä H, Broas M, Suramo I, Ojala A, Lähde S (1998) High-resolution computed tomography for the diagnosis of community-acquired pneumonia. Clin Infect Dis 27:358–363PubMedCrossRefGoogle Scholar
  20. 20.
    Heiskanen-Kosma T, Korppi M, Jokinen C, Kurki S, Heiskanen L, Juvonen H, Kallinen S, Sten M, Tarkiainen A, Rönnberg PR, Kleemola M, Mäkelä PH, Leinonen M (1998) Etiology of childhood pneumonia: serologic results of a prospective, population-based study. Pediatr Infect Dis J 17:986–991PubMedCrossRefGoogle Scholar
  21. 21.
    Wubbel L, Muniz L, Ahmed A, Trujillo M, Carubelli C, McCoig C, Abramo T, Leinonen M, McCracken GH Jr (1999) Etiology and treatment of community-acquired pneumonia in ambulatory children. Pediatr Infect Dis J 18:98–104PubMedCrossRefGoogle Scholar
  22. 22.
    Juven T, Mertsola J, Waris M, Leinonen M, Meurman O, Roibainen M, Eskola J, Saikku P, Ruuskanen O (2000) Etiology of community-acquired pneumonia in 254 hospitalized children. Pediatr Infect Dis J 19:293–298PubMedCrossRefGoogle Scholar
  23. 23.
    Michelow IC, Lozano J, Olsen K, Goto C, Rollins NK, Ghaffar F, Rodriguez-Cerrato V, Leinonen M, McCracken GH Jr (2002) Diagnosis of Streptococcus pneumoniae lower respiratory infection in hospitalized children by culture, polymerase chain reaction, serological testing, and urinary antigen detection. Clin Infect Dis 34:e1-e11, (
  24. 24.
    Korppi M, Launiala K, Leinonen M, Häkelä PH (1990) Bacterial involvement in laryngeal infections in children. Acta Paediatr Scand 79:564–565PubMedCrossRefGoogle Scholar
  25. 25.
    Mäkelä MJ, Puhakka T, Ruuskanen O, Leinonen M, Saikku P, Kimpimäki M, Blomqvist S, Hyypiä T, Arstila P (1998) Viruses and bacteria in the etiology of the common cold. J Clin Microbiol 36:539–542PubMedGoogle Scholar
  26. 26.
    Nohynek H, Eskola J, Kleemola M, Jalonen E, Saikku P, Leinonen M (1995) Bacterial antibody assays in the diagnosis of acute lower respiratory tract infection in children. Pediatr Infect Dis J 14:478–484PubMedCrossRefGoogle Scholar
  27. 27.
    Virolainen A, Jero J, Chattopadhyay P, Karma P, Eskola J, Leinonen M (1996) Comparison of serum antibodies to pneumolysin with those to pneumococcal capsular polysaccharides in children with acute otitis media. Pediatr Infect Dis J 15:128–133PubMedCrossRefGoogle Scholar
  28. 28.
    Rapola S, Jäntti V, Haikala R, Syrjänen R, Carlone GM, Sampson JS, Briles DE, Paton JC, Takala AK, Kilpi TM, Käyhty H (2000) Natural development of antibodies to pneumococcal surface protein A, pneumococcal surface adhesin A, and pneumolysin in relation to pneumococcal carriage and acute otitis media. J Infect Dis 182:1146-1152, ( - fn1)PubMedCrossRefGoogle Scholar
  29. 29.
    Freymuth F, Vabret A, Brouard J, Toutain F, Verdon R, Petitjean J, Gouarin S, Duhamel J, Guillois B (1999) Detection of viral, Chlamydia pneumoniae and Mycoplasma pneumoniae infections in exacerbations of asthma in children. J Clin Virol 13:131–139PubMedCrossRefGoogle Scholar
  30. 30.
    Esposito S, Blasi F, Arosio C, Fioravanti L, Fagetti L, Droghetti R, Tarsia P, Allegra L, Principi N (2000) Importance of acute Mycoplasma pneumoniae and Chlamydia pneumoniae infections in children with wheezing. Eur Respir J 16:1142–1146PubMedCrossRefGoogle Scholar
  31. 31.
    Biscardi S, Lorrot M, Marc E, Moulin F, Boutonnat-Faucher B, Heilbronner C, Iniquez JL, Chaussain M, Nicand E, Raymond J, Gendrel D (2004) Mycoplasma pneumoniae and asthma in children. Clin Infect Dis 38:1341–1346PubMedCrossRefGoogle Scholar
  32. 32.
    Ruuskanen O, Putto A, Sarkkinen H, Meurman O, Irjala K (1985) C-reactive protein in respiratory virus infections. J Pediatr 107:97–100PubMedCrossRefGoogle Scholar
  33. 33.
    Putto A, Ruuskanen O, Meurman O, Ekblad H, Korvenranta H, Mertsola J, Peltola H, Sarkkinen H, Viljanen MK, Halonen P (1986) C-reactive protein in the evaluation of febrile illness. Arch Dis Child 61:24–29PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • P. Lehtinen
    • 1
  • T. Jartti
    • 1
  • R. Virkki
    • 2
  • T. Vuorinen
    • 3
  • M. Leinonen
    • 4
  • V. Peltola
    • 1
  • A. Ruohola
    • 1
  • O. Ruuskanen
    • 1
    Email author
  1. 1.Department of PediatricsTurku University HospitalTurkuFinland
  2. 2.Department of RadiologyTurku University HospitalTurkuFinland
  3. 3.Department of VirologyUniversity of TurkuTurkuFinland
  4. 4.National Public Health InstituteOuluFinland

Personalised recommendations