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Volume 72, Issue 6

Long-term surveillance of group B strains isolated from infection and colonization in pregnant women and newborns No Access

Abstract

Group B (GBS) remains the leading cause of bacterial neonatal infections worldwide, despite the spread of recommendations on vaginal screening and antibiotic prophylaxis.

There is a need to evaluate the potential changes in GBS epidemiology over time following the introduction of such guidelines.

Our aim was to perform a descriptive analysis of the epidemiological characteristics of GBS by conducting a long-term surveillance of strains isolated between 2000 and 2018, using molecular typing methods.

A total of 121 invasive strains, responsible for maternal infections (20 strains), fetal infections (8 strains) and neonatal infections (93 strains), were included in the study, representing all the invasive isolates during the period; in addition, 384 colonization strains isolated from vaginal or newborn samples were randomly selected. The 505 strains were characterized by capsular polysaccharide (CPS) type multiplex PCR assay and the clonal complex (CC) was assigned using a single nucleotide polymorphism PCR assay. Antibiotic susceptibility was also determined.

CPS types III (32.1 % of the strains), Ia (24.6 %) and V (19 %) were the most prevalent. The five main CCs observed were CC1 (26.3 % of the strains), CC17 (22.2 %), CC19 (16.2 %), CC23 (15.8 %) and CC10 (13.9 %). Neonatal invasive GBS diseases were predominantly due to CC17 isolates (46.3 % of the strains), which mainly express CPS type III (87.5 %), with a very high prevalence in late-onset diseases (76.2 %).

Between 2000 and 2018, we observed a decrease in the proportion of CC1 strains, which mainly express CPS type V, and an increase in the proportion of CC23 strains, mainly expressing CPS type Ia. Conversely, there was no significant change in the proportion of strains resistant to macrolides, lincosamides or tetracyclines. The two molecular techniques used in our study provide almost as much information as classical serotyping and multilocus sequence typing, but are quicker, easy to perform, and avoid long sequencing and analysis steps.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): colonization , group B Streptococcus , infection and neonatal
© 2023 The Authors
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2023-06-19
2024-05-17
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References

