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Abstract

We characterised Lancefield group B streptococcal (GBS) isolates causing invasive disease among non-pregnant adults in Portugal between 2009 and 2015. All isolates (n = 555) were serotyped, assigned to clonal complexes (CCs) by multilocus sequence typing and characterised by surface protein and pilus island gene profiling. Antimicrobial susceptibility was tested by disk diffusion and resistance genotypes identified by PCR. Overall, serotype Ia was most frequent in the population (31%), followed by serotypes Ib (24%) and V (18%). Serotype Ib increased significantly throughout the study period (p < 0.001) to become the most frequent serotype after 2013. More than 40% of isolates clustered in the CC1/3/PI-1+PI-2a genetic lineage, including most isolates of serotypes Ib (n = 110) and V (n = 65). Erythromycin and clindamycin resistance rates were 35% and 34%, respectively, both increasing from 2009 to 2015 (p < 0.010) and associated with CC1 and serotype Ib (p < 0.001). The Ib/CC1 lineage probably resulted from acquisition of the type Ib capsular operon in a single recombination event by a representative of the V/CC1 macrolide-resistant lineage. Expansion of the new serotype Ib/CC1 lineage resulted in increased macrolide resistance in GBS, causing invasive disease among adults in Portugal. The presence of this clone elsewhere may predict more widespread increase in resistance.

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/content/10.2807/1560-7917.ES.2018.23.21.1700473
2018-05-24
2024-04-23
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2018.23.21.1700473
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References

  1. Schuchat A. Epidemiology of group B streptococcal disease in the United States: shifting paradigms. Clin Microbiol Rev. 1998;11(3):497-513. PMID: 9665980 
  2. Skoff TH, Farley MM, Petit S, Craig AS, Schaffner W, Gershman K, et al. Increasing burden of invasive group B streptococcal disease in nonpregnant adults, 1990-2007. Clin Infect Dis. 2009;49(1):85-92.  https://doi.org/10.1086/599369  PMID: 19480572 
  3. Lamagni TL, Keshishian C, Efstratiou A, Guy R, Henderson KL, Broughton K, et al. Emerging trends in the epidemiology of invasive group B streptococcal disease in England and Wales, 1991-2010. Clin Infect Dis. 2013;57(5):682-8.  https://doi.org/10.1093/cid/cit337  PMID: 23845950 
  4. Alhhazmi A, Hurteau D, Tyrrell GJ. Epidemiology of invasive group B streptococcal disease in Alberta, Canada, from 2003 to 2013. J Clin Microbiol. 2016;54(7):1774-81.  https://doi.org/10.1128/JCM.00355-16  PMID: 27098960 
  5. Kimura K, Nagano N, Arakawa Y. Classification of group B streptococci with reduced β-lactam susceptibility (GBS-RBS) based on the amino acid substitutions in PBPs. J Antimicrob Chemother. 2015;70(6):1601-3. PMID: 25667406 
  6. Castor ML, Whitney CG, Como-Sabetti K, Facklam RR, Ferrieri P, Bartkus JM, et al. Antibiotic resistance patterns in invasive group B streptococcal isolates. Infect Dis Obstet Gynecol. 2008;2008:727505.
  7. Nuccitelli A, Rinaudo CD, Maione D. Group B Streptococcus vaccine: state of the art. Ther Adv Vaccines. 2015;3(3):76-90.  https://doi.org/10.1177/2051013615579869  PMID: 26288735 
  8. Jones N, Bohnsack JF, Takahashi S, Oliver KA, Chan M-S, Kunst F, et al. Multilocus sequence typing system for group B streptococcus. J Clin Microbiol. 2003;41(6):2530-6.  https://doi.org/10.1128/JCM.41.6.2530-2536.2003  PMID: 12791877 
  9. Manning SD. Emergence of a hypervirulent neonatal pathogen. Lancet Infect Dis. 2014;14(11):1028-30.  https://doi.org/10.1016/S1473-3099(14)70938-7  PMID: 25444396 
  10. Bergseng H, Rygg M, Bevanger L, Bergh K. Invasive group B streptococcus (GBS) disease in Norway 1996-2006. Eur J Clin Microbiol Infect Dis. 2008;27(12):1193-9.  https://doi.org/10.1007/s10096-008-0565-8  PMID: 18560908 
  11. Tazi A, Morand PC, Réglier-Poupet H, Dmytruk N, Billoët A, Antona D, et al. Invasive group B streptococcal infections in adults, France (2007-2010). Clin Microbiol Infect. 2011;17(10):1587-9.  https://doi.org/10.1111/j.1469-0691.2011.03628.x  PMID: 21883671 
  12. Teatero S, McGeer A, Low DE, Li A, Demczuk W, Martin I, et al. Characterization of invasive group B streptococcus strains from the greater Toronto area, Canada. J Clin Microbiol. 2014;52(5):1441-7.  https://doi.org/10.1128/JCM.03554-13  PMID: 24554752 
  13. Martins ER, Melo-Cristino J, Ramirez MPortuguese Group for the Study of Streptococcal Infections. Dominance of serotype Ia among group B Streptococci causing invasive infections in nonpregnant adults in Portugal. J Clin Microbiol. 2012;50(4):1219-27.  https://doi.org/10.1128/JCM.05488-11  PMID: 22219307 
  14. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement. CLSI document M100-S24. Wayne: CLSI; 2014.
