Skip to main content

Advertisement

Log in

Genetic diversity of fluoroquinolone-nonsusceptible Streptococcus pneumoniae clinical isolates and the first identification of serotype 20B in China

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The purpose of this study was to investigate the genetic characteristics of fluoroquinolone-nonsusceptible Streptococcus pneumoniae clinical isolates in China. A total of 377 S. pneumoniae clinical isolates, including 307 pediatric strains and 70 adult strains, were collected from eight centers in China. The minimal inhibitory concentrations (MICs) of 10 antimicrobial agents were determined by agar dilution. Multilocus sequence typing (MLST), serotyping, and quinolone resistance-determining region (QRDR) variations were conducted in levofloxacin-nonsusceptible isolates by polymerase chain reaction (PCR)-based methods. Seven levofloxacin-nonsusceptible isolates were found, with an overall resistance rate of 1.9 % (7/377) and 8.6 % (6/70) in adults. Sequence analyses of parC, gyrA, and parE QRDRs in levofloxacin-resistant isolates demonstrated mutations in dual target sites at the hot spots. These seven strains represented multiple clones: two strains were serotype 19F (Taiwan19F-14) and MLST clonal complex (CC) 271/320, two were typed as 23F (Spain23F-1) and CC81, two were determined as serotype 20B and a new sequence type of ST6935, and one non-serotypeable pediatric strain belonged to a new sequence type of ST6946. Two serotype 19F strains possessed a variety of characteristic alterations of viridans group streptococci in gyrA (Ser114Gly) or parC (Ser52Gly, Asn91Asp). Fluoroquinolone-nonsusceptible S. pneumoniae isolates showed a substantial degree of genetic diversity and belonged to pre-existing epidemic clones together with native clones. S. pneumoniae strains with serotype 20B was recovered for the first time to be associated with levofloxacin resistance in China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. 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):1346–1354

    Article  PubMed  Google Scholar 

  2. Calix JJ, Porambo RJ, Brady AM, Larson TR, Yother J, Abeygunwardana C, Nahm MH (2012) Biochemical, genetic, and serological characterization of two capsule subtypes among Streptococcus pneumoniae serotype 20 strains: discovery of a new pneumococcal serotype. J Biol Chem 287(33):27885–27894

    Article  CAS  PubMed  Google Scholar 

  3. Song JH, Jung SI, Ko KS, Kim NY, Son JS, Chang HH, Ki HK, Oh WS, Suh JY, Peck KR, Lee NY, Yang Y, Lu Q, Chongthaleong A, Chiu CH, Lalitha MK, Perera J, Yee TT, Kumarasinghe G, Jamal F, Kamarulzaman A, Parasakthi N, Van PH, Carlos C, So T, Ng TK, Shibl A (2004) High prevalence of antimicrobial resistance among clinical Streptococcus pneumoniae isolates in Asia (an ANSORP study). Antimicrob Agents Chemother 48(6):2101–2107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Canton R, Morosini M, Enright MC, Morrissey I (2003) Worldwide incidence, molecular epidemiology and mutations implicated in fluoroquinolone-resistant Streptococcus pneumoniae: data from the global PROTEKT surveillance programme. J Antimicrob Chemother 52(6):944–952

    Article  CAS  PubMed  Google Scholar 

  5. Fuller JD, Low DE (2005) A review of Streptococcus pneumoniae infection treatment failures associated with fluoroquinolone resistance. Clin Infect Dis 41(1):118–121

    Article  PubMed  Google Scholar 

  6. Xue L, Yao K, Xie G, Zheng Y, Wang C, Shang Y, Wang H, Wan L, Liu L, Li C, Ji W, Xu X, Wang Y, Xu P, Liu Z, Yu S, Yang Y (2010) Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae isolates that cause invasive disease among chinese children. Clin Infect Dis 50(5):741–744

    Article  PubMed  Google Scholar 

  7. Yang F, Xu X-G, Yang M-J, Zhang Y-Y, Klugman KP, McGee L (2008) Antimicrobial susceptibility and molecular epidemiology of Streptococcus pneumoniae isolated from Shanghai, China. Int J Antimicrob Agents 32(5):386–391

    Article  PubMed  Google Scholar 

  8. Zhang B, Gertz RE Jr, Liu Z, Li Z, Fu W, Beall B (2012) Characterization of highly antimicrobial-resistant clinical pneumococcal isolates recovered in a Chinese hospital during 2009–2010. J Med Microbiol 61(Pt 1):42–48

