1887

Abstract

We evaluated temporal fluctuations in macrolide resistance rates, analysing genetic determinants of resistance and clonal evolution in a population of 2744 isolates collected in the period 2000–2013. The total resistance rate to erythromycin of the isolates was 17.9 %. A maximum of erythromycin resistance emerged in 2000 (38.6 %), followed by a significant decrease to 5.2 % in 2012 ( < 0.0001). Molecular analysis revealed the presence and co-presence of known genetic resistance determinants , , and , in line with phenotypes. PFGE analysis identified genetically related groups in 2000 and 2007–2008, mainly the MLS and M phenotypes, respectively. The most prevalent types among a representative subset of resistant isolates were , and . All and 88.2 % of the strains harbouring the gene were only recorded in M-phenotype strains, whilst all -positive strains had the inducible MLS phenotype. The analysed susceptible isolates showed several types partially shared with resistant ones. Our results suggest that changes in bacterial population clonality, rather than horizontal transfer of resistance determinants, plays a major epidemiological role in . Continuous monitoring of microbiological epidemiology seems to be crucial for correct and effective management of streptococcal infections.

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2015-10-01
2024-04-19
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References

  1. Albrich W. C., Monnet D. L., Harbarth S. 2004; Antibiotic selection pressure and resistance in Streptococcus pneumoniae and Streptococcus pyogenes . Emerg Infect Dis 10:514–517 [View Article][PubMed]
    [Google Scholar]
  2. Bacciaglia A., Brenciani A., Varaldo P. E., Giovanetti E. 2007; SmaI typeability and tetracycline susceptibility and resistance in Streptococcus pyogenes isolates with efflux-mediated erythromycin resistance. Antimicrob Agents Chemother 51:3042–3043 [View Article][PubMed]
    [Google Scholar]
  3. Bingen E., Fitoussi F., Doit C., Cohen R., Tanna A., George R., Loukil C., Brahimi N., Le Thomas I., Deforche D. 2000; Resistance to macrolides in Streptococcus pyogenes in France in pediatric patients. Antimicrob Agents Chemother 44:1453–1457 [View Article][PubMed]
    [Google Scholar]
  4. Bisno A. L., Stevens D. L. 2007; Streptococcus pyogenes. In Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases pp. 2593–2610 Edited by Mandell G. L., Bennett J. E., Dolin R. Philadelphia, PA: Churchill Livingstone;
    [Google Scholar]
  5. Bisno A. L., Gerber M. A., Gwaltney J. M. Jr, Kaplan E. L., Schwartz R. H., Infectious Diseases Society of America. 2002; Practice guidelines for the diagnosis and management of group A streptococcal pharyngitis. Clin Infect Dis 35:113–125 [View Article][PubMed]
    [Google Scholar]
  6. Carriço J. A., Silva-Costa C., Melo-Cristino J., Pinto F. R., de Lencastre H., Almeida J. S., Ramirez M. 2006; Illustration of a common framework for relating multiple typing methods by application to macrolide-resistant Streptococcus pyogenes . J Clin Microbiol 44:2524–2532 [View Article][PubMed]
    [Google Scholar]
  7. Cascone C., Santagati M., Noviello S., Iannelli F., Esposito S., Pozzi G., Stefani S. 2002; Macrolide-resistance genes in clinical isolates of Streptococcus pyogenes . Microb Drug Resist 8:129–132 [View Article][PubMed]
    [Google Scholar]
  8. CLSI 2012; Performance Standards for Antimicrobial Susceptibility Testings; 22nd Informational Supplement M100-S22. Wayne, PA: Clinical, Laboratory Standards Institute;
    [Google Scholar]
  9. Cornaglia G., Ligozzi M., Mazzariol A., Masala L., Lo Cascio G., Orefici G., Fontana R., Italian Surveillance Group for Antimicrobial Resistance. 1998; Resistance of Streptococcus pyogenes to erythromycin and related antibiotics in Italy. Clin Infect Dis 27:(Suppl. 1)S87–S92 [View Article][PubMed]
    [Google Scholar]
