1887

Abstract

Purpose. To assess the antibiotic resistance, transposon profiles, serotype distribution and vaccine coverage rates in 110 erythromycin-resistant S. pneumoniae clinical isolates.

Methodology. Erythromycin, clindamycin, tetracycline, chloramphenicol and kanamycin susceptibilities were assessed using the E-test/disc diffusion method. Inducible macrolide resistance was tested using the erythromycin-clindamycin double disc diffusion test. Serogrouping and serotyping were performed using latex particle agglutination and the Quellung reaction, respectively. Drug resistance genes and transposon-specific genes were investigated by PCR.

Results. Of the isolates, 93  % were resistant to clindamycin; 81  % were resistant to tetracycline; 76  % were multi-drug-resistant, having resistance to both clindamycin and tetracycline; and 12  % had extended-drug resistance, being resistant to clindamycin, tetracycline, chloramphenicol and kanamycin. The majority of isolates (88.2 %) exhibited the cMLSB phenotype. The association between the cMLSB phenotype and tetracycline resistance was related to transposons Tn2010 (38.2 %), Tn6002 (21.8 %) and Tn3872 (18.2 %). M and iMLSB phenotypes were observed in 7 and 5  % of the isolates, respectively. The most frequent serotype was 19 F (40 %). Among the erythromycin-resistant pneumococci, vaccine coverage rates for the 13-valent pneumococcal conjugate vaccine (PCV-13) and the 23-valent pneumococcal polysaccharide vaccine (PPSV-23) were 76.4 and 79.1  %, respectively, compared to 82.2 and 85.1 % transposon-carrying isolates.

Conclusions. Multi-drug resistance among erythromycin-resistant S. pneumoniae isolates mainly occurs due to the horizontal spread of the Tn916 family of transposons. The majority of the transposon-carrying isolates are covered by 13- and 23-valent pneumococcal vaccines. Since serotype distribution and transposons in S. pneumoniae isolates may change over time, close monitoring is essential.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000995
2019-05-22
2020-01-28
Loading full text...

Full text loading...

