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. 2023 Mar 6;21(3):e07867.
doi: 10.2903/j.efsa.2023.7867. eCollection 2023 Mar.

The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021

European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC)

The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021

European Food Safety Authority (EFSA) et al. EFSA J. .

Abstract

Antimicrobial resistance (AMR) data on zoonotic and indicator bacteria from humans, animals and food are collected annually by the EU Member States (MSs) and reporting countries, jointly analysed by EFSA and ECDC and presented in a yearly EU Summary Report. This report provides an overview of the main findings of the 2020-2021 harmonised AMR monitoring in Salmonella spp., Campylobacter jejuni and C. coli in humans and food-producing animals (broilers, laying hens and turkeys, fattening pigs and bovines under 1 year of age) and relevant meat thereof. For animals and meat thereof, indicator E. coli data on the occurrence of AMR and presumptive Extended spectrum β-lactamases (ESBL)-/AmpC β-lactamases (AmpC)-/carbapenemases (CP)-producers, as well as the occurrence of methicillin-resistant Staphylococcus aureus are also analysed. In 2021, MSs submitted for the first time AMR data on E. coli isolates from meat sampled at border control posts. Where available, monitoring data from humans, food-producing animals and meat thereof were combined and compared at the EU level, with emphasis on multidrug resistance, complete susceptibility and combined resistance patterns to selected and critically important antimicrobials, as well as Salmonella and E. coli isolates exhibiting ESBL-/AmpC-/carbapenemase phenotypes. Resistance was frequently found to commonly used antimicrobials in Salmonella spp. and Campylobacter isolates from humans and animals. Combined resistance to critically important antimicrobials was mainly observed at low levels except in some Salmonella serotypes and in C. coli in some countries. The reporting of a number of CP-producing E. coli isolates (harbouring bla OXA-48, bla OXA-181, and bla NDM-5 genes) in pigs, bovines and meat thereof by a limited number of MSs (4) in 2021, requests a thorough follow-up. The temporal trend analyses in both key outcome indicators (rate of complete susceptibility and prevalence of ESBL-/AmpC- producers) showed that encouraging progress have been registered in reducing AMR in food-producing animals in several EU MSs over the last years.

Keywords: ESBL; MRSA; antimicrobial resistance; indicator bacteria; zoonotic bacteria.

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Figures

Figure 1
Figure 1
Occurrence of resistance to selected and critically important antimicrobials in Salmonella spp. and selected serovars isolated from humans, 2021

  1. Horizontal line: median; diamond: resistance at reporting MS group level; lower and upper box boundaries: 25th and 75th percentiles. For each serovar, only countries reporting 10 or more isolates are included. S. Kentucky is excluded from analysis as only three countries reported sufficient number of isolates.

Figure 2
Figure 2
Spatial distribution of combined ‘microbiological’ resistance to ciprofloxacin and cefotaxime among (a) Salmonella spp., (b) S. Infantis and (c) monophasic S. Typhimurium isolated from human cases, 2021 (pink indicates fewer than ten isolates tested)
Figure 3
Figure 3
Number of multidrug (MDR) resistant isolates, isolates resistant to one and/or two antimicrobial classes and completely susceptible Salmonella isolates from humans in 2021
Figure 4
Figure 4
Trends in resistance to ampicillin, ciprofloxacin/pefloxacin/nalidixic acid, cefotaxime and tetracycline in Salmonella spp. from humans in 27 reporting countries and EU MSs group, 2013–2021

  1. Data from the United Kingdom included up to 2019. Trend at EU MS group level is excluding UK data.

Figure 5
Figure 5
Occurrence of resistance to selected antimicrobials in Salmonella spp. recovered from (a) carcases of broilers and fattening turkeys, and (b) broilers, laying hens, fattening turkeys, fattening pigs and bovine animals under 1 year of age (calves), 2020/2021.

  1. AMP: ampicillin; SMX: sulfamethoxazole; TET: tetracycline; CIP: ciprofloxacin; CTX: cefotaxime; CIP/CTX: combined ‘microbiological’ resistance to ciprofloxacin and cefotaxime; AMK: amikacin; N: total number of Salmonella spp. isolates reported by MSs; blue diamond shows resistance at the reporting‐MS group level. Horizontal lines represent median; Lower and upper box boundaries, 25th and 75th percentiles, respectively; Blue diamond: resistance at the reporting MS group level Note: Only MSs reporting data for 10 or more isolates are shown in the graph; however, all isolates are included in the calculation of resistance at the reporting‐MS group level.

Figure 6
Figure 6
Breakdown of the number of tigecycline‐resistant Salmonella isolates by serovar from (a) broilers, fattening turkeys, laying hens, broiler carcases, and (b) fattening pigs and calves, bovine animals under 1 year old (calves) using harmonised ECOFFs, 2020/2021

  1. n: Total number of tigecycline‐resistant isolates reported by MSs; predominant serovars are also expressed as a percentage; *Monophasic S. Typhimurium includes antigenic formulas; salmonellas in the legend are listed according to their predominance within all the animal/carcase origins. The ECOFF used to determine resistance to tigecycline in boilers, turkeys, laying hens was MIC > 1 mg/L. The ECOFF used to determine tigecycline resistance in pig and calf data was MIC > 0.5 mg/L.

Figure 7
Figure 7
Breakdown of the number of colistin‐resistant Salmonella isolates by serovar, where detected among the animal/carcase origins by reporting MSs in 2020/2021

  1. n: Total number of colistin‐resistant isolates reported by the MSs; predominant serovars are expressed as a percentage.

