The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in

Transcription

1 EFSA Journal 2010; 8(7):1658 SCIENTIFIC REPORT OF EFSA The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in European Food Safety Authority 2, 3 European Food Safety Authority (EFSA), Parma, Italy ABSTRACT Zoonoses are infections that are transmissible between animals and humans. Zoonotic bacteria that are resistant to antimicrobials are of special concern since they might compromise the effective treatment of infections in humans. For the year 2008, 25 European Union Member States and two other countries submitted information on the occurrence of antimicrobial resistance in zoonotic bacteria originating from animals and food to the European Commission and to the European Food Safety Authority. Quantitative and qualitative data on antimicrobial resistance was reported regarding Salmonella, Campylobacter, indicator Escherichia coli and indicator enterococci isolates from poultry, pigs and cattle as well as from meat. The quantitative data was analysed by using epidemiological cutoff values defining resistance. Resistance to commonly used antimicrobials, such as tetracycline, ampicillin and sulfonamides were frequently found among the isolates tested. For some antimicrobials, large differences in the occurrence of resistance were observed between Member States. The reported high occurrence of fluoroquinolone resistance in Salmonella isolates from poultry and in Campylobacter isolates from poultry, pigs and cattle as well as from broiler meat is of concern, since fluoroquinolones are defined as critically important antimicrobials in human medicine. Some Member States also reported resistance to third generation cephalosporins and macrolides, which are also antimicrobial groups of critical importance in human medicine. KEY WORDS Antimicrobial resistance, food, animals, Salmonella, Campylobacter, Escherichia coli, enterococci. 1 On request of EFSA, Question No EFSA-Q , issued on 15 June Correspondence: zoonoses@efsa.europa.eu. 3 Acknowledgement: EFSA wishes to thank the members of the Task Force on Zoonoses Data Collection that endorsed and reviewed this report: Andrea Ammon, Marta Bedriova, Veronica Cibin, Susan Chircop, Georgi Chobanov, Jürg Danuser, Kris De Smet, Matthias Hartung, Birgitte Helwigh, Merete Hofshagen, Simona Iannetti, Sarolta Idei, Patrícia Inácio, Eva Kukk, Elina Lahti, Lesley Larkin, Peter Much, Edith Nagy, Iona Neghirla, Lisa O Connor, Rob Van Oosterom, Jacek Osek, Manca Pavšič, Christodoulos Pipis, Saara Raulo, Tatiana Ribakova, Jose Luis Saez Llorente, Julien Santolini, Petr Šatrán, Snieguole Sceponaviciene, Joseph Schon, Ana María Troncoso González, Kilian Unger, Luc Vanholme, Dimitris Vourvidis. Also the contributions of Hanne-Dorthe Emborg, Antonio Vieira and Frank Aarestrup, as well as EFSA s staff members: Pierre-Alexandre Belœil, Elena Mazzolini, Francesca Riolo and Kenneth Mulligan, for the support provided to this EFSA scientific output is gratefully acknowledged. Suggested citation: European Food Safety Authority; The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in EFSA Journal. [261 pp.]. doi: /j.efsa Available online: European Food Safety Authority,

2 EFSA Journal 2010; 8(7):1658 2

3 THE COMMUNITY SUMMARY REPORT 1 Antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2008 Issued on 15 June 2010 Published on 6 July 2010 For citation purposes: The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2008, EFSA Journal 2010; 8(7):1658. EFSA Journal 2010; 8(7):1658 3

4 DOI: /j.efsa EFSA Journal 2010; 8(7):1658 4

5 FOREWORD About EFSA The European Food Safety Authority (EFSA), located in Parma, Italy, was established and funded by the European Community as an independent agency in 2002 following a series of food scares that caused the European public to voice concerns about food safety and the ability of regulatory authorities to protect consumers. In close collaboration with national authorities and in open consultation with its stakeholders, EFSA provides objective scientific advice on all matters with a direct or indirect impact on food and feed safety, including animal health and welfare and plant protection. EFSA is also consulted on nutrition in relation to Community legislation. EFSA s work falls into two areas: risk assessment and risk communication. In particular, EFSA s risk assessments provide risk managers European Union (EU) institutions with political accountability, i.e. the European Commission, the European Parliament and the Council) with a sound scientific basis for defining policy-driven legislative or regulatory measures required to ensure a high level of consumer protection with regard to food and feed safety. EFSA communicates to the public in an open and transparent way on all matters within its remit. Collection and analysis of scientific data, identification of emerging risks and scientific support to the European Commission, particularly in the case of a food crisis, are also part of EFSA s mandate, as laid down in the founding Regulation (EC) No 178/ of 28 January About the report Based on Article 33 in the Regulation (EC) 178/2002, EFSA s Zoonoses unit is responsible for examining data on zoonoses, antimicrobial resistance and food-borne outbreaks collected from the Member States in accordance with Directive 2003/99/EC 5 and for preparing the Community Summary Report from the results. Regarding antimicrobial resistance data from , this Community Summary Report was produced in collaboration with the National Food Institute, Technical University of Denmark, contracted by EFSA. The contributions of Hanne-Dorthe Emborg, Antonio Vieira, Pia Christiansen, Eliza Bielak, Frank Aarestrup, Pierre-Alexandre Belœil and Elena Mazzolini in the preparation of this report are gratefully acknowledged. For more information about EFSA, please contact: European Food Safety Authority Largo N. Palli 5/A I Parma Italy Tel: Fax: zoonoses@efsa.europa.eu 4. Regulation (EC) No 178/2002 of the European Parliament and of the Council as regards the number and names of the Scientific Panels of the European Food Safety Authority, OJ L 60, , p Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EECOJ L 325, , p EFSA Journal 2010; 8(7):1658 5

6 EFSA Journal 2010; 8(7):1658 6

7 SUMMARY Zoonoses are infections and diseases that are transmissible between animals and humans. The 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, information is collected and analysed from all European Union Member States. In 2008, 25 Member States submitted information on the occurrence of antimicrobial resistance in zoonotic bacteria to the European Commission and the European Food Safety Authority. In addition, two countries that were not European Union Member States provided information for the report. Assisted by its contractor, the Technical University of Denmark, the European Food Safety Authority analysed all the data, the results of which are published in this Community Summary Report. Information on antimicrobial resistance was reported regarding Salmonella, Campylobacter, indicator Escherichia coli, and indicator enterococci isolates from animals and food. The quantitative data on antimicrobial resistance were interpreted using harmonised epidemiological cut-off values defining the resistant isolates. This makes the data more comparable between reporting countries. Resistance to antimicrobials was commonly found among Salmonella, Campylobacter, and indicator E. coli and enterococci isolates from animals and food in the EU. For many tested antimicrobials, large differences in the occurrence of resistance were observed between the Member States. Among Salmonella isolates, resistance to the commonly used antimicrobials of tetracycline, ampicillin and sulfonamide were frequently reported, and the proportion of resistant isolates in animals varied between 13%-47% in the reporting MS group. The resistance levels were higher in isolates from pigs and cattle compared to isolates from fowl. However, resistance to ciprofloxacin and nalidixic acid was highest among Salmonella isolates from Gallus gallus where it reached 18%-19%, at reporting MS group level. Antimicrobial resistance in Campylobacter isolates was more common than in Salmonella isolates from food and animals. Resistance to ciprofloxacin and nalidixic acid varied between 34%-62% in the reporting MS group, and were highest among Campylobacter isolates from Gallus gallus and broiler meat. Within indicator E. coli isolates, resistance to tetracycline, ampicillin and sulfonamide were common and reported resistance levels ranged from 18% to 55% in the reporting MS group. Resistance levels were lowest among E. coli isolates from cattle. Resistance to ciprofloxacin and nalidixic acid in E. coli isolates varied between 3% and 46%, and were highest for isolates from fowl. Among indicator enterococci isolates, resistance to tetracycline and erythromycin were common, varying from 27% to 71%. Resistance to vancomycin was also recorded among the enterococci isolates. The observed high ciprofloxacin resistance levels in Salmonella, Campylobacter and indicator E. coli isolates are of concern, since fluoroquinolones are critically important antimicrobials in human medicine. Other critically important antimicrobial groups in human medicine include macrolides and third generation cephalosporins and some resistance to these antimicrobial groups were also recorded among the Salmonella, Campylobacter, indicator E. coli and enterococci isolates tested.. EFSA Journal 2010; 8(7):1658 7

8 TABLE OF CONTENTS Summary Introduction Main findings Main conclusions on the Community Summary Report on antimicrobial resistance Zoonotic and indicator agent-specific summaries Materials and methods Antimicrobial susceptibility data available in Data reported under Directive 2003/99/EC in Antimicrobials for susceptibility testing Antimicrobials for susceptibility testing of Salmonella Antimicrobials for susceptibility testing of Campylobacter Antimicrobials for susceptibility testing of Escherichia coli Antimicrobials for susceptibility testing of enterococci Data description and analysis Antimicrobial resistance in Salmonella - quantitative data Poultry and broiler meat Fowl (Gallus gallus) Meat from broilers (Gallus gallus) Pigs and pig meat Pigs Meat from pigs Cattle (bovine animals) Overview of the findings of antimicrobial resistance in Salmonella at reporting MS group level, Antimicrobial resistance in Campylobacter - quantitative data Poultry and broiler meat Fowl (Gallus gallus) Meat from broilers (Gallus gallus) Pigs Cattle (bovine animals) Overview of the findings on antimicrobial resistance in Campylobacter at reporting MS group level, Antimicrobial resistance in indicator Escherichia coli - quantitative data Poultry Pigs and pig meat Pigs Pig meat Cattle (bovine animals) Antimicrobial resistance in enterococci - quantitative data Fowl (Gallus gallus) Pigs Cattle (bovine animals) Overview of the findings on enterococci resistance at reporting MS group level, EFSA Journal 2010; 8(7):1658 8

9 TABLE OF CONTENTS 8. Antimicrobial resistance among Salmonella isolates from animals and food in 2008, qualitative data Poultry and broiler meat Fowl (Gallus gallus) Meat from broilers Turkeys Pigs and pig meat Pigs Meat from pigs Cattle References Appendices Appendix 1. List of abbreviations, Member States and other reporting countries, Definitions Appendix 2.1 MIC distributions of Salmonella Appendix 2.2 Salmonella quantitative data Appendix 2.3 Salmonella qualitative data Appendix 3.1 MIC distributions of Campylobacter Appendix 3.2 Campylobacter quantitative data Appendix 4.1 MIC distributions of indicator Escherichia coli Appendix 4.2 Escherichia coli quantitative data Appendix 5.1 MIC distributions of indicator enterococci Appendix 5.2 Enterococci quantitative data EFSA Journal 2010; 8(7):1658 9

10 EFSA Journal 2010; 8(7):

11 INTRODUCTION 1. Introduction EFSA Journal 2010; 8(7):

12 1. INTRODUCTION The antimicrobial agents used for food-producing animals are frequently the same or belong to the same classes as those used in human medicine (Aarestrup et al., 2008). Resistant bacteria that may develop and be carried by food-producing animals can spread to people (mainly via foods but also by water and by direct animal contact). Examples include Campylobacter, Escherichia coli, Salmonella, Enterococcus and Staphylococcus aureus. If these bacteria are resistant to commonly used antibiotics, then this causes an added problem for people acquiring these infections. Also of importance, the genes that encode this antibiotic resistance may be transferred to other bacterial species, and many of these latter bacteria may reside for longer periods in people s bowels or on their skin (EFSA, 2008b). Continuous monitoring of antimicrobial consumption and resistance in different food animal reservoirs is a prerequisite for the understanding of the dissemination of resistance and for planning targeted interventions. (Franklin et al., 2001, White et al., 2001, Aarestrup, 2004; McEwen et al., 2006). To address the need for the standardised monitoring of antimicrobial resistance in animals and food, the European Food Safety Authority (EFSA) has, on request by the European Commission, prepared detailed specifications for harmonised monitoring schemes on antimicrobial resistance. An expert working group established under the Task Force on Zoonoses Data Collection recommended concrete guidelines for the monitoring of antimicrobial resistance in animal populations initially among Salmonella and Campylobacter (EFSA, 2007), but later also in indicator Escherichia coli and enterococci isolates (EFSA, 2008a) for use in all 27 EU Member States (MSs). These published reports include detailed protocols on sampling strategies, methods for susceptibility testing, antimicrobials to be tested, criteria for categorising isolates as susceptible or non-susceptible, quality control and data to be reported. According to Directive 2003/99/EC on the monitoring of zoonoses and zoonotic agents, MSs are obliged to monitor and report antimicrobial resistance in Salmonella and Campylobacter isolates from animals and food. The monitoring and reporting of resistance data from the indicator organisms E. coli and enterococci, is voluntary. The monitoring and reporting of antimicrobial resistance information on Salmonella isolates from poultry populations and pigs sampled in the framework of national Salmonella control programmes are harmonised with Commission Decision 2007/407/EC 4. One of the main issues when comparing data between countries has been the use of different interpretative criteria in different countries. Using a single universal threshold to achieve both the detection of the early stages of resistance development within a bacterial population, and to predict the outcome of therapy, will continue to cause confusion. Breakpoints for clinical purposes are defined against a background of data, including therapeutic indications, clinical response data, dosing schedules, pharmacokinetics, and pharmacodynamics, which might differ between countries (see text box hereafter for a detailed explanation). Thus, to avoid confusion the term epidemiological cut-off value, has been established to separate between the original wild-type population and isolates that have developed reduced susceptibility to a given antimicrobial agent (Kahlmeter et al., 2003). In the EFSA reports, such cut-off values have been consistently recommended. In the Community Summary Report on antimicrobial resistance from 2004 to 2007 (EFSA, 2010) epidemiological cut-off values for Minimum Inhibitory Concentrations (MIC) and inhibition zone diameters were used for the first time to define resistant Salmonella, Campylobacter, E. coli and enterococci isolates. This has improved the comparability of data over time at country level and comparisons between countries. The same epidemiological cut-off values are used in this report. In this report, Campylobacter, Salmonella, E. coli and enterococci antimicrobial susceptibility data reported to EFSA for the year 2008 were analysed, and all quantitative data were interpreted using epidemiological cutoff values. 4. Commission Decision 2007/407/EC on a harmonised monitoring of antimicrobial resistance in Salmonella in poultry and pigs, OJ L 153, , p. 26. EFSA Journal 2010; 8(7):

