Community Summary Report. Antimicrobial resistance in zoonotic agents from animals and food in the European Union in

Community Summary Report Antimicrobial resistance in zoonotic agents from animals and food in the European Union in 2004-2007 April 2010

THE COMMUNITY SUMMARY REPORT 1 Antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2004-2007 ISSUED ON 28 FEBRUARY 2009 PUBLISHED ON 27 APRIL 2010 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 2004-2007. EFSA Journal 2010; 8(4):1309. [304 pp.]. doi:10.2903/j.efsa.2010.1309. Available online: www.efsa.europa.eu. EFSA Journal 2010; 8(4):1309 3/304 3

European Food Safety Authority 2010 ISBN: 978-92-9199-256-0 doi:10.2903/j.efsa.2010.1309 Reproduction is authorised, provided the source is acknowledged, save where otherwise stated. The views or positions expressed in this booklet do not necessarily represent in legal terms the official position of the European Food Safety Authority. The European Food Safety Authority assumes no responsibility or liability for any errors or inaccuracies that may appear. 4 EFSA Journal 2010; 8(4):1309 4/304

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 (EC), 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 EC, particularly in the case of a food crisis, are also part of EFSA s mandate, as laid down in the founding Regulation (EC) No 178/2002 of 28 January 2002. 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 Member States in accordance with Directive 2003/99/EC and for preparing the Community Summary Report from the results. Regarding antimicrobial resistance data from 2004-2007, this Community Summary Report was produced in collaboration with the National Food Institute, the Technical University of Denmark, contracted by EFSA. 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. The contributions of Hanne-Dorthe Emborg, Antonio Vieira, 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 43121 Parma ITALY Tel. +39 0521 036 111 Fax +39 0521 036 110 zoonoses@efsa.europa.eu www.efsa.europa.eu EFSA Journal 2010; 8(4):1309 5/304 5

SUMMARY Zoonoses are infections and diseases that are transmissible between animals and humans. Infection in humans can be acquired directly from animals, or through the ingestion of contaminated foodstuffs. Severity of zoonotic diseases in humans varies from mild symptoms to life-threatening conditions. 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 resistant zoonotic bacteria in animals and food, information is collected and analysed from all European Union Member States. During the years 2004 to 2007, 26 Member States submitted information on the occurrence of antimicrobial resistance in zoonotic bacteria originating from poultry, pigs and cattle as well as from meat to the European Commission and the European Food Safety Authority (EFSA). In addition, Norway and Switzerland provided information for the report. The reported information covered resistance to 51 antimicrobial substances. Assisted by its contractor, the Technical University of Denmark, EFSA analysed the data, the results of which are published in this Community Summary Report. Information on antimicrobial resistance was reported regarding Salmonella, Campylobacter, indicator (commensal) Escherichia coli and indicator (commensal) enterococci isolates from animals and food. The Member States reported both quantitative and qualitative data on antimicrobial resistance and both types of data are included in the report giving priority to quantitative data. A special effort was made to analyse the quantitative information reported on antimicrobial resistance. These data, expressed either as Minimum Inhibitory Concentrations or as disk inhibition zones, were interpreted using epidemiological cut-off values defining the resistance. This makes the data more comparable between reporting countries. The number of Member States reporting quantitative data on antimicrobial resistance increased from 18 Member States in 2004 to 21 Member States in 2006. Resistance to antimicrobials was commonly found among the Salmonella, Campylobacter and the indicator E. coli and enterococci isolates from animals and food in the European Union. For some tested antimicrobials, large differences in the occurrence of resistance over time were observed between Member States. These observations may reflect real differences in resistance situations in countries, but may also be partly due to differences in the monitoring and reporting systems in place and in the case of Salmonella, due to serovars present in the country. At Member State level the occurrence of antimicrobial resistance over time remained, in most cases, relatively stable over the reporting years. However, some decreases and increases in resistance were observed. The proportion of Salmonella and E. coli isolates resistant to ampicillin, sulfonamide and tetracycline varied between 5% and 68% among the isolates from poultry, pigs and cattle in the reporting Member State group. Some Member States reported a high occurrence of fluoroquinolone resistance in Salmonella isolates from poultry and in Campylobacter isolates from poultry, pigs and cattle as well as from meat. At Member State group level these resistance levels varied from 5% to 38% and from 20% to 64% for the Salmonella and Campylobacter isolates, respectively, during the years 2004 to 2007. This 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. The occurrence of resistance to tetracycline, ampicillin and sulfonamide in Salmonella isolates from fowl was at a lower level than in Salmonella isolates from pigs and cattle, whereas quinolone resistance levels were higher in Salmonella isolates from fowl. In indicator E. coli isolates from fowl and pigs, large variations in the reported resistance levels were observed between Member States. In cattle, the occurrence of resistant E. coli isolates was lower compared to fowl and pigs. Vancomycin resistance was still reported in some enterococci isolates from fowl, pigs and cattle even though avoparcin, a similar substance used in animals, had already been banned in 1997. Key words Antimicrobial resistance, food, animals, Salmonella, Campylobacter, Escherichia coli, enterococco. 6 EFSA Journal 2010; 8(4):1309 6/304

TABLE OF CONTENTS Summary...6 1. Introduction...9 1.1 Scientific background...10 1.2 Legal framework...10 1.3 Epidemiological cut-off values...11 2. Main findings...13 2.1 Main conclusions of the report...14 2.2 Agent specific summaries...16 3. Materials and methods...21 3.1 The antimicrobial susceptibility data available...22 3.1.1 Data reported under Directive 2003/99/EC from 2004 to 2007...23 3.1.2 Data reported from the EU-wide Salmonella baseline surveys...23 3.2 Antimicrobials for susceptibility testing...23 3.2.1 Antimicrobials for susceptibility testing of Salmonella...23 3.2.2 Antimicrobials for susceptibility testing of Campylobacter...24 3.2.3 Antimicrobials for susceptibility testing of Escherichia coli...27 3.2.4 Antimicrobials for susceptibility testing of enterococci...29 3.3 MIC and inhibition zone diameter interpretation...30 3.4 Data description and analysis...32 4. Antimicrobial resistance in Salmonella - quantitative data...33 4.1 Poultry (Gallus gallus) and broiler meat...36 4.1.1 Fowl (Gallus gallus)...36 4.1.2 Meat from broilers (Gallus gallus)...51 4.2 Turkeys...54 4.2.1 Resistance data from the baseline survey on the prevalence of Salmonella in turkey flocks in the EU......59 4.3 Pigs and pig meat...66 4.3.1 Pigs...66 4.3.2 Meat from pigs...79 4.3.3 Resistance data from the baseline survey on the prevalence of Salmonella in slaughter pigs in the EU......84 4.4 Cattle and bovine meat...92 4.4.1 Cattle (bovine animals)...92 4.4.2 Meat from bovine animals...103 4.5 Comparison of antimicrobial resistance among Salmonella isolates from food and animals within and between MSs...105 5. Antimicrobial resistance in Campylobacter - quantitative data...109 5.1 Poultry (Gallus gallus) and broiler meat...111 5.1.1 Fowl (Gallus gallus)...111 5.1.2 Meat from broilers...122 5.2 Pigs...125 5.3 Cattle...131 5.4 Comparison of antimicrobial resistance among Campylobacter jejuni and Campylobacter coli from food and animals within and between MSs...135 EFSA Journal 2010; 8(4):1309 7/304 7

TABLE OF CONTENTS 6. Antimicrobial resistance in indicator Escherichia coli - quantitative data...137 6.1 Poultry : Fowl (Gallus gallus)...139 6.2 Pigs...148 6.3 Cattle...157 7. Antimicrobial resistance in indicator enterococci - quantitative data...167 7.1 Poultry: Fowl (Gallus gallus)...169 7.2 Pigs...174 7.3 Cattle...178 8. Antimicrobial resistance in Salmonella and indicator Escherichia coli - qualitative data...183 8.1 Antimicrobial resistance among Salmonella isolates from animals and food - qualitative data...184 8.1.1 Poultry (Gallus gallus) and broiler meat...185 8.1.1.1 Fowl (Gallus gallus)...185 8.1.1.2 Meat from broilers...191 8.1.2 Turkeys...196 8.1.3 Pigs and pig meat...201 8.1.3.1 Pigs...201 8.1.3.2 Meat from pigs...206 8.1.4 Cattle and bovine meat...208 8.1.4.1 Cattle...208 8.1.4.2 Meat from bovine animals...212 8.2 Antimicrobial resistance among indicator Escherichia coli isolates from animals - qualitative data...214 8.2.1 Poultry: Fowl (Gallus gallus)...214 8.2.2 Turkeys...217 8.2.3 Pigs...220 8.2.4 Cattle...222 9. General discussions of the most interesting findings from the descriptive analyses...227 9.1 Antimicrobial resistance in Salmonella and Campylobacter...228 9.2 Indicator organisms, Escherichia coli and enterococci...232 10. References...235 Appendices...239 Appendix 1. List of abbreviations, Member States and other reporting countries, Definitions...240 Appendix 2. MIC distributions of Salmonella...243 Appendix 3. MIC distributions of Campylobacter...269 Appendix 4. MIC distributions of indicator Escherichia coli...281 Appendix 5. MIC distributions of indicator enterococci...293 Appendix 6. Setting the epidemiological cut-off values for inhibition zone diameters (disk diffusion)...299 8 EFSA Journal 2010; 8(4):1309 8/304

INTRODUCTION 1 Introduction 1 9

1. INTRODUCTION 1.1 Scientific background The introduction of antimicrobials in human clinical medicine and animal husbandry was one of the most significant achievements of the 20 th century. Antimicrobials have literally changed the way of living. It is now possible to successfully treat infections that were previously almost always lethal (e.g. Staphylococcus aureus bacteraemia). Unfortunately, after the introduction of antimicrobials, bacteria resistant to antimicrobial drugs began to emerge, sometimes rapidly. This problem has continued to follow the introduction of all new antimicrobial compounds. This emergence of antimicrobial resistance poses a major threat to the continued successful use of antimicrobial agents in both human and veterinary medicine. Antimicrobials are important for the treatment of infectious diseases in food animals and thereby play an important role in ensuring animal welfare and global food production. The antimicrobials 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). In addition, bacteria might be resistant to several classes of antimicrobials, whereby the use of one class of antimicrobial may result in the selection of resistance against another, unrelated class (co-resistance). Resistant bacteria, that develop and are carried in food-producing animals, can spread to people, mainly via foods but also by water and by direct animal contact. Examples include Escherichia coli, Salmonella, Campylobacter, Enterococcus, and Staphylococcus aureus. Out of these Salmonella and Campylobacter are frequent causes of human gastro-intestinal infections. Furthermore, the commensal bacteria (E. coli and enterococci) can also be carried in human bowels, although most probably only transiently. If the zoonotic bacteria are resistant to commonly used antibiotics, it poses an added problem for humans acquiring infections caused by these bacteria. Also, the genes that encode antimicrobial resistance may be transferred to other bacterial species, and many of these latter bacteria may reside for longer periods in human bowels or on their skin (EFSA, 2008b). 1.2 Legal framework Continuous and updated information on antimicrobial resistance is essential to guide risk profiling, risk assessment and risk management, and to determine the effect of possible interventions. For that purpose, Directive 2003/99/EC on the monitoring of zoonoses and zoonotic agents 1 lays down that Member States (MSs) are obliged to monitor and report on antimicrobial resistance in Salmonella and Campylobacter isolates from animals and food. The monitoring and reporting of resistance data from indicator organisms (commensal E. coli and enterococci) is voluntary. Furthermore, Directive 2003/99/ EC foresees that the monitoring of antimicrobial resistance is based on the surveillance systems in place in MSs which may differ in terms of origin of the isolates and laboratory testing of isolates. Antimicrobial resistance data for the years 2004 to 2007, reported by MSs and analysed in the framework of this report, were therefore presumably not fully harmonised as regards the origin of tested isolates, nevertheless a major endeavour was made to harmonise results from different laboratory methods. Priority in the analyses was given to quantitative data in this report. Another important source of data for the report were two EU-wide baseline surveys on Salmonella in slaughter pigs and turkey flocks conducted in 2006-2007. In the surveys, MSs were also invited to monitor and report voluntarily, data on antimicrobial resistance of Salmonella isolates. To address the need for standardised monitoring, EFSA, on request by the European Commission, has prepared detailed specifications for harmonised schemes on antimicrobial resistance. Two reports on the technical specifications for the monitoring and reporting of antimicrobial resistance among Salmonella and Campylobacter, Escherichia coli and enterococci were issued to guide MSs (EFSA, 2007 and 2008a). These published reports include detailed protocols on sampling strategies, methods 1. 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/EEC. OJ L 325, 12.12.2003, p. 31. 10 EFSA Journal 2010; 8(4):1309 10/304

INTRODUCTION 1 for susceptibility testing, antimicrobials for testing, criteria for categorising isolates as susceptible or non-susceptible, quality control and data to be reported. Based on these technical specifications on Salmonella, Commission Decision 2007/407/EC 2 harmonised the monitoring and reporting of antimicrobial resistance information on Salmonella isolates in poultry populations and pigs, specifically covered by Salmonella control programmes, and has been applicable from 1 January 2008 onwards. However, in most cases, these technical specifications could not be used for data already generated and reported to national authorities and to EFSA for the years 2004 to 2007. Such data can nonetheless be of great value to determine the situation within a country and for comparison between countries, especially if quantitative data on resistance were originally reported, which enables the use of common cut-off values to define the resistant bacteria. 1.3 Epidemiological cut-off values One of the major problems in the comparison of antimicrobial resistance data between countries has been the use of different criteria for determining resistant strains in different countries. The use of a single universal breakpoint for resistance, in order that both the detection of the early stages of resistance development within a bacterial population and the prediction of the outcome of therapy are achieved simultaneously, will continue to be difficult (see box overleaf for a detailed explanation). Therefore, different values for these two purposes are often used. Resistance 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. Epidemiological cut-off values have been established to separate between the original wild-type bacterial population and isolates that have developed reduced susceptibility to a given antimicrobial agent (Kahlmeter et al., 2003). In the EFSA reports on the technical specifications for harmonised monitoring and reporting, such epidemiological cut-off values have been consistently recommended for monitoring purposes. In this report, antimicrobial susceptibility data reported for the period 2004 to 2007 for Campylobacter, Salmonella, indicator E. coli and indicator enterococci are analysed. Whenever it has been permitted by the data format, the same or similar epidemiological cut-off values for resistance have been used. The cut-off values are given as Minimal Inhibitory Concentrations (MIC). Additionally, for the purpose of this report, epidemiological cut-off values were also determined for the antimicrobial resistance data expressed as disk inhibition zones. Epidemiological cut-off values are often lower than clinical breakpoints and cannot therefore be used directly to predict therapy outcome. They indicate more the emergence of resistance in the bacterial population. 2. Commission Decision 2007/407/EC of 12 June 2007 on a harmonised monitoring of antimicrobial resistance in Salmonella in poultry and pigs. OJ L 153, 14.06.2007, p. 26. EFSA Journal 2010; 8(4):1309 11/304 11

1. INTRODUCTION 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 a 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, a 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 a 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 the 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 the 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 diameter 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. 12 EFSA Journal 2010; 8(4):1309 12/304

MAIN FINDINGS 2 Main findings 2 13

2. MAIN FINDINGS 2.1 Main conclusions on the Community Summary Report on antimicrobial resistance 2004-2007 This report compiles and analyses data on antimicrobial resistance in Salmonella, Campylobacter, indicator (or commensal) E. coli and indicator (commensal) enterococci isolates from animals and food that were reported by the European Union (EU) Member States (MSs) and two non-mss during the 2004-2007 period. A special attempt was made to investigate the quantitative data reported on the resistance. Quantitative antimicrobial resistance data expressed as Minimum Inhibitory Concentrations (MIC) or inhibition zone diameters were, for the first time, interpreted using similar epidemiological cut-off values, which means that data are comparable as regards the limits used to define the resistant 1 isolates. This enables better data analyses between the reporting countries. The monitoring and reporting of antimicrobial resistance in bacteria from animals and food were not harmonised during the years 2004-2007. Antimicrobial resistance in Salmonella and Campylobacter bacteria originating from animals and food may compromise the effective treatment of human salmonellosis and campylobacteriosis cases caused by these bacteria. Resistance in commensal E. coli and enterococci is an indicator of the general resistance levels among intestinal bacterial flora in animals and food, and additionally these bacteria may also contribute to the exchange of genes carrying the resistance and occasionally cause human illnesses. Resistance to antimicrobials was commonly found among the Salmonella, Campylobacter and the indicator E. coli and enterococci isolates from animals and food in the EU. For most of the tested antimicrobials, large differences in the occurrence of resistance were observed between MSs. The differences observed between MSs may be due to real differences in the resistance situation but sometimes also because of differences in the monitoring system in place and in the case of Salmonella, because of the serovars present in MSs. Fluoroquinolones are critically important antimicrobials in human medicine and fluoroquinolone resistant bacteria in animals and food may particularly hamper the effective treatment of food-borne bacterial infections in humans. Therefore, the high occurrence of resistance to ciprofloxacin, a fluoroquinolone substance, in Salmonella isolates from fowl (Gallus gallus) reported by some MSs is worrisome, as well as the fluoroquinolone resistance commonly reported among the C. jejuni and C. coli isolates from animals and broiler meat in several MSs. Third generation cephalosporins are also antimicrobials of critical importance in human medicine. Epidemiological resistance to third generation cephalosporins was detected at low levels by some MSs in tested Salmonella isolates from both animals and meat and in E. coli isolates from animals. Macrolides are another critically important antimicrobial group for human medicine, and moderate to high levels of resistance to these substances were reported by some MSs in Campylobacter isolates from broilers and pigs. The occurrence of antimicrobial resistance in Salmonella spp. and particularly in S. Enteritidis from fowl (Gallus gallus) was at a lower level than in Salmonella spp. and S. Typhimurium isolates from pigs and cattle. Only ciprofloxacin and nalidixic acid resistance levels were higher in Salmonella spp. and S. Enteritidis isolates from fowl (Gallus gallus). Ampicillin, sulfonamide, tetracycline and chloramphenicol resistance were more commonly observed in Salmonella spp. and S. Typhimurium isolates from pigs and cattle. 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 than S. Enteritidis, a serovar typically related to fowl. 1 Isolates having higher MIC than the cut-off value or lower/equal to the inhibition zone diameter than the cut-off value. 14 EFSA Journal 2010; 8(4):1309 14/304

MAIN FINDINGS 2. In indicator E. coli isolates from fowl (Gallus gallus) and pigs, large variations in the resistance levels reported were observed between MSs. For isolates from Gallus gallus and pigs, the same MSs tended to report high resistance levels to several antimicrobials and some of these countries also reported high resistance levels in both Gallus gallus and pig isolates. In cattle, the occurrence of resistance in E. coli isolates was lower compared to isolates from Gallus gallus and pigs. Resistance to vancomycin, an important substance in human medicine and a relative to avoparcin, was still reported in indicator E. faecium or E. faecalis isolates from Gallus gallus, pigs and cattle. These findings show that although the use of avoparcin as a feed additive was banned across the EU in 1997, the resistance genes still remain present in the bacterial population for a number of years. At MS level, the occurrence of antimicrobial resistance over time remained in most cases relatively stable. However, some decreasing and increasing tendencies were observed. With few exceptions, no major differences in resistance were observed when comparing antimicrobial resistance levels in C. jejuni and C. coli isolates from Gallus gallus and meat from broilers. However, significant differences in resistance levels were observed between Salmonella spp. from Gallus gallus and broiler meat. That may be because the Gallus gallus category included isolates not only from broilers but also from laying hens and breeding flocks. The number of MSs reporting quantitative data on antimicrobial resistance in isolates from animals and food in accordance with Directive 2003/99/EC has increased during the period 2004 to 2007, from 18 MSs in 2004 to 21 MSs in 2006 and 20 MSs in 2007. This progress is promising and will provide valuable information for further analyses of antimicrobial resistance trends in the EU. EFSA Journal 2010; 8(4):1309 15/304 15

2. MAIN FINDINGS 2.2 Agent-specific summaries Salmonella Information on antimicrobial resistance in tested Salmonella isolates from animals and food were reported by 26 MSs. Annual quantitative data was provided by 21 MSs. Most of the data derived from animals, mainly from poultry, pigs and cattle. Food data were in most cases from the meat of these animal species. Data were analysed for Salmonella spp., i.e. for all Salmonella serovars that were reported grouped together, as well as separately, for the most significant for public health and common serovars. As certain Salmonella serovars and phage types are recognised to be more resistant than others, some of the observed differences in antimicrobial resistance in Salmonella spp. between animal species and reporting MSs may in part be due to different serotype and phage type distributions among animal species and countries as included in the national reports. Poultry quantitative data Only small differences in the occurrence of antimicrobial resistance in S. Enteritidis isolates from fowl (Gallus gallus) were observed between the reporting MSs, except in the case of ciprofloxacin and nalidixic acid. Together, at reporting MS group level 5% to 26% of the isolates were found resistant to ciprofloxacin or nalidixic acid in the years 2004 to 2007 and resistance varied between countries from 0% to 66% and from 0% to 86%, respectively. For the remaining tested antimicrobials, the reported occurrences of resistance were low and no resistance was reported for a number of antimicrobials in several countries. When resistance data from all Salmonella serotypes from Gallus gallus were compiled, the occurrence of resistance was higher compared to the resistance reported on S. Enteritidis isolates. In particular, tetracycline, ampicillin and sulfonamide resistance became more prevalent among all the Salmonella spp. isolates being at the levels of 5% to 25% of the tested isolates at reporting MS group level. The reported ciprofloxacin and nalidixic acid resistance varied between 6% to 36% and between 15% to 41%, respectively, among the Salmonella spp. isolates at MS group level. Resistance to tetracycline, ampicillin, sulfonamide, ciprofloxacin and nalidixic acid were commonly reported among Salmonella spp. isolates from broiler meat, and the resistance levels in 2007 were up to 37% at reporting MS group level. The reported MS group resistance level for ciprofloxacin was 29% in 2007. Reported antimicrobial resistance levels in Salmonella spp. isolates from fowl and broiler meat were compared. Fowl (Gallus gallus) represents both the laying hen and the broiler productions, and both breeding and production animals are included in the category as well, while meat from broilers is assumed to originate mainly from broilers. This might explain some of the significant differences observed between resistance levels. The broiler meat sampled in countries may have originated from domestic meat production or be imported. As the occurrence of resistance varies between countries, the proportion of isolates that originate from imported products might have a large influence on the reported occurrence of resistance and therefore the occurrence of resistance in isolates from animals and food is not necessarily comparable. Among Salmonella spp. isolates from turkeys, resistance to tetracycline, ampicillin, sulfonamide, ciprofloxacin and nalidixic acid were common and the resistance levels were 60%, 37%, 47%, 38% and 33%, respectively, in the reporting MS group in 2007. Together 13 MSs provided data on antimicrobial resistance from the 2006 to 2007 EU-wide baseline survey on the prevalence of Salmonella in turkey flocks. Tetracycline, ampicillin, sulfonamide, streptomycin and nalidixic acid resistance were commonly reported by the nine MSs whose data was analysed. The resistance levels varied between 25% and 53% in this group of reporting MSs. The serovars most often tested from the baseline survey for antimicrobial resistance were S. Hadar, S. Derby, S. Kottbus and S. Typhimurium. In 2007, the occurrence of resistance to most antimicrobials was clearly higher in Salmonella spp. isolates from turkeys compared to those collected from Gallus gallus. The reported proportions of ceftiofur and cefotaxime resistant isolates from Gallus gallus, turkeys and broiler meat varied between 0% and 2%. Pigs quantitative data During the period 2004 to 2007, the resistance levels in Salmonella spp. isolates to ampicillin, tetracycline and sulfonamide were high and varied between 23% and 57% over the years at reporting MS group level, although considerable variation was also observed between reporting MSs. Finland and Sweden 16 EFSA Journal 2010; 8(4):1309 16/304

MAIN FINDINGS 2. reported the lowest occurrences of resistance. In general, ciprofloxacin and nalidixic acid resistance was low at reporting MS group level, representing 1% to 7% of tested isolates. S. Typhimurium was the main serovar susceptibility tested from pigs and therefore, the overall picture of the occurrence of resistance in S. Typhimurium is similar to that described for Salmonella spp. in pigs. Resistance to tetracycline, ampicillin and sulfonamide was the most commonly observed resistance in Salmonella spp. from pig meat, and resistance levels observed in the reporting MS group ranged from 40% to 56% in 2007. A relatively low (between 0% and 4%) occurrence of resistance to ciprofloxacin and nalidixic acid was observed in the reporting MS group over the period. During 2004 to 2007, the reported levels of resistance to third generation cephalosporin (ceftiofur and cefotaxime) in tested Salmonella spp. isolates from pigs and meat thereof were low, even though reported data were relatively scarce. Together, 14 MSs provided antimicrobial resistance data from the EU-wide baseline survey in 2006 to 2007 on the prevalence of Salmonella in slaughter pigs. The data were analysed for nine MSs, and resistance to tetracycline, ampicillin, sulfonamide and streptomycin was commonly reported. In this MS group resistance levels varied between 25% to 40% for Salmonella spp. and 41% to 58% for S. Typhimurium. Resistance to nalidixic acid among the Salmonella spp. and S. Typhimurium isolates tested were 13% and 11%, respectively. Gentamicin resistance was rarely reported. The main serovars tested in the baseline survey were S. Typhimurium, S. Derby and S. Enteritidis. Cattle quantitative data Resistance to ampicillin, tetracycline and sulfonamide were common among Salmonella spp. isolates from cattle, and resistance levels varied between 18% and 40% over the years in the reporting MS group. However, large variations were observed between MSs. Ciprofloxacin and nalidixic acid resistance were relatively moderate in most MSs, and remained at reporting MS group level between 1% and 23%. Although the number of MSs reporting data on resistance to ceftiofur and cefotaxime in tested Salmonella spp. isolates from cattle was low, reported resistance was almost non-existent over the years. Resistance levels for tetracycline and chloramphenicol appeared to be decreasing in several MSs over the years. Qualitative data Qualitative data on antimicrobial resistance in Salmonella isolates were analysed for Gallus gallus, broiler meat, turkeys, pigs, pig meat, cattle and bovine meat. In the analyses of qualitative data on antimicrobial resistance in Salmonella for the countries not providing adequate quantitative data, in most cases no general trends over the reporting years in resistance levels were observed. However, there was a general increasing tendency in tetracycline resistance in Salmonella spp. from turkeys among reporting MSs. In contrast, reported resistance levels to tetracycline and ampicillin in Salmonella spp. isolates from cattle seemed to be generally decreasing among reporting MSs. Campylobacter Information on antimicrobial resistance in Campylobacter isolates from animals and food were reported by 13 MSs. Most of the data derived from poultry, pigs and cattle as well as meat thereof. Data were analysed separately for C. jejuni and C. coli due to their different resistance patterns. Generally, resistance ratios reported among C. jejuni were lower than those reported among C. coli isolates from fowl and cattle. Fowl (Gallus gallus) quantitative data Resistance data among Campylobacter isolates from fowl derived mainly from broilers. At reporting MS group level the occurrence of resistance to tetracycline in C. jejuni and C. coli isolates from fowl varied between 6% to 35% and 73% to 77%, respectively, throughout 2004 to 2007. During the same period the resistance levels to ciprofloxacin and nalidixic acid were between 33% to 64% and 4% to 68%, respectively, among the tested C. jejuni and C. coli isolates in the reporting MS group. Within C. jejuni isolates from fowl, the occurrence of tetracycline, ciprofloxacin and nalidixic acid resistance varied considerably between MSs with some countries having no or low occurrence of resistance, while other countries reported more than 50% resistance levels. In some MSs the reported occurrence of ciprofloxacin resistance was very high varying between 50% and 100% of the isolates tested. Resistance to erythromycin (a macrolide) reported at MS group level was at a low level among C. jejuni isolates and at a moderate level for C. coli, with up to 4% and 21% of resistance levels reported, respectively, during the years. Resistance to gentamicin (an aminoglycoside) was reported at low levels (0% to 5%). EFSA Journal 2010; 8(4):1309 17/304 17

2. MAIN FINDINGS Among the C. jejuni isolates from broiler meat, the reported resistance levels to tetracycline, ciprofloxacin, nalidixic acid and erythromycin were 37%, 39%, 36% and 3%, respectively, in the reporting MSs group for the year 2007. The reported resistance levels were higher for C. coli isolates from broiler meat, but only very few MSs provided the data. Comparison of antimicrobial resistance among isolates from fowl and broiler meat was possible for C. jejuni and C. coli isolates from 2007. Resistance levels to the different antimicrobials in isolates from broiler meat and Gallus gallus were at the same levels within each country, although the levels of resistance varied between countries. Only one country reported significant differences in resistance observed between isolates from Gallus gallus and broiler meat. Pigs quantitative data In the reporting MS group, the occurrences of tetracycline, ciprofloxacin and nalidixic acid resistance among C. coli isolates varied between 64% to 80%, 35% to 46%, and 30% to 47%, respectively, during 2004 to 2007. Similarly to fowl, considerable variations in resistance to tetracycline, ciprofloxacin and nalidixic acid among C. coli were observed between reporting MSs. The erythromycin resistant levels ranged from 24% to 39% in the reporting MS group. The highest erythromycin resistance was observed among C. coli isolates from pigs, compared to the isolates from fowl and cattle. Cattle quantitative data At reporting MS level resistance to tetracycline among C. jejuni isolates from cattle, varied between 23% to 33% in the years 2004 to 2007, whereas resistance levels to ciprofloxacin and nalidixic acid were between 20%-35%. Resistance to erythromycin varied between 1% to 3% and resistance to gentamicin between 0% to 1% among the C. jejuni isolates. The reported resistance levels were higher for C. coli isolates from cattle, but only very few MSs provided the data Indicator Escherichia coli (commensal) Information on antimicrobial resistance in indicator E. coli isolates from animals and food were reported by 20 MSs. Out of these, 16 MSs provided quantitative data. Most of the data derived from poultry, pigs and cattle as well as from meat thereof. Poultry quantitative data Among indicator E. coli isolates from fowl (Gallus gallus), the occurrence of resistance to tetracycline, ampicillin and sulfonamide varied between levels of 7% and 44% in the reporting MS group during the years 2004 to 2007. Resistance levels to ciprofloxacin and nalidixic acid were between 13% to 50%. However, there was a substantial variation between MSs in the resistance levels. In several countries the occurrence of resistance remained relatively constant over time and the same countries tended to report a high occurrence of resistance to several antimicrobials. The reported ceftiofur resistance in E. coli from Gallus gallus varied between 0% and 3% in the reporting MS group in 2004-2007 and the reported MS group cefotaxime resistance level was 4% in 2007. However, resistance levels up to 28% were reported by some MSs. Pigs quantitative data Similarly, among E. coli isolates from pigs, the occurrence of resistance to tetracycline, ampicillin and sulfonamide varied considerably between reporting MSs, at reporting MS group level; resistance levels ranged from 17% to 68% over the period. Resistance levels to ciprofloxacin and nalidixic acid were between 4% to 24%. In most cases the countries that reported a high occurrence of resistance in E. coli from Gallus gallus also had a high occurrence of resistance in E. coli from pigs. The occurrence of ceftiofur and cefotaxime resistance among E. coli isolates from pigs varied between 0% to 1% in the reporting MS group. Cattle quantitative data In general, resistance to tetracycline, ampicillin, sulfonamide, ciprofloxacin and nalidixic acid among E. coli isolates from cattle was less often observed compared to isolates from Gallus gallus and pigs, and the variation in resistance levels between countries was much smaller compared to the variation observed for Gallus gallus and pigs. The reported tetracycline, ampicillin and sulfonamide resistance levels varied between 8% to 28% in the reporting MS group in 2004-2007, and the resistance levels to ciprofloxacin and nalidixic acid between 3% to 33%, The occurrence of ceftiofur and cefotaxime resistance among E. coli isolates from cattle varied between 0% to 2% in the reporting MS group. 18 EFSA Journal 2010; 8(4):1309 18/304

