A one-health sampling strategy to explore the dissemination and relationship between colistin resistance in human, animal, and environmental sectors in laos
This study was designed to investigate the molecular epidemiology ofmobile colistin resistance (mcr)using a “one-health” approach in Laos and to predict whether any dominant plasmid backbone and/or strain type influences the dissemination ofmcr.We collected 673 samples from humans (rectal normal flo...
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| Abstract | This study was designed to investigate the molecular epidemiology ofmobile colistin resistance (mcr)using a “one-health” approach in Laos and to predict whether any dominant plasmid backbone and/or strain type influences the dissemination ofmcr.We collected 673 samples from humans (rectal normal flora), poultry, and the environment (water, flies, birds, etc.) in Vientiane, Laos, from May to September 2018. A total of 238 Escherichia coli (E. coli)isolated from non-duplicative samples, consisting of 98MCR-positive E. coli(MCRPEC) (“mcr” denotes the gene encoding mobile colistin resistance, and “MCR” denotes the subsequent protein encoded by mcr) and 140MCR-negativeE. coli(MCRNEC), were characterized by phenotype and Illumina sequencing. A subset of MCRPEC was selected for MinION sequencing, conjugation assay, plasmid stability, andgrowth kinetics in vitro. The prevalence of MCRPEC was found to be 14.6% (98/673), with the highest prevalence in human rectal swabs (45.9% (45/98),p < 0.0001, odds ratio (OR): 0.125, 95% CI: 0.077–0.202). The percentages of MCRPEC from other samples were 14.3% (2/14) in dog feces, 12.0% (24/200) in flies, 11.0% (11/100) in chicken meat, 8.9% (8/90) in chicken cloacal, 8.0% (4/50) in chicken caeca, and 7.5% (4/53) in wastewater. MCRPEC was significantly more resistant to co-amoxiclav, sulfamethoxazole-trimethoprim, levofloxacin, ciprofloxacin, and gentamicin than MCRNEC(p < 0.05). Genomic analysis revealed the distribution of MCRPEC among diverse clonal types. The putative plasmid Inc types associated withmcr-1were IncX4, IncHI2, IncP1, IncI2, and IncFIA, and those associated withmcr-3were IncFII, IncFIA, IncFIB, IncP1, and IncR. Recovery of highly similar plasmids from both flies and other sampling sectors implied the role of flies in the dissemination ofmcr-1. mcr-positive plasmids were shown to be conjugative, and a significantly high transfer rate into a hypervirulent clone ST1193 was observed. Plasmids containingmcrirrespective of Inc type were highly stable and invariably did not exert a fitness effect upon introduction into a new host. These findings signify the urgent need for a standard infection control program to radically decontaminate the source of resistance. |
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| AbstractList | This study was designed to investigate the molecular epidemiology of mobile colistin resistance (mcr) using a “One-Health” approach in Laos and to predict whether any dominant plasmid backbone and/or strain type influences the dissemination of mcr. We collected 673 samples from humans (rectal normal flora), poultry, and the environment (water, flies, birds, etc.) in Vientiane, Lao People’s Democratic Republic (Laos), from May to September 2018. A total of 238 Escherichia coli (E. coli) isolated from non-duplicative samples, consisting of 98 MCR-positive E. coli (MCRPEC) (“mcr” denotes the gene encoding mobile colistin resistance, and “MCR” denotes the subsequent protein encoded by mcr) and 140 MCR-negative E. coli (MCRNEC), were characterized by phenotype and Illumina sequencing. A subset of MCRPEC was selected for MinION sequencing, conjugation assay, plasmid stability, and growth kinetics in vitro. The prevalence of MCRPEC was found to be 14.6% (98/673), with the highest prevalence in human rectal swabs (45.9% (45/98), p < 0.0001, odds ratio (OR): 0.125, 95% confidence interval (CI): 0.077–0.202). The percentages of MCRPEC from other samples were 14.3% (2/14) in dog feces, 12.0% (24/200) in flies, 11.0% (11/100) in chicken meat, 8.9% (8/90) in chicken cloacal, 8.0% (4/50) in chicken caeca, and 7.5% (4/53) in wastewater. MCRPEC was significantly more resistant to co-amoxiclav, sulfamethoxazole-trimethoprim, levofloxacin, ciprofloxacin, and gentamicin than MCRNEC (p < 0.05). Genomic analysis revealed the distribution of MCRPEC among diverse clonal types. The putative plasmid Inc types associated with mcr-1 were IncX4, IncHI2, IncP1, IncI2, and IncFIA, and those associated with mcr-3 were IncFII, IncFIA, IncFIB, IncP1, and IncR. Recovery of highly similar plasmids from both flies and other sampling sectors implied the role of flies in the dissemination of mcr-1. mcr-positive plasmids were shown to be conjugative, and a significantly high transfer rate into a hypervirulent clone ST1193 was observed. Plasmids containing mcr irrespective of Inc type were highly stable and invariably did not exert a fitness effect upon introduction into a new host. These findings signify the urgent need