  10. Cresti S., Lattanzi M., Zanchi A., Montagnani F., Pollini S., Cellesi C., Rossolini G. M. 2002; Resistance determinants and clonal diversity in group A streptococci collected during a period of increasing macrolide resistance. Antimicrob Agents Chemother 46:1816–1822 [View Article][PubMed]
    [Google Scholar]
  11. Creti R., Gherardi G., Imperi M., von Hunolstein C., Baldassarri L., Pataracchia M., Alfarone G., Cardona F., Dicuonzo G., Orefici G. 2005; Association of group A streptococcal emm types with virulence traits and macrolide-resistance genes is independent of the source of isolation. J Med Microbiol 54:913–917 [View Article][PubMed]
    [Google Scholar]
  12. d'Humières C., Cohen R., Levy C., Bidet P., Thollot F., Wollner A., Bingen E. 2012; Decline in macrolide-resistant Streptococcus pyogenes isolates from French children. Int J Med Microbiol 302:300–303 [View Article][PubMed]
    [Google Scholar]
  13. de la Pedrosa E. G., Morosini M. I., van der Linden M., Ruiz-Garbajosa P., Galán J. C., Baquero F., Reinert R. R., Cantón R. 2008; Polyclonal population structure of Streptococcus pneumoniae isolates in Spain carrying mef and mef plus erm(B). Antimicrob Agents Chemother 52:1964–1969 [View Article][PubMed]
    [Google Scholar]
  14. Gherardi G., Petrelli D., Di Luca M. C., Pimentel de Araujo F., Bernaschi P., Repetto A., Bellesi J., Vitali L. A. 2015 [Epub ahead of print.] Decline in macrolide resistance rates among Streptococcus pyogenes causing pharyngitis in children isolated in Italy. Eur J Clin Microbiol Infect Dis [View Article][PubMed]
    [Google Scholar]
  15. Giovanetti E., Montanari M. P., Mingoia M., Varaldo P. E. 1999; Phenotypes and genotypes of erythromycin-resistant Streptococcus pyogenes strains in Italy and heterogeneity of inducibly resistant strains. Antimicrob Agents Chemother 43:1935–1940[PubMed]
    [Google Scholar]
  16. Giovanetti E., Brenciani A., Tiberi E., Bacciaglia A., Varaldo P. E. 2012; ICESp2905, the erm(TR)-tet(O) element of Streptococcus pyogenes, is formed by two independent integrative and conjugative elements. Antimicrob Agents Chemother 56:591–594 [View Article][PubMed]
    [Google Scholar]
  17. Grivea I. N., Al-Lahham A., Katopodis G. D., Syrogiannopoulos G. A., Reinert R. R. 2006; Resistance to erythromycin and telithromycin in Streptococcus pyogenes isolates obtained between 1999 and 2002 from Greek children with tonsillopharyngitis: phenotypic and genotypic analysis. Antimicrob Agents Chemother 50:256–261 [View Article][PubMed]
    [Google Scholar]
  18. Horn D. L., Zabriskie J. B., Austrian R., Cleary P. P., Ferretti J. J., Fischetti V. A., Gotschlich E., Kaplan E. L., McCarty M., other authors. 1998; Why have group A streptococci remained susceptible to penicillin? Report on a symposium. Clin Infect Dis 26:1341–1345 [View Article][PubMed]
    [Google Scholar]
  19. Huang C. Y., Lai J. F., Huang I. W., Chen P. C., Wang H. Y., Shiau Y. R., Cheng Y. W., Hsieh L. Y., Chang S. C., others authors. 2014; Epidemiology and molecular characterization of macrolide-resistant Streptococcus pyogenes in Taiwan. J Clin Microbiol 52:508–516 [View Article][PubMed]
    [Google Scholar]
  20. Lamagni T. L., Darenberg J., Luca-Harari B., Siljander T., Efstratiou A., Henriques-Normark B., Vuopio-Varkila J., Bouvet A., Creti R., other authors. 2008; Epidemiology of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 46:2359–2367 [View Article][PubMed]
    [Google Scholar]
  21. Lorino G., Gherardi G., Angeletti S., De Cesaris M., Graziano N., Maringhini S., Merlino F., Di Bernardo F., Dicuonzo G. 2006; Molecular characterisation and clonal analysis of group A streptococci causing pharyngitis among paediatric patients in Palermo, Italy. Clin Microbiol Infect 12:189–192 [View Article][PubMed]
    [Google Scholar]
  22. Montagnani F., Stolzuoli L., Croci L., Rizzuti C., Arena F., Zanchi A., Cellesi C. 2009; Erythromycin resistance in Streptococcus pyogenes and macrolide consumption in a central Italian region. Infection 37:353–357 [View Article][PubMed]