  1. Hanna M, Noor A. Streptococcus group B. In StatPearls Treasure Island, FL: StatPearls; 2020 [PubMed]
     [Google Scholar]
  2. Fry RM. Fatal infections by haemolytic streptococcus group B. The Lancet 1938; 231:199–201 [View Article]
     [Google Scholar]
  3. Mannik M, Baringer JR, Stokes J III. Infections due to group B beta-hemolytic streptococci. N Engl J Med 1962; 266:910–913 [View Article]
     [Google Scholar]
  4. Six A, Joubrel C, Tazi A, Poyart C. Infections materno-fœtales à Streptococcus agalactiae. La Presse Médicale 2014; 43:706–714 [View Article]
     [Google Scholar]
  5. van der Mee-Marquet N, Jouannet C, Domelier A-S, Arnault L, Lartigue M-F et al. Genetic diversity of Streptococcus agalactiae strains and density of vaginal carriage. J Med Microbiol 2009; 58:169–173 [View Article] [PubMed]
     [Google Scholar]
  6. Raabe VN, Shane AL. Group B Streptococcus (Streptococcus agalactiae). Microbiol Spectr 2019; 7:gpp3-0007-2018 [View Article]
     [Google Scholar]
  7. Cho C-Y, Tang Y-H, Chen Y-H, Wang S-Y, Yang Y-H et al. Group B streptococcal infection in neonates and colonization in pregnant women: an epidemiological retrospective analysis. J Microbiol Immunol Infect 2019; 52:265–272 [View Article] [PubMed]
     [Google Scholar]
  8. Money D, Allen VM. The prevention of early-onset neonatal group B streptococcal disease. J Obstet Gynaecol Can 2016; 38:S326–S335 [View Article] [PubMed]
     [Google Scholar]
  9. Russell NJ, Seale AC, O’Driscoll M, O’Sullivan C, Bianchi-Jassir F et al. Maternal colonization with group B Streptococcus and serotype distribution worldwide: systematic review and meta-analyses. Clin Infect Dis Off Publ Infect Dis Soc Am 2017; 65:S100–S111 [View Article]
     [Google Scholar]
  10. Hasperhoven G, Al‐Nasiry S, Bekker V, Villamor E, Kramer B. Universal screening versus risk‐based protocols for antibiotic prophylaxis during childbirth to prevent early‐onset group B streptococcal disease: a systematic review and meta‐analysis. BJOG Int J Obstet Gy 2020; 127:680–691 [View Article]
     [Google Scholar]
  11. Cieslewicz MJ, Chaffin D, Glusman G, Kasper D, Madan A et al. Structural and genetic diversity of group B streptococcus capsular polysaccharides. Infect Immun 2005; 73:3096–3103 [View Article] [PubMed]
     [Google Scholar]
  12. Toniolo C, Balducci E, Romano MR, Proietti D, Ferlenghi I et al. Streptococcus agalactiae capsule polymer length and attachment is determined by the proteins CpsABCD. J Biol Chem 2015; 290:9521–9532 [View Article] [PubMed]
     [Google Scholar]
  13. Marques MB, Kasper DL, Pangburn MK, Wessels MR. Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci. Infect Immun 1992; 60:3986–3993 [View Article] [PubMed]
     [Google Scholar]
  14. Slotved HC, Kong F, Lambertsen L, Sauer S, Gilbert GL. Serotype IX, a proposed new Streptococcus agalactiae serotype. J Clin Microbiol 2007; 45:2929–2936 [View Article] [PubMed]
     [Google Scholar]
  15. Afshar B, Broughton K, Creti R, Decheva A, Hufnagel M et al. International external quality assurance for laboratory identification and typing of Streptococcus agalactiae (group B streptococci). J Clin Microbiol 2011; 49:1475–1482 [View Article] [PubMed]
     [Google Scholar]
  16. Jones N, Bohnsack JF, Takahashi S, Oliver KA, Chan M-S et al. Multilocus sequence typing system for group B streptococcus. J Clin Microbiol 2003; 41:2530–2536 [View Article] [PubMed]
     [Google Scholar]
  17. Sun Y, Kong F, Zhao Z, Gilbert GL. Comparison of a 3-set genotyping system with multilocus sequence typing for Streptococcus agalactiae (group B Streptococcus). J Clin Microbiol 2005; 43:4704–4707 [View Article] [PubMed]
     [Google Scholar]
  18. Li J, Ji W, Gao K, Zhou H, Zhang L et al. Molecular characteristics of group B Streptococcus isolates from infants in southern mainland China. BMC Infect Dis 2019; 19:812 [View Article] [PubMed]
     [Google Scholar]
  19. van der Mee-Marquet N, Fourny L, Arnault L, Domelier A-S, Salloum M et al. Molecular characterization of human-colonizing Streptococcus agalactiae strains isolated from throat, skin, anal margin, and genital body sites. J Clin Microbiol 2008; 46:2906–2911 [View Article] [PubMed]
