View More View Less
  • 1 Department of Medical Microbiology, Faculty of Medicine, University of Debrecen, , Nagyerdei krt. 98, Debrecen, H-4032, , Hungary
  • | 2 Doctoral School of Pharmaceutical Sciences, University of Debrecen, Debrecen, , Hungary
  • | 3 Debrecen Laboratory, Veterinary Diagnostic Directorate, National Food Chain Safety Office, Debrecen, , Hungary
  • | 4 Hajdúszoboszló, HAGE Hajdúsági Agráripari Zrt., , Hungary
  • | 5 Private Veterinarian
Open access

Abstract

Multidrug resistance due to the production of extended-spectrum beta-lactamases (ESBLs) is a major problem in human as well as in veterinary medicine. These strains appear in animal and human microbiomes and can be the source of infection both in animal and in human healthcare, in accordance with the One Health theorem. In this study we examined the prevalence of ESBL-producing bacteria in food-producing animals. We collected 100 porcine and 114 poultry samples to examine the prevalence of ESBL producers. Isolates were identified using the MALDI-TOF system and their antibiotic susceptibility was tested using the disk diffusion method. ESBL gene families and phylogroups were detected by polymerase chain reactions. The prevalence of ESBL producers was relatively high in both sample groups: 72 (72.0%) porcine and 39 (34.2%) poultry isolates were ESBL producers. Escherichia coli isolates were chosen for further investigations. The most common ESBL gene was CTX-M-1 (79.3%). Most of the isolates belong to the commensal E. coli phylogroups. The porcine isolates could be divided into three phylogroups, while the distribution of the poultry isolates was more varied. In summary, ESBL-producing bacteria are prevalent in the faecal samples of the examined food-producing animals, with a dominance of the CTX-M-1 group enzymes and commensal E. coli phylogroups.

Abstract

Multidrug resistance due to the production of extended-spectrum beta-lactamases (ESBLs) is a major problem in human as well as in veterinary medicine. These strains appear in animal and human microbiomes and can be the source of infection both in animal and in human healthcare, in accordance with the One Health theorem. In this study we examined the prevalence of ESBL-producing bacteria in food-producing animals. We collected 100 porcine and 114 poultry samples to examine the prevalence of ESBL producers. Isolates were identified using the MALDI-TOF system and their antibiotic susceptibility was tested using the disk diffusion method. ESBL gene families and phylogroups were detected by polymerase chain reactions. The prevalence of ESBL producers was relatively high in both sample groups: 72 (72.0%) porcine and 39 (34.2%) poultry isolates were ESBL producers. Escherichia coli isolates were chosen for further investigations. The most common ESBL gene was CTX-M-1 (79.3%). Most of the isolates belong to the commensal E. coli phylogroups. The porcine isolates could be divided into three phylogroups, while the distribution of the poultry isolates was more varied. In summary, ESBL-producing bacteria are prevalent in the faecal samples of the examined food-producing animals, with a dominance of the CTX-M-1 group enzymes and commensal E. coli phylogroups.

Introduction

Bacteria producing extended spectrum β-lactamases (ESBLs) cause serious problem in human and veterinary healthcare, as these bacteria are resistant to penicillins, broad-spectrum cephalosporins and monobactams. Beta-lactam antibiotics are used frequently in human and veterinary medicine against infections caused by Enterobacterales (Nüesch-Inderbinen et al., 2016). Correlation between the consumption of 3rd and 4th generation cephalosporins and cephalosporin resistance of Escherichia coli was reported in human medicine and in food-producing animals by the European Centre for Disease Prevention and Control (ECDC), the European Food Safety Authority (EFSA) and the European Medicines Agency (EMA) in a joint report (ECDC, EFSA and EMA, 2017). In this manner, ESBL enzymes, found frequently in the background of resistance to multiple beta-lactam antibiotics, became ubiquitous in Enterobacterales, especially in E. coli, spreading on mobile genetic elements and occurring frequently in the gut microbiome of humans or animals. The microbiome thus serves as a reservoir of ESBL producers and ESBL genes, and the human and animal microbiomes are interconnected through the food chain (Silva et al., 2019). Recognising the importance of this relationship, the World Health Organization (WHO), the World Organisation for Animal Health (OIE) and the Food and Agriculture Organization (FAO) established the One-Health concept ‘to achieve optimal health and well-being outcomes recognising the interconnections between people, animals, plants and their shared environment’ (https://www.onehealthcommission.org/en/why_one_health/what_is_one_health/).

