Biofilms: An extra hurdle for effective antimicrobial therapy

Current Pharmaceutical Design

Volumn 16, Issue 20, 2010, Pages 2279-2295

  Cos, P ^a   Tote K ^a   Horemans, T ^a   Maes, L ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Antibiotic; Biocide; In vitro; Laboratory model; Quorum sensing; Resistance; Review

Indexed keywords

ANTIBIOTIC AGENT; BIOCIDE;

BACTERIAL CELL; BACTERIUM ADHERENCE; BIOFILM; EXTRACELLULAR MATRIX; MOLECULAR DOCKING; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY;

ANTI-INFECTIVE AGENTS; BACTERIA; BIOFILMS; DRUG RESISTANCE; HUMANS; MICROBIAL INTERACTIONS; MICROBIAL SENSITIVITY TESTS;

EID: 77955613075     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161210791792868     Document Type: Review

References (177)

1. Szymanska J. Biofilm and dental unit waterlines. Ann Agric Environ Med 2003; 10: 151-7.
2. Carpentier B and Cerf O. Biofilms and their consequences, with particular reference to hygiene in the food industry. J Appl Bacteriol 1993; 75: 499-511.
3. Donlan RM and Costerton JW. Biofilms: survival mechanisms of clinically relevant micro-organisms. Clin Microbiol Rev 2002; 15: 167-93.
4. Costerton JW, Geesey GG and Cheng GK. How bacteria stick. Sci Am 1978; 238: 86-95.
5. Hall-Stoodley L, Costerton JW and Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2: 95-108.
6. Marshall KC. Interfaces in microbial ecology. Cambridge: Harvard University Press 1976.
7. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin- Scott HM. Microbial biofilms. Annu Rev Microbiol 1995; 49: 711-45.
8. Lindsay D and von Holy A. Bacterial biofilms within the clinical setting: what healthcare professionals should know. J Hosp Infect 2006; 64: 313-25.
9. Dunne WM jr. Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 2002; 15: 155-66.
10. O'Toole G, Kaplan HB and Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000; 54: 49-79.
11. Gilbert P, McBain AJ and Rickard AH. Formation of microbial biofilm in hygienic situations: a problem of control. Int Biodeter Biodegr 2003; 51: 245-8.
12. Beloin C and Ghigo JM. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 2005; 13: 16-19.
13. Costerton JW, Lewandowski Z, Debeer D, Caldwell D, Korber D and James G. Biofilms, the customized microniche. J Bacteriol 1994; 176: 2137-42.
14. Allison DG. The biofilm matrix. Biofouling 2003; 19: 139-50.
15. Miqueleto AP, Dolosic CC, Pozzi E, Foresti E and Zaiat M. Influence of carbon sources and C/N ratio on EPS production in anaerobic sequencing batch biofilm reactors for wastewater treatment. Bioresour Technol 2010; 101: 1324-30.
16. Bryers JD. Medical biofilms. Biotechnol Bioeng 2008; 100: 1-18.
17. Monds RD and O'Toole GA. The developmental model of microbial biofilms: ten years of a paradigm up for a review. Trends Microbiol 2009; 17: 73-87.
18. Margolis JJ, El-Etr S, Joubert LM, et al. Contributions of Francisella tularensis subsp. novicida chitinases and Sec secretion system to biofilm formation on chitin. Appl Environ Microb 2010; 76: 596-608.
19. Vuong C and Otto M. Staphylococcus epidermidis infections. Microbes Infect 2002; 4: 481-9.
20. Whitchurch CB, Tolker-Nielsen T, Ragas PC and Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 2002; 295: 1487.
21. Zhang HJ, Tsang TK, Jack CA and Pollack J. Role of bile mucin in bacterial adherence to biliary stents. J Lab Clin Med 2002; 139: 28- 34.
