1887

Microbial Genomics

Volume 7, Issue 7

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

Abstract

Travel to tropical regions is associated with high risk of acquiring extended-spectrum beta-lactamase-producing (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 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 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, =0.021). Genes encoding iron capture systems (), toxins (, ), adhesins (, , ) and colicin () 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 strains belonging to epidemic clones and harbouring ‘virulence genes’, allowing good adaptation to the intestinal microbiota.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): carriage , E. coli , ESBL , long-term carriage , persistence , travel and whole-genome sequencing
Funding
This study was supported by the:
  • FRM (Award DEQ20161136698)
    • Principle Award Recipient: NotApplicable
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-07-19
2021-10-18
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References

  1. Woerther PL, Burdet C, Chachaty E, Andremont A. Trends in human fecal carriage of extended-spectrum β-Lactamases in the community: toward the globalization of CTX-M. Clin Microbiol Rev 2013; 26:744–758 [View Article] [PubMed]
     [Google Scholar]
  2. Ruppé E, Armand-Lefèvre L, Estellat C, Consigny PH, El Mniai A. High rate of acquisition but short duration of carriage of multidrug-resistant Enterobacteriaceae after travel to the tropics. Clin Infect Dis 2015; 61:593–600 [View Article] [PubMed]
     [Google Scholar]
  3. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis 2017; 17:78–85 [View Article] [PubMed]
     [Google Scholar]
  4. Schaumburg F, Sertic SM, Correa-Martinez C, Mellmann A, Köck R et al. Acquisition and colonization dynamics of antimicrobial-resistant bacteria during international travel: A prospective cohort study. Clin Microbiol Infect 2019; 25:1287e1-1287.e7 [View Article] [PubMed]
     [Google Scholar]
  5. Leo S, Lazarevic V, Gaïa N, Estellat C, Girard M. The intestinal microbiota predisposes to traveler’s diarrhea and to the carriage of multidrug-resistant Enterobacteriaceae after traveling to tropical regions. Gut Microbes 2019; 10:631–641 [View Article] [PubMed]
     [Google Scholar]
  6. Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010; 8:207–217 [View Article] [PubMed]
     [Google Scholar]
  7. Nowrouzian F, Hesselmar B, Saalman R, Strannegård IL, Åberg N. Escherichia coli in infants’ intestinal microflora: colonization rate, strain turnover, and virulence gene carriage. Pediatr Res 2003; 54:8–14 [View Article] [PubMed]
     [Google Scholar]
  8. Ostblom A, Adlerberth I, Wold AE, Nowrouzian FL. Pathogenicity island markers, virulence determinants malX and usp, and the capacity of Escherichia coli to persist in infants’ commensal microbiotas. Appl Environ Microbiol 2011; 77:2303–2308 [View Article] [PubMed]
     [Google Scholar]
  9. Nowrouzian FL, Adlerberth I, Wold AE. Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells. Microbes Infect 2006; 8:834–840 [View Article] [PubMed]
     [Google Scholar]
  10. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5:58–65 [View Article] [PubMed]
     [Google Scholar]
  11. Desvillechabrol D, Bouchier C, Kennedy S, Cokelaer T. n.d Sequana coverage: detection and characterization of genomic variations using running median and mixture models. Gigascience 7: [View Article] [PubMed]
     [Google Scholar]
  12. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  13. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
     [Google Scholar]
  14. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article] [PubMed]
     [Google Scholar]
  15. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
     [Google Scholar]
  16. Bourrel AS, Poirel L, Royer G, Darty M, Vuillemin X. Colistin resistance in Parisian inpatient faecal Escherichia coli as the result of two distinct evolutionary pathways. J Antimicrob Chemother 2019; 74:1521–1530 [View Article] [PubMed]
     [Google Scholar]
