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Journal of Medical Microbiology logo Journal of Medical Microbiology

Volume 72, Issue 3

Emergence of carbapenem-resistant and clinical isolates with plasmids harbouring in Japan No Access

Abstract

The emergence of carbapenem-resistant species producing metallo-β-lactamase (MBL) has become a serious medical problem worldwide. IMP-type MBL was firstly detected in 1991 in Japan. Since then, it has become one of the most prevalent types of MBLs.

Avirulent species of , such as , function as reservoirs of drug resistance-associated genes encoding carbapenemases in clinical settings.

Active surveillance for carbapenem-resistant Gram-negative pathogens was conducted in 2019 at a hospital in Tokyo, Japan. Of the 543 samples screened for carbapenem-resistant isolates, 2 were species of . One was from a stool sample from a medical staff member, and the other was from a stool sample from a hospitalized patient.

Whole-genome sequencing showed that the former isolate was a strain of , and the latter was a strain of , a species close to . Both isolates were resistant to all carbapenems and harboured genes encoding IMP-1 MBL, which conferred resistance to carbapenems. The genes of and were located on the plasmids, pMRCP2, 323125 bp in size, and pMRCP1333, 16592 bp in size, respectively. The sequence of 82 % of pMRCP2 was 92 % similar to the sequence of a plasmid of PA83, whereas the sequence of 79 % of pMRCP1333 was >95 % similar to the sequence of a plasmid of FDAARGOS 162. The genomic environments surrounding the of pMRCP2 and pMRCP1333 differed completely from each other.

These results indicate that the two isolates acquired from different sources and that and function as vectors and reservoirs of carbapenem-resistant genes in hospitals.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): carbapenemase , IMP-1 metallo-β-lactamase , Pseudomonas alcaligenes and Pseudomonas paralcaligenes
Funding
This study was supported by the:
  • Institute for Fermentation (Award Y-2021-1-002)
    • Principle Award Recipient: MariTohya
  • the Japan Agency for Medical Research and Developmen (Award 21fk0108604h0701)
    • Principle Award Recipient: TeruoKirikae
  • Japan Society for the Promotion of Science (Award 22K15460)
    • Principle Award Recipient: MariTohya
  • Japan Society for the Promotion of Science (Award 20K16252)
    • Principle Award Recipient: TomomiHishinuma
  • Japan Society for the Promotion of Science
    • Principle Award Recipient: TeruoKirikae
  • Japan Society for the Promotion of Science (Award 19K16652)
    • Principle Award Recipient: MariTohya
© 2023 The Authors
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/content/journal/jmm/10.1099/jmm.0.001684
2023-03-23
2025-04-19
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References

