Dynamics of extended-spectrum cephalosporin-resistant Escherichia coli in pig farms: A longitudinal study

Julia Moor,Suzanne Aebi,Susanne Rickli,Nadezda Mostacci,Gudrun Overesch,Anne Oppliger,Markus Hilty

doi:10.1016/j.ijantimicag.2021.106382

Julia Moor, Suzanne Aebi + Show 5 more

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https://doi.org/10.1016/j.ijantimicag.2021.106382

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Abstract

ObjectivesPoint prevalence estimates of extended-spectrum cephalosporin-resistant Escherichia coli (ESC-R-Ec) are important surveillance measures but may not uncover the ESC-R-Ec dynamics within pig farms. A longitudinal study was therefore performed by sampling individual pigs, pig farmers and the environment. MethodsOn average, 30 (range 10–46) piglets of 31 Swiss farms were sampled during the suckling, weaning and fattening stages (n= 2437 samples). In addition, stool from pig farmers and environmental samples were obtained and metadata collected by questionnaires. ESC-R-Ec was identified by routine culture, and clonal relationships and resistance genes were derived from whole genome sequencing data. ResultsWorking on pig farms was not associated with an increased prevalence of ESC-R-Ec in humans. ESC-R-Ec prevalence significantly decreased from 6.2% to 3.9% and 1.8% for the suckling, weaned and fattening pigs, respectively (P < 0.001). Within the 57 ESC-R-positive suckling piglets, persisting carriage was detected in 25 animals at two consecutive time points and one animal at three consecutive time points. Clonal spread (n=7 farms, 22.6%) and horizontal gene transfer (n=1 farm, 3%) within pigs but not between humans and animals was detected. Liquid manure (n=10 samples, 16.7%) was identified as the major environmental reservoir of ESC-R-Ec in the pig farm environment. ConclusionsPig farming practices like all-in-all-out systems, but not antimicrobial usage, were associated with reduced risk of ESC-R-Ec at the farm level. As carriage duration is normally short within the individual pigs, the risk of recolonisation and clonal spread of ESC-R-Ec might be reduced by applying appropriate decontamination strategies.

Highlights

The spread of extended-spectrum cephalosporin-resistant Escherichia coli (ESC-R-Ec) constitutes a major public health problem
Considering data submitted by 28 EU member states, the proportion of presumptive extended-spectrum beta-lactamase (ESBL) and/ or AmpC producers was low among all indicator E. coli isolates recovered from fattening pigs (52/4205, 1.2%) [4]; large differences among the reporting countries were observed
Rectal swabs of 30 piglets were collected per farm (31 farms) and the individual animals were tracked throughout the different farm units, resulting in samples from three time points (2437 samples in total)

Summary

Introduction

The spread of extended-spectrum cephalosporin-resistant Escherichia coli (ESC-R-Ec) constitutes a major public health problem. Modern animal food production depends on antimicrobial treatment and, livestock has been described as a reservoir of antibiotic resistance [1]. Depending on the life stage, pigs are exposed to distinct nourishment, housing and antibiotic treatment [5,6]. This may have consequences on the development of the animals’ pool of resistance genes. As longitudinal studies of ESC-R carriage in pigs are scarce, little is known about when pigs acquire resistant bacteria and how long they persist in the animals’ gastrointestinal tract. An important contribution of indigenous enterobacteria maternally transmitted along the sow lineage has beenrecently suggested [7]

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