Longitudinal study of prevalence and antimicrobial resistance of thermotolerant Campylobacter spp. in German organic meat chicken farms

ABSTRACT Widespread prevalence of fluoroquinolone-resistant Campylobacter spp. in meat chicken is a major concern for public health. We examined the prevalence and antimicrobial resistance of thermotolerant Campylobacter spp. in 14 German organic meat chicken farms rearing slow-growing broilers, male layer hybrids, or dual-purpose cockerels in a longitudinal study. Most farms participated with four subsequent flocks. Each flock was sampled three times: approximately 1 month after hatching (before outdoor access), 2 weeks after first outdoor access, and at the end of the fattening period. Strikingly, most flocks were already Campylobacter -positive before first outdoor access. At the end of the fattening period, 98% of all flocks were positive, with C. jejuni being the predominant species. Antimicrobial resistance of 405 C. jejuni and 79 C. coli revealed overall high levels of ciprofloxacin and tetracycline resistance but absence of macrolide resistance. Ertapenem resistance was observed in individual farms. Generalized linear mixed models with random factors for farm and flocks within farm were used to assess predictors for the occurrence of ciprofloxacin- and tetracycline-resistant C. jejuni . Season, fattening type, and the interaction of sampling time point and fattening type were significant fixed effects. Results for flocks within farms showed clustering effects (ICC CIP = 0.447; ICC TET = 0.412). Whole-genome sequencing of representative isolates confirmed great overall genetic variety, with farm- or fattening type-dependent dissemination of certain multi-locus sequence types. ST21 clonal complex for sequenced C. jejuni and ST828 clonal complex for sequenced C. coli were most commonly detected. IMPORTANCE Campylobacter spp. are major foodborne pathogens associated with the consumption and handling of chicken meat. This longitudinal study provides further insight into the prevalence and antimicrobial resistance of thermotolerant C. jejuni and C. coli in German organic meat chicken farms, a growing sector with strict limitations on antibiotic treatment. We included multiple flocks of farms fattening either slow-growing broilers, male layer hybrids, or dual-purpose cockerels to account for a variety of fattening types. Consequently, we were able to demonstrate significant differences in the occurrence of ciprofloxacin- and tetracycline-resistant C. jejuni based on fattening type, sampling time point, and season. Our findings highlight the successful spread and persistence of ciprofloxacin-, tetracycline-, and ertapenem-resistant C. jejuni and C. coli among all three types of organic meat chicken regardless of the lack of antibiotic treatment.