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Persistence of group B Streptococcus vaginal colonization and prevalence of hypervirulent CC-17 clone correlate with the country of birth: a prospective 3-month follow-up cohort study

European Journal of Clinical Microbiology & Infectious Diseases volume 40, pages 133–140 (2021)Cite this article

Abstract

To identify factors associated with vaginal colonization and persistence by group B Streptococcus (GBS) and by the hypervirulent neonatal CC-17 clone in late pregnancy and after delivery, a multicentre prospective observational cohort with 3-month follow-up was established in two university hospitals, Paris area, France. Pregnant women were recruited when antenatal screening for GBS vaginal colonization at 34–38 weeks of gestational age was positive. Vaginal samples were analysed by conventional culture methods at antenatal screening, delivery, and 21 and 60 days following delivery. Identification of the hypervirulent neonatal GBS CC-17 was performed. Colonization was defined as persistent when all vaginal samples were positive for GBS. A total of 754 women were included. GBS vaginal colonization was persistent in 63% of the cases (95% CI 59%–67%). Persistent colonization was more likely in women born in Sub-Saharan Africa compared with women born in France (OR = 1.88, 95% CI 1.05–3.52), and GBS CC-17 was overrepresented in women born in Sub-Saharan Africa (OR = 2.09, 95% CI 1.20–3.57). Women born in Sub-Saharan Africa are at higher risk for GBS vaginal persistence than women born in France. This observation correlates with an increased prevalence of the hypervirulent GBS CC-17 in the former group, which likely reflect variations linked to ethnicity and vaginal community-state types and might account for the increased susceptibility of black neonates to GBS infections.

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Data availability

All data were collected in a computerized database, and all biological samples were anonymized before their inclusion in the collection.

References

  1. Le Doare K, Heath PT (2013) An overview of global GBS epidemiology. Vaccine 31:D7–D12. https://doi.org/10.1016/j.vaccine.2013.01.009

  2. Verani JR, McGee L, Schrag SJ, Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention (CDC) (2010) Prevention of perinatal group B streptococcal disease--revised guidelines from CDC, 2010. MMWR Recomm Rep Morb Mortal Wkly Rep Recomm Rep Cent Dis Control 59:1–36

    Google Scholar 

  3. Schrag SJ, Verani JR (2013) Intrapartum antibiotic prophylaxis for the prevention of perinatal group B streptococcal disease: experience in the United States and implications for a potential group B streptococcal vaccine. Vaccine 31:D20–D26. https://doi.org/10.1016/j.vaccine.2012.11.056

    Article  CAS  PubMed  Google Scholar 

  4. Hansen SM, Uldbjerg N, Kilian M, Sørensen UBS (2004) Dynamics of Streptococcus agalactiae colonization in women during and after pregnancy and in their infants. J Clin Microbiol 42:83–89

    Article  Google Scholar 

  5. Goodman JR, Berg RL, Gribble RK, Meier PR, Fee SC, Mitchell PD (1997) Longitudinal study of group B Streptococcus carriage in pregnancy. Infect Dis Obstet Gynecol 5:237–243. https://doi.org/10.1155/S1064744997000409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kwatra G, Adrian PV, Shiri T, Buchmann EJ, Cutland CL, Madhi SA (2014) Serotype-specific acquisition and loss of group B Streptococcus recto-vaginal colonization in late pregnancy. PLoS One 9:e98778. https://doi.org/10.1371/journal.pone.0098778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kwatra G, Cunnington MC, Merrall E, Adrian PV, Ip M, Klugman KP et al (2016) Prevalence of maternal colonisation with group B Streptococcus: a systematic review and meta-analysis. Lancet Infect Dis 16:1076–1084. https://doi.org/10.1016/S1473-3099(16)30055-X

    Article  PubMed  Google Scholar 

  8. Joubrel C, Tazi A, Six A, Dmytruk N, Touak G, Bidet P et al (2015) Group B Streptococcus neonatal invasive infections, France 2007-2012. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 21:910–916. https://doi.org/10.1016/j.cmi.2015.05.039

    Article  CAS  Google Scholar 

  9. Manning SD, Springman AC, Lehotzky E, Lewis MA, Whittam TS, Davies HD (2009) Multilocus sequence types associated with neonatal group B streptococcal sepsis and meningitis in Canada. J Clin Microbiol 47:1143–1148. https://doi.org/10.1128/JCM.01424-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Tazi A, Plainvert C, Anselem O, Ballon M, Marcou V, Seco A et al (2019) Risk factors for infant colonization by hypervirulent CC17 group B Streptococcus : toward the understanding of late-onset disease. Clin Infect Dis 69(10):1740–1748. https://doi.org/10.1093/cid/ciz033

