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Effect of veterinary feed directive rule changes on tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the United States
Antimicrobial-resistant bacteria are a growing public health threat. In 2017 the U.S. Food and Drug Administration implemented Veterinary Feed Directive (VFD) rules changes to limit medically important antimicrobial use in food-producing animals, combating antimicrobial-resistant bacteria. The effec...
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Published in: | PloS one 2023-08, Vol.18 (8), p.e0289208 |
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description | Antimicrobial-resistant bacteria are a growing public health threat. In 2017 the U.S. Food and Drug Administration implemented Veterinary Feed Directive (VFD) rules changes to limit medically important antimicrobial use in food-producing animals, combating antimicrobial-resistant bacteria. The effect of the VFD rule changes on the occurrence of bacteria resistant to medically-important antimicrobials in retail meats is yet to be investigated in the U.S. This study investigates whether the VFD rule changes affected the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the U.S.
Multivariable mixed effect logistic regression models were used to analyze 2002-2019 retail meats surveillance data from the National Antimicrobial Resistance Monitoring System (NARMS) in the U.S. Variables included VFD rule changes, meat type, quarter of year, and raising claims. A potential association between these variables and the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats was estimated.
Analysis included data regarding tetracycline-resistant Salmonella (n = 8,501), Escherichia (n = 20, 283), Campylobacter (n = 9,682), and erythromycin-resistant Campylobacter (n = 10,446) in retail meats. The odds of detecting tetracycline-resistant Escherichia (OR = 0.60), Campylobacter (OR = 0.89), and erythromycin-resistant Campylobacter (OR = 0.43) in chicken breast significantly decreased after the VFD rule changes, compared to the pre-VFD rule change period. The odds of detecting tetracycline-resistant Salmonella (0.66), Escherichia (OR = 0.56), and Campylobacter (OR = 0.33) in ground turkey also significantly decreased. However, the odds of detecting tetracycline-resistant Salmonella (OR = 1.49) in chicken breast and erythromycin-resistant Campylobacter (OR = 4.63) in ground turkey significantly increased. There was no significant change in the odds of detecting tetracycline-resistant Salmonella and Escherichia in ground beef or pork chops.
The implementation of VFD rule changes had a beneficial effect by reducing the occurrence of tetracycline-resistant and erythromycin-resistant bacteria in chicken and ground turkey. Ongoing surveillance of antimicrobial resistance and antimicrobial use could complement the implementation of stewardship such as VFD rule in food-producing animals in the U.S. |
doi_str_mv | 10.1371/journal.pone.0289208 |
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Multivariable mixed effect logistic regression models were used to analyze 2002-2019 retail meats surveillance data from the National Antimicrobial Resistance Monitoring System (NARMS) in the U.S. Variables included VFD rule changes, meat type, quarter of year, and raising claims. A potential association between these variables and the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats was estimated.
Analysis included data regarding tetracycline-resistant Salmonella (n = 8,501), Escherichia (n = 20, 283), Campylobacter (n = 9,682), and erythromycin-resistant Campylobacter (n = 10,446) in retail meats. The odds of detecting tetracycline-resistant Escherichia (OR = 0.60), Campylobacter (OR = 0.89), and erythromycin-resistant Campylobacter (OR = 0.43) in chicken breast significantly decreased after the VFD rule changes, compared to the pre-VFD rule change period. The odds of detecting tetracycline-resistant Salmonella (0.66), Escherichia (OR = 0.56), and Campylobacter (OR = 0.33) in ground turkey also significantly decreased. However, the odds of detecting tetracycline-resistant Salmonella (OR = 1.49) in chicken breast and erythromycin-resistant Campylobacter (OR = 4.63) in ground turkey significantly increased. There was no significant change in the odds of detecting tetracycline-resistant Salmonella and Escherichia in ground beef or pork chops.
