Geographical distribution of Enterobacterales with a carbapenemase IMP-6 phenotype and its association with antimicrobial use: An analysis using comprehensive national surveillance data on antimicrobial resistance
Enterobacterales resistant to carbapenems, a class of last-resort antimicrobials, are ranked as an "urgent" and "critical" public health hazard by CDC and WHO. IMP-type carbapenemase-containing Enterobacterales are endemic in Japan, and blaIMP-6 is one of the notable carbapenemas...
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| Veröffentlicht in: | PloS one 2020-12, Vol.15 (12), p.e0243630-e0243630 |
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| creator | Hirabayashi, Aki Yahara, Koji Kajihara, Toshiki Sugai, Motoyuki Shibayama, Keigo |
| description | Enterobacterales resistant to carbapenems, a class of last-resort antimicrobials, are ranked as an "urgent" and "critical" public health hazard by CDC and WHO. IMP-type carbapenemase-containing Enterobacterales are endemic in Japan, and blaIMP-6 is one of the notable carbapenemase genes responsible for the resistance. The gene is plasmid-encoded and confers resistance to meropenem, but not to imipenem. Therefore, IMP-6-producing Enterobacterales isolates are occasionally overlooked in clinical laboratories and are referred to as 'stealth-type'. Since previous reports in Japan were confined only to some geographical regions, their distribution across prefectures and the factors affecting the distribution remain unclear. Here, we revealed the dynamics of the geographical distribution of Enterobacterales with IMP-6 phenotype associated with antimicrobial use in Japan. We utilized comprehensive national surveillance data of all routine bacteriological test results from more than 1,400 hospitals in 2015 and 2016 to enumerate Escherichia coli and Klebsiella pneumoniae isolates with the antimicrobial susceptibility pattern (phenotype) characteristic of IMP-6 (imipenem susceptible, meropenem resistant), and to tabulate the frequency of isolates with the phenotype for each prefecture. Isolates were detected in approximately half of all prefectures, and combined analysis with the national data of antimicrobial usage revealed a statistically significant association between the frequency and usage of not carbapenems but third-generation cephalosporins (p = 0.006, logistic mixed-effect regression) and a weaker association between the frequency and usage of fluoroquinolones (p = 0.043). The usage of third-generation cephalosporins and fluoroquinolones may select the strains with the IMP-6 phenotype, and contribute to their occasional spread. We expect the findings will promote antimicrobial stewardship to reduce the spread of the notable carbapenemase gene. |
| doi_str_mv | 10.1371/journal.pone.0243630 |
| format | Article |
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IMP-type carbapenemase-containing Enterobacterales are endemic in Japan, and blaIMP-6 is one of the notable carbapenemase genes responsible for the resistance. The gene is plasmid-encoded and confers resistance to meropenem, but not to imipenem. Therefore, IMP-6-producing Enterobacterales isolates are occasionally overlooked in clinical laboratories and are referred to as 'stealth-type'. Since previous reports in Japan were confined only to some geographical regions, their distribution across prefectures and the factors affecting the distribution remain unclear. Here, we revealed the dynamics of the geographical distribution of Enterobacterales with IMP-6 phenotype associated with antimicrobial use in Japan. We utilized comprehensive national surveillance data of all routine bacteriological test results from more than 1,400 hospitals in 2015 and 2016 to enumerate Escherichia coli and Klebsiella pneumoniae isolates with the antimicrobial susceptibility pattern (phenotype) characteristic of IMP-6 (imipenem susceptible, meropenem resistant), and to tabulate the frequency of isolates with the phenotype for each prefecture. Isolates were detected in approximately half of all prefectures, and combined analysis with the national data of antimicrobial usage revealed a statistically significant association between the frequency and usage of not carbapenems but third-generation cephalosporins (p = 0.006, logistic mixed-effect regression) and a weaker association between the frequency and usage of fluoroquinolones (p = 0.043). The usage of third-generation cephalosporins and fluoroquinolones may select the strains with the IMP-6 phenotype, and contribute to their occasional spread. We expect the findings will promote antimicrobial stewardship to reduce the spread of the notable carbapenemase gene.