1887

Abstract

In 2016–2017, there was an increase in the number of paediatric invasive pneumococcal disease (IPD) cases caused by serotype 12F in Chiba Prefecture, Japan. Serotype 12F is one of the major causative serotypes of IPD following the introduction of pneumococcal conjugate vaccine 13 (PCV13), and outbreaks of IPD caused by serotype 12F have recently been reported in several countries.

Our goal here was to clarify the relationship among local outbreak strains and the outbreak strains in other countries, and for this we analysed clinical isolates of serotype 12F using several genetic identification methods.

All reported IPD cases caused by serotype 12F were reviewed and bacterial strains were collected and analysed. We also analysed serotype 12F strains isolated from other time periods, geographical areas, cases of adult IPD and respiratory specimens as control strains. Multi-locus sequence typing, PFGE and multi-locus variable number tandem repeat analysis (MLVA) were conducted on all isolates.

All 26 . serotype 12F isolates, including control strains, belonged to a single sequence type (ST4846) that was the specific ST in Japan. All tested strains demonstrated five MLVA patterns and two PFGE patterns.

We determined that the 2016–2017 outbreak of IPD in Chiba Prefecture was caused by clonally related isolates of serotype 12F. The continuous monitoring of IPD caused by serotype 12F is important for evaluating the impact of re-emerging pneumococcal serotypes following the PCV13 introduction era, and MLVA could be a useful tool for identification of outbreak strains.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001047
2019-09-01
2019-09-18
Loading full text...

Full text loading...

