Abstract
Fungal biofilms are an important clinical problem. A number of factors including the increasing use of indwelling medical devices wider prescription of broad spectrum antibiotics and an aging and more immuno-compromised patient population has combined to create an opportunity for yeasts and moulds to cause infection. It is also becoming increasingly clear that for a number of serious infections the development of a fungal biofilm is important in the pathophysiology of the infection.
This chapter will discuss the importance of fungal biofilms in different anatomical areas, will try to provide insights into how fungal biofilm infection should be diagnosed and treated and provide an explanation as to why biofilms may be difficult to treat effectively with routine antifungal regimens.
Finally it will discuss how our current level of knowledge of the development and biology of fungal biofilms may, in future, lead to a wider choice of therapeutic interventions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Agirbasli H, Bilgen H, Ozcan SK, Otlu B, Sinik G et al (2008) Two possible cases of Trichosporon infections in bone-marrow-transplanted children: the first case of T. japonicum isolated from clinical specimens. Jpn J Infect Dis 61:130–132
Ajesh K, Sreejith K (2012) Cryptococcus laurentii biofilms: structure, development and antifungal drug resistance. Mycopathologia 174:409–419
Amin R, Dupuis A, Aaron SD, Ratjen F (2010) The effect of chronic infection with Aspergillus fumigatus on lung function and hospitalization in patients with cystic fibrosis. Chest 137:171–176
Anaissie EJ, Stratton SL, Dignani MC, Lee CK, Mahfouz TH et al (2002) Cleaning patient shower facilities: a novel approach to reducing patient exposure to aerosolized Aspergillus species and other opportunistic molds. Clin Infect Dis 35:E86–E88
Andes D, Nett J, Oschel P, Albrecht R, Marchillo K et al (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72:6023–6031
Andes DR, Safdar N, Baddley JW, Playford G, Reboli AC et al (2012) Impact of treatment strategy on outcomes in patients with candidemia and other forms of invasive candidiasis: a patient-level quantitative review of randomized trials. Clin Infect Dis 54:1110–1122
Angel-Moreno A, Boronat M, Bolanos M, Carrillo A, Gonzalez S et al (2005) Candida glabrata fungemia cured by antibiotic-lock therapy: case report and short review. J Infect 51:e85–e87
Ariani N, Vissink A, van Oort RP, Kusdhany L, Djais A et al (2012) Microbial biofilms on facial prostheses. Biofouling 28:583–591
Arnow PM, Kushner R (1991) Malassezia furfur catheter infection cured with antibiotic lock therapy. Am J Med 90:128–130
Arslan SG, Akpolat N, Kama JD, Ozer T, Hamamci O (2008) One-year follow-up of the effect of fixed orthodontic treatment on colonization by oral Candida. J Oral Pathol Med 37:26–29
Bachmann SP, VandeWalle K, Ramage G, Patterson TF, Wickes BL et al (2002) In vitro activity of caspofungin against Candida albicans biofilms. Antimicrob Agents Chemother 46:3591–3596
Bakaletz LO (2007) Bacterial biofilms in otitis media: evidence and relevance. Pediatr Infect Dis J 26:S17–S19
Bamford CV, d’Mello A, Nobbs AH, Dutton LC, Vickerman MM et al (2009) Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect Immun 77:3696–3704
Bandara HM, Yau JY, Watt RM, Jin LJ, Samaranayake LP (2009) Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation. J Med Microbiol 58:1623–1631
Banerjee U, Gupta K, Venugopal P (1997) A case of prosthetic valve endocarditis caused by Cryptococcus neoformans var. neoformans. J Med Vet Mycol 35:139–141
Bauters TG, Moerman M, Pini G, Vermeersch H, Nelis HJ (2001) Colonization of a voice prosthesis by Cryptococcus neoformans. Med Mycol 39:379–381
Beikler T, Flemmig TF (2011) Oral biofilm-associated diseases: trends and implications for quality of life, systemic health and expenditures. Periodontol 2000 55:87–103
Benoit JL, Carandang G, Sitrin M, Arnow PM (1995) Intraluminal antibiotic treatment of central venous catheter infections in patients receiving parenteral nutrition at home. Clin Infect Dis 21:1286–1288
Berkowitz ID, Robboy SJ, Karchmer AW, Kunz LJ (1979) Torulopsis glabrata fungemia – a clinical pathological study. Medicine (Baltimore) 58:430–440
Blackwood RA, Klein KC, Micel LN, Willers ML, Mody RJ et al (2011) Ethanol locks therapy for resolution of fungal catheter infections. Pediatr Infect Dis J 30:1105–1107