References

  1. Calatayud L, Ardanuy C, Cercenado E, Fenoll A, Bouza E et al. Serotypes, clones, and mechanisms of resistance of erythromycin-resistant Streptococcus pneumoniae isolates collected in Spain. Antimicrob Agents Chemother 2007;51:3240–3246 [CrossRef]
    [Google Scholar]
  2. Xu X, Cai L, Xiao M, Kong F, Oftadeh S et al. Distribution of serotypes, genotypes, and resistance determinants among macrolide-resistant Streptococcus pneumoniae isolates. Antimicrob Agents Chemother 2010;54:1152–1159 [CrossRef]
    [Google Scholar]
  3. Hawkins PA, Chochua S, Jackson D, Beall B, McGee L et al. Mobile elements and chromosomal changes associated with MLS resistance phenotypes of invasive pneumococci recovered in the United States. Microb Drug Resist 2015;21:121–129 [CrossRef]
    [Google Scholar]
  4. Schroeder MR. Stephens DS Macrolide resistance in Streptococcus pneumoniae. Mini Rev. Front Cell Infect Microbiol 2016;6:98
    [Google Scholar]
  5. Sirekbasan L, Gönüllü N, Sirekbasan S, Kuskucu M, Midilli K et al. Phenotypes and genotypes of macrolide-resistant Streptococcus pneumoniae. Balkan Med J 2015;32:84–88 [CrossRef]
    [Google Scholar]
  6. Korona-Glowniak I, Siwiec R, Malm A. Resistance determinants and their association with different transposons in the antibiotic-resistant Streptococcus pneumoniae. BioMed Res Int 2015;836496:1–6
    [Google Scholar]
  7. Zhou L, Ma X, Gao W, Yao KH, Shen AD et al. Molecular characteristics of erythromycin-resistant Streptococcus pneumoniae from pediatric patients younger than five years in Beijing, 2010. BMC Microbiol 2012;12:228 [CrossRef]
    [Google Scholar]
  8. Calatayud L, Ardanuy C, Tubau F, Rolo D, Grau I et al. Serotype and genotype replacement among macrolide-resistant invasive Pneumococci in adults: mechanisms of resistance and association with different transposons. J Clin Microbiol 2010;48:1310–1316 [CrossRef]
    [Google Scholar]
  9. Chancey ST, Agrawal S, Schroeder MR, Farley MM, Tettelin H et al. Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae. Front Microbiol 2015;6:26 [CrossRef]
    [Google Scholar]
  10. Brenciani A, Bacciaglia A, Vecchi M, Vitali LA, Varaldo PE et al. Genetic elements carrying erm(B) in Streptococcus pyogenes and association with tet(M) tetracycline resistance gene. Antimicrob Agents Chemother 2007;51:1209–1216 [CrossRef]
    [Google Scholar]
  11. Santagati M, Iannelli F, Cascone C, Campanile F, Oggioni MR et al. The novel conjugative transposon Tn1207.3 carries the macrolide efflux gene mef(A) in Streptococcus pyogenes. Microb Drug Resist 2003;9:243–247 [CrossRef]
    [Google Scholar]
  12. Widdowson CA, Adrian PV, Klugman KP. Acquisition of chloramphenicol resistance by the linearization and integration of the entire staphylococcal plasmid pC194 into the chromosome of Streptococcus pneumoniae. Antimicrob Agents Chemother 2000;44:393–395 [CrossRef]
    [Google Scholar]
  13. Koneman EW.(editor) Koneman's Color Atlas and Textbook of Diagnostic Microbiology, 6th ed. 2006
    [Google Scholar]
  14. CLSI M100 Performance Standards for Antimicrobial Susceptibility Testing, 27th ed. 2017; pp78–82
    [Google Scholar]
  15. Golden AR, Rosenthal M, Fultz B, Nichol KA, Adam HJ et al. Characterization of MDR and XDR Streptococcus pneumoniae in Canada, 2007–13. J Antimicrob Chemother 2015;70:2199–2202 [CrossRef]
    [Google Scholar]
  16. Sutcliffe J, Tait-Kamradt A, Wondrack L. Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system. Antimicrob Agents Chemother 1996;40:1817–1824 [CrossRef]
    [Google Scholar]
  17. Pérez-Trallero E, Montes M, Orden B, Tamayo E, Garcia-Arenzana JM et al. Phenotypic and genotypic characterization of Streptococcus pyogenes isolates displaying the MLSB phenotype of macrolide resistance in Spain, 1999 to 2005. Antimicrob Agents Chemother 2007;51:1228–1233 [CrossRef]
    [Google Scholar]
  18. Li Y, Tomita H, Lv Y, Liu J, Xue F et al. Molecular characterization of erm(B)- and mef(E)-mediated erythromycin-resistant Streptococcus pneumoniae in China and complete DNA sequence of Tn2010. J Appl Microbiol 2011;110:254–265 [CrossRef]
    [Google Scholar]