The implementation of VFD rule changes had a beneficial effect by reducing the occurrence of tetracycline-resistant and erythromycin-resistant bacteria in chicken and ground turkey. Ongoing surveillance of antimicrobial resistance and antimicrobial use could complement the implementation of stewardship such as VFD rule in food-producing animals in the U.S.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0289208</identifier><identifier>PMID: 37535600</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Anti-Bacterial Agents - pharmacology ; Antibiotics ; Antimicrobial agents ; Antimicrobial resistance ; Bacteria ; Biology and Life Sciences ; Campylobacter ; Cattle ; Chickens ; Chickens - microbiology ; Coliforms ; Datasets ; Drug resistance ; Drug Resistance, Bacterial ; Erythromycin ; Erythromycin - pharmacology ; Escherichia ; Feeds ; Food ; Health risks ; Illnesses ; Management ; Meat ; Meat - microbiology ; Meat industry ; Meat products ; Medicine and Health Sciences ; Microbial Sensitivity Tests ; Monitoring systems ; Poultry ; Prevention ; Protein Synthesis Inhibitors - pharmacology ; Proteins ; Public health ; Regression analysis ; Regression models ; Salmonella ; Surveillance ; Tetracycline - pharmacology ; Turkeys ; Turkeys - microbiology ; United States ; Variables</subject><ispartof>PloS one, 2023-08, Vol.18 (8), p.e0289208</ispartof><rights>Copyright: © 2023 Sarkar, Okafor. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Sarkar, Okafor. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Sarkar, Okafor 2023 Sarkar, Okafor</rights><rights>2023 Sarkar, Okafor. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c594t-d4f2f060c39141dfa499d5ff6578ce48e2329eb7dc1de6a53e3fd6c8371f6d653</citedby><cites>FETCH-LOGICAL-c594t-d4f2f060c39141dfa499d5ff6578ce48e2329eb7dc1de6a53e3fd6c8371f6d653</cites><orcidid>0000-0002-2895-8347 ; 0000-0001-8922-5676</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2845498549/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2845498549?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37535600$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Varga, Csaba</contributor><creatorcontrib>Sarkar, Shamim</creatorcontrib><creatorcontrib>Okafor, Chika</creatorcontrib><title>Effect of veterinary feed directive rule changes on tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the United States</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Antimicrobial-resistant bacteria are a growing public health threat. In 2017 the U.S. Food and Drug Administration implemented Veterinary Feed Directive (VFD) rules changes to limit medically important antimicrobial use in food-producing animals, combating antimicrobial-resistant bacteria. The effect of the VFD rule changes on the occurrence of bacteria resistant to medically-important antimicrobials in retail meats is yet to be investigated in the U.S. This study investigates whether the VFD rule changes affected the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the U.S.
Multivariable mixed effect logistic regression models were used to analyze 2002-2019 retail meats surveillance data from the National Antimicrobial Resistance Monitoring System (NARMS) in the U.S. Variables included VFD rule changes, meat type, quarter of year, and raising claims. A potential association between these variables and the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats was estimated.
Analysis included data regarding tetracycline-resistant Salmonella (n = 8,501), Escherichia (n = 20, 283), Campylobacter (n = 9,682), and erythromycin-resistant Campylobacter (n = 10,446) in retail meats. The odds of detecting tetracycline-resistant Escherichia (OR = 0.60), Campylobacter (OR = 0.89), and erythromycin-resistant Campylobacter (OR = 0.43) in chicken breast significantly decreased after the VFD rule changes, compared to the pre-VFD rule change period. The odds of detecting tetracycline-resistant Salmonella (0.66), Escherichia (OR = 0.56), and Campylobacter (OR = 0.33) in ground turkey also significantly decreased. However, the odds of detecting tetracycline-resistant Salmonella (OR = 1.49) in chicken breast and erythromycin-resistant Campylobacter (OR = 4.63) in ground turkey significantly increased. There was no significant change in the odds of detecting tetracycline-resistant Salmonella and Escherichia in ground beef or pork chops.
The implementation of VFD rule changes had a beneficial effect by reducing the occurrence of tetracycline-resistant and erythromycin-resistant bacteria in chicken and ground turkey. Ongoing surveillance of antimicrobial resistance and antimicrobial use could complement the implementation of stewardship such as VFD rule in food-producing animals in the U.S.</description><subject>Analysis</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotics</subject><subject>Antimicrobial agents</subject><subject>Antimicrobial resistance</subject><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Campylobacter</subject><subject>Cattle</subject><subject>Chickens</subject><subject>Chickens - microbiology</subject><subject>Coliforms</subject><subject>Datasets</subject><subject>Drug resistance</subject><subject>Drug Resistance, Bacterial</subject><subject>Erythromycin</subject><subject>Erythromycin - pharmacology</subject><subject>Escherichia</subject><subject>Feeds</subject><subject>Food</subject><subject>Health risks</subject><subject>Illnesses</subject><subject>Management</subject><subject>Meat</subject><subject>Meat - microbiology</subject><subject>Meat industry</subject><subject>Meat products</subject><subject>Medicine and Health Sciences</subject><subject>Microbial Sensitivity Tests</subject><subject>Monitoring systems</subject><subject>Poultry</subject><subject>Prevention</subject><subject>Protein Synthesis Inhibitors - pharmacology</subject><subject>Proteins</subject><subject>Public