Genomic surveillance of antimicrobial resistance shows cattle and poultry are a moderate source of multi-drug resistant non-typhoidal Salmonella in Mexico

Abstract

Multi-drug resistant (MDR) non-typhoidal Salmonella (NTS) is a public health concern globally. This study reports the phenotypic and genotypic antimicrobial resistance (AMR) profiles of NTS isolates from bovine lymph nodes (n = 48) and ground beef (n = 29). Furthermore, we compared genotypic AMR data of our isolates with those of publicly available NTS genomes from Mexico (n = 2400). The probability of finding MDR isolates was higher in ground beef than in lymph nodes:χ2 = 12.0, P = 0.0005. The most common resistant phenotypes involved tetracycline (40.3%), carbenicillin (26.0%), amoxicillin-clavulanic acid (20.8%), chloramphenicol (19.5%) and trimethoprim-sulfamethoxazole (16.9%), while more than 55% of the isolates showed decreased susceptibility to ciprofloxacin and 26% were MDR. Conversely, resistance to cephalosporins and carbapenems was infrequent (0–9%). MDR phenotypes were strongly associated with NTS serovar (χ2 = 24.5, P<0.0001), with Typhimurium accounting for 40% of MDR strains. Most of these (9/10), carried Salmonella genomic island 1, which harbors a class-1 integron with multiple AMR genes (aadA2, blaCARB-2, floR, sul1, tetG) that confer a penta-resistant phenotype. MDR phenotypes were also associated with mutations in the ramR gene (χ2 = 17.7, P<0.0001). Among public NTS isolates from Mexico, those from cattle and poultry had the highest proportion of MDR genotypes. Our results suggest that attaining significant improvements in AMR meat safety requires the identification and removal (or treatment) of product harboring MDR NTS, instead of screening for Salmonella spp. or for isolates showing resistance to individual antibiotics. In that sense, massive integration of whole genome sequencing (WGS) technologies in AMR surveillance provides the shortest path to accomplish these goals.

Comparative Genomic Analysis Discloses Differential Distribution of Antibiotic Resistance Determinants between Worldwide Strains of the Emergent ST213 Genotype of Salmonella Typhimurium

“…The qnr and oqxAB genes associated with quinolone resistance are mainly related to plasmids [ 59 , 60 ]. Despite being found in other serotypes in Mexico, the qnr genes were absent in Typhimurium strains of animal origin [ 61 , 62 ], but present in Mexican human strains of this serotype [ 63 ]. The oqxAB genes found here have also been previously reported for several serotypes of human isolates in Mexico [ 61 , 62 ].…”

“…Despite being found in other serotypes in Mexico, the qnr genes were absent in Typhimurium strains of animal origin [ 61 , 62 ], but present in Mexican human strains of this serotype [ 63 ]. The oqxAB genes found here have also been previously reported for several serotypes of human isolates in Mexico [ 61 , 62 ]. Resistance to quinolones is considered low for S. enterica strains in the USA, although in this country it has been documented the presence of genes conferring resistance to such antimicrobial compounds in the serotype Typhimurium strains coming from clinical, pork meat, and livestock samples [ 64 , 65 , 66 , 67 ].…”

“…Regarding the five point mutations that occur in the quinolone resistance-determining regions (QRDR) of DNA gyrase ( gyrA ) and topoisomerase IV ( parC ) [ 60 ] found in the genomes of ST213 strains, the double mutant S83Y in gyrA and S80I in parC is interesting, since S. Typhimurium mutations in gyrA , in addition to playing a dominant role in resistance to fluoroquinolones, have a synergistic effect with other resistance mechanisms, while the S80I mutation in parC appears to have no effect on quinolone resistance without gyrA mutations [ 69 ]. Whereas QRDR mutations are frequent in bovine S. enterica isolated strains of different serotypes in Mexico [ 62 ] and Canada [ 70 ], it appears to be absent or to occur with low frequency in the USA [ 36 , 71 ].…”

Healthy carriage of Salmonella within cattle lymph nodes is a key source of ground beef contamination with strains of clinical significance

“…We used SPAdes version 3.1.3.1 [15] to perform de novo genome assembly using trimmed sequences, while assembly quality was assessed using QUAST version 5.02 [16]. Data of assembly quality attributes was reported in our previous paper [17]. Genome annotation was conducted at the RAST web server using the RASTtk algorithm [18].…”

Bacterial enrichment prior to third-generation metagenomic sequencing improves detection of BRD pathogens and genetic determinants of antimicrobial resistance in feedlot cattle

“…In contrast, whole genome sequencing (WGS) produces high resolution genomic information for outbreak and AMR surveillance and management ( Harrison et al, 2013 ; Besser et al, 2019 ; Delgado-Suárez et al, 2021 ). However, WGS requires culture, isolation, and nucleic acid extraction prior to sequencing.…”