High Rates of Antimicrobial Drug Resistance Gene Acquisition after International Travel, the Netherlands

Wintersdorff, Christian J. H. von; Penders, John; Stobberingh, Ellen E.; Lashof, Astrid M. L. Oude; Hoebe, Christian J. P. A.; Savelkoul, Paul H. M.; Wolffs, Petra

doi:10.3201/eid2004.131718

Cited by 117 publications

(73 citation statements)

References 35 publications

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“…Significant changes in average abundances between before and after specimens were assessed using paired Student's t tests on log 10 -transformed values. The Wilcoxon signed-rank test was used as a complement to find genes with changed median abundance.…”

Section: Methodsmentioning

confidence: 99%

“…The studies have largely been focused on a select subset of Enterobacteriaceae species (18)(19)(20)(21) or a small number of genes or antibiotics (10,15,22). Although many species of the Enterobacteriaceae are important human pathogens, it has repeatedly been shown that these bacteria usually constitute less than 1% of the human gut microbiota (23,24).…”

mentioning

confidence: 99%

“…In recent years, acquisition of Enterobacteriaceae strains resistant to cephalosporin antibiotics by production of extendedspectrum beta-lactamases (ESBLs) have been quantified in travelers from the Netherlands (9, 10), France (11), Australia (12), Sweden (13)(14)(15), Germany (16), and Finland (17). Certain risk factors, such as intake of antibiotics and a travel destination on the Indian peninsula, appear to increase the risk of acquisition (9,10,(12)(13)(14)(15)17). Consequently, there is general concern over the contribution of travel to the global dispersal of antibiotic-resistant bacteria.…”

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confidence: 99%

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The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents

Bengtsson‐Palme

Angelin

Huss

et al. 2015

Antimicrob Agents Chemother

167

109

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e 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.

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Section: Methodsmentioning

confidence: 99%

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confidence: 99%

mentioning

confidence: 99%

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The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents

Bengtsson‐Palme

Angelin

Huss

et al. 2015

Antimicrob Agents Chemother

167

109

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“…Similarly, rates of ESBL E. coli and K. pneumoniae isolates in Saudi Arabia between 2009 and 2010 were high at approximately 30% (19). A previous report showed a high acquisition rate of the CTX-M gene in Netherlands travelers, rising from 9% to 33.6% after travel (8). A total of 17 CTX-M variants were found in the rectal samples of 48 pilgrims (Fig.…”

mentioning

confidence: 94%

“…Pilgrims can be carriers of infectious diseases when returning home. Several reports have shown the dissemination of resistant genes and multidrug-resistant bacteria (MDR) in travelers (5,6), including extended-spectrum-␤-lactamase (ESBL)-producing bacteria in travelers from the Netherlands (7,8), Spain (9), and Japan (10). However, studies of the acquisition of antibiotic resistance (AR) genes in pilgrims during the Hajj are few.…”

mentioning

confidence: 99%

Acquisition of Extended-Spectrum β-Lactamases by Escherichia coli and Klebsiella pneumoniae in Gut Microbiota of Pilgrims during the Hajj Pilgrimage of 2013

Leangapichart

Dia

Olaitan

et al. 2016

Antimicrob Agents Chemother

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We reported the acquisition of extended-spectrum-␤-lactamase (ESBL)-producing bacteria in rectal samples of 129 pilgrims during the 2013 Hajj (pilgrimage to Makkah). When returning from the Hajj, there was a significant increase in the number of pilgrims carrying E. coli resistant to ceftriaxone (P ‫؍‬ 0.008). The CTX-M gene was detected in rectal samples, with the detection rate increasing from 10.08% to 32.56% of samples after the Hajj (P < 0.001). The Hajj (pilgrimage to Makkah) is well recognized as a source for transmission of infectious diseases (1-4). Pilgrims can be carriers of infectious diseases when returning home. Several reports have shown the dissemination of resistant genes and multidrug-resistant bacteria (MDR) in travelers (5, 6), including extended-spectrum-␤-lactamase (ESBL)-producing bacteria in travelers from the Netherlands (7, 8), Spain (9), and Japan (10). However, studies of the acquisition of antibiotic resistance (AR) genes in pilgrims during the Hajj are few. We aim to investigate the change and acquisition of MDR bacteria in pilgrims returning from the 2013 Hajj with specific focus on Escherichia coli and Klebsiella pneumoniae.Rectal swabs were collected from a cohort of 129 pilgrims traveling to Saudi Arabia with the same travel agency. Samples were collected 10 days before travel (22 September 2013) and 1 day before returning (23 October 2013) as described by Gautret et al. (11). One hundred microliters from each swab was inoculated into Trypticase soy broth (Becton, Dickinson and Company, Sparks, MD, USA). After 24 h of incubation, samples were plated onto Hektoen enteric agar (Oxoid Deutschland GmbH, Wesel, Germany). MacConkey agar with 2 mg/liter cefotaxime and Cepacia agar (bioMérieux, Marcy-l'Étoile, France) were used to isolate ESBL-producing bacteria and colistin-resistant bacteria. Species were identified by matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry (Microflex; Bruker Daltonic, Bremen, Germany). E. coli and K. pneumoniae isolates were tested against six antibiotics (colistin, ticarcillin-clavulanic acid, piperacillin-tazobactam, ceftriaxone, gentamicin, and imipenem) by the disk diffusion method for an overview of antibiotic-resistant bacteria in pilgrims and were interpreted using EUCAST guidelines (http://www.eucast.org).Total DNA was extracted from E. coli, K. pneumoniae, and rectal samples using an EZ1 BioRobot machine (Qiagen S.A., Courtaboeuf, France) according to the manufacturer's instructions. ESBL-encoding genes (CTX-M, TEM, and SHV) were detected by PCR and sequencing and were then analyzed with the ARG-ANNOT (12) and NCBI databases. Primers used in this study have previously been described elsewhere (13)(14)(15)(16)(17). Multilocus sequence typing (MLST) was performed as described in the database (http://mlst.warwick.ac.uk/mlst/dbs/Ecoli/, http://bigsdb .web.pasteur.fr/klebsiella/). A phylogenetic tree was constructed

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Strategies to Reduce or Eliminate Resistant Pathogens in the Environment

Bengtsson‐Palme

Heß

2019

Antibiotic Drug Resistance

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High Rates of Antimicrobial Drug Resistance Gene Acquisition after International Travel, the Netherlands

Cited by 117 publications

References 35 publications

The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents

The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents

Acquisition of Extended-Spectrum β-Lactamases by Escherichia coli and Klebsiella pneumoniae in Gut Microbiota of Pilgrims during the Hajj Pilgrimage of 2013

Strategies to Reduce or Eliminate Resistant Pathogens in the Environment

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