Longitudinal and cross-sectional sampling and whole genome sequencing of <i>Campylobacter</i> in a chicken abattoir reveal highly dynamic population structure

<i>Campylobacter</i> is a leading cause of human gastroenteritis worldwide and is commonly identified in poultry products. Current knowledge of its dissemination patterns in poultry production largely relies on the less sensitive traditional genotyping methods. In this study, whole-genome sequencing was applied to 324 <i>Campylobacter</i> isolates sampled from a chicken abattoir in the Greater Vancouver area throughout 2020. Core genome multi-locus sequence typing analysis revealed a highly diverse and dynamic <i>Campylobacter</i> population containing 27 distinct lineages. A wide range of plasmids was characterized, and a high prevalence of antibiotic resistance was observed among these isolates. Distinct subpopulations were identified in 10 lineages, suggesting that some <i>Campylobacter</i> populations may have diversified within the local agricultural environment. Some lineages were frequently reintroduced to the abattoir, suggesting the potential presence of hidden <i>Campylobacter</i> reservoirs upstream of slaughter. Comparisons between biological and environmental samples suggest a high probability of between-batch cross-contamination. Locally sourced public <i>Campylobacter</i> isolates showed strong genomic correlations with the lineages identified in this study. Notably, lineages 1629a and 1629b were identified to have persisted within the local poultry production ecosystem for several years, explaining their recurrent detection. In conclusion, this study enhances our understanding of <i>Campylobacter</i> population dynamics in the chicken abattoir environment, providing insights for controlling this foodborne pathogen in poultry production systems.IMPORTANCEUsing whole-genome sequencing, this study revealed a highly diverse and dynamic <i>Campylobacter</i> population within the chicken abattoir. The high prevalence of antibiotic resistance marked the critical need for surveillance in this region. The findings highlighted the likely existence of a hidden common source of <i>Campylobacter</i> upstream in the poultry production chain, which significantly contributes to the repeated introduction of the same lineages into the abattoir. Given the frequent reintroductions, the current understanding of <i>Campylobacter</i> persistence in the abattoir environment (up to 21 days) may require revision. Additionally, batch-to-batch dissemination of <i>Campylobacter</i> strains during processing is highly possible. A robust geographic association was also observed between the <i>Campylobacter</i> population in the abattoir and the local community. In sum, this study provides insights into the dynamics of <i>Campylobacter</i> contamination in the poultry production chain, offering guidance for improving prevention and control strategies.