Contribution of the AcrAB-TolC efflux pump to high-level fluoroquinolone resistance in Escherichia coli isolated from dogs and humans

Journal of Veterinary Medical Science

Volumn 75, Issue 4, 2013, Pages 407-414

  Sato, Toyotaka ^a   Yokota, Shin Ichi ^b   Okubo, Torahiko ^a   Ishihara, Kanako ^a   Ueno, Hiroshi ^a   Muramatsu, Yasukazu ^a   Fujii, Nobuhiro ^b   Tamura, Yutaka ^a  

^a RAKUNO GAKUEN UNIVERSITY   (Japan)

^b SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

E. Coli; Efflux pump; Enrofloxacin; Fluoroquinolone resistance

Indexed keywords

ACRA PROTEIN, E COLI; ANTIINFECTIVE AGENT; BACTERIAL DNA; CARRIER PROTEIN; ENROFLOXACIN; ESCHERICHIA COLI PROTEIN; LIPOPROTEIN; QUINOLONE DERIVATIVE;

ANIMAL; ANIMAL DISEASE; ANTIBIOTIC RESISTANCE; ARTICLE; CHEMISTRY; DOG; DOG DISEASE; DRUG EFFECT; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; ANTI-INFECTIVE AGENTS; DNA, BACTERIAL; DOG DISEASES; DOGS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FLUOROQUINOLONES; HUMANS; LIPOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; POLYMERASE CHAIN REACTION;

CANIS FAMILIARIS; ESCHERICHIA COLI;

EID: 84877125769     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.12-0186     Document Type: Article

References (38)

