The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014


European Food Safety Authority
EFSA Journal
EFSA Journal 2016;14(2):4380 [207 pp.].

EFSA and ECDC wish to thank the members of the Scientific Network for Zoonoses Monitoring Data (EFSA) and the Food- and Waterborne Diseases and Zoonoses Network (ECDC) who provided the data and reviewed the report and the members of the Scientific Network for Zoonoses Monitoring Data, for their endorsement of this scientific output. Also, the contribution of EFSA staff members: Pierre-Alexandre Belœil, Beatriz Guerra, Anca-Violeta Stoicescu, Kenneth Mulligan, Krisztina Nagy and Mirena Ivanova, the contributions of ECDC staff member: Therese Westrell, and the contributions of EFSA’s contractor: Christopher Teale (Animal and Plant Health Laboratories Agency – United Kingdom), for the support provided to this scientific output.

European Centre for Disease Prevention and Control
Scientific Report of EFSA
On request from
European Commission
Question Number
9 February 2016
11 February 2016
Last Updated
11 March 2016. This version replaces the previous one/s.
European Food Safety Authority (EFSA), Parma, Italy
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The data on antimicrobial resistance in zoonotic and indicator bacteria in 2014, submitted by 28 EU Member States (MSs), were jointly analysed by EFSA and ECDC. Resistance in zoonotic Salmonella and Campylobacter species from humans, animals and food, and resistance in indicator Escherichia coli as well as meticillin-resistant Staphylococcus aureus in animals and food was assessed. ‘Microbiological’ resistance was assessed using epidemiological cut-off (ECOFF) values; for some countries, quantitative data on human isolates were interpreted in a way which corresponds closely to the ECOFF-defined ‘microbiological’ resistance. In Salmonella from humans, high proportions of isolates were resistant to ampicillin, sulfonamides and tetracyclines, whereas resistance to third-generation cephalosporins and to fluoroquinolones remained generally low, although it was markedly higher in some serovars commonly associated with broilers and turkeys. In Salmonella and Escherichia coli isolates from broilers, fattening turkeys and meat thereof, resistance to ampicillin, (fluoro)quinolones, tetracyclines and sulfonamides was frequently detected, whereas resistance to third-generation cephalosporins was uncommon. For the first time, presumptive extended spectrum beta-lactamase (ESBL)-/AmpC-/carbapenemase production in Salmonella and Escherichia coli was monitored in poultry. The occurrence of ESBL-/AmpC-producers was low, and carbapenemase-producers were not detected. Resistance to colistin was observed at low levels in Salmonella and Escherichia coli from poultry and meat thereof. In Campylobacter from humans, a high to very high proportion of isolates were resistant to ciprofloxacin and tetracyclines, whereas resistance to erythromycin was low to moderate. Resistance to fluoroquinolones in some MSs was extremely high; in such settings, the effective treatment options for human enteric Campylobacter infection may be significantly reduced. High resistance to ciprofloxacin and tetracyclines was observed in Campylobacter isolates from broilers and broiler meat, whereas much lower levels were recorded for erythromycin. Co-resistance to critically important antimicrobials in both human and animal isolates was generally uncommon, but very high to extremely high MDR levels were observed in some Salmonella serovars. A minority of Salmonella isolates from animals belonging to a few serovars (notably Kentucky and Infantis) exhibited high-level resistance to ciprofloxacin. 


Zoonoses are infections that are transmissible between animals and humans. Infections can be acquired directly from animals, via environmental exposure or through the ingestion of contaminated foodstuffs. The severity of these diseases in humans can vary from mild symptoms to life-threatening conditions. Zoonotic bacteria that are resistant to antimicrobials are of particular concern, as they might compromise the effective treatment of infections in humans. Data from the EU Member States (MSs) are collected and analysed in order to monitor the occurrence of antimicrobial resistance (AMR) in zoonotic bacteria isolated from humans, animals and food in the European Union (EU).