    *: Monophasic S. Typhimurium includes antigenic formulas; †: serovar unspecified; salmonellas in the legend are listed according to their predominance within all the animal/carcase origins.

Figure 8
Figure 8
MDR and CS Salmonella spp. recovered from the carcases of broilers and fattening turkeys for all reporting countries (including two non‐MSs in broiler carcases) in 2020

  1. The MDR analysis of carcase isolates included the following antimicrobials: ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, gentamicin, meropenem, sulfamethoxazole, tetracycline, tigecycline and trimethoprim.

    MDR and complete susceptibility levels are also expressed as a percentage; N: total number of Salmonella spp. reported by MSs and non‐MSs. The ECOFFs used to determine microbiological resistance in 2020 data were from the Commission Implementing Decision (EU) 2013/652.

Figure 9
Figure 9
Spatial distributions of complete susceptibility to the selected antimicrobials tested among Salmonella spp. from (a) broiler carcases and (b) fattening turkey carcases, using harmonised ECOFFs laid down in Commission Implementing Decision (EU) 2013/652 for 2020 AMR data

  1. The CS analysis of carcase isolates included the following antimicrobials: ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, gentamicin, meropenem, sulfamethoxazole, tetracycline/tigecycline and trimethoprim.

Figure 10
Figure 10
MDR and CS Salmonella spp. isolates recovered from broilers, laying hens, fattening turkeys, fattening pigs and calves (< 1 year of age) for all reporting countries, 2020/2021, using harmonised EUCAST ECOFFs

  1. The MDR analysis of animal isolates included the following antimicrobials: amikacin/gentamicin (for pigs and calves) or gentamicin only (for poultry populations), ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, meropenem, sulfamethoxazole, tetracycline/tigecycline and trimethoprim.

    MDR and complete susceptibility are expressed as percentages; N: total number of Salmonella spp. reported by MSs and non‐MSs. Only MS with 10 or more isolates are included in the MDR analysis. The ECOFFs used to determine microbiological resistance in 2020 data were from the previous legislation (2013/652/EU) and the ECOFFs used for 2021 data are from the current legislation (2020/1729/EU).

Figure 11
Figure 11
Spatial distributions of complete susceptibility to the selected antimicrobials tested among Salmonella spp. from (a) broilers, (b) laying hens and (c) fattening turkeys, (d) fattening pigs and (e) bovine animals under 1 year old (calves) using harmonised ECOFFs, 2020/2021

  1. The ECOFF used to determine microbiological resistance in 2020 data were from the previous legislation (Commission Implementing Decision (EU) 2013/652) and the ECOFFs used for 2021 data are from the current legislation (Commission Implementing Decision (EU) 2020/1729).

    The CS analysis included the following antimicrobials: amikacin/gentamicin (for pigs and calves) or gentamicin only (for poultry populations), ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, meropenem, sulfamethoxazole, tetracycline/ tigecycline and trimethoprim.

Figure 12
Figure 12
Distribution of MIC levels among ciprofloxacin‐resistant Salmonella spp. from carcases of broilers, turkeys, as well as broilers, laying hens, fattening turkeys, fattening pigs and calves (< 1 year of age), for all reporting EU MSs, 2020/2021

  1. n: Total number of Salmonella spp. isolates exhibiting ciprofloxacin (CIP) resistance (MSs only); N: total number of Salmonella spp. reported by MSs.

    (1) In accordance with breakpoints stated in Decision 2013/652/EU (used for the analyses of poultry data) and Commission Implementing Decision (EU) 2020/1729 (used for the analysis of pigs and calves data).

    The proportion of isolates showing high‐level resistance is not included with those exhibiting ‘clinical’ or ‘microbiological’ resistance; similarly, the proportion of isolates showing ‘clinical’ resistance is not included with those displaying ‘microbiological’ resistance. Figure 12 excludes one isolate reported from laying hens (by the Republic of North Macedonia), which was ‘microbiologically’ resistant to ciprofloxacin.

Figure 13
Figure 13
Box‐plot of the occurrence of resistance to a selection of antimicrobials in C. jejuni and C. coli isolates from humans, 2021
Figure 14
Figure 14
Spatial distribution of combined resistance to ciprofloxacin and erythromycin in (a) C. jejuni and (b) C. coli isolates from humans, 2021
Figure 15
Figure 15
Number of multidrug isolates, isolates resistant to 1 and/or 2 antimicrobials and completely susceptible Campylobacter isolates from humans in 2021

  1. N: Total number of isolates reported.

Figure 16
Figure 16
Trends in ciprofloxacin, erythromycin and tetracycline resistance in Campylobacter jejuni from humans in 22 reporting countries and EU MSs group, 2013–2021

  1. Data from the United Kingdom included up to 2019. Trend at EU MS group level is excluding UK data.

Figure 17
Figure 17
Trends in ciprofloxacin, erythromycin and tetracycline resistance in Campylobacter coli from humans in 15 reporting countries and EU MSs group, 2013–2021

  1. Data from the United Kingdom included up to 2019. Trend at EU MS group level is excluding UK data.

Figure 18
Figure 18
Erythromycin MIC distribution in C. jejuni and C. coli isolates from humans, 2021
Figure 19
Figure 19
Occurrence of resistance to antimicrobials in C. jejuni and C. coli and from food‐producing animals, 2020/2021

  1. GEN: gentamicin; STR: streptomycin; TET: tetracycline; CIP: ciprofloxacin; ERY: erythromycin; ETP: ertapenem CIP/ERY: combined ‘microbiological’ resistance to ciprofloxacin and erythromycin; N: Total number of isolates reported by all Member States (MSs); Horizontal line represents median; Light green diamond: resistance at reporting MS group level (excluding UK, 2020). Lower and upper box boundaries, 25th and 75th percentiles, line inside box median, diamond mean.

