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VETMIC-6593; No. of Pages 4 Veterinary Microbiology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Veterinary Microbiology journal homepage: www.elsevier.com/locate/vetmic
Preface
Antimicrobial resistance in bacteria from animals and the environment
Antimicrobial resistance in bacteria has become a major public health issue during the past decade. Antimicrobial agents are indispensable in the control of bacterial infections, not only in humans, but also in animals and plants. Every use of an antimicrobial agent selects for bacteria with elevated minimal inhibitory concentrations. Under the selective pressure imposed by the use of antimicrobial agents, bacteria which possess resistance mechanisms can multiply and expand at the expense of the bacteria that are inhibited by the respective antimicrobial agents. Moreover, bacteria can pass resistance genes to other bacteria through horizontal gene transfer and thereby contribute to the dissemination of resistance genes within bacterial populations of different ecosystems. In polymicrobial environments, such horizontal gene transfer processes may involve donors and recipients that belong to different bacterial species and genera. These basic facts apply not only to bacteria of human origin, but also to those of animal and environmental origin – a situation that is reflected by the ‘‘One Health’’ concept. Antimicrobial resistance in bacteria is a highly multifaceted topic at the interface of human, animal and plant health, food hygiene and environmental science. Besides the analysis of resistance genes and resistancemediating mutations, the dissemination of resistance properties and the analysis of mobile genetic elements that play a role in the spreading of resistance genes across species and genus boundaries, numerous other aspects play an important role when dealing with antimicrobial resistance. These include among others (i) pharmacological aspects with regard to the application of antimicrobial agents, (ii) methodological aspects with regard to the correct performance of antimicrobial susceptibility testing, (iii) antimicrobial resistance monitoring programmes, (iv) antimicrobial stewardship, (v) animal models, (vi) antimicrobial resistance in bacteria from specific sources, such as wildlife, aquaculture, foodproducing animals, companion animals and the environment, and (vii) alternative, non-antimicrobial strategies
to control bacterial infections. All these aspects were addressed during the 5th Symposium on Antimicrobial Resistance in Animals and the Environment (ARAE 2013), which was held from June 30 to July 3, 2013 in Ghent, Belgium. The forum provided an important venue for networking between and discussion among scientists engaged in understanding different aspects of the antibiotic resistance problem, and in finding ways to mitigate the impact of resistance. This Special Issue of Veterinary Microbiology captures the flavour and quality of the wideranging presentations made at the Symposium, and will be a useful single source resource for workers in this field. This symposium, which is held in 2-years intervals since 2005, comprised one keynote lecture and another six invited lectures given by experts in the specific fields. In his keynote lecture, John F. Prescott summarized the situation with regard to antimicrobial agents and antimicrobial resistance during the past 60 years. He illustrated that changes in the practice of how we use antimicrobial agents are unavoidable and that Good Stewardship Practice should be adopted by everyone involved in antimicrobial use and application. Despite increasing percentages of resistant bacteria and decreasing numbers of new antimicrobial agents – especially for use in veterinary medicine – he also emphasized the availability of new technologies, such as whole genome sequencing, which may be used for the identification of new bacterial targets that serve for the development of future antimicrobial agents for specific bacterial pathogens and disease conditions (Prescott, 2014). Moreover, 42 oral presentations (selected from the submissions) and 83 poster presentations completed the programme of this symposium. This Special Issue of Veterinary Microbiology comprises a collection of review articles, original research papers and short communications from contributions presented at the ARAE 2013 symposium. The following paragraphs provide a short summary of the different studies compiled in this Special Issue based on their assignment to topics of the symposium.
http://dx.doi.org/10.1016/j.vetmic.2014.04.009 0378-1135/ß 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Butaye, P., et al., Antimicrobial resistance in bacteria from animals and the environment. Vet. Microbiol. (2014), http://dx.doi.org/10.1016/j.vetmic.2014.04.009
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1. Antimicrobial resistance monitoring and susceptibility testing One review compared the technical specifications on monitoring of antimicrobial resistance in zoonotic Salmonella, Campylobacter and indicator Escherichia coli and Enterococcus as performed by the European Food Safety Authority (EFSA) with veterinary pharmaceutical industry’s European Antimicrobial Susceptibility Surveillance in Animals (EASSA) programme. The major difference between the two programmes is the classification into ‘susceptible’ versus ‘resistant’. Whilst EFSA categorizes all isolates with an MIC value above the epidemiological cutoff value as ‘resistant’, EASSA differentiates between ‘percentage decreased susceptible’ and ‘percentage clinical resistant’ strains by applying both epidemiological cut-off values and clinical breakpoints (Moyaert et al., 2014). Another study dealt with the determination of quality control (QC) ranges for cefoperazone 30 mg disks for the internationally accepted QC strains Staphylococcus aureus ATCC1 25923 and E. coli ATCC1 25922. QC parameters are indispensable instruments to assure the correct performance of in vitro susceptibility testing (Feßler et al., 2014). 