MAIN FINDINGS 2. Qualitative data Qualitative data on antimicrobial resistance in indicator E. coli isolates were analysed for Gallus gallus, turkeys, pigs, pig meat and cattle. In the analyses of the qualitative data on antimicrobial resistance in indicator E. coli for countries not providing adequate quantitative data, no general trends over the reporting years in resistance levels were observed. Indicator enterococci (commensal) quantitative data Quantitative information on antimicrobial resistance in enterococci isolates from animals and food were reported by eight MSs. Most of the data derived from Gallus gallus, pigs and cattle. Data were analysed separately for E. faecium and E. faecalis. The majority of data on antimicrobial resistance in indicator E. faecium and E. faecalis were reported for 2007. In particular, the occurrence of tetracycline resistance (31% to 85% at reporting MS group level), streptomycin (16% to 59%) and erythromycin resistance (23% to 48%) occurred frequently in E. faecium and E. faecalis isolates from Gallus gallus, pigs and cattle. However, a large variation was observed between reporting MSs. Also, E. faecium isolates resistant to vancomycin were reported from Gallus gallus, pigs and cattle (1% to 2% in the reporting MS group), even though the use of avoparcin as a growth promoter was banned in the EU in 1997. In addition, two countries reported vancomycin resistance in E. faecalis isolates. Cross-resistance is observed between avoparcin and vancomycin, an important antimicrobial used in humans. EFSA Journal 2010; 8(4):1309 19/304 19

20 EFSA Journal 2010; 8(4):1309 20/304

MATERIALS AND METHODS 3 Materials and methods 3 21

3. MATERIALS AND METHODS 3.1 Antimicrobial susceptibility data available During the period 2004 to 2007, 26 MSs and two non-mss monitored and reported annually on antimicrobial resistance in tested Salmonella and Campylobacter isolates from animals and food, as well as on indicator organisms (commensal E. coli and commensal enterococci). In addition, some MSs also reported data on antimicrobial resistance among Salmonella isolated from the EU-wide baseline surveys on Salmonella in turkeys and slaughter pigs. Both dilution and diffusion methods were used by countries for susceptibility testing, and both quantitative and qualitative data were reported. Quantitative data reported as 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. 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 Salmonella isolates 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. 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. An exception for this rule is when quantitative data were only available from one year and qualitative data were available for more than one year. In this case the qualitative data were used. Also, in the case of qualitative results, data from less than 10 tested isolates per MS were not included in the report. A total of 26 MSs and two non-mss provided information on antimicrobial resistance in the years 2004 to 2007. All susceptibility data reported were addressed and the vast majority were included in this report. An overview of data included in the report is shown in Table MM1. Table MM1. Data included in the report: number of isolates tested for antimicrobial susceptibility by MIC and disk diffusion, and number of isolates where only qualitative data were reported, 2004-2007 Data included in the report Quantitative data Isolates tested by: Qualitative data MIC Disk diffusion Salmonella 128,184 19,895 204,712 Campylobacter 52,697 0 0 Indicator E. coli 149,061 28,065 129,363 Indicator enterococci 28,701 0 0 Throughout the report, reference is made to the United Kingdom, although most of the data reported originates almost exclusively from England and Wales. 22 EFSA Journal 2010; 8(4):1309 22/304

MATERIALS AND METHODS 3. 3.1.1 Data reported under Directive 2003/99/EC from 2004 to 2007 MSs generated data on antimicrobial susceptibility through the testing of bacteria isolated from animal/ food samples collected by using different schemes. Often the isolates tested constituted 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. From 2004 to 2007, 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. Many MSs reported antimicrobial resistance data both as quantitative and qualitative data. However, some countries only reported qualitative data or only a subset of all data as quantitative 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 were analysed separately and are presented in Chapter 8 for both Salmonella and indicator E. coli. Data were provided in aggregated format, and therefore it was not possible to describe and analyse cross-resistance among isolates. 3.1.2 Data reported from the EU-wide Salmonella baseline surveys Two European Union-wide baseline surveys were carried out in 2006 to 2007 to assess Salmonella prevalence in slaughter pigs and in breeding and fattening turkey flocks. In the framework of these baseline surveys, MSs were also invited to submit antimicrobial susceptibility data among the Salmonella isolates collected. However, susceptibility testing was not a compulsory requirement of the survey. Therefore only a limited number of MSs reported the data. Both broth dilution and disk diffusion methods were applied by MSs to test the susceptibility of isolates from the baselines surveys. Inhibition zone diameters, for several isolates, were reported as zero, which is an inconsistent result as the minimum disk diameter can be 6 mm. In the baseline survey on Salmonella prevalence in slaughter pigs, 4.8% of the tested isolates were reported as an inhibition zone diameter equal to zero. For 95.9% of these isolates the susceptibility status was coded susceptible, and for 4.1% it was coded resistant. For the baseline survey on Salmonella prevalence in turkey flocks fewer inhibition zones equal to zero were reported (together 4%) and those were classified by MSs as susceptible (21%) and resistant (79%). However, since 0 is out of the test range and it is not possible, based on the reported susceptibility status, to interpret the results or to define the actual inhibition zone diameter, these isolates were excluded from this report. 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 for different antimicrobial classes and taking into account EFSA s reports on harmonised monitoring and reporting on antimicrobial resistance data (EFSA, 2007, 2008a). 3.2.1 Antimicrobials for susceptibility testing of Salmonella MIC distributions were made for the following antimicrobials: ampicillin, apramycin, chloramphenicol, cefotaxime, ceftazidime, ceftiofur, ciprofloxacin, florfenicol, gentamicin, nalidixic acid, neomycin, spectinomycin, streptomycin, sulfonamide, tetracycline and trimethoprim (Appendix 2). Tables MM2 and MM3 present the antimicrobials selected by the different countries for the susceptibility testing of Salmonella isolates from animals and food by dilution and disk diffusion methods. Quantitative data are described and analysed in Chapter 4. Qualitative data are described in Chapter 8. EFSA Journal 2010; 8(4):1309 23/304 23

3. MATERIALS AND METHODS 3.2.2 Antimicrobials for susceptibility testing of Campylobacter In this report antimicrobial resistance was reported for C. jejuni and C. coli. From 2004 to 2007, almost all quantitative Campylobacter data were reported as MIC values, the only exception being Spain who tested a few antimicrobials (colistin, kanamycin, streptomycin, sulfonamide and tylosin) by diffusion methods. All qualitative data for Campylobacter had also been reported by MSs as quantitative data, except data on meat from broilers from Hungary. Quantitative data are described and analysed in Chapter 5, no qualitative data are described for Campylobacter. Table MM4 presents the antimicrobials selected by the different countries for the susceptibility testing of Campylobacter isolates from animals and food. For the following antimicrobials, MIC distributions were made: tetracycline, chloramphenicol, erythromycin, gentamicin, streptomycin, ciprofloxacin and nalidixic acid (Appendix 3). Table MM2. Antimicrobials selected for susceptibility testing of Salmonella isolates by MS and non-ms reporting quantitative data as MIC distributions Antimicrobial agent Austria Belgium Czech Republic Denmark Estonia Finland Germany Ireland Italy Netherlands Poland Slovakia Spain Sweden Norway Switzerland 3rd generation cephalosporins Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Ampicillin / Sulbactum Apramycin Cefotaxime Cefpodoxime Ceftazidime Ceftiofur Ceftriaxon Cefuroxime Cephalothin Chloramphenicol Ciprofloxacin Colistin Enrofloxacin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Oxolinic acid Spectinomycin Streptomycin Sulfonamide Tetracycline Tobramycin Trimethoprim Trimethoprim + Sulfonamide 24 EFSA Journal 2010; 8(4):1309 24/304

MATERIALS AND METHODS 3. Table MM3. Antimicrobials selected for susceptibility testing of Salmonella isolates by MS and non-ms reporting quantitative data as inhibitions zones Antimicrobial agent Czech Republic Estonia France Greece Hungary Italy Lithuania Portugal Romania Slovakia Slovenia Spain United Kingdom 3rd generation cephalosporins Amikacin Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Apramycin Aztreonam Cefalexin Cefoperazone Cefotaxime Cefoxitin Cefpodoxime Ceftazidime Ceftiofur Ceftriaxon Cefuroxime Cephalothin Chloramphenicol Ciprofloxacin Colistin Doxycyclin Enrofloxacin Florfenicol Flumequin Gentamicin Imipenem Kanamycin Nalidixic acid Neomycin Nitrofurantoin Oxolinic acid Streptomycin Sulfonamide Tetracycline Tobramycin Trimethoprim Trimethoprim + Sulfonamide EFSA Journal 2010; 8(4):1309 25/304 25

3. MATERIALS AND METHODS Table MM4. Antimicrobials selected for susceptibility testing of Campylobacter isolates by MS and non-ms reporting quantitative data as MIC distributions Antimicrobial agent Austria Belgium Czech Republic Denmark Estonia Finland France Germany Hungary Italy Netherlands Slovenia Spain Sweden Norway Switzerland 3rd generation cephalosporins Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Ampicillin / Sublactam Apramycin Chloramphenicol Ciprofloxacin Colistin Enrofloxacin Erythromycin Florfenicol Gentamicin Meropenem Metronidazole Nalidixic acid Neomycin Streptomycin Sulfamethoxazol Tetracycline Trimethoprim Trimethoprim + Sulfamethoxazol 26 EFSA Journal 2010; 8(4):1309 26/304

MATERIALS AND METHODS 3. 3.2.3 Antimicrobials for susceptibility testing of Escherichia coli From 2004 to 2007, both dilution and diffusion methods were used for the susceptibility testing of E. coli isolates from animals and food. Tables MM5 and MM6 display 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. Quantitative data are described and analysed in Chapter 6. Some countries only reported susceptibility data as qualitative data for indicator E. coli. Qualitative data are presented in Chapter 8. MIC distributions were made for the following antimicrobials: tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin, streptomycin, ciprofloxacin and nalidixic acid (Appendix 4). Table MM5. Antimicrobials selected for susceptibility testing of Escherichia coli isolates by MS and non-ms reporting quantitative data as MIC distributions Antimicrobial agent Austria Denmark Estonia Finland France Germany Italy Netherlands Spain Sweden Norway Switzerland 3rd generation cephalosporins Amikacin Amoxicillin Amoxicillin / Clavulanic acid Ampicillin Apramycin Cefotaxime Cefoxitin Cefpodoxime Ceftazidime Ceftiofur Cefuroxime Cephalothin Chloramphenicol Ciprofloxacin Colistin Enrofloxacin Florfenicol Gentamicin Kanamycin Nalidixic acid Neomycin Spectinomycin Streptomycin Sulfonamide Tetracycline Tobramycin Trimethoprim Trimethoprim + Sulfamethoxazol EFSA Journal 2010; 8(4):1309 27/304 27

3. MATERIALS AND METHODS Table MM6. Antimicrobials selected for susceptibility testing of Escherichia coli isolates by MS and non-ms reporting quantitative data as disk inhibition zones Antimicrobial agent Estonia Greece Hungary Italy Poland Portugal Slovakia Slovenia Spain United Kingdom 3rd generation cephalosporins Amikacin Amoxicillin Amoxicillin/Clavulanic acid Ampicillin Apramycin Aztreonam Cefalexin Cefazolin Cefotaxime Cefoxitin Ceftazidime Ceftiofur Ceftriaxon Cefuroxime Cephalothin Chloramphenicol Ciprofloxacin Colistin Doxycyclin Enrofloxacin Florfenicol Flumequin Gentamicin Imipenem Kanamycin Nalidixic acid Neomycin Nitrofurantoin Norfloxacin Oxolinic acid Spectinomycin Streptomycin Sulfonamide Tetracycline Trimethoprim Trimethoprim + Sulfamethoxazol 28 EFSA Journal 2010; 8(4):1309 28/304

MATERIALS AND METHODS 3. 3.2.4 Antimicrobials for susceptibility testing of enterococci From 2004 to 2007, enterococci susceptibility data were only reported by MSs using the dilution method. 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. All qualitative data for E. faecium and E. faecalis were also reported as quantitative data. Quantitative data are described and analysed in Chapter 7, no qualitative data are described for enterococci. For the following antimicrobials, MIC distributions were made: tetracycline, chloramphenicol, ampicillin, erythromycin, streptomycin, vancomycin, quinupristin/dalfopristin, avilamycin and linezolid (Appendix 5). Table MM7. Antimicrobials selected for susceptibility testing of Enterococcus faecium and Enterococcus faecalis isolates by MS and non-ms reporting quantitative data as MIC distributions Antimicrobial agent Austria Denmark Estonia Finland France Netherlands Spain Sweden Norway Switzerland Amoxicillin Amoxicillin/Clavulanic acid Ampicillin Avilamycin Bacitracin Bambermycin Chloramphenicol Ciprofloxacin Erythromycin Flavofosfolipol Florfenicol Gentamicin Kanamycin Lincomycin Linezolid Narasin Neomycin Nitrofurantoin Penicillin Quinupristin/Dalfopristin Salinomycin Streptogramins Streptomycin Teicoplanin Tetracycline Trimethoprim Vancomycin Virginiamycin EFSA Journal 2010; 8(4):1309 29/304 29

3. MATERIALS AND METHODS 3.3 MIC and inhibition zone diameter interpretation In order to evaluate antimicrobial resistance, most countries used standard methods and breakpoints published by the Clinical Standards Laboratory Institute (CLSI, 2008; NCCLS 2001) for the interpretation of MIC and inhibition zone diameter data. However, for some antimicrobials (e.g. ciprofloxacin) not all countries used the same breakpoint for antimicrobial susceptibility testing and, for a few antimicrobials, no CLSI standard breakpoints were established. The use of different breakpoints has a large influence on the proportion of isolates categorised as resistant or susceptible. Thus, to avoid confusion with clinical breakpoints, the term epidemiological cut-off value, has been established to separate between the original wild-type bacterial population and isolates that have developed reduced susceptibility to a given antimicrobial agent (EUCAST; Kahlmeter et al., 2003). In 2007, EFSA recommended that the interpretation of MIC values be changed from using clinical breakpoints to using epidemiological cut-off values (EFSA, 2007). In order not to lose all the data reported as inhibition zone diameters, and as there are currently no available harmonised epidemiological cut-off values for inhibition zone diameters (coming from the disk diffusion method), cut-off values for inhibition zones were set for the use of this report in collaboration with the European Union Reference Laboratory for Antimicrobial Resistance (EU-RL-AR) and where possible and meaningful, based on EUCAST guidelines. The wild-type populations were identified for each individual combination of country, antimicrobial substance and microorganism species, and finally, all inhibition zone diameter data were aggregated, together forming a database of wild-type inhibition zone diameter distributions and a common cut-off was chosen. The dataset used was the combined antimicrobial resistance data reported by the MSs and non-mss in accordance with Directive 2003/99/EC for the years 2004 to 2007. The cut-off value was set at the zone of the distribution where the wild-type population had its end-point. The possible differences in the disk diffusion methods applied were not accounted for in the determination of the cut-off values. More detailed information on the methodology used to establish cut-off values for inhibition zone diameters is given in Appendix 6. Epidemiological cut-off values for MIC and inhibition zone diameters are given in Table MM8. 30 EFSA Journal 2010; 8(4):1309 30/304

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 b) <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-AR from disk diffusion distribution of MSs data were used. b) Cut-off values were not defined by EUCAST, instead cut-off values defined by the EU-RL-AR 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) 141:1-44. 2. Ciprofloxacin disk diffusion data were submitted all as qualitative data not as quantitative (i.e. inhibition zone diameters) therefore no disk diffusion cut-off values were calculated. EFSA Journal 2010; 8(4):1309 31/304 31

3. MATERIALS AND METHODS 3.4 Data description and analysis Data on antimicrobial resistance, submitted by reporting MSs and non-mss under Directive 2003/99/ EC and under the framework of the baseline studies on Salmonella in turkeys and slaughter pigs, were stored in EFSA s zoonoses and baseline databases. A specific flatfile of resistance data was extracted from the databases. In this report, reported antimicrobial resistance 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 to this rule are quantitative data from the United Kingdom and Germany. In the case of the United Kingdom, quantitative data of Salmonella isolates from cattle and pigs were not collapsed into Salmonella spp., whereas for Germany, quantitative data of Salmonella isolates from all the food and animal categories tested were not collapsed into 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 value or the disk diffusion diameter (in mm) was below the cut-off value. The cut-off values for both MIC and disk diffusion are presented in Table MM8. In the case of qualitative data submitted, the proportion of resistant isolates reported by the 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; reporting MS 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. 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). 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. Significance of differences between proportions of resistant isolates was tested by Fishers exact test (2-tailed). In this analysis, a test result was considered significant when the p-value was less then 0.05; p-values were reported to the first significant figure, except p-values smaller than 0.01, which were reported as p<0.01. 32 EFSA Journal 2010; 8(4):1309 32/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4 Antimicrobial resistance in Salmonella - quantitative data 4 33

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA In total, 21 MSs reported quantitative data as MIC values or inhibition zones diameters for Salmonella isolates between 2004 and 2007 in accordance with Directive 2003/99/EC (Tables SA1-3). This includes results of 128,184 Salmonella isolates tested by MIC and 19,895 isolates tested by disk diffusion. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. (covering all reported serovars) for each country, year and food/animal category. In addition, the most prevalent Salmonella serotypes S. Enteritidis and S. Typhimurium were reported separately when sufficient data were available. Thereby, Salmonella spp. represents the overall occurrence of antimicrobial resistance in Salmonella from the different food/animal categories. Exceptions from this rule are quantitative data from the United Kingdom and Germany. In the case of the United Kingdom, quantitative data of Salmonella isolates from cattle and pigs were not collapsed into Salmonella spp. and for Germany, quantitative data of Salmonella isolates from all the food and animal categories reported were not collapsed into Salmonella spp. During 2004 to 2007, the occurrence of resistance to the most relevant antimicrobial agents among Salmonella spp., S. Typhimurium and S. Enteritidis are presented in tables and figures in the following text. The following antimicrobials were selected for in-depth analyses: 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, for Salmonella spp., S. Typhimurium and S. Enteritidis, are presented in Appendix 2. The spatial distributions of tetracycline, ampicillin, and nalidixic acid resistance levels in Salmonella spp. from Gallus gallus, turkeys, pigs and cattle are presented for 2007. For countries where data for 2007 were not available, 2006 resistance levels were used. Table SA1. Overview of countries reporting MIC distributions and inhibition zones on Salmonella spp. from various sampling origins, 2004-2007 Method Origin Total number of MSs reporting Countries Dilution Diffusion Meat from broilers 5 MSs: BE, CZ, DE, EE, SK Non-MS: CH Meat from turkeys 3 MSs: CZ, DE, IT Meat from bovine animals 6 MSs: BE, CZ, DE, FI, IT, SK Meat from pigs 7 MSs: BE, CZ, DE, DK, FI, IT, SK Gallus gallus 11 MSs: AT, CZ, DE, DK, ES, FI, IT, NL, PL, SE, SK Non-MS: NO Turkeys 7 MSs: DE, ES, FI, IE, IT, PL, SK Pigs 11 MSs: DE, DK, EE, ES, FI, IE, IT, NL, PL, SE, SK Non-MS: NO Cattle 9 MSs: DE, DK, EE, ES, FI, IT, NL, SE, SK Non-MS: NO Meat from broilers 7 MSs: CZ, EE, FR, HU, LT, RO, SI Meat from turkeys 2 MSs: EE, SI Meat from pigs 6 MSs: CZ, EE, FR, LT, RO, SI Meat from bovine animals 5 MSs: CZ, EE, FR, RO, SI Gallus gallus 11 MSs: CZ, EE, ES, FR, GR, HU, LT, RO, SI, SK, UK Turkeys 6 MSs: CZ, FR, GR, HU, SI, SK Pigs 11 MSs: CZ, EE, ES, FR, GR, HU, LT, RO, SI, SK, UK Cattle 11 MSs: CZ, EE, ES, FR, GR, HU, LT, RO, SI, SK, UK 34 EFSA Journal 2010; 8(4):1309 34/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA2. Overview of countries reporting MIC distributions and inhibition zones on Salmonella Typhimurium from various sampling origins, 2004-2007 Method Origin Total number of MSs reporting Countries Dilution Diffusion Meat from broilers 2 MSs: CZ, SK Meat from bovine animals 3 MSs: CZ, DE, IT Meat from pig 6 MSs: BE, CZ, DE, DK, IT, SK Gallus gallus 10 MSs: CZ, DE, DK, ES, FI, IT, NL, PL, SE, SK Turkeys 5 MSs: FI, DE, ES, IT, PL Pigs 11 MSs: DE, DK, EE, ES, FI, IE, IT, NL, PL, SE, SK Non-MS: NO Cattle 8 MSs: DK, EE, FI, DE, IT, NL, SE, SK Non-MS: NO Meat from broilers 4 MSs: CZ, EE, FR, SI Meat from turkey 1 MS: SI Meat from pig 5 MSs: CZ, EE, FR, RO, SI Meat from bovine animals 4 MSs: CZ, EE, FR, SI Gallus gallus 6 MSs: CZ, FR, GR, HU, SI, SK Turkeys 3 MSs: CZ, FR, SI Pigs 10 MSs: CZ, EE, ES, FR, GR, HU, RO, SI, SK, UK Cattle 9 MSs: CZ, EE, FR, GR, HU, RO, SI, SK, UK Table SA3. Overview of countries reporting MIC distributions and inhibition zones on Salmonella Enteritidis from various sampling origins, 2004-2007 Method Origin Total number of MSs reporting Countries Dilution Diffusion Meat from broilers 3 MSs: CZ, EE, SK Meat from bovine animals 2 MSs: IT, SK Gallus gallus 7 MSs: CZ, DE, ES, IT, NL, PL, SK Non-MS: NO Turkeys 4 MSs: DE, ES, FI, PL Pigs 5 MSs: EE, ES, DE, PL, SK Cattle 2 MSs: DE, SK Humans 3 MSs: DK, IT, NL Meat from broilers 7 MSs: CZ, EE, FR, HU, LT, RO, SI Meat from turkey 1 MS: SI Meat from pig 2 MSs: RO, SI Meat from bovine animals 2 MSs: EE, FR Gallus gallus 10 MSs: CZ, EE, FR, GR, HU, LT, RO, SI, SK, UK Turkeys 4 MSs: CZ, FR, HU, SI Pigs 6 MSs: CZ, EE, FR, GR, HU, SI Cattle 5 MSs: CZ, EE, FR, GR, SK Humans 2 MSs: GR, IT EFSA Journal 2010; 8(4):1309 35/304 35

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.1 Poultry (Gallus gallus) and broiler meat 4.1.1 Fowl (Gallus gallus) In this report, fowl (Gallus gallus) includes breeding flocks, laying hen flocks, and broiler flocks of Gallus gallus. Overall, 19 MSs and one non-ms provided quantitative data on Salmonella spp. in Gallus gallus (Table SA1). Resistance levels among Salmonella In Salmonella spp. from Gallus gallus susceptibility tested isolates (Table SA4 and Appendix Tables SA1a-d), tetracycline, ampicillin and sulfonamide resistance ranged between 5% and 25%, while resistance to chloramphenicol and gentamicin varied from 0% to 7% in the reporting MS group during the years 2004 to 2007. At the same reporting MS group level, ciprofloxacin and nalidixic acid resistance levels in Salmonella spp. varied between 6% and 36%, and 15% and 41%, respectively, in 2004 to 2007. However, resistance levels reported for ciprofloxacin and nalidixic acid varied between 0% and 92% at MS-specific level (Table SA4). Resistance to third generation cephalosporins was reported at low levels, from 0% to 5% in the reporting MS group in 2007, the Netherlands and Spain reporting in 2007 the highest cefotaxime resistance (13% and 8%, respectively) and the Netherlands the highest ceftazidime resistance levels (13%) in Salmonella spp. isolates (Table SA4 and Appendix 2 Table SA1b). The occurrence of resistance among Salmonella spp. was generally higher compared to resistance in S. Enteritidis. In S. Enteritidis isolates, low levels of resistance were reported for most antimicrobials tested by reporting MSs. In the reporting MS group, the levels of tetracycline, cloramphenicol, ampicillin and sulfonamides varied between 0% and 6% (Table SA5). However, the percentages of resistant isolates reported for ciprofloxacin and nalidixic acid were at a higher level and varied in the reporting MS group between 5% to 25% and 7% to 26%, respectively, during 2004 to 2007. The highest occurrence of ciprofloxacin resistance (66%) was reported by Spain followed by the Netherlands and Poland, where 37% and 24% of the tested isolates were reported resistant (Table SA5). For nalidixic acid, the highest occurrence of resistance was reported by Romania with 86% of resistant isolates, followed by Spain (66%), the United Kingdom (65%) and Slovenia (65%) (Table SA5). Reported resistance levels in the reporting MS group were highest in 2007 for ciprofloxacin and in 2004 for nalidixic acid. Reported resistance levels for third generation cephalosporins were at a very low level, between 0% and 1% for ceftiofur and cefotaxime during the years. The highest occurrence of third generation cephalosporin resistance was reported by Hungary with 6% of resistant isolates, in 2006. Among S. Typhimurium isolates from Gallus gallus the occurrence of resistance to tetracycline, ampicillin and sulfonamide was high and the resistance levels in the reporting MS group were 17%-34%, 17%- 39% and 11%-39%, respectively, during the reporting years (Table SA6). Resistance levels for nalidixic acid and ciprofloxacin were 0%-22% and 0%-17%, respectively. Cefotaxime and ceftiofur resistance was not reported in S. Typhimurium isolates from Gallus gallus. The ability to become resistant varies considerably between Salmonella serovars. Salmonella spp. from Gallus gallus includes serovars such as S. Typhimurium, S. Hadar and S. Virchow, which are often more resistant than S. Enteritidis. This might explain some of the differences between the resistance levels reported between S. Enteritidis and Salmonella spp. in Tables SA4-5. 36 EFSA Journal 2010; 8(4):1309 36/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA4. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 78 0 28 0 78 0 28 0 78 1 28 14 Czech Republic 31 6 25 4 234 0 31 0 25 0 234 0 30 0 25 4 234 0 Denmark 18 17 13 8 18 6 10 20 18 6 13 0 18 0 10 10 18 17 13 0 18 11 10 10 Estonia 11 0 11 18 11 45 Finland 10 0 10 0 10 10 France 132 4 132 2 132 4 Greece 105 22 176 10 116 44 105 14 163 2 117 40 105 7 135 2 111 14 Hungary 122 61 135 60 122 2 144 0 122 3 154 3 Italy 136 49 136 19 136 43 Lithuania 19 11 12 0 19 0 12 0 19 16 12 0 Netherlands 52 21 164 26 52 10 164 4 52 25 164 40 Poland 104 0 443 8 178 4 91 22 105 1 443 2 178 0 91 10 105 4 443 7 178 5 91 16 Romania 81 35 28 4 21 5 Slovakia 173 40 89 2 137 10 110 5 89 1 137 0 110 9 89 6 137 1 Slovenia 31 6 29 0 26 8 33 12 31 0 29 0 26 0 33 0 32 9 29 0 25 0 33 3 Spain 36 14 36 0 294 23 36 3 18 0 294 3 36 22 93 2 Sweden 15 0 15 0 15 7 United Kingdom 46 2 51 0 120 4 46 0 51 0 116 0 46 2 51 4 120 4 Total (18 MSs) 435 25 1,025 12 741 21 1,457 18 436 5 931 2 751 7 1,400 4 437 7 884 5 754 8 1,196 13 EFSA Journal 2010; 8(4):1309 37/304 37

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA4. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 78 0 28 0 78 0 28 7 Czech Republic 234 0 31 6 25 0 234 1 Denmark 18 0 13 0 18 0 20 0 16 11 13 8 18 17 10 10 Estonia 11 27 Finland 10 0 10 0 France 132 3 Greece 102 4 164 5 115 13 Hungary 122 0 153 1 122 65 139 61 Italy 136 3 136 38 Lithuania 12 0 Netherlands 52 2 164 13 52 21 164 41 Poland 105 0 178 0 105 3 443 7 178 11 91 18 Romania 27 52 Slovakia 110 0 89 0 137 0 110 7 89 2 137 10 Slovenia 25 0 33 0 31 0 29 0 25 8 33 3 Spain 36 8 18 6 295 8 18 6 93 0 Sweden 15 0 15 0 United Kingdom 45 0 51 2 120 5 Total (18 MSs) 245 0 91 0 402 0 53 0 36 8 128 1 141 1 991 5 376 23 931 5 743 19 1,202 15 38 EFSA Journal 2010; 8(4):1309 38/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA4. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 78 0 28 0 78 0 28 0 78 0 28 0 Czech Republic 31 0 25 0 234 0 232 3 31 0 25 4 234 3 Denmark 18 0 13 0 18 0 10 0 18 0 13 0 18 6 10 0 18 0 13 0 18 6 10 0 Estonia 11 9 11 55 Finland 10 0 10 10 10 0 France 132 0 132 1 Greece 105 0 160 0 116 0 61 11 174 7 117 40 Hungary 122 0 146 0 70 80 75 87 Italy 136 4 136 31 136 31 Lithuania 19 32 12 0 19 11 12 0 Netherlands 52 0 164 1 52 13 164 43 52 13 164 39 Poland 105 1 443 1 178 1 78 0 105 24 185 21 105 23 441 25 178 25 91 36 Romania 81 1 79 59 Slovakia 110 0 89 0 137 0 110 5 89 3 137 12 110 6 89 3 137 12 Slovenia 31 0 29 0 25 0 33 0 31 61 29 0 25 12 34 6 Spain 36 0 18 0 294 2 36 92 18 61 278 69 36 92 18 61 256 65 Sweden 15 0 15 0 15 0 United Kingdom 46 0 51 0 120 0 45 0 51 65 120 4 Total (18 MSs) 436 2 928 0 751 0 1,444 1 159 36 404 14 187 6 982 33 340 41 939 15 681 31 1,418 27 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. EFSA Journal 2010; 8(4):1309 39/304 39

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA5. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Enteritidis isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Czech Republic 15 0 22 5 195 0 15 0 22 0 195 0 15 0 22 5 195 1 Estonia 11 0 11 18 11 45 France 48 2 48 0 48 2 Germany 426 0 40 0 97 4 426 0 40 0 97 0 426 0 40 0 97 1 Greece 26 0 27 0 19 11 26 0 25 0 19 11 26 0 15 0 Hungary 10 0 19 0 10 0 19 0 10 0 19 5 Lithuania 15 0 12 0 15 0 12 0 15 13 12 0 Netherlands 34 0 19 0 34 0 19 0 34 6 19 0 Poland 104 0 235 1 139 5 44 2 105 1 235 0 139 0 44 0 105 4 235 1 139 4 44 9 Romania 21 14 Slovakia 98 0 73 0 79 0 98 0 73 0 79 0 98 1 73 0 79 0 Slovenia 26 0 22 0 17 0 26 0 22 0 17 0 27 7 22 0 16 0 Spain 185 2 185 1 83 2 United Kingdom 46 2 51 0 120 4 46 0 51 0 116 0 46 2 51 4 120 4 Total (14 MSs) 181 0 869 0 437 2 808 2 182 1 867 0 437 1 783 0 183 4 842 1 432 4 685 2 40 EFSA Journal 2010; 8(4):1309 40/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA5 (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Enteritidis isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Czech Republic 195 0 15 0 22 0 195 0 Estonia 11 27 France 48 0 Germany 426 0 40 0 86 0 426 0 40 0 97 5 Greece 26 0 25 0 19 16 Hungary 10 0 18 6 10 20 19 26 Lithuania 12 0 Netherlands 34 3 19 0 34 0 19 0 Poland 105 0 139 0 105 3 235 3 139 10 44 2 Romania Slovakia 98 0 73 0 79 0 98 1 73 0 79 0 Slovenia 16 0 26 0 22 0 16 0 Spain 186 2 83 0 United Kingdom 45 0 51 2 120 5 Total (14 MSs) 115 0 426 0 213 0 86 0 98 0 107 1 479 1 167 3 866 1 436 6 685 2 EFSA Journal 2010; 8(4):1309 41/304 41