Blyth CC, Middleton PG, Harun A, Sorrell TC, Meyer W et al (2010) Clinical associations and prevalence of Scedosporium spp. in Australian cystic fibrosis patients: identification of novel risk factors? Med Mycol 48(Suppl 1):S37–S44
Boase S, Valentine R, Singhal D, Tan LW, Wormald PJ (2011) A sheep model to investigate the role of fungal biofilms in sinusitis: fungal and bacterial synergy. Int Forum Allergy Rhinol 1:340–347
Boland JM, Chung HH, Robberts FJ, Wilson WR, Steckelberg JM et al (2011) Fungal prosthetic valve endocarditis: Mayo Clinic experience with a clinicopathological analysis. Mycoses 54:354–360
Bonhomme J, Chauvel M, Goyard S, Roux P, Rossignol T et al (2011) Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol Microbiol 80:995–1013
Branski LK, Al-Mousawi A, Rivero H, Jeschke MG, Sanford AP et al (2009) Emerging infections in burns. Surg Infect (Larchmt) 10:389–397
Braun DK, Janssen DA, Marcus JR, Kauffman CA (1994) Cryptococcal infection of a prosthetic dialysis fistula. Am J Kidney Dis 24:864–867
Buckler BS, Sams RN, Goei VL, Krishnan KR, Bemis MJ et al (2008) Treatment of central venous catheter fungal infection using liposomal amphotericin-B lock therapy. Pediatr Infect Dis J 27:762–764
Buijssen KJ, van der Laan BF, van der Mei HC, Atema-Smit J, van den Huijssen P et al (2012) Composition and architecture of biofilms on used voice prostheses. Head Neck 34:863–871
Canabarro A, Valle C, Farias MR, Santos FB, Lazera M et al (2012) Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res 48:428–432
Cannizzo FT, Eraso E, Ezkurra PA, Villar-Vidal M, Bollo E et al (2007) Biofilm development by clinical isolates of Malassezia pachydermatis. Med Mycol 45:357–361
Carlson E (1982) Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality. Infect Immun 38:921–924
Caserta RA, Marra AR, Durao MS, Silva CV, Pavao Dos Santos OF et al (2012) A program for sustained improvement in preventing ventilator associated pneumonia in an intensive care setting. BMC Infect Dis 12:234
Castagnola E, Marazzi MG, Tacchella A, Giacchino R (2005) Broviac catheter-related candidemia. Pediatr Infect Dis J 24:747
Cateau E, Rodier MH, Imbert C (2008) In vitro efficacies of caspofungin or micafungin catheter lock solutions on Candida albicans biofilm growth. J Antimicrob Chemother 62:153–155
Cateau E, Berjeaud JM, Imbert C (2011) Possible role of azole and echinocandin lock solutions in the control of Candida biofilms associated with silicone. Int J Antimicrob Agents 37:380–384
Cecchin E, De Marchi S, Panarello G, Franceschin A, Chiaradia V et al (1984) Torulopsis glabrata peritonitis complicating continuous ambulatory peritoneal dialysis: successful management with oral 5-fluorocytosine. Am J Kidney Dis 4:280–284
Cetrulo CL Jr, Leto Barone AA, Jordan K, Chang DS, Louie K et al (2012) A multi-disciplinary approach to the management of fungal osteomyelitis: current concepts in post-traumatic lower extremity reconstruction: a case report. Microsurgery 32:144–147
Chassot F, Negri MF, Svidzinski AE, Donatti L, Peralta RM et al (2008) Can intrauterine contraceptive devices be a Candida albicans reservoir? Contraception 77:355–359
Chotirmall SH, O’Donoghue E, Bennett K, Gunaratnam C, O’Neill SJ et al (2010) Sputum Candida albicans presages FEV decline and hospital-treated exacerbations in cystic fibrosis. Chest 138:1186–1195
Chowdhary A, Randhawa HS, Gaur SN, Agarwal K, Kathuria S et al (2013) Schizophyllum commune as an emerging fungal pathogen: a review and report of two cases. Mycoses 56:1–10
Cimon B, Carrere J, Vinatier JF, Chazalette JP, Chabasse D et al (2000) Clinical significance of Scedosporium apiospermum in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis 19:53–56
Coco BJ, Bagg J, Cross LJ, Jose A, Cross J et al (2008) Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol Immunol 23:377–383
Cornely OA, Bassetti M, Calandra T, Garbino J, Kullberg BJ et al (2012) ESCMID* guideline for the diagnosis and management of Candida diseases 2012: non-neutropenic adult patients. Clin Microbiol Infect 18(Suppl 7):19–37
Coulthwaite L, Verran J (2007) Potential pathogenic aspects of denture plaque. Br J Biomed Sci 64:180–189
Cugini C, Calfee MW, Farrow JM 3rd, Morales DK, Pesci EC et al (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65:896–906