2. Antimicrobial resistance in Gram-negative bacteria from livestock and companion animals One review recapitulated carbapenemase producing E. coli, Salmonella spp. (VIM-1 producers) and Acinetobacter spp. (producing OXA-23 and NDM-1) in livestock animals (poultry, cattle and swine) and their environment, but also NDM-1-producing E. coli, OXA-48 in E. coli and Klebsiella pneumoniae or OXA-23 in Acinetobacter spp. from companion animals (cats, dogs or horses), NDM-1-producing Salmonella isolated from wild birds, as well as OXA-23like-producing Acinetobacter baumanii in ectoparasites (Guerra et al., 2014). A survey study on antimicrobial resistance among Salmonella isolates from healthy pigs (n = 368) and chickens (n = 452) in Belgium was conducted during the years 2008–2011. ESBL/AmpC producers were particularly prevalent in chickens (12.8%), and much less in pigs (1.9%). Among the cephalosporin-resistant isolates, blaCTX-M (mostly blaCTXM-1, but also blaCTXM-2 and blaCTXM9) and blaTEM-52 were the predominant ESBL genes (de Jong et al., 2014). Another study focused on the characterization of quinolone resistance mechanisms in Salmonella isolated from animals, food, and feed between 2008 and 2011 in Poland. Besides resistance-mediating mutations in gyrA, plasmidic quinolone resistance genes qnrS1/qnrS3 and qnrB19/qnrB10 were also identified (Wasyl et al., 2014). A study from Norway aimed at estimating the prevalence of cephalosporin-resistant E. coli at the different levels of the Norwegian broiler production pyramid and identifying the respective resistance mechanisms. The occurrence of cephalosporin-resistant E. coli at the different production levels ranged from 8 to 43%. All resistant isolates had an AmpC-phenotype and the majority carried the blaCMY-2 gene (Sølverød Mo et al., 2014). In France, 491 veal calves from different slaughtering batches at twelve abattoirs were investigated in 2012 for the presence of ESBL-producing Enterobacteriaceae. A prevalence of 29.4%
of ESBL-producers in the faecal flora was identified and various blaCTX-M genes were detected. The authors suggested that veal calves may constitute one of the major ESBL reservoirs in food animals (Haenni et al., 2014). Trends in resistance to antimicrobials among Actinobacillus pleuropneumoniae, Pasteurella multocida, Mannheimia haemolytica and E. coli isolates from clinical cases of cattle and swine diseases in the Czech Republic from 2007 to 2011 were determined. Moreover, sales figures for betalactam antimicrobial agents during the same period were determined and compared for pigs and cattle (Nedbalcova et al., 2014). 3. Antimicrobial resistance in Gram-positive bacteria from livestock and companion animals One review dealt with the antimicrobial resistance of methicillin-susceptible (MSSP) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) – a commensal and common opportunistic pathogen in dogs. For this, the authors revisited the published literature during 1980– 2013. Stratified by MSSP and MRSP, no significant increases in antimicrobial resistance were observed over time, except for the penicillinase-labile penicillins (penicillin and ampicillin) among MSSP. The review highlighted inconsistencies between studies as a result of several factors, for example the use of different antimicrobial susceptibility testing methods and interpretation criteria (Moodley et al., 2014). Another comprehensive review dealt with the ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Although often considered as harmless commensals, members of the S. sciuri species group have also been found to carry multiple virulence and resistance genes including genes implicated in biofilm formation or coding for toxins responsible of toxic shock syndrome and multi-resistance. The authors concluded that further studies into the role of the S. sciuri species group as commensal and pathogenic bacteria are required to fully assess its medical and veterinary importance (Nemeghaire et al., 2014a). Methicillin-resistant S. sciuri (MRSS) in healthy chickens were the topic of a study conducted in Belgium. Eighty-seven MRSS were isolated resulting in an estimated prevalence of 31.0%. The prevalence in broilers did not significantly differ from that in layers. Most MRSS isolates harboured a non-typeable or type III SCCmec and were multiresistant (Nemeghaire et al., 2014b). A study conducted in The Netherlands focused on methicillin-resistant Staphylococcus aureus (MRSA) from dairy cattle at slaughter. Sixteen of 411 (3.9%) cows, all originating from different farms, were found to be MRSA positive. All MRSA isolates belonged to livestock-associated clonal complex 398, were PVL-negative and spa type t011 predominated. No isolates carrying mecC were detected (van Duijkeren et al., 2014). In a study conducted in Germany, 112 S. aureus and 110 coagulasenegative Staphylococcus spp. (CoNS) isolates from cases of bovine mastitis were tested comparatively for tylosin and erythromycin susceptibility by broth microdilution and agar disc diffusion with 30 mg tylosin disks. PCR analysis of the 25 erythromycin-resistant staphylococcal isolates identified the resistance genes erm(A), erm(B), erm(C), erm(T), mph(C) and msr(A) alone or in different combinations. An excellent
Please cite this article in press as: Butaye, P., et al., Antimicrobial resistance in bacteria from animals and the environment. Vet. Microbiol. (2014), http://dx.doi.org/10.1016/j.vetmic.2014.04.009
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correlation between the results of broth microdilution and disc diffusion were seen for S. aureus and CoNS isolates (Entorf et al., 2014). A study conducted in Belgium reported the zone diameter distributions for numerous antimicrobial agents among S. aureus (n = 768), Streptococcus uberis (n = 939), Streptococcus dysgalactiae (n = 444), E. coli (n = 563), and Klebsiella spp. (n = 59) obtained from cases of (sub) clinical mastitis. The authors emphasized the need for clinical breakpoints applicable to causative agents of bovine mastitis (Supre´ et al., 2014). In a study on MRSA isolates from Dutch broiler farms, an MRSA CC398 isolate was identified which harboured two structurally unrelated erm(C)-carrying plasmids of 2458 bp and 3882 bp. The fact that both plasmids belong to different incompatibility groups as specified by the different rep genes, repL and repF, explains why they can stably coexist in the same bacterial cell (Wendlandt et al., 2014). Another study investigated the influence of specific and non-specific selective pressure on the in vivo spread of macrolide-lincosamide-streptogramin B (MLSB) resistance in chickens. For this, chickens were inoculated with Enterococcus faecalis harbouring the erm(B)-carrying plasmid pAMb1. The results of that study suggested that (i) erm(B)-mediated MLSB resistance may spread within the gut microbiota under specific and non-specific pressure and even in the absence of any antimicrobial pressure, and (ii) different bacterial species seem to be involved in the spread of MLSB resistance (Marosevic et al., 2014). 