Unraveling antimicrobial resistance genes and phenotype patterns among Enterococcus faecalis isolated from retail chicken products in Japan
Multidrug-resistant enterococci are considered crucial drivers for the dissemination of antimicrobial resistance determinants within and beyond a genus. These organisms may pass numerous resistance determinants to other harmful pathogens, whose multiple resistances would cause adverse consequences....
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| creator | Hidano, Arata Yamamoto, Takehisa Hayama, Yoko Muroga, Norihiko Kobayashi, Sota Nishida, Takeshi Tsutsui, Toshiyuki |
| description | Multidrug-resistant enterococci are considered crucial drivers for the dissemination of antimicrobial resistance determinants within and beyond a genus. These organisms may pass numerous resistance determinants to other harmful pathogens, whose multiple resistances would cause adverse consequences. Therefore, an understanding of the coexistence epidemiology of resistance genes is critical, but such information remains limited. In this study, our first objective was to determine the prevalence of principal resistance phenotypes and genes among Enterococcus faecalis isolated from retail chicken domestic products collected throughout Japan. Subsequent analysis of these data by using an additive Bayesian network (ABN) model revealed the co-appearance patterns of resistance genes and identified the associations between resistance genes and phenotypes. The common phenotypes observed among E. faecalis isolated from the domestic products were the resistances to oxytetracycline (58.4%), dihydrostreptomycin (50.4%), and erythromycin (37.2%), and the gene tet(L) was detected in 46.0% of the isolates. The ABN model identified statistically significant associations between tet(L) and erm(B), tet(L) and ant(6)-Ia, ant(6)-Ia and aph(3')-IIIa, and aph(3')-IIIa and erm(B), which indicated that a multiple-resistance profile of tetracycline, erythromycin, streptomycin, and kanamycin is systematic rather than random. Conversely, the presence of tet(O) was only negatively associated with that of erm(B) and tet(M), which suggested that in the presence of tet(O), the aforementioned multiple resistance is unlikely to be observed. Such heterogeneity in linkages among genes that confer the same phenotypic resistance highlights the importance of incorporating genetic information when investigating the risk factors for the spread of resistance. The epidemiological factors that underlie the persistence of systematic multiple-resistance patterns warrant further investigations with appropriate adjustments for ecological and bacteriological factors. |
| doi_str_mv | 10.1371/journal.pone.0121189 |
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These organisms may pass numerous resistance determinants to other harmful pathogens, whose multiple resistances would cause adverse consequences. Therefore, an understanding of the coexistence epidemiology of resistance genes is critical, but such information remains limited. In this study, our first objective was to determine the prevalence of principal resistance phenotypes and genes among Enterococcus faecalis isolated from retail chicken domestic products collected throughout Japan. Subsequent analysis of these data by using an additive Bayesian network (ABN) model revealed the co-appearance patterns of resistance genes and identified the associations between resistance genes and phenotypes. The common phenotypes observed among E. faecalis isolated from the domestic products were the resistances to oxytetracycline (58.4%), dihydrostreptomycin (50.4%), and erythromycin (37.2%), and the gene tet(L) was detected in 46.0% of the isolates. The ABN model identified statistically significant associations between tet(L) and erm(B), tet(L) and ant(6)-Ia, ant(6)-Ia and aph(3')-IIIa, and aph(3')-IIIa and erm(B), which indicated that a multiple-resistance profile of tetracycline, erythromycin, streptomycin, and kanamycin is systematic rather than random. Conversely, the presence of tet(O) was only negatively associated with that of erm(B) and tet(M), which suggested that in the presence of tet(O), the aforementioned multiple resistance is unlikely to be observed. Such heterogeneity in linkages among genes that confer the same phenotypic resistance highlights the importance of incorporating genetic information when investigating the risk factors for the spread of resistance. The epidemiological factors that underlie the persistence of systematic multiple-resistance patterns warrant further investigations with appropriate adjustments for ecological and bacteriological factors.