The aim of this study was to investigate the occurrence of ESBL producers in food-producing animals, and to determine their human pathogenic potential through phylogroup analysis. We also compared these isolates to contemporary isolates from asymptomatic human carriage.

Materials and methods

Samples and culturing

A total of 100 porcine and 114 poultry faecal samples were investigated. The samples were cultured on eosin–methylene blue agar supplemented with 2 mg L−1 cefotaxime. This culturing method helped screen the ESBL strains. The antibiogram (antibiotic susceptibility testing) was determined using the Kirby–Bauer disk diffusion method based on the European Committee on Antimicrobial Susceptibility Testing (EUCAST) recommendations against carbapenems (ertapenem, meropenem, imipenem), amoxicillin/clavulanic acid, cefotaxime, cefepime, ciprofloxacin, sulphamethoxazole/trimethoprim (Sumetrolim, SXT) amikacin, tobramycin, and gentamicin; colistin susceptibility was tested by microdilution (Merlin GmBH, Berlin, Germany). The identification of bacterial colonies was performed using Matrix-Assisted Laser Desorption/Ionization Time-of Flight (MALDI-TOF) Biotyper (Bruker Daltonics, Bremen, Germany). The ESBL phenotype was examined using the double-disk synergy test, the cefotaxime and amoxicillin/clavulanic acid disks placed at 30 mm apart. The double-disk synergy test was positive when the inhibition zone was enhanced between the two disks (synergy between cefotaxime and the lactamase-inhibitor clavulanic acid). Animal-derived isolates were compared to 17 contemporary human isolates originating from asymptomatic faecal or oral carriage collected at the University of Debrecen.

Resistance genes and phylogenetic analysis

The bla TEM, bla CTX-M and bla SHV genes were detected by PCR, as described previously (Ebrahimi et al., 2014). The bla CTX-M genes in the CTX-M-1 group were sequenced using group-specific PCR primers. Sequences were analysed by means of CLC DNA Workbench v4.0 (CLC Bio, Aarhus, Denmark).

The phylogenetic analysis of E. coli isolates was performed by the multiplex PCR method of Clermont et al. (2013). This method defines eight phylogroups: phylogroups A1, B1, C, E, F and clade I contain mainly commensal strains, while phylogroups B2 and D are responsible for extraintestinal infections in humans. The pandemic ST131 clone and its subclades C1-M27 and the C2 carrying bla CTX-M-15 were detected using the method of Matsumura et al. (2017).

Results

Prevalence of ESBL producers

The prevalence of ESBL-producing isolates was markedly different between the porcine and poultry samples, 72 (72.0%) and 39 (34.2%) ESBL-producing isolates were found, respectively. All poultry and 43 porcine isolates were E. coli; 21 Proteus spp., 7 Myroides odoratimimus, 5 Citrobacter freundii, 2 Morganella morganii and 1 Providencia rettgeri were also found among the porcine isolates. Only E. coli isolates were investigated further.

Phenotypic resistance

The phenotypic resistance was similar among the porcine and the poultry E. coli isolates: colistin (0.0% vs. 2.6%), amikacin (39.5% vs. 35.9%), tobramycin (39.5% vs. 35.9%), and all E. coli isolates were resistant to cefotaxime and cefepime. In the case of gentamicin, the resistance was higher within porcine isolates (79.1% vs. 12.8%). The SXT resistance showed similar results (81.4% vs. 35.9%). All of the poultry isolates were resistant to ciprofloxacin, while 68.9% (30/43) of the porcine E. coli were resistant to it. All isolates were susceptible to carbapenems (ertapenem, meropenem, imipenem), the drug group of first choice against ESBL-producers in human medicine (Fig. 1).

Fig. 1.
Fig. 1.

