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Erva Rakici Department of Medical Microbiology, Faculty of Medicine, Recep Tayyip Erdogan University, 53020 Rize, Turkey

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Abdullah Altunisik Department of Biology, Faculty of Arts and Sciences, Recep Tayyip Erdogan University, Rize, Turkey

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Kazim Sahin Department of Medical Microbiology, Faculty of Medicine, Recep Tayyip Erdogan University, 53020 Rize, Turkey

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Osman Birol Ozgumus Department of Medical Microbiology, Faculty of Medicine, Recep Tayyip Erdogan University, 53020 Rize, Turkey

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Abstract

The aim of this study was to evaluate the prevalence and types of antimicrobial resistance among Gram-negative enteric bacteria isolated from Pelophylax sp. Fifty-four frogs were collected from six provinces in the Eastern Black Sea Region of Turkey. In the cloacal swab cultures, bacteria from 160 different colonies were identified by biochemical tests, automated systems, and matrix-assisted laser desorption ionisation-time of flight mass spectrometry. The antimicrobial susceptibility tests were performed by the disk diffusion method. The observed drug resistance rate was the highest to ampicillin and cefazolin, while the lowest against ciprofloxacin and tetracycline. In the molecular assays, bla TEM (8 Citrobacter spp.), bla SHV (2 Escherichia coli, 1 Hafnia alvei, and a Serratia liquefaciens), tetA genes (E. coli and Klebsiella spp.) and a class 1 integron without any gene cassette (E. coli) were detected. Among the strains, no plasmid-mediated quinolone resistance [qnrA, qnrB, qnrS, qepA and aac (6 ′)-Ib-cr] was found. However, two of three quinolone-resistant Klebsiella strains showed the novel amino acid substitution in the gyrA gene resulting in Ser83Asp and Asp87Glu.The clonality between E. coli isolates was also examined by pulsed-field gel electrophoresis. We consider that multidrug-resistant Gram-negative enteric bacteria in the intestinal microbiota of a cosmopolitan frog species might be a reservoir for antibiotic resistance genes.

  • Altschul, S. F. , Gish, W. , Miller, W. , Myers, E. W. and Lipman, D. J. (1990): Basic local alignment search tool. J. Mol. Biol. 215, 403410.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Arlet, G. , Brami, G. , Decre, D. , Flippo, A. , Gaillot, O. , Lagrange, P. H. and Philippon, A. (1995): Molecular characterisation by PCR-restriction fragment length polymorphism of TEM beta-lactamases. FEMS Microb. Lett. 134, 203208.

    • Search Google Scholar
    • Export Citation
  • Arlet, G. , Rouveau, M. and Philippon, A. (1997): Substitution of alanine for aspartate at position 179 in the SHV-6 extended spectrum beta lactamase. FEMS Microb. Lett. 152, 163167.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ausubel, F. M. , Brient, R. , Kingston, R. E. , Moore, D. D. , Seidman, J. G. , Smith, J. A. and Struhl, K. (1995): Short Protocols in Molecular Biology. 2nd edition. John Wiley & Sons, New York.

    • Search Google Scholar
    • Export Citation
  • Balta, F. , Sandalli, C. , Kayis, S. and Ozgumus, O. B. (2010): Molecular analysis of antimicrobial resistance in Yersinia ruckeri strains isolated from rainbow trout (Oncorhynchus mykiss) grown in commercial fish farms in Turkey. Bull. Eur. Ass. Fish Pathol. 30, 211219.

    • Search Google Scholar
    • Export Citation
  • Boman, H. G. (2000): Innate immunity and the normal microflora. Immun. Rev. 173, 516.

  • Bryne-Bailey, K. G. , Gaze, W. H. , Zhang, L. , Kay, P. , Boxall, A. , Hawkey, P. M. and Wellington, E. M. (2011): Integron prevalence and diversity in manured soil. Appl. Environ. Microb. 77 ,684687.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Carroll, D. , Wang, J. , Fanning, S. and McMahon, B. J. (2015): Antimicrobial resistance in wildlife: Implications for public health. Zoonoses Public Health 62, 534542.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cattoir, V. , Poirel, L. , Rotimi, V. , Soussy, C. J. and Nordmann, P. (2007): Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 60, 394397.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Chaibi, E. B. , Sirot, D. , Paul, G. and Labia, R. (1999): Inhibitor resistant TEM β-lactamases: phenotypic, genetic and biochemical characteristics. J. Antimicrob. Chemother. 43, 447458.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cissell, R. L. (2006): Occurrence of Antibiotic Resistance in Environmental and Amphibian E. coli Isolates Associated with Cattle and Aquatic Environments. Master’s Thesis, University of Tennessee, Knoxville, USA.