13 INTRODUCTION 1. DEFINITION AND ESTABLISHMENT OF CUT-OFF VALUES The MIC breakpoint for an antimicrobial agent and a bacterial pathogen has traditionally been the threshold above which the pathogen is unlikely to respond to treatment with the specified antimicrobial agent. However, breakpoints are becoming contentious because of differing and incompatible demands being placed on what has hitherto been a single parameter. In particular, the needs of the clinician and the epidemiologist are different. What the clinician needs A clinician choosing an antimicrobial agent to treat humans or animals suffering from a specific infection needs to know that the compound chosen should be effective against the pathogen involved (although a clinical result may be affected by several other factors such as formulation and dosage). To this end, the MIC is ideally obtained for the pathogen in vitro, and this is compared with the predetermined clinical breakpoint to determine whether the organism is likely to respond in vivo. The clinical breakpoint should have taken account of the behaviour of the drug following administration, and assumes that if an isolate shows an MIC below the allocated clinical breakpoint for the pathogen, then a clinical response should be obtained if the drug is dosed as recommended and there are no other factors to affect the outcome. Conversely, an MIC for the target pathogen found to be above the clinical breakpoint indicates resistance and that an alternative treatment should be considered. Knowledge of the appropriate breakpoint (whether expressed as an MIC, or indirectly through an inhibition zone diameter) is even more important as doctors and veterinarians are increasingly expected to defend their choice of antimicrobial agent amid concerns about imprudent or indiscriminate use. What the epidemiologist needs The pattern of a MIC distribution (as well as that of an inhibition zone diameter distribution) often enables identification of two or more populations of micro-organisms that can be differentiated by the presence or absence of resistance factors. The wild-type susceptible subpopulation is assumed to show the antibiogram profile before any resistance has developed or has been acquired, and its distribution can be differentiated clearly from the resistant subpopulation. Where full resistance is achieved by a single step (perhaps through acquisition of a plasmid or a single point mutation), then an isolate may be expected to fall clearly into one of the two major subpopulations either fully susceptible, or having acquired the plasmid, fully resistant. However, where resistance is achieved in a series of steps then an isolate may fall somewhere in-between depending on the number of steps passed. A dividing or cut-off MIC value can thus be established to indicate the MIC above which the pathogen has some discernable reduction in susceptibility. This value should be based on an adequate number of isolates to ensure confidently that the wild-type population has been identified, and will normally be placed close to the wild-type population. The epidemiological cut-off value will often (although not always) be lower for MIC or higher for disk diameters than the breakpoint used for clinical prediction. Thus, a breakpoint set by clinical criteria may fail to identify emerging resistance, although it may be perfectly adequate to predict clinical efficacy. Conversely, a breakpoint set by epidemiological criteria may imply that a potential treatment would fail, yet in fact it could respond since it may fall below the clinical breakpoint for the particular agent and organism. The term breakpoint should be retained solely for clinical breakpoints and be distinguished from the epidemiological cut-off value, where the latter shows that a change away from the wild-type population may have occurred in a subpopulation. This terminology is used by the European Committee on Antimicrobial Sensitivity Testing (EUCAST; Kahlmeter et al., 2003). Universal adoption and understanding of such separate terminology would enable clinicians to choose appropriate treatment based on information relevant to the individual patient, yet would recognise that epidemiologists need to be aware of small changes in bacterial susceptibility which may indicate emerging resistance and allow for appropriate control measures to be considered. EFSA Journal 2010; 8(7):

14 EFSA Journal 2010; 8(7):

15 MAIN FINDINGS 2. Main findings EFSA Journal 2010; 8(7):

16 2. MAIN FINDINGS 2.1 Main conclusions on the Community Summary Report on antimicrobial resistance 2008 This report compiles and analyses data on antimicrobial resistance in Salmonella, Campylobacter, indicator E. coli and indicator enterococci isolates from animals and food that were reported by the European Union (EU) Member States (MSs) and two non-member States for the year Quantitative antimicrobial resistance data expressed as Minimum Inhibitory Concentrations (MIC) or inhibition zone diameters were interpreted using harmonised epidemiological cut-off values, which means that data are comparable as regards the limits used to define the resistant isolates. This enables a better comparison of data between reporting countries. In 2008, resistance to antimicrobials was commonly found among isolates of Salmonella, Campylobacter and the indicator E. coli and enterococci from animals and food in the EU. For most of the antimicrobials tested, large differences in the occurrence of resistance were observed between MSs. The differences observed between MSs may be partly due to real differences in the resistance situation but sometimes also because of differences in the monitoring system in place. Among Salmonella isolates, resistance to commonly used antimicrobials, tetracycline, ampicillin and sulfonamide, were frequently reported and resistance levels among reporting MSs were higher in isolates from pigs and cattle compared to isolates from fowl (Gallus gallus). These differences may be partly explained by the different serovar distribution among these animal species since S. Typhimurium, which is more common in pigs and cattle, is known to be more resistant to tetracycline, ampicillin and sulfonamide than S. Enteritidis, a serovar typically related to fowl. However, resistance to ciprofloxacin and nalidixic acid were higher among the Salmonella isolates from Gallus gallus when compared to isolates from pigs and cattle. Antimicrobial resistance in Campylobacter isolates from meat and animals was more common than in Salmonella isolates. Moreover, resistance was more frequently reported for C. coli isolates than C. jejuni isolates. Resistance to ciprofloxacin and nalidixic acid were the highest among Campylobacter isolates from Gallus gallus and broiler meat. Within indicator (commensal) E. coli isolates, resistance to tetracycline, ampicillin and sulfonamide were commonly recorded, and overall resistance levels were lowest among E. coli isolates from cattle when compared to isolates from Gallus gallus and pigs. Also, resistance to ciprofloxacin and nalidixic acid were reported for E. coli isolates and resistance levels were highest for isolates from Gallus gallus. Among indicator (commensal) enterococci isolates, resistance to tetracycline and erythromycin were common among the isolates from Gallus gallus, pigs and cattle. Some resistance to vancomycin was also recorded. The high resistance levels to ciprofloxacin reported in 2008 are of concern among Salmonella spp. isolates from Gallus gallus and broiler meat, and among Campylobacter isolates from Gallus gallus, broiler meat, pigs and cattle. Fluoroquinolones are critically important antimicrobials in human medicine and an increase in fluoroquinolone resistant bacteria in animals and food may compromise the effective treatment of food-borne bacterial infections in humans. Third generation cephalosporins and macrolides are also regarded as critically important antimicrobials in human medicine. In 2008, third generation cephalosporin resistance was mainly reported among Salmonella and E. coli isolates from Gallus gallus. Erythromycin (a macrolide) resistance was mostly detected among Campylobacter isolates and enterococci isolates from Gallus gallus, broiler meat, pigs and cattle. No major changes in the general occurrence of antimicrobial resistance in Salmonella, Campylobacter and indicator bacteria were observed in 2008 compared to the results in EFSA Journal 2010; 8(7):

17 MAIN FINDINGS Zoonotic and indicator agent-specific summaries Salmonella In 2008, information on antimicrobial resistance in Salmonella isolates from animals and food were reported by 22 MSs and two non-mss. In this report Salmonella spp. represents the overall occurrence of antimicrobial resistance in Salmonella in the different animal or food categories. Therefore some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and animal species. The spread of certain Salmonella serotypes and phage types within an animal population with a particular resistance pattern (clonal spreading) might also explain some of the differences in the occurrence of resistance observed between animal species. However, the selective pressure caused by the use of antimicrobials in animal populations might also contribute to the spread of resistant clones. In 2008, among Salmonella spp. isolates from fowl (Gallus gallus), the resistance levels to tetracycline, ampicillin and sulfonamide in the reporting MS group were 15%, 13% and 18%, respectively. Levels of resistance to ciprofloxacin and nalidixic acid were 18% and 19%, respectively, in the reporting MS group. Generally, large variations were observed between the resistance levels among reporting MSs. The resistance level for cefotaxime among reporting MSs was 4%. Resistance in S. Enteritidis isolates was generally lower than in all Salmonella spp. isolates from Gallus gallus. Resistance levels among S. Enteritidis isolates within the reporting MS group were 2% for tetracycline, ampicillin and sulfonamide, whereas ciprofloxacin and nalidixic acid resistance were 20% and 19%, respectively. In Salmonella isolates from broiler meat, resistance levels in the reporting MS group for tetracycline, ampicillin and sulfonamide were 23%, 30% and 28%, respectively. Ciprofloxacin and nalidixic acid resistance were also commonly reported with overall resistance levels of 43% and 44%, respectively. The resistance level for cefotaxime was 13%, but this was mostly due to one reporting MS. Among the Salmonella isolates from pigs, resistance levels in the reporting MS group were 47% for tetracycline, 34% for ampicillin and 46% for sulfonamide. Ciprofloxacin and nalidixic acid resistance levels were low, at 4% for both, and the resistance level for cefotaxime was 1%. Resistance to tetracycline, ampicillin and sulfonamide were commonly observed in Salmonella spp. from pig meat, with levels of 56%, 46%, and 56%, respectively, in the reporting MS group. Resistance to ciprofloxacin and nalidixic acid were 5% and 4%, respectively, whereas cefotaxime and ceftiofur resistance was rarely reported. In Salmonella isolates from cattle, resistance levels to tetracycline, ampicillin and sulfonamide in the reporting MS group were 24%, 20% and 23%, respectively. The reported resistance levels for ciprofloxacin and nalidixic acid were 5% for both. Ceftiofur, ceftazidime and cefotaxime resistance were not reported by MSs. Campylobacter In 2008, information on antimicrobial resistance in Campylobacter isolates from animals and food were reported by 22 MSs and two non-mss. Most of the data derived from poultry, pigs and cattle and meat thereof. Overall, reported levels of resistance in Campylobacter isolates from food and animals were higher than those reported in Salmonella isolates. Resistance was also generally more frequent among C. coli than among C. jejuni isolates. In the case of resistance to tetracycline, ciprofloxacin and nalidixic acid, there were large variations between reporting MSs. Among C. jejuni isolates from Gallus gallus, the occurrence of tetracycline, ciprofloxacin and nalidixic acid resistance among reporting MSs was high, 37%, 50% and 51%, respectively. The levels of resistance were 3% for erythromycin and 4% for gentamicin. In C. coli isolates from Gallus gallus, tetracycline, ciprofloxacin, and nalidixic acid resistance among the reporting MS group was very high reaching 53% 62%, and 61%, respectively. Erythromycin resistance at MS reporting level was 12% and gentamicin resistance level was 3% among C.coli isolates. EFSA Journal 2010; 8(7):

18 2. MAIN FINDINGS In the case of C. jejuni isolates from broiler meat, levels of resistance to tetracycline, ciprofloxacin and nalidixic acid among reporting MSs were 38%, 46% and 50%, respectively. Resistance to erythromycin was 6%. In C. coli isolates from pigs, tetracycline, ciprofloxacin and nalidixic acid resistance in the reporting MS group were 79%, 39% and 39%, respectively. Erythromycin resistance at MS reporting level was 25%. Among the C. jejuni isolates from cattle, resistance levels in the reporting MS group for tetracycline, ciprofloxacin and nalidixic acid were 28%, 34% and 34%, respectively, whereas for erythromycin it was 1%. Indicator Escherichia coli (commensal, indicator) In 2008, information on antimicrobial resistance in indicator E. coli isolates from animals and food were reported by 14 MSs. Most of the data derived from poultry, pigs and cattle and meat thereof. In E. coli isolates from Gallus gallus, resistance levels to tetracycline, ampicillin and sulfonamide were 40%, 42% and 37%, respectively, in the reporting MS group. Resistance levels for ciprofloxacin were 45%, for nalidixic acid 46% and for cefotaxime 9% in the reporting MS group. Overall, the occurrence of resistance to these antibiotics varied importantly between MSs. Among E. coli isolates from pigs, resistance levels in the reporting MS group were 55% for tetracycline, 27% for ampicillin and 32% for sulfonamide. Resistance to ciprofloxacin and nalidixic acid were both at 3% in the reporting MS group. No or very low resistance levels to third generation cephalosporins were detected. The occurrence of tetracycline, ampicillin, sulfonamide and streptomycin resistance varied considerably between MSs. Resistance to tetracycline, ampicillin and sulfonamide were commonly detected in E. coli isolates from pig meat, and resistance levels were 48%, 25% and 42%, respectively, in the reporting MS group. Generally, low to very low levels of nalidixic acid (3%), ciprofloxacin (3%) and cefotaxime (0%) resistance were observed at MS group level. In indicator E. coli isolates from cattle, resistance levels in the reporting MS group were 27% for tetracycline, 18% for ampicillin and 22% for sulfonamide. Resistance to ciprofloxacin and nalidixic acid were 10% and 6%, respectively, whereas in general, resistance to ceftiofur, cefotaxime and ceftazidime was rarely reported. Indicator enterococci (commensal, indicator) In 2008, information on antimicrobial resistance in enterococci isolates from animals and food was reported by nine MSs. Most of the data derived from poultry, pigs and cattle and meat thereof. A wide variation in reported resistance levels between MSs was observed. For E. faecium and E. faecalis isolates from Gallus gallus, resistance levels to tetracycline and erythromycin in the reporting MS group were respectively 47% and 45% in E. faecium, and 62% and 55% among E. faecalis. In E. faecium isolates from pigs, tetracycline and erythromycin resistance levels in the reporting MS group were 54% and 42%, respectively, and for E. faecalis the levels were 71% and 27%, respectively. In the case of E. faecium isolates from cattle, tetracycline and erythromycin, resistance levels were 37% and 32%, respectively. As cross-resistance is observed between avoparcin and the important human antimicrobial vancomycin, the use of avoparcin as a feed additive was banned in the EU in However, in 2008, vancomycin-resistant E. faecium and E. faecalis were still reported from Gallus gallus, pigs and cattle. In the reporting MS group between 0% and 3% vancomycin-resistant E. faecium and E. faecalis were reported. EFSA Journal 2010; 8(7):