Figure 20
Figure 20
Spatial distribution of combined resistance to ciprofloxacin and erythromycin in Campylobacter jejuni isolates from (a) broilers (27 EU MSs and three non‐MSs, 2020); (b) fattening turkeys (nine EU MSs and two non‐MS, 2020); and (c) calves less than 1 year of age (10 EU MSs and two non‐MSs, 2021)
Figure 21
Figure 21
Spatial distribution of combined resistance to ciprofloxacin and erythromycin in Campylobacter coli isolates from (a) broilers (seven EU MSs and one non‐MS, 2020); (b) fattening pigs (26 EU MSs plus United Kingdom (Northern Ireland) and three non‐MSs, 2021) and (c) calves less than 1 year of age (10 EU MSs, 2021)
Figure 22
Figure 22
Prevalence of resistances to ciprofloxacin (a), erythromycin (b), tetracycline (c) and related 95% confidence intervals in C. coli from fattening pigs, per reporting country, 2021
Figure 23
Figure 23
Number of isolates completely susceptible, resistant to one or two antimicrobial classes and MDR in C. jejuni and/or C. coli from broilers, fattening turkeys, fattening pigs and calves (< 1 age) in reporting EU MSs, 2020/2021

  1. N: Total number of isolates reported by the EU MSs. Complete susceptibility is defined as susceptibility to ciprofloxacin/nalidixic acid, erythromycin, gentamicin and tetracycline. MDR (multidrug resistance) is defined as resistance to at least three antimicrobial classes (including: GEN: gentamicin; CIP: ciprofloxacin; ERY: erythromycin; TET: tetracycline).

Figure 24
Figure 24
Trends in ciprofloxacin (CIP), erythromycin (ERY) and tetracycline (TET) resistance in C. coli from fattening pigs, 2015–2021/2009–2021*

  1. CIP: ciprofloxacin; ERY: erythromycin; TET: tetracycline. Arrows indicate significant increasing (up) or decreasing (down) trend over the entire period. *The trend analysis was performed for different periods depending on the data availability. Czechia, Estonia, Germany and Sweden: the trend analysis was performed for the reporting period 2015–2021. The Netherlands, Spain, Norway and Switzerland: The trend analysis was performed for the reporting period 2009–2021.

Figure 25
Figure 25
Distribution of MIC values related to erythromycin resistance in (a) C. jejuni from broilers and fattening turkeys, (b) C. coli from broilers and fattening turkeys, (c) C. jejuni from calves and (d) C. coli from fattening pigs and calves, in reporting EU MSs and non‐EU MSs, 2020 and 2021
Figure 26
Figure 26
Number of isolates (and percentage) exhibiting different levels of erythromycin resistance in broilers, fattening turkeys, fattening pigs and calves in reporting EU MSs and non‐EU MSs, 2020–2021

  1. N: Total number of C. jejuni or C. coli isolates exhibiting erythromycin resistance. ERY: erythromycin. ERY resistance in C. jejuni isolates: 4 mg/L < MIC ≤ 128 mg/L. ERY resistance in C. coli isolates: 8 mg/L < MIC ≤ 128 mg/L. For 2021 data, it is possible to discriminate between ERY‐resistant C. coli and C. jejuni isolates with MIC ranging from 128 mg/L to (equal) 512 mg/L and those with MIC above 512 mg/L.

Figure 27
Figure 27
Comparison of clinical breakpoints (CBPs) and epidemiological cut‐off values (ECOFFs) used to interpret MIC data reported for Campylobacter spp. from humans, animals or food
Figure 28
Figure 28
Comparison of C. jejuni occurrence of resistance between humans and animals
Figure 29
Figure 29
Comparison of C. coli occurrence of resistance between humans and animals
Figure 30
Figure 30
Distribution of occurrence of resistance to selected antimicrobials in indicator E. coli isolates recovered from fattening pigs (pigs) and bovines under 1 year of age (calves) in 2019 and from broilers and fattening turkeys (turkeys) in 2020. MSs and non‐MSs

  1. N: Total number of isolates reported by Member States (MSs) and non‐Member States (non‐MSs); AMP: ampicillin; SMX: sulfamethoxazole; TET: tetracycline; CIP: ciprofloxacin, CTX: cefotaxime; CIP/CTX: combined ‘microbiological’ resistance to ciprofloxacin and cefotaxime; AMK: Amikacin; Horizontal lines represent median; Lower and upper box boundaries, 25th and 75th percentiles, respectively; Blue diamond: resistance at the reporting MS group level.

Figure 31
Figure 31
Spatial distribution of combined microbiological resistance to cefotaxime and ciprofloxacin in indicator Escherichia coli. (a) fattening pigs, 2021; (b) bovines under 1 year of age, 2021; (c) broilers, 2020; and (d) fattening turkeys, 2020, EU MSs and non‐MSs
Figure 32
Figure 32
Trends in resistance to ampicillin (AMP), cefotaxime (CTX), ciprofloxacin (CIP) and tetracyclines (TET) in indicator E. coli from fattening pigs (pigs), EU MSs and non‐MSs, 2009–2021

  1. (↘)(↗): indicates statistically significant trends over the study period.

Figure 33
Figure 33
Trends in resistance to ampicillin (AMP), cefotaxime (CTX), ciprofloxacin (CIP) and tetracyclines (TET) in indicator E. coli from bovines under 1 year of age (calves), EU MSs and non‐MSs 2009–2021

  1. (↘)(↗): indicates statistically significant trends over the study period.

