Bacterial biofilms: A diagnostic and therapeutic challenge

Expert Review of Anti-Infective Therapy

Volumn 1, Issue 4, 2003, Pages 667-683

  Fux, Christoph A ^a   Stoodley, Paul ^b   Hall Stoodley, Luanne ^a   Costerton, J William ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b Idaho National Laboratory   (United States)

Author keywords

Antibiotic resistance; Biofilm; Gene expression; Human disease; Metabolic activity; Protein expression; Quorum sensing; Shear forces

Indexed keywords

ALGINIC ACID; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; CLARITHROMYCIN; FURANONE DERIVATIVE; GLUCOSE; IMIPENEM; LYASE; MACROLIDE; POLITEF; POLYPEPTIDE ANTIBIOTIC AGENT; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN;

BACTERIAL GROWTH; BACTERIAL INFECTION; BIOFILM; DEVICE; EXTRACELLULAR MATRIX; GROWTH REGULATION; HUMAN; IMMUNITY; NONHUMAN; PLANKTON; PREVALENCE; REVIEW; RISK FACTOR; TREATMENT FAILURE;

EID: 3042781113     PISSN: 14787210     EISSN: None     Source Type: Journal    
DOI: 10.1586/14787210.1.4.667     Document Type: Review

References (152)

1. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322(1999).
2. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298 (1998).
3. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181, 5993-6002 (1999).
4. Xu KD, McFeters GA, Stewart PS. Biofilm resistance to antimicrobial agents. Microbiology 146, 547-549 (2000).
5. Tunney MM, Patrick S, Curran MD et al. Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene. J. Clin. Microbiol. 37, 3281-3290 (1999).
6. Rayner MG, Zhang Y, Gorry MC, Chen Y, Post JC, Ehrlich GD. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. JAMA 279, 296-299 (1998).
7. Zimmerli W, Ochsner PE. Management of infection associated with prosthetic joints. Injection 31, 99-108 (2003).
8. Zimmerli W, Widmer AF, Blatter M, Frei R, Ochsner PE. Role of rifampin for treatment of orthopedic implant-related staphylococcal infections: a randomized controlled trial. Foreign-Body Infection (FBI) Study Group. JAMA 279, 1537-1541 (1998).
9. Drancourt M, Stein A, Argenson JN, Roiron R, Groulier P, Raoult D. Oral treatment of Staphylococcus spp. infected orthopaedic implants with fusidic acid or ofloxacin in combination with rifampicin. J. Antimicrob. Chemother. 39, 235-240 (1997).
10. Stein A, Bataille JF, Drancourt M et al. Ambulatory treatment of multi-drug resistant Staphylococcus-infected orthopedic implants with high-dose oral co-trimoxazole (trimethoprim-sulfamethoxazole). Antimicrob. Agents Chemother 42, 3086-3091 (1998).
11. Widmer AF, Wiestner A, Frei R, Zimmerli W. Killing of nongrowing and adherent Escherichia coli determines drug efficacy in device-related infections. Antimicrob. Agents Chemother. 35, 741-746 (1991).
12. Mermel LA, Farr BM, Sherertz RJ et al. Guidelines for the management of intravascular catheter-related infections. Clin. Infect. Dis. 32, 1249-1272 (2001).
13. Raad I, Costerton W, Sabharwal U, Sacilowski M, Anaissie E, Bodey GP. Ultrastructural analysis of indwelling vascular catheters: a quantitative relationship between luminal colonization and duration of placement. J. Infect. Dis. 168, 400-407 (1993).
14. DesJardin JA, Falagas ME, Ruthazer R et al. Clinical utility of blood cultures drawn from indwelling central venous catheters in hospitalized patients with cancer. Ann. Intern. Med. 131, 641-647 (1999).
15. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140-1154 (2002).
16. deBeer D, Stoodley P, Lewandowski Z. Liquid flow in heterogeneous biofilms. Biotechnol. Bioeng. 44, 636-641 (1994).
17. Sauer F, Camper AK. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183, 6579-6589 (2001).
18. Stanley NP, Britton RA, Grossman AD, Lazazzera BA. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J. Bacteriol. 185, 1951-1957 (2003).
19. Whiteley M, Bangera MG, Bumgarner RE et al. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864 (2001).
20. Lopez-Lopez G, Pascual A, Perea EJ. Effect of plastic catheter material on bacterial adherence and viability. J. Med. Microbiol. 34, 349-353 (1991).
