Epidemiology of Streptococcus pneumoniae in France before introduction of the PCV-13 vaccine

  • N. Grall
  • O. Hurmic
  • M. Al Nakib
  • M. Longo
  • C. Poyart
  • M.-C. Ploy
  • E. Varon
  • J. Raymond
  • ORP Ile de France Ouest


The purpose of this article was to describe the serotype incidence and antibiotic susceptibility of Streptococcus pneumoniae strains isolated from adults and children with invasive disease (IPD) or acute otitis media (AOM) before introduction of the 13-valent pneumococcal vaccine. During 2009, 494 strains of S. pneumoniae isolated were collected. Complete serotyping by latex antisera and molecular methods was performed. The most frequent serotypes isolated from children with IPD were 1 (26.2%), 19A (25%) and 7F (14.3%). Serotype 19A was predominant (42.1%) in children ≤ 2 years, whereas serotype 1 was predominant (63.3%) after the age of 5. Serotype 19A was the most frequently isolated serotype from AOM (62.3%). In adults, serotypes responsible for IPD were 7F (19.4%), 19A (13.7%), 1 (8.4%) and 3 (7.5%). The serotype 19A was predominant in adults older than 65 years (19.1%). The emergence of serotype 12F was observed in adults. Between 2007 and 2009, the introduction of PCV-7 has resulted in a significant decrease of IPD caused by serotypes included in the vaccine, in children as well as in adults, confirming the herd effect. Serotype coverage of PCV-13 was 70% and 80.9% for adult and children’s IPD, respectively. PCV-13 will be more efficient in preventing invasive diseases among children and adults.


Cefotaxime Acute Otitis Medium Pleural Fluid Invasive Pneumococcal Disease Serotype Distribution 
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.


