Effect of antimicrobial use and production system on Campylobacter spp., Staphylococcus spp. and Salmonella spp. resistance in Spanish swine: A cross-sectional study

Antimicrobial resistance is a worldwide public health threat; hence, current trends tend to reduce antimicrobial use in food-producing animals and to monitor resistance in primary production. This study aimed at evaluating the impact of antimicrobial use and production system on swine farms in the antimicrobial resistance of Campylobacter, Salmonella and Staphylococcus, the main zoonotic pathogens in pig herds, in order to assess their potential value as sentinel microorganisms in antimicrobial resistance surveillance schemes. A total of 37 Spanish swine farms, 18 intensive and 19 organic/extensive farms, were included in the study. The antimicrobial resistance of 104 Campylobacter, 84 Staphylococcus and 17 Salmonella isolates was evaluated using Sensititre plates following the EUCAST guidelines. Mixed-effects logistic regression was used to evaluate the influence of production system and antimicrobial use in resistant and multidrug-resistant (MDR) phenotypes to the antimicrobials tested. The results showed that antimicrobial use was higher (p < .001) on intensive farms than on organic/extensive farms. MDR in Campylobacter and Staphylococcus was lower on organic/extensive farms (OR p < .001). Antimicrobial resistance in Campylobacter and Staphylococcus isolates was, also for most of the antimicrobials studied, significantly higher in intensive than organic/extensive pig herds. Tetracycline resistance was associated with total antimicrobial consumption in both microbial species (p < .05), and some cross-associations between distinct antimicrobial substances were established, for instance resistance to erythromycin was associated with macrolide and phenicol consumption. No significant associations could be established for Salmonella isolates. The results demonstrate the link between antimicrobial consumption and resistance in zoonotic bacteria and evidence the potential value of using Campylobacter and Staphylococcus species in monitoring activities aimed at determining the impact of antimicrobials use/reduction on the occurrence and spread of antimicrobial resistance.