21. Vaudaux PE LD, Waldvogel FA. Host factors predisposing to and influencing therapy of foreign body infections. In: Infections Associated with Indwelling Medical Devices. 2nd Edition. Bisno AL, Waldvogel FA (Ed.), American Society for Microbiology Press, Washington DC, USA 1-29 (1994).
22. Shenkman B, Varon D, Tamarin I et al. Role of agr (RNAIII) in Staphylococcus aureus adherence to fibrinogen, fibronectin, platelets and endothelial cells under static and flow conditions. J. Med. Microbiol. 51, 747-754 (2002).
23. Hanssen AD, Rand JA, Osmon DR. Treatment of the infected total knee arthroplasty with insertion of another prosthesis. The effect of antibiotic-impregnated bone cement. Clin. Orthop. 44-55 (1994).
24. Carratala J, Niubo J, Fernandez-Sevilla A et al. Randomized, double-blind trial of an antibiotic-lock technique for prevention of Gram-positive central venous catheter-related infection in neutropenic patients with cancer. Antimicrob. Agents Chemother. 43, 2200-2204 (1999).
25. Raad I, Hachem R, Tcholakian RK, Sherertz R. Efficacy of minocycline and EDTA lock solution in preventing catheter-related bacteremia, septic phlebitis and endocarditis in rabbits. Antimicrob. Agents Chemother. 46, 327-332 (2002).
26. Veenstra DL, Saint S, Saha S, Lumley T, Sullivan SD. Efficacy of antiseptic-impregnated central venous catheters in preventing catheter-related bloodstream infection: a meta-analysis. JAMA 281, 261-267 (1999).
27. Raad I, Darouiche R, Dupuis J et al. Central venous catheters coated with minocycline and rifampin for the prevention of catheter-related colonization and bloodstream infections. A randomized, double-blind trial. The Texas Medical Center Catheter Study Group. Ann. Intern. Med. 127, 267-274 (1997).
28. Raad I, Darouiche R, Hachem R, Mansouri M, Bodey GP. The broad spectrum activity and efficacy of catheters coated with minocycline and rifampin. J. Infect. Dis. 173, 418-424 (1996).
29. Kalmanti M, Germanakis J, Stiakaki E et al. Prophylaxis with urokinase in pediatric oncology patients with central venous catheters. Pediatr. Hematol. Oncol. 19, 173-179 (2002).
30. Aquino VM, Sandler ES, Mustafa MM, Steele JW, Buchanan GR. A prospective double-blind randomized trial of urokinase flushes to prevent bacteremia resulting from luminal colonization of subcutaneous central venous catheters. J. Pediatr. Hematol. Oncol. 24, 710-713 (2002).
31. Ehrlich GD, Veeh R, Wang X et al. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287, 1710-1725 (2002).
32. Nickel JC, Costerton JW. Bacterial localization in antibiotic-refractory chronic bacterial prostatitis. Prostate 23, 107-114 (1993).
33. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbial. 37, 1771-1776 (1999).
34. Joly V, Pangon B, Vallois JM et al. Value of antibiotic levels in serum and cardiac vegetations for predicting antibacterial effect of ceftriaxone in experimental Escherichia coli endocarditis. Antimicrob. Agents Chemother. 31, 1632-1639 (1987).
35. Hancock E. Artificial valve disease. In: The Heart Arteries and Veins. (8th Edition). Schlant RC, O'Rourke RA, Roberts R, Sonnenblick EH (Ed.), McGraw-Hill, Inc., NY, USA 1539-1545 (1994).
36. Heldman AW, Hartert TV, Ray SC et al. Oral antibiotic treatment of right-sided staphylococcal endocarditis in injection drug users: prospective randomized comparison with parenteral therapy. Am. J. Med. 101, 68-76 (1996).
37. Wellman N, Fortun SM, McLeod BR. Bacterial biofilms and the bioelectric effect. Antimicrob. Agents Chemother. 40, 2012-2014 (1996).
38. Leid JG, Shirtliff ME, Costerton JW, Stoodley AP. Human leukocytes adhere to, penetrate and respond to Staphylococcus aureus biofilms. Infect. Immun. 70, 6339-6345 (2002).
39. Lam J, Chan R, Lam K, Costerton JW. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect. Immun. 28, 546-556 (1980).
40. de Beer D SP, Lewandowski Z. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 53(2), 151-158 (1997).
41. Zhu M, Takenaka S, Sato M, Hoshino E. Extracellular polysaccharides do not inhibit the reaction between Streptococcus mutans and its specific immunoglobulin G (IgG) or penetration of the IgG through S. mutans biofilm. Oral Microbiol. Immunol. 16, 54-56 (2001).