    • Search Google Scholar
    • Export Citation
  • Cullen, M. E. , Wyke, A. W. , Kuroda, R. and Fisher, L. M. (1989): Cloning and characterization of a DNA gyrase A gene from Escherichia coli that confers clinical resistance to 4-quinolones. Antimicrob. Agents Chemother. 33, 886894.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Durmaz, R. , Otlu, B. and Koksal, F. (2009): The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn. J. Infect. Dis. 62, 372377.

    • Search Google Scholar
    • Export Citation
  • Erismis, U. C. (2011): Abundance, demography and population structure of Pelophylax ridibundus (Anura: Ranidae) in 26 August National Park (Turkey). North-West J. Zool. 7, 516.

    • Search Google Scholar
    • Export Citation
  • EUCAST (2016): Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 6.0, 2016. The European Committee on Antimicrobial Susceptibility Testing. http://www.eucast.org.

    • Search Google Scholar
    • Export Citation
  • Ferranti, M. , Cicogna, G. T. , Sattin, A. and Alaibac, M. (2018): Citrobacter freundii sepsis in an immunosuppressed patient with pemphigus vulgaris. BMJ Case Rep. 11, 227091.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fluit, A. C. and Schmitz, F. J. (2004): Resistance integrons and superintegrons. Clin. Microbiol. Infect. 10, 272288.

  • Gilliver, M. A. , Bennet, M. , Begon, M. , Hazel, S. M. and Hart, C. A. (1999): Antibiotic resistance found in wild rodents. Nature 401, 233234.

  • Gonçalves, A. , Igrejas, G. , Radhouani, H. , Estepa, V. , Alcaide, E. , Zorrilla, I. , Serra, R. , Torres, C. and Poeta, P. (2012): Detection of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of Iberian lynx. Lett. App. Microbiol. 54, 7377.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Grinsted, J. F. , Cruz, D. L. and Schmitt, R. (1990): The Tn21 subgroup of bacterial transposable elements. Plasmid 24, 163189.

  • Guardabassi, L. , Dijkshoorn, L. , Collard, J. M. , Olsen, J. E. and Dalsgaard, A. (2000): Distribution and in-vitro transfer of tetracycline resistance determinants in clinical and aquatic Acinetobacter strains. J. Med. Microbiol. 49, 929936.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hacioglu, N. and Tosunoglu, M. (2014): Determination of antimicrobial and heavy metal resistance profiles of some bacteria isolated from aquatic amphibian and reptile species. Environ. Monit. Assess. 86, 407413.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hird, D. W. , Diesch, S. L. , McKinnell, R. G. , Gorham, E. , Martin, F. B. , Meadows, C. A. and Gasiorowski, M. (1983): Enterobacteriaceae and Aeromonas hydrophila in Minnesota frogs and tadpoles (Rana pipiens). Appl. Environ. Microbiol. 46, 14231425.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hosoglu, S. , Esen, S. , Ozturk, R. , Altındis, M. , Ertek, M. , Kaygusuz, S. , Caylan, R. , Demirdag, K. , Sencan, I. , Ertem, G.T. , Aslan, S. , Bosnak, V. , Aygun, P. , Erol, S. and Celen, M. K. (2005): The effect of a restriction policy on the antibiotic consumption in Turkey: a country-wide study. Eur. J. Clin. Pharmacol. 61, 727731.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jacoby, G. A. (2005): Mechanisms of resistance to quinolones. Clin. Infec. Dis. 41, 120126.

  • Kadavy, D. R. , Hornby, J. M. , Haverkost, T. and Nickerson, K. W. (2000): Natural antibiotic resistance of bacteria isolated from larvae of the oil fly, Helaeomyia petrolei. Appl. Environ. Microbiol. 66, 46154619.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kim, H. B. , Park, C. H. , Kim, C. J. , Kim, E. C. , Jacoby, G. A. and Hooper, D. C. (2009): Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob. Agents Chemother. 53, 639645.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lévesque, C. , Piche, L. , Larose, C. and Roy, P. H. (1995): PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob. Agents Chemother. 39, 185191.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lim, K. T. , Yasin, R. , Yeo, C. C. , Puthucheary, S. and Thong, K. L. (2009): Characterization of multidrug resistant ESBL-producing Escherichia coli isolates from hospitals in Malaysia. J. Biomed. Biotechnol. 2009, 165637.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Machado, E. , Canto, R. , Baquero, F. , Gala, J. C. , Rolla, A. , Peixe, L. and Coque, T. M. (2005): Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain. Antimicrob. Agents Chemother. 49, 18231829.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Magiorakos, A.-P. , Srinivasan, A. , Carey, R. B. , Carmeli, Y. , Falagas, M. E. , Giske, C. G. , Harbarth, S. , Hindler, J. F. , Kahlmeter, G. , Olsson-Liljequist, B. , Paterson, D. L. , Rice, L. B. , Stelling, J. , Struelens, M. J. , Vatopoulos, A. , Weber, J. T. and Monnet, D. L. (2012): Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mahaney, P. A. (1994): Effects of fresh water petroleum contamination on amphibian hatching and metamorphosis. Environ. Toxicol. Chem. 13, 259265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marshall, B. , Tachibana, C. and Levy, S. B. (1983): Frequency of tetracycline resistance determinant classes among lactose fermenting coliforms. Antimicrob. Agents Chemother. 24, 835840.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marti, E. , Variatza, E. and Balcazar, J. L. (2014): The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol. 22, 3641.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Minette, H. P. (1984): Epidemiologic aspects of salmonellosis in reptiles, amphibians, mollusks and crustaceans – a review. Int. J. Zoonoses. 11, 95104.

