National genomic surveillance integrating standardized quantitative susceptibility testing clarifies antimicrobial resistance in Enterobacterales

Shizuo Kayama (), Koji Yahara (), Yo Sugawara (), Sayoko Kawakami, Kohei Kondo, Hui Zuo, Shoko Kutsuno, Norikazu Kitamura, Aki Hirabayashi, Toshiki Kajihara, Hitomi Kurosu, Liansheng Yu, Masato Suzuki, Junzo Hisatsune and Motoyuki Sugai ()
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Shizuo Kayama: National Institute of Infectious Diseases
Koji Yahara: National Institute of Infectious Diseases
Yo Sugawara: National Institute of Infectious Diseases
Sayoko Kawakami: National Institute of Infectious Diseases
Kohei Kondo: National Institute of Infectious Diseases
Hui Zuo: National Institute of Infectious Diseases
Shoko Kutsuno: National Institute of Infectious Diseases
Norikazu Kitamura: National Institute of Infectious Diseases
Aki Hirabayashi: National Institute of Infectious Diseases
Toshiki Kajihara: National Institute of Infectious Diseases
Hitomi Kurosu: National Institute of Infectious Diseases
Liansheng Yu: National Institute of Infectious Diseases
Masato Suzuki: National Institute of Infectious Diseases
Junzo Hisatsune: National Institute of Infectious Diseases
Motoyuki Sugai: National Institute of Infectious Diseases

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Antimicrobial resistance is a global health concern; Enterobacterales resistant to third-generation cephalosporins (3GCs) and carbapenems are of the highest priority. Here, we conducted genome sequencing and standardized quantitative antimicrobial susceptibility testing of 4,195 isolates of Escherichia coli and Klebsiella pneumoniae resistant to 3GCs and Enterobacterales with reduced meropenem susceptibility collected across Japan. Our analyses provided a complete classification of 3GC resistance mechanisms. Analyses with complete reference plasmids revealed that among the blaCTX-M extended-spectrum β-lactamase genes, blaCTX-M-8 was typically encoded in highly similar plasmids. The two major AmpC β-lactamase genes were blaCMY-2 and blaDHA-1. Long-read sequencing of representative plasmids revealed that approximately 60% and 40% of blaCMY-2 and blaDHA-1 were encoded by such plasmids, respectively. Our analyses identified strains positive for carbapenemase genes but phenotypically susceptible to carbapenems and undetectable by standard antimicrobial susceptibility testing. Systematic long-read sequencing enabled reconstruction of 183 complete plasmid sequences encoding three major carbapenemase genes and elucidation of their geographical distribution stratified by replicon types and species carrying the plasmids and potential plasmid transfer events. Overall, we provide a blueprint for a national genomic surveillance study that integrates standardized quantitative antimicrobial susceptibility testing and characterizes resistance determinants.

Date: 2023
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DOI: 10.1038/s41467-023-43516-4

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