42. Hoiby N, Fomsgaard A, Jensen ET et al. The immune response to bacterial biofilms. In: Microbial Biofilms. Lappin-Scott HM, Costerton JW (Ed.), Cambridge University Press, Cambridge, UK 233-250 (1995).
43. Hassett DJ, Ma JF, Elkins JG et al. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol. Microbiol. 34, 1082-1093 (1999).
44. Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44, 1818-1824 (2000).
45. Anwar H, Strap JL, Costerton JW. Eradication of biofilm cells of Staphylococcus aureus with tobramycin and cephalexin. Can. J. Microbiol. 38, 618-625 (1992).
46. Williams I, Venables WA, Lloyd D, Paul F, Critchley I. The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus. Microbiology 143, 2407-2413 (1997).
47. Anderl JN, Zahller J, Roe F, Stewart PS. Role of nutrient limitation and stationary-phase existence in klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 47, 1251-1256 (2003).
48. Eng RH, Padberg FT, Smith SM, Tan EN, Cherubin CE. Bactericidal effects of antibiotics on slowly growing and nongrowing bacteria. Antimicrob. Agents Chemother. 35, 1824-1828 (1991).
49. Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A. The rate of killing of Escherichia coli by β-lactam antibiotics is strictly proportional to the rate of bacterial growth. J. Genet. Microbiol. 132, 1297-1304 (1986).
50. Spoering AL, Lewis K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183, 6746-6751 (2001).
51. Xu KD, Franklin MJ, Park CH, McFeters GA, Stewart PS. Gene expression and protein levels of the stationary phase sigma factor, RpoS, in continuously-fed Pseudomonas aeruginosa biofilms. FEMS Microbiol Lett. 199, 67-71 (2001).
52. Zheng Z, Stewart PS. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 46, 900-903 (2002).
53. Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47, 317-323 (2003).
54. Gordon CA, Hodges NA, Marriott C. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother. 22, 667-674 (1988).
55. Konig C, Schwank S, Blaser J. Factors compromising antibiotic activity against biofilms of Staphylococcus epidermidis. Eur. J. Clin. Microbiol. Infect. Dis. 20, 20-26 (2001).
56. Souli M, Giamarellou H. Effects of slime produced by clinical isolates of coagulase-negative staphylococci on activities of various antimicrobial agents. Antimicrob. Agents Chemother. 42, 939-941 (1998).
57. Durack DT, Beeson PB. Experimental bacterial endocarditis. II. Survival of a bacteria in endocardial vegetations. Br. J. Exp. Pathol. 53, 50-53 (1972).
58. Xu KD, Stewart PS, Xia F, Huang CT, McFeters GA. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64, 4035-4039 (1998).
59. Stewart PS, Griebe T, Srinivasan R et al. Comparison of respiratory activity and culturability during monochloramine disinfection of binary population biofilms. Appl. Environ. Microbiol. 60, 1690-1692 (1994).
60. Mason DJ, Power EG, Talsania H, Phillips I, Gant VA. Antibacterial action of ciprofloxacin. Antimicrob. Agents Chemother. 39, 2752-2758 (1995).
61. Zambrano MM, Kolter R. GASPing for life in stationary phase. Cell 86, 181-184 (1996).
62. Lazazzera BA. Quorum sensing and starvation: signals for entry into stationary phase. Curr. Opin. Microbiol. 3, 177-182 (2000).
63. Nystrom T. Aging in bacteria. Curr. Opin. Microbiol. 5, 596-601 (2002).
64. Drenkard E, Ausubel FM. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416, 740-743 (2002).
65. Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48, 1429-1449 (2003).
66. Testerman TL, Vazquez-Torres A, Xu Y, Jones-Carson J, Libby SJ, Fang FC. The alternative sigma factor sigmaE controls anti-oxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43, 771-782 (2002).
67. Bateman BT, Donegan NP, Jarry TM, Palma M, Cheung AL. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69, 7851-7857 (2001).
68. Foley I, Marsh P, Wellington EM, Smith AW, Brown MR. General stress response master regulator rpoS is expressed in human infection: a possible role in chronicity. J. Antimicrob. Chemother. 43, 164-165 (1999).
69. Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48, 253-67 (2003).
