Genetic relatedness of third-generation cephalosporin-resistant Escherichia coli among livestock, farmers, and patients in Japan

Ryuichi Nakano; Akiyo Nakano; Ryuji Nishisouzu; Kenji Hikosaka; Yuki Suzuki; Go Kamoshida; Shigeru Tansho-Nagakawa; Shiro Endo; Kei Kasahara; Yasuo Ono; Hisakazu Yano

doi:10.1016/j.onehlt.2023.100524

Genetic relatedness of third-generation cephalosporin-resistant Escherichia coli among livestock, farmers, and patients in Japan

One Health. 2023 Mar 9:16:100524. doi: 10.1016/j.onehlt.2023.100524. eCollection 2023 Jun.

Authors

Affiliations

¹ Department of Microbiology and Infectious Diseases, Nara Medical University, 840 Shijo-cho, Kashihara-shi, Nara 634-8521, Japan.
² Soo High School Kagoshima, 6080 Ninokata, Sueyoshi-cho, Soo-shi, Kagoshima 899-8605, Japan.
³ Department of Infection and Host Defense, Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan.
⁴ Department of Microbiology and Infection Control Sciences, Kyoto Pharmaceutical University, 5 Misasaginakauchi-cho, Yamashina-ku, Kyoto 607-8414, Japan.
⁵ Department of Microbiology and Immunology, Teikyo University School of Medicine, 2-11-1 Kaga, Itabashi-ku, Tokyo 173-8605, Japan.
⁶ Division of Infectious Diseases, Tohoku Medical and Pharmaceutical University Hospital, Sendai-shi, Miyagi 983-8512, Japan.
⁷ Center of Infectious Diseases, Nara Medical University, 840 Shijo-cho, Kashihara-shi, Nara 634-8521, Japan.

Abstract

Objectives: The third-generation cephalosporin (3GC)-resistant E. coli strains have been detected worldwide in humans and animals. Hence, in this study, we evaluated the prevalence and genetic characteristics of 3GC-resistant E. coli in livestock, farmers, and patients to further analyse if livestock serves as a potential reservoir of antimicrobial-resistant bacteria.

Methods: Faecal samples were collected from 330 healthy livestock (216 cattle and 114 swine), 61 healthy livestock farmers (52 cattle farmers and 9 swine farmers), and 68 non-duplicate 3GC-resistant E. coli isolates were also obtained from the clinical specimens of patients in Japan between 2013 and 2015. Genes associated with resistance in 3GC-resistant E. coli were identified using polymerase chain reaction (PCR) and DNA sequencing. Genotypic diversity was determined by multilocus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE).

Results: We obtained 39 and 17 non-duplicated 3GC-resistant E. coli strains from healthy livestock (33 cattle and six swine) and livestock farmers, respectively. All isolates carried either CTX-M-type extended-spectrum β-lactamase or plasmid-mediated AmpC β-lactamase genes, with CTX-M-14 being the most frequent. CTX-M producers from livestock and patients belonged to 22 and 19 different sequence types (STs), respectively, and only three STs were the same. Among the 3GC-resistant E. coli from livestock and farmers, three types of CTX-M producers have shown similar characteristics (CTX-M genotype, ST, PFGE patterns, and antimicrobial susceptibilities) and were identified as clonal isolates shared among their farms.

Conclusions: Our study findings indicate that CTX-M-14 is predominant in Japan. No distinct relationship was observed between the 3GC-resistant E. coli isolated from livestock and patients; however, some clonal relatedness was observed between the isolates from livestock and farmers due to their close contact.

Keywords: CTX-M β-lactamase; Escherichia coli; Farmers; Genotype; Livestock.