4. Antimicrobial resistance in fish bacterial pathogens The molecular characterization of antibiotic resistance among 116 Pseudomonas and 92 Aeromonas isolates from catfish of the Mekong Delta, Vietnam, showed percentages of multiple drug resistance of 96.6% and 61.9% among Pseudomonas and Aeromonas isolates, respectively. Large resistance plasmids (>55 kb) were frequently detected and conjugation and transformation experiments demonstrated the successful transfer of all or part of the resistance phenotypes of catfish isolates to the recipient strains (Nguyen et al., 2014). A study from Germany investigated the antimicrobial resistance pheno- and genotypes of Yersinia ruckeri from fish. Elevated MICs to fluoroquinolones were associated with mutations in gyrA. A single isolate showed elevated MICs for sulfonamides and trimethoprim and harboured a 8.9 kb plasmid, which carried the genes sul2, strB and a dfrA14 gene cassette integrated into the strA gene (Huang et al., 2014). The role of ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids was investigated in a study conducted in the Czech Republic. Fifteen (19%, n = 80) isolates from koi carps and 18 (24%, n = 76) isolates from imported ornamental fish were positive for qnrS2, aac(60 )-Ib-cr or qnrB17 genes. Related IncU plasmids harbouring qnrS2 and aac(60 )-Ib-cr genes were found in Aeromonas spp. from imported ornamental fish and koi carp (Dobiasova et al., 2014). 5. Antimicrobial resistance in bacteria from wildlife The antimicrobial resistance of Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic, was investigated with emphasis on
3
ESBL and plasmid-mediated quinolone resistance (PMQR) genes. Among wildlife, the most significant findings were CTX-M-15-producing K. pneumoniae in a habituated gorilla and a multi-resistant E. coli isolate with the qepA gene in an unhabituated gorilla. Other isolates from wildlife were mostly qnrB-harbouring Citrobacter spp. (Janatova et al., 2014). During a study on Enterobacteriaceae in wild birds in Arctic Svalbard, Norway, an E. cloacae isolate originating from Glaucous gull (Larus hyperboreus) carrying the novel blaACT-23 AmpC beta-lactamase gene was identified (Literak et al., 2014). A study conducted in Portugal investigated the antimicrobial resistance determinants of Staphylococcus spp. recovered from birds of prey. A wide variety of resistance genes, including blaZ, mecA, tet(K), tet(L), dfrA, dfrG, fusC, msr(A), mph(C), ant60 -Ia, catpC221, catpC223 and catpC194, were mainly detected in CoNS (Sousa et al., 2014). 6. The environment as a reservoir of resistance genes One review investigated the impact of wastewater treatment plant (WWTP) effluents into a river by comparatively investigating water samples upstream and downstream of the WWTP. For this, metagenomic libraries were constructed in E. coli and screened for pheno- and genotypic resistance. An increasing number of resistant clones from downstream waters was detected. The authors conclude that waste water disposal increases the reservoir of resistance mechanisms in the environment either by addition of resistance genes or by input of agents selective for resistant phenotypes (Amos et al., 2014). A study conducted in The Netherlands investigated the prevalence and the characteristics of ESBL-producing E. coli in four Dutch recreational waters and the possible role of nearby WWTPs as contamination source. ESBL-producing E. coli were detected in all four recreational waters. WWTPs were shown to contribute to the presence of these bacteria in surface waters, although other yet unidentified sources were likely to co-contribute to the presence of ESBLproducing E. coli (Blaak et al., 2014). 7. Phages as an alternative to antimicrobial agents A review about phage therapy argued that phage therapy has not revealed all of its secrets and many parameters remain understudied, making the outcome of phage therapy highly variable depending on the disease condition. According to the authors, the main obstacles on the way to a successful phage therapy include poorly understood mechanisms of phage penetration and distribution throughout the body, the variable expression and accessibility of phage receptors on the bacterial host under in vivo conditions and the unusual (non-linear) phage pharmacokinetics. These parameters are not easily measured in realistic in vivo settings, but are nevertheless important hurdles to overcome the high variability of phage therapy trials (Tsonos et al., 2014b). A study was conducted to evaluate the effect of a cocktail of in vitro efficient phages to protect experimentally infected chickens against avian pathogenic E. coli. The phage cocktail was administered two hours after the infection intratracheally, intraoesophageally or via the drinking water. Treated groups did not show
Please cite this article in press as: Butaye, P., et al., Antimicrobial resistance in bacteria from animals and the environment. Vet. Microbiol. (2014), http://dx.doi.org/10.1016/j.vetmic.2014.04.009
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a significant decrease in mortality, lesion scores or weight loss compared to untreated groups. The authors concluded that the efficiency of the phage cocktail used in treating APEC-infected chickens in vivo is negligible, even though in vitro, the phages in the cocktail were able to efficiently lyse the APEC strain (Tsonos et al., 2014a). 8. Pharmacological aspects A review dealt with the application of pharmacokinetic–pharmacodynamic (PK–PD) principles to dosing regimens as a strategy to decrease inappropriate use of antimicrobial agents in veterinary medicine. The author emphasized applying these PK–PD principles to attain targets for area-under-the-curve to MIC ratio (AUC/MIC), peak concentration to MIC ratio (CMAX/MIC), and time above MIC (T > MIC) as a prerequisite for a more effective antimicrobial therapy. In addition, the author pointed towards the use of accurate interpretive criteria, such as the CLSI-approved veterinary-specific clinical breakpoints for identifying the most efficient antimicrobial agent for therapeutic applications (Papich, 2014). References Amos, G.C., Zhang, L., Hawkey, P.M., Gaze, W.H., Wellington, E.M., 2014. Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet. Microbiol., VETMIC-D-138994R1/VETMIC_6519. Blaak, H., de Kruijf, P., Hamidjaja, R.A., van Hoek, A.H.A.M., de Roda Husman, A.M., Schets, F.M., 2014. Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants. VETMIC-D-13-8770R1/VETMIC_6554 de Jong, A., Smet, A., Ludwig, C., Stephan, B., De Graef, E., Vanrobaeys, M., Haesebrouck, F., 2014. Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008–2011). Vet. Microbiol., VETMIC-D-13-8797R1/VETMIC_6490. Dobiasova, H., Kutilova, I., Piackova, V., Vesely, T., Cizek, A., Dolejska, M., 2014. Ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids. Vet. Microbiol., VETMIC-D-13-8912R1/VETMIC_6513. Entorf, M., Feßler, A.T., Kadlec, K., Kaspar, H., Mankertz, J., Peters, T., Schwarz, S., 2014. Tylosin susceptibility of staphylococci from bovine mastitis. Vet. Microbiol., VETMIC-D-13-8854R1/VETMIC_6450. Feßler, A.T., Turnidge, J., Schwarz, S., 2014. Quality control ranges for cefoperazone 30 mg disks for Staphylococcus aureus ATCC1 25923 and Escherichia coli ATCC1 25922. Vet. Microbiol., VETMIC-D-13-8849/ VETMIC_6541. Guerra, B., Fischer, J., Helmuth, R., 2014. An emerging public health problem: acquired carbapenemase producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet. Microbiol., VETMIC-D-138882R1/VETMIC_6500. Haenni, M., Chaˆtre, P., Me´tayer, V., Bour, M., Signol, E., Madec, J.-Y., Gay, E., 2014. Comparative prevalence and characterization of ESBL-producing Enterobacteriaceae in dominant versus subdominant enteric flora in veal calves at slaughterhouse, France. Vet. Microbiol., VETMIC-D13-8904R2/VETMIC_6525. Huang, Y., Michael, G.B., Becker, R., Kaspar, H., Mankertz, J., Schwarz, S., Runge, M., Steinhagen, D., 2014. Pheno- and genotypic analysis of antimicrobial resistance properties of Yersinia ruckeri from fish. Vet. Microbiol., VETMIC-D-13-8621R1/VETMIC_6394. Janatova, M., Albrechtova, K., Petrzelkova, K.J., Dolejska, M., Papousek, I., Masarikova, M., Cizek, A., Todd, A., Shutt, K., Kalousova, B., Profousova, I., Modry, D., Literak, I., 2014. Antimicrobial-resistant Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic. Vet. Microbiol., VETMIC-D-13-8656R1/VETMIC_6516. Literak, I., Manga, I., Wojczulanis-Jakubas, K., Chroma, M., Jamborova, I., Dobiasova, H., Htoutou Sedlakova, M., Cizek, A., 2014. Enterobacter cloacae with a novel variant of ACT AmpC beta-lactamase originating
from Glaucous gull (Larus hyperboreus) in Svalbard. Vet. Microbiol., VETMIC-D-13-8648R1/VETMIC_6517. Marosevic, D., Cervinkova, D., Vlkova, H., Videnska, P., Babak, V., Jaglic, Z., 2014. In vivo spread of macrolide-lincosamide-streptogramin B (MLSB) resistance – a model study in chickens. Vet. Microbiol., VETMIC-D-13-8599R1/VETMIC_6543. Moodley, A., Damborg, P., Nielsen, S.S., 2014. Antimicrobial resistance in methicillin susceptible and methicillin resistant Staphylococcus pseudintermedius of canine origin: literature review from 1980–2013. Vet. Microbiol., VETMIC-D-13-8877R1/VETMIC_6510. Moyaert, H., de Jong, A., Simjee, S., Thomas, V., 2014. Antimicrobial resistance monitoring projects for zoonotic and indicator bacteria of animal origin: common aspects and differences between EASSA and EFSA. Vet. Microbiol., VETMIC-D-13-8875R1/VETMIC_6540. Nedbalcova, K., Nechvatalova, K., Pokludova, L., Bures, J., Kucerova, Z., Koutecka, L., Hera, A., 2014. Resistance to selected beta-lactam antibiotics. Vet. Microbiol., VETMIC-D-13-8773R1/VETMIC_6504. Nemeghaire, S., Argudı´n, M.A., Feßler, A.T., Hauschild, T., Schwarz, S., Butaye, P., 2014a. The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Vet. Microbiol., VETMIC-D-13-8881R1/VETMIC_6505. Nemeghaire, S., Argudı´n, M.A., Haesebrouck, F., Butaye, P., 2014b. Molecular epidemiology of methicillin-resistant Staphylococcus sciuri in healthy chickens. Vet. Microbiol., VETMIC-D-13-8853R1/VETMIC_6507. Nguyen, H.N.K., Van, T.T.H., Nguyen, H.T., Smooker, P.M., Shimeta, J., Coloe, P.J., 2014. Molecular characterization of antibiotic resistance in Pseudomonas and Aeromonas isolates from catfish of the Mekong Delta, Vietnam. Vet. Microbiol., VETMIC-D-13-8796R2/VETMIC_6488. Papich, M.G., 2014. Pharmacokinetic–pharmacodynamic (PK–PD) modeling and the rational selection of dosage regimens for the prudent use of antimicrobial drugs. Vet. Microbiol., VETMIC-D-13-8924R1/VETMIC_6459. Prescott, J.F., 2014. The resistance tsunami, antimicrobial stewardship, and the golden age of microbiology. Vet. Microbiol., VETMIC-D-138722R1/VETMIC_6537. Sølverød Mo, S., Norstro¨m, M., Slettemea˚s, J.S., Løvland, A., Urdahl, A.M., Sunde, M., 2014. Emergence of AmpC- producing Escherichia coli in the broiler production chain in a country with a low antimicrobial usage profile. Vet. Microbiol., VETMIC-D-13-8878R1/ VETMIC_6501. Sousa, M., Silva, N., Igrejas, G., Silva, F., Sargo, R., Alegria, N., Benito, D., Go´mez, P., Lozano, C., Go´mez-Sanz, E., Torres, C., Canic¸a, M., Poeta, P., 2014. Antimicrobial resistance determinants in Staphylococcus spp. recovered from birds of prey in Portugal. Vet. Microbiol., VETMIC-D13-8767R1/VETMIC_6536. Supre´, K., Lommelen, K., De Meulemeester, L., 2014. Antimicrobial susceptibility and distribution of inhibition zone diameters of bovine mastitis pathogens in Flanders, Belgium. Vet. Microbiol., VETMIC-D13-8769R1/VETMIC_6549. Tsonos, J., Oosterik, L.H., Tuntufye, H.N., Klumpp, J., Butaye, P., De Greve, H., Hernalsteens, J.-P., Lavigne, R., Goddeeris, B.M., 2014a. A cocktail of in vitro efficient phages is not a guarantee for in vivo therapeutic results against avian colibacillosis. Vet. Microbiol., VETMIC-D-138764R1/VETMIC_6389. Tsonos, J., Vandenheuvel, D., Briers, Y., De Greve, H., Hernalsteens, J.-P., Lavigne, R., 2014b. Hurdles in bacteriophage therapy: deconstructing the parameters. Vet. Microbiol., VETMIC-D-13-8772R1/VETMIC_6395. van Duijkeren, E., Hengeveld, P., Albers, M., Pluister, G., Jacobs, P., Heres, L., van de Giessen, A., 2014. Prevalence of methicillin-resistant Staphylococcus aureus carrying mecA or mecC in dairy cattle. Vet. Microbiol., VETMIC-D-13-8852R1/VETMIC_6463. Wasyl, D., Hoszowski, A., Zaja˛c, M., 2014. Prevalence and characterisation of quinolone resistance mechanisms in Salmonella spp. Vet. Microbiol., VETMIC-D-13-8768R1/VETMIC_6503. Wendlandt, S., Kadlec, K., Feßler, A.T., van Duijkeren, E., Schwarz, S., 2014. Two different erm(C)-carrying plasmids in the same methicillin-resistant Staphylococcus aureus CC398 isolate from a broiler farm. Vet. Microbiol., VETMIC-D-13-8700R1/VETMIC_6469.