22. Francois P, Schrenzel J, Stoerman-Chopard C, et al. Identification of plasma proteins adsorbed on hemodialysis tubing that promote Staphylococcus aureus adhesion. J Lab Clin Med 2000; 135: 32-42.
23. Dexter SJ, Pearson RG, Davies MC, Camara M and Shakesheff KM. A comparison of the adhesion of mammalian cells and Staphylococcus epidermidis on fibronectin-modified polymer surfaces. J Biomed Mater Res 2001; 56: 222-7.
24. Aparna MS and Yadav S. Biofilms: microbes and disease. Braz J Infect Dis 2008; 12: 526-30.
25. O'Toole GA and Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998; 30: 295-304.
26. Giltner CL, van Schaik EJ, Audette GF, et al. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol Microbiol 2006; 59: 1083-96.
27. Craig L, Pique ME and Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004; 2: 363-78.
28. Van Dellen KL and Watnick PI. The vibrio cholerae biofilm: a target for novel therapies to prevent and treat cholera. Drug Discov Today Dis Mech 2006; 3: 261-6.
29. Deziel E, Comeau Y and Villemur R. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 2001; 183: 1195-204.
30. Darzins AL and Russell MA. Molecular genetic analysis of type-4 pilus biogenesis and twitching motility using Pseudomonas aeruginosa as a model system - a review. Gene 1997; 192: 109-15.
31. von Bodman SB, Willey JM and Diggle SP. Cell-cell communication in bacteria: united we stand. J Bacteriol 2008; 190: 4377-91.
32. Diggle SP, Crusz SA and Camara M. Quorum sensing. Curr Biol 2007; 17: R907-10.
33. Fuqua C and Greenberg EP. Listening in on bacteria: acylhomoserine lactone signalling. Nat Rev Mol Cell Biol 2002; 3: 685-95.
34. Skindersoe ME, Alhede M, Phipps R, et al. Effect of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2008; 52: 3648-63.
35. Cvitkovitch DG, Li Y and Ellen RP. Quorum sensing and biofilm formation in Streptococcal infections. J Clin Invest 2003; 112: 1626-32.
36. Cvitkovitch DG. Genetic competence and transformation in oral streptococci. Crit Rev Oral Biol Med 2001; 12: 217-43.
37. Li YH, Tang N, Aspiras MB, et al. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 2002; 184: 2699-708.
38. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW and Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998; 280: 295-8.
39. Kleerebezem M, Quadri LEN, Kuipers OP and de Vos WM. Quorum sensing by peptide pheromones and two-component signal transduction systems in Gram-positive bacteria. Mol Microbiol 1997; 24: 895-904.
40. Ng WL and Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet 2009; 43: 197-222.
41. Chavez de Paz LE, Hamilton IR and Svensäter G. Oral bacteria in biofilms exhibit slow reactivation from nutrient deprivation. Microbiology 2008; 154: 1927-38.
42. Chavez de Paz L. Redefining the persistent infection in root canals: possible role of biofilm communities. J Endod 2007; 33: 652-62.
43. Kolenbrander PE, Palmer RJ Jr., Rickard AH, Jakubovics NS, Chalmers NI and Diaz PI. Bacterial interactions and successions during plaque development. Periodontol 2000 2006; 42: 47-79.
44. Zijnge V, van Leeuwen MBM, Degener JE, et al. Oral biofilm architecture on natural teeth. PLoS One 2010; 5: e9321.
45. Hall-Stoodley L and Stoodley P. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 2005; 13: 7-10.
46. Karatan E and Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 2009; 73: 310-47.
47. Purevdorj-Gage B, Costerton JW, Stoodley P. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiol SGM 2005; 151: 1569-76.
48. Frank JF and Koffi RA. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to sanitizers and heat. J Food Protect 1990; 53: 550-4.
49. Anderson GG and O'Toole GA. Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 2008; 322: 85-105.
50. Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 2002; 292: 107-13.