    Article  PubMed  Google Scholar 

  9. Richter SS, Heilmann KP, Beekmann SE, Miller NJ, Rice CL, Doern GV (2005) The molecular epidemiology of Streptococcus pneumoniae with quinolone resistance mutations. Clin Infect Dis 40(2):225–235

    Article  CAS  PubMed  Google Scholar 

  10. de la Campa AG, Balsalobre L, Ardanuy C, Fenoll A, Pérez-Trallero E, Liñares J; Spanish Pneumococcal Infection Study Network G03/103 (2004) Fluoroquinolone resistance in penicillin-resistant Streptococcus pneumoniae clones, Spain. Emerg Infect Dis 10(10):1751–1759

    Article  PubMed  Google Scholar 

  11. Chen DK, McGeer A, de Azavedo JC, Low DE; Canadian Bacterial Surveillance Network (1999) Decreased susceptibility of Streptococcus pneumoniae to fluoroquinolones in Canada. N Engl J Med 341(4):233–239

    Article  CAS  PubMed  Google Scholar 

  12. Clinical and Laboratory Standards Institute (CLSI) (2009) Performance standards for antimicrobial susceptibility testing; 19th informational supplement. CLSI document M100-S19. CLSI, Wayne

    Google Scholar 

  13. Pan XS, Ambler J, Mehtar S, Fisher LM (1996) Involvement of topoisomerase IV and DNA gyrase as ciprofloxacin targets in Streptococcus pneumoniae. Antimicrob Agents Chemother 40(10):2321–2326

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Enright MC, Spratt BG (1998) A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144(Pt 11):3049–3060

    Article  CAS  PubMed  Google Scholar 

  15. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186(5):1518–1530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Liu Y, Wang H, Chen M, Sun Z, Zhao R, Zhang L, Wang H, Zhang H, Wang L, Chu Y, Liu Y, Ni Y (2008) Serotype distribution and antimicrobial resistance patterns of Streptococcus pneumoniae isolated from children in China younger than 5 years. Diagn Microbiol Infect Dis 61(3):256–263

    Article  CAS  PubMed  Google Scholar 

  17. Kim SH, Song JH, Chung DR, Thamlikitkul V, Yang Y, Wang H, Lu M, So TM, Hsueh PR, Yasin RM, Carlos CC, Pham HV, Lalitha MK, Shimono N, Perera J, Shibl AM, Baek JY, Kang CI, Ko KS, Peck KR; ANSORP Study Group (2012) Changing trends in antimicrobial resistance and serotypes of Streptococcus pneumoniae isolates in Asian countries: an Asian Network for Surveillance of Resistant Pathogens (ANSORP) study. Antimicrob Agents Chemother 56(3):1418–1426

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Ho PL, Tse WS, Tsang KW, Kwok TK, Ng TK, Cheng VC, Chan RM (2001) Risk factors for acquisition of levofloxacin-resistant Streptococcus pneumoniae: a case–control study. Clin Infect Dis 32(5):701–707

    Article  CAS  PubMed  Google Scholar 

  19. Ho PL, Cheng VC, Chow KH (2009) Decreasing prevalence of levofloxacin-resistant Streptococcus pneumoniae in Hong Kong, 2001 to 2007. J Antimicrob Chemother 63(4):836–838

    Article  CAS  PubMed  Google Scholar 

  20. Beall B, McEllistrem MC, Gertz RE Jr, Wedel S, Boxrud DJ, Gonzalez AL, Medina MJ, Pai R, Thompson TA, Harrison LH, McGee L, Whitney CG; Active Bacterial Core Surveillance Team (2006) Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002. J Clin Microbiol 44(3):999–1017

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank David C. Hooper (Massachusetts General Hospital, Boston, MA, USA) very much for his critical review of the manuscript. We are grateful to the pneumococcal MLST database, which is located at Imperial College London and funded by the Wellcome Trust, and we thank its curator, Cynthia Bishop, for the designation of the new alleles and allelic profiles.

This work was supported by grant nos. 81102509 and 81120108024 from the National Natural Science Foundation of China and grant no. 10ZR1405600 from the Shanghai Municipal Science and Technology Commission.

Conflict of interest

None of the authors has any conflicts of interest to disclose.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, Q., Zhuo, C., Xu, Y. et al. Genetic diversity of fluoroquinolone-nonsusceptible Streptococcus pneumoniae clinical isolates and the first identification of serotype 20B in China. Eur J Clin Microbiol Infect Dis 33, 465–470 (2014). https://doi.org/10.1007/s10096-013-1979-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-013-1979-5

Keywords

Navigation