Increase in resistance to extended-spectrum cephalosporins in Salmonella isolated from retail chicken products in Japan

PLoS One. 2015 Feb 2;10(2):e0116927. doi: 10.1371/journal.pone.0116927. eCollection 2015.

Abstract

Extended-spectrum β-lactamase (ESBL)-producing Salmonella are one of the most important public health problems in developed countries. ESBL-producing Salmonella strains have been isolated from humans in Asian countries neighboring Japan, along with strains harboring the plasmid-mediated extended-spectrum cephalosporin (ESC)-resistance gene, ampC (pAmpC). However, only a few studies have investigated the prevalence of ESC-resistant Salmonella in chicken products in Japan, which are the main vehicle of Salmonella transmission. The aim of this study was to investigate the prevalence of ESBL-producing, pAmpC-harboring, or carbapenem-resistant Salmonella in chicken products in Japan. In total, 355 out of 779 (45.6%) chicken product samples collected from 1996-2010 contained Salmonella, resulting in 378 distinct isolates. Of these isolates, 373 were tested for resistance to ESCs, cephamycins, or carbapenems. Isolates that showed resistance to one or more of these antimicrobials were then examined by PCR and DNA sequence analysis for the presence of the bla(CMY), bla(CTX-M), bla(TEM), and bla(SHV) resistance genes. Thirty-five resistant isolates were detected, including 26 isolates that contained pAmpC (bla(CMY-2)), and nine ESBL-producing isolates harboring bla(CTX-M) (n = 4, consisting of two bla(CTX-M-2) and two bla(CTX-M-15 genes)), bla(TEM) (n = 4, consisting of one bla(TEM-20) and three bla(TEM-52) genes), and bla(SHV) (n = 1, bla(SHV-12)). All pAmpC-harboring and ESBL-producing Salmonella isolates were obtained from samples collected after 2005, and the percentage of resistant isolates increased significantly from 0% in 2004 to 27.9% in 2010 (P for trend = 0.006). This increase was caused in part by an increase in the number of Salmonella enterica subsp. enterica serovar Infantis strains harboring an approximately 280-kb plasmid containing bla(CMY-2) in proximity to ISEcp1. The dissemination of ESC-resistant Salmonella containing plasmid-mediated bla(CMY-2) in chicken products indicates the need for the development of continuous monitoring strategies in the interests of public health.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology*
  • Bacterial Proteins / genetics
  • Cephalosporins / pharmacology*
  • Chickens / microbiology*
  • Japan
  • Meat / microbiology
  • Molecular Sequence Data
  • Phenotype
  • Polymerase Chain Reaction
  • Salmonella / drug effects*
  • Salmonella / enzymology
  • Salmonella / genetics*
  • beta-Lactam Resistance / genetics*
  • beta-Lactamases / genetics

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Cephalosporins
  • AmpC beta-lactamases
  • beta-Lactamases

Associated data

  • GENBANK/AB750370
  • GENBANK/AB750371
  • GENBANK/AB750372
  • GENBANK/AB750373
  • GENBANK/AB750374
  • GENBANK/AB750375
  • GENBANK/AB750378
  • GENBANK/AB750379
  • GENBANK/AB750380
  • GENBANK/AB750382
  • GENBANK/AB750385
  • GENBANK/AB750386
  • GENBANK/AB751201
  • GENBANK/AB751202
  • GENBANK/AB751205
  • GENBANK/AB751206
  • GENBANK/AB751207
  • GENBANK/AB751210
  • GENBANK/AB751211
  • GENBANK/AB751213
  • GENBANK/AB751215
  • GENBANK/AB751218
  • GENBANK/AB751219
  • GENBANK/AB751221
  • GENBANK/AB751223
  • GENBANK/AB751225
  • GENBANK/AB751227
  • GENBANK/AB751229
  • GENBANK/AB751230
  • GENBANK/AB751232
  • GENBANK/AB751234
  • GENBANK/AB751237
  • GENBANK/AB751238
  • GENBANK/AB751240
  • GENBANK/AB751244
  • GENBANK/AB758624
  • GENBANK/AB906452
  • GENBANK/AB915634
  • GENBANK/AB916358
  • GENBANK/LC008131

Grants and funding

This work was supported by the Japan Society for the Promotion of Sciences KAKENHI, Grant No. 24590846 and the Daido Life Welfare Foundation, Osaka, Japan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.