Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli
Abstract Objectives Escherichia coli is characterized by three resistance patterns to β-lactams/β-lactamase inhibitors (BLs/BLIs): (i) resistance to ampicillin/sulbactam and susceptibility to amoxicillin/clavulanic acid and piperacillin/tazobactam (RSS); (ii) resistance to ampicillin/sulbactam and a...
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| Veröffentlicht in: | Journal of antimicrobial chemotherapy 2020-01, Vol.75 (1), p.77-85 |
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| creator | Rodríguez-Villodres, Ángel Gil-Marqués, María Luisa Álvarez-Marín, Rocío Bonnin, Rémy A Pachón-Ibáñez, María Eugenia Aguilar-Guisado, Manuela Naas, Thierry Aznar, Javier Pachón, Jerónimo Lepe, José Antonio Smani, Younes |
| description | Abstract
Objectives
Escherichia coli is characterized by three resistance patterns to β-lactams/β-lactamase inhibitors (BLs/BLIs): (i) resistance to ampicillin/sulbactam and susceptibility to amoxicillin/clavulanic acid and piperacillin/tazobactam (RSS); (ii) resistance to ampicillin/sulbactam and amoxicillin/clavulanic acid, and susceptibility to piperacillin/tazobactam (RRS); and (iii) resistance to ampicillin/sulbactam, amoxicillin/clavulanic acid and piperacillin/tazobactam (RRR). These resistance patterns are acquired consecutively, indicating a potential risk of developing resistance to piperacillin/tazobactam, but the precise mechanism of this process is not completely understood.
Methods
Clinical isolates incrementally pressured by piperacillin/tazobactam selection in vitro and in vivo were used. We determined the MIC of piperacillin/tazobactam in the presence and absence of piperacillin/tazobactam pressure. We deciphered the role of the blaTEM genes in the new concept of extended-spectrum resistance to BLs/BLIs (ESRI) using genomic analysis. The activity of β-lactamase was quantified in these isolates.
Results
We show that piperacillin/tazobactam resistance is induced in E. coli carrying blaTEM genes. This resistance is due to the increase in copy numbers and transcription levels of the blaTEM gene, thus increasing β-lactamase activity and consequently increasing piperacillin/tazobactam MICs. Genome sequencing of two blaTEM-carrying representative isolates showed that piperacillin/tazobactam treatment produced two types of duplications of blaTEM (8 and 60 copies, respectively). In the clinical setting, piperacillin/tazobactam treatment of patients infected by E. coli carrying blaTEM is associated with a risk of therapeutic failure.
Conclusions
This study describes for the first time the ESRI in E. coli. This new concept is very important in the understanding of the mechanism involved in the acquisition of resistance to BLs/BLIs. |
| doi_str_mv | 10.1093/jac/dkz393 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2306211724</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/jac/dkz393</oup_id><sourcerecordid>2306211724</sourcerecordid><originalsourceid>FETCH-LOGICAL-c317t-48b24fb6bf9656b22256c125da81151d6398c9d3df1211365e04dd6c4ac2c4f33</originalsourceid><addsrcrecordid>eNp9kMtKAzEUQIMoWh8bP0CyEaowNq9JO0uRqoWC4GM9ZJI7NJppapKpr7_yQ_wmR6pdurp3ce7hchA6pOSMkoIPHpUemKd3XvAN1KNCkoyRgm6iHuEkz4Yi5ztoN8ZHQojM5Wgb7XAqKS-k6KGP8WuCuQGTxQXoFNoGB4g2JjXXgJPHX5-ZUzqpJg7Wq4qA7XxmK5t8iLg_vrudnGBYercEg-vgG-z8S-ZgCW6tS3gc9QyC1TOrsPbO7qOtWrkIB79zDz1cju8vrrPpzdXk4nyaaU6HKROjiom6klVddO9XjLFcaspyo0aU5tRIXox0YbipKaOUyxyIMEZqoTTTouZ8D_VX3kXwzy3EVDY2anBOzcG3sWScyO5yyESHnq5QHXyMAepyEWyjwltJSfkTu-xil6vYHXz0622rBswa_avbAccrwLeL_0TfrHCKfQ</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2306211724</pqid></control><display><type>article</type><title>Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli</title><source>Oxford University Press Journals All Titles (1996-Current)</source><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Rodríguez-Villodres, Ángel ; Gil-Marqués, María Luisa ; Álvarez-Marín, Rocío ; Bonnin, Rémy A ; Pachón-Ibáñez, María Eugenia ; Aguilar-Guisado, Manuela ; Naas, Thierry ; Aznar, Javier ; Pachón, Jerónimo ; Lepe, José Antonio ; Smani, Younes</creator><creatorcontrib>Rodríguez-Villodres, Ángel ; Gil-Marqués, María Luisa ; Álvarez-Marín, Rocío ; Bonnin, Rémy A ; Pachón-Ibáñez, María Eugenia ; Aguilar-Guisado, Manuela ; Naas, Thierry ; Aznar, Javier ; Pachón, Jerónimo ; Lepe, José Antonio ; Smani, Younes</creatorcontrib><description>Abstract
Objectives
Escherichia coli is characterized by three resistance patterns to β-lactams/β-lactamase inhibitors (BLs/BLIs): (i) resistance to ampicillin/sulbactam and susceptibility to amoxicillin/clavulanic acid and piperacillin/tazobactam (RSS); (ii) resistance to ampicillin/sulbactam and amoxicillin/clavulanic acid, and susceptibility to piperacillin/tazobactam (RRS); and (iii) resistance to ampicillin/sulbactam, amoxicillin/clavulanic acid and piperacillin/tazobactam (RRR). These resistance patterns are acquired consecutively, indicating a potential risk of developing resistance to piperacillin/tazobactam, but the precise mechanism of this process is not completely understood.
