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

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

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4 THE COMMUNITY SUMMARY REPORT 1 Antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 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 EFSA Journal 2010; 8(4):1309. [304 pp.]. doi: /j.efsa Available online: EFSA Journal 2010; 8(4):1309 3/304 3

5 European Food Safety Authority 2010 ISBN: doi: /j.efsa 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

6 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 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 , 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 Parma ITALY Tel Fax zoonoses@efsa.europa.eu EFSA Journal 2010; 8(4):1309 5/304 5

7 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 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 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 Key words Antimicrobial resistance, food, animals, Salmonella, Campylobacter, Escherichia coli, enterococco. 6 EFSA Journal 2010; 8(4):1309 6/304

8 TABLE OF CONTENTS Summary Introduction Scientific background Legal framework Epidemiological cut-off values Main findings Main conclusions of the report Agent specific summaries Materials and methods The antimicrobial susceptibility data available Data reported under Directive 2003/99/EC from 2004 to Data reported from the EU-wide Salmonella baseline surveys Antimicrobials for susceptibility testing Antimicrobials for susceptibility testing of Salmonella Antimicrobials for susceptibility testing of Campylobacter Antimicrobials for susceptibility testing of Escherichia coli Antimicrobials for susceptibility testing of enterococci MIC and inhibition zone diameter interpretation Data description and analysis Antimicrobial resistance in Salmonella - quantitative data Poultry (Gallus gallus) and broiler meat Fowl (Gallus gallus) Meat from broilers (Gallus gallus) Turkeys Resistance data from the baseline survey on the prevalence of Salmonella in turkey flocks in the EU Pigs and pig meat Pigs Meat from pigs Resistance data from the baseline survey on the prevalence of Salmonella in slaughter pigs in the EU Cattle and bovine meat Cattle (bovine animals) Meat from bovine animals Comparison of antimicrobial resistance among Salmonella isolates from food and animals within and between MSs Antimicrobial resistance in Campylobacter - quantitative data Poultry (Gallus gallus) and broiler meat Fowl (Gallus gallus) Meat from broilers Pigs Cattle Comparison of antimicrobial resistance among Campylobacter jejuni and Campylobacter coli from food and animals within and between MSs EFSA Journal 2010; 8(4):1309 7/304 7

9 TABLE OF CONTENTS 6. Antimicrobial resistance in indicator Escherichia coli - quantitative data Poultry : Fowl (Gallus gallus) Pigs Cattle Antimicrobial resistance in indicator enterococci - quantitative data Poultry: Fowl (Gallus gallus) Pigs Cattle Antimicrobial resistance in Salmonella and indicator Escherichia coli - qualitative data Antimicrobial resistance among Salmonella isolates from animals and food - qualitative data Poultry (Gallus gallus) and broiler meat Fowl (Gallus gallus) Meat from broilers Turkeys Pigs and pig meat Pigs Meat from pigs Cattle and bovine meat Cattle Meat from bovine animals Antimicrobial resistance among indicator Escherichia coli isolates from animals - qualitative data Poultry: Fowl (Gallus gallus) Turkeys Pigs Cattle General discussions of the most interesting findings from the descriptive analyses Antimicrobial resistance in Salmonella and Campylobacter Indicator organisms, Escherichia coli and enterococci References Appendices Appendix 1. List of abbreviations, Member States and other reporting countries, Definitions Appendix 2. MIC distributions of Salmonella Appendix 3. MIC distributions of Campylobacter Appendix 4. MIC distributions of indicator Escherichia coli Appendix 5. MIC distributions of indicator enterococci Appendix 6. Setting the epidemiological cut-off values for inhibition zone diameters (disk diffusion) EFSA Journal 2010; 8(4):1309 8/304

10 INTRODUCTION 1 Introduction 1 9

11 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 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, , p EFSA Journal 2010; 8(4): /304

12 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 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, , p. 26. EFSA Journal 2010; 8(4): /304 11

13 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): /304

14 MAIN FINDINGS 2 Main findings 2 13

15 2. MAIN FINDINGS 2.1 Main conclusions on the Community Summary Report on antimicrobial resistance 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 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 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): /304

16 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 This progress is promising and will provide valuable information for further analyses of antimicrobial resistance trends in the EU. EFSA Journal 2010; 8(4): /304 15

17 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 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 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): /304

18 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 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 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): /304 17

19 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 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 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 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 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 and the reported MS group cefotaxime resistance level was 4% in 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 , 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): /304

20 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 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 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): /304 19

21 20 EFSA Journal 2010; 8(4): /304

22 MATERIALS AND METHODS 3 Materials and methods 3 21

23 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 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, Data included in the report Quantitative data Isolates tested by: Qualitative data MIC Disk diffusion Salmonella 128,184 19, ,712 Campylobacter 52, Indicator E. coli 149,061 28, ,363 Indicator enterococci 28, 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): /304

24 MATERIALS AND METHODS 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 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) 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): /304 23

25 3. MATERIALS AND METHODS 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): /304

