Fusarium and Candida albicans biofilms on soft contact lenses: Model development, influence of lens type, and susceptibility to lens care solutions

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 1, 2008, Pages 171-182

  Imamura, Yoshifumi ^a   Chandra, Jyotsna ^a   Mukherjee, Pranab K ^a   Lattif, Ali Abdul ^a   Szczotka Flynn, Loretta B ^a   Pearlman, Eric ^a   Lass, Jonathan H ^a   O'Donnell, Kerry ^b   Ghannoum, Mahmoud A ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAFILCON A; BALAFILCON A; BIOMEDICAL AND DENTAL MATERIALS; CONTACT LENS SOLUTION; ETAFILCON A; GALYFILCON A; LOTRAFILCON A; POLYMACON; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CANDIDA ALBICANS; DISEASE MODEL; FUNGAL STRAIN; FUNGUS HYPHAE; FUNGUS ISOLATION; FUSARIUM; KERATOMYCOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHYLOGENY; PRIORITY JOURNAL; SOFT CONTACT LENS; SPECIES DIFFERENCE; TIME;

BIOFILMS; CANDIDA ALBICANS; CONTACT LENS SOLUTIONS; CONTACT LENSES, HYDROPHILIC; CULTURE MEDIA; FUSARIUM; HUMANS; KERATITIS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; POLYMERS; SEQUENCE ANALYSIS, DNA;

EID: 37849029477     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00387-07     Document Type: Article

References (51)

