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Phenotypes, genotypes, serotypes and molecular epidemiology of erythromycin-resistant Streptococcus agalactiae in Italy

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Abstract

The purpose of this investigation was to analyse Streptococcus agalactiae (group B Streptococcus, GBS) isolates collected in Italy from vaginal and urine samples in respect to their clonality, distribution of virulence factors and antimicrobial resistance determinants. Three hundred and eighty-eight GBS were recovered from clinical samples. They were analysed for antibiotic resistance profiling. Erythromycin-resistant strains were further characterised by multilocus sequence typing (MLST), serotyping and the detection of alp genes of the alpha-like protein (Alp) family. GBS isolates represented 40 different sequence types (STs), grouped in five clonal complexes (CCs) and belonged to seven serotypes. Most serotype V strains (81%) possessed alp2-3; serotype Ia carried mainly epsilon, while the serotype III mainly rib. All isolates were susceptible to penicillin, whereas resistance to erythromycin was detected in 15% of isolates. Most erythromycin-resistant GBS strains were of serotype V (56.8%) and belonged to the CC-1 group (50%). Macrolide resistance phenotypes were the cMLSB (46.5%) and the M phenotypes (46.5%) due to the presence of ermB and mefA/E genes, respectively. These results provide data which establish a baseline for monitoring erythromycin resistance in this region and also provide an insight into the correlation among clonal types, serotypes, surface protein and resistance genes. The increased prevalence of strains that displayed the M phenotype strengthens the importance of the epidemiological surveillance of macrolide resistance in GBS, which may also represent an important reservoir of resistance genes for other species.

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References

  1. Baker CJ (2000) Group B streptococcal infections. In: Stevens DL, Kaplan EL (eds) Streptococcal infections: clinical aspects, microbiology, and molecular pathogenesis. Oxford University Press, New York, pp 222–237

    Google Scholar 

  2. Acikgoz ZC, Almayanlar E, Gamberzade S, Gocer S (2004) Macrolide resistance determinants of invasive and noninvasive group B streptococci in a Turkish hospital. Antimicrob Agents Chemother 48:1410–1412

    Article  PubMed  CAS  Google Scholar 

  3. Borchardt SM, DeBusscher JH, Tallman PA, Manning SD, Marrs CF, Kurzynski TA, Foxman B (2006) Frequency of antimicrobial resistance among invasive and colonizing Group B streptococcal isolates. BMC Infect Dis 6:57

    Article  PubMed  Google Scholar 

  4. Gherardi G, Imperi M, Baldassarri L, Pataracchia M, Alfarone G, Recchia S, Orefici G, Dicuonzo G, Creti R (2007) Molecular epidemiology and distribution of serotypes, surface proteins, and antibiotic resistance among group B streptococci in Italy. J Clin Microbiolol 45:2909–2916

    Article  CAS  Google Scholar 

  5. Leclercq R (2002) Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clin Infect Dis 34:482–492

    Article  PubMed  CAS  Google Scholar 

  6. Arpin C, Daube H, Tessier F, Quentin C (1999) Presence of mefA and mefE genes in Streptococcus agalactiae. Antimicrob Agents Chemother 43:944–946

    PubMed  CAS  Google Scholar 

  7. Jones N, Bohnsack JF, Takahashi S, Oliver KA, Chan MS, Kunst F, Glaser P, Rusniok C, Crook DWM, Harding RM, Bisharat N, Spratt BG (2003) Multilocus sequence typing system for group B Streptococcus. J Clin Microbiol 41:2530–2536

    Article  PubMed  CAS  Google Scholar 

  8. Slotved HC, Kong F, Lambertsen L, Sauer S, Gilbert GL (2007) Serotype IX, a proposed new Streptococcus agalactiae serotype. J Clin Microbiol 45:2929–2936

    Article  PubMed  CAS  Google Scholar 

  9. Cieslewicz MJ, Chaffin D, Glusman G, Kasper D, Madan A, Rodrigues S, Fahey J, Wessels MR, Rubens CE (2005) Structural and genetic diversity of group B Streptococcus capsular polysaccharides. Infect Immun 73:3096–3103

    Article  PubMed  CAS  Google Scholar 

  10. Sinha A, Lieu TA, Paoletti LC, Weinstein MC, Platt R (2005) The projected health benefits of maternal group B streptococcal vaccination in the era of chemoprophylaxis. Vaccine 23:3187–3195

    Article  PubMed  Google Scholar 

  11. Gilbert GL (2004) Vaccines for other neonatal infections: are group B streptococcal infections vaccine-preventable? Expert Rev Vaccines 3:371–374