Figure 34
Figure 34
Trends in resistance to ampicillin (AMP), cefotaxime (CTX), ciprofloxacin (CIP) and tetracyclines (TET) in indicator E. coli from broilers, EU MSs and non‐MSs, 2009–2020

  1. (↘)(↗) indicates statistically significant trends over the study period.

Figure 35
Figure 35
Trends in resistance to ampicillin (AMP), cefotaxime (CTX), ciprofloxacin (CIP) and tetracycline (TET) in indicator E. coli from fattening turkeys (turkeys), EU MSs and non‐MSs, 2014–2020

  1. (↘)(↗): indicates statistically significant trends over the study period.

Figure 36
Figure 36
Spatial distribution of complete susceptibility to the antimicrobials tested in indicator E. coli. (a) fattening pigs (pigs) 2021; (b) bovines under 1 year of age (calves) 2021; (c) broilers 2020; (d) fattening turkeys (turkeys) 2020
Figure 37
Figure 37
Trends in the occurrence of complete susceptibility to the panel of antimicrobials tested in indicator E. coli from (a) fattening pigs (pigs) and (b) bovines under 1 year of age (calves) in the years, EU MSs and non‐MSs, 2015–2021

  1. (↓)/(↑): indicates statistically significant trends over the period 2015–2021.

Figure 38
Figure 38
Trends in the occurrence of complete susceptibility to the panel of antimicrobials tested in indicator E. coli from (a) broilers and (b) fattening turkeys (turkeys), EU MSs and non‐MSs, 2014–2020

  1. (↓)/(↑): indicates statistically significant trends over the period 2014–2020.

Figure 39
Figure 39
Changes in weighted key outcome indicator of complete susceptibility (KOICS) in 27 MSs and 4 non‐MSs

  1. (↓)/(↑): indicates statistically significant decreasing/increasing trends over the 2014–2021 period. Rates of change are given for statistically significant trends.

Figure 40
Figure 40
E. coli isolates harbouring (a) ESBL‐encoding genes and (b) AmpC‐encoding genes in fattening pigs, bovine animals < 1 year of age, meat from pigs and meat from bovines in 2021

  1. ESBL: extended‐spectrum β‐lactamase; AmpC: AmpC β‐lactamase; N: Total number of isolates harbouring an ESBL or AmpC gene.

    The breakdown of AmpC genes does not include point mutations in the AmpC promotor, only the genes listed in the legend.

    These figures incorporate data from countries that supplied WGS results to be used for analysis instead of MIC values. This excludes countries that provided MIC results as well as WGS results voluntarily.

Figure 41
Figure 41
Prevalence of presumptive ESBL‐producing (a) and AmpC‐producing (b) E. coli from the specific monitoring of ESBL/AmpC‐producing E. coli, 2020/2021

  1. N: number of samples tested; Diamond with white outline is the data (one data point per country); Diamond with black outline is Total EU. Outliers (> 1.5 IQR from 75th percentile) are spotted using a different symbol for each matrix (for example square for Pig meat 2021)

Figure 42
Figure 42
Spatial distribution of the prevalence of presumptive ESBL and/or AmpC‐producing E. coli from (a) meat from broilers in 2020, (b) meat from pigs in 2021 and (c) meat from bovines in 2021, EU MSs and non‐MSs, 2020/2021
Figure 43
Figure 43
Spatial distribution of the prevalence of presumptive ESBL and/or AmpC‐producing E. coli from (a) broilers in 2020, (b) fattening turkeys in 2020, (c) fattening pigs in 2021 and (d) bovines under 1 year of age in 2021, EU MSs and non‐MSs, 2020/2021
Figure 44
Figure 44
Prevalence of presumptive ESBL‐producing versus AmpC‐producing E. coli from (a) meat from broilers, (b) broilers and (c) fattening turkeys, EU MSs and non‐EU MSs, 2020

  1. The upper bounds of the 95% confidence interval of the prevalence of ESBL‐ and/or AmpC‐producing E. coli are also indicated.

Figure 45
Figure 45
Prevalence of presumptive ESBL‐producing versus AmpC‐producing E. coli from (a) meat from pigs and (b) fattening pigs, EU MSs and non‐EU MSs, 2021

  1. Prevalence was assessed using genotypic data reported by Czechia, Finland, Germany and Italy.

    The upper bounds of the 95% confidence interval of the prevalence of ESBL‐ and/or AmpC‐producing E. coli are also indicated. Please note the different scales used for the x‐axis in the subfigures to improve the visibility of the variations among countries.

Figure 46
Figure 46
Prevalence of presumptive ESBL‐producing versus AmpC‐producing E. coli from (a) bovine meat and (b) bovines under 1 year of age, EU MSs and non‐EU MSs, 2021

  1. Prevalence was assessed using genotypic data reported by Czechia, Finland, Germany and Italy.

    The upper bounds of the 95% confidence interval of the prevalence of ESBL‐ and/or AmpC‐producing E. coli are also indicated. Please note the different scales used for the x‐axis in the subfigures to improve the visibility of the variations among countries.

Figure 47
Figure 47
Trends on the prevalence of presumptive ESBL and/or AmpC‐producing E. coli in (a) meat from broilers, (b) meat from pigs and (c) bovine meat over the period 2015–2021, EU MSs and non‐MSs

  1. Prevalence was assessed using genotypic data reported by Czechia, Germany and Italy in 2021.

    The upper bounds of the 95% confidence interval of the prevalence of ESBL‐ and/or AmpC‐producing E. coli are also indicated.