  1. Nordmann P, Poirel L. Epidemiology and diagnostics of carbapenem resistance in gram-negative bacteria. Clin Infect Dis 2019; 69:S521–S528 [View Article] [PubMed]
     [Google Scholar]
  2. Queenan AM, Bush K. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 2007; 20:440–458 [View Article] [PubMed]
     [Google Scholar]
  3. Watanabe M, Iyobe S, Inoue M, Mitsuhashi S. Transferable imipenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1991; 35:147–151 [View Article] [PubMed]
     [Google Scholar]
  4. Sekiguchi J, Asagi T, Miyoshi-Akiyama T, Fujino T, Kobayashi I et al. Multidrug-resistant Pseudomonas aeruginosa strain that caused an outbreak in a neurosurgery ward and its aac(6’)-Iae gene cassette encoding a novel aminoglycoside acetyltransferase. Antimicrob Agents Chemother 2005; 49:3734–3742 [View Article] [PubMed]
     [Google Scholar]
  5. Sekiguchi J-I, Asagi T, Miyoshi-Akiyama T, Kasai A, Mizuguchi Y et al. Outbreaks of multidrug-resistant Pseudomonas aeruginosa in community hospitals in Japan. J Clin Microbiol 2007; 45:979–989 [View Article] [PubMed]
     [Google Scholar]
  6. Kirikae T, Mizuguchi Y, Arakawa Y. Investigation of isolation rates of Pseudomonas aeruginosa with and without multidrug resistance in medical facilities and clinical laboratories in Japan. J Antimicrob Chemother 2008; 61:612–615 [View Article] [PubMed]
     [Google Scholar]
  7. Lagatolla C, Tonin EA, Monti-Bragadin C, Dolzani L, Gombac F et al. Endemic carbapenem-resistant Pseudomonas aeruginosa with acquired metallo-beta-lactamase determinants in European hospital. Emerg Infect Dis 2004; 10:535–538 [View Article] [PubMed]
     [Google Scholar]
  8. Horcajada JP, Montero M, Oliver A, Sorlí L, Luque S et al. Epidemiology and treatment of multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa infections. Clin Microbiol Rev 2019; 32:e00031-19 [View Article] [PubMed]
     [Google Scholar]
  9. Suzuki M, Suzuki S, Matsui M, Hiraki Y, Kawano F et al. A subclass B3 metallo-β-lactamase found in Pseudomonas alcaligenes. J Antimicrob Chemother 2014; 69:1430–1432 [View Article] [PubMed]
     [Google Scholar]
  10. Tohya M, Tada T, Watanabe S, Kuwahara-Arai K, Zin KN et al. Emergence of carbapenem-resistant Pseudomonas asiatica producing NDM-1 and VIM-2 metallo-β-lactamases in Myanmar. Antimicrob Agents Chemother 2019; 63:e00475-19 [View Article] [PubMed]
     [Google Scholar]
  11. Koh TH, Wang GCY, Sng LH. IMP-1 and a novel metallo-beta-lactamase, VIM-6, in fluorescent pseudomonads isolated in Singapore. Antimicrob Agents Chemother 2004; 48:2334–2336 [View Article] [PubMed]
     [Google Scholar]
  12. Tohya M, Uechi K, Tada T, Hishinuma T, Kinjo T et al. Emergence of clinical isolates of Pseudomonas asiatica and Pseudomonas monteilii from Japan harbouring an acquired gene encoding a carbapenemase VIM-2. J Med Microbiol 2021; 70:10 [View Article] [PubMed]
     [Google Scholar]
  13. Holmgaard DB, Hansen F, Hasman H, Justesen US, Hammerum AM. Characterization of a novel blaIMP gene, blaIMP-58, using whole genome sequencing in a Pseudomonas putida isolate detected in Denmark. Diagn Microbiol Infect Dis 2017; 87:68–70 [View Article] [PubMed]
     [Google Scholar]
  14. Pan L, Li J, Wang R, Wang Y, Lin Q et al. Biosynthesis of polyhydroxyalkanoate from food waste oil by Pseudomonas alcaligenes with simultaneous energy recovery from fermentation wastewater. Waste Manag 2021; 131:268–276 [View Article] [PubMed]
     [Google Scholar]
  15. Valenstein P, Bardy GH, Cox CC, Zwadyk P. Pseudomonas alcaligenes endocarditis. Am J Clin Pathol 1983; 79:245–247 [View Article] [PubMed]
     [Google Scholar]
  16. Martino P, Micozzi A, Venditti M, Gentile G, Girmenia C et al. Catheter-related right-sided endocarditis in bone marrow transplant recipients. Rev Infect Dis 1990; 12:250–257 [View Article] [PubMed]
     [Google Scholar]
  17. Flores-Carrero A, Paniz-Mondolfi A, Araque M. Nosocomial bloodstream infection caused by Pseudomonas alcaligenes in a preterm neonate from Mérida, Venezuela. J Clin Neonatol 2016; 5:131 [View Article]
     [Google Scholar]
