Effect of subinhibitory concentrations of benzalkonium chloride on the competitiveness of Pseudomonas aeruginosa grown in continuous culture

Microbiology

Volumn 156, Issue 1, 2010, Pages 30-38

  Mc Cay, Paul H ^a   Ocampo Sosa, Alain A ^a   Fleming, Gerald T A ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AZTREONAM; BACTERIAL PROTEIN; BENZALKONIUM CHLORIDE; BIOCIDE; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; GENTAMICIN; GLUCOSE; IMIPENEM; MAGNESIUM; MEXAB PROTEIN; MEXB PROTEIN; MEXCD PROTEIN; MEXD PROTEIN; MEXF PROTEIN; MEXR PROTEIN; MEXY PROTEIN; MINOCYCLINE; NFXB PROTEIN; OPRJ PROTEIN; OPRM PROTEIN; POLYMYXIN B; PROTEIN PARC; TOBRAMYCIN; UNCLASSIFIED DRUG; VANCOMYCIN;

ADAPTATION; AMINO ACID SUBSTITUTION; ANTIBIOTIC SENSITIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTINUOUS CULTURE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; INTERSPECIFIC COMPETITION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; STRAIN DIFFERENCE;

ANTI-INFECTIVE AGENTS, LOCAL; BENZALKONIUM COMPOUNDS; CULTURE MEDIA; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL SENSITIVITY TESTS; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 76849110640     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.029751-0     Document Type: Article

References (47)

