Browsing by Author "Themudo, Patrícia"
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- Antimicrobial susceptibility of Escherichia coli strains isolated from food-producing, companion and wild animals, in Portugal – Characterization of isolates with reduced susceptibility to third generation cephalosporins and cephamycinsPublication . Clemente, Lurdes; Manageiro, Vera; Jones-Dias, Daniela; Ferreira, Eugénia; Correia, Ivone; Albuquerque, Teresa; Geraldes, Margarida; Matos, Filipa; Almendra, Claúdia; Themudo, Patrícia; Caniça, ManuelaEscherichia coli is a common inhabitant of the gastrointestinal tract of humans and animals, but is also a causative agent of diarrhea and extraintestinal infections. There is ongoing concern about the risks posed to human health by antimicrobial resistant bacteria isolated from animals. This study was conducted on 602 Escherichia coli isolates recovered from food-producing (n=217), companion (n=114) and wild animals (n=271), over the period of 2009-2013, to determine their antimicrobial susceptibility to a panel of ten antimicrobials (ampicillin, cefotaxime, ciprofloxacin, nalidixic acid, trimethoprim, sulfamethoxazole, chloramphenicol, streptomycine, gentamicine and tetracycline), through the determination of Minimum Inhibitory Concentration (MIC), using the agar dilution technique. Susceptibility to cefoxitin was determined through disk diffusion method. Molecular characterization of isolates showing a non-wild type MIC to cefotaxime was performed, to determine extended spectrum β-lactamases (ESBL), plasmid mediated AmpC (PMAβ), plasmid mediated quinolone (PMQR) resistance determinants and mobile genetic elements involved in the dissemination of resistance genes. Overall, isolates recovered from food producing animals showed higher frequencies of resistance towards all antimicrobials tested and multidrug resistance (MDR) (53%), followed by companion (43%) and wild animals (30%). Fifty isolates presented a non-wild phenotype to cefotaxime and resistance or intermediate susceptibility to cefoxitin, being 14 (12.3%) from pets, 19 (8.8%) from food producing animals and 17 (6.3%) from wild animals. Polymerase chain reaction and sequencing of the amplicons confirmed the presence of blaCTX-M-type (n=14), blaSHV-type (n=2), blaTEM-type (n=31), blaOXA-type (n=6) and plasmid-mediated AmpC β-lactamases (PMAβ) genes (n=8). Plasmid-mediated quinolone resistance-encoding genes were detected in ten isolates: aac(6')-Ib-cr (n=6) qnrB17 (n=1), qnrS1(n=1) and qnrB19 (n=2). Twenty five isolates carried class 1 integrons and two carried class 2 integrons. This study agrees that animals may act as important reservoirs of E. coli isolates carrying ESBL and PMAβ-encoding genes, which might be transmissible to humans through direct contact or the food chain and, a potential source for human pathogens to acquire these resistance genes.
- Antimicrobial susceptibility of Salmonella enterica isolated from food-producing animals, animal feed and food products of animal origin, in Portugal - Genetic analysis of isolates with reduced susceptibility/resistance to third generation cephalosporins and cephamycinsPublication . Clemente, Lurdes; Manageiro, Vera; Jones-Dias, Daniela; Ferreira, Eugénia; Correia, Ivone; Themudo, Patrícia; Albuquerque, Teresa; Caniça, ManuelaSalmonella is a widely distributed foodborne pathogen and one of the most common causes of bacterial foodborne illnesses in humans. An epidemiologic study was conducted on 1600 Salmonella spp isolates recovered from poultry, swine, other animal species, animal feed and food products of animal origin, over the period of 2009-2013, to determine their serotype and antimicrobial susceptibility to a panel of ten antimicrobials (ampicillin, cefotaxime, ciprofloxacin, nalidixic acid, trimethoprim, sulfamethoxazole, chloramphenicol, streptomycine, gentamicine and tetracycline), through the determination of Minimum Inhibitory Concentration (MIC), using the agar dilution technique. Molecular characterization of isolates showing a non-wild type MIC to cefotaxime was performed, to determine extended spectrum β-lactamases (ESBL), plasmid mediated AmpC (PMAβ), plasmid mediated quinolone (PMQR) resistance determinants and mobile genetic elements involved in the dissemination of resistance genes. In live poultry (breeders, broilers, layers) of the 843 isolates recovered, 27.9% comprised S. Enteritidis, 23,5% Salmonella Havana and 14.1% Salmonella Mbandaka; in turkeys, Salmonella Derby was the most common serovar isolated (44%), followed by Salmonella I 4,[5],12:i:- (16%). In swine, of 101 isolates 21.8% comprised Salmonella Rissen and Salmonella Typhimurium, 10.9% Salmonella Derby and Salmonella London. In other animal species, Salmonella Typhimurium was the prevalent serovar with 65.6% of the isolates, followed by Salmonella I 4,[5],12:i:- (9.8%). Overall, S. 4,[5],12:i:- was the most common serotype recovered from food products (25.8%), followed by S. Typhimurium (19.2%) and Salmonella Rissen (18.4%). S. Enteritidis was the most frequent serotype in poultry products (36.3%). Susceptibility profiles differed according with the serotype and the origin of the isolates. A higher frequency of multidrug resistant isolates was recovered from food of swine and bovine origin, with 62.6% and 59.4%, respectively. Polymerase chain reaction and sequencing of the amplicons confirmed the presence of blaCTX-M-type (n=8), blaSHV-type (n=2), blaTEM-type (n=2) and plasmid-mediated AmpC β-lactamases (PMAβ) genes (n=2). No plasmid mediated quinolone resistance-encoding genes were detected. Six isolates( three S. I 4,[5],12:i:-, two S. Havana and one S. Enteritidis) carried class 1 integrons and one S. I 4,[5],12:i:- isolate harboured a class 2 integron. In conclusion, the growing concern of the emergence of bacterial strains bearing ESBL in food-producing animals highlights the importance of continuous monitoring.
- Antimicrobial susceptibility of Salmonella enterica isolates from healthy breeder and broiler flocks in PortugalPublication . Clemente, Lurdes; Correia, Ivone; Themudo, Patrícia; Neto, Isabel; Caniça, Manuela; Bernardo, FernandoThree hundred and thirty-three isolates representing 40 different serotypes of Salmonella enterica, recovered from environmental and faecal samples of breeder and broiler flocks from 2009 to 2011, were studied. Antimicrobial susceptibility was determined by measuring the minimal inhibitory concentration of 11 antimicrobials using the agar dilution method. Salmonella Havana, S. Enteritidis and S. Mbandaka were the most common serotypes isolated from broiler flocks, while S. Enteritidis was the common isolate from breeder flocks. The frequency of non-wild-type Salmonella isolates (those with decreased susceptibility to the different antimicrobials) varied according to serotype. S. Mbandaka in broilers and S. Enteritidis in both breeders and broilers showed higher frequencies of reduced susceptibility to quinolones, but clinical resistance towards ciprofloxacin was not observed. Reduced susceptibility to sulfamethoxazole, tetracycline, ampicillin and streptomycin were common in Salmonella Typhimurium isolates. Two isolates of S. Havana from broilers were resistant to cefotaxime and phenotypically categorised as extended-spectrum β-lactamase producers. The results presented in this study provide useful data on the antimicrobial susceptibility of different Salmonella serotypes and highlight the high diversity of multi-drug resistance patterns present.