Proportion of isolates resistant to different antibiotics (SXT = sulphamethoxazole/trimethoprim)

Citation: Acta Veterinaria Hungarica 69, 3; 10.1556/004.2021.00036

Prevalence of ESBL gene families

The distribution of ESBL gene families differed between the two groups of isolates. Group CTX-M-1 was the most common; its prevalence was higher in porcine than in poultry isolates (39/43, 90.7% and 27/39, 69.7%, respectively). All but one porcine isolates and all poultry isolates carried the bla CTX-M-1 gene, the remaining one porcine isolate harboured bla CTX-M-3; the bla CTX-M-15 gene was not found in the animal isolates. The CTX-M-2 gene family was found only in porcine isolates (4.7%), while the CTX-M-9 was found in poultry E. coli (7.7%). The CTX-M-8 family was totally absent (Fig. 2). The genes of these groups were not sequenced.

Fig. 2.
Fig. 2.

Result of the PCR examination of ESBL gene families – comparison of porcine and poultry E. coli isolates

Citation: Acta Veterinaria Hungarica 69, 3; 10.1556/004.2021.00036

Fig. 3.
Fig. 3.

Result of E. coli extended phylogroup multiplex PCR based on the method of Clermont et al. (2013)

Citation: Acta Veterinaria Hungarica 69, 3; 10.1556/004.2021.00036

Prevalence of E. coli phylogroups

The occurrence of E. coli phylogroups was different in the two types of isolates. Most of the isolates belonged to commensal phylogroups, but the distribution was different, the porcine isolates could be distributed into three phylogroups, while the poultry isolates were more varied, and only phylogroup D was absent from both types of samples (Fig. 3). Of the porcine isolates, 67.4% (29/43) belonged to phylogroup C, while 11.6% (5/43) and 14.0% (6/43) of these isolates were members of phylogroups A and B1, respectively. Most of the poultry isolates belonged to phylogroups B1 and E (30.8% and 30.8%, 12/39, respectively), while 7.7% (3/39) and 12.8% (5/39) of them could be classified into two other commensal phylogroups, C and F (Fig. 3).

Human isolates

The antibiotic resistance of human isolates was higher against all examined antibiotics. SXT and aminoglycoside resistance rates were 16/17 and 14/17, respectively; one human isolate was resistant against ertapenem.

The most common ESBL gene was the CTX-M-15 (11/17); as expected, four of the isolates proved to be of the clone ST131 clade C2. A single isolate carried blactxm1, another carried CTX-M27 and belonged to the clade ST131/C1-M27. The occurrence of the TEM and SHV gene families was similar among the human isolates (5/17).

Most isolates belonged to the B2 and D phylogroups (10/17, 58.9% and 4/17, 23.5%, respectively); five isolates from the B2 group were of sequence type 131. The remaining isolates belonged to the A and E phylogroups.

Discussion

A high prevalence of ESBL-producing bacteria was found among the poultry and pork isolates. Although the prevalence of ESBL producers was different, the gene distribution was highly similar. These gene patterns did not differ from data of the literature; the vast majority of animal isolates carried bla CTX-M-1 among both types of animal isolates, while in the human isolates bla CTX-M-15 dominated (Bush, 2013; Abraham et al., 2018). This is in line with a previous Hungarian study surveying the faecal carriage of ESBL producers in animals (Tóth et al., 2013) and reporting bla CTX-M-1 as the most common gene.

Very similar results have been reported worldwide, with the dominance of bla CTX-M-1 in poultry (Girlich et al., 2007; Saliu et al., 2017; Gundran et al., 2019), which is horizontally transmitted among different strains (Zurfluh et al., 2014) and may reach humans through the food chain (de Been et al., 2014). Similar dominance and transmission were reported in the case of porcine samples (Abraham et al., 2018). Interestingly, among pig slaughterhouse workers, direct animal contact was associated with a higher risk of carrying ESBL producers (Dohmen et al., 2017), pointing out the importance of transmission through the pork food chain.

Human isolates contemporary with those investigated by Tóth et al. (2013), derived from asymptomatic individuals including animal keepers and abattoir workers, showed a marked dominance of bla CTX-M-1 (Ebrahimi et al., 2014), the other frequent gene was bla CTX-M-15. This proportion shifted towards dominance of the pandemic bla CTX-M-15 carrying the ST131 clone (Ebrahimi et al., 2016a, 2016b), which was also detected in human isolates but, importantly, not in animal isolates in this study.

In general, commensal phylogroups were frequently found among ESBL carriers in animals. In poultry, the phylogroups B2 and D containing extraintestinal pathogens were rare, in line with earlier results (Saliu et al., 2017; op. cit.). In contrast, among porcine isolates the dominant phylogroups among ESBL producers were those associated with intestinal (C) and extraintestinal (A and B1) infections, in the same way as among human isolates (B2 and D).

