Antifungal activity against Candida biofilms

International Journal of Artificial Organs

Volumn 35, Issue 10, 2012, Pages 780-791

  Iñigo, Melania ^a   Pemán, Javier ^b   Del Pozo, Jose L ^a  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b HOSPITAL UNIVERSITARIO LA FE   (Spain)

Author keywords

Amphotericin B; Azole; Biofilm; Candida; Echinocandin; Foreign body

Indexed keywords

CANDIDA; CELL ADHESION; COMPLEX NETWORKS; YEAST;

AMPHOTERICIN B; ANTIFUNGAL ACTIVITIES; ANTIFUNGALS; AZOLE; BIOFILM FORMATION; CANDIDA SPECIES; ECHINOCANDIN; FOREIGN BODIES; SPATIAL HETEROGENEITY; THREE-DIMENSIONAL ARCHITECTURE;

BIOFILMS;

AMPHOTERICIN; AMPHOTERICIN B; AMPHOTERICIN B LIPID COMPLEX; ANIDULAFUNGIN; ANTIFUNGAL AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; CASPOFUNGIN; ECHINOCANDIN; ERGOSTEROL; FLUCONAZOLE; FLUCYTOSINE; ITRACONAZOLE; KETOCONAZOLE; MICAFUNGIN; NYSTATIN; POSACONAZOLE; RAVUCONAZOLE; SIMVASTATIN; TERBINAFINE; VORICONAZOLE;

ADAPTIVE IMMUNITY; ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; BACTERIAL SURVIVAL; BIOFILM; CANDIDA; CANDIDA ALBICANS; CANDIDA GLABRATA; CANDIDA KRUSEI; CANDIDA METAPSILOSIS; CANDIDA ORTHOPSILOSIS; CANDIDA PARAPSILOSIS; CANDIDA TROPICALIS; CELL ADHESION; DRUG PENETRATION; ENVIRONMENTAL STRESS; FOREIGN BODY; FUNGUS HYPHAE; IN VITRO STUDY; MICROENVIRONMENT; MORTALITY; MYCOSIS; NONHUMAN; QUORUM SENSING; REVIEW; YEAST;

EID: 84870480265     PISSN: 03913988     EISSN: None     Source Type: Journal    
DOI: 10.5301/ijao.5000170     Document Type: Review

References (90)