- Diversity of β-lactamase-encoding genes in Escherichia coli strains isolated from food-producing, companion and zoo animals in PortugalPublication . Clemente, Lurdes; Correia, Ivone; Albuquerque, Teresa; Geraldes, Margarida; Matos, Filipa; Themudo, Patrícia; Manageiro, Vera; Jones-Dias, Daniela; Ferreira, Eugénia; Caniça, ManuelaA rapid development of plasmid-mediated resistance to extended-spectrum cephalosporins has been observed in Enterobacteriaceae worldwide, predominantly due to the dissemination of extended-spectrum beta-lactamases (ESBL) and plasmid-mediated AmpC beta-lactamases (PMAB). The aim of the present study was to evaluate the extension of ESBL- and PMAB-producing E. coli strains isolated from different animal origins in Portugal. For surveillance purposes, 376 E. coli isolates identified at National Laboratory of Veterinary Research (2009-2011) were submitted to antimicrobial susceptibility testing: 123, 51 and 202 were isolated from food-producing, companion and zoo animals, respectively. Minimum Inhibitory Concentrations (MIC) of 11 antimicrobials for all isolates was determined through agar dilution method. Susceptibility towards cefoxitina was determined through disk diffusion method. Breakpoints were interpreted accordingly to EUCAST epidemiological cut-off values. ‘Non-wild type’ (NWT) isolates for cefotaxime (MIC>0.25mg/L) and/or cefoxitina (<19mm) were screened for the presence of ESBL (blaTEM, blaOXA, blaSHV, blaCTX) and PMAB encoding genes, using PCR method. Sequencing was applied to fully identify beta-lactamases. Seventeen isolates (4.5%) were ‘NWT’ strains for cefotaxime, being 5 (29.4%) from companion animals, 4 (23.5%) from food-producing animals and 8 (47.1%) from zoo animals. We identified blaCTX-M-14 (n=1) in a dog and blaCTX-M-15-type genes (n=9) in 6 zoo animals and 3 in food-producing animals. We also identified blaCMY-type genes (n=3) in ‘NWT’ isolates for cefoxitin, one from each animal category. Other beta-lactamase encoding genes were identified: blaOXA in 5 strains (29.4%) isolated from dolphins, blaTEM in 7 strains (41.2%) isolated from 3 companion animals, 2 food-producing and 2 zoo animals, and blaSHV identified in one isolate (5.9%) from a zoo animal; 13 beta-lactamase-producing isolates (76.5%) were multidrug resistant. Among ‘NWT’ E. coli isolates for cefotaxime, we identified an important diversity of ESBL encoding genes, belonging to different families, being blaCTX-M-15-type gene the predominant. The spread of ESBL-producing bacteria among species from different origins, such as food-producing, companion and zoo animals, is a concern at public health level. Thus, it should be a priority to monitor and identify the reservoirs of antimicrobial resistance, contributing to a single health for all.
- Epidemiology and zoonotic potential of Escherichia coli CTX-M-15-producing isolates in PortugalPublication . Caniça, Manuela; Clemente, Lurdes; Jones-Dias, Daniela; Manageiro, Vera; Themudo, Patrícia; Albuquerque, Teresa; Francisco, Ana Patrícia; Louro, Deolinda; Ferreira, EugéniaBackground: The recent spread of plasmid-located CTX-M-ESBL-encoding genes is a serious threat to the clinical efficacy of expanded-spectrum cephalosporins. This study proposes to identify the epidemiology of plasmid-mediated CTX-M-encoding genes between an Escherichia coli strain isolated from a dolphin and several E. coli strains of human origin and, explain the responsible mechanism and reservoirs of current spread of CTX-M-type enzymes. Molecular typing of these strains establishes the linkage of dissemination between human and animal isolates. Methods: Sixty two ESBL-positive E. coli strains isolated from different clinical specimens in seven hospitals (2004 to 2009), from four different geographic regions, were screened for the presence of CTX-M encoding genes. An E. coli isolated from a respiratory exsudate in a dolphin in 2009, at the National Laboratory of Veterinary Research (LNIV) and characterized as CTX-M-producer, was also included in this study. Antimicrobial susceptibility was performed by broth-microdilution method. PCR and sequencing were used to screen and identify bla genes. Genetic relatedness among all isolates was examined by PFGE using XbaI enzyme. MLST was performed among the clinical epidemic human isolates clustering together and the isolate from the dolphin, according to the MLST database. Results: Forty eight human clinical isolates (77%) were CTX-M producers. Susceptibility towards beta-lactams confirmed all isolates as ESBL producers and also suggesting CTX-M enzymes expression. We detected blaCTX-M-15 (n=34), blaCTX-M-1 (n=4), blaCTX-M-3 (n=3), blaCTX-M-32 (n=3), blaCTX-M-14 (n=4), blaTEM-1 (n=39), and blaSHV-12 (n=8) genes; the dolphin isolate presented the blaCTX-M-15 gene. Genetic relatedness analysis by PFGE revealed one major cluster corresponding to a single epidemic clone A, which included 22 (35%) of all human isolates and the dolphin isolate, which clustered together with this clone A and, exhibited the same combination of MLST alleles across the seven sequenced loci, corresponding to the ST131. Twenty-one clinical isolates corresponding to the CTX-M-15-positive clone A were multidrug-resistant (95%), as well as the dolphin isolate. Conclusions: This study illustrated that genetic relatedness between human and animal E. coli CTX-M-15-producing clone strengthens its zoonotic potential. It may also explain the current spread of CTX-M-type enzymes worldwide among species from different origins and highlights the importance to identify antimicrobial resistance reservoirs, contributing to a single health for all.
