Longitudinal Study Detects the Co-Carriage of ESBL and mcr-1 and -4 Genes in Escherichia coli Strains in a Portuguese Farrow-to-Finish Swine Herd

SIMPLE SUMMARY: The difficulty of treating bacterial infections has become a worldwide health concern due to the evolution of bacterial antibiotic resistance. Antibiotics are routinely used to prevent and treat infections in food-producing animals, especially in young animals. This procedure may lead to resistant bacteria in the animal gut that may indirectly cause a broader public health issue. Therefore, we conducted a study in a pig farrow-to-finish operation during five months to understand how the administration of antibiotics in sows and piglets impact the emergence of antibiotic resistance in Escherichia coli and its maintenance in the gut until the slaughter weight is reached. Our results showed that sows and their piglets carried antibiotic resistant E. coli throughout their life cycle that can be associated to farm administration of antibiotics. These antibiotics are critical in human medicine, which includes the antibiotic colistin used as a last-resort therapy in some multidrug resistant bacteria in human infections. In addition, these bacteria demonstrated the presence of virulence genes that support pathogenesis. Overall, this study highlights the need to reduce antibiotic use in animal husbandry or to find alternatives to antibiotics in food-animal production to reduce the emergence and potential spread of antibiotic–resistant pathogens. ABSTRACT: Cephalosporins and polymyxins are employed in antimicrobial protocols to control and treat neonatal infections and post-weaning diarrhoea in swine operations. We conducted a longitudinal study to evaluate the colonization and transmission of antibiotic–resistant Escherichia coli in sows and their piglets in a farrow-to-finish operation, focusing on characterization of Extended Spectrum Beta-Lactamase (ESBL) and mcr genes, virulence traits and genetic relatedness. A total of 293 E. coli isolates were obtained from faecal samples collected in five time points. At birth bla(CTX-M-1group) cluster was detected in E. coli isolates from 9 sows and 49 piglets (73.41%), while in the following four’ piglets sampling moments it was detected in 91.8%, 57.6%, 71.4% and 97.4%. The gene mcr-1 was detected in E. coli from one sow and from three piglets from different litters at birth and increased in the first weeks of piglet life (68.85%, 100%, 90% and 8.1%). A new mcr-4 allele, mcr-4.7, was identified in 3.28%, 28.57%, 7.5% of E. coli isolates. Most mcr-positive E. coli isolates (96,7%) carried bla(CTX-M-1Group) genes and 93,33% carried both mcr-4 and mcr-1. CTX-M-1 and CTX-M-32 were the most predominant ESBLs. Plasmids belonged to IncI1, IncF and IncN groups. Most isolates belong to phylogenetic group B1; PAI IV(536) marker was detected in nine isolates. The strains were kept in the different stages of the piglets’ life. The use of ceftiofur and colistin may explain the high prevalence and co-selection of bla(CTX-M-1Group) and mcr-1 and/or -4 genes, contributing to the maintenance of resistant and virulent isolates throughout the pig life cycle that may reach the food chain.