Understanding biofilm resistance to antibacterial agents (original) (raw)

References

1. Lawrence, J. R., Korber, D. R., Hoyle, B. D., Costerton, J. W. & Caldwell, D. E. Optical sectioning of microbial biofilms. J. Bacteriol. 173, 6558–6567 (1991). One of the first descriptions of the 3-dimensional structure of natural biofilms.
   CAS PubMed PubMed Central Google Scholar
2. Lawrence, J. R. & Neu, T. R. Confocal laser scanning microscopy for analysis of microbial biofilms. Methods Enzymol. 310, 131–144 (1999).
   CAS PubMed Google Scholar
3. Lewandowski, Z., Stoodley, P., Altobelli, S. & Fukushima, E. Hydrodynamics and kinetics in biofilm systems — recent advances and new problems. Proceedings of the Second IAWQ International Specialized Conference on Biofilm Reactors. Paris, France, pp. 313–319 (1993).
4. DeBeer, D., Stoodley, P., Roe, F. & Lewandowski, Z. Effects of biofilm structure on oxygen distribution and mass transport. Biotech. Bioeng. 43, 1131–1138 (1994).
   CAS Google Scholar
5. Davies, D. G. et al. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295–298 (1998). The first paper to link biofilm development with intercellular communication.
   CAS PubMed Google Scholar
6. Martinelli, D., Bachofen, R. & Brandl, H. Effect of medium composition, flow rate, and signaling compounds on the formation of soluble extracellular materials by biofilms of Chromobacterium violaceum. Appl. Microbiol. Biotechnol. 59, 278–283 (2002).
   CAS PubMed Google Scholar
7. Huber, B. et al. Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol. Microbiol. 46, 411–426 (2002).
   CAS PubMed Google Scholar
8. National Institute of Dental Research. The Oral Health of United States Adults. The National Survey of Dental Caries in US Employed Adults and Seniors: 1985–1986. DHHS Pub. No. (NIH) 87–2868. (US Department of Health and Human Services, Bethesda, Maryland 1987).
9. National Institute of Dental Research. Oral health of United States children. The National Survey of Dental Caries in US School Children, 1986–1987. DHHS Pub. No. (NIH) 89–2247. (Department of Health and Human Services, Bethesda, Maryland 1989).
10. Passerini, L., Lam, K., Costerton, J. W. & King, E. G. Biofilms on indwelling vascular catheters. Crit. Care Med. 20, 665–673 (1992).
    CAS PubMed Google Scholar
11. Pople, I. J., Bayston, R. & Hayward, R. D. Infection of cerebrospinal fluid shunts in infants: a study of etiological factors. J. Neurosurg. 77, 29–36 (1992).
    CAS PubMed Google Scholar
12. Costerton, J. W. et al. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41, 435–464 (1987).
    CAS PubMed Google Scholar
13. Hoiby, N. et al. in Microbial Biofilms (eds Lappin–Scott, H. M. & Costerton, J. W.) (Cambridge University Press, Cambridge, 1995).
    Google Scholar
14. Luppens, S. B., Reij, M. W. van der Heijden, R. W., Rombouts, F. M. & Abee, T. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl. Environ. Microbiol. 68, 4194–4200 (2002).
    CAS PubMed PubMed Central Google Scholar
15. Brown, M. R., Allison, D. G. & Gilbert, P. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J. Antimicrob. Chemother. 22, 777–783 (1988).
    CAS PubMed Google Scholar
16. Anwar, H., Strap, J. L. & Costerton, J. W. Establishment of aging biofilms: possible mechanism of bacterial resistance to antimicrobial therapy. Antimicrob. Agents Chemother. 36, 1347–1351 (1992).
    CAS PubMed PubMed Central Google Scholar
17. Mah, T. F. & O'Toole, G. A. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34–39 (2001).
    CAS PubMed Google Scholar
18. Sauer, K. & Camper, A. K. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183, 6579–6589 (2001).
    CAS PubMed PubMed Central Google Scholar
19. Stewart, P. S. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292, 107–113 (2002). An excellent review from an engineering perspective on antibiotic resistance in bacterial biofilms.
