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Chapter 14 : Biofilm Antimicrobial Resistance

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Abstract:

This chapter describes the phenomenon of biofilm-reduced susceptibility to antimicrobial agents, discusses factors that influence biofilm tolerance, and outlines possible protective mechanisms. Microorganisms that band together in biofilms are protected from killing by biocides, disinfectants, and antibiotics. The phenomenon of biofilm resistance to drugs and antimicrobials is easily reproduced in the laboratory. The antimicrobial agents range from brute-force oxidants, such as chlorine, to antibiotics with exquisitely specific cellular targets. The microorganisms range from bacteria to yeast and from obligate aerobes to sulfate reducing bacteria and other finicky anaerobes. When microorganisms are dispersed from a biofilm, their antimicrobial susceptibility is usually rapidly restored. Fungal biofilms are commonly encountered in cases of invasive catheter-related infections as well as superficial infections like denture stomatitis. Biofilm susceptibility is influenced significantly by such factors as biofilm thickness, biofilm age, biofilm areal cell density, antimicrobial dose concentration, biofilm species composition, and genotype. In bacterial biofilms, it has been suggested that the thick extracellular matrix (ECM) may contribute to antimicrobial resistance by preventing the diffusion of drugs to target cells. The cellular target of fluconazole in is a cytochrome P-450 hemoprotein involved in the ergosterol biosynthetic pathway. Microorganisms are equipped with numerous genetic and biochemical systems for responding to environmental stresses. Reduced antimicrobial susceptibility of microorganisms in biofilms is thought to be due to a combination of antimicrobial depletion through reactions with biofilm constituents, poor antimicrobial penetration, slow growth or stationary-phase existence in the biofilm, adaptive stress responses, and the formation of protected persister cells.

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Figures

Image of FIGURE 1
FIGURE 1

Comparison of biofilm (●) and planktonic (○) killing by antimicrobial agents. (A) challenged with 0.1 μg of rifampin per ml (from ). (B) challenged with 50 mg of glutaraldehyde per liter (reprinted from ). (C) challenged with 10 μg of tobramycin per ml (from ).

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Image of FIGURE 2
FIGURE 2

Correlation of biofilm development and metabolic activity with antifungal resistance Antifungal susceptibility of at different stages of biofilm development against FLU (A), AMB (B), NYT (C), CHX (D), respectively, are represented as histograms. The line curves show percent metabolic activity of growing biofilms exposed to FLU (64 μg/ml), AMB (4 μg/ml), NYT (8 μg/ml) or CHX (64 μg/ml). Metabolic activity was normalized to the control without drugs, which was taken as 100%. Redrawn with permission from ( ).

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Image of FIGURE 3
FIGURE 3

Effect of amphotericin B (a), flucytosine (b), and fluconazole (c) on biofilms grown statically (●) or with gentle shaking (○). [H]Leucine incorporation by biofilms was determined as a percentage of that for control biofilms incubated in the absence of the antifungal agent. Redrawn from Baillie and Douglas, 2000, by permission of Oxford University Press.

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Image of FIGURE 4
FIGURE 4

Effect of amphotericin B on biofilms grown statically (a) or with shaking (b) on PVC discs cut from Faucher tubes (Vygon) (●) or vena cava catheters ( Jostra) (○). [H]Leucine incorporation by biofilms was determined as a percentage of that for control biofilms incubated in the absence of the antifungal agent. Redrawn from Baillie and Douglas, 2000, by permission from Oxford University Press.

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Image of FIGURE 5
FIGURE 5

Variations of sterol profile of biofilm at different developmental phases. Sterol pattern for biofilms grown to early (A), intermediate (B), or mature (C) phases were determined by gas-liquid chromatography. (D) Percentage levels of sterols identified in biofilms and planktonic cells (chromatograph not shown), determined from the corresponding peak areas and retention times relative to ergosterol. Peaks 1 to 7 (panels A to C) represent sterols described in panel D. Redrawn with permission from ( ).