  1. 1.
    Whitney CG, Farley MM, Hadler J, Harrison LH, Bennett NM, Lynfield R, Reingold A, Cieslak PR, Pilishvili T, Jackson D, Facklam RR, Jorgensen JH, Schuchat A (2003) Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med 348(18):1737–1746PubMedCrossRefGoogle Scholar
  2. 2.
    Lepoutre A, Varon E, Georges S, Gutmann L, Levy-Bruhl D (2008) Impact of infant pneumococcal vaccination on invasive pneumococcal diseases in France, 2001–2006. Euro Surveill 13(35)Google Scholar
  3. 3.
    Agam Y, Hyun JS, Danker JF, Zhou F, Kahana MJ, Sekuler R (2009) Early neural signatures of visual short-term memory. Neuroimage 44(2):531–536PubMedCrossRefGoogle Scholar
  4. 4.
    Lexau CA, Lynfield R, Danila R, Pilishvili T, Facklam R, Farley MM, Harrison LH, Schaffner W, Reingold A, Bennett NM, Hadler J, Cieslak PR, Whitney CG (2005) Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine. JAMA 294(16):2043–2051PubMedCrossRefGoogle Scholar
  5. 5.
    Black S, Shinefield H, Baxter R, Austrian R, Elvin L, Hansen J, Lewis E, Fireman B (2006) Impact of the use of heptavalent pneumococcal conjugate vaccine on disease epidemiology in children and adults. Vaccine 24 Suppl 2:S2-79–80Google Scholar
  6. 6.
    Kyaw MH, Lynfield R, Schaffner W, Craig AS, Hadler J, Reingold A, Thomas AR, Harrison LH, Bennett NM, Farley MM, Facklam RR, Jorgensen JH, Besser J, Zell ER, Schuchat A, Whitney CG (2006) Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med 354(14):1455–1463PubMedCrossRefGoogle Scholar
  7. 7.
    Singleton RJ, Hennessy TW, Bulkow LR, Hammitt LL, Zulz T, Hurlburt DA, Butler JC, Rudolph K, Parkinson A (2007) Invasive pneumococcal disease caused by nonvaccine serotypes among Alaska native children with high levels of 7-valent pneumococcal conjugate vaccine coverage. JAMA 297(16):1784–1792PubMedCrossRefGoogle Scholar
  8. 8.
    Hsu KK, Pelton SI (2003) Heptavalent pneumococcal conjugate vaccine: current and future impact. Expert Rev Vaccines 2(5):619–631PubMedCrossRefGoogle Scholar
  9. 9.
    Hicks LA, Harrison LH, Flannery B, Hadler JL, Schaffner W, Craig AS, Jackson D, Thomas A, Beall B, Lynfield R, Reingold A, Farley MM, Whitney CG (2007) Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998–2004. J Infect Dis 196(9):1346–1354PubMedCrossRefGoogle Scholar
  10. 10.
    Dortet L, Ploy MC, Poyart C, Raymond J (2009) Emergence of Streptococcus pneumoniae of serotype 19A in France: molecular capsular serotyping, antimicrobial susceptibilities, and epidemiology. Diagn Microbiol Infect Dis 65(1):49–57PubMedCrossRefGoogle Scholar
  11. 11.
    Moore MR, Gertz RE Jr, Woodbury RL, Barkocy-Gallagher GA, Schaffner W, Lexau C, Gershman K, Reingold A, Farley M, Harrison LH, Hadler JL, Bennett NM, Thomas AR, McGee L, Pilishvili T, Brueggemann AB, Whitney CG, Jorgensen JH, Beall B (2008) Population snapshot of emergent Streptococcus pneumoniae serotype 19A in the United States, 2005. J Infect Dis 197(7):1016–1027PubMedCrossRefGoogle Scholar
  12. 12.
    Pai R, Moore MR, Pilishvili T, Gertz RE, Whitney CG, Beall B (2005) Postvaccine genetic structure of Streptococcus pneumoniae serotype 19A from children in the United States. J Infect Dis 192(11):1988–1995PubMedCrossRefGoogle Scholar
  13. 13.
    Romney MG, Hull MW, Gustafson R, Sandhu J, Champagne S, Wong T, Nematallah A, Forsting S, Daly P (2008) Large community outbreak of Streptococcus pneumoniae serotype 5 invasive infection in an impoverished, urban population. Clin Infect Dis 47(6):768–774PubMedCrossRefGoogle Scholar
  14. 14.
    Dagan R, Gradstein S, Belmaker I, Porat N, Siton Y, Weber G, Janco J, Yagupsky P (2000) An outbreak of Streptococcus pneumoniae serotype 1 in a closed community in southern Israel. Clin Infect Dis 30(2):319–321PubMedCrossRefGoogle Scholar
  15. 15.
    Brueggemann AB, Griffiths DT, Meats E, Peto T, Crook DW, Spratt BG (2003) Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis 187(9):1424–1432PubMedCrossRefGoogle Scholar
  16. 16.
    Shouval DS, Greenberg D, Givon-Lavi N, Porat N, Dagan R (2006) Site-specific disease potential of individual Streptococcus pneumoniae serotypes in pediatric invasive disease, acute otitis media and acute conjunctivitis. Pediatr Infect Dis J 25(7):602–607PubMedCrossRefGoogle Scholar
  17. 17.
    Pai R, Gertz RE, Beall B (2006) Sequential multiplex PCR approach for determining capsular serotypes of Streptococcus pneumoniae isolates. J Clin Microbiol 44(1):124–131PubMedCrossRefGoogle Scholar
  18. 18.
    Hammitt LL, Bruden DL, Butler JC, Baggett HC, Hurlburt DA, Reasonover A, Hennessy TW (2006) Indirect effect of conjugate vaccine on adult carriage of Streptococcus pneumoniae: an explanation of trends in invasive pneumococcal disease. J Infect Dis 193(11):1487–1494PubMedCrossRefGoogle Scholar
  19. 19.
    Aguiar SI, Serrano I, Pinto FR, Melo-Cristino J, Ramirez M (2008) Changes in Streptococcus pneumoniae serotypes causing invasive disease with non-universal vaccination coverage of the seven-valent conjugate vaccine. Clin Microbiol Infect 14(9):835–843PubMedCrossRefGoogle Scholar
