Comparative Phenotypic and Genotypic Characterization of Temporally Related NontyphoidalSalmonellaIsolated from Human Clinical Cases, Pigs, and the Environment in North Carolina

Abstract

Nontyphoidal Salmonella infections caused by antimicrobial-resistant (AMR) strains are of great public health concern. We compared the phenotypic and genotypic relationships among temporally and spatially related AMR Salmonella isolates (n=1058) representing several predominant serovars, including Salmonella Typhimurium, Salmonella Typhimurium var. 5-, Salmonella Derby, Salmonella Heidelberg, Salmonella Muenchen, Salmonella Schwarzengrund, and Salmonella Rissen of human clinical cases (n=572), pig (n=212), and farm environment (n=274) origin in North Carolina. Antimicrobial susceptibility testing was performed using the broth microdilution method, and genotypic resistance determinants, including class I and II integrons, were identified. Overall, Salmonella isolates exhibited the highest frequency of resistance to tetracycline (50%), followed by sulfisoxazole (36%) and streptomycin (27%). We identified 16 different antimicrobial resistance genes, including extended spectrum and AmpC β-lactamases-producing genes (bla(TEM), bla(PSE), and bla(CMY-2)), in all the β-lactam- and cephalosporin-resistant Salmonella isolates from humans, pigs, and the environment. Class I integrons of 1-kb and 1.2-kb size were identified from all the three sources (humans, 66%; pigs, 85%; environment, 58%), while Class II integrons of 2-kb size were identified only in pig (10%) and environmental (19%) isolates. We detected genotypic similarity between Salmonella Typhimurium isolated from humans, pigs, and the environment while serovars Derby, Heidelberg, and Muenchen exhibited genotypic diversity. Detection of AMR Salmonella isolates from humans, pigs, and the environment is a concern for clinicians and veterinarians to mitigate the dissemination of AMR Salmonella strains.

Dissemination of plasmid-encoded AmpC β-lactamases in antimicrobial resistant Salmonella serotypes originating from humans, pigs and the swine environment

“…In this study, we selected 21 AMR Salmonella strains from humans, pigs and the swine environment that were representative of multiple resistance patterns, serotypes, stages of production, and genotypic characteristics. The AMR Salmonella strains characterized in this study were part of longitudinal study by our group involving temporally and spatially related Salmonella isolates from humans, pigs and the swine environment (Keelara et al, 2013(Keelara et al, , 2014. Briefly, the frequency of AMR and MDR was higher in Salmonella isolates of pig origin (AMR: 82.6%; MDR: 36%) followed by the swine environmental (AMR: 67.6%; MDR: 21.4%) and human clinical isolates (AMR: 28%; MDR: 21.3%).…”

“…Salmonella isolates from temporally and spatially (originating from multiple counties in North Carolina) related pigs (n = 386), swine environment (n = 536) and human clinical cases (n = 572) were isolated and characterized for their antimicrobial susceptibility, resistance determinants and fingerprint profile (Keelara et al, 2013(Keelara et al, , 2014. The Salmonella isolates from pigs and their environment were collected as part of longitudinal study conducted from October 2008 to December 2011 on 30 conventional farms at different stages of production from farm to slaughter, including once at farrowing (7-10 day old), twice at each of nursery (4 and 7 weeks of age) and finishing stages (16 and 26 weeks of age), and finally once at slaughter in North Carolina.…”

“…In addition, lagoon (repository of waste water draining from the barns), barn floor and inter-farm truck floor swab samples were also collected at farms. The details of the study design, sampling and microbiological methods, estimates of Salmonella prevalence in pigs and their environment at farm and slaughter, antimicrobial susceptibility profiles, and their phenotypic and genotypic characterizations have been reported elsewhere (Keelara et al, 2013(Keelara et al, , 2014. The conventional pigs were reared indoors and given antimicrobials for growth, prophylaxis and therapeutic purposes.…”

“…MDR Salmonella isolates, including those resistant to 3rd generation cephalosporins, associated with different serotypes from humans, pigs, and the swine environment have been reported worldwide, including in the US (Frye and Fedorka-Cray, 2007;Patchanee et al, 2008;Eller et al, 2013;Glenn et al, 2013;Keelara et al, 2014). These MDR isolates often carry resistance genes either on the chromosome or on mobile genetic elements, such as plasmids and integrons (Aarestrup et al, 2008).…”

“…Previously we reported Salmonella prevalence, AMR profile, common MDR patterns, molecular characterization of resistance determinants and genotypic similarity among Salmonella isolates from humans, pigs and the swine environment at various stages of production (Keelara et al, 2013(Keelara et al, , 2014. Based on genotypic and phenotypic results, we were interested in determining whether different Salmonella serotypes with multiple resistance pattern (including MDR) harbor or exchange similar and/or different plasmids within temporally and spatially related MDR Salmonella serotypes in humans, pigs and the swine environment.…”