Curvale-Fauchet N, Botterel F, Legrand P, Guillot J, Bretagne S (2004) Frequency of intravascular catheter colonization by Malassezia spp. in adult patients. Mycoses 47:491–494
D’Antonio D, Parruti G, Pontieri E, Di Bonaventura G, Manzoli L et al (2004) Slime production by clinical isolates of Blastoschizomyces capitatus from patients with hematological malignancies and catheter-related fungemia. Eur J Clin Microbiol Infect Dis 23:787–789
Damman CJ, Miller SI, Surawicz CM, Zisman TL (2012) The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol 107:1452–1459
Davis LE, Cook G, Costerton JW (2002) Biofilm on ventriculo-peritoneal shunt tubing as a cause of treatment failure in coccidioidal meningitis. Emerg Infect Dis 8:376–379
de Carvalho FG, Silva DS, Hebling J, Spolidorio LC, Spolidorio DM (2006) Presence of mutans streptococci and Candida spp. in dental plaque/dentine of carious teeth and early childhood caries. Arch Oral Biol 51:1024–1028
Deelstra JJ, Neut D, Jutte PC (2013) Successful treatment of Candida albicans-infected total hip prosthesis with staged procedure using an antifungal-loaded cement spacer. J Arthroplasty 28(374):e375–e378
Delhaes L, Monchy S, Frealle E, Hubans C, Salleron J et al (2012) The airway microbiota in cystic fibrosis: a complex fungal and bacterial community – implications for therapeutic management. PLoS One 7:e36313
Delisle MS, Williamson DR, Albert M, Perreault MM, Jiang X et al (2011) Impact of Candida species on clinical outcomes in patients with suspected ventilator-associated pneumonia. Can Respir J 18:131–136
Denning DW (1998) Invasive aspergillosis. Clin Infect Dis 26:781–803, quiz 804–785
Di Bonaventura G, Pompilio A, Picciani C, Iezzi M, D’Antonio D et al (2006) Biofilm formation by the emerging fungal pathogen Trichosporon asahii: development, architecture, and antifungal resistance. Antimicrob Agents Chemother 50:3269–3276
Ding C, Vidanes GM, Maguire SL, Guida A, Synnott JM et al (2011) Conserved and divergent roles of Bcr1 and CFEM proteins in Candida parapsilosis and Candida albicans. PLoS One 6:e28151
Dongari-Bagtzoglou A, Kashleva H, Dwivedi P, Diaz P, Vasilakos J (2009) Characterization of mucosal Candida albicans biofilms. PLoS One 4:e7967
Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
Dowd SE, Delton Hanson J, Rees E, Wolcott RD, Zischau AM et al (2011) Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care 20:40–47
Dutronc H, Dauchy FA, Cazanave C, Rougie C, Lafarie-Castet S et al (2010) Candida prosthetic infections: case series and literature review. Scand J Infect Dis 42:890–895
Ebbens FA, Georgalas C, Fokkens WJ (2009a) Fungus as the cause of chronic rhinosinusitis: the case remains unproven. Curr Opin Otolaryngol Head Neck Surg 17:43–49
Ebbens FA, Georgalas C, Fokkens WJ (2009b) The mold conundrum in chronic hyperplastic sinusitis. Curr Allergy Asthma Rep 9:114–120
Ell SR (1996) Candida ‘the cancer of silastic’. J Laryngol Otol 110:240–242
Ellis ME, Al-Abdely H, Sandridge A, Greer W, Ventura W (2001) Fungal endocarditis: evidence in the world literature, 1965–1995. Clin Infect Dis 32:50–62
Elving GJ, van Der Mei HC, Busscher HJ, van Weissenbruch R, Albers FW (2001) Air-flow resistances of silicone rubber voice prostheses after formation of bacterial and fungal biofilms. J Biomed Mater Res 58:421–426
Escande W, Fayad G, Modine T, Verbrugge E, Koussa M et al (2011) Culture of a prosthetic valve excised for streptococcal endocarditis positive for Aspergillus fumigatus 20 years after previous a fumigatus endocarditis. Ann Thorac Surg 91:e92–e93
Falcone M, Barzaghi N, Carosi G, Grossi P, Minoli L et al (2009) Candida infective endocarditis: report of 15 cases from a prospective multicenter study. Medicine (Baltimore) 88:160–168
Fanning S, Mitchell AP (2012) Fungal biofilms. PLoS Pathog 8:e1002585
Fanning S, Xu W, Solis N, Woolford CA, Filler SG et al (2012) Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell 11:896–904
Fazli M, Bjarnsholt T, Kirketerp-Moller K, Jorgensen B, Andersen AS et al (2009) Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47:4084–4089
Finkel JS, Mitchell AP (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9:109–118
Foreman A, Jervis-Bardy J, Wormald PJ (2011) Do biofilms contribute to the initiation and recalcitrance of chronic rhinosinusitis? Laryngoscope 121:1085–1091