Patrick Butaye Engeline van Duijkeren John F. Prescott Stefan Schwarz* *Corresponding author. Tel.: +49 5034 871241 E-mail address: stefan.schwarz@fli.bund.de
Please cite this article in press as: Butaye, P., et al., Antimicrobial resistance in bacteria from animals and the environment. Vet. Microbiol. (2014), http://dx.doi.org/10.1016/j.vetmic.2014.04.009
VETMIC-6593; No. of Pages 4 Veterinary Microbiology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Veterinary Microbiology journal homepage: www.elsevier.com/locate/vetmic
Preface
Antimicrobial resistance in bacteria from animals and the environment
Antimicrobial resistance in bacteria has become a major public health issue during the past decade. Antimicrobial agents are indispensable in the control of bacterial infections, not only in humans, but also in animals and plants. Every use of an antimicrobial agent selects for bacteria with elevated minimal inhibitory concentrations. Under the selective pressure imposed by the use of antimicrobial agents, bacteria which possess resistance mechanisms can multiply and expand at the expense of the bacteria that are inhibited by the respective antimicrobial agents. Moreover, bacteria can pass resistance genes to other bacteria through horizontal gene transfer and thereby contribute to the dissemination of resistance genes within bacterial populations of different ecosystems. In polymicrobial environments, such horizontal gene transfer processes may involve donors and recipients that belong to different bacterial species and genera. These basic facts apply not only to bacteria of human origin, but also to those of animal and environmental origin – a situation that is reflected by the ‘‘One Health’’ concept. Antimicrobial resistance in bacteria is a highly multifaceted topic at the interface of human, animal and plant health, food hygiene and environmental science. Besides the analysis of resistance genes and resistancemediating mutations, the dissemination of resistance properties and the analysis of mobile genetic elements that play a role in the spreading of resistance genes across species and genus boundaries, numerous other aspects play an important role when dealing with antimicrobial resistance. These include among others (i) pharmacological aspects with regard to the application of antimicrobial agents, (ii) methodological aspects with regard to the correct performance of antimicrobial susceptibility testing, (iii) antimicrobial resistance monitoring programmes, (iv) antimicrobial stewardship, (v) animal models, (vi) antimicrobial resistance in bacteria from specific sources, such as wildlife, aquaculture, foodproducing animals, companion animals and the environment, and (vii) alternative, non-antimicrobial strategies
to control bacterial infections. All these aspects were addressed during the 5th Symposium on Antimicrobial Resistance in Animals and the Environment (ARAE 2013), which was held from June 30 to July 3, 2013 in Ghent, Belgium. The forum provided an important venue for networking between and discussion among scientists engaged in understanding different aspects of the antibiotic resistance problem, and in finding ways to mitigate the impact of resistance. This Special Issue of Veterinary Microbiology captures the flavour and quality of the wideranging presentations made at the Symposium, and will be a useful single source resource for workers in this field. This symposium, which is held in 2-years intervals since 2005, comprised one keynote lecture and another six invited lectures given by experts in the specific fields. In his keynote lecture, John F. Prescott summarized the situation with regard to antimicrobial agents and antimicrobial resistance during the past 60 years. He illustrated that changes in the practice of how we use antimicrobial agents are unavoidable and that Good Stewardship Practice should be adopted by everyone involved in antimicrobial use and application. Despite increasing percentages of resistant bacteria and decreasing numbers of new antimicrobial agents – especially for use in veterinary medicine – he also emphasized the availability of new technologies, such as whole genome sequencing, which may be used for the identification of new bacterial targets that serve for the development of future antimicrobial agents for specific bacterial pathogens and disease conditions (Prescott, 2014). Moreover, 42 oral presentations (selected from the submissions) and 83 poster presentations completed the programme of this symposium. This Special Issue of Veterinary Microbiology comprises a collection of review articles, original research papers and short communications from contributions presented at the ARAE 2013 symposium. The following paragraphs provide a short summary of the different studies compiled in this Special Issue based on their assignment to topics of the symposium.
http://dx.doi.org/10.1016/j.vetmic.2014.04.009 0378-1135/ß 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Butaye, P., et al., Antimicrobial resistance in bacteria from animals and the environment. Vet. Microbiol. (2014), http://dx.doi.org/10.1016/j.vetmic.2014.04.009
G Model
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1. Antimicrobial resistance monitoring and susceptibility testing One review compared the technical specifications on monitoring of antimicrobial resistance in zoonotic Salmonella, Campylobacter and indicator Escherichia coli and Enterococcus as performed by the European Food Safety Authority (EFSA) with veterinary pharmaceutical industry’s European Antimicrobial Susceptibility Surveillance in Animals (EASSA) programme. The major difference between the two programmes is the classification into ‘susceptible’ versus ‘resistant’. Whilst EFSA categorizes all isolates with an MIC value above the epidemiological cutoff value as ‘resistant’, EASSA differentiates between ‘percentage decreased susceptible’ and ‘percentage clinical resistant’ strains by applying both epidemiological cut-off values and clinical breakpoints (Moyaert et al., 2014). Another study dealt with the determination of quality control (QC) ranges for cefoperazone 30 mg disks for the internationally accepted QC strains Staphylococcus aureus ATCC1 25923 and E. coli ATCC1 25922. QC parameters are indispensable instruments to assure the correct performance of in vitro susceptibility testing (Feßler et al., 2014). 