    Article  PubMed  CAS  Google Scholar 

  12. Creti R, Fabretti F, Orefici G, von Hunolstein C (2004) Multiplex PCR assay for direct identification of group B streptococcal α-protein-like protein genes. J Clin Microbiol 42:1326–1329

    Article  PubMed  CAS  Google Scholar 

  13. Lindahl G, Stålhammar-Carlemalm M, Areschoug T (2005) Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin Microbiol Rev 18:102–127

    Article  PubMed  CAS  Google Scholar 

  14. 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 186:1518–1530

    Article  PubMed  CAS  Google Scholar 

  15. Bisharat N, Jones N, Marchaim D, Block C, Harding RM, Yagupsky P, Peto T, Crook DW (2005) Population structure of group B Streptococcus from a low-incidence region for invasive neonatal disease. Microbiology 151:1875–1881

    Article  PubMed  CAS  Google Scholar 

  16. Clinical and Laboratory Standards Institute (CLSI) (2010) Performance standards for antimicrobial susceptibility testing, M100-S20 (2010), M02-A10 and M07-A8. CLSI, Wayne, PA

  17. Gygax SE, Schuyler JA, Kimmel LE, Trama JP, Mordechai E, Adelson ME (2006) Erythromycin and clindamycin resistance in group B streptococcal clinical isolates. Antimicrob Agents Chemother 50:1875–1877

    Article  PubMed  CAS  Google Scholar 

  18. Sutcliffe JA, Grebe T, Tait-Kamradt A, Wondrack L (1996) Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40:2562–2566

    PubMed  CAS  Google Scholar 

  19. De Azavedo JCS, Yeung RH, Bast DJ, Duncan CL, Borgia SB, Low DE (1999) Prevalence and mechanisms of macrolide resistance in clinical isolates of group A streptococci from Ontario, Canada. Antimicrob Agents Chemother 43:2144–2147

    PubMed  Google Scholar 

  20. Desjardins M, Delgaty KL, Ramotar K, Seetaram C, Toye B (2004) Prevalence and mechanisms of erythromycin resistance in group A and group B Streptococcus: implications for reporting susceptibility results. J Clin Microbiol 42:5620–5623

    Article  PubMed  CAS  Google Scholar 

  21. Sadowy E, Matynia B, Hryniewicz W (2010) Population structure, virulence factors and resistance determinants of invasive, non-invasive and colonizing Streptococcus agalactiae in Poland. J Antimicrob Chemother 65:1907–1914

    Article  PubMed  CAS  Google Scholar 

  22. Brochet M, Couvé E, Zouine M, Vallaeys T, Rusniok C, Lamy MC, Buchrieser C, Trieu-Cuot P, Kunst F, Poyart C, Glaser P (2006) Genomic diversity and evolution within the species Streptococcus agalactiae. Microbes infect 8:1227–1243

    Article  PubMed  CAS  Google Scholar 

  23. Quentin R, Huet H, Wang FS, Geslin P, Goudeau A, Selander RK (1995) Characterization of Streptococcus agalactiae strains by multilocus enzyme genotype and serotype: identification of multiple virulent clone families that cause invasive neonatal disease. J Clin Microbiol 33:2576–2581

    PubMed  CAS  Google Scholar 

  24. Amin A, Abdulrazzaq YM, Uduman S (2002) Group B streptococcal serotype distribution of isolates from colonized pregnant women at the time of delivery in United Arab Emirates. J Infect 45:42–46

    Article  PubMed  CAS  Google Scholar 

  25. Lachenauer CS, Kasper DL, Shimada J, Ichiman Y, Ohtsuka H, Kaku M, Paoletti LC, Ferrieri P, Madoff LC (1999) Serotypes VI and VIII predominate among group B streptococci isolated from pregnant Japanese women. J Infect Dis 179:1030–1033

    Article  PubMed  CAS  Google Scholar 

  26. Diekema DJ, Andrews JI, Huynh H, Rhomberg PR, Doktor SR, Beyer J, Shortridge VD, Flamm RK, Jones RN, Pfaller MA (2003) Molecular epidemiology of macrolide resistance in neonatal bloodstream isolates of group B streptococci. J Clin Microbiol 41:2659–2661

    Article  PubMed  CAS  Google Scholar 

  27. Lin FY, Azimi PH, Weisman LE, Philips JB 3rd, Regan J, Clark P, Rhoads GG, Clemens J, Troendle J, Pratt E, Brenner RA, Gill V (2000) Antibiotic susceptibility profiles for group B streptococci isolated from neonates, 1995–1998. Clin Infect Dis 31:76–79