Fortun J, Martin-Davila P, Gomez-Garcia de la Pedrosa E, Pintado V, Cobo J et al (2012) Emerging trends in candidemia: a higher incidence but a similar outcome. J Infect 65:64–70
Fox PM, Lee GK (2012) Tissue expander with acellular dermal matrix for breast reconstruction infected by an unusual pathogen: Candida parapsilosis. J Plast Reconstr Aesthet Surg 65:e286–e289
Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM et al (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med 4:132ra152
Gangell C, Gard S, Douglas T, Park J, de Klerk N et al (2011) Inflammatory responses to individual microorganisms in the lungs of children with cystic fibrosis. Clin Infect Dis 53:425–432
Garzoni C, Nobre VA, Garbino J (2007) Candida parapsilosis endocarditis: a comparative review of the literature. Eur J Clin Microbiol Infect Dis 26:915–926
Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M et al (2010) Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6:e1000713
Gibson J, Sood A, Hogan DA (2009) Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 75:504–513
Golmia R, Bello I, Marra A, Hamerschlak N, Osawa A et al (2011) Aspergillus fumigatus joint infection: a review. Semin Arthritis Rheum 40:580–584
Goodman JS, Seibert DG, Reahl GE Jr, Geckler RW (1983) Fungal infection of prosthetic joints: a report of two cases. J Rheumatol 10:494–495
Gottlieb K, Leya J, Kruss DM, Mobarhan S, Iber FL (1993) Intraluminal fungal colonization of gastrostomy tubes. Gastrointest Endosc 39:413–415
Grosjean P, Weber R (2007) Fungus balls of the paranasal sinuses: a review. Eur Arch Otorhinolaryngol 264:461–470
Gutierrez-Correa M, Ludena Y, Ramage G, Villena GK (2012) Recent advances on filamentous fungal biofilms for industrial uses. Appl Biochem Biotechnol 167:1235–1253
Hamet M, Pavon A, Dalle F, Pechinot A, Prin S et al (2012) Candida spp. airway colonization could promote antibiotic-resistant bacteria selection in patients with suspected ventilator-associated pneumonia. Intensive Care Med 38:1272–1279
Harding MW, Marques LL, Howard RJ, Olson ME (2009) Can filamentous fungi form biofilms? Trends Microbiol 17:475–480
Harriott MM, Noverr MC (2009) Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53:3914–3922
Harriott MM, Lilly EA, Rodriguez TE, Fidel PL Jr, Noverr MC (2010) Candida albicans forms biofilms on the vaginal mucosa. Microbiology 156:3635–3644
Heffner DK, Franklin WA (1978) Endocarditis caused by Torulopsis glabrata. Am J Clin Pathol 70:420–423
Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:2229–2232
Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212–1223
Holmes AR, van der Wielen P, Cannon RD, Ruske D, Dawes P (2006) Candida albicans binds to saliva proteins selectively adsorbed to silicone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102:488–494
Honraet K, De Vos MM, Summerbell RC, van Kempen I, De Saeger S et al (2005) Recurrent colonization of successively implanted tracheoesophageal vocal prostheses by a member of the Fusarium solani species complex. J Clin Microbiol 43:770–777
Jakubovics NS (2010) Talk of the town: interspecies communication in oral biofilms. Mol Oral Microbiol 25:4–14
Janagond A, Krishnan KM, Kindo AJ, Sumathi G (2012) Trichosporon inkin, an unusual agent of fungal sinusitis: a report from south India. Indian J Med Microbiol 30:229–232
Jayshree RS, Shafiulla M, George J, David JK, Bapsy PP et al (2006) Microscopic, cultural and molecular evidence of disseminated invasive aspergillosis involving the lungs and the gastrointestinal tract. J Med Microbiol 55:961–964
Jeloka TK, Shrividya S, Wagholikar G (2011) Catheter outflow obstruction due to an aspergilloma. Perit Dial Int 31:211–212
Johannsson B, Callaghan JJ (2009) Prosthetic hip infection due to Cryptococcus neoformans: case report. Diagn Microbiol Infect Dis 64:76–79
Johnson DC, Johnson FL, Goldman S (1994) Preliminary results treating persistent central venous catheter infections with the antibiotic lock technique in pediatric patients. Pediatr Infect Dis J 13:930–931
Kania RE, Lamers GE, van de Laar N, Dijkhuizen M, Lagendijk E et al (2010) Biofilms on tracheoesophageal voice prostheses: a confocal laser scanning microscopy demonstration of mixed bacterial and yeast biofilms. Biofouling 26:519–526
Karkas A, Rtail R, Reyt E, Timi N, Righini CA (2012) Sphenoid sinus fungus ball. Eur Arch Otorhinolaryngol 270:893–898
