Clonal spread of salmonella enterica serovar infantis in Serbia: Acquisition of mutations in the topoisomerase genes gyrA and parC leads to increased resistance to fluoroquinolones

Zoonoses and Public Health

Volumn 61, Issue 5, 2014, Pages 364-370

  Velhner, M ^a   Kozoderovic G ^b   Grego, E ^c   Galic N ^c   Stojanov, I ^a   Jelesic Z ^b   Kehrenberg, C ^d  

^a Scientific Veterinary Institute 'Novi Sad'   (Serbia)

^b INSTITUTE OF PUBLIC HEALTH OF VOJVODINA   (Serbia)

^c Institute of Public Health of Serbia 'Dr Milan Jovanovic Batut'   (Serbia)

^d UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Antimicrobial resistance; Foodborne pathogens; Microbiology; Poultry; Public health; Salmonella spp

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; CEFOTAXIME; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; GENTAMICIN; NALIDIXIC ACID; QUINOLINE DERIVED ANTIINFECTIVE AGENT; STREPTOMYCIN; SULFONAMIDE; TETRACYCLINE; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE IV; TRANSCRIPTOME;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; DISK DIFFUSION; GENE; GENE MUTATION; GYRA GENE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PARC GENE; PHENOTYPE; PRIORITY JOURNAL; SALMONELLA INFANTIS; SERBIA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SALMONELLA ENTERICA; SALMONELLA INFECTIONS;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR INFANTIS;

DNA GYRASE; DNA TOPOISOMERASE IV; DNA TOPOISOMERASES; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SERBIA; TRANSCRIPTOME;

EID: 84903820692     PISSN: 18631959     EISSN: 18632378     Source Type: Journal    
DOI: 10.1111/zph.12081     Document Type: Article

References (29)