  15. Martins ER, Pedroso-Roussado C, Melo-Cristino J, Ramirez MPortuguese Group for the Study of Streptococcal Infections. Streptococcus agalactiae causing neonatal infections in Portugal (2005-2015): diversification and emergence of a CC17/PI-2b multidrug resistant sublineage. Front Microbiol. 2017;8:499.  https://doi.org/10.3389/fmicb.2017.00499  PMID: 28400757 
  16. Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner SA, Chow JW. Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother. 2003;47(4):1423-6.  https://doi.org/10.1128/AAC.47.4.1423-1426.2003  PMID: 12654683 
  17. Clark NC, Olsvik O, Swenson JM, Spiegel CA, Tenover FC. Detection of a streptomycin/spectinomycin adenylyltransferase gene (aadA) in Enterococcus faecalis. Antimicrob Agents Chemother. 1999;43(1):157-60. PMID: 9869582 
  18. Nascimento M, Sousa A, Ramirez M, Francisco AP, Carriço JA, Vaz C. PHYLOViZ 2.0: providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics. 2017;33(1):128-9.  https://doi.org/10.1093/bioinformatics/btw582  PMID: 27605102 
  19. Creti R, Fabretti F, Orefici G, von Hunolstein C. Multiplex PCR assay for direct identification of group B streptococcal alpha-protein-like protein genes. J Clin Microbiol. 2004;42(3):1326-9.  https://doi.org/10.1128/JCM.42.3.1326-1329.2004  PMID: 15004110 
  20. Martins ER, Melo-Cristino J, Ramirez M. Evidence for rare capsular switching in Streptococcus agalactiae. J Bacteriol. 2010;192(5):1361-9.  https://doi.org/10.1128/JB.01130-09  PMID: 20023016 
  21. Carriço JA, Silva-Costa C, Melo-Cristino J, Pinto FR, de Lencastre H, Almeida JS, et al. Illustration of a common framework for relating multiple typing methods by application to macrolide-resistant Streptococcus pyogenes. J Clin Microbiol. 2006;44(7):2524-32.  https://doi.org/10.1128/JCM.02536-05  PMID: 16825375 
  22. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289-300.
  23. Resident population (2009–2015). Lisbon: Instituto Nacional de Estatística – Portugal (Statistics Portugal); [Accessed: July 2017]. Available from: http://www.ine.pt
  24. Neemuchwala A, Teatero S, Athey TBT, McGeer A, Fittipaldi N. Capsular switching and other large-scale recombination events in invasive sequence type 1 group B Streptococcus. Emerg Infect Dis. 2016;22(11):1941-4.  https://doi.org/10.3201//eid2211.152064  PMID: 27767925 
  25. Flores AR, Galloway-Peña J, Sahasrabhojane P, Saldaña M, Yao H, Su X, et al. Sequence type 1 group B Streptococcus, an emerging cause of invasive disease in adults, evolves by small genetic changes. Proc Natl Acad Sci USA. 2015;112(20):6431-6.  https://doi.org/10.1073/pnas.1504725112  PMID: 25941374 
  26. Rosini R, Rinaudo CD, Soriani M, Lauer P, Mora M, Maione D, et al. Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol. 2006;61(1):126-41.  https://doi.org/10.1111/j.1365-2958.2006.05225.x  PMID: 16824100 
  27. McDougal LK, Tenover FC, Lee LN, Rasheed JK, Patterson JE, Jorgensen JH, 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(9):2312-8. PMID: 9736555 
  28. Björnsdóttir ES, Martins ER, Erlendsdóttir H, Haraldsson G, Melo-Cristino J, Kristinsson KG, et al. Changing epidemiology of group B streptococcal infections among adults in Iceland: 1975-2014. Clin Microbiol Infect. 2016;22(4):379.e9-16.  https://doi.org/10.1016/j.cmi.2015.11.020  PMID: 26691681 
  29. Meehan M, Cunney R, Cafferkey M. Molecular epidemiology of group B streptococci in Ireland reveals a diverse population with evidence of capsular switching. Eur J Clin Microbiol Infect Dis. 2014;33(7):1155-62.  https://doi.org/10.1007/s10096-014-2055-5  PMID: 24469423 
  30. Morozumi M, Wajima T, Takata M, Iwata S, Ubukata K. Molecular characteristics of group B streptococci isolated from adults with invasive infections in Japan. J Clin Microbiol. 2016;54(11):2695-700.  https://doi.org/10.1128/JCM.01183-16  PMID: 27558182 