    [Google Scholar]
  23. Montes M., Tamayo E., Mojica C., García-Arenzana J. M., Esnal O., Pérez-Trallero E. 2014; What causes decreased erythromycin resistance in Streptococcus pyogenes? Dynamics of four clones in a southern European region from 2005 to 2012. J Antimicrob Chemother 69:1474–1482 [View Article][PubMed]
    [Google Scholar]
  24. Pérez-Trallero E., Montes M., Orden B., Tamayo E., García-Arenzana J. M., Marimón J. M. 2007; Phenotypic and genotypic characterization of Streptococcus pyogenes isolates displaying the MLSB phenotype of macrolide resistance in Spain, 1999 to 2005. Antimicrob Agents Chemother 51:1228–1233 [View Article][PubMed]
    [Google Scholar]
  25. Ruoff K. 2003; Streptococcus. In Manual of Clinical Microbiology pp. 405–422 Edited by Murray P. R., Baron E. J., Jorgensen J. H., Pfaller M. A., Yolken R. H. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  26. Seppälä H., Skurnik M., Soini H., Roberts M. C., Huovinen P. 1998; A novel erythromycin resistance methylase gene (ermTR) in Streptococcus pyogenes . Antimicrob Agents Chemother 42:257–262[PubMed] [CrossRef]
    [Google Scholar]
  27. Shulman S. T., Bisno A. L., Clegg H. W., Gerber M. A., Kaplan E. L., Lee G., Martin J. M., Van Beneden C. 2012; Clinical practice guideline for the diagnosis and management of group A streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America. Clin Infect Dis 55:1279–1282 [Erratum: Clin Infect Dis 58, 1496] [PubMed] [CrossRef]
    [Google Scholar]
  28. Silva-Costa C., Pinto F. R., Ramirez M., Melo-Cristino J., Portuguese Surveillance Group for the Study of Respiratory Pathogens. 2008; Decrease in macrolide resistance and clonal instability among Streptococcus pyogenes in Portugal. Clin Microbiol Infect 14:1152–1159 [View Article][PubMed]
    [Google Scholar]
  29. Sneath P. H. A., Sokal R. R. 1973 Numerical Taxonomy: the Principles and Practice of Numerical Classification New York: W.H. Freeman;
    [Google Scholar]
  30. Sutcliffe J., Tait-Kamradt A., Wondrack L. 1996; Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system. Antimicrob Agents Chemother 40:1817–1824[PubMed]
    [Google Scholar]
  31. Tenover F. C., Arbeit R. D., Goering R. V., Mickelsen P. A., Murray B. E., Persing D. H., Swaminathan B. 1995; Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239[PubMed]
    [Google Scholar]
  32. Tewodros W., Kronvall G. 2005; M protein gene (emm type) analysis of group A (-hemolytic streptococci from Ethiopia reveals unique patterns. J Clin Microbiol 43:4369–4376 [View Article][PubMed]
    [Google Scholar]
  33. van Belkum A., Tassios P. T., Dijkshoorn L., Haeggman S., Cookson B., Fry N. K., Fussing V., Green J., Feil E., others authors. 2007; Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13:(Suppl. 3)1–46 [View Article][PubMed]
    [Google Scholar]
  34. Varaldo P. E., Montanari M. P., Giovanetti E. 2009; Genetic elements responsible for erythromycin resistance in streptococci. Antimicrob Agents Chemother 53:343–353 [View Article][PubMed]
    [Google Scholar]
  35. Villaseñor-Sierra A., Katahira E., Jaramillo-Valdivia A. N., Barajas-García M. L., Bryant A., Morfín-Otero R., Márquez-Díaz F., Tinoco J. C., Sánchez-Corona J., Stevens D. L. 2012; Phenotypes and genotypes of erythromycin-resistant Streptococcus pyogenes strains isolated from invasive and non-invasive infections from Mexico and the USA during 1999-2010. Int J Infect Dis 16:e178–e181 [View Article][PubMed]
    [Google Scholar]
  36. Zampaloni C., Cappelletti P., Prenna M., Vitali L. A., Ripa S. 2003; emm gene distribution among erythromycin-resistant and -susceptible Italian isolates of Streptococcus pyogenes. . J Clin Microbiol 41:1307–1310 [View Article][PubMed]
    [Google Scholar]
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