The role of animals as a source of antimicrobial resistant nontyphoidal Salmonella causing invasive and non-invasive human disease in Vietnam
Nontyphoidal Salmonella (NTS) are associated with both diarrhea and bacteremia. Antimicrobial resistance (AMR) is common in NTS in low-middle income countries, but the major source(s) of AMR NTS in humans are not known. Here, we aimed to assess the role of animals as a source of AMR in human NTS inf...
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| creator | Parisi, Andrea Phuong, Tu Le Thi Mather, Alison E. Jombart, Thibaut Tuyen, Ha Thanh Lan, Nguyen Phu Huong Trang, Nguyen Hoang Thu Carrique-Mas, Juan Campbell, James I. Trung, Nguyen Vinh Glass, Kathryn Kirk, Martyn D. Baker, Stephen |
| description | Nontyphoidal Salmonella (NTS) are associated with both diarrhea and bacteremia. Antimicrobial resistance (AMR) is common in NTS in low-middle income countries, but the major source(s) of AMR NTS in humans are not known. Here, we aimed to assess the role of animals as a source of AMR in human NTS infections in Vietnam. We retrospectively combined and analyzed 672 NTS human and animal isolates from four studies in southern Vietnam and compared serovars, sequence types (ST), and AMR profiles. We generated a population structure of circulating organisms and aimed to attribute sources of AMR in NTS causing invasive and noninvasive disease in humans using Bayesian multinomial mixture models.
Among 672 NTS isolates, 148 (22%) originated from human blood, 211 (31%) from human stool, and 313 (47%) from animal stool. The distribution of serovars, STs, and AMR profiles differed among sources; serovars Enteritidis, Typhimurium, and Weltevreden were the most common in human blood, human stool, and animals, respectively. We identified an association between the source of NTS and AMR profile; the majority of AMR isolates were isolated from human blood (p |
| doi_str_mv | 10.1016/j.meegid.2020.104534 |
| format | Article |
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Among 672 NTS isolates, 148 (22%) originated from human blood, 211 (31%) from human stool, and 313 (47%) from animal stool. The distribution of serovars, STs, and AMR profiles differed among sources; serovars Enteritidis, Typhimurium, and Weltevreden were the most common in human blood, human stool, and animals, respectively. We identified an association between the source of NTS and AMR profile; the majority of AMR isolates were isolated from human blood (p < 0.001). Modelling by ST-AMR profile found chickens and pigs were likely the major sources of AMR NTS in human blood and stool, respectively; but unsampled sources were found to be a major contributor.
Antimicrobial use in food animals is hypothesized to play role in the emergence of AMR in human pathogens. Our cross-sectional population-based approach suggests a significant overlap between AMR in NTS in animals and humans, but animal NTS does explain the full extent of AMR in human NTS infections in Vietnam.
•The major source(s) of antimicrobial resistance (AMR) in nontyphoidal Salmonella (NTS) are unknown.•We analyzed 672 NTS isolates, 148 (41%) from human blood, 211 (59%) from human stool, and 136 (43%) from animal stool.•Enteritidis, Typhimurium, and Weltevreden were the common serovars in human blood, human stool, and animals, respectively.•The majority of AMR isolates were associated with human blood.•NTS from animals does explain the full extent of AMR in human NTS infections.</description><identifier>ISSN: 1567-1348</identifier><identifier>EISSN: 1567-7257</identifier><identifier>DOI: 10.1016/j.meegid.2020.104534</identifier><identifier>PMID: 32920195</identifier><language>eng</language><publisher>AMSTERDAM: Elsevier B.V</publisher><subject>Animals ; Anti-Bacterial Agents - therapeutic use ; Antimicrobial resistance ; Bacteremia ; Bacterial Zoonoses - epidemiology ; Chickens - virology ; Cross-Sectional Studies ; Diarrhea ; Disease Transmission, Infectious - veterinary ; Disease Vectors ; Drug Resistance, Bacterial - drug effects ; Ducks - virology ; Genetic Variation ; Infectious Diseases ; Life Sciences & Biomedicine ; Microbial Sensitivity Tests ; Nontyphoidal Salmonella ; Retrospective Studies ; Rodentia - virology ; Salmonella Infections - drug therapy ; Salmonella Infections - epidemiology ; Salmonella Infections - transmission ; Salmonella typhimurium - drug effects ; Science & Technology ; Serogroup ; Swine - virology ; Vietnam - epidemiology ; Zoonosis</subject><ispartof>Infection, genetics and evolution, 2020-11, Vol.85, p.104534-104534, Article 104534</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier B.V. All rights reserved.