  17. Royer G, Decousser JW, Branger C, Dubois M, Médigue C. n.d PlaScope: a targeted approach to assess the plasmidome from genome assemblies at the species level. Microb Genom 4: [View Article] [PubMed]
     [Google Scholar]
  18. Cokelaer T, Desvillechabrol D, Legendre R, Cardon M. Sequana’: a Set of Snakemake NGS pipelines. JOSS 2017; 2:352 [View Article]
     [Google Scholar]
  19. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article] [PubMed]
     [Google Scholar]
  20. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article] [PubMed]
     [Google Scholar]
  21. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST. Nucleic Acids Res 2014; 42:D206–214 [View Article] [PubMed]
     [Google Scholar]
  22. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
     [Google Scholar]
  23. Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S. MicroScope--an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res 2013; 41:D636–647 [View Article] [PubMed]
     [Google Scholar]
  24. Ghalayini M, Magnan M, Dion S, Zatout O, Bourguignon L. Long-term evolution of the natural isolate of Escherichia coli 536 in the mouse gut colonized after maternal transmission reveals convergence in the constitutive expression of the lactose operon. Mol Ecol 2019; 28:4470–4485 [View Article] [PubMed]
     [Google Scholar]
  25. Galardini M, Clermont O, Baron A, Busby B, Dion S et al. Major role of iron uptake systems in the intrinsic extra-intestinal virulence of the genus Escherichia revealed by a genome-wide association study. PLoS Genet 2020; 16:e1009065 [View Article] [PubMed]
     [Google Scholar]
  26. Denamur E, Clermont O, Bonacorsi S, Gordon D. The population genetics of pathogenic Escherichia coli. Nat Rev Microbiol 2021; 19:37–54 [View Article] [PubMed]
     [Google Scholar]
  27. van Duijkeren E, Wielders CCH, Dierikx CM, van Hoek AHAM, Hengeveld P et al. Long-term carriage of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in the general population in the Netherlands. Clin Infect Dis 2018; 66:1368–1376 [View Article] [PubMed]
     [Google Scholar]
  28. Löhr IH, Rettedal S, Natås OB, Naseer U, Øymar K. Long-term faecal carriage in infants and intra-household transmission of CTX-M-15-producing Klebsiella pneumoniae following a nosocomial outbreak. J Antimicrob Chemother 2013; 68:1043–1048
     [Google Scholar]
  29. Birgy A, Cohen R, Levy C, Bidet P, Courroux C. Community faecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in french children. BMC Infect Dis 2012; 12:315 [View Article] [PubMed]
     [Google Scholar]
  30. Nicolas-Chanoine MH, Gruson C, Bialek-Davenet S, Bertrand X, Thomas-Jean F. 10-Fold increase (2006–11) in the rate of healthy subjects with extended-spectrum β-lactamase-producing Escherichia coli faecal carriage in a Parisian check-up centre. J Antimicrob Chemother 2013; 68:562–568 [View Article]
     [Google Scholar]
  31. Nilsen E, Haldorsen BC, Sundsfjord A, Simonsen GS, Ingebretsen A. Large IncHI2-plasmids encode extended-spectrum β-lactamases (ESBLs) in Enterobacter spp. bloodstream isolates, and support ESBL-transfer to Escherichia coli. Clin Microbio Infect 2013; 19:E516–E518 [View Article]
     [Google Scholar]
  32. Rashid H, Rahman M. Possible transfer of plasmid mediated third generation cephalosporin resistance between Escherichia coli and Shigella sonnei in the human gut. Infect Genet Evol 2015; 30:15–18 [View Article] [PubMed]
     [Google Scholar]
  33. Ghalayini M, Launay A, Bridier-Nahmias A, Clermont O, Denamur E et al. Evolution of a dominant natural isolate of Escherichia coli in the human gut over the course of a year suggests a neutral evolution with reduced effective population size. Appl Environ Microbiol 2018; 84: [View Article] [PubMed]
     [Google Scholar]
  34. Tenaillon O, Barrick JE, Ribeck N, Deatherage DE, Blanchard JL. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 2016; 536:165–170 [View Article] [PubMed]
     [Google Scholar]
  35. Good BH, McDonald MJ, Barrick JE, Lenski RE, Desai MM. The dynamics of molecular evolution over 60,000 generations. Nature 2017; 551:45–50 [View Article] [PubMed]