1. Almirante B, Rodríguez D, Park BJ, et al; Barcelona Candidemia Project Study Group. Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, barcelona, Spain, from 2002 to 2003. J Clin Microbiol. 2005;43(4):1829-1835.
2. Tumbarello M, Posteraro B, Trecarichi EM, et al. Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol. 2007;45(6):1843-1850.
3. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol. 2001;183(18):5385-5394.
4. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 2003;11(1):30-36.
5. Seneviratne CJ, Jin LJ, Samaranayake YH, Samaranayake LP. Cell density and cell aging as factors modulating antifungal resistance of Candida albicans biofilms. Antimicrob Agents Chemother. 2008;52(9):3259-3266.
6. Růzicka F, Holá V, Votava M, Tejkalová R. Importance of biofilm in Candida parapsilosis and evaluation of its susceptibility to antifungal agents by colorimetric method. Folia Microbiol (Praha). 2007;52(3):209-214.
7. El-Azizi MA, Starks SE, Khardori N. Interactions of Candidaalbicans with other Candida spp. and bacteria in the biofilms. J Appl Microbiol. 2004;96(5):1067-1073.
8. Ramage G, Vande Walle K, Wickes BL, López-Ribot JL. Biofilm formation by Candida dubliniensis. J Clin Microbiol. 2001;39(9):3234-3240.
9. Kojic EM, Darouiche RO. Comparison of adherence of Candida albicans and Candida parapsilosis to silicone catheters in vitro and in vivo. Clin Microbiol Infect. 2003;9(7):684-690.
10. Bizerra FC, Nakamura CV, de Poersch C, et al. Characteristics of biofilm formation by Candida tropicalis and antifungal resistance. FEMS Yeast Res. 2008;8(3):442-450.
11. Blankenship JR, Mitchell AP. How to build a biofilm: a fungal perspective. Curr Opin Microbiol. 2006;9(6):588-594.
12. França EJ, Andrade CG, Furlaneto-Maia L, et al. Ultrastructural architecture of colonies of different morphologies produced by phenotypic switching of a clinical strain of Candida tropicalis and biofilm formation by variant phenotypes. Micron. 2011;42(7):726-732.
13. Hornby JM, Jensen EC, Lisec AD, et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol. 2001;67(7):2982-2992.
14. Ramage G, Saville SP, Wickes BL, López-Ribot JL. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol. 2002;68(11): 5459-5463.
15. Deveau A, Hogan DA. Linking quorum sensing regulation and biofilm formation by Candida albicans. Methods Mol Biol. 2011;692:219-233. Es el año 2011.
16. Ferreira JA, Carr JH, Starling CE, de Resende MA, Donlan RM. Biofilm formation and effect of caspofungin on biofilm structure of Candida species bloodstream isolates. Antimicrob Agents Chemother. 2009;53(10):4377-4384.
17. Kuhn DM, Chandra J, Mukherjee PK, Ghannoum MA. Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun. 2002;70(2):878-888.
18. Sun QN, Fang K. [Architecture, influencing factors, and sensitivity to antifungal agents of Candida biofilm] (Article in Chinese). Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2002; 24(4):385-388.
19. Murillo LA, Newport G, Lan CY, Habelitz S, Dungan J, Agabian NM. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell. 2005;4(9):1562-1573.
20. García-Sánchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM, d'Enfert C. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell. 2004;3(2):536-545.
21. Tripathi G, Wiltshire C, Macaskill S, Tournu H, Budge S, Brown AJ. Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J. 2002;21(20):5448-5456.
22. Ramage G, Vande Walle K, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2001;45(9):2475-2479.
23. Baillie GS, Douglas LJ. Iron-limited biofilms of Candida albicans and their susceptibility to amphotericin B. Antimicrob Agents Chemother. 1998;42(8):2146-2149.
24. Chandra J, Mukherjee PK, Leidich SD, et al. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res. 2001;80(3):903-908.
25. Hawser SP, Douglas LJ. Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother. 1995;39(9):2128-2131.
26. Lewis RE, Kontoyiannis DP, Darouiche RO, Raad II, Prince RA. Antifungal activity of amphotericin B, fluconazole, and voriconazole in an in vitro model of Candida catheter-related bloodstream infection. Antimicrob Agents Chemother. 2002; 46(11):3499-3505.
27. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother. 2002;46(6):1773-1780.
28. Ramage G, Bachmann S, Patterson TF, Wickes BL, López- Ribot JL. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother. 2002;49(6):973-980.
29. Bachmann SP, VandeWalle K, Ramage G, et al. In vitro activity of caspofungin against Candida albicans biofilms. Antimicrob Agents Chemother. 2002;46(11):3591-3596.
30. Gilbert P, Maira-Litran T, McBain AJ, Rickard AH, Whyte FW. The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol. 2002;46:202-256.
31. Al-Fattani MA, Douglas LJ. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol. 2006;55(Pt 8):999-1008.
32. Mukherjee PK, Chandra J. Candida biofilm resistance. Drug Resist Updat. 2004;7(4/5):301-309.
33. Kumamoto CA. Candida biofilms. Curr Opin Microbiol. 2002;5(6):608-611.