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA5. (contd.) Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Enteritidis isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Czech Republic 15 0 22 0 195 0 193 3 15 0 22 5 195 3 Estonia 11 9 11 55 France 48 0 48 0 Germany 426 0 40 0 97 4 426 4 40 0 97 9 426 4 40 0 97 9 Greece 26 0 25 0 19 0 36 14 19 16 Hungary 10 0 17 0 10 0 Lithuania 15 40 12 0 15 0 12 0 Netherlands 34 0 19 0 34 18 19 37 34 18 19 37 Poland 105 1 235 1 139 1 44 0 105 24 105 18 105 23 233 16 139 30 44 30 Romania 21 0 21 86 Slovakia 98 0 73 0 79 0 98 2 73 3 79 1 98 2 73 3 79 1 Slovenia 26 0 22 0 16 0 26 65 22 0 16 0 Spain 185 1 185 66 185 66 United Kingdom 46 0 51 0 120 0 45 0 51 65 120 4 Total (14 MSs) 182 4 867 0 434 0 808 1 105 24 629 6 147 5 573 25 156 26 875 7 417 22 808 22 42 EFSA Journal 2010; 8(4):1309 42/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA6. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Typhimurium isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Denmark 18 17 13 8 18 6 10 20 18 6 13 0 18 0 10 10 18 17 13 0 18 11 10 10 France 23 17 23 13 23 17 Germany 22 9 22 5 22 9 Italy 14 71 14 71 14 86 Netherlands 18 61 11 64 18 28 11 27 18 61 11 55 Poland 12 92 12 67 12 67 Slovakia 10 50 10 50 10 90 Spain 15 33 15 20 10 0 Sweden 12 0 12 0 12 8 Total (9 MSs) 18 17 23 26 36 33 119 34 18 6 23 22 36 14 119 24 18 17 23 39 36 36 114 30 Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Denmark 18 0 13 0 18 0 20 0 16 11 13 8 18 17 10 10 France 23 17 Germany 22 0 22 14 Italy 14 0 14 79 Netherlands 18 0 11 0 18 61 11 73 Poland 12 92 Slovakia 10 0 10 50 Spain 15 0 10 0 Sweden 12 0 12 0 Total (9 MSs) 18 0 13 0 18 0 42 0 10 0 18 0 52 0 16 11 23 26 36 39 114 33 EFSA Journal 2010; 8(4):1309 43/304 43

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA6. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella Typhimurium isolates from Gallus gallus, 2004-2007, using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Denmark 18 0 13 0 18 0 10 0 18 0 13 0 18 6 10 0 18 0 13 0 18 6 10 0 France 23 0 23 4 Germany 22 0 22 0 22 0 Italy 14 0 14 14 14 14 Netherlands 18 0 11 0 18 6 11 0 18 6 11 0 Poland 12 0 12 67 Slovakia 10 0 10 40 10 50 Spain 15 0 15 33 15 33 Sweden 12 0 12 0 12 0 Total (9 MSs) 18 0 23 0 36 0 119 0 18 0 23 17 36 6 84 8 18 0 23 22 36 6 119 13 44 EFSA Journal 2010; 8(4):1309 44/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Temporal trends in resistance among Salmonella spp. In general, the occurrence of resistance among Salmonella spp. from Gallus gallus remained relatively low for most antimicrobials over time and did not vary considerably between countries (Figures SA1-6). However, there were some exceptions: in Hungary, resistance levels of 60% to 65% to tetracycline and sulfonamide were observed and 80% to 87% level for nalidixic acid, while in Spain 61% to 92% of the isolates were resistant to nalidixic acid and/or ciprofloxacin during the reporting years. Although the occurrence of resistance remained relatively stable over time in Salmonella spp. isolates from fowl, some changes were observed and the majority of these changes were increases. Figure SA1. Trends in tetracycline resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Czech Republic Denmark Greece Hungary Lithuania Netherlands Poland Slovakia Slovenia Spain UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA2. Trends in chloramphenicol resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Czech Republic Denmark Greece Hungary Lithuania Netherlands Poland Slovakia Slovenia Spain UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. EFSA Journal 2010; 8(4):1309 45/304 45

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA3. Trends in ampicillin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Czech Republic Denmark Greece Hungary Lithuania Netherlands Poland Slovakia Slovenia Spain UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA4. Trends in sulfonamide resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Czech Republic Denmark Greece Hungary Netherlands Poland Slovakia Slovenia Spain UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. 46 EFSA Journal 2010; 8(4):1309 46/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA5. Trends in ciprofloxacin resistance in Salmonella spp. from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Netherlands Poland Slovakia Spain Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA6. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Czech Republic Denmark Greece Hungary Lithuania Netherlands Poland Slovakia Slovenia Spain UK Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. EFSA Journal 2010; 8(4):1309 47/304 47

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Temporal trends in resistance among S. Enteritidis For S. Enteritidis, only trends in resistance to nalidixic acid and ciprofloxacin are presented (Figures SA7 and SA8) due to low levels of resistance reported for most other antimicrobials. In most MSs, the occurrence of ciprofloxacin and nalidixic acid resistance remained relatively unchanged over the years. However, in 2006, an important increase in nalidixic acid resistance was observed in the United Kingdom who reported that this increase was caused by infections with nalidixic acid resistant S. Enteritidis PT1 and epidemiologically linked to poultry farms. Figure SA7. Trends in nalidixic acid resistance in tested Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Germany Greece Lithuania Netherlands Poland Slovakia Slovenia UK Figure SA8. Trends in ciprofloxacin resistance in tested Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Germany Netherlands Poland Slovakia 48 EFSA Journal 2010; 8(4):1309 48/304

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. are shown in Figures SA9-11. Tetracycline resistance levels ranged from 0% to 60% among reporting MSs. Sweden, Finland, Estonia, Lithuania, the Czech Republic and Austria reported no resistance to tetracycline, while higher occurrences of resistance were reported by southern European countries (Figure SA9). Less variation was reported on ampicillin resistance, where most countries reported resistance levels below 17%, except Estonia, Italy and the Netherlands (Figure SA10). The Nordic MSs, Austria and Lithuania, reported 0% resistance to nalidixic acid, while Spain, Hungary and Romania reported resistance levels equal to or higher than 59% (Figure SA11). For resistance to ampicillin and nalidixic acid, no clear spatial distribution at EU level could be observed. Figure SA9. Spatial distribution of tetracycline resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, Estonia, Greece, Hungary, Lithuania and Portugal, 2006 data were used. EFSA Journal 2010; 8(4):1309 49/304 49

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA10. Spatial distribution of ampicillin resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, Estonia, Greece, Hungary, Lithuania and Portugal, 2006 data were used. 50 EFSA Journal 2010; 8(4):1309 50/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA11. Spatial distribution of nalidixic acid resistance among Salmonella spp. from Gallus gallus in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, Estonia, Greece, Hungary, Lithuania and Portugal, 2006 data were used. 4.1.2 Meat from broilers (Gallus gallus) Resistance levels among Salmonella Overall 10 MSs and one non-ms provided quantitative data on Salmonella spp. isolates from broiler meat. MIC distributions from Salmonella spp. isolated from broiler meat were only reported in 2007, while a few countries reported inhibition zones before 2007. Most of the data derive from 2007. Resistance to tetracycline, ampicillin, sulfonamide, ciprofloxacin and nalidixic acid were the most commonly reported, and in 2007 the resistance levels in the reporting MS group were 28%, 39%, 37%, 29% and 34%, respectively. Ciprofloxacin resistance varied between 4% to 36% in individual MSs (Table SA7 and Appendix Table SA4). Only Hungary and Switzerland tested for ceftiofur resistance and no resistance was reported (Table SA7). EFSA Journal 2010; 8(4):1309 51/304 51

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA7. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. from meat from broilers, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2006 2007 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Belgium 459 24 459 6 459 44 Czech Republic 24 8 24 0 24 0 24 0 Estonia 17 53 21 5 12 8 17 6 22 0 12 0 17 18 22 14 12 8 France 28 36 28 14 28 21 Hungary 20 0 20 0 20 0 20 0 Romania 75 57 75 3 75 31 Slovakia 11 27 11 0 11 9 10 0 Slovenia 13 38 13 15 13 23 Total (8 MSs) 17 53 34 18 32 3 597 28 17 6 35 6 32 0 597 6 17 18 35 17 32 3 597 39 20 0 0 0 34 0 Switzerland 25 64 25 12 25 12 25 0 52 EFSA Journal 2010; 8(4):1309 52/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA7. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. from meat from broilers, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Country Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid 2004 2005 2006 2007 2004 2005 2006 2007 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Belgium 800 38 459 30 459 27 Czech Republic 24 8 24 0 24 4 24 4 Estonia 17 53 21 5 12 0 17 0 22 0 12 0 17 47 22 86 12 92 France 28 39 28 0 28 21 Hungary 20 0 20 0 Romania 52 29 75 4 75 88 Slovakia 11 27 11 0 11 36 11 36 Slovenia 13 31 13 8 13 23 Total (8 MSs) 17 53 34 15 12 0 915 37 17 0 35 3 32 0 138 2 494 29 17 47 35 63 32 35 597 34 Switzerland 25 72 25 4 25 88 25 88 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. EFSA Journal 2010; 8(4):1309 53/304 53

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.2 Turkeys Resistance levels among Salmonella Together, 12 MSs provided quantitative data on Salmonella spp. isolates from turkeys (Table SA1). Most data derive from 2007. In general, resistance to most antimicrobials was common among Salmonella spp. from turkeys, although differences were observed between MSs. In 2007, resistance levels in the reporting MS group were 60% for tetracycline, 38% for ciprofloxacin, 33% for nalidixic acid, 5% for gentamicin and 47% for sulfonamides (Table SA8). Ireland was the only country that reported no ciprofloxacin and nalidixic acid resistance. In the case of third generation cephalosporins, resistance levels in the reporting MS group ranged between 0% and 2% in 2005 to 2007. Italy reported 4% of the isolates resistant to cefotaxime and ceftazidime (Table SA8 and Appendix 2 Table SA5). When comparing resistance levels in Salmonella spp. isolated from Gallus gallus and turkeys in 2007 at country level, the occurrence of resistance to most antimicrobials was significantly higher in isolates from turkeys compared to isolates from Gallus gallus. The observed differences in antimicrobial resistance between these two poultry species may partly be due to differences in serotype and phage type distributions in Gallus gallus and turkeys. 54 EFSA Journal 2010; 8(4):1309 54/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA8. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from turkeys, 2005-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Country 2005 2006 2007 2005 2006 2007 2005 2006 2007 2005 2006 2007 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Czech Republic 73 14 73 5 73 8 France 50 74 50 10 50 20 Greece 13 31 13 23 13 0 Ireland 90 22 90 0 90 7 90 0 90 0 Italy 247 89 247 6 247 58 247 4 247 4 Poland 96 46 96 19 96 39 Slovakia 40 85 40 8 40 48 40 0 40 0 Slovenia 20 20 20 0 20 20 20 0 20 0 Total (8 MSs) 0 13 31 616 60 0 13 23 616 7 0 13 0 616 37 0 0 20 0 377 2 377 2 EFSA Journal 2010; 8(4):1309 55/304 55

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA8. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from turkeys, 2005-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2005 2006 2007 2005 2006 2007 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Czech Republic 73 14 73 3 73 7 France 50 76 50 4 50 6 Greece 10 40 10 0 13 31 Ireland 90 22 90 0 90 0 90 0 Italy 247 59 247 7 247 55 247 55 Poland 96 43 67 4 96 50 Slovakia 40 78 40 8 40 20 40 20 Slovenia 12 83 20 25 20 5 20 10 Total (8 MSs) 12 83 10 40 616 47 0 10 0 587 5 0 0 377 38 0 13 31 616 33 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. 56 EFSA Journal 2010; 8(4):1309 56/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Spatial distribution of resistance among Salmonella The spatial distributions of tetracycline, ampicillin and nalidixic acid resistance in turkey isolates are shown in Figures SA12-14. Only eight countries reported enough quantitative data on antimicrobial resistance in Salmonella spp. isolates from turkeys which makes it difficult to show spatial patterns. However, resistance to tetracycline seems to be highest in southern European MSs. Figure SA12. Spatial distribution of tetracycline resistance among Salmonella spp. from turkeys in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Greece and the Netherlands, 2006 data were used. EFSA Journal 2010; 8(4):1309 57/304 57

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA13. Spatial distribution of ampicillin resistance among Salmonella spp. from turkeys in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Greece and the Netherlands 2006 data were used. 58 EFSA Journal 2010; 8(4):1309 58/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA14. Spatial distribution of nalidixic acid resistance among Salmonella spp. from turkeys in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Greece and the Netherlands, 2006 data were used. 4.2.1 Resistance data from the baseline survey on the prevalence of Salmonella in turkey flocks in the EU An EU-wide baseline survey was carried out to determine the prevalence of Salmonella in commercial turkey holdings. The sampling of turkey flocks took place between October 2006 and September 2007. A total of 539 breeding turkey flocks and 3,769 fattening turkey flocks, from EU MSs and Norway, were included in the survey analyses. MSs were also invited to submit antimicrobial susceptibility data if the Salmonella isolates were susceptibility tested. However, this was not a compulsory requirement of the survey and was not addressed by the baseline report. Together, 13 MSs provided data on antimicrobial resistance. Together, 4.8% of the antimicrobial resistance test results were reported with an inhibition zone equal to zero. However, since zero is not a valid result when determining inhibition zones and zero was interpreted both as resistant (95.9%) and as susceptible (4.1%) to a given antimicrobial, these results were excluded from this report. Table SABT1 shows the countries reporting MIC values and inhibition zones on Salmonella from breeding and fattening turkeys. EFSA Journal 2010; 8(4):1309 59/304 59

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SABT1. Overview of MSs reporting MIC distributions and inhibition zones on Salmonella in breeding and fattening turkeys baseline survey, 2006-2007 Production type Method Total number of MSs reporting Countries Breeding Dilution 1 MS: SK Diffusion 3 MSs: IT, SK, UK Fattening Dilution 6 MSs: AT, DE, ES, NL, PL, SK Diffusion 8 MSs: BE, CY, CZ, IT, LT, SI, SK, UK Table SABT2. Antimicrobials selected for susceptibility testing of Salmonella isolates by MSs in the turkey baseline survey Antimicrobial agent Amikacin Amoxicillin Amoxicillin / Clavulanic acid Amoxicillin / Ampicillin Ampicillin Apramycin Cefotaxime Ceftiofur Cefuroxime Ceftazidime Ceftriaxone Cephalotin Chloramphenicol Ciprofloxacin Colistine Enrofloxacin Florfenicol Flumequin Gentamicin Kanamycin Nalidixic acid Neomycin Nitrofurans Spectinomycin Streptomycin Sulfonamide / Trimethoprim Sulfonamides Tetracycline Trimethoprim Austria Belgium Cyprus Italy Lithuania Czech Republic Netherlands Poland Slovakia Slovenia Spain United Kingdom 60 EFSA Journal 2010; 8(4):1309 60/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Since the number of isolates tested by MSs was not necessarily proportional to the number of samples included in the baseline survey, data from MSs either susceptibility testing less than 10 isolates or reporting their data only as resistant or susceptible (i.e. qualitative data), without reporting the MIC or inhibition zone diameter, were excluded from the description. Since only three countries susceptibility tested isolates from breeding flocks, only data on the occurrence of resistance among isolates from fattening turkey flocks are described. This meant that data from nine MSs were analysed.the following antimicrobials are included in Table SABT4: tetracycline, chloramphenicol, florfenicol, ampicillin, sulfonamide, gentamicin, neomycin, streptomycin and nalidixic acid. Salmonella Bredeney, S. Hadar and S. Saintpaul were the most commonly reported serovars from fattening flocks among participating MSs (Table SABT3). However, Salmonella Kottbus, S. Saintpaul and S. Typhimurium were most often susceptibility tested as shown in Table SABT3. Table SABT4 shows the occurrence of resistance to selected antimicrobials among all Salmonella isolates susceptibility tested (Salmonella spp.). EFSA Journal 2010; 8(4):1309 61/304 61

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SABT3. Distribution of Salmonella serovars from fattening turkey flocks susceptibility tested by MSs in the baseline survey 1 Antimicrobial agent Other S. 13,23:i:- S. Agama S. Agona S. Albany S. Anatum S. Blockley S. Braenderup S. Bredeney S. Coeln S. Corvallis S. Derby S. Eko S. Enteritidis S. Hadar S. Heidelberg S. Indiana S. Infantis S. Kedougou S. Kiambu S. Kottbus S. Mbandaka S. Montevideo S. Newport S. Paratyphi B var. J S. Saintpaul S. Senftenberg S. Stanleyville S. Stourbridge S. Tananarive S. Teddington S. Typhimurium 1Austria 4Cyprus 1 1 15 1 3 1 11 1 1 1 1 2 1 3 Czech Republic 13 2Italy 1 5 2 7 1 25 1 23 2 2 14 4 7 6 1 3 1 2Lithuania 2 1Netherlands 1 5 3 6 2 7Poland 1 1 4 2 4 11 8 7 2 4 1 39 1 16 2Slovakia 3 1Slovenia 1 2 5United Kingdom S. Zanzibar 11 1 1. For Spain, the serovar distribution of the susceptibility tested isolates is unknown. However, in this country, the five most prevalent serovars in fattening flocks in the baseline survey were S. Hadar, S. Derby, S. London, S. Typhimurium and S. Newport. 4 1 43 25 39 22 12 8 6 2 55 62 EFSA Journal 2010; 8(4):1309 62/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Resistance levels among Salmonella MSs included in the report tested between 12 and 402 Salmonella isolates. Among all Salmonella isolates, the occurrence of resistance to tetracycline (53%), ampicillin (25%), sulfonamide (36%), streptomycin (27%) and nalidixic acid (29%) was relatively higher than for the other antimicrobials tested, while resistance to chloramphenicol (13%) was rarely reported in the MS group. The only country that did not follow the general outline was Lithuania, where only streptomycin resistance was observed. Italy and Poland reported data for fattening turkeys both under the Directive 2003/99/EC and the baseline survey, therefore it was possible to compare reported resistance. The results are quite similar except that Italy reported lower sulfonamide and streptomycin resistance in the baseline survey compared to the annual zoonoses reporting (19% and 40% vs. 59% and 88% and Poland reported higher gentamicin resistance in the baseline survey (15% vs. 4%) (Tables SA8, SABT4 and Appendix 2 Table SA5). EFSA Journal 2010; 8(4):1309 63/304 63

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SABT4. Resistance (%) to selected antimicrobials among Salmonella spp. from fattening turkey flocks sampled by the baseline survey, 2006-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Country Tetracycline Chloramphenicol Florfenicol Ampicillin Sulfonamide Gentamicin Neomycin Streptomycin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Austria 53 45 53 0 53 2 52 23 53 21 53 13 53 2 53 40 53 4 Cyprus 13 54 12 0 13 46 13 0 13 8 13 62 Czech Republic 72 14 70 6 72 8 72 14 72 3 72 4 72 14 72 7 Italy 61 79 62 0 61 54 62 19 58 2 62 40 62 45 Lithuania 14 0 14 0 13 0 13 0 14 0 14 0 14 21 12 0 Netherlands 18 56 18 0 18 0 18 56 18 33 18 17 17 12 18 56 Poland 118 43 118 19 118 19 117 44 118 43 118 15 118 5 118 58 118 53 United Kingdom 402 44 402 8 402 17 402 43 402 0 402 2 402 17 402 6 Spain 227 81 227 30 227 3 227 62 Total (9 MSs) 964 53 976 13 203 12 735 25 751 36 975 4 676 3 734 27 977 29 In this table, 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. 64 EFSA Journal 2010; 8(4):1309 64/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Spatial distribution of resistance among Salmonella Figures SABT1-2 show the spatial distributions of tetracycline and nalidixic acid resistance levels in Salmonella spp. from fattening turkey flocks sampled by the baseline survey. Figure SABT1. Spatial distribution of tetracycline resistance among Salmonella spp. from fattening turkey flocks sampled by the baseline survey, 2006-2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. EFSA Journal 2010; 8(4):1309 65/304 65

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SABT2. Spatial distribution of nalidixic acid resistance among Salmonella spp. from fattening turkey flocks sampled by the baseline survey, 2006-2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 4.3 Pigs and pig meat 4.3.1 Pigs Together, 19 MSs reported quantitative antimicrobial resistance data for Salmonella spp. from pigs (Table SA1). Resistance levels among Salmonella High to very high levels of resistance in Salmonella spp. were reported for tetracycline, ampicillin and sulfonamides, in 2004 to 2007 and the resistance levels in the reporting MS group varied between 41% and 57%, 23% and 35%, 38% and 47%, respectively. There was considerable variation in the reported resistance among the MSs. Finland and Sweden did not report tetracycline resistance levels over 10% during the years, while, for example, Spain reported consistently resistance levels between 77% and 97% (Table SA9). In general, ciprofloxacin and nalidixic acid resistance among Salmonella spp. from pigs was low in all MSs with recorded levels in the reporting MS group of 1% to 3% and 1% to 7%, respectively. However, some MSs reported higher ciprofloxacin and nalidixic acid resistance levels, up to 69% in Romania (Table SA9). Denmark, Finland, Hungary, Slovenia and Sweden reported no ceftiofur resistance in 2004 to 2007 while Estonia, Ireland, Italy and Spain reported between 1% and 5% cefotaxime resistance in 2005-2007 (Table SA9). Resistance levels for S. Typhimurium from pigs are presented in Tables SA10 and MIC distributions are presented in the Salmonella Appendix (Appendix 2 Tables SA7a-c). 66 EFSA Journal 2010; 8(4):1309 66/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA9. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 17 53 21 67 59 20 17 29 21 67 59 12 17 53 21 67 59 24 Denmark 814 40 737 41 509 43 575 47 814 9 736 10 509 13 575 11 814 22 737 27 509 32 575 36 Estonia 19 16 19 16 19 11 Finland 11 0 11 0 11 0 France 175 67 175 27 12 17 175 30 Greece 16 25 28 54 16 13 28 18 16 0 28 36 Hungary 17 47 17 6 17 6 Ireland 66 62 66 45 66 55 Italy 140 64 140 7 140 22 Netherlands 75 72 144 53 75 32 144 21 75 60 144 42 Poland 88 28 88 17 88 28 Romania 60 78 14 7 10 30 Slovakia 13 31 18 44 77 22 13 31 18 0 77 3 13 31 18 28 77 9 Slovenia 22 36 22 18 22 27 Spain 30 97 172 77 199 95 30 47 172 18 199 35 30 67 Sweden 13 0 20 10 13 0 29 7 13 0 20 10 13 0 29 3 13 0 20 10 13 8 29 7 Total (16 MSs) 874 41 970 46 851 57 1,482 49 874 10 969 12 851 21 1,436 15 886 23 798 27 652 35 1,432 32 EFSA Journal 2010; 8(4):1309 67/304 67

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA9. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 17 53 21 81 59 27 Denmark 814 0 737 0 509 0 1,150 0 814 38 737 39 509 43 575 47 Estonia 19 5 19 32 Finland 12 0 11 0 France 175 65 Greece 16 31 28 64 Hungary 19 0 17 53 Ireland 66 2 66 59 Italy 140 1 140 46 Netherlands 75 0 144 0 75 65 144 58 Poland 88 26 Romania 15 93 Slovakia 13 0 18 0 77 0 13 62 18 33 77 18 Slovenia 22 0 22 27 Spain 172 2 199 0 172 45 199 53 Sweden 13 0 20 0 13 0 20 0 13 0 29 0 13 0 20 10 13 8 29 7 Total (16 MSs) 846 0 769 0 522 0 1,172 0 205 2 305 0 475 1 844 38 970 40 851 47 1,437 47 68 EFSA Journal 2010; 8(4):1309 68/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA9. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 17 0 21 0 53 0 17 6 21 5 59 2 Denmark 814 1 736 1 509 2 575 1 814 1 737 0 509 1 575 1 814 1 736 1 509 1 575 1 Estonia 12 0 19 21 19 21 Finland 11 0 11 0 France 175 0 175 0 Greece 16 0 27 0 16 6 27 0 Hungary 17 0 17 18 Ireland 66 0 66 3 66 3 Italy 140 1 140 8 140 10 Netherlands 75 0 144 1 75 1 144 3 75 0 144 3 Poland 88 5 88 39 Romania 61 10 59 69 Slovakia 13 0 18 0 77 0 13 38 18 0 77 4 13 38 18 0 77 0 Slovenia 22 14 22 14 Spain 30 0 132 2 199 2 30 7 172 8 199 5 30 3 172 6 199 4 Sweden 13 0 20 0 13 0 29 0 13 0 29 0 13 0 20 0 13 0 29 0 Total (16 MSs) 874 1 929 1 851 2 1,469 2 844 1 922 2 814 2 1,050 3 874 1 969 2 851 2 1,480 7 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. EFSA Journal 2010; 8(4):1309 69/304 69

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA10. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 10 90 18 78 21 57 10 50 18 78 21 33 10 90 18 78 21 57 Denmark 814 0 737 0 509 43 575 47 814 9 736 10 509 13 575 11 814 22 737 27 509 32 575 36 Finland 11 0 11 0 11 0 France 90 66 90 53 12 17 90 58 Germany 302 0 297 77 276 84 302 51 297 43 276 43 302 78 297 81 276 85 Ireland 41 80 41 66 41 76 Netherlands 75 72 84 67 75 32 84 30 75 60 84 55 Poland 17 82 17 65 17 76 Slovakia 11 45 11 9 11 36 Spain 30 0 40 90 35 100 30 47 40 25 35 66 30 67 Sweden 15 13 15 7 15 13 United Kingdom 98 88 96 44 97 63 Total (12 MSs) 942 9 1,100 4 934 59 1,130 60 940 14 1,099 22 934 27 1,130 27 953 28 1,060 42 899 52 1,130 53 70 EFSA Journal 2010; 8(4):1309 70/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA10. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 10 90 18 94 21 67 Denmark 814 0 737 0 509 0 1,150 0 814 38 737 39 509 43 575 47 Finland 11 0 11 0 France 90 61 Germany 302 0 297 0 272 0 302 86 297 84 276 88 Ireland 41 0 41 76 Netherlands 75 0 84 0 75 65 84 63 Poland 17 76 Slovakia 11 0 11 36 Spain 40 5 35 0 40 65 35 77 Sweden 15 0 15 13 United Kingdom 97 74 Total (12 MSs) 814 0 1,050 0 806 0 1,422 0 40 5 110 0 151 0 911 42 1,100 53 934 60 1,130 61 EFSA Journal 2010; 8(4):1309 71/304 71

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA10. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Czech Republic 10 0 18 0 21 0 10 10 18 6 21 5 Denmark 814 1 736 1 509 2 575 1 814 1 737 0 509 1 575 1 814 1 736 1 509 1 575 1 Finland 11 0 11 0 France 90 0 90 0 Germany 302 6 297 6 276 4 302 5 297 5 276 6 302 4 297 4 276 3 Ireland 41 0 41 5 41 5 Netherlands 75 0 84 0 75 1 84 4 75 0 84 4 Poland 17 0 17 59 Slovakia 11 0 11 0 11 0 Spain 30 0 40 8 35 3 30 7 40 8 35 3 30 3 40 8 35 3 Sweden 15 0 15 0 15 0 United Kingdom 87 7 97 2 Total (12 MSs) 931 2 1,099 3 934 3 1,130 2 844 1 1,079 2 916 3 1,002 3 941 1 1,099 2 934 2 1,130 3 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. 72 EFSA Journal 2010; 8(4):1309 72/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Temporal trends in resistance among Salmonella Figures SA15-21 demonstrate the large variation in the occurrence of resistance among Salmonella spp. from pigs observed between 2004 and 2007. Finland and Sweden had a consistently low occurrence of resistance to all antimicrobials tested and both countries reported zero percent resistance to nalidixic acid. In general, some decreasing trends over time in resistance among Salmonella spp. from pigs were mainly observed in reporting MSs. Figure SA15. Trends in tetracycline resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Greece Slovakia Spain Sweden Netherlands Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA16. Trends in chloramphenicol resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Greece Slovakia Spain Sweden Netherlands Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. EFSA Journal 2010; 8(4):1309 73/304 73

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA17. Trends in ampicillin resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark France Greece Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA18. Trends in sulfonamide resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Greece Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. 74 EFSA Journal 2010; 8(4):1309 74/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA19. Trends in ciprofloxacin resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Denmark 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. Figure SA20. Trends in nalidixic acid resistance in Salmonella spp. from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Greece 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. EFSA Journal 2010; 8(4):1309 75/304 75

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Spatial distribution of resistance among Salmonella The spatial distribution of tetracycline, ampicillin and nalidixic acid resistance among Salmonella spp. isolated from pigs in 2007 are shown in Figures SA21-23. The figures underline the large differences in resistance levels observed between the countries. The highest tetracycline resistance levels were reported by several southern and central European countries and Romania and Ireland (Figure SA21). For ampicillin resistance, Ireland and the Netherlands reported the highest resistance levels (Figure SA22). Eight countries reported nalidixic acid resistance levels below 4%. The occurrence of nalidixic acid resistance was highest in Romania, Poland and Estonia (Figure SA23). Figure SA21. Spatial distribution of tetracycline resistance among Salmonella spp. from pigs in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Luxembourg, 2006 data were used. 76 EFSA Journal 2010; 8(4):1309 76/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA22. Spatial distribution of ampicillin resistance among Salmonella spp. from pigs in countries reporting quantitative data in 2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. EFSA Journal 2010; 8(4):1309 77/304 77

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA23. Spatial distribution of nalidixic acid resistance among Salmonella spp. from pigs in countries reporting quantitative data in 2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 78 EFSA Journal 2010; 8(4):1309 78/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. 4.3.2 Meat from pigs Together 12 MSs reported quantitative data for Salmonella spp. from pig meat (Table SA1). Resistance levels among Salmonella Ampicillin, sulfonamide and tetracycline were the antimicrobials where resistance was most commonly observed among Salmonella spp. from pig meat. Table SA11 show the resistance levels in the reporting MS group, ranging between 27% and 75% for tetracycline, 34% and 54% for ampicillin and 37% and 61% for sulfonamide. The resistance level to chloramphenicol ranged between 13% and 38% from 2004 to 2007. In general, in the reporting period, a relatively low occurrence of ciprofloxacin and nalidixic acid resistance was observed in all reporting MSs and the resistance level in the reporting MS group ranged between 0% and 4%, and 0% and 3%, respectively. The highest nalidixic acid resistance was observed in Slovenia with 17% of resistant isolates (Table SA11). No resistance against ceftiofur, cefotaxime and ceftazidime was found in Salmonella isolates from pig meat in the reporting MSs (Table SA11, Appendix Table SA8). The levels of resistance among S. Typhimurium isolates in the reporting MS group varied between 53% and 76% for tetracycline, 42% and 62% for ampicillin and 49% and 68% for sulfonamide. Chloramphenicol resistance ranged from 20% to 38% in 2004 to 2007. Low resistance was reported for gentamicin (0%-2%), ciprofloxacin (0%-4%) and nalidixic acid (1%-4%) for S. Typhimurium (Table SA12). EFSA Journal 2010; 8(4):1309 79/304 79

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA11. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from meat from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 188 39 146 28 21 38 727 49 188 13 146 19 21 5 727 17 188 32 145 44 21 19 727 45 Denmark 13 92 72 19 71 38 13 15 94 5 71 6 13 54 94 21 71 35 France 54 83 58 88 225 65 54 54 58 50 225 20 54 63 58 66 225 27 Italy 231 74 231 10 231 40 Romania 52 63 52 13 44 30 Slovenia 24 42 24 8 24 25 Total (6 MSs) 255 51 242 27 79 75 1,306 56 255 22 264 13 79 38 1,306 16 255 40 263 34 79 54 1,298 40 Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 188 51 146 38 21 24 727 48 Denmark 13 0 94 0 71 0 94 36 71 39 France 54 67 58 74 225 60 Italy 231 0 231 65 Romania 36 33 Slovenia 24 38 Total (6 MSs) 13 0 94 0 0 0 71 0 231 0 242 55 264 37 79 61 1,290 52 80 EFSA Journal 2010; 8(4):1309 80/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA11. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from meat from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 137 0 188 3 146 3 21 0 727 4 188 3 146 1 21 0 727 2 Denmark 13 8 94 0 71 3 13 0 94 1 71 0 13 0 94 2 71 0 France 54 0 58 2 225 0 54 6 58 0 225 3 Italy 231 3 231 7 231 6 Romania 52 4 52 2 Slovenia 24 8 24 17 Total (6 MSs) 67 2 118 2 58 2 716 2 201 3 240 2 21 0 1,029 4 255 3 264 3 79 0 1,306 3 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. EFSA Journal 2010; 8(4):1309 81/304 81