51. Cloete TE. Resistance mechanisms of bacteria to antimicrobial compounds. Int Biodeter Biodegr 2003; 51: 277-82.
52. Chambless JD, Hunt SM and Stewart PS. A three-dimensional computer model of four hypothetical mechanisms protecting biofilms from antimicrobials. Appl Environ Microbiol 2006; 72: 2005-13.
53. Ryder C, Byrd M and Wozniak DJ. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 2007; 10: 644-8.
54. Shigeta M, Tanaka G, Komatsuzawa H, Sugai M, Suginaka H and Usui T. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 1997; 43: 340-5.
55. Hatch RA and Schiller NL. Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob Agents Chemother 1998; 42: 974-7.
56. Brown ML, Aldrich HC and Gauthier JJ. Relationship between glycocalyx and povidone-iodine resistance in Pseudomonas aeruginosa (ATCC-27853) biofilms. Appl Environ Microb 1995; 61: 187-93.
57. Dibdin GH, Assinder SJ, Nichols WW and Lambert PA. Mathematical model of β-lactam penetration into a biofilm of Pseudomonas aeruginosa while undergoing simultaneous inactivation by released β-lactamases. J Antimicrob Chemother 1996; 38: 757-69.
58. Xu KD, Stewart PS, Xia F, Huang CT and McFeters GA. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 1998; 64: 4035-9.
59. Schembri MA, Kjaergaard K and Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol 2003; 48: 253-67.
60. Beloin C, Valle J, Latour-Lambert P, et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 2004; 51: 659-74.
61. Beenken KE, Dunman PM, McAleese F, et al. Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 2004; 186: 4665-84.
62. Ito A, May T, Taniuchi A, Kawata K and Okabe S. Localized expression profiles of rpoS in Escherichia coli biofilms. Biotechnol Bioeng 2009; 103: 975-83.
63. Stanley NR, Britton RA, Grossman AD and Lazazzera BA. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 2003; 185: 1951-7.
64. Jayaraman R. Bacterial persistence: some new insights into an old phenomenon. J Biosci 2008; 33: 795-805.
65. Spoering AL and Lewis K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 2001; 183: 6746-51.
66. Gilbert P, Allison DG and McBain AJ. Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? J Appl Microbiol Symp Suppl 2002; 92: 98S-110S.
67. Chapman JS. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegr 2003; 51: 271-76.
68. Goeres DM, Loetterle LR, Hamilton MA, Murga R, Kirby DW and Donlan RM. Statistical assessment of a laboratory method for growing biofilms. Microbiology 2005; 151: 757-62.
69. Donlan RM, Piede JA, Heyes CD, et al. Model system for growing and quantifying Streptococcus pneumoniae biofilms in situ and in real time. Appl Environ Microbiol 2004; 70: 4980-8.
70. Curtin J, Cormican M, Fleming G, Keelehan J and Colleran E. Linezolid compared with eperezolid, vancomycin and gentamycin in an in vitro model of antimicrobial lock therapy for Staphylococcus epidermidis central venous catheter-related biofilm infections. Antimicrob Agents Chemother 2003; 47: 3145-8.
71. Honraet K and Nelis HJ. Use of the modified robbins device and fluorescent staining to screen plant extracts for the inhibition of S. mutans biofilm formation. J Microbiol Methods 2006; 64: 217-24.
72. An YH and Friedman RJ. Laboratory methods for studies of bacterial adhesion. J Microbiol Methods 1997; 30: 141-52.
73. Moskowitz SM, Foster JM, Emerson J and Burns JL. Clinically feasible biofilm susceptibility assay for isolates of Pseudomonas aeruginosa from patients with cystic fibrosis. J Clin Microbiol 2004; 42: 1915-22.
74. Meyer B. Approaches to prevention, removal and killing of biofilms. Int Biodeter Biodegr 2003; 51: 249-53.
75. Liaqat I and Sabri AN. Effect of biocides on biofilm bacteria from dental unit water lines. Curr Microbiol 2008; 56: 619-24.