health</subject><subject>Regression analysis</subject><subject>Regression models</subject><subject>Salmonella</subject><subject>Surveillance</subject><subject>Tetracycline - pharmacology</subject><subject>Turkeys</subject><subject>Turkeys - microbiology</subject><subject>United States</subject><subject>Variables</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptUtFu0zAUjRCIjcEfILDEy5BosWPHiZ_QVBWYNImHsWfLta9bT4ldbLdS_45Pw1m7qUVTFCW-95yTe09OVb0neEpoS77eh030qp-ug4cprjtR4-5FdU4ErSe8xvTl0ftZ9Sale4wb2nH-ujqjbUMbjvF59XduLeiMgkVbyBCdV3GHLIBBxsXScVtAcdMD0ivll5BQ8ChDjkrvdO88TCIkl7LyGSlvEMRdXsUw7LTzR62F0qO4Qpe3qh_KxH2vvqB50qtS1StXDiN7pob1rg979GfkPIqQlevRACqn8ZxXgO68y2W-26wypLfVK6v6BO8Oz4vq7vv89-zn5ObXj-vZ1c1EN4LliWG2tphjTQVhxFjFhDCNtbxpOw2sg5rWAhat0cQAVw0Fag3XXXHacsMbelF93Ouu-5Dkwfwk6441THTlLojrPcIEdS_X0Q3FShmUkw-FEJdSxex0D1IxxutFx0FjxgzFApQlTAnGNQaxoEXr2-Frm8UARoMvjvcnoqcd71ZyGbaSYCrKOKQoXB4UYvizgZTl4JIeffcQNg-Dc0ExIeNqn_6DPr_eAbVUZQPnbRhDMIrKq7Z43HYdawtq-gyqXAYGp8uPt67UTwhsT9AxpBTBPi1JsByD_jiMHIMuD0EvtA_HBj2RHpNN_wHoI_-a</recordid><startdate>20230803</startdate><enddate>20230803</enddate><creator>Sarkar, Shamim</creator><creator>Okafor, Chika</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-2895-8347</orcidid><orcidid>https://orcid.org/0000-0001-8922-5676</orcidid></search><sort><creationdate>20230803</creationdate><title>Effect of veterinary feed directive rule changes on tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the United States</title><author>Sarkar, Shamim ; Okafor, Chika</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c594t-d4f2f060c39141dfa499d5ff6578ce48e2329eb7dc1de6a53e3fd6c8371f6d653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sarkar, Shamim</au><au>Okafor, Chika</au><au>Varga, Csaba</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effect of veterinary feed directive rule changes on tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the United States</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-08-03</date><risdate>2023</risdate><volume>18</volume><issue>8</issue><spage>e0289208</spage><pages>e0289208-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Antimicrobial-resistant bacteria are a growing public health threat. In 2017 the U.S. Food and Drug Administration implemented Veterinary Feed Directive (VFD) rules changes to limit medically important antimicrobial use in food-producing animals, combating antimicrobial-resistant bacteria. The effect of the VFD rule changes on the occurrence of bacteria resistant to medically-important antimicrobials in retail meats is yet to be investigated in the U.S. This study investigates whether the VFD rule changes affected the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the U.S.
Multivariable mixed effect logistic regression models were used to analyze 2002-2019 retail meats surveillance data from the National Antimicrobial Resistance Monitoring System (NARMS) in the U.S. Variables included VFD rule changes, meat type, quarter of year, and raising claims. A potential association between these variables and the occurrence of tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats was estimated.
Analysis included data regarding tetracycline-resistant Salmonella (n = 8,501), Escherichia (n = 20, 283), Campylobacter (n = 9,682), and erythromycin-resistant Campylobacter (n = 10,446) in retail meats. The odds of detecting tetracycline-resistant Escherichia (OR = 0.60), Campylobacter (OR = 0.89), and erythromycin-resistant Campylobacter (OR = 0.43) in chicken breast significantly decreased after the VFD rule changes, compared to the pre-VFD rule change period. The odds of detecting tetracycline-resistant Salmonella (0.66), Escherichia (OR = 0.56), and Campylobacter (OR = 0.33) in ground turkey also significantly decreased. However, the odds of detecting tetracycline-resistant Salmonella (OR = 1.49) in chicken breast and erythromycin-resistant Campylobacter (OR = 4.63) in ground turkey significantly increased. There was no significant change in the odds of detecting tetracycline-resistant Salmonella and Escherichia in ground beef or pork chops.
The implementation of VFD rule changes had a beneficial effect by reducing the occurrence of tetracycline-resistant and erythromycin-resistant bacteria in chicken and ground turkey. Ongoing surveillance of antimicrobial resistance and antimicrobial use could complement the implementation of stewardship such as VFD rule in food-producing animals in the U.S.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37535600</pmid><doi>10.1371/journal.pone.0289208</doi><orcidid>https://orcid.org/0000-0002-2895-8347</orcidid><orcidid>https://orcid.org/0000-0001-8922-5676</orcidid><oa>free_for_read</oa></addata></record> |
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recordid | cdi_plos_journals_2845498549 |
source | Publicly Available Content Database; PubMed Central |
subjects | Analysis Animals Anti-Bacterial Agents - pharmacology Antibiotics Antimicrobial agents Antimicrobial resistance Bacteria Biology and Life Sciences Campylobacter Cattle Chickens Chickens - microbiology Coliforms Datasets Drug resistance Drug Resistance, Bacterial Erythromycin Erythromycin - pharmacology Escherichia Feeds Food Health risks Illnesses Management Meat Meat - microbiology Meat industry Meat products Medicine and Health Sciences Microbial Sensitivity Tests Monitoring systems Poultry Prevention Protein Synthesis Inhibitors - pharmacology Proteins Public health Regression analysis Regression models Salmonella Surveillance Tetracycline - pharmacology Turkeys Turkeys - microbiology United States Variables |
title | Effect of veterinary feed directive rule changes on tetracycline-resistant and erythromycin-resistant bacteria (Salmonella, Escherichia, and Campylobacter) in retail meats in the United States |
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