Estimating the likelihood of ESBL-producing E. coli carriage in slaughter-aged pigs following bacterial introduction onto a farm: A multiscale risk assessment

Abstract

The transmission of antimicrobial resistance (AMR) between animals, their environment, food and humans is a complex issue. Previous pharmacokinetic-pharmacodynamic (PKPD) models indicate that extended-spectrum β-lactamase (ESBL) resistant bacterial populations may be self-sustaining through horizontal and vertical gene transfer, even in the absence of antimicrobial pressure. However, models focusing purely on the biochemical aspects fail to incorporate the complicated host population dynamics which occur within a farm environment. Models of disease transmission within commercial farm environments can provide further insight to the on-farm transmission dynamics of AMR between animals and their environment, as well as predict the effect of various on-farm interventions. Here, we present a risk assessment which predicts the likelihood that slaughter-aged pigs would carry resistant bacteria after a single introduction of ESBL E. coli on commercial pig farms. We incorporate outputs from a PKPD model which explores the complex host/gastrointestinal bacteria interplay after antimicrobial treatment; with an on-farm model of bacterial transmission. The risk assessment is designed to be adaptable for the simultaneous transmission of multiple bacteria and resistant strains. We predicted that after introduction onto a pig farm, ESBL E. coli bacteria are likely to persist on the farm for more than a year, leading to a high batch prevalence (39.4% slaughter pigs, 5th and 95th percentiles: 0.0–57.5) and high faecal shedding. A comparison of different farm management types suggested that all-in-all-out housing was a protective measure for both prevalence in slaughter-aged pigs and faecal shedding rates. We applied two main interventions at the farm level, an enhanced cleaning and disinfectant (C&D) protocol and isolation of pigs in sick pens for the duration of their antibiotic treatment. Both interventions were able to reduce the number of pigs shedding more than 2 log10 ESBL E. coli from 18.7% (5th and 95th percentiles: 5.9–30.4) in the baseline scenario, to 7.2% (5th and 95th percentiles: 0.0–21.5) when an enhanced C&D protocol was applied, 0.1% (5th and 95th percentiles: 0.0–0.3) when sick pens were used and 0.1% (5th and 95th percentiles: 0.0–0.3) when a combination of enhanced C&D plus sick pens was used. Both scenarios also reduced the prevalence in batches of pigs going to slaughter. This effect was largest when sick pens were used, where 75% of batches had 0% positive pigs. The results suggest that a single introductory event is sufficient to cause a substantial risk of carriage in slaughter-aged pigs. Further quantitative microbial risk assessments (QMRA) are needed to consider the onwards risk posed to later parts of the food chain.