26 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): /304 25

27 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): /304

28 MATERIALS AND METHODS 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): /304 27

29 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): /304

30 MATERIALS AND METHODS 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): /304 29

31 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 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): /304

32 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: 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): /304 31

33 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< EFSA Journal 2010; 8(4): /304

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

35 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 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, 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): /304

36 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, 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, 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): /304 35

37 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.1 Poultry (Gallus gallus) and broiler meat 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 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 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 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 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 SA EFSA Journal 2010; 8(4): /304

38 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, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Czech Republic Denmark Estonia Finland France Greece Hungary Italy Lithuania Netherlands Poland Romania Slovakia Slovenia Spain Sweden United Kingdom Total (18 MSs) , , , , EFSA Journal 2010; 8(4): /304 37

39 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, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Czech Republic Denmark Estonia Finland France Greece Hungary Italy Lithuania 12 0 Netherlands Poland Romania Slovakia Slovenia Spain Sweden United Kingdom Total (18 MSs) , EFSA Journal 2010; 8(4): /304

40 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, , 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 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 Czech Republic Denmark Estonia Finland France Greece Hungary Italy Lithuania Netherlands Poland Romania Slovakia Slovenia Spain Sweden United Kingdom Total (18 MSs) , , 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): /304 39

41 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, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Estonia France Germany Greece Hungary Lithuania Netherlands Poland Romania Slovakia Slovenia Spain United Kingdom Total (14 MSs) EFSA Journal 2010; 8(4): /304

42 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, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Estonia France 48 0 Germany Greece Hungary Lithuania 12 0 Netherlands Poland Romania Slovakia Slovenia Spain United Kingdom Total (14 MSs) EFSA Journal 2010; 8(4): /304 41

43 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, , 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 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 Estonia France Germany Greece Hungary Lithuania Netherlands Poland Romania Slovakia Slovenia Spain United Kingdom Total (14 MSs) EFSA Journal 2010; 8(4): /304

44 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, , using harmonised epidemiological cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 France Germany Italy Netherlands Poland Slovakia Spain Sweden Total (9 MSs) Ceftiofur Cefotaxime Sulfonamide Country 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 France Germany Italy Netherlands Poland Slovakia Spain Sweden Total (9 MSs) EFSA Journal 2010; 8(4): /304 43

45 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, , 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 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 France Germany Italy Netherlands Poland Slovakia Spain Sweden Total (9 MSs) EFSA Journal 2010; 8(4): /304

46 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304 45

47 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA3. Trends in ampicillin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , quantitative data % resistant isolates Austria Czech Republic Denmark 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, , quantitative data % resistant isolates 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): /304

48 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA5. Trends in ciprofloxacin resistance in Salmonella spp. from Gallus gallus in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304 47

49 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Germany Netherlands Poland Slovakia 48 EFSA Journal 2010; 8(4): /304

50 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 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): /304 49

51 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 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): /304

52 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 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 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 Most of the data derive from 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): /304 51

53 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, , 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 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 Czech Republic Estonia France Hungary Romania Slovakia Slovenia Total (8 MSs) Switzerland EFSA Journal 2010; 8(4): /304

54 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, , 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 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 Czech Republic Estonia France Hungary Romania Slovakia Slovenia Total (8 MSs) Switzerland 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): /304 53

55 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 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 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): /304

56 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, , 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 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 France Greece Ireland Italy Poland Slovakia Slovenia Total (8 MSs) EFSA Journal 2010; 8(4): /304 55

57 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, , 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 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 France Greece Ireland Italy Poland Slovakia Slovenia Total (8 MSs) 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): /304

58 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 SA 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 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): /304 57

59 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 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): /304

60 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 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 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 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): /304 59

61 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, 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): /304

62 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): /304 61

63 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 Czech Republic 13 2Italy Lithuania 2 1Netherlands Poland Slovakia 3 1Slovenia 1 2 5United Kingdom S. Zanzibar 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 EFSA Journal 2010; 8(4): /304

64 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): /304 63

65 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, , 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 Cyprus Czech Republic Italy Lithuania Netherlands Poland United Kingdom Spain Total (9 MSs) 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): /304

66 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, 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): /304 65

67 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, 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 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 (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): /304

68 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Estonia Finland France Greece Hungary Ireland Italy Netherlands Poland Romania Slovakia Slovenia Spain Sweden Total (16 MSs) , , , EFSA Journal 2010; 8(4): /304 67

69 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Denmark , Estonia Finland France Greece Hungary Ireland Italy Netherlands Poland Romania Slovakia Slovenia Spain Sweden Total (16 MSs) , , EFSA Journal 2010; 8(4): /304

70 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Estonia Finland France Greece Hungary Ireland Italy Netherlands Poland Romania Slovakia Slovenia Spain Sweden Total (16 MSs) , , ,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): /304 69

71 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Finland France Germany Ireland Netherlands Poland Slovakia Spain Sweden United Kingdom Total (12 MSs) , , , , , , EFSA Journal 2010; 8(4): /304

72 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Denmark , Finland France Germany Ireland Netherlands Poland Slovakia Spain Sweden United Kingdom Total (12 MSs) , , , , EFSA Journal 2010; 8(4): /304 71

