Twenty-four-month longitudinal study suggests little to no horizontal gene transfer in situ between third-generation cephalosporin-resistant Salmonella and third-generation cephalosporin-resistant Escherichia coli

Authors: Schmidt, John; Murray, Sarah; Dickey, Aaron; Wheeler, Tommy; Harhay, Dayna; Arthur, Terrance

Submitted to: Journal of Food Protection
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/17/2021
Publication Date: 2/1/2022
Citation: Schmidt, J.W., Murray, S.A., Dickey, A.M., Wheeler, T.L., Harhay, D.M., Arthur, T.M. 2022. Twenty-four-month longitudinal study suggests little to no horizontal gene transfer in situ between third-generation cephalosporin-resistant Salmonella and third-generation cephalosporin-resistant Escherichia coli in a beef cattle feedyard. Journal of Food Protection. 85(2):323-335. https://doi.org/10.4315/JFP-21-371.
DOI: https://doi.org/10.4315/JFP-21-371

Interpretive Summary: It has been theorized that Salmonella present at cattle feedyards may become resistant to the primary antibiotic used to treat serious human Salmonella infections by acquiring the genes responsible for resistance from non-pathogenic resistant E. coli. This theory has not been tested because although this gene transfer can be shown in artificial laboratory conditions, it has not been conclusively demonstrated in real world conditions. This study characterized resistance genes in 242 Salmonella and 203 E. coli isolated from a beef feedyard over two years. The primary resistance gene in resistant Salmonella was present in only 37.9% of the resistant E. coli. Likewise, the primary resistance gene in most resistant E. coli was at low levels in resistant Salmonella. These results demonstrated that resistant Salmonella at this feedlot were primarily due the persistence of a well-adapted Salmonella sub-population with very minimal or no contribution of resistance genes from E. coli.

Technical Abstract: Third-generation cephalosporins (3GCs) are preferred treatments for serious human Salmonella enterica infections. Beef cattle are suspected to contribute to human 3GC-resistant Salmonella infections. Commensal 3GC-resistant Escherichia coli are thought to act as reservoirs of 3GC resistance because these strains are isolated more frequently than are 3GC-resistant Salmonella strains at beef cattle feedyards. During each of 24 consecutive months, four samples of pen surface material were obtained from five pens (N=480) at a Nebraska feedyard to determine to the contribution of 3GC-resistant E. coli to the occurrence of 3GC-resistant Salmonella. Illumina whole genome sequencing was performed, and susceptibility to 14 antimicrobial agents was determined for 121 3GC-susceptible Salmonella, 121 3GC-resistant Salmonella, and 203 3GCresistant E. coli isolates. 3GC-susceptible Salmonella isolates were predominantly from serotypes Muenchen (70.2%) and Montevideo clade 1 (23.1%). 3GC-resistant Salmonella isolates were predominantly from serotypes Montevideo clade 2 (84.3%). One bla gene type (blaCMY-2) and the IncC plasmid replicon were present in 100 and 97.5% of the 3GC-resistant Salmonella, respectively. Eleven bla gene types were detected in the 3GC-resistant E. coli, which were distributed across 42 multilocus sequence types. The blaCMY-2 gene and IncC plasmid replicon were present in 37.9 and 9.9% of the 3GC-resistant E. coli, respectively. These results suggest that 3GC resistance in Salmonella was primarily due the persistence of Salmonella Montevideo clade 2 with very minimal or no contribution from 3GC-resistant E. coli via horizontal gene transfer and that 3GCresistant E. coli may not be a useful indicator for 3GC-resistant Salmonella in beef cattle production environments.