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0243630</identifier><identifier>PMID: 33332370</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anti-Bacterial Agents - pharmacology ; Anti-Bacterial Agents - therapeutic use ; Antibiotics ; Antimicrobial agents ; Antimicrobial resistance ; Asymptomatic ; Bacteria ; Bacterial infections ; Bacterial Proteins - genetics ; beta-Lactamases - genetics ; Biology and Life Sciences ; Carbapenemase ; Carbapenems ; Carbapenems - pharmacology ; Carbapenems - therapeutic use ; Cephalosporins ; Distribution ; Drug resistance ; Drug resistance in microorganisms ; Drug Resistance, Bacterial ; Drug therapy ; E coli ; Earth Sciences ; Enterobacter ; Enterobacterales ; Enterobacteriaceae ; Enterobacteriaceae - drug effects ; Enterobacteriaceae - genetics ; Enterobacteriaceae infections ; Enterobacteriaceae Infections - drug therapy ; Enterobacteriaceae Infections - epidemiology ; Enterobacteriaceae Infections - microbiology ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Escherichia coli Infections - drug therapy ; Escherichia coli Infections - epidemiology ; Escherichia coli Infections - microbiology ; Fluoroquinolones ; Genes ; Genetic aspects ; Genotype & phenotype ; Geographical distribution ; Health aspects ; Health hazards ; Hospitals ; Humans ; Imipenem ; Imipenem - pharmacology ; Imipenem - therapeutic use ; Infectious diseases ; Japan - epidemiology ; Klebsiella ; Klebsiella Infections - drug therapy ; Klebsiella Infections - epidemiology ; Klebsiella Infections - microbiology ; Klebsiella pneumoniae - drug effects ; Klebsiella pneumoniae - genetics ; Medical laboratories ; Medicine and Health Sciences ; Meropenem ; Meropenem - pharmacology ; Meropenem - therapeutic use ; Nosocomial infections ; People and Places ; Phenotype ; Phenotypes ; Physiological aspects ; Plasmids ; Public health ; Regression analysis ; Statistical analysis ; Surveillance</subject><ispartof>PloS one, 2020-12, Vol.15 (12), p.e0243630-e0243630</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Hirabayashi 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. 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We utilized comprehensive national surveillance data of all routine bacteriological test results from more than 1,400 hospitals in 2015 and 2016 to enumerate Escherichia coli and Klebsiella pneumoniae isolates with the antimicrobial susceptibility pattern (phenotype) characteristic of IMP-6 (imipenem susceptible, meropenem resistant), and to tabulate the frequency of isolates with the phenotype for each prefecture. Isolates were detected in approximately half of all prefectures, and combined analysis with the national data of antimicrobial usage revealed a statistically significant association between the frequency and usage of not carbapenems but third-generation cephalosporins (p = 0.006, logistic mixed-effect regression) and a weaker association between the frequency and usage of fluoroquinolones (p = 0.043). The usage of third-generation cephalosporins and fluoroquinolones may select the strains with the IMP-6 phenotype, and contribute to their occasional spread. 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drug effects</topic><topic>Klebsiella pneumoniae - genetics</topic><topic>Medical laboratories</topic><topic>Medicine and Health Sciences</topic><topic>Meropenem</topic><topic>Meropenem - pharmacology</topic><topic>Meropenem - therapeutic use</topic><topic>Nosocomial infections</topic><topic>People and Places</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Physiological aspects</topic><topic>Plasmids</topic><topic>Public health</topic><topic>Regression analysis</topic><topic>Statistical analysis</topic><topic>Surveillance</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hirabayashi, Aki</creatorcontrib><creatorcontrib>Yahara, Koji</creatorcontrib><creatorcontrib>Kajihara, Toshiki</creatorcontrib><creatorcontrib>Sugai, Motoyuki</creatorcontrib><creatorcontrib>Shibayama, Keigo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hirabayashi, Aki</au><au>Yahara, Koji</au><au>Kajihara, Toshiki</au><au>Sugai, Motoyuki</au><au>Shibayama, Keigo</au><au>Karunasagar, Iddya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Geographical distribution of Enterobacterales with a carbapenemase IMP-6 phenotype and its association with antimicrobial use: An analysis