</rights><rights>2020 The Author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>8</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000593913700001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c463t-e74754382bb576a4d8398ed41b6ec6310e5ab0adbe33999a9a03723d0f6907613</citedby><cites>FETCH-LOGICAL-c463t-e74754382bb576a4d8398ed41b6ec6310e5ab0adbe33999a9a03723d0f6907613</cites><orcidid>0000-0003-1308-5755 ; 0000-0001-9161-8890 ; 0000-0001-5905-1310</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.meegid.2020.104534$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,315,782,786,887,3552,27931,27932,28255,46002</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32920195$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Parisi, Andrea</creatorcontrib><creatorcontrib>Phuong, Tu Le Thi</creatorcontrib><creatorcontrib>Mather, Alison E.</creatorcontrib><creatorcontrib>Jombart, Thibaut</creatorcontrib><creatorcontrib>Tuyen, Ha Thanh</creatorcontrib><creatorcontrib>Lan, Nguyen Phu Huong</creatorcontrib><creatorcontrib>Trang, Nguyen Hoang Thu</creatorcontrib><creatorcontrib>Carrique-Mas, Juan</creatorcontrib><creatorcontrib>Campbell, James I.</creatorcontrib><creatorcontrib>Trung, Nguyen Vinh</creatorcontrib><creatorcontrib>Glass, Kathryn</creatorcontrib><creatorcontrib>Kirk, Martyn D.</creatorcontrib><creatorcontrib>Baker, Stephen</creatorcontrib><title>The role of animals as a source of antimicrobial resistant nontyphoidal Salmonella causing invasive and non-invasive human disease in Vietnam</title><title>Infection, genetics and evolution</title><addtitle>INFECT GENET EVOL</addtitle><addtitle>Infect Genet Evol</addtitle><description>Nontyphoidal Salmonella (NTS) are associated with both diarrhea and bacteremia. Antimicrobial resistance (AMR) is common in NTS in low-middle income countries, but the major source(s) of AMR NTS in humans are not known. Here, we aimed to assess the role of animals as a source of AMR in human NTS infections in Vietnam. We retrospectively combined and analyzed 672 NTS human and animal isolates from four studies in southern Vietnam and compared serovars, sequence types (ST), and AMR profiles. We generated a population structure of circulating organisms and aimed to attribute sources of AMR in NTS causing invasive and noninvasive disease in humans using Bayesian multinomial mixture models.
Among 672 NTS isolates, 148 (22%) originated from human blood, 211 (31%) from human stool, and 313 (47%) from animal stool. The distribution of serovars, STs, and AMR profiles differed among sources; serovars Enteritidis, Typhimurium, and Weltevreden were the most common in human blood, human stool, and animals, respectively. We identified an association between the source of NTS and AMR profile; the majority of AMR isolates were isolated from human blood (p < 0.001). Modelling by ST-AMR profile found chickens and pigs were likely the major sources of AMR NTS in human blood and stool, respectively; but unsampled sources were found to be a major contributor.
Antimicrobial use in food animals is hypothesized to play role in the emergence of AMR in human pathogens. Our cross-sectional population-based approach suggests a significant overlap between AMR in NTS in animals and humans, but animal NTS does explain the full extent of AMR in human NTS infections in Vietnam.
•The major source(s) of antimicrobial resistance (AMR) in nontyphoidal Salmonella (NTS) are unknown.•We analyzed 672 NTS isolates, 148 (41%) from human blood, 211 (59%) from human stool, and 136 (43%) from animal stool.•Enteritidis, Typhimurium, and Weltevreden were the common serovars in human blood, human stool, and animals, respectively.•The majority of AMR isolates were associated with human blood.•NTS from animals does explain the full extent of AMR in human NTS infections.