     [Google Scholar]
  20. Bergal A, Loucif L, Benouareth DE, Bentorki AA, Abat C et al. Molecular epidemiology and distribution of serotypes, genotypes, and antibiotic resistance genes of Streptococcus agalactiae clinical isolates from Guelma, Algeria and Marseille, France. Eur J Clin Microbiol Infect Dis 2015; 34:2339–2348 [View Article] [PubMed]
     [Google Scholar]
  21. Rao GG, Khanna P. To screen or not to screen women for group B Streptococcus (Streptococcus agalactiae) to prevent early onset sepsis in newborns: recent advances in the unresolved debate. Ther Adv Infect Dis 2020; 7:2049936120942424 [View Article] [PubMed]
     [Google Scholar]
  22. Prevention of perinatal group B streptococcal disease: a public health perspective. Centers for disease control and prevention. MMWR Recomm Rep 1996; 45:1–24 [PubMed]
     [Google Scholar]
  23. Filkins L, Hauser JR, Robinson-Dunn B, Tibbetts R, Boyanton BL et al. American Society for Microbiology provides 2020 guidelines for detection and identification of group B Streptococcus. J Clin Microbiol 2020; 59:e01230–20 [View Article]
     [Google Scholar]
  24. Agence Nationale d’Accreditation et d’Evaluation en Sante Antenatal Prevention of the Risk of Early Neonatal Bacterial Infection France: ANAES; 2001
     [Google Scholar]
  25. Zangwill KM, Schuchat A, Wenger JD. Group B streptococcal disease in the United States, 1990: report from a multistate active surveillance system. MMWR CDC Surveill Summ 1992; 41:25–32
     [Google Scholar]
  26. Centers for Disease Control and Prevention Active Bacterial Core Surveillance Report, Emerging Infections Program Network, Group B Streptococcus, 2019 Atlanta, GA: CDC; 2019
     [Google Scholar]
  27. Comité de l’antibiogramme de la Société Française de Microbiologie/European Committee on Antimicrobial Susceptibility Testing Recommendations France: Société Française de Microbiologie; 2020
     [Google Scholar]
  28. Imperi M, Pataracchia M, Alfarone G, Baldassarri L, Orefici G et al. A multiplex PCR assay for the direct identification of the capsular type (Ia to IX) of Streptococcus agalactiae. J Microbiol Methods 2010; 80:212–214 [View Article] [PubMed]
     [Google Scholar]
  29. Honsa E, Fricke T, Stephens AJ, Ko D, Kong F et al. Assignment of Streptococcus agalactiae isolates to clonal complexes using a small set of single nucleotide polymorphisms. BMC Microbiol 2008; 8:140 [View Article] [PubMed]
     [Google Scholar]
  30. Slotved HC, Sauer S, Konradsen HB. False-negative results in typing of group B streptococci by the standard lancefield antigen extraction method. J Clin Microbiol 2002; 40:1882–1883 [View Article] [PubMed]
     [Google Scholar]
  31. Kong F, Lambertsen LM, Slotved HC, Ko D, Wang H et al. Use of phenotypic and molecular serotype identification methods to characterize previously nonserotypeable group B streptococci. J Clin Microbiol 2008; 46:2745–2750 [View Article] [PubMed]
     [Google Scholar]
  32. Ramaswamy SV, Ferrieri P, Madoff LC, Flores AE, Kumar N et al. Identification of novel cps locus polymorphisms in nontypable group B Streptococcus. J Med Microbiol 2006; 55:775–783 [View Article]
     [Google Scholar]
  33. Rallu F, Barriga P, Scrivo C, Martel-Laferrière V, Laferrière C. Sensitivities of antigen detection and PCR assays greatly increased compared to that of the standard culture method for screening for group B Streptococcus carriage in pregnant women. J Clin Microbiol 2006; 44:725–728 [View Article]
     [Google Scholar]
  34. Plainvert C, El Alaoui F, Tazi A, Joubrel C, Anselem O et al. Intrapartum group B Streptococcus screening in the labor ward by Xpert GBS real-time PCR. Eur J Clin Microbiol Infect Dis 2018; 37:265–270 [View Article] [PubMed]
     [Google Scholar]
  35. Di Renzo GC, Melin P, Berardi A, Blennow M, Carbonell-Estrany X et al. Intrapartum GBS screening and antibiotic prophylaxis: a European consensus conference. J Matern Fetal Neonatal Med 2015; 28:766–782 [View Article] [PubMed]