In animal-derived isolates, bla CTX-M-1 has been the dominant gene in ESBL-producing E. coli for more than a decade, which is also detected continuously, but only in a relatively small proportion of human isolates. In contrast, the gene most important in human isolates, blA CTX-M-15 is found exclusively in human isolates and has failed to cross the species barrier. This suggests that the gene flow is continuous between humans and animal isolates but the proportion of shared genes or isolates is small and unimportant in terms of public health epidemiology in Hungary.

Acknowledgements

The authors thank Ákos Tóth for the critical review of the manuscript. Funding: Bence Balázs, Zoltán Tóth and Fuzsina Nagy were supported by ÚNKP-9/3-I (New National Excellence Program of the Ministry for Innovation and Technology) and the EFOP-3.6.3-VEKOP-16-2017-00009 project co-financed by the EU and the European Social Fund.

References

  • Abraham, S. , Kirkwood, R. N. , Laird, T. , Saputra, S. , Mitchell, T. , Singh, M. , Linn, B. , Abraham, R. J. , Pang, S. , Gordon, D., M. , Trott, D. J. and O’Dea, M. (2018): Dissemination and persistence of extended-spectrum cephalosporin-resistance encoding IncI1-bla CTXM-1 plasmid among Escherichia coli in pigs. ISME J. 12, 23522362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bush, K. (2013): Proliferation and significance of clinically relevant β-lactamases. Ann. N. Y. Acad. Sci. 1277, 8490.

  • Clermont, O. , Christenson, J. K. , Denamur, E. and Gordon, D. M. (2013): The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ. Microbiol. Rep. 5, 5865.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • de Been, M. , Lanza, V. F. , de Toro, M. , Scharringa, J. , Dohmen, W. , Du, Y. , Hu, J. , Lei, Y. , Li, N. , Tooming-Klunderud, A. , Heederik, D. J. , Fluit, A. C. , Bonten, M. J. M. , Willems, R. J. L. , de la Cruz, F. and van Schaik, W. (2014): Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 10, e1004776.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dohmen, W. , Van Gompel, L. , Schmitt, H. , Liakopoulos, A. , Heres, L. , Urlings, B. A. , Mevius, D. , Bonten, M. J. M. and Heederik, D. J. J. (2017): ESBL carriage in pig slaughterhouse workers is associated with occupational exposure. Epidem. Infect. 145, 20032010.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Mészáros, J. , Juhász, Á. and Kardos, G. (2014): Carriage rates and characteristics of Enterobacteriaceae producing extended-spectrum beta-lactamases in healthy individuals: comparison of applicants for long-term care and individuals screened for employment purposes. Chemotherapy 60, 239249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Mészáros, J. , Juhász, Á. , Majoros, L. , Szarka, K. and Kardos, G. (2016a): Asymptomatic faecal carriage of ESBL producing Enterobacteriaceae in Hungarian healthy individuals and in long-term care applicants: A shift towards CTX-M producers in the community. Infect. Dis. 48, 557559.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Monostori, J. , Gorácz, O. , Fésűs, A. , Majoros, L. , Szarka, K. and Kardos, G. (2016b): Comparison of rates of fecal colonization with extended-spectrum beta-lactamase-producing enterobacteria among patients in different wards, outpatients and medical students. Microbiol. Immunol. 60, 285294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ECDC (European Centre for Disease Prevention and Control), EFSA (European Food Safety Authority), and EMA (European Medicines Agency) (2017): ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals – Joint Interagency Antimicrobial Consumption and Resistance Analysis (JIACRA) Report. EFSA J. 15(4872), 135.

