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. 1993;152(1):24–30. doi: 10.1007/BF02072512

Aetiology of community-acquired pneumonia in children treated in hospital

M Korppi 1,, T Heiskanen-Kosma 1, E Jalonen 2, P Saikku 3, M Leinonen 2, P Halonen 4, P H Mäkela 2
PMCID: PMC7087117  PMID: 8444202

Abstract

Viral and bacterial antigen and antibody assays were prospectively applied to study the microbial actiology of community-acquired pneumonia in 195 hospitalised children during a surveillance period of 12 months. A viral infection alone was indicated in 37 (19%), a bacterial infection alone in 30 (15%) and a mixed viral-bacterial infection in 32 (16%) patients. Thus, 46% of the 69 patients with viral infection and 52% of the 62 patients with bacterial infection had a mixed viral and bacterial aetiology. Respiratory syncytial virus (RSV) was identified in 52 patients andStreptococcus pneumoniae in 41 patients. The next common agents in order were non-classifiedHaemophilus influenzae (17 cases), adenoviruses (10 cases) andChlamydia species (8 cases). The diagnosis of an RSV infection was based on detecting viral antigen in nasopharyngeal secretions in 79% of the cases. Pneumococcal infections were in most cases identified by antibody assays; in 39% they were indicated by demonstrating pneumococcal antigen in acute phase serum. An alveolar infiltrate was present in 53 (27%) and an interstitial infiltrate in 108 (55%) of the 195 patients. The remaining 34 patients had probable pneumonia. C-reactive protein (CRP), erythrocyte sedimentation rate and total white blood cell count were elevated in 25%, 40% and 36% of the patients, respectively, CRP was more often elevated in patients with bacterial infection alone than in those with viral or mixed viral-bacterial infections. No other correlation was seen between the radiological or laboratory findings and serologically identified viral, bacterial or mixed viralbacterial infections. By using a comprehensive serological panel, the causative agent could be found in over 50% of patients with pneumonia. We conclude that RSV and pneumococcus are the two most common organisms causing pneumonia in children. Our results suggest that mixed viral-bacterial aetiology is common in lower respiratory tract infections affecting children.

Key words: Pneumonia, Respiratory syncytial virus, Pneumococcus, Enzyme immunoassay, Radioimmunoassay