    Prevalence was assessed using genotypic data reported by Czechia, Germany and Italy in 2021.

Figure 48
Figure 48
Trends on the prevalence of presumptive ESBL and/or AmpC‐producing E. coli in (a) broilers, (b) fattening turkeys, (c) fattening pigs and (d) bovines under 1 year of age, over the period 2015–2021, EU MSs and non‐MSs

  1. The upper bounds of the 95% confidence interval of the prevalence of ESBL‐ and/or AmpC‐producing E. coli are also indicated.

Figure 49
Figure 49
Changes in outcome indicator of ESBL‐ and/or AmpC producing E. coli (OIESC), 27 EU MSs and 4 non‐MSs, 2014–2021

  1. (↓)/(↑): indicates statistically significant decreasing/increasing trends over the 2014–2021 period.

    Rates of change are shown for the statistically significant decreasing/increasing trends observed.

Figure 50
Figure 50
E. coli isolates with carbapenemase encoding genes in fattening pigs and bovines animals under > 1 year of age, isolated within the specific CP‐monitoring in 2021

  1. N = Total number of isolates harbouring a CP‐encoding gene.

    These figures incorporate data from countries that provided WGS results to be used for analysis instead of MIC values. This excludes countries that provided MIC results as well as WGS results voluntarily.

Figure 51
Figure 51
MRSA occurrence in food, 2020/2021 (only food origins where positive isolates were obtained are presented)

  1. N: Total number of sample units tested; AT: Austria; DE: Germany; FI: Finland; NL: the Netherlands; SK: Slovakia; CH: Switzerland.

    • Broiler meat (AT, 2020): spa‐types: t011 (4 isolates) t034 (4).

    •Bovine meat (DE, 2021): spa‐types: t1346 (1 isolate), t002 (2), t008 (2), t311 (2), t2112 (1), t174 ST41110 (1), t011 (4), t034 (4), t359 (1), t559 (1), t843 mecC positive (1), t899 (1), t1430 (1), t1451 (1).

    •Pig meat (FI, 2021): spa‐types: t728 St45 (1 isolate), t034 ST398 (14), t899 ST398 (1), t2741 ST398 (9), t4677 ST398 (1).

    •Pig meat (DE, 2021) spa‐types: t1430 (1 isolate).

    •Sheep meat (DE, 2020) spa‐type: t011 (1 isolate), t034 (2), t1451 (1), t2576 (1), t19979 ST 398 (1), t223 (2), t267 (1), t1154 ST5 (1) t15010 ST97 (1).

Figure 52
Figure 52
MRSA occurrence in food‐producing animals, 2020/2021 (only origins where positive isolates were obtained are presented)

  1. N: Total number of sample units tested; BE: Belgium; CH: Switzerland; DE: Germany; NL: the Netherlands; NO: Norway; SK: Slovakia.

    • Broiler flocks, BE 2020: spa‐types: t011 CC398 (2 isolates).

    • Fattening turkey flocks, BE 2020: spa‐types: t011 CC398 (2 isolates).

    • Fattening pigs, SK 2020: data were reported as suspect sampling.

    • Veal calf herds, BE 2021: spa‐types: t386 ST1 (1), t011 (65), t034 (6), t1451 (1), t1456 (1), t2346 (1), t2370 (1), t3423 (1), t5210 (1), t6228 (1).

    • Dairy cow herds, BE 2021: spa‐types: t037 ST239 (3 isolates), t011 (10), t034 (2).

    • Production cattle herds, BE 2021: spa‐types: t037 ST239 (2 isolates), t011 (2).

Figure 53
Figure 53
MRSA types reported from food and animals in 2020 and 2021, inferred from molecular typing data.

  1. N = number of reported isolates with typing data, mecC: MRSA harbouring the mecC gene, HA‐MRSA: hospital acquired MRSA, CA‐MRSA: community acquired MRSA, LA‐MRSA: livestock associated MRSA, CC: clonal complex.

    Inferred MRSA types recovered from animals in 2020 were derived from broiler flocks (2 isolates) and fattening turkey flocks (2 isolates). In 2021 these were recovered from veal calves (79 isolates), dairy cows (15 isolates) and cattle (4 isolates).

    Inferred MRSA types recovered from food in 2020 were derived from broiler meat (8 isolates) and meat from sheep (11). In 2021 these were recovered from bovine meat (21 isolates) and pig meat (27 isolates). Eight bovine meat isolates and 1 pig meat isolate were identified at border in imported meat from border control posts in 2021. Four bovine meat isolates (t898 ST399, t588 ST402, t034 ST4562, t311 St5/CC5) and 1 pig meat isolate (t588 ST400) were excluded from the graph as it was unclear whether they were LA, HA or CA.

Figure 54
Figure 54
Temporal trends of MRSA occurrence in various types of meat, 2011–2021

  1. AT: Austria; CH: Switzerland; DE: Germany; NL: the Netherlands.

    The 2‐S method of isolation was used by CH and DE from 2011 to 2018; while the 1‐S method was used by the NL from 2018 to 2021, as well as CH in 2019.

    Bovine meat (CH): In 2019, spa‐types were not reported; however, both isolates were confirmed to belong to CC398 using the sau1‐hsdS1 CC398 PCR reaction (Stegger et al., 2011).

    Pig meat (CH): In 2017, spa‐type: t011 (1 isolate), t002 (1). PVL status of the t002 isolate was not reported. In 2019, spa‐type was not reported; however, the isolate was confirmed to belong to CC398 using the sau1‐hsdS1 CC398 PCR reaction (Stegger et al., 2011).