19 MATERIALS AND METHODS 3. Materials and methods EFSA Journal 2010; 8(7):

20 3. MATERIALS AND METHODS 3. Materials and methods 3.1 Antimicrobial susceptibility data available in 2008 For the year 2008, 25 MSs and two non-mss collectively reported data on antimicrobial resistance in tested Salmonella and Campylobacter or commensal E. coli and commensal enterococci isolates from animals and food. Dilution and diffusion testing methods were used by reporting countries for susceptibility testing, and both quantitative and qualitative data were reported. Quantitative data reported as minimum inhibitory concentrations (MIC, measured in mg/l) were the number of isolates having a specific MIC value out of the total number of isolates tested, for each antimicrobial agent and in each specific food/animal category. Quantitative data reported as inhibition zone diameters (measured in millimetres) were the number of isolates having a specific diameter of inhibition zone out of the total number of isolates tested, for each antimicrobial agent and in each food/animal category. Qualitative data were reported as the number of resistant isolates out of the total number of isolates that were tested against each antimicrobial agent, in each food/animal category. A total of 23 MSs and two non-mss provided information on antimicrobial resistance in An overview of MSs reporting and data reported in 2008 is shown in Table MM1. In this report, quantitative results, determined by broth dilution method and disk diffusion, were reported and analysed together, while qualitative data were reported separately. The antimicrobial resistance data reported by MSs are presented and analysed in this report for Salmonella, Campylobacter and indicator E. coli and enterococci isolates from Gallus gallus, pigs and cattle, and in the case of Salmonella isolates also from turkeys. The report also includes data from Salmonella and Campylobacter isolates from meat from broilers, and Salmonella isolates from meat from pigs. These are the animal and food categories most frequently reported on. The data are included in the report if more than four MSs provided data for the bacterium animal/food category combination. Data from less than 10 tested isolates per MS are not included in this report. In case both quantitative and qualitative data were reported for a given animal/food population by a country, only the quantitative data are presented in this report. Also, in the case of qualitative results, data from less than 10 tested isolates per MS were not included in the report. For data reported only as qualitative, no cut-off values are applicable. As countries might not have used the same breakpoints, direct comparisons between the proportions of resistant isolates between MSs reporting only qualitative data should be interpreted with caution. Table MM1. MSs reporting data in 2008 and description of data included in the report. No of MSs and non- Data included in the report MSs reporting Quantitative data quantitative and/or qualitative data MIC test Disk diffusion test Qualitative data Salmonella 22 MSs + 2 non-mss 77,958 3,984 25,533 Campylobacter 22 MSs + 2 non-mss 28,052 5,742 - Indicator E. coli 15 MSs + 2 non-mss 50, Indicator enterococci 9 MSs + 2 non-mss 17, EFSA Journal 2010; 8(7):

21 MATERIALS AND METHODS Data reported under Directive 2003/99/EC in 2008 MSs generated data on antimicrobial susceptibility through the testing of bacteria isolated from animal/food samples collected through different schemes. Often the isolates tested constituted of a subsample of the isolates available at the National Reference Laboratory (NRL). Isolates might be gathered by different monitoring approaches, either by active monitoring of animals and foods, or in some cases, by passive monitoring based on diagnostic submissions of samples from clinical cases in animals, or from foods sampled on suspicion. In 2008, MSs reported the results of antimicrobial susceptibility testing of isolates from various animal species and from various food categories. Antimicrobial resistance was defined by MIC evaluations, performed either by broth or agar dilution methods, or disk diffusion method. Some MSs reported antimicrobial resistance data both as quantitative and qualitative data. Quantitative data determined by dilution method (i.e. MIC) and those by disk diffusion method (i.e. diameters of inhibition zones) were analysed for resistance to a number of antibiotics using respective harmonised epidemiological cut-offs, and reported together in the chapters dedicated to each microorganism. Qualitative data for Salmonella were analysed separately and are presented in Chapter 8. Data were provided in aggregated format, and therefore it was not possible to describe and analyse multiresistance among isolates. 3.2 Antimicrobials for susceptibility testing Among antimicrobials included in antimicrobial resistance national monitoring programmes, those incorporated in the analysis were selected based on their relative public health importance and as representatives of different antimicrobial classes and taking into account EFSA s reports on the harmonised monitoring and reporting of antimicrobial resistance data (EFSA, 2007, 2008a) Antimicrobials for susceptibility testing of Salmonella In 2008, both dilution and disk diffusion methods were used to test the susceptibility of Salmonella isolates from animals and food by MS. Tables MM2 and MM3 show the antimicrobials selected by the different countries for susceptibility testing. MIC distributions were made for the following antimicrobials: tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, ciprofloxacin, nalidixic acid, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin and streptomycin (Appendix 2.3). Data on Salmonella reported only as qualitative were presented in Chapter 8. However, despite exercising caution when comparing countries, it was anticipated that breakpoints would not have changed over time within a country and, therefore, comparisons of the proportion of resistant isolates over time within a country are possible. EFSA Journal 2010; 8(7):

22 3. MATERIALS AND METHODS Table MM2. Antimicrobials selected for susceptibility testing of Salmonella isolates by MS and non-ms reporting quantitative data as MIC distributions, in rd generation cephalosporins Country Amikacin Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Apramycin Cefotaxime Cefoxitin Ceftazidime Ceftiofur Ceftriaxon Cephalothin Chloramphenicol Ciprofloxacin Colistin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Spectinomycin Streptomycin Sulfamethoxazol Sulfisoxazol (sulfafurazol) Sulfonamide Tetracycline Trimethoprim Trimethoprim + Sulfamethoxazol Trimethoprim + Sulfonamides Austria Belgium Czech Republic Denmark Estonia Finland France Germany Ireland Italy Latvia Netherlands Norway Poland Portugal Slovakia Slovenia Spain Sweden Switzerland United Kingdom EFSA Journal 2010; 8(7):

23 MATERIALS AND METHODS 3. Table MM3. Antimicrobials selected for susceptibility testing of Salmonella isolates by MS and non- MS reporting quantitative data as disk inhibition zones, in 2008 Country 3rd generation cephalosporins Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Cefotaxime Cefpodoxime Ceftazidime Cephalothin Chloramphenicol Czech Republic Greece Hungary Romania Slovenia United Kingdom Ciprofloxacin Enrofloxacin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Streptomycin Sulfonamide Tetracycline Trimethoprim Trimethoprim + Sulfonamide Antimicrobials for susceptibility testing of Campylobacter In 2008, all quantitative Campylobacter data were reported as MIC values by dilution methods. Table MM4 shows the antimicrobials selected by the different countries for susceptibility testing. For the following antimicrobials MIC distributions were made: tetracycline, chloramphenicol, erythromycin, gentamicin, streptomycin, ciprofloxacin and nalidixic acid. (Appendix 3.2). These antimicrobials were selected for further description, based on public health relevance and as representatives of different antimicrobial classes. In this report antimicrobial resistance was reported for C. jejuni and C. coli. All qualitative data for Campylobacter were also reported as quantitative data. Table MM4. Antimicrobials selected for susceptibility testing of Campylobacter isolates by MS and non-ms reporting quantitative data as MIC distributions Country Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Chloramphenicol Ciprofloxacin Clarithromycin Colistin Erythromycin Florfenicol Austria Belgium Czech Republic Denmark Estonia Finland France Germany Hungary Ireland Italy Latvia Malta Netherlands Norway Poland Portugal Romania Slovakia Slovenia Spain Sweden Switzerland United Kingdom Gentamicin Meropenem Nalidixic acid Neomycin Oxolinic acid Spectinomycin Streptomycin Sulfamethoxazol Sulfonamides Tetracycline Tulathromycin EFSA Journal 2010; 8(7):

24 3. MATERIALS AND METHODS Antimicrobials for susceptibility testing of Escherichia coli In 2008, both dilution and diffusion methods were used to test the susceptibility of E. coli isolates from animals and food. Tables MM5 and MM6 show the antimicrobials selected by the different countries for susceptibility testing. In this report, mainly susceptibility data from animal isolates are presented. Due to very few countries reporting susceptibility data from food isolates, sufficient data were available only for the sampling category meat from pigs. MIC distributions were made for the following antimicrobials: tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, ciprofloxacin, nalidixic acid, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin and streptomycin, (Appendix 4.2). These antimicrobials were selected based on public health relevance and as representatives of different antimicrobial classes. In 2008, all qualitative data were also reported as quantitative data, thus no special subsection with qualitative E. coli data are presented in the 2008 report. Table MM5. Antimicrobials selected for susceptibility testing of Escherichia coli isolates by MS and non-ms reporting quantitative data as MIC distributions Country Amikacin Amoxicillin / Clavulanic acid Ampicillin Apramycin Cefotaxime Cefoxitin Ceftazidime Ceftiofur Ceftriaxon Cephalothin Chloramphenicol Ciprofloxacin Austria Denmark Estonia Finland France Germany Latvia Netherlands Norway Spain Sweden Switzerland Colistin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Spectinomycin Streptomycin Sulfamethoxazol Sulfisoxazol (sulfafurazol) Sulfonamide Tetracycline Trimethoprim Trimethoprim + Sulfamethoxazol Trimethoprim + Sulfonamides Table MM6. Antimicrobials selected for susceptibility testing of Escherichia coli isolates by MS and non-ms reporting quantitative data as disk inhibition zones Country 3rd generation cephalosporins Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Cefalexin Cefazolin Cefoperazone Cefotaxime Cefpodoxime Ceftazidime Cefuroxime Hungary Poland Portugal Romania Slovenia Cephalothin Chloramphenicol Ciprofloxacin Enrofloxacin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Streptomycin Sulfonamide Tetracycline Trimethoprim Trimethoprim + Sulfonamides EFSA Journal 2010; 8(7):

25 MATERIALS AND METHODS Antimicrobials for susceptibility testing of enterococci In 2008, enterococci susceptibility data were only reported using dilution method by MS. Table MM7 shows the antimicrobials selected by the different countries for susceptibility testing. In this report only susceptibility data from animal isolates are presented due to very few countries reporting susceptibility data from food isolates. For the following antimicrobials MIC distributions were made: tetracycline, chloramphenicol, ampicillin, erythromycin, streptomycin, vancomycin, quinupristin/dalfopristin, avilamycin and linezolid (Appendix 5.2). All qualitative data for E. faecium and E. faecalis were also reported as quantitative data. Table MM7. Antimicrobials selected for susceptibility testing of isolates of Enterococcus faecium and Enterococcus faecalis, by MS and non-ms reporting quantitative data as MIC distributions and disk inhibition zones Country Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Avilamycin Bacitracin Chloramphenicol Ciprofloxacin Clindamycin Daptomycin Erythromycin Flavofosfolipol Florfenicol Gentamicin Kanamycin Austria Denmark Estonia Finland France Hungary Netherlands Norway Spain Sweden Switzerland Linezolid Narasin Neomycin Nitrofurantoin Penicillin Quinupristin Quinupristin/ Dalfopristin Salinomycin Spectinomycin Streptomycin Tetracyclin Tetracycline Tigecycline Vancomycin Virginiamycin 3.3 Data description and analysis Methods to interpret, describe and analyse antimicrobial resistance data have been presented in detail in the antimicrobial report (EFSA, 2010). Typically, quantitative data were interpreted using epidemiological cut-off values presented in Decision 2007/407/EC for MIC data (corresponding to those published by EUCAST at the time of writing of the Decision) and those derived from the data reported by MSs under Directive 2003/99/EC for the years for inhibition zone diameters. Epidemiological cutoff values for MIC and inhibition zone diameters are given in Table MM8. In this report, antimicrobial resistance reported in tested Salmonella isolates were collapsed into Salmonella spp. for each country, year and food/animal category. In addition, whenever sufficient data had been transmitted by MSs for the different food/animal categories, the most prevalent Salmonella serovars, S. Enteritidis and S. Typhimurium, were also reported separately by food/animal category. Exceptions from this rule are quantitative data for the United Kingdom of Salmonella isolates from cattle which were not collapsed to Salmonella spp., whereas for Germany quantitative data of Salmonella isolates from broiler meat were not collapsed to Salmonella spp. For quantitative data, an isolate was defined as resistant for a selected antimicrobial when its MIC value (in mg/l) was above the cut-off or the disk diffusion diameter (in mm) was below the cut-off. The cut-off values for both MIC and disk diffusion are indicated in Table MM8. If qualitative data were submitted, the proportion of resistant isolates reported by countries were used, even though the countries may have used different resistance break points. Throughout the report the following definitions apply: level of antimicrobial resistance means the percentage of resistant isolates from the tested isolates; and MS reporting group means the MSs that provided data and were included in the relevant table for antimicrobial resistance data for the bacteria-food/animal category-antimicrobial combination. EFSA Journal 2010; 8(7):

26 3. MATERIALS AND METHODS Terms used to describe the antimicrobial resistance levels are: rare: <0.1% very low: 0.1% to 1% low: >1% to 10% moderate: >10% to 20% high: >20% to 50% very high: >50% to 70% extremely high: >70%. MIC distributions were presented as frequency tables by the number of tested isolates having the MIC in each test dilution (mg/l) of the antimicrobial. For each combination of micro-organism, antimicrobial, food/animal category and year of reporting, a summarising figure was calculated as the percentage of isolates being resistant among those tested. Variance is given by estimates of exact 95% (two-sided) confidence intervals for proportions based on binomial probability distributions as described in Armitage & Berry (2001). Where the minimum criteria were met, temporal trend graphs were generated showing resistance to different antimicrobials against micro-organisms from animals and food over the period, by plotting resistance percentages in susceptibility tested isolates for the year of sampling. Historical data for the period are available in appendices according to each micro-organism. MS-specific antimicrobial resistance levels for selected bacteria-food/animal category-antimicrobial combinations were plotted in maps for 2007, using ArcGIS 9.3. Whenever the 2007 resistance levels were not available, the 2006 resistance levels were used instead, as indicated by a footnote to the map. In the maps, resistance levels are presented with colours reflecting the continuous scale that takes decimals into account, whereas the labels reported on MS levels are rounded without decimal digits, therefore there might be some apparent discrepancies among map colours and resistance prevalence. Resistance levels were calculated based on quantitative data. If a country reported qualitative data, this country is shown on the map as having provided qualitative data but without any resistance percentage. Also, countries reporting data from less than 10 isolates for that specific combination were included in the qualitative data category. EFSA Journal 2010; 8(7):