using comprehensive national surveillance data on antimicrobial resistance</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-12-17</date><risdate>2020</risdate><volume>15</volume><issue>12</issue><spage>e0243630</spage><epage>e0243630</epage><pages>e0243630-e0243630</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Enterobacterales resistant to carbapenems, a class of last-resort antimicrobials, are ranked as an "urgent" and "critical" public health hazard by CDC and WHO. IMP-type carbapenemase-containing Enterobacterales are endemic in Japan, and blaIMP-6 is one of the notable carbapenemase genes responsible for the resistance. The gene is plasmid-encoded and confers resistance to meropenem, but not to imipenem. Therefore, IMP-6-producing Enterobacterales isolates are occasionally overlooked in clinical laboratories and are referred to as 'stealth-type'. Since previous reports in Japan were confined only to some geographical regions, their distribution across prefectures and the factors affecting the distribution remain unclear. Here, we revealed the dynamics of the geographical distribution of Enterobacterales with IMP-6 phenotype associated with antimicrobial use in Japan. We utilized comprehensive national surveillance data of all routine bacteriological test results from more than 1,400 hospitals in 2015 and 2016 to enumerate Escherichia coli and Klebsiella pneumoniae isolates with the antimicrobial susceptibility pattern (phenotype) characteristic of IMP-6 (imipenem susceptible, meropenem resistant), and to tabulate the frequency of isolates with the phenotype for each prefecture. Isolates were detected in approximately half of all prefectures, and combined analysis with the national data of antimicrobial usage revealed a statistically significant association between the frequency and usage of not carbapenems but third-generation cephalosporins (p = 0.006, logistic mixed-effect regression) and a weaker association between the frequency and usage of fluoroquinolones (p = 0.043). The usage of third-generation cephalosporins and fluoroquinolones may select the strains with the IMP-6 phenotype, and contribute to their occasional spread. We expect the findings will promote antimicrobial stewardship to reduce the spread of the notable carbapenemase gene.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33332370</pmid><doi>10.1371/journal.pone.0243630</doi><tpages>e0243630</tpages><orcidid>https://orcid.org/0000-0003-3115-0645</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2020-12, Vol.15 (12), p.e0243630-e0243630 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2470907109 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Antibiotics Antimicrobial agents Antimicrobial resistance Asymptomatic Bacteria Bacterial infections Bacterial Proteins - genetics beta-Lactamases - genetics Biology and Life Sciences Carbapenemase Carbapenems Carbapenems - pharmacology Carbapenems - therapeutic use Cephalosporins Distribution Drug resistance Drug resistance in microorganisms Drug Resistance, Bacterial Drug therapy E coli Earth Sciences Enterobacter Enterobacterales Enterobacteriaceae Enterobacteriaceae - drug effects Enterobacteriaceae - genetics Enterobacteriaceae infections Enterobacteriaceae Infections - drug therapy Enterobacteriaceae Infections - epidemiology Enterobacteriaceae Infections - microbiology Escherichia coli - drug effects Escherichia coli - genetics Escherichia coli Infections - drug therapy Escherichia coli Infections - epidemiology Escherichia coli Infections - microbiology Fluoroquinolones Genes Genetic aspects Genotype & phenotype Geographical distribution Health aspects Health hazards Hospitals Humans Imipenem Imipenem - pharmacology Imipenem - therapeutic use Infectious diseases Japan - epidemiology Klebsiella Klebsiella Infections - drug therapy Klebsiella Infections - epidemiology Klebsiella Infections - microbiology Klebsiella pneumoniae - drug effects Klebsiella pneumoniae - genetics Medical laboratories Medicine and Health Sciences Meropenem Meropenem - pharmacology Meropenem - therapeutic use Nosocomial infections People and Places Phenotype Phenotypes Physiological aspects Plasmids Public health Regression analysis Statistical analysis Surveillance |
| title | Geographical distribution of Enterobacterales with a carbapenemase IMP-6 phenotype and its association with antimicrobial use: An analysis using comprehensive national surveillance data on antimicrobial resistance |
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