Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan

We investigated the prevalence of livestock-associated methicillin-resistant <i>Staphylococcus aureus</i> (LA-MRSA) in pig slaughterhouses from 2018 to 2022 in Japan and the isolates were examined for antimicrobial susceptibility and genetic characteristics by whole-genome analysis. Alth...

Full description

Bibliographic Details
Main Authors: Michiko Kawanishi, Mari Matsuda, Hitoshi Abo, Manao Ozawa, Yuta Hosoi, Yukari Hiraoka, Saki Harada, Mio Kumakawa, Hideto Sekiguchi
Format: Article
Language:English
Published: MDPI AG 2024-02-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/13/2/155
_version_ 1797299068866658304
author Michiko Kawanishi
Mari Matsuda
Hitoshi Abo
Manao Ozawa
Yuta Hosoi
Yukari Hiraoka
Saki Harada
Mio Kumakawa
Hideto Sekiguchi
author_facet Michiko Kawanishi
Mari Matsuda
Hitoshi Abo
Manao Ozawa
Yuta Hosoi
Yukari Hiraoka
Saki Harada
Mio Kumakawa
Hideto Sekiguchi
author_sort Michiko Kawanishi
collection DOAJ
description We investigated the prevalence of livestock-associated methicillin-resistant <i>Staphylococcus aureus</i> (LA-MRSA) in pig slaughterhouses from 2018 to 2022 in Japan and the isolates were examined for antimicrobial susceptibility and genetic characteristics by whole-genome analysis. Although the positive LA-MRSA rates on farms (29.6%) and samples (9.9%) in 2022 in Japan remained lower than those observed in European countries exhibiting extremely high rates of confirmed human LA-MRSA infections, these rates showed a gradually increasing trend over five years. The ST398/t034 strain was predominant, followed by ST5/t002, and differences were identified between ST398 and ST5 in terms of antimicrobial susceptibility and the resistance genes carried. Notably, LA-MRSA possessed resistance genes toward many antimicrobial classes, with 91.4% of the ST398 strains harboring zinc resistance genes. These findings indicate that the co-selection pressure associated with multidrug and zinc resistance may have contributed markedly to LA-MRSA persistence. SNP analysis revealed that ST398 and ST5 of swine origin were classified into a different cluster of MRSA from humans, showing the same ST in Japan and lacking the immune evasion genes (<i>scn</i>, <i>sak</i>, or <i>chp</i>). Although swine-origin LA-MRSA is currently unlikely to spread to humans and become a problem in current clinical practice, preventing its dissemination requires using antimicrobials prudently, limiting zinc utilization to the minimum required nutrient, and practicing fundamental hygiene measures.
first_indexed 2024-03-07T22:44:12Z
format Article
id doaj.art-0bffff761f784b608cd57d2ff109747e
institution Directory Open Access Journal
issn 2079-6382
language English
last_indexed 2024-03-07T22:44:12Z
publishDate 2024-02-01
publisher MDPI AG
record_format Article
series Antibiotics
spelling doaj.art-0bffff761f784b608cd57d2ff109747e2024-02-23T15:05:06ZengMDPI AGAntibiotics2079-63822024-02-0113215510.3390/antibiotics13020155Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in JapanMichiko Kawanishi0Mari Matsuda1Hitoshi Abo2Manao Ozawa3Yuta Hosoi4Yukari Hiraoka5Saki Harada6Mio Kumakawa7Hideto Sekiguchi8Veterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanVeterinary AMR Center, National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, Tokyo 185-8511, JapanWe investigated the prevalence of livestock-associated methicillin-resistant <i>Staphylococcus aureus</i> (LA-MRSA) in pig slaughterhouses from 2018 to 2022 in Japan and the isolates were examined for antimicrobial susceptibility and genetic characteristics by whole-genome analysis. Although the positive LA-MRSA rates on farms (29.6%) and samples (9.9%) in 2022 in Japan remained lower than those observed in European countries exhibiting extremely high rates of confirmed human LA-MRSA infections, these rates showed a gradually increasing trend over five years. The ST398/t034 strain was predominant, followed by ST5/t002, and differences were identified between ST398 and ST5 in terms of antimicrobial susceptibility and the resistance genes carried. Notably, LA-MRSA possessed resistance genes toward many antimicrobial classes, with 91.4% of the ST398 strains harboring zinc resistance genes. These findings indicate that the co-selection pressure associated with multidrug and zinc resistance may have contributed markedly to LA-MRSA persistence. SNP analysis revealed that ST398 and ST5 of swine origin were classified into a different cluster of MRSA from humans, showing the same ST in Japan and lacking the immune evasion genes (<i>scn</i>, <i>sak</i>, or <i>chp</i>). Although swine-origin LA-MRSA is currently unlikely to spread to humans and become a problem in current clinical practice, preventing its dissemination requires using antimicrobials prudently, limiting zinc utilization to the minimum required nutrient, and practicing fundamental hygiene measures.https://www.mdpi.com/2079-6382/13/2/155LA-MRSAST398ST8antimicrobial resistancezinc resistanceSNP analysis
spellingShingle Michiko Kawanishi
Mari Matsuda
Hitoshi Abo
Manao Ozawa
Yuta Hosoi
Yukari Hiraoka
Saki Harada
Mio Kumakawa
Hideto Sekiguchi
Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
Antibiotics
LA-MRSA
ST398
ST8
antimicrobial resistance
zinc resistance
SNP analysis
title Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
title_full Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
title_fullStr Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
title_full_unstemmed Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
title_short Prevalence and Genetic Characterization of Methicillin-Resistant <i>Staphylococcus aureus</i> Isolated from Pigs in Japan
title_sort prevalence and genetic characterization of methicillin resistant i staphylococcus aureus i isolated from pigs in japan
topic LA-MRSA
ST398
ST8
antimicrobial resistance
zinc resistance
SNP analysis
url https://www.mdpi.com/2079-6382/13/2/155
work_keys_str_mv AT michikokawanishi prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT marimatsuda prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT hitoshiabo prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT manaoozawa prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT yutahosoi prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT yukarihiraoka prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT sakiharada prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT miokumakawa prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan
AT hidetosekiguchi prevalenceandgeneticcharacterizationofmethicillinresistantistaphylococcusaureusiisolatedfrompigsinjapan