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0121189</identifier><identifier>PMID: 25781022</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Anti-Bacterial Agents - pharmacology ; Antibacterial agents ; Antibiotics ; Antiinfectives and antibacterials ; Antimicrobial agents ; Antimicrobial resistance ; Bacteria ; Bayesian analysis ; Chickens - microbiology ; Cities ; Coexistence ; Data processing ; Dihydrostreptomycin ; Drug resistance ; Drug Resistance, Multiple, Bacterial - genetics ; Ecological monitoring ; Enterococcus ; Enterococcus faecalis ; Enterococcus faecalis - genetics ; Enterococcus faecalis - isolation & purification ; Enterococcus faecium ; Epidemiology ; Erythromycin ; Food contamination & poisoning ; Food Microbiology ; Genes ; Genes, Bacterial ; Genetic aspects ; Genotype & phenotype ; Japan ; Kanamycin ; Microbial drug resistance ; Models, Biological ; Multidrug resistance ; Oxytetracycline ; Phenotypes ; Poultry ; Poultry Products - microbiology ; Resistance factors ; Risk analysis ; Risk factors ; Statistical analysis ; Streptomycin ; Studies ; Suidae ; Tetracycline Resistance - genetics</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0121189-e0121189</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Hidano et al. 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>2015 Hidano et al 2015 Hidano et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-8835c926c7194d0df1f95a59f7e541363c0fd19e1cba6656ca06f97f03c92ceb3</citedby><cites>FETCH-LOGICAL-c692t-8835c926c7194d0df1f95a59f7e541363c0fd19e1cba6656ca06f97f03c92ceb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4363150/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4363150/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25781022$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hidano, Arata</creatorcontrib><creatorcontrib>Yamamoto, Takehisa</creatorcontrib><creatorcontrib>Hayama, Yoko</creatorcontrib><creatorcontrib>Muroga, Norihiko</creatorcontrib><creatorcontrib>Kobayashi, Sota</creatorcontrib><creatorcontrib>Nishida, Takeshi</creatorcontrib><creatorcontrib>Tsutsui, Toshiyuki</creatorcontrib><title>Unraveling antimicrobial resistance genes and phenotype patterns among Enterococcus faecalis isolated from retail chicken products in Japan</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Multidrug-resistant enterococci are considered crucial drivers for the dissemination of antimicrobial resistance determinants within and beyond a genus. These organisms may pass numerous resistance determinants to other harmful pathogens, whose multiple resistances would cause adverse consequences. Therefore, an understanding of the coexistence epidemiology of resistance genes is critical, but such information remains limited. In this study, our first objective was to determine the prevalence of principal resistance phenotypes and genes among Enterococcus faecalis isolated from retail chicken domestic products collected throughout Japan. Subsequent analysis of these data by using an additive Bayesian network (ABN) model revealed the co-appearance patterns of resistance genes and identified the associations between resistance genes and phenotypes. The common phenotypes observed among E. faecalis isolated from the domestic products were the resistances to oxytetracycline (58.4%), dihydrostreptomycin (50.4%), and erythromycin (37.2%), and the gene tet(L) was detected in 46.0% of the isolates. The ABN model identified statistically significant associations between tet(L) and erm(B), tet(L) and ant(6)-Ia, ant(6)-Ia