For 2014, 28 MSs reported data on AMR in zoonotic bacteria to the European Food Safety Authority (EFSA), and 21 MSs submitted data to the European Centre for Disease Prevention and Control (ECDC). In addition, three other European countries provided information. The enhanced monitoring of AMR in bacteria from food and food-producing animals set out in the Commission Implementing Decision 2013/652/EU was successfully implemented in reporting MSs and non-MSs in the EU during 2014. In accordance with the legislation, the 2014 AMR data on food and food-producing animals specifically targeted different poultry populations and meat derived thereof. EFSA and ECDC performed the analyses of the data, the results of which are published in this EU Summary Report on AMR. Data on resistance were reported regarding Salmonella and Campylobacter isolates from humans, poultry and meat thereof, whereas data on indicator Escherichia coli isolates were related only to poultry and meat derived thereof. Some MSs also reported data on the occurrence of meticillin-resistant Staphylococcus aureus (MRSA) in animals and food; the antimicrobial susceptibility of MRSA isolates was additionally reported by two countries.

The quantitative data on AMR in isolates from humans, poultry and meat thereof were assessed using harmonised epidemiological cut-off values that define ‘microbiological’ resistance, i.e. reduced susceptibility to the antimicrobials tested, as well as using clinical breakpoints (CBPs), where considered appropriate. The categorical (qualitative) data on AMR in isolates from humans interpreted by using CBPs were aligned with ‘microbiological’ resistance by combining ‘clinically resistant’ and ‘intermediate resistant’ isolates into a non-susceptible group. Isolates from different sources should only be directly compared when methods and interpretive criteria are comparable.

For the first time, all MSs reported AMR data on poultry and meat thereof at the isolate level. This enabled analysis of multi-drug resistance (MDR) and co-resistance patterns to critically important antimicrobials in both human and animal isolates at the EU level but also at country level. In addition, for all bacterial species, AMR data could be analysed at the production-type level, such as broilers and laying hens of Gallus gallus and fattening turkeys, which allows the analysis of the data to be fine-tuned. More specifically, reporting data at isolate level allowed characterisation of important patterns of resistance, enabling Salmonella serovars to be linked to particular resistance patterns and to identify high-level resistance to fluoroquinolones and important resistance phenotypes in both Salmonella and indicator E. coli. The information published in this report provides an overview of resistance in most MSs with detailed consideration of certain important aspects.

Highlights of this report include the continued monitoring of the spread of certain highly resistant Salmonella serovars. Two serovars in particular, S. Infantis and S. Kentucky, contribute significantly to the overall numbers of multidrug-resistant Salmonella in Europe. Both serovars display high-level resistance to ciprofloxacin, which is an important public health concern because ciprofloxacin is a common first-line treatment for invasive salmonellosis in humans.

The introduction of Commission implementing Decision 2013/652/EU with revised panels of antimicrobials to be tested has been timely, preceding recent reports of emergence of transferable colistin and erythromycin resistance in Asia (Liu et al., 2015; Wang et al., 2015). The continually evolving threat from emerging resistance underlines the need to review the data collected, interpret the findings and assess trends. This report has attempted to highlight some of the most important findings in 2014, but space constraints mean that it is necessarily selective.

The inclusion within the harmonised monitoring scheme of a supplementary panel of antimicrobials, to be tested when certain resistances to an initial panel of antimicrobials are detected, enabled detailed screening of resistance to three carbapenem compounds. No resistance to meropenem was detected and this is a crucial finding, because carbapenems are critically important in human medicine. Only nine E. coli isolates from broilers and one from fattening turkeys isolated in 6 MSs showed resistance to ertapenem, and all these isolates presented a putative extended spectrum beta-lactamase (ESBL) or AmpC phenotype. These isolates are being further investigated.

The supplementary testing also allowed, for the first time, detailed characterisation of the beta-lactam resistance phenotypes occurring in Salmonella and indicator E. coli. It enabled further phenotypic characterisation of third-generation cephalosporin and carbapenem resistance in Salmonella and indicator E. coli, by inferring presumptive profiles of ESBL-/AmpC-/carbapenemase-producers. The occurrence of ESBL-/AmpC-producers in Salmonella and indicator E. coli from poultry was assessed as being at low levels. It also showed that S. Infantis in Italy and S. Heidelberg in the Netherlands have probably each acquired a different mechanism of third-generation cephalosporin resistance (an ESBL enzyme in S. Infantis and an AmpC enzyme in S. Heidelberg) and have subsequently spread within each MS.

antimicrobial resistance, zoonotic bacteria, indicator bacteria, ESBL
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