Kauffman CA, Fisher JF, Sobel JD, Newman CA (2011) Candida urinary tract infections – diagnosis. Clin Infect Dis 52(Suppl 6):S452–S456
Keir J, Pedelty L, Swift AC (2011) Biofilms in chronic rhinosinusitis: systematic review and suggestions for future research. J Laryngol Otol 125:331–337
Kelesidis T, Tsiodras S (2010) Candida albicans prosthetic hip infection in elderly patients: is fluconazole monotherapy an option? Scand J Infect Dis 42:12–21
Klaerner HG, Uknis ME, Acton RD, Dahlberg PS, Carlone-Jambor C et al (1997) Candida albicans and Escherichia coli are synergistic pathogens during experimental microbial peritonitis. J Surg Res 70:161–165
Ko KS, Lee JY, Song JH, Peck KR (2010) In vitro evaluation of antibiotic lock technique for the treatment of Candida albicans, C. glabrata, and C. tropicalis biofilms. J Korean Med Sci 25:1722–1726
Komshian SV, Uwaydah AK, Sobel JD, Crane LR (1989) Fungemia caused by Candida species and Torulopsis glabrata in the hospitalized patient: frequency, characteristics, and evaluation of factors influencing outcome. Rev Infect Dis 11:379–390
Kondori N, Gilljam M, Lindblad A, Jonsson B, Moore ER et al (2011) High rate of Exophiala dermatitidis recovery in the airways of patients with cystic fibrosis is associated with pancreatic insufficiency. J Clin Microbiol 49:1004–1009
Krzossok S, Birck R, Henke S, Hof H, van der Woude FJ et al (2004) Trichosporon asahii infection of a dialysis PTFE arteriovenous graft. Clin Nephrol 62:66–68
Krzywda EA, Andris DA, Edmiston CE Jr, Quebbeman EJ (1995) Treatment of Hickman catheter sepsis using antibiotic lock technique. Infect Control Hosp Epidemiol 16:596–598
Kucharikova S, Tournu H, Holtappels M, Van Dijck P, Lagrou K (2010) In vivo efficacy of anidulafungin against mature Candida albicans biofilms in a novel rat model of catheter-associated Candidiasis. Antimicrob Agents Chemother 54:4474–4475
Kuhn DM, Chandra J, Mukherjee PK, Ghannoum MA (2002a) Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun 70:878–888
Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA (2002b) Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46:1773–1780
Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA (2003) Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol 41:506–508
Kumamoto CA (2011) Inflammation and gastrointestinal Candida colonization. Curr Opin Microbiol 14:386–391
Langer P, Kassim RA, Macari GS, Saleh KJ (2003) Aspergillus infection after total knee arthroplasty. Am J Orthop 32:402–404
Lazzell AL, Chaturvedi AK, Pierce CG, Prasad D, Uppuluri P et al (2009) Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis. J Antimicrob Chemother 64:567–570
Leclair LW, Hogan DA (2010) Mixed bacterial-fungal infections in the CF respiratory tract. Med Mycol 48(Suppl 1):S125–S132
Lee SW (2010) An Aspergilloma mistaken for a pelviureteral stone on nonenhanced CT: a fungal bezoar causing ureteral obstruction. Korean J Urol 51:216–218
Lermann U, Morschhauser J (2008) Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 154:3281–3295
Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K et al (2007) Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 6:931–939
Ma B, Forney LJ, Ravel J (2012) Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol 66:371–389
Macfarlane S (2008) Microbial biofilm communities in the gastrointestinal tract. J Clin Gastroenterol 42(Suppl 3 Pt 1):S142–S143
Macfarlane S, Dillon JF (2007) Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102:1187–1196
Mansur AJ, Safi J Jr, Markus MR, Aiello VD, Grinberg M et al (1996) Late failure of surgical treatment for bioprosthetic valve endocarditis due to Candida tropicalis. Clin Infect Dis 22:380–381
Martin TJ, Kerschner JE, Flanary VA (2005) Fungal causes of otitis externa and tympanostomy tube otorrhea. Int J Pediatr Otorhinolaryngol 69:1503–1508
Mason KL, Erb Downward JR, Mason KD, Falkowski NR, Eaton KA et al (2012) Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun 80:3371–3380
McMillan A, Dell M, Zellar MP, Cribby S, Martz S et al (2011) Disruption of urogenital biofilms by lactobacilli. Colloids Surf B Biointerfaces 86:58–64
Mignogna MD, Fortuna G, Leuci S, Adamo D, Ruoppo E et al (2011) Mucormycosis in immunocompetent patients: a case-series of patients with maxillary sinus involvement and a critical review of the literature. Int J Infect Dis 15:e533–e540
