The prevalence of multidrug resistance is higher among bovine than human Salmonella enterica serotype Newport, Typhimurium, and 4,5,12:i:- isolates in the United States but differs by serotype and geographic region

Abstract

Salmonella represents an important zoonotic pathogen worldwide, but the transmission dynamics between humans and animals as well as within animal populations are incompletely understood. We characterized Salmonella isolates from cattle and humans in two geographic regions of the United States, the Pacific Northwest and the Northeast, using three common subtyping methods (pulsed-field gel electrophoresis [PFGE], multilocus variable number of tandem repeat analysis [MLVA], and multilocus sequence typing [MLST]). In addition, we analyzed the distribution of antimicrobial resistance among human and cattle Salmonella isolates from the two study areas and characterized Salmonella persistence on individual dairy farms. For both Salmonella enterica subsp. enterica serotypes Newport and Typhimurium, we found multidrug resistance to be significantly associated with bovine origin of isolates, with the odds of multidrug resistance for Newport isolates from cattle approximately 18 times higher than for Newport isolates from humans. Isolates from the Northwest were significantly more likely to be multidrug resistant than those from the Northeast, and susceptible and resistant isolates appeared to represent distinct Salmonella subtypes. We detected evidence for strain diversification during Salmonella persistence on farms, which included changes in antimicrobial resistance as well as genetic changes manifested in PFGE and MLVA pattern shifts. While discriminatory power was serotype dependent, the combination of PFGE data with either MLVA or resistance typing data consistently allowed for improved subtype discrimination. Our results are consistent with the idea that cattle are an important reservoir of multidrug-resistant Salmonella infections in humans. In addition, the study provides evidence for the value of including antimicrobial resistance data in epidemiological investigations and highlights the benefits and potential problems of combining subtyping methods.

FIG. 1.

Characterization of Salmonella enterica serotype 4,5,12:i:− isolates from farm NE299 by PFGE, MLVA, and antimicrobial resistance pattern. The isolate designations, MLVA pattern, PFGE pattern, and antimicrobial resistance pattern are shown to the right of the figure. The antimicrobial resistance pattern is shown as follows: SUSCEPT, susceptible; ACSTAmcSu, resistance to ampicillin, chloramphenicol, streptomycin, tetracycline, amoxicillin-clavulanic acid, and sulfonamides; ACSTAmcSuCaz, resistance to ampicillin, chloramphenicol, streptomycin, tetracycline, amoxicillin-clavulanic acid, sulfonamides, and ceftazidime. Absent PFGE bands distinguishing the two clusters of isolates are indicated by red lines.

FIG. 2.

Minimum spanning tree (MST) based on MLVA data for Salmonella enterica serotype Typhimurium isolates (A) and Salmonella enterica serotype 4,5,12:i:− or Newport isolates (B) included in this study. The size of the circle is proportional to the number of isolates represented by each node, and the length of the branch is based on categorical coefficients and proportional to the number of differences between nodes. Hypothetical nodes are indicated by broken lines. Nodes encompassing multidrug-resistant isolates are shown in red, and those encompassing susceptible isolates are shown in yellow. Pansusceptible Salmonella serotype Newport isolates from farm NE299, which are characterized in the text, are indicated by their respective accession number in the tree. Interpretation of central nodes as ancestral is dependent on linear relationship between phylogenetic relationship and difference in the number of repeats, an assumption that might not be valid in all cases, particularly for isolates from Salmonella serotype Newport lineages A and B.