    Article  PubMed  CAS  Google Scholar 

  28. von Both U, Ruess M, Mueller U, Fluegge K, Sander A, Berner R (2003) A serotype V clone is predominant among erythromycin-resistant Streptococcus agalactiae isolates in a southwestern region of Germany. J Clin Microbiol 41:2166–2169

    Article  Google Scholar 

  29. Figueira-Coelho J, Ramirez M, Salgado MJ, Melo-Cristino J (2004) Streptococcus agalactiae in a large Portuguese teaching hospital: antimicrobial susceptibility, serotype distribution, and clonal analysis of macrolide-resistant isolates. Microb Drug Resist 10:31–36

    Article  PubMed  CAS  Google Scholar 

  30. Florindo C, Viegas S, Paulino A, Rodrigues E, Gomes JP, Borrego MJ (2010) Molecular characterization and antimicrobial susceptibility profiles in Streptococcus agalactiae colonizing strains: association of erythromycin resistance with subtype III-1 genetic clone family. Clin Microbiol Infect 16(9):1458–1463

    Article  PubMed  CAS  Google Scholar 

  31. Fluegge K, Supper S, Siedler A, Berner R (2004) Antibiotic susceptibility in neonatal invasive isolates of Streptococcus agalactiae in a 2-year nationwide surveillance study in Germany. Antimicrob Agents Chemother 48:4444–6

    Article  PubMed  CAS  Google Scholar 

  32. Gonzalez JJ, Andreu A; Spanish Group for the Study of Perinatal infection from the Spanish Society for Clinical Microbiology and Infectious Diseases (2005) Multicenter study of the mechanisms of resistance and clonal relationships of Streptococcus agalactiae isolates resistant to macrolides, lincosamides, and ketolides in Spain. Antimicrob Agents Chemother 49:2525–2527

    Article  PubMed  CAS  Google Scholar 

  33. de Azavedo JC, McGavin M, Duncan C, Low DE, McGeer A (2001) Prevalence and mechanisms of macrolide resistance in invasive and noninvasive group B streptococcus isolates from Ontario, Canada. Antimicrob Agents Chemother 45:3504–3508

    Article  PubMed  Google Scholar 

  34. Fitoussi F, Loukil C, Gros I, Clermont O, Mariani P, Bonacorsi S, Le Thomas I, Deforche D, Bingen E (2001) Mechanisms of macrolide resistance in clinical group B streptococci isolated in France. Antimicrob Agents Chemother 45:1889–1891

    Article  PubMed  CAS  Google Scholar 

  35. Motlová J, Straková L, Urbásková P, Sak P, Sever T (2004) Vaginal and rectal carriage of Streptococcus agalactiae in the Czech Republic: incidence, serotypes distribution and susceptibility to antibiotics. Indian J Med Res 119:84–87

    PubMed  Google Scholar 

  36. Bronzwaer SL, Cars O, Buchholz U, Mölstad S, Goettsch W, Veldhuijzen IK, Kool JL, Sprenger MJ, Degener JE; European Antimicrobial Resistance Surveillance System (2002) A European study on the relationship between antimicrobial use and antimicrobial resistance. Emerg Infect Dis 8:278–282

    Article  PubMed  Google Scholar 

  37. Dahesh S, Hensler ME, Van Sorge NM, Gertz RE Jr, Schrag S, Nizet V, Beall BW (2008) Point mutation in the group B streptococcal pbp2x gene conferring decreased susceptibility to β-lactam antibiotics. Antimicrob Agents Chemother 52:2915–2918

    Article  PubMed  CAS  Google Scholar 

  38. Kimura K, Suzuki S, Wachino J, Kurokawa H, Yamane K, Shibata N, Nagano N, Kato H, Shibayama K, Arakawa Y (2008) First molecular characterization of group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother 52:2890–2897

    Article  PubMed  CAS  Google Scholar 

  39. 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are sincerely obliged to Ilaria Medeghini for her excellent technical assistance

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Authors and Affiliations

  1. Institute of Microbiology, Department of Experimental and Applied Medicine, University of Brescia, P. le Spedali Civili, 1, 25123, Brescia, Italy

    M. A. De Francesco, S. Caracciolo, F. Gargiulo & N. Manca

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  1. M. A. De Francesco
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  2. S. Caracciolo
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  3. F. Gargiulo
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Correspondence to M. A. De Francesco.

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De Francesco, M.A., Caracciolo, S., Gargiulo, F. et al. Phenotypes, genotypes, serotypes and molecular epidemiology of erythromycin-resistant Streptococcus agalactiae in Italy. Eur J Clin Microbiol Infect Dis 31, 1741–1747 (2012). https://doi.org/10.1007/s10096-011-1495-4

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