- Multidrug-Resistant Salmonella enterica Serovar Rissen Clusters Detected in Azores Archipelago, PortugalPublication . Silveira, Leonor; Pinto, Miguel; Isidro, Joana; Pista, Ângela; Themudo, Patrícia; Vieira, Luís; Machado, Jorge; Gomes, João PauloGastrointestinal infections caused by nontyphoidal Salmonella (NTS) remain one of the main causes of foodborne illness worldwide. Within the multiple existing Salmonella enterica serovars, the serovar Rissen is rarely reported, particularly as a cause of human salmonellosis. Between 2015 and 2017, the Portuguese National Reference Laboratory of Gastrointestinal Infections observed an increase in the number of clinical cases caused by multidrug-resistant (MDR) S. enterica serovar Rissen, particularly from the Azores archipelago. In the present study, we analyzed by whole genome sequencing (WGS) all clinical, animal, food, and environmental isolates received up to 2017 in the Portuguese Reference Laboratories. As such, through a wgMLST-based gene-by-gene analysis, we aimed to identify potential epidemiological clusters linking clinical and samples from multiple sources, while gaining insight into the genetic diversity of S. enterica serovar Rissen. We also investigated the genetic basis driving the observed multidrug resistance. By integrating 60 novel genomes with all publicly available serovar Rissen genomes, we observed a low degree of genetic diversity within this serovar. Nevertheless, the majority of Portuguese isolates showed high degree of genetic relatedness and a potential link to pork production. An in-depth analysis of these isolates revealed the existence of two major clusters from the Azores archipelago composed of MDR isolates, most of which were resistant to at least five antimicrobials. Considering the well-known spread of MDR between gastrointestinal bacteria, the identification of MDR circulating clones should constitute an alert to public health authorities. Finally, this study constitutes the starting point for the implementation of the "One Health" approach for Salmonella surveillance in Portugal.
- Occurrence of extended-spectrum beta-lactamases in Salmonella enterica strains isolated from broilers and food of animal origin in PortugalPublication . Clemente, Lurdes; Correia, Ivone; Themudo, Patrícia; Albuquerque, Teresa; Manageiro, Vera; Jones-Dias, Daniela; Ferreira, Eugénia; Caniça, ManuelaSalmonella enterica is a zoonotic bacteria transmitted through the food chain and isolates harbouring extended-spectrum beta-lactamases (ESBLs) have emerged worldwide during the last decade, with the CTX-M group being particularly important. The aim of the present study was to determine the antimicrobial susceptibility of S. enterica strains isolated from broilers and food of animal origin and to characterize ESBLs producers. On the scope of the national antimicrobial resistance surveillance programme on Salmonella, a total of 283 strains isolated from broilers (n=100) and food of animal origin (n=183), were received at the National Laboratory of Veterinary Research in 2011. The minimum inhibitory concentration (MIC) of 11 antimicrobials (nalidixic acid, ciprofloxacin, ampicillin, cefotaxime, chloramphenicol, florfenicol, streptomycin, gentamicin, tetracycline, sulphamethoxazole and trimethoprim) for all isolates was determined by agar dilution method. Susceptibility towards cefoxitin was determined through disk diffusion method. Breakpoints were interpreted accordingly to EUCAST epidemiological cut-off values. ‘Non-wild type’ (‘NWT’) isolates for cefotaxime (MIC>0.5mg/L) and cefoxitin (<19mm) were screened for the presence of ESBL- (blaTEM, blaOXA, blaSHV, blaCTX) and PMA_-encoding genes, using PCR method. Sequencing was applied to fully identify beta-lactamases. Among broilers, we identified 62% of ‘NWT’ isolates for ciprofloxacin, 57% for nalidixic acid and 28% for sulphamethoxazole, whereas in isolates from food of animal origin, 71%, 63% and 56% were ‘NWT’ isolates for tetracycline, sulphamethoxazole and ampicillin, respectively. Among all, 5/283 (1.8%) strains presented ‘NWT’ MICs for cefotaxime and were multidrug resistant: 2 Salmonella Havana isolated from broilers and 3 Salmonella S. 4,[5],12:i:- isolated from food of animal origin (swine); these isolates had one blaCTX-M-type gene, and 2 from food of animal origin presented 1 blaTEM-type gene and 1 blaSHV-type gene, respectively; they were ‘wild type’ for cefoxitin and no PMAB-encoding gene was detected. To our knowledge, this is the first time in Portugal that ESBL-encoding genes, particularly from blaCTXM family, were detected in isolates of Salmonella Havana, a very common serotype isolated from our broiler population. It should also be emphasised that third generation cephalosporins are not allowed in the national poultry production, contrary to the large animal production, which may explain the detection of ESBL-encoding genes in our strains from swine origin. Horizontal gene transfer may be responsible for the coresistance of strains to non-beta-lactam antibiotics. This study shows that national animal health monitoring systems play an important role and should be improved in an international level.