     [Google Scholar]
  36. Mahérault A-C, Kemble H, Magnan M, Gachet B, Roche D et al. Advantage of the F2:A1:B-IncF pandemic plasmid over IncC plasmids in in vitro acquisition and evolution of blaCTX-M gene-bearing plasmids in Escherichia coli. Antimicrob Agents Chemother 2019; 63: [View Article] [PubMed]
     [Google Scholar]
  37. Rogers BA, Kennedy KJ, Sidjabat HE, Jones M, Collignon P. Prolonged carriage of resistant E. coli by returned travellers: clonality, risk factors and bacterial characteristics. Eur J Clin Microbiol Infect Dis 2012; 31:2413–2420 [View Article] [PubMed]
     [Google Scholar]
  38. Schaufler K, Semmler T, Wieler LH, Trott DJ, Pitout J et al. Genomic and functional analysis of emerging virulent and multidrug-resistant Escherichia coli lineage sequence type 648. Antimicrob Agents Chemother 2019; 63: [View Article] [PubMed]
     [Google Scholar]
  39. Dautzenberg MJD, Haverkate MR, Bonten MJM, Bootsma MCJ. Epidemic potential of Escherichia coli ST131 and Klebsiella pneumoniae ST258: a systematic review and meta-analysis. BMJ Open 2016; 6:e009971
     [Google Scholar]
  40. Hu YY, Cai JC, Zhou HW, Chi D, Zhang XF et al. Molecular typing of CTX-M-producing Escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Appl Environ Microbiol 2013; 79:5988–5996 [View Article]
     [Google Scholar]
  41. Massot M, Daubié A-S, Clermont O, Jauréguy F, Couffignal C et al. Phylogenetic, virulence and antibiotic resistance characteristics of commensal strain populations of Escherichia coli from community subjects in the Paris area in 2010 and evolution over 30 years. Microbiology (Reading) 2016; 162:642–650 [View Article] [PubMed]
     [Google Scholar]
  42. Servin AL. Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/Dr DAEC): current insights and future challenges. Clin Microbiol Rev 2014; 27:823–869 [View Article] [PubMed]
     [Google Scholar]
  43. Ulett GC, Valle J, Beloin C, Sherlock O, Ghigo JM. Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 2007; 75:3233–3244 [View Article] [PubMed]
     [Google Scholar]
  44. Blackburn D, Husband A, Saldaña Z, Nada RA, Klena J. Distribution of the Escherichia coli common pilus among diverse strains of human enterotoxigenic E. J Clin Microbiol 2009; 47:1781–1784 [View Article] [PubMed]
     [Google Scholar]
  45. Navarro-Garcia F, Ruiz-Perez F, Cataldi Á, Larzábal M. Type VI secretion system in pathogenic Escherichia coli: Structure, role in virulence, and acquisition. Front Microbiol 2019; 10:1965 [View Article]
     [Google Scholar]
  46. Dautin N. Serine protease autotransporters of enterobacteriaceae (SPATEs): biogenesis and function. Toxins (Basel) 2010; 2:1179–1206 [View Article] [PubMed]
     [Google Scholar]
  47. Smajs D, Weinstock GM. The iron- and temperature-regulated cjrBC genes of Shigella and enteroinvasive Escherichia coli strains code for colicin Js uptake. J Bacteriol 2001; 183:3958–3966 [View Article] [PubMed]
     [Google Scholar]
  48. Le Gall T, Clermont O, Gouriou S, Picard B, Nassif X. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol Biol Evol 2007; 24:2373–2384 [View Article] [PubMed]
     [Google Scholar]
  49. Diard M, Garry L, Selva M, Mosser T, Denamur E et al. Pathogenicity-associated islands in extraintestinal pathogenic Escherichia coli are fitness elements involved in intestinal colonization. J Bacteriol 2010; 192:4885–4893 [View Article] [PubMed]
     [Google Scholar]
  50. Leimbach A, Hacker J, Dobrindt UE. coli as an all-rounder: the thin line between commensalism and pathogenicity. Curr Top Microbiol Immunol 2013; 358:3–32 [View Article] [PubMed]
     [Google Scholar]
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Dynamics of extended-spectrum beta-lactamase-producing Enterobacterales colonization in long-term carriers following travel abroad
M Gen 7, 000576 (2021); https://doi.org/10.1099/mgen.0.000576
/content/journal/mgen/10.1099/mgen.0.000576
/content/journal/mgen/10.1099/mgen.0.000576
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