    • Search Google Scholar
    • Export Citation
  • Girlich, D. , Poirel, L. , Carattoli, A. , Kempf, I. , Lartigue, M. F. , Bertini, A. and Nordmann, P. (2007): Extended-spectrum β-lactamase CTX-M-1 in Escherichia coli isolates from healthy poultry in France. Appl. Environ. Microbiol. 73, 46814685.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gundran, R. S. , Cardenio, P. A. , Villanueva, M. A. , Sison, F. B. , Benigno, C. C. , Kreausukon, K. , Pichpol, D. and Punyapornwithaya, V. (2019): Prevalence and distribution of bla CTX-M, bla SHV, bla TEM genes in extended-spectrum β-lactamase-producing E. coli isolates from broiler farms in the Philippines. BMC Vet. Res. 15, 227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Matsumura, Y. , Pitout, J. D. , Peirano, G. , DeVinney, R. , Noguchi, T. , Yamamoto, M. , Gomi, R. , Matsuda, T. , Nakano., S. , Nagao, M. , Tanaka, M. and Ichiyama, S. (2017): Rapid identification of different Escherichia coli sequence type 131 clades. Antimicrob. Agents Chemother. 61, e0017917.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nüesch-Inderbinen, M. and Stephan, R. (2016): Epidemiology of extended-spectrum β-lactamase-producing Escherichia coli in the human-livestock environment. Curr. Clin. Microbiol. Rep. 3, 19.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Saliu, E. , Vahjen, W. and Zentek, J. (2017): Types and prevalence of extended-spectrum beta-lactamase producing Enterobacteriaceae in poultry. Anim. Health Res. Rev. 18, 4657.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Silva, N. , Carvalho, I. , Currie, C. , Sousa, M. , Igrejas, G. and Poeta, P. (2019): Extended-spectrum-β-lactamase and carbapenemase-producing Enterobacteriaceae in food-producing animals in Europe: An impact on public health? In: Capelo-Martínez, J.-L. and Igrejas, G. (eds) Antibiotic Drug Resistance. Chapter 12. John Wiley and Sons, Inc. pp. 261273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tóth, Á. , Juhász-Kaszanyitzky, É. , Mag, T. , Hajbel-Vékony, G. , Pászti, J. and Damjanova, I. (2013): Characterization of extended-spectrum β-lactamase (ESBL) producing Escherichia coli strains isolated from animal and human clinical samples in Hungary in 2006–2007. Acta Microbiol. Immunol. Hung. 60, 175185.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Zurfluh, K. , Wang, J. , Klumpp, J. , Nüesch-Inderbinen, M. , Fanning, S. and Stephan, R. (2014): Vertical transmission of highly similar blaCTX-M-1-harbouring IncI1 plasmids in Escherichia coli with different MLST types in the poultry production pyramid. Front. Microbiol. 5, 519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Abraham, S. , Kirkwood, R. N. , Laird, T. , Saputra, S. , Mitchell, T. , Singh, M. , Linn, B. , Abraham, R. J. , Pang, S. , Gordon, D., M. , Trott, D. J. and O’Dea, M. (2018): Dissemination and persistence of extended-spectrum cephalosporin-resistance encoding IncI1-bla CTXM-1 plasmid among Escherichia coli in pigs. ISME J. 12, 23522362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bush, K. (2013): Proliferation and significance of clinically relevant β-lactamases. Ann. N. Y. Acad. Sci. 1277, 8490.

  • Clermont, O. , Christenson, J. K. , Denamur, E. and Gordon, D. M. (2013): The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ. Microbiol. Rep. 5, 5865.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • de Been, M. , Lanza, V. F. , de Toro, M. , Scharringa, J. , Dohmen, W. , Du, Y. , Hu, J. , Lei, Y. , Li, N. , Tooming-Klunderud, A. , Heederik, D. J. , Fluit, A. C. , Bonten, M. J. M. , Willems, R. J. L. , de la Cruz, F. and van Schaik, W. (2014): Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 10, e1004776.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dohmen, W. , Van Gompel, L. , Schmitt, H. , Liakopoulos, A. , Heres, L. , Urlings, B. A. , Mevius, D. , Bonten, M. J. M. and Heederik, D. J. J. (2017): ESBL carriage in pig slaughterhouse workers is associated with occupational exposure. Epidem. Infect. 145, 20032010.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Mészáros, J. , Juhász, Á. and Kardos, G. (2014): Carriage rates and characteristics of Enterobacteriaceae producing extended-spectrum beta-lactamases in healthy individuals: comparison of applicants for long-term care and individuals screened for employment purposes. Chemotherapy 60, 239249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Mészáros, J. , Juhász, Á. , Majoros, L. , Szarka, K. and Kardos, G. (2016a): Asymptomatic faecal carriage of ESBL producing Enterobacteriaceae in Hungarian healthy individuals and in long-term care applicants: A shift towards CTX-M producers in the community. Infect. Dis. 48, 557559.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ebrahimi, F. , Mózes, J. , Monostori, J. , Gorácz, O. , Fésűs, A. , Majoros, L. , Szarka, K. and Kardos, G. (2016b): Comparison of rates of fecal colonization with extended-spectrum beta-lactamase-producing enterobacteria among patients in different wards, outpatients and medical students. Microbiol. Immunol. 60, 285294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ECDC (European Centre for Disease Prevention and Control), EFSA (European Food Safety Authority), and EMA (European Medicines Agency) (2017): ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals – Joint Interagency Antimicrobial Consumption and Resistance Analysis (JIACRA) Report. EFSA J. 15(4872), 135.