Methods
Clinical isolates incrementally pressured by piperacillin/tazobactam selection in vitro and in vivo were used. We determined the MIC of piperacillin/tazobactam in the presence and absence of piperacillin/tazobactam pressure. We deciphered the role of the blaTEM genes in the new concept of extended-spectrum resistance to BLs/BLIs (ESRI) using genomic analysis. The activity of β-lactamase was quantified in these isolates.
Results
We show that piperacillin/tazobactam resistance is induced in E. coli carrying blaTEM genes. This resistance is due to the increase in copy numbers and transcription levels of the blaTEM gene, thus increasing β-lactamase activity and consequently increasing piperacillin/tazobactam MICs. Genome sequencing of two blaTEM-carrying representative isolates showed that piperacillin/tazobactam treatment produced two types of duplications of blaTEM (8 and 60 copies, respectively). In the clinical setting, piperacillin/tazobactam treatment of patients infected by E. coli carrying blaTEM is associated with a risk of therapeutic failure.
Conclusions
This study describes for the first time the ESRI in E. coli. This new concept is very important in the understanding of the mechanism involved in the acquisition of resistance to BLs/BLIs.</description><identifier>ISSN: 0305-7453</identifier><identifier>EISSN: 1460-2091</identifier><identifier>DOI: 10.1093/jac/dkz393</identifier><identifier>PMID: 31613964</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Anti-Bacterial Agents - pharmacology ; beta-Lactamase Inhibitors - pharmacology ; beta-Lactamases - analysis ; beta-Lactamases - genetics ; beta-Lactams - pharmacology ; Drug Resistance, Multiple, Bacterial - genetics ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Humans ; Microbial Sensitivity Tests ; Mutation ; Phylogeny ; Whole Genome Sequencing</subject><ispartof>Journal of antimicrobial chemotherapy, 2020-01, Vol.75 (1), p.77-85</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com. 2019</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c317t-48b24fb6bf9656b22256c125da81151d6398c9d3df1211365e04dd6c4ac2c4f33</citedby><cites>FETCH-LOGICAL-c317t-48b24fb6bf9656b22256c125da81151d6398c9d3df1211365e04dd6c4ac2c4f33</cites><orcidid>0000-0002-2307-3232 ; 0000-0001-9302-8384</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31613964$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rodríguez-Villodres, Ángel</creatorcontrib><creatorcontrib>Gil-Marqués, María Luisa</creatorcontrib><creatorcontrib>Álvarez-Marín, Rocío</creatorcontrib><creatorcontrib>Bonnin, Rémy A</creatorcontrib><creatorcontrib>Pachón-Ibáñez, María Eugenia</creatorcontrib><creatorcontrib>Aguilar-Guisado, Manuela</creatorcontrib><creatorcontrib>Naas, Thierry</creatorcontrib><creatorcontrib>Aznar, Javier</creatorcontrib><creatorcontrib>Pachón, Jerónimo</creatorcontrib><creatorcontrib>Lepe, José Antonio</creatorcontrib><creatorcontrib>Smani, Younes</creatorcontrib><title>Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli</title><title>Journal of antimicrobial chemotherapy</title><addtitle>J Antimicrob Chemother</addtitle><description>Abstract
Objectives
Escherichia coli is characterized by three resistance patterns to β-lactams/β-lactamase inhibitors (BLs/BLIs): (i) resistance to ampicillin/sulbactam and susceptibility to amoxicillin/clavulanic acid and piperacillin/tazobactam (RSS); (ii) resistance to ampicillin/sulbactam and amoxicillin/clavulanic acid, and susceptibility to piperacillin/tazobactam (RRS); and (iii) resistance to ampicillin/sulbactam, amoxicillin/clavulanic acid and piperacillin/tazobactam (RRR). These resistance patterns are acquired consecutively, indicating a potential risk of developing resistance to piperacillin/tazobactam, but the precise mechanism of this process is not completely understood.