  18. Büchler AC, Wüthrich D, Jauslin MW, Egli A, Widmer AF. Nosocomial transmission of a blavim-2 carbapenemase integron between isolates of two different Pseudomonas species. Infect Control Hosp Epidemiol 2022; 43:245–247
     [Google Scholar]
  19. Ono E, Tohya M, Watanabe S, Tada T, Kuwahara-Arai K et al. Pseudomonas paralcaligenes sp. nov., isolated from a hospitalized patient. Int J Syst Evol Microbiol 2023; 73: [View Article] [PubMed]
     [Google Scholar]
  20. Kuwahara-Arai K, Morito A, Yanagisawa I, Hishinuma T, Mya S et al. Evaluation of a new selective agar medium for detection of carbapenem-resistant Enterobacteriaceae. Diagn Microbiol Infect Dis 2019; 95:114882 [View Article] [PubMed]
     [Google Scholar]
  21. Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing; 29th informational supplement. In CLSI Document M100-S29 Wayne, PA: Clinical and Laboratory Standards Institute; 2019
     [Google Scholar]
  22. Uechi K, Tada T, Shimada K, Kuwahara-Arai K, Arakaki M et al. A modified carbapenem inactivation method, CIMTris, for carbapenemase production in Acinetobacter and Pseudomonas species. J Clin Microbiol 2017; 55:3405–3410 [View Article] [PubMed]
     [Google Scholar]
  23. Uechi K, Tada T, Kuwahara-Arai K, Sekiguchi J-I, Yanagisawa I et al. An improved carbapenem inactivation method, CIMTrisII, for carbapenemase production by Gram-negative pathogens. J Med Microbiol 2019; 68:124–131 [View Article] [PubMed]
     [Google Scholar]
  24. Arakawa Y, Shibata N, Shibayama K, Kurokawa H, Yagi T et al. Convenient test for screening metallo-beta-lactamase-producing gram-negative bacteria by using thiol compounds. J Clin Microbiol 2000; 38:40–43 [View Article] [PubMed]
     [Google Scholar]
  25. Kitao T, Miyoshi-Akiyama T, Tanaka M, Narahara K, Shimojima M et al. Development of an immunochromatographic assay for diagnosing the production of IMP-type metallo-β-lactamases that mediate carbapenem resistance in Pseudomonas. J Microbiol Methods 2011; 87:330–337 [View Article] [PubMed]
     [Google Scholar]
  26. Tada T, Sekiguchi J-I, Watanabe S, Kuwahara-Arai K, Mizutani N et al. Assessment of a newly developed immunochromatographic assay for NDM-type metallo-β-lactamase producing Gram-negative pathogens in Myanmar. BMC Infect Dis 2019; 19:565 [View Article] [PubMed]
     [Google Scholar]
  27. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  28. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 2005; 102:2567–2572 [View Article] [PubMed]
     [Google Scholar]
  29. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  30. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  31. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
     [Google Scholar]
  32. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
     [Google Scholar]
  33. Tanizawa Y, Fujisawa T, Kaminuma E, Nakamura Y, Arita M. DFAST and DAGA: web-based integrated genome annotation tools and resources. Biosci Microbiota Food Health 2016; 35:173–184 [View Article] [PubMed]
     [Google Scholar]
  34. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018; 34:1037–1039 [View Article] [PubMed]
     [Google Scholar]
  35. Xiong J, Alexander DC, Ma JH, Déraspe M, Low DE et al. Complete sequence of pOZ176, a 500-kilobase IncP-2 plasmid encoding IMP-9-mediated carbapenem resistance, from outbreak isolate Pseudomonas aeruginosa 96. Antimicrob Agents Chemother 2013; 57:3775–3782 [View Article] [PubMed]
     [Google Scholar]
  36. Janice J, Agyepong N, Owusu-Ofori A, Govinden U, Essack SY et al. Carbapenem resistance determinants acquired through novel chromosomal integrations in extensively drug-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother 2021; 65:e0028921 [View Article] [PubMed]
     [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001684
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Emergence of carbapenem-resistant Pseudomonas alcaligenes and Pseudomonas paralcaligenes clinical isolates with plasmids harbouring blaIMP-1 in Japan
J. Med. Microbiol. 72, 001684 (2023); https://doi.org/10.1099/jmm.0.001684
/content/journal/jmm/10.1099/jmm.0.001684
/content/journal/jmm/10.1099/jmm.0.001684
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