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http://dx.doi.org/10.4014/jmb.0800.221

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)
Publication Information
Journal of Microbiology and Biotechnology / v.18, no.11, 2008 , pp. 1853-1857 More about this Journal
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
Salmonella enterica serotype Haardt; chicken; antimicrobial resistance; quinolone; PFGE;
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1 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   DOI   ScienceOn
2 Hooper, D. C. and J. S. Wolfson. 1991. Fluoroquinolone antimicrobial agents. N. Engl. J. Med. 324: 384-394   DOI   ScienceOn
3 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
4 Mcewen, S. A. and P. J. Fedorka-Cary. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34: S93-S106   DOI   ScienceOn
5 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   DOI   ScienceOn
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 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   DOI   ScienceOn
8 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
9 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
10 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   DOI   ScienceOn
11 Buchata, R. M. and M. Dunn. 2003. Urinary tract infection due to Salmonella species in children/adolescents. Clin. Pediat. 42: 647-648   DOI   ScienceOn
12 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   DOI   ScienceOn
13 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   DOI   ScienceOn
14 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   DOI   ScienceOn
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   DOI   ScienceOn
16 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   DOI   ScienceOn
17 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
18 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   DOI   ScienceOn
19 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   DOI   ScienceOn
20 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
21 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
22 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   DOI   ScienceOn
23 Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Nat. Acad. Sci. USA 74: 5463-5467
24 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   DOI   ScienceOn
25 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
26 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   DOI   ScienceOn
27 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   DOI   ScienceOn
28 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   DOI   ScienceOn
29 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   DOI   ScienceOn
30 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   DOI   ScienceOn
31 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   DOI   ScienceOn
32 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   DOI   ScienceOn
33 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
34 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   DOI   ScienceOn