and aph(3')-IIIa, and aph(3')-IIIa and erm(B), which indicated that a multiple-resistance profile of tetracycline, erythromycin, streptomycin, and kanamycin is systematic rather than random. Conversely, the presence of tet(O) was only negatively associated with that of erm(B) and tet(M), which suggested that in the presence of tet(O), the aforementioned multiple resistance is unlikely to be observed. Such heterogeneity in linkages among genes that confer the same phenotypic resistance highlights the importance of incorporating genetic information when investigating the risk factors for the spread of resistance. The epidemiological factors that underlie the persistence of systematic multiple-resistance patterns warrant further investigations with appropriate adjustments for ecological and bacteriological factors.</description><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibacterial agents</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Antimicrobial agents</subject><subject>Antimicrobial resistance</subject><subject>Bacteria</subject><subject>Bayesian analysis</subject><subject>Chickens - microbiology</subject><subject>Cities</subject><subject>Coexistence</subject><subject>Data processing</subject><subject>Dihydrostreptomycin</subject><subject>Drug resistance</subject><subject>Drug Resistance, Multiple, Bacterial - genetics</subject><subject>Ecological monitoring</subject><subject>Enterococcus</subject><subject>Enterococcus faecalis</subject><subject>Enterococcus faecalis - genetics</subject><subject>Enterococcus faecalis - isolation & purification</subject><subject>Enterococcus faecium</subject><subject>Epidemiology</subject><subject>Erythromycin</subject><subject>Food contamination & poisoning</subject><subject>Food Microbiology</subject><subject>Genes</subject><subject>Genes, Bacterial</subject><subject>Genetic aspects</subject><subject>Genotype & phenotype</subject><subject>Japan</subject><subject>Kanamycin</subject><subject>Microbial drug resistance</subject><subject>Models, Biological</subject><subject>Multidrug resistance</subject><subject>Oxytetracycline</subject><subject>Phenotypes</subject><subject>Poultry</subject><subject>Poultry Products - microbiology</subject><subject>Resistance factors</subject><subject>Risk analysis</subject><subject>Risk factors</subject><subject>Statistical analysis</subject><subject>Streptomycin</subject><subject>Studies</subject><subject>Suidae</subject><subject>Tetracycline Resistance - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk8Fu1DAQhiMEoqXwBggiISE47GLHsZNckKqqwKJKlYBytSbOZNeL1w62U9Fn4KXxsttqg3pAOTgZf__vzHgmy55TMqesou_WbvQWzHxwFueEFpTWzYPsmDasmImCsIcH70fZkxDWhHBWC_E4Oyp4VVNSFMfZ7yvr4RqNtsscbNQbrbxrNZjcY9AhglWYL9FiSNtdPqzQungzYD5AjOhtCm9c0p7b9OWUU2oMeQ-owOiQ6-AMROzy3rtNcoygTa5WWv1Amw_edaOKibL5ZxjAPs0e9WACPtuvJ9nVh_NvZ59mF5cfF2enFzMlmiLO6ppx1RRCVbQpO9L1tG848KavkJeUCaZI39EGqWpBCC4UENE3VU9YUils2Un2cuc7GBfkvo5BUiHKoqhYzROx2BGdg7UcvN6Av5EOtPwbcH4pwUetDEoFbQOtIEXNsOwYtGWtGOOMcF52lEPyer8_bWw32Cm00YOZmE53rF7JpbuWZUqFcpIM3uwNvPs5Yohyo4NCY8CiG3f_XVVCNFVCX_2D3p_dnlpCSkDb3qVz1dZUnpYFZ6JiVZmo-T1UejpMTZKartcpPhG8nQgSE_FXXMIYglx8_fL_7OX3Kfv6gF0hmLhKfTVG7WyYguUOTC0cgsf-rsiUyO3M3FZDbmdG7mcmyV4cXtCd6HZI2B-V1RRE</recordid><startdate>20150317</startdate><enddate>20150317</enddate><creator>Hidano, Arata</creator><creator>Yamamoto, Takehisa</creator><creator>Hayama, Yoko</creator><creator>Muroga, Norihiko</creator><creator>Kobayashi, Sota</creator><creator>Nishida, Takeshi</creator><creator>Tsutsui, Toshiyuki</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>IOV</scope><scope>ISR</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>AEUYN</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>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150317</creationdate><title>Unraveling antimicrobial resistance genes and phenotype patterns among Enterococcus faecalis isolated from retail chicken products in Japan</title><author>Hidano, Arata ; Yamamoto, Takehisa ; Hayama, Yoko ; Muroga, Norihiko ; Kobayashi, Sota ; Nishida, Takeshi ; Tsutsui, Toshiyuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-8835c926c7194d0df1f95a59f7e541363c0fd19e1cba6656ca06f97f03c92ceb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Anti-Bacterial Agents - 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These organisms may pass numerous resistance determinants to other harmful pathogens, whose multiple resistances would cause adverse consequences. Therefore, an understanding of the coexistence epidemiology of resistance genes is critical, but such information remains limited. In this study, our first objective was to determine the prevalence of principal resistance phenotypes and genes among Enterococcus faecalis isolated from retail chicken domestic products collected throughout Japan. Subsequent analysis of these data by using an additive Bayesian network (ABN) model revealed the co-appearance patterns of resistance genes and identified the associations between resistance genes and phenotypes. The common phenotypes observed among E. faecalis isolated from the domestic products were the resistances to oxytetracycline (58.4%), dihydrostreptomycin (50.4%), and erythromycin (37.2%), and the gene tet(L) was detected in 46.0% of the isolates. The ABN model identified statistically significant associations between tet(L) and erm(B), tet(L) and ant(6)-Ia, ant(6)-Ia and aph(3')-IIIa, and aph(3')-IIIa and erm(B), which indicated that a multiple-resistance profile of tetracycline, erythromycin, streptomycin, and kanamycin is systematic rather than random. Conversely, the presence of tet(O) was only negatively associated with that of erm(B) and tet(M), which suggested that in the presence of tet(O), the aforementioned multiple resistance is unlikely to be observed. Such heterogeneity in linkages among genes that confer the same phenotypic resistance highlights the importance of incorporating genetic information when investigating the risk factors for the spread of resistance. The epidemiological factors that underlie the persistence of systematic multiple-resistance patterns warrant further investigations with appropriate adjustments for ecological and bacteriological factors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25781022</pmid><doi>10.1371/journal.pone.0121189</doi><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2015-03, Vol.10 (3), p.e0121189-e0121189 |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Animals Anti-Bacterial Agents - pharmacology Antibacterial agents Antibiotics Antiinfectives and antibacterials Antimicrobial agents Antimicrobial resistance Bacteria Bayesian analysis Chickens - microbiology Cities Coexistence Data processing Dihydrostreptomycin Drug resistance Drug Resistance, Multiple, Bacterial - genetics Ecological monitoring Enterococcus Enterococcus faecalis Enterococcus faecalis - genetics Enterococcus faecalis - isolation & purification Enterococcus faecium Epidemiology Erythromycin Food contamination & poisoning Food Microbiology Genes Genes, Bacterial Genetic aspects Genotype & phenotype Japan Kanamycin Microbial drug resistance Models, Biological Multidrug resistance Oxytetracycline Phenotypes Poultry Poultry Products - microbiology Resistance factors Risk analysis Risk factors Statistical analysis Streptomycin Studies Suidae Tetracycline Resistance - genetics |
| title | Unraveling antimicrobial resistance genes and phenotype patterns among Enterococcus faecalis isolated from retail chicken products in Japan |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T23%3A41%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Unraveling%20antimicrobial%20resistance%20genes%20and%20phenotype%20patterns%20among%20Enterococcus%20faecalis%20isolated%20from%20retail%20chicken%20products%20in%20Japan&rft.jtitle=PloS%20one&rft.au=Hidano,%20Arata&rft.date=2015-03-17&rft.volume=10&rft.issue=3&rft.spage=e0121189&rft.epage=e0121189&rft.pages=e0121189-e0121189&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0121189&rft_dat=%3Cgale_plos_%3EA425367374%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1664227385&rft_id=info:pmid/25781022&rft_galeid=A425367374&rft_doaj_id=oai_doaj_org_article_cab9ab60283e4d3ab48c33530554d15a&rfr_iscdi=true |