73 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Finland France Germany Ireland Netherlands Poland Slovakia Spain Sweden United Kingdom Total (12 MSs) , , , , , ,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): /304

74 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 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304 73

75 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA17. Trends in ampicillin resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304

76 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA19. Trends in ciprofloxacin resistance in Salmonella spp. from pigs in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304 75

77 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 SA 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 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): /304

78 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): /304 77

79 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): /304

80 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 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 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 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): /304 79

81 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark France Italy Romania Slovenia Total (6 MSs) , , , Ceftiofur Cefotaxime Sulfonamide Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium Denmark France Italy Romania Slovenia Total (6 MSs) , EFSA Journal 2010; 8(4): /304

82 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark France Italy Romania Slovenia Total (6 MSs) , ,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): /304 81

83 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark France Germany Italy Total (5 MSs) Ceftiofur Cefotaxime Sulfonamide Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from pigs Belgium Denmark France Germany Italy Total (5 MSs) EFSA Journal 2010; 8(4): /304

84 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, , using harmonised cut-off values in countries reporting quantitative data. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark France Germany Italy Total (5 MSs) EFSA Journal 2010; 8(4): /304 83

85 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 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 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, 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): /304

86 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): /304 85

87 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): /304

88 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 Cyprus Czech Republic Denmark 50 Estonia 5 1 2Latvia Lithuania Netherlands Poland 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): /304 87

89 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): /304

90 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Table SABS4. Resistance (%) to selected antimicrobials among Salmonella spp. from slaughter pigs sampled by the baseline survey, , 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 Cyprus Czech Republic Denmark Lithuania Latvia Netherlands Poland Spain Total (9 MSs) Table SABS5. Resistance (%) to selected antimicrobials among Salmonella Typhimurium from slaughter pigs sampled by the baseline survey, , 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 Czech Republic Denmark Netherlands Poland Spain Total (6 MSs) 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): /304 89

91 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, 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): /304

92 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, 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): /304 91

93 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4.4 Cattle and bovine meat 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 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 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): /304

94 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Estonia Finland France Italy Netherlands Romania Slovakia Spain Sweden Total (11 MSs) EFSA Journal 2010; 8(4): /304 93

95 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Denmark Estonia Finland France Italy Netherlands Romania Slovakia Spain Sweden Total (11 MSs) EFSA Journal 2010; 8(4): /304

96 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Estonia Finland France Italy Netherlands Romania Slovakia Spain Sweden Total (11 MSs) 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): /304 95

97 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Finland France Germany Netherlands United Kingdom Total (6 MSs) Ceftiofur Cefotaxime Sulfonamide Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Denmark Finland France Germany Netherlands United Kingdom Total (6 MSs) EFSA Journal 2010; 8(4): /304

98 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Finland France Germany Netherlands United Kingdom Total (6 MSs) EFSA Journal 2010; 8(4): /304 97

99 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304

100 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 4. Figure SA26. Trends in ampicillin resistance in Salmonella spp. from cattle in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates 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): /304 99

101 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Figure SA28. Trends in nalidixic acid resistance in Salmonella spp. from cattle in the reporting MSs, , quantitative data % resistant isolates 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): /304

102 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 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 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): /

103 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 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): /304

104 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 , 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 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): /

105 4. ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA Table SA15. Resistance (%) to selected antimicrobials among Salmonella spp. isolates from meat from bovine animals, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Ceftiofur Cefotaxime Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Belgium France Italy Total (3 MSs) Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from bovine animals Belgium France Italy Total (3 MSs) 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): /304

106 ANTIMICROBIAL RESISTANCE IN SALMONELLA - QUANTITATIVE DATA 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): /

107 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 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 Chloramphenicol Florfenicol Ampicillin Ceftiofur 0 1 Sulfonamide Apramycin Gentamicin Neomycin 0 10 Spectinomycin Streptomycin Ciprofloxacin Nalidixic acid Number of isolates 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): /304

108 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 Chloramphenicol Florfenicol Ampicillin Ceftiofur 0 0 Cefpodoxime 0 0 Sulfonamide Apramycin 1 1 Gentamicin Neomycin 8 10 Spectinomycin Streptomycin Ciprofloxacin Nalidixic acid Number of isolates EFSA Journal 2010; 8(4): /

109 108 EFSA Journal 2010; 8(4): /304

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

111 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 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, 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): /304

112 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Poultry (Gallus gallus) and broiler meat 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 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 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 , 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): /

113 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA2. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from Gallus gallus, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 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 Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden Total (11 MSs) Norway Switzerland EFSA Journal 2010; 8(4): /304

114 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, , using harmonised cut-off values Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria Czech Republic Denmark Finland France Germany Italy Netherlands Slovenia Spain Sweden 94 5 Total (11 MSs) Norway Switzerland EFSA Journal 2010; 8(4): /

115 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA3. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from Gallus gallus, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria France Germany Italy Netherlands Slovenia Spain Total (7 MSs) Switzerland Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria France Germany Italy Netherlands Slovenia Spain Total (7 MSs) Switzerland EFSA Journal 2010; 8(4): /304