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA12. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from meat from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 60 53 62 27 178 65 60 18 62 23 178 27 60 43 62 48 178 63 Denmark 13 92 72 19 71 38 13 15 94 5 71 6 13 54 94 21 71 35 France 54 83 58 88 91 89 54 54 58 50 91 51 54 63 58 66 91 66 Germany 281 67 98 68 281 25 98 32 281 47 98 59 Italy 29 83 29 28 29 76 Total (5 MSs) 127 70 415 53 156 76 369 67 127 33 437 20 156 38 369 29 127 53 437 42 156 62 369 59 Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 60 53 62 37 178 63 Denmark 13 0 94 0 71 0 94 36 71 39 France 54 67 58 74 91 70 Germany 281 0 98 0 281 57 98 64 Italy 29 0 29 83 Total (5 MSs) 13 0 375 0 98 0 71 0 29 0 114 60 437 49 156 68 369 62 82 EFSA Journal 2010; 8(4):1309 82/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA12. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium isolates from meat from pigs, 2004-2007, using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium 60 0 62 2 178 3 60 0 62 2 178 1 Denmark 13 8 94 0 71 3 13 0 94 1 71 0 13 0 94 2 71 0 France 54 0 58 2 91 0 54 6 58 0 91 3 Germany 281 0 98 2 281 5 98 2 281 5 98 1 Italy 29 7 29 3 29 3 Total (5 MSs) 67 1 375 0 156 2 191 2 73 0 437 4 98 2 278 2 127 2 437 4 156 1 369 2 EFSA Journal 2010; 8(4):1309 83/304 83

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.3.3 Resistance data from the baseline survey on the prevalence of Salmonella in slaughter pigs in the EU An EU-wide baseline survey was carried out to determine, at the point of slaughter, the prevalence of pigs infected with Salmonella in 2006 to 2007. The pigs were randomly selected from those slaughterhouses that together accounted for 80% of pigs slaughtered within each MS. All participating MSs and Norway sampled ileo-caecal lymph nodes from the selected slaughtered pigs and 14 MSs also collected carcass swabs to determine the prevalence of external contamination with Salmonella. MSs were also invited to submit antimicrobial resistance data if the Salmonella isolates were susceptibility tested. However, this was not a compulsory requirement of the survey and was not addressed by the baseline report. Together, 14 MSs and one non-ms provided data on antimicrobial resistance. About 4% of the antimicrobial resistance tests were reported with an inhibition zone equal to zero. However, since zero is not a valid result when determining inhibition zones and zero was interpreted both as resistant (84%) and as susceptible (16%) to a given antimicrobial, these results were excluded from this report. Table SABS1 shows the countries reporting MIC values and inhibition zones on Salmonella from slaughter pigs. Table SABS1. Overview of countries reporting MIC distributions and inhibition zones on Salmonella in slaughter pigs, 2006-2007 Method Total no of countries reporting Countries Dilution 7 MSs: BE, DK, ES, NL, PL, SE Non-MS: NO Diffusion 9 MSs: BE, BG, CY, CZ, EE, IT, LT, LV, UK 84 EFSA Journal 2010; 8(4):1309 84/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SABS2. Antimicrobials selected for susceptibility testing of Salmonella isolates by MSs and non- MSs in the slaughter pig baseline survey Antimicrobial agent Belgium Bulgaria Cyprus Czech Republic Denmark Estonia Italy Latvia Lithuania Netherlands Poland Spain Sweden United Kingdom Norway Amikacin Amoxicillin / Ampicillin Amoxicillin / Clavulanic acid Ampicillin Apramycin Cefoperazone Cefotaxime Cefpodoxime Ceftazidime Ceftiofur Ceftriaxone Cefuroxime Cephalotin Chloramphenicol Ciprofloxacin Colistin Enrofloxacin Florfenicol Flumiquin Furazolidone Gentamicin Kanamycin Nalidixic acid Neomycin Spectinomycin Streptomycin Sulfonamides Sulfonamide / Trimethoprim Tetracycline Trimethoprim EFSA Journal 2010; 8(4):1309 85/304 85

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA The following antimicrobials are included in the prevalence tables: tetracycline, chloramphenicol, florfenicol, ampicillin, sulfonamide, gentamicin, neomycin, streptomycin and nalidixic acid. When more than one isolate per pig was susceptibility tested, only the first isolate was considered for the resistance prevalence estimate calculation, thus avoiding clustering of data at individual pig level. As the number of isolates susceptibility tested by MSs was not necessarily proportional to the total number of isolates collected in the baseline survey, data from countries who susceptibility tested less than 10 isolates were excluded from this description. In addition, countries who reported qualitative data only (i.e. as resistant or susceptible without reporting the MIC or inhibition zone diameter) were also excluded from this description. This meant that data from nine MSs were analysed. Salmonella Typhimurium, S. Enteritidis and S. Derby were the most commonly reported serovars among participating countries. The same serovars were also most commonly susceptibility tested, as shown in Table SABS3. 86 EFSA Journal 2010; 8(4):1309 86/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SABS3. Distribution of Salmonella serovars on isolates susceptibility tested by MSs and non-mss in the slaughter pig baseline survey 1 Antimicrobial agent O6,7:Z29 Other S. Muenchen S. 3,1:-:1,7 S. 4:-:1,2 S. 6,7:-:I,w S. Agona S. Amersfoort S. Anatum S. Bareilly S. Bovismorbificans S. Brandenburg S. Bredeney S. Chartres S. Choleraesuis S. Coeln S. Derby S. Dublin S. Ebeko S. Enteritidis S. Essen S. Freetown S. Goldcoast S. Hadar S. Infantis S. Isangi S. Kottbus S. Livingstone S. London S. Mbandaka S. Montevideo S. Newport S. Panama S. Rissen S. Senegal S. Senftenberg S.Thompson S. Typhimurium S. Virchow Untypeable 1Belgium 1 1 5 1 1 1 10 1 2 1 1 2 1 2 1 1 1 47 1 1 1Cyprus 20 4 2 8 2 1 4 4 1 6 Czech Republic 1 5 7 10 1 1 1 12 Denmark 50 Estonia 5 1 2Latvia 1 11 1 1 9 1 1 Lithuania 1 4 2 7 4Netherlands 1 3 6 1 1 1 3 2 43 1Poland 2 2 3 9 29 1 4 3 1 3 3 1 17 2 Sweden 2 3 Norway 1 1. The serovar distribution of the susceptibility tested isolates is unknown for Spain. However, in this country, the five most prevalent serovars in slaughter pigs in the baseline survey were S. Typhimurium, S. Rissen, S. 4,[5],12:i:-, S. Derby and S. Anatum. EFSA Journal 2010; 8(4):1309 87/304 87

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Resistance levels among Salmonella Table SABS4 shows the occurrence of resistance to selected antimicrobials among all Salmonella isolates susceptibility tested (Salmonella spp.), while Table SABS5 shows the occurrence of resistance among S. Typhimurium isolates from the baseline survey. Nine MSs tested between 14 and 167 Salmonella isolates. Among all Salmonella isolates, in the reporting MS group, the calculated resistance levels for tetracycline (40%), ampicillin (31%), sulfonamide (38%) and streptomycin (25%) were relatively higher than for other antimicrobials tested, while gentamicin (3%) and neomycin (3%) resistance was rarely reported. The only exception was Latvia that only reported 4% resistance to gentamicin among Salmonella spp. while resistance to the other antimicrobials was not observed. Six MSs reported antimicrobial resistance of S. Typhimurium from the baseline survey, and resistance to tetracycline (58%), ampicillin (49%), sulfonamide (51%) and streptomycin (41%) were reported. Overall, the Czech Republic, Denmark, the Netherlands and Poland reported similar resistance levels for Salmonella spp. and S. Typhimurium in the baseline survey and in the data that are reported annually under Directive 2003/99/EC. 88 EFSA Journal 2010; 8(4):1309 88/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SABS4. Resistance (%) to selected antimicrobials among Salmonella spp. from slaughter pigs sampled by the baseline survey, 2006-2007, using harmonised cut-off values in countries reporting quantitative data. Country Tetracycline Chloramphenicol Florfenicol Ampicillin Sulfonamide Gentamicin Neomycin Streptomycin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Belgium 83 40 84 12 82 6 79 38 83 47 22 0 84 27 85 1 Cyprus 52 17 15 7 28 32 53 0 53 6 19 0 Czech Republic 38 21 38 13 38 13 38 24 38 26 38 0 37 0 38 18 38 3 Denmark 50 40 50 6 50 6 49 31 50 28 50 0 50 2 50 32 50 2 Lithuania 14 43 14 0 14 0 14 43 14 43 14 21 14 14 14 43 14 7 Latvia 25 0 26 0 27 0 27 0 20 0 25 4 26 0 27 0 Netherlands 65 46 65 20 65 17 65 37 65 49 65 0 65 35 65 8 Poland 81 26 82 18 82 13 82 26 82 24 82 1 82 4 81 30 82 38 Spain 167 57 167 22 83 35 83 54 167 7 167 17 Total (9 MSs) 575 40 541 15 358 10 437 31 463 38 516 3 183 3 411 25 547 13 Table SABS5. Resistance (%) to selected antimicrobials among Salmonella Typhimurium from slaughter pigs sampled by the baseline survey, 2006-2007, using harmonised cut-off values in countries reporting quantitative data. Country Tetracycline Chloramphenicol Florfenicol Ampicillin Sulfonamide Gentamicin Neomycin Streptomycin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Belgium 47 60 47 19 66 11 46 61 48 63 11 0 47 40 49 2 Czech Republic 12 67 12 42 12 42 12 58 12 67 12 0 12 0 12 33 12 8 Denmark 50 40 50 6 50 6 49 31 50 28 50 0 50 2 50 32 50 2 Netherlands 43 53 43 23 43 21 43 44 43 51 43 0 43 42 43 12 Poland 17 82 17 65 17 59 17 76 17 76 17 0 17 12 17 71 17 59 Spain 19 84 19 79 19 11 19 11 Total (6 MSs) 188 58 188 28 188 18 167 49 170 51 152 1 79 4 169 41 190 11 In these tables, 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. EFSA Journal 2010; 8(4):1309 89/304 89

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Spatial distribution of resistance among Salmonella The spatial distributions of tetracycline and nalidixic acid resistance levels in Salmonella spp. from slaughter pigs sampled by the baseline survey are shown in Figures SABS1-2. Figure SABS1. Spatial distribution of tetracycline resistance among Salmonella spp. from slaughter pigs sampled by the baseline survey, 2006-2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 90 EFSA Journal 2010; 8(4):1309 90/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SABS2. Spatial distribution of nalidixic acid resistance among Salmonella spp. from slaughter pigs sampled by the baseline survey, 2006-2007 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. EFSA Journal 2010; 8(4):1309 91/304 91

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.4 Cattle and bovine meat 4.4.1 Cattle (bovine animals) In this report, cattle covers calves, dairy and beef cows and heifers. Together, 17 MSs reported quantitative data for Salmonella spp. from cattle (Table SA1). Resistance levels among Salmonella In 2004 to 2007, the resistance levels in Salmonella spp. in the reporting MS group varied between 24% to 39% for tetracycline, 10% to 28% for chloramphenicol, 18% to 40% for ampicillin and 19% to 38% for sulfonamide. However, large variations were observed between the different MSs with up to 70% ampicillin and 75% tetracycline and sulfonamide resistance in Italy in 2007. While, in 2007, Estonia and Sweden observed between 0% and 5% resistance to tetracycline, between 0% and 15% resistance to ampicillin, no resistance to chloramphenicol and between 0% and 15% resistance to sulfonamide (Tables SA13). Resistance levels for ciprofloxacin and nalidixic acid in the reporting MS group ranged between 0% and 23%, and 3% and 13%, respectively, and did not exceed 15% in most MSs. However, in Slovakia 50% of the Salmonella spp. isolates were resistant to ciprofloxacin and nalidixic acid in 2005 and in the Czech Republic a resistance level of 20% was detected for nalidixic acid in 2006 (Table SA13). Among the seven MS reporting quantitative data for ceftiofur and cefotaxime, no resistance was detected (Table SA13 and Appendix Tables SA10a and SA10b). The reported MSs group resistance levels in S. Typhimurium varied between 54% and 75% for tetracycline, 37% and 67% for chloramphenicol, 52% and 77% for ampicillin and 3% and 76% for sulfonamide in 2004 to 2007. Over the same period, low resistance levels were reported in the MS group for ciprofloxacin (1%-6%) and for nalidixic acid (2%-4%) (Table SA14). 92 EFSA Journal 2010; 8(4):1309 92/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA13. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Czech Republic 11 45 10 40 11 36 10 20 11 45 10 20 Denmark 28 21 17 29 26 69 13 62 28 14 17 24 26 19 13 15 28 32 17 35 26 69 13 62 Estonia 11 18 18 33 14 14 10 0 11 0 18 0 14 0 10 0 11 0 18 0 14 14 10 0 Finland 15 0 18 39 15 0 18 6 15 0 18 6 France 39 46 43 40 72 17 27 59 43 37 72 15 21 0 43 40 72 15 Italy 20 75 20 40 20 70 Netherlands 40 40 78 8 40 23 78 6 40 45 78 9 Romania 10 10 Slovakia 14 50 17 35 14 50 17 12 14 57 13 0 Spain 29 41 30 0 Sweden 20 40 26 23 21 14 20 5 20 40 26 23 21 5 20 0 20 40 26 23 21 19 20 15 Total (11 MSs) 113 30 86 33 154 39 287 24 101 28 86 24 154 21 278 10 95 18 86 29 154 40 244 18 EFSA Journal 2010; 8(4):1309 93/304 93

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA13. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Czech Republic 11 45 10 20 Denmark 28 0 17 0 26 0 26 0 19 32 17 35 26 73 13 69 Estonia 11 18 18 33 14 14 10 0 Finland 15 0 18 0 15 0 18 33 France 21 0 43 40 72 17 Italy 20 0 20 75 Netherlands 40 0 78 0 40 35 78 12 Romania Slovakia 14 0 17 0 14 50 17 12 Spain 30 0 30 30 Sweden 20 0 26 0 21 0 26 0 21 0 20 0 20 40 23 13 21 19 20 15 Total (11 MSs) 63 0 43 0 47 0 26 0 40 0 61 0 183 0 86 19 83 32 154 38 278 24 94 EFSA Journal 2010; 8(4):1309 94/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA13. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella spp. isolates from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Czech Republic 11 0 10 0 11 18 10 20 Denmark 28 0 17 0 26 0 13 0 28 0 17 0 26 0 13 0 28 0 17 0 26 0 13 0 Estonia 11 0 18 0 14 0 10 0 11 0 17 12 14 0 Finland 15 0 18 0 18 0 15 0 18 0 France 39 0 43 0 72 0 39 10 43 12 72 1 Italy 20 10 20 10 20 10 Netherlands 40 0 78 1 40 3 78 3 40 3 78 3 Romania 11 0 11 18 Slovakia 14 0 17 0 14 50 17 6 14 50 17 6 Spain 30 0 30 0 30 0 Sweden 20 0 26 0 21 0 20 0 21 0 20 0 20 0 26 0 21 0 20 0 Total (11 MSs) 113 0 86 0 154 0 289 1 28 0 31 23 87 1 196 3 113 3 85 13 154 5 279 3 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. EFSA Journal 2010; 8(4):1309 95/304 95

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA14. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur and cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Denmark 28 21 17 29 26 69 13 62 28 14 17 24 26 19 13 15 28 32 17 35 26 69 13 62 Finland 12 0 14 43 12 0 14 0 12 0 14 0 France 27 67 29 59 28 36 27 59 29 55 28 32 29 59 28 32 Germany 188 89 153 79 163 69 112 46 188 73 153 73 163 43 112 34 188 88 153 80 163 62 112 51 Netherlands 40 40 40 23 40 45 United Kingdom 71 73 173 80 87 69 71 63 173 75 85 53 71 75 173 78 87 66 Total (6 MSs) 255 75 241 74 431 70 254 54 255 62 241 67 431 53 252 37 228 77 241 76 431 67 254 52 Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Denmark 28 0 17 0 26 0 26 0 19 32 17 35 26 73 13 69 Finland 12 0 14 0 12 0 14 43 France 29 59 28 36 Germany 188 0 153 0 163 1 107 0 188 0 153 80 163 73 112 55 Netherlands 40 0 40 35 United Kingdom 71 75 173 80 87 78 Total (6 MSs) 228 0 170 0 189 1 133 0 40 0 14 0 219 3 241 76 431 71 254 61 96 EFSA Journal 2010; 8(4):1309 96/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SA14. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur and cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among Salmonella Typhimurium from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Denmark 28 0 17 0 26 0 13 0 28 0 17 0 26 0 13 0 28 0 17 0 26 0 13 0 Finland 12 8 14 0 14 0 12 0 14 0 France 27 0 29 0 28 0 27 15 29 17 28 0 Germany 188 2 153 2 163 1 112 2 188 1 152 3 163 2 112 7 188 1 153 3 163 1 112 6 Netherlands 40 0 40 3 40 3 United Kingdom 71 0 173 0 87 0 71 7 173 0 87 2 Total (6 MSs) 255 2 241 1 431 0 254 1 216 1 169 2 229 2 139 6 255 2 241 4 431 2 254 4 EFSA Journal 2010; 8(4):1309 97/304 97

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Temporal trends in resistance among Salmonella Figures SA24-28 display trends in resistance to tetracycline, ampicillin, chloramphenicol, florfenicol, sulfonamide and nalidixic acid among Salmonella isolates from cattle. The figures show that, although there were large variations in ampicillin, chloramphenicol, florfenicol, sulfonamide and tetracycline resistance between countries, similar decreasing resistance trends over time were observed in several reporting countries. This might indicate that the occurrence of penta-resistant S. Typhimurium DT104 has a large influence on the occurrence of resistance in Salmonella spp. in cattle and that the reported prevalence of penta-resistant S. Typhimurium DT 104 in cattle is decreasing. Figure SA24. Trends in tetracycline resistance in Salmonella spp. from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Estonia Finland France Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA25. Trends in chloramphenicol resistance in Salmonella spp. from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Estonia Finland France Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. 98 EFSA Journal 2010; 8(4):1309 98/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA26. Trends in ampicillin resistance in Salmonella spp. from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Estonia Finland France Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. Figure SA27. Trends in sulfonamide resistance in Salmonella spp. from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic France Denmark Estonia Finland Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. EFSA Journal 2010; 8(4):1309 99/304 99

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA28. Trends in nalidixic acid resistance in Salmonella spp. from cattle in the reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark Estonia Finland France Netherlands Slovakia Sweden Note: In this figure, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and year. 100 EFSA Journal 2010; 8(4):1309 100/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Spatial distribution of resistance among Salmonella Figures SA29-31 show the spatial distribution of tetracycline, ampicillin and nalidixic acid resistance among Salmonella spp. from cattle in 2007. The figures underline the large variation in tetracycline and ampicillin resistance observed between reporting countries. The figures also indicate that there was no clear spatial pattern in tetracycline, ampicillin and nalidixic acid resistance among reporting countries. Resistance to nalidixic acid was 20% or below for all countries, with the Nordic MSs, Estonia and Spain reporting zero percent resistance to this antimicrobial. Figure SA29. Spatial distribution of tetracycline resistance among Salmonella spp. from cattle in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, Czech Republic and Greece, 2006 data were used. EFSA Journal 2010; 8(4):1309 101/304 101

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA30. Spatial distribution of ampicillin resistance among Salmonella spp. from cattle in countries reporting quantitative data in 2007 1 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, the Czech Republic and Greece, 2006 data were used. 102 EFSA Journal 2010; 8(4):1309 102/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA31. Spatial distribution of nalidixic acid resistance among Salmonella spp. from cattle in countries reporting quantitative data in 2007 1, 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. Antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country. 1. For Austria, the Czech Republic, Estonia and Greece, 2006 data were used. 4.4.2 Meat from bovine animals Together, 10 MSs provided quantitative data on Salmonella spp. in bovine meat (Table SA1). Resistance levels among Salmonella The occurrence of resistance in Salmonella spp. from meat from bovine animals is provided in Table SA15. Although several MSs reported quantitative data on Salmonella spp. from bovine meat, often less than 10 isolates were available per year. Highest resistance levels in the MS group include the occurrence of resistance to tetracycline (67%), ampicillin (61%) and sulfonamide (67%) in 2006 while in 2007 low resistance levels were reported for ceftiofur and cefotaxime (both 0%), ciprofloxacin (0%) and nalidixic acid (2%). EFSA Journal 2010; 8(4):1309 103/304 103

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA15. Resistance (%) to selected antimicrobials among Salmonella spp. isolates from meat from bovine animals, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Country 2006 2007 2006 2007 2006 2007 2006 2007 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Belgium 22 23 22 5 22 14 France 18 67 19 79 18 44 19 68 18 61 19 79 Italy 19 53 19 0 19 26 19 0 Total (3 MSs) 18 67 60 50 18 44 60 23 18 61 60 38 0 0 0 0 19 0 Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2006 2007 2006 2007 2006 2007 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Belgium 22 23 22 0 22 0 France 18 67 19 79 18 11 19 0 18 0 19 5 Italy 19 37 19 0 19 0 19 0 Total (3 MSs) 18 67 60 45 18 11 38 0 0 0 41 0 18 0 60 2 In this table, 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. 104 EFSA Journal 2010; 8(4):1309 104/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. 4.5 Comparison of antimicrobial resistance among Salmonella isolates from food and animals within and between MSs Comparison of antimicrobial resistance among Salmonella from food and animals was possible for Salmonella spp. from Gallus gallus and broiler meat in 2007 and Salmonella spp. from pigs and meat from pigs in 2007 (Tables SA16 and SA17). When comparing antimicrobial resistance data from animals and food there are a few things that can have a large impact on comparability. Previous data have shown that the occurrence of resistance varies between countries. Samples from animals are often collected from domestic animals. However, large proportions of the food consumed might be imported, which can result in large differences between the reported occurrence of resistance in isolates from food and animals. In addition, the reported sampling categories are not necessarily comparable e.g. Gallus gallus represent both laying hen and broiler production and both breeding and production animals are included, while meat from broilers is assumed to originate mainly from broilers. Therefore, antimicrobial resistance in isolates from Gallus gallus and broiler meat are not necessarily comparable. The occurrence of resistance in Salmonella spp. from Gallus gallus in quantitative data was relatively low, while a larger variation in the reported occurrence of resistance was observed in isolates from meat from broilers (Tables SA4 and SA7). In the Czech Republic, tetracycline (p<0.01) and sulfonamide (p=0.04) resistance were significantly higher in isolates from broiler meat compared to Gallus gallus. In France, the occurrence of resistance in isolates from broiler meat were significantly higher for most antimicrobials, with p-values lower than 0.01 and the only exception was gentamicin where no significant differences were found. In Slovakia, only ciprofloxacin resistance (p=0.04) and nalidixic acid resistance (p=0.04) were significantly higher in isolates from meat from broilers. Differences between sampling origins may explain the differences in antimicrobial resistance observed between isolates from Gallus gallus and meat from broilers. The broiler meat sampled in the different countries might be domestic products or imported products. As the occurrence of resistance varies between countries, the proportion of isolates that originates from imported products might have a large influence on the reported occurrence of resistance. EFSA Journal 2010; 8(4):1309 105/304 105

4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA16. Comparison of resistance (%) among Salmonella spp. from Gallus gallus and meat from broilers (quantitative data) in 2007 1 Compound Czech Republic France Germany Slovakia Gallus gallus Meat from broilers Gallus gallus Meat from broilers Gallus gallus Meat from broilers Gallus gallus Meat from broilers Tetracycline 0 8 4 36 5 21 10 27 Chloramphenicol 0 0 2 14 1 4 0 0 Florfenicol 0 0 1 1 0 0 Ampicillin 0 0 4 21 2 24 1 9 Ceftiofur 0 1 Sulfonamide 1 8 3 40 6 23 10 27 Apramycin Gentamicin 0 0 0 0 3 1 0 0 Neomycin 0 10 Spectinomycin Streptomycin 1 4 3 43 7 26 7 27 Ciprofloxacin 3 4 11 32 12 36 Nalidixic acid 3 4 1 21 11 32 12 36 Number of isolates 234 24 132 28 124 221 137 11 1. In this table, antimicrobial resistance in all reported Salmonella isolates were collapsed into Salmonella spp. for each country and origin. 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. 106 EFSA Journal 2010; 8(4):1309 106/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. In general, the occurrence of resistance in Salmonella spp. from pigs and pork were higher compared to isolates from Gallus gallus and broiler meat, except nalidixic acid and ciprofloxacin resistance. No significant differences were observed between the occurrence of resistance in Salmonella spp. from pigs and pig meat in Denmark and in France in quantitative data, where only nalidixic acid resistance (p=0.02) was significantly higher in isolates from pork compared to pigs. In Denmark, only isolates from domestically produced pork were included. In Italy, resistance to tetracycline (p=0.03), ampicillin (p<0.01) and sulfonamide (p<0.01) were significantly higher in isolates from pig meat compared to isolates from pigs. In Italy the sample sizes from pork were rather large, however, the proportion of imported pig meat in the sample sizes is not known. Table SA17. Comparison of resistance (%) among Salmonella spp. from pigs and pig meat (quantitative data) in 2007 Compound Denmark France Italy Pigs Pork Pigs Pork Pigs Pork Tetracycline 47 38 67 65 64 74 Chloramphenicol 11 6 27 20 7 10 Florfenicol 7 4 5 3 Ampicillin 36 35 30 27 22 40 Ceftiofur 0 0 Cefpodoxime 0 0 Sulfonamide 47 39 65 60 46 65 Apramycin 1 1 Gentamicin 1 3 0 0 1 3 Neomycin 8 10 Spectinomycin 17 13 Streptomycin 44 41 62 58 44 54 Ciprofloxacin 1 0 8 7 Nalidixic acid 1 0 0 3 10 6 Number of isolates 575 71 175 225 140 231 EFSA Journal 2010; 8(4):1309 107/304 107

108 EFSA Journal 2010; 8(4):1309 108/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5 Antimicrobial resistance in Campylobacter - quantitative data 5 109

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA The vast majority of antimicrobial susceptibility data reported on C. jejuni and C. coli were quantitative data, most of them being MIC values. Spain, however, although reporting mostly MIC values, tested also a few antimicrobials (colistin, kanamycin, streptomycin, sulfonamide, and tylosin) using disk diffusion method. These latter data have not been included in the report. Table CA1 displays countries reporting Campylobacter MIC values between 2004 and 2007. As all qualitative data were also reported as quantitative data (the only exception being Hungary that reported qualitative data only for Campylobacter in broiler meat) and furthermore, the additional qualitative Campylobacter data submitted were scarce, no qualitative data have been presented for Campylobacter in this report. The different antimicrobials selected by MSs and non-mss for susceptibility testing of tested C. jejuni and C. coli isolates are set out in Table MM4. The report analysis refers to 52,697 Campylobacter isolates (Table MM1). Table CA1. Overview of countries reporting MIC distributions on Campylobacter jejuni and Campylobacter coli from animals and food, 2004-2007 Bacterial species Origin Total number of MSs reporting Countries C. jejuni C. coli Meat from broilers 6 MSs: AT, BE, DE, DK, EE, FR Non-MSs: CH, NO Meat from pigs 1 MS: BE Gallus gallus 11 MSs: AT, CZ, DE, DK, ES, FI, FR, IT, NL, SI, SE Non-MSs: CH, NO Turkeys 1 MS: IT Non-MS: NO Meat from turkeys 1 MS: EE Pigs 2 MSs: AT, IT Cattle 6 MSs: AT, DK, ES, IT, NL, SE Non-MS: CH MSs: AT, BE, DK, EE, FR Meat from broilers 5 Non-MS: CH Meat from pigs 1 MS: BE MSs: AT, DE, ES, FR, IT, NL, SI Gallus gallus 7 Non-MS: CH Turkeys 1 MS: IT MSs: AT, DK, DE, ES, FR, IT, NL, SE Pigs 8 Non-MS: CH MSs: AT, DK, ES, IT, NL Cattle 5 Non-MS: CH Data on antimicrobial resistance to tetracycline, erythromycin, gentamicin, ciprofloxacin, and nalidixic acid are presented hereafter since either of these substances are of critical importance in human medicine or have shown interesting trends in MIC tables. Tables were generated where more than three countries reported quantitative data per Campylobacter species and sampling origin. Only data where 10 or more isolates were available per country, food/animal category and year are included in this report. Where data were available, the spatial distributions of tetracycline, erythromycin and ciprofloxacin resistance levels were plotted. Where 2007 data were not available for MSs, 2006 resistance levels were used. MIC distributions and resistance levels to tetracycline, chloramphenicol, erythromycin, gentamicin, streptomycin, ciprofloxacin, and nalidixic acid among the C. jejuni and C. coli isolates susceptibility tested over the period 2004 to 2007, are set out in Appendix 3 tables. 110 EFSA Journal 2010; 8(4):1309 110/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. 5.1 Poultry (Gallus gallus) and broiler meat 5.1.1 Fowl (Gallus gallus) In this report fowl (Gallus gallus) includes breeders, laying hens and broilers of Gallus gallus. Resistance levels among C. jejuni Together, 11 MSs and two non-mss provided quantitative data on C. jejuni isolates from Gallus gallus (Table CA2). For tetracycline, resistance levels ranged from 6% to 35% in the reporting MS group during 2004-2007. Resistance levels reported for ciprofloxacin and nalidixic acid at reporting MS level varied between 33% to 43% and 4% to 49%, respectively, during 2004 to 2007; the highest resistance in the tested isolates was reported in 2007. In the Nordic countries, either 0% or less than 10% ciprofloxacin and nalidixic acid resistance were reported, whereas the reported ciprofloxacin and nalidixic acid resistance levels ranged from 50% up to almost 100% in certain other reporting MSs. In Spain in particular, ciprofloxacin and nalidixic acid resistance reached levels close to 100% among tested isolates over the years of reporting. Most countries reported either 0% or less than 10% erythromycin and gentamicin resistance among tested C. jejuni isolates, although a few countries observed erythromycin and gentamicin resistance above 10% but for a single year only. Resistance levels in the reporting MSs group varied between 0% and 4% for erythromycin and between 0% and 5% for gentamicin. Resistance levels among C. coli Overall seven MSs and one non-ms provided quantitative data on C. coli isolates from Gallus gallus (Table CA3). For tetracycline, resistance levels ranged from 73% to 77% in the reporting MS group during 2004-2007, while resistance levels to ciprofloxacin and nalidixic acid varied between 55% and 64% and 39% and 68%, respectively. Resistance levels in the reporting MS group varied between 13% and 21% for erythromycin and between 1% and 4% for gentamicin. In the reporting MS group, the reported occurrence of resistance to tested antimicrobials among the C. coli isolates was higher compared to C. jejuni, except for gentamicin. EFSA Journal 2010; 8(4):1309 111/304 111