70. Heydorn A, Ersboll B, Kato J et al. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility cell-to-cell signaling and stationary-phase sigma factor expression. Appl. Environ. Microbiol. 68, 2008-2017 (2002).
71. Massey RC, Buckling A, Peacock SJ. Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus. Curr. Biol. 11, 1810-1814 (2001).
72. Lewis K. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64, 503-514 (2000).
73. Lewis K. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45, 999-1007 (2001).
74. Cochran WL, McFeters GA, Stewart PS. Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88, 22-30 (2000).
75. Das JR, Bhakoo M, Jones MV, Gilbert P. Changes in the biocide susceptibility of Staphylococcus epidermidis and Escherichia coli cells associated with rapid attachment to plastic surfaces. J. Appl. Microbiol. 84, 852-858 (1998).
76. Camara M, Williams P, Hardman A. Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect. Dis. 2, 667-676 (2002).
77. Purevdorj B, Costerton JW, Stoodley P. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 68, 4457-4464 (2002).
78. Bollinger N, Hassett DJ, Iglewski BH, Costerton JW, McDermott TR. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J. Bacteriol. 183, 1990-1996 (2001).
79. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67, 1865-1873 (2001).
80. Blevins JS, Beenken KE, Elasri MO, Hurlburt BK, Smeltzer MS. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect. Immun. 70, 470-480 (2002).
81. Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, Penades JR, Lasa I. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48, 1075-1087 (2003).
82. Vuong C, Saenz HL, Gotz F, Otto M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182, 1688-1693 (2000).
83. Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184, 2699-2708 (2002).
84. Balaban N, Gov Y, Bitler A, Boelaert JR. Prevention of Staphylococcus aureus biofilm on dialysis catheters and adherence to human cells. Kidney Int. 63, 340-345 (2003).
85. Giacometti A, Cirioni O, Gov Y et al. G. RNA III inhibiting peptide inhibits in vivo biofilm formation by drug-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47, 1979-1983 (2003).
86. Balaban N, Giacometti A, Cirioni O et al. Use of the quorum-sensing inhibitor RNAIII-inhibiting peptide to prevent biofilm formation in vivo by drug-resistant Staphylococcus epidermidis. J. Infect. Dis. 187, 625-630 (2003).
87. Stickler DJ, Morris NS, McLean RJ, Fuqua C. Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro. Appl. Environ. Microbiol. 64, 3486-3490 (1998).
88. Erickson DL, Endersby R, Kirkham A et al. Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect. Immun. 70, 1783-1790 (2002).
89. Shih PC, Huang CT. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. J. Antimicrob. Chemother. 49, 309-314 (2002).
90. Yoon SS, Hennigan RF, Hilliard GM et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell. 3, 593-603 (2002).
91. Pesci EC, Milbank JB, Pearson JP et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96, 11229-11234 (1999).
92. You Z, Fukushima J, Tanaka K, Kawamoto S, Okuda K. Induction of entry into the stationary growth phase in Pseudomonas aeruginosa by N-acylhomoserine lactone. FEMS Microbiol. Lett. 164, 99-106 (1998).
93. Thorne SH, Williams HD. Cell density-dependent starvation survival of Rhizobium leguminosarum bv. phaseoli: identification of the role of an N-acyl homoserine lactone in adaptation to stationary-phase survival. J. Bacteriol. 181, 981-990 (1999).
94. Smith RS, Iglewski BH. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6, 56-60 (2003).
95. Schuster M, Lostroh CP, Ogi T, Greenberg EP. Identification, timing and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066-2079 (2003).
96. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185, 2080-2095 (2003).
97. Vasil ML. DNA microarrays in analysis of quorum sensing: strengths and limitations. J. Bacteriol. 185, 2061-2065 (2003).
98. Reimmann C, Ginet N, Michel L et al. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148, 923-932 (2002).