116 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, , quantitative data 100 % resistant isolates 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, , quantitative data % resistant isolates Czech Republic Germany Norway Denmark Finland France Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(4): /

117 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA3. Trends in gentamicin resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates 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, , quantitative data % resistant isolates Czech Republic Denmark France Germany Italy Netherlands Spain Switzerland 116 EFSA Journal 2010; 8(4): /304

118 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA5. Trends in nalidixic acid resistance in Campylobacter jejuni from Gallus gallus in reporting MSs, , quantitative data 100 % resistant isolates 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 (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, , quantitative data % resistant isolates France Italy Netherlands Spain EFSA Journal 2010; 8(4): /

119 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Figure CA7. Trends in erythromycin resistance in Campylobacter coli from Gallus gallus in reporting MSs, , quantitative data % resistant isolates France Italy Netherlands Spain Figure CA8. Trends in gentamicin resistance in Campylobacter coli from Gallus gallus in reporting MSs, , quantitative data % resistant isolates France Italy Netherlands Spain 118 EFSA Journal 2010; 8(4): /304

120 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA9. Trends in ciprofloxacin resistance in Campylobacter coli from Gallus gallus in reporting MSs, , quantitative data % resistant isolates France Italy Netherlands Spain Figure CA10. Trends in nalidixic acid resistance in Campylobacter coli from Gallus gallus in reporting MSs, , quantitative data % resistant isolates France Italy Netherlands Spain EFSA Journal 2010; 8(4): /

121 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 CA 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 For Slovenia, 2006 data were used. 120 EFSA Journal 2010; 8(4): /304

122 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 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 For Slovenia, 2006 data were used. EFSA Journal 2010; 8(4): /

123 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 For Slovenia, 2006 data were used 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): /304

124 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, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 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 Belgium Denmark France Germany Total (5 MSs) Norway Switzerland Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria Belgium Denmark France Germany Total (5 MSs) Norway Switzerland EFSA Journal 2010; 8(4): /

125 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, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria Belgium France Total (3 MSs) Switzerland EFSA Journal 2010; 8(4): /304

126 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 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 ( ) 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 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 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 At reporting MS group level, gentamicin resistance varied between 4% to 8% of tested isolates during the years EFSA Journal 2010; 8(4): /

127 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA6. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from pigs, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 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 Denmark France Germany Italy Netherlands Spain Sweden Total (8 MSs) Switzerland Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Pigs Austria Denmark France Germany Italy Netherlands Spain Sweden Total (8 MSs) Switzerland EFSA Journal 2010; 8(4): /304

128 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, , quantitative data % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland Figure CA16. Trends in erythromycin resistance in Campylobacter coli from pigs in reporting MSs, , quantitative data % resistant isolates Austria Denmark France Germany Italy Netherlands Spain Switzerland EFSA Journal 2010; 8(4): /

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

130 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA19. Trends in nalidixic acid resistance in Campylobacter coli from pigs in reporting MSs, , quantitative data % resistant isolates 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 CA 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): /

131 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 EFSA Journal 2010; 8(4): /304

132 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 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 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): /

133 5. ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA Table CA7. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter jejuni from cattle, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 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 Denmark Italy Netherlands Spain Sweden Total (6 MSs) Switzerland Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria Denmark Italy Netherlands Spain Sweden 68 9 Total (6 MSs) Switzerland EFSA Journal 2010; 8(4): /304

134 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Table CA8. Resistance (%) to tetracycline, erythromycin, gentamicin, ciprofloxacin and nalidixic acid among Campylobacter coli from cattle, , using harmonised cut-off values Tetracycline Erythromycin Gentamicin Country 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 Denmark Netherlands Spain Total (4 MSs) Switzerland Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria Denmark Netherlands Spain Total (4 MSs) Switzerland EFSA Journal 2010; 8(4): /

135 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, , quantitative data % resistant isolates Austria Denmark Italy Netherland Figure CA24. Trends in erythromycin resistance in Campylobacter jejuni from cattle in reporting MSs, , quantitative data % resistant isolates Austria Denmark Italy Netherland 134 EFSA Journal 2010; 8(4): /304

136 ANTIMICROBIAL RESISTANCE IN CAMPYLOBACTER - QUANTITATIVE DATA 5. Figure CA25. Trends in ciprofloxacin resistance in Campylobacter jejuni from cattle in reporting MSs, , quantitative data % resistant isolates Austria Denmark Italy Netherland Figure CA26. Trends in nalidixic acid resistance in Campylobacter jejuni from cattle in reporting MSs, , quantitative data % resistant isolates 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): /

137 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 Chloramphenicol Erythromycin Gentamicin Streptomycin Ciprofloxacin Nalidixic acid Number of isolates 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 Chloramphenicol Erythromycin Gentamicin Streptomycin Ciprofloxacin Nalidixic acid Number of isolates EFSA Journal 2010; 8(4): /304

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

139 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 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, 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): /304