Methods
Clinical isolates incrementally pressured by piperacillin/tazobactam selection in vitro and in vivo were used. We determined the MIC of piperacillin/tazobactam in the presence and absence of piperacillin/tazobactam pressure. We deciphered the role of the blaTEM genes in the new concept of extended-spectrum resistance to BLs/BLIs (ESRI) using genomic analysis. The activity of β-lactamase was quantified in these isolates.
Results
We show that piperacillin/tazobactam resistance is induced in E. coli carrying blaTEM genes. This resistance is due to the increase in copy numbers and transcription levels of the blaTEM gene, thus increasing β-lactamase activity and consequently increasing piperacillin/tazobactam MICs. Genome sequencing of two blaTEM-carrying representative isolates showed that piperacillin/tazobactam treatment produced two types of duplications of blaTEM (8 and 60 copies, respectively). In the clinical setting, piperacillin/tazobactam treatment of patients infected by E. coli carrying blaTEM is associated with a risk of therapeutic failure.
Conclusions
This study describes for the first time the ESRI in E. coli. This new concept is very important in the understanding of the mechanism involved in the acquisition of resistance to BLs/BLIs.</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>beta-Lactamase Inhibitors - pharmacology</subject><subject>beta-Lactamases - analysis</subject><subject>beta-Lactamases - genetics</subject><subject>beta-Lactams - pharmacology</subject><subject>Drug Resistance, Multiple, Bacterial - genetics</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - genetics</subject><subject>Humans</subject><subject>Microbial Sensitivity Tests</subject><subject>Mutation</subject><subject>Phylogeny</subject><subject>Whole Genome Sequencing</subject><issn>0305-7453</issn><issn>1460-2091</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kMtKAzEUQIMoWh8bP0CyEaowNq9JO0uRqoWC4GM9ZJI7NJppapKpr7_yQ_wmR6pdurp3ce7hchA6pOSMkoIPHpUemKd3XvAN1KNCkoyRgm6iHuEkz4Yi5ztoN8ZHQojM5Wgb7XAqKS-k6KGP8WuCuQGTxQXoFNoGB4g2JjXXgJPHX5-ZUzqpJg7Wq4qA7XxmK5t8iLg_vrudnGBYercEg-vgG-z8S-ZgCW6tS3gc9QyC1TOrsPbO7qOtWrkIB79zDz1cju8vrrPpzdXk4nyaaU6HKROjiom6klVddO9XjLFcaspyo0aU5tRIXox0YbipKaOUyxyIMEZqoTTTouZ8D_VX3kXwzy3EVDY2anBOzcG3sWScyO5yyESHnq5QHXyMAepyEWyjwltJSfkTu-xil6vYHXz0622rBswa_avbAccrwLeL_0TfrHCKfQ</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Rodríguez-Villodres, Ángel</creator><creator>Gil-Marqués, María Luisa</creator><creator>Álvarez-Marín, Rocío</creator><creator>Bonnin, Rémy A</creator><creator>Pachón-Ibáñez, María Eugenia</creator><creator>Aguilar-Guisado, Manuela</creator><creator>Naas, Thierry</creator><creator>Aznar, Javier</creator><creator>Pachón, Jerónimo</creator><creator>Lepe, José Antonio</creator><creator>Smani, Younes</creator><general>Oxford University Press</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>7X8</scope><orcidid>https://orcid.org/0000-0002-2307-3232</orcidid><orcidid>https://orcid.org/0000-0001-9302-8384</orcidid></search><sort><creationdate>20200101</creationdate><title>Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli</title><author>Rodríguez-Villodres, Ángel ; Gil-Marqués, María Luisa ; Álvarez-Marín, Rocío ; Bonnin, Rémy A ; Pachón-Ibáñez, María Eugenia ; Aguilar-Guisado, Manuela ; Naas, Thierry ; Aznar, Javier ; Pachón, Jerónimo ; Lepe, José Antonio ; Smani, Younes</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c317t-48b24fb6bf9656b22256c125da81151d6398c9d3df1211365e04dd6c4ac2c4f33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Anti-Bacterial Agents - pharmacology</topic><topic>beta-Lactamase Inhibitors - pharmacology</topic><topic>beta-Lactamases - analysis</topic><topic>beta-Lactamases - genetics</topic><topic>beta-Lactams - pharmacology</topic><topic>Drug Resistance, Multiple, Bacterial - genetics</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - genetics</topic><topic>Humans</topic><topic>Microbial Sensitivity Tests</topic><topic>Mutation</topic><topic>Phylogeny</topic><topic>Whole Genome Sequencing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rodríguez-Villodres, Ángel</creatorcontrib><creatorcontrib>Gil-Marqués, María