The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2011

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Article
European Food Safety Authority
EFSA Journal
EFSA Journal 2013;11(5):3196 [359 pp.].
doi
10.2903/j.efsa.2013.3196
Acknowledgements

EFSA and ECDC wish to thank the members of the Task Force on Zoonoses Data Collection and the Food and Waterborne Disease Network who provided the data and reviewed the report. Also, the contribution of EFSA’s staff members: Pierre-Alexandre Belœil, Pia Mäkelä, Patrizia Oelker, Anca Stoicescu, Lucia Senini, Anne-Laure Mouffle, Ilaria Inverardi, Francesca Riolo and Kenneth Mulligan, the contributions of ECDC’s staff members: Robert Whittaker, Therese Westrell and Liselott Diaz Högberg, and the contributions of EFSA’s contractors: the Animal Health and Veterinary Laboratory Agency of the United Kingdom: Christopher Teale, Lucy Brunton, Tanya Cheney, Daisy Duncan, Peter Sewell, Ian Hillis and Ruth Blackwell and the University of Hasselt: Stijn Jaspers and Marc Aerts, as well as the reviewer: Björn Bengtsson, for the support provided to this scientific output.

European Centre for Disease Prevention and Control
Type
Scientific Report of EFSA
On request from
EFSA
Question Number
EFSA-Q-2012-00429
Approved
15 aprile 2013
Published
16 maggio 2013
Affiliation
European Food Safety Authority (EFSA), Parma, Italy; European Centre for Disease Prevention and Control (ECDC), Stockholm , Sweden
Note
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Abstract

The antimicrobial resistance data among zoonotic and indicator bacteria in 2011, submitted by 26 European Union Member States, were jointly analysed by the European Food Safety Authority and the European Centre for Disease Prevention and Control. Data covered resistance in zoonotic Salmonella and Campylobacter isolates from humans, food and animals, and in indicator Escherichia coli and enterococci isolates from animals and food. Data on methicillin-resistant Staphylococcus aureus in animals and food were also presented. Resistance in isolates from humans were mainly interpreted using clinical breakpoints, while animal and food isolate resistance was interpreted using epidemiological cut-off values. Resistance was commonly found in isolates from humans, animals and food, although disparities in resistance were frequently observed between Member States. High resistance levels were recorded to ampicillin, tetracyclines and sulfonamides in Salmonella isolates from humans, while resistance to third-generation cephalosporins and fluoroquinolones remained low. In Salmonella and indicator Escherichia coli isolates from fowl, pigs, cattle and meat thereof, resistance to ampicillin, tetracyclines and sulfonamides was also commonly detected, while resistance to third-generation cephalosporins was low. Moderate to high resistance to (fluoro)quinolones was observed in Salmonella isolates from turkeys, fowl and broiler meat. In Campylobacter isolates from human cases, resistance to ampicillin, ciprofloxacin, nalidixic acid and tetracyclines was high, while resistance to erythromycin was low to moderate. High resistance to ciprofloxacin, nalidixic acid and tetracyclines was observed in Campylobacter isolates from fowl, broiler meat, pigs and cattle, whereas much lower levels were observed for erythromycin and gentamicin. Among the indicator enterococci isolates from animals and food, resistance to tetracyclines and erythromycin was commonly detected. The report also presents for the first time results on multi-resistance and co-resistance to critically important antimicrobials in both human and animal isolates. Very few isolates from animals were co-resistant to critically important antimicrobials.

Summary

Zoonoses are infections and diseases that are transmissible between animals and humans. Infection can be acquired directly from animals, or through the ingestion of contaminated foodstuffs. The severity of these diseases in humans can vary from mild symptoms to life-threatening conditions. The zoonotic bacteria that are resistant to antimicrobials are of special concern since they might compromise the effective treatment of infections in humans. In order to follow the occurrence of antimicrobial resistance in zoonotic bacteria isolated from animals and food in the European Union, information is collected and analysed from the European Union Member States.

In 2011, 26 Member States submitted information on the occurrence of antimicrobial resistance in zoonotic bacteria to the European Commission and the European Food Safety Authority, and 21 Member States submitted information to the European Centre for Disease Prevention and Control. In addition, three other European countries provided information. Assisted by its contractors, the Animal Health and Veterinary Laboratories Agency in the United Kingdom and the University of Hasselt in Belgium, the European Food Safety Authority and the European Centre for Disease Prevention and Control analysed the data, the results of which are published in this European Union Summary Report on antimicrobial resistance. Information on resistance was reported regarding Salmonella and Campylobacter isolates from human cases, food and animals, whereas data on indicator Escherichia coli and indicator enterococci isolates related only to animals and food. Information was reported by some Member States on the occurrence of methicillin-resistant Staphylococcus aureus in animals and food; the antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates was additionally reported by two countries. Data on antimicrobial resistance in isolates from human cases were mainly interpreted by using clinical breakpoints, while the quantitative data on antimicrobial resistance in isolates from food and animals were interpreted using harmonised epidemiological cut-off values that detect microbiological resistance.

The reporting of antimicrobial resistance data at isolate-based level by an important number of Member States has allowed the first analysis at the European Union level of multi-resistance and co-resistance patterns to critically important antimicrobials in both human and animal isolates, which is a new feature of the present report. Also, for certain bacterial species, antimicrobial resistance data could be analysed at the production-type level, such as broilers and laying hens of Gallus gallus, which allows the analysis of the data to be fine-tuned.

Antimicrobial resistance was commonly detected in isolates of Salmonella and Campylobacter from human cases as well as from food-producing animals and food in the European Union. This was also the case for indicator (commensal) Escherichia coli and enterococci isolated from animals and food. For many of the antimicrobials, the levels of resistance varied greatly between different Member States.