  19. Caillaud F, Trieu-Cuot P, Carlier C, Courvalin P, Caillaud F. Nucleotide sequence of the kanamycin resistance determinant of the pneumococcal transposon Tn1545: evolutionary relationships and transcriptional analysis of aphA-3 genes. Mol Gen Genet 1987;207:509–513 [CrossRef]
    [Google Scholar]
  20. El Moujaber G, Osman M, Rafei R, Dabboussi F, Hamze M et al. Molecular mechanisms and epidemiology of resistance in Streptococcus pneumoniae in the Middle East region. J Med Microbiol 2017;66:847–858 [CrossRef]
    [Google Scholar]
  21. Centers for Disease Control and Prevention Active bacterial core surveillance report, emerging infections program network, Streptococcus pneumoniae, 2014 Atlanta: CDC; 2016
    [Google Scholar]
  22. Jacobs MR, Felmingham D, Appelbaum PC, Grüneberg RN et al. The Alexander project 1998–2000: susceptibility of pathogens isolated from community-acquired respiratory tract infection to commonly used antimicrobial agents. J Antimicrob Chemother 2003;52:229–246 [CrossRef]
    [Google Scholar]
  23. Riedel S, Beekmann SE, Heilmann KP, Richter SS, Garcia-de-Lomas J et al. Antimicrobial use in Europe and antimicrobial resistance in Streptococcus pneumoniae. Eur J Clin Microbiol Infect Dis 2007;26:485–490 [CrossRef]
    [Google Scholar]
  24. Borg MA, Tiemersma E, Scicluna E, van de Sande-Bruinsma N, de Kraker M et al. Prevalence of penicillin and erythromycin resistance among invasive Streptococcus pneumoniae isolates reported by laboratories in the southern and eastern Mediterranean region. Clin Microbiol Infect 2009;15:232–237 [CrossRef]
    [Google Scholar]
  25. Ilki A, Sağiroğlu P, Elgörmüş N, Söyletir G. Trends in antibiotic susceptibility patterns of Streptococcus pneumoniae and Haemophilus influenzae isolates: four years follow up. Mikrobiyol Bul 2010;44:169–175
    [Google Scholar]
  26. Soyletir G, Altinkanat G, Gur D, Altun B, Tunger A et al. Results from the survey of antibiotic resistance (SOAR) 2011–13 in Turkey. J Antimicrob Chemother 2016;71:i71–i83 [CrossRef]
    [Google Scholar]
  27. Hasçelik G, Gürler N, Ceyhan M, Özakın C, Bayramoğlu G et al. Serotype distribution and antibiotic resistance among isolates of Streptococcus pneumoniae causing invasive pneumococcal disease in adults in Turkey: 2005–2015. Int J Infect Dis 2016;45:91 [CrossRef]
    [Google Scholar]
  28. Reinert RR, Ringelstein A, van der Linden M, Cil MY, Al-Lahham A et al. Molecular epidemiology of macrolide-resistant Streptococcus pneumoniae isolates in Europe. J Clin Microbiol 2005;43:1294–1300 [CrossRef]
    [Google Scholar]
  29. Zhou W, Yao K, Zhang G, Yang Y, Li Y et al. Mechanism for transfer of transposon Tn2010 carrying macrolide resistance genes in Streptococcus pneumoniae and its effects on genome evolution. J Antimicrob Chemother 2014;69:1470–1473 [CrossRef]
    [Google Scholar]
  30. Okitsu N, Kaieda S, Yano H, Nakano R, Hosaka Y et al. Characterization of ermB gene transposition by Tn1545 and Tn917 in macrolide-resistant Streptococcus pneumoniae isolates. J Clin Microbiol 2005;43:168–173 [CrossRef]
    [Google Scholar]
  31. McDougal LK, Tenover FC, Lee LN, Rasheed JK, Patterson JE et al. Detection of Tn917-like sequences within a Tn916-like conjugative transposon (Tn3872) in erythromycin-resistant isolates of Streptococcus pneumoniae. Antimicrob Agents Chemother 1998;42:2312–2318 [CrossRef]
    [Google Scholar]
  32. Mingoia M, Morici E, Morroni G, Giovanetti E, Del Grosso M et al. Tn5253 family integrative and conjugative elements carrying mef(I) and catQ determinants in Streptococcus pneumoniae and Streptococcus pyogenes. Antimicrob Agents Chemother 2014;58:5886–5893 [CrossRef]
    [Google Scholar]
  33. Centers for Disease Control and Prevention Pneumococcal vaccination recommendations. https://www.cdc.gov/vaccines/vpd/pneumo/index.html
  34. Turkish Republic Public Health Institute Chart of the high risk group pneumococcal vaccination programme. https://dosyaism.saglik.gov.tr/Eklenti/20721,risk-grubu-asilamalaripdf.pdf?0
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000995
Loading
/content/journal/jmm/10.1099/jmm.0.000995
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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