1. Adler, D. E., T. H. Milhorat, and J. I. Miller. 1998. Treatment of rhinocerebral mucormycosis with intravenous, interstitial, and cerebrospinal fluid administration of amphotericin B: case report. Neurosurgery 42:644-648.
2. Agarwal, A., A. Gupta, V. Sakhuja, P. Talwar, K. Joshi, and K. S. Chugh. 1991. Retinitis following disseminated cryptococcosis in a renal allograft recipient. Efficacy of oral fluconazole. Acta Ophthalmol. (Copenhagen) 69: 402-405.
3. Agrawal, V., J. Biswas, H. N. Madhavan, G. Mangat, M. K. Reddy, J. S. Saini, S. Sharma, and M. Srinivasan. 1994. Current perspectives in infectious keratitis. Ind. J. Ophthalmol. 42:171-192.
4. Ahearn, D. G., R. B. Simmons, S. Zhang, R. D. Stulting, S. A. Crow, B. L. Schwam, and G. E. Pierce. 2007. Attachment to and penetration of conventional and silicone hydrogel contact lenses by Fusarium solani and Ulocladium sp. in vitro. Cornea 26:831-839.
5. Ajayi, B. G., B. Osuntokun, O. Olurin, O. O. Kale, and T. A. Junaid. 1986. Orbital histoplasmosis due to Histoplasma capsulatum var. duboisii: successful treatment with Septrin. J. Trop. Med. Hyg. 89:179-187.
6. Alfonso, E. C., J. Cantu-Dibildox, W. M. Munir, D. Miller, T. P. O'Brien, C. L. Karp, S. H. Yoo, R. K. Forster, W. W. Culbertson, K. Donaldson, J. Rodila, and Y. Lee. 2006. Insurgence of Fusarium keratitis associated with contact lens wear. Arch. Ophthalmol. 124:941-947.
7. Bachmann, S. P., G. Ramage, K. VandeWalle, T. F. Patterson, B. L. Wickes, and J. L. Lopez-Ribot. 2003. Antifungal combinations against Candida albicans biofilms in vitro. Antimicrob. Agents Chemother. 47:3657-3659.
8. Baillie, G. S., and L. J. Douglas. 1999. Candida biofilms and their susceptibility to antifungal agents. Methods Enzymol. 310:644-656.
9. Banin, E., K. M. Brady, and E. P. Greenberg. 2006. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72:2064-2069.
10. Beattie, T. K., A. Tomlinson, A. K. McFadyen, D. V. Seal, and A. M. Grimason. 2003. Enhanced attachment of acanthamoeba to extended-wear silicone hydrogel contact lenses: a new risk factor for infection? Ophthalmology 110:765-771.
11. Burn, A. K., K. A. VandeWalle, J. L. Lopez-Ribot, W. R. Kirkpatrick, B. J. Coco, T. F. Patterson, and S. W. Redding. 2004. Mixed biofilm formation by Candida albicans and C. glabrata, abstr. 0334. Presented at the IADR/AADR/CADR 82nd General Session Conference, 10 to 13 March 2004, Honolulu, HI.
12. Cavanagh, H. D. 2006. Fusarium, contact lens solutions, and patient compliance: a tangled, critical web. Eye Contact Lens 32:255.
13. Chandra, J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick, and M. A. Ghannoum. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183: 5385-5394.
14. Chandra, J., P. K. Mukherjee, S. D. Leidich, F. F. Faddoul, L. L. Hoyer, L. J. Douglas, and M. A. Ghannoum. 2001. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J. Dent. Res. 80:903-908.
15. Chandra, J., J. D. Patel, J. Li, G. Zhou, P. K. Mukherjee, T. S. McCormick, J. M. Anderson, and M. A. Ghannoum. 2005. Modification of surface properties of biomaterials influences the ability of C. albicans to form biofilms. Appl. Environ. Microbiol. 71:8795-8801.
16. Chang, D. C., G. B. Grant, K. O'Donnell, K. A. Wannemuehler, J. Noble-Wang, C. Y. Rao, L. M. Jacobson, C. S. Crowell, R. S. Sneed, F. M. T. Lewis, J. K. Schaffzin, M. A. Kainer, C. A. Genese, E. C. Alfonso, D. B. Jones, A. Srinivasan, S. K. Fridkin, and B. J. Park for the Fusarium Keratitis Investigation Team. 2006. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. JAMA 296:953-963.
17. Distel, J. W., J. F. Hatton, and M. J. Gillespie. 2002. Biofilm formation in medicated root canals. J. Endod. 28:689-693.
18. Donnio, A., D. N. G. Van Nuoi, M. Catanese, N. Desbois, L. Ayeboua, and H. Merle. 2007. Outbreak of keratomycosis attributable to Fusarium solani in the French West Indies. Am. J. Ophthalmol. 143:356-358.
19. Dyavaiah, M., R. Ramani, D. Chu, D. Ritterband, M. Shah, W. Samsonoff, S. Chaturvedi, and V. Chaturvedi. 2007. Molecular characterization, biofilm analysis and experimental biofouling study of Fusarium isolates from recent cases of fungal keratitis in New York State. BMC Ophthalmol. 7:1.
20. Elder, M. J., F. Stapleton, E. Evans, and J. K. Dart. 1995. Biofilm-related infections in ophthalmology. Eye 9:102-109.
21. Evans, E., and J. K. Dart. 1995. Efficacy of contact lens disinfecting solutions on Pseudomonas aeruginosa biofilms growing on contact lens storage case plastics. Investig. Ophthalmol. Vis. Sci. 36:4714.
22. Ghannoum, M. A., and S. S. Radwan. 1990. Candida adherence to epithelial cells. CRC Press, Boca Raton, FL.
23. Hawser, S. P., and L. J. Douglas. 1994. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect. Immun. 62:915-921.
24. International Organization for Standardization. 2001. ISO 14729. Ophthalmic optics - contact lens products - microbial requirements and test method for products and regimes for hygienic management of contact lenses. International Organization for Standardization, Geneva, Switzerland.