140 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 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 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 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 , Spain reported 18% to 24% in 2004 to 2006, while Italy found 11% resistance in 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): /

141 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, , using harmonised cut-off values, Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Estonia Finland France Greece Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (14 MSs) , , , , , Norway Switzerland EFSA Journal 2010; 8(4): /304

142 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country N % N % N % N % N % N % N % N % N % N % N % N % Gallus gallus Austria Denmark Estonia 21 5 Finland France Greece Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (14 MSs) , , Norway Switzerland EFSA Journal 2010; 8(4): /

143 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Estonia 21 5 Finland France Greece Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (14 MSs) , , , Norway Switzerland EFSA Journal 2010; 8(4): /304

144 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark France Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland EFSA Journal 2010; 8(4): /

145 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland 144 EFSA Journal 2010; 8(4): /304

146 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark France Germany Hungary Italy Netherlands Poland Spain Sweden Norway Switzerland EFSA Journal 2010; 8(4): /

147 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 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): /304

148 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 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): /

149 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 (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 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 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): /304

150 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovakia Slovenia Spain Sweden Total (14 MSs) 1, , , , , , , , , , , Norway Switzerland EFSA Journal 2010; 8(4): /

151 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country 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 Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovakia 67 0 Slovenia Spain Sweden Total (14 MSs) , , , , Norway Switzerland EFSA Journal 2010; 8(4): /304

152 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovakia Slovenia Spain Sweden Total (14 MSs) 1, , , , , , ,215 7 Norway Switzerland EFSA Journal 2010; 8(4): /

153 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, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Spain Norway Switzerland 152 EFSA Journal 2010; 8(4): /304

154 ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC11. Trends in ampicillin resistance in indicator Escherichia coli from pigs in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark Estonia Finland Hungary Italy Netherlands Poland Spain Norway Switzerland EFSA Journal 2010; 8(4): /

155 6. ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - QUANTITATIVE DATA Figure EC13. Trends in gentamicin resistance in indicator Escherichia coli from pigs in reporting MSs, , quantitative data % resistant isolates 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, , quantitative data % resistant isolates Austria Denmark Estonia Finland France Hungary Italy Netherlands Poland Spain Norway Switzerland 154 EFSA Journal 2010; 8(4): /304

156 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 EC Between 9 and 13 countries reported quantitative resistance data to the selected antimicrobials in 2006 and/or 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 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): /

157 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 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): /304

158 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 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): /

159 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, , using harmonised cut-off values, Values in bold were obtained by disk diffusion method Tetracycline Chloramphenicol Ampicillin Country 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 Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (13 MSs) 1, , , , , , , , , , , Norway Switzerland EFSA Journal 2010; 8(4): /304

160 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Ceftiofur Cefotaxime Sulfonamide Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Austria Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (13 MSs) , , , Norway Switzerland EFSA Journal 2010; 8(4): /

161 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, , using harmonised cut-off values. Values in bold were obtained by disk diffusion method Gentamicin Ciprofloxacin Nalidixic acid Country 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 Denmark Estonia Finland France Germany Hungary Italy Netherlands Poland Slovenia Spain Sweden Total (13 MSs) , , , , ,138 4 Norway Switzerland EFSA Journal 2010; 8(4): /304

162 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, , quantitative data % resistant isolates Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia Figure EC18. Trends in chloramphenicol resistance in indicator Escherichia coli from cattle in reporting MSs, , quantitative data % resistant isolates Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia EFSA Journal 2010; 8(4): /

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

164 ANTIMICROBIAL RESISTANCE IN INDICATOR ESCHERICHIA COLI - 6. QUANTITATIVE DATA Figure EC21. Trends in gentamicin resistance in indicator Escherichia coli from cattle in reporting MSs, , quantitative data % resistant isolates Austria Denmark Estonia France Netherlands Figure EC22. Trends in nalidixic acid resistance in indicator Escherichia coli from cattle in reporting MSs, , quantitative data % resistant isolates Austria Denmark Estonia France Hungary Italy Netherlands Poland Slovenia EFSA Journal 2010; 8(4): /

165 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 EC 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 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): /304

166 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 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): /

167 166 EFSA Journal 2010; 8(4): /304

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

169 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, 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, 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): /304

170 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 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 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 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 Ampicillin resistance was detected only in E. faecium and occurrence varied between 1% in Sweden and 23% in Switzerland, in 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 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): /

171 7. ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA Table EN3. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from Gallus gallus, Tetracycline Ampicillin Erythromycin Country 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 Denmark Finland France Netherlands Spain Sweden Total (7 MSs) Switzerland Streptomycin Vancomycin Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria Denmark Finland France Netherlands Spain Sweden Total (7 MSs) Switzerland EFSA Journal 2010; 8(4): /304

172 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN4. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from Gallus gallus, Tetracycline Ampicillin Erythromycin Country 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 Denmark Finland Netherlands Sweden Total (5 MSs) Switzerland Streptomycin Vancomycin Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Austria Denmark Finland Netherlands Sweden Total (5 MSs) Switzerland EFSA Journal 2010; 8(4): /

