Mechanisms of quinolone resistance and clonal relationship among strains isolated from reared fish with furunculosis Free

Abstract

The mechanisms of resistance to quinolone and epidemiological relationships among strains isolated from diseased fish in French marine farms from 1998 to 2000 were investigated. The quinolone resistance-determining regions of the and genes of 12 clinical isolates with different levels of quinolone susceptibility were sequenced. MICs were determined in the presence of the efflux pump inhibitor (EPI) Phe-Arg β-naphthylamide and values (MIC without EPI/MIC in the presence of EPI) were calculated. Isolates fell into two classes: (i) those that had a wild-type gene with oxolinic acid MIC ⩽ 0.5, flumequine MIC ⩽ 1 and ciprofloxacin MIC ⩽ 0.25 μg ml; and (ii) those that had a single mutation in encoding Asp-87 → Asn with oxolinic acid MIC ⩾ 2, flumequine MIC ⩾ 4 and ciprofloxacin MIC ⩾ 0.125 μg ml. No mutations were found in . High values obtained for flumequine and oxolinic acid (up to 16 and 8, respectively, for the most resistant isolates of the two classes) indicated an important contribution of efflux to the resistance phenotype. Flumequine accumulation experiments confirmed that high values were associated with a much lower level of accumulation. PCR/RFLP assays conducted on 34 additional isolates showed the presence of a mutation at codon 87 of in nearly all the quinolone-resistant isolates. This finding, together with PFGE typing results, strongly suggests a common clonal origin of these quinolone-resistant isolates.

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2004-09-01
2024-03-29
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References