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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FIGURE 6

Chlorine concentration profiles in a mixed species biofilm. Chlorine at a concentration of approximately 2.5 mg/liter was flowed continuously over a biofilm, which was probed with a chlorinesensitive microelectrode. At 10 min (●), 30 min (○), and 105 min (■) of exposure, chlorine penetrated only into the surface layers of the biofilm. Redrawn with permission from ( ).

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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Image of FIGURE 7
FIGURE 7

Induction of catalase in biofilms (●) and planktonic cells (○) of in response to hydrogen peroxide treatment. Biofilm cells are able to express this stress response while planktonic cells are not able to respond to the same challenge. Biofilm cells that are not exposed to hydrogen peroxide show no change in activity (■). Redrawn with permission from ( ).

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
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References

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1. Adam, B.,, G. S. Baillie,, and L. J. Douglas. 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J. Med. Microbiol. 51: 344 349.
2. Anderl, J. N.,, M. J. Franklin,, and P. S. Stewart. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44: 1818 1824.
3. Anwar, H.,, T. van Biesen,, M. Dasgupta,, K. Lam,, and J. W. Costerton. 1989. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system. Antimicrob. Agents Chemother. 33: 1824 1826.
4. Baillie, G. S.,, and L. J. Douglas. 2000. Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J. Antimicrob. Chemother. 46: 397 403.
5. Brooun, A., Liu, S., and K. Lewis. 2000. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44: 640 646.
6. Budhani, R. K.,, and J. K. Struthers. 1998. Interaction of Streptococcus pneumoniae and Moraxella catarrhalis: investigation of the indirect pathogenic role of a beta-lactamase-producing Moraxelae by use of a continuous-culture biofilm system. Antimicrob. Agents Chemother. 42: 2521 2526.
7. Catalan, A.,, R. Herrera,, and A. Martinez. 1987. Denture plaque and palatal mucosa in denture stomatitis: scanning electron microscopic and microbiologic study. J. Prosthet. Dent. 57: 581 586.
8. Chandra, J.,, D. M. Kuhn,, P. K. Mukherjee,, L. L. Hoyer,, T. McCormick,, and M. A. Ghannoum. 2001a. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. J. Bacteriol. 183: 5385 5394.
9. Chandra, J.,, P. K. Mukherjee,, S. D. Leidich,, F. F. Faddoul,, L. L. Hoyer,, L. J. Douglas,, and M. A. Ghannoum. 2001b. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J. Dent. Res. 80: 903 908.
10. Chaudhary, P. M.,, and I. B. Roninson. 1991. Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell 66: 85 94.
11. Clark, F. S.,, T. Parkinson,, C. A. Hitchcock,, and N. A. Gow. 1996. Correlation between rhodamine 123 accumulation and azole sensitivity in Candida species: possible role for drug efflux in drug resistance. Antimicrob. Agents Chemother. 40: 419 425.
12. Cochran, W. L.,, S.-J. Suh,, G. A. McFeters,, and P. S. Stewart. 2000. Role of RpoS and AlgT in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88: 546 553.
13. Darouiche, R. O.,, A. Dhir,, A. J. Miller,, G. C. Landon,, I. I. Raad,, and D. M. Musher. 1994. Vancomycin penetration into biofilm covering infected prostheses and effect on bacteria. J. Infect. Dis. 170: 720 723.
14. Davies, D. G.,, M. R. Parsek,, J. P. Pearson,, B. H. Iglewski,, J. W. Costerton,, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295 298.