    Broiler meat (AT): In 2018, spa‐types: t011 (2 isolates), t034 (1 isolate). In 2020, spa‐types: t011 (4 isolates), t034 (4 isolates).

    Broiler meat (CH): In 2016, spa‐types: t034 (3 isolates), t153 (1), t1430 (3), t2123 (2). PVL status of the t153 isolate was not reported.

    In 2018, spa‐types: t034 CC398 (1 isolate), t1430 (1), t571 CC398 (1), t13177 (1).

    *spa‐types were not provided for Bovine meat (NL), Pig meat (NL), Broiler meat (DE), Turkey meat (DE and NL).

Figure 55
Figure 55
Temporal trends of MRSA occurrence in bovine animals, 2009–2021

  1. BE: Belgium; CH: Switzerland; DK: Denmark. The 2‐S method of isolation was used by Belgium and Switzerland from 2012 to 2018; while the 1‐S method was used by Denmark since 2018 and by Switzerland since 2019.

    *spa‐types not reported.

    Veal calf herds < 1(BE): In 2012, spa‐types: t011 (40 isolates), t1451 (3), t1456 (1), t1985 (3), t3423 (1), untypable (1).

    In 2015, spa‐types: t011 (64 isolates), t034 (15), t037 (8), t044 (3), t1451 (3), t1580 (7), t1985 (8), t2287 (2), t3423 (5), untypable (1). The t044 isolates were PVL‐negative. In 2018, spa‐types: t011 CC398 (65 isolates), t034 CC398 (8), t1451 CC398 (1), t1580 CC398 (2), t3423 CC398 (1), t3479 CC398 (1), t9433 CC398 (1). In 2021, spa‐types: t386 (1), t011 (65), t034 (6), t1451 (1), t1456 (1), t2346 (1), t2370 (1), t3423 (1), t5210 (1), t6228 (1)

    Veal calf herds < 1(CH): In 2015, spa‐types: t011 (11 isolates), t034 (6) and t008 (2). The t008 isolates were PVL‐positive.

    In 2017, spa‐types: t011 (14 isolates), t034 (7), t127 (1), t17339 (2). PVL status of the t127 isolate was not reported. In 2019, spa‐types were not reported; however, all 11 isolates were confirmed to belong to CC398 using the sau1‐hsdS1 CC398 PCR reaction (Stegger et al., 2011).

    Dairy cow herds (BE): In 2012, spa‐types: t011 (8 isolates), t037 (1), t388 (1), t1456 (1), t6228 (2), untypable (1). In 2015, t011 (4 isolates), t034 (1), t1580 (1), t1985 (2), t2383 (1), untypable (1). In 2018, spa‐types: t011 CC398 (8 isolates), t034 CC398 (1), t223 (3), t1257 (1). The t223 isolates were PVL‐negative; TSST status was not determined. The PVL status of the t1257 isolate was not reported. In 2021, spa‐types: t037 (3), t011 (10), t034 (2).

    Dairy cow herds (DK): In 2018, spa‐types: t034 (7 isolates), t267 CC97 (1). In 2019, spa‐types: t127 CC1 (1 isolate), t843 CC130 (1). The t127 isolate was PVL‐negative, as well as negative for the human IEC gene scn. spa‐type t843 was confirmed to carry the mecC gene.

    Meat production cattle herds (BE): In 2012, spa‐types: t011 (16 isolates), t121 (1), t1456 (1), t1985 (1). In 2015, spa‐types: t011 (9 isolates), t034 (2), t1451 (1), t1580 (2), t2287 (1), t3423 (1). In 2018, spa‐types: t011 CC398 (5 isolates), t1451 CC398 (1), t223 (2), t223 ST22 (1). All three t223 isolates were PVL‐negative. One t223 isolate was confirmed to belong to ST22, harbour the tst gene and IEC genes (chp, sak and scn) from WGS data. In 2021, spa‐types: t037 (2), t011 (2).

Figure 56
Figure 56
Temporal trends of MRSA occurrence in pigs, 2010–2020

  1. BE: Belgium; CH: Switzerland; DE: Germany; DK: Denmark; NO: Norway.

    Note: The 2‐S method of isolation was used by Belgium and Germany from 2016 to 2019, as well as by Denmark in 2016, in Switzerland from 2010 to 2017 and in Norway from 2014 to 2017. The 1‐S method was used by Switzerland in 2019 and 2021, by Denmark in 2018 and 2019, and by Norway in 2018–2021.

    All isolates tested by Norway in 2018, 2020 and 2021 (n = 716 in 2018, n = 641 in 2020 and n = 763 in 2021) were MRSA negative; extremely low % positive MRSA isolates (range: 0.1%–0.5%) were reported in the other years. Norway is the only country with a control programme in place for MRSA in pigs.

    Fattening pigs (CH): In 2010, spa‐types: t034 ST398 (17 isolates), t011 ST398 (1), t208 ST49 (5). In 2011, spa‐types: t034 ST398 (19 isolates), t011 ST398 (1), t208 ST49 (1), t2279 ST1 (1). In 2012, spa‐types: t034 CC398 (61 isolates), t011 CC398 (9), t208 ST49 (2). In 2013, spa‐types: t034 (63 isolates), t011 (10). In 2014, spa‐types: t034 (57 isolates), t011 (19), t208 (1), t899 (1), t2741 (1). In 2015, spa‐types: t034 (48 isolates), t011 (23), t032 (1), t571 (1), t899 (1), t1145 (1), t1250 (1), t4475 (1). In 2017, spa‐types: t034 (63 isolates), t011 (61), t899 (2), t1451 (3), t2330 (1), t2876 (1). In 2019, spa‐types were not reported; however, 159/160 isolates were confirmed to belong to CC398 using the sau1‐hsdS1 CC398 PCR reaction (Stegger et al., 2011). The remaining isolate did not survive cryo‐conservation, therefore typing could not be performed.