34. Al-Fattani MA, Douglas LJ. Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother. 2004;48(9):3291-3297.
35. Martins M, Uppuluri P, Thomas DP, et al. Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia. 2010;169(5):323-331.
36. Montanaro L, Poggi A, Visai L, et al. Extracellular DNA in biofilms. Int J Artif Organs. 2011;34(9):824-831.
37. Martins M, Henriques M, Lopez-Ribot JL, Oliveira R. Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses. 2012;55(1):80-85.
38. Robbins N, Uppuluri P, Nett J, et al. Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog. 2011;7(9):e1002257.
39. Baillie GS, Douglas LJ. Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother. 1998;42(8):1900-1905.
40. Cuellar-Cruz M, Vega-Gonzalez A, Mendoza-Novelo B, Lopez-Romero E, Ruiz-Baca E, Quintanar-Escorza MA, et al. The effect of biomaterials and antifungals on biofilm formation by Candida species: a review. Eur J Clin Microbiol Infect Dis. 2012;31(10):2513-2527.
41. Ramage G, Vandewalle K, Wickes BL, López-Ribot JL. Characteristics of biofilm formation by Candida albicans. Rev Iberoam Micol. 2001;18(4):163-170.
42. Niimi K, Maki K, Ikeda F, et al. Overexpression of Candida albicans CDR1, CDR2, or MDR1 does not produce significant changes in echinocandin susceptibility. Antimicrob Agents Chemother. 2006;50(4):1148-1155.
43. Stewart PS. New ways to stop biofilm infections. Lancet. 2003;361(9352):97.
44. LaFleur MD, Kumamoto CA, Lewis K. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother. 2006;50(11):3839-3846.
45. Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev. 1999;12(4):501-517.
46. Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49(3):253-262.
47. Nweze EI, Ghannoum A, Chandra J, Ghannoum MA, Mukherjee PK. Development of a 96-well catheter-based microdilution method to test antifungal susceptibility of Candida biofilms. J Antimicrob Chemother. 2012;67(1): 149-153.
48. Kaneko Y, Ohno H, Fukazawa H, et al. Anti-Candida-biofilm activity of micafungin is attenuated by voriconazole but restored by pharmacological inhibition of Hsp90-related stress responses. Med Mycol. 2010;48(4):606-612.
49. Shuford JA, Piper KE, Steckelberg JM, Patel R. In vitro biofilm characterization and activity of antifungal agents alone and in combination against sessile and planktonic clinical Candida albicans isolates. Diagn Microbiol Infect Dis. 2007;57(3):277-281.
50. Seidler M, Salvenmoser S, Müller FM. Liposomal amphotericin B eradicates Candida albicans biofilm in a continuous catheter flow model. FEMS Yeast Res. 2010;10(4):492-495.
51. Uppuluri P, Srinivasan A, Ramasubramanian A, Lopez-Ribot JL. Effects of fluconazole, amphotericin B, and caspofungin on Candida albicans biofilms under conditions of flow and on biofilm dispersion. Antimicrob Agents Chemother. 2011;55(7):3591-3593.
52. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun. 2003;71(8):4333-4340.
53. Nailis H, Vandenbosch D, Deforce D, Nelis HJ, Coenye T. Transcriptional response to fluconazole and amphotericin B in Candida albicans biofilms. Res Microbiol. 2010;161(4): 284-292.
54. Katragkou A, Chatzimoschou A, Simitsopoulou M, et al. Differential activities of newer antifungal agents against Candida albicans and Candida parapsilosis biofilms. Antimicrob Agents Chemother. 2008;52(1):357-360.
55. DiDone L, Oga D, Krysan DJ. A novel assay of biofilm antifungal activity reveals that amphotericin B and caspofungin lyse Candida albicans cells in biofilms. Yeast. 2011;28(8): 561-568.
56. Cateau E, Rodier MH, Imbert C. In vitro efficacies of caspofungin or micafungin catheter lock solutions on Candida albicans biofilm growth. J Antimicrob Chemother. 2008;62(1): 153-155.
57. Del Pozo JL, Francés ML, Hernáez S, Serrera A, Alonso M, Rubio MF. Effect of amphotericin B alone or in combination with rifampicin or clarithromycin against Candida species biofilms. Int J Artif Organs. 2011;34(9):766-770.
58. Toulet D, Debarre C, Imbert C. Could liposomal amphotericin B (L-AMB) lock solutions be useful to inhibit Candida spp. biofilms on silicone biomaterials? J Antimicrob Chemother. 2012;67(2):430-432.
59. Ramage G, VandeWalle K, Bachmann SP, Wickes BL, López-Ribot JL. In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob Agents Chemother. 2002;46(11):3634-3636.
60. Lazzell AL, Chaturvedi AK, Pierce CG, Prasad D, Uppuluri P, Lopez-Ribot JL. Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis. J Antimicrob Chemother. 2009;64(3):567-570.
61. Arciola CR, Montanaro L, Costerton JW. New trends in diagnosis and control strategies for implant infections. Int J Artif Organs. 2011;34(9):727-736.
62. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials. 2012; 33(26):5967-5982.
63. Tobudic S, Kratzer C, Lassnigg A, Graninger W, Presterl E. In vitro activity of antifungal combinations against Candida albicans biofilms. J Antimicrob Chemother. 2010;65(2): 271-274.
