Quinolone resistance of Salmonella enterica serovar virchow isolates from humans and poultry in Israel: Evidence for clonal expansion

Journal of Clinical Microbiology

Volumn 45, Issue 8, 2007, Pages 2575-2579

  Solnik Isaac, Hadas ^a   Weinberger, Miriam ^b,c   Tabak, Mina ^a   Ben David, Alon ^a   Shachar, Dina ^a   Yaron, Sima ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b ASSAF HAROFEH MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ASPARTIC ACID; CEFTRIAXONE; CHLORAMPHENICOL; CIPROFLOXACIN; COLISTIN; COTRIMOXAZOLE; GENTAMICIN; NALIDIXIC ACID; NEOMYCIN; POLYMYXIN B; QUINOLINE DERIVED ANTIINFECTIVE AGENT; STREPTOMYCIN; TETRACYCLINE; TYROSINE;

ACRAB GENE; AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL OVERGROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATE; BLOOD; CLONAL EXPANSION; CONTROLLED STUDY; EFFLUX PUMP GENE; FECES; FOOD CHAIN; GENE MUTATION; GYRA GENE; HUMAN; ISRAEL; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; POULTRY; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SALMONELLA ENTERICA; SALMONELLA VIRCHOW; SEROTYPE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; CLUSTER ANALYSIS; DNA FINGERPRINTING; DNA GYRASE; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; GENOTYPE; HUMANS; ISRAEL; MOLECULAR EPIDEMIOLOGY; POINT MUTATION; POULTRY; QUINOLONES; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL;

ANIMALIA; SALMONELLA; SALMONELLA ENTERICA;

EID: 34548071428     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.00062-07     Document Type: Article

References (45)