    Fattening pigs (BE): In 2016, spa‐types: t011 CC398 (71 isolates), t1451 (1), t1456 (1), t1456 CC398 (1), t1580 (5), t1985 (8), t1985 CC398 (3), t034 (7), t034 CC398 (2), t037 (1), t898 (1), unspecified (11). In 2019, spa‐types: t011 CC398 (67 isolates), t034 CC398 (11), t1451 CC398 (2), t1457 CC398 (1), t2346 CC398 (1), t2370 CC398 (2), t2383 CC398 (1), t3041 CC398 (1), t3119 CC398 (1), unspecified (18).

    Fattening pigs (DE): No molecular typing results available.

    Fattening pigs (DK): In 2016, spa‐types not reported. In 2018, spa‐types: t011 CC398 (22 isolates), t034 CC398 (85), t571 CC398 (3), t898 CC398 (1), t2383 CC398 (1), t2974 CC398 (1), t3423 CC398 (1), t4652 CC398 (1), t9266 CC398 (1). Prevalence data for fattening pig herds (not raised under controlled housing conditions) from 2018 are not included.

    Breeding pigs (BE): In 2016, spa‐types: t011 CC398 (55 isolates), t1451 (2), t1456 (1), t1456 CC398 (3), t1580 (1), t1985 (5), t1985 CC398 (1), t034 (1), t034 CC398 (4), t4659 CC398 (1), unspecified (17). In 2019, spa‐types: t011 CC398 (57 isolates), t034 CC398 (18), t108 CC398 (2), t779 CC398 (1), t2346 CC398 (1), t2582 CC398 (1), t2922 CC398 (1), t3119 CC398 (2).

    Breeding pigs (DK): In 2016, spa‐types not reported. In 2018, spa‐types: t011 CC398 (6 isolates), t034 CC398 (24), t1250 CC398 (2), t1793 CC398 (1), t3171 CC398 (1). In 2019, spa‐types t011 CC398 (10), t034 CC398 (57), t1928 CC398 (1), t4652 CC398 (1) were identified in isolates from multiplier pig herds.

    Pig herds (NO): In 2014, spa‐type: t011 CC398 (1). In 2015, spa‐type: t034 CC398 (2), t177 CC1 (2). In 2016, spa‐type: t034 CC398 (1). In 2017, spa‐types: t091 CC7 (1 isolate), t843 CC130 (1), t6292 CC425 (1). The t091 isolate was PVL‐negative, spa‐types t843 and t6292 were confirmed to carry the mecC gene. In 2019, spa‐type: t034 CC398 (1).

Figure 57
Figure 57
Antimicrobial resistance in MRSA from animals, in 2021

  1. BE: Belgium; CH: Switzerland. N: number of tested isolates. All isolates were resistant to Penicillin and Cefoxitin.

Figure 58
Figure 58
Antimicrobial resistance in MRSA from food in 2020 and 2021

  1. DE: Germany. N: number of tested isolates. All isolates were resistant to Penicillin and Cefoxitin. Eight bovine meat samples and 1 pig meat sample from DE were from imported meat at border control posts.

Figure A.1
Figure A.1
Resistance levels among MDR Salmonella Kentucky isolates exhibiting high‐level ciprofloxacin resistance from poultry, reported by MSs in 2020

  1. n: Total number of S. Kentucky isolates exhibiting high‐level ciprofloxacin resistance.

    NB: A single S. Kentucky isolate recovered from a fattening pig in 2021 with high‐level ciprofloxacin resistance was also resistant to nalidixic acid only and susceptible to all the other antimicrobials tested. None of the S. Kentucky isolates reported in poultry exhibited either azithromycin or colistin resistance.

Figure A.2
Figure A.2
Number of Salmonella isolates displaying high‐level ciprofloxacin resistance by serovar, reported from the different poultry origins by MSs in 2020

  1. n: Total number of Salmonella isolates exhibiting high‐level ciprofloxacin resistance; ns: number of isolates by serovar exhibiting high‐level ciprofloxacin resistance; In addition, a single S. Kentucky isolate displaying high‐level ciprofloxacin resistance was also recovered from a fattening pig in 2021.

Figure C.1
Figure C.1
Commonly reported Salmonella serovars from carcases of broilers and fattening turkeys, for all reporting countries (including two non‐MSs in broiler carcases) in 2020

  1. *Monophasic S. Typhimurium includes antigenic formulas; serovars in the legend are listed according to their predominance within all the carcase origins.

Figure C.2
Figure C.2
Proportions of isolates completely susceptible (green), resistant to 1 or 2 antimicrobial classes (gold) and multidrug‐resistant (red) in Salmonella spp. and particular Salmonella serovars from carcases of broilers and fattening turkeys, for all reporting countries (including 2 non‐MSs in broiler carcases) in 2020

  1. N: Total number of Salmonella spp. or total number of particular serovars recovered from the carcase monitoring.

    *Monophasic S. Typhimurium includes antigenic formulas. The ECOFF used to determine resistance to tigecycline was MIC > 1 mg/L.