Morales DK, Jacobs NJ, Rajamani S, Krishnamurthy M, Cubillos-Ruiz JR et al (2010) Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78:1379–1392
Mowat E, Lang S, Williams C, McCulloch E, Jones B et al (2008) Phase-dependent antifungal activity against Aspergillus fumigatus developing multicellular filamentous biofilms. J Antimicrob Chemother 62:1281–1284
Mowat E, Williams C, Jones B, McChlery S, Ramage G (2009) The characteristics of Aspergillus fumigatus mycetoma development: is this a biofilm? Med Mycol 47(Suppl 1):S120–6
Mowat E, Rajendran R, Williams C, McCulloch E, Jones B et al (2010) Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett 313:96–102
Mukherjee PK, Long L, Kim HG, Ghannoum MA (2009) Amphotericin B lipid complex is efficacious in the treatment of Candida albicans biofilms using a model of catheter-associated Candida biofilms. Int J Antimicrob Agents 33:149–153
Muller FM, Seidler M, Beauvais A (2011) Aspergillus fumigatus biofilms in the clinical setting. Med Mycol 49(Suppl 1):S96–S100
Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67:400–428, Table of contents
Naglik J, Albrecht A, Bader O, Hube B (2004) Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 6:915–926
Naglik JR, Fostira F, Ruprai J, Staab JF, Challacombe SJ et al (2006) Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J Med Microbiol 55:1323–1327
Naglik JR, Moyes D, Makwana J, Kanzaria P, Tsichlaki E et al (2008) Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 154:3266–3280
Negri M, Silva S, Henriques M, Oliveira R (2012) Insights into Candida tropicalis nosocomial infections and virulence factors. Eur J Clin Microbiol Infect Dis 31:1399–1412
Nett JE, Sanchez H, Cain MT, Andes DR (2010a) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202:171–175
Nett JE, Marchillo K, Spiegel CA, Andes DR (2010b) Development and validation of an in vivo Candida albicans biofilm denture model. Infect Immun 78:3650–3659
Newton A (1962) Denture sore mouth. A possible aetiology. Br Dent J 112:357–360
Nobile CJ, Mitchell AP (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8:1382–1391
Nucci M, Anaissie E, Betts RF, Dupont BF, Wu C et al (2010) Early removal of central venous catheter in patients with candidemia does not improve outcome: analysis of 842 patients from 2 randomized clinical trials. Clin Infect Dis 51:295–303
O’Grady NP, Alexander M, Burns LA, Dellinger EP, Garland J et al (2011) Guidelines for the prevention of intravascular catheter-related infections. Clin Infect Dis 52:e162–e193
Odds F (1988) Candida and candidosis. Bailliere Tindall, London
Ozdemir H, Karbuz A, Ciftci E, Dincaslan HU, Ince E et al (2011) Successful treatment of central venous catheter infection due to Candida lipolytica by caspofungin-lock therapy. Mycoses 54:e647–e649
Paige C, Pinson CW, Antonovic R, Strausbaugh LJ (1987) Catheter-related thrombophlebitis of the superior vena cava caused by Candida glabrata. West J Med 147:333–335
Pammi M, Holland L, Butler G, Gacser A, Bliss JM (2013) Candida parapsilosis is a significant neonatal pathogen: a systematic review and meta-analysis. Pediatr Infect Dis J 32:e206–e216
Pannanusorn S, Fernandez V, Romling U (2012) Prevalence of biofilm formation in clinical isolates of Candida species causing bloodstream infection. Mycoses 56:264–272
Pereira-Cenci T, Del Bel Cury AA, Crielaard W, Ten Cate JM (2008) Development of Candida-associated denture stomatitis: new insights. J Appl Oral Sci 16:86–94
Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW et al (2010) Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493–503
Peters BM, Jabra-Rizk MA, O’May GA, Costerton JW, Shirtliff ME (2012) Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25:193–213
Pini G, Faggi E, Donato R, Fanci R (2005) Isolation of Trichosporon in a hematology ward. Mycoses 48:45–49
Puri S, Kumar R, Chadha S, Tati S, Conti HR et al (2012) Secreted aspartic protease cleavage of Candida albicans Msb2 activates Cek1 MAPK signaling affecting biofilm formation and oropharyngeal candidiasis. PLoS One 7:e46020
Rajendran R, Robertson DP, Hodge PJ, Lappin DF, Ramage G (2010) Hydrolytic enzyme production is associated with Candida albicans biofilm formation from patients with type 1 diabetes. Mycopathologia 170:229–235
Ramage G, VandeWalle K, Lopez-Ribot JL, Wickes BL (2002) The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214:95–100