76. Toté K, Vanden Berghe D, Maes L and Cos P. A new colorimetric microtitre model for the detection of Staphylococcus aureus biofilms. Lett Appl Microbiol 2008; 46: 249-54.
77. Luppens SB, Reij MW, van der Heijden RW, Rombouts FM and Abee T. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl Environ Microbiol 2002; 68: 4194-4200.
78. Anonymous. Chemical disinfectants and antiseptics - basic bactericidal activity - test method and requirements (phase 1). European Standard EN 1040. Belgisch Instituut voor Normalisatie (BIN), Brussels, Belgium 1997.
79. Toté K, Horemans T, Vanden Berghe D, Maes L and Cos P. Inhibitory effect of biocides on viable mass and matrix of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2010; 76: 3135-42.
80. Kirketerp-Moller K, Jensen PO, Fazli M, et al. Distribution, organization and ecology of bacteria in chronic wounds. J Clin Microbiol 2008; 46: 2717-22.
81. Hoiby N, Bjarnsholt T, Givskov M, Molin S and Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010; 35: 322-32.
82. Kobayashi N, Bauer TW, Tuohy MJ, Fujishiro T and Procop GW. Brief ultrasonication improves detection of biofilm-formative bacteria around a metal implant. Clin Orthop Relat Res 2007; 475: 210-3.
83. Pettit RK, Weber CA, Kean MJ, et al. Microplate alamar blue assay for Staphylococcus epidermidis biofilm susceptiblity testing. Antimicrob Agents Chemother 2005; 49: 2612-17.
84. Peeters E, Nelis HJ and Coenye T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 2008; 72: 157-65.
85. O'Brien J, Wilson I, Orton T and Pognan F. Investigation of the alamar blue (resazurin) fluorescent dye for the assessment of mammalian cell toxicity. Eur J Biochem 2000; 267: 5421-26.
86. Schwartz T, Jungfer C, Heiβler S, Friedrich F, Faubel W and Obst U. Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks. Chemosphere 2009; 77: 249-57.
87. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for the quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175-9.
88. Denkhaus E, Meisen S, Telgheder U and Wingender J. Chemical and physical methods for characterisation of biofilms. Microchim Acta 2007; 158: 1-27.
89. Sandberg M, Määtänen A, Peltonen J, Vuorela PM and Fallarero A. Automating a 96-well microtitre plate model for Staphylococcus aureus biofilms: an approach to screening of natural antimicrobial compounds. Int J Antimicrob Agents 2008; 32: 233-40.
90. Macfarlane S and Dillon JF. Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 2007; 102: 1187-96.
91. Jones SE and Versalovic J. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 2009; 9: 35.
92. Saunders S, Bocking A, Challis J and Reid G. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Colloids Surf B Biointerfaces 2007; 55: 138-42.
93. Penner R, Fedorak RN and Madsen KL. Probiotics and nutraceuticals: non-medicinal treatments of gastrointestinal diseases. Curr Opin Pharmacol 2005; 5: 596-603.
94. Reid G. The importance of guidelines in the development and application of probiotics. Curr Pharm Design 2005; 11: 11-6.
95. Gibson GR and Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995; 125: 1401-12.
96. Macfarlane S and Macfarlane GT. Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 2006; 72: 6204-11.
97. Langlands SJ, Hopkins MJ, Coleman N and Cummings JH. Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 2004; 53: 1610-6.
98. Del Pozo JL, Rouse MS, Mandrekar JN, Sampedro MF, Steckelberg JM and Patel R. Effect of electrical current on the activities of antimicrobial agents against Pseudomonas aeruginosa, Staphylococcus aureus and Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 2008; 53: 35-40.
99. Stewart PS and Costerton WJ. Antibiotic resistance of bacteria in biofilms. Lancet 2001; 358: 135-8.
100. Fux CA, Costerton JW, Stewart PS and Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol 2005; 13: 34-40.
101. O'Gara JP. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 2007; 270: 179-88.
102. Costerton JW, Montanaro L and Arciola CR. Biofilm in implant infections: its production and regulation. Int J Artif Organs 2005; 28: 1062-8.