    CAS PubMed Google Scholar
20. Donlan, R. M. & Costerton, J. W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167–193 (2002). A comprehensive review outlining many organisms of medical importance and what is known about their resistance to specific antibiotics.
    CAS PubMed PubMed Central Google Scholar
21. Gilbert, P., Maira-Litran, T., McBain, A. J., Rickard, A. H. & White, F. W. The physiology and collective recalcitrance of microbial biofilm communities. Adv. Microb. Physiol. 46, 202–256 (2002). A thoughtful and insightful look at the mechanisms underlying the resistance of biofilms to antibiotic treatments.
    PubMed Google Scholar
22. Gilbert, P., Allison, D. G. & McBain, A. J. Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance?. J. Appl. Microbiol. Suppl. 98, S–110S (2002).
    Google Scholar
23. Yu, F. P. & McFeters, G. A. Rapid in situ assessment of physiological activities in bacterial biofilms using fluorescent probes. J. Microbiol. Methods 20, 1–10 (1994).
    CAS PubMed Google Scholar
24. Huang, C. -T., Yu, F. P., McFeters, G. A. & Stewart, P. S. Nonuniform spatial patterns of respiratory activity within biofilms during disinfection. Appl. Environ. Microbiol. 61, 2252–2256 (1995). A classic paper that visually demonstrates the effect of an antimicrobial agent against a biofilm in situ.
    CAS PubMed PubMed Central Google Scholar
25. Onarheim, H. et al. Outbreak of multiresistant Acenetobacter baumannii infection. Tidsskr. Nor. Laegeforen. 120, 1028–1033 (2000).
    CAS PubMed Google Scholar
26. Still, J., Law, E., Friedman, B., Furman, S. & Newton, T. Vancomycin resistant organisms in a burn unit. South Med. J. 94, 810–812 (2001).
    CAS PubMed Google Scholar
27. Rastegar, L. A., Bahrami, H. H. & Alaghebandan, R. Pseudomonas infections in Tohid Burn Center, Iran. Burns 24, 637–641 (1998).
    Google Scholar
28. Olson, M. E., Ceri, H., Morck, D. W., Buret, A. G. & Read, R. R. Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can. J. Vet. Res. 66, 86–92 (2002).
    PubMed PubMed Central Google Scholar
29. Jensen, E. T. et al. Complement activation by Pseudomonas aeruginosa biofilms. Microb. Pathol. 15, 377–388 (1993).
    CAS Google Scholar
30. Rogers, J., Phillip, F. & Olliff, C. The effects of extracellular slime from Staphylococcus epidermidis on phagocytic ingestion and killing. FEMS Immunol. Med. Microbiol. 9, 109–115 (1994).
    Google Scholar
31. Moran, F. J. et al. Phagocytosis and killing of slime-producing Staphylococcus epidermidis by polymorphonuclear leukocytes. Effects of sparfloxacin. Rev. Esp. Quimioter. 11, 52–57 (1998).
    CAS PubMed Google Scholar
32. Costerton, J. W., Lewandowski, Z., Caldwell, D., Korber, D. & Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol. 49, 711–745 (1995).
    CAS PubMed Google Scholar
33. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322 (1999).
    CAS PubMed Google Scholar
34. Meluleni, G. J., Grout, M., Evans, D. J. & Pier, G. B. Mucoid Pseudomonas aeruginosa growing in a biofilm in vitro are killed by opsonic antibodies to the mucoid exopolysaccharide capsule but not by antibodies produced during chronic lung infection in cystic fibrosis patients. J. Immunol. 155, 2029–2038 (1995).
    CAS PubMed Google Scholar
35. Dasgupta, M. K. Biofilm causes decreased production of interferon-γ. J. Am. Soc. Nephrol. 7, 877–882 (1996).
    CAS PubMed Google Scholar
36. Suci, P. A., Mittelman, M. W., Yu, F. P. & Geesey, G. G. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 38, 2125–2133 (1994). An excellent paper describing a novel in situ method for determining antibiotic penetration into biofilms.
    CAS PubMed PubMed Central Google Scholar
37. Vrany, J. D., Stewart, P. S. & Suci, P. S. Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa bofilms displaying rapid-transport characteristics. Antimicrob. Agents Chemother. 41, 1352–1358 (1997).
