Dogs fed raw meat-based diets are vectors of drug-resistant Salmonella infection in humans

Salmonella enterica serovar 4,[5],12:i:- (S. 4,[5],12:i:-), the monophasic variant of Typhimurium, is among the most prevalent surface antigen subtypes and most frequent carriers of multidrug-resistance in Salmonella worldwide, therefore becoming a prominent public health threat. Genomic surveillance data analysis, in addition to human case and animal health investigations and food inspections from Quebec, Canada were conducted to identify the source of an emerging S. 4,[5],12:i:- cluster from 2021–2023. We performed antimicrobial susceptibility testing, whole genome sequencing, phylogeny and comparative genomic analyses to characterize this local strain. We show that a cluster of 41 S. 4,[5],12:i:- emerged in Quebec, Canada, after acquiring a self-conjugative IncHI2A plasmid encoding extensive drug-resistance (mph(A), blaCTX-M-55, qnrS1) and potential reduced biocide susceptibility via efflux pump regulators (ramAp, marR), metal resistance (terZABCDE, copG) and oxidative stress responses (umuDC, dsbC), among other mechanisms. Genomic epidemiology identifies 20 human cases, 16 veal calves, 3 dogs, one piglet, one moose, and 4 raw meat-based diet isolates belonging to this cluster. Infants are mainly (50%) affected, and dogs fed raw meat-based diets are the major source identified, followed by exposure to cattle. Retrospective genomic analyses demonstrates its association to USA porcine and shared plasmid pool among many food-producing animals, but indicated different niches for different plasmid subtypes. This study highlights the threat of S. 4,[5],12:i:- ST34 and its raw pet food-based transmission to vulnerable human populations, where impacted veal farms and asymptomatic dogs can act as disease carriers with limited treatment options and possible environmental persistence. Antimicrobial drug resistance is a major public health concern. Understanding its transmission is important to identify sources of human infection where efforts might be required to reduce the burden and spread of infectious diseases. This study aimed to characterize, by means of genomics and epidemiology, a Canadian bacterial outbreak of Salmonella that did not respond to any of the recommended treatment options. Our results demonstrate the increased disease risk of feeding raw meat-based diets to dogs, which led to frequent hospitalizations in young children. We hope this study will encourage the inclusion of more companion animals and their food in health surveillance systems and deter pet owners from adopting raw meat-based diets in the future. Bernaquez et al. investigate the genomic epidemiology of a cluster of extensively drug-resistant Salmonella enterica serovar 4,[5],12:i:- ST34 affecting Canadians and cattle following the acquisition of an IncHI2A plasmid. Findings reveal dogs fed raw meat-based diets as the main source of transmission in young infants.