103. Rohde H, Burandt EC, Siemssen N, et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 2007; 28: 1711-20.
104. Russell AD. Antibiotic and biocide resistance in bacteria: Introduction. J Appl Microbiol Symp Suppl 2002; 92: 1-3.
105. Ha US and Cho YH. Catheter-associated urinary tract infections: new aspects of novel urinary catheters. In J Antimicrob Agents 2006; 28: 485-90.
106. Parker DL, Callan L, Harwood J, Thompson DL, Wilde M and Gray M. Nursing interventions to reduce the risk of catheterassociated urinary tract infection. Part 1: catheter selection. J Wound Ostomy Continence Nurs 2009; 36: 23-34.
107. Johnson JR, Kuskowski MA and Wilt TJ. Systematic review: antimicrobial urinary catheters to prevent catheter-associated urinary tract infection in hospitalized patients. Ann Intern Med 2006; 144: 116-26.
108. Orme R, Douglas CWI, Rimmer S and Webb M. Proteomic analysis of Escherichia coli biofilms reveals the overexpression of the outer membrane protein OmpA. Proteomics 2006; 6: 4269-77.
109. Stickler DJ. Susceptibility of antibiotic-resistant Gram-negative bacteria to biocides: a perspective from the study of catheter biofilms. J Appl Microbiol Symp Suppl 2002; 92: 163S-70S.
110. Danese PN. Antibiofilm approaches: prevention of catheter colonization. Chem Biol 2002; 9: 873-80.
111. Tambyah PA. Catheter-associated urinary tract infections: diagnosis and prophylaxis. In J Antimicrob Agents 2004; 24: S44-8.
112. Casey AL, Mermel LA, Nightingale P and Elliott TS. Antimicrobial central venous catheters in adults: a systematic review and meta-analysis. Lancet Infect Dis 2008; 8: 763-6.
113. Leon C, Ruiz-Santana S, Rello J, et al. Benefits of minocycline and rifampin-impregnated central venous catheters. A prospective, randomized, double-blind, controlled, multicenter trial. Intensive Care Med 2004; 30: 1891-9.
114. Sampath LA, Tambe SM and Modak SM. In vitro and in vivo efficacy of catheters impregnated with antiseptics or antibiotics: evaluation of the risk of bacterial resistance to the antimicrobials in the catheters. Infect Control Hosp Epidemiol 2001; 22: 640-6.
115. Chatzinikolaou I, Hanna H, Graviss L, et al. Clinical experience with minocycline and rifampin-impregnated central venous catheters in bone marrow transplantation recipients: efficacy and low risk of developing staphylococcal resistance. Infect Control Hosp Epidemiol 2003; 24: 961-5.
116. Tambe SM, Sampath L and Modak SM. In vitro evaluation of the risk of developing bacterial resistance to antiseptics and antibiotics used in medical devices. J Antimicrob Chemother 2001; 47: 589- 98.
117. Wright F, Heyland DK, Drover JW, McDonald S and Zoutman D. Antibiotic-coated central lines: do they work in the critical care setting? Clin Intensive Care 2001; 12: 21-8.
118. Giacometti A, Cirioni O, Ghiselli R, et al. Distinctin improves the efficacies of glycopeptides and betalactams against staphylococcal biofilm in an experimental model of central venous catheter infection. J Biomed Mater Res A 2007; 81: 233-9.
119. Raad I, Fang X, Keutgen XM, Jiang Y, Sherertz R and Hachem R. The role of chelators in preventing biofilm formation and catheterrelated bloodstream infections. Curr Opin Infect Dis 2008; 21: 385- 92.
120. Grau S, Gil MJ, Mateu-de Antonio J, Pera M and Marin-Casino M. Antibiotic-lock technique using daptomycin for subcutaneous injection ports in a patient on home parenteral nutrition. J Infect 2009; 59: 298-9.