    CAS PubMed PubMed Central Google Scholar
38. Anderl, J., Franklin, M. J. & Stewart, P. S. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxicin. Antimicrob. Agents Chemother. 44, 1818–1824 (2000).
    CAS PubMed PubMed Central Google Scholar
39. Stone, G., Wood, P., Dixon, M., Keyhan, M. & Matin, A. Tetracycline rapidly reaches all the constituent cells of uropothogenic Escherichia coli biofilms. Antimicrob. Agents Chemother. 46, 2458–2461 (2002).
    CAS PubMed PubMed Central Google Scholar
40. Larsen, T. Susceptibility of Porphyromonas gingivalis in biofilms to amoxicillin, doxycycline and metronidazole. Oral Microbiol. Immunol. 5, 267–271 (2002).
    Google Scholar
41. Campanac, C., Pineau, L., Payard, A., Baziard-Mouysset, G. & Roques, C. Interactions between biocide cationic agents and bacterial biofilms. Antimicrob. Agents Chemother. 46, 1469–1474 (2002).
    CAS PubMed PubMed Central Google Scholar
42. Stoodley, P., deBeer, D. & Lappin-Scott, H. M. Influence of electric fields and pH on biofilm structure as related to the bioelectric effect. Antimicrob. Agents Chemother. 41, 1876–1879 (1997).
    CAS PubMed PubMed Central Google Scholar
43. Costerton, J. W., Ellis, B., Lam, K., Johnson, F. & Koury, A. E. Mechanism of electrical enhancement of efficacy of antibiotics in killing biofilm bacteria. Antimicrob. Agents Chemother. 38, 2803–2809 (1994). Introduction of a novel strategy using electrical fields to enhance the effectiveness of antibiotics against biofilms.
    CAS PubMed PubMed Central Google Scholar
44. McLeod, B. R., Fortun, S., Costerton, J. W. & Stewart, P. S. Enhanced bacterial biofilm control using electromagnetic fields in combination with antibiotics. Methods Enzymol. 310, 656–670 (1999).
    CAS PubMed Google Scholar
45. Sternberg, C. et al. Distribution of bacterial growth activity in flow-chamber biofilms. Appl. Environ. Microbiol. 65, 4108–4117 (1999). A landmark paper demonstrating the activity and positioning of single cells in biofilms in real time.
    CAS PubMed PubMed Central Google Scholar
46. Ashby, M. J., Neale, J. E. & Critchley, I. A. Effect of antibiotics on non-growing planktonic cells and biofilms of Escherichia coli. J. Antimicrob. Chemotherapy 33, 443–452 (1994).
    CAS Google Scholar
47. Shigeta, M. G. et al. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43, 340–345 (1997).
    CAS PubMed Google Scholar
48. Shigeta, M., Komatsuzawa, M., Sugai, M., Suginaka, H. & Usui, T. Effect of the growth rate of Pseudomonas aeruginosa biofilms on the susceptibility to antimicrobial agents. Chemotherapy 43, 137–141 (1997).
    CAS PubMed Google Scholar
49. Tanaka G. et al. Effect of the growth rate of Pseudomonas aeruginosa biofilms on the susceptibility to antimicrobial agents: beta-lactams and fluoroquinolones. Chemotherapy 45, 28–36 (1999).
    CAS PubMed Google Scholar
50. Spoering A. L. & K. Lewis, K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183, 6746–6751 (2001). An examination of bacterial resistance based on defects in preprogrammed cell death. This paper has stimulated considerable debate regarding the mechanism of biofilm resistance.
    CAS PubMed PubMed Central Google Scholar
51. McCoy, W. F. & Costerton, J. W. Fouling biofilm development in tubular flow systems. Dev. in Indust. Microbiol. 23, 551–558 (1982).
    Google Scholar
52. Morisaki, H. Effect of solid-liquid interface on metabolic activity of E. coli. J. Gen. Appl. Microbiol. 29, 195–204 (1983).
    CAS Google Scholar
53. Jeffrey, W. H. & Paul, J. H. Activity of an attached and free-living Vibrio sp. As measured by thymidine incorporation, _p_-iodonitrotetrazolium reduction, and ATP/ADP ratios. Appl. Environ. Microbiol. 51, 150–156 (1986).
