Screening of antimicrobial resistance and molecular detection of fluoroquinolone resistance mechanisms in chicken faeces-derived Escherichia coli

https://doi.org/10.17221/8721-VETMEDCitation:Lenart-Boron A., Augustyniak K., Boron P. (2016): Screening of antimicrobial resistance and molecular detection of fluoroquinolone resistance mechanisms in chicken faeces-derived Escherichia coli . Veterinarni Medicina, 61: 80-89.
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This study was aimed at investigating the resistance to antimicrobial agents and to assess the predominant molecular mechanisms of fluoroquinolone resistance in faecal E. coli strains isolated from chickens farmed in central Poland. Bacterial strains were isolated from faecal samples of chickens reared on four conventional and one organic farm. The disk-diffusion method was applied to assess antimicrobial resistance and the prevalence of particular resistance mechanisms to fluoroquinolones was determined using specific polymerase chain reactions and sequencing of the gyrA and parC genes. Rep-PCR was used to determine the intra-specific variation of E. coli strains. The greatest resistance was observed for ß-lactams (e.g. from 25 to 100% of strains resistant to amoxicillin/clavulanate) and the smallest – for cephalotin (0 to 18.75% resistant strains). Three out of four conventional farms were characterised by very high resistance rates, particularly to enrofloxacin (from 87 to 93.3% of resistant isolates). The majority of multidrug-resistant strains were also isolated from these farms. The presence of plasmid-mediated quinolone resistance genes (qnrB and qnrS) was detected very frequently, even in strains that exhibited phenotypic susceptibility to fluoroquinolones. With respect to point mutations in quinolone resistance determining regions, Ser-83 substitution was observed in numerous strains. Some of the fluoroquinolone-resistant strains appeared to possess both qnr genes coupled with point mutations, which indicates that a high level of resistance can be affected by multiple factors. Nevertheless, excessive use of antimicrobial agents in food-producing animals decreases the susceptibility of commensal strains, even those that never had contact with antibiotics.
References:
Abdi-Hachesoo B, Asasi K, Sharifiyazdi H (2013): Rapid detection of Escherichia coli gyrA and parC mutants in one-day-old broiler chicks in Iran. Veterinaria Italiana 49, 291–297.
 
Bayer HealthCare LLC, Animal Health Division (2010): Baytril® (enrofloxacin) – Antibacterial injectable solution 2.27%. Technical Bulletin. Shawnee Mission, Kansas, USA.
 
Blanco JE, Blanco M, Mora A, Blanco J (1997): Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain. Journal of Clinical Microbiology 35, 2184–2185.
 
Cattoir V., Weill F.-X., Poirel L., Fabre L., Soussy C.-J., Nordmann P. (2007): Prevalence of qnr genes in Salmonella in France. Journal of Antimicrobial Chemotherapy, 59, 751-754  https://doi.org/10.1093/jac/dkl547
 
Drlica K, Zhao XL (1997): DNA gyrase, topoisomerase IV and the 4-quinolones. Microbiology and Molecular Biology Reviews 61, 377–392.
 
Dzierzawski A, Cybulski W (2012): The need for prudent use of antibiotics in veterinary practice (in Polish). Veterinary Life 87, 316–321.
 
EXCOFFIER LAURENT, LISCHER HEIDI E. L. (2010): Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567  https://doi.org/10.1111/j.1755-0998.2010.02847.x
 
European Committee on Antimicrobial Susceptibility Testing (2013): Breakpoint tables for interpretation of MICs and zone diameters.
 
Gniadkowski M, Zabicka D, Hryniewicz W (2009): Recommended selection of the antimicrobial susceptibility tests for bacteria. Determination of Gram-negative rods susceptibility. National Reference Centre for Antimicrobial Susceptibility. Warsaw, Poland.
 