- Occurrence of extended-spectrum β-lactamases among isolates of Salmonella enterica subsp. enterica from food-producing animals and food products, in PortugalPublication . Clemente, Lurdes; Manageiro, Vera; Ferreira, Eugénia; Jones-Dias, Daniela; Correia, Ivone; Themudo, Patrícia; Albuquerque, Teresa; Caniça, ManuelaA total of 1120 Salmonella spp. isolates, recovered from poultry, swine and food products of animal origin (bovine, swine and poultry) over the period of 2009-2011, were investigated in order to determine their serotype, susceptibility to a panel of eleven antimicrobials (A, ampicillin; Ct, cefotaxime; Cp, ciprofloxacin; Tm, trimethoprim; Su, sulfamethoxazole; C, chloramphenicol; S, streptomycin; G, gentamicin; T, tetracycline; NA, nalidixic acid; Fl, florfenicol), and the presence of resistance determinants of extended-spectrum cephalosporins. Overall, Salmonella Enteritidis was the most common serotype in all three animal species. In 618 isolates of poultry, 32.8% comprised S. Enteritidis, 18.3% Salmonella Havana and 16.5% Salmonella Mbandaka; in 101 isolates of pigs, 21.8% comprised Salmonella Rissen and Salmonella Typhimurium, 10.9% Salmonella Derby and Salmonella London. Salmonella I 4,[5],12:i:- was the most common serotype recovered from pork and beef food products comprising 32.6% and 30% of isolates respectively, followed by S. Rissen (26% and 24%) and S. Typhimurium (18.2% and 19%), respectively. In poultry products, S. Enteritidis was the most frequent serotype (62.7%), followed by S. Mbandaka (10.2%) and S. Derby (8.5%). Susceptibility profiles differed according to the origin of the isolates. Five multidrug resistant isolates (0.45%) were further characterized as extended-spectrum β-lactamase (ESBL) producers. Polymerase chain reaction and sequencing of the amplicons confirmed the presence of bla(CTX-M-1) (n = 2), bla(CTX-M-14) (n = 1), bla(CTX-M-15) (n = 1) and bla(CTX-M-32) (n = 1); bla(SHV-12) and bla(TEM-1) genes were also detected in two isolates of S. I 4,[5],12:i:-. Four isolates, two S. Havana and two S. I 4,[5],12:i:-, carried class 1 integrons and in three, two S. I 4,[5],12:i:- and one S. Havana, ISEcp1 was identified associated to bla(CTX-M-1), bla(CTX-M-32) and bla(CTX-M-14) genes. Additionally, in one S. I 4,[5],12:i:- isolate, orf477 was identified linked to bla(CTX-M-32). No plasmid mediated quinolone resistance-encoding genes were detected. Here, we report for the first time the presence of bla(CTX-M) genes in Salmonella enterica subsp enterica isolates recovered from poultry and food products of swine origin, in Portugal.