    CAS PubMed PubMed Central Google Scholar
54. Davies, D. G. & McFeters, G. A. Growth and comparative physiology of Klebsiella oxytoca attached to granular activated carbon particles and in liquid media. Microb. Ecol. 15, 165–175 (1988).
    CAS PubMed Google Scholar
55. Davies, D. G. & Geesey, G. G. Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl. Environ. Microbiol. 61, 860–867 (1995).
    CAS PubMed PubMed Central Google Scholar
56. Prigent-Combaret, C., Vidal, O., Dorel, C. & Lejeune, P. Abiotic surface sensing and biofilm-dependent regulation of gene expression in E. coli. J. Bacteriol. 181, 5993–6002 (1999).
    CAS PubMed PubMed Central Google Scholar
57. Whiteley, M. et al. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860–864 (2001).
    CAS PubMed Google Scholar
58. Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W. & Davies, D. G. Pseudomonas aeruginosa displays multiple phenotypes as a biofilm. J. Bacteriol. 184, 1140–1154 (2002). A paper describing the different phenotypic stages of biofilm development using primarily a proteomics approach. It was the first paper to outline the complete life-cycle of a biofilm-forming pathogen.
    CAS PubMed PubMed Central Google Scholar
59. Drenkard, E. & Ausubel, F. M. _Pseudomona_s biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416, 740–743 (2002). An important paper linking phenotypic differences in biofilms to antibiotic susceptibility.
    CAS PubMed Google Scholar
60. Schurr, M. J., Martin, D. W., Mudd, M. H. & Deretic, V. Gene cluster controlling conversion to alginate-overproducing phenotype in Pseudomonas aeruginosa: functional analysis in a heterologous host and role in the instability of mucoidy. J. Bacteriol. 176, 3375–3382 (1994).
    CAS PubMed PubMed Central Google Scholar
61. O'Toole, G. A., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49–79 (2000).
    CAS PubMed Google Scholar
62. Belas, R., Simon, M. & Silverman, M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167, 210–218 (1986).
    CAS PubMed PubMed Central Google Scholar
63. Dagastino, L., Goodman, A. E. & Marshall, K. C. Physiological responses induced in bacteria adhering to surfaces. Biofouling 4, 113–119 (1991).
    Google Scholar
64. Santos, R., Callow, M. E. & Bott, T. R. The structure of Pseudomonas fluorescens biofilms in contact with flowing systems. Biofouling 4, 319–336 (1991).
    Google Scholar
65. Davies, D. G., Chakrabarty, A. M. & Geesey, G. G. Exopolysaccharide production in biofilms: substratum activation of alginate gene expression in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 59, 1181–1186 (1993). First report of the the detection of specific gene activity in bacteria at the single-cell level, in real time and in situ.
    CAS PubMed PubMed Central Google Scholar
66. Dalton, H. M. & March, P. E. Molecular genetics of bacterial attachment and biofouling. Biotechnology 9, 252–255 (1998).
    CAS Google Scholar
67. Dekkers, L. C. et al. Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and of NADH:ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol. Plant Microbe Interact. 11, 763–771 (1998).
    CAS PubMed Google Scholar
68. O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295–304 (1998).
    CAS PubMed Google Scholar
69. O'Toole, G. A. & Kolter, R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28, 419–461 (1998).
    Google Scholar
70. DeFlaun, M. F., Oppenheimer, S. R., Streger, S., Condee, C. W. & Fletcher, M. Alterations in adhesion, transport, and membrane characteristics in an adhesion-deficient pseudomonad. Appl. Environ. Microbiol. 65, 759–765 (1999).
    CAS PubMed PubMed Central Google Scholar
71. Genevaux, P., Bauda, P., DuBow, M. S. & Oudega, B. Identification of Tn10 insertions in the rfaG, rfaP, and galU genes involved in lipopolysaccharide core biosynthesis that affect Escherichia coli adhesion. Arch. Microbiol. 172, 1–8 (1999).
