Salmonella Diversity Along the Farm-to-Fork Continuum of Pastured Poultry Flocks in the Southeastern United States

Abstract

Greater consumer demand for all natural, antibiotic-free poultry products has led to an increase in pastured poultry operations. Given the increased level of environmental interaction, and the potential increase in exposure to foodborne pathogens, a greater understanding of the prevalence and diversity of Salmonella populations inherent within pastured poultry flocks. To achieve this, 42 pastured poultry flocks from 11 farms were sampled using a farm-to-fork strategy and Salmonella was isolated and characterized through pre-harvest (feces, soil) to post-harvest (ceca, whole carcass rinse) to the final product (whole carcass rinse) the consumer would purchase. Salmonella was isolated from 353 of a total of 2,305 samples, representing an overall prevalence of 18.1%. By far the most prevalent serotype was Kentucky (72.7% of all isolates), with <16% of all Salmonella representing a top serotype of concern for human health according to the CDC. Even though these flocks were raised antibiotic-free, Salmonella isolates exhibited resistances to a variety of antibiotics, with the two most common resistances being toward tetracycline and streptomycin (68.8 and 64.4% of all isolates, respectively); however, almost 98% of the multidrug resistant isolates were serotype Kentucky. Salmonella prevalence and diversity (both in terms of serotypes and antibiotic resistance profiles) were related more to the farm location than to the type of sample from which the Salmonella was isolated from along the farm-to-fork continuum. Based on these data, while Salmonella prevalence was similar to that from conventional poultry operations, serotypes of lesser concern to human health (Kentucky, Indiana) tended to fill the ecological niche for Salmonella species throughout the farm-to-fork continuum in these pastured poultry flocks. The diversity of these Salmonella populations tended to be farm specific, indicating the need for more tailored intervention strategies to continue to enhance the safety of these products.

Molecular Epidemiology of Salmonella enterica in Poultry in South Africa Using the Farm-to-Fork Approach

“…The results of this study are also higher than those reported in the European Union (EU) (Finland and Sweden: <1%; Ireland: 19.8%), Asia (China: 12.6%; Korea: 15.3%), and South America (Columbia: 17.8%) [ 35 – 38 ]. Studies done in the USA and India along the farm-to-fork pathway reported an overall lower prevalence of 18.1% and 25.8%, respectively, than that in the current study [ 39 , 40 ]. The proportion of Salmonella isolated from poultry can be influenced and varies by geographical location, environmental contamination, nature of farm management systems, type of production systems, breed of the flock, age of birds, sample size, sampling procedures, and the methods used for isolation [ 6 , 11 ].…”

“…A similar resistance phenotype was reported in Saudi Arabia, where clinical and environmental samples showed resistance to cefuroxime (90.9%) and cefoxitin (87.9%), while most isolates were susceptible to β -lactams [ 49 ]. Previous studies in Africa, Australia, and the USA have reported a higher frequency of resistance to cefuroxime or cefoxitin among Salmonella -positive poultry isolates [ 14 , 39 , 46 , 50 ].…”

“…In comparison to the results of the current study, higher rates of fluoroquinolone resistance (ciprofloxacin and nalidixic) have been reported in poultry in the EU (64.7% and 61.5%), Brazil (86.5% and 89%), and China (25.7% and 46.7%) [ 37 , 45 , 60 ]. However, Salmonella isolated from broilers in Canada (3% and <1%) and in the USA (0% and <1%) have shown a low resistance frequency to fluoroquinolones, which can be attributed to the restricted use of fluoroquinolones in poultry [ 39 , 60 , 62 , 63 ].…”

“…In this study, low resistance frequencies were also observed for chloramphenicol (1.9%), nitrofurantoin (0.4%), and azithromycin (11%). Similarly, low rates of chloramphenicol resistance were reported among poultry isolates in Brazil (0.6%) and the USA (0.3%) [ 39 , 60 ]. The low chloramphenicol and nitrofurantoin resistance in this study can be attributed to the prohibited use of these antibiotics in food animals in SA [ 64 ].…”

Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance toSalmonellain chickens

“…Moreover, continuous variables did not meet the assumption of a normal distribution; therefore, non-parametric testing for direct comparisons was performed using Wilcoxon rank sum and signed rank tests, and the Kruskal-Wallis rank sum test was used for one-way analysis of variance tests. Additionally, a generalized linear model with a binomial distributed outcome and a log link function was performed as described earlier [66] to determine if there are significant differences in Salmonella prevalence (presence/absence) and the litter used for raising broiler chicks. The significance of the model was established using a likelihood ratio test (R function ANOVA with argument test set to “Chisq”).…”