A survey of the levels of Campylobacter spp. contamination and prevalence of selected antimicrobial resistance determinants in fresh whole UK-produced chilled chickens at retail sale (non-major retailers)
Authors: Jorgensen Frieda , Charlett Andre , Swift Craig , Painset Anais , Corcionivoschi Nicolae 
Published: June 2021

Campylobacter spp. are the most common bacterial cause of foodborne illness in the UK, with chicken considered to be the most important vehicle for this organism. The UK Food Standards Agency (FSA) agreed with industry to reduce Campylobacter spp. contamination in raw chicken and issued a target to reduce the prevalence of the most contaminated chickens (those with more than 1000 cfu per g chicken neck skin) to below 10 % at the end of the slaughter process, initially by 2016. To help monitor progress, a series of UK-wide surveys were undertaken to determine the levels of Campylobacter spp. on whole UK-produced, fresh chicken at retail sale in the UK. The data obtained for the first four years was reported in FSA projects FS241044 (2014/15) and FS102121 (2015 to 2018). The FSA has indicated that the retail proxy target for the percentage of highly contaminated raw whole retail chickens should be less than 7% and while continued monitoring has demonstrated a sustained decline for chickens from major retailer stores, chicken on sale in other stores have yet to meet this target. This report presents results from testing chickens from non-major retailer stores (only) in a fifth survey year from 2018 to 2019. In line with previous practise, samples were collected from stores distributed throughout the UK (in proportion to the population size of each country). Testing was performed by two laboratories - a Public Health England (PHE) laboratory or the Agri-Food & Biosciences Institute (AFBI), Belfast. Enumeration of Campylobacter spp. was performed using the ISO 10272-2 standard enumeration method applied with a detection limit of 10 colony forming units (cfu) per gram (g) of neck skin. Antimicrobial resistance (AMR) to selected antimicrobials in accordance with those advised in the EU harmonised monitoring protocol was predicted from genome sequence data in Campylobacter jejuni and Campylobacter coli isolates The percentage (10.8%) of fresh, whole chicken at retail sale in stores of smaller chains (for example, Iceland, McColl’s, Budgens, Nisa, Costcutter, One Stop), independents and butchers (collectively referred to as non-major retailer stores in this report) in the UK that are highly contaminated (at more than 1000 cfu per g) with Campylobacter spp. has decreased since the previous survey year but is still higher than that found in samples from major retailers. 8 whole fresh raw chickens from non-major retailer stores were collected from August 2018 to July 2019 (n = 1009). Campylobacter spp. were detected in 55.8% of the chicken skin samples obtained from non-major retailer shops, and 10.8% of the samples had counts above 1000 cfu per g chicken skin. Comparison among production plant approval codes showed significant differences of the percentages of chicken samples with more than 1000 cfu per g, ranging from 0% to 28.1%. The percentage of samples with more than 1000 cfu of Campylobacter spp. per g was significantly higher in the period May, June and July than in the period November to April. The percentage of highly contaminated samples was significantly higher for samples taken from larger compared to smaller chickens. There was no statistical difference in the percentage of highly contaminated samples between those obtained from chicken reared with access to range (for example, free-range and organic birds) and those reared under standard regime (for example, no access to range) but the small sample size for organic and to a lesser extent free-range chickens, may have limited the ability to detect important differences should they exist. Campylobacter species was determined for isolates from 93.4% of the positive samples. C. jejuni was isolated from the majority (72.6%) of samples while C. coli was identified in 22.1% of samples. A combination of both species was found in 5.3% of samples. C. coli was more frequently isolated from samples obtained from chicken reared with access to range in comparison to those reared as standard birds. C. jejuni was less prevalent during the summer months of June, July and August compared to the remaining months of the year. Resistance to ciprofloxacin (fluoroquinolone), erythromycin (macrolide), tetracycline, (tetracyclines), gentamicin and streptomycin (aminoglycosides) was predicted from WGS data by the detection of known antimicrobial resistance determinants. Resistance to ciprofloxacin was detected in 185 (51.7%) isolates of C. jejuni and 49 (42.1%) isolates of C. coli; while 220 (61.1%) isolates of C. jejuni and 73 (62.9%) isolates of C. coli isolates were resistant to tetracycline. Three C. coli (2.6%) but none of the C. jejuni isolates harboured 23S mutations predicting reduced susceptibility to erythromycin. Multidrug resistance (MDR), defined as harbouring genetic determinants for resistance to at least three unrelated antimicrobial classes, was found in 10 (8.6%) C. coli isolates but not in any C. jejuni isolates. Co-resistance to ciprofloxacin and erythromycin was predicted in 1.7% of C. coli isolates. 9 Overall, the percentages of isolates with genetic AMR determinants found in this study were similar to those reported in the previous survey year (August 2016 to July 2017) where testing was based on phenotypic break-point testing. Multi-drug resistance was similar to that found in the previous survey years. It is recommended that trends in AMR in Campylobacter spp. isolates from retail chickens continue to be monitored to realise any increasing resistance of concern, particulary to erythromycin (macrolide). Considering that the percentage of fresh, whole chicken from non-major retailer stores in the UK that are highly contaminated (at more than 1000 cfu per g) with Campylobacter spp. continues to be above that in samples from major retailers more action including consideration of interventions such as improved biosecurity and slaughterhouse measures is needed to achieve better control of Campylobacter spp. for this section of the industry. The FSA has indicated that the retail proxy target for the percentage of highly contaminated retail chickens should be less than 7% and while continued monitoring has demonstrated a sustained decline for chickens from major retailer stores, chicken on sale in other stores have yet to meet this target.