From farm to fork: Colistin voluntary withdrawal in Portuguese farms reflected in decreasing occurrence of mcr-1-carrying Enterobacteriaceae from chicken meat

Expansion of mcr-carrying Enterobacteriaceae (MCR-E) is a well-recognized problem affecting animals, humans and the environment. Ongoing global control actions involve colistin restrictions among food-animal production, but their impact on poultry-derived products is largely unknown, justifying comprehensive farm-to-fork studies. Occurrence of MCR-E among 53 chicken-meat batches supplied from 29 Portuguese farms shortly after colistin withdrawal was evaluated. Strains (FT-IR/MLST/WGS), mcr plasmids and their adaptive features were characterized by cultural, molecular and genomic approaches. We found high rates of chicken-meat batches (80%-100% - 4 months; 12% - the last month) with multiple MDR + mcr-1-carrying Escherichia coli (Ec-including ST117 and ST648-Cplx) and Klebsiella pneumoniae (Kp-ST147-O5:K35) clones, some of them persisting over time. The mcr-1 was located in the chromosome (Ec-ST297/16-farms) or dispersed IncX4 (Ec-ST602/ST6469/5-farms), IncHI2-ST2/ST4 (Ec-ST533/ST6469/5 farms and Kp-ST147/6-farms) or IncI2 (Ec-ST117/1-farm) plasmids. WGS revealed high load and diversity in virulence, antibiotic resistance and metal tolerance genes. This study supports colistin withdrawal potential efficacy in poultry production and highlights both poultry-production chain as a source of mcr-1 and the risk of foodborne transmission to poultry-meat consumers. Finally, in the antibiotic reduction/replacement context, other potential co-selective pressures (e.g., metals-Cu as feed additives) need to be further understood to guide concerted, effective and durable actions under 'One Health' perspective.