27 MATERIALS AND METHODS 3. Table MM8. Epidemiological cut-off values used to interpret MIC distributions (mg/l) and inhibition zone diameter-distributions (mm) for bacteria from animals and food 1 Antimicrobial agent Salmonella E. coli E. faecium E. faecalis C. jejuni C. coli mg/l mm a) mg/l mm a) mg/l mg/l mg/l mg/l Ampicillin >4 <13 >8 <11 >4 >4 Apramycin >16 b) <16 >16 b) <13 Avilamycin >16 >8 Cefotaxime >0.5 >0.25 Ceftazidime >2 >0.5 Ceftiofur >2 <17 >1 <16 Chloramphenicol >16 <13 >16 <16 >32 >32 >16 >16 Ciprofloxacin 2 >0.06 >0.03 >1 >1 Erythromycin >4 >4 >4 >16 Florfenicol >16 <14 >16 <14 Gentamicin >2 <13 >2 >1 >2 Linezolid >4 >4 Nalidixic acid >16 <13 >16 <13 >16 >32 Neomycin >4 <13 >8 Spectinomycin <18 >64 <18 Streptomycin >32 <10 >16 <11 >128 >512 >2 >4 Sulfonamide >256 b) <13 >256 b) <13 Quinupristin/dalfopristin >1 Tetracycline >8 <13 >8 <14 >2 >2 >2 >2 Trimethoprim >2 >2 Vancomycin >4 >4 Note: a) Cut-off values were not defined by EUCAST, instead cut-off values defined by the EU-RL from disk diffusion distribution of MS data were used. b) Cut-off values were not defined by EUCAST, instead cut-off values defined by the EU-RL were used. 1. Based on the Report of the Task Force of Zoonoses Data Collection including a proposal for a harmonised monitoring scheme of antimicrobial resistance in Salmonella in fowl (Gallus gallus), turkeys and pigs and Campylobacter jejuni and C. coli in broilers, the EFSA Journal (2007), 96, 1-46 and the Report from the Task Force on Zoonoses Data Collection including guidance for harmonised monitoring and reporting of antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. from food animals. EFSA Journal (2008) 141: Ciprofloxacin disk diffusion data were all submitted as qualitative data not as quantitative data (i.e. inhibition zone diameters) therefore no disk diffusion cut-off values were calculated. EFSA Journal 2010; 8(7):

28 EFSA Journal 2010; 8(7):

29 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Antimicrobial resistance in Salmonella - quantitative data EFSA Journal 2010; 8(7):

30 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Antimicrobial resistance in Salmonella - quantitative data Twenty-two MSs and two non-mss (Norway and Switzerland) collectively reported quantitative data on antimicrobial resistance in Salmonella isolates tested from animals and food for susceptibility. The results of 77,958 MIC susceptibility tests and 3,984 disk diffusion susceptibility tests of Salmonella isolates were included in the analyses. The susceptibility test results on Salmonella isolates reported as qualitative data are presented in Chapter 8. Tables SA1-3 present the countries reporting MIC values and inhibition zones in Table SA1. Overview of countries reporting MIC distributions and disk inhibition zones on Salmonella spp. from various sampling origins in 2008 Method Dilution Diffusion Origin Meat from broilers Total number of MSs reporting 10 Countries MSs: AT, BE, CZ, IT, LV, PL, PT, SK, SI Non-MS: CH Meat from turkey 4 MSs: CZ, FI, IT, SI Meat from bovine animals 3 MSs: CZ, EE, IT Meat from pig 9 MSs: BE, CZ, DK, EE, FI, IT, LV, NL, SK Gallus gallus 18 MSs: AT, BE, CZ, DE, EE, ES, FI, FR, IE, IT, LV, NL, PL, PT, SE, SI, SK, UK Turkeys Pigs Cattle MSs: FI, IT, SK MSs: AT, CZ, DK, EE, ES, FI, FR, IE, IT, LV, NL, PL, PT, SE, SK, SI Non-MS: CH MSs: CZ, DK, EE, ES, FI, IT, NL, SE, SI, SK Non-MS: NO Meat from broilers 2 MSs: CZ, RO Meat from Turkey 1 MS: RO Meat from bovine animals 1 MS: RO Meat from pig 2 MSs: CZ, RO Gallus gallus 4 MSs: GR, HU, SI, UK Turkeys 1 MS: HU Pigs 2 MSs: HU, SI Cattle 2 MSs: HU, UK Table SA2. Overview of countries reporting MIC distributions and inhibition zones on Salmonella Typhimurium from various sampling origins in 2008 Method Dilution Diffusion Origin Total number of MSs reporting Countries Meat from broilers 4 MSs: BE, CZ, IT, PL Meat from bovine animals 2 MSs: CZ, IT Meat from pig 6 MSs: BE, CZ, DK, FI, IT, SK Meat from turkeys 3 MSs: FI, IT, SI Gallus gallus 12 MSs: AT, CZ, ES, FI, FR, IT, LV, NL, PL, SE, SI, SK Turkeys 3 MSs: FI, IT, SK Pigs Cattle 14 8 MSs: CZ, DK, EE, ES, FI, FR, IE, IT, LV, NL, PL, PT, SE, SK MSs: CZ, DK, EE, FI, IT, NL, SE, SK Non-MS: NO Meat from Turkey 1 MS: RO Meat from pig 2 MSs: CZ, RO Gallus gallus 1 MS: HU Pigs 1 MS: HU Cattle 1 MS: UK EFSA Journal 2010; 8(7):

31 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA3. Overview of countries reporting MIC distributions and inhibition zones on Salmonella Enteritidis from various sampling origins in 2008 Method Dilution Diffusion Origin Total number of MSs reporting Countries Meat from broilers 9 MSs: BE, CZ, DE, IT, LV, PL, PT, SI, SK Meat from bovine animals 2 MSs: CZ, IT Gallus gallus 15 MSs: AT, BE, CZ, DE, EE, ES, FR, IT, LV, NL, PL, PT, SI, SK, UK Pigs 5 MSs: CZ, EE, PL, SI, SK Cattle 1 MS: CZ Meat from broilers 2 MSs: CZ, RO Gallus gallus 4 MSs: GR, HU, SI, UK Turkeys 1 MS: HU Pigs 1 MS: SI Tables SA1-3 indicate that several countries reported quantitative antimicrobial resistance data for Salmonella. However, whenever less than 10 isolates from one country were available for susceptibility testing or less than 10 isolates per year and per sampling origin were reported, these data were not included in any further analyses. In this report, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. (covering all serovars) for each country, year and sampling origin. In addition, the most prevalent Salmonella serotypes S. Enteritidis and S. Typhimurium were reported separately when sufficient data were available. Exceptions to this rule are quantitative data from the United Kingdom where quantitative data of Salmonella isolates from cattle were not collapsed into Salmonella spp. Given this exception, Salmonella spp. represents the overall occurrence of antimicrobial resistance in Salmonella from the different sampling origins. For Salmonella, resistance for the following antimicrobials is analysed in detail: tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid. In addition, tables showing MIC distributions, occurrence of resistance and 95% confidence intervals for tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin, streptomycin, ciprofloxacin and nalidixic acid are presented in Appendix 2.1 on Salmonella. Where the minimum criteria were met, temporal trend graphs were generated showing resistance to different antimicrobials against Salmonella isolates from animals and food over the period, by plotting resistance percentages in susceptibility tested isolates for the year of sampling. Historical data for the period are available in Appendix 2.2. The spatial distributions of tetracycline, ampicillin and nalidixic acid resistance rates in Salmonella spp. from Gallus gallus, pigs and cattle are presented. For countries where 2008 resistance data were not available, 2007 resistance data were used. 4.1 Poultry and broiler meat Fowl (Gallus gallus) In this report fowl (Gallus gallus) includes data from breeding flocks, laying hen flocks and broiler flocks of Gallus gallus. In 2008, quantitative antimicrobial susceptibility data on Salmonella spp. from Gallus gallus from 18 MSs were included in the following antimicrobial resistance analyses. Resistance levels among Salmonella In 2008 among Salmonella spp., resistance levels to tetracycline, chloramphenicol, ampicillin and sulfonamide in the reporting MS group varied between 3% and 18%. Among Salmonella spp., resistance levels for ciprofloxacin and nalidixic acid were 18% and 19%, respectively; however, a large variation was EFSA Journal 2010; 8(7):

32 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA observed between reporting countries. In 2008, the resistance level for cefotaxime in the reporting group of 14 MSs was 4%. (Table SA4). The highest occurrence of cefotaxime resistance was reported in the Netherlands (13%) and Italy (12%); whereas in the remaining countries resistance varied between 0% and 1 %. Low levels of antimicrobial resistance were reported for most antimicrobials in S. Enteritidis isolates, and no resistance was reported for a number of antimicrobials in several countries. At reporting MS group level, resistance levels to tetracycline, chloramphenicol, ampicillin and sulfonamide varied between 0% and 2% (Table SA5). In general, the occurrence of ciprofloxacin and nalidixic acid resistance were higher, and in the reporting MS group, resistance levels for these antimicrobials were 20% for ciprofloxacin and 19% for nalidixic acid. The highest occurrence of ciprofloxacin resistance was reported by Spain (60%) followed by Portugal (58%), Italy (50%) and Poland (31%) (Table SA5). For nalidixic acid the highest occurrence of resistance was reported by Spain (58%) followed by Portugal (54%) and Poland (31%). Belgium, Germany and the United Kingdom reported no ciprofloxacin and nalidixic acid resistance among S. Enteritidis in Cefotaxime resistance was reported only in one isolate from the Netherlands (Table SA5). Reported resistance levels in S. Enteritidis were lower than those in Salmonella spp. from Gallus gallus. EFSA Journal 2010; 8(7):

33 EFSA Journal 2010; 8(7): Table SA4. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from Gallus gallus in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gallus gallus Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Belgium Czech Republic France Germany Greece Hungary Ireland Italy Latvia Netherlands Poland Portugal Slovakia Slovenia Spain Sweden United Kingdom Total (18 MSs) 2, , , , , , , , Note: In these tables, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.

34 EFSA Journal 2010; 8(7): Table SA5. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Enteritidis isolates from Gallus gallus in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gallus gallus Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Belgium Czech Republic France Germany Greece Hungary Italy Latvia Netherlands Poland Portugal Slovakia Slovenia Spain United Kingdom Total (16 MSs) 1, , Table SA6. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Typhimurium isolates from Gallus gallus, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gallus Gallus Tetracycline Chloramphenicol Ampicillin Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria France Netherlands Poland Spain Total (5 MSs) ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA

35 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Temporal trends in resistance among Salmonella spp. In several countries the occurrence of resistance among Salmonella spp. were at similar levels in 2008, as in In general, resistance among Salmonella spp. from Gallus gallus was higher compared to S. Enteritidis. However, one of the few exceptions was Spain where resistance to nalidixic acid and ciprofloxacin decreased from 65% and 69% in 2007 to 30% and 31% in 2008, respectively. From 2004 to 2008, resistance remained relatively low for most antimicrobials over time and did not vary considerably between countries (Figures SA3-8). Although the occurrence of resistance remained relatively stable over time in Salmonella spp. isolates, some changes were observed. Figure SA1: Trends in tetracycline resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark France Greece Hungary Italy Lithuania Netherlands Poland Slovakia Slovenia Spain Sweden UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

36 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA2: Trends in chloramphenicol resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark France Greece Hungary Italy Lithuania Netherlands Poland Slovakia Slovenia Spain Sweden UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Figure SA3: Trends in ampicillin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data % resistant isolates Austria Czech Republic Denmark France Greece Hungary Italy Lithuania Netherlands Poland Slovakia Slovenia Spain Sweden UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

37 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA4: Trends in sulfonamide resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark France Greece Hungary Italy Netherlands Poland Slovakia Slovenia Spain Sweden UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries years. Figure SA5: Trends in ciprofloxacin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data % resistant isolates Austria Czech Republic Denmark Italy Netherlands Poland Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

38 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA6: Trends in nalidixic acid resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark France Greece Hungary Italy Lithuania Netherlands Poland Slovakia Slovenia Spain Sweden UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

39 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Temporal trends in resistance among S. Enteritidis As for S. Enteritidis, low levels of resistance were reported for most antimicrobials, only trends in resistance to ciprofloxacin and nalidixic acid are presented (Figures SA7 and SA8). In 2008, the occurrence of ciprofloxacin and nalidixic acid resistance remained relatively unchanged in most countries compared to previous years. As previously described, the large increase in nalidixic acid resistance observed in the United Kingdom in 2006 was linked to a wide outbreak of nalidixic acid resistant S. Enteritidis PT1. Figure SA7: Trends in ciprofloxacin resistance in tested Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, , quantitative data 100 s te la o t is n ta is s re % Czech Republic Netherlands Poland Slovakia Spain Figure SA8: Trends in nalidixic acid resistance in tested Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic France Greece Lithuania Netherlands Poland Slovakia Slovenia Spain United Kingdom EFSA Journal 2010; 8(7):

40 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Spatial distribution of resistance among Salmonella The spatial distributions of tetracycline, ampicillin and nalidixic acid resistance among Salmonella spp. isolated from Gallus gallus in 2008 are shown in Figures SA9-11. Figures SA9-10 illustrate the relatively low occurrence of tetracycline and ampicillin resistance among Salmonella spp. in many reporting countries and absence of clear spatial distribution across the EU. For nalidixic acid, there is a tendency towards higher resistance rates in southern and eastern parts of the EU (Figure SA11). Figure SA9: Spatial distribution of tetracycline resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Denmark, Finland and Romania, 2007 data were used. EFSA Journal 2010; 8(7):

41 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA10: Spatial distribution of ampicillin resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Denmark, Finland and Romania, 2007 data were used. EFSA Journal 2010; 8(7):

42 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA11: Spatial distribution of nalidixic acid resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Denmark, Finland and Romania, 2007 data were used. EFSA Journal 2010; 8(7):

43 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Meat from broilers (Gallus gallus) In 2008, quantitative susceptibility data on Salmonella spp. isolates from broiler meat from 9 MSs and one non-ms were included in the following analyses of antimicrobial resistance. Resistance levels among Salmonella Resistance to tetracycline, ampicillin and sulfonamide varied between 23% and 30% (Table SA7) in the reporting MS group. Ciprofloxacin and nalidixic acid resistance was also commonly reported with resistance levels of 43% and 44%, respectively. In 2008, the lowest occurrence of ciprofloxacin (0%) and nalidixic acid (10%) resistance was reported from Switzerland, while the highest occurrence (77%) was reported for both antimicrobials from Latvia. The resistance levels to ceftiofur and cefotaxime were 6% and 13%, respectively. Belgium reported 26% cefotaxime resistance and 25% ceftazidime resistance, while Latvia and Italy, reported between 2% and 6% resistance to ceftiofur, cefotaxime and ceftazidime. In the remaining countries no resistance to these three cephalosporins was reported (Table SA7 and Appendix 2.1. Tables SA4a-b). As for Gallus gallus, resistance among S. Enteritidis from meat from broilers was lower than that reported among Salmonella spp. (Table SA8). Resistance levels were 2% (tetracycline), 3% (ampicillin) and 3% (sulfonamide) among S. Enteritidis. However, the moderate occurrence of resistance did not apply for ciprofloxacin and nalidixic acid for which resistance levels were 33% (ciprofloxacin) and 33% (nalidixic acid) in the reporting MS group. EFSA Journal 2010; 8(7):

44 EFSA Journal 2010; 8(7): Table SA7. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. from meat from broilers in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Meat from Broilers Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Belgium Czech Republic Italy Latvia Poland Portugal Romania Slovakia Total (9 MSs) Switzerland Note: In these tables, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years Table SA8. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Enteritidis from meat from broilers in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Meat from broilers Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Belgium Czech Republic Latvia Poland Portugal Romania Total (6 MSs) ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA

