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      Emergence of carbapenem-resistant and colistin-susceptible Enterobacter cloacae complex co-harboring bla IMP-1 and mcr-9 in Japan

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          Abstract

          Background

          The spread of Enterobacteriaceae producing both carbapenemases and Mcr, encoded by plasmid-mediated colistin resistance genes, has become a serious public health problem worldwide. This study describes three clinical isolates of Enterobacter cloacae complex co-harboring bla IMP-1 and mcr-9 that were resistant to carbapenem but susceptible to colistin.

          Methods

          Thirty-two clinical isolates of E. cloacae complex non-susceptible to carbapenems were obtained from patients at 14 hospitals in Japan. Their minimum inhibitory concentrations (MICs) were determined by broth microdilution methods and E-tests. Their entire genomes were sequenced by MiSeq and MinION methods. Multilocus sequence types were determined and a phylogenetic tree constructed by single nucleotide polymorphism (SNP) alignment of whole genome sequencing data.

          Results

          All 32 isolates showed MICs of ≥2 μg/ml for imipenem and/or meropenem. Whole-genome analysis revealed that all these isolates harbored bla IMP-1, with three also harboring mcr-9. These three isolates showed low MICs of 0.125 μg/ml for colistin. In two of these isolates, bla IMP-1 and mcr-9 were present on two separate plasmids, of sizes 62 kb and 280/290 kb, respectively. These two isolates did not possess a qseBC gene encoding a two-component system, which is thought to regulate the expression of mcr-9. In the third isolate, however, both bla IMP-1 and mcr-9 were present on the chromosome.

          Conclusion

          The mcr-9 is silently distributed among carbapenem-resistant E. cloacae complex isolates, of which are emerging in hospitals in Japan. To our knowledge, this is the first report of isolates of E. cloacae complex harboring both bla IMP-1 and mcr-9 in Japan.

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          Most cited references23

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          Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections.

          The emergence of multidrug-resistant gram-negative bacteria and the lack of new antibiotics to combat them have led to the revival of polymyxins, an old class of cationic, cyclic polypeptide antibiotics. Polymyxin B and polymyxin E (colistin) are the 2 polymyxins used in clinical practice. Most of the reintroduction of polymyxins during the last few years is related to colistin. The polymyxins are active against selected gram-negative bacteria, including Acinetobacter species, Pseudomonas aeruginosa, Klebsiella species, and Enterobacter species. These drugs have been used extensively worldwide for decades for local use. However, parenteral use of these drugs was abandoned approximately 20 years ago in most countries, except for treatment of patients with cystic fibrosis, because of reports of common and serious nephrotoxicity and neurotoxicity. Recent studies of patients who received intravenous polymyxins for the treatment of serious P. aeruginosa and Acinetobacter baumannii infections of various types, including pneumonia, bacteremia, and urinary tract infections, have led to the conclusion that these antibiotics have acceptable effectiveness and considerably less toxicity than was reported in old studies.
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            The difficult-to-control spread of carbapenemase producers among Enterobacteriaceae worldwide.

            The spread of carbapenemase producers in Enterobacteriaceae has now been identified worldwide. Three main carbapenemases have been reported; they belong to three classes of β-lactamases, which are KPC, NDM, and OXA-48. The main reservoirs of KPC are Klebsiella pneumoniae in the USA, Israel, Greece, and Italy, those of NDM are K. pneumoniae and Escherichia coli in the Indian subcontinent, and those of OXA-48 are K. pneumoniae and Escherichia coli in North Africa and Turkey. KPC producers have been mostly identified among nosocomial isolates, whereas NDM and OXA-48 producers are both nosocomial and community-acquired pathogens. Control of their spread is still possible in hospital settings, and relies on the use of rapid diagnostic techniques and the strict implemention of hygiene measures.
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              Resistance to polymyxins in Gram-negative organisms.

              Polymyxins have recently been re-introduced into the therapeutic arsenal to combat infections caused by multidrug-resistant Gram-negative bacteria. However, the emergence of strains resistant to these last-resort drugs is becoming a critical issue in a growing number of countries. Both intrinsic and transferable mechanisms of polymyxin resistance have been characterised. These mechanisms as well as the epidemiological data regarding four relevant bacterial pathogens (Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii and Pseudomonas aeruginosa) are considered in this review. A special focus is made on plasmid-mediated resistance and the spread of mcr genes.
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                Author and article information

                Contributors
                k.pegah.sw@juntendo.ac.jp
                s.oshiro.zt@juntendo.ac.jp
                snwatana@juntendo.ac.jp
                med2117016@stud.juntendo.ac.jp
                kkuwa@juntendo.ac.jp
                masahiro_shimojima@bml.co.jp
                miho-o@blm.co.jp
                t-tada@juntendo.ac.jp
                t-kirikae@juntendo.ac.jp
                Journal
                BMC Infect Dis
                BMC Infect. Dis
                BMC Infectious Diseases
                BioMed Central (London )
                1471-2334
                16 April 2020
                16 April 2020
                2020
                : 20
                : 282
                Affiliations
                [1 ]GRID grid.258269.2, ISNI 0000 0004 1762 2738, Department of Microbiology, , Juntendo University Graduate School of Medicine, ; 2-1-1 Hongo, Bunkyo-ku, Tokyo, 113-8421 Japan
                [2 ]GRID grid.410848.1, BML, Inc Department of Microbiology, ; Kawagoe, Saitama, Japan
                Article
                5021
                10.1186/s12879-020-05021-7
                7161257
                32299378
                7460b1d2-4fc1-4029-934d-74419d473bc9
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 15 January 2020
                : 8 April 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 18K07120
                Award ID: 18K07121
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100009619, Japan Agency for Medical Research and Development;
                Award ID: 19fk0108061h0302
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007676, Asahi Group Holdings;
                Award ID: AM227CH501
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100005731, Juntendo University;
                Award ID: 6119002
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Infectious disease & Microbiology
                enterobacter cloacae complex,e. xiangfangensis,e. asburiae,mcr-9,blaimp-1,carbapenem resistance,colistin resistance

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