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Contamination of Chicken Meat with Salmonella enterica Serovar Haardt with Nalidixic Acid Resistance and Reduced Fluoroquinolone Susceptibility

  • Lee, Ki-Eun (Culture Collection of Antimicrobial Resistant Microbes, Department of Biology, Seoul Women's University) ;
  • Lee, Min-Young (Culture Collection of Antimicrobial Resistant Microbes, Department of Biology, Seoul Women's University) ;
  • Lim, Ji-Youn (Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho) ;
  • Jung, Ji-Hun (Department of Epidemiology, Division of Microbiology, Seoul Metropolitan Government Research Institute of Public Health and Environment) ;
  • Park, Yong-Ho (Department of Microbiology, College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Lee, Yeon-Hee (Culture Collection of Antimicrobial Resistant Microbes, Department of Biology, Seoul Women's University)
  • Published : 2008.11.30

Abstract

Salmonella contamination in chicken meat was studied with 100 chicken meat samples purchased from 55 shops located in various regions. A total of 21 isolates of Salmonella enterica were isolated from 21 chicken meat samples from four shops located at open markets, whereas there were none from supermarkets with well-equipped cold systems. Among these, 18 isolates were identified as Salmonella enterica serotype Haardt (S. Haardt) and three isolates were S. enterica serotype Muenchen. When the minimal inhibitory concentrations of the S. Haardt isolates were assayed with the agar dilution method to determine susceptibility to ampicillin, chloramphenicol, sulfisoxazole, tetracycline, and nalidixic acid, all 18 isolates were resistant to tetracycline and nalidixic acid and nine of these were resistant to ampicillin. These isolates showed reduced susceptibility to eight fluoroquinolones including ciprofloxacin, enrofloxacin, levofloxacin, gatifloxacin, gemifloxacin, moxifloxacin, norfloxacin, and ofloxacin. When quinolone resistance determining regions of gyrA and gyrB were sequenced, every isolate had the same missense mutation Ser83$\rightarrow$Tyr (TCC$\rightarrow$+TAC) in gyrA, whereas no mutation was found in gyrB. Pulsed-field gel electrophoresis with XbaI revealed a close relationship among these isolates, suggesting a contamination of raw chicken meat with clonal spread of nalidixic acid-resistant and quinolone-reduced susceptibility S. Haardt in chickens. Results in this study show the importance of a well-equipped cold system and the prudent use of fluoroquinolone in chickens to prevent the occurrence of quinolone-resistant isolates.