99. Givskov M, de Nys R, Manefield M et al. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178, 6618-6622 (1996).
100. Hentzer M, Riedel K, Rasmussen TB et al. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148, 87-102 (2002).
101. Ren D, Sims JJ, Wood TK. Inhibition of biofilm formation and swarming of Bacillus subtilis by (5Z)-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Lett. Appl. Microbiol. 34, 293-299 (2002).
102. Hentzer M, Wu H, Andersen JB et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803-3815 (2003).
103. Bassler BL, Wright M, Showalter RE, Silverman MR. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9, 773-786 (1993).
104. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS, Lamont RJ. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185, 274-284 (2003).
105. Merritt J, Qi F, Goodman SD, Anderson MH, Shi W. Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun. 71, 1972-1979 (2003).
106. Wen ZT, Burne RA. Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl. Environ. Microbiol. 68, 1196-1203 (2002).
107. Winzer K, Hardie KR, Williams P. Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch! Curr. Opin. Microbiol. 5, 216-222 (2002).
108. Anwar H, van Biesen T, Dasgupta M, Lam K, Costerton JW. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system. Antimicrob. Agents Chemother. 33, 1824-1826 (1989).
109. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67, 5427-5433 (1999).
110. Rapp ME, Ulphani JS, Fey PD, Bartscht K, Mack D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect. Immun. 67, 2627-2632 (1999).
111. Ziebuhr W, Heilmann C, Gotz F et al. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect. Immun. 65, 890-896 (1997).
112. de Silva GD, Kantzanou M, Justice A et al. The ica operon and biofilm production in coagulase-negative Staphylococci associated with carriage and disease in a neonatal intensive care unit. J. Clin. Microbiol. 40, 382-388 (2002).
113. Knobloch JK, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med. Microbiol Immunol (Berl). 191, 101-106 (2002).
114. Dobinsky S, Kiel K, Rohde H et al. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J. Bacteriol. 185, 2879-2886 (2003).
115. Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob. Agents Chemother. 44, 3357-3363 (2000).
116. Ziebuhr W, Krimmer V, Rachid S, Lossner I, Gotz F, Hacker J. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the msertion sequence element IS256. Mol. Microbiol. 32, 345-356 (1999).
117. Conlon KM, Humphreys H, O'Gara JP. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J. Bacteriol. 184, 4400-4408 (2002).
118. Francois P, Tu Quoc PH, Bisognano C et al. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol. Med. Microbiol. 35, 135-140 (2003).
119. Becker P, Hufnagle W, Peters G, Herrmann M. Detection of differential gene expression in biofilm-forming versus planktonic populations of Staphylococcus aureus using micro-representational-difference analysis. Appl. Environ. Microbiol. 67, 2958-2965 (2001).
120. Finelli A, Gallant CV, Jarvi K, Burrows LL. Use of in-biofilm expression technology to identify genes involved in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, 2700-2710 (2003).
121. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181, 5993-6002 (1999).
122. Sutherland I. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147, 3-9 (2001).
123. Durack DT. Experimental bacterial endocarditis. IV. Structure and evolution of very early lesions. J. Pathol. 115, 81-89 (1975).
124. Wozniak DJ, Wyckoff TJ, Starkey M et al. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc. Natl Acad. Sci USA 100, 7907-7912 (2003).
125. Zielinski NA, Maharaj R, Roychoudhury S, Danganan CE, Hendrickson W, Chakrabarty AM. Alginate synthesis in Pseudomonas aeruginosa: environmental regulation of the algC promoter. J. Bacteriol. 174, 7680-7688 (1992).
126. Nivens DE, Ohman DE, Williams J, Franklin MJ. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J. Bacteriol. 183, 1047-1057 (2001).
127. Nguyen T, Louie SG, Beringer PM, Gill MA. Potential role of macrolide antibiotics in the management of cystic fibrosis lung disease. Curr. Opin. Pulm. Med. 8, 521-528 (2002).