  31. Teatero S, Ferrieri P, Martin I, Demczuk W, McGeer A, Fittipaldi N. Serotype distribution, population structure, and antimicrobial resistance of group B Streptococcus strains recovered from colonized pregnant women. J Clin Microbiol. 2017;55(2):412-22.  https://doi.org/10.1128/JCM.01615-16  PMID: 27852675 
  32. Bellais S, Six A, Fouet A, Longo M, Dmytruk N, Glaser P, et al. Capsular switching in group B Streptococcus CC17 hypervirulent clone: a future challenge for polysaccharide vaccine development. J Infect Dis. 2012;206(11):1745-52.  https://doi.org/10.1093/infdis/jis605  PMID: 23002446 
  33. Da Cunha V, Davies MR, Douarre P-E, Rosinski-Chupin I, Margarit I, Spinali S, et al. Streptococcus agalactiae clones infecting humans were selected and fixed through the extensive use of tetracycline. Nat Commun. 2014;5(1):4544.  https://doi.org/10.1038/ncomms5544  PMID: 25088811 
  34. Manning SD, Springman AC, Lehotzky E, Lewis MA, Whittam TS, Davies HD. Multilocus sequence types associated with neonatal group B streptococcal sepsis and meningitis in Canada. J Clin Microbiol. 2009;47(4):1143-8.  https://doi.org/10.1128/JCM.01424-08  PMID: 19158264 
  35. Martins ER, Andreu A, Correia P, Juncosa T, Bosch J, Ramirez M, et al. Group B streptococci causing neonatal infections in barcelona are a stable clonal population: 18-year surveillance. J Clin Microbiol. 2011;49(8):2911-8.  https://doi.org/10.1128/JCM.00271-11  PMID: 21697333 
  36. European Centre for Disease Prevention and Control (ECDC). The European Surveillance of Antimicrobial Consumption Network interactive database on antimicrobial consumption (ESAC-Net). Stockholm: ECDC. [Accessed July 2017]. Available from: http://ecdc.europa.eu/en/healthtopics/antimicrobial_resistance/esac-net-database/Pages/database.aspx
  37. Silva-Costa C, Friães A, Ramirez M, Melo-Cristino J. Macrolide-resistant Streptococcus pyogenes: prevalence and treatment strategies. Expert Rev Anti Infect Ther. 2015;13(5):615-28.  https://doi.org/10.1586/14787210.2015.1023292  PMID: 25746210 
  38. Brochet M, Couvé E, Bercion R, Sire JM, Glaser P. Population structure of human isolates of Streptococcus agalactiae from Dakar and Bangui. J Clin Microbiol. 2009;47(3):800-3.  https://doi.org/10.1128/JCM.01103-08  PMID: 19109468 
Increasing macrolide resistance among Streptococcus agalactiae causing invasive disease in non-pregnant adults was driven by a single capsular-transformed lineage, Portugal, 2009 to 2015
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=El%C3%ADsia+Lopes&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lopes Elísia</a>, <a href="/search?value1=T%C3%A2nia+Fernandes&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fernandes Tânia</a>, <a href="/search?value1=Miguel+P+Machado&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Machado Miguel P</a>, <a href="/search?value1=Jo%C3%A3o+Andr%C3%A9+Carri%C3%A7o&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Carriço João André</a>, <a href="/search?value1=Jos%C3%A9+Melo-Cristino&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Melo-Cristino José</a>, <a href="/search?value1=M%C3%A1rio+Ramirez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ramirez Mário</a>, <a href="/search?value1=Elisabete+R+Martins&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Martins Elisabete R</a>, <a href="/search?value1=the+Portuguese+Group+for+the+Study+of+Streptococcal+Infections&option1=author&noRedirect=true" class="nonDisambigAuthorLink">the Portuguese Group for the Study of Streptococcal Infections</a></span>. Increasing macrolide resistance among Streptococcus agalactiae causing invasive disease in non-pregnant adults was driven by a single capsular-transformed lineage, Portugal, 2009 to 2015. <a href="/content/ecdc">Euro Surveill.</a> 2018;23(21):pii=1700473. <a href="https://doi.org/10.2807/1560-7917.ES.2018.23.21.1700473" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2018.23.21.1700473</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 13 Jul 2017;&nbsp;&nbsp; <span class="generated">Accepted</span>: 23 Nov 2017 </span> </p>
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