64. Bachmann SP, Ramage G, VandeWalle K, Patterson TF, Wickes BL, López-Ribot JL. Antifungal combinations against Candida albicans biofilms in vitro. Antimicrob Agents Chemother. 2003;47(11):3657-3659.
65. Alves IA, Bandeira LA, Mario DA, et al. Effects of antifungal agents alone and in combination against Candida glabrata strains susceptible or resistant to fluconazole. Mycopathologia. 2012;174(3):215-221.
66. Vogel M, Hartmann T, Köberle M, Treiber M, Autenrieth IB, Schumacher UK. Rifampicin induces MDR1 expression in Candida albicans. J Antimicrob Chemother. 2008;61(3): 541-547.
67. Edwards JE Jr, Morrison J, Henderson DK, Montgomerie JZ. Combined effect of amphotericin B and rifampin on Candida species. Antimicrob Agents Chemother. 1980;17(3):484-487.
68. Arroyo J, Medoff G, Kobayashi GS. Therapy of murine aspergillosis with amphotericin B in combination with rifampin of 5-fluorocytosine. Antimicrob Agents Chemother. 1977;11(1):21-25.
69. Deren YT, Ozdek S, Kalkanci A, Akyürek N, Hasanreisoǧlu B. Comparison of antifungal efficacies of moxifloxacin, liposomal amphotericin B, and combination treatment in experimental Candida albicans endophthalmitis in rabbits. Can J Microbiol. 2010;56(1):1-7.
70. Yalçin B, Kalkanci A, Gürelik F, Fidan I, Kustimur S, Ozdek S. [In vitro synergistic effect of moxifloxacin and amphotericin B combination against Candida strains]. Mikrobiyol Bul. 2010;44(1):65-70.
71. Stergiopoulou T, Meletiadis J, Sein T, et al. Comparative pharmacodynamic interaction analysis between ciprofloxacin, moxifloxacin and levofloxacin and antifungal agents against Candida albicans and Aspergillus fumigatus. J Antimicrob Chemother. 2009;63(2):343-348.
72. El-Azizi M. Enhancement of the in vitro activity of amphotericin B against the biofilms of non-albicans Candida spp. by rifampicin and doxycycline. J Med Microbiol. 2007;56 (Pt 5):645-649.
73. Liu G, Vellucci VF, Kyc S, Hostetter MK. Simvastatin inhibits Candida albicans biofilm in vitro. Pediatr Res. 2009;66(6):600-604.
74. Balestrino D, Souweine B, Charbonnel N, et al. Eradication of microorganisms embedded in biofilm by an ethanol-based catheter lock solution. Nephrol Dial Transplant. 2009;24(10):3204-3209.
75. Stepanović S, Vuković D, Jesić M, Ranin L. Influence of acetylsalicylic acid (aspirin) on biofilm production by Candida species. J Chemother. 2004;16(2):134-138.
76. Zhou Y, Wang G, Li Y, et al. In vitro interactions between aspirin and amphotericin B against planktonic cells and biofilm cells of Candida albicans and C. parapsilosis. Antimicrob Agents Chemother. 2012;56(6):3250-3260.
77. Ricardo E, Costa-de-Oliveira S, Dias AS, Guerra J, Rodrigues AG, Pina-Vaz C. Ibuprofen reverts antifungal resistance on Candida albicans showing overexpression of CDR genes. FEMS Yeast Res. 2009;9(4):618-625.
78. Pulcrano G, Panellis D, De Domenico G, Rossano F, Catania MR. Ambroxol influences voriconazole resistance of Candida parapsilosis biofilm. FEMS Yeast Res. 2012;12(4):430-438.
79. Jabra-Rizk MA, Shirtliff M, James C, Meiller T. Effect of farnesol on Candida dubliniensis biofilm formation and fluconazole resistance. FEMS Yeast Res. 2006;6(7): 1063-1073.
80. Yu LH, Wei X, Ma M, Chen XJ, Xu SB. Possible inhibitory molecular mechanism of farnesol on the development of fluconazole resistance in Candida albicans biofilm. Antimicrob Agents Chemother. 2012;56(2):770-775.
81. Harrison JJ, Turner RJ, Ceri H. A subpopulation of Candida albicans and Candida tropicalis biofilm cells are highly tolerant to chelating agents. FEMS Microbiol Lett. 2007;272(2):172-181.
82. Raad II, Hachem RY, Hanna HA, et al. Role of ethylene diamine tetra-acetic acid (EDTA) in catheter lock solutions: EDTA enhances the antifungal activity of amphotericin B lipid complex against Candida embedded in biofilm. Int J Antimicrob Agents. 2008;32(6):515-518.
83. Enjalbert B, Whiteway M. Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell. 2005;4(7): 1203-1210.
84. Zhai B, Zhou H, Yang L, et al. Polymyxin B, in combination with fluconazole, exerts a potent fungicidal effect. J Antimicrob Chemother. 2010;65(5):931-938.
85. Chandra J, Patel JD, Li J, et al. Modification of surface properties of biomaterials influences the ability of Candida albicans to form biofilms. Appl Environ Microbiol. 2005;71(12):8795-8801.
86. Nobile CJ, Mitchell AP. Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol. 2006;8(9):1382-1391.
87. Nobile CJ, Schneider HA, Nett JE, et al. Complementary adhesin function in C. albicans biofilm formation. Curr Biol. 2008;18(14):1017-1024.
88. Norice CT, Smith FJ Jr, Solis N, Filler SG, Mitchell AP. Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot Cell. 2007;6(11):2046-2055.
89. Tobudic S, Kratzer C, Lassnigg A, Willinger B, Graninger W, Presterl E. Biofilm formation of Candida spp. isolates from patients at a cardiothoracic intensive care unit. Int J Artif Organs. 2011;34(9):818-823.
90. Aslam S, Darouiche RO. Role of antibiofilm-antimicrobial agents in controlling device-related infections. J Artif Organs. 2011;34(9):752-758.