Efficacy of the combination of tobramycin and a macrolide in an in vitro Pseudomonas aeruginosa mature biofilm model

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 10, 2010, Pages 4409-4415

  Tré Hardy, Marie ^a   Nagant, Carole ^a   El Manssouri, Naïma ^a   Vanderbist, Francis ^b   Traore, Hamidou ^b   Vaneechoutte, Mario ^c   Dehaye, Jean Paul ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Laboratoires SMB SA   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; CLARITHROMYCIN; TOBRAMYCIN;

AEROSOL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIUM CULTURE; BACTERIUM ISOLATE; BIOFILM; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG EFFICACY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SIMULATION;

ANTI-BACTERIAL AGENTS; BIOFILMS; DRUG SYNERGISM; MACROLIDES; PSEUDOMONAS AERUGINOSA; TOBRAMYCIN;

EID: 77957358644     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00372-10     Document Type: Article

References (40)

1. Anwar, H., M. K. Dasgupta, and J. W. Costerton. 1990. Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrob. Agents Chemother. 34:2043-2046.
2. Borriello, G., L. Richards, G. D. Ehrlich, and P. S. Stewart. 2006. Arginine or nitrate enhances antibiotic susceptibility of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 50:382-384.
3. Boucher, R. C. 2004. New concepts of the pathogenesis of cystic fibrosis lung disease. Eur. Respir. J. 23:146-158.
4. Bush, A., and B. K. Rubin. 2003. Macrolides as biological response modifiers in cystic fibrosis and bronchiectasis. Semin. Respir. Crit. Care Med. 24:737-748.
5. Chambless, J. D., S. M. Hunt, and P. S. Stewart. 2006. A three-dimensional computer model of four hypothetical mechanisms protecting biofilms from antimicrobials. Appl. Environ. Microbiol. 72:2005-2013.
6. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549.
7. Clinical and Laboratory Standards Institute. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 6th ed. Approved standard M7-A6. CLSI, Wayne, PA.
8. Conte, J. E., Jr., J. A. Golden, S. Duncan, E. McKenna, and E. Zurlinden. 1995. Intrapulmonary pharmacokinetics of clarithromycin and of erythromycin. Antimicrob. Agents Chemother. 39:334-338.
9. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
10. Drenkard, E., and F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740-743.
11. Equi, A., I. M. Balfour-Lynn, A. Bush, and M. Rosenthal. 2002. Long term azithromycin in children with cystic fibrosis: a randomised, placebo-controlled crossover trial. Lancet 360:978-984. (Pubitemid 35284109)
12. Fajardo, A., N. Martinez-Martin, M. Mercadillo, J. C. Galan, B. Ghysels, S. Matthijs, P. Cornelis, L. Wiehlmann, B. Tummler, F. Baquero, and J. L. Martinez. 2008. The neglected intrinsic resistome of bacterial pathogens. PLoS One 3:e1619.
13. Frederiksen, B., C. Koch, and N. Hoiby. 1997. Antibiotic treatment of initial colonization with Pseudomonas aeruginosa postpones chronic infection and prevents deterioration of pulmonary function in cystic fibrosis. Pediatr. Pulmonol. 23:330-335.
14. Frederiksen, B., S. Lanng, C. Koch, and N. Hoiby. 1996. Improved survival in the Danish center-treated cystic fibrosis patients: results of aggressive treatment. Pediatr. Pulmonol. 21:153-158.
15. George, A. M., P. M. Jones, and P. G. Middleton. 2009. Cystic fibrosis infections: treatment strategies and prospects. FEMS Microbiol. Lett. 300:153-164.
16. Gillis, R. J., K. G. White, K. H. Choi, V. E. Wagner, H. P. Schweizer, and B. H. Iglewski. 2005. Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 49:3858-3867.
17. Hickey, A. J., D. Lu, E. D. Ashley, and J. Stout. 2006. Inhaled azithromycin therapy. J. Aerosol Med. 19:54-60.
18. Hill, D., B. Rose, A. Pajkos, M. Robinson, P. Bye, S. Bell, M. Elkins, B. Thompson, C. Macleod, S. D. Aaron, and C. Harbour. 2005. Antibiotic susceptibilities of Pseudomonas aeruginosa isolates derived from patients with cystic fibrosis under aerobic, anaerobic, and biofilm conditions. J. Clin. Microbiol. 43:5085-5090.
