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Phenotypic and genotypic characteristics of Escherichia coli with non-susceptibility to quinolones isolated from environmental samples on pig farms.

ABSTRACT: Background:In the last decade, the growth of the pig-farming industry has led to an increase in antibiotic use, including several used in human medicine, e.g. (fluoro)quinolones. Data from several studies suggest that there is a link between the agricultural use of antibiotics and the prevalence of antibiotic-resistant bacteria in the pig farm environment, including (fluoro)quinolone resistance. This poses a threat to human and animal health. Our goal was to phenotypically and genotypically characterize 174 E. coli showing non-susceptibility to quinolones isolated from environmental samples from pig farms. Antimicrobial susceptibility testing (AST) was performed using the disk diffusion method. PCR and sequence analysis were performed to identify chromosomal mutations in the quinolone resistance-determining regions (QRDR) of gyrA and the isolates were screened for the presence of the plasmid-mediated quinolone resistance (PMQR) genes aac-(6')-Ib-cr, qepA, qnrA, qnrB, qnrC, qnrD and qnrS.Strain relatedness was assessed by phylogenetic classification and multilocus sequence typing (MLST). Results:Of 174 isolates, 81% (n?=?141) were resistant to nalidixic acid, and 19% (n?=?33) were intermediately resistant. Overall, 68.4% (n?=?119) were multidrug resistant. This study revealed a prevalence of 79.9% (n?=?139) for gyrA QRDR mutations, and detected 21.8% (n?=?38) isolates with at least one PMQR gene. The two most frequently detected PMQR genes were qnrB and qnrS (13.8% (n?=?24) and 9.8% (n?=?17, respectively). E. coli belonging to phylogenetic group A (48.3%/n?=?84) and group B1 (33.3% /n?=?58) were the most frequent. E. coli ST10 (n?=?20) and ST297 (n?=?20) were the most common STs. Conclusions:E. coli with non-susceptibility to quinolones are widespread among the environment of Swiss pig farms and are often associated with an MDR phenotype. In several cases these isolates possess at least one PMQR gene, which could spread by horizontal gene transfer. E. coli from pig farms have diverse STs, some of which are associated with human and animal disease.

SUBMITTER: Kindle P

PROVIDER: S-EPMC6396500 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Phenotypic and genotypic characteristics of <i>Escherichia coli</i> with non-susceptibility to quinolones isolated from environmental samples on pig farms.

Kindle Patrick P Zurfluh Katrin K Nüesch-Inderbinen Magdalena M von Ah Sereina S Sidler Xaver X Stephan Roger R Kümmerlen Dolf D

Porcine health management 20190228

<h4>Background</h4>In the last decade, the growth of the pig-farming industry has led to an increase in antibiotic use, including several used in human medicine, e.g. (fluoro)quinolones. Data from several studies suggest that there is a link between the agricultural use of antibiotics and the prevalence of antibiotic-resistant bacteria in the pig farm environment, including (fluoro)quinolone resistance. This poses a threat to human and animal health. Our goal was to phenotypically and genotypica ...[more]

PMID: 30867937

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Project description:BackgroundDespite their indispensability in human medicine, fluoroquinolones (FQ) are used for the treatment of bacterial infections in farm animals which increases the risk of transferring FQ-resistant bacteria into the environment and via the food chain to humans. The objectives of this observational study were to follow-up of the presence of quinolone non-susceptible Escherichia coli (QNSE) qualitatively and quantitatively in faecal samples of pigs at four time points (2 weeks old, 4 weeks old, 2 weeks post weaning and during fattening period). Moreover differences between groups of FQ-treated pigs, pigs with contact to treated pigs and control pigs were investigated. Additionally, quinolone and FQ resistance of Escherichia coli isolates of the faecal samples were investigated by determining minimum inhibitory concentrations (MICs).Results40.9% of 621 fecal samples contained QNSE. Proportion of samples with detectable QNSE from treated and contact pigs did not differ significantly and were highest in piglets of 2 and 4 weeks of age. However, the proportions of samples with QNSE were significantly lowest in control pigs (7/90; 7.8%; CI = 3.5-14.7%) among all groups. Also, the number of colony-forming units was lowest in both weaners and fattening pigs of the control group compared to treated and contact groups. Following CLSI human breakpoints, in total, 50.4% out of 254 isolates in faecal samples were intermediate or resistant to ciprofloxacin.ConclusionsQNSE were present in faeces of pigs independent of age or FQ background but significantly less were found in pigs from farms without FQ usage. Due to the long half-life of FQ, it is likely that only a prolonged absence of fluoroquinolone treatments in pig farming will lead to a reduced frequency of QNSE in the farm environment. Solutions need to be found to minimise the emergence and transfer of quinolone and FQ-resistant bacteria from treated pigs to contact pigs and to farms without FQ usage.

Project description:Neomycin is the first-choice antibiotic for the treatment of porcine enteritis caused by enterotoxigenic Escherichia coli. Resistance to this aminoglycoside is on the rise after the increased use of neomycin due to the ban on zinc oxide. We identified the neomycin resistance determinants and plasmid contents in a historical collection of 128 neomycin-resistant clinical E. coli isolates from Danish pig farms. All isolates were characterized by whole-genome sequencing and antimicrobial susceptibility testing, followed by conjugation experiments and long-read sequencing of eight selected representative strains. We detected 35 sequence types (STs) with ST100 being the most prevalent lineage (38.3%). Neomycin resistance was associated with two resistance genes, namely aph(3')-Ia and aph(3')-Ib, which were identified in 93% and 7% of the isolates, respectively. The aph(3')-Ia was found on different large conjugative plasmids belonging to IncI1α, which was present in 67.2% of the strains, on IncHI1, IncHI2, and IncN, as well as on a multicopy ColRNAI plasmid. All these plasmids except ColRNAI carried genes encoding resistance to other antimicrobials or heavy metals, highlighting the risk of co-selection. The aph(3')-Ib gene occurred on a 19 kb chimeric, mobilizable plasmid that contained elements tracing back its origin to distantly related genera. While aph(3')-Ia was flanked by either Tn903 or Tn4352 derivatives, no clear association was observed between aph(3')-Ib and mobile genetic elements. In conclusion, the spread of neomycin resistance in porcine clinical E. coli is driven by two resistance determinants located on distinct plasmid scaffolds circulating within a highly diverse population dominated by ST100. IMPORTANCE Neomycin is the first-choice antibiotic for the management of Escherichia coli enteritis in pigs. This work shows that aph(3')-Ia and to a lesser extent aph(3')-Ib are responsible for the spread of neomycin resistance that has been recently observed among pig clinical isolates and elucidates the mechanisms of dissemination of these two resistance determinants. The aph(3')-Ia gene is located on different conjugative plasmid scaffolds and is associated with two distinct transposable elements (Tn903 and Tn4352) that contributed to its spread. The diffusion of aph(3')-Ib is mediated by a small non-conjugative, mobilizable chimeric plasmid that likely derived from distantly related members of the Pseudomonadota phylum and was not associated with any detectable mobile genetic element. Although the spread of neomycin resistance is largely attributable to horizontal transfer, both resistance determinants have been acquired by a predominant lineage (ST100) associated with enterotoxigenic E. coli, which accounted for approximately one-third of the strains.

Dataset Information

Phenotypic and genotypic characteristics of Escherichia coli with non-susceptibility to quinolones isolated from environmental samples on pig farms.

Publications

Phenotypic and genotypic characteristics of <i>Escherichia coli</i> with non-susceptibility to quinolones isolated from environmental samples on pig farms.

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