Dynamics of extended-spectrum beta-lactamase-producing Enterobacterales colonization in long-term carriers following travel abroad

Author:

Armand-Lefèvre Laurence12ORCID,Rondinaud Emilie12,Desvillechabrol Dimitri3ORCID,Mullaert Jimmy1,Clermont Olivier1,Petitjean Marie1ORCID,Ruppe Etienne12ORCID,Cokelaer Thomas43,Bouchier Christiane3ORCID,Tenaillon Olivier1ORCID,Ma Laurence3,Nooroya Yasmine1,Matheron Sophie51,Andremont Antoine12,Denamur Erick61,Kennedy Sean P.7ORCID,

Affiliation:

1. Université de Paris, IAME, INSERM UMR 1137, F-75018 Paris, France

2. Laboratoire de Bactériologie, Hôpital Bichat-Claude Bernard, AP-HP Nord-Université de Paris, F-75018 Paris, France

3. Plate-forme Technologique Biomics – Centre de Ressources et Recherches Technologiques (C2RT), Institut Pasteur, F-75015 Paris, France

4. Hub de Bioinformatique et Biostatistique – Département Biologie Computationnelle, Institut Pasteur, USR 3756 CNRS, F-75015 Paris, France

5. Service de Maladies Infectieuses et Tropicales, Hôpital Bichat-Claude Bernard, AP-HP Nord-Université de Paris, F-75018 Paris, France

6. Laboratoire de Génétique Moléculaire, Hôpital Bichat-Claude Bernard, AP-HP Nord-Université de Paris, F-75018 Paris, France

7. Département Biologie Computationnelle, Institut Pasteur, USR 3756 CNRS, F-75015 Paris, France

Abstract

Travel to tropical regions is associated with high risk of acquiring extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) that are typically cleared in less than 3 months following return. The conditions leading to persistent carriage that exceeds 3 months in some travellers require investigation. Whole-genome sequencing (Illumina MiSeq) was performed on the 82 ESBL-E isolates detected upon return and 1, 2, 3, 6 and 12 months later from the stools of 11 long-term (>3 months) ESBL-E carriers following travel abroad. One to five different ESBL Escherichia coli strains were detected per traveller upon return, and this diminished to one after 3 months. Long-term carriage was due to the presence of the same ESBL E. coli strain, for more than 3 months, in 9 out of 11 travellers, belonging to epidemic sequence type complexes (STc 10, 14, 38, 69, 131 and 648). The mean carriage duration of strains belonging to phylogroups B2/D/F, associated with extra-intestinal virulence, was higher than that for commensal-associated A/B1/E phylogroups (3.5 vs 0.5 months, P=0.021). Genes encoding iron capture systems (fyuA, irp), toxins (senB, sat), adhesins (flu, daaF, afa/nfaE, pap, ecpA) and colicin (cjrA) were more often present in persistent strains than in transient ones. Single-nucleotide polymorphism (SNP) analysis in persistent strains showed a maximum divergence of eight SNPs over 12 months without signs of adaptation. Genomic plasticity was observed during the follow-up with the loss or gain of mobile genetic elements such as plasmids, integrons and/or transposons that may contain resistance genes at different points in the follow-up. Long-term colonization of ESBL-E following travel is primarily due to the acquisition of E. coli strains belonging to epidemic clones and harbouring ‘virulence genes’, allowing good adaptation to the intestinal microbiota.

Funder

FRM

Publisher

Microbiology Society

Subject

General Medicine

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