2. Antimicrobial resistance in Gram-negative bacteria from livestock and companion animals One review recapitulated carbapenemase producing E. coli, Salmonella spp. (VIM-1 producers) and Acinetobacter spp. (producing OXA-23 and NDM-1) in livestock animals (poultry, cattle and swine) and their environment, but also NDM-1-producing E. coli, OXA-48 in E. coli and Klebsiella pneumoniae or OXA-23 in Acinetobacter spp. from companion animals (cats, dogs or horses), NDM-1-producing Salmonella isolated from wild birds, as well as OXA-23like-producing Acinetobacter baumanii in ectoparasites (Guerra et al., 2014). A survey study on antimicrobial resistance among Salmonella isolates from healthy pigs (n = 368) and chickens (n = 452) in Belgium was conducted during the years 2008–2011. ESBL/AmpC producers were particularly prevalent in chickens (12.8%), and much less in pigs (1.9%). Among the cephalosporin-resistant isolates, blaCTX-M (mostly blaCTXM-1, but also blaCTXM-2 and blaCTXM9) and blaTEM-52 were the predominant ESBL genes (de Jong et al., 2014). Another study focused on the characterization of quinolone resistance mechanisms in Salmonella isolated from animals, food, and feed between 2008 and 2011 in Poland. Besides resistance-mediating mutations in gyrA, plasmidic quinolone resistance genes qnrS1/qnrS3 and qnrB19/qnrB10 were also identified (Wasyl et al., 2014). A study from Norway aimed at estimating the prevalence of cephalosporin-resistant E. coli at the different levels of the Norwegian broiler production pyramid and identifying the respective resistance mechanisms. The occurrence of cephalosporin-resistant E. coli at the different production levels ranged from 8 to 43%. All resistant isolates had an AmpC-phenotype and the majority carried the blaCMY-2 gene (Sølverød Mo et al., 2014). In France, 491 veal calves from different slaughtering batches at twelve abattoirs were investigated in 2012 for the presence of ESBL-producing Enterobacteriaceae. A prevalence of 29.4%
of ESBL-producers in the faecal flora was identified and various blaCTX-M genes were detected. The authors suggested that veal calves may constitute one of the major ESBL reservoirs in food animals (Haenni et al., 2014). Trends in resistance to antimicrobials among Actinobacillus pleuropneumoniae, Pasteurella multocida, Mannheimia haemolytica and E. coli isolates from clinical cases of cattle and swine diseases in the Czech Republic from 2007 to 2011 were determined. Moreover, sales figures for betalactam antimicrobial agents during the same period were determined and compared for pigs and cattle (Nedbalcova et al., 2014). 3. Antimicrobial resistance in Gram-positive bacteria from livestock and companion animals One review dealt with the antimicrobial resistance of methicillin-susceptible (MSSP) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) – a commensal and common opportunistic pathogen in dogs. For this, the authors revisited the published literature during 1980– 2013. Stratified by MSSP and MRSP, no significant increases in antimicrobial resistance were observed over time, except for the penicillinase-labile penicillins (penicillin and ampicillin) among MSSP. The review highlighted inconsistencies between studies as a result of several factors, for example the use of different antimicrobial susceptibility testing methods and interpretation criteria (Moodley et al., 2014). Another comprehensive review dealt with the ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Although often considered as harmless commensals, members of the S. sciuri species group have also been found to carry multiple virulence and resistance genes including genes implicated in biofilm formation or coding for toxins responsible of toxic shock syndrome and multi-resistance. The authors concluded that further studies into the role of the S. sciuri species group as commensal and pathogenic bacteria are required to fully assess its medical and veterinary importance (Nemeghaire et al., 2014a). Methicillin-resistant S. sciuri (MRSS) in healthy chickens were the topic of a study conducted in Belgium. Eighty-seven MRSS were isolated resulting in an estimated prevalence of 31.0%. The prevalence in broilers did not significantly differ from that in layers. Most MRSS isolates harboured a non-typeable or type III SCCmec and were multiresistant (Nemeghaire et al., 2014b). A study conducted in The Netherlands focused on methicillin-resistant Staphylococcus aureus (MRSA) from dairy cattle at slaughter. Sixteen of 411 (3.9%) cows, all originating from different farms, were found to be MRSA positive. All MRSA isolates belonged to livestock-associated clonal complex 398, were PVL-negative and spa type t011 predominated. No isolates carrying mecC were detected (van Duijkeren et al., 2014). In a study conducted in Germany, 112 S. aureus and 110 coagulasenegative Staphylococcus spp. (CoNS) isolates from cases of bovine mastitis were tested comparatively for tylosin and erythromycin susceptibility by broth microdilution and agar disc diffusion with 30 mg tylosin disks. PCR analysis of the 25 erythromycin-resistant staphylococcal isolates identified the resistance genes erm(A), erm(B), erm(C), erm(T), mph(C) and msr(A) alone or in different combinations. An excellent
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correlation between the results of broth microdilution and disc diffusion were seen for S. aureus and CoNS isolates (Entorf et al., 2014). A study conducted in Belgium reported the zone diameter distributions for numerous antimicrobial agents among S. aureus (n = 768), Streptococcus uberis (n = 939), Streptococcus dysgalactiae (n = 444), E. coli (n = 563), and Klebsiella spp. (n = 59) obtained from cases of (sub) clinical mastitis. The authors emphasized the need for clinical breakpoints applicable to causative agents of bovine mastitis (Supre´ et al., 2014). In a study on MRSA isolates from Dutch broiler farms, an MRSA CC398 isolate was identified which harboured two structurally unrelated erm(C)-carrying plasmids of 2458 bp and 3882 bp. The fact that both plasmids belong to different incompatibility groups as specified by the different rep genes, repL and repF, explains why they can stably coexist in the same bacterial cell (Wendlandt et al., 2014). Another study investigated the influence of specific and non-specific selective pressure on the in vivo spread of macrolide-lincosamide-streptogramin B (MLSB) resistance in chickens. For this, chickens were inoculated with Enterococcus faecalis harbouring the erm(B)-carrying plasmid pAMb1. The results of that study suggested that (i) erm(B)-mediated MLSB resistance may spread within the gut microbiota under specific and non-specific pressure and even in the absence of any antimicrobial pressure, and (ii) different bacterial species seem to be involved in the spread of MLSB resistance (Marosevic et al., 2014). 