In the European Union, the occurrence of resistance in Salmonella isolates from cases of salmonellosis in humans was high for ampicillin, tetracyclines and sulfonamides and moderate for nalidixic acid and streptomycin, with high levels of multi-drug resistance observed in some countries. However, resistance to the critically important antimicrobials for human medicine, cefotaxime (a third-generation cephalosporin) and ciprofloxacin (a fluoroquinolone), was relatively low, although for ciprofloxacin reported resistance levels were higher in countries where epidemiological cut-off values were used as the interpretive criteria. Co-resistance to ciprofloxacin and cefotaxime among Salmonella isolates was low. The resistance levels also differed substantially between serovars, with higher resistance to ciprofloxacin and nalidixic acid observed in Salmonella Enteritidis than in Salmonella Typhimurium and the opposite for the other antimicrobials. There was a high level of resistance to ampicillin, ciprofloxacin, nalidixic acid and tetracyclines among Campylobacter isolates from human cases, with high and very high levels of multi-drug resistance observed in some countries. However, relatively low resistance was recorded to erythromycin, which is the clinically most important antimicrobial for treatment of Campylobacteriosis in humans. In addition, co-resistance to ciprofloxacin and erythromycin was low among Campylobacter jejuni isolates.

The high proportions of Salmonella, Campylobacter and indicator Escherichia coli isolates exhibiting resistance to fluoroquinolones (ciprofloxacin) remain of concern. In Salmonella spp. isolates of food and animal origin, the highest occurrence of resistance to ciprofloxacin was noted in turkeys, fowl (Gallus gallus) and broiler meat, where the proportion of resistant isolates varied between 29 % and 50 % in the reporting Member State group. Ciprofloxacin resistance was recorded more often in broilers than in laying hens. Three Member States demonstrated a significant increasing trend for ciprofloxacin and nalidixic acid resistance and one a decreasing trend for both antimicrobials in Salmonella species from Gallus gallus over the period 2005 to 2011. Considering the indicator Escherichia coli isolates, the levels of ciprofloxacin resistance observed in isolates from broilers and pigs were 53.1 % and 8.3 %, respectively. Furthermore, high to extremely high resistance to fluoroquinolones was commonly observed in Campylobacter isolates from Gallus gallus and broiler meat, as well as from pigs and cattle, at levels ranging from 36 % to 78 %.

Resistance to the third-generation cephalosporin cefotaxime was observed in Salmonella isolates from Gallus gallus, turkeys, pigs, cattle and meat derived from broilers, at very low or low levels varying between 0 % and 3 %, as well as in indicator Escherichia coli isolates from Gallus gallus, pigs and cattle at levels ranging from <1 % to 6.4 %. Resistance to erythromycin was detected in Campylobacter isolates from Gallus gallus, poultry meat and pigs at levels of 2 % to 25 %.

Among Salmonella isolates from meat and animals, resistance to tetracyclines, ampicillin and sulfonamides was reported at levels of 7 % to 61 % and it was higher in isolates from pigs and turkeys than in those from broilers, laying hens and cattle. Resistance to ciprofloxacin and nalidixic acid was higher in Salmonella isolates from broilers and turkeys (33–50 %) than it was in isolates from laying hens, pigs or cattle (1–13 %). In isolates of Campylobacter from meat and animals, resistance was commonly detected to tetracyclines at levels up to 75 %, whereas much lower resistance was reported to gentamicin (levels lower than 7 %).

Among indicator Escherichia coli from broilers and pigs, resistance to tetracyclines, ampicillin and sulfonamides was commonly reported at levels of 37 % to 57 %, resistance levels being lower in laying hens (14 % to 18 %). In the case of cattle, levels of resistance to these antimicrobials fell within the range 20 % to 74 % in younger age groups, mainly fattening veal calves, but values were much lower in older cattle, mainly adult cows. In general, resistance levels were lower among isolates from cattle and layers than in isolates from broilers and pigs.

Among indicator enterococci, resistance to tetracyclines and erythromycin was common in isolates from Gallus gallus, pigs and cattle at levels of 23 % to 79 %, the resistance being the lowest for isolates from cattle. Resistance to vancomycin continued to be detected, albeit at very low levels (maximum 0.7 %), in enterococcal isolates from animals.

Multi-resistance (reduced susceptibility to at least three antimicrobial classes according to epidemiological cut-off values) was high in Salmonella isolates from broilers, turkeys and pigs and in indicator Escherichia coli isolates from broilers and pigs in those countries reporting isolate-based data. However, co-resistance to the clinically important antimicrobials ciprofloxacin and cefotaxime was detected in very few isolates of Salmonella species and indicator Escherichia coli. Multi-resistance was generally low in Campylobacter jejuni isolates from broilers, and co-resistance to ciprofloxacin and erythromycin was either not detected or recorded at low levels.

Several statistically significant national trends in resistance levels in isolates from animals and food were observed. Among Salmonella isolates more decreasing than increasing trends were found, whereas, in the case of Campylobacter, the statistically significant national trends were mostly increasing.

Keywords
Antimicrobial resistance, zoonotic bacteria, indicator bacteria
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EFSA - European Food Safety Authority , ECDC — European Centre for Disease Prevention and Control
Corporate author
EFSA - European Food Safety Authority , ECDC — European Centre for Disease Prevention and Control
Themes
Medical and biological research, Food technology and food safety
ISBN number
978-92-9199-552-3
Catalogue number
TM-AF-13-001-EN-C
Price
€ 10.00
Number of Pages
359
Order status
Available