Ramage G, Tomsett K, Wickes BL, Lopez-Ribot JL, Redding SW (2004) Denture stomatitis: a role for Candida biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 98:53–59
Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J (2009) Our current understanding of fungal biofilms. Crit Rev Microbiol 35:340–355
Ramage G, Rajendran R, Gutierrez-Correa M, Jones B, Williams C (2011) Aspergillus biofilms: clinical and industrial significance. FEMS Microbiol Lett 324:89–97
Ramage G, Coco B, Sherry L, Bagg J, Lappin DF (2012) In vitro Candida albicans biofilm induced proteinase activity and SAP8 expression correlates with in vivo denture stomatitis severity. Mycopathologia 174:11–19
Ramage G, Jose A, Sherry L, Lappin DF, Jones B et al (2013) Liposomal formulations of amphotericin B displays rapid dose dependant activity against Candida albicans biofilms. Antimicrob Agents Chemother 57:2369–2371
Rautemaa R, Ramage G (2011) Oral candidosis–clinical challenges of a biofilm disease. Crit Rev Microbiol 37:328–336
Reddy BT, Torres HA, Kontoyiannis DP (2002) Breast implant infection caused by Trichosporon beigelii. Scand J Infect Dis 34:143–144
Reid G, Denstedt JD, Kang YS, Lam D, Nause C (1992) Microbial adhesion and biofilm formation on ureteral stents in vitro and in vivo. J Urol 148:1592–1594
Reis LJ, Barton TD, Pochettino A, Velazquez O, McGarvey M et al (2005) Successful treatment of Aspergillus prosthetic valve endocarditis with oral voriconazole. Clin Infect Dis 41:752–753
Rex JH, Bennett JE, Sugar AM, Pappas PG, Serody J et al (1995) Intravascular catheter exchange and duration of candidemia. NIAID Mycoses Study Group and the Candidemia Study Group. Clin Infect Dis 21:994–996
Richardson M (2009) The ecology of the zygomycetes and its impact on environmental exposure. Clin Microbiol Infect 15(Suppl 5):2–9
Rombaux P, Eloy P, Bertrand B, Delos M, Doyen C (1996) Lethal disseminated Fusarium infection with sinus involvement in the immunocompromised host: case report and review of the literature. Rhinology 34:237–241
Rosenblatt WB, Pollock A (1997) Aspergillus flavus cultured from a saline-filled implant. Plast Reconstr Surg 99:1470–1472
Ruan SY, Chien JY, Hsueh PR (2009) Invasive trichosporonosis caused by Trichosporon asahii and other unusual Trichosporon species at a medical center in Taiwan. Clin Infect Dis 49:e11–e17
Sa HS, Ko KS, Woo KI, Peck KR, Kim YD (2012) A case of sino-orbital infection caused by the Schizophyllum commune. Diagn Microbiol Infect Dis 73:376–377
Sardi JC, Duque C, Mariano FS, Peixoto IT, Hofling JF et al (2010) Candida spp. in periodontal disease: a brief review. J Oral Sci 52:177–185
Sato FR, Sawazaki R, Berretta D, Moreira RW, Vargas PA et al (2010) Aspergillosis of the maxillary sinus associated with a zygomatic implant. J Am Dent Assoc 141:1231–1235
Sayed SI, Datta S, Deore N, Kazi RA, Jagade MV (2012) Prevention of voice prosthesis biofilms: current scenario and future trends in prolonging prosthesis lifetime. J Indian Med Assoc 110:175–178, 180
Schinabeck MK, Long LA, Hossain MA, Chandra J, Mukherjee PK et al (2004) Rabbit model of Candida albicans biofilm infection: liposomal amphotericin B antifungal lock therapy. Antimicrob Agents Chemother 48:1727–1732
Seidler MJ, Salvenmoser S, Muller FM (2008) Aspergillus fumigatus forms biofilms with reduced antifungal drug susceptibility on bronchial epithelial cells. Antimicrob Agents Chemother 52:4130–4136
Serban RI, Dan M, Panzaru CV, Anghel D, Dascalescu D et al (2010) Fungi as emergent etiologic agents in ventilator-associated pneumonia after cardiac surgery. Rev Med Chir Soc Med Nat Iasi 114:1077–1082
Seth AK, Geringer MR, Hong SJ, Leung KP, Mustoe TA et al (2012) In vivo modeling of biofilm-infected wounds: a review. J Surg Res 178:330–338
Short DP, O’Donnell K, Zhang N, Juba JH, Geiser DM (2011) Widespread occurrence of diverse human pathogenic types of the fungus Fusarium detected in plumbing drains. J Clin Microbiol 49:4264–4272
Shuford JA, Rouse MS, Piper KE, Steckelberg JM, Patel R (2006) Evaluation of caspofungin and amphotericin B deoxycholate against Candida albicans biofilms in an experimental intravascular catheter infection model. J Infect Dis 194:710–713
Sibley CD, Duan K, Fischer C, Parkins MD, Storey DG et al (2008a) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4:e1000184
