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Mechanisms of Resistance

Role of TEM-1 β-Lactamase in the Predominance of Ampicillin-Sulbactam-Nonsusceptible Escherichia coli in Japan

Taro Noguchi, Yasufumi Matsumura, Toru Kanahashi, Michio Tanaka, Yasuhiro Tsuchido, Takuro Matsumura, Satoshi Nakano, Masaki Yamamoto, Miki Nagao, Satoshi Ichiyama
Taro Noguchi
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Yasufumi Matsumura
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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  • ORCID record for Yasufumi Matsumura
Toru Kanahashi
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Michio Tanaka
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Yasuhiro Tsuchido
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Takuro Matsumura
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Satoshi Nakano
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Masaki Yamamoto
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Miki Nagao
Department of Clinical Laboratory Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
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Satoshi Ichiyama
Shiga General Hospital, Shiga, Japan
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DOI: 10.1128/AAC.02366-18
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ABSTRACT

We investigated the epidemiology and resistance mechanisms of ampicillin-sulbactam-nonsusceptible Escherichia coli, focusing on the role of the TEM-1 β-lactamase. We collected all nonduplicate E. coli clinical isolates at 10 Japanese hospitals during December 2014 and examined their antimicrobial susceptibility, β-lactamases, TEM-1 transferability, TEM-1 β-lactamase activity, outer membrane protein profile, membrane permeability, and clonal genotypes. Among the 329 isolates collected, 95 were ampicillin-sulbactam nonsusceptible. Of these ampicillin-sulbactam-nonsusceptible isolates, β-lactamases conferring resistance to sulbactam, such as AmpC, were present in 33%. Hyperproduction of sulbactam-susceptible β-lactamases, TEMs with a strong promoter, were rare (5%). The remaining 59 isolates (62%) had only sulbactam-susceptible β-lactamases, including TEM-1 with a wild-type promoter (n = 28), CTX-Ms (n = 13), or both (n = 17). All 45 transconjugants from 96 donors with TEM-1 had higher ampicillin-sulbactam MICs (4 to 96 mg/liter) than the recipient (2 mg/liter). In donors with only TEM-1, TEM-1 activity correlated with the 50% inhibitory concentration of sulbactam and ampicillin-sulbactam MICs. The decreased membrane permeation of sulbactam was associated with an increased ampicillin-sulbactam MIC. The reduced permeation was partly attributable to deficient outer membrane proteins, which were observed in 57% of the ampicillin-sulbactam-nonsusceptible isolates with only TEM-1 and a wild-type promoter. Sequence type 131 (ST131) was the most common clonal type (52%). TEM-1 with a wild-type promoter primarily contributed to ampicillin-sulbactam nonsusceptibility in E. coli, with the partial support of other mechanisms, such as reduced permeation. Conjugative TEM-1 and the clonal spread of ST131 may contribute to the prevalence of Japanese ampicillin-sulbactam-nonsusceptible isolates.

FOOTNOTES

    • Received 6 November 2018.
    • Accepted 7 November 2018.
    • Accepted manuscript posted online 19 November 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AAC.02366-18.

  • Copyright © 2019 American Society for Microbiology.

All Rights Reserved.

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Role of TEM-1 β-Lactamase in the Predominance of Ampicillin-Sulbactam-Nonsusceptible Escherichia coli in Japan
Taro Noguchi, Yasufumi Matsumura, Toru Kanahashi, Michio Tanaka, Yasuhiro Tsuchido, Takuro Matsumura, Satoshi Nakano, Masaki Yamamoto, Miki Nagao, Satoshi Ichiyama
Antimicrobial Agents and Chemotherapy Jan 2019, 63 (2) e02366-18; DOI: 10.1128/AAC.02366-18

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Role of TEM-1 β-Lactamase in the Predominance of Ampicillin-Sulbactam-Nonsusceptible Escherichia coli in Japan
Taro Noguchi, Yasufumi Matsumura, Toru Kanahashi, Michio Tanaka, Yasuhiro Tsuchido, Takuro Matsumura, Satoshi Nakano, Masaki Yamamoto, Miki Nagao, Satoshi Ichiyama
Antimicrobial Agents and Chemotherapy Jan 2019, 63 (2) e02366-18; DOI: 10.1128/AAC.02366-18
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KEYWORDS

Escherichia coli
TEM-1
ampicillin-sulbactam

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