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The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents
Umeå University, Faculty of Medicine, Department of Clinical Microbiology, Infectious Diseases.
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2015 (English)In: Antimicrobial Agents and Chemotherapy, ISSN 0066-4804, E-ISSN 1098-6596, Vol. 59, no 10, 6551-6560 p.Article in journal (Refereed) Published
Abstract [en]

Previous studies of antibiotic resistance dissemination by travel have, by targeting only a select number of cultivable bacterial species, omitted most of the human microbiome. Here, we used explorative shotgun metagenomic sequencing to address the abundance of >300 antibiotic resistance genes in fecal specimens from 35 Swedish students taken before and after exchange programs on the Indian peninsula or in Central Africa. All specimens were additionally cultured for extended-spectrum beta-lactamase (ESBL)-producing enterobacteria, and the isolates obtained were genome sequenced. The overall taxonomic diversity and composition of the gut microbiome remained stable before and after travel, but there was an increasing abundance of Proteobacteria in 25/35 students. The relative abundance of antibiotic resistance genes increased, most prominently for genes encoding resistance to sulfonamide (2.6-fold increase), trimethoprim (7.7-fold), and beta-lactams (2.6-fold). Importantly, the increase observed occurred without any antibiotic intake. Of 18 students visiting the Indian peninsula, 12 acquired ESBL-producing Escherichia coli, while none returning from Africa were positive. Despite deep sequencing efforts, the sensitivity of metagenomics was not sufficient to detect acquisition of the low-abundant genes responsible for the observed ESBL phenotype. In conclusion, metagenomic sequencing of the intestinal microbiome of Swedish students returning from exchange programs in Central Africa or the Indian peninsula showed increased abundance of genes encoding resistance to widely used antibiotics.

Place, publisher, year, edition, pages
2015. Vol. 59, no 10, 6551-6560 p.
National Category
Microbiology in the medical area Pharmacology and Toxicology
Identifiers
URN: urn:nbn:se:umu:diva-110685DOI: 10.1128/AAC.00933-15ISI: 000367591800082PubMedID: 26259788OAI: oai:DiVA.org:umu-110685DiVA: diva2:864203
Available from: 2015-10-26 Created: 2015-10-26 Last updated: 2016-02-10Bibliographically approved
In thesis
1. Travel – a risk factor for disease and spread of antibiotic resistance
Open this publication in new window or tab >>Travel – a risk factor for disease and spread of antibiotic resistance
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

As international travel is rapidly increasing, more people are being exposed to potentially more antibiotic resistant bacteria, a changed infectious disease epidemiology, and an increased risk of accidents and crime. Research-based advice is needed to adequately inform travellers about these risks. We studied travellers who sought advice from the Travel Medicine Clinic at the Department of Infectious Diseases, Umeå University Hospital, as well as university students from Umeå, Stockholm, and Gothenburg travelling abroad for study, research, and clinical exchange programs.

From retrospective data at the Travel Medicine Clinic, we found that pre-existing health problems were rare among travellers from Umeå seeking pre- travel health advice and vaccinations. In addition, we found that the travel destination and the sex of the traveller affected vaccination levels. Although hepatitis A is endemic to both Thailand and Turkey, compared to travellers to Thailand few travellers to Turkey visited the clinic for hepatitis A vaccination. The data also revealed that more women than men were vaccinated against Japanese encephalitis despite comparable trips.

A prospective survey study showed that travellers felt that the pre-travel health advice they received was helpful. Two-thirds of the travellers followed the advice given although they still fell ill to the same extent as those who were not compliant with the advice. Factors outside the control of travellers likely affect the travel-related morbidity. Compared to older travellers, younger travellers were less compliant with advice, fell ill to a greater extent, and took greater risks during travel.

In a prospective survey study, we found that healthcare students had higher illness rates and risk exposure when abroad compared to students from other disciplines. This difference was mainly due to the fact that healthcare students more often travelled to developing regions during their study period abroad. When abroad, half of all students increased their alcohol consumption and this was linked to an increased risk of theft and higher likelihood of meeting a new sex partner.

The healthcare students participating in the survey study also submitted stool samples before and after travel. These samples were tested for the presence of antibiotic resistance, both by selective culturing for ESBL-PE (Extended-Spectrum Beta-Lactamase Producing Enterobacteriaceae) as well as by metagenomic sequencing. About one-third (35%) of the students became colonised by ESBL-PE following their study abroad. The strongest risk factor for colonisation was travel destination; for example, 70% of students who had travelled to India became colonised. Antibiotic treatment during travel was also a significant risk factor for colonisation.

The stool samples from a subset of study subjects were analysed using metagenomic sequencing. From this we learned that although the majority of resistance genes in the gut microbiome remained unchanged following travel, several clinically important resistance genes increased, most prominently genes encoding resistance to sulphonamide, trimethoprim, and beta-lactams. Overall, taxonomic changes associated with travel were small but the proportion of Proteobacteria, which includes several clinically important bacteria (e.g., Enterobacteriaceae), increased in a majority of the study subjects.

Clearly, there are risks associated with international travel and these risks include outside factors as well as the personal behaviour of travellers. We believe our results can be used to develop better pre-travel advice for tourists as well as university students studying abroad resulting in safer travel.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2015. 66 p.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 1754
Keyword
Accident Prevention; Alcohol Drinking; Anti-Bacterial Agents; Antimalarials; Beta-Lactamases; Drug-Resistance, Bacterial; Enterobacteriaceae; Health Knowledge, Attitudes, Practice; High-Throughput Nucleotide Sequencing; Medication Adherence; Metagenome; Metagenomics; Patient Compliance; Proteobacteria; Risk Reduction Behaviour; Risk-Taking; Safe Sex; Travel medicine; Travel; Vaccination
National Category
Infectious Medicine Microbiology in the medical area
Research subject
Infectious Diseases; Microbiology
Identifiers
urn:nbn:se:umu:diva-111057 (URN)978-91-7601-348-9 (ISBN)
Public defence
2015-11-27, Sal A5, byggnad 6A, Norrlands universitetssjukhus, Umeå, 09:00 (English)
Opponent
Supervisors
Funder
The Kempe Foundations
Available from: 2015-11-06 Created: 2015-11-02 Last updated: 2015-12-11Bibliographically approved

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Angelin, MartinPalmgren, HelenaJohansson, Anders
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