15. de Beer, D.,, R. Srinivasan,, and P. S. Stewart. 1994a. Direct measurement of chlorine penetration into biofilms during disinfection. Appl. Environ. Microbiol. 60: 4339 4344.
16. de Beer, D.,, P. Stoodley,, F. Roe,, and Z. Lewandowski. 1994b. Effects of biofilm structure on oxygen distribution and mass transport. Biotechnol. Bioeng. 43: 1131 1138.
17. De Kievit, T. R.,, M. D. Parkins,, R. J. Gillis,, R. Srikumar,, H. Ceri,, K. Poole,, B. H. Iglewski,, and D. G. Storey. 2001. Multidrug efflux pumps: Expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 45: 1761 1770.
18. Douglas, L. J. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11: 30 36.
19. Drenkard, E.,, and F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740 742.
20. Dunne, W. M., Jr.,, E. O. Mason, Jr.,, and S. L. Kaplan. 1993. Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm. Antimicrob. Agents Chemother. 37: 2522 2526.
21. Elkins, J. G.,, D. J. Hassett,, P. S. Stewart,, H. P. Schweizer,, and T. R. McDermott. 1999. Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65: 4594 4600.
22. Elvers, K. T.,, K. Leeming,, and H. M. Lappin- Scott. 2002. Binary and mixed population biofilms: time-lapse image analysis and disinfection with biocides. J. Ind. Microbiol. Biotechnol. 29: 331 338.
23. Ghannoum, M. A.,, N. M. Moussa,, P. Whittaker,, I. Swairjo,, and K. H. Abu-Elteen. 1992. Subinhibitory concentration of octenidine and pirtenidine: influence on the lipid and sterol contents of Candida albicans. Chemotherapy 38: 46 56.
24. Ghannoum, M. A.,, and L. B. Rice. 1999. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12: 501 517.
25. Gilbert, P.,, J. R. Das,, M. V. Jones,, and D. G. Allison. 2001. Assessment of resistance towards biocides following the attachment of micro-organisms to, and growth on, surfaces. J. Appl. Microbiol. 91: 248 254.
26. Gordon, C. A.,, N. A. Hodges,, and C. Marriott. 1988. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother. 22: 667 674.
27. Grobe, K. J.,, J. Zahller,, and P. S. Stewart. 2002. Role of dose concentration in biocide efficacy against Pseudomonas aeruginosa biofilms. J. Ind. Microbiol. Biotechnol. 29: 10 15.
28. Hassett, D. J.,, J.-F. Ma,, J. G. Elkins,, T. R. McDermott,, U. A. Ochsner,, S. E. H. West,, C.-T. Huang,, J. Fredericks,, S. Burnett,, P. S. Stewart,, G. A. McFeters,, L. Passador,, and B. H. Iglewski. 1999. 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.
29. Hawser, S. P.,, G. S. Baillie,, and L. J. Douglas. 1998. Production of extracellular matrix by Candida albicans biofilms. J. Med. Microbiol. 47: 253 256.
30. Hawser, S. P.,, and L. J. Douglas. 1995. Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob. Agents Chemother. 39: 2128 2131.
31. Hentzer, M.,, G. M. Teitzel,, G. J. Balzer,, A. Heydorn,, S. Molin,, M. Givskov,, and M. R. Parsek. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183: 5395 5401.
32. Heydorn, A.,, B. K. Ersboll,, M. Hentzer,, M. R. Parsek,, M. Givskov,, and S. Molin. 2000. Experimental reproducibility in flow-chamber biofilms. Microbiology 146: 2409 2415.
33. Hitchcock, C. A.,, N. J. Russell,, and K. J. Barrett-Bee. 1987. Sterols in Candida albicans mutants resistant to polyene or azole antifungals, and of a double mutant C. albicans 6.4. Crit. Rev. Microbiol. 15: 111 115.
34. Hodgson, A. E.,, S. M. Nelson,, M. R. W. Brown,, and P. Gilbert. 1995. A simple in vitro model for growth control of bacterial biofilms. J. Appl. Bacteriol. 79: 87 93.
