Unravelling the genetic threads: Comparative genomic analysis of Salmonella from food and clinical cases in England, 2015–2019

Despite advances in Salmonella testing, surveillance, and improved food safety practices, salmonellosis remains prevalent in the UK. The primary challenge of preventing infections is determining how to ensure that food safety management plans are effective and to prioritise food sampling activities before the outbreaks occur. In this genomic study, we assessed the relative contribution of various foods over a five-year period to cases of human salmonellosis in England, aiming to rank the associated food risks based on genetic similarity. To achieve this, we conducted a comparative genomic analysis of Salmonella recovered from food (802) and environmental samples (131) against routinely tested Salmonella isolates from clinical cases (37,673) between 2015 and 2019. The analysis revealed that of all Salmonella -positive food and environmental isolates, 19.7 % were genetically related to Salmonella from clinical cases. A significant portion of these isolates was collected due to reactive sampling, which occurs in response to recognised public health concerns. In terms of Salmonella from clinical cases, only 2.5 % were genetically similar to isolates from food and 2.6 % from the environment. This relatively low rate of similarity may be due to other infection pathways, such as travel-related exposure or contact with animals, as well as infection from food items that are not subject to regular microbiological testing by public health bodies in the UK. We found that isolates from food products of animal origin, specifically eggs and poultry, were genetically linked to a higher number of isolates from clinical cases compared to non-animal origin products or composite foods, potentially indicating a greater public health risk. Meanwhile, non-animal origin foods were mostly associated with sporadic cases or clusters of fewer than five cases that had not previously been identified. The findings from this study underscore the need to shift from primarily reactive to additional proactive, risk-based food testing to better mitigate foodborne hazards and reduce the potential for outbreaks. While our genomic approach offers a valuable method for ranking food-related risks through genetic linkages, it does not replace the need for integrated epidemiological analysis. Such data are essential for understanding exposure pathways and quantifying foodborne risks, but were beyond the scope of this study. Nevertheless, the proposed genomic framework has the potential to inform future microbiological risk assessments, guide prioritisation of food sampling activities, support outbreak investigations, and contribute to the development of genomics-based public health interventions. • High-scale global genomic screening ranks Salmonella foodborne risks in England. • 19.7 % of food and environmental isolates were linked to human salmonellosis cases. • Poultry and egg products pose the highest public health risk among food types. • Non-animal origin foods were more associated with sporadic or smaller clusters of cases. • The study supports a One Health genomic approach for proactive food safety measures.