- Occurrence of plasmid-mediated quinolone resistance among bacteria isolated in animals in PortugalPublication . Ferreira, Eugénia; Clemente, Lurdes; Jones-Dias, Daniela; Francisco, Ana Patrícia; Manageiro, Vera; Themudo, Patrícia; Albuquerque, Teresa; Amado, Alice; Caniça, ManuelaBackground: Plasmid-mediated quinolone resistance (PMQR) is increasingly identified worldwide in Enterobacteriaceae. The aim of this study was to evaluate the extension of PMQR in isolates from animals in Portugal. Methods: We screened 186 Enterobacteriaceae isolates for the presence of PMQR determinants, identified at National Laboratory of Veterinary Research (2008-2009). A total of 92 Salmonella isolates were isolated from broilers, layers and pigs, and 94 Escherichia coli were from farm animals, birds and mammals. Susceptibility testing of all isolates was performed by disk diffusion method, and MICs against nalidixic acid, ciprofloxacin, gatifloxacin, levofloxacin, ofloxacin, enrofloxacin, morbifloxacin and norfloxacin were determined by E-test for PMQR-positive isolates. PCR and nucleotide sequencing, by using specific primers, were used to screen for the presence of PMQR-encoding genes. The genetic context of PMQR genes was evaluated by using different molecular methods. Results: We identified 5 qnrC-positive isolates: 2 Salmonella enteritidis collected in 2 layer chicken and in 3 E. coli from 2 broilers and one pig; 3 qnrS1 genes were detected in E. coli isolates from a broiler (co-expressing a qnr-C gene), a dog and a turtle-dove. The aac-(6’)-Ib-cr gene was detected in an E. coli isolated from a mammalian. Seven PMQR-positive isolates showed diminished susceptibility to at least one quinolone, and one was detected in the range of susceptibility against the seven (fluoro)quinolones tested. Three E. coli and one S. enteritidis were PMQR- and TEM-1 and/or CTX-M-15-producing isolates. An E. coli with qnrC, qnrS1, and blaTEM-1 genes and an E. coli with qnrC gene were positive for genes coding to class 1 integrons. Conclusions: This survey showed that PMQR determinants are present in animals from different environments in Portugal, including food-producing animals, with a high frequency (3%) of QnrC-producing isolates. Susceptibility results demonstrate the difficulty to predict the PMQR mechanisms by phenotypic methods. Overall, the study suggests that PMQR genes are undergoing a dissemination process, which needs surveillance.
- QnrS1- and Aac(6')-Ib-cr-Producing Escherichia coli among Isolates from Animals of Different Sources: Susceptibility and Genomic CharacterizationPublication . Jones-Dias, Daniela; Manageiro, Vera; Graça, Rafael; Sampaio, Daniel A.; Albuquerque, Teresa; Themudo, Patrícia; Vieira, Luís; Ferreira, Eugénia; Clemente, Lurdes; Caniça, ManuelaSalmonella enterica and Escherichia coli can inhabit humans and animals from multiple origins. These bacteria are often associated with gastroenteritis in animals, being a frequent cause of resistant zoonotic infections. In fact, bacteria from animals can be transmitted to humans through the food chain and direct contact. In this study, we aimed to assess the antibiotic susceptibility of a collection of S. enterica and E. coli recovered from animals of different sources, performing a genomic comparison of the plasmid-mediated quinolone resistance (PMQR)-producing isolates detected. Antibiotic susceptibility testing revealed a high number of non-wild-type isolates for fluoroquinolones among S. enterica recovered from poultry isolates. In turn, the frequency of non-wild-type E. coli to nalidixic acid and ciprofloxacin was higher in food-producing animals than in companion or zoo animals. Globally, we detected two qnrS1 and two aac(6')-Ib-cr in E. coli isolates recovered from animals of different origins. The genomic characterization of QnrS1-producing E. coli showed high genomic similarity (O86:H12 and ST2297), although they have been recovered from a healthy turtle dove from a Zoo Park, and from a dog showing symptoms of infection. The qnrS1 gene was encoded in a IncN plasmid, also carrying bla TEM-1-containing Tn3. Isolates harboring aac(6')-Ib-cr were detected in two captive bottlenose dolphins, within a time span of two years. The additional antibiotic resistance genes of the two aac(6')-Ib-cr-positive isolates (bla OXA-1, bla TEM-1,bla CTX-M-15, catB3, aac(3)-IIa, and tetA) were enclosed in IncFIA plasmids that differed in a single transposase and 60 single nucleotide variants. The isolates could be assigned to the same genetic sublineage-ST131 fimH30-Rx (O25:H4), confirming clonal spread. PMQR-producing isolates were associated with symptomatic and asymptomatic hosts, which highlight the aptitude of E. coli to act as silent vehicles, allowing the accumulation of antibiotic resistance genes, mobile genetic elements and other relevant pathogenicity determinants. Continuous monitoring of health and sick animals toward the presence of PMQR should be strongly encouraged in order to restrain the clonal spread of these antibiotic resistant strains.