35. Ibrahim, A. S.,, and M. A. Ghannoum. 1996. Chromatographic analysis of lipids, p. 52 79. In R. Prasad (ed.), Manual on Membrane Lipids. Springer-Verlag, New York, N.Y.
36. Kuhn, D. M.,, T. George,, J. Chandra,, P. K. Mukherjee,, and M. A. Ghannoum. 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob. Agents Chemother. 46: 1773 1780.
37. Kumon, H.,, K. Tomochika,, T. Matunaga,, M. Ogawa,, and H. Ohmori. 1994. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol. Immunol. 38: 615 619.
38. Leriche, V.,, and B. Carpentier. 1995. Viable but nonculturable Salmonella typhimurium in single- and binary-species biofilms in response to chlorine treatment. J. Food Prot. 58: 1186 1191.
39. Lindsay, D.,, V. S. Brozel,, J. F. Mostert,, and A. Von Holy. 2002. Differential efficacy of a chlorine dioxide-containing sanitizer agasint single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J. Appl. Microbiol. 92: 352 361.
40. Liu, X.,, F. Roe,, A. Jesaitis,, and Z. Lewandowski. 1998. Resistance of biofilms to the catalase inhibitor 3-amino-1,2,4-triazole. Biotechnol. Bioeng. 59: 156 162.
41. Maira-Litran, T.,, D. G. Allison,, and P. Gilbert. 2000a. An evaluation of the potential of the multiple antibiotic resistance operon ( mar) and the multidrug efflux pump acrAB to moderate resistance towards ciprofloxacin in Escherichia coli biofilms. J. Antimicrob. Chemother. 45: 789 795.
42. Maira-Litran, T.,, D. G. Allison,, and P. Gilbert. 2000b. Expression of the multiple antibiotic resistance operon ( mar) during growth of Escherichia coli as a biofilm. J. Appl. Microbiol. 88: 243 247.
43. Mukherjee, P. K.,, J. Chandra,, D. M. Kuhn,, and M. A. Ghannoum. 2003. Mechanism of drug resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71: 4333 4340.
44. National Committee for Clinical Laboratory Standards. 1997. Reference method for broth dilution antifungal susceptibility testing of yeasts. M-27A. National Committee for Clinical Laboratory Standards, Villanova, Pa.
45. Neu, T. R.,, G. J. Verkerke,, I. F. Herrmann,, H. K. Schutte,, H. C. van der Mei,, and H. J. Busscher. 1994. Microflora on explanted silicone rubber voice prostheses: taxonomy, hydrophobicity and electrophoretic mobility. J. Appl. Bacteriol. 76: 521 528.
46. Nichols, W. W.,, S. M. Dorrington,, M. P. E. Slack,, and H. L. Walmsley. 1988. Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother. 32: 518 523.
47. Parkins, M. D.,, H. Ceri,, and D. G. Storey. 2001. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40: 1215 1226.
48. Radford, D. R.,, and J. R. Radford. 1993. A SEM study of denture plaque and oral mucosa of denture-related stomatitis. J. Dent. 21: 87 93.
49. Ramage, G.,, S. Bachmann,, T. F. Patterson,, B. L. Wickes,, and J. L. Lopez-Ribot. 2002. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J. Antimicrob. Chemother. 49: 973 980.
50. Sanati, H.,, P. Belanger,, R. Fratti,, and M. Ghannoum. 1997. A new triazole, voriconazole (UK-109,496), blocks sterol biosynthesis in Candida albicans and Candida krusei. Antimicrob. Agents Chemother. 41: 2492 2496.
51. Sanderson, S. S.,, and P. S. Stewart. 1997. Evidence of bacterial adaptation to monochloramine in Pseudomonas aeruginosa biofilms and evaluation of biocide action model. Biotechnol. Bioeng. 56: 201 209.
52. Shigeta, M.,, G. Tanaka,, H. Komatsuzawa,, M. Sugai,, H. Suginaka,, and T. Usui. 1997. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43: 340 345.
53. Shih, P.-C.,, and C.-T. Huang. 2002. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. J. Antimicrob. Chemother. 49: 309 314.