121. Giacometti A, Cirioni O, Ghiselli R, et al. Comparative efficacies of quinupristin-dalfopristin, linezolid, vancomycin and ciprofloxacin in treatment, using the antibiotic-lock technique, of experimental catheter-related infection due to Staphylococcus aureus. Antimicrob Agents Chemother 2005; 49: 4042-5.
122. Keays T, Ferris W, Vandemheen KL, et al. A retrospective analysis of biofilm antibiotic susceptibility testing: A better predictor of clinical response in cystic fibrosis exacerbations. J Cyst Fibros 2009; 8: 122-7.
123. Peeters E, Nelis HJ and Coenye T. In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocycline, tobramycin and trimethoprim/ sulfamethoxazole against planktonic and sessile Burkholderia cepacia complex bacteria. J Antimicrob Chemother 2009; 64: 801- 9.
124. Toté K, Vanden Berghe D, Deschacht M, de Wit K, Maes L and Cos P. Inhibitory efficacy of various antibiotics on matrix and viable mass of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Int J Antimicrob Agents 2009; 33: 525-31.
125. Bagge N, Schuster M, Hentzer M, Ciofu O, Givskov M and Greenberg EP. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob Agents Chemother 2004; 48: 1175-87.
126. Whiteley M, Bangera MG, Bumgarner RE, et al. Gene expression in Pseudomonas aeruginosa biofilms. Nature 2001; 413: 860-4.
127. Frank KL, Reichert EJ, Piper KE and Patel R. In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrob Agents Chemother 2007; 51: 888-95.
128. Rachid S, Ohlsen K, Witte W, Hacker J and Ziebuhr W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesion expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 2000; 44: 3357-63.
129. Smith K, Gould KA, Ramage G, Gemmell CG, Hinds J and Lang S. Influence of tigecycline on expression of virulence factors in biofilm-associated cells of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2010; 54: 380-7.
130. Smith K, Perez A, Ramage G, Gemmell CG and Lang S. Comparison of biofilm-associated cell survival following in vitro exposure of methicillin-resistant Staphylococcus aureus biofilms to the antibiotics clindamycin, daptomycin, linezolid, tigecycline and vancomycin. Int J Antimicrob Agents 2009; 33: 374-8.
131. Rupp ME, Lisco SJ, Lipsett PA, et al. Effect of a secondgeneration venous catheter impregnated with chlorhexidine and silver sulfadiazine on central catheter - related infections. Ann Intern Med 2005; 143: 570-80.
132. Borschel DM, Chenoweth CE, Kaufman SR, et al. Are antisepticcoated central venous catheters effective in a real-world setting? Am J Infect Control 2006; 34: 388-93.
133. Alonso A, Sanchez P and Martinez JL. Environmental selection of antibiotic resistance genes. Environ Microbiol 2001; 3: 1-9.
134. Aizawa SI, Harwood CS and Kadner RJ. Signaling components in bacterial locomotion and sensory reception. J Bacteriol 2000; 182: 1459-71.
135. Russell AD. Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Inf Dis 2003; 3: 794-803.
136. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR and Schweizer HP. 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 2001; 45: 428-32.
137. Mariscal A, Carnero-Varo M, Gutierrez-Bedmar M, Garcia- Rodriguez A and Fernandez-Crehuet J. A fluorescent method for assessing the antimicrobial efficacy of disinfectant against Escherichia coli ATCC 35218 biofilm. Appl Microbiol Biotechnol 2007; 77: 233-40.
138. Tashikawa M, Yamanaka K and Nakamuro K. Studies on the disinfection and removal of biofilms by ozone-water using an artificial microbial biofilm system. Ozone Sci Eng 2009; 31: 3-9.
139. Harrison JJ, Ceri H, Stremick CA and Turner RJ. Biofilm susceptibility to metal toxicity. Environ Microbiol 2004; 6: 1220-7.