     [Google Scholar]
  36. Kimura K, Suzuki S, Wachino J, Kurokawa H, Yamane K et al. First molecular characterization of group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother 2008; 52:2890–2897 [View Article]
     [Google Scholar]
  37. Nagano N, Nagano Y, Kimura K, Tamai K, Yanagisawa H et al. Genetic heterogeneity in pbp genes among clinically isolated group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother 2008; 52:4258–4267 [View Article]
     [Google Scholar]
  38. Vuillemin X, Hays C, Plainvert C, Dmytruk N, Louis M et al. Invasive group B Streptococcus infections in non-pregnant adults: a retrospective study, France, 2007–2019. Clin Microbiol Infect 2021; 27:129E1–129E4 [View Article]
     [Google Scholar]
  39. Lopes E, Fernandes T, Machado MP, Carriço JA, Melo-Cristino J et al. 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. Euro Surveill 2018; 23:1700473 [View Article] [PubMed]
     [Google Scholar]
  40. Kaminska D, Ratajczak M, Szumała-Kąkol A, Dlugaszewska J, Nowak-Malczewska DM et al. Increasing resistance and changes in distribution of serotypes of Streptococcus agalactiae in Poland. Pathogens 2020; 9:526 [View Article] [PubMed]
     [Google Scholar]
  41. Gizachew M, Tiruneh M, Moges F, Tessema B. Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profiles in Africa: a meta-analysis. Ann Clin Microbiol Antimicrob 2019; 18:14 [View Article] [PubMed]
     [Google Scholar]
  42. de Azavedo JCS, McGavin M, Duncan C, Low DE, McGeer A. Prevalence and mechanisms of macrolide resistance in invasive and noninvasive group B streptococcus isolates from Ontario, Canada. Antimicrob Agents Chemother 2001; 45:3504–3508 [View Article] [PubMed]
     [Google Scholar]
  43. Centers for Disease Control and Prevention Antibiotic Resistance Threats in the United States, 2019 Atlanta, GA: Centers for Diseases Control and Prevention; 2019
     [Google Scholar]
  44. Tong Z, Kong F, Wang B, Zeng X, Gilbert GL. A practical method for subtyping of Streptococcus agalactiae serotype III, of human origin, using rolling circle amplification. J Microbiol Methods 2007; 70:39–44 [View Article] [PubMed]
     [Google Scholar]
  45. Brimil N, Barthell E, Heindrichs U, Kuhn M, Lütticken R et al. Epidemiology of Streptococcus agalactiae colonization in Germany. Int J Med Microbiol 2006; 296:39–44 [View Article] [PubMed]
     [Google Scholar]
  46. Campisi E, Rosini R, Ji W, Guidotti S, Rojas-López M et al. Genomic analysis reveals multi-drug resistance clusters in group B Streptococcus CC17 hypervirulent isolates causing neonatal invasive disease in Southern mainland China. Front Microbiol 2016; 7:01265 [View Article]
     [Google Scholar]
  47. Nanduri SA, Petit S, Smelser C, Apostol M, Alden NB et al. Epidemiology of invasive early-onset and late-onset group B streptococcal disease in the United States, 2006 to 2015: multistate laboratory and population-based surveillance. JAMA Pediatr 2019; 173:224–233 [View Article]
     [Google Scholar]
  48. Joubrel C, Tazi A, Six A, Dmytruk N, Touak G et al. Group B streptococcus neonatal invasive infections, France 2007–2012. Clin Microbiol Infect 2015; 21:910–916 [View Article] [PubMed]
     [Google Scholar]
  49. Furfaro LL, Chang BJ, Payne MS. Perinatal Streptococcus agalactiae epidemiology and surveillance targets. Clin Microbiol Rev 2018; 31:e00049-18 [View Article] [PubMed]
     [Google Scholar]
  50. Björnsdóttir ES, Martins ER, Erlendsdóttir H, Haraldsson G, Melo-Cristino J et al. Changing epidemiology of group B streptococcal infections among adults in Iceland: 1975–2014. Clin Microbiol Infect 2016; 22:379E9–379E16 [View Article] [PubMed]
     [Google Scholar]
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Long-term surveillance of group B Streptococcus strains isolated from infection and colonization in pregnant women and newborns
J. Med. Microbiol. 72, 001717 (2023); https://doi.org/10.1099/jmm.0.001717
/content/journal/jmm/10.1099/jmm.0.001717
/content/journal/jmm/10.1099/jmm.0.001717
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