for a standard infection control program to radically decontaminate the source of resistance. This study was designed to investigate the molecular epidemiology ofmobile colistin resistance (mcr)using a “one-health” approach in Laos and to predict whether any dominant plasmid backbone and/or strain type influences the dissemination ofmcr.We collected 673 samples from humans (rectal normal flora), poultry, and the environment (water, flies, birds, etc.) in Vientiane, Laos, from May to September 2018. A total of 238 Escherichia coli (E. coli)isolated from non-duplicative samples, consisting of 98MCR-positive E. coli(MCRPEC) (“mcr” denotes the gene encoding mobile colistin resistance, and “MCR” denotes the subsequent protein encoded by mcr) and 140MCR-negativeE. coli(MCRNEC), were characterized by phenotype and Illumina sequencing. A subset of MCRPEC was selected for MinION sequencing, conjugation assay, plasmid stability, andgrowth kinetics in vitro. The prevalence of MCRPEC was found to be 14.6% (98/673), with the highest prevalence in human rectal swabs (45.9% (45/98),p < 0.0001, odds ratio (OR): 0.125, 95% CI: 0.077–0.202). The percentages of MCRPEC from other samples were 14.3% (2/14) in dog feces, 12.0% (24/200) in flies, 11.0% (11/100) in chicken meat, 8.9% (8/90) in chicken cloacal, 8.0% (4/50) in chicken caeca, and 7.5% (4/53) in wastewater. MCRPEC was significantly more resistant to co-amoxiclav, sulfamethoxazole-trimethoprim, levofloxacin, ciprofloxacin, and gentamicin than MCRNEC(p < 0.05). Genomic analysis revealed the distribution of MCRPEC among diverse clonal types. The putative plasmid Inc types associated withmcr-1were IncX4, IncHI2, IncP1, IncI2, and IncFIA, and those associated withmcr-3were IncFII, IncFIA, IncFIB, IncP1, and IncR. Recovery of highly similar plasmids from both flies and other sampling sectors implied the role of flies in the dissemination ofmcr-1. mcr-positive plasmids were shown to be conjugative, and a significantly high transfer rate into a hypervirulent clone ST1193 was observed. Plasmids containingmcrirrespective of Inc type were highly stable and invariably did not exert a fitness effect upon introduction into a new host. These findings signify the urgent need for a standard infection control program to radically decontaminate the source of resistance. This study was designed to investigate the molecular epidemiology of mobile colistin resistance(mcr)using a"One-Health"approach in Laos and to predict whether any dominant plasmid backbone and/or strain type influences the dissemination of mcr.We collected 673 samples from humans(rectal normal flora),poultry,and the environment(water,flies,birds,etc.)in Vientiane,Lao People's Democratic Republic(Laos),from May to September 2018.A total of 238 Escherichia coli(E.coli)isolated from non-duplicative samples,consisting of 98 MCR-positive E.coli(MCRPEC)("mcr"denotes the gene encoding mobile colistin resistance,and"MCR"denotes the subsequent protein encoded by mcr)and 140 MCR-negative E.coli(MCRNEC),were characterized by phenotype and Illumina sequencing.A subset of MCRPEC was selected for MinION sequencing,conjugation assay,plasmid stability,and growth kinetics in vitro.The prevalence of MCRPEC was found to be 14.6％(98/673),with the highest prevalence in human rectal swabs(45.9％(45/98),p＜0.0001,odds ratio(OR):0.125,95％confidence interval(CI):0.077-0.202).The percentages of MCRPEC from other samples were 14.3％(2/14)in dog feces,12.0％(24/200)in flies,11.0％(11/100)in chicken meat,8.9％(8/90)in chicken cloacal,8.0％(4/50)in chicken caeca,and 7.5％(4/53)in wastewater.MCRPEC was significantly more resistant to co-amoxiclav,sulfamethoxazole-trimethoprim,levofloxacin,ciprofloxacin,and gentamicin than MCRNEC(p＜0.05).Genomic analysis revealed the distribution of MCRPEC among diverse clonal types.The putative plasmid Inc types associ-ated with mcr-1 were IncX4,IncHI2,IncP1,IncI2,and IncFIA,and those associated with mcr-3 were IncFII,IncFIA,IncFIB,IncP1,and IncR.Recovery of highly similar plasmids from both flies and other sampling sectors implied the role of flies in the dissemination of mcr-1.mcr-positive plasmids were shown to be conjugative,and a significantly high transfer rate into a hypervirulent clone ST1 193 was observed.Plasmids containing mcr irrespective of Inc type were highly stable and invariably did not exert a fitness effect upon introduction into a new host.These findings signify the urgent need for a standard infection control program to radically decontaminate the source of resistance. |
| Author | Farzana, Refath Dance, David A.B. Vongsouvath, Manivanh Walsh, Timothy R. Sands, Kirsty Hassan, Brekhna Sihalath, Somsavanh Mayxay, Mayfong Rattanavong, Sayaphet Newton, Paul N. Zhou, Yuqing |
