Epidemiology of antimicrobial resistance in commercial eggs across different production systems in Spain

The European poultry sector is transitioning towards alternative production systems, driven by consumer concerns about animal welfare. However, these systems, by providing access to the outdoors, increase exposure to the environment and wildlife, raising the risk of disease spread and antimicrobial resistance (AMR). The objective of this study was to evaluate the occurrence of AMR and multidrug resistance (MDR) in Escherichia coli isolates from commercial eggs from the four production systems in Spain: organic, free-range, floor and cage, and their genetic diversity using pulsed-field gel electrophoresis (PFGE) analysis. To this end, 1200 eggs were collected from the main supermarket chains over the course of a year. The shell and contents were analysed, evaluating the susceptibility of isolates to 15 antimicrobials. A total of 49 E. coli isolates were found, only on the shell. Overall, resistance to at least one antimicrobial was found in 69.4% of the isolates, and 44.9% showed MDR. When compared, the prevalence of MDR was significantly higher in organic systems (61.5%) than in cage systems (22.2%; p < 0.05). Moreover, PFGE analysis revealed great genetic diversity with 37 distinct pulsotypes, observing that E. coli isolates with similar genetic profiles presented different AMR patterns. These results suggest that the outdoor environment and contact with wildlife are crucial for AMR acquisition, even in organic systems with restricted antimicrobial use. It is imperative to implement rigorous perimeter and environmental biosecurity measures in poultry production systems to mitigate the spread of AMR, addressing this public health challenge through a comprehensive One Health perspective.