Keywords

References

  1. Brinas, L., M. Zarazaqa, Y. Saenz, F. Ruiz-Larrea, and C. Torres. 2002. Beta-lactamases in ampicillin-resistant Esherichia coli isolates from foods, humans, and healthy animals. Antimicrob. Agents Chemother. 46: 3156-3163 https://doi.org/10.1128/AAC.46.10.3156-3163.2002
  2. Buchata, R. M. and M. Dunn. 2003. Urinary tract infection due to Salmonella species in children/adolescents. Clin. Pediat. 42: 647-648 https://doi.org/10.1177/000992280304200712
  3. Chen, S., S. Zhao, D. G. White, C. M. Schroeder, R. Lu, H. Yang, P. F. McDermott, S. Ayers, and J. Meng. 2004. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl. Environ. Microbiol. 70: 1-7 https://doi.org/10.1128/AEM.70.1.1-7.2004
  4. Chiu, C. H., L. H. Su, C. C. Hung, K. L. Chen, and C. Chiu. 2004. Prevalence and antimicrobial susceptibility of serogroup D nontyphoidal Salmonella in a university hospital in Taiwan. J. Clin. Microbiol. 42: 415-417 https://doi.org/10.1128/JCM.42.1.415-417.2004
  5. Choi, S. H., J. H. Woo, J. E. Lee, S. J. Park, E. J. Choo, Y. G. Kwak, et al. 2005. Increasing incidence of quinolone resistance in human non-typhoid Salmonella enterica isolates in Korea and mechanisms involved in quinolone resistance. J. Antimicrob. Chemother. 56: 1-4 https://doi.org/10.1093/jac/dki184
  6. Clinical and Laboratory Standards Institute. 2003. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically - Approved Standards, 6th Ed. NCCLS, Wayne, PA
  7. Cook, T. M., W. A. Goss, and W. H. Deitz. 1966. Mechanism of action of nalidixic acid on Escherichia coli V. Possible mutagenic effect. J. Bacteriol. 91: 780-783
  8. Esaki, H., A. Morioka, A. Orioka, K. Ishihara, A. Kojima, S. Shiroki, T. Tamura, and T. Takahashi. 2004. Antimicrobial susceptibility of Salmonella isolated from cattle, swine and poultry (2001-2002): Report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. J. Antimicrob. Chemother. 53: 266-270 https://doi.org/10.1093/jac/dkh081
  9. Escribano, I., J. C. Rodriguaz, and G. Royo. 2004. Mutations in the gyrA gene in Salmonella enterica clinical isolates with decreased ciprofloxacin susceptibility. J. Antimicrob. Agents 24: 102-105
  10. Ewin, W. H. 1986. Serologic identification of Salmonella, pp. 201-238. In W. H. Ewing (ed.), Edwards and Ewing's Identification of Enterobacteriaceae, 4th Ed. Elsevier Science Publishing Co., Inc., New York, NY
  11. Gaillot, O., C. Clement, M. Simonet, and A. Philippon. 1997. Novel transferable $\beta$-lactam resistance with cephalosporinase characteristics in Salmonella enteritidis. J. Antimicrob. Chemother. 39: 85-87 https://doi.org/10.1093/jac/39.1.85
  12. Giraud, E., A. Brisabois, J. L. Martel, and E. Chaslus-Dancla. 1999. Comparative studies of mutations in animal isolates and experimental in vitro- and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinolone-resistant strains in the field. Antimicrob. Agents Chemother. 43: 2131-2137
  13. Griggs, D. J., K. Gensberg, and L. J. V. Piddock. 1996. Mutations in gyrA gene of quinolone-resistant Salmonella serotypes isolated from humans and animals. Antimicrob. Agents Chemother. 40: 1009-1013
  14. Guerra, B., B. Malorny, A. Schroeter, and R. Helmuth. 2003. Multiple resistance mechanisms in fluoroquinolone-resistant Salmonella isolates from Germany. Antimicrob. Agents Chemother. 47: 2059 https://doi.org/10.1128/AAC.47.6.2059.2003
  15. Gupta, A., J. Fontana, C. Crowe, B. Bolstorff, A. Stout, S. Van Duyne, et al. 2003. The National Antimicrobial Resistance Monitoring System PulseNet Working Group, 2003. Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. J. Infect. Dis. 188: 1707-1716 https://doi.org/10.1086/379668
  16. Hakanen, A., P. Kotilainen, P. Huovinen, H. Helenius, and A. Siitonen. 2001. Reduced fluoroquinolone susceptibility in Salmonella enterica serotypes in travelers returning from Southeast Asia. Emerg. Infect. Dis. 7: 996-1003 https://doi.org/10.3201/eid0706.010613
  17. Hakanen, A., P. Kotilainen, J. Jalava, A. Siitonen, and P. Huovinen. 1999. Detection of decreased fluoroquinolone susceptibility in Salmonella and validation of nalidixic acid screening test. J. Clin. Microbiol. 37: 3572-3577