173 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 EFSA Journal 2010; 8(4): /304

174 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): /

175 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 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 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 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 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): /304

176 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN5. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from pigs, Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 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 Denmark France Netherlands Spain Total (5 MSs) Norway Switzerland Table EN6. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from pigs, Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 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 Denmark Finland Netherlands Total (4 MSs) Norway Switzerland EFSA Journal 2010; 8(4): /

177 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 EFSA Journal 2010; 8(4): /304

178 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): /

179 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 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 At reporting MS group level, ampicillin resistance levels among E. faecium from cattle were 3% in 2007 and 4% in 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 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 EFSA Journal 2010; 8(4): /304

180 ANTIMICROBIAL RESISTANCE IN INDICATOR ENTEROCOCCI - QUANTITATIVE DATA 7. Table EN7. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecium from cattle, Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 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 France Netherlands Spain Sweden Total (5 MSs) Switzerland Table EN8. Resistance (%) to tetracycline, ampicillin, erythromycin, streptomycin and vancomycin among Enterococcus faecalis from cattle, Tetracycline Ampicillin Erythromycin Streptomycin Vancomycin Country 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 Netherlands Sweden Total (3 MSs) Switzerland EFSA Journal 2010; 8(4): /

181 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 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): /304

182 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 For Sweden and Switzerland, 2006 data were used. EFSA Journal 2010; 8(4): /

183 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 For Sweden and Switzerland, 2006 data were used. 182 EFSA Journal 2010; 8(4): /304

184 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): /

185 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, 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): /304

186 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, 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, 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 Poultry (Gallus gallus) and broiler meat 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): /

187 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Estonia Germany Italy Latvia Portugal Table QSA4b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from Gallus gallus, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Estonia Germany Italy Latvia Portugal EFSA Journal 2010; 8(4): /304

188 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Germany Greece Italy Poland United Kingdom Table QSA5b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from Gallus gallus, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Germany Greece Italy Poland United Kingdom EFSA Journal 2010; 8(4): /

189 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Italy Latvia Table QSA6b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Enteritidis isolates from Gallus gallus, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Italy Latvia EFSA Journal 2010; 8(4): /304

190 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, , qualitative data % resistant isolates Belgium Estonia Germany Italy Latvia Figure QSA2. Trends in ampicillin resistance in tested Salmonella spp. isolates from Gallus gallus in reporting MSs, , qualitative data % resistant isolates Belgium Estonia Germany Italy Latvia EFSA Journal 2010; 8(4): /

191 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, , qualitative data % resistant isolates Belgium Estonia Germany Italy Latvia Portugal Figure QSA4. Trends in tetracycline resistance in tested S. Typhimurium isolates from Gallus gallus in reporting MSs, , based on qualitative data % resistant isolates Austria Germany Italy Poland United Kingdom 190 EFSA Journal 2010; 8(4): /304

192 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, , qualitative data % resistant isolates Austria Germany Italy Poland United Kingdom Figure QSA6. Trends in nalidixic acid resistance in tested S. Typhimurium isolates from Gallus gallus in reporting MSs, , qualitative data % resistant isolates Austria Germany Italy Poland United Kingdom 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 Few countries reported S. Enteritidis susceptibility data before 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): /

193 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Cyprus Czech Republic Estonia France Germany Greece Hungary Italy Latvia Netherlands Poland Romania Slovakia Slovenia United Kingdom Switzerland EFSA Journal 2010; 8(4): /304

194 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, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Cyprus Czech Republic Estonia France Germany Greece Hungary Italy Latvia Netherlands Poland Romania Slovakia Slovenia United Kingdom Switzerland EFSA Journal 2010; 8(4): /

195 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Meat from broilers Austria Estonia Hungary Italy Latvia Poland Romania 16 6 Table QSA8b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Enteritidis isolates from broiler meat, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Estonia Hungary Italy Latvia Poland Romania EFSA Journal 2010; 8(4): /304

196 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, , qualitative data % resistant isolates 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, , qualitative data % resistant isolates Austria Belgium Estonia Germany Hungary Italy Slovakia Slovenia United Kingdom EFSA Journal 2010; 8(4): /

197 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, , qualitative data % resistant isolates Austria Belgium Estonia Germany Hungary Italy Latvia Slovakia Slovenia United Kingdom 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): /304

198 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Hungary Ireland Germany Italy Netherlands Poland Slovakia United Kingdom EFSA Journal 2010; 8(4): /

199 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, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Hungary Ireland Germany Italy Netherlands Poland Slovakia United Kingdom EFSA Journal 2010; 8(4): /304

200 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 France Germany Italy Poland United Kingdom Table QSA10b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from turkeys, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 France Germany Italy Poland United Kingdom EFSA Journal 2010; 8(4): /

201 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, , qualitative data % resistant isolates Austria Germany Italy Netherlands Poland Slovakia United Kingdom Figure QSA11. Trends in ampicillin resistance in tested Salmonella spp. isolates from turkeys in reporting MSs, , qualitative data % resistant isolates Austria Germany Italy Netherlands Poland Slovakia United Kingdom 200 EFSA Journal 2010; 8(4): /304