  20. 20.
    Whitney CG, Pilishvili T, Farley MM, Schaffner W, Craig AS, Lynfield R, Nyquist AC, Gershman KA, Vazquez M, Bennett NM, Reingold A, Thomas A, Glode MP, Zell ER, Jorgensen JH, Beall B, Schuchat A (2006) Effectiveness of seven-valent pneumococcal conjugate vaccine against invasive pneumococcal disease: a matched case-control study. Lancet 368(9546):1495–1502PubMedCrossRefGoogle Scholar
  21. 21.
    Kaplan SL, Barson WJ, Lin PL, Stovall SH, Bradley JS, Tan TQ, Hoffman JA, Givner LB, Mason EO Jr (2010) Serotype 19A is the most common serotype causing invasive pneumococcal infections in children. Pediatrics 125(3):429–436PubMedCrossRefGoogle Scholar
  22. 22.
    Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, Bennett NM, Reingold A, Thomas A, Schaffner W, Craig AS, Smith PJ, Beall BW, Whitney CG, Moore MR (2010) Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 201(1):32–41PubMedCrossRefGoogle Scholar
  23. 23.
    Raymond J, Le Thomas I, Moulin F, Commeau A, Gendrel D, Berche P (2000) Sequential colonization by Streptococcus pneumoniae of healthy children living in an orphanage. J Infect Dis 181(6):1983–1988PubMedCrossRefGoogle Scholar
  24. 24.
    Choi EH, Kim SH, Eun BW, Kim SJ, Kim NH, Lee J, Lee HJ (2008) Streptococcus pneumoniae serotype 19A in children, South Korea. Emerg Infect Dis 14(2):275–281PubMedCrossRefGoogle Scholar
  25. 25.
    Kellner JD, Vanderkooi OG, MacDonald J, Church DL, Tyrrell GJ, Scheifele DW (2009) Changing epidemiology of invasive pneumococcal disease in Canada, 1998–2007: update from the Calgary-area Streptococcus pneumoniae research (CASPER) study. Clin Infect Dis 49(2):205–212PubMedCrossRefGoogle Scholar
  26. 26.
    Hoge CW, Reichler MR, Dominguez EA, Bremer JC, Mastro TD, Hendricks KA, Musher DM, Elliott JA, Facklam RR, Breiman RF (1994) An epidemic of pneumococcal disease in an overcrowded, inadequately ventilated jail. N Engl J Med 331(10):643–648PubMedCrossRefGoogle Scholar
  27. 27.
    Hausdorff WP (2007) The roles of pneumococcal serotypes 1 and 5 in paediatric invasive disease. Vaccine 25(13):2406–2412PubMedCrossRefGoogle Scholar
  28. 28.
    Gray BM, Converse GM 3rd, Dillon HC Jr (1980) Epidemiologic studies of Streptococcus pneumoniae in infants: acquisition, carriage, and infection during the first 24 months of life. J Infect Dis 142(6):923–933PubMedCrossRefGoogle Scholar
  29. 29.
    Henriques-Normark B, Blomberg C, Dagerhamn J, Battig P, Normark S (2008) The rise and fall of bacterial clones: Streptococcus pneumoniae. Nat Rev Microbiol 6(11):827–837PubMedCrossRefGoogle Scholar
  30. 30.
    He X, McDaniel LS (2007) The genetic background of Streptococcus pneumoniae affects protection in mice immunized with PspA. FEMS Microbiol Lett 269(2):189–195PubMedCrossRefGoogle Scholar
  31. 31.
    Weatherholtz R, Millar EV, Moulton LH, Reid R, Rudolph K, Santosham M, O'Brien KL (2010) Invasive pneumococcal disease a decade after pneumococcal conjugate vaccine use in an American Indian population at high risk for disease. Clin Infect Dis 50(9):1238–1246PubMedCrossRefGoogle Scholar
  32. 32.
    Melegaro A, Choi YH, George R, Edmunds WJ, Miller E, Gay NJ (2010) Dynamic models of pneumococcal carriage and the impact of the Heptavalent Pneumococcal Conjugate Vaccine on invasive pneumococcal disease. BMC Infect Dis 10:90PubMedCrossRefGoogle Scholar
  33. 33.
    Nuorti JP, Whitney CG (2010) Prevention of pneumococcal disease among infants and children - use of 13-valent pneumococcal conjugate vaccine and 23-valent pneumococcal polysaccharide vaccine - recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 59(RR-11):1–18PubMedGoogle Scholar
  34. 34.
    Chiba N, Morozumi M, Sunaoshi K, Takahashi S, Takano M, Komori T, Sunakawa K, Ubukata K (2010) Serotype and antibiotic resistance of isolates from patients with invasive pneumococcal disease in Japan. Epidemiol Infect 138(1):61–68PubMedCrossRefGoogle Scholar
  35. 35.
    Shouval DS, Greenberg D, Givon-Lavi N, Porat N, Dagan R (2009) Serotype coverage of invasive and mucosal pneumococcal disease in Israeli children younger than 3 years by various pneumococcal conjugate vaccines. Pediatr Infect Dis J 28(4):277–282PubMedCrossRefGoogle Scholar
  36. 36.
    Guzvinec M, Tesovic G, Tambic-Andrasevic A, Zidovec-Lepej S, Vukic BT, Begovac J (2008) The epidemiology of invasive Streptococcus pneumoniae disease in Croatian children. Med Sci Monit 14(12):PH59–PH64PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • N. Grall
    • 1
  • O. Hurmic
    • 1
  • M. Al Nakib
    • 1
  • M. Longo
    • 1
  • C. Poyart
    • 1
  • M.-C. Ploy
    • 2
  • E. Varon
    • 3
  • J. Raymond
    • 1
  • ORP Ile de France Ouest
  1. 1.Faculté de Médecine Paris Descartes, Service de Bactériologie, Groupe Hospitalier Cochin-Broca-Hôtel-DieuParisFrance
  2. 2.CHU Limoges, ORP LimousinLimogesFrance
  3. 3.Centre National de Référence des Pneumocoques, Hôpital Georges PompidouUniversity Paris DescartesParis 15France

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