Luisa</creatorcontrib><creatorcontrib>Álvarez-Marín, Rocío</creatorcontrib><creatorcontrib>Bonnin, Rémy A</creatorcontrib><creatorcontrib>Pachón-Ibáñez, María Eugenia</creatorcontrib><creatorcontrib>Aguilar-Guisado, Manuela</creatorcontrib><creatorcontrib>Naas, Thierry</creatorcontrib><creatorcontrib>Aznar, Javier</creatorcontrib><creatorcontrib>Pachón, Jerónimo</creatorcontrib><creatorcontrib>Lepe, José Antonio</creatorcontrib><creatorcontrib>Smani, Younes</creatorcontrib><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><jtitle>Journal of antimicrobial chemotherapy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rodríguez-Villodres, Ángel</au><au>Gil-Marqués, María Luisa</au><au>Álvarez-Marín, Rocío</au><au>Bonnin, Rémy A</au><au>Pachón-Ibáñez, María Eugenia</au><au>Aguilar-Guisado, Manuela</au><au>Naas, Thierry</au><au>Aznar, Javier</au><au>Pachón, Jerónimo</au><au>Lepe, José Antonio</au><au>Smani, Younes</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli</atitle><jtitle>Journal of antimicrobial chemotherapy</jtitle><addtitle>J Antimicrob Chemother</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>75</volume><issue>1</issue><spage>77</spage><epage>85</epage><pages>77-85</pages><issn>0305-7453</issn><eissn>1460-2091</eissn><abstract>Abstract
Objectives
Escherichia coli is characterized by three resistance patterns to β-lactams/β-lactamase inhibitors (BLs/BLIs): (i) resistance to ampicillin/sulbactam and susceptibility to amoxicillin/clavulanic acid and piperacillin/tazobactam (RSS); (ii) resistance to ampicillin/sulbactam and amoxicillin/clavulanic acid, and susceptibility to piperacillin/tazobactam (RRS); and (iii) resistance to ampicillin/sulbactam, amoxicillin/clavulanic acid and piperacillin/tazobactam (RRR). These resistance patterns are acquired consecutively, indicating a potential risk of developing resistance to piperacillin/tazobactam, but the precise mechanism of this process is not completely understood.
Methods
Clinical isolates incrementally pressured by piperacillin/tazobactam selection in vitro and in vivo were used. We determined the MIC of piperacillin/tazobactam in the presence and absence of piperacillin/tazobactam pressure. We deciphered the role of the blaTEM genes in the new concept of extended-spectrum resistance to BLs/BLIs (ESRI) using genomic analysis. The activity of β-lactamase was quantified in these isolates.
Results
We show that piperacillin/tazobactam resistance is induced in E. coli carrying blaTEM genes. This resistance is due to the increase in copy numbers and transcription levels of the blaTEM gene, thus increasing β-lactamase activity and consequently increasing piperacillin/tazobactam MICs. Genome sequencing of two blaTEM-carrying representative isolates showed that piperacillin/tazobactam treatment produced two types of duplications of blaTEM (8 and 60 copies, respectively). In the clinical setting, piperacillin/tazobactam treatment of patients infected by E. coli carrying blaTEM is associated with a risk of therapeutic failure.
Conclusions
This study describes for the first time the ESRI in E. coli. This new concept is very important in the understanding of the mechanism involved in the acquisition of resistance to BLs/BLIs.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>31613964</pmid><doi>10.1093/jac/dkz393</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-2307-3232</orcidid><orcidid>https://orcid.org/0000-0001-9302-8384</orcidid></addata></record> |
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| ispartof | Journal of antimicrobial chemotherapy, 2020-01, Vol.75 (1), p.77-85 |
| issn | 0305-7453 1460-2091 |
| language | eng |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Anti-Bacterial Agents - pharmacology beta-Lactamase Inhibitors - pharmacology beta-Lactamases - analysis beta-Lactamases - genetics beta-Lactams - pharmacology Drug Resistance, Multiple, Bacterial - genetics Escherichia coli - drug effects Escherichia coli - genetics Humans Microbial Sensitivity Tests Mutation Phylogeny Whole Genome Sequencing |
| title | Extended-spectrum resistance to β-lactams/β-lactamase inhibitors (ESRI) evolved from low-level resistant Escherichia coli |
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