202 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, , qualitative data % resistant isolates Austria Germany Italy Netherlands Poland Slovakia United Kingdom Pigs and pig meat 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): /

203 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Germany Italy Ireland Luxembourg Netherlands United Kingdom Table QSA11b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from pigs, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Germany Italy Ireland Luxembourg Netherlands United Kingdom EFSA Journal 2010; 8(4): /304

204 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Italy Poland Spain Sweden United Kingdom Table QSA12b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from pigs, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Italy Poland Spain Sweden United Kingdom EFSA Journal 2010; 8(4): /

205 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 Figure QSA13. Trends in tetracycline resistance in tested Salmonella spp. isolates from pigs in reporting MSs, , qualitative data % resistant isolates Austria Belgium Germany Italy Ireland Netherlands United Kingdom Figure QSA14. Trends in ampicillin resistance in tested Salmonella spp. isolates from pigs in reporting MSs, , qualitative data % resistant isolates Austria Belgium Germany Italy Netherlands United Kingdom 204 EFSA Journal 2010; 8(4): /304

206 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, , qualitative data % resistant isolates Austria Belgium Germany Italy Netherlands United Kingdom Figure QSA16. Trends in tetracycline resistance in tested S. Typhimurium isolates from pigs in reporting MSs, , qualitative data % resistant isolates Italy Poland Spain United Kingdom EFSA Journal 2010; 8(4): /

207 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, , qualitative data % resistant isolates Italy Poland United Kingdom Figure QSA18. Trends in nalidixic acid resistance in tested S. Typhimurium isolates from pigs in reporting MSs, , qualitative data % resistant isolates Italy Poland Spain United Kingdom 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): /304

208 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Germany Italy Latvia Netherlands Slovakia Spain Table QSA13b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from meat from pigs, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Germany Italy Latvia Netherlands Slovakia Spain EFSA Journal 2010; 8(4): /

209 8. ANTIMICROBIAL RESISTANCE IN SALMONELLA AND INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA Cattle and bovine meat 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 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): /304

210 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Belgium Germany Italy Greece Ireland Table QSA14b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from cattle, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Belgium Germany Italy Greece Ireland EFSA Journal 2010; 8(4): /

211 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Belgium Ireland Italy Netherlands Slovakia Table QSA15b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested S. Typhimurium isolates from cattle, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Ireland Italy Netherlands Slovakia EFSA Journal 2010; 8(4): /304

212 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, , qualitative data % resistant isolates Austria Belgium Germany Italy Ireland Figure QSA20. Trends in ampicillin resistance in tested Salmonella spp. isolates from cattle in reporting MSs, , qualitative data % resistant isolates Austria Belgium Germany Italy EFSA Journal 2010; 8(4): /

213 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, , qualitative data % resistant isolates Austria Belgium Germany Italy 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): /304

214 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Germany Italy Netherlands Slovakia Table QSA16b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among tested Salmonella spp. isolates from meat from bovine animals, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Germany Italy Netherlands Slovakia EFSA Journal 2010; 8(4): /

215 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, 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 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): /304

216 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Greece Ireland 1, Latvia Portugal Slovakia Table QEC2b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from Gallus gallus, , qualitative data Country Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Gallus gallus Greece Ireland Latvia Portugal Slovakia EFSA Journal 2010; 8(4): /

217 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, , qualitative data % resistant isolates Greece Ireland Portugal Figure QEC2. Trends in ampicillin resistance in indicator Escherichia coli from Gallus gallus in reporting MSs, , qualitative data % resistant isolates Greece Portugal 216 EFSA Journal 2010; 8(4): /304

218 ANTIMICROBIAL RESISTANCE IN SALMONELLA AND 8. INDICATOR ESCHERICHIA COLI - QUALITATIVE DATA 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 , 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): /

219 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Hungary Italy Poland Slovenia United Kingdom Norway Table QEC3b. Resistance (%) to sulfonamide, gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from turkeys, , qualitative data Sulfonamide Gentamicin Ciprofloxacin Nalidixic acid Country 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 Hungary Italy Poland Slovenia United Kingdom Norway EFSA Journal 2010; 8(4): /304

220 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, , qualitative data % resistant isolates Italy Poland United Kingdom Figure QEC4. Trends in ampicillin resistance in indicator Escherichia coli from turkeys in reporting MSs, , qualitative data % resistant isolates Italy Poland United Kingdom EFSA Journal 2010; 8(4): /

221 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, , qualitative data % resistant isolates Italy Poland 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 , which might indicate that the samples tested in 2004 and in were not comparable. 220 EFSA Journal 2010; 8(4): /304

222 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, , qualitative data Country Tetracycline Chloramphenicol Ampicillin Ceftiofur Gentamicin 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, Latvia Portugal United Kingdom Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res Pigs Ireland Latvia Portugal United Kingdom EFSA Journal 2010; 8(4): /

