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Real-time sampling of travelers shows intestinal colonization by multidrug-resistant bacteria to be a dynamic process with multiple transient acquisitions

A Kantele, E Kuenzli, View ORCID ProfileSJ Dunn, View ORCID ProfileDAB Dance, PN Newton, V Davong, S Mero, View ORCID ProfileSH Pakkanen, View ORCID ProfileA Neumayr, View ORCID ProfileC Hatz, View ORCID ProfileA Snaith, View ORCID ProfileT Kallonen, View ORCID ProfileJ Corander, View ORCID ProfileA McNally
doi: https://doi.org/10.1101/827915
A Kantele
1Inflammation Centre, University of Helsinki and Helsinki University Hospital, Helsinki, Finland
2Human Microbiome Research Program, Faculty of Medicine, University of Helsinki
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  • For correspondence: anu.kantele@hus.fi
E Kuenzli
3Swiss Tropical and Public Health Institute, Basel, Switzerland
4University of Basel, Basel, Switzerland
5Epidemiology, Biostatistics and Prevention Institute, University of Zurich, Zurich, Switzerland
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SJ Dunn
6Institute of Microbiology and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom
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DAB Dance
7Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, Lao People’s Democratic Republic
8Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK
9Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK
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PN Newton
7Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, Lao People’s Democratic Republic
8Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK
9Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK
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V Davong
7Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, Lao People’s Democratic Republic
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S Mero
2Human Microbiome Research Program, Faculty of Medicine, University of Helsinki
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SH Pakkanen
2Human Microbiome Research Program, Faculty of Medicine, University of Helsinki
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A Neumayr
3Swiss Tropical and Public Health Institute, Basel, Switzerland
4University of Basel, Basel, Switzerland
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  • ORCID record for A Neumayr
C Hatz
3Swiss Tropical and Public Health Institute, Basel, Switzerland
4University of Basel, Basel, Switzerland
10Department of Infectious Diseases and Hospital Hygiene, Cantonal Hospital, St. Gallen, Switzerland
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A Snaith
6Institute of Microbiology and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom
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T Kallonen
11Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, Oslo, Norway
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J Corander
11Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, Oslo, Norway
12Wellcome Sanger Institute, Cambridge, United Kingdom
13Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland
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A McNally
6Institute of Microbiology and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom
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Abstract

Background Antimicrobial resistance (AMR) is highly prevalent in low- and middle-income countries. International travel contributes substantially to the global spread of intestinal multidrug-resistant gram-negative (MDR-GN) bacteria. Of the 100 million annual visitors to tropical countries, 30–70% become colonized by MDR-GN bacteria. The phenomenon has been well documented, but since sampling has only been conducted after travelers’ return home, data on the actual colonization process are scarce.

Methods A group of 20 European volunteers visiting Lao People’s Democratic Republic for three weeks provided daily stool samples and filled in daily questionnaires. Acquisition of extended-spectrum beta-lactamase-producing gram-negative bacteria (ESBL-GN) was examined by selective stool cultures followed by whole-genome sequencing (WGS) of isolates.

Results While colonization rates were 70% at the end of the study, daily sampling revealed that all participants had acquired ESBL-GN at some time point during their overseas stay, the status varying day by day. WGS analysis ascribed the transient pattern of colonization to sequential acquisition of new strains, resulting in a loss of detectable colonization by the initial MDR-GN strains. All but one participant acquired multiple strains (2–5). Of the total of 83 unique strains identified (53 E. coli, 10 Klebsiella, 20 other ESBL-GN species), some were shared by as many as four subjects.

Conclusions This is the first study to characterize in real time the dynamics of acquiring MDR-GN during travel. Our data show multiple transient colonization events indicative of constant microbial competition.

Summary While 14 of 20 Europeans carried multidrug-resistant bacteria at the end of their 3-week visit to Laos, whole-genome sequencing of daily stool samples revealed acquisition by all, involving multiple transient acquisitions with a potential for longer MDR-GN colonization.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 07, 2019.
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Real-time sampling of travelers shows intestinal colonization by multidrug-resistant bacteria to be a dynamic process with multiple transient acquisitions
A Kantele, E Kuenzli, SJ Dunn, DAB Dance, PN Newton, V Davong, S Mero, SH Pakkanen, A Neumayr, C Hatz, A Snaith, T Kallonen, J Corander, A McNally
bioRxiv 827915; doi: https://doi.org/10.1101/827915
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Real-time sampling of travelers shows intestinal colonization by multidrug-resistant bacteria to be a dynamic process with multiple transient acquisitions
A Kantele, E Kuenzli, SJ Dunn, DAB Dance, PN Newton, V Davong, S Mero, SH Pakkanen, A Neumayr, C Hatz, A Snaith, T Kallonen, J Corander, A McNally
bioRxiv 827915; doi: https://doi.org/10.1101/827915

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