45 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Pigs and pig meat Pigs In 2008, quantitative data for Salmonella spp. in pigs from 15 MSs and one non-ms were included in the following antimicrobial resistance analyses. Resistance levels among Salmonella MIC distributions for Salmonella spp. from pigs are presented in Appendix 2.1 (Tables SA6a-c). In 2008, ampicillin, sulfonamide and tetracycline resistance varied considerably between MSs (Table SA9) and the average resistance levels in the reporting MS group were 34% for ampicillin, 46% for sulfonamide and 47% for tetracycline. In general, ciprofloxacin and nalidixic acid resistance were low in all MSs with 4% resistance levels for both antimicrobials. In Austria, Estonia, France and Slovenia no ciprofloxacin and nalidixic acid resistance was reported, in the remaining countries occurrence was between 1% and 19% (Table SA9 and Appendix 2.1, Table SA6c). The average resistance level was 0% for ceftiofur and 1% for cefotaxime. Several countries reported no cefotaxime and ceftazidime resistance, in the remaining countries occurrence ranged from 0.2% to 3.7%. Ceftiofur resistance was reported in 0.2% of the Danish isolates and in 2.2% of the isolates from Switzerland (Table SA9 and Appendix 2.1, Table SA6b). MIC distributions for S. Typhimurium from pigs are presented in Appendix 2.1 (Tables SA7a and 7b) and resistance to selected antimicrobials are presented in Table SA10. In general, the occurrence of resistance among S. Typhimurium was higher compared to Salmonella spp. with resistance levels in the reporting MS group being 51% for ampicillin, 58% for sulfonamide, 24% for chloramphenicol and 53% for tetracycline. As for Salmonella spp., moderate levels of ciprofloxacin and nalidixic acid resistance were reported from all countries and the resistance level was 3% for both ciprofloxacin and nalidixic acid. In S. Typhimurium from pigs, cefotaxime resistance among reporting MSs was 1%, ranging from zero in most reporting MSs to 11% and 8% in Spain and Portugal, respectively. In addition, only Denmark reported data for ceftiofur with 0.2% resistance among the 543 isolates tested. EFSA Journal 2010; 8(7):

46 EFSA Journal 2010; 8(7): Table SA9. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from pigs in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Czech Republic Denmark Estonia France Hungary Ireland Italy Netherlands Poland Portugal Slovakia Slovenia Spain Sweden Total (15 MSs) 2, , , , , , , ,380 4 Switzerland Note: In these tables, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Table SA10. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from pigs in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Czech Republic Denmark Hungary Ireland Italy Netherlands Portugal Slovakia Spain Sweden Total (10 MSs) ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA

47 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Temporal trends in resistance among Salmonella Figures SA12-14 show the large variation in the occurrence of tetracycline, ampicillin and sulfonamide resistance among Salmonella spp. from pigs in The figures SA12-17 also show that for some countries large differences in resistance were observed from 2007 to However, there are still countries where the occurrence of resistance remained unchanged compared to previous years. In general, decreasing trends over time in resistance among Salmonella spp. from pigs were mainly observed in reporting countries. Figure SA12: Trends in tetracycline resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia France Greece Hungary Ireland Italy Netherlands Poland Slovakia Slovenia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

48 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA13: Trends in chloramphenicol resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia France Greece Hungary Ireland Italy Netherlands Poland Slovakia Slovenia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Figure SA14: Trends in ampicillin resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia France Greece Hungary Ireland Italy Netherlands Poland Slovakia Slovenia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

49 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA15: Trends in sulfonamide resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia France Greece Hungary Ireland Italy Netherlands Poland Slovakia Slovenia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Figure SA16: Trends in ciprofloxacin resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Denmark Estonia Ireland Italy Netherlands Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

50 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA17: Trends in nalidixic acid resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia France Greece Hungary Ireland Italy Netherlands Poland Slovakia Slovenia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

51 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Spatial distribution of resistance among Salmonella The spatial distribution of tetracycline, ampicillin and nalidixic acid resistance among Salmonella spp. isolated from pigs in 2008 is shown in Figures SA Figures SA18-19 underline the large differences in tetracycline and ampicillin resistance rates observed between countries. However, no clear spatial distributions were observed. In most countries, a low occurrence of nalidixic acid resistance in Salmonella spp. from pigs was reported with no clear spatial distribution observed (Figure SA20). Figure SA18: Spatial distribution of tetracycline resistance among Salmonella spp. from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1.. For Germany, Greece and Romania,2007 data were used. EFSA Journal 2010; 8(7):

52 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA19: Spatial distribution of ampicillin resistance among Salmonella spp. from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Germany, Greece and Romania,2007 data were used. EFSA Journal 2010; 8(7):

53 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA20: Spatial distribution of nalidixic acid resistance among Salmonella spp. from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Germany, Greece and Romania,2007 data were used. EFSA Journal 2010; 8(7):

54 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Meat from pigs In 2008, quantitative data for Salmonella spp. from pig meat from five MSs were included in the following antimicrobial resistance analyses. Resistance levels among Salmonella In the reporting MS group, resistance to ampicillin, sufonamide and tetracycline was commonly observed in Salmonella spp. from pig meat, with resistance levels of 46% for ampicillin and 56% for tetracycline and sulfonamide (Table SA11 and Appendix 2.1, Table SA8). In general, a low occurrence of nalidixic acid and ciprofloxacin resistance was observed in all reporting countries with resistance rates at reporting MS level of 4% and 5%, respectively. The highest occurrences of ciprofloxacin (9%) and nalidixic acid (7%) resistance were observed in Italy and in Romania (Table SA11). Cefotaxime and ceftiofur resistance varied between 0% and 1% in reporting MSs; Denmark reported 0.8% cefotaxime and ceftiofur resistance, while Italy reported 0.5% ceftazidime resistance. (Appendix 2.1, Table SA8). Among S. Typhimurium from meat from pigs, the occurrence of resistance was higher for some antimicrobials compared to Salmonella spp. At reporting MS level, resistance levels for S. Typhimurium were 59% for ampicillin, 59% for sulfonamide and 52% for tetracycline (Table SA12). EFSA Journal 2010; 8(7):

55 EFSA Journal 2010; 8(7): Table SA11. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from meat from pigs in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Meat from pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Belgium Czech Republic Denmark Italy Romania Total (5 MSs) Note: In these tables, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Table SA12. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from meat from pigs in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Meat from pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Belgium Denmark Italy Romania Total (4 MSs) ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.

56 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.3 Cattle (bovine animals) Cattle cover in this report calves, dairy and beef cows and heifers. In 2008, quantitative data for Salmonella spp. in cattle from eight MSs were included in the following antimicrobial resistance analyses. Resistance levels among Salmonella Resistance to ampicillin, sulfonamide and tetracycline were commonly reported in Salmonella spp. Resistance in the reporting MS group was 24% for tetracycline, 20% for ampicillin and 23% for sulfonamide. As in previous years, a large variation in the occurrence of resistance was observed between countries, for example tetracycline resistance varied between 10% and 45% and sulfonamide resistance varied between 9% and 75% (Table SA13). Resistance rates for ciprofloxacin and nalidixic acid were both 5% at reporting MS level. The highest occurrence of ciprofloxacin and nalidixic acid resistance was observed in the Czech epublic with a value of 31%, followed by 21% nalidixic acid resistance in Hungary and 14% ciprofloxacin resistance in Italy. In the remaining countries, ciprofloxacin resistance varied between 0% and 9% (Table SA13). Ceftiofur, ceftazidime and cefotaxime resistance were not reported among Salmonella spp. in any of the countries reporting quantitative data (Table SA13, Appendix 2.1, Table SA9). Resistance rates for S. Typhimurium are reported in Table SA14. In some countries most or all of the Salmonella spp. isolates were S. Typhimurium, thus the reported occurrence of resistance in Salmonella spp. and S. Typhimurium were found to be quite similar. EFSA Journal 2010; 8(7):

57 EFSA Journal 2010; 8(7): Table SA13. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from cattle in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Cattle Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Czech Republic Denmark Finland Hungary Italy Netherlands Spain Sweden Totel (8 MSs) Note: In these tables, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Table SA14. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium from cattle in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Cattle Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Czech Republic Denmark Netherlands Sweden United Kingdom Total (5 MSs) ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.

58 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Temporal trends in resistance among Salmonella Figures SA21-25 show that for some antimicrobials there were large variations in resistance between countries in 2008 and for example, in Denmark and Italy, large decreases in resistance were observed for some antimicrobial agents from 2007 to The figures also illustrate trends in resistance to tetracycline, ampicillin, chloramphenicol, sulfonamide and nalidixic acid among Salmonella isolates from cattle from 2004 to In general, decreasing trends in resistance were mainly observed over time among Salmonella spp. from cattle. Figure SA21: Trends in tetracycline resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia Finland France Italy Netherlands Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

59 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA22: Trends in chloramphenicol resistance in Salmonella spp. from cattle in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia Finland France Italy Netherlands Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Figure SA23: Trends in ampicillin resistance in Salmonella spp. from cattle in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia Finland France Italty Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

60 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA24: Trends in sulfonamide resistance in Salmonella spp. from cattle in reporting MSs, , quantitative data % resistant isolates Czech Republic Denmark Estonia Finland France Italy Netherlands Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. Figure SA25: Trends in nalidixic acid resistance in Salmonella spp. from cattle in reporting MSs, , quantitative data 100 % resistant isolates Czech Republic Denmark Estonia Finland France Italy Netherlands Slovakia Spain Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries and years. EFSA Journal 2010; 8(7):

61 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Spatial distribution of resistance among Salmonella Figures SA26-28 present the spatial distributions of tetracycline, ampicillin and nalidixic acid resistance among Salmonella spp. from cattle in A large variation in tetracycline resistance was observed between reporting countries but no clear spatial distribution was evident (Figure SA26). For ampicillin the lowest occurrence of resistance was reported in Spain and in eastern Europe (Figure SA27). A low occurrence of nalidixic acid resistance was observed in most reporting countries (Figure SA28) with no clear spatial pattern. Figure SA26: Spatial distribution of tetracycline resistance among Salmonella spp. from cattle in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Estonia, France, Germany, Romania, Slovenia and Spain,2007 data were used. EFSA Journal 2010; 8(7):

62 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA27: Spatial distribution of ampicillin resistance among Salmonella spp. from cattle in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Estonia, France, Germany, Slovenia and Spain, 2007 data were used. EFSA Journal 2010; 8(7):

63 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA28: Spatial distribution of nalidixic acid resistance among Salmonella spp. from cattle in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. Since some Salmonella serotypes and phage types are often more resistant than others, some of the observed differences in antimicrobial resistance may be due to differences in serotype and phage type distributions between countries. 1. For Estonia, France, Germany, Romania, Slovenia and Spain, 2007 data were used. EFSA Journal 2010; 8(7):

64 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.4 Overview of the findings of antimicrobial resistance in Salmonella at MS reporting group level, 2008 Figures SA29-SA30 display resistance levels in the reporting MS group based on quantitative data in Figure SA29: Antimicrobial resistance to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide, ciprofloxacin, nalidixic acid and cefotaxime in Salmonella spp., S. Enteritidis and S. Typhimurium. from Gallus gallus and broiler meat at reporting MS group level in % resistance at reporting MS Salmonella spp. from Gallus gallus in 18MSs, 2008 Salmonella Enteritidis from Gallus gallus in 16MSs, 2008 Salmonella Typhimurium from Gallus gallus in 5 MSs, 2008 Salmonella spp from broilers meat in 10 MSs, 2008 tetracycline ampicillin chloramphenicol gentamicin sulfonamide ciprofloxacin nalidixic acid cefotaxime EFSA Journal 2010; 8(7):

65 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA30: Antimicrobial resistance to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide, ciprofloxacin, nalidixic acid and cefotaxim in Salmonella spp. from Gallus gallus, turkeys, pigs and cattle at reporting MS group level in 2008 % resistance at reporting MS Salmonella spp. from Gallus gallus in 18 MSs, 2008 Salmonella spp. from pigs in 15 MSs, 2008 Salmonella spp. from cattle in 8 MSs, 2007 tetracycline ampicillin cloramphenicol gentamicin sulfonamide ciprofloxacin nalidixic acid ceftiofur cefotaxime EFSA Journal 2010; 8(7):

66 EFSA Journal 2010; 8(7):

67 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Antimicrobial resistance in Campylobacter - quantitative data EFSA Journal 2010; 8(7):

68 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA In total 22 MSs and two non-mss (Norway and Switzerland) reported data on antimicrobial resistance in Campylobacter isolates from animals and food. This information covers also the data from Campylobacter isolates deriving from the EU-wide baseline surveys carried out in All quantitative Campylobacter data were reported as MIC values. Table CA1 shows the countries reporting Campylobacter MIC values in A maximum of two countries for each food/animal category reported qualitative data that were not reported as quantitative data. This was the case for Denmark and Luxembourg for C. coli in Gallus gallus, for the Netherlands for C. jejuni and C. coli in meat from broilers, for the United Kingdom for C. jejuni and C. coli in pigs, and for Belgium in the case of C. jejuni in meat from pigs. Due to very few additional qualitative Campylobacter data, no specific subsection on qualitative data is presented for Campylobacter. In the following, results from 28,052 MIC susceptibility tests of Campylobacter isolates are analysed. Table CA1. Overview of countries reporting MIC distributions on Campylobacter jejuni and Campylobacter coli from animals and food in 2008 Bacterial species C. jejuni C. coli Origin Total number of MSs reporting Meat from broilers 7 Meat from turkeys 1 Gallus gallus Turkeys 1 Pigs 1 Cattle Meat from broilers 2 Meat from pig 1 Gallus gallus Turkeys 1 Pigs 22 Cattle MSs: AT, BE, DE, DK, EE, LV, PT MS: BE Countries MSs: AT, BE, CZ, DE, DK, EE, ES, FI, FR, HU, IE, IT, LV, MT, NL, PL, PT, RO, SE, SI, SK, UK Non-MSs: NO, CH MS: FR MS: HU MSs: AT, DK, ES, HU, NL Non-MS: CH MSs: BE, PT MS: BE MSs: AT, BE, ES, FI, FR, HU, IE, IT, LV, MT, NL, PL, PT, RO, SI, UK Non-MS: CH MS: FR MSs: AT, ES, HU, IT, NL Non-MS: CH MSs: AT, NL Antimicrobials selected by the different MSs and non-mss for susceptibility testing of C. jejuni and C. coli are shown in the Chapter 3 Material and Methods, Table MM4. Resistance to the following antimicrobial agents are described in detail in the following text: tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid. The tables were generated if more than three countries reported quantitative data per Campylobacter species and sampling origin. Only data where ten or more isolates were available per country, per sampling origin, per year are included in this report. Appendix 3.1 includes tables displaying MIC distributions, occurrence of resistance and 95% confidence intervals for tetracycline, chloramphenicol, erythromycin, gentamicin, streptomycin, ciprofloxacin and nalidixic acid resistance rates for C. jejuni and C. coli. Where the minimum criteria were met, temporal trend graphs were generated showing resistance to different antimicrobials against Campylobacter isolates from animals and food over the period, by plotting resistance percentages in susceptibility tested isolates for the year of sampling. Historical data for the period are available in Appendix 3.2. Spatial distributions of tetracycline, erythromycin and ciprofloxacin resistance rates were plotted for C. jejuni and C. coli. For countries where data for 2008 were not available, data for 2007 were used. 7. Commission Decision 2007/516/EC of 19 July 2007 concerning a financial contribution from the Community towards a survey on the prevalence and antimicrobial resistance of Campylobacter spp. in broiler flocks and on the prevalence of Campylobacter spp. and Salmonella spp. in broiler carcasses to be carried out in the Member States OJ L 190, , p EFSA Journal 2010; 8(7):