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA2. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from Gallus gallus, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 26 27 26 0 26 0 Czech Republic 50 12 53 9 50 4 53 6 50 8 53 0 Denmark 77 5 76 5 75 7 94 10 77 1 76 0 75 0 94 1 77 0 76 0 75 0 94 0 Finland 69 10 90 0 66 3 94 3 69 0 90 0 66 0 94 0 69 0 90 0 66 0 94 5 France 32 44 49 57 56 50 32 0 49 0 56 0 32 9 49 0 56 0 Germany 49 61 95 43 100 54 49 2 95 2 100 13 49 8 95 4 100 7 Italy 19 21 108 56 48 77 36 0 108 11 48 4 36 0 108 2 48 0 Netherlands 78 42 16 50 45 51 78 0 16 0 45 2 78 0 16 0 45 0 Slovenia 71 37 71 3 71 20 Spain 16 69 17 82 19 89 16 6 17 12 19 5 16 6 17 6 19 11 Sweden 94 3 94 0 94 1 Total (11 MSs) 240 6 360 27 547 35 535 34 240 0 377 1 547 4 535 4 240 0 377 2 547 5 535 3 Norway 75 1 69 0 108 0 99 1 75 0 69 0 108 0 99 0 75 0 69 1 108 0 99 0 Switzerland 77 23 122 20 77 1 122 3 77 1 122 3 112 EFSA Journal 2010; 8(4):1309 112/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Table CA2. (contd.). Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from Gallus gallus, 2004-2007, using harmonised cut-off values Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 26 58 26 50 Czech Republic 50 48 53 70 50 48 53 75 Denmark 77 8 77 8 75 7 94 9 73 3 76 8 75 8 94 9 Finland 94 0 69 4 90 2 66 0 France 32 13 49 14 56 30 32 28 49 18 Germany 49 41 95 53 100 74 49 37 95 52 Italy 24 50 108 57 48 67 12 0 108 58 48 69 Netherlands 78 44 16 56 45 58 78 42 16 56 45 58 Slovenia 71 73 Spain 16 94 17 94 19 100 15 93 17 94 19 100 Sweden 94 5 Total (11 MSs) 77 8 276 33 410 42 535 43 236 4 352 23 547 42 285 49 Norway 99 1 75 0 69 3 108 2 99 1 Switzerland 77 12 122 15 77 13 122 18 EFSA Journal 2010; 8(4):1309 113/304 113

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA3. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from Gallus gallus, 2005-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2005 2006 2007 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 25 60 25 8 25 0 France 74 76 81 86 76 79 74 15 81 11 76 13 74 3 81 0 76 0 Germany 21 71 21 14 49 0 Italy 96 63 23 74 16 0 96 29 23 17 57 0 96 2 23 0 Netherlands 12 58 21 48 12 0 21 14 12 0 21 0 Slovenia 27 67 27 7 27 19 Spain 16 88 29 90 21 90 15 20 29 41 21 10 15 13 29 10 21 5 Total (7 MSs) 111 77 245 74 166 73 126 13 245 21 166 13 195 2 245 4 166 1 Switzerland 17 24 17 0 17 0 Ciprofloxacin Nalidixic acid Country 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 25 68 25 68 France 74 35 81 42 76 55 74 42 81 19 Germany 49 41 21 24 Italy 51 84 96 73 23 43 19 0 96 54 23 43 Netherlands 12 67 21 76 12 58 21 76 Slovenia 27 93 Spain 16 94 29 93 21 100 16 94 29 83 21 86 Total (7 MSs) 190 55 218 64 166 64 130 39 245 50 90 68 Switzerland 17 24 17 24 114 EFSA Journal 2010; 8(4):1309 114/304

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 from Gallus gallus. These figures show that tetracycline, ciprofloxacin and nalidixic acid resistance levels vary considerably between MSs, some MSs have no or a low occurrence of resistance while others have more than 50% resistance (Figures CA1, CA4 and CA5). Erythromycin and gentamicin resistance levels remain, in all reporting countries, at a constantly low level (Figures CA2 and CA3). Although figures indicate that the occurrence of resistance in tested isolates remains relatively constant over the study period for many countries, some changes in resistance among C. jejuni were also observed, mainly increases. Figure CA1. Trends in tetracycline resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 % resistant isolates 80 60 40 20 0 2004 2005 2006 2007 Czech Republic Germany Norway Denmark Finland France Italy Netherlands Spain Switzerland Figure CA2. Trends in erythromycin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Germany Norway Denmark Finland France Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(4):1309 115/304 115

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA3. Trends in gentamicin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 % resistant isolates 80 60 40 20 0 2004 2005 2006 2007 Czech Republic Germany Norway Denmark Finland France Italy Netherlands Spain Switzerland Figure CA4. Trends in ciprofloxacin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Czech Republic Denmark France Germany Italy Netherlands Spain Switzerland 116 EFSA Journal 2010; 8(4):1309 116/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA5. Trends in nalidixic acid resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 % resistant isolates 80 60 40 20 0 2004 2005 2006 2007 Czech Republic Germany Norway Denmark Finland France Italy Netherlands Spain Switzerland Temporal trends in resistance among C. coli Only four countries reported antimicrobial resistance in C. coli from Gallus gallus over the three-year period 2004-2007 (Figures CA6-10). As for C. jejuni from Gallus gallus tetracycline, ciprofloxacin and nalidixic acid resistance occurred frequently in C. coli. In addition, erythromycin resistance occurred more often among C. coli compared to C. jejuni in all four countries. Figure CA6 Trends in tetracycline resistance in Campylobacter coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2005 2006 2007 France Italy Netherlands Spain EFSA Journal 2010; 8(4):1309 117/304 117

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA7. Trends in erythromycin resistance in Campylobacter coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2005 2006 2007 France Italy Netherlands Spain Figure CA8. Trends in gentamicin resistance in Campylobacter coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2005 2006 2007 France Italy Netherlands Spain 118 EFSA Journal 2010; 8(4):1309 118/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA9. Trends in ciprofloxacin resistance in Campylobacter coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2005 2006 2007 France Italy Netherlands Spain Figure CA10. Trends in nalidixic acid resistance in Campylobacter coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2005 2006 2007 France Italy Netherlands Spain EFSA Journal 2010; 8(4):1309 119/304 119

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Spatial distribution of resistance among C. jejuni and C. coli The spatial distribution of tetracycline and erythromycin resistance in tested C. jejuni and C. coli isolates from Gallus gallus in 2007 are shown in Figures CA11-14. The figures underline a high occurrence of tetracycline resistance compared to erythromycin. The most apparent spatial patterns are the low occurrence of tetracycline resistance in C. jejuni from Gallus gallus in the Nordic countries and a higher occurrence in southern Europe (Figure CA11). For erythromycin, no clear spatial distribution was observed (Figure CA12). Resistance levels to tetracycline in C. coli over 66% were reported by Spain, France, Italy and Slovenia (Figures CA13). The highest erythromycin resistance levels (equal or over 13%) in C. coli were reported by France, the Netherlands and Italy (Figure CA14). Figure CA11. Spatial distribution of tetracycline resistance among Campylobacter jejuni from Gallus gallus in countries reporting quantitative data in 2007 1 1. For Slovenia, 2006 data were used. 120 EFSA Journal 2010; 8(4):1309 120/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA12. Spatial distribution of erythromycin resistance among Campylobacter jejuni from Gallus gallus in countries reporting quantitative data in 2007 1 1. For Slovenia, 2006 data were used. Figure CA13. Spatial distribution of tetracycline resistance among Campylobacter coli from Gallus gallus in countries reporting quantitative data in 2007 1 1. For Slovenia, 2006 data were used. EFSA Journal 2010; 8(4):1309 121/304 121

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA14. Spatial distribution of erythromycin resistance among Campylobacter coli from Gallus gallus in countries reporting quantitative data in 2007 1 1. For Slovenia, 2006 data were used. 5.1.2 Meat from broilers Resistance levels among C. jejuni Together six MSs and two non-mss reported quantitative antimicrobial resistance data on C. jejuni isolates from broiler meat. The majority of the data were reported in 2007 as only a few MSs reported data before that year. At reporting MS group level in 2007, resistance levels in tested C. jejuni isolates were high for tetracycline (37%), ciprofloxacin (39%) and nalidixic acid (36%), and low for erythromycin (3%) and gentamicin (2%). As for C. jejuni from Gallus gallus, either 0% or less than 10% erythromycin and gentamicin resistance was reported in tested isolates by the countries. A resistance level of 0% for ciprofloxacin and nalidixic acid was reported by Norway, while Denmark reported a level less than 12%. In the remaining countries, between 20% and 66% ciprofloxacin and nalidixic acid resistance was reported. Tetracycline resistance occurred frequently in tested C. jejuni isolates in most countries (Table CA4). Resistance levels among C. coli Overall five MSs and one non-ms reported data on antimicrobial resistance among C. coli isolates from broiler meat. In 2007, resistance levels in the reporting MS group were 76% for tetracycline, 6% for erythromycin, 0% for gentamicin, 54% for ciprofloxacin and 54% for nalidixic acid (Table CA5). These MS group resistance levels are higher for some antimicrobials than the ones observed for C. jejuni in meat from broilers. 122 EFSA Journal 2010; 8(4):1309 122/304

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, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 80 16 80 0 80 0 Belgium 66 41 64 47 66 2 64 0 66 0 64 0 Denmark 102 0 76 4 114 10 103 0 76 1 114 2 103 0 76 0 113 0 France 70 44 114 57 70 0 114 3 70 0 114 3 Germany 99 54 99 8 99 6 Total (5 MSs) 102 0 76 4 136 43 471 37 103 0 76 1 136 1 471 3 103 0 76 0 136 0 470 2 Norway 33 0 35 0 29 0 33 0 35 0 29 0 33 9 35 3 29 0 Switzerland 109 32 109 0 109 0 Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 80 66 80 66 Belgium 66 36 64 42 66 32 64 42 Denmark 103 3 76 5 114 11 103 3 76 8 114 11 France 70 23 114 23 70 20 Germany 99 64 Total (5 MSs) 103 3 76 5 136 29 471 39 103 3 76 8 136 26 258 36 Norway 29 0 33 0 35 0 29 0 Switzerland 109 30 109 30 EFSA Journal 2010; 8(4):1309 123/304 123

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA5. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from meat from broilers, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid Country 2006 2007 2006 2007 2006 2007 2006 2007 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 22 68 22 0 22 0 22 73 22 64 Belgium 25 100 31 77 25 8 31 3 25 0 31 0 25 56 31 48 25 52 30 47 France 125 71 98 78 125 5 98 8 125 0 98 0 125 50 98 51 124 34 Total (3 MSs) 150 76 151 76 150 5 151 6 150 0 151 0 150 51 151 54 149 37 52 54 Switzerland 37 54 37 5 37 0 37 46 37 46 124 EFSA Journal 2010; 8(4):1309 124/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. 5.2 Pigs Resistance levels among C. coli Together eight MSs and one non-ms provided quantitative data on C. coli isolates from pigs (Table CA6). Tetracycline resistance among tested C. coli isolates from pigs was over 60% in most countries, resulting in a very high resistance level at reporting MS group level ranging from 64% to 80% over the years. Resistance levels to ciprofloxacin and nalidixic acid among tested C. coli isolates from pigs were both high, varying between 35% to 46% and 30% to 47%, respectively, over the 2004 to 2007 period. However, wide variations were observed between reporting MSs. Only the Netherlands reported ciprofloxacin and nalidixic acid resistance lower than or equal to 10% for three consecutive years (2005-2007) while Spain reported ciprofloxacin and nalidixic acid resistance levels of over 80% during the 2004 to 2007 period in tested C. coli isolates from pigs. The resistance levels to erythromycin at reporting MS group level ranged from 24% to 39% during the 2004-2007 period. The reported occurrence of erythromycin resistance among tested C. coli isolates varied between reporting MSs from 0% in Italy and Sweden in 2005 to 70% in Spain in 2005. In contrast, gentamicin resistance level was 0% or below 10% in most countries except in Italy where 14% was reported in 2007 and in Spain, where levels of 16% to 26% were reported from 2004 to 2007. At reporting MS group level, gentamicin resistance varied between 4% to 8% of tested isolates during the years 2004-2007. EFSA Journal 2010; 8(4):1309 125/304 125

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA6. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from pigs, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 346 78 210 80 346 16 219 18 346 2 219 0 Denmark 100 2 105 6 103 9 104 5 100 23 105 20 103 13 104 11 100 0 105 0 103 0 104 0 France 97 97 67 67 80 83 77 95 97 54 67 37 80 20 77 32 97 1 67 3 80 0 77 3 Germany 236 76 91 88 236 7 91 27 236 0 91 9 Italy 78 92 143 97 25 0 78 44 143 60 40 3 78 6 143 14 Netherlands 153 86 40 83 103 88 153 9 40 28 103 18 153 0 40 0 103 0 Spain 111 98 141 99 132 100 144 99 141 70 132 59 144 63 113 23 141 26 132 19 144 16 Sweden 97 4 97 0 97 0 Total (8 MSs) 654 73 773 64 669 74 662 80 543 24 807 25 669 25 662 39 656 5 822 5 669 4 662 8 Switzerland 52 37 46 39 52 12 46 11 52 0 46 0 Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 346 38 219 32 346 32 219 28 Denmark 100 16 105 14 103 13 104 10 88 5 105 15 103 11 104 10 France 97 25 67 36 80 25 77 35 97 28 67 25 80 15 Germany 236 23 91 45 236 15 Italy 39 33 78 59 143 64 27 0 78 50 143 63 Netherlands 153 5 40 10 103 10 153 5 40 10 103 10 Spain 113 85 140 88 132 86 144 88 112 83 139 87 132 84 144 85 Sweden 97 24 Total (8 MSs) 656 41 723 35 669 38 662 46 643 37 807 30 669 32 494 47 Switzerland 52 25 46 30 52 31 46 30 126 EFSA Journal 2010; 8(4):1309 126/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Temporal trends in resistance among C. coli For eight countries it was possible to observe temporal trends for C. coli from pigs (Figures CA15-19). Six out of eight countries reported more than 60% tetracycline resistance over time. In contrast, Denmark found less than 10% tetracycline resistance from 2004 to 2007 (Figure CA15). Erythromycin resistance was commonly found in C. coli from many reporting MSs and, as for the occurrence of ciprofloxacin and nalidixic acid resistance, the occurrence of erythromycin resistance varied between reporting MSs (Figure CA16). Gentamicin resistance in C. coli from pigs was below 10% in most countries, except for Spain where more than 20% gentamicin resistance was found in 2004 and 2005 (Figure CA17). In general, most changes observed among C. coli from pigs from 2004 to 2007 were increases. Figure CA15. Trends in tetracycline resistance in Campylobacter coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Italy Netherlands Spain Switzerland Figure CA16. Trends in erythromycin resistance in Campylobacter coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(4):1309 127/304 127

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA17. Trends in gentamicin resistance in Campylobacter coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Italy Netherlands Spain Switzerland Figure CA18. Trends in ciprofloxacin resistance in Campylobacter coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Italy Netherlands Spain Switzerland 128 EFSA Journal 2010; 8(4):1309 128/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA19. Trends in nalidixic acid resistance in Campylobacter coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Italy Netherlands Spain Switzerland Spatial distribution of resistance among C. coli The spatial distributions of tetracycline, erythromycin and ciprofloxacin resistance levels in tested C. coli isolates from pigs are displayed for 2007 in Figures CA20-22. Due to the high occurrence of tetracycline resistance in most reporting MSs, no clear pattern could be detected. For erythromycin and ciprofloxacin, the highest occurrence of resistance in tested C. coli isolates was observed in the southern part of Europe. Figure CA20. Spatial distribution of tetracycline resistance among Campylobacter coli from pigs in countries reporting quantitative data in 2007 EFSA Journal 2010; 8(4):1309 129/304 129

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA21. Spatial distribution of erythromycin resistance among Campylobacter coli from pigs in countries reporting quantitative data in 2007 Figure CA22. Spatial distribution of ciprofloxacin resistance among Campylobacter coli from pigs in countries reporting quantitative data in 2007 130 EFSA Journal 2010; 8(4):1309 130/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. 5.3 Cattle Resistance levels among C. jejuni Together, six MSs and one non-ms provided quantitative data on C. jejuni isolates from cattle during the 2004 to 2007 period. Tetracycline resistance varied between 23% to 33% in the reporting MS group during the period. At country level it ranged from 3% in Denmark and Sweden up to 80% in Spain. At reporting MS group level, resistance levels to ciprofloxacin and nalidixic acid among tested C. jejuni isolates ranged from 20% to 35% and 23% to 35%, respectively, during 2004 to 2007. The different reporting MSs detected either 0% or less than 10% erythromycin and gentamicin resistance among C. jejuni with resistance levels to erythromycin and gentamicin ranging from 0% to 3% and from 0% to 1%, respectively, in the reporting MS group. (Table CA7). Resistance levels among C. coli Overall quantitative data on C. coli isolates from cattle provided by four MSs and one non-ms were included in the analysis. Resistance levels in the reporting MS group varied between 59% and 92% for tetracycline, between 56% and 75% for ciprofloxacin, between 56% and 73% for nalidixic acid and between 4% and 16% for erythromycin. The reported occurrence of erythromycin resistance among C. coli varied more than for C. jejuni, the highest occurrence of 30% being reported by Denmark. Ciprofloxacin and nalidixic acid resistance varied from 10% in Denmark to 86% in Spain while tetracycline resistance varied from 30% in Denmark to 98% in the Netherlands (Table CA8). EFSA Journal 2010; 8(4):1309 131/304 131

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA7. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from cattle, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 126 40 141 32 205 32 202 27 126 1 141 3 205 0 202 0 126 0 141 1 205 0 202 0 Denmark 42 0 41 0 74 3 84 1 42 0 41 2 74 0 84 1 42 0 41 0 74 0 84 0 Italy 44 11 40 25 54 0 40 0 54 0 40 3 Netherlands 44 64 50 44 71 52 44 7 50 6 71 0 44 5 50 0 71 0 Spain 55 80 55 0 55 2 Sweden 68 0 68 0 68 0 Total (6 MSs) 168 30 270 29 437 23 412 33 168 1 280 3 437 1 412 0 168 0 280 1 437 0 412 0 Switzerland 137 34 137 0 137 1 Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 126 26 141 32 205 31 202 41 126 30 141 35 205 33 202 42 Denmark 42 2 41 29 74 19 84 17 41 2 41 29 74 20 84 17 Italy 54 13 40 28 48 4 40 35 Netherlands 44 34 50 28 71 28 44 34 50 28 71 28 Spain 55 47 55 47 Sweden 68 9 Total (6 MSs) 168 20 280 24 369 28 412 35 167 23 274 29 437 27 412 35 Switzerland 137 38 137 37 132 EFSA Journal 2010; 8(4):1309 132/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Table CA8. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from cattle, 2004-2007, using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 17 59 22 41 30 50 17 6 22 0 30 0 17 0 22 0 30 0 Denmark 10 30 10 30 10 0 Netherlands 59 98 68 96 77 92 59 5 68 19 77 18 59 3 68 4 77 6 Spain 14 93 14 7 14 14 Total (4 MSs) 17 59 81 83 108 77 91 92 17 6 81 4 108 15 91 16 17 0 81 2 108 3 91 8 Switzerland 27 70 27 11 27 0 Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 17 53 22 59 30 40 17 53 22 50 30 40 Denmark 10 10 10 20 Netherlands 59 81 68 69 77 69 59 81 68 68 77 69 Spain 14 86 14 86 Total (4 MSs) 17 53 81 75 108 56 91 71 17 53 81 73 108 56 91 71 Switzerland 27 44 27 44 EFSA Journal 2010; 8(4):1309 133/304 133

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Temporal trends in resistance among C. jejuni Fewer MSs reported resistance levels among tested C. jejuni isolates from cattle (Figures CA23-26) and differences in the occurrence of resistance between MSs were not as large as for C. jejuni from Gallus gallus. As for C. jejuni in Gallus gallus, resistance to tetracycline, ciprofloxacin, and nalidixic acid was the most often reported. Figure CA23. Trends in tetracycline resistance in Campylobacter jejuni from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Italy Netherland Figure CA24. Trends in erythromycin resistance in Campylobacter jejuni from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Italy Netherland 134 EFSA Journal 2010; 8(4):1309 134/304

ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA25. Trends in ciprofloxacin resistance in Campylobacter jejuni from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Italy Netherland Figure CA26. Trends in nalidixic acid resistance in Campylobacter jejuni from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Italy Netherland 5.4 Comparison of antimicrobial resistance among Campylobacter jejuni and Campylobacter coli from food and animals within and between MSs The comparison of antimicrobial resistance among C. jejuni and C. coli from food and animals was possible for C. jejuni and C. coli from Gallus gallus and broiler meat in 2007 (Tables CA9 and CA10). Both for C. jejuni and C. coli the levels of resistance to the different antimicrobials in tested isolates from broiler meat and from Gallus gallus were similar within each country although the levels of resistance varied between countries. Among C. jejuni, no significant differences in resistance were observed between isolates from Gallus gallus and broiler meat, except for Switzerland where the occurrence of resistance to tetracycline (p=0.03), ciprofloxacin (p<0.01) and nalidixic acid (p<0.01) was significantly higher in isolates from broiler meat compared to Gallus gallus. In C. coli, only among isolates from Switzerland, the occurrence of tetracycline resistance (p=0.04) was significantly higher in isolates from broiler meat compared to Gallus gallus. EFSA Journal 2010; 8(4):1309 135/304 135

5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA9. Comparison of resistance (%) among Campylobacter jejuni from Gallus gallus and broiler meat (Gallus gallus) in 2007 Compound Austria Denmark France Germany Norway Switzerland Gallus gallus Broiler meat Gallus gallus Broiler meat Gallus gallus Broiler meat Gallus gallus Broiler meat Gallus gallus Broiler meat Gallus gallus Broiler meat Tetracycline 27 16 10 10 50 57 54 54 1 0 20 32 Chloramphenicol 0 0 0 0 0 Erythromycin 0 0 1 2 0 3 13 8 0 0 3 0 Gentamicin 0 0 0 0 0 3 7 6 0 0 3 0 Streptomycin 0 0 2 4 4 3 2 0 5 2 Ciprofloxacin 58 66 9 11 30 23 74 64 1 0 15 30 Nalidixic acid 50 66 9 11 1 0 18 30 Number of isolates 26 80 94 114 56 114 100 99 99 29 122 109 Table CA10. Comparison of resistance (%) among Campylobacter coli from Gallus gallus and broiler meat (Gallus gallus) in 2007 Compound Austria France Switzerland Gallus gallus Broiler meat Gallus gallus Broiler meat Gallus gallus Broiler meat Tetracycline 60 68 79 78 24 54 Chloramphenicol 0 0 0 0 Erythromycin 8 0 13 8 0 5 Gentamicin 0 0 0 0 0 0 Streptomycin 32 27 16 27 24 27 Ciprofloxacin 68 73 55 51 24 46 Nalidixic acid 68 64 24 46 Number of isolates 25 22 76 98 17 37 136 EFSA Journal 2010; 8(4):1309 136/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA 6 Antimicrobial resistance in indicator Escherichia coli - quantitative data 6 137

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA 6 Antimicrobial resistance in indicator Escherichia coli Escherichia coli are commensal bacteria common to all animals and humans, and can serve as an indicator bacterium that easily become resistant to antimicrobials. It is generally considered that resistance in E. coli is an indicator of the general resistance level encountered in the populations of gram-negative bacteria in healthy animals and food thereof. Collecting indicator E. coli from representative random samples of healthy animals enables direct comparison of resistance between different animal species and analyses of trends over time. Furthermore, changes in the resistance in E. coli may also serve as an early warning system for resistance in potentially pathogenic bacteria. E. coli are also considered to constitute a reservoir of resistance genes, which may be transferred to pathogenic bacteria causing disease in animals or humans. During the period 2004 to 2007, antimicrobial susceptibility data on commensal E. coli were reported by 16 MSs and two non-mss. The data derived either from dilution method (149,061 isolates) or disk diffusion methods (28,065 isolates) (Table MM1). Table EC1 present the MSs reporting E. coli MIC values and inhibition zones from 2004 to 2007. As no more than four countries reported MIC or inhibition zone data on indicator E. coli isolates collected from food, which is insufficient data to indicate the level of resistance among indicator E. coli from food sources at European level, only reported data from animals were used in the analysis and are presented hereafter. Table EC1. Overview of countries reporting MIC and inhibition zone diameter distributions on indicator Escherichia coli from animals and food, 2004-2007 Method Dilution Diffusion Origin Total number of MSs reporting Meat from broilers 2 MSs: DK, FR Non-MS: NO Countries Meat from bovine animals 2 MSs: DK, SI Non-MS: NO Meat from turkeys 1 MS: FR Non-MS: NO Meat from pigs 2 MSs: DK, FR Non-MS: NO Gallus gallus 9 MSs: AT, DE, DK, ES, FI, FR, IT, NL, SE Non-MSs: CH, NO Pigs 10 MSs: AT, DE, DK, EE, ES, FI, FR, IT, NL, SE Non-MSs: CH, NO Cattle 9 MSs: AT, DE, DK, EE, ES, FI, FR, NL, SE Non-MSs: CH, NO Meat from bovine animals 1 MS: SI Gallus gallus 7 MSs: EE, ES, GR, HU, IT, PL, SI Pigs 8 MSs: EE, ES, HU, IT, PL, SK, SI, UK Cattle 7 MSs: EE, ES, HU, IT, PL, SI, UK Resistance levels to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin, and nalidixic acid over time among the tested E. coli isolates are presented in the tables and figures hereafter. They were chosen either because they have been recognised as being critically important for human medicine (e.g. fluoroquinolones, third generation cephalosporin and macrolides) (Collignon et al., 2009), or because of interesting trends shown in MIC values. MIC distributions and resistance levels to tetracycline, chloramphenicol, florfenicol, ampicillin, cefotaxime, ceftazidime, ceftiofur, sulfonamide, trimethoprim, apramycin, gentamicin, neomycin, spectinomycin, streptomycin, ciprofloxacin, and nalidixic acid among the E. coli isolates, susceptibility tested over the period 2004 to 2007, are set out in Appendix 4 tables. 138 EFSA Journal 2010; 8(4):1309 138/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA A statistical analysis of temporal trends at MS level was carried out over the period 2004 to 2007. In the figures displaying trends in the development of antimicrobial resistance over time, both MIC and inhibition zone diameter data interpreted by using epidemiological cut-off values are included. Only a few EU MSs reported data for four consecutive years. More frequently, data were reported for two or three out of the four 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 also as point estimates. In addition, the spatial distributions of tetracycline and nalidixic acid resistance levels in E. coli from Gallus gallus, turkeys, pigs and cattle are presented for 2007. Whenever data for 2007 were not available, 2006 resistance percentages were used instead. 6.1 Poultry: Fowl (Gallus gallus) In this report, fowl (Gallus gallus) includes breeding flocks, laying hen flocks, and broiler flocks of Gallus gallus. Together, 14 MSs and two non-mss provided quantitative data on E. coli in Gallus gallus (Table EC1). Resistance levels among Escherichia coli The proportion of resistant E. coli isolates in the reporting MS group were for tetracycline 29%-43%, for ampicillin 25%-44%, for sulfonamide 7%-43%, for ciprofloxacin 13%-44% and for nalidixic acid 30%-50% during the years 2004-2007. Lower resistance levels were reported for ceftiofur (0%-3%), and gentamicin (1%-4%) in the same period. The Nordic countries, Denmark, Finland, Norway and Sweden, reported the lowest occurrence of resistance to tetracycline with an overall variance between 3% and 17%, while in Spain, Italy and France, resistance to tetracycline among E. coli varied between 68% and 78%. Similarly for ampicillin, the resistance level was 4% to 18% in the Nordic countries and among France, Italy and Spain it was 37% to 83% in the 2004 to 2007 period (Table EC2). Denmark reported less than 15% ciprofloxacin-resistant isolates, while Sweden, Italy, Austria and the Netherlands in 2007 and Germany in 2005 and 2006 reported more than 40% ciprofloxacin-resistant isolates. Resistance levels in the reporting MS group for ciprofloxacin was highest in 2007, where 44% of the isolates were resistant (Table EC2). From 2004 to 2006, the MIC test range for ciprofloxacin in the Netherlands and Spain did not include concentrations below 0.06 mg/l and consequently, during these years, ciprofloxacin resistance could not be calculated, and these data are not presented in Table EC2. Ten countries reported quantitative data for ceftiofur, but most of them reported for one or two years only. Ceftiofur resistance was detected in Austria, Denmark, Finland, France, Hungary, Slovenia and Sweden, with resistance levels not exceeding 3%, except for Germany where 28% of 50 isolates were resistant to ceftiofur in 2006 (Table EC2). Seven countries reported cefotaxime data and among these only Austria found no resistance. The Netherlands reported 14% to 21% cefotaxime resistance in 2005-2007, Spain reported 18% to 24% in 2004 to 2006, while Italy found 11% resistance in 2007. France and Sweden in 2007 and Norway in 2006 reported between 1% and 2% cefotaxime resistance. Three out of the seven countries also reported on ceftazidime and the results were similar to cefotaxime (Table EC2 and Appendix 4 Table EC1b). EFSA Journal 2010; 8(4):1309 139/304 139

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Table EC2, Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur and cefotaxime among indicator Escherichia coli from Gallus gallus, 2004-2007, using harmonised cut-off values, Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 266 27 43 14 266 5 43 5 266 25 43 19 Denmark 142 11 133 8 123 7 114 8 142 0 132 0 123 0 114 0 142 18 132 16 123 17 114 11 Estonia 21 24 21 0 21 10 Finland 380 17 380 0 380 16 France 100 73 101 78 100 8 101 4 100 37 101 48 Greece 10 70 10 50 10 50 Germany 42 57 50 38 42 2 50 2 42 43 50 64 Hungary 147 43 404 44 147 7 417 7 147 40 420 42 Italy 77 71 186 68 54 69 77 29 176 24 54 39 77 60 186 67 54 83 Netherlands 304 61 154 53 43 56 304 18 154 19 43 16 154 66 43 60 Poland 73 47 216 57 73 5 223 9 73 55 222 54 Slovenia 66 42 66 9 66 61 Spain 152 76 74 68 96 70 149 17 74 19 96 27 152 58 Sweden 300 6 296 3 300 0 296 0 305 4 286 5 Total (14 MSs) 741 29 1,214 42 1,345 43 867 33 738 5 1,213 9 1,348 11 874 6 746 25 835 27 1,265 44 863 32 Norway 86 7 190 4 86 0 190 0 86 17 190 13 Switzerland 310 39 284 34 310 4 284 4 309 16 284 14 140 EFSA Journal 2010; 8(4):1309 140/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Table EC2. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur and cefotaxime among indicator Escherichia coli from Gallus gallus, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % N % N % N % N % N % N % N % N % N % N % N % Gallus gallus Austria 266 2 43 0 266 30 43 28 Denmark 142 1 132 1 123 0 114 2 129 9 132 12 123 9 114 18 Estonia 21 5 Finland 380 0 380 13 France 101 2 101 2 101 92 Greece Germany 42 0 50 28 42 52 50 24 Hungary 147 0 377 1 96 0 415 35 Italy 54 11 172 58 54 69 Netherlands 304 14 154 16 43 21 303 72 308 71 43 63 Poland 72 32 224 43 Slovenia 66 3 66 29 Spain 152 18 74 24 96 21 74 54 96 54 87 49 Sweden 300 0 296 1 296 1 300 9 296 6 Total (14 MSs) 589 0 554 0 882 3 511 1 152 18 378 16 250 18 537 4 525 7 1,024 36 1,496 43 962 36 Norway 86 0 190 1 190 1 86 14 190 9 Switzerland 310 0 284 1 310 41 284 40 EFSA Journal 2010; 8(4):1309 141/304 141

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Table EC2. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur and cefotaxime among indicator Escherichia coli from Gallus gallus, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 266 1 43 0 266 50 43 49 266 49 43 49 Denmark 142 0 132 0 123 0 114 0 142 13 132 11 123 8 114 14 140 12 132 10 123 7 114 11 Estonia 21 5 Finland 380 2 380 1 France 100 1 101 0 100 27 101 21 100 26 101 19 Greece 10 90 Germany 42 7 50 4 42 48 50 44 42 48 50 44 Hungary 146 72 170 78 Italy 54 9 54 54 77 36 186 37 54 54 Netherlands 304 4 154 8 43 2 43 49 304 52 154 50 43 49 Poland 68 60 222 66 Slovenia 66 62 Spain 152 10 74 16 96 14 152 78 74 89 96 82 Sweden 300 1 296 0 296 59 300 5 296 7 Total (14 MSs) 594 3 1,032 3 689 4 651 1 142 13 274 23 439 38 651 44 738 35 1,208 30 1,111 50 873 31 Norway 86 0 190 1 190 20 86 0 190 1 Switzerland 310 4 284 2 310 37 284 25 310 35 284 24 142 EFSA Journal 2010; 8(4):1309 142/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Temporal trends in resistance among Escherichia coli Figures EC1-6 present trends in resistance levels to selected antimicrobials in E. coli isolates from Gallus gallus. In particular the occurrence of tetracycline, ampicillin, sulfonamide and nalidixic acid resistance varied considerably between reporting MSs. Figures show that a number of countries tend to report high resistance levels to several antimicrobials. Figures EC1-6 also indicate that, in several countries, the occurrence of resistance remains relatively constant over time, although some changes may also be observed. Figure EC1. Trends in tetracycline resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Netherlands Poland Spain Sweden Norway Switzerland Figure EC2. Trends in chloramphenicol resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland EFSA Journal 2010; 8(4):1309 143/304 143