    CAS PubMed Google Scholar
72. Pratt, L. A. & Kolter, R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30, 285–293 (1998).
    CAS PubMed Google Scholar
73. Rodriguez-Herva, J. J., Reniero, D., Galli, E. & Ramos, J. L. Cell envelope mutants of Pseudomonas putida: physiological characterization and analysis of their ability to survive in soil. Environ. Microbiol. 1, 479–488 (1999).
    CAS PubMed Google Scholar
74. Steyn B, Oosthuizen, M. C., MacDonald, R., Theron, J. & Brozel, V. S. The use of glass wool as an attachment surface for studying phenotypic changes in Pseudomonas aeruginosa biofilms by two-dimensional gel electrophoresis. Proteomics 1, 871–879 (2001).
    CAS PubMed Google Scholar
75. Brözel, V. S., Strydom, G. M. & Cloete, T. E. E. A method for the study of de novo protein synthesis in Pseudomonas aeruginosa after attachment. Biofouling 8, 195–210 (1995).
    Google Scholar
76. Svensater, G., Welin, J., Wilkins, J. C., Beighton, D. & Hamilton, I. R. Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol. Lett. 205, 139–146 (2001).
    CAS PubMed Google Scholar
77. Espinosa-Urgel, M., Salido, A. & Ramos, J. L. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 182, 2363–2369 (2000).
    CAS PubMed PubMed Central Google Scholar
78. Grobe, K. J., Zahller, J. J. & Stewart, P. S. Role of dose concentraion in biocide efficacy against Pseudomonas aeruginosa. J. Indust. Microbiol. Biotechnol. 29, 10–15 (2002).
    CAS Google Scholar
79. Allison, D. G., B. Ruiz, B., SanJose, C., Jaspe, A. & Gilbert, P. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167, 179–184 (1988).
    Google Scholar
80. Vats, N. & Lee, S. F. Active detachment of Streptococcus mutans cells adhered to epon-hydroxylapatite surfaces coated with salivary proteins in vitro. Arch. Oral Biol. 45, 305–314 (2000). An interesting and significant report on the regulation of autodispersion of biofilms.
    CAS PubMed Google Scholar
81. Jackson, D. W. et al. Biofilm formation and dispersion under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184, 290–301 (2002).
    CAS PubMed PubMed Central Google Scholar
82. Choi, J. Y. et al. Identificationof virulence genes in a pathogenic strain of Pseudomonas aeruginosa by representational difference analysis. J. Bacteriol. 184, 952–961 (2002).
    CAS PubMed PubMed Central Google Scholar
83. Hubank, M. & Schatz, D. G. Identifying differences in mRNA expression by representational difference analysis of cDNA. Nucleic Acids Res. 22, 5640–5648 (1994).
    CAS PubMed PubMed Central Google Scholar
84. Jander, G., Rahme, L. G. & Ausubel, F. M. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182, 3843–3845 (2000). A well-conducted investigation of the differences in virulence of an important pathogen in different model hosts.
    CAS PubMed PubMed Central Google Scholar
85. Tan, M. W., Mahajan-Miklos, S. & Ausubel, F. M. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl Acad. Sci. USA 96, 715–720 (1999).
    CAS PubMed PubMed Central Google Scholar
86. Tan, M. W., Rahme, L. G., Sternberg, J. A., Tompkins, R. G. & Ausubel, F. M. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc. Natl Acad. Sci. USA 96, 2408–2413 (1999).
    CAS PubMed PubMed Central Google Scholar
87. Brooun, A., Liu, S. & Lewis, K. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44, 640–466 (2000).
    CAS PubMed PubMed Central Google Scholar
88. Lewis, K. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45, 999–1007 (2001).
    CAS PubMed PubMed Central Google Scholar
89. Latifi, A., Foglino, M., Tanaka, K., Williams, P. & Lazdunski, A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21, 1137–1146 (1996).
    CAS PubMed Google Scholar
90. Fuqua, W. C., Winans, S. C. & Greenberg, E. P. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269–275 (1994).
    CAS PubMed PubMed Central Google Scholar
91. May, T. B. et al. Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin. Microbiol. Rev. 4, 191–206 (1991).
    CAS PubMed PubMed Central Google Scholar
92. Singh, P. et al. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407, 762–764 (2000).
    CAS PubMed Google Scholar

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