140. Walker JT, Bradshaw DJ, Fulford MR and Marsh PD. Microbiological evaluation of a range of disinfectant products to control mixed-species biofilm contamination in a laboratory model of a dental unit water system. Appl Environ Microbiol 2003; 69: 3327-32.
141. Kim J, Pitts B, Stewart PS, Camper A and Yoon J. Comparison of the antimicrobial effect of chlorine, silver ion and tobramycin on biofilm. Antimicrob Agents Chemother 2008; 52: 1446-53.
142. Surdeau N, Laurent-Maquin D, Bouthors S and Gellé MP. Sensitivity of bacterial biofilms and planktonic cells to a new antimicrobial agent, Oxsil® 320N. J Hosp Infect 2006; 62: 487-93.
143. Stewart PS. New ways to stop biofilm infections. Lancet 2003; 361: 97.
144. Rasko DA and Sperandio V. Anti-virulence strategies to combat bacterial-mediated disease. Nat Rev Drug Discov 2010; 9: 117-28.
145. Kadry AA, Fouda SI, Shibl AM and Abu El-Asrar AA. Impact of slime dispersants and anti-adhesives on in vitro biofilm formation of Staphylococcus epidermidis on intraocular lenses and on antibiotic activities. J Antimicrob Chemother 2009; 63: 480-4.
146. Raad I, Chatzinikolaou I, Chaiban G, et al. In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob Agents Chemother 2003; 47: 3580-5.
147. Bleyer AJ, Mason L, Russell G, Raad II and Sherertz RJ. A randomized, controlled trial of a new vascular catheter flush solution (minocycline-EDTA) in temporary hemodialysis access. Infect Control Hosp Epidemiol 2005; 26: 520-4.
148. Raad I, Hanna H, Dvorak T, Chaiban G and Hachem R. Optimal antimicrobial catheter lock solution, using different combinations of minocycline, EDTA, and 25-percent ethanol, rapidly eradicates organisms embedded in biofilm. Antimicrob Agents Chemother 2007; 51: 73-83.
149. Peeters E, Nelis HJ and Coenye T. Resistance of planktonic and biofilm-grown Burkholderia cepacia complex isolates to the transition metal gallium. J Antimicrob Chemother 2008; 61: 1062-5.
150. Banin E, Vasil ML and Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 2005; 102: 11076-81.
151. Liamas MA, Sparrius M, Kloet R, Jimenez CR, Vandenbroucke-Grauls C and Bitter W. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 2006; 188: 1882-91.
152. Banin E, Lozinski A, Brady KM, et al. The potential of desferrioxamine- gallium as an anti-Pseudomonas therapeutic agent. Proc Natl Acad Sci USA 2008; 105: 16761-6.
153. Ramsey DM and Wozniak DJ. Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol Microbiol 2005; 56: 309-22.
154. Hertle R, Mrsny R, Fitzgerald DJ. Dual-function vaccine for Pseudomonas aeruginosa: characterization of chimeric exotoxin A-pilin protein. Infect Immun 2001; 69: 6962-9.
155. Kumagai Y, Yagishita H, Yajima A, Okamoto T and Konishi K. Molecular mechanism for connective tissue destruction by dipeptidyl aminopeptidase IV produced by the periodontal pathogen Porphyromonas gingivalis. Infect Immun 2005; 73: 2655-64.
156. Sauer FG, Remaut H, Hultgren SJ and Waksman G. Fiber assembly by the chaperone-usher pathway. Biochim Biophys Acta 2004; 1694: 259-67.
157. Aberg V, Das P, Chorell E, et al. Carboxylic acid isosteres improve the activity of ring-fused 2-pyridones that inhibit pilus biogenesis in E. coli. Bioorg Med Chem Lett 2008; 18: 3536-40.
158. Pinkner JS, Remaut H, Buelens F, et al. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci USA 2006; 103: 17897-902.