1. Aarestrup, F. M. 1999. Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals. Int. J. Antimicrob. Agents 12: 279-285. [Medline] [CrossRef]
2. Breines, D. M., Ouabdesselam, S., Ng, E. Y., Tankovic, J., Shah, S., Soussy, C. J. and Hooper, D. C. 1997. Quinolone resistance locus nfxD of Escherichia coli is a mutant allele of the parE gene encoding a subunit of topoisomerase IV. Antimicrob. Agents Chemother. 41: 175-179. [Medline]
3. Cattoir, V., Poirel, L., Rotimi, V., Soussy, C. J. and Nordmann, P. 2007. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 60: 394-397. [Medline] [CrossRef]
4. Clinical and Laboratory Standards Institute. 2002. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved standard, 2nd ed. NCCLS document M31-A2. Clinical and Laboratory Standards Institute, Wayne.
5. Cohen, S. P., McMurry, L. M., Hooper, D. C., Wolfson, J. S. and Levy, S. B. 1989. Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob. Agents Chemother. 33: 1318-1325. [Medline] [CrossRef]
6. Cohen, S. P., McMurry, L. M. and Levy, S. B. 1988. marA locus causes decreased expression of OmpF porin in multiple-antibiotic-resistant (Mar) mutants of Escherichia coli. J. Bacteriol. 170: 5416-5422. [Medline]
7. Cohn, L. A., Gary, A. T., Fales, W. H. and Madsen, R. W. 2003. Trends in fluoroquinolone resistance of bacteria isolated from canine urinary tracts. J. Vet. Diagn. Invest. 15: 338-343. [Medline] [CrossRef]
8. Conrad, S., Oethinger, M., Kaifel, K., Klots, G., Marre, R. and Kern, W. V. 1996. gyrA mutations in high-level fluoroquinoloneresistant clinical isolates of Escherichia coli. J. Antimicrob. Chemother. 38: 443-455. [Medline] [CrossRef]
9. Eaves, D. J., Ricci, V. and Piddock, L. J. 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. [Medline] [CrossRef]
10. Everett, M. J., Jin, Y. F., Ricci, V. and Piddock, L. J. 1996. Contributions of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob. Agents Chemother. 40: 2380-2386. [Medline]
11. Heisig, P. 1996. Genetic evidence for a role of parC mutations in development of high-level fluoroquinolone resistance in Escherichia coli. Antimicrob. Agents Chemother. 40: 879-885. [Medline]
12. Jacoby, G. A. 2005. Mechanisms of resistance to quinolones. Clin. Infect. Dis. 41: S120-S126. [Medline] [CrossRef]
13. Jellen-Ritter, A. S. and Kern, W. V. 2001. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob. Agents Chemother. 45: 1467-1472. [Medline] [CrossRef]
14. Kern, W. V., Steinke, P., Schumacher, A., Schuster, S., Von, B. H. and Bohnert, J. A. 2006. Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Escherichia coli. J. Antimicrob. Chemother. 57: 339-343. [Medline] [CrossRef]
15. Kim, E. S., Jeong, J. Y., Jun, J. B., Choi, S. H., Lee, S. O., Kim, M. N., Woo, J. H. and Kim, Y. S. 2009. Prevalence of aac(6')-Ib-cr encoding a ciprofloxacin-modifying enzyme among Enterobacteriaceae blood isolates in Korea. Antimicrob. Agents Chemother. 53: 2643-2645. [Medline] [CrossRef]
16. Kim, H. B., Park, C. H., Kim, C. J., Kim, E. C., Jacoby, G. A. and Hooper, D. C. 2009. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob. Agents Chemother. 53: 639-645. [Medline] [CrossRef]
17. Kojima, A., Ishii, Y., Ishihara, K., Esaki, H., Asai, T., Oda, C., Tamura, Y., Takahashi, T. and Yamaguchi, K. 2005. Extendedspectrum-beta-lactamase-producing Escherichia coli strains isolated from farm animals from 1999 to 2002: report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. Antimicrob. Agents Chemother. 49: 3533-3537. [Medline] [CrossRef]
18. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. [Medline] [CrossRef]
19. Lavigne, J. P., Marchandin, H., Delamas, J., Bouziges, N., Lecaillon, E., Cavalie, L., Jean-Pierre, H., Bonnet, R. and Sotto, A. 2006. qnrA in CTX-M-producing Escherichia coli isolates from France. Antimicrob. Agents Chemother. 50: 4224-4228. [Medline] [CrossRef]
20. Martínez-Martínez, L., Pascual, A., Conejo Mdel, C., García, I., Joyanes, P., Doménech-Sánchez, A. and Benedí, V. J. 2002. Energy-dependent accumulation of norfloxacin and porin expression in clinical isolates of Klebsiella pneumoniae and relationship to extended-spectrum beta-lactamase production. Antimicrob. Agents Chemother. 46: 3926-3932. [Medline] [CrossRef]
21. Mortimer, P. G. and Piddock, L. J. 1993. The accumulation of five antimicrobial agents in porin-deficient mutations of Escherichia coli. J. Antimicrob. Chemother. 32: 195-213. [Medline] [CrossRef]
22. Park, C. H., Robicsek, A., Jacoby, G. A., Sahm, D. and Hooper, D. C. 2006. Prevalence in the United States of aac(6')-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob. Agents Chemother. 50: 3953-3955. [Medline] [CrossRef]
23. Pedersen, K., Pedersen, K., Jensen, H., Finster, K., Jensen, V. F. and Heuer, O. E. 2007. Occurrence of antimicrobial resistance in bacteria from diagnostic samples from dogs. J. Antimicrob. Chemother. 60: 775-781. [Medline] [CrossRef]
24. Peña, C., Albareda, J. M., Pallares, R., Pujol, M., Tubau, F. and Ariza, J. 1995. Relationship between quinolone use and appearance of ciprofloxacin-resistant Escherichia coli in bloodstream infections. Antimicrob. Agents Chemother. 39: 520-524. [Medline] [CrossRef]
25. Pérez-Pérez, F. J. and Hanson, N. D. 2002. Detection of plasmid mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol. 40: 2153-2162. [Medline] [CrossRef]
26. Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C., Jones, R., Nightingale, C., Preston, R. and Waddell, J. 2004. Dose the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J. Antimicrob. Chemother. 53: 28-52. [Medline] [CrossRef]
27. Platell, J. L., Cobbold, R. N., Johnson, J. R., Heisig, A., Heisig, P., Clabots, C., Kuskowski, M. A. and Trott, D. J. 2011. Commonality among fluoroquinolone-resistant sequence type ST131 extraintestinal Escherichia coli isolates from humans and companion animals in Australia. Antimicrob. Agents Chemother. 55: 3782-3787. [Medline] [CrossRef]
28. Poole, K. 2005. Efflux-mediated antimicrobial resistance. J. Antimicrob. Chemother. 56: 20-51. [Medline] [CrossRef]
29. Robicsek, A., Strahilevitzl, J., Jacoby, G. A., Macielag, M., Abbanat, D., Park, C. H., Bush, K. and Hooper, D. C. 2006. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat. Med. 12: 83-88. [Medline] [CrossRef]
30. Ruppé, E., Hem, S., Lath, S., Gautier, V., Ariey, F., Sarthou, J. L., Monchy, D. and Arlet, G. 2009. CTX-M beta-lactamases in Escherichia coli from community-acquired urinary tract infections, Cambodia. Emerg. Infect. Dis. 15: 741-748. [Medline] [CrossRef]
31. Sáenz, Y., Ruiz, J., Zarazaga, M., Teixidó, M., Torres, C. and Vila, J. 2004. Effect of the efflux pump inhibitor Phe-Arg-betanaphthylamide on the MIC values of the quinolones, tetracycline and chloramphenicol, in Escherichia coli isolates of different origin. J. Antimicrob. Chemother. 53: 544-545. [Medline] [CrossRef]
32. Sorlozano, A., Gutierrez, J., Jimenez, A., de Dios Luna, J. and Martinez, J. L. 2007. Contribution of a new mutation in parE to quinolone resistance in extended-spectrum-beta-lactamaseproducing Escherichia coli isolates. J. Clin. Microbiol. 45: 2740-2742. [Medline] [CrossRef]
33. Tamura, Y. 2003. Trends in antimicrobial agents for veterinary use and control measures of antimicrobial resistance. J. Jpn. Vet. Med. 56: 685-691.
34. Usui, M., Uchiyama, M., Iwanaka, M., Nagai, H., Yamamoto, Y. and Asai, T. 2009. Intracellular concentrations of enrofloxacin in quinolone-resistant Salmonella enterica subspecies enterica serovar Choleraesuis. Int. J. Antimicrob. Agents 34: 592-595. [Medline] [CrossRef]
35. Yamane, K., Wachino, J., Suzuki, S., Kimura, K., Shibata, N., Kato, H., Shibayama, K., Konda, T. and Arakawa, Y. 2007. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob. Agents Chemother. 51: 3354-3360. [Medline] [CrossRef]
36. Yang, H., Chen, S., White, D. G., Zhao, S., McDermott, P., Walker, R. and Meng, J. 2004. Characterization of multipleantimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. J. Clin. Microbiol. 42: 3483-3489. [Medline] [CrossRef]
37. Yoshida, H., Bogaki, M., Nakamura, M., Yamanaka, L. M. and Nakamura, S. 1991. Quinolone resistance-determining region in the DNA gyrase gyrB gene of Escherichia coli. Antimicrob. Agents Chemother. 35: 1647-1650. [Medline] [CrossRef]
38. Xu, L., Ensor, V., Gossain, S., Nye, K. and Hawkey, P. 2005. Rapid and simple detection of blaCTX-M genes by multiplex PCR assay. J. Med. Microbiol. 54: 1183-1187. [Medline] [CrossRef]