References

  1. Lynch JP 3rd, Zhanel GG. Streptococcus pneumoniae: epidemiology, risk factors, and strategies for prevention. Semin Respir Crit Care Med 2009;30:189–209 [CrossRef]
    [Google Scholar]
  2. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH et al. Active bacterial core Surveillance/Emerging infections program network. sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 2010;201:32–41
    [Google Scholar]
  3. Balsells E, Guillot L, Nair H, Kyaw MH. Serotype distribution of Streptococcus pneumoniae causing invasive disease in children in the post-PCV era: A systematic review and meta-analysis. PLoS One 2017;12:e0177113 [CrossRef]
    [Google Scholar]
  4. Suga S, Chang B, Asada K, Akeda H, Nishi J et al. Nationwide population-based surveillance of invasive pneumococcal disease in Japanese children: effects of the seven-valent pneumococcal conjugate vaccine. Vaccine 2015;33:6054–6060 [CrossRef]
    [Google Scholar]
  5. Ubukata K, Takata M, Morozumi M, Chiba N, Wajima T et al. Invasive pneumococcal diseases surveillance study group. Effects of pneumococcal conjugate vaccine on genotypic penicillin resistance and serotype changes, Japan, 2010-2017. Emerg Infect Dis 2018;24:2010–2020
    [Google Scholar]
  6. Saitoh A, Okabe N. Recent progress and concerns regarding the Japanese immunization program: addressing the "vaccine gap". Vaccine 2014;32:4253–4258 [CrossRef]
    [Google Scholar]
  7. Ladhani SN, Collins S, Djennad A, Sheppard CL, Borrow R et al. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000-17: a prospective national observational cohort study. Lancet Infect Dis 2018;18:441–451 [CrossRef]
    [Google Scholar]
  8. Chiba N, Morozumi M, Sunaoshi K, Takahashi S, Takano M et al. Serotype and antibiotic resistance of isolates from patients with invasive pneumococcal disease in Japan. Epidemiol Infect 2010;138:61–68 [CrossRef]
    [Google Scholar]
  9. Rokney A, Ben-Shimol S, Korenman Z, Porat N, Gorodnitzky Z et al. Emergence of Streptococcus pneumoniae Serotype 12F after Sequential Introduction of 7- and 13-Valent Vaccines, Israel. Emerg Infect Dis 2018;24:453–461 [CrossRef]
    [Google Scholar]
  10. Deng X, Peirano G, Schillberg E, Mazzulli T, Gray-Owen SD et al. Whole-genome sequencing reveals the origin and rapid evolution of an emerging outbreak strain of Streptococcus pneumoniae 12F. Clin Infect Dis 2016;62:1126–1132 [CrossRef]
    [Google Scholar]
  11. Schillberg E, Isaac M, Deng X, Peirano G, Wylie JL et al. Outbreak of invasive Streptococcus pneumoniae serotype 12F among a marginalized inner-city population in Winnipeg, Canada, 2009-2011. Clin Infect Dis 2014;59:651–657 [CrossRef]
    [Google Scholar]
  12. Zulz T, Wenger JD, Rudolph K, Robinson DA, Rakov AV et al. Molecular characterization of Streptococcus pneumoniae serotype 12F isolates associated with rural community outbreaks in Alaska. J Clin Microbiol 2013;51:1402–1407 [CrossRef]
    [Google Scholar]
  13. Ikuse T, Habuka R, Wakamatsu Y, Nakajima T, Saitoh N et al. Local outbreak of Streptococcus pneumoniae serotype 12F caused high morbidity and mortality among children and adults. Epidemiol Infect 2018;146:1793–1796 [CrossRef]
    [Google Scholar]
  14. Ishiwada N, Hishiki H, Nagasawa K, Naito S, Sato Y et al. The incidence of pediatric invasive Haemophilus influenzae and pneumococcal disease in Chiba prefecture, Japan before and after the introduction of conjugate vaccines. Vaccine 2014;32:5425–5431 [CrossRef]
    [Google Scholar]
  15. Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing; 26th informational supplement, CLSI M100-S26. Wayne, PA: Clinical and Laboratory Standards Institute; 2016
    [Google Scholar]
  16. Nagai K, Shibasaki Y, Hasegawa K, Davies TA, Jacobs MR et al. Evaluation of PCR primers to screen for Streptococcus pneumoniae isolates and beta-lactam resistance, and to detect common macrolide resistance determinants. J Antimicrob Chemother 2001;48:915–918 [CrossRef]
    [Google Scholar]
  17. Koeck J-L, Njanpop-Lafourcade B-M, Cade S, Varon E, Sangare L et al. Evaluation and selection of tandem repeat loci for Streptococcus pneumoniae MLVA strain typing. BMC Microbiol 2005;5:66 [CrossRef]
    [Google Scholar]
  18. Hoskins J, Alborn WE, Arnold J, Blaszczak LC, Burgett S et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 2001;183:5709–5717 [CrossRef]
    [Google Scholar]
  19. McEllistrem MC, Stout JE, Harrison LH. Simplified protocol for pulsed-field gel electrophoresis analysis of Streptococcus pneumoniae. J Clin Microbiol 2000;38:351–353
    [Google Scholar]
  20. Song JY, Nahm MH, Moseley MA. Clinical implications of pneumococcal serotypes: invasive disease potential, clinical presentations, and antibiotic resistance. J Korean Med Sci 2013;28:4–15 [CrossRef]
    [Google Scholar]
  21. Rakov AV, Ubukata K, Ashley Robinson D, Robinson DA. Population structure of hyperinvasive serotype 12F, clonal complex 218 Streptococcus pneumoniae revealed by multilocus boxB sequence typing. Infection, Genetics and Evolution 2011;11:1929–1939 [CrossRef]
    [Google Scholar]
  22. Hoge CW, Reichler MR, Dominguez EA, Bremer JC, Mastro TD et al. An epidemic of pneumococcal disease in an overcrowded, inadequately ventilated jail. N Engl J Med 1994;331:643–648 [CrossRef]
    [Google Scholar]
  23. Cherian T, Steinhoff MC, Harrison LH, Rohn D, McDougal LK. A cluster of invasive pneumococcal disease in young children in child care. JAMA 1994;271:695–697 [CrossRef]
    [Google Scholar]
  24. Robinson DA, Turner JS, Facklam RR, Parkinson AJ, Breiman RF et al. Molecular characterization of a globally distributed lineage of serotype 12F Streptococcus pneumoniae causing invasive disease. J Infect Dis 1999;179:414–422 [CrossRef]
    [Google Scholar]
  25. Brueggemann AB, Muroki BM, Kulohoma BW, Karani A, Wanjiru E et al. Population genetic structure of Streptococcus pneumoniae in Kilifi, Kenya, prior to the introduction of pneumococcal conjugate vaccine. PLoS One 2013;8:e81539 [CrossRef]
    [Google Scholar]
  26. Del Amo E, Esteva C, Hernandez-Bou S, Galles C, Navarro M et al. Catalan Study Group of Invasive Pneumococcal Disease. Serotypes and clonal diversity of Streptococcus pneumoniae causing invasive disease in the era of PCV13 in Catalonia, Spain. PLoS One 2016;11:e0151125
    [Google Scholar]
  27. Antonio M, Dada-Adegbola H, Biney E, Awine T, O'Callaghan J et al. Molecular epidemiology of pneumococci obtained from Gambian children aged 2-29 months with invasive pneumococcal disease during a trial of a 9-valent pneumococcal conjugate vaccine. BMC Infect Dis 2008;8:81 [CrossRef]
    [Google Scholar]
  28. Izumiya H, Pei Y, Terajima J, Ohnishi M, Hayashi T et al. New system for multilocus variable-number tandem-repeat analysis of the enterohemorrhagic Escherichia coli strains belonging to three major serogroups: O157, O26, and O111. Microbiol Immunol 2010;54:569–577 [CrossRef]
    [Google Scholar]
  29. Dahyot S, Lebeurre J, Argemi X, François P, Lemée L et al. Multiple-Locus variable number tandem repeat analysis (MLVA) and tandem repeat sequence typing (TRST), helpful tools for subtyping Staphylococcus lugdunensis. Sci Rep 2018;8:11669 [CrossRef]
    [Google Scholar]
  30. Martin B, Humbert O, Camara M, Guenzi E, Walker J et al. A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 1992;20:3479–3483 [CrossRef]
    [Google Scholar]
  31. Gutiérrez Rodríguez MA, Ordobás Gavín MA, García-Comas L, Sanz Moreno JC, Córdoba Deorador E et al. Effectiveness of 23-valent pneumococcal polysaccharide vaccine in adults aged 60 years and over in the region of Madrid, Spain, 2008-2011. Euro Surveill 2014;19:20922 [CrossRef]
    [Google Scholar]
  32. Andrews NJ, Waight PA, George RC, Slack MPE, Miller E. Impact and effectiveness of 23-valent pneumococcal polysaccharide vaccine against invasive pneumococcal disease in the elderly in England and Wales. Vaccine 2012;30:6802–6808 [CrossRef]
    [Google Scholar]
  33. Licciardi PV, Balloch A, Russell FM, Burton RL, Lin J et al. Pneumococcal polysaccharide vaccine at 12 months of age produces functional immune responses. J Allergy Clin Immunol 2012;129:794–800 [CrossRef]
    [Google Scholar]
  34. Lo SW, Gladstone RA, van Tonder AJ, Lees JA, du Plessis M et al. Pneumococcal lineages associated with serotype replacement and antibiotic resistance in childhood invasive pneumococcal disease in the post-PCV13 era: an international whole-genome sequencing study. Lancet Infect Dis 2019;19:759–769 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001047
Loading
/content/journal/jmm/10.1099/jmm.0.001047
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error