    • Search Google Scholar
    • Export Citation
  • Moon, D. C. , Seol, S. Y. , Gurung, M. , Jin, J. S. , Choi, C. H. , Kim, J. , Lee, Y. C. , Cho, D. T. and Lee, J. C. (2010): Emergence of a new mutation and its accumulation in the topoisomerase IV gene confers high levels of resistance to fluoroquinolone in Escherichia coli isolates. Int. J. Antimicrob. Agents 35, 7679.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Napier, M. D. , Haugland, R. , Poole, C. , Dufour, A. P. , Stewart, J. R. and Weber, D. J. (2017): Exposure to human-associated faecal indicators and self-reported illness among swimmers at recreational beaches: a cohort study. Environ. Health 16, 103.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ozgumus, O. B. , Caylan, R. , Tosun, I. , Sandalli, C. , Aydin, K. and Koksal, I. (2007): Molecular epidemiology of clinical Pseudomonas aeruginosa isolates carrying the IMP-1 metallo-beta-lactamase gene in a university hospital in Turkey. Microb. Drug Resist. 13, 191198.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ozgumus, O. B. , Sandalli, C. , Sevim, A. , Celik-Sevim, E. and Sivri, N. (2009): Class 1 and class 2 integrons and plasmid-mediated antibiotic resistance in coliforms isolated from ten rivers in northern Turkey. J. Microbiol. 47, 1927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Park, C. H. , Robicsek, A. , Jacoby, G. A. , Sahm, D. and Hooper, D. C. (2006): Prevalence in the United States of aac(6)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob. Agents Chemother. 50, 39533955.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Robicsek, A. , Strahilevitz, J. , Sahm, D. F. , Jacoby, G. A. and Hooper, D.C. (2006): qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob. Agents Chemother. 50, 28722874.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rowe-Magnus, D. A. and Mazel, D. (2002): The role of integrons in antibiotic resistance gene capture. Int. J. Med. Microbiol. 292, 115125.

  • Sandalli, C. , Ozgumus, O. B. and Sevim, A. (2010): Characterization of tetracycline resistance genes in tetracycline resistant Enterobacteriaceae obtained from a coliform collection. World J. Microbiol. Biotechnol. 26, 20992103.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Schmidt, A. S. , Bruun, M. S. , Dalsgaard, I. and Larsen, J. L. (2001): Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile aeromonads from a fish farming environment. Appl. Environ. Microbiol. 67, 56755682.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sewell, D. and Griffiths, R. A. (2009): Can a single amphibian species be a good biodiversity indicator? Diversity 1, 102117.

  • Taylor, N. G. H. (2011): Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol. Evol. 26, 278284.

  • Tenover, F. C. , Arbeit, R. D. and Goering, R. V. (1995): Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33, 22332239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thompson, J. D. , Higgins, D. G. and Gipson, T. J. (1994): CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 46734680.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Villa, J. , Ruiz, J. , Goni, P. and Jimenes de Anta, M. T. (1996): Detection of mutations of parC in quinolone-resistance clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40, 491493.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wang, J. T. , Chang, S. C. , Chen, Y. C. and Luh, K. T. (2000): Comparison of antimicrobial susceptibility of Citrobacter freundii isolates in two different time periods. J. Microbiol. Immunol. Infect. 33, 258362.

    • Search Google Scholar
    • Export Citation
  • Webber, M. and Piddock, L. J. V. (2001): Quinolone resistance in Escherichia coli. Vet. Res. 32, 275284.

  • Wells, K. D. (2007): The Ecology and Behavior of Amphibians. The University of Chicago Press.

  • White, P. A. , McIver, C. J. and Rawlinson, W. D. (2001): Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob. Agents Chemother. 45, 26586261.

    • Crossref
    • Search Google Scholar
    • Export Citation
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Senior editors

Editor-in-Chief: Ferenc BASKA

Editorial assistant: Szilvia PÁLINKÁS

 

Editorial Board

  • Mária BENKŐ (Acta Veterinaria Hungarica, Budapest, Hungary)
  • Gábor BODÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Béla DÉNES (University of Veterinary Medicine, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (University of Veterinary Medicine, Budapest, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • János GÁL (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)
  • Dušan PALIĆ (Ludwig Maximilian University, Munich, Germany)
  • 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)

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Acta Veterinaria Hungarica
Language English
Size A4
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1951
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1
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4
Founder Magyar Tudományos Akadémia
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