Sci. report, recommendat°, guidance doc., directive, monograph
Engels
SCIENSANO
Samenvatting:
Samenvatting
In Belgium, the FASFC monitors the evolution of antimicrobial resistance (AMR) in food and foodproducing animals (primary production). Resistance in the zoonotic bacteria Salmonella spp. and Campylobacter spp. and in methicillin-resistant Staphylococcus aureus (MRSA) as well as resistance in indicator bacteria Escherichia coli, Enterococcus faecalis and Enterococcus faecium was monitored in 2023. Moreover, a specific monitoring of presumptive extended spectrum βlactamases/AmpC/carbapenemase producing E. coli is done on strains isolated from food-producing animals and meat derived thereof. Microbiological resistance was assessed using epidemiological cutoff values (ECOFF) according to EUCAST (European Committee on Antimicrobial Susceptibility Testing). In 2023, the European Commission Implementing Decision 2020/1729 of the 17th of November 2020 was applicable for the determination of the epidemiological cut-off values as well as for the selection of antimicrobial panels (a.o. EUVSEC3/EUCAMP3). In Campylobacter jejuni isolated from poultry meat, the predominant resistance profiles included ciprofloxacin combined with tetracycline. However, resistance to tetracycline was lower in 2023 (42.9%) than in 2022 (54.3%). Resistance to ertapenem in C. jejuni increased in 2022 (13.0%) and again in 2023 (14.3%) in comparison with 2021 (11.1%) when the antibiotic was added to the test panel. Multidrug resistance in C. jejuni decreased to 10.2% in 2023 compared to 15.2% in 2022. In Campylobacter coli isolated from poultry meat, while ciprofloxacin resistance decreased in 2023, resistance to erythromycin, ertapenem and tetracycline increased, thus increasing the multidrug resistance rate as well from 39,1% in 2022 to 48.6%. In primary production, the monitoring of Campylobacter coli in fattening pigs showed overall stable resistance levels in comparison with 2022 except for a decreased resistance to ciprofloxacin (from 45.7% to 40.8%) and to erythromycin (from 19.5% to 10.9%). However, in C. coli isolated from veal calves, resistances to ciprofloxacin, ertapenem, gentamicin and tetracycline were lower in 2023 than in 2022 but resistances to chloramphenicol and erythromycin were higher. In C. jejuni, resistance to ertapenem keeps increasing since its addition in 2021. Resistances to gentamicin and tetracycline increased in 2023 as well. However, resistances to ciprofloxacin, erythromycin and chloramphenicol decreased in 2023. Overall, as seen in previous reports, antimicrobial resistance levels are lower in C. jejuni than in C. coli. In 2023, Salmonella spp. recovered from food matrices have been analysed by whole genome sequencing (WGS). The highest levels of predicted antimicrobial resistance considering all serotypes and all matrices are to sulfamethoxazole (57%), followed by ampicillin (48%), tetracycline (43%) and trimethoprim (30%). Resistance to (fluoro)-quinolones associated to the qnrB gene was mainly predicted in isolates from broiler neck skin (11.2%) all belonging to serotype Chester (ST1954). Two isolates showed a predicted resistance to 3rd generation cephalosporins, one isolate from sunflower seeds belonging to the serotype Kentucky (ST198). This isolate harbored a blaCTX-M-14b together with the following genes: aac(3)-Id; aac(6')-Iaa, aadA7; aph(3'')-Ib, aph(3')-Ia; aph(6)-Id; sul1; tet(A) which confer a multidrug resistant profile including sulfamethoxazole, tetracycline and gentamicin among other aminoglycosides. The second isolate harboring a gene conferring resistance to extended spectrum β-lactams was isolated from cut poultry meat and belonged to the serotype Infantis (ST8662). The isolate harbored the following genes: blaCTX-M-3, aac(6')-Iaa; aadA1; aadA1; dfrA14; sul1; tet(A) conferring a multi drug resistance profile including extended spectrum β-lactams, aminoglycosides, trimethoprim, sulfonamides and tetracyclines. Resistance to colistin is rare, and was only predicted in one isolate from broiler neck skin. The isolate belonged to Salmonella Paratyphi B var. Java (ST28) and harbored the mobile colistin resistance gene mcr-9.1. The isolate carried the following genes as well, aac(6')-Iaa; dfrA1; formA; lnu(F); aph(3')-Ia; sul1; and qacE conferring a multidrug resistant profile including trimethoprim, fosfomycin, lincosamide, aminoglycosides, sulfonamides, and quaternary ammonium biocides. In Salmonella spp. isolated from food-producing animals, the most prevalent serotypes found in samples from pig caecal content were Monophasic Typhimurium (31%), Typhimurium (26%) and Derby (20%). Resistances to all antimicrobials but trimethoprim and amikacin, which is detected for the first time in this matrix, decreased in 2023. In the 3 Salmonella spp. isolates retrieved from veal calves caecal content, 2 belonged to the serovar Typhimurium and the last one to its monophasic variant. In both matrices, no resistance to 3rd generation cephalosporins, colistin or meropenem was detected in 2023. In 2023, all Salmonella spp. isolates from fattening pigs and bovines were analysed by WGS as well. Considering all serotypes, the resistance pattern predicted for isolates from fattening pigs were as follows: tetracycline (53.50%), ampicillin (46.51%), sulfamethoxazole (44.19%) and trimethoprim (27.91%). The gene aac(6')-Iaa was found in all genomes independently of the serovars. This gene encodes for a chromosomal aminoglycoside acetyltransferase which confers resistance to aminoglycosides. However, aac(6′)-Iaa and similar genes usually are transcriptionally silent and rarely become transcriptionally active. The mere presence of this gene does not confer aminoglycoside resistance in Salmonella. All but two isolates belonging to the serovar Typhimurium and its variant monophasic harbored the following resistance genes blaTEM-1B, tet (B or M) and sul (1 or 3) conferring resistance to penicillins, tetracyclines and sulfamides. Other serotypes found in fattening pigs, such as S. Derby and S. Rissen were predicted to be occasionally resistant to the above mentioned antimicrobials and not any other resistance was predicted. None of the isolates from either category of food-producing animals were predicted to be resistant to 3rd generation cephalosporins, ciprofloxacin or colistin. No known associated genes to the mentioned antimicrobials were found in any of the isolates. The specific monitoring of ESBL, AmpC and carbapenemase producing E.coli was performed in broilers, turkeys, fattening pigs and bovines at slaughterhouse and in meat derived from these 4 categories of food producing animals at retail. In 2023, the highest prevalence of ESBL E.coli was found in caecal content from bovines (66.60%) followed by broilers (61.72%) and fattening pigs (29.26%). We have observed a significant decrease in the prevalence of ESBL E. coli isolated from broilers and fresh meat. As reported in previous years, the prevalence of ESBL E. coli on broiler fresh meat was the highest (45.51%) among the fresh meat categories followed by bovine fresh meat (3.19%) and pig meat (1.92%) which remains low. No meropenem-resistant isolates were detected in 2023. However, ESBL E.coli isolated from these matrices showed extremely high levels of multidrug resistance (>80%). The most frequent determinants encoding for ESBL enzymes found in isolates from broilers at slaughterhouse and fresh poultry meat were blaSHV-12, bla CTX-M-55 and bla TEM-52. Isolates from bovines and fattening pigs carried genes encoding for enzyme production CTX-M group 1. In addition, a significant number of isolates from bovines carried the gene blaCTX-M-2, suggesting this category of food producing animals as a reservoir of this particular mechanism of resistance. In indicator E.coli, in comparison with 2022 an overall decreased resistance to most antibiotics was detected in food-producing animals: in broilers, veal calves of less than one year and fattening pigs sampled at the slaughterhouse as well as in laying hens, breeding hens and meat bovines of less than 7 months old sampled at the farm. The highest prevalences to the critically important antimicrobials 3rd generation cephalosporins and (fluoro)quinolones were detected in E. coli from broiler caecal content sampled at the slaughterhouse but were lower in 2023 than in previous years. Low or very low rates of 3 resistance to amikacin were detected in E. coli isolated from pig caecal content every year since its addition in 2021. And low colistin resistance was also detected continuously over the previous years in E. coli isolated from veal calves caecal content. At the level of the farm, the highest resistance to (fluoro)quinolones was found in E. coli isolated from breeding hens while resistance to 3rd generation cephalosporins was detected in 3 E. coli isolates from fecal samples of bovine animals, and in one isolate from breeding hens and in one isolate from laying hens. No resistance to meropenem was detected in any of the indicator E. coli isolates. Monitoring of methicillin-resistant Staphylococcus aureus (MRSA) was carried out in broilers, laying hens and fattening turkeys on farm in 2023. The bovines and pigs were monitored in 2021 