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Chapter 14 : Biofilm Antimicrobial Resistance
Authors:
Philip S. Stewart1,
Pranab K. Mukherjee2,
Mahmoud A. Ghannoum3
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Affiliations:
1: Center for Biofilm Engineering, Montana State University–Bozeman, Bozeman, Montana 59717- 3980;
2: Center for Medical Mycology, Department of Dermatology, University Hospitals of Cleveland and Case Western Reserve University, Cleveland, Ohio 44106;
3: Center for Medical Mycology, Department of Dermatology, University Hospitals of Cleveland and Case Western Reserve University, Cleveland, Ohio 44106
Content Type: Monograph
Publication Year:
2004
Category: Environmental Microbiology; Microbial Genetics and Molecular Biology
Book DOI:
10.1128/9781555817718
Chapter DOI:
10.1128/9781555817718.ch14
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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 Candida albicans 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
Figures
Biofilm Antimicrobial Resistance
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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
/content/10.1128/9781555817718.chap14.fig14-1
FIGURE 1
Comparison of biofilm (●) and planktonic (○) killing by antimicrobial agents. (A) S. epidermidis challenged with 0.1 μg of rifampin per ml (from Zheng and Stewart, 2002 ). (B) P. aeruginosa challenged with 50 mg of glutaraldehyde per liter (reprinted from Grobe et al., 2002, with permission from Springer Verlag ). (C) P. aeruginosa challenged with 10 μg of tobramycin per ml (from Walters et al., 2003 ).
10.1128/9781555817718/fig14-1_thmb.gif
10.1128/9781555817718/fig14-1.gif
FIGURE 1
Comparison of biofilm (●) and planktonic (○) killing by antimicrobial agents. (A) S. epidermidis challenged with 0.1 μg of rifampin per ml (from Zheng and Stewart, 2002 ). (B) P. aeruginosa challenged with 50 mg of glutaraldehyde per liter (reprinted from Grobe et al., 2002, with permission from Springer Verlag ). (C) P. aeruginosa challenged with 10 μg of tobramycin per ml (from Walters et al., 2003 ).
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
/content/10.1128/9781555817718.chap14.fig14-2
FIGURE 2
Correlation of biofilm development and metabolic activity with antifungal resistance Antifungal susceptibility of C. albicans 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 C. albicans 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 Journal of Bacteriology ( Chandra et al., 2001a ).
10.1128/9781555817718/fig14-2_thmb.gif
10.1128/9781555817718/fig14-2.gif
FIGURE 2
Correlation of biofilm development and metabolic activity with antifungal resistance Antifungal susceptibility of C. albicans 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 C. albicans 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 Journal of Bacteriology ( Chandra et al., 2001a ).
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
/content/10.1128/9781555817718.chap14.fig14-3
FIGURE 3
Effect of amphotericin B (a), flucytosine (b), and fluconazole (c) on C. albicans biofilms grown statically (●) or with gentle shaking (○). [3H]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.
10.1128/9781555817718/fig14-3_thmb.gif
10.1128/9781555817718/fig14-3.gif
FIGURE 3
Effect of amphotericin B (a), flucytosine (b), and fluconazole (c) on C. albicans biofilms grown statically (●) or with gentle shaking (○). [3H]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
/content/10.1128/9781555817718.chap14.fig14-4
FIGURE 4
Effect of amphotericin B on C. albicans biofilms grown statically (a) or with shaking (b) on PVC discs cut from Faucher tubes (Vygon) (●) or vena cava catheters ( Jostra) (○). [3H]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.
10.1128/9781555817718/fig14-4_thmb.gif
10.1128/9781555817718/fig14-4.gif
FIGURE 4
Effect of amphotericin B on C. albicans biofilms grown statically (a) or with shaking (b) on PVC discs cut from Faucher tubes (Vygon) (●) or vena cava catheters ( Jostra) (○). [3H]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
/content/10.1128/9781555817718.chap14.fig14-5
FIGURE 5
Variations of sterol profile of C. albicans 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 C. albicans 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 Infection and Immunity ( Mukherjee et al., 2003 ).
10.1128/9781555817718/fig14-5_thmb.gif
10.1128/9781555817718/fig14-5.gif
FIGURE 5
Variations of sterol profile of C. albicans 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 C. albicans 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 Infection and Immunity ( Mukherjee et al., 2003 ).
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
/content/10.1128/9781555817718.chap14.fig14-6
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 Applied and Environmental Microbiology ( de Beer et al., 1994a ).
10.1128/9781555817718/fig14-6_thmb.gif
10.1128/9781555817718/fig14-6.gif
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 Applied and Environmental Microbiology ( de Beer et al., 1994a ).
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
/content/10.1128/9781555817718.chap14.fig14-7
FIGURE 7
Induction of catalase in biofilms (●) and planktonic cells (○) of P. aeruginosa 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 Applied and Environmental Microbiology ( Elkins et al., 1999 ).
10.1128/9781555817718/fig14-7_thmb.gif
10.1128/9781555817718/fig14-7.gif
FIGURE 7
Induction of catalase in biofilms (●) and planktonic cells (○) of P. aeruginosa 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 Applied and Environmental Microbiology ( Elkins et al., 1999 ).
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
References
/content/book/10.1128/9781555817718.chap14
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
Biofilm Antimicrobial Resistance
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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
/content/10.1128/9781555817718.chap14.tab14-1
TABLE 1
Microorganisms shown to exhibit reduced antimicrobial susceptibility in biofilms
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
/content/10.1128/9781555817718.chap14.tab14-2
TABLE 2
Antimicrobial agents shown to exhibit reduced efficacy against microorganisms in biofilms
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
/content/10.1128/9781555817718.chap14.tab14-3
TABLE 3
MICs (iAg/ml) of antifungal agents against biofilms formed by Candida albicans
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