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Medical Microbiology and Immunology

, Volume 207, Issue 5–6, pp 287–296 | Cite as

A clone of the emergent Streptococcus pyogenes emm89 clade responsible for a large outbreak in a post-surgery oncology unit in France

  • Céline Plainvert
  • Magalie Longo
  • Elise Seringe
  • Benjamin Saintpierre
  • Elisabeth Sauvage
  • Laurence Ma
  • Johann Beghain
  • Nicolas Dmytruk
  • Gislène Collobert
  • Eric Hernandez
  • Christian Manuel
  • Pascal Astagneau
  • Philippe Glaser
  • Frédéric Ariey
  • Claire Poyart
  • Agnès Fouet
Original Investigation
  • 194 Downloads

Abstract

An outbreak of nosocomial infections due to Streptococcus pyogenes (Group A Streptococcus; GAS) occurred in a post-surgery oncology unit and concerned more than 60 patients and lasted 20 months despite enhanced infection control and prophylaxis measures. All GAS strains were characterized (emm genotype, toxin gene profile and pulse-field gel electrophoresis subtype). Selected strains were sequenced and phylogenetic relationship established. Capacity to form biofilm and interaction with human pulmonary epithelial cells and macrophages were determined. Twenty-six GAS strains responsible for invasive infections (II) and 57 for non-II or colonization were isolated from patients (n = 66) or healthcare workers (n = 13). Seventy strains shared the same molecular markers and 69 the same PFGE pattern; 56 were sequenced. They all belonged to the emerging emm89 clade 3; all but 1 were clonal. Whole genome sequencing identified 43 genetic profiles with sporadic mutations in regulatory genes and acquired mutations in 2 structural genes. Except for two regulatory gene mutants, all strains tested had the same biofilm formation capacity and displayed similar adherence and invasion of pulmonary epithelial cells and phagocytosis and survival in human macrophages. This large outbreak of GAS infection in a post-surgery oncology unit, a setting that contains highly susceptible patients, arose from a strain of the emergent emm89 clade. No relationship between punctual or acquired mutations, invasive status, and strain phenotypic characteristics was found. Noteworthy, the phenotypic characteristics of this clone account for its emergence and its remarkable capacity to elicit outbreaks.

Keywords

Group A Streptococcus emm89 Emerging clade Phylogeny Biofilm Bacterium–cell interaction Outbreak 

Notes

Acknowledgements

This work was supported by Santé Publique France, INSERM, CNRS, Université Paris Descartes and by the High Council for Scientific and Technological Cooperation between France-Israel “Complexity in Biology” program.

Author contributions

Conceived and designed the study: Céline Plainvert, Agnès Fouet, and Claire Poyart. Provided clinical and epidemiological data Elise Seringe, Eric Hernandez, and Pascal Astagneau. Performed the bacteriological analyses Magalie Longo, Nicolas Dmytruk, and Gislaine Collobert. Performed biofilms and phagocytosis analyses Magalie Longo. Performed whole genome sequencing of bacterial strains Benjamin Saintpierre, Elisabeth Sauvage, Laurence Ma and Johann Beghain. Analyzed genomes data Philippe Glaser, Frédéric Ariey, and Agnès Fouet. Wrote the manuscript Claire Poyart, Céline Plainvert, and Agnès Fouet.

Compliance with ethical standards

Conflict of interest

The other authors declare no competing financial interests.

Supplementary material

430_2018_546_MOESM1_ESM.tiff (1.5 mb)
Figure S1. The outbreak emm89-F isolates form substantial biofilms compared to other non-emm89 GAS strains. A tendency curve was calculated using the means shown in Fig. 4, y = 0.0362 x + 8.8 excluding the mutants in regulatory genes. The sampling year is indicated below. Symbols are the same as in Fig. 1 (TIFF 1521 KB)
430_2018_546_MOESM2_ESM.docx (56 kb)
Supplementary material 2 (DOCX 56 KB)
430_2018_546_MOESM3_ESM.docx (24 kb)
Supplementary material 3 (DOCX 23 KB)
430_2018_546_MOESM4_ESM.xlsx (27 kb)
Supplementary material 4 (XLSX 26 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Céline Plainvert
    • 1
    • 2
    • 3
    • 4
  • Magalie Longo
    • 1
    • 2
    • 3
  • Elise Seringe
    • 5
  • Benjamin Saintpierre
    • 1
    • 2
    • 3
  • Elisabeth Sauvage
    • 6
    • 7
  • Laurence Ma
    • 8
  • Johann Beghain
    • 9
  • Nicolas Dmytruk
    • 4
  • Gislène Collobert
    • 4
  • Eric Hernandez
    • 10
  • Christian Manuel
    • 10
  • Pascal Astagneau
    • 5
    • 11
  • Philippe Glaser
    • 6
    • 7
  • Frédéric Ariey
    • 1
    • 2
    • 3
  • Claire Poyart
    • 1
    • 2
    • 3
    • 4
  • Agnès Fouet
    • 1
    • 2
    • 3
  1. 1.INSERM, U1016Institut CochinParisFrance
  2. 2.Université Sorbonne Paris DescartesParisFrance
  3. 3.CNRS (UMR 8104)ParisFrance
  4. 4.Assistance Publique Hôpitaux de Paris, Service de Bactériologie, Centre National de Référence des StreptocoquesGroupe Hospitalier Paris Centre Cochin-Hôtel Dieu-BrocaParisFrance
  5. 5.Centre de Prévention des infections associées aux soinsAssistance Publique Hôpitaux de ParisParisFrance
  6. 6.Unité Ecologie et Evolution de la Résistance aux AntibiotiquesInstitut PasteurParisFrance
  7. 7.CNRS UMR3525ParisFrance
  8. 8.Institut Pasteur, Pôle BiomicsParisFrance
  9. 9.GGIV UnitInstitut PasteurParisFrance
  10. 10.Centre Médical de ForcillesLesignyFrance
  11. 11.Faculté de MédecineAPHP, Pitie-Salpétrière, Sorbonne UniversitéParisFrance

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