25. Iyer, S. A., S. S. Tuli, and R. C. Wagoner. 2006. Fungal keratitis: emerging trends and treatment outcomes. Eye Contact Lens 32:267-271.
26. Jeng, B. H., G. S. Hall, L. Schoenfield, and D. M. Meisler. 2007. The Fusarium keratitis outbreak: not done yet? Arch. Ophthalmol. 125:981-983.
27. Jin, Y., L. P. Samaranayake, Y. Samaranayake, and H. K. Yip. 2004. Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch. Oral Biol. 49:789-798.
28. Jin, Y., H. K. Yip, Y. H. Samaranayake, J. Y. Yau, and L. P. Samaranayake. 2003. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage in cases of human immunodeficiency virus infection. J. Clin. Microbiol. 41:2961-2967.
29. Khor, W. B., T. Aung, S. M. Saw, T. Y. Wong, P. A. Tambyah, A. L. Tan, R. Beuerman, L. Lim, W. K. Chan, W. J. Heng, J. Lim, R. S. Loh, S. B. Lee, and D. T. Tan. 2006. An outbreak of Fusarium keratitis associated with contact lens wear in Singapore. JAMA 295:2867-2873.
30. Khot, P. D., P. A. Suci, R. L. Miller, R. D. Nelson, and B. J. Tyler. 2006. A small subpopulation of blastospores in Candida albicans biofilms exhibit resistance to amphotericin B associated with differential regulation of ergosterol and β-1,6-glucan pathway genes. Antimicrob. Agents Chemother. 50: 3708-3716.
31. Kuhn, D. M., J. Chandra, P. K. Mukherjee, and M. A. Ghannoum. 2002. Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect. Immun. 70:878-888.
32. 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.
33. Lakkis, C., and S. M. Fleiszig. 2001. Resistance of Pseudomonas aeruginosa isolates to hydrogel contact lens disinfection correlates with cytotoxic activity. J. Clin. Microbiol. 39:1477-1486.
34. Margolis, T. P., and J. P. Whitcher. 2006. Fusarium - a new culprit in the contact lens case. JAMA 296:985-987.
35. Martinez, L. R., and A. Casadevall. 2005. Specific antibody can prevent fungal biofilm formation, and this effect correlates with protective efficacy. Infect. Immun. 73:6350-6362.
36. May, L. L., M. M. Gabriel, R. B. Simmons, L. A. Wilson, and D. G. Ahearn. 1995. Resistance of adhered bacteria to rigid gas permeable contact lens solutions. CLAO J. 21:242-246.
37. McLaughlin-Borlace, L., F. Stapleton, M. Matheson, and J. K. Dart. 1998. Bacterial biofilm on contact lenses and lens storage cases in wearers with microbial keratitis. J. Appl. Microbiol. 84:827-838.
38. Meshulam, T., S. M. Levitz, L. Christin, and R. D. Diamond. 1995. A simplified new assay for assessment of fungal cell damage with the tetrazolium dye, (2,3)-bis-(2-methoxy-4-nitro-5-sulphenyl)-(2H)-tetrazolium-5-carboxanil ide (XTT). J. Infect. Dis. 172:1153-1156.
39. O'Donnell, K., B. A. J. Sarver, M. Brandt, D. C. Chang, J. Noble-Wang, B. J. Park, D. A. Sutton, L. Benjamin, M. Lindsley, A. Padhye, D. M. Geiser, and T. J. Ward. 2007. Phylogenetic diversity and microsphere array-based genotyping of human pathogenic fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J. Clin. Microbiol. 45:2235-2248.
40. O'Donnell, K., D. A. Sutton, M. G. Rinaldi, K. C. Magnon, P. A. Cox, S. G. Revankar, S. Sanche, D. M. Geiser, J. H. Juba, J. A. van Burik, A. Padhye, E. J. Anaissie, A. Francesconi, T. J. Walsh, and J. S. Robinson. 2004. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. J. Clin. Microbiol. 42:5109-5120.
41. Okajima, Y., S. Kobayakawa, A. Tsuji, and T. Tochikubo. 2006. Biofilm formation by Staphylococcus epidermidis on intraocular lens material. Investig. Ophthalmol. Vis. Sci. 47:2971-2975.
42. Perumal, P., S. Mekala, and W. L. Chaffin. 2007. Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob. Agents Chemother. 51:2454-2463.
43. Picioreanu, C., M. C. van Loosdrecht, and J. J. Heijnen. 1998. Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol. Bioeng. 58:101-116.
44. Picioreanu, C., M. C. van Loosdrecht, and J. J. Heijnen. 2001. Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnol. Bioeng. 72:205-218.
45. Shimizu, K., S. Kobayakawa, A. Tsuji, and T. Tochikubo. 2006. Biofilm formation on hydrophilic intraocular lens material. Curr. Eye Res. 31:989-997.
46. Simmons, R. B., J. R. Buffington, M. Ward, L. A. Wilson, and D. G. Ahearn. 1986. Morphology and ultrastructure of fungi in extended-wear soft contact lenses. J. Clin. Microbiol. 24:21-25.
47. Thomas, P. A. 2003. Current perspectives on ophthalmic mycoses. Clin. Microbiol. Rev. 16:730-797.
48. U.S. Department of Health and Human Services. 1997. Premarket notification [510(k)] guidance document for contact lens care products. Center for Devices and Radiological Health, Washington, DC.
49. Wilson, L. A., A. D. Sawant, and D. G. Ahearn. 1991. Comparative efficacies of soft contact lens disinfectant solutions against microbial films in lens cases. Arch. Ophthalmol. 109:1155-1157.
50. Zegans, M. E., H. I. Becker, J. Budzik, and G. O'Toole. 2002. The role of bacterial biofilms in ocular infections. DNA Cell Biol. 21:415-420.
51. Zhang, N., K. O'Donnell, D. A. Sutton, F. A. Nalim, R. C. Summerbell, A. A. Padhye, and D. M. Geiser. 2006. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J. Clin. Microbiol. 44:2186-2190.