Prevalence of antimicrobial resistance and potential pathogenicity, and possible spread of third generation cephalosporin resistance, in Escherichia coli isolated from healthy chicken farms in the region of Dakar, Senegal.

Passoret Vounba,Rianatou Bada-Alambédji,Julie Arsenault,John M Fairbrother,Iddya Karunasagar

doi:10.1371/journal.pone.0214304

Passoret Vounba, Rianatou Bada-Alambédji + Show 3 more

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https://doi.org/10.1371/journal.pone.0214304

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Abstract

Escherichia coli is a normal inhabitant of the intestinal microbiota of chickens, a small proportion of which may be avian pathogenic E. coli (APEC) or potential extraintestinal pathogenic E. coli (ExPEC), capable of causing disease in humans. These E. coli may also be resistant to antimicrobials of critical importance in human or veterinary health. This study aims to 1) determine the prevalence of antimicrobial resistance (AMR) and resistance genes, multidrug resistance (MDR), chromosomal mechanisms of quinolone-resistance and virulence profiles of E. coli isolated from healthy chicken farms in the region of Dakar, Senegal, 2) investigate the spread of third-generation cephalosporins (3GC) resistance in E. coli isolated from healthy chicken farms with respect to virulence and resistance genes, serogroups, Pulsed-Field Gel Electrophoresis (PFGE), phylogenetic groups, plasmid types and transferability and 3) determine whether nonsusceptibility against 3GC on farms could be linked to risk factors. More than 68% of isolates from environmental faecal and drinking water samples, carcasses and carcass washes collected on 32 healthy chicken farms were multidrug resistant (MDR), resistance to antimicrobials critical in human health (3GC or ciprofloxacin) being found in all types of samples. Ciprofloxacin resistance was due to mutations in the gyrA and parC genes, 95% of tested farms harboring isolates carrying three mutations, in gyrA (Ser83Ile and Asp87Asn) and parC (Ser80Ile). Nine of the 32 farms (28.1%) demonstrated the presence of one or more 3GC-nonsusceptible indicator isolates but none of the potential risk factors were significantly associated with this presence on farms. Following ceftriaxone enrichment, presumptive extended-spectrum beta-lactamase/AmpC-beta-lactamase (ESBL/AmpC)-producer isolates were found in 17 of the 32 farms. 3GC resistance was mediated by blaCMY-2 or blaCTX-M genes, blaCTX-M being of genotypes blaCTX-M-1, blaCTX-M-8 and for the first time in chickens in Senegal, the genotype blaCTX-M-15. Clonally related ESBL/AmpC-producer isolates were found on different farms. In addition, blaCTX-M genes were identified on replicon plasmids I1 and K/B and blaCMY-2 on K/B, I1 and B/O. These plasmids were found in isolates of different clusters. In addition, 18 isolates, some of which were ESBL/AmpC-producers, were defined as potential human ExPEC. In conclusion, E. coli isolates potentially pathogenic for humans and demonstrating MDR, with resistance expressed against antimicrobials of critical importance in human health were found in healthy chickens in Senegal. Our results suggest that both clonal spreading and horizontal gene transfer play a role in the spread of 3GC-resistance and that chickens in Senegal could be a reservoir for AMR and ExPEC for humans. These results highlight the importance of raising awareness about compliance with biosecurity measures and prudent use of antimicrobials.

Highlights

Escherichia coli is a normal inhabitant of intestinal flora of warm-blooded animals including humans, but may be a potential pathogenic agent
E. coli isolates potentially pathogenic for humans and demonstrating multidrug resistance (MDR), with resistance expressed against antimicrobials of critical importance in human health were found in healthy chickens in Senegal
Our results suggest that both clonal spreading and horizontal gene transfer play a role in the spread of 3rd generation cephalosporins (3GC)-resistance and that chickens in Senegal could be a reservoir for antimicrobial resistance (AMR) and Extraintestinal pathogenic E. coli (ExPEC) for humans

Summary

Introduction

Escherichia coli is a normal inhabitant of intestinal flora of warm-blooded animals including humans, but may be a potential pathogenic agent. Pathogenic strains are termed avian pathogenic E. coli (APEC), a sub-group of the pathotype of Extraintestinal pathogenic E. coli (ExPEC). E. coli isolates may be classified into four phylogroups A, B1, B2 and D. Isolates from phylogroups B2 and D possess more virulence genes associated with ExPEC than those of phylogroups A and B1 [2]. Several studies have demonstrated a genetic similarity between E. coli involved in urinary tract infections, meningitis, and septicaemia in humans and those found in poultry and poultry products for human consumption [3,4,5,6], suggesting that the chicken could act as a reservoir of human pathogenic E. coli

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