Hawkey P. M. (): Mechanisms of quinolone action and microbial response. Journal of Antimicrobial Chemotherapy, 51, 29-35  https://doi.org/10.1093/jac/dkg207
 
Yousef D. O. (): DNA Strand Cleavage Is Required for Replication Fork Arrest by a Frozen Topoisomerase-Quinolone-DNA Ternary Complex. Journal of Biological Chemistry, 271, 26424-26429  https://doi.org/10.1074/jbc.271.42.26424
 
Hopkins Katie L., Davies Robert H., Threlfall E. John (2005): Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. International Journal of Antimicrobial Agents, 25, 358-373  https://doi.org/10.1016/j.ijantimicag.2005.02.006
 
Kaplan T (2014): The role of horizontal gene transfer in antibiotic resistance. Eukaryon 10, 80–81.
 
Liu J.-H., Deng Y.-T., Zeng Z.-L., Gao J.-H., Chen L., Arakawa Y., Chen Z.-L. (): Coprevalence of Plasmid-Mediated Quinolone Resistance Determinants QepA, Qnr, and AAC(6')-Ib-cr among 16S rRNA Methylase RmtB-Producing Escherichia coli Isolates from Pigs. Antimicrobial Agents and Chemotherapy, 52, 2992-2993  https://doi.org/10.1128/AAC.01686-07
 
Łebkowska M (2009): Antibiotic resistant bacteria in drinking water (in Polish). Environmental Protection 31, 11–15.
 
Martínez-Martínez Luis, Pascual Alvaro, Jacoby George A (1998): Quinolone resistance from a transferable plasmid. The Lancet, 351, 797-799  https://doi.org/10.1016/S0140-6736(97)07322-4
 
Miles TD, McLaughlin W, Brown PD (2006): Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Veterinary Research 2, 1–9. https://doi.org/10.1186/1746-6148-2-7
 
Moniri R, Dastehgoli K (2005): Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: is there a link? Microbial Ecology and Disease 17, 69–74.
 
Namboodiri Sreela S, Opintan Japheth A, Lijek Rebeccah S, Newman Mercy J, Okeke Iruka N (2011): Quinolone resistance in Escherichia coli from Accra, Ghana. BMC Microbiology, 11, 44-  https://doi.org/10.1186/1471-2180-11-44
 
Phillips I. (2003): Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. Journal of Antimicrobial Chemotherapy, 53, 28-52  https://doi.org/10.1093/jac/dkg483
 
Rysz Michal, Alvarez Pedro J.J. (2004): Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Research, 38, 3705-3712  https://doi.org/10.1016/j.watres.2004.06.015
 
. T. Zahraei Salehi, . S. Farashi Bonab (2006): Antibiotics Susceptibility Pattern of Escherichia coli Strains Isolated from Chickens with Colisepticemia in Tabriz Province, Iran. International Journal of Poultry Science, 5, 677-684  https://doi.org/10.3923/ijps.2006.677.684
 
Sapkota Amy R., Hulet R. Michael, Zhang Guangyu, McDermott Patrick, Kinney Erinna L., Schwab Kellogg J., Joseph Sam W. (2011): Lower Prevalence of Antibiotic-Resistant Enterococci on U.S. Conventional Poultry Farms that Transitioned to Organic Practices. Environmental Health Perspectives, 119, 1622-1628  https://doi.org/10.1289/ehp.1003350
 
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (): MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725-2729  https://doi.org/10.1093/molbev/mst197
 
TOLLEFSON L., ALTEKRUSE S.F., POTTER M.E. (1997): Therapeutic antibiotics in animal feeds and antibiotic resistance. Revue Scientifique et Technique de l'OIE, 16, 709-715  https://doi.org/10.20506/rst.16.2.1054
 
Tran J. H., Jacoby G. A. (2002): Mechanism of plasmid-mediated quinolone resistance. Proceedings of the National Academy of Sciences, 99, 5638-5642  https://doi.org/10.1073/pnas.082092899
 
van den Bogaard A. E. (): Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy, 47, 763-771  https://doi.org/10.1093/jac/47.6.763
 
Veldman K., Cavaco L. M., Mevius D., Battisti A., Franco A., Botteldoorn N., Bruneau M., Perrin-Guyomard A., Cerny T., De Frutos Escobar C., Guerra B., Schroeter A., Gutierrez M., Hopkins K., Myllyniemi A.-L., Sunde M., Wasyl D., Aarestrup F. M. (): International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. Journal of Antimicrobial Chemotherapy, 66, 1278-1286  https://doi.org/10.1093/jac/dkr084
 
Versalovic J, Schneider M, De Bruin FJ, Lupski JR (1994): Genomic fingerprinting of bacteria uusing repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cell Biology 5, 25–40.
 