Abbreviations

AOM

acute otitis media

CF

complement fixation

EIA

enzyme immunoassay

IF

immunofluorescence

NPS

nasopharyngeal secretion

PNC

pneumococcal

PV

parainfluenza

RSV

respiratory syncytial virus

References

  • 1.Aldous MB, Wang S, Foy HM, Grayston JT (1990)Chlamydia pneumoniae, strain TWAR, infection in Seattle children and their families, 1965–1979. In: Bowie et al (eds) Chlamydial Infections, Cambridge University Press
  • 2.Arstila P, Halonen P. Direct antigen detection. In: Lennette EH, Halonen P, Murphy FA, editors. Laboratory diagnosis of infectious disease; principles and practice, vol. II, viral, rickettsial, and chlamydial diseases. Berlin Heidelberg New York: Springer; 1988. pp. 60–75. [Google Scholar]
  • 3.Chang M, Rodriquez W, Mohla C. Chlamydia trachomatis in otitis media in children. Pediatr Infect Dis. 1982;1:95–97. doi: 10.1097/00006454-198203000-00006. [DOI] [PubMed] [Google Scholar]
  • 4.Claesson BA, Trollfors B, Brolin J, et al. Etiology community-acquired pneumonia in children based on antibody responses to bacterial and viral antigens. Pediatr Infect Dis J. 1989;8:856–862. doi: 10.1097/00006454-198912000-00006. [DOI] [PubMed] [Google Scholar]
  • 5.Coch WM. Bronchitis and pneumonia in ambulatory patients. Pediatr Infect Dis J. 1987;6:137–140. doi: 10.1097/00006454-198701000-00055. [DOI] [PubMed] [Google Scholar]
  • 6.Degre M. Interaction between viral and bacterial infections in the respiratory tract. Scand J Infect Dis. 1986;49:140–145. [PubMed] [Google Scholar]
  • 7.Halonen P, Obert G, Hierholzer JC. Direct detection of viral antigens in respiratory infections by immunoassays: a four year experience and new development. In: de la Maza LM, Peterson EM, editors. Medical virology IV. Hillsdale: Lawrence Erlbaum Associates Publishers; 1985. pp. 65–85. [Google Scholar]
  • 8.Hammerschlag M, Hammerschlag P, Russel EA. The role of Chlamydia trachomatis in middle ear effusions in children. Pediatrics. 1980;66:615–617. [PubMed] [Google Scholar]
  • 9.Hawkes RA. General principles underlying laboratory diagnosis of viral infections. In: Lennette EH, Schmidt NJ, editors. Diagnostic procedures for viral, rickettsial and chlamydial infections. 5th edn. Washington DC: American Public Health Association; 1979. pp. 35–42. [Google Scholar]
  • 10.Hietala J, Uhari M, Tuokko H. Antigen detection in the diagnosis of viral infections. Scand J Infect Dis. 1988;20:595–599. doi: 10.3109/00365548809035659. [DOI] [PubMed] [Google Scholar]
  • 11.Hietala J, Uhari M, Tuokko H, Leinonen M. Mixed viral and bacterial infections are common in children. Pediatr Infect Dis J. 1989;8:683–686. doi: 10.1097/00006454-198910000-00004. [DOI] [PubMed] [Google Scholar]
  • 12.Isaacs D. Problems in determining the etiology of community-acquired childhood pneumonia. Pediatr Infect Dis J. 1989;8:143–148. [PubMed] [Google Scholar]
  • 13.Jalonen E, Paton J, Koskela M, Kerttula Y, Leinonen M. Measurement of antibody responses to pneumolysin —a promising diagnosis of pneumococcal pneumonia. J Infect. 1989;19:127–134. doi: 10.1016/s0163-4453(89)91864-1. [DOI] [PubMed] [Google Scholar]
  • 14.Kalin M, Lindberg AA. Diagnosis of pneumococcal pneumonia: a comparison between microscopic examination of expectorates, antigen detection and cultural procedures. Scand J Infect Dis. 1983;15:247–255. doi: 10.3109/inf.1983.15.issue-3.04. [DOI] [PubMed] [Google Scholar]
  • 15.Kalin M, Lindberg AA, Olausson EH. Diagnosis of pneumococcal pneumonia by coagglutination and counterimmunoelectrophoresis of sputum samples. Eur J Clin Microbiol. 1982;1:91–96. doi: 10.1007/BF02014198. [DOI] [PubMed] [Google Scholar]
  • 16.Kanclercki K, Blomqvist S, Granström Möllby R. Serum antibodies to pneumolysin in patients with pneumonia. J Clin Microbiol. 1988;26:96–100. doi: 10.1128/jcm.26.1.96-100.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Kerttula Y, Leinonen M, Koskela M, et al. The aetiology of pneumonia. Application of bacterial serology and basic laboratory methods. J Infect. 1987;14:21–30. doi: 10.1016/s0163-4453(87)90730-4. [DOI] [PubMed] [Google Scholar]
  • 18.Korppi M, Halonen P, Kleemola M, Launiala K. Viral findings in children under the age of two years with expiratory difficulties. Acta Paediatr Scand. 1986;75:457–464. doi: 10.1111/j.1651-2227.1986.tb10230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Korppi M, Halonen P, Kleemola M, Launiala K. The role of parainfluenza viruses in inspiratory difficulties in children. Acta Paediatr Scand. 1988;77:105–111. doi: 10.1111/j.1651-2227.1988.tb10607.x. [DOI] [PubMed] [Google Scholar]