  1. Akasaka T., Tanaka M., Yamaguchi A., Sato K. 2001; Type II topoisomerase mutations in fluoroquinolone-resistant clinical strains of Pseudomonas aeruginosa isolated in 1998 and 1999: role of target enzyme in mechanism of fluoroquinolone resistance. Antimicrob Agents Chemother 45:2263–2268 [CrossRef]
    [Google Scholar]
  2. Angulo F. 2000; Antimicrobial agents in aquaculture: potential impact on public health. APUA Newsl 18:1–5
    [Google Scholar]
  3. Bachoual R., Tankovic J., Soussy C. J. 1998; Analysis of the mutations involved in fluoroquinolone resistance of in vivo and in vitro mutants of Escherichia coli . Microb Drug Resist 4:271–276 [CrossRef]
    [Google Scholar]
  4. Bagel S., Hullen V., Wiedemann B., Heisig P. 1999; Impact of gyrA and parC mutations on quinolone resistance, doubling time, and supercoiling degree of Escherichia coli . Antimicrob Agents Chemother 43:868–875
    [Google Scholar]
  5. Blanc G., Donnay-Moreno C., Giraud E., Ganiere J. P. 2002 Antibiorésistance et efficacité thérapeutique des traitements antimicrobiens en pisciculture marine . Report of studies no. 99.16369 and no. 00.5071 pp 1–45 ENV Nantes (in French
    [Google Scholar]
  6. CEFAS 1999 Report of the Concerted Action Workshop on Development of Standard Reference Methods for Antimicrobial Agent Susceptibility Testing for Bacterial Fish Pathogens Weymouth, UK: Centre for Environment, Fisheries and Aquaculture Science;
    [Google Scholar]
  7. Chomarat M., Guérin-Faublée V., Kodjo A., Breysse F., Flandrois J. P. 1998; Molecular analysis of the fish pathogen Aeromonas salmonicida subsp. salmonicida by pulsed-field electrophoresis. Rev Med Vet 149:245–250
    [Google Scholar]
  8. Cloeckaert A., Chaslus-Dancla E. 2001; Mechanisms of quinolone resistance in Salmonella . Vet Res 32:291–300 [CrossRef]
    [Google Scholar]
  9. Deguchi T., Fukuoka A., Yasuda M. & 7 other authors; 1997; Alterations in the GyrA subunit of DNA gyrase and the ParC subunit of topoisomerase IV in quinolone-resistant clinical isolates of Klebsiella pneumoniae . Antimicrob Agents Chemother 41:699–701
    [Google Scholar]
  10. Ervik A., Thorsen B., Eriksen V., Lunestad B. T., Samuelsen O. B. 1994; Impact of administering antibacterial agents on wild fish and blue mussels Mytilus edulis in the vicinity of fish farms. Dis Aquat Org 18:45–51 [CrossRef]
    [Google Scholar]
  11. FAO 2002; Résidus d'antibiotiques dans les produits d'aquaculture. In La Situation Mondiale des Pêches et de l'Aquaculture . Rome: Food & Agriculture Organization of the United Nations (in French
  12. Garcia J. A., Larsen J. L., Dalsgaard I., Pedersen K. 2000; Pulsed-field gel electrophoresis analysis of Aeromonas salmonicida ssp. salmonicida . FEMS Microbiol Lett 190:163–166 [CrossRef]
    [Google Scholar]
  13. Gibreel A., Sjogren E., Kaijser B., Wretlind B., Skold O. 1998; Rapid emergence of high-level resistance to quinolones in Campylobacter jejuni associated with mutational changes in gyrA and parC . Antimicrob Agents Chemother 42:3276–3278
    [Google Scholar]
  14. Giraud E., Brisabois A., Martel J. L., Chaslus-Dancla E. 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
    [Google Scholar]
  15. Goni-Urriza M., Arpin C., Capdepuy M., Dubois V., Caumette P., Quentin C. 2002; Type II topoisomerase quinolone resistance-determining regions of Aeromonas caviae , A.hydrophila , and A. sobria complexes and mutations associated with quinolone resistance. Antimicrob Agents Chemother 46:350–359 [CrossRef]
    [Google Scholar]
  16. Grant A. N., Laidler L. A. 1993; Assessment of the antimicrobial sensitivity of Aeromonas salmonicida isolates from farmed Atlantic salmon in Scotland. Vet Rec 133:389–391 [CrossRef]
    [Google Scholar]
  17. Guardabassi L., Dalsgaard A., Raffatellu M., Olsen J. E. 2000; Increase in the prevalence of oxolinic acid resistant Acinetobacter spp.observed in a stream receiving the effluent from a freshwater trout farm following the treatment with oxolinic acid-medicated feed. Aquaculture 188:205–218 [CrossRef]
    [Google Scholar]
  18. Haliassos A., Chomel J. C., Tesson L., Baudis M., Kruh J., Kaplan J. C., Kitzis A. 1989; Modification of enzymatically amplified DNA for the detection of point mutations. Nucleic Acids Res 17:3606 [CrossRef]
    [Google Scholar]
  19. Hastings T. S., McKay A. 1987; Resistance of Aeromonas salmonicida to oxolinic acid. Aquaculture 61:165–171 [CrossRef]
    [Google Scholar]
  20. Hooper D. C. 2001; Mechanisms of action of antimicrobials: focus on fluoroquinolones. Clin Infect Dis 32 (Suppl. 1):S9–S15 [CrossRef]
    [Google Scholar]
  21. Inglis V., Richards R. H. 1991; The in vitro susceptibility of Aeromonas salmonicida and other fish-pathogenic bacteria to 29 antimicrobial agents. J Fish Dis 14:641–650 [CrossRef]
    [Google Scholar]
  22. Lehane L., Rawlin G. T. 2000; Topically acquired bacterial zoonoses from fish: a review. Med J Aust 173:256–259
    [Google Scholar]
  23. Lomovskaya O., Warren M. S., Lee A. & 13 other authors; 2001; Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa : novel agents for combination therapy. Antimicrob Agents Chemother 45:105–116 [CrossRef]
    [Google Scholar]
  24. Martinsen B., Horsberg T. E. 1995; Comparative single-dose pharmacokinetics of four quinolones, oxolinic acid, flumequine, sarafloxacin, and enrofloxacin, in Atlantic salmon ( Salmo salar ) held in seawater at 10 degrees C. Antimicrob Agents Chemother 39:1059–1064 [CrossRef]
    [Google Scholar]
  25. Nakano M., Deguchi T., Kawamura T., Yasuda M., Kimura M., Okano Y., Kawada Y. 1997; Mutations in the gyrA and parC genes in fluoroquinolone-resistant clinical isolates of Pseudomonas aeruginosa . Antimicrob Agents Chemother 41:2289–2291
    [Google Scholar]
  26. Noga E. J. 2000 Fish Disease: Diagnosis and Treatment Ames, IA: Iowa State University Press;
    [Google Scholar]
  27. Oppegaard H., Sorum H. 1994; gyrA mutations in quinolone-resistant isolates of the fish pathogen Aeromonas salmonicida . Antimicrob Agents Chemother 38:2460–2464 [CrossRef]
    [Google Scholar]
  28. Poole K. 2000; Efflux-mediated resistance to fluoroquinolones in gram-negative bacteria. Antimicrob Agents Chemother 44:2233–2241 [CrossRef]
    [Google Scholar]
  29. Pouliquen H., Pinault L. 1994; Determination of oxolinic acid in seawater, marine sediment and Japanese oyster by high performance liquid chromatography. J Liq Chromatogr 17:929–945 [CrossRef]
    [Google Scholar]
  30. Samuelsen O. B., Lunestad B. T., Husevag B., Holleland T., Ervik A. 1992; Residues of oxolinic acid in wild fauna following medication in fish farms. Dis Aquat Org 12:111–119 [CrossRef]
    [Google Scholar]
  31. Santos Y., Garcia-Marquez P. G., Pereira A., Riaza A., Silva R., Pazos F. 2003; Evaluation of vaccines and vaccination strategies to protect cultured turbot against furunculosis. In 11th International Conference of the European Association of Fish Pathologists , Maltap– 219 (abstract
    [Google Scholar]
  32. Schmidt A. S., Bruun M. S., Dalsgaard I., Pedersen K., Larsen J. L. 2000; Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four Danish rainbow trout farms. Appl Environ Microbiol 66:4908–4915 [CrossRef]
    [Google Scholar]
  33. Smith P., Hiney M. P., Samuelsen O. B. 1994; Bacterial resistance to antimicrobial agents used in fish farming: a critical evaluation of method and meaning. Annu Rev Fish Dis 4:273–313 [CrossRef]
    [Google Scholar]
  34. Spanggaard B., Jorgensen F., Gram L., Huss H. H. 1993; Antibiotic resistance in bacteria isolated from three freshwater fish farms and an unpolluted stream in Denmark. Aquaculture 115:195–207 [CrossRef]
    [Google Scholar]
  35. Tsoumas A., Alderman D. J., Rodgers C. J. 1989; Aeromonas salmonicida : development of resistance to 4-quinolone antimicrobials. J Fish Dis 12:493–507 [CrossRef]
    [Google Scholar]
  36. Twiddy D. R. 1995; Antibiotic-resistant human pathogens in integrated fish farms. ASEAN Food J 10:22–29
    [Google Scholar]
  37. Wood S. C., McCashion R. N., Lynch W. H. 1986; Multiple low-level antibiotic resistance in Aeromonas salmonicida . Antimicrob Agents Chemother 29:992–996 [CrossRef]
    [Google Scholar]
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