1. Cavaco, L. M., H. Hasman, S. Xia, and F. M. Aarestrup, 2009: qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob. Agents Chemother. 53, 603-608.
2. Clinical and Laboratory Standards Institute, 2012a: Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard-Ninth Edition. CLSI document M07-A9. CLSI, Wayne, PA, USA.
3. Clinical and Laboratory Standards Institute, 2012b: Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement. Clinical and Laboratory Standards Institute document M100-S22. CLSI, Wayne, PA, USA.
4. Clinical and Laboratory Standards Institute, 2012c: Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard-Eleventh Edition. Preparation of PFGE Plugs from Agar Cultures. section 5.11 PulseNet, CDC, CLSI document M02-A11. CLSI, Wayne, PA, USA.
5. Dionisi, A. M., C. Lucarelli, I. Benedetti, S. Owczarek, and I. Luzzi, 2011: Molecular characterization of multidrug-resistant S. enterica serotype Infantis from humans, animals and the environment in Italy. Int. J. Antimicrob. Agents 38, 384-389.
6. Dunowska, M., P. S. Morley, J. L. Traub-Dargatz, M. A. Davis, G. Patterson, J. G. Frye, D. R. Hyatt, and D. A. Dargatz, 2007: Comparison of S. enterica serotype Infantis isolates from veterinary teaching hospital. J. Appl. Microbiol. 102, 1527-1536.
7. Eaves, D. J., L. Randall, D. T. Gray, A. Buckley, M. J. Woodward, A. P. White, and L. J. V. Piddock, 2004: Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC and parE and association with antibiotic resistance in quinolone-resistant S. enterica. Antimicrob. Agents Chemother. 48, 4012-4015.
8. EFSA and ECDC - European Food Safety Authority and European Centre for Disease Prevention and Control, 2011: The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic agents and food-borne outbreaks in 2009. EFSA J. 9, 2090. [378 pp.] www.efsa.europa.eu/efsajournal
9. Escribano, I., J. C. Rodríguez, and G. Royo, 2004: Mutations in the gyrA gene in S. enterica clinical isolates with decreased ciprofloxacin susceptibility. Int. J. Antimicrob. Agents 24, 102-105.
10. Fonseca, E. L., O. L. Mykytczuk, M. D. Asensi, E. M. F. Reis, L. R. Ferraz, F. L. Paula, L. K. Ng, and D. P. Rodrigues, 2006: Clonality and antimicrobial resistance gene profiles of multidrug-resistant S. enterica serovar Infantis isolates from four public hospitals in Rio de Janeiro, Brazil. J. Clin. Microbiol. 44, 2767-2772.
11. Galanis, E., M. A. Danilo, L. F. Wong, M. E. Patrick, N. Binsztein, A. Cieslik, T. Chalermchaikit, A. Aidara-Kane, A. Ellis, F. J. Angulo, and H. C. Wegener, 2006: Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg. Infect. Dis. 12, 381-388.
12. Gal-Mor, O., L. Valinsky, M. Weinberger, S. Guy, J. Jaffe, Y. I. Schorr, A. Raisfeld, V. Agmon, and I. Nissan, 2010: Multidrug-resistant S. enterica serovar Infantis, Israel. Emerg. Infect. Dis. 16, 1754-1757.
13. Giraud, E., S. Baucheron, and A. Cloeckaert, 2006: Resistance to fluoroquinolones in Salmonella: emerging mechanism and resistance prevention strategies. Microbes Infect. 8, 1937-1944.
14. Hauser, E., E. Tietze, R. Helmuth, E. Junker, R. Prager, A. Schroeter, W. Rabsch, A. Fruth, A. Toboldt, and B. Malorny, 2012: Clonal dissemination of S. enterica serovar Infantis in Germany. Foodborne Pathog. Dis. 9, 352-360.
15. Kehrenberg, C., S. Friederich, A. de Jong, G. Brenner Michael, and S. Schwarz, 2006: Identification of the plasmid-borne quinolone resistant gene qnrS in S. enterica serovar Infantis. J. Antimicrob. Chemother. 58, 18-22.
16. Kehrenberg, C., A. de Jong, S. Friederichs, A. Cloeckaert, and S. Schwarz, 2007: Molecular mechanisms of decreased susceptibility to fluoroquinolones in avian Salmonella serovars and their mutants selected during determination of mutant prevention concentration. J. Antimicrob. Chemother. 59, 886-892.
17. Kehrenberg, C., A. Cloeckaert, G. Klein, and S. Schwarz, 2009: Decreased fluoroquinolone susceptibility in mutants of Salmonella serovars other than Typhimurium: detection of novel mutations involved in modulated expression of ramA and soxS. J. Antimicrob. Chemother. 64, 1175-1180.
18. Kohl, K. S., and T. A. Farley, 2000: Initially unrecognized distribution of a commercially cooked meat product contaminated over several months with Salmonella serotype Infantis. Epidemiol. Infect. 125, 491-498.
19. Koutsolioutsou, A., E. A. Martins, D. G. White, S. B. Levy, and B. Demple, 2001: A soxRS-constitutive mutation contributing to antibiotic resistance in a clinical isolate of S. enterica (Serovar Typhimurium). Antimicrob. Agents Chemother. 45, 38-43.
20. Najjar, Z., C. Furlong, N. Stephens, C. Shadbolt, P. Maywood, S. Conaty, and G. Hogg, 2012: An outbreak of Salmonella Infantis gastroenteritis in a residential age care facility associated with thickened fluids. Epidemiol. Infect. 140, 2264-2272.
21. Nógrády, N., Á. Tóth, Á. Kostyák, J. Pászti, and B. Nagy, 2007: Emergence of multidrug-resistant clones of Salmonella Infantis in broiler chickens and humans in Hungary. J. Antimicrob. Chemother. 60, 645-648.
22. Petrović, V., S. Stefanović, and P. Durić, 2005: Epidemiološke karakteristike salmoneloza u Vojvodini. Med. Preg. 58, 136-141 (serbian).
23. Sasaki, Y., A. Ikeda, K. Ishikawa, M. Murakami, M. Kusukawa, T. Asai, and Y. Yamada, 2012: Prevalence and antimicrobial susceptibility of Salmonella in Japanese broiler flocks. Epidemiol. Infect. 140, 2074-2081.
24. Shahada, F., T. Chuma, T. Tobata, K. Okamoto, M. Sueyoshi, and K. Takase, 2006: Molecular epidemiology of antimicrobial resistance among S. enterica serovar Infantis from poultry in Kagoshima Japan. Int. J. Antimicrob. Agents 28, 302-307.
25. Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. Persing, and B. Swaminathan, 1995: Interpreting chromosomal DNA restriction fragment patterns produced by pulse-field gel electrophoresis. Criteria for bacterial strain typing. J. Clin. Microbiol. 33, 2233-2239.
26. Veldman, K., L. M. Cavaco, D. Mevius, A. Battisti, A. Franco, N. Botteldoorn, M. Bruneau, A. Perrin-Guyomard, T. Cerny, C. De Frutos Escobar, B. Guerra, A. Schroeter, M. Gutierrez, K. Hopkins, A. L. Myllyniemi, M. Sunde, D. Wasyl, and F. M. Aarestrup, 2011: International collaborative study on the occurrence of plasmid-mediated quinolone resistance in S. enterica and Escherichia coli isolated from animals, humans, food and the environment. J. Antimicrob. Chemother. 66, 1278-1286.
27. Velhner, M., and D. Stojanović, 2012: Mutational Polymorphism in the bacterial topoisomerase genes driven by treatment with quinolones. In: Logie, C. (ed.), Point Mutation, pp. 185-210. InTech, Croatia.
28. Wang, M., Q. Guo, X. Xu, X. Wang, X. Ye, S. Wu, D. C. Hooper, and M. Wang, 2009: New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob. Agents Chemother. 53, 1892-1897.
29. Yamane, K., J. Wachino, S. Suzuki, and Y. Arakawa, 2007: Plasmid-mediated qepA gene among E. coli clinical isolates from Japan. Antimicrob. Agents Chemother. 52, 1564-1566.