159. Denstedt JD and Cadieux PA. Eliminating biofilm from ureteral stents: the holy grail. Curr Opin Urol 2009; 19: 205-10.
160. Lange D, Elwood CN, Choi K, Hendlin K, Monga M and Chew BH. Uropathogen interaction with the surface of urological stents using different surface properties. J Urol 2009; 182: 1194-1200.
161. Azeredo J and Sutherland IW. The use of phages for the removal of infectious biofilms. Curr Pharm Bioetechnol 2008; 9: 261-66.
162. Ishida T, Ikeda T, Takiguchi N, Kuroda A, Ohtake H and Kato J. Inhibition of quorum sensing in Pseudomonas aeruginosa by Nacyl cyclopentylamides. Appl Environ Microbiol 2007; 73: 3183-8.
163. Wu H, Song Z, Hentzer M, et al. Synthetic furanones inhibit quorum- sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 2004; 53: 1054-61.
164. Lönn-Stensrud J, Landin MA, Benneche T, Petersen FC and Scheie AA. Furanones, potential agents for preventing Staphylococcus epidermidis biofilm infections? J Antimicrob Chemother 2009; 63: 309-16.
165. Müh U, Schuster M, Heim R, Singh A, Olson ER and Greenberg EP. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 2006; 50: 3674-9.
166. Adonizio A, Kong KF and Mathee K. Inhibition of quorum sensing -controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 2008; 52: 198-203.
167. Cos P, Vlietinck AJ, Vanden Berghe D and Maes L. Anti-infective potential of natural products: how to develop a stronger in vitro 'proof-of-concept'. J Ethnopharmacol 2006; 106: 290-302.
168. Hoiby N, Johansen HK, Moser C, Song Z, Ciofu O and Kharazmi A. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 2001; 3: 23-35.
169. Kim J, Hahn JS, Franklin MJ, Stewart PS and Yoon J. Tolerance of dormant and active cells in Pseudomonas aeruginosa PA01 biofilm to antimicrobial agents. J Antimicrob Chemother 2009; 63: 129-35.
170. Tré-Hardy M, Vanderbist F, Traore H and Devleeschouwer MJ. In vitro activity of antibiotic combinations against Pseudomonas aeruginosa biofilm and planktonic cultures. Int J Antimicrob Agents 2008; 31: 329-36.
171. Lee MY, Ko KS, Song JH and Peck KR. In vitro effectiveness of the antibiotic lock technique (ALT) for the treatment of catheterrelated infections by Pseudomonas aeruginosa and Klebsiella pneumoniae. J Antimicrob Chemother 2007; 60: 782-7.
172. Raad I, Hanna H, Jiang Y, et al. Comparative activities of daptomycin, linezolid and tigecycline against catheter-related methicillin- resistant Staphylococcus bacteremic isolates embedded in biofilm. Antimicrob Agents Chemother 2007; 51: 1656-60.
173. Abdi-Ali A, Mohammadi-Mehr M and Alaei YA. Bactericidal activity of various antibiotics against biofilm-producing Pseudomonas aeruginosa. Int J Antimicrob Agents 2006; 27: 196-200.
174. Edmiston CE Jr, Goheen MP, Seabrook GR, Johnson CP, Lewis BD, Brown KR et al. Impact of selective antimicrobial agents on staphylococcal adherence to biomedical devices. Am J Surg 2006; 192: 344-54.
175. Saginur R, St. Denis M, Ferris W, et al. Multiple combination bactericidal testing of staphylococcal biofilms from implantassociated infections. Antimicrob Agents Chemother 2006; 50: 55- 61.
176. Mikuniya T, Kato Y, Kariyama R, Monden K, Hikida M and Kuman H. Synergistic effect of fosfomycin and fluoroquinolones against Pseudomonas aeruginosa growing in a biofilm. Acta Med Okayama 2005; 59: 209-16.
177. Amorena B, Gracia E, Monzon M, et al. Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J Antimicrob Chemother 1999; 44: 43-55.