1. Asako, H., H. Nakajima, K. Kobayashi, M. Kobayashi, and R. Aono. 1997. Organic solvent tolerance and antibiotic resistance increased by overexpression of marA in Escherichia coli. Appl. Environ. Microbiol. 63:1428-1433.
2. Baucheron, S., H. Imberechts, E. Chaslus-Dancla, and A. Cloeckaert. 2002. The AcrB multidrug transporter plays a major role in high-level fluoroquinolone resistance in Salmonella enterica serovar Typhimurium phage type DT204. Microb. Drug Resist. 8:281-289.
3. Ben-Barak, Z., W. Streckel, S. Yaron, S. Cohen, R. Prager, and H. Tschape. 2006. The expression of the virulence-associated effector protein gene avrA is dependent on a Salmonella enterica-specific regulatory function. Int. J. Med. Microbiol. 296:25-38.
4. Bennett, C. M., C. Dalton, M. Beers-Deeble, A. Milazzo, E. Kraa, D. Davos, M. Puech, A. Tan, and M. W. Heuzenroeder. 2003. Fresh garlic: a possible vehicle for Salmonella Virchow. Epidemiol. Infect. 131:1041-1048.
5. Bertrand, S., F. X. Weill, A. Cloeckaert, M. Vrints, E. Mairiaux, K. Fraud, K. Dierick, C. Wildemauve, C. Godard, P. Butaye, H. Imberechts, P. A. Grimont, and J. M. Collard. 2006. Clonal emergence of extended-spectrum beta-lactamase (CTX-M-2)-producing Salmonella enterica serovar Virchow isolates with reduced susceptibilities to ciprofloxacin among poultry and humans in Belgium and France (2000 to 2003). J. Clin. Microbiol. 44:2897-2903.
6. Casin, I., J. Breuil, J. P. Darchis, C. Guelpa, and E. Collatz. 2003. Fluoroquinolone resistance linked to GyrA, GyrB, and ParC mutations in Salmonella enterica typhimurium isolates in humans. Emerg. Infect. Dis. 9:1455-1457.
7. Chiu, C. H., T. L. Wu, L. H. Su, C. Chu, J. H. Chia, A. J. Kuo, M. S. Chien, and T. Y. Lin. 2002. The emergence in Taiwan of fluoroquinolone resistance in Salmonella enterica serotype Choleraesuis. N. Engl. J. Med. 346:413-419.
8. Chiu, C. H., T. L. Wu, L. H. Su, J. W. Liu, and C. Chu. 2004. Fluoroquinolone resistance in Salmonella enterica serotype Choleraesuis, Taiwan, 2000-2003. Emerg. Infect. Dis. 10:1674-1676.
9. Choi, S. H., J. H. Woo, J. E. Lee, S. J. Park, E. J. Choo, Y. G. Kwak, M. N. Kim, M. S. Choi, N. Y. Lee, B. K. Lee, N. J. Kim, J. Y. Jeong, J. Ryu, and Y. S. Kim. 2005. Increasing incidence of quinolone resistance in human non-typhoid Salmonella enterica isolates in Korea and mechanisms involved in quinolone resistance. J. Antimicrob. Chemother. 56:1111-1114.
10. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A7. Clinical and Laboratory Standards Institute, Wayne, PA.
11. Crump, J. A., T. J. Barrett, J. T. Nelson, and F. J. Angulo. 2003. Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi salmonellae. Clin. Infect. Dis. 37:75-81.
12. Eaves, D. J., E. Liebana, M. J. Woodward, and L. J. Piddock. 2002. Detection of gyrA mutations in quinolone-resistant Salmonella enterica by denaturing high-performance liquid chromatography. J. Clin. Microbiol. 40:4121-4125.
13. Eaves, D. J., V. Ricci, and L. J. Piddock. 2004. Expression of acrB, acrF, acrD, marA, and soxS in Salmonella enterica serovar Typhimurium: role in multiple antibiotic resistance. Antimicrob. Agents Chemother. 48:1145-1150.
14. Escribano, I., J. C. Rodriguez, L. Cebrian, and G. Royo. 2004. The importance of active efflux systems in the quinolone resistance of clinical isolates of Salmonella spp. Int. J. Antimicrob. Agents 24:428-432.
15. Gay, K., A. Robicsek, J. Strahilevitz, C. H. Park, G. Jacoby, T. J. Barrett, F. Medalla, T. M. Chiller, and D. C. Hooper. 2006. Plasmid-mediated quinolone resistance in non-Typhi serotypes of Salmonella enterica. Clin. Infect. Dis. 43:297-304.
16. George, A. M., and S. B. Levy. 1983. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J. Bacteriol. 155:531-540.
17. Giraud, E., S. Baucheron, and A. Cloeckaert. 2006. Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies. Microbes Infect. 8:1937-1944.
18. Helms, M., J. Simonsen, and K. Molbak. 2004. Quinolone resistance is associated with increased risk of invasive illness or death during infection with Salmonella serotype Typhimurium. J. Infect. Dis. 190:1652-1654.
19. Helms, M., P. Vastrup, P. Gerner-Smidt, and K. Molbak. 2002. Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium. Emerg. Infect. Dis. 8:490-495.
20. Hirose, K., A. Hashimoto, K. Tamura, Y. Kawamura, T. Ezaki, H. Sagara, and H. Watanabe. 2002. DNA sequence analysis of DNA gyrase and DNA topoisomerase IV quinolone resistance-determining regions of Salmonella enterica serovar Typhi and serovar Paratyphi A. Antimicrob. Agents Chemother. 46:3249-3252.
21. Hopkins, K. L., C. Arnold, and E. J. Threlfall. 2007. Rapid detection of gyrA and parC mutations in quinolone-resistant Salmonella enterica using pyrose-quencing technology. J. Microbiol. Methods 68:163-171.
22. 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.