Figure C.3
Figure C.3
Commonly reported Salmonella serovars recovered from broilers, laying hens, fattening turkeys, fattening pigs and calves (< 1 year of age), for all reporting countries (including 1 non‐MS in broilers, laying hens, fattening pigs), 2020/2021

  1. *Monophasic S. Typhimurium includes antigenic formulas; serovars in the legend are listed according to their predominance within all the animal origins.

Figure C.4
Figure C.4
Proportions of isolates completely susceptible (green), resistant to 1 or 2 antimicrobial classes (gold), and MDR (red) in Salmonella spp. and certain serovars recovered from (a) fattening pigs, (b) calves, for all reporting countries, 2021

  1. N: Total number of isolates recovered; *monophasic S. Typhimurium includes antigenic formulas.

    The MDR analysis of animal isolates included the following antimicrobials: ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, gentamicin/amikacin, meropenem, sulfamethoxazole, tetracycline/tigecycline and trimethoprim. In 2021, amikacin was also included in the analysis of pigs and calves, for the MDR analysis it was considered together with gentamicin for the aminoglycosides antimicrobial class The ECOFF used to determine resistance to tigecycline for pig and calf data was MIC > 0.5 mg/L, while for poultry data was MIC > 1 mg/L.

Figure C.5
Figure C.5
Proportions of isolates completely susceptible (green), resistant to 1 or 2 antimicrobial classes (gold) and MDR (red) in Salmonella spp. and certain serovars recovered from (a) broilers, (b) laying hens and (c) fattening turkeys, for all reporting countries, 2020/2021

  1. N: Total number of isolates recovered; *monophasic S. Typhimurium includes antigenic formulas. The MDR analysis of animal isolates included the following antimicrobials: ampicillin, cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/nalidixic acid, gentamicin, meropenem, sulfamethoxazole, tetracycline, tigecycline and trimethoprim. The ECOFF used to determine resistance to tigecycline for poultry data was MIC > 1 mg/L while for pig and calf data MIC > 0.5 mg/L.

Figure C.6
Figure C.6
Proportions of certain serovars exhibiting multiresistance to overall MDR levels in Salmonella spp. recovered from each of the food‐producing animal populations and derived carcases, for all reporting countries in 2020/2021

  1. n: Total number of Salmonella isolates exhibiting MDR; serovars contributing the highest levels of MDR to overall MDR levels in Salmonella spp. are illustrated with a percentage; *monophasic S. Typhimurium includes antigenic formulas; serovars in the legend are listed according to their predominance within all the animal/carcase origins.

Figure D.1
Figure D.1
Comparison of CBPs and ECOFFs used to interpret MIC data reported for Salmonella spp. from humans, animals or food

  1. *EUCAST has changed the definitions of SIR from 2019 (EUCAST, – http://www.eucast.org/newsiandr/). For Intermediate (I), the new definition ‘susceptible, increased exposure’ is used when there is a high likelihood of therapeutic success because exposure to the agent is increased by adjusting the dosing regimen or by its concentration at the site of infection. †EFSA Manual for reporting 2021 antimicrobial resistance data within the framework of Directive 2003/99/EC and Decision 2020/1729/EU. ‡Only R category included.

Figure D.2
Figure D.2
Occurrence of resistance to selected antimicrobials in S. Infantis from humans (2021) and poultry and poultry carcases (2020), reported by MSs

  1. N: Total number of isolates reported by MSs.

Figure D.3
Figure D.3
Occurrence of resistance to selected antimicrobials in S. Enteritidis from humans (2021) and poultry and broiler carcases (2020), reported by MSs

  1. N: Total number of isolates reported by MSs.

    NB. S. Enteritidis was not reported from turkey carcases.

Figure D.4
Figure D.4
Occurrence of resistance to selected antimicrobials in S. Kentucky from humans (2021) and poultry and poultry carcases (2020), reported by MSs

  1. N: Total number of isolates reported by MSs.

Figure D.5
Figure D.5
Occurrence of resistance to selected antimicrobials in S. Typhimurium from humans, pig and calves, reported by MSs in 2021

  1. N: Total number of isolates reported by MSs.

Figure D.6
Figure D.6
Occurrence of resistance to selected antimicrobials in monophasic S. Typhimurium from humans, fattening pigs and calves, reported by MSs in 2021

  1. N: Total number of isolates reported by MSs.

Figure D.7
Figure D.7
Occurrence of resistance to selected antimicrobials in S. Derby from humans, fattening pigs and calves, reported by MSs in 2021

  1. N: Total of isolates reported by MSs.

Figure E.1
Figure E.1
Temporal trends in resistance to colistin in indicator E. coli from calves under 1 year of age, 11 EU MSs and 2 non‐MSs, 2015–2021

  1. Statistically significant increase (↑) or decrease (↓) indicated (p < 0.05).

Figure E.2
Figure E.2
Temporal trends in resistance to colistin in indicator E. coli from fattening pigs, 28 EU MSs and 3 non‐MSs, 2015–2021

  1. Statistically significant increase (↑) or decrease (↓) indicated (p < 0.05).

Figure E.3
Figure E.3
Temporal trends in resistance to colistin in indicator E. coli from broilers, 25 EU MSs and 4 non‐MSs, 2014–2020

  1. Statistically significant increase (↑) or decrease (↓) indicated (p < 0.05).

Figure E.4
Figure E.4
Temporal trends in resistance to colistin in indicator E. coli from fattening turkeys (turkeys), 10 EU MSs and 2 non‐MS, 2014–2020

  1. Statistically significant increase (↑) or decrease (↓) indicated (p < 0.05).

Figure F.1
Figure F.1
Phenotypes inferred based on the resistance to the b‐lactams included in Panel 2
See this image and copyright information in PMC

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