  • 20.Korppi M, Leinonen M, Mäkelä PH, Launiala K. Bacterial coinfection in children hospitalized with respiratory syncytial virus infections. Pediatr Infect Dis J. 1989;8:687–692. doi: 10.1097/00006454-198910000-00005. [DOI] [PubMed] [Google Scholar]
  • 21.Korppi M, Leinonen M, Mäkelä PH, Launiala K. Bacterial involvement in parainfluenza virus infection in children. Scand J Infect Dis. 1990;22:307–312. doi: 10.3109/00365549009027052. [DOI] [PubMed] [Google Scholar]
  • 22.Korppi M, Leinonen M, Mäkelä PH, Launiala K. Mixed infection is common in children with respiratory adenovirus infection. Acta Paediatr Scand. 1991;80:413–417. doi: 10.1111/j.1651-2227.1991.tb11875.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Koskela M. Serum antibodies to pneumococcal C-polysaccharide in children: a response to acute pneumococcal otitis media or to vaccination. Pediatr Infect Dis J. 1987;6:519–526. doi: 10.1097/00006454-198706000-00006. [DOI] [PubMed] [Google Scholar]
  • 24.Koskela M, Leinonen M, Luotonen J. Serum antibody response to pneumococcal otitis media. Pediatr Infect Dis. 1982;1:245–252. doi: 10.1097/00006454-198207000-00013. [DOI] [PubMed] [Google Scholar]
  • 25.Koskela M, Leinonen M, Häivä V-M, Timonen M, Mäkelä PH. First and second dose antibody responses to pneumococcal polysaccaride vaccine in infants. Pediatr Infect Dis. 1986;5:45–50. doi: 10.1097/00006454-198601000-00009. [DOI] [PubMed] [Google Scholar]
  • 26.Lancet: Editorial (1982) How does influenza pave the way for bacteria? Lancet I:485–486 [DOI] [PubMed]
  • 27.Lehtomäki K, Leinonen M, Takala A, Hovi T, Herva E, Koskela M. Etiological diagnosis of pneumonia in military conscripts by combined use of bacterial culture and serological methods. Eur J Clin Microbiol Infect Dis. 1988;7:348–354. doi: 10.1007/BF01962335. [DOI] [PubMed] [Google Scholar]
  • 28.Leinonen MK. Detection of pneumococcal capsular polysaccharide antigens by latex agglutination, counterimmunoelectrophoresis, and radioimmunoassay in middle ear exudates in acute otitis media. J Clin Microbiol. 1980;11:135–140. doi: 10.1128/jcm.11.2.135-140.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Leinonen M, Luotonen J, Herva E, Valkonen K, Mäkelä PH. Preliminary serologic evidence for a pathogenic role ofBranhamella catarrhalis. J Infect Dis. 1981;144:570–574. doi: 10.1093/infdis/144.6.570. [DOI] [PubMed] [Google Scholar]
  • 30.Leinonen M, Säkkinen A, Kalliokoski R, Luotonen J, Timonen M, Mäkelä PH. Antibody response to 14-valent pneumococcal capsular polysaccharide vaccine in preschool age children. Pediatr Infect Dis. 1986;5:39–44. doi: 10.1097/00006454-198601000-00008. [DOI] [PubMed] [Google Scholar]
  • 31.Loda FA, Collier AM, Glezen WP, Strangert K, Clyde WA, Denny FW. Occurrence ofDiplococcus pneumoniae in the upper respiratory tract of children. J Pediatr. 1975;87:1087–1093. doi: 10.1016/s0022-3476(75)80120-x. [DOI] [PubMed] [Google Scholar]
  • 32.Meurman O, Ruuskanen O, Sarkkinen H, Hänninen P, Halonen P. Immunoglobulin class-specific antibody response in respiratory syncytial virus infection measured by enzyme immunoassay. J Med Virol. 1984;14:67–72. doi: 10.1002/jmv.1890140110. [DOI] [PubMed] [Google Scholar]
  • 33.Nohynek H, Eskola J, Laine E, Halonen P, Ruutu P, Saikku P, Kleemola M, Leinonen M. The etiology of hospitaltreated acute lower respiratory tract infection in children. Am J Dis Child. 1991;145:618–622. doi: 10.1001/archpedi.1991.02160060036016. [DOI] [PubMed] [Google Scholar]
  • 34.Ogawa H, Hashigucki K, Kazuyama Y. Isolation of chlamydia trachomatis from the middle ear aspirates of otitis media. Acta Otolaryngol (Stockholm) 1990;110:105–109. doi: 10.3109/00016489009122522. [DOI] [PubMed] [Google Scholar]
  • 35.Payne R. Aetiology of pneumonia in children in Goroka Hospital, Papua New Guinea. Lancet. 1984;II:537–541. doi: 10.1016/s0140-6736(84)90764-5. [DOI] [PubMed] [Google Scholar]
  • 36.Peter G. The child with pneumonia: diagnostic and therapeutic considerations. Pediatr Infect Dis J. 1988;7:453–456. doi: 10.1097/00006454-198806000-00035. [DOI] [PubMed] [Google Scholar]
  • 37.Puolakkainen M, Saikku P, Leinonen M, Nurminen M, Väänanen P, Mäkelä PH. Chlamydial pneumonitis and its serodiagnosis in infants. J Infect Dis. 1984;149:598–604. doi: 10.1093/infdis/149.4.598. [DOI] [PubMed] [Google Scholar]