</description><subject>Animals</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Antimicrobial resistance</subject><subject>Bacteremia</subject><subject>Bacterial Zoonoses - epidemiology</subject><subject>Chickens - virology</subject><subject>Cross-Sectional Studies</subject><subject>Diarrhea</subject><subject>Disease Transmission, Infectious - veterinary</subject><subject>Disease Vectors</subject><subject>Drug Resistance, Bacterial - drug effects</subject><subject>Ducks - virology</subject><subject>Genetic Variation</subject><subject>Infectious Diseases</subject><subject>Life Sciences & Biomedicine</subject><subject>Microbial Sensitivity Tests</subject><subject>Nontyphoidal Salmonella</subject><subject>Retrospective Studies</subject><subject>Rodentia - virology</subject><subject>Salmonella Infections - drug therapy</subject><subject>Salmonella Infections - epidemiology</subject><subject>Salmonella Infections - transmission</subject><subject>Salmonella typhimurium - drug effects</subject><subject>Science & Technology</subject><subject>Serogroup</subject><subject>Swine - virology</subject><subject>Vietnam - epidemiology</subject><subject>Zoonosis</subject><issn>1567-1348</issn><issn>1567-7257</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><recordid>eNqNUV2L1DAULaK4H_oPRPIoyIz5bJoXQQZdhQUfXH0NaXM7k6FNxiSdZX-E_9mUqaO-iBDI5eTck3vuqaoXBK8JJvWb_XoE2Dq7ppjOEBeMP6ouiajlSlIhHy81Yby5qK5S2mNMJKbN0-qCUUUxUeKy-nG3AxTDACj0yHg3miEhUw5KYYrdAmc3ui6G1pkBRUgu5YIhH3x-OOyCswX-YoYxeBgGgzozJee3yPmjSe4IRcDO5NUZ2E2j8ci6BCZB4aFvDrI347PqSV8GgOfLfV19_fD-bvNxdfv55tPm3e2q4zXLK5BcCs4a2rZC1obbhqkGLCdtDV3NCAZhWmxsC4wppYwymEnKLO5rhWVN2HX19qR7mNoRbAc-RzPoQyz-44MOxum_X7zb6W04aimxoAQXgVeLQAzfJ0hZjy51s3sPYUqack6FanAjCpWfqGWBKUXoz98QrOck9V6fktRzkvqUZGl7-eeI56Zf0RXC6xPhHtrQp86B7-BMwxgLxRRhslR4dtz8P3vjssku-E2YfP69LCiJHB1EvbRbF6HL2gb3bys_Aes01So</recordid><startdate>202011</startdate><enddate>202011</enddate><creator>Parisi, Andrea</creator><creator>Phuong, Tu Le Thi</creator><creator>Mather, Alison E.</creator><creator>Jombart, Thibaut</creator><creator>Tuyen, Ha Thanh</creator><creator>Lan, Nguyen Phu Huong</creator><creator>Trang, Nguyen Hoang Thu</creator><creator>Carrique-Mas, Juan</creator><creator>Campbell, James I.</creator><creator>Trung, Nguyen Vinh</creator><creator>Glass, Kathryn</creator><creator>Kirk, Martyn D.</creator><creator>Baker, Stephen</creator><general>Elsevier B.V</general><general>Elsevier</general><general>Elsevier Science</general><scope>6I.</scope><scope>AAFTH</scope><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1308-5755</orcidid><orcidid>https://orcid.org/0000-0001-9161-8890</orcidid><orcidid>https://orcid.org/0000-0001-5905-1310</orcidid></search><sort><creationdate>202011</creationdate><title>The role of animals as a source of antimicrobial resistant nontyphoidal Salmonella causing invasive and non-invasive human disease in Vietnam</title><author>Parisi, Andrea ; Phuong, Tu Le Thi ; Mather, Alison E. ; Jombart, Thibaut ; Tuyen, Ha Thanh ; Lan, Nguyen Phu Huong ; Trang, Nguyen Hoang Thu ; Carrique-Mas, Juan ; Campbell, James I. ; Trung, Nguyen Vinh ; Glass, Kathryn ; Kirk, Martyn D. ; Baker, Stephen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-e74754382bb576a4d8398ed41b6ec6310e5ab0adbe33999a9a03723d0f6907613</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Anti-Bacterial Agents - therapeutic use</topic><topic>Antimicrobial resistance</topic><topic>Bacteremia</topic><topic>Bacterial Zoonoses - epidemiology</topic><topic>Chickens - virology</topic><topic>Cross-Sectional Studies</topic><topic>Diarrhea</topic><topic>Disease Transmission, Infectious - veterinary</topic><topic>Disease Vectors</topic><topic>Drug Resistance, Bacterial - drug effects</topic><topic>Ducks - virology</topic><topic>Genetic Variation</topic><topic>Infectious Diseases</topic><topic>Life Sciences & Biomedicine</topic><topic>Microbial Sensitivity Tests</topic><topic>Nontyphoidal Salmonella</topic><topic>Retrospective Studies</topic><topic>Rodentia - virology</topic><topic>Salmonella Infections - drug therapy</topic><topic>Salmonella Infections - epidemiology</topic><topic>Salmonella Infections - transmission</topic><topic>Salmonella typhimurium - drug effects</topic><topic>Science & Technology</topic><topic>Serogroup</topic><topic>Swine - virology</topic><topic>Vietnam - epidemiology</topic><topic>Zoonosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Parisi, Andrea</creatorcontrib><creatorcontrib>Phuong, Tu Le Thi</creatorcontrib><creatorcontrib>Mather, Alison E.</creatorcontrib><creatorcontrib>Jombart, Thibaut</creatorcontrib><creatorcontrib>Tuyen, Ha Thanh</creatorcontrib><creatorcontrib>Lan, Nguyen Phu Huong</creatorcontrib><creatorcontrib>Trang, Nguyen Hoang Thu</creatorcontrib><creatorcontrib>Carrique-Mas, Juan</creatorcontrib><creatorcontrib>Campbell, James I.</creatorcontrib><creatorcontrib>Trung, Nguyen Vinh</creatorcontrib><creatorcontrib>Glass, Kathryn</creatorcontrib><creatorcontrib>Kirk, Martyn D.