| AuthorAffiliation | Department of Zoology,University of Oxford,Oxford OX1 3SZ,UK;Ineos Oxford Institute for Antimicrobial Research(IOI),University of Oxford,Oxford OX1 3RE,UK;Department of Medical Microbiology,Institute of Infection and Immunity,School of Medicine,Cardiff University,Cardiff CF14 4XN,UK%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR;Centre for Tropical Medicine&Global Health,Nuffield Department of Medicine,University of Oxford,Oxford OX3 7BN,UK;Institute of Research and Education Development,University of Health Sciences,Vientiane PO Box 7444,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR;Centre for Tropical Medicine&Global Health,Nuffield Department of Medicine,University of Oxford,Oxford OX3 7BN,UK |
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| Author_xml | – sequence: 1 givenname: Yuqing surname: Zhou fullname: Zhou, Yuqing email: yuqing.zhou@zoo.ox.ac.uk, yuqing.zhou@st-hughs.ox.ac.uk, yuqing.zhou@zoo.ox.ac.uk organization: Department of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom – sequence: 2 givenname: Refath surname: Farzana fullname: Farzana, Refath organization: Department of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom – sequence: 3 givenname: Somsavanh surname: Sihalath fullname: Sihalath, Somsavanh organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 4 givenname: Sayaphet surname: Rattanavong fullname: Rattanavong, Sayaphet organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 5 givenname: Manivanh surname: Vongsouvath fullname: Vongsouvath, Manivanh organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 6 givenname: Mayfong surname: Mayxay fullname: Mayxay, Mayfong organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 7 givenname: Kirsty surname: Sands fullname: Sands, Kirsty organization: Department of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom – sequence: 8 givenname: Paul N. surname: Newton fullname: Newton, Paul N. organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 9 givenname: David A.B. surname: Dance fullname: Dance, David A.B. organization: Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Microbiology Laboratory, Mahosot Hospital, Vientiane, PO Box 292, Lao People’s Democratic Republic – sequence: 10 givenname: Brekhna surname: Hassan fullname: Hassan, Brekhna organization: Department of Medical Microbiology, Institute of Infection and Immunity, School of Medicine, Cardiff University, Cardiff CF14 4XN, United Kingdom – sequence: 11 givenname: Timothy R. surname: Walsh fullname: Walsh, Timothy R. organization: Department of Zoology, University of Oxford, Oxford OX1 3SZ, United Kingdom |
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| Keywords | Horizontal transmission Colistin resistance Mcr Laos Escherichia coli Colistin resistance mcr |
| Language | English |
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| Publisher | Elsevier Ltd Faculty of Infectious and Tropical Diseases,London School of Hygiene and Tropical Medicine,London WC1E 7HT,UK%Department of Medical Microbiology,Institute of Infection and Immunity,School of Medicine,Cardiff University,Cardiff CF14 4XN,UK%Department of Zoology,University of Oxford,Oxford OX1 3SZ,UK Centre for Tropical Medicine&Global Health,Nuffield Department of Medicine,University of Oxford,Oxford OX3 7BN,UK Institute of Research and Education Development,University of Health Sciences,Vientiane PO Box 7444,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR Department of Zoology,University of Oxford,Oxford OX1 3SZ,UK Ineos Oxford Institute for Antimicrobial Research(IOI),University of Oxford,Oxford OX1 3RE,UK Department of Medical Microbiology,Institute of Infection and Immunity,School of Medicine,Cardiff University,Cardiff CF14 4XN,UK%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR Elsevier |
| Publisher_xml | – name: Elsevier Ltd – name: Institute of Research and Education Development,University of Health Sciences,Vientiane PO Box 7444,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR – name: Department of Medical Microbiology,Institute of Infection and Immunity,School of Medicine,Cardiff University,Cardiff CF14 4XN,UK%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR%Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit,Microbiology Laboratory,Mahosot Hospital,Vientiane PO Box 292,Lao PDR – name: Department of Zoology,University of Oxford,Oxford OX1 3SZ,UK – name: Ineos Oxford Institute for Antimicrobial Research(IOI),University of Oxford,Oxford OX1 3RE,UK – name: Centre for Tropical Medicine&Global Health,Nuffield Department of Medicine,University of Oxford,Oxford OX3 7BN,UK – name: Faculty of Infectious and Tropical Diseases,London School of Hygiene and Tropical Medicine,London WC1E 7HT,UK%Department of Medical Microbiology,Institute of Infection and Immunity,School of Medicine,Cardiff University,Cardiff CF14 4XN,UK%Department of Zoology,University of Oxford,Oxford OX1 3SZ,UK – name: Elsevier |
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| SubjectTerms | Colistin resistance Escherichia coli Horizontal transmission Laos Mcr |
| Title | A one-health sampling strategy to explore the dissemination and relationship between colistin resistance in human, animal, and environmental sectors in laos |
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