Longitudinal Study of Distributions of Similar Antimicrobial-Resistant Salmonella Serovars in Pigs and Their Environment in Two Distinct Swine Production Systems

Abstract

The aim of this longitudinal study was to determine and compare the prevalences and genotypic profiles of antimicrobial-resistant (AR) Salmonella isolates from pigs reared in antimicrobial-free (ABF) and conventional production systems at farm, at slaughter, and in their environment. We collected 2,889 pig fecal and 2,122 environmental (feed, water, soil, lagoon, truck, and floor swabs) samples from 10 conventional and eight ABF longitudinal cohorts at different stages of production (farrowing, nursery, finishing) and slaughter (postevisceration, postchill, and mesenteric lymph nodes [MLN]). In addition, we collected 1,363 carcass swabs and 205 lairage and truck samples at slaughter. A total of 1,090 Salmonella isolates were recovered from the samples; these were isolated with a significantly higher prevalence in conventionally reared pigs (4.0%; n ‫؍‬ 66) and their environment (11.7%; n ‫؍‬ 156) than in ABF pigs (0.2%; n ‫؍‬ 2) and their environment (0.6%; n ‫؍‬ 5) (P < 0.001). Salmonella was isolated from all stages at slaughter, including the postchill step, in the two production systems. Salmonella prevalence was significantly higher in MLN extracted from conventional carcasses than those extracted from ABF carcasses (P < 0.001). We identified a total of 24 different serotypes, with Salmonella enterica serovar Typhimurium, Salmonella enterica serovar Anatum, Salmonella enterica serovar Infantis, and Salmonella enterica serovar Derby being predominant. The highest frequencies of antimicrobial resistance (AR) were exhibited to tetracycline (71%), sulfisoxazole (42%), and streptomycin (17%). Multidrug resistance (resistance to >3 antimicrobials; MDR) was detected in 27% (n ‫؍‬ 254) of the Salmonella isolates from the conventional system. Our study reports a low prevalence of Salmonella in both production systems in pigs on farms, while a higher prevalence was detected among the carcasses at slaughter. The dynamics of Salmonella prevalence in pigs and carcasses were reciprocated in the farm and slaughter environment, clearly indicating an exchange of this pathogen between the pigs and their surroundings. Furthermore, the phenotypic and genotypic fingerprint profile results underscore the potential role played by environmental factors in dissemination of AR Salmonella to pigs.

Horizontal Dissemination of Antimicrobial Resistance Determinants in Multiple Salmonella Serotypes following Isolation from the Commercial Swine Operation Environment after Manure Application

“…This is in comparison to our previous report where we identified from a farm environment in North Carolina a 90-to 100-kb plasmid in a tetracyclineresistant S. Rissen isolate carrying the tet(A) gene (31). This serotype is not common in the U.S. agricultural system and was identified for the first time in North Carolina swine farms in 2009 (42).…”

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

“…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.…”

“…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.…”

Perceptions of information gaps in farm-to-table studies

“…These studies fall into three major categories: (1) the experimental study, which measures the effects of specified treatments under controlled environments. This type of study can be traced back many decades and a very short list finds research on feeds and their impacts on reducing survival of Salmonella (Hansen, 2004), the impacts of transportation and related stress (Mulder, 1995;Warriss, Brown, Edwards, Anil, & Fordham, 1992), the impacts of polishing process (Hald, Wingstrand, Swanenburg, von Altrock, & Thorberg, 2003), and so forth; (2) the cohort study, which, following the life span of a herd of livestock, examines the effectiveness of mitigation strategies in multiple phases of pre-harvest practices (Hurd, McKean, Wesley, & Karricker, 2001;Keelara et al, 2013;Pires, Funk, Manuzon, Darr, & Zhao, 2013;Rostagno, Hurd, & McKean, 2012;van Winsen et al, 2002); and (3) the farm-to-table study, which explores the entire meat supply chain, including both the pre-and post-harvest practices, for solutions to mitigating pathogens shedding and reducing social costs (FAO/WHO, 2002;Hope et al, 2002;McNamara, Miller, Liu, & Barber, 2007;Miller, Liu, McNamara, & Barber, 2005;Nauta, van der Fels-Klerx, & Havelaar, 2005;Nauta et al, 2009;Roberts, Ahl, & McDowell, 1995;Romero-Barrios, Hempen, Messens, Stella, & Hugas, 2013;Smid, Verloo, Barker, & Havelaar, 2010;Smith, Fazil, & Lammerding, 2013;VLA, 2011;USDA 1998).…”