VILLESEN P. (2007): FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes, 7, 965-968  https://doi.org/10.1111/j.1471-8286.2007.01821.x
 
Wang H., Dzink-Fox J. L., Chen M., Levy S. B. (2001): Genetic Characterization of Highly Fluoroquinolone-Resistant Clinical Escherichia coli Strains from China: Role of acrR Mutations. Antimicrobial Agents and Chemotherapy, 45, 1515-1521  https://doi.org/10.1128/AAC.45.5.1515-1521.2001
 
Witte W. (): BIOMEDICINE: Medical Consequences of Antibiotic Use in Agriculture. Science, 279, 996-997  https://doi.org/10.1126/science.279.5353.996
 
https://www.soilassociation.org/LinkClick.aspx?fileticket=T_9ATk3bieI%3D&tabid=1715
 
Abdi-Hachesoo B, Asasi K, Sharifiyazdi H (2013): Rapid detection of Escherichia coli gyrA and parC mutants in one-day-old broiler chicks in Iran. Veterinaria Italiana 49, 291–297.
 
Bayer HealthCare LLC, Animal Health Division (2010): Baytril® (enrofloxacin) – Antibacterial injectable solution 2.27%. Technical Bulletin. Shawnee Mission, Kansas, USA.
 
Blanco JE, Blanco M, Mora A, Blanco J (1997): Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain. Journal of Clinical Microbiology 35, 2184–2185.
 
Cattoir V., Weill F.-X., Poirel L., Fabre L., Soussy C.-J., Nordmann P. (2007): Prevalence of qnr genes in Salmonella in France. Journal of Antimicrobial Chemotherapy, 59, 751-754  https://doi.org/10.1093/jac/dkl547
 
Drlica K, Zhao XL (1997): DNA gyrase, topoisomerase IV and the 4-quinolones. Microbiology and Molecular Biology Reviews 61, 377–392.
 
Dzierzawski A, Cybulski W (2012): The need for prudent use of antibiotics in veterinary practice (in Polish). Veterinary Life 87, 316–321.
 
EXCOFFIER LAURENT, LISCHER HEIDI E. L. (2010): Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567  https://doi.org/10.1111/j.1755-0998.2010.02847.x
 
European Committee on Antimicrobial Susceptibility Testing (2013): Breakpoint tables for interpretation of MICs and zone diameters.
 
Gniadkowski M, Zabicka D, Hryniewicz W (2009): Recommended selection of the antimicrobial susceptibility tests for bacteria. Determination of Gram-negative rods susceptibility. National Reference Centre for Antimicrobial Susceptibility. Warsaw, Poland.
 
Hawkey P. M. (): Mechanisms of quinolone action and microbial response. Journal of Antimicrobial Chemotherapy, 51, 29-35  https://doi.org/10.1093/jac/dkg207
 
Yousef D. O. (): DNA Strand Cleavage Is Required for Replication Fork Arrest by a Frozen Topoisomerase-Quinolone-DNA Ternary Complex. Journal of Biological Chemistry, 271, 26424-26429  https://doi.org/10.1074/jbc.271.42.26424
 
Hopkins Katie L., Davies Robert H., Threlfall E. John (2005): Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. International Journal of Antimicrobial Agents, 25, 358-373  https://doi.org/10.1016/j.ijantimicag.2005.02.006
 
Kaplan T (2014): The role of horizontal gene transfer in antibiotic resistance. Eukaryon 10, 80–81.
 
Liu J.-H., Deng Y.-T., Zeng Z.-L., Gao J.-H., Chen L., Arakawa Y., Chen Z.-L. (): Coprevalence of Plasmid-Mediated Quinolone Resistance Determinants QepA, Qnr, and AAC(6')-Ib-cr among 16S rRNA Methylase RmtB-Producing Escherichia coli Isolates from Pigs. Antimicrobial Agents and Chemotherapy, 52, 2992-2993  https://doi.org/10.1128/AAC.01686-07
 
Łebkowska M (2009): Antibiotic resistant bacteria in drinking water (in Polish). Environmental Protection 31, 11–15.
 