</creatorcontrib><creatorcontrib>Baker, Stephen</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Infection, genetics and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Parisi, Andrea</au><au>Phuong, Tu Le Thi</au><au>Mather, Alison E.</au><au>Jombart, Thibaut</au><au>Tuyen, Ha Thanh</au><au>Lan, Nguyen Phu Huong</au><au>Trang, Nguyen Hoang Thu</au><au>Carrique-Mas, Juan</au><au>Campbell, James I.</au><au>Trung, Nguyen Vinh</au><au>Glass, Kathryn</au><au>Kirk, Martyn D.</au><au>Baker, Stephen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The role of animals as a source of antimicrobial resistant nontyphoidal Salmonella causing invasive and non-invasive human disease in Vietnam</atitle><jtitle>Infection, genetics and evolution</jtitle><stitle>INFECT GENET EVOL</stitle><addtitle>Infect Genet Evol</addtitle><date>2020-11</date><risdate>2020</risdate><volume>85</volume><spage>104534</spage><epage>104534</epage><pages>104534-104534</pages><artnum>104534</artnum><issn>1567-1348</issn><eissn>1567-7257</eissn><abstract>Nontyphoidal Salmonella (NTS) are associated with both diarrhea and bacteremia. Antimicrobial resistance (AMR) is common in NTS in low-middle income countries, but the major source(s) of AMR NTS in humans are not known. Here, we aimed to assess the role of animals as a source of AMR in human NTS infections in Vietnam. We retrospectively combined and analyzed 672 NTS human and animal isolates from four studies in southern Vietnam and compared serovars, sequence types (ST), and AMR profiles. We generated a population structure of circulating organisms and aimed to attribute sources of AMR in NTS causing invasive and noninvasive disease in humans using Bayesian multinomial mixture models.
Among 672 NTS isolates, 148 (22%) originated from human blood, 211 (31%) from human stool, and 313 (47%) from animal stool. The distribution of serovars, STs, and AMR profiles differed among sources; serovars Enteritidis, Typhimurium, and Weltevreden were the most common in human blood, human stool, and animals, respectively. We identified an association between the source of NTS and AMR profile; the majority of AMR isolates were isolated from human blood (p < 0.001). Modelling by ST-AMR profile found chickens and pigs were likely the major sources of AMR NTS in human blood and stool, respectively; but unsampled sources were found to be a major contributor.
Antimicrobial use in food animals is hypothesized to play role in the emergence of AMR in human pathogens. Our cross-sectional population-based approach suggests a significant overlap between AMR in NTS in animals and humans, but animal NTS does explain the full extent of AMR in human NTS infections in Vietnam.
•The major source(s) of antimicrobial resistance (AMR) in nontyphoidal Salmonella (NTS) are unknown.•We analyzed 672 NTS isolates, 148 (41%) from human blood, 211 (59%) from human stool, and 136 (43%) from animal stool.•Enteritidis, Typhimurium, and Weltevreden were the common serovars in human blood, human stool, and animals, respectively.•The majority of AMR isolates were associated with human blood.•NTS from animals does explain the full extent of AMR in human NTS infections.</abstract><cop>AMSTERDAM</cop><pub>Elsevier B.V</pub><pmid>32920195</pmid><doi>10.1016/j.meegid.2020.104534</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0003-1308-5755</orcidid><orcidid>https://orcid.org/0000-0001-9161-8890</orcidid><orcidid>https://orcid.org/0000-0001-5905-1310</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Anti-Bacterial Agents - therapeutic use Antimicrobial resistance Bacteremia Bacterial Zoonoses - epidemiology Chickens - virology Cross-Sectional Studies Diarrhea Disease Transmission, Infectious - veterinary Disease Vectors Drug Resistance, Bacterial - drug effects Ducks - virology Genetic Variation Infectious Diseases Life Sciences & Biomedicine Microbial Sensitivity Tests Nontyphoidal Salmonella Retrospective Studies Rodentia - virology Salmonella Infections - drug therapy Salmonella Infections - epidemiology Salmonella Infections - transmission Salmonella typhimurium - drug effects Science & Technology Serogroup Swine - virology Vietnam - epidemiology Zoonosis |
| title | The role of animals as a source of antimicrobial resistant nontyphoidal Salmonella causing invasive and non-invasive human disease in Vietnam |
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