1. Akimitsu, N., Hamamoto, H., Inoue, R. I., Shoji, M., Takemori, K., Hamasaki, N. & Sekimizu, K. (1999). Increase in resistance of methicillin-resistant Staphylococcus aureus to β-lactams caused by mutations conferring resistance to benzalkonium chloride, a dis-infectant widely used in hospitals. Antimicrob Agents Chemother 43, 3042-3043.
2. Anderson, R. L., Carr, J. H., Bond, W. W. & Favero, M. S. (1997). Susceptibility of vancomycin-resistant enterococci to environmental disinfectants. Infect Control Hosp Epidemiol 18, 195-199.
3. Chuanchuen, R., Beinlich, K., Hoang, T. T., Becher, A., Karkhoff-Schweizer, R. R. & Schweizer, H. P. (2001). Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 45, 428-432.
4. Chuanchuen, R., Karkhoff-Schweizer, R. R. & Schweizer, H. P. (2003). High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am J Infect Control 31, 124-127.
5. Cole, E. C., Addison, R. M., Rubino, J. R., Leese, K. E., Dulaney, P. D., Newell, M. S., Wilkins, J., Gaber, D. J., Wineinger, T. & Criger, D. A. (2003). Investigation of antibiotic and antibacterial agent cross-resistance in target bacteria from homes of antibacterial product users and nonusers. J Appl Microbiol 95, 664-676.
6. Dean, C. R., Visalli, M. A., Projan, S. J., Sum, P. E. & Bradford, P. A. (2003). Efflux-mediated resistance to tigecycline (GAR-936) in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 47, 972-978.
7. Dykhuizen, D. E. (1993). Chemostats used for studying natural selection and adaptive evolution. Methods Enzymol 224, 613-631.
8. Fernandez-Astorga, A., Hijarrubia, M. J., Hernandez, M., Arana, I. & Sunen, E. (1995). Disinfectant tolerance and antibiotic resistance in psychrotrophic Gram-negative bacteria isolated from vegetables. Lett Appl Microbiol 20, 308-311.
9. Fleming, G. & Patching, J. W. (2008). The fermenter in research and development. In Practical Fermentation Technology, pp. 347-377. Edited by B. Mc Neil & L. M. Harvey. Chichester: Wiley.
10. Fleming, G. T., McCarthy, D. M., Colombet, N. & Patching, J. W. (2002). The effect of levofloxacin concentration on the development and maintenance of antibiotic-resistant clones of Escherichia coli in chemostat culture. J Ind Microbiol Biotechnol 29, 155-162.
11. Fraise, A. P. (2002). Biocide abuse and antimicrobial resistance - a cause for concern? J Antimicrob Chemother 49, 11-12.
12. Gilbert, P. & McBain, A. J. (2003). Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev 16, 189-208.
13. Goldberg, I. & Er-el, Z. (1981). The chemostat - an efficient technique for medium optimization. Process Biochem 16, 2-4.
14. Higgins, P. G., Fluit, A. C., Milatovic, D., Verhoef, J. & Schmitz, F. J. (2003). Mutations in GyrA, ParC, MexR and NfxB in clinical isolates of Pseudomonas aeruginosa. Int J Antimicrob Agents 21, 409-413.
15. Irizarry, L., Merlin, T., Rupp, J. & Griffith, J. (1996). Reduced susceptibility of methicillin-resistant Staphylococcus aureus to cetylpyridinium chloride and chlorhexidine. Chemotherapy 42, 248-252.
16. Jalal, S. & Wretlind, B. (1998). Mechanisms of quinolone resistance in clinical strains of Pseudomonas aeruginosa. Microb Drug Resist 4, 257-261.
17. Jones, M. V., Herd, T. M. & Christie, H. J. (1989). Resistance of Pseudomonas aeruginosa to amphoteric and quaternary ammonium biocides. Microbios 58, 49-61.
18. Karatzas, K. A. G., Webber, M. A., Jorgensen, F., Woodward, M. J., Piddock, L. J. V. & Humphrey, T. J. (2007). Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness. J Antimicrob Chemother 60, 947-955.
19. Langsrud, S., Sundheim, G. & Borgmann-Strahsen, R. (2003). Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. J Appl Microbiol 95, 874-882.
20. Lee, J. K., Lee, Y. S., Park, Y. K. & Kim, B. S. (2005). Alterations in the GyrA and GyrB subunits of topoisomerase II and the ParC and ParE subunits of topoisomerase IV in ciprofloxacin-resistant clinical isolates of Pseudomonas aeruginosa. Int J Antimicrob Agents 25, 290-295.
21. -ΔΔCt method. Methods 25, 402-408.
22. Lomovskaya, O. & Bostian, K. A. (2006). Practical applications and feasibility of efflux pump inhibitors in the clinic - a vision for applied use. Biochem Pharmacol 71, 910-918.
23. Lomovskaya, O., Lee, A., Hoshino, K., Ishida, H., Mistry, A., Warren, M. S., Boyer, E., Chamberland, S. & Lee, V. J. (1999). Use of a genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 43, 1340-1346.
24. Loughlin, M. F., Jones, M. V. & Lambert, P. A. (2002). Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother 49, 631-639.