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Figure EC3. Trends in ampicillin resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Hungary Italy Netherlands Poland Sweden Norway Switzerland Figure EC4. Trends in sulfonamide resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland 144 EFSA Journal 2010; 8(4):1309 144/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC5. Trends in gentamicin resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Italy Netherlands Norway Spain Sweden Switzerland Figure EC6. Trends in nalidixic acid resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark France Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland EFSA Journal 2010; 8(4):1309 145/304 145

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Spatial distribution of resistance among Escherichia coli The spatial distributions of tetracycline and nalidixic acid resistance among E. coli from Gallus gallus are displayed in Figures EC7-8. Figure EC7 indicates an increase in tetracycline resistance levels from northern to southern Europe. For nalidixic acid the spatial pattern is not as clear, however the lowest nalidixic resistance levels were observed in the Nordic countries and an increase was observed towards the southern and eastern parts of Europe. Figure EC7. Spatial distribution of tetracycline resistance among indicator Escherichia coli from Gallus gallus in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Germany, Hungary, Portugal, Slovenia, Spain and Norway, 2006 data were used. 146 EFSA Journal 2010; 8(4):1309 146/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC8. Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from Gallus gallus in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Germany, Hungary, Slovenia, Spain and Norway, 2006 data were used. EFSA Journal 2010; 8(4):1309 147/304 147

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA 6.2 Pigs Together 15 MSs and two non-mss provided quantitative data on E. coli in pigs (Table EC1). Resistance levels among Escherichia coli In indicator E. coli from pigs at reporting MS group level, resistance levels to tetracycline varied between 45% and 68% and to ampicillin between 17% and 31%; the ranges of resistance levels to sulfonamide and to ciprofloxacin were 22% to 47% and 4% to 24%, respectively, in 2004-2007 (Table EC3). The occurrence of tetracycline, ampicillin, sulfonamide and ciprofloxacin resistance varied considerably between MSs. In contrast, small differences were observed for ceftiofur, cefotaxime, gentamicin and nalidixic acid resistance. Ceftiofur and cefotaxime resistance varied in the reporting MS group between 0% and 1%, and the resistance levels for gentamicin and nalidixic acid ranged between 2% and 4% and between 4% and 7%, respectively, in 2004 to 2007 (Table EC3). In general, Sweden, Norway and Finland reported low occurrences of resistance to most antimicrobials (e.g. tetracycline resistance did not exceed 18%), while in France, Italy, Hungary, Slovakia, Slovenia and Spain, tetracycline resistance varied between 71% and 96% among tested E. coli isolates from pigs (Table EC3). All MSs reported data on ciprofloxacin and resistance in the MS group was highest in 2007, where 24% of the isolates were resistant. A large variation was observed in the reported ciprofloxacin resistance, with the highest occurrence of 74% reported by Estonia in 2007, followed by 54% in 2007 in the Netherlands. In Denmark legal restrictions have been in place on the use of fluoroquinolones in food animals since 2002 and ciprofloxacin resistance decreased from 3% in 2004 to 0% in 2007 (Table EC3). Also for pigs, the MIC test range for ciprofloxacin in the Netherlands and Spain did not include concentrations below 0.06 mg/l from 2004 to 2006. Consequently, during these years, ciprofloxacin resistance could not be calculated (data not presented in Table EC3). Twelve countries reported quantitative data for ceftiofur. Ceftiofur resistance was reported by Denmark, France, Hungary, Slovenia, Norway and Switzerland and the highest occurrence (3%) was observed in Slovenia in 2007. In the remaining reporting countries: Austria, Estonia, Finland, Germany, Slovakia and Sweden the occurrence was 0% (Table EC3). Nine countries reported cefotaxime data and resistance to cefotaxime was reported by France, Italy, the Netherlands, Spain and Norway at levels from 0% to 1%. In addition, three out of the nine countries reported on ceftazidime and the results were similar to the reported cefotaxime resistance (Appendix 4 Table EC2b). 148 EFSA Journal 2010; 8(4):1309 148/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Table EC3. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from pigs, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 217 58 226 60 301 56 46 52 217 4 226 3 301 4 46 4 217 6 226 11 301 12 46 2 Denmark 208 44 119 18 148 28 150 28 208 9 136 1 148 1 150 4 208 33 136 18 148 20 150 19 Estonia 40 23 11 0 19 37 40 3 11 0 19 5 40 10 11 9 19 16 Finland 391 16 135 18 391 1 135 1 391 6 135 7 France 101 81 100 86 100 86 126 83 99 21 100 14 100 20 126 25 99 26 100 22 100 28 126 30 Germany 30 57 30 33 30 40 Hungary 171 74 306 78 171 9 309 19 171 23 316 40 Italy 166 80 73 79 174 73 149 82 166 30 73 32 153 24 149 29 166 52 73 53 174 55 149 60 Netherlands 299 62 79 70 169 73 299 9 79 10 169 12 299 30 79 34 169 37 Poland 272 35 341 21 161 17 278 2 344 4 162 0 278 10 344 9 161 11 Slovakia 73 78 Slovenia 34 71 34 26 34 76 Spain 183 96 192 90 193 88 229 93 183 31 192 31 193 31 223 33 183 73 Sweden 390 9 390 3 390 6 Total (14 MSs) 1,709 52 1,883 45 1,312 68 1,218 58 1,713 10 1,830 9 1,294 15 1,213 15 1,713 24 1,638 17 1,129 31 989 28 Norway 125 10 198 9 125 1 198 0 125 8 198 10 Switzerland 90 26 98 36 90 6 98 8 90 21 98 24 EFSA Journal 2010; 8(4):1309 149/304 149

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Table EC3. (contd.). (Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from pigs, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 217 0 226 0 301 0 46 0 217 30 226 35 301 36 46 24 Denmark 208 0 136 0 148 0 150 1 208 47 136 30 148 26 150 24 Estonia 11 0 19 0 11 0 19 0 40 10 11 0 19 32 Finland 391 0 135 0 391 12 135 12 France 126 1 126 1 126 87 Germany 30 0 30 77 Hungary 171 0 303 1 171 27 306 50 Italy 149 1 80 79 152 60 149 64 Netherlands 299 1 79 0 169 1 299 51 158 53 169 55 Poland 278 16 340 20 159 8 Slovakia 67 0 Slovenia 34 3 34 71 Spain 183 1 192 1 193 1 229 1 192 67 193 66 229 66 Sweden 284 0 390 0 351 1 Total (14 MSs) 987 0 743 0 763 0 329 1 183 1 881 0 283 1 873 1 1,256 22 1,614 31 1,269 47 1,216 46 Norway 125 0 198 1 198 1 125 12 198 13 Switzerland 90 2 98 0 90 53 98 47 150 EFSA Journal 2010; 8(4):1309 150/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Table EC3. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from pigs, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 217 3 226 1 301 2 46 0 217 3 226 5 301 4 46 4 217 2 226 4 301 3 46 4 Denmark 208 4 136 0 148 1 150 0 208 3 136 1 148 1 150 0 208 3 136 1 148 1 150 0 Estonia 11 18 19 5 19 74 40 0 11 0 19 0 Finland 391 1 135 0 391 1 135 1 France 100 4 100 1 100 1 126 2 100 9 100 4 100 7 126 3 99 7 100 3 100 6 126 2 Germany 30 17 30 23 30 23 Hungary 171 1 174 6 Italy 149 9 149 17 166 7 73 11 174 5 149 17 Netherlands 79 3 169 5 169 54 299 0 79 1 169 2 Poland 277 4 344 6 158 3 Slovakia Slovenia 34 32 Spain 183 9 192 5 193 6 229 5 183 21 192 17 193 20 229 17 Sweden 390 2 390 0 Total (14 MSs) 1,099 4 1,074 2 832 3 1,023 4 525 4 492 5 549 4 794 24 1,712 5 1,830 4 1,180 6 1,215 7 Norway 125 0 198 0 198 35 125 0 198 1 Switzerland 90 0 98 5 90 3 98 6 90 3 98 5 EFSA Journal 2010; 8(4):1309 151/304 151

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Temporal trends in resistance among Escherichia coli Figures EC9-14 display trends in resistance to selected antimicrobials in E. coli from pigs. The occurrences of tetracycline, ampicillin, sulfonamide and streptomycin resistance varied considerably among reporting countries. Tetracycline and streptomycin resistance were higher in E. coli from pigs compared to E. coli from Gallus gallus. In contrast, nalidixic acid resistance levels were lower in E. coli from pigs compared to E. coli from Gallus gallus. 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 EC9-14 indicate that, in several countries, the occurrence of resistance in E. coli from pigs remains relatively constant over time, although some changes may also be observed over time. Figure EC9. Trends in tetracycline resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Spain Norway Switzerland Figure EC10. Trends in chloramphenicol resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Spain Norway Switzerland 152 EFSA Journal 2010; 8(4):1309 152/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC11. Trends in ampicillin resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Norway Switzerland Figure EC12. Trends in sulfonamide resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland Hungary Italy Netherlands Poland Spain Norway Switzerland EFSA Journal 2010; 8(4):1309 153/304 153

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Figure EC13. Trends in gentamicin resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland France Netherlands Spain Norway Switzerland Figure EC14. Trends in nalidixic acid resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Spain Norway Switzerland 154 EFSA Journal 2010; 8(4):1309 154/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Spatial distribution of resistance among Escherichia coli The spatial distribution of tetracycline and nalidixic acid resistance in E. coli from pigs is shown in Figures EC15-16. Between 9 and 13 countries reported quantitative resistance data to the selected antimicrobials in 2006 and/or 2007. For tetracycline resistance, a clear spatial pattern was detected where high resistance levels were reported by southern and western European countries and much lower levels by northern and eastern countries. The reported nalidixic acid resistance levels in E. coli from pigs were in general low and no clear spatial distribution was observed. Figure EC15. Spatial distribution of tetracycline resistance among indicator Escherichia coli from pigs in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Hungary and Portugal, 2006 data were used. EFSA Journal 2010; 8(4):1309 155/304 155

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Figure EC16. Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from pigs in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Hungary and Portugal, 2006 data were used. 156 EFSA Journal 2010; 8(4):1309 156/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA 6.3 Cattle Together 14 MSs and two non-mss provided quantitative data for indicator Escherichia coli in cattle. Resistance levels among Escherichia coli In indicator E. coli from cattle, resistance levels at reporting MS group level was for tetracycline 15% to 28%, for ampicillin 11% to 18%, for sulfonamide 8% to 23% and lower for chloramphenicol (5% to 10%) and gentamicin (2% to 6%) (Tables EC4). In general, resistance levels in indicator E. coli from cattle were lower compared to indicator E. coli from Gallus gallus and pigs from the same MSs (Tables EC2 and EC3). Resistance levels for ciprofloxacin in the MS group in 2006 and 2007 were 24% and 33%, respectively. A large variation was observed in reported ciprofloxacin resistance, ciprofloxacin resistance was not reported in Austria in 2007 and in Denmark in 2004 and 2007, while the highest occurrence of 72% was reported by Estonia followed by 47% in the Netherlands in 2007 (Table EC4). Also for cattle, the MIC test-range for the Netherlands and Spain did not include concentrations below 0.06 mg/l from 2004 to 2006. Consequently, during these years, ciprofloxacin resistance could not be calculated; these data are not presented in Table EC4. Eleven countries reported quantitative data for ceftiofur, and resistance was reported by Austria, Estonia, France and Switzerland, with the highest occurrence (17%) observed in Switzerland in 2006 followed by 9% and 4% in Estonia in 2006 and 2007, respectively. In the remaining three countries occurrence was 1% or below (Table EC4). Six countries reported data on cefotaxime. Resistance to cefotaxime was reported by Estonia, France and the Netherlands at levels from 1% to 4%. In addition, two out of the six countries reported on ceftazidime and the results were similar to the reported cefotaxime resistance (Appendix 4 Table EC3b). EFSA Journal 2010; 8(4):1309 157/304 157

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Table EC4, Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from cattle, 2004-2007, using harmonised cut-off values, Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 212 5 284 15 168 8 43 12 212 0 284 1 168 2 43 0 212 2 284 6 168 2 43 2 Denmark 97 12 101 6 93 10 98 7 97 0 101 1 93 0 98 0 97 8 101 3 93 2 98 4 Estonia 49 12 23 9 25 20 49 2 23 4 25 12 49 8 23 4 25 20 Finland 185 1 185 0 185 1 France 100 42 100 26 100 27 103 35 100 18 100 14 100 17 103 19 99 28 100 14 100 17 103 28 Germany 20 50 20 5 20 35 Hungary 263 13 346 18 263 0 395 8 263 4 398 19 Italy 421 35 341 44 71 17 421 12 341 19 71 1 421 19 341 29 71 10 Netherlands 304 45 325 36 432 33 304 18 325 14 424 14 304 26 325 24 432 25 Poland 182 10 220 7 191 10 257 7 181 0 215 1 186 1 259 0 184 7 219 6 193 9 260 7 Slovenia 13 15 22 45 13 8 22 32 13 8 22 45 Spain 158 55 158 13 Sweden 314 2 314 0 314 0 Total (13 MSs) 1,275 21 1,419 28 1,829 15 1,138 27 1,274 6 1,414 10 1,873 5 1,132 10 1,276 11 1,418 17 1,883 11 983 18 Norway 98 1 98 0 98 2 Switzerland 560 48 560 22 560 41 158 EFSA Journal 2010; 8(4):1309 158/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Table EC4. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 212 1 284 1 168 1 43 0 212 2 284 13 168 8 43 9 Denmark 97 0 101 0 93 0 98 0 83 0 101 9 93 12 98 0 Estonia 23 9 25 4 23 0 25 4 49 12 23 9 25 20 Finland 185 0 185 0 185 0 France 103 1 103 1 103 51 Germany 20 0 20 45 Hungary 263 0 291 0 253 6 297 27 Italy 157 26 71 7 Netherlands 304 2 325 1 432 2 304 30 605 30 431 27 Poland 181 5 219 4 193 4 259 0 Slovenia 13 0 22 0 13 15 22 50 Spain 158 0 158 42 Sweden 314 0 314 0 314 2 Total (13 MSs) 757 0 405 1 1,087 0 248 1 304 2 662 1 761 2 886 8 977 16 1,962 16 1,139 23 Norway 98 0 98 1 Switzerland 560 17 560 56 EFSA Journal 2010; 8(4):1309 159/304 159

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Table EC4. (contd.). Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, cefotaxime, sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from cattle, 2004-2007, using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 212 0 284 0 168 1 43 0 212 1 284 4 168 1 43 0 212 1 284 1 168 0 43 0 Denmark 97 1 101 0 93 0 98 0 97 0 101 1 93 1 98 0 97 0 101 1 93 0 98 0 Estonia 23 9 25 12 23 35 25 72 49 0 23 0 25 0 Finland 185 3 185 0 France 101 6 100 7 100 3 103 2 101 15 100 10 100 6 103 7 99 9 100 9 100 5 103 4 Germany 20 5 20 10 20 10 Hungary 263 0 220 2 Italy 421 14 318 14 71 11 Netherlands 304 7 325 5 459 9 432 47 304 14 325 9 432 7 Poland 184 1 220 2 193 2 257 1 Slovenia 13 8 22 23 Spain 158 4 158 2 Sweden 314 1 314 26 314 1 Total (13 MSs) 410 2 809 4 1,208 3 886 6 410 4 505 5 883 24 701 33 1,276 6 1,396 8 1,705 3 1,138 4 Norway 98 0 98 0 Switzerland 560 5 560 4 560 3 160 EFSA Journal 2010; 8(4):1309 160/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Temporal trends in resistance among Escherichia coli Figures EC17-22 display temporal trends in resistance to selected antimicrobials in E. coli from cattle. In general, the variation in resistance levels between countries was much smaller compared to the variation observed for Gallus gallus and pigs. Some changes over time in the occurrence of resistance were observed. Figure EC17. Trends in tetracycline resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia Figure EC18. Trends in chloramphenicol resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia EFSA Journal 2010; 8(4):1309 161/304 161

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Figure EC19. Trends in ampicillin resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia Figure EC20. Trends in sulfonamide resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia Hungary Italy Netherlands Poland Slovenia 162 EFSA Journal 2010; 8(4):1309 162/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC21. Trends in gentamicin resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia France Netherlands Figure EC22. Trends in nalidixic acid resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, quantitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia EFSA Journal 2010; 8(4):1309 163/304 163

6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Spatial distribution of resistance among Escherichia coli The spatial distribution of tetracycline and nalidixic acid resistance among indicator E. coli from cattle are shown in Figures EC23-24. The highest tetracycline resistance levels were observed in south-western Europe while lower resistance levels were observed in northern and eastern parts of Europe. In general the nalidixic acid resistance levels were low and no clear patterns could be detected. Figure EC23. Spatial distribution of tetracycline resistance among indicator Escherichia coli from cattle in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Finland, Hungary, Italy, Sweden and Switzerland, 2006 data were used. 164 EFSA Journal 2010; 8(4):1309 164/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC24. Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from cattle in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Finland, Hungary, Italy, Portugal, Sweden and Switzerland, 2006 data were used. EFSA Journal 2010; 8(4):1309 165/304 165

166 EFSA Journal 2010; 8(4):1309 166/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7 Antimicrobial resistance in indicator enterococci - quantitative data 7 EFSA Journal 2010; 8(4):1309 167/304 167

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7 Antimicrobial resistance in indicator enterococci Together, eight MSs and two non-mss reported data on antimicrobial resistance in enterococci. A total of 28,701 isolates tested by quantitative methods on antimicrobial resistance reported by MSs from 2004 to 2007 were analysed to describe the occurrence of resistance among Enterococcus faecium and Enterococcus faecalis (Table MM1). The countries reporting data in E. faecium and E. faecalis during this period are presented in Tables EN1-2 by food/animal category and by testing method. Quantitative enterococci resistance data were only reported as MIC values, and very few countries reported MIC data on isolates collected from food. Only data reported from animals were therefore used for the analyses presented hereafter. For enterococci all qualitative data were also reported as quantitative data, the only exception was Ireland who reported only qualitative data for E. faecium isolated from cattle. Due to scarce additional qualitative data no subsection on qualitative data is presented for enterococci. Table EN1. Overview of countries reporting MIC distributions for Enterococcus faecium from animals and food, 2004-2007 Method Origin Total no of MSs reporting Countries Dilution Meat from broilers 0 Non-MS: CH Meat from turkeys 0 Non-MS: NO Gallus gallus 7 MSs: AT, DK, ES, FI, FR, NL, SE Non-MS: CH Turkeys 0 Non-MS: NO Pigs 6 MSs: AT, DK, EE, ES, FR, NL Non-MSs: CH, NO Cattle 6 MSs: AT, EE, ES, FR, NL, SE Non-MS: CH Table EN2. Overview of countries reporting MIC distributions for Enterococcus faecalis from animals and food, 2004-2007 Method Origin Total no of MSs reporting Countries Dilution Meat from broilers 0 Non-MS: CH Meat from turkeys 0 Non-MS: NO Gallus gallus 5 MSs: AT, DK, FI, NL, SE Non-MS: CH Turkeys 0 Non-MS: NO Pigs 5 MSs: AT, DK, EE, FI, NL Non-MSs: CH, NO Cattle 4 MSs: AT, EE, NL, SE Non-MS: CH 168 EFSA Journal 2010; 8(4):1309 168/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Tetracycline, ampicillin, erythromycin, streptomycin and vancomycin resistance results in E. faecium and E. faecalis are presented in the tables and figures hereafter. They were chosen either because of their critical importance in human medicine or because of interesting tendencies observed in MIC tables. Tables were generated where more than three countries reported quantitative data per Enterococcus species and sampling origin. Only data where 10 or more isolates were available per country per sampling origin and per year were included in the analysis. MIC distributions and resistance levels to tetracycline, chloramphenicol, ampicillin, erythromycin, streptomycin, vancomycin, quinupristin/ dalfopristin and avilamycin among enterococci over the period 2004 to 2007 are set out in Appendix 5 tables. The majority of data on antimicrobial resistance in E. faecium and E. faecalis was reported in 2007 and only very few countries reported resistance data for more than one out of the four years. Therefore, it was not possible to analyse temporal trends in resistance at MS level. The spatial distributions of tetracycline, erythromycin and vancomycin resistance levels in E. faecium from Gallus gallus, pigs and cattle are presented for 2007. For countries where 2007 data were not available, 2006 resistance percentages were used, as indicated in footnotes. There were insufficient resistance data available to enable spatial distribution analysis for E. faecalis. 7.1 Fowl (Gallus gallus) In this report, fowl (Gallus gallus) includes breeding flocks, laying hen flocks and broiler flocks of Gallus gallus. Together, seven MSs and one non-ms provided quantitative data on enterococci in Gallus gallus. Tables EN3 and EN4 show the occurrence of resistance to selected antimicrobials among E. faecium and E. faecalis from Gallus gallus. Resistance levels in tested isolates Tetracycline and erythromycin resistance occurred frequently in E. faecium and E. faecalis isolates from Gallus gallus. At reporting MS group level resistance levels to tetracycline and erythromycin among E. faecium were 42% and 34%, respectively, in 2007. Among E. faecalis, resistance levels in the reporting MS group equalled 62% for tetracycline and 38% for erythromycin. A large variation was observed between reporting MSs: in E. faecium, resistance levels to tetracycline varied from 11% in Denmark to 94% in France, and resistance to erythromycin varied from 11% in Sweden to 68% in France and Spain in 2007. Variation among reporting MSs was large also for E. faecalis: from 40% in Denmark to 73% in Austria for tetracycline and from 23% in Denmark to 47% in Austria for erythromycin, in 2007. Ampicillin resistance was detected only in E. faecium and occurrence varied between 1% in Sweden and 23% in Switzerland, in 2007. Ampicillin-resistant E. faecium causing infection in humans is emerging, making it of interest to follow the development of this resistance in isolates from animals. In E. faecalis no resistance to ampicillin was detected by reporting MSs. In 2007, resistance to vancomycin was detected in 1% of the tested E. faecium isolates from Gallus gallus due to 7% of the isolates from Austria and 2% from Denmark. In 2007, 3% of the tested isolates in Switzerland were also vancomycin-resistant. This finding is interesting, as cross-resistance is observed between the important human antimicrobial, vancomycin, and the former growth promoter for animals, avoparcin. Avoparcin was indeed banned from animal use in the EU in 1997 due to causing this cross-resistance to vancomycin. However, many years after the ban, resistance to vancomycin is still detectable. Similarly, the growth promoter avilamycin was phased out in the EU by the end of 2005. In 2007, resistance levels ranging between 0% and 39% were reported in E. faecium and E. faecalis isolates from Gallus gallus (Appendix 5). EFSA Journal 2010; 8(4):1309 169/304 169

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Table EN3. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from Gallus gallus, 2004-2007 Tetracycline Ampicillin Erythromycin Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 22 64 60 53 60 8 22 41 60 32 Denmark 64 11 64 6 64 30 Finland 108 28 108 19 108 12 France 97 94 97 6 97 68 Netherlands 49 47 15 47 49 2 49 49 15 40 Spain 38 74 38 68 Sweden 197 16 197 1 197 11 Total (7 MSs) 22 64 108 28 49 47 471 42 108 19 49 2 418 4 22 41 108 12 49 49 471 34 Switzerland 10 10 30 43 10 20 30 23 10 20 30 40 Streptomycin Vancomycin Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 22 23 60 18 22 5 60 7 Denmark 64 13 64 2 Finland 108 3 France 97 40 97 0 Netherlands 49 100 15 100 49 0 15 0 Spain 38 21 38 0 Sweden 197 1 197 0 Total (7 MSs) 22 23 108 100 49 100 471 18 22 5 108 3 49 0 471 1 Switzerland 30 3 10 10 30 3 170 EFSA Journal 2010; 8(4):1309 170/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN4. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from Gallus gallus, 2004-2007 Tetracycline Ampicillin Erythromycin Country 2004 2005 2006 2007 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 136 82 120 73 120 0 136 28 120 47 Denmark 57 40 57 0 57 23 Finland 239 41 239 0 239 22 Netherlands 64 78 64 0 64 52 Sweden 28 57 28 0 28 29 Total (5 MSs) 136 82 239 41 64 78 205 62 239 0 64 0 205 0 136 28 239 22 64 52 205 38 Switzerland 109 96 216 89 109 0 216 0 109 17 216 15 Streptomycin Vancomycin Country 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 136 16 120 25 136 0 120 0 Denmark 57 4 57 0 Finland 239 2 239 0 Netherlands 64 36 64 0 Sweden 28 0 28 0 Total (5 MSs) 136 16 239 2 64 36 205 16 136 0 239 0 64 0 205 0 Switzerland 109 17 216 22 109 0 216 0 EFSA Journal 2010; 8(4):1309 171/304 171

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Spatial distribution of resistance among Enterococcus faecium The spatial distributions of resistance levels to tetracycline, erythromycin, and vancomycin in E. faecium are displayed in Figures EN1-3. In E. faecium from Gallus gallus, tetracycline and erythromycin resistance had similar spatial distributions, with MSs reporting similar resistance levels for both antimicrobials. Due to scarce MS reporting data, it is difficult to determine particular spatial patterns, although there is a tendency towards lower resistance levels in the north that increase towards the south-west for tetracycline and erythromycin (Figures EN1 and EN2). For vancomycin no clear spatial pattern could be observed at EU level (Figure EN3). Figure EN1. Spatial distribution of tetracycline resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in 2007 172 EFSA Journal 2010; 8(4):1309 172/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN2. Spatial distribution of erythromycin resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in 2007 EFSA Journal 2010; 8(4):1309 173/304 173

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Figure EN3. Spatial distribution of vancomycin resistance among Enterococcus faecium from Gallus gallus in countries reporting quantitative data in 2007 7.2 Pigs Quantitative antimicrobial resistance data in enterococci from pigs reported by six MSs and two non- MSs were included in the analysis. Resistance levels in tested isolates In 2007, the occurrence of tetracycline, erythromycin and streptomycin resistance were high in E. faecium and E. faecalis isolates from pigs. At reporting MS group level, resistance levels in E. faecium were 65% for tetracycline, 48% for erythromycin, and 43% for streptomycin, while for E. faecalis resistance levels were 85% for tetracycline, 41% for erythromycin and 33% for streptomycin (Tables EN5 and EN6). As for Gallus gallus, large variations were observed between reporting countries, e.g. in 2007, Switzerland reported 3% erythromycin resistance in E. faecium, while Spain reported 64%. For streptomycin, Switzerland reported 0% resistance while the Netherlands found 100% strains resistant in 2007. Resistance levels to ampicillin in E. faecium isolates were very low in 2007, between 0% and 2% in the three reporting MSs. No ampicillin resistance was reported in E. faecalis in 2007. In 2007, vancomycin-resistant E. faecium isolates represented 2% of those tested by all reporting MSs. Vancomycin resistance in E. faecalis was not observed in reporting MSs in 2007. However, in 2004, Austria reported 1% vancomycin resistance among E. faecalis isolates from pigs. Avilamycin resistance in E. faecium and E. faecalis from pigs was reported by countries ranging between 0% and 4% of the tested isolates (Appendix 5). 174 EFSA Journal 2010; 8(4):1309 174/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN5. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from pigs, 2004-2007 Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 2004 2006 2007 2006 2007 2004 2006 2007 2004 2006 2007 2004 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 192 18 56 14 56 0 192 4 56 34 192 6 56 2 192 4 56 0 Denmark 153 67 153 1 153 47 153 41 153 2 France 92 77 92 2 92 55 92 42 92 4 Netherlands 35 89 61 84 35 6 35 31 61 36 35 100 61 100 35 0 61 3 Spain 58 72 58 64 58 29 58 2 Total (5 MSs) 192 18 35 89 420 65 35 6 301 1 192 4 35 31 420 48 192 6 35 100 420 43 192 4 35 0 420 2 Norway 67 19 67 1 67 30 67 13 67 0 Switzerland 13 15 29 14 13 15 29 3 13 15 29 3 13 15 29 0 13 0 29 0 Table EN6. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from pigs, 2004-2007 Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 2004 2006 2007 2006 2007 2004 2006 2007 2004 2006 2007 2004 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 144 59 44 70 44 0 144 19 44 41 144 19 44 27 144 1 44 0 Denmark 148 89 148 0 148 41 148 30 148 0 Finland 38 82 38 0 38 24 38 0 Netherlands 22 86 34 91 22 0 22 41 34 59 22 32 34 53 22 0 34 0 Total (4 MSs) 144 59 22 86 264 85 22 0 230 0 144 19 22 41 264 41 144 19 22 32 226 33 144 1 22 0 264 0 Norway 19 79 19 0 19 11 19 21 19 0 Switzerland 26 50 26 73 26 0 26 0 26 19 26 27 26 62 26 23 26 0 26 0 EFSA Journal 2010; 8(4):1309 175/304 175

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Spatial distribution of resistance among Enterococcus faecium The spatial distributions of resistance levels to tetracycline, erythromycin, and vancomycin among E. faecium from pigs are presented in Figures EN4-6. No clear spatial pattern could be observed at EU level. Figure EN4. Spatial distribution of tetracycline resistance among Enterococcus faecium from pigs in countries reporting quantitative data in 2007 176 EFSA Journal 2010; 8(4):1309 176/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN5. Spatial distribution of erythromycin resistance among Enterococcus faecium from pigs in countries reporting quantitative data in 2007 Figure EN6. Spatial distribution of vancomycin resistance among Enterococcus faecium from pigs in countries reporting quantitative data in 2007 EFSA Journal 2010; 8(4):1309 177/304 177

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7.3 Cattle Quantitative antimicrobial resistance data among enterococci from cattle reported by five MSs and one non-ms, mainly in 2007, were included in the analysis. Resistance levels in tested isolates Tetracycline, erythromycin and streptomycin resistance occurred frequently in E. faecium and E. faecalis isolates from cattle (Tables EN7 and EN8). Resistance to tetracycline (31%), erythromycin (34%) and streptomycin (59%) was reported at reporting MS group level in E. faecium isolates in 2007. In E. faecalis isolates, 34% were resistant to tetracycline, 23% to erythromycin and 21% to streptomycin at reporting MS level. As for Gallus gallus and pigs, a large variation was observed between reporting MSs with, e.g., Austria reporting in 0% erythromycin resistance in E. faecium 2004 and the Netherlands reporting 43% in 2007. At reporting MS group level, ampicillin resistance levels among E. faecium from cattle were 3% in 2007 and 4% in 2006. In tested E. faecalis isolates, ampicillin resistance was not detected in reporting MSs in 2006 and 2007, but was detected in 1% of Swiss isolates in 2006. In 2007, vancomycin resistance was reported in 8% of tested E. faecium isolates from Austria and in 1% of isolates from the Netherlands. In addition, vancomycin resistance was reported in 1% of the E. faecalis isolates from Switzerland in 2006. 178 EFSA Journal 2010; 8(4):1309 178/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN7. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from cattle, 2004-2007 Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 2004 2006 2007 2006 2007 2004 2006 2007 2004 2006 2007 2004 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 146 3 50 2 50 0 146 0 50 10 146 0 50 0 146 8 50 8 France 76 26 76 5 76 33 76 18 76 0 Netherlands 147 46 155 39 147 7 147 41 155 43 147 100 155 100 147 1 155 1 Spain 17 59 17 29 17 47 17 0 Sweden 98 3 98 0 98 7 98 0 98 0 Total (5 MSs) 146 3 245 29 298 31 245 4 126 3 146 0 245 27 298 34 146 0 245 60 298 59 146 8 245 0 298 2 Switzerland 179 16 179 2 179 11 179 10 179 0 Table EN8. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from cattle, 2004-2007 Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 2004 2006 2007 2006 2007 2004 2006 2007 2004 2006 2007 2004 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 84 15 37 8 37 0 84 2 37 3 84 2 37 3 84 0 37 0 Netherlands 52 48 50 54 52 0 52 31 50 38 52 37 50 34 52 0 50 0 Sweden 13 15 13 0 13 0 13 0 13 0 Total (3 MSs) 84 15 65 42 87 34 65 0 37 0 84 2 65 25 87 23 84 2 65 29 87 21 84 0 65 0 87 0 Switzerland 199 67 199 1 199 48 199 50 199 1 EFSA Journal 2010; 8(4):1309 179/304 179

