Proximity to Other Commercial Turkey Farms Affects Colonization Onset, Genotypes, and Antimicrobial Resistance Profiles of Campylobacter spp. in Turkeys: Suggestive Evidence from a Paired-Farm Model

Abstract

Campylobacter is a leading foodborne pathogen, and poultry products are major vehicles for human disease. However, determinants impacting Campylobacter colonization in poultry remain poorly understood, especially with turkeys. Here, we used a paired-farm design to concurrently investigate Campylobacter colonization and strain types in two turkey breeds (Hybrid and Nicholas) at two farms in eastern North Carolina. One farm (the Teaching Animal Unit [TAU]) was a university teaching unit at least 40 km from commercial turkey farms, while the other (SIB) was a commercial farm in an area with a high density of turkey farms. Day-old birds were obtained from the same breeder flock and hatchery and placed at TAU and SIB on the same day. Birds were marked to identify turkey breed and then commingled on each farm. TAU birds became colonized 1 week later than SIB and had lower initial Campylobacter levels in the cecum. Interestingly, Campylobacter genotypes and antimicrobial resistance profiles differed markedly between the farms. Most TAU isolates were resistant only to tetracycline, whereas multidrug-resistant isolates predominated at SIB. Multilocus sequence typing revealed that no Campylobacter genotypes were shared between TAU and SIB. A bovine-associated genotype (sequence type 1068 [ST1068]) predominated in Campylobacter coli from TAU, while SIB isolates had genotypes commonly encountered in commercial turkey production in the region. One multidrug-resistant Campylobacter jejuni strain (ST1839) showed significant association with one of the two turkey breeds. The findings highlight the need to further characterize the impact of farm-specific factors and host genetics on antimicrobial resistance and genotypes of C. jejuni and C. coli that colonize turkeys.IMPORTANCE Colonization of poultry with Campylobacter at the farm level is complex, poorly understood, and critically linked to contamination of poultry products, which is known to constitute a leading risk factor for human campylobacteriosis. Here, we investigated the use of a paired-farm design under standard production conditions and in the absence of experimental inoculations to assess potential impacts of farm and host genetics on prevalence, antimicrobial resistance and genotypes of Campylobacter in commercial turkeys of two different breeds. Data suggest impacts of farm proximity to other commercial turkey farms on the onset of colonization, genotypes, and antimicrobial resistance profiles of Campylobacter colonizing the birds. Furthermore, the significant association of a specific multidrug-resistant Campylobacter jejuni strain with turkeys of one breed suggests colonization partnerships at the Campylobacter strain-turkey breed level. The study design avoids potential pitfalls associated with experimental inoculations, providing novel insights into the dynamics of turkey colonization with Campylobacter in actual farm ecosystems.

Keywords: Campylobacter; antimicrobial resistance; colonization; genotype; turkey.