The amount of antimicrobial resistance in bacteria found in pork and chicken on sale in the United Kingdom has been revealed by a Food Standards Agency survey.

Antimicrobial resistance (AMR) was detected in a proportion of all the types of bacteria examined, with resistance to the most clinically important drugs generally more prevalent in chicken isolates than pork.

However, the Food Standards Agency (FSA) said risk of acquiring AMR related bacterial infections from these foods is low, provided they are cooked and handled hygienically.

The survey done in September and October 2017 determined the prevalence of AMR in pathogenic and hygiene indicator bacteria isolated from fresh and frozen chicken for sale as whole birds or portions, and fresh ground pork on retail sale in the United Kingdom. Forty samples in the study had a non-UK approval code, only five chicken samples and no pork mince were from outside the European Union.

Antibiotics are used in agriculture to treat or prevent disease. This may increase the risk of antimicrobial resistance in pathogenic bacteria or organisms in the animal gut or farm environment. Meat may become contaminated with antimicrobial-resistant pathogens from the animal gut during slaughter, or through cross-contamination from the environment, whilst fruit and vegetables may be tainted from the environment or irrigation water.

A review of AMR in the food chain by the FSA in 2016 found there was a lack of data on prevalence in British-produced food, leading to difficulty in monitoring trends or producing risk assessments for the exposure of consumers.

Steve Wearne, director of food policy at the FSA, said the emergence and spread of AMR poses a significant global threat in terms of public health and economic impact.

“As well as reducing antibiotic use on farms we also need to understand the role that food plays in AMR and we are working with the Quadram Institute to understand how resistance arises and how resistant bacteria survive and are transmitted through the food chain. The use of antibiotics in the poultry meat sector declined by 82 percent between 2012 and 2017 and antibiotic use in UK pigs has halved between 2015 and 2017,” he said.

Salmonella and Campylobacter sampling results
A total of 339 samples of raw chicken and 342 samples of raw pork mince from retailers in England, Wales, Scotland and Northern Ireland were collected. They were produced by 63 different establishments. Most are in the UK, but four in Poland and the Netherlands, three in Denmark and one each in Spain, Ireland and Germany.

These were tested for E. coli, including ESBL-producing E. coli, Klebsiella spp. and enterococci, as well as Campylobacter spp. for chicken samples and Salmonella spp. in pork. One isolate of each bacterial type from each sample was used to determine the minimum inhibitory concentration (MIC) for a range of antimicrobials.

For some samples, additional Campylobacter isolates were examined to assess the variation in resistance between multiple isolates from the same sample of chicken. Whole Genome Sequencing further characterized all Salmonella isolates and a selection of E. coli and Klebsiella isolates that showed resistance to multiple antibiotic groups.

Salmonella spp. were detected in five of 342 pork mince samples, of which four were Salmonella Typhimurium and one Salmonella Derby. The four samples positive for Salmonella Typhimurium came from the same UK processing plant, with three bought from two different outlets of the same supermarket chain and one from a separate supermarket.

All four Salmonella Typhimurium isolates were resistant to ampicillin and tetracycline and had reduced susceptibility to sulfamethoxazole, with one showing resistance to chloramphenicol, whilst the Salmonella Derby isolate was susceptible to all antimicrobials except sulfamethoxazole.

Campylobacter spp. were detected in 85 of 339, for 25 percent, of chicken samples with one whole chicken giving a result of greater than 1000 cfu/g. Campylobacter spp. were detected more frequently in whole chickens, 42 out of 120 (42/120), and leg/wing portions, with 21 out of 73 samples testing positive. Breast meat was lower, with 19 out of 132 samples were positive. All 34 frozen samples were negative for the pathogen.

Determination of MICs was performed for 157 Campylobacter jejuni and 45 Campylobacter coli isolates from 79 samples. Of the Campylobacter coli isolates 46.7 percent (21/45) were resistant to ciprofloxacin, three resistant to erythromycin and 60 percent (27) resistant to tetracycline.

For the Campylobacter jejuni isolates 38.9 percent (61/157) were resistant to ciprofloxacin, twelve were resistant to erythromycin and 61.8 percent (97) resistant to tetracycline. All isolates were sensitive to gentamicin and only one Campylobacter coli isolate was resistant to streptomycin.

Of 66 samples from which Campylobacter jejuni was detected, ciprofloxacin resistant Campylobacter jejuni were detected in 25 of them, erythromycin resistant in six samples and tetracycline resistant in 39 samples. Of 21 samples were Campylobacter coli was detected, ciprofloxacin resistant Campylobacter coli were detected in eight of them, erythromycin resistant in three and tetracycline resistant in 11 samples (52 percent).

Multidrug resistance defined as reduced susceptibility to at least three unrelated antimicrobial classes was found in four Campylobacter coli (8.9 percent of isolates) and one Campylobacter jejuni from five samples.

E. coli and Klebsiella findings
E. coli were also detected at levels of at least 20 cfu/g more frequently in chicken samples (165/339) than in pork mince (35/342).

Of isolates examined for MIC determination, a higher percentage of those from chicken had resistance to c fluoroquinolones such as ciprofloxacin (34/131) and nalidixic acid (33/131) as well as gentamicin (nine) compared to those from pork (12/94; three and zero respectively). Resistance to chloramphenicol and tetracycline occurred more in isolates from pork (68/94 and 22/94) than from chicken (48/131 and 9 of 131).

Resistance to three or more groups of antimicrobials was seen in 56.5 percent (74/131) and 55.3 percent (52/94) of chicken and pork isolates, respectively.

E. coli organisms demonstrating the ESBL phenotype were detected in 16/342 of pork and 28/339 of chicken samples. Results from retail chicken showed a decrease in samples positive for ESBL-producing E. coli compared to other UK studies, which found that 29.7 percent in 2016 and 65.4 percent in 2013/2014 of samples were positive.

Klebsiella species were detected more frequently in pork mince (127/342) than chicken (22/339). Of 85 Klebsiella isolates examined for MIC determination, rates of resistance were lower than in E. coli isolates for all antimicrobials tested, except ampicillin, to which the species are intrinsically resistant.

Gwyn Jones, chair of the Responsible Use of Medicines in Agriculture (RUMA) Alliance, said the research would help identify additional interventions to reduce antimicrobial resistant bacteria in food.

“Our focus is on reducing, refining or replacing antibiotic use; while some livestock sectors have already achieved extraordinary results, there is definitely more to do in others. It’s important to recognize that antibiotic resistance is a naturally-occurring phenomenon which happens as bacteria defend themselves against attack,” he said.

“Resistant bacteria can be found anywhere and everywhere, and any use of antibiotics in human or animal medicine can lead to the development of resistance. However, cutting antibiotic use doesn’t necessarily cut the levels of resistant bacteria found, and that is why this study will prove valuable over time as more datasets are added.”

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