19. Hoffman, L. R., D. A. D'Argenio, M. J. MacCoss, Z. Zhang, R. A. Jones, and S. I. Miller. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171-1175.
20. Ichimiya, T., K. Takeoka, K. Hiramatsu, K. Hirai, T. Yamasaki, and M. Nasu. 1996. The influence of azithromycin on the biofilm formation of Pseudomonas aeruginosa in vitro. Chemotherapy 42:186-191.
21. Kesser, K. C., and D. E. Geller. 2009. New aerosol delivery devices for cystic fibrosis. Respir. Care 54:754-767; discussion, 767-768.
22. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
23. Mah, T. F., B. Pitts, B. Pellock, G. C. Walker, P. S. Stewart, and G. A. O'Toole. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306-310.
24. Mor, N., and L. Heifets. 1993. MICs and MBCs of clarithromycin against Mycobacterium avium within human macrophages. Antimicrob. Agents Chemother. 37:111-114.
25. Mulet, X., M. D. Macia, A. Mena, C. Juan, J. L. Perez, and A. Oliver. 2009. Azithromycin in Pseudomonas aeruginosa biofilms: bactericidal activity and selection of nfxB mutants. Antimicrob. Agents Chemother. 53:1552-1560.
26. Ramsey, B. W., M. S. Pepe, J. M. Quan, K. L. Otto, A. B. Montgomery, J. Williams-Warren, K. M. Vasiljev, D. Borowitz, C. M. Bowman, B. C. Marshall, S. Marshall, and A. L. Smith. 1999. Intermittent administration of inhaled tobramycin in patients with cystic fibrosis. Cystic Fibrosis Inhaled Tobramycin Study Group. N. Engl. J. Med. 340:23-30.
27. Riordan, J. R., J. M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, J. L. Chou, et al. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073. (Pubitemid 19231814)
28. Rodvold, K. A. 1999. Clinical pharmacokinetics of clarithromycin. Clin. Pharmacokinet. 37:385-398.
29. Schurek, K. N., A. K. Marr, P. K. Taylor, I. Wiegand, L. Semenec, B. K. Khaira, and R. E. Hancock. 2008. Novel genetic determinants of low-level aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:4213-4219.
30. Singh, P. K., A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762-764.
31. Skindersoe, M. E., M. Alhede, R. Phipps, L. Yang, P. O. Jensen, T. B. Rasmussen, T. Bjarnsholt, T. Tolker-Nielsen, N. Hoiby, and M. Givskov. 2008. Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:3648-3663.
32. Southern, K. W., and P. M. Barker. 2004. Azithromycin for cystic fibrosis. Eur. Respir. J. 24:834-838.
33. Staab, D. 2004. Cystic fibrosis - therapeutic challenge in cystic fibrosis children. Eur. J. Endocrinol. 151(Suppl. 1):S77-S80.
34. Tateda, K., Y. Ishii, S. Kimura, M. Horikawa, S. Miyairi, and K. Yamaguchi. 2007. Suppression of Pseudomonas aeruginosa quorum-sensing systems by macrolides: a promising strategy or an oriental mystery? J. Infect. Chemother. 13:357-367.
35. Treerat, P., F. Widmer, P. G. Middleton, J. Iredell, and A. M. George. 2008. In vitro interactions of tobramycin with various nonantibiotics against Pseudomonas aeruginosa and Burkholderia cenocepacia. FEMS Microbiol. Lett. 285:40-50.
36. Tre-Hardy, M., C. Mace, N. El Manssouri, F. Vanderbist, H. Traore, and M. J. Devleeschouwer. 2009. Effect of antibiotic co-administration on young and mature biofilms of cystic fibrosis clinical isolates: the importance of the biofilm model. Int. J. Antimicrob. Agents 33:40-45.
37. Tre-Hardy, M., H. Traore, N. El Manssouri, F. Vanderbist, M. Vaneechoutte, and M. J. Devleeschouwer. 2009. Evaluation of long-term co-administration of tobramycin and clarithromycin in a mature biofilm model of cystic fibrosis clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 34:370-374.
38. Tre-Hardy, M., F. Vanderbist, H. Traore, and M. J. Devleeschouwer. 2008. In vitro activity of antibiotic combinations against Pseudomonas aeruginosa biofilm and planktonic cultures. Int. J. Antimicrob. Agents 31:329-336.
39. Worlitzsch, D., R. Tarran, M. Ulrich, U. Schwab, A. Cekici, K. C. Meyer, P. Birrer, G. Bellon, J. Berger, T. Weiss, K. Botzenhart, J. R. Yankaskas, S. Randell, R. C. Boucher, and G. Doring. 2002. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109:317-325.
40. Zhang, L., and T. F. Mah. 2008. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 190:4447-4452.