A farm-to-fork quantitative risk assessment model for Salmonella Heidelberg resistant to third-generation cephalosporins in broiler chickens in Canada

Abstract

Salmonella Heidelberg resistant to ceftiofur (a third-generation cephalosporin antimicrobial agent) in broiler chicken products pose a risk to public health in Canada. The objective of this study was to assess the extent of that risk and to evaluate the effect of intervention measures along the agri-food chain. A stochastic farm-to-fork quantitative microbial risk assessment model was developed following the Codex Alimentarius Guidelines for Risk Analysis of Foodborne Antimicrobial Resistance. Different scenarios were analyzed to assess the individual relative effects of 18 possible interventions in comparison to a baseline scenario. The baseline scenario represented the first year of on-farm antimicrobial use surveillance in the Canadian broiler industry and the year before an industry-imposed ban on the preventive use of antimicrobials of very high importance to human health (2013), where 31.3% of broiler flocks consisted of birds to which ceftiofur was administered. The baseline scenario predicted an average probability of illness of 1.1 per 100,000 servings (SE: 0.064 per 100,000), corresponding to an average of 22,000 human infections (SE: 1900) with ceftiofur-resistant S. Heidelberg per year, which is likely an overestimation. This risk was reduced by 90% or 20% when two separate scenarios designed to capture the effect of withdrawing preventive ceftiofur use from poultry production were simulated using different approaches; data used for the former scenario were confounded by other potential concomitant control measures (e.g. Salmonella vaccination programme), so the true effect likely lies somewhere between the two estimates. A theoretical 'worst case' scenario where all flocks had birds exposed to ceftiofur increased the risk by 107%. A 50% reduction in the probability of human prior exposure to antimicrobials, which has a selective and competitive effect for Salmonella spp. following ingestion of contaminated products, reduced the risk by 65%. Other promising measures that could be considered for further risk management included improved cleaning and disinfection between broiler flocks on farm (risk reduction by 26%), exclusive use of air chilling (risk reduction by 34%), and the improvement of meat storage and preparation conditions, e.g., no temperature abuse at retail (risk reduction by 88%). These findings showed the importance of a structured approach to assessing and potentially implementing effective interventions to reduce the risk associated with ceftiofur-resistant S. Heidelberg at different steps along the agri-food chain. Major data gaps included information on concentrations of resistant bacteria, cross contamination at processing and how ceftiofur-resistant S. Heidelberg behave in comparison with susceptible ones, e.g., in terms of growth and survival ability, as well as pathogenicity and virulence.

Keywords: Antimicrobial resistance; Food safety; Microbial risk assessment; Public health; Risk analysis; Scenario analysis.