4. Antimicrobial resistance in fish bacterial pathogens The molecular characterization of antibiotic resistance among 116 Pseudomonas and 92 Aeromonas isolates from catfish of the Mekong Delta, Vietnam, showed percentages of multiple drug resistance of 96.6% and 61.9% among Pseudomonas and Aeromonas isolates, respectively. Large resistance plasmids (>55 kb) were frequently detected and conjugation and transformation experiments demonstrated the successful transfer of all or part of the resistance phenotypes of catfish isolates to the recipient strains (Nguyen et al., 2014). A study from Germany investigated the antimicrobial resistance pheno- and genotypes of Yersinia ruckeri from fish. Elevated MICs to fluoroquinolones were associated with mutations in gyrA. A single isolate showed elevated MICs for sulfonamides and trimethoprim and harboured a 8.9 kb plasmid, which carried the genes sul2, strB and a dfrA14 gene cassette integrated into the strA gene (Huang et al., 2014). The role of ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids was investigated in a study conducted in the Czech Republic. Fifteen (19%, n = 80) isolates from koi carps and 18 (24%, n = 76) isolates from imported ornamental fish were positive for qnrS2, aac(60 )-Ib-cr or qnrB17 genes. Related IncU plasmids harbouring qnrS2 and aac(60 )-Ib-cr genes were found in Aeromonas spp. from imported ornamental fish and koi carp (Dobiasova et al., 2014). 5. Antimicrobial resistance in bacteria from wildlife The antimicrobial resistance of Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic, was investigated with emphasis on
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ESBL and plasmid-mediated quinolone resistance (PMQR) genes. Among wildlife, the most significant findings were CTX-M-15-producing K. pneumoniae in a habituated gorilla and a multi-resistant E. coli isolate with the qepA gene in an unhabituated gorilla. Other isolates from wildlife were mostly qnrB-harbouring Citrobacter spp. (Janatova et al., 2014). During a study on Enterobacteriaceae in wild birds in Arctic Svalbard, Norway, an E. cloacae isolate originating from Glaucous gull (Larus hyperboreus) carrying the novel blaACT-23 AmpC beta-lactamase gene was identified (Literak et al., 2014). A study conducted in Portugal investigated the antimicrobial resistance determinants of Staphylococcus spp. recovered from birds of prey. A wide variety of resistance genes, including blaZ, mecA, tet(K), tet(L), dfrA, dfrG, fusC, msr(A), mph(C), ant60 -Ia, catpC221, catpC223 and catpC194, were mainly detected in CoNS (Sousa et al., 2014). 6. The environment as a reservoir of resistance genes One review investigated the impact of wastewater treatment plant (WWTP) effluents into a river by comparatively investigating water samples upstream and downstream of the WWTP. For this, metagenomic libraries were constructed in E. coli and screened for pheno- and genotypic resistance. An increasing number of resistant clones from downstream waters was detected. The authors conclude that waste water disposal increases the reservoir of resistance mechanisms in the environment either by addition of resistance genes or by input of agents selective for resistant phenotypes (Amos et al., 2014). A study conducted in The Netherlands investigated the prevalence and the characteristics of ESBL-producing E. coli in four Dutch recreational waters and the possible role of nearby WWTPs as contamination source. ESBL-producing E. coli were detected in all four recreational waters. WWTPs were shown to contribute to the presence of these bacteria in surface waters, although other yet unidentified sources were likely to co-contribute to the presence of ESBLproducing E. coli (Blaak et al., 2014). 7. Phages as an alternative to antimicrobial agents A review about phage therapy argued that phage therapy has not revealed all of its secrets and many parameters remain understudied, making the outcome of phage therapy highly variable depending on the disease condition. According to the authors, the main obstacles on the way to a successful phage therapy include poorly understood mechanisms of phage penetration and distribution throughout the body, the variable expression and accessibility of phage receptors on the bacterial host under in vivo conditions and the unusual (non-linear) phage pharmacokinetics. These parameters are not easily measured in realistic in vivo settings, but are nevertheless important hurdles to overcome the high variability of phage therapy trials (Tsonos et al., 2014b). A study was conducted to evaluate the effect of a cocktail of in vitro efficient phages to protect experimentally infected chickens against avian pathogenic E. coli. The phage cocktail was administered two hours after the infection intratracheally, intraoesophageally or via the drinking water. Treated groups did not show
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a significant decrease in mortality, lesion scores or weight loss compared to untreated groups. The authors concluded that the efficiency of the phage cocktail used in treating APEC-infected chickens in vivo is negligible, even though in vitro, the phages in the cocktail were able to efficiently lyse the APEC strain (Tsonos et al., 2014a). 8. Pharmacological aspects A review dealt with the application of pharmacokinetic–pharmacodynamic (PK–PD) principles to dosing regimens as a strategy to decrease inappropriate use of antimicrobial agents in veterinary medicine. The author emphasized applying these PK–PD principles to attain targets for area-under-the-curve to MIC ratio (AUC/MIC), peak concentration to MIC ratio (CMAX/MIC), and time above MIC (T > MIC) as a prerequisite for a more effective antimicrobial therapy. In addition, the author pointed towards the use of accurate interpretive criteria, such as the CLSI-approved veterinary-specific clinical breakpoints for identifying the most efficient antimicrobial agent for therapeutic applications (Papich, 2014). References Amos, G.C., Zhang, L., Hawkey, P.M., Gaze, W.H., Wellington, E.M., 2014. Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet. Microbiol., VETMIC-D-138994R1/VETMIC_6519. Blaak, H., de Kruijf, P., Hamidjaja, R.A., van Hoek, A.H.A.M., de Roda Husman, A.M., Schets, F.M., 2014. Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants. VETMIC-D-13-8770R1/VETMIC_6554 de Jong, A., Smet, A., Ludwig, C., Stephan, B., De Graef, E., Vanrobaeys, M., Haesebrouck, F., 2014. Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008–2011). Vet. Microbiol., VETMIC-D-13-8797R1/VETMIC_6490. Dobiasova, H., Kutilova, I., Piackova, V., Vesely, T., Cizek, A., Dolejska, M., 2014. Ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids. Vet. Microbiol., VETMIC-D-13-8912R1/VETMIC_6513. Entorf, M., Feßler, A.T., Kadlec, K., Kaspar, H., Mankertz, J., Peters, T., Schwarz, S., 2014. Tylosin susceptibility of staphylococci from bovine mastitis. Vet. Microbiol., VETMIC-D-13-8854R1/VETMIC_6450. Feßler, A.T., Turnidge, J., Schwarz, S., 2014. Quality control ranges for cefoperazone 30 mg disks for Staphylococcus aureus ATCC1 25923 and Escherichia coli ATCC1 25922. Vet. Microbiol., VETMIC-D-13-8849/ VETMIC_6541. Guerra, B., Fischer, J., Helmuth, R., 2014. An emerging public health problem: acquired carbapenemase producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet. Microbiol., VETMIC-D-138882R1/VETMIC_6500. Haenni, M., Chaˆtre, P., Me´tayer, V., Bour, M., Signol, E., Madec, J.-Y., Gay, E., 2014. Comparative prevalence and characterization of ESBL-producing Enterobacteriaceae in dominant versus subdominant enteric flora in veal calves at slaughterhouse, France. Vet. Microbiol., VETMIC-D13-8904R2/VETMIC_6525. Huang, Y., Michael, G.B., Becker, R., Kaspar, H., Mankertz, J., Schwarz, S., Runge, M., Steinhagen, D., 2014. Pheno- and genotypic analysis of antimicrobial resistance properties of Yersinia ruckeri from fish. Vet. Microbiol., VETMIC-D-13-8621R1/VETMIC_6394. Janatova, M., Albrechtova, K., Petrzelkova, K.J., Dolejska, M., Papousek, I., Masarikova, M., Cizek, A., Todd, A., Shutt, K., Kalousova, B., Profousova, I., Modry, D., Literak, I., 2014. Antimicrobial-resistant Enterobacteriaceae from humans and wildlife in Dzanga-Sangha Protected Area, Central African Republic. Vet. Microbiol., VETMIC-D-13-8656R1/VETMIC_6516. Literak, I., Manga, I., Wojczulanis-Jakubas, K., Chroma, M., Jamborova, I., Dobiasova, H., Htoutou Sedlakova, M., Cizek, A., 2014. Enterobacter cloacae with a novel variant of ACT AmpC beta-lactamase originating
from Glaucous gull (Larus hyperboreus) in Svalbard. Vet. Microbiol., VETMIC-D-13-8648R1/VETMIC_6517. Marosevic, D., Cervinkova, D., Vlkova, H., Videnska, P., Babak, V., Jaglic, Z., 2014. In vivo spread of macrolide-lincosamide-streptogramin B (MLSB) resistance – a model study in chickens. Vet. Microbiol., VETMIC-D-13-8599R1/VETMIC_6543. Moodley, A., Damborg, P., Nielsen, S.S., 2014. Antimicrobial resistance in methicillin susceptible and methicillin resistant Staphylococcus pseudintermedius of canine origin: literature review from 1980–2013. Vet. Microbiol., VETMIC-D-13-8877R1/VETMIC_6510. Moyaert, H., de Jong, A., Simjee, S., Thomas, V., 2014. Antimicrobial resistance monitoring projects for zoonotic and indicator bacteria of animal origin: common aspects and differences between EASSA and EFSA. Vet. Microbiol., VETMIC-D-13-8875R1/VETMIC_6540. Nedbalcova, K., Nechvatalova, K., Pokludova, L., Bures, J., Kucerova, Z., Koutecka, L., Hera, A., 2014. Resistance to selected beta-lactam antibiotics. Vet. Microbiol., VETMIC-D-13-8773R1/VETMIC_6504. Nemeghaire, S., Argudı´n, M.A., Feßler, A.T., Hauschild, T., Schwarz, S., Butaye, P., 2014a. The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Vet. Microbiol., VETMIC-D-13-8881R1/VETMIC_6505. Nemeghaire, S., Argudı´n, M.A., Haesebrouck, F., Butaye, P., 2014b. Molecular epidemiology of methicillin-resistant Staphylococcus sciuri in healthy chickens. Vet. Microbiol., VETMIC-D-13-8853R1/VETMIC_6507. Nguyen, H.N.K., Van, T.T.H., Nguyen, H.T., Smooker, P.M., Shimeta, J., Coloe, P.J., 2014. Molecular characterization of antibiotic resistance in Pseudomonas and Aeromonas isolates from catfish of the Mekong Delta, Vietnam. Vet. Microbiol., VETMIC-D-13-8796R2/VETMIC_6488. Papich, M.G., 2014. Pharmacokinetic–pharmacodynamic (PK–PD) modeling and the rational selection of dosage regimens for the prudent use of antimicrobial drugs. Vet. Microbiol., VETMIC-D-13-8924R1/VETMIC_6459. Prescott, J.F., 2014. The resistance tsunami, antimicrobial stewardship, and the golden age of microbiology. Vet. Microbiol., VETMIC-D-138722R1/VETMIC_6537. Sølverød Mo, S., Norstro¨m, M., Slettemea˚s, J.S., Løvland, A., Urdahl, A.M., Sunde, M., 2014. Emergence of AmpC- producing Escherichia coli in the broiler production chain in a country with a low antimicrobial usage profile. Vet. Microbiol., VETMIC-D-13-8878R1/ VETMIC_6501. Sousa, M., Silva, N., Igrejas, G., Silva, F., Sargo, R., Alegria, N., Benito, D., Go´mez, P., Lozano, C., Go´mez-Sanz, E., Torres, C., Canic¸a, M., Poeta, P., 2014. Antimicrobial resistance determinants in Staphylococcus spp. recovered from birds of prey in Portugal. Vet. Microbiol., VETMIC-D13-8767R1/VETMIC_6536. Supre´, K., Lommelen, K., De Meulemeester, L., 2014. Antimicrobial susceptibility and distribution of inhibition zone diameters of bovine mastitis pathogens in Flanders, Belgium. Vet. Microbiol., VETMIC-D13-8769R1/VETMIC_6549. Tsonos, J., Oosterik, L.H., Tuntufye, H.N., Klumpp, J., Butaye, P., De Greve, H., Hernalsteens, J.-P., Lavigne, R., Goddeeris, B.M., 2014a. A cocktail of in vitro efficient phages is not a guarantee for in vivo therapeutic results against avian colibacillosis. Vet. Microbiol., VETMIC-D-138764R1/VETMIC_6389. Tsonos, J., Vandenheuvel, D., Briers, Y., De Greve, H., Hernalsteens, J.-P., Lavigne, R., 2014b. Hurdles in bacteriophage therapy: deconstructing the parameters. Vet. Microbiol., VETMIC-D-13-8772R1/VETMIC_6395. van Duijkeren, E., Hengeveld, P., Albers, M., Pluister, G., Jacobs, P., Heres, L., van de Giessen, A., 2014. Prevalence of methicillin-resistant Staphylococcus aureus carrying mecA or mecC in dairy cattle. Vet. Microbiol., VETMIC-D-13-8852R1/VETMIC_6463. Wasyl, D., Hoszowski, A., Zaja˛c, M., 2014. Prevalence and characterisation of quinolone resistance mechanisms in Salmonella spp. Vet. Microbiol., VETMIC-D-13-8768R1/VETMIC_6503. Wendlandt, S., Kadlec, K., Feßler, A.T., van Duijkeren, E., Schwarz, S., 2014. Two different erm(C)-carrying plasmids in the same methicillin-resistant Staphylococcus aureus CC398 isolate from a broiler farm. Vet. Microbiol., VETMIC-D-13-8700R1/VETMIC_6469.
Patrick Butaye Engeline van Duijkeren John F. Prescott Stefan Schwarz* *Corresponding author. Tel.: +49 5034 871241 E-mail address: stefan.schwarz@fli.bund.de
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