    • Search Google Scholar
    • Export Citation
  • Girlich, D. , Poirel, L. , Carattoli, A. , Kempf, I. , Lartigue, M. F. , Bertini, A. and Nordmann, P. (2007): Extended-spectrum β-lactamase CTX-M-1 in Escherichia coli isolates from healthy poultry in France. Appl. Environ. Microbiol. 73, 46814685.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gundran, R. S. , Cardenio, P. A. , Villanueva, M. A. , Sison, F. B. , Benigno, C. C. , Kreausukon, K. , Pichpol, D. and Punyapornwithaya, V. (2019): Prevalence and distribution of bla CTX-M, bla SHV, bla TEM genes in extended-spectrum β-lactamase-producing E. coli isolates from broiler farms in the Philippines. BMC Vet. Res. 15, 227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Matsumura, Y. , Pitout, J. D. , Peirano, G. , DeVinney, R. , Noguchi, T. , Yamamoto, M. , Gomi, R. , Matsuda, T. , Nakano., S. , Nagao, M. , Tanaka, M. and Ichiyama, S. (2017): Rapid identification of different Escherichia coli sequence type 131 clades. Antimicrob. Agents Chemother. 61, e0017917.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nüesch-Inderbinen, M. and Stephan, R. (2016): Epidemiology of extended-spectrum β-lactamase-producing Escherichia coli in the human-livestock environment. Curr. Clin. Microbiol. Rep. 3, 19.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Saliu, E. , Vahjen, W. and Zentek, J. (2017): Types and prevalence of extended-spectrum beta-lactamase producing Enterobacteriaceae in poultry. Anim. Health Res. Rev. 18, 4657.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Silva, N. , Carvalho, I. , Currie, C. , Sousa, M. , Igrejas, G. and Poeta, P. (2019): Extended-spectrum-β-lactamase and carbapenemase-producing Enterobacteriaceae in food-producing animals in Europe: An impact on public health? In: Capelo-Martínez, J.-L. and Igrejas, G. (eds) Antibiotic Drug Resistance. Chapter 12. John Wiley and Sons, Inc. pp. 261273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tóth, Á. , Juhász-Kaszanyitzky, É. , Mag, T. , Hajbel-Vékony, G. , Pászti, J. and Damjanova, I. (2013): Characterization of extended-spectrum β-lactamase (ESBL) producing Escherichia coli strains isolated from animal and human clinical samples in Hungary in 2006–2007. Acta Microbiol. Immunol. Hung. 60, 175185.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Zurfluh, K. , Wang, J. , Klumpp, J. , Nüesch-Inderbinen, M. , Fanning, S. and Stephan, R. (2014): Vertical transmission of highly similar blaCTX-M-1-harbouring IncI1 plasmids in Escherichia coli with different MLST types in the poultry production pyramid. Front. Microbiol. 5, 519.

    • Crossref
    • Search Google Scholar
    • Export Citation

Author information is available in PDF.
Please, download the file from HERE.

The manuscript preparation instructions is available in PDF.
Please, download the file from HERE.