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Spatial distribution of resistance among Enterococcus faecium The spatial distributions of resistance levels to tetracycline, erythromycin and vancomycin among E. faecium from cattle are displayed in Figures EN7-9. No clear spatial pattern could be observed at EU level. Figure EN7. Spatial distribution of tetracycline resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2007 1 Note: In this map, countries reporting 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 Sweden and Switzerland, 2006 data were used. 180 EFSA Journal 2010; 8(4):1309 180/304

ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Figure EN8. Spatial distribution of erythromycin resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2007 1 1. For Sweden and Switzerland, 2006 data were used. EFSA Journal 2010; 8(4):1309 181/304 181

7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Figure EN9. Spatial distribution of vancomycin resistance among Enterococcus faecium from cattle in countries reporting quantitative data in 2007 1 1. For Sweden and Switzerland, 2006 data were used. 182 EFSA Journal 2010; 8(4):1309 182/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 8 Antimicrobial resistance in Salmonella and indicator Escherichia coli - qualitative data 8 EFSA Journal 2010; 8(4):1309 183/304 183

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 8 Antimicrobial resistance in Salmonella and indicator E. coli - qualitative data In this chapter qualitative antimicrobial resistance data reported by MSs and non-mss are presented in cases when: 1) data were only reported as qualitative data, or 2) quantitative data were only reported for one out of four years but qualitative data were reported for two or more years. If quantitative data were reported by countries for more than one year the corresponding qualitative data are not included in this analysis. When less than 10 isolates were available for susceptibility testing or less than 10 isolates per year per food/animal category were reported, the data are not included. It is noteworthy that the qualitative data reported by MSs are in most cases not comparable between MSs because different breakpoints or cut-off values for resistance may have been used by MSs. However, within a given MS data should be comparable between years, unless the monitoring schemes were changed or e.g. interpretation of data was changed from clinical breakpoints to epidemiological cut-off values. Due to the characteristics of the qualitative antimicrobial resistance data, it is possible to make an overall description of trends within the MS. However, the resistance percentages between MSs are not necessarily comparable, therefore no overall MS group figures were calculated. 8.1 Antimicrobial resistance among Salmonella isolates from animals and food qualitative data Countries reporting qualitative data on antimicrobial resistance in Salmonella are presented in Tables QSA1-3. These tables cover all countries reporting qualitative data, while in the following analyses only data meeting the criteria described above are included. Table QSA1. Overview of countries reporting qualitative data on tested Salmonella spp. isolates from various sampling origins, 2004-2007 Origin Total number of MSs reporting Meat from broilers 14 Countries MSs: AT, BE, CZ, DE, EE, FR, HU, IT, LV, PL, RO, SI, SK, UK Non-MS: CH Meat from turkeys 3 MSs: DE, IT, SI Meat from bovine animals 13 MSs: AT, BE, CZ, DE, EE, FI, FR, HU, IT, LV, RO, SI, SK Meat from pigs 16 MSs: AT, BE, CZ, DE, DK, EE, ES, FI, FR, HU, IT, LU, LV, RO, SI, SK Gallus gallus 22 MSs: AT, BE, CZ, DE, DK, EE, ES, FI, FR, GR, HU, IT, LU, LV, NL, PL, PT, RO, SE, SI, SK, UK Non-MS: NO Turkeys 17 MSs: AT, BE, CZ, DE, FI, FR, GR, HU, IE, IT, NL, PL, RO, SE, SI, SK, UK Pigs 22 MSs: AT, BE, CZ, DE, DK, EE, ES, FI, FR, GR, HU, IE, IT, LU, LV, NL, PL, RO, SE, SI, SK, UK Non-MS: NO Cattle 21 MSs: AT, BE, CZ, DE, DK, EE, FI, FR, GR, HU, IE, IT, LU, LV, NL, PT, RO, SE, SI, SK, UK Non-MS: NO 184 EFSA Journal 2010; 8(4):1309 184/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA2. Overview of countries reporting qualitative data on tested Salmonella Typhimurium isolates from various sampling origins, 2004-2007 Origin Total number of MSs reporting Meat from broilers 9 MSs: AT, CZ, EE, FR, HU, IT, PL, SI, SK Meat from turkeys 1 MS: SI Meat from bovine animals 7 MSs: CZ, EE, FR, HU, IT, LV, SI Meat from pigs 10 MSs: CZ, DK, EE, FR, HU, IT, LV, RO, SI, SK Countries Gallus gallus 18 MSs: AT, CZ, DE, DK, FI, FR, GR, HU, IT, LV, NL, PL, PT, RO, SE, SI, SK, UK Non-MS: NO Turkeys 9 MSs: AT, CZ, DE, FI, FR, IT, PL, SE, UK Pigs 20 MSs: AT, CZ, DE, DK, EE, ES, FI, FR, GR, HU, IE, IT, LU, NL, PL, RO, SE, SI, SK, UK Non-MS: NO Cattle 19 MSs: AT, CZ, DE, DK, EE, FI, FR, GR, HU, IE, IT, LV, LU, NL, RO, SE, SI, SK, UK Non-MS: NO Table QSA3. Overview of countries reporting qualitative data on tested Salmonella Enteritidis isolates from various sampling origins, 2004-2007 Origin Total number of MSs reporting Countries Meat from broilers 11 MSs: AT, CZ, EE, FR, HU, IT, LV, PL, RO, SI, SK Meat from turkeys 1 MS: SI Meat from bovine animals 5 MSs: EE, FR, HU, IT, SK Meat from pigs 4 MSs: HU, IT, LV, SI Gallus gallus 19 MSs: AT, CZ, DE, EE, ES, FR, GR, HU, IT, LU, LV, NL, PL, PT, RO, SE, SI, SK, UK Non-MS: NO Turkeys 9 MSs: CZ, DE, FI, FR, HU, IT, PL, SI, SK Pigs 16 MSs: AT, CZ, DE, EE, ES, FI, FR, GR, HU, IE, IT, PL, SE, SI, SK, UK Cattle 11 MSs: AT, CZ, DE, EE, FR, GR, HU, IE, IT, SK, UK 8.1.1 Poultry (Gallus gallus) and broiler meat 8.1.1.1 Fowl (Gallus gallus) Resistance levels in tested isolates The occurrence of resistance to selected antimicrobials among tested Salmonella spp., S. Typhimurium and S. Enteritidis isolates from Gallus gallus based on qualitative data are displayed in Tables QSA4-6. Generally, MSs found more often resistance to tetracycline, ampicillin, sulfonamide and nalidixic acid than resistance to gentamicin and ciprofloxacin among the Salmonella isolates. Austria, Belgium and Italy reported qualitative data on both S. Typhimurium and S. Enteritidis from Gallus gallus and within each MS the occurrence of resistance was in most cases lower among S. Enteritidis isolates compared to S. Typhimurium isolates from Gallus gallus. 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(4):1309 185/304 185

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA4a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Belgium 621 15 583 13 392 17 621 6 583 3 392 4 621 24 583 30 392 24 621 5 583 9 Estonia 12 33 11 9 12 0 11 18 12 0 11 46 Germany 11 13 788 5 149 28 175 9 788 2 149 4 175 1 10 12 788 5 149 12 175 6 788 0 149 0 175 0 Italy 584 24 739 18 287 15 582 1 741 3 302 1 583 18 741 12 303 10 Latvia 46 13 25 16 48 0 54 13 25 0 14 0 32 31 15 0 Portugal 17 47 12 50 17 12 17 24 Table QSA4b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Belgium 621 19 583 24 392 18 621 0 583 0 392 0 621 19 583 23 392 17 Estonia 12 0 11 27 12 0 11 9 12 0 11 0 12 67 11 55 Germany 15 17 788 7 149 21 175 7 788 0 149 1 175 0 788 0 149 1 175 0 10 12 788 8 149 21 175 8 Italy 580 15 739 10 293 16 583 2 741 2 304 2 583 0 741 0 302 0 584 26 741 14 304 18 Latvia 10 0 17 0 20 0 18 0 37 0 56 73 25 16 Portugal 12 42 17 35 12 50 17 35 12 50 17 77 186 EFSA Journal 2010; 8(4):1309 186/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA5a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from Gallus gallus, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 50 14 48 6 67 8 13 0 50 6 48 6 67 0 13 0 50 8 48 10 67 5 13 0 Belgium 43 40 43 26 43 42 43 0 Germany 49 59 26 31 15 13 22 9 49 53 26 23 15 13 22 5 49 63 26 27 15 13 22 9 49 0 26 0 15 0 22 0 Greece 10 70 10 70 10 70 Italy 37 24 25 16 14 50 37 8 25 16 14 29 37 14 25 12 13 31 Poland 15 93 12 92 15 87 12 67 15 87 12 67 15 0 United Kingdom 10 60 13 54 10 60 13 46 10 60 13 54 Table QSA5b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from Gallus gallus, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 50 14 48 6 67 9 13 0 50 6 48 2 67 0 13 0 50 0 48 0 67 0 13 0 50 0 48 0 67 0 13 0 Belgium 43 42 43 0 43 7 Germany 49 82 26 35 15 40 22 14 49 0 26 0 15 0 22 0 49 0 26 0 15 0 22 0 49 2 26 4 15 13 22 0 Greece 10 70 10 70 10 70 10 70 Italy 36 22 25 4 13 31 37 3 25 8 14 0 37 0 25 0 13 0 37 5 25 8 14 14 Poland 15 87 12 92 15 0 12 0 15 87 12 67 United Kingdom 10 60 13 54 10 0 13 0 10 0 13 0 10 20 13 23 EFSA Journal 2010; 8(4):1309 187/304 187

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA6a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested S. Enteritidis isolates from Gallus gallus, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 338 1 406 1 183 1 78 0 338 0 406 0 183 0 78 0 338 0 406 3 183 0 78 0 Belgium 144 0 144 0 144 2 144 0 Italy 67 10 100 15 55 4 67 0 100 4 59 0 67 6 100 7 59 3 Latvia 44 14 20 20 46 0 52 14 20 0 13 0 30 33 15 0 Table QSA6b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Enteritidis isolates from Gallus gallus, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria 338 1 406 1 183 1 78 0 338 1 406 0 183 0 78 0 338 0 406 0 183 0 78 0 338 2 406 4 183 1 78 0 Belgium 144 0 144 0 144 2 Italy 66 8 100 9 58 14 67 0 100 0 59 7 67 0 100 0 59 0 67 34 100 12 59 7 Latvia 15 0 19 0 16 0 36 0 52 79 20 15 188 EFSA Journal 2010; 8(4):1309 188/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among tested isolates Figures QSA1-3 display trends in tetracycline, ampicillin and nalidixic acid resistance over time for Salmonella spp. from Gallus gallus. For Belgium, Germany and Italy trends in resistance remained rather stable over time, while in Latvia and Estonia large changes were observed over time. In Latvia, the same number of isolates were not susceptibility tested to each antimicrobial and in Estonia only 11 and 12 isolates were susceptibility tested per year. Both low and varying numbers of susceptibility tested isolates may influence comparability over time. Figures QSA4-6 display trends in resistance over time for S. Typhimurium from Gallus gallus. The figures indicate that in Austria the occurrence of resistance to tetracycline, ampicillin and nalidixic acid was almost unchanged over time, while tetracycline and ampicillin resistance decreased in Germany and increased in Italy. In Poland and the United Kingdom, only two years of data of between 10 and 15 isolates only were available per year, which makes it difficult to describe trends. Temporal trend graphs for S. Enteritidis isolates from Gallus gallus have not been presented due to the very low levels of resistance reported. Figure QSA1. Trends in tetracycline resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Belgium Estonia Germany Italy Latvia Figure QSA2. Trends in ampicillin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Belgium Estonia Germany Italy Latvia EFSA Journal 2010; 8(4):1309 189/304 189

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA3. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Belgium Estonia Germany Italy Latvia Portugal Figure QSA4. Trends in tetracycline resistance in tested S. Typhimurium isolates from Gallus gallus in reporting MSs, 2004-2007, based on qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Poland United Kingdom 190 EFSA Journal 2010; 8(4):1309 190/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA5. Trends in ampicillin resistance in tested S. Typhimurium isolates from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Poland United Kingdom Figure QSA6. Trends in nalidixic acid resistance in tested S. Typhimurium isolates from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Poland United Kingdom 8.1.1.2 Meat from broilers Resistance levels in tested isolates The resistance levels for selected antimicrobials among tested Salmonella spp. and S. Enteritidis isolates from broiler meat based on qualitative data are presented in Tables QSA7a-b and QSA8a-b. Resistance to tetracycline, ampicillin, sulfonamide and nalidixic acid were commonly reported among Salmonella spp. isolates, whereas resistance to gentamicin and ciprofloxacin were generally more seldom found. However, some of the countries reported high ciprofloxacin resistance levels, particularly in 2007. Few countries reported S. Enteritidis susceptibility data before 2007. Austria, Estonia, Hungary, Italy, Poland and Romania reported qualitative data on both Salmonella spp. and S. Enteritidis isolates from broiler meat and within each country. The occurrence of resistance was in general lower among S. Enteritidis isolates compared to Salmonella spp. isolates from broiler meat. EFSA Journal 2010; 8(4):1309 191/304 191

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA7a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from broiler meat, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 148 18 384 19 114 46 55 31 148 3 384 2 114 1 55 0 148 9 384 9 114 6 55 4 Belgium 172 20 44 14 172 12 44 5 172 41 44 32 Cyprus 41 85 41 85 41 85 Czech Republic 24 8 24 0 24 0 Estonia 44 9 13 8 44 0 13 0 44 14 13 8 France 28 39 28 14 28 21 Germany 202 24 148 18 230 20 221 21 202 1 148 1 230 1 221 4 202 22 148 18 230 13 221 24 148 1 230 1 214 1 Greece Hungary 202 84 58 3 202 0 58 2 202 4 58 9 202 1 58 0 Italy 365 29 104 30 365 2 108 0 367 25 108 21 Latvia 11 0 20 40 11 0 20 20 Netherlands 999 1 999 0 999 6 Poland 64 30 64 17 64 20 Romania 53 83 70 39 Slovakia 11 9 24 25 11 0 24 0 11 0 24 8 Slovenia 13 39 10 20 13 15 10 10 13 23 10 10 10 0 United Kingdom 40 8 68 18 40 5 68 0 40 10 68 6 Switzerland 25 64 25 12 25 12 25 0 192 EFSA Journal 2010; 8(4):1309 192/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA7b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin, and nalidixic acid among tested Salmonella spp. isolates from broiler meat, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 148 14 384 15 114 40 55 35 148 0 384 0 114 0 55 0 148 0 384 1 114 0 55 0 148 19 384 28 114 54 55 40 Belgium 172 55 44 34 172 0 44 0 172 27 44 27 Cyprus 41 85 41 27 41 93 41 85 Czech Republic 24 8 24 0 24 4 24 4 Estonia 44 5 13 0 44 0 13 0 44 0 13 0 44 86 13 85 France 28 39 28 0 28 25 Germany 202 31 148 22 230 19 221 23 202 0 148 0 230 0 221 1 202 0 148 0 230 0 221 0 202 16 148 16 230 22 221 32 Greece Hungary 202 0 58 0 58 71 202 90 58 17 Italy 366 34 105 16 366 1 108 0 367 0 108 0 367 32 108 25 Latvia 10 0 15 47 16 25 Netherlands 999 0 999 0 999 5 Poland 64 27 64 2 64 52 Romania 38 40 18 17 31 32 67 97 Slovakia 11 9 24 25 11 0 24 0 11 0 24 42 11 9 24 42 Slovenia 13 31 10 20 13 8 10 0 13 0 10 0 13 23 10 50 United Kingdom 40 8 68 27 40 0 68 0 68 10 40 0 68 13 Switzerland 25 72 25 4 25 88 25 88 EFSA Journal 2010; 8(4):1309 193/304 193

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA8a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested S. Enteritidis isolates from broiler meat, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2005 2006 2007 2005 2006 2007 2005 2006 2007 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 61 0 14 0 34 0 61 0 14 0 34 0 61 5 14 7 34 0 Estonia 21 10 21 0 21 14 Hungary 51 0 51 0 51 2 51 0 Italy 12 0 12 0 12 0 Latvia 20 40 20 20 Poland 13 0 13 0 13 0 Romania 16 6 Table QSA8b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Enteritidis isolates from broiler meat, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2005 2006 2007 2005 2006 2007 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria 61 0 14 0 34 0 61 0 14 0 34 0 61 0 14 0 34 0 61 21 14 29 34 9 Estonia 21 5 21 0 21 0 21 91 Hungary 51 0 51 69 51 16 Italy 12 25 12 0 12 0 12 8 Latvia 20 100 Poland 13 0 13 0 13 46 Romania 16 6 16 6 16 94 194 EFSA Journal 2010; 8(4):1309 194/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among tested isolates Figures QSA7-9 present trends in resistance in tested Salmonella spp. isolates from broiler meat over the study period. Figures indicate that resistance levels to tetracycline, ampicillin, and nalidixic acid were rather stable in some MSs. In 2004 and in 2007, a large number of Salmonella spp. isolates from broiler meat were susceptibility tested in Italy and a decreasing trend was observed for sulfonamide. In Latvia and Hungary, very large changes in resistance in tested isolates were observed from 2006 to 2007, which might indicate that the sampling scheme may have changed over time. Figure QSA7. Trends in tetracycline resistance in tested Salmonella spp. isolates from broiler meat in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Estonia Germany Hungary Italy Latvia Slovakia Slovenia United Kingdom Figure QSA8. Trends in ampicillin resistance in tested Salmonella spp. isolates from broiler meat in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Estonia Germany Hungary Italy Slovakia Slovenia United Kingdom EFSA Journal 2010; 8(4):1309 195/304 195

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA9. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from broiler meat in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Estonia Germany Hungary Italy Latvia Slovakia Slovenia United Kingdom 8.1.2 Turkeys Tables QSA9a-b and QSA10a-b show the occurrence of resistance to selected antimicrobials among Salmonella spp. and S. Typhimurium, respectively, from turkeys based on qualitative data. Resistance to tetracycline, ampicillin, sulfonamide and nalidixic acid were commonly reported, whereas resistance to gentamicin and ciprofloxacin were less often found. 196 EFSA Journal 2010; 8(4):1309 196/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA9a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from turkeys, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 87 8 136 12 126 41 164 66 87 0 136 2 126 0 164 2 87 10 136 7 126 17 164 17 Belgium 18 11 18 11 18 22 Hungary 14 100 Ireland 90 22 90 0 90 7 Germany 117 30 141 65 80 30 117 14 141 5 80 6 117 45 141 44 80 45 117 4 141 0 80 0 Italy 204 77 88 89 139 80 196 84 204 6 88 1 140 6 197 2 204 36 88 59 140 44 196 65 Netherlands 10 10 20 45 10 10 20 0 10 50 20 45 Poland 354 7 96 46 346 5 96 19 354 7 96 39 354 7 Slovakia 22 82 18 56 18 67 80 85 22 82 18 0 18 0 80 10 22 82 18 0 18 22 80 48 United Kingdom 371 53 585 45 300 50 371 19 585 24 300 13 371 26 585 36 300 21 EFSA Journal 2010; 8(4):1309 197/304 197

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA9b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from turkeys, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 87 12 136 4 126 8 164 22 87 15 136 2 126 0 164 6 87 0 136 0 126 0 164 0 87 9 136 2 126 9 164 14 Belgium 18 22 18 0 18 11 Hungary Ireland 90 22 90 0 90 0 90 0 Germany 117 45 141 30 80 43 117 3 141 4 80 9 117 4 141 4 80 0 117 17 141 12 80 34 Italy 204 59 88 9 140 33 196 67 204 3 88 5 140 4 197 2 204 0 88 0 140 0 196 0 204 0 88 82 140 61 197 57 Netherlands 10 50 20 30 10 20 20 10 10 0 20 50 10 40 20 45 Poland 354 7 96 43 354 7 96 13 354 7 354 7 96 50 Slovakia 22 82 18 56 18 67 80 78 22 82 18 0 16 0 80 8 22 82 18 0 18 11 80 20 22 82 18 11 18 11 80 20 United Kingdom 371 56 585 50 300 48 371 0 585 0 300 0 371 0 585 0 300 7 371 18 585 18 300 12 198 EFSA Journal 2010; 8(4):1309 198/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA10a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested S. Typhimurium isolates from turkeys, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 10 30 10 30 10 30 France 10 50 10 50 10 50 Germany 34 94 12 92 13 23 34 91 12 83 13 15 34 94 12 92 13 23 34 0 12 0 13 0 Italy 55 96 68 91 55 16 69 1 55 86 69 96 Poland 14 93 14 93 United Kingdom 37 92 86 76 54 70 37 92 86 77 54 67 37 92 86 83 54 65 Table QSA10b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from turkeys, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 10 0 10 0 10 0 France 10 60 10 10 10 10 Germany 12 92 13 23 34 0 12 0 13 0 34 0 12 0 13 0 34 0 12 0 13 0 Italy 55 96 69 91 55 2 69 0 55 0 69 0 55 82 69 84 Poland 14 0 14 93 United Kingdom 37 95 86 84 54 74 37 0 86 0 54 0 37 0 86 0 54 15 37 84 86 52 54 35 EFSA Journal 2010; 8(4):1309 199/304 199

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among tested isolates Figures QSA10-12 display trends in resistance for tested Salmonella spp. isolates from turkeys over the study period. Figures indicate varying trends: graphs suggest increasing trends for tetracycline in several MSs while no clear trend is apparent for ampicillin and nalidixic acid. Figure QSA10. Trends in tetracycline resistance in tested Salmonella spp. isolates from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Netherlands Poland Slovakia United Kingdom Figure QSA11. Trends in ampicillin resistance in tested Salmonella spp. isolates from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Netherlands Poland Slovakia United Kingdom 200 EFSA Journal 2010; 8(4):1309 200/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA12. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Germany Italy Netherlands Poland Slovakia United Kingdom 8.1.3 Pigs and pig meat 8.1.3.1 Pigs Resistance levels in tested isolates Resistance levels to selected antimicrobials among tested Salmonella spp. and S. Typhimurium isolates from pigs based on qualitative data are set out in Tables QSA11a-b and QSA12a-b. Resistance to tetracycline, ampicillin, chloramphenicol and sulfonamide were commonly reported among Salmonella isolates, whereas resistance to gentamicin, ciprofloxacin and nalidixic acid was less often found. EFSA Journal 2010; 8(4):1309 201/304 201

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA11a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from pigs, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 19 42 24 33 26 50 14 57 19 21 24 13 26 12 14 29 19 26 24 25 26 31 14 57 Belgium 395 60 271 31 256 42 395 40 271 12 256 11 395 54 271 43 256 38 395 1 414 0 271 0 Germany 414 75 457 67 498 73 414 41 457 31 498 29 414 68 457 67 498 70 457 67 498 70 Italy 679 64 328 74 434 68 159 68 679 14 326 19 436 6 158 11 680 36 328 38 436 47 157 64 Ireland 19 84 66 62 66 44 66 52 Luxembourg 21 95 42 17 Netherlands 116 56 205 65 113 57 144 53 116 22 205 34 113 24 144 21 116 38 205 53 113 46 144 42 United Kingdom 715 78 1424 84 1284 88 715 53 1424 56 1284 46 715 70 1424 68 1284 64 Table QSA11b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from pigs, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 19 47 24 33 26 54 14 57 19 0 24 0 26 15 14 0 19 0 24 0 26 0 14 0 19 16 24 0 26 0 14 7 Belgium 395 59 271 42 256 40 395 0 271 0 256 0 395 3 271 4 256 1 Germany 414 75 457 70 498 74 414 4 457 4 498 2 414 0 457 0 498 0 414 3 457 4 498 2 Italy 680 68 330 58 435 49 158 73 679 3 330 9 436 3 159 0 680 0 326 0 436 0 158 0 679 0 279 12 436 7 159 6 Ireland 66 59 66 0 66 3 66 3 Luxembourg 48 2 49 0 Netherlands 116 52 205 59 188 59 144 58 116 0 184 0 113 1 144 1 116 0 205 0 113 2 144 4 116 1 205 0 113 1 144 4 United Kingdom 715 79 1424 79 1284 82 715 1 1424 2 1284 1 715 1 1424 0 1284 1 715 2 1424 3 1284 3 202 EFSA Journal 2010; 8(4):1309 202/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA12a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested S. Typhimurium isolates from pigs, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 14 57 14 29 14 57 Belgium 175 65 175 43 175 59 175 1 Italy 216 81 54 93 79 89 31 84 215 33 54 39 79 15 31 39 216 66 54 74 79 94 29 79 Poland 11 91 17 82 11 91 17 65 11 91 17 77 11 91 Spain 40 90 35 100 19 84 40 25 35 66 19 79 Sweden 15 13 15 7 15 13 United Kingdom 317 81 555 88 889 91 317 58 555 70 889 65 317 78 555 84 889 88 Table QSA12b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from pigs, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria 14 57 14 0 14 0 14 7 Belgium 175 64 175 0 175 2 Italy 216 82 55 82 79 77 31 74 216 1 55 11 79 5 31 0 216 0 54 0 79 0 30 0 216 10 79 5 31 7 Poland 11 91 17 77 11 91 17 0 11 91 11 91 17 59 Spain 40 65 35 77 19 95 40 8 35 3 19 11 40 0 35 3 19 11 40 8 35 3 19 11 Sweden 15 13 15 0 15 0 15 0 United Kingdom 317 84 555 89 889 95 317 1 555 2 889 2 317 1 555 0 889 1 317 2 555 4 889 4 EFSA Journal 2010; 8(4):1309 203/304 203

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among tested isolates Figures QSA13-15 present trends in resistance levels to tetracycline, ampicillin and nalidixic acid over time for tested Salmonella spp. isolates from pigs. Figures indicate that within each MS resistance remains rather stable over time. Figures QSA16-18 display trends in resistance to tetracycline, ampicillin and nalidixic acid for S. Typhimurium from pigs over the study period. In general, high levels of tetracycline and ampicillin resistance, and low levels of nalidixic acid resistance are reported in both Salmonella spp. and S. Typhimurium isolates from pigs in reporting MSs based on qualitative data between 2004 and 2007. Figure QSA13. Trends in tetracycline resistance in tested Salmonella spp. isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy Ireland Netherlands United Kingdom Figure QSA14. Trends in ampicillin resistance in tested Salmonella spp. isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy Netherlands United Kingdom 204 EFSA Journal 2010; 8(4):1309 204/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA15. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy Netherlands United Kingdom Figure QSA16. Trends in tetracycline resistance in tested S. Typhimurium isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland Spain United Kingdom EFSA Journal 2010; 8(4):1309 205/304 205

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA17. Trends in ampicillin resistance in tested S. Typhimurium isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland United Kingdom Figure QSA18. Trends in nalidixic acid resistance in tested S. Typhimurium isolates from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland Spain United Kingdom 8.1.3.2 Meat from pigs Resistance levels in tested isolates Tables QSA13a and QSA13b show the occurrence of resistance to selected antimicrobials among Salmonella spp. from meat from pigs based on qualitative data. Most countries reported qualitative resistance data in 2007 and only Germany and Italy reported data over years. Resistance to tetracycline, ampicillin, chloramphenicol, sulfonamide and nalidixic acid were commonly reported among the Salmonella isolates, whereas resistance to gentamicin and ciprofloxacin were less often found by MSs. 206 EFSA Journal 2010; 8(4):1309 206/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA13a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from meat from pigs, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Hungary 57 90 57 81 57 88 57 0 Germany 568 49 176 55 128 67 568 15 176 19 128 16 568 33 176 45 128 63 176 1 117 1 Italy 415 57 349 57 253 63 322 69 415 16 349 16 253 12 324 9 416 37 349 35 253 40 324 41 416 0 Latvia 22 32 22 23 Netherlands 999 0 999 0 999 0 Slovakia 10 50 10 0 10 60 Spain 22 59 22 55 22 32 Table QSA13b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from meat from pigs, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Hungary 57 11 57 53 57 88 Germany 568 45 176 52 128 64 568 0 176 0 128 0 568 0 176 0 128 0 568 5 176 2 128 2 Italy 416 64 347 52 251 54 324 59 415 2 349 2 253 1 324 3 416 0 349 0 253 1 324 5 416 6 349 12 253 10 324 7 Latvia 22 23 Netherlands 999 0 999 0 999 0 Slovakia 10 20 10 20 10 0 10 0 Spain 22 14 22 0 22 0 EFSA Journal 2010; 8(4):1309 207/304 207

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 8.1.4 Cattle and bovine meat 8.1.4.1 Cattle Resistance levels in tested isolates Resistance to selected antimicrobials among tested Salmonella spp. and S. Typhimurium isolates from cattle based on qualitative data are presented in Tables QSA14a-b and QSA15a-b. Most countries reported qualitative data in 2006. Resistance to tetracycline, ampicillin, chloramphenicol and sulfonamide were commonly reported among the Salmonella isolates, whereas resistance to nalidixic acid was less often detected. Only few MSs reported resistance to gentamicin or ciprofloxacin. 208 EFSA Journal 2010; 8(4):1309 208/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA14a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from cattle, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 14 57 26 46 14 21 14 43 26 46 14 21 14 43 26 12 14 21 Belgium 120 46 28 36 52 27 120 53 28 43 52 39 120 50 28 39 52 29 120 0 28 0 Germany 278 46 338 37 304 30 278 41 338 22 304 13 278 47 338 33 304 31 278 0 338 0 304 0 Italy 126 74 97 92 121 85 31 52 126 66 45 53 121 68 31 26 126 65 97 78 121 78 31 45 Greece 11 36 11 55 11 36 Ireland 616 51 236 10 206 12 307 19 Table QSA14b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from cattle, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria 14 43 26 46 14 21 14 0 26 0 14 0 14 0 26 0 14 0 14 0 26 46 14 0 Belgium 120 67 28 54 52 54 120 0 28 0 52 2 120 16 28 21 52 25 Germany 338 39 304 30 278 0 338 0 304 0 278 0 338 0 304 0 278 3 338 0 304 3 Italy 125 68 96 82 121 65 30 57 380 126 1 1 121 0 31 7 124 0 97 0 121 0 31 7 126 0 97 21 121 10 31 7 Greece 11 55 11 0 11 0 11 0 Ireland 299 2 EFSA Journal 2010; 8(4):1309 209/304 209

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA15a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested S. Typhimurium isolates from cattle, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2004 2005 2006 2004 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Belgium 31 71 31 65 31 84 31 0 Ireland 10 50 16 19 23 83 Italy 82 92 35 100 49 92 82 70 35 60 49 84 82 89 35 89 49 94 Netherlands 12 58 40 40 12 33 40 23 12 75 40 45 Slovakia 10 80 10 80 10 80 Table QSA15b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from cattle, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2004 2005 2006 2004 2005 2006 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Belgium 31 90 31 0 31 19 Ireland Italy 81 90 35 83 49 69 82 1 35 0 49 0 81 0 35 0 49 0 82 6 35 26 49 10 Netherlands 12 75 80 35 10 0 40 0 12 0 40 3 12 8 40 3 Slovakia 10 80 10 80 10 80 10 80 210 EFSA Journal 2010; 8(4):1309 210/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among tested isolates Figures QSA19-21 present trends in resistance to tetracycline, ampicillin, and nalidixic acid over time for tested Salmonella spp. isolates from cattle. Figure QSA19. Trends in tetracycline resistance in tested Salmonella spp. isolates from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy Ireland Figure QSA20. Trends in ampicillin resistance in tested Salmonella spp. isolates from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy EFSA Journal 2010; 8(4):1309 211/304 211