25. Maniatis, T. (1982). Appendix A. Biochemical techniques: liquid media. In Molecular Cloning: a Laboratory Manual, p. 440. Edited by T. Maniatis, E. F. Fritsch & J. Sambrook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
26. Manzoor, S. E., Lambert, P. A., Griffiths, P. A., Gill, M. J. & Fraise, A. P. (1999). Reduced glutaraldehyde susceptibility in Mycobacterium chelonae associated with altered cell wall polysaccharides. J Antimicrob Chemother 43, 759-765.
27. McBain, A. J. & Gilbert, P. (2001). Biocide tolerance and the harbingers of doom. Int Biodeterior Biodegradation 47, 55-61.
28. McMahon, M. A. S., Blair, I. S., Moore, J. E. & McDowell, D. A. (2007). Habituation to sub-lethal concentrations of tea tree oil ( Melaleuca alternifolia) is associated with reduced susceptibility to antibiotics in human pathogens. J Antimicrob Chemother 59, 125-127.
29. Méchin, L., Dubois-Brissonnet, F., Heyd, B. & Leveau, J. Y. (1999). Adaptation of Pseudomonas aeruginosa ATCC 15442 to didecyldimethylammonium bromide induces changes in membrane fatty acid composition and in resistance of cells. J Appl Microbiol 86, 859-866.
30. Moken, M. C., McMurry, L. M. & Levy, S. B. (1997). Selection of multiple-antibiotic-resistant (mar) mutants of Escherichia coli by using the disinfectant pine oil: roles of the mar and acrAB loci. Antimicrob Agents Chemother 41, 2770-2772.
31. NCCLS (2003). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard M7-A6. Wayne, PA: National Committee for Clinical Laboratory Standards.
32. Noguchi, N., Hase, M., Kitta, M., Sasatsu, M., Deguchi, K. & Kono, M. (1999). Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 172, 247-253.
33. O'Reilly, A. & Smith, P. (1999). Development of methods for predicting the minimum concentrations of oxytetracycline capable of exerting a selection for resistance to this agent. Aquaculture 180, 1-11.
34. Piddock, L. J. V. (2006). Multidrug-resistance efflux pumps are not just for resistance. Nat Rev Microbiol 4, 629-636.
35. Poole, K. (2005). Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56, 20-51.
36. Price, C. T. D., Singh, V. K., Jayaswal, R. K., Wilkinson, B. J. & Gustafson, J. E. (2002). Pine oil cleaner-resistant Staphylococcus aureus: reduced susceptibility to vancomycin and oxacillin and involvement of SigB. Appl Environ Microbiol 68, 5417-5421.
37. Russell, A. D. (1999). Bacterial resistance to disinfectants: present knowledge and future problems. J Hosp Infect 43 (Supplement), S57-S68.
38. Russell, A. D. (2002). Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. Symp Ser Soc Appl Microbiol 31, 121S-135S.
39. Russell, A. D., Tattawasart, U., Maillard, J. Y. & Furr, J. R. (1998). Possible link between bacterial resistance and use of antibiotics and biocides. Antimicrob Agents Chemother 42, 2151.
40. Rutala, W. A., Stiegel, M. M., Sarubbi, F. A. & Weber, D. J. (1997). Susceptibility of antibiotic-susceptible and antibiotic-resistant hospital bacteria to disinfectants. Infect Control Hosp Epidemiol 18, 417-421.
41. Savli, H., Karadenizli, A., Kolayli, F., Gundes, S., Ozbek, U. & Vahaboglu, H. (2003). Expression stability of six housekeeping genes: a proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52, 403-408.
42. Schwartz, L. S., Jansen, N. B., Ho, N. W. Y. & Tsao, G. T. (1988). Plasmid instability kinetics of the yeast S288C pUCKm8 [Cir(+)] in non-selective and selective media. Biotechnol Bioeng 32, 733-740.
43. Stecchini, M. L., Manzano, M. & Sarais, I. (1992). Antibiotic and disinfectant susceptibility in Enterobacteriaceae isolated from minced meat. Int J Food Microbiol 16, 79-85.
44. Suller, M. T. E. & Russell, A. D. (2000). Triclosan and antibiotic resistance in Staphylococcus aureus. J Antimicrob Chemother 46, 11-18.
45. Tabata, A., Nagamune, H., Maeda, T., Murakami, K., Miyake, Y. & Kourai, H. (2003). Correlation between resistance of Pseudomonas aeruginosa to quaternary ammonium compounds and expression of outer membrane protein OprR. Antimicrob Agents Chemother 47, 2093-2099.
46. Thorrold, C. A., Letsoalo, M. E., Duse, A. G. & Marais, E. (2007). Efflux pump activity in fluoroquinolone and tetracycline resistant Salmonella and Escherichia coli implicated in reduced susceptibility to household antimicrobial cleaning agents. Int J Food Microbiol 113, 315-320.
47. To, M. S., Favrin, S., Romanova, N. & Griffiths, M. W. (2002). Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol 68, 5258-5264.