Enterobacteriaceae and Bacteroidaceae provide resistance to travel-associated intestinal colonization by multi-drug resistant Escherichia coli

Matthew Davies, Gianluca Galazzo, Jarne M van Hattem, Maris S Arcilla, Damian C Melles, Menno D de Jong, Constance Schultsz, Petra Wolffs, Alan McNally, Willem van Schaik, John Penders

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Abstract

Previous studies have shown high acquisition risks of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) among international travelers visiting antimicrobial resistance (AMR) hotspots. Although antibiotic use and travelers' diarrhea have shown to influence the ESBL-E acquisition risk, it remains largely unknown whether successful colonization of ESBL-E during travel is associated with the composition, functional capacity and resilience of the traveler's microbiome. The microbiome of pre- and post-travel fecal samples from 190 international travelers visiting Africa or Asia was profiled using whole metagenome shotgun sequencing. A metagenomics species concept approach was used to determine the microbial composition, population diversity and functional capacity before travel and how it is altered longitudinally. Eleven travelers were positive for ESBL-E before travel and removed from the analysis. Neither the microbial richness (Chao1), diversity (effective Shannon) and community structure (Bray-Curtis dissimilarity) in pretravel samples nor the longitudinal change of these metrics during travel were predictive for ESBL-E acquisition. A zero-inflated two-step beta-regression model was used to determine how the longitudinal change in both prevalence and abundance of each taxon was related to ESBL acquisition. There were detected increases in both the prevalence and abundance of Citrobacter freundii and two members of the genus Bacteroides, in association with remaining uncolonized by ESBL-E. These results highlight the potential of these individual microbes as a microbial consortium to prevent the acquisition of ESBL-E. The ability to alter a person's colonization resistance to a bacterium could be key to intervention strategies that aim to minimize the spread of MDR bacteria.

Original languageEnglish
Article number2060676
JournalGut Microbes
Volume14
Issue number1
DOIs
Publication statusPublished - 7 Apr 2022

Bibliographical note

Funding Information:
This study was funded by a PhD studentship jointly between The University of Birmingham and Maastricht University. The COMBAT study was funded by The Netherlands Organization for Health, Research and Development [ZonMw; 50-51700-98-120]. This work was supported in part by awards to JP through the Dutch Research Council [VIDI grant nederlandse organisatie voor wetenschappelijk onderzoek 016.156.427]. We thank all the employees of the travel clinics (Institute for Tropical Diseases, Havenziekenhuis; Centre of Tropical Medicine and Travel Medicine, Amsterdam University Medical Centre; EASE Travel Health & Support) for their help in the recruitment of participants. We would like to thank Pernille Neve Myers for their guidance with the coabundance gene clustering. We would like to thank all additional members of the COMBAT consortium, which is composed of Martin C.J. Bootsma, Perry J. van Genderen, Abraham Goorhuis, Martin P. Grobusch, Nicky Molhoek, Astrid M.L. Oude Lashof, Ellen E. Stobberingh and Henri A. Verbrugh.

Publisher Copyright:
© 2022 The Author(s). Published with license by Taylor & Francis Group, LLC.

Keywords

  • Extended-spectrum beta-lactamase
  • antimicrobial resistance
  • metagenome
  • microbiome
  • travel

ASJC Scopus subject areas

  • Gastroenterology
  • Microbiology (medical)
  • Infectious Diseases
  • Microbiology

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