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QSA21. Trends in nalidixic acid resistance in tested Salmonella spp. isolates from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Austria Belgium Germany Italy 8.1.4.2 Meat from bovine animals Resistance levels in tested isolates Resistance to selected antimicrobials among tested Salmonella spp. isolates from bovine meat based on qualitative data are presented in Tables QSA16a-b. Only five countries provided qualitative data from this source and only Germany and Italy provided data over years. Resistance to tetracycline, ampicillin, chloramphenicol, sulfonamide and nalidixic acid were often reported. Only few MSs reported resistance to gentamicin or ciprofloxacin. 212 EFSA Journal 2010; 8(4):1309 212/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QSA16a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among tested Salmonella spp. isolates from meat from bovine animals, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Estonia 10 0 10 0 10 0 Germany 149 49.0 32 63.0 28 43.0 11 9.0 64 21.0 32 13.0 28 36.0 11 9.0 142 47.0 32 59.0 28 36.0 11 9.0 32 0 28 0 10 0 Italy 60 55.0 34 61.8 37 45.9 40 45.0 95 60.0 15 9.1 37 5.4 40 0 40 0 33 27.3 37 27.0 40 22.5 Netherlands 999 0.2 999 0.1 999 0 Slovakia 14 28.6 14 0 14 0 Table QSA16b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from meat from bovine animals, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Estonia 10 0 10 0 10 0 10 20.0 Germany 178 59.0 32 59.0 28 36.0 11 18.0 32 0 28 0 11 0 32 0 28 0 11 0 32 3.0 28 0 11 27.0 Italy 60 43.0 33 30.3 37 37.8 40 32.5 60 0 34 5.9 37 8.1 40 0 60 0 33 0 37 0 40 0 60 22.0 34 23.5 37 16.2 40 5.0 Netherlands 999 0 999 0 999 0 Slovakia 14 28.6 14 0 14 28.6 14 28.6 EFSA Journal 2010; 8(4):1309 213/304 213

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 8.2 Antimicrobial resistance among indicator Escherichia coli isolates from animals qualitative data Table QEC1 presents all the countries reporting qualitative data on antimicrobial resistance in indicator E. coli. These tables cover all countries reporting qualitative data, while in the following analyses only data meeting the criteria described at the beginning of this chapter are included. Table QEC1. Overview of countries reporting qualitative data on indicator Escherichia coli from various sampling origins, 2004-2007 Origin Total number of MSs reporting Meat from broilers 4 MSs: BE, FR, LV, PT Non-MS: NO Meat from turkeys 1 MS: FR Countries Meat from bovine animals 6 MSs: BE, DE, ES, LV, PT, SI Non-MS: NO Meat from pigs 4 MSs: BE, DE, FR, LV Gallus gallus 19 MSs: AT, DE, DK, EE, ES, FI, FR, GR, HU, IE, IT, LV, NL, PL, PT, SE, SI, SK, UK Non-MSs: CH, NO Pigs 19 MSs: AT, DE, DK, EE, ES, FI, FR, GR, HU, IE, IT, LV, NL, PL, PT, SE, SI, SK, UK Non-MSs: CH, NO Cattle 19 MSs: AT, DE, DK, EE, ES, FI, FR, GR, HU, IE, IT, LV, NL, PL, PT, SE, SI, SK, UK Non-MS: NO Turkeys 10 MSs: AT, DE, GR, HU, IE, IT, PL, PT, SI, UK Non-MS: NO 8.2.1 Poultry: Fowl (Gallus gallus) Tables QEC2 a-b show the occurrence of resistance to selected antimicrobials among indicator E. coli from Gallus gallus, based on qualitative data. Resistance levels among Escherichia coli Among the E. coli isolates from Gallus gallus, resistance to tetracycline, chloramphenicol, ampicillin, gentamicin, ciprofloxacin and nalidixic acid were often reported by most countries (Tables QEC2a and QEC2b). For some countries a large variation in the occurrence of resistance was reported between the years. 214 EFSA Journal 2010; 8(4):1309 214/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QEC2a. Resistance (%) to tetracycline, chloramphenicol and ampicillin among isolates of indicator Escherichia coli from Gallus gallus, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Country 2004 2005 2006 2007 2004 2005 2006 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Greece 52 98 20 65 15 40 52 98 12 42 Ireland 1,652 5 33 82 39 77 826 7 Latvia 13 15 13 31 13 69 Portugal 32 19 51 88 13 85 32 19 20 50 13 8 51 80 13 39 Slovakia 401 87 401 99 Table QEC2b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from Gallus gallus, 2004-2007, qualitative data Country Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid 2005 2004 2005 2006 2004 2005 2006 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Greece 14 57 10 10 Ireland Latvia 13 92 13 46 Portugal 32 19 24 29 13 23 32 19 20 60 13 31 32 72 51 71 13 39 Slovakia 390 58 EFSA Journal 2010; 8(4):1309 215/304 215

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among Escherichia coli Only a few countries reported data for two or more years. Therefore, graphs showing trends in resistance over time based on qualitative data were only possible for a few antimicrobials (Figures QEC1-2). Figure QEC1. Trends in tetracycline resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Greece Ireland Portugal Figure QEC2. Trends in ampicillin resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Greece Portugal 216 EFSA Journal 2010; 8(4):1309 216/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 8.2.2 Turkeys Resistance levels among Escherichia coli Overall, qualitative data reported by six MSs and one non-ms were included in the analysis. Compared to Gallus gallus more qualitative data on antimicrobial resistance are available in commensal E. coli from turkeys (Tables QEC3a-b). Particularly, resistance to tetracycline was very commonly reported in E. coli isolates from turkeys. Also ampicillin, sulfonamide and nalidixic acid resistance was often detected, whereas resistance to gentamicin and ciprofloxacin were less frequently found. Only one MS reported resistance to ceftiofur. In Italy, an increasing trend in tetracycline and ampicillin resistance was observed, while nalidixic acid resistance seemed to decrease. The reported occurrence of tetracycline, ampicillin and nalidixic acid resistance from Poland, in 2004, varied considerably compared to 2005-2007, it is therefore difficult to make conclusions about antimicrobial resistance trends in Poland. In the United Kingdom, tetracycline resistance remained constant while ampicillin resistance increased (Figures QEC3-5). EFSA Journal 2010; 8(4):1309 217/304 217

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QEC3a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among isolates of indicator Escherichia coli from turkeys, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 11 64 11 18 11 18 11 0 Hungary 96 70 93 37 96 63 94 1 Italy 73 90 53 96 138 93 43 100 73 21 53 32 138 22 43 30 73 69 138 70 43 93 Poland 52 89 24 46 116 50 72 64 52 87 24 4 116 13 73 10 52 89 116 52 73 48 Slovenia 11 64 11 18 11 27 11 0 United Kingdom 17 65 36 72 18 67 17 29 36 53 18 56 13 0 Norway 53 13 53 2 53 15 53 0 Table QEC3b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from turkeys, 2004-2007, qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Turkeys Austria 11 27 11 0 11 9 11 9 Hungary 95 60 96 2 102 0 102 0 Italy 43 84 73 7 53 4 138 3 43 14 43 61 73 56 53 51 138 44 43 58 Poland 52 89 24 42 113 19 73 43 52 87 24 8 116 2 73 6 52 89 20 0 52 89 24 13 116 35 72 50 Slovenia 11 18 11 9 11 9 11 46 United Kingdom Norway 53 6 53 0 53 2 53 2 218 EFSA Journal 2010; 8(4):1309 218/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among Escherichia coli Figure QEC3. Trends in tetracycline resistance in indicator Escherichia coli from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland United Kingdom Figure QEC4. Trends in ampicillin resistance in indicator Escherichia coli from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland United Kingdom EFSA Journal 2010; 8(4):1309 219/304 219

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QEC5. Trends in nalidixic acid resistance in indicator Escherichia coli from turkeys in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Italy Poland 8.2.3 Pigs Four countries reported antimicrobial resistance in E. coli from pigs only as qualitative data (Table QEC4). Resistance to tetracycline, ampicillin, gentamicin and nalidixic acid was often reported. Figures QEC6-7 indicate that trends are rather constant over time except in Ireland where an extremely high increase in tetracycline resistance was observed from 2004 to 2006-2007, which might indicate that the samples tested in 2004 and in 2006-2007 were not comparable. 220 EFSA Journal 2010; 8(4):1309 220/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QEC4. Resistance (%) to tetracycline, chloramphenicol, ampicillin, ceftiofur, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from pigs, 2004-2007, qualitative data Country Tetracycline Chloramphenicol Ampicillin Ceftiofur Gentamicin 2004 2005 2006 2007 2004 2004 2005 2006 2007 2005 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Ireland 1,298 6 63 92 70 89 649 9 Latvia 39 64 39 8 39 90 11 82 39 77 13 39 Portugal 11 73 11 9 United Kingdom 263 80 305 75 231 78 263 49 304 45 231 46 125 0 Ciprofloxacin Nalidixic acid Country 2004 2005 2004 2005 2006 N % Res N % Res N % Res N % Res N % Res Pigs Ireland Latvia 39 95 10 0 39 62 10 50 Portugal 11 27 United Kingdom EFSA Journal 2010; 8(4):1309 221/304 221

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QEC6. Trends in tetracycline resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Ireland United Kingdom Figure QEC7. Trends in ampicillin resistance in indicator Escherichia coli from pigs in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Latvia United Kingdom 8.2.4 Cattle Resistance levels among Escherichia coli The occurrence of resistance among E. coli from cattle based on qualitative data is shown in Tables QEC5a-b. Resistance to tetracycline, chloramphenicol, ampicillin, gentamicin and nalidixic acid were commonly reported by countries. 222 EFSA Journal 2010; 8(4):1309 222/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Table QEC5a. Resistance (%) to tetracycline, chloramphenicol, ampicillin and ceftiofur among isolates of indicator Escherichia coli from cattle, 2004-2007, qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 2004 2005 2006 2007 2004 2005 2006 2007 2004 2005 2006 2007 2005 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Greece 50 70 85 98 50 96 85 100 Ireland 59,206 6 3,302 79 3,178 75 430 84 29,603 6 Latvia 20 40 20 40 20 80 Portugal 43 2 18 89 12 67 17 35 43 2 13 23 18 61 17 41 Slovakia 96 49 42 86 17 0 United Kingdom 3,106 56 2,260 74 1,921 75 590 42 1,651 43 3,106 53 2,260 70 1,921 71 Table QEC5b. Resistance (%) to gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from cattle, 2004-2007, qualitative data Gentamicin Ciprofloxacin Nalidixic acid Country 2004 2005 2006 2007 2004 2005 2004 2005 2006 2007 N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Greece 50 86 85 48 49 49 85 88 Ireland Latvia 20 90 10 20 20 80 10 0 20 40 12 8 Portugal 18 6 16 50 43 2 13 31 13 39 12 42 Slovakia 15 53 United Kingdom 590 2 1,652 2 EFSA Journal 2010; 8(4):1309 223/304 223

8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Temporal trends in resistance among Escherichia coli Figures QEC8-10 display trends in resistance to tetracycline, gentamicin and nalidixic acid in indicator Escherichia coli from cattle. Data from the United Kingdom indicate an increase in tetracycline resistance while gentamicin resistance remained unchanged. For the other reporting countries, considerable changes in resistance were observed over time e.g. in Portugal, tetracycline resistance increased from 2% in 2004 to 89% in 2005, as well in Ireland from 6% in 2004 to 79% and 75% in 2006 and 2007, respectively. Considerable changes in resistance over one or two years may indicate that samples were not comparable over time, which make it difficult to determine trends over the period. Figure QEC8. Trends in tetracycline resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Greece Ireland Portugal United Kingdom Figure QEC9. Trends in gentamicin resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Greece Latvia Portugal United Kingdom 224 EFSA Journal 2010; 8(4):1309 224/304

ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Figure QEC10. Trends in nalidixic acid resistance in indicator Escherichia coli from cattle in reporting MSs, 2004-2007, qualitative data 100 80 % resistant isolates 60 40 20 0 2004 2005 2006 2007 Greece Latvia Portugal EFSA Journal 2010; 8(4):1309 225/304 225

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GENERAL DISCUSSION 9 General discussion of the most interesting findings from the descriptive analyses 9 EFSA Journal 2010; 8(4):1309 227/304 227

9. GENERAL DISCUSSION 9. General discussion Directive 2003/99/EC obliges MSs to monitor and report antimicrobial resistance in Salmonella and Campylobacter isolates from animals and food, whereas the monitoring and reporting of resistance data from indicator organisms (commensal E. coli and enterococci) is voluntary. Directive 2003/99/EC foresees that the monitoring of antimicrobial resistance is based on the surveillance systems in place in MSs which may differ in terms of origin of the isolates and laboratory testing of isolates. Antimicrobial resistance data from the years 2004 to 2007 reported by MSs and analysed in the framework of this report were therefore presumably not fully harmonised as regards the origin of tested isolates, nevertheless a major endeavour was made in order to harmonise results from different laboratory methods. The reporting system foresees both the reporting of qualitative and quantitative data. Therefore, both types of data were included in this report. The number of MSs reporting quantitative data on antimicrobial resistance in isolates from animals and food increased from 18 in 2004 to 21 in 2006 and 20 in 2007. This progress is promising and will provide valuable information for further analysis of trends in antimicrobial resistance in food-producing animals in the EU. In this report quantitative antimicrobial resistance data reported by the EU MSs and non-mss deriving from different testing methods (MIC and inhibition zone diameter data) were for the first time interpreted using same epidemiological cut-off values across the reporting countries and years. This means that within a reporting country, data were more comparable over the years and data were more comparable between different countries. In addition, using similar epidemiological cut-off values enabled the comparison of MIC and inhibition zone data. However, it should be kept in mind that as the monitoring of antimicrobial resistance was not harmonised across EU MSs in the years 2004-2007, the differences in sampling schemes applied still had an impact on the MS results. Thus, the differences observed between the reporting countries may be partly due to real differences in the resistance situation but sometimes also because of differences in the monitoring system in place. Furthermore, in the case of Salmonella, different serovar distributions in MSs may influence the results, because some serovars are known to be more resistant. Generally, by using epidemiological cut-off values, high levels of resistance to different antimicrobial agents were observed in MSs and the two reporting non-mss among the bacterial isolates tested from poultry, pigs and cattle. This could be the result of a common use of these antimicrobials in veterinary medicine for treatment of the animal species. In the following, Figures D1-5 display and summarise resistance levels for the most relevant antimicrobials tested for different animal/food categories at reporting MS group level in 2007, based on reported quantitative data. The differences between the set of MSs reporting may influence the comparability of results. 9.1 Antimicrobial resistance in Salmonella and Campylobacter Campylobacter and Salmonella are the two leading causes of food-borne infections in the EU (EFSA, 2009). Antimicrobial-resistant Salmonella and Campylobacter from animals and food are therefore of public health significance. Resistance to antimicrobials commonly used to treat salmonellosis and campylobacteriosis cases in humans can compromise effective treatment. Some resistant Salmonella and Campylobacter strains have been reported to be the cause of worse patient outcomes (Varma et al., 2005a; Engberg et al., 2004), longer hospitalisations (Varma et al., 2005b) and increased mortality (Helms et al., 2002). Salmonella Based on reported data, the occurrence of antimicrobial resistance to ampicillin, sulfonamide, tetracycline and chloramphenicol in the S. Enteritidis and Salmonella spp. isolates tested from Gallus gallus were low compared to the Salmonella spp. and S. Typhimurium isolates tested from pigs and cattle. However, ciprofloxacin and nalidixic acid resistance were higher in S. Enteritidis and Salmonella spp. tested isolates from Gallus gallus compared to pigs and cattle. In this report Salmonella spp. represents the overall occurrence of antimicrobial resistance in Salmonella from the different animal species or food categories investigated. It is known that antimicrobial resistance varies among Salmonella serovars, and some serovars, such as S. Typhimurium, 228 EFSA Journal 2010; 8(4):1309 228/304

GENERAL DISCUSSION 9. are more often found resistant. However, these resistant serovars consist of a number of phagetypes of which some are resistant, while others are susceptible to most antimicrobials. Some of the observed differences in antimicrobial resistance in Salmonella spp. may be due to differences in serotype and phage type distributions between countries, years and animal species. Moreover, it was only possible to analyse data reported by MSs and therefore differences in the ways of reporting between MSs may also have contributed to overall differences. In animal populations, selective pressure caused by the use of antimicrobials, as well as clonal spreading of Salmonella strains, may also impact the selection and diffusion of resistant clones. In all cases, however, resistance among Salmonella spp. gives a picture of the general exposure to humans that the presence of resistant Salmonella in animal and food may cause. The high occurrence of ciprofloxacin and nalidixic acid resistance reported in Salmonella isolates from Gallus gallus and turkeys as compared to pigs and cattle might reflect that fluoroquinolones are more extensively used to treat infections among these poultry species. Fluoroquinolones are identified by WHO as critically important antimicrobials in human medicine (WHO, 2007), and an increase in the number of fluoroquinolone-resistant Salmonella isolates in animals might compromise the effective treatment of infections in humans caused by Salmonella originating from the animal reservoir. The results of the comparison of antimicrobial resistance among Salmonella spp. from Gallus gallus and turkeys in 2007 at reporting MS group level show that the occurrence of resistance to most antimicrobials was significantly higher in isolates from turkeys compared to those from Gallus gallus. When comparing sources of resistance results in turkey isolates of Salmonella spp., data from the 2006-2007 baseline survey displayed lower levels of antimicrobial resistance compared to those derived from data submitted under the scope of Directive 2003/99/EC in 2007 for almost all antimicrobials. This is most likely due to different sets of MSs reporting baseline survey data and annual monitoring data. Sampling schemes to collect isolates may also have been different in the baseline survey and routine monitoring. For Salmonella spp. isolates from cattle, a decrease in resistance to ampicillin, chloramphenicol, sulfonamide and tetracycline was observed over time in several reporting countries. This might reflect a decrease in the prevalence of penta-resistant S. Typhimurium DT 104, as this phage type is likely to contribute substantially to the occurrence of resistance in Salmonella spp. in cattle. The reported occurrence of resistance to ceftiofur, a third generation cephalosporin, in Salmonella spp.- tested isolates was low, even though some MSs reported moderate resistance levels. Some third generation cephalosporins, such as ceftiofur, are used in veterinary medicine. Third generation cephalosporins are also one of the critically important antimicrobials in human medicine according to WHO (2007). Third generation cephalosporin-resistant bacteria, especially if, in addition, they produce extended spectrum beta-lactamases (ESBLs), are considered to be a public health threat. In this report, antimicrobial resistance in Salmonella isolates from animals and food was compared at country level. However, there are factors that can have a large impact on such a comparison. Previous data have shown that the occurrence of resistance varies between countries. Samples from animals are often collected from domestically raised animals while large proportions of the food consumed might be imported and also slaughter animals might derive from other countries. This can result in large differences between the reported occurrence of resistance in isolates from food and animals at country level. When comparing antimicrobial resistance among Salmonella spp. from Gallus gallus and meat from broilers at country level, significant differences were observed. Gallus gallus consists of both laying hen and broiler production, including both breeding and production animals, while meat from broilers is assumed to originate mainly from broilers. This might explain some of the significant differences observed between resistance levels in isolates from Gallus gallus and broiler meat. The occurrence of resistance in Salmonella spp. isolates from pigs and pig meat were quite similar in many countries, whereas significant differences were observed in some other reporting countries. EFSA Journal 2010; 8(4):1309 229/304 229

9. GENERAL DISCUSSION Figure D1. Resistance levels to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide ciprofloxacin, nalidixic acid, ceftiofur and cefotaxime in Salmonella spp., S. Enteritidis and S. Typhimurium from Gallus gallus and broiler meat at reporting MS group level in 2007 100 90 % resistance at reporting MS 80 70 60 50 40 30 20 10 0 Salmonella spp. from Gallus gallus in 13 MSs, 2007 Salmonella Enteritidis from Gallus gallus in 9 MSs, 2007 Salmonella Typhimurium from Gallus gallus in 8 MSs, 2007 Salmonella spp. from broiler meat in 5 MSs, 2007 tetracycline ampicillin chloramphenicol gentamicin sulfonamide ciprofloxacin nalidixic acid ceftiofur cefotaxime Figure D2. Resistance levels to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide, ciprofloxacin, nalidixic acid, ceftiofur and cefotaxime in Salmonella spp. from Gallus gallus, turkeys, pigs and cattle at reporting MS group level in 2007 100 % resistance at reporting MS 90 80 70 60 50 40 30 20 10 0 Salmonella spp. from Gallus gallus in 13 MSs, 2007 Salmonella spp. in turkeys in 8 MSs, 2007 Salmonella spp. from fattening turkeys baseline survey in 8 Mss, 2006-2007 Salmonella spp. from pigs in 13 MSs, 2007 Salmonella spp. from slaughter pigs baseline survey in 8 MSs, 2006-2007 Salmonella spp. from cattle in 10 MSs, 2007 tetracycline ampicillin chloramphenicol gentamicin sulfonamide ciprofloxacin 1 nalidixic acid ceftiofur cefotaxime 1. Ciprofloxacin was not analysed in baseline survey isolates of Salmonella. 230 EFSA Journal 2010; 8(4):1309 230/304

GENERAL DISCUSSION 9. Campylobacter Overall, the 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. In C. jejuni isolates from Gallus gallus, the occurrence of tetracycline and ciprofloxacin resistance varied widely among reporting countries. Most countries reported more than 60% tetracycline resistance among C. coli isolates from pigs from 2004 to 2007, except Sweden and Denmark where occurrence was below 10%. Fluoroquinolones and macrolides are regarded as critically important antimicrobials in human medicine by WHO (2007). Fluoroquinolone resistance was commonly reported among C. jejuni and C. coli isolates from animals and food in several countries. Several countries reported low to moderate levels of resistance to macrolides among C. jejuni isolates and only a few countries reported resistance levels above 10%. Macrolide resistance was more frequently observed among C. coli isolates where also high resistance levels were found. The high occurrence of fluoroquinolone resistance observed in several countries, added to the occurrence of macrolide resistance, may compromise the effective treatment of infections in humans caused by Campylobacter originating from the animal reservoir in these countries. In this report, antimicrobial resistance in Campylobacter isolates from animals and food at country level was compared. The comparisons were possible for C. jejuni and C. coli isolates from Gallus gallus and broiler meat, and, with a few exceptions, no significant differences were observed at country level despite that the reported level of resistance varied between countries. This suggests that resistance observed in Campylobacter isolates from animals is indicative of consumer exposure to raw broiler meat. Eggs are not an important source of human Campylobacter infections and therefore it is often only broiler production that is included in Campylobacter surveillance programmes. This makes Campylobacter samples from Gallus gallus and meat from broilers more comparable and might explain why very few significant differences in resistance were observed between these two sources. Figure D3. Resistance levels to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid in Campylobacter jejuni and Campylobacter coli from fowl, turkeys, pigs and cattle at reporting MS group level in 2007 100 90 80 % resistance at reporting MS 70 60 50 40 30 20 10 0 C. jejuni from Gallus gallus in 9 MSs, 2007 C. coli from Gallus gallus in 5 MSs, 2007 C. jejuni from broiler meat in 5 MSs, 2007 C. coli from C. coli from pigs broiler meat in 6 MSs, 2007 in 3 MSs, 2007 C. jejuni from cattle in 2 MSs, 2007 C. coli from cattle in 6 MSs, 2007 tetracycline erythromycin gentamicin ciprofloxacin nalidixic acid EFSA Journal 2010; 8(4):1309 231/304 231

9. GENERAL DISCUSSION 9.2 Indicator organisms, Escherichia coli and enterococci The monitoring of antimicrobial resistance in commensal bacteria isolated from randomly selected healthy animals or food can provide valuable data on the pool of resistance determinants present in bacteria of animal origin. Commensal bacteria from the intestine of farm animals (Enterococcus spp., E. coli) are considered as a potential source of resistance genes that can spread horizontally to zoonotic and other bacteria through the food chain (Neidhardt et al., 1996; Winokur et al., 2001; Wang et al., 2006), and are considered good indicators of the selective pressure exerted by the use of antimicrobials on intestinal populations of bacteria in food animals. The monitoring of resistance frequencies among different animal species and different production types within the same species (e.g. dairy cattle, beef cattle, veal calves) allows for the comparison of the effects of selective pressure and is a useful early alert system tool for tracking emerging resistance in livestock and possible spread to animal-derived food. Indicator Escherichia coli Generally, reported resistance levels to commonly used antimicrobials were higher in E. coli isolates from pigs than in isolates from Gallus gallus and cattle, particularly for tetracycline. In E. coli isolates from Gallus gallus and pigs, large variations in reported resistance rates were observed between reporting countries, in particular in 2007 for tetracycline, ampicillin and sulfonamide. In the case of both Gallus gallus and pig isolates, the same countries tended to report high resistance rates to several antimicrobials. In cattle, the occurrence of resistance in E. coli was lower compared to isolates from Gallus gallus and pigs, and variation in resistance rates between countries was also much smaller. Differences in resistance between countries might reflect differences in the consumption of antimicrobials in animals among countries, although the dissemination of certain E. coli types within animal populations might also contribute to differences in the occurrence of resistance, observed between countries. Several countries reported resistance levels over 40% for nalidixic acid and ciprofloxacin in E. coli isolates from Gallus gallus, which is higher than in isolates from cattle and pigs. These differences are in line with the findings in Salmonella isolates where the highest occurrence of quinolone and fluoroquinolone resistance was reported in isolates from Gallus gallus. It may be because fluoroquinolones are more often used to treat diseases among Gallus gallus. Fluoroquinolones are critically important antimicrobials in human medicine and an increase in fluoroquinolone-resistant E. coli isolates in animals may indicate a general resistance trend of concern among gram-negative bacteria originating from the animal reservoir. Reported resistance levels to third generation cephalosporins were generally low among E. coli isolates, even though some countries recorded moderate resistance levels. 232 EFSA Journal 2010; 8(4):1309 232/304

GENERAL DISCUSSION 9. Figure D4. Resistance levels to tetracycline, ampicillin, chloramphenicol, gentamicin, sulfonamide, ciprofloxacin, nalidixic acid, ceftiofur and cefotaxime in indicator E. coli from Gallus gallus, pigs and cattle at reporting MS group level in 2007 100 90 80 % resistance at reporting MS 70 60 50 40 30 20 10 0 Indicator E. coli from Gallus gallus in 7 MSs, 2007 Indicator E. coli from pigs in 10 MSs, 2007 Indicator E. coli from cattle in 8 MSs, 2007 tetracycline ampicillin chloramphenicol gentamicin sulfonamide ciprofloxacin nalidixic acid ceftiofur cefotaxime Enterococcus faecium and Enterococcus faecalis (indicator bacteria) The occurrence of antimicrobial resistance to tetracycline, erythromycin and streptomycin in commensal enterococci was common in isolates from fowl, pigs and cattle (Figure D5). The growth promoter avoparcin was banned in the EU in 1997 due to concerns regarding crossresistance to vancomycin, a critically important antibiotic in the treatment of human infections with resistant gram-positive bacteria according to WHO (2007). However, in 2007, vancomycin resistance was still reported in E. faecium and E. faecalis isolates from Gallus gallus, pigs and cattle in the EU, though at low levels. These findings show that after banning an antimicrobial for animal usage, the resistance genes may still remain in the bacterial population for years. In this report ampicillin-resistant E. faecium was reported in Gallus gallus, pigs and cattle from almost all reporting countries. As ampicillin-resistant E. faecium infections in humans are emerging (Lester et al., 2008; Top et al., 2008), it seems advisable to follow the development of this resistance in animal isolates. EFSA Journal 2010; 8(4):1309 233/304 233

9. GENERAL DISCUSSION Figure D5. Resistance levels to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin in indicator Enterococcus faecium and Enterococcus faecalis from fowl, pigs and cattle at reporting MS group level in 2007 100 90 % resistance at reporting MS 80 70 60 50 40 30 20 10 0 E. faecium from Gallus gallus in 6 MSs, 2007 E. faecalis Gallus gallus in 3 MSs, 2007 E. faecium from pigs in 5 MSs, 2007 E. faecalis from pigs in 4 MSs, 2007 E. faecium from cattle in 4 MSs, 2007 E. faecalis from cattle in 2 MSs, 2007 tetracycline ampicillin erythromycin streptomycin vancomycin 234 EFSA Journal 2010; 8(4):1309 234/304

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10. REFERENCES 10. References Aarestrup FM, Wegener HC and Collignon P, 2008. Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Review of Anti-Infective Therapy; 6(5):733-50. Armitage P and Berry G, 2001. Statistical Methods in Medical Research, 4th ed. 2001, Oxford: Blackwell Scientific Publications. CLSI (Clinical and Laboratory Standards Institute), 2008. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard-Third ed. [ISBN Number 1-56238-659-X]. CLSI Document M31-A3. Clinical and Laboratory Standards Institute, Wayne, PA, USA. Collignon P, Powers JH, Chiller TM, Aidara-Kane A and Aarestrup FM, 2009. World Health Organization Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies for the Use of Antimicrobials in Food Production Animals. Clinical Infectious Diseases; 49(1):132-41. EFSA, 2007. Report of the Task Force of Zoonoses Data Collection including a proposal for a harmonized 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. EFSA, 2008a. Report from the Task Force on Zoonoses Data Collection including guidance for harmonized monitoring and reporting of antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. from food animals. The EFSA Journal (2008) 141, 1-44. EFSA, 2008b. Scientific Opinion of the Panel on Biological Hazards on a request from the European Food Safety Authority on foodborne antimicrobial resistance as a biological hazard. The EFSA Journal (2008) 765, 1-87. EFSA, 2009. The Community Summary Report on Trends and Sources of Zoonoses and Zoonotic Agents in the European Union in 2007, The EFSA Journal (2009), 223, 1-310. Engberg J, Neimann J, Nielsen EM, Aarestrup FM and Fussing V, 2004. Quinolone-resistant Campylobacter infections: risk factors and clinical consequences. Emerging Infectious Diseases; 10(6):1056-63. EUCAST (European Committee on Antimicrobial Susceptibility Testing), definitions. Available at http://www.srga.org/eucastwt/eucastdefinitions.htm Helms M, Vastrup P, Gerner-Smidt P and Molbak K, 2002. Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerging Infectious Diseases; 8(5):490-5. Kahlmeter G, Brown DF, Goldstein FW, MacGowan AP, Mouton JW, Osterlund A, Rodloff A, Steinbakk M, Urbaskova P and Vatopoulos A, 2003. European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. Journal of Antimicrobial Chemotherapy; 52(2):145-8. Lester CH, Sandvang D, Olsen SS, Schønheyder HC, Jarløv JO, Bangsborg J, Hansen DS, Jensen TG, Frimodt-Møller N, Hammerum AM, 2008. Emergence of ampicillin-resistant Enterococcus faecium in Danish hospitals. Journal of Antimicrobial Chemotherapy; 62(6):1203-6. NCCLS (National Committee for Clinical Laboratory Standards), 2001. Performance Standards for Antimicrobial Susceptibility Testing: Eleventh Informational Supplement. NCCLS document M100-S11 [ISBN 1-56238-426-0]. Neidhardt, FC (Ed. in Chief), Curtiss R., Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M and Umbarger HE (eds). 1996. Escherichia coli and Salmonella: Cellular and Molecular Biology. American Society for Microbiology Press. 2 vols. p. 2898. Top J, Willems R, van der Velden S, Asbroek M and Bonten M, 2008. Emergence of clonal complex 17 Enterococcus faecium in The Netherlands. Journal of Clinical Microbiology; 46(1):214-9. 236 EFSA Journal 2010; 8(4):1309 236/304

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APPENDICES Appendices EFSA Journal 2010; 8(4):1309 239/304 239