  • 38.Putto A, Ruuskanen O, Meurman O, et al. C-reactive protein in the evaluation of febrile illness. Arch Dis Child. 1986;61:24–29. doi: 10.1136/adc.61.1.24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Ramsey BW, Marcuse EK, Foy HM, et al. Use of bactetial antigen detection in the diagnosis of pediatric lower respiratory tract infections. Pediatrics. 1986;78:1–9. [PubMed] [Google Scholar]
  • 40.Rusconi F, Rancilio L, Assael BM, et al. Counterimmunoelectrophoresis and latex particle agglutination in the etiologic diagnosis of presumed bacterial pneumonia in pediatric patients. Pediatr Infect Dis J. 1988;7:781–785. doi: 10.1097/00006454-198811000-00007. [DOI] [PubMed] [Google Scholar]
  • 41.Saikku P, Ruutu P, Leinonen M, Panelius J, Tupasi TE, Grayston JT. Acute lower-respiratory-tract infection associated with chlamydial TWAR antibody in Filipino children. J Infect Dis. 1988;158:1095–1097. doi: 10.1093/infdis/158.5.1095. [DOI] [PubMed] [Google Scholar]
  • 42.Sarkkinen HK, Halonen PE, Arstila PP, Salmi AA. Detection of respiratory syncytial, parainfluenza type 2, and adenovirus antigens by radioimmunoassay and enzyme immunoassay in nasopharyngeal specimens from children with acute respiratory disease. J Clin Microbiol. 1981;13:256–265. doi: 10.1128/jcm.13.2.258-265.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Sarkkinen HK, Halonen PE, Salmi AA. Detection of influenza A virus by radioimmunoassay and enzyme immunoassay from nasopharyngeal specimens. J Med Virol. 1981;17:213–220. doi: 10.1002/jmv.1890070305. [DOI] [PubMed] [Google Scholar]
  • 44.Sarkkinen HK, Halonen PE, Salmi AA. Type specific detection of parainfluenza viruses by enzyme immunoassay and radioimmunoassay in nasopharyngeal specimens of patients with acute respiratory disease. J Gen Virol. 1981;56:49–57. doi: 10.1099/0022-1317-56-1-49. [DOI] [PubMed] [Google Scholar]
  • 45.Schultzer S, Coyle PK, Belman AL, Golighty MG, Drulle J. Sequestration of antibodies toBorrelia burgdorferi in immune complexes in seronegative Lyme disease. Lancet. 1990;335:312–315. doi: 10.1016/0140-6736(90)90606-6. [DOI] [PubMed] [Google Scholar]
  • 46.Silverman M, Stratton D, Dialo A, et al. Diagnosis of acute bacterial pneumonia in Nigerian Children. Arch Dis Child. 1977;52:925–931. doi: 10.1136/adc.52.12.925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Similä S, Linna O, Lanning P, Heikkinen E, Ala-Houhala M. Chronic lung damage caused by adenovirus type 7: a ten-year follow-up study. Chest. 1981;80:127–131. doi: 10.1378/chest.80.2.127. [DOI] [PubMed] [Google Scholar]
  • 48.Teele DW, Pelton SI, Grant MJA. Bacteremia in febrile children under 2 years of age: Results of cultures of blood in 600 consecutive children seen in a “walk-in” clinic. J Pediatr. 1975;87:227–230. doi: 10.1016/s0022-3476(75)80584-1. [DOI] [PubMed] [Google Scholar]
  • 49.Trottier S, Stenberg K, Svanborg-Eden C. Turnover of nontypableHaemophilus influenzae in the nasopharynges of healthy children. J Clin Microbiol. 1989;27:1275–1279. doi: 10.1128/jcm.27.10.2175-2179.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Turner RB, Hayden FG, Hendley JO. Counterimmuno-electrophoresis of urine for diagnosis of bacterial pneumonia in pediatric patients. Pediatrics. 1983;71:780–783. [PubMed] [Google Scholar]
  • 51.Ukkonen P, Hovi T, Bonsdorff CH, Saikku P, Penttinen K. Age-specific prevalence of complement-fixing antibodies to sixteen viral antigens: a computer analysis of 58.500 patients covering a period of eight years. J Med Virol. 1984;13:131–148. doi: 10.1002/jmv.1890130204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Wang SP, Grayston JT. Immunologic relationship between genital TRIC, lymphogranuloma venereum, and related organisms in a new microtiter immuno-fluorence test. Am J Ophtalmol. 1970;70:367–374. doi: 10.1016/0002-9394(70)90096-6. [DOI] [PubMed] [Google Scholar]
  • 53.Waris M, Ziegler T, Kiviranta M, Ruuskanen O. Rapid detection of respiratory syncytial virus and influenza A virus in cell cultures by immunoperoxidase staining with monoclonal antibodies. J Clin Microbiol. 1990;28:1159–1162. doi: 10.1128/jcm.28.6.1159-1162.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Weinberg GA, Ghafoor A, Ishag Z, et al. Clonal analysis ofHaemophilus influenzae isolated from children from Pakistan with lower respiratory tract infections. J Infect Dis. 1989;160:634–643. doi: 10.1093/infdis/160.4.634. [DOI] [PubMed] [Google Scholar]
  • 55.Yamasaki T, Nakada H, Sakurai N, Kuo CC, Wang SP, Grayston JT. Transmission ofChlamydia pneumoniae in young children in Japanese family. J Infect Dis. 1990;162:1390–1392. doi: 10.1093/infdis/162.6.1390. [DOI] [PubMed] [Google Scholar]

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