High prevalence of ciprofloxacin resistance in Escherichia coli isolated from chickens, humans and the environment: An emerging one health issue

PLoS One. 2023 Nov 20;18(11):e0294043. doi: 10.1371/journal.pone.0294043. eCollection 2023.

Abstract

The emergence of antimicrobial resistance in commensal bacteria poses a serious public health burden worldwide. Commensals can disseminate the resistance genes to pathogenic bacteria causing life-threatening infections. This cross-sectional study was designed to investigate the antimicrobial resistance pattern and molecular mechanism(s) of ciprofloxacin resistance in commensal E. coli from three major one health components (humans, animals and the environment) in Bangladesh. Samples were randomly collected from broiler chickens, broiler farm environments and hospitalized human patients from the same geographical area. Isolation and identification of E. coli were performed following standard bacteriological techniques. Antimicrobial susceptibility testing (AST) was performed by disk diffusion and broth microdilution methods. Mutation at the quinolone-resistance determining region (QRDR) was analyzed by sequencing. Of 450 samples, a total of 287 (63.8%; 95% CI 59.2-68.1%) E. coli strains was isolated, where 240 (83.6%; 95% CI 78.9-87.5%) strains were phenotypically resistant to ciprofloxacin. The prevalence of ciprofloxacin-resistant E. coli in broiler chicken, broiler farm environments and hospitalized human patients are 77.6%, 88.8% and 89% respectively. In AST against nine antimicrobials, all the isolates were found to be multidrug-resistant (MDR). The minimum inhibitory concentration (MIC) of ciprofloxacin was ranged from 4 to >128mg/L. Point mutations were detected in several sites of QRDR, specifically at 83 and 87 amino acid positions in gyrA gene, and 56, 57, 78, 80 and 84 amino acid positions in parC gene. Mutations resulted in amino acid substitutions. Phylogenetic analysis of gyrA and parC gene sequences showed a close relationship between the strains isolated from different sources. This study demonstrates a high prevalence of ciprofloxacin resistance in commensal E. coli in humans, animals and environment interface and their genealogically similarity poses an alarming public health consequence.

MeSH terms

  • Amino Acids / genetics
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Anti-Infective Agents* / pharmacology
  • Chickens / microbiology
  • Ciprofloxacin / pharmacology
  • Cross-Sectional Studies
  • DNA Gyrase / genetics
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli
  • Humans
  • Microbial Sensitivity Tests
  • One Health*
  • Phylogeny
  • Prevalence
  • Quinolones* / pharmacology

Substances

  • Ciprofloxacin
  • Anti-Bacterial Agents
  • DNA Gyrase
  • Anti-Infective Agents
  • Quinolones
  • Amino Acids

Grants and funding

This project work was funded by the University Grant Commission of the Peoples Republic of Bangladesh. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The salary of the author MZI was supported by the Lundbeck Foundation, Copenhagen, Denmark (Grant ID R288-2018-1123).