and 2022, respectively (3 years-rotation). The aim of this monitoring is to assess the MRSA prevalence in these animal categories and determine the genotypes (STs and spa-types) of the collected MRSA isolates together with their AMR and virulence genes. In 2023, the MRSA prevalence was very low in broilers (1.0%) and moderate in fattening turkeys (18.5%) while null in laying hens. The MRSA prevalence remains stable since 2011 in broiler and laying hens and compared to 2020 (first year of turkey monitoring) in fattening turkeys. In 2023, all isolates (n=1 from broilers, n=5 from fattening turkeys) were genotyped as LA-MRSA according to their STs/spa-types combinations. All MRSA isolated in 2023 were harboring the mecA gene and the tet(M) tetracycline resistance gene, which are also characteristics of LA-MRSA. Several other resistance genes were observed and detailed in the results. All the 6 MRSA isolates were genetically multi-drug resistant (i.e., carrying genes conferring resistance to at least 3 different antibiotic classes). However, in 2023, no gene encoding resistance to the critically important antibiotics (linezolid and vancomycin) was detected. Moreover, several virulence genes associated with the human immune evasion cluster (sak, scn), associated with toxins (hlgA, hlgB, hlgC and selw) and/or exoenzymes (aur) were detected among the 6 MRSA isolates analysed in 2023. One LA-MRSA isolate from fattening turkeys carried the sak and scn genes associated with the human immune evasion cluster and several genes associated with toxins (hlgA, hlgB, hlgC, and selw) and exoenzyme (aur). This isolate would probably not have been recently transmitted from humans to turkeys, given the livestock-associated genetic background and the carriage of the tet(M) gene. The genes associated with the immune evasion cluster were not observed in the other isolates. The presence of MRSA in food-producing animals and their carriage of several AMR and virulence genes represents a public health risk. The monitoring of Enterococcus faecalis and Enterococcus faecium, organized in Belgium in foodproducing animals between 2011 and 2013, and resumed in 2019, continued. Investigation of the AMR prevalence in these commensal indicator bacteria was assessed in order to complete the picture of the situation of antimicrobial resistance within our farms and slaughterhouses. Enterococci are also considered to be reservoirs of antibiotic resistance genes, present in both humans and animals. In 2023, the prevalences of enterococci species by animal category were similar to those observed in previous years. Indeed, Enterococcus faecium was more frequently isolated than Enterococcus faecalis within the samples of breeding hens (88.4%), laying hens (72.0%), veal calves (54.8%) and pigs (62.3%). Conversely, E. faecalis was isolated more frequently than E. faecium in broiler (68.8%) samples. The antimicrobial susceptibility tests carried out this year showed that, in general, the resistance rates observed in Enterococcus faecalis and Enterococcus faecium within the various animal matrices studied have remained stable since 2019, with a few exceptions (significant decreases). Significant decreases in antimicrobial resistance were observed in 2023 for erythromycin in E. faecalis isolated from breeders, and for tetracycline in E. faecalis isolated from broilers in comparison to 2021. Resistance to tetracycline, erythromycin and to quinupristin/dalfopristin were still the most observed resistances, both in E. faecalis and E. faecium. Resistance to linezolid (n=16), a critical antibiotic for human health, was also observed in 2023, in 12 E. faecalis isolated from veal calves (n=11), pigs (n=1) and in 4 E. faecium isolated from pigs (n=3) and veal calves (n=1). Daptomycin resistance was low and observed in E. faecalis isolated 4 from breeders (n=1), layers (n=1) and pigs (n=1). Multidrug resistance was mainly observed in broilers and veal calves with 53.6% of multi-resistant E. faecium and 63.3 % of multi-resistant E. faecalis, respectively. No resistance to teicoplanin, tigecycline or vancomycin was observed in 2023. In 2023, some enterococci were sequenced by WGS. This report also presents these WGS results and the detailed characterization of these strains, including the detection of optrA gene encoding linezolid resistance. Taking together all results from both gram-negative (E. coli) and gram-positive indicators (enterococci) isolated from food-producing animals, resistance rates showed overall a decrease in 2023 in E. coli and a global status quo in enterococci (except 2 particular significant decreases).