128. Mitsuya Y, Kawai S, Kobayashi H. Influence of macrolides on guanosine diphospho-D-mannose dehydrogenase activity in Pseudomonas biofilm. J. Infect. Chemother. 6, 45-50 (2000).
129. Sano M, Hirose T, Nishimura M, Takahashi S, Matsukawa M, Tsukamoto T. Inhibitory action of clarithromycin on glycocalyx produced by MRSA. J. Infect. Chemother. 5, 10-15 (1999).
130. Yamasaki O, Akiyama H, Toi Y, Arata J. A combination of roxithromycin and imipenem as an antimicrobial strategy against biofilms formed by Staphylococcus aureus. J. Antimicrob. Chemother. 48, 573-577 (2001).
131. Huang CT, Stewart PS. Reduction of polysaccharide production in Pseudomonas aeruginosa biofilms by bismuth dimercaprol (BisBAL) treatment. J. Antimicrob. Chemother. 44, 601-5 (1999).
132. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002).
133. Hook EW 3rd, Sande MA. Role of the vegetation in experimental Streptococcus viridans endocarditis. Infect. Immun. 10, 1433-1438 (1974).
134. Kupferwasser LI, Yeaman MR, Shapiro SM et al. Acetylsalicylic acid reduces vegetation bacterial density, hematogenous bacterial dissemination and frequency of embolic events in experimental Staphylococcus aureus endocarditis through antiplatelet and antibacterial effects. Circulation 99, 2791-2797 (1999).
135. Isberg RR, Barnes P. Dancing with the host; flow-dependent bacterial adhesion. Cell 110, 1-4 (2002).
136. Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J. Ind. Microbiol. Biotechnol. 29, 361-367 (2002).
137. Wilson JW, Ott CM, Ramamurthy R et al. Low-Shear modeled microgravity alters the Salmonella enterica serovar typhimurium stress response in an RpoS-independent manner. Appl. Environ Microbiol. 68, 5408-5416 (2002).
138. Koerner RJ. Contribution of endotracheal tubes to the pathogenesis of ventilator-associated pneumonia. J. Hosp. Infect. 35, 83-89 (1997).
139. Stoodley P, Hall-Stoodley L, Lappin-Scott HM. Detachment, surface migration and other dynamic behavior in bacterial biofilms revealed by digital time-lapse imaging. Meth. Enzymol. 337, 306-319 (2001).
140. Inglis TJ. Evidence for dynamic phenomena in residual tracheal tube biofilm. Br J Anaesth. 70, 22-24 (1993).
141. Liu Y, Tay JH. Metabolic response of biofilm to shear stress in fixed-film culture. J. Appl. Microbiol. 90, 337-342 (2001).
142. Peyton B. Effects of shear-stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density. Water Res. 30, 29-36 (1996).
143. Flemming HC, Mayer C, Koerstgens V and Borchard W. Cohesiveness in biofilm matrix polymers. In: Community Structure and Co-operation in Biofilms. SGM Symposium Series 59. Allison D, Lappin-Scott HM and Wilson M (Ed.), Cambridge Uni. Press, Cambridge, UK 87-105 (2000).
144. Stoodley P, Wilson S, Hall-Stoodley L, Boyle JD, Lappin-Scott HM, Costerton JW. Growth and detachment of cell clusters from mature mixed-species biofilms. Appl. Environ. Microbiol. 67, 5608-5613 (2001).
145. Characklis W. Biofilm processes. In: Biofilms. Characklis WG, Marshall DC (Ed.), John Wiley & Sons, NY, USA 195-232 (1990).
146. Daly B, Betts WB, Brown AP, O'Neill JG. Bacterial loss from biofilms exposed to free chlorine. Microbios 96, 7-21 (1998).
147. Boyd A, Chakrabarty AM. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60, 2355-2359 (1994).
148. Lee SF, Li YH, Bowden GH. Detachment of Streptococcus mutans biofilm cells by an endogenous enzymatic activity. Infect. Immun. 64, 1035-1038 (1996).
149. Allison DG, Ruiz B, SanJose C, Jaspe A, Gilbert P. Extracelllar products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol Lett. 167, 179-184 (1998).
150. Webb JS, Thompson LS, James S et al. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, 4585-4592 (2003).
151. Xiong YQ, Van Wamel W, Nast CC, Yeaman MF, Cheung AL, Bayer AS. Activation and transcriptional interaction between agr RNAII and RNAIII in Staphylococcus aureus in vitro and in an experimental endocarditis model. J. Infect. Dis. 186, 668-677 (2002).
152. Beenken KE, Blevins JS, Smeltzer MS. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71, 4206-4211 (2003).