    Article  CAS  PubMed  Google Scholar 

  11. Poyart C, Tazi A, Réglier-Poupet H, Billoët A, Tavares N, Raymond J et al (2007) Multiplex PCR assay for rapid and accurate capsular typing of group B streptococci. J Clin Microbiol 45:1985–1988. https://doi.org/10.1128/JCM.00159-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lamy M-C, Dramsi S, Billoët A, Réglier-Poupet H, Tazi A, Raymond J et al (2006) Rapid detection of the “highly virulent” group B Streptococcus ST-17 clone. Microbes Infect 8:1714–1722. https://doi.org/10.1016/j.micinf.2006.02.008

    Article  CAS  PubMed  Google Scholar 

  13. Berardi A, Rossi C, Creti R, China M, Gherardi G, Venturelli C et al (2013) Group B streptococcal colonization in 160 mother-baby pairs: a prospective cohort study. J Pediatr 163:1099–104.e1. https://doi.org/10.1016/j.jpeds.2013.05.064

    Article  PubMed  Google Scholar 

  14. Russell NJ, Seale AC, O’Driscoll M, O’Sullivan C, Bianchi-Jassir F, Gonzalez-Guarin J et al (2017) Maternal colonization with group B Streptococcus and serotype distribution worldwide: systematic review and meta-analyses. Clin Infect Dis 65:S100–S111. https://doi.org/10.1093/cid/cix658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gopal Rao G, Hiles S, Bassett P, Lamagni T (2019) Differential rates of group B streptococcus (GBS) colonisation in pregnant women in a racially diverse area of London, UK : a cross-sectional study. BJOG Int J Obstet Gynaecol 126:1347–1353. https://doi.org/10.1111/1471-0528.15648

    Article  CAS  Google Scholar 

  16. National Institute of statistics and economic studies (Insee). [French, foreign and immigrant populations in France since 2006] in French. 2015 [cited 2018 31]. doi: https://www.insee.fr/fr/statistiques/1410693. Accessed May 31 2020

  17. Davies HD, Miller MA, Faro S, Gregson D, Kehl SC, Jordan JA (2004) Multicenter study of a rapid molecular-based assay for the diagnosis of group B Streptococcus colonization in pregnant women. Clin Infect Dis Off Publ Infect Dis Soc Am 39:1129–1135. https://doi.org/10.1086/424518

    Article  Google Scholar 

  18. Daniels JP, Gray J, Pattison HM, Gray R, Hills RK, Khan KS et al (2011) Intrapartum tests for group B streptococcus: accuracy and acceptability of screening. BJOG Int J Obstet Gynaecol 118:257–265. https://doi.org/10.1111/j.1471-0528.2010.02725.x

    Article  CAS  Google Scholar 

  19. Lin F-YC, Weisman LE, Azimi P, Young AE, Chang K, Cielo M et al (2011) Assessment of intrapartum antibiotic prophylaxis for the prevention of early-onset group B streptococcal disease. Pediatr Infect Dis J 30:759–763. https://doi.org/10.1097/INF.0b013e31821dc76f

    Article  PubMed  PubMed Central  Google Scholar 

  20. Manning SD, Lewis MA, Springman AC, Lehotzky E, Whittam TS, Davies HD (2008) Genotypic diversity and serotype distribution of group B Streptococcus isolated from women before and after delivery. Clin Infect Dis 46:1829–1837. https://doi.org/10.1086/588296

    Article  CAS  PubMed  Google Scholar 

  21. Johri AK, Paoletti LC, Glaser P, Dua M, Sharma PK, Grandi G et al (2006) Group B Streptococcus: global incidence and vaccine development. Nat Rev Microbiol 4:932–942. https://doi.org/10.1038/nrmicro1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Madrid L, Seale AC, Kohli-Lynch M, Edmond KM, Lawn JE, Heath PT et al (2017) Infant group B streptococcal disease incidence and serotypes worldwide: systematic review and meta-analyses. Clin Infect Dis 65:S160–S172. https://doi.org/10.1093/cid/cix656

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bergal A, Loucif L, Benouareth DE, Bentorki AA, Abat C, Rolain J-M (2015) 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 34:2339–2348. https://doi.org/10.1007/s10096-015-2487-6

    Article  CAS  PubMed  Google Scholar 

  24. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL et al (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci 108:4680–4687. https://doi.org/10.1073/pnas.1002611107

    Article  PubMed  Google Scholar 

  25. Jordan HT, Farley MM, Craig A, Mohle-Boetani J, Harrison LH, Petit S et al (2008) Revisiting the need for vaccine prevention of late-onset neonatal group B streptococcal disease: a multistate, Population-Based Analysis. Pediatr Infect Dis J 27:1057–1064. https://doi.org/10.1097/INF.0b013e318180b3b9

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Florence Artiguebieille, Valerie Fauroux, Farah Ketroussi, Chahrazed Guettouche, and Alexandra Bruneau from URC-CIC Cochin-Necker, AP-HP, Paris, for the management of the clinical trial. We thank all the women who participated in the study as well as the clinical teams for their assistance in recruiting patients to the study.

