Campylobacter dynamics in conventiónal and antimicrobial-free (abf) swine and their environment

Abstract

Campylobacter is an internationally recognized food-borne pathogen of public health importance. Food animals are important reservoirs of Campylobacter species, of which swine are known to be a main reservoir of Campylobacter coli. Conventionally reared swine receive antimicrobials in their feed at sub-therapeutic concentrations to enhance their growth; this use has been under debate due to associations with the development of antimicrobial resistant (AR) bacterial strains. However, AR bacteria are also shed by swine reared under no antimicrobial selection pressure, highlighting the potential role played by other factors including environmental reservoirs in the transmission of AR strains to pigs which needs to be identified. The objectives of this study were to 1) determine the Campylobacter prevalence and antimicrobial resistance profile in the ABF and conventional swine production systems at farm, slaughter, and the environment, 2) determine associations between potential risk factors and the prevalence of AR C. coli at the pre-harvest level, and 3) compare the population biology of antimicrobial resistant C. coli in the two systems. C. coli was the predominant species isolated at farm, slaughter, and environment in both production systems. The persistence of multidrug-resistant (MDR) C. coli in all the farm and slaughter stages in our study clearly indicates the ability of C. coli strains to disseminate across the production chain and persist in the farm and slaughter environment. Associations were determined between exposure to enrofloxacin, tetracycline, tiamulin, and resistance to ciprofloxacin and nalidixic acid, tetracycline, and macrolides, respectively in C. coli isolated from conventional pigs. The high frequency of MDR C. coli isolated from pigs reared in the ABF system, which did not receive antimicrobials for treatment or growth promotion, clearly indicate the lack of antimicrobial use does not necessarily result in absence of AR bacterial populations. Multiple MDR patterns were observed in the ABF pigs, including resistance to seven antimicrobials. Associations between swine management practices and the prevalence of AR C. coli in the ABF and conventional productions systems revealed the presence of cattle, and the presence of pigs with diarrhea to be potential risk factors for the C. coli prevalence and AR in swine farms. Data analysis identified plastic farrowing floors, the use of antiparasitics, cleaning ≤ 1week prior to the pigs entry to the barns, and the use of a glutaraldehide and ammonium chloride solution in addition to chlorhexidine, to be significantly associated with a lower prevalence of AR Campylobacter. Multilocus sequence typing (MLST) of the C. coli populations from ABF and conventional swine production systems revealed freely recombining populations close to linkage equilibrium. Identical sequence types (STs) between the pigs and their environment, both at farm and slaughter, were detected. The close clustering of C. coli STs from swine and carcasses with those from the environment revealed a C. coli population that shares a common ancestry in the conventional and ABF swine production systems. This could potentially explain the high prevalence of AR C. coli in ABF production systems. Overall, our results highlight the definitive role of the environment in the persistence and dissemination of AR Campylobacter, particularly in alternative swine production systems that do not use antimicrobials. The phenotypic and genotypic similarity of C. coli isolates from the two production systems, and the environmental reservoirs present in ABF and conventional farms could potentially explain antimicrobial resistance in pigs that were not exposed to antimicrobials.