Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia
ABSTRACT Over 80% of travelers from the United Kingdom to the Indian subcontinent acquire CTX-M-producing Escherichia coli (CTX-M-EC), but the mechanism of CTX-M-EC acquisition is poorly understood. We aimed to investigate the dynamics of CTX-M-EC acquisition in healthy travelers and how this relate...
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American Society for Microbiology
2018
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oai:doaj.org-article:daea5e0535754922a4e102a36d4254a12021-11-15T15:52:19ZAcquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia10.1128/mBio.02408-182150-7511https://doaj.org/article/daea5e0535754922a4e102a36d4254a12018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02408-18https://doaj.org/toc/2150-7511ABSTRACT Over 80% of travelers from the United Kingdom to the Indian subcontinent acquire CTX-M-producing Escherichia coli (CTX-M-EC), but the mechanism of CTX-M-EC acquisition is poorly understood. We aimed to investigate the dynamics of CTX-M-EC acquisition in healthy travelers and how this relates to populations of non-CTX-M-EC in the fecal microbiome. This is a prospective observational study of healthy volunteers traveling from the United Kingdom to South Asia. Fecal samples were collected pre- and post-travel at several time points up to 12 months post-travel. A toothpicking experiment was used to determine the proportion of cephalosporin-sensitive E. coli in fecal samples containing CTX-M-EC. MLST and SNP type of pre-travel and post-travel E. coli were deduced by WGS. CTX-M-EC was acquired by 89% (16/18) of volunteers. Polyclonal acquisition of CTX-M-EC was seen in 8/15 volunteers (all had >3 STs across post-travel samples), suggesting multiple acquisition events. Indistinguishable CTX-M-EC clones (zero SNPs apart) are detectable in serial fecal samples up to 7 months after travel, indicating stable maintenance in the fecal microbiome on return to the United Kingdom in the absence of selective pressure. CTX-M-EC-containing samples were often co-colonized with novel, non-CTX-M strains after travel, indicating that acquisition of non-CTX-M-EC occurs alongside CTX-M-EC. The same pre-travel non-CTX-M strains (<10 SNPs apart) were found in post-travel fecal samples after CTX-M-EC had been lost, suggesting return of the fecal microbiome to the pre-travel state and long-term persistence of minority strains in travelers who acquire CTX-M-EC. IMPORTANCE Escherichia coli strains which produce CTX-M extended-spectrum beta-lactamases are endemic as colonizers of humans and in the environment in South Asia. This study demonstrates that acquisition of CTX-M-producing E. coli (CTX-M-EC) in travelers from the United Kingdom to South Asia is polyclonal, which is likely due to multiple acquisition events from contaminated food and drinking water during travel. CTX-M-EC frequently persists in the fecal microbiome for at least 1 year after acquisition, often alongside newly acquired non-CTX-M E. coli strains. In travelers who acquire CTX-M-EC, pre-travel non-CTX-M E. coli remains as a minority population in the gut until the CTX-M-EC strains are lost. The non-CTX-M strains are then reestablished as the predominant E. coli population. This study has shed light on the dynamics of CTX-M-EC acquisition, colonization, and loss after travel. Future work involving manipulation of nonvirulent resident E. coli could be used to prevent colonization with antibiotic-resistant E. coli.Edward R. BevanAlan McNallyChristopher M. ThomasLaura J. V. PiddockPeter M. HawkeyAmerican Society for MicrobiologyarticleEscherichia colicolonizationmicrobiometravelMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Escherichia coli colonization microbiome travel Microbiology QR1-502 |
| spellingShingle |
Escherichia coli colonization microbiome travel Microbiology QR1-502 Edward R. Bevan Alan McNally Christopher M. Thomas Laura J. V. Piddock Peter M. Hawkey Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| description |
ABSTRACT Over 80% of travelers from the United Kingdom to the Indian subcontinent acquire CTX-M-producing Escherichia coli (CTX-M-EC), but the mechanism of CTX-M-EC acquisition is poorly understood. We aimed to investigate the dynamics of CTX-M-EC acquisition in healthy travelers and how this relates to populations of non-CTX-M-EC in the fecal microbiome. This is a prospective observational study of healthy volunteers traveling from the United Kingdom to South Asia. Fecal samples were collected pre- and post-travel at several time points up to 12 months post-travel. A toothpicking experiment was used to determine the proportion of cephalosporin-sensitive E. coli in fecal samples containing CTX-M-EC. MLST and SNP type of pre-travel and post-travel E. coli were deduced by WGS. CTX-M-EC was acquired by 89% (16/18) of volunteers. Polyclonal acquisition of CTX-M-EC was seen in 8/15 volunteers (all had >3 STs across post-travel samples), suggesting multiple acquisition events. Indistinguishable CTX-M-EC clones (zero SNPs apart) are detectable in serial fecal samples up to 7 months after travel, indicating stable maintenance in the fecal microbiome on return to the United Kingdom in the absence of selective pressure. CTX-M-EC-containing samples were often co-colonized with novel, non-CTX-M strains after travel, indicating that acquisition of non-CTX-M-EC occurs alongside CTX-M-EC. The same pre-travel non-CTX-M strains (<10 SNPs apart) were found in post-travel fecal samples after CTX-M-EC had been lost, suggesting return of the fecal microbiome to the pre-travel state and long-term persistence of minority strains in travelers who acquire CTX-M-EC. IMPORTANCE Escherichia coli strains which produce CTX-M extended-spectrum beta-lactamases are endemic as colonizers of humans and in the environment in South Asia. This study demonstrates that acquisition of CTX-M-producing E. coli (CTX-M-EC) in travelers from the United Kingdom to South Asia is polyclonal, which is likely due to multiple acquisition events from contaminated food and drinking water during travel. CTX-M-EC frequently persists in the fecal microbiome for at least 1 year after acquisition, often alongside newly acquired non-CTX-M E. coli strains. In travelers who acquire CTX-M-EC, pre-travel non-CTX-M E. coli remains as a minority population in the gut until the CTX-M-EC strains are lost. The non-CTX-M strains are then reestablished as the predominant E. coli population. This study has shed light on the dynamics of CTX-M-EC acquisition, colonization, and loss after travel. Future work involving manipulation of nonvirulent resident E. coli could be used to prevent colonization with antibiotic-resistant E. coli. |
| format |
article |
| author |
Edward R. Bevan Alan McNally Christopher M. Thomas Laura J. V. Piddock Peter M. Hawkey |
| author_facet |
Edward R. Bevan Alan McNally Christopher M. Thomas Laura J. V. Piddock Peter M. Hawkey |
| author_sort |
Edward R. Bevan |
| title |
Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| title_short |
Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| title_full |
Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| title_fullStr |
Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| title_full_unstemmed |
Acquisition and Loss of CTX-M-Producing and Non-Producing <named-content content-type="genus-species">Escherichia coli</named-content> in the Fecal Microbiome of Travelers to South Asia |
| title_sort |
acquisition and loss of ctx-m-producing and non-producing <named-content content-type="genus-species">escherichia coli</named-content> in the fecal microbiome of travelers to south asia |
| publisher |
American Society for Microbiology |
| publishDate |
2018 |
| url |
https://doaj.org/article/daea5e0535754922a4e102a36d4254a1 |
| work_keys_str_mv |
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