Senior editors

Editor-in-Chief: Mária BENKŐ

Managing Editor: András SZÉKELY

Editorial Board

  • Béla DÉNES (National Food Chain Safety Office, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (National Agricultural Innovation Centre, Herceghalom, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • Balázs HARRACH (Veterinary Medical Research Institute, Budapest, Hungary)
  • Peter MASSÁNYI (Slovak University of Agriculture in Nitra, Nitra, Slovak Republic)
  • Béla NAGY (Veterinary Medical Research Institute, Budapest, Hungary)
  • Tibor NÉMETH (University of Veterinary Medicine, Budapest, Hungary)
  • Zsuzsanna NEOGRÁDY (University of Veterinary Medicine, Budapest, Hungary)
  • Alessandra PELAGALLI (University of Naples Federico II, Naples, Italy)
  • Kurt PFISTER (Ludwig-Maximilians-University of Munich, Munich, Germany)
  • László SOLTI (University of Veterinary Medicine, Budapest, Hungary)
  • József SZABÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Péter VAJDOVICH (University of Veterinary Medicine, Budapest, Hungary)
  • János VARGA (University of Veterinary Medicine, Budapest, Hungary)
  • Štefan VILČEK (University of Veterinary Medicine in Kosice, Kosice, Slovak Republic)
  • Károly VÖRÖS (University of Veterinary Medicine, Budapest, Hungary)
  • Herbert WEISSENBÖCK (University of Veterinary Medicine, Vienna, Austria)
  • Attila ZSARNOVSZKY (Szent István University, Gödöllő, Hungary)

ACTA VETERINARIA HUNGARICA
Institute for Veterinary Medical Research
Centre for Agricultural Research
Hungarian Academy of Sciences
P.O. Box 18, H-1581 Budapest, Hungary
Phone: (36 1) 467 4081 (ed.-in-chief) or (36 1) 213 9793 (editor) Fax: (36 1) 467 4076 (ed.-in-chief) or (36 1) 213 9793

Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • Chemical Abstracts
  • Current Contents: Agriculture, Biology and Environmental Sciences
  • Elsevier Science Navigator
  • Focus On: Veterinary Science and Medicine
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Science Citation Index
  • Science Citation Index Expanded (SciSearch)
  • SCOPUS
  • The ISI Alerting Services
  • Zoological Abstracts

 

2020  
Total Cites 987
WoS
Journal
Impact Factor
0,955
Rank by Veterinary Sciences 101/146 (Q3)
Impact Factor  
Impact Factor 0,920
without
Journal Self Cites
5 Year 1,164
Impact Factor
Journal  0,57
Citation Indicator  
Rank by Journal  Veterinary Sciences 93/166 (Q3)
Citation Indicator   
Citable 49
Items
Total 49
Articles
Total 0
Reviews
Scimago 33
H-index
Scimago 0,395
Journal Rank
Scimago Veterinary (miscellaneous) Q2
Quartile Score  
Scopus 355/217=1,6
Scite Score  
Scopus General Veterinary 73/183 (Q2)
Scite Score Rank  
Scopus 0,565
SNIP  
Days from  145
submission  
to acceptance  
Days from  150
acceptance  
to publication  
Acceptance 19%
Rate

 

2019  
Total Cites
WoS
798
Impact Factor 0,991
Impact Factor
without
Journal Self Cites
0,897
5 Year
Impact Factor
1,092
Immediacy
Index
0,119
Citable
Items
59
Total
Articles
59
Total
Reviews
0
Cited
Half-Life
9,1
Citing
Half-Life
9,2
Eigenfactor
Score
0,00080
Article Influence
Score
0,253
% Articles
in
Citable Items
100,00
Normalized
Eigenfactor
0,09791
Average
IF
Percentile
42,606
Scimago
H-index
32
Scimago
Journal Rank
0,372
Scopus
Scite Score
335/213=1,6
Scopus
Scite Score Rank
General Veterinary 62/178 (Q2)
Scopus
SNIP
0,634
Acceptance
Rate
18%

 

Acta Veterinaria Hungarica
Publication Model Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article
Printed Color Illustrations 40 EUR (or 10 000 HUF) + VAT / piece
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription fee 2021 Online subsscription: 696 EUR / 872 USD
Print + online subscription: 804 EUR / 1004 USD
Subscription fee 2022 Online subsscription: 710 EUR / 892 USD
Print + online subscription: 824 EUR / 1028 USD
Subscription Information Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content.
Purchase per Title Individual articles are sold on the displayed price.

Acta Veterinaria Hungarica
Language English
Size A4
Year of
Foundation
1951
Publication
Programme
2020 Volume 68
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-6290 (Print)
ISSN 1588-2705 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jun 2021 0 0 0
Jul 2021 0 0 0
Aug 2021 0 0 0
Sep 2021 0 0 0
Oct 2021 0 87 90
Nov 2021 0 78 81
Dec 2021 0 0 0