23. Kadhiravan, T., N. Wig, A. Kapil, S. K. Kabra, K. Renuka, and A. Misra. 2005. Clinical outcomes in typhoid fever: adverse impact of infection with nalidixic acid-resistant Salmonella typhi. BMC Infect. Dis. 5:37.
24. 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.
25. Levy, S. B. 2002. Active efflux, a common mechanism for biocide and antibiotic resistance. J. Appl. Microbiol. 92(Suppl.):65S-71S.
26. Liebana, E., C. Clouting, C. A. Cassar, L. P. Randall, R. A. Walker, E. J. Threlfall, F. A. Clifton-Hadley, A. M. Ridley, and R. H. Davies. 2002. Comparison of gyrA mutations, cyclohexane resistance, and the presence of class I integrons in Salmonella enterica from farm animals in England and Wales. J. Clin. Microbiol. 40:1481-1486.
27. Ling, J. M., E. W. Chan, A. W. Lam, and A. F. Cheng. 2003. Mutations in topoisomerase genes of ftuoroquinolone-resistant salmonellae in Hong Kong. Antimicrob. Agents Chemother. 47:3567-3573.
28. Martin, R. G., and J. L. Rosner. 2004. Transcriptional and translational regulation of the marRAB multiple antibiotic resistance operon in Escherichia coli. Mol. Microbiol. 53:183-191.
29. Mates, A., V. Agmon, R. Yishai, N. Andorn, and A. Reisfeld. 2002. Salmonella 1997-2000. A report of the National Salmonella Center. State of Israel Ministry of Health, Jerusalem, Israel.
30. Molbak, K. 2005. Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clin. Infect. Dis. 41:1613-1620.
31. National Committee for Clinical Laboratory Standards. 2000. Performance standards for antimicrobial disk susceptibility tests for bacteria that grow aerobically. Approved standard M2-A7. National Committee for Clinical Laboratory Standards, Wayne, PA.
32. Paulsen, I. T. 2003. Multidrug efflux pumps and resistance: regulation and evolution. Curr. Opin. Microbiol. 6:446-451.
33. Randall, L. P., S. W. Cooles, L. J. Piddock, and M. J. Woodward. 2004. Effect of triclosan or a phenolic farm disinfectant on the selection of antibiotic-resistant Salmonella enterica. J. Antimicrob. Chemother. 54:621-627.
34. Randall, L. P., S. W. Cooles, A. R. Sayers, and M. J. Woodward. 2001. Association between cyclohexane resistance in Salmonella of different serovars and increased resistance to multiple antibiotics, disinfectants and dyes. J. Med. Microbiol. 50:919-924.
35. Randall, L. P., and M. J. Woodward. 2002. The multiple antibiotic resistance (mar) locus and its significance. Res. Vet. Sci. 72:87-93.
36. Renuka, K., S. Sood, B. K. Das, and A. Kapil. 2005. High-level ciprofloxacin resistance in Salmonella enterica serotype Typhi in India. J. Med. Microbiol. 54:999-1000.
37. Robicsek, A., G. A. Jacoby, and D. C. Hooper. 2006. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis. 6:629-640.
38. Rupali, P., O. C. Abraham, M. V. Jesudason, T. J. John, A. Zachariah, S. Sivaram, and D. Mathai. 2004. Treatment failure in typhoid fever with ciprofloxacin susceptible Salmonella enterica serotype Typhi. Diagn. Microbiol. Infect. Dis. 49:1-3.
39. Slinger, R., M. Desjardins, A. E. McCarthy, K. Ramotar, P. Jessamine, C. Guibord, and B. Toye. 2004. Suboptimal clinical response to ciprofloxacin in patients with enteric fever due to Salmonella spp. with reduced fluoroquinolone susceptibility: a case series. BMC Infect. Dis. 4:36.
40. Threlfall, E. J., I. S. Fisher, C. Berghold, P. Gerner-Smidt, H. Tschape, M. Cormican, I. Luzzi, F. Schnieder, W. Wannet, J. Machado, and G. Edwards. 2003. Antimicrobial drug resistance in isolates of Salmonella enterica from cases of salmonellosis in humans in Europe in 2000: results of international multi-centre surveillance. Eur. Surveill. 8:41-45.
41. Tibbetts, R. J., T. L. Lin, and C. C. Wu. 2003. Phenotypic evidence for inducible multiple antimicrobial resistance in Salmonella choleraesuis. FEMS Microbiol. Lett. 218:333-338.
42. Walker, R. A., N. Saunders, A. J. Lawson, E. A. Lindsay, M. Dassama, L. R. Ward, M. J. Woodward, R. H. Davies, E. Liebana, and E. J. Threlfall. 2001. Use of a LightCycler gyrA mutation assay for rapid identification of mutations conferring decreased susceptibility to ciprofloxacin in multiresistant Salmonella enterica serotype Typhimurium DT104 isolates. J. Clin. Microbiol. 39:1443-1448.
43. Weinberger, M., and N. Keller. 2005. Recent trends in the epidemiology of non-typhoid Salmonella and antimicrobial resistance: the Israeli experience and worldwide review. Curr. Opin. Infect. Dis. 18:513-521.
44. Weinberger, M., H. Solnik-Isaac, D. Shachar, A. Reisfeld, L. Valinsky, N. Andorn, V. Agmon, R. Yishai, R. Bassal, A. Fraser, S. Yaron, and D. Cohen. 2006. Salmonella enterica serotype Virchow: epidemiology, resistance patterns and molecular characterisation of an invasive Salmonella serotype in Israel. Clin. Microbiol. Infect. 12:999-1005.
45. White, D. G., K. Maneewannakul, E. von Hofe, M. Zillman, W. Eisenberg, A. K. Field, and S. B. Levy. 1997. Inhibition of the multiple antibiotic resistance (mar) operon in Escherichia coli by antisense DNA analogs. Antimicrob. Agents Chemother. 41:2699-2704.