223 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, , qualitative data % resistant isolates Ireland United Kingdom Figure QEC7. Trends in ampicillin resistance in indicator Escherichia coli from pigs in reporting MSs, , qualitative data % resistant isolates Latvia United Kingdom 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): /304

224 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, , qualitative data Tetracycline Chloramphenicol Ampicillin Ceftiofur Country 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 Ireland 59, , , ,603 6 Latvia Portugal Slovakia United Kingdom 3, , , , , , , Table QEC5b. Resistance (%) to gentamicin, ciprofloxacin and nalidixic acid among isolates of indicator Escherichia coli from cattle, , qualitative data Gentamicin Ciprofloxacin Nalidixic acid Country N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res N % Res Cattle Greece Ireland Latvia Portugal Slovakia United Kingdom ,652 2 EFSA Journal 2010; 8(4): /

225 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, , qualitative data % resistant isolates Greece Ireland Portugal United Kingdom Figure QEC9. Trends in gentamicin resistance in indicator Escherichia coli from cattle in reporting MSs, , qualitative data % resistant isolates Greece Latvia Portugal United Kingdom 224 EFSA Journal 2010; 8(4): /304

226 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, , qualitative data % resistant isolates Greece Latvia Portugal EFSA Journal 2010; 8(4): /

227 226 EFSA Journal 2010; 8(4): /304

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

229 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 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 , 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): /304

230 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 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): /

231 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 % resistance at reporting MS 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 % resistance at reporting MS 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, Salmonella spp. from pigs in 13 MSs, 2007 Salmonella spp. from slaughter pigs baseline survey in 8 MSs, 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): /304

232 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 % resistance at reporting MS 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): /

233 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): /304

234 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 % resistance at reporting MS 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): /

235 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 % resistance at reporting MS 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): /304

236 10 REFERENCES References 10 EFSA Journal 2010; 8(4): /

237 10. REFERENCES 10. References Aarestrup FM, Wegener HC and Collignon P, Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Review of Anti-Infective Therapy; 6(5): Armitage P and Berry G, Statistical Methods in Medical Research, 4th ed. 2001, Oxford: Blackwell Scientific Publications. CLSI (Clinical and Laboratory Standards Institute), Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard-Third ed. [ISBN Number 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, 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): EFSA, 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, 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, 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, EFSA, The Community Summary Report on Trends and Sources of Zoonoses and Zoonotic Agents in the European Union in 2007, The EFSA Journal (2009), 223, Engberg J, Neimann J, Nielsen EM, Aarestrup FM and Fussing V, Quinolone-resistant Campylobacter infections: risk factors and clinical consequences. Emerging Infectious Diseases; 10(6): EUCAST (European Committee on Antimicrobial Susceptibility Testing), definitions. Available at Helms M, Vastrup P, Gerner-Smidt P and Molbak K, Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerging Infectious Diseases; 8(5): Kahlmeter G, Brown DF, Goldstein FW, MacGowan AP, Mouton JW, Osterlund A, Rodloff A, Steinbakk M, Urbaskova P and Vatopoulos A, European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. Journal of Antimicrobial Chemotherapy; 52(2): Lester CH, Sandvang D, Olsen SS, Schønheyder HC, Jarløv JO, Bangsborg J, Hansen DS, Jensen TG, Frimodt-Møller N, Hammerum AM, Emergence of ampicillin-resistant Enterococcus faecium in Danish hospitals. Journal of Antimicrobial Chemotherapy; 62(6): NCCLS (National Committee for Clinical Laboratory Standards), Performance Standards for Antimicrobial Susceptibility Testing: Eleventh Informational Supplement. NCCLS document M100-S11 [ISBN ]. 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) Escherichia coli and Salmonella: Cellular and Molecular Biology. American Society for Microbiology Press. 2 vols. p Top J, Willems R, van der Velden S, Asbroek M and Bonten M, Emergence of clonal complex 17 Enterococcus faecium in The Netherlands. Journal of Clinical Microbiology; 46(1): EFSA Journal 2010; 8(4): /304

238 REFERENCES 10. Varma JK, Molbak K, Barrett TJ, Beebe JL, Jones TF, Rabatsky-Ehr T, Smith KE, Vugia DJ, Chang HG and Angulo FJ, 2005a. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. Journal of Infectious Diseases; 191(4): Varma JK, Greene KD, Ovitt J, Barrett TJ, Medalla F and Angulo FJ, 2005b. Hospitalization and antimicrobial resistance in Salmonella outbreaks, Emerging Infectious Diseases; 11(6): Wang HH, Manuzon M, Lehman M, Wan K, Luo H, Wittum TE, Yousef A and Backaletz L, Food commensal microbes as a potentially important avenue in transmitting antibiotic resistance genes. FEMS Microbiology Letters; 254(2): WHO (World Health Organization), Report of the Second WHO Expert Meeting: Critically important antimicrobials for human medicine: Categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use. Available at: Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK and Doern GV, Evidence for transfer of CMY-2 AmpC-Lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrobial Agents and Chemotherapy; 45(10): EFSA Journal 2010; 8(4): /

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240 APPENDICES Appendices EFSA Journal 2010; 8(4): /