  18. Hooper, D. C. and J. S. Wolfson. 1991. Fluoroquinolone antimicrobial agents. N. Engl. J. Med. 324: 384-394 https://doi.org/10.1056/NEJM199102073240606
  19. Hopkins, K. L., R. H. Davies, and E. J. Threlfall. 2005. Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. Int. J. Antimicrob. Agents 25: 358-373 https://doi.org/10.1016/j.ijantimicag.2005.02.006
  20. Jung, Y. S., H. J. Hong, H. R. Nam, and Y. H. Lee. 2002. Isolation of norfloxacin resistant Escherichia coli from the Han river and characterization of resistance mechanism. J. Microbiol. 40: 63-69
  21. Kilmartin, D., D. Morris, C. O'Hare, G. Corbett-Feeney, and M. Cormican. 2005. Clonal expansion may account for high levels of quinolone resistance in Salmonella enterica serovar Enteritidis. Appl. Environ. Microbiol. 71: 2587-2591 https://doi.org/10.1128/AEM.71.5.2587-2591.2005
  22. Laconcha, I., D. L. Baggesen, A. Rementeria, and J. Garaizar. 2000. Genotypic characterization by PFGE of Salmonella enterica serotype Enteritidis phage types 1, 4, 6, and 8 isolated from animal and human sources in three European countries. Vet. Microbiol. 75: 155-165 https://doi.org/10.1016/S0378-1135(00)00208-X
  23. Lawson, A. J., M. Desai, S. J. O'Brien, R. H. Davies, L. R. Ward, and E. J. Threlfall. 2004. Molecular characterization of an outbreak strain of multiresistant Salmonella enterica serovar Typhimurium DT104 in the UK. Clin. Microbiol. Infect. 10: 143-147 https://doi.org/10.1111/j.1469-0691.2004.00754.x
  24. Lee, Y. J., K. S. Kim, J. H. Kim, and R. B. Tak. 2004. Salmonella gallinarum gyrA mutations associated with fluoroquinolone resistance. Avian Pathol. 33: 251-257 https://doi.org/10.1080/0301945042000195759
  25. Ling, J. M., E. W. Chan, A. W. Lam, and A. F. Cheng. 2003. Mutations in topoisomerase genes of fluoroquinolone-resistant Salmonella in Hong Kong. Antimicrob. Agents Chemother. 47: 3567-3573 https://doi.org/10.1128/AAC.47.11.3567-3573.2003
  26. Mcewen, S. A. and P. J. Fedorka-Cary. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34: S93-S106 https://doi.org/10.1086/340246
  27. McKellar, Q., I. Gibson, A. Monteiro, and M. Bregante. 1999. Pharmacokinetics of enrofloxacin and danofloxacin in plasma, inflammatory exudate, and bronchial secretions of calves following subcutaneous administration. Antimicrob. Agents Chemother. 43: 1988-1992
  28. Mead, P. S., L. Slutsker, V. Dietz, L. F. Macaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5: 607-625 https://doi.org/10.3201/eid0505.990502
  29. Miko, A., K. Pries, A. Schroeter, and R. Helmuth. 2003. Multiple-drug resistance in D-tartrate-positive Salmonella enterica serovar Paratyphi B isolates from poultry is mediated by class 2 integrons inserted into the bacterial chromosome. Antimicrob. Agents Chemother. 47: 3640-3643 https://doi.org/10.1128/AAC.47.11.3640-3643.2003
  30. Molbak, K., D. L. Baggesen, F. M. Aarestrup, J. M. Ebbesen, J. Engberg, K. Frydendahl, P. Gerner-Smidt, A. M. Petersen, and H. C. Wegener. 1999. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT104. N. Engl. J. Med. 341: 1420-1425 https://doi.org/10.1056/NEJM199911043411902
  31. Piddock, L. J. V., V. Ricci, I. McLaren, and D. J. Griggs. 1998. Role of mutations in the gyrA and parC genes of nalidixic-acidresistant Salmonella serotypes isolated from animals in the United Kingdom. J. Antimicrob. Chemother. 41: 635-641 https://doi.org/10.1093/jac/41.6.635
  32. Prats, G., B. Mirelis, T. Llovet, C. Munoz, E. Miro, and F. Navarro. 2000. Antibiotic resistance trends in enteropathogenic bacteria isolated in 1985-1987 and 1995-1998 in Barcelona. Antimicrob. Agents Chemother. 44: 1140-1145 https://doi.org/10.1128/AAC.44.5.1140-1145.2000
  33. Ridley, A. and E. J. Threlafall. 1998. Molecular epidemiology of antibiotic resistance genes in multiresistant epidemic Salmonella typhimurium DT104. Microb. Drug Resist. 4: 113-118 https://doi.org/10.1089/mdr.1998.4.113
  34. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Nat. Acad. Sci. USA 74: 5463-5467

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