69 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Poultry and broiler meat Fowl (Gallus gallus) In this report fowl (Gallus gallus) includes data from breeding flocks, laying hen flocks and broiler flocks of Gallus gallus. Resistance levels among C. jejuni In 2008, quantitative data on C. jejuni isolates from Gallus gallus provided by 21 MSs and two non-mss (Table CA2) were included in the analyses. In particular, resistance to tetracycline, ciprofloxacin and nalidixic acid varied considerably between countries. At reporting MS group level the resistance level to tetracycline was 37%. Tetracycline resistance occurred frequently in C. jejuni in most MSs; the exceptions being the Nordic countries and the Czech Republic whose resistance rates were equal to or less than 10% (Table CA2). The resistance levels to ciprofloxacin and nalidixic acid were 50% and 51%, respectively, at reporting MS group level. In many countries the reported occurrence of ciprofloxacin and nalidixic acid resistance ranged from 50% up to almost 100% in 2008, except in the Nordic countries where ciprofloxacin and nalidixic acid resistance rates were equal to or less than 12% (Table CA2). The reported resistance level for erythromycin was 3% and for gentamicin, 4% (Table CA2) in the reporting MS group, and very little variation was observed in erythromycin and gentamicin resistance between MSs. Most countries reported either no or less than 10% erythromycin and gentamicin resistance among C. jejuni in 2008, with the exception of Hungary (12%) and Malta (15%) for erythromycin, and Belgium and Malta (both 23%), Latvia (19%), Spain (17%) and Romania (13%) for gentamicin. Resistance levels among C. coli In 2008, quantitative data on C. coli isolates from Gallus gallus from 14 MSs and one non-ms (Table CA3) were included in the analysis. Tetracycline, ciprofloxacin and nalidixic acid resistance among C. coli in the reporting MS group were 53%, 62% and 61%, respectively, and as previously observed for C. jejuni, levels of resistance also varied considerably between MSs. In many countries the reported occurrence of resistance to ciprofloxacin and nalidixic acid varied between 50% and almost 100% in Most MSs reported either no or less than 10% gentamicin resistance among C. coli isolates and resistance at reporting MS level was 3% in The reported occurrence of erythromycin resistance in C. coli was generally higher compared to C. jejuni with a level of resistance of 12% in the reporting MS group. However, in 2008, 13 out of 15 countries reported erythromycin resistance below 20%. EFSA Journal 2010; 8(7):

70 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA2. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from Gallus gallus in 2008, using harmonised cut-off values Gallus gallus Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res Austria Belgium Czech Republic Denmark Finland France Germany Hungary Ireland Italy Latvia Malta Netherlands Poland Portugal Romania Slovakia Slovenia Spain Sweden United Kingdom Total (21 MSs) 1, , , , , Norway Switzerland Table CA3. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from Gallus gallus in 2008, using harmonised cut-off values Gallus gallus Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res Austria Belgium France Hungary Ireland Italy Malta Netherlands Poland Portugal Romania Slovenia Spain United Kingdom Total (14 MSs) , , , Switzerland EFSA Journal 2010; 8(7):

71 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Temporal trends in resistance among C. jejuni Figures CA1-5 display trends in antimicrobial resistance in C. jejuni isolates from Gallus gallus. The figures underline that the occurrence of tetracycline, ciprofloxacin and nalidixic acid resistance vary considerably between countries: some countries have no or a low occurrence of resistance while other countries report more than 50% resistance (Figures CA1, CA4 and CA5). In many countries the occurrence of resistance in 2008 appeared to be similar to those observed in Spain is, however, an exception with marked decreases in tetracycline, ciprofloxacin, and nalidixic acid resistance observed from 2007 to Erythromycin and gentamicin resistance remained in all reporting countries at a constantly low level (Figures CA2 and CA3). Although the occurrence of resistance among C. jejuni remained relatively constant over time for many countries, some changes in resistance were also observed, mainly increases. No general trends among MSs were apparent over the period Figure CA1. Trends in tetracycline resistance in Campylobacter jejuni from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

72 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA2. Trends in erythromycin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden Norway Switzerland Figure CA3. Trends in gentamicin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

73 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA4. Trends in ciprofloxacin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark Finland France Germany Italy Netherlands Spain Norway Switzerland Figure CA5. Trends in nalidixic acid resistance in Campylobacter jejuni from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

74 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Temporal trends in resistance among C. coli Figures CA6-10 present trends in antimicrobial resistance in C. coli from Gallus gallus. A large variation in tetracycline, ciprofloxacin and nalidixic acid resistance was observed between countries in In addition, erythromycin resistance occurred more often among C. coli compared to C. jejuni from Gallus gallus. From 2007 to 2008, marked decreases in tetracycline, ciprofloxacin, and nalidixic acid resistance were observed for C. coli isolates from Gallus gallus in Spain and similar decreases were observed for C. jejuni isolates from Spain. In Italy, marked increases in erythromycin, ciprofloxacin and nalidixic acid were observed from 2007 to No general trends among MSs were apparent. Figure CA6. Trends in tetracycline resistance in Campylobacter coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria France Italy Netherlands Slovenia Spain Switzerland EFSA Journal 2010; 8(7):

75 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA7. Trends in erythromycin resistance in Campylobacter coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria France Italy Netherlands Slovenia Spain Switzerland Figure CA8. Trends in gentamicin resistance in Campylobacter coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria France Italy Netherlands Slovenia Spain Switzerland EFSA Journal 2010; 8(7):

76 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA9. Trends in ciprofloxacin resistance in Campylobacter coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria France Italy Netherlands Spain Switzerland Figure CA10. Trends in nalidixic acid resistance in Campylobacter coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria France Italy Netherlands Slovenia Spain Switzerland EFSA Journal 2010; 8(7):

77 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Spatial distribution of resistance among C. jejuni and C. coli The spatial distributions of tetracycline, erythromycin and ciprofloxacin resistance in C. jejuni and C. coli from Gallus gallus are shown in Figures CA Figure CA11 underlines the high occurrence of tetracycline resistance and the most apparent spatial pattern is the low occurrence of tetracycline resistance in C. jejuni from Gallus gallus in the northern part of Europe and a higher occurrence in southern Europe and the United Kingdom. The occurrence of erythromycin resistance was generally low and very small differences were observed between countries, therefore no spatial distribution could be determined (Figure CA12). Figure CA13 shows a higher occurrence of ciprofloxacin resistance in the eastern and central parts of Europe. Figures CA14 and CA16 underline the high occurrence of tetracycline and ciprofloxacin resistance in C. coli from Gallus gallus. For tetracycline, erythromycin and ciprofloxacin, no clear spatial distributions could be determined (Figures CA14-CA16). Figure CA11. Spatial distribution of tetracycline resistance among Campylobacter jejuni from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

78 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA12. Spatial distribution of erythromycin resistance among Campylobacter jejuni from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

79 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA13. Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

80 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA14. Spatial distribution of tetracycline resistance among Campylobacter coli from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

81 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA15. Spatial distribution of erythromycin resistance among Campylobacter coli from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

82 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA16. Spatial distribution of ciprofloxacin resistance among Campylobacter coli from Gallus gallus in countries reporting quantitative data, in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category Meat from broilers (Gallus gallus) Resistance levels among C. jejuni For 2008, quantitative antimicrobial resistance data for C. jejuni isolates from broiler meat provided by six MSs (Table CA4) were included in the following analyses. Resistance to tetracycline was 38% in the reporting MS group, with the lowest occurrence observed in Denmark (12%) and the highest occurrence in Portugal (73%) (Table CA4). Resistance levels to erythromycin and gentamicin were 6% and 13%, respectively, and in most MSs, either no or less than 10% erythromycin and gentamicin resistance were reported, except in Belgium where a 20% gentamicin resistance level was observed. The resistance levels for ciprofloxacin and nalidixic acid were, at reporting MS group level, 46% and 50%, respectively. In 2008, Germany reported a nalidixic acid resistance level of 17%, while Denmark reported 19% of the isolates resistant to ciprofloxacin and nalidixic acid. In the remaining countries ciprofloxacin and nalidixic acid resistance varied between 31% and 100%. EFSA Journal 2010; 8(7):

83 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Table CA4. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from meat from broilers in 2008, using harmonised cut-off values Meat from broilers Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res Austria Belgium Denmark Germany Latvia Portugal Total (6 MSs) Pigs Resistance levels among C. coli For 2008, quantitative data on C. coli isolates from pigs provided by five MSs (Table CA5) were included in the following analyses. The average resistance level in the reporting MS group for tetracycline was 79%, with the reported occurrence of resistance varying between 69% and 100%. Average resistance levels were 25% for erythromycin, 4% for gentamicin and 39% for both ciprofloxacin and nalidixic acid. For erythromycin, ciprofloxacin and nalidixic acid, the occurrence of resistance varied consistently between countries (Table CA5). Table CA5. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from pigs in 2008, using harmonised cut-off values Pigs Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res Austria Hungary Italy Netherlands Spain Total (5 MSs) EFSA Journal 2010; 8(7):

84 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Temporal trends in resistance among C. coli Figures CA17-21 show trends in antimicrobial resistance in C. coli from pigs. In general, the occurrence of resistance remained rather stable over time for most countries. In 2008, all countries reported 69% or more tetracycline resistance (Figure CA17). Also erythromycin resistance was commonly found in C. coli from many reporting countries (Figure CA18). Figure CA17. Trends in tetracycline resistance in Campylobacter coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland Figure CA18. Trends in erythromycin resistance in Campylobacter coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

85 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA19. Trends in gentamicin resistance in Campylobacter coli from pigs in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland Figure CA20. Trends in ciprofloxacin resistance in Campylobacter coli from pigs in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

86 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA21. Trends in nalidixic acid resistance in Campylobacter coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark France Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

87 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Spatial distribution of resistance among C. coli The spatial distributions of tetracycline, erythromycin and ciprofloxacin resistance in C. coli from pigs are shown in Figures CA Due to the high occurrence of tetracycline resistance in most countries, no clear pattern could be detected. For erythromycin and ciprofloxacin the highest occurrence of resistance was observed in the southern part of Europe. Figure CA22. Spatial distribution of tetracycline resistance among Campylobacter coli from pigs in countries reporting quantitative data in Note: In this map, countries reporting their resistance data only as a proportion of resistant isolates, as well as those testing less than 10 isolates for susceptibility, are reported within the qualitative data category. 1. For France, Denmark, Germany and Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

88 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA23. Spatial distribution of erythromycin resistance among Campylobacter coli from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. 1. For Denmark, France, Germany, Italy and Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

89 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA24. Spatial distribution of ciprofloxacin resistance among Campylobacter coli from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. 1. For Denmark, France, Germany, Italy and Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

90 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5.3 Cattle (bovine animals) Resistance levels among C. jejuni For 2008, quantitative data on C. jejuni isolates from cattle provided by four MSs and one non-ms (Table CA6) were used in the following analyses. The average resistance levels in the reporting MS group were 28% for tetracycline. Resistance varied between countries from 0% to 73% (Table CA6). Resistance levels at reporting MS level were 1% for both erythromycin and gentamicin, and among reporting countries, no or less than 6% erythromycin and gentamicin resistance levels were detected. The resistance levels for ciprofloxacin and nalidixic acid were both 34% at reporting MS level, varying between MSs from 20% to 56% (Table CA6). Table CA6. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from cattle in 2008, using harmonised cut-off values Cattle Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res Austria Denmark Netherlands Spain Total (4 MSs) Switzerland EFSA Journal 2010; 8(7):

91 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Temporal trends in resistance among C. jejuni Fewer countries reported resistance in C. jejuni from cattle (Figures CA25-29) and the difference in the occurrence of resistance between countries was not as large as for C. jejuni from Gallus gallus. As for C. jejuni in Gallus gallus, resistance to tetracycline, ciprofloxacin and nalidixic acid were also most often reported in C. jejuni from cattle. No general trends among the MSs were apparent. Figure CA25. Trends in tetracycline resistance in Campylobacter jejuni from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Italy Netherlands Spain Switzerland Figure CA26. Trends in erythromycin resistance in Campylobacter jejuni from cattle in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

92 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA27. Trends in gentamicin resistance in Campylobacter jejuni from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Italy Netherlands Spain Switzerland Figure CA28. Trends in ciprofloxacin resistance in Campylobacter jejuni from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

93 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA29. Trends in nalidixic acid resistance in Campylobacter jejuni from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Italy Netherlands Spain Switzerland 5.4 Overview of the findings on antimicrobial resistance in Campylobacter at reporting MS group level, 2008 Figure CA30 displays resistance levels in the reporting MS group based on quantitative data in Figure CA30. Antimicrobial resistance to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid in Campylobacter jejuni and Campylobacter coli from fowl, pigs and cattle at reporting MS group level in % resistance at reporting MS C.jejuni from Gallus gallus in 21MSs, 2008 C.coli from Gallus gallus in 14MSs, 2008 C. jejuni from broiler meat in 6 MSs, 2008 C.coli from broiler meat in 3 MSs, 2008 C.coli from pigs in 5 MSs, 2008 C.jejuni from cattle in 4 MSs, 2008 tetracycline erytromycin gentamicin ciprofloxacin nalidixic acid EFSA Journal 2010; 8(7):

94 EFSA Journal 2010; 8(7):

95 ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA 6. Antimicrobial resistance in indicator Escherichia coli - quantitative data EFSA Journal 2010; 8(7):

