Multidrug Resistance Dynamics in Salmonella in Food Animals in the United States: An Analysis of Genomes from Public Databases

The number of bacterial genomes deposited each year in public databases is growing exponentially. However, efforts to use these genomes to track trends in antimicrobial resistance (AMR) have been limited thus far. We used 22,102 genomes from public databases to track AMR trends in nontyphoidal Salmonella in food animals in the United States. In 2018, genomes deposited in public databases carried genes conferring resistance, on average, to 2.08 antimicrobial classes in poultry, 1.74 in bovines, and 1.28 in swine. This represents a decline in AMR of over 70% compared to the levels in 2000 in bovines and swine, and an increase of 13% for poultry. Trends in resistance inferred from genomic data showed good agreement with U.S. phenotypic surveillance data (weighted mean absolute difference +/- standard deviation, 5.86% +/- 8.11%). In 2018, resistance to 3rd-generation cephalosporins in bovines, swine, and poultry decreased to 9.97% on average, whereas in quinolones and 4th-generation cephalosporins, resistance increased to 12.53% and 3.87%, respectively. This was concomitant with a decrease of bla(CMY-2) but an increase in bla(CTX-M-65) and gyrA D87Y (encoding a change of D to Y at position 87). Core genome single-nucleotide polymorphism (SNP) phylogenies show that resistance to these antimicrobial classes was predominantly associated with Salmonella enterica serovar Infantis and, to a lesser extent, S. enterica serovar Typhimurium and its monophasic variant I 4,[5],12:i:-, whereas quinolone resistance was also associated with S. enterica serovar Dublin. Between 2000 and 2018, trends in serovar prevalence showed a composition shift where S. Typhimurium decreased while S. Infantis increased. Our findings illustrate the growing potential of using genomes in public databases to track AMR in regions where sequencing capacities are currently expanding. IMPORTANCE Next-generation sequencing has led to an exponential increase in the number of genomes deposited in public repositories. This growing volume of information presents opportunities to track the prevalence of genes conferring antimicrobial resistance (AMR), a growing threat to the health of humans and animals. Using 22,102 public genomes, we estimated that the prevalence of multidrug resistance (MDR) in the United States decreased in nontyphoidal Salmonella isolates recovered from bovines and swine between 2000 and 2018, whereas it increased in poultry. These trends are consistent with those detected by national surveillance systems that monitor resistance using phenotypic testing. However, using genomes, we identified that genes conferring resistance to critically important antimicrobials were associated with specific MDR serovars that could be the focus for future interventions. Our analysis illustrates the growing potential of public repositories to monitor AMR trends and shows that similar efforts could soon be carried out in other regions where genomic surveillance is increasing.

Automated summary

The rapid growth of bacterial genomes in public databases presents opportunities to track antimicrobial resistance (AMR) trends. Using genomic data, it was found that resistance in nontyphoidal Salmonella varied among food animals in the United States, showing a decline in bovines and swine but an increase in poultry. Results from genomic surveillance were consistent with national surveillance data, indicating the potential for using genomes to monitor AMR trends in expanding sequencing capacities.