Code availability

Not applicable.

Funding

The sponsors were Assistance Publique–Hôpitaux de Paris (AP-HP) (Department of Clinical Research), Institut Mérieux and IRT BioAster (Lyon bioPôle). This work was funded by grants from APHP (P111008), Institut Mérieux and IRT BioAster (ColSGB ST-17), Agence Nationale de la Recherche (ANR 13-PRTS-0006), and FRM (DBF20160635740).

The funders had no role in study design, data collection, analysis, or interpretation, in the writing of the manuscript or the decision to submit it for publication. All authors had full access to all the data, and the corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.

Author information

Authors and Affiliations

  1. Department of Bacteriology, University Hospitals Paris Centre Cochin Port Royal, French National Reference Centre for Streptococci, AP-HP, Paris, France

    Céline Plainvert, Caroline Joubrel, Amandine Frigo, Claire Poyart & Asmaa Tazi

  2. FHU Prema, Paris, France

    Céline Plainvert, Olivia Anselem, Caroline Joubrel, Valérie Marcou, Amandine Frigo, Pierre Henri Jarreau, Laurent Mandelbrot, Claire Poyart & Asmaa Tazi

  3. Department of Obstetrics and Gynaecology, Port-Royal Maternity, University Hospitals Paris Centre Cochin Port Royal, AP-HP, Paris, France

    Olivia Anselem & François Goffinet

  4. Department of Neonatal Medicine, University Hospitals Paris Centre Cochin Port Royal, AP-HP, Paris, France

    Valérie Marcou & Pierre Henri Jarreau

  5. Department of Neonatal Medicine, Louis Mourier Hospital, AP-HP, Colombes, France

    Amiel Falloukh

  6. Department of Microbiology, Louis Mourier Hospital, AP-HP, Colombes, France

    Fatma Magdoud El Alaoui

  7. Université de Paris, Paris, France

    Fatma Magdoud El Alaoui, Pierre-Yves Ancel, Pierre Henri Jarreau, Laurent Mandelbrot, François Goffinet, Claire Poyart & Asmaa Tazi

  8. Obstetrical, Perinatal and Paediatric Epidemiology Research Team (EPOPé), INSERM UMR 1153, Paris, France

    Pierre-Yves Ancel & François Goffinet

  9. URC-CIC P1419, University Hospitals Paris Centre Cochin Port Royal, AP-HP, Paris, France

    Pierre-Yves Ancel

  10. Department of Obstetrics and Gynaecology, Louis Mourier Hospital, AP-HP, Colombes, France

    Laurent Mandelbrot

Authors
  1. Céline Plainvert
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  2. Olivia Anselem
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  3. Caroline Joubrel
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  4. Valérie Marcou
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  5. Amiel Falloukh
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  6. Amandine Frigo
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  7. Fatma Magdoud El Alaoui
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  8. Pierre-Yves Ancel
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  9. Pierre Henri Jarreau
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  10. Laurent Mandelbrot
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  11. François Goffinet
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  12. Claire Poyart
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  13. Asmaa Tazi
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Contributions

CPo, AT, and FG conceived and planned the study; all authors collected clinical and epidemiological data. CPl and AT coordinated the microbiological analysis. AT, CPl, and FG performed statistical analysis. AF carried out microbiological technics. CPl, AT, and CPo wrote the first draft of manuscript. CPl, OA, VM, CJ, AF, CB, PHJ, PYA, L.M, FG, CPo, and AT contributed to further drafts, and all authors reviewed and edited the final manuscript.

Corresponding author

Correspondence to Asmaa Tazi.

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Conflict of interest

CPo has received reimbursement for attending meetings from bioMérieux, Cepheid, and Becton-Dickinson and has received research funding from Institut Mérieux. CPo was a member of the SAB of Arsanis Inc. and received honorarium from it in 2015, 2016, and 2017. CPl has received reimbursement from Cepheid for attending ECCMID meeting in 2016. Other authors report no conflicts of interest.

Ethical approval and informed consent

This study was conducted in agreement with French regulations on privacy, data collection, and treatment and was approved by the Comité consultatif sur le traitement de l’information en matière de recherche (CCTIRS, Advisory committee on information processing for research, authorization 12005 of March 1st 2012) and registered at ClinicalTrials.gov, number NCT01719510.

Consent to participate

All women included gave written informed consent to participate.

Consent for publication (include appropriate statements)

All women included gave written informed consent for publication of data.

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Trial registration number NCT01719510 of November 1st 2012.

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Plainvert, C., Anselem, O., Joubrel, C. et al. Persistence of group B Streptococcus vaginal colonization and prevalence of hypervirulent CC-17 clone correlate with the country of birth: a prospective 3-month follow-up cohort study. Eur J Clin Microbiol Infect Dis 40, 133–140 (2021). https://doi.org/10.1007/s10096-020-04011-6

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  • DOI: https://doi.org/10.1007/s10096-020-04011-6

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