96 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Antimicrobial resistance in indicator Escherichia coli Forteen MSs and two non-mss (Norway and Switzerland) collectively reported quantitative data on antimicrobial resistance in commensal (indicator) Escherichia coli isolates from animals and food in The results cover 50,129 MIC susceptibility tests and 5,742 disk diffusion susceptibility tests of E. coli isolates. In 2008, all qualitative E. coli data were also reported as quantitative data. Therefore, no section showing qualitative indicator E. coli data will be presented. Table EC1 shows the countries reporting E. coli MIC values and inhibition zones in Table EC1. Overview of countries reporting MIC distributions and disk inhibition zones on indicator Escherichia coli from animals and food in 2008 Method Dilution Diffusion Origin Total number of MSs reporting Countries Meat from broilers 3 MSs: DK, FR, LV Meat from turkeys 2 MSs: FR, NL Meat from bovine animals 4 MSs: DE, DK, LV, NL Meat from pig 4 MSs: DK, FR, NL, SE Gallus gallus 6 MSs: AT, DK, ES, FI, FR, NL Non-MS: CH Turkeys 1 MS: FR Pigs Cattle 7 MSs: AT, DK, EE, ES, FR, NL, SE Non-MS: NO 7 MSs: AT, DE, DK, EE, ES, FR, NL Non-MS: CH Turkeys 2 MSs: PL. SI Gallus gallus 4 MSs: HU, PL, RO, SI Pigs 3 MSs: HU, PL, SI Cattle 4 MSs: HU, PL, RO, SI For 2008, the occurrence of resistance to the most relevant antimicrobials in E. coli are presented hereafter. The antimicrobial agents covered are tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid. MIC distributions, occurrence of resistance and 95% confidence intervals for tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin, streptomycin, ciprofloxacin and nalidixic acid in 2008 are presented in Appendix 4.1. The spatial distributions of tetracycline and nalidixic acid resistance rates in E. coli from Gallus gallus, turkeys, pigs and cattle in 2008 are presented. For countries where data for 2008 were not available, 2007 resistance rates were used. In the graphs showing trends in the development of antimicrobial resistance over time, both MIC and inhibition zone data interpreted using epidemiological cut-off values are included (see Chapter 3. Material and Methods for further details). Only a few MSs reported data for five consecutive years. More frequently, data were reported for two or three out of the five years. In particular for indicator E. coli, some countries only reported resistance data every second year. In order not to lose resistance data from these countries, data were included in the figures as point estimates. Historical data for the period are available in Appendix 4.2. EFSA Journal 2010; 8(7):

97 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Poultry Fowl (Gallus gallus) In this report fowl, (Gallus gallus) includes data from breeding flocks, laying hen flocks and broiler flocks of Gallus gallus. In 2008, quantitative data from nine MSs and one non-ms were included in the analyses of antimicrobial resistance in E. coli from Gallus gallus (Table EC1). Resistance levels among Escherichia coli The occurrences of tetracycline, ampicillin, sulfonamide, streptomycin, nalidixic acid and ciprofloxacin resistance varied considerably between countries in 2008, similarly to the previous years. In 2008, resistance levels in the reporting MS group were 40% for tetracycline, 42% for ampicillin and 37% for sulfonamide (Table EC2). In particular, the lowest tetracycline resistance was reported in Finland (6%) and Denmark (11%). In the same year the remaining countries reported tetracycline resistance levels that varied between 26% in Austria to 73% in Spain and France. The resistance levels to ciprofloxacin and nalidixic acid were 45% and 46%, respectively, at reporting MS group level. The lowest occurrence of ciprofloxacin resistance was reported by Denmark (12%) and the highest, by Spain (88%). In Austria, the Netherlands, Finland and France between 21% and 69% ciprofloxacin resistance was reported (Table EC2). Denmark and Switzerland reported MIC distributions for ceftiofur, and no resistant isolates were detected (Table EC2 and Appendix 4.1, Table EC1). Six MSs reported cefotaxime MIC distributions. In 2008, resistance to cefotaxime was 9% in the reporting MS group. Cefotaxime resistance can be regarded as a possible indicator for extended-spectrum beta-lactamase resistance (ESBL). No cefotaxime resistance was reported from Denmark, while cefotaxime resistance ranged from 1% to 30% in the remaining reporting countries. Three out of the six above-mentioned countries also reported ceftazidime distributions and the results were similar to cefotaxime resistance levels in 2008 (Table EC2 and Appendix 4.1, Table EC1). EFSA Journal 2010; 8(7):

98 EFSA Journal 2010; 8(7): Table EC2. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Escherichia coli from Gallus gallus in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gallus gallus Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Denmark Finland France Hungary Netherlands Poland Slovenia Spain Total (9 MSs) 2, , , , , , , , Switzerland ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA

99 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Temporal trends in resistance among Escherichia coli Figures EC1-7 display trends in resistance to selected antimicrobials in E. coli from Gallus gallus. The figures show that the occurrences of resistance varied considerably between countries in 2008, and that in most countries the occurrences of resistance remained relatively constant over time for several antimicrobials. In addition, the figures also indicate that the same countries tend to report high resistance rates to several antimicrobials. Although the occurrence of resistance remained rather stable, some changes were observed. No general trends among reporting MSs were apparent over the period Figure EC1. Trends in tetracycline resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

100 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC2. Trends in chloramphenicol resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland Figure EC3. Trends in ampicillin resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Sweden Spain Norway Switzerland EFSA Journal 2010; 8(7):

101 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Figure EC4. Trends in sulfonamide resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Sweden Spain Norway Switzerland Figure EC5. Trends in gentamicin resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Netherlands Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

102 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC6. Trends in streptomycin resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland Figure EC7. Trends in nalidixic acid resistance in Escherichia coli from Gallus gallus in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

103 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Spatial distribution of resistance among Escherichia coli The spatial distributions of tetracycline and nalidixic acid resistance among E. coli from Gallus gallus are shown in Figures EC8-9. Figure EC8 indicates an increase in tetracycline resistance rates from the north to the south of Europe. Although, for nalidixic acid, the spatial pattern is not as clear, the lowest nalidixic resistance rates are found in the Nordic countries, and an increase is observed towards southern and eastern parts of Europe. Figure EC8. Spatial distribution of tetracycline resistance among Escherichia coli from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. For Italy and Sweden, 2007 data were used. EFSA Journal 2010; 8(7):

104 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC9. Spatial distribution of nalidixic acid resistance among Escherichia coli from Gallus gallus in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. For Italy and Sweden, 2007 data were used. 6.2 Pigs and pig meat Pigs For 2008, quantitative data on commensal E. coli in pigs from ten MSs and one non-ms (Table EC3) were included in the following antimicrobial resistance analyses. Resistance levels among Escherichia coli The occurrence of tetracycline, ampicillin, sulfonamide and streptomycin resistance varied considerably between MSs. In 2008, resistance levels in the reporting MS group were 55% for tetracycline, 27% for ampicillin and 32% for sulfonamide (Table EC3). In general, Sweden and Norway had the lowest occurrence of resistance to most antimicrobials, e.g. these countries did not report more than 9% tetracycline resistance in During the same year the highest occurrences of resistance were reported in France, the Netherlands, Hungary, Slovenia and Spain where tetracycline resistance varied from 67% to 85% (Table EC3). Small or no differences between MSs were observed for cefotaxime, ceftazidime, ceftiofur, gentamicin, nalidixic acid and ciprofloxacin resistance, and resistance levels were 3% for both nalidixic acid and ciprofloxacin at reporting MS group level (Table EC3). The highest occurrence of ciprofloxacin resistance was observed in Norway (23%) followed by Spain (10%). In the remaining countries between 0% and 4% EFSA Journal 2010; 8(7):

105 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. resistance was observed. The highest occurrence of nalidixic acid resistance was observed in Slovenia (27%) followed by Spain (11%), while in the remaining countries between 0% and 4% resistance levels were observed (Table EC3). In 2008, Denmark and Estonia, reported MIC data for ceftiofur and no resistance was detected (Table EC3 and Appendix 4.1, Table EC2). Eight countries reported cefotaxime MIC distributions and resistance levels of 1% were reported in Austria, France, the Netherlands and Spain, whereas no resistant isolates were detected in Denmark, Estonia, Sweden and Norway. Cefotaxime resistance can be regarded as a possible indicator for ESBL resistance. In addition, three out of the above mentioned eight countries also reported ceftazidime resistance and the results were similar to the reported cefotaxime resistance (Appendix 4.1, Table EC2). EFSA Journal 2010; 8(7):

106 EFSA Journal 2010; 8(7): Table EC3. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of Escherichia coli from pigs in 2008, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Denmark Estonia France Hungary Netherlands Poland Slovenia Spain Sweden Total (10 MSs) 1, , , , , , , ,850 3 Norway ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA

107 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Temporal trends in resistance among Escherichia coli Figures EC10-16 display trends in resistance to selected antimicrobials in E. coli from pigs. In 2008, the occurrence of tetracycline, ampicillin, sulfonamide and streptomycin resistance varied considerably between reporting countries. However, in most countries resistance remained at the same level as in previous years. In particular, nalidixic acid and ciprofloxacin resistance rates were lower in E. coli from pigs (both 3% in the reporting MS group) compared to E. coli from Gallus gallus (46% and 45%, respectively, at reporting MS group level). Some of the countries reporting a high occurrence of resistance in E. coli from Gallus gallus are also among the countries having a high occurrence of resistance in E. coli from pigs. Figures EC10-16 also show that in most countries the occurrence of resistance in E. coli from pigs remained relatively constant from 2004 to 2008, although in some of the reporting countries changes were observed over time as well. No general trends among reporting MSs were apparent over the period. Figure EC10. Trends in tetracycline resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

108 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC11. Trends in chloramphenicol resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland Figure EC12. Trends in ampicillin resistance in Escherichia coli from pigs in reporting MSs and non- MSs, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

109 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Figure EC13. Trends in sulfonamide resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland Figure EC14. Trends in gentamicin resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Netherlands Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

110 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC15. Trends in streptomycin resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland Figure EC16. Trends in nalidixic acid resistance in Escherichia coli from pigs in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Slovenia Spain Sweden Norway Switzerland EFSA Journal 2010; 8(7):

111 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Spatial distribution of resistance among Escherichia coli The spatial distributions of tetracycline and nalidixic acid resistance in E. coli from pigs are shown in Figures EC17 and EC18. For tetracycline resistance, a clear spatial pattern was detected with low resistance rates in Norway, Sweden and Finland. The resistance rates increase towards central and south-western Europe. The reported nalidixic acid resistance rates in E. coli from pigs were in general low and no clear spatial distribution was observed. Figure EC17. Spatial distribution of tetracycline resistance among Escherichia coli from pigs in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. For Finland, Italy and Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

112 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC18. Spatial distribution of nalidixic acid resistance among Escherichia coli from pigs in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those testing the susceptibility of less than 10 isolates, are reported within the qualitative data category. For Finland, Italy and Switzerland, 2007 data were used Pig meat For 2008, quantitative data for E. coli isolates from pig meat from four MSs (Table EC4) were included in the following antimicrobial resistance analyses. Resistance levels among Escherichia coli Resistance to tetracycline, sulfonamide and ampicillin were the most commonly detected and at reporting MS group level, resistance levels to these antimicrobials were 48%, 42%, and 25%, respectively. Similarly to pigs, large variations were observed between countries ranging from 0% tetracycline resistance in Sweden to 71% in France (Table EC4). Sulfonamide resistance varied from 5% in Sweden to 94% in the Netherlands. Generally, low levels of nalidixic acid and ciprofloxacin resistance were observed, with rates ranging between 0 and 6%. Cefotaxime resistance was only reported by France where the occurrence was 1%. EFSA Journal 2010; 8(7):

113 EFSA Journal 2010; 8(7): Table EC4. Resistance to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Escherichia coli isolates from meat from pigs in 2008, using harmonised cut-off values Meat from pigs Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Denmark France Netherlands Sweden Total (4 MSs) ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6.

114 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6.3 Cattle (bovine animals) For 2008, quantitative data for E. coli in cattle from eleven MSs and one non-ms (Table EC5) were included in the following antimicrobial resistance analyses. Resistance levels among Escherichia coli In general, the occurrence of resistance in indicator E. coli from cattle (Table EC5) were lower compared to those in indicator E. coli from Gallus gallus and pigs from the same MSs (Tables EC2 and EC3). Resistance levels in the reporting MS group were 27% for tetracycline, 18% for ampicillin and 22% for sulfonamide (Table EC5). The only exception was France, where the occurrence of resistance in E. coli isolates from cattle was higher for several antimicrobials compared to isolates from Gallus gallus and pigs in In 2008, at reporting MS group level, resistance to ciprofloxacin and nalidixic acid was 10% and 6%, respectively, and reported resistance levels ranged from 0% to 17% at MS level (Table EC5). Three countries reported MIC data for ceftiofur in 2008, and resistance was not detected in the isolates tested for susceptibility from any of these countries. Six countries reported cefotaxime MIC distributions and resistant isolates were detected in two of these, e.g. 1% in France and 2% in the Netherlands (Table EC5). Cefotaxime resistance can be regarded as a possible indicator for ESBL resistance. In addition, Germany and the Netherlands reported 12% and 2%, respectively, of resistance to ceftazidime in 2008 (Appendix 4.1, Table EC4a). EFSA Journal 2010; 8(7):

115 EFSA Journal 2010; 8(7): Table EC5. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of Escherichia coli from cattle in 2008, using harmonized cut-off values. Values in bold were obtained by disk diffusion method Cattle Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria Denmark Estonia France Germany Hungary Netherlands Poland Romania Slovenia Spain Total (11 MSs) Switzerland ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6.