Martínez-Martínez Luis, Pascual Alvaro, Jacoby George A (1998): Quinolone resistance from a transferable plasmid. The Lancet, 351, 797-799  https://doi.org/10.1016/S0140-6736(97)07322-4
 
Miles TD, McLaughlin W, Brown PD (2006): Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Veterinary Research 2, 1–9. https://doi.org/10.1186/1746-6148-2-7
 
Moniri R, Dastehgoli K (2005): Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: is there a link? Microbial Ecology and Disease 17, 69–74.
 
Namboodiri Sreela S, Opintan Japheth A, Lijek Rebeccah S, Newman Mercy J, Okeke Iruka N (2011): Quinolone resistance in Escherichia coli from Accra, Ghana. BMC Microbiology, 11, 44-  https://doi.org/10.1186/1471-2180-11-44
 
Phillips I. (2003): Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. Journal of Antimicrobial Chemotherapy, 53, 28-52  https://doi.org/10.1093/jac/dkg483
 
Rysz Michal, Alvarez Pedro J.J. (2004): Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Research, 38, 3705-3712  https://doi.org/10.1016/j.watres.2004.06.015
 
. T. Zahraei Salehi, . S. Farashi Bonab (2006): Antibiotics Susceptibility Pattern of Escherichia coli Strains Isolated from Chickens with Colisepticemia in Tabriz Province, Iran. International Journal of Poultry Science, 5, 677-684  https://doi.org/10.3923/ijps.2006.677.684
 
Sapkota Amy R., Hulet R. Michael, Zhang Guangyu, McDermott Patrick, Kinney Erinna L., Schwab Kellogg J., Joseph Sam W. (2011): Lower Prevalence of Antibiotic-Resistant Enterococci on U.S. Conventional Poultry Farms that Transitioned to Organic Practices. Environmental Health Perspectives, 119, 1622-1628  https://doi.org/10.1289/ehp.1003350
 
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (): MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725-2729  https://doi.org/10.1093/molbev/mst197
 
TOLLEFSON L., ALTEKRUSE S.F., POTTER M.E. (1997): Therapeutic antibiotics in animal feeds and antibiotic resistance. Revue Scientifique et Technique de l'OIE, 16, 709-715  https://doi.org/10.20506/rst.16.2.1054
 
Tran J. H., Jacoby G. A. (2002): Mechanism of plasmid-mediated quinolone resistance. Proceedings of the National Academy of Sciences, 99, 5638-5642  https://doi.org/10.1073/pnas.082092899
 
van den Bogaard A. E. (): Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy, 47, 763-771  https://doi.org/10.1093/jac/47.6.763
 
Veldman K., Cavaco L. M., Mevius D., Battisti A., Franco A., Botteldoorn N., Bruneau M., Perrin-Guyomard A., Cerny T., De Frutos Escobar C., Guerra B., Schroeter A., Gutierrez M., Hopkins K., Myllyniemi A.-L., Sunde M., Wasyl D., Aarestrup F. M. (): International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. Journal of Antimicrobial Chemotherapy, 66, 1278-1286  https://doi.org/10.1093/jac/dkr084
 
Versalovic J, Schneider M, De Bruin FJ, Lupski JR (1994): Genomic fingerprinting of bacteria uusing repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cell Biology 5, 25–40.
 
VILLESEN P. (2007): FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes, 7, 965-968  https://doi.org/10.1111/j.1471-8286.2007.01821.x
 
Wang H., Dzink-Fox J. L., Chen M., Levy S. B. (2001): Genetic Characterization of Highly Fluoroquinolone-Resistant Clinical Escherichia coli Strains from China: Role of acrR Mutations. Antimicrobial Agents and Chemotherapy, 45, 1515-1521  https://doi.org/10.1128/AAC.45.5.1515-1521.2001
 
Witte W. (): BIOMEDICINE: Medical Consequences of Antibiotic Use in Agriculture. Science, 279, 996-997  https://doi.org/10.1126/science.279.5353.996
 
https://www.soilassociation.org/LinkClick.aspx?fileticket=T_9ATk3bieI%3D&tabid=1715
 
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