54. Spoering, A. L.,, and K. Lewis. 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183: 6746 6751.
55. Srinivasan, R.,, P. S. Stewart,, T. Griebe,, C.-I. Chen,, and X. Xu. 1995. Biofilm parameters influencing biocide efficacy. Biotechnol. Bioeng. 46: 553 560.
56. Sternberg C., , B. B. Christensen, , T. Johansen, , A. T. Nielsen, , J. B. Andersen, , M. Givskov, , and S. Molin. 1999. Distribution of bacterial growth activity in flow-chamber biofilms. Appl. Environ. Microbiol. 65: 4108 4117.
57. Stewart, P. S. 2003. Diffusion in biofilms. J. Bacteriol. 185: 1485 1491.
58. Stewart, P. S.,, J. Rayner,, F. Roe,, and W. M. Rees. 2001 Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J. Appl. Microbiol. 91: 525 532.
59. Stewart, P. S.,, F. Roe,, J. Rayner,, J. G. Elkins,, Z. Lewandowski,, U. A. Ochsner,, and D. J. Hassett. 2000. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 66: 836 838.
60. Stone, G.,, P. Wood,, L. Dixon,, M. Keyhan,, and A. Matin. 2002. Tetracycline rapidly reaches all the constituent cells of uropathogenic Escherichia coli biofilms. Antimicrob. Agents Chemother. 46: 2458 2461.
61. Suci, P.,, M. W. Mittelman,, F. P. Yu,, and G. G. Geesey. 1994. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 38: 2125 2133.
62. Vandenheuvel, F. A.,, and A. S. Court. 1968. Reference high-efficiency nonpolar packed columns for the gas-liquid chromatography of nanogram amounts of steroids. I. Retention time data. J. Chromatogr. 38: 439 459.
63. Walters, M. C.,, F. Roe,, A. Bugnicourt,, M. J. Franklin,, and P. S. Stewart. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to the tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47: 317 323.
64. Wentland, E. J.,, P. S. Stewart,, C.-T. Huang,, and G. A. McFeters. 1996. Spatial variations in growth rate within Klebsiella pneumoniae colonies and biofilm. Biotechnol. Prog. 12: 316 321.
65. Whiteley, M.,, M. G. Bangera,, R. E. Bumgarner,, M. R. Parsek,, G. M. Teitzel,, S. Lory,, and E. P. Greenberg. 2001a. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413: 860 864.
66. Whiteley, M.,, J. R. Ott,, E. A. Weaver,, and R. J. C. McLean. 2001b. Effects of community composition and growth rate on aquifer biofilm bacteria and their susceptibility to betadine disinfection. Environ. Microbiol. 3: 43 52.
67. Xu, K. D.,, M. J. Franklin,, C.-H. Park,, G. A. McFeters,, and P. S. Stewart. 2001. Gene expression and protein levels of the stationary phase sigma factor, RpoS, in continuously-fed Pseudomonas aeruginosa biofilms. FEMS Microbiol. Lett. 199: 67 71.
68. Xu, K. D.,, P. S. Stewart,, F. Xia,, C.-T. Huang,, and G. A. McFeters. 1998. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64: 4035 4039.
69. Zhang, T. C.,, Y.-C. Fu,, and P. L. Bishop. 1995. Competition for substrate and space in biofilms. Water Environ. Res. 67: 992 1003.
70. Zheng, Z.,, and P. S. Stewart. 2002. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 46: 900 903.

Tables

Generic image for table
TABLE 1

Microorganisms shown to exhibit reduced antimicrobial susceptibility in biofilms

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
Generic image for table
TABLE 2

Antimicrobial agents shown to exhibit reduced efficacy against microorganisms in biofilms

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14
Generic image for table
TABLE 3

MICs (iAg/ml) of antifungal agents against biofilms formed by Candida albicans

Citation: Stewart P, Mukherjee P, Ghannoum M. 2004. Biofilm Antimicrobial Resistance, p 250-268. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch14

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