116 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Temporal trends in resistance among Escherichia coli Figures EC19-25 present trends in resistance to selected antimicrobials in E. coli from cattle. In 2008, the occurrence of resistance for most countries was similar to the occurrence reported during previous years, the only exceptions being France and Slovenia. In France, a marked increase in resistance was observed from 2007 to 2008 for several antimicrobials, while a decrease was observed for Slovenia. In general, the variation in resistance rates between MSs was much smaller for cattle compared to the variation observed for Gallus gallus and pigs. Although the occurrence of resistance remained rather stable, some changes over time in the occurrence of resistance were also observed. Figure EC19. Trends in tetracycline resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Spain Switzerland EFSA Journal 2010; 8(7):

117 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Figure EC20. Trends in chloramphenicol resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Spain Switzerland Figure EC21. Trends in ampicillin resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Switzerland EFSA Journal 2010; 8(7):

118 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Figure EC22. Trends in sulfonamide resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Spain Switzerland Figure EC23. Trends in gentamicin resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

119 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Figure EC24. Trends in streptomycin resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Spain Switzerland Figure EC25. Trends in nalidixic acid resistance in Escherichia coli from cattle in reporting MSs and non-mss, , quantitative data 100 % resistant isolates Austria Denmark Estonia France Germany Hungary Italy Netherlands Poland Slovenia Spain Switzerland EFSA Journal 2010; 8(7):

120 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA Spatial distribution of resistance among Escherichia coli The spatial distributions of tetracycline and nalidixic acid resistance among E. coli from cattle are shown in Figures EC For both antimicrobials it is difficult to determine a clear spatial pattern. However, the highest tetracycline resistance rates were observed in south-western Europe, while lower resistance rates were observed in northern and eastern Europe. In general nalidixic acid resistance rates were low and no clear pattern could be detected. Figure EC26. Spatial distribution of tetracycline resistance among Escherichia coli from cattle in countries reporting quantitative data in 2008 Note: In this map, countries reporting their resistance data only as a proportion of resistant isolates, as well as those testing less than 10 isolates for susceptibility, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

121 ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6. Figure EC27. Spatial distribution of nalidixic acid resistance among Escherichia coli from cattle in countries reporting quantitative data in 2008 Note: In this map, countries reporting their resistance data only as a proportion of resistant isolates, as well as those testing less than 10 isolates for susceptibility, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

122 6. ANTIMICROBIAL RESISTANCE IN INDICATOR E. COLI - QUANTITATIVE DATA 6.4 Overview of findings on E.coli resistance at reporting MS group level, 2008 Figure EC28 displays resistance levels in the reporting MS group based on quantitative data in Figure EC28. Antimicrobial resistance in indicator Escherichia coli from fowl, pigs and cattle to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide, ciprofloxacin, nalidixic acid, ceftiofur and cefotaxime at reporting MS group, in % resistance at reporting MS indicator E.coli from Gallus gallus in 9 MSs, 2008 indicator E.coli from pigs in 10 MSs, 2008 indicator E.coli from cattle in 11 MSs, 2008 tetracycline ampicillin cloramphenicol gentamicin sulfonamide ciprofloxacin nalidixic acid cefotaxime EFSA Journal 2010; 8(7):

123 ANTIMICROBIAL RESISTANCE IN ENTEROCOCCI - QUANTITATIVE DATA 7. Antimicrobial resistance in indicator enterococci - quantitative data EFSA Journal 2010; 8(7):

124 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Antimicrobial resistance in indicator enterococci In 2008, nine MSs and two non-mss (Norway and Switzerland) collectively reported data on antimicrobial resistance in enterococci isolated from animals and food. Almost all quantitative Enterococcus faecium and Enterococcus faecalis antimicrobial resistance data were reported as MIC values. The results of 17,303 MIC susceptibility tests of enterococci isolates are set out hereafter. Tables EN1-2 present the countries reporting MIC values in For E. faecium and E. faecalis very few countries reported MIC data on isolates collected from food (Tables EN1-2). Therefore, only data reported from animals were used in this chapter. For enterococci all qualitative data were also reported as quantitative data, the only exception was Ireland who only reported qualitative data for E. faecium isolated from cattle. Due to very few additional qualitative enterococci data, no subsection on qualitative data are presented for enterococci. Table EN1. Overview of countries reporting MIC distributions for Enterococcus faecium from animals and food in 2008 Method Dilution Origin Total number of MSs reporting Countries Meat from broilers 1 MS: DK Meat from pig 2 MSs: DK, NL Meat from bovine animals Gallus gallus 2 5 MSs: DK, NL MSs: AT, DK, ES, FI, NL Non-MS: CH Turkeys Pigs Cattle MS: FR MSs: AT, DK, EE, ES, FR, NL, SE Non-MS: NO MSs: AT, EE, ES, FR, NL Non-MS: CH Table EN2. Overview of countries reporting MIC distributions for Enterococcus faecalis from animals and food in 2008 Method Dilution Diffusion Origin Total number of MSs reporting Countries Meat from pig 2 MSs: NL, SE Meat from bovine animals Gallus gallus Pigs Cattle MS: NL MSs: AT, FI, NL Non-MS: CH MSs: AT, EE, NL, SE Non-MS: NO MSs: AT, EE, NL Non-MS: CH Gallus gallus 1 MS: HU Pigs 1 MS: HU Cattle 1 MS: HU EFSA Journal 2010; 8(7):

125 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. For 2008, the occurrence of resistance to the most relevant substances of these antimicrobials among E. faecium and E. faecalis are presented in Tables EN3-7 while trends over time in resistance are presented in Figures EN1-2, EN6-7 and EN The antimicrobials covered for E. faecium and E. faecalis are tetracycline, ampicillin, erythromycin, streptomycin and vancomycin. MIC distributions, occurrence of resistance and 95% confidence intervals for tetracycline, chloramphenicol, ampicillin, erythromycin, streptomycin, vancomycin. quinupristin/dalfopristin, avilamycin and linezolid are presented in Appendix 5.1. The spatial distributions of tetracycline, erythromycin and vancomycin resistance rates in E. faecium from Gallus gallus, pigs and cattle are presented for For countries where data for 2008 were not available, 2007 resistance rates were used. A limited number of countries reported antimicrobial resistance for enterococci until Therefore, only temporal resistance trends at MS level are shown for erythromycin and tetracycline resistance in E. faecium. Fowl (Gallus gallus). Historical data for the period are available in Appendix Fowl (Gallus gallus) In this report fowl (Gallus gallus) includes data from breeding flocks, laying hen flocks and broiler flocks of Gallus gallus. For 2008, quantitative data on enterococci in Gallus gallus from five MSs and one non-ms were used in the following analyses. Resistance levels in tested isolates Tables EN3 and EN4 present the occurrences of resistance to selected antimicrobials among E. faecium and E. faecalis from Gallus gallus. In 2008, similarly to the previous year, the occurrence of tetracycline and erythromycin resistance was detected frequently in E. faecium and E. faecalis isolates from Gallus gallus. In E. faecium resistance levels in the reporting MS group were 47% (tetracycline) and 45% (erythromycin). Among E. faecalis resistance levels were 62% (tetracycline) and 55% (erythromycin) at reporting MS group level. A large variation was observed between the reporting countries especially in the data for E. faecium, e.g. in Finland and Denmark erythromycin and tetracycline resistance occurred in 8% to 16% of the isolates, while in Austria, the Netherlands and Spain the occurrences of resistance to the same two antimicrobials were 63% to 83%. In 2008, ampicillin resistant E. faecalis were not detected in Gallus gallus, and the occurrence of ampicillin resistance in E. faecium ranged from 1% to 10%. Cross-resistance is observed between the growth promoter, avoparcin, and the important human antimicrobial, vancomycin. Avoparcin was banned in the EU in 1997; however, in Austria and in Finland in 2008 vancomycin resistant E. faecium was still reported in up to 5% of isolates from Gallus gallus. The growth promoter avilamycin was phased out in the EU in 2006 and three countries reported avilamycin data in In Denmark, 2% of all E. faecium isolates from Gallus gallus were resistant to avilamicyn while in Austria it reached 6% and in Spain 20%. Avilamycin resistance was also reported in 3% of E. faecalis isolates from Austria (Appendix 5.1, Tables EN1 and EN2). Table EN3. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from Gallus gallus in 2008 Gallus gallus Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin N % Res N % Res N % Res N % Res N % Res Austria Denmark Finland Netherlands Spain Total (5 MSs) Switzerland EFSA Journal 2010; 8(7):

126 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Table EN4. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from Gallus gallus in 2008 Gallus gallus Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin N % Res N % Res N % Res N % Res N % Res Austria Finland Netherlands Total (3 MSs) Switzerland Spatial distribution of resistance among Enterococcus faecium Figures EN1-2 display trends in resistance to tetracycline and erythromycin in E. faecium from Gallus gallus in the period For both tetracycline and erythromycin, the occurrence of resistance varies between countries. Resistance to tetracycline and to erythromycin in E. faecium, tested for susceptibility respectively in Switzerland and in the Netherlands, seems to increase over the period Figure EN1. Trends in tetracycline resistance in Enterococcus faecium from Gallus gallus in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark Finland Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

127 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN2. Trends in erythromycin resistance in Enterococcus faecium from Gallus gallus in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark Finland Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

128 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Spatial distribution of resistance among Enterococcus faecium The spatial distributions of tetracycline, erythromycin and vancomycin resistance in E. faecium are shown in Figures EN3-5. In E. faecium from Gallus gallus, tetracycline and erythromycin resistance had a similar spatial distribution, with MSs reporting similar resistance rates for both antimicrobials. Due to few countries reporting data it is difficult to determine spatial distributions, however for tetracycline and erythromycin there is a tendency towards lower resistance rates in the north that increases towards the south-west (Figure EN3 and Figure EN4). For vancomycin, no clear spatial distribution could be observed at EU level (Figure EN5). Figure EN3. Spatial distribution of tetracycline resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. 1. For France and Sweden, 2007 data were used. EFSA Journal 2010; 8(7):

129 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN4. Spatial distribution of erythromycin resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. 1. For France and Sweden, 2007 data were used. EFSA Journal 2010; 8(7):

130 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Figure EN5. Spatial distribution of vancomycin resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates for, are reported within the qualitative data category. 1. For France and Sweden, 2007 data were used. EFSA Journal 2010; 8(7):

131 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Pigs Quantitative antimicrobial resistance data for enterococci from pigs from six MSs and one non-ms were included in the following analyses for Resistance levels in tested isolates In 2008, the occurrence of tetracycline, erythromycin and streptomycin resistance was detected most frequently in E. faecium and E. faecalis isolates from pigs (Tables EN5 and EN6). As for Gallus gallus, large variations were observed between reporting countries e.g. in 2008, the average resistance level in the reporting MS group for erythromycin resistance in E. faecium, was 42%. The lowest occurrence was observed in Sweden with 13%, while Spain reported 65%. In 2008, the average resistance level for ampicillin was 4% with Denmark and Norway reporting 9% and 6%, respectively. Vancomycin resistant E. faecium was detected in 5% of the isolates from Spain, in 2% of the isolates from France and Austria, and 1% of the isolates from the Netherlands. During the same year vancomycin resistance in E. faecalis from pigs was detected only among isolates from the Netherlands at a level of 2%. Avilamycin resistance was not detected among E. faecium from pigs, while 2.6% of E. faecalis isolates from pigs in Austria were avilamycin resistant (Appendix 5.1, Tables EN3 and EN4). Table EN5. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from pigs in 2008 Pigs Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin N % Res N % Res N % Res N % Res N % Res Austria Denmark France Netherlands Spain Sweden Total (6 MSs) Norway Table EN6. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from pigs in 2008 Pigs Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin N % Res N % Res N % Res N % Res N % Res Austria Netherlands Sweden Total (3 MSs) Norway EFSA Journal 2010; 8(7):

132 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Temporal trends in resistance among Enterococcus faecium Figures EN6-7 show trends in resistance to tetracycline and erythromycin in E. faecium from pigs from 2004 to In 2007 and 2008, the occurrence of resistance to tetracycline and erythromycin varied between countries, and in particular for tetracycline, countries were divided into two groups according to either a high or low occurrence of tetracycline resistance. Figure EN6. Trends in tetracycline resistance in Enterococcus faecium from pigs in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark Finland France Netherlands Spain Norway Switzerland Figure EN7. Trends in erythromycin resistance in Enterococcus faecium from pigs in reporting MSs and non-mss, , quantitative data % resistant isolates Austria Denmark France Netherlands Spain Norway Switzerland EFSA Journal 2010; 8(7):

133 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Spatial distribution of resistance among Enterococcus faecium The spatial distributions of tetracycline, erythromycin and vancomycin among E. faecium from pigs are presented in Figures EN8-10. Due to few countries reporting data it is difficult to determine spatial distributions at EU level. No clear spatial distribution could be observed for tetracycline, while there might be an increase in erythromycin and vancomycin resistance when moving from the north towards the south-west. Figure EN8. Spatial distribution of tetracycline resistance among Enterococcus faecium from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. 1. For Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

134 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Figure EN9. Spatial distribution of erythromycin resistance among Enterococcus faecium from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. 1. For Switzerland, 2007 data were used. EFSA Journal 2010; 8(7):

135 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN10. Spatial distribution of vancomycin resistance among Enterococcus faecium from pigs in countries reporting quantitative data in Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. 1. For Switzerland 2007, data were used. 7.3 Cattle (bovine animals) For 2008, quantitative data for enterococci in cattle from four MSs and one non-ms were used in the following analyses. Resistance levels in tested isolates Tetracycline, erythromycin and streptomycin resistance occurred frequently in E. faecium from cattle (Table EN7). As in Gallus gallus and pigs, a large variation was observed between the reporting countries. For E. faecium, the resistance level in the reporting MS group for erythromycin was 32%, with Austria reporting 5% erythromycin resistant isolates and France reporting 51%. Ampicillin resistant isolates among E. faecium from cattle were detected only in France at a level of 9%. Vancomycin resistance was reported in 6% of the E. faecium isolates from Spain, in 5% of the isolates from Austria and in 1% of the isolates from the Netherlands. EFSA Journal 2010; 8(7):

136 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Table EN7. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from cattle in 2008 Cattle Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin N % Res N % Res N % Res N % Res N % Res Austria France Netherlands Spain Total (4 MSs) Switzerland Temporal trends in resistance among Enterococcus faecium Figures EN11-12 show trends in resistance to tetracycline and erythromycin in E. faecium from cattle from 2004 to In 2007 and 2008 the occurrence of tetracycline and erythromycin resistance varied between countries. Figure EN11. Trends in tetracycline resistance in Enterococcus faecium from cattle in reporting MSs and non-mss, , quantitative data % resistant isolates Austria France Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

137 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN12. Trends in erythromycin resistance in Enterococcus faecium from cattle in reporting MSs and non-mss, , quantitative data % resistant isolates Austria France Netherlands Spain Switzerland EFSA Journal 2010; 8(7):

138 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Spatial distribution of resistance among Enterococcus faecium The spatial distributions of tetracycline, erythromycin and vancomycin resistance among E. faecium from cattle are shown in Figures EN Due to very few countries reporting data for cattle, no spatial distributions could be determined. Figure EN13. Spatial distribution of tetracycline resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

139 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN14. Spatial distribution of erythromycin resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):

140 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Figure EN15. Spatial distribution of vancomycin resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2008 Note: In this map, countries reporting resistance data only as a proportion of resistant isolates, as well as those susceptibility testing less than 10 isolates, are reported within the qualitative data category. EFSA Journal 2010; 8(7):