Sibley CD, Parkins MD, Rabin HR, Duan K, Norgaard JC et al (2008b) A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A 105:15070–15075
Silva S, Henriques M, Hayes A, Oliveira R, Azeredo J et al (2011) Candida glabrata and Candida albicans co-infection of an in vitro oral epithelium. J Oral Pathol Med 40:421–427
Silverman RJ, Nobbs AH, Vickerman MM, Barbour ME, Jenkinson HF (2010) Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78:4644–4652
Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ et al (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764
Singh R, Shivaprakash MR, Chakrabarti A (2011) Biofilm formation by zygomycetes: quantification, structure and matrix composition. Microbiology 157:2611–2618
Singhal D, Baker L, Wormald PJ, Tan L (2011) Aspergillus fumigatus biofilm on primary human sinonasal epithelial culture. Am J Rhinol Allergy 25:219–225
Siqueira VM, Oliveira HM, Santos C, Paterson RR, Gusmao NB et al (2011) Filamentous fungi in drinking water, particularly in relation to biofilm formation. Int J Environ Res Public Health 8:456–469
Sobel JD, Fisher JF, Kauffman CA, Newman CA (2011) Candida urinary tract infections – epidemiology. Clin Infect Dis 52(Suppl 6):S433–S436
Stonecypher K (2010) Ventilator-associated pneumonia: the importance of oral care in intubated adults. Crit Care Nurs Q 33:339–347
Taff HT, Nett JE, Andes DR (2012) Comparative analysis of Candida biofilm quantitation assays. Med Mycol 50:214–218
Trevisani L, Sartori S, Rossi MR, Bovolenta R, Scoponi M et al (2005) Degradation of polyurethane gastrostomy devices: what is the role of fungal colonization? Dig Dis Sci 50:463–469
Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M et al (2007) Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol 45:1843–1850
Tumbarello M, Fiori B, Trecarichi EM, Posteraro P, Losito AR et al (2012) Risk factors and outcomes of candidemia caused by biofilm-forming isolates in a tertiary care hospital. PLoS One 7:e33705
Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK et al (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6:e1000828
Valdivieso M, Luna M, Bodey GP, Rodriguez V, Groschel D (1976) Fungemia due to Torulopsis glabrata in the compromised host. Cancer 38:1750–1756
Viale P, Petrosillo N, Signorini L, Puoti M, Carosi G (2001) Should lock therapy always be avoided for central venous catheter-associated fungal bloodstream infections? Clin Infect Dis 33:1947–1948, Author reply 1949–1951
Wada M, Baba H, Imura S (1998) Prosthetic knee Candida parapsilosis infection. J Arthroplasty 13:479–482
Wallner M, Steyer G, Krause R, Gstettner C, von Lewinski D (2012) Fungal endocarditis of a bioprosthetic aortic valve: pharmacological treatment of a Candida parapsilosis endocarditis. Herz 38:431–434
Walraven CJ, Lee SA (2013) Antifungal lock therapy. Antimicrob Agents Chemother 57:1–8
Walsh TJ, Schlegel R, Moody MM, Costerton JW, Salcman M (1986) Ventriculoatrial shunt infection due to Cryptococcus neoformans: an ultrastructural and quantitative microbiological study. Neurosurgery 18:373–375
Walter EB Jr, Gingras JL, McKinney RE Jr (1990) Systemic Torulopsis glabrata infection in a neonate. South Med J 83:837–838
Warkentien T, Rodriguez C, Lloyd B, Wells J, Weintrob A et al (2012) Invasive mold infections following combat-related injuries. Clin Infect Dis 55:1441–1449
Williams DW, Kuriyama T, Silva S, Malic S, Lewis MA (2011) Candida biofilms and oral candidosis: treatment and prevention. Periodontol 2000 55:250–265
Wolcott RD, Gontcharova V, Sun Y, Dowd SE (2009) Evaluation of the bacterial diversity among and within individual venous leg ulcers using bacterial tag-encoded FLX and titanium amplicon pyrosequencing and metagenomic approaches. BMC Microbiol 9:226
Wu CY, Lee PI (2007) Antibiotic-lock therapy and erythromycin for treatment of catheter-related Candida parapsilosis and Staphylococcus aureus infections. J Antimicrob Chemother 60:706–707
Yang SP, Chen YY, Hsu HS, Wang FD, Chen LY et al (2013) A risk factor analysis of healthcare-associated fungal infections in an intensive care unit: a retrospective cohort study. BMC Infect Dis 13:10
Yao M, Messner AH (2001) Fungal malignant otitis externa due to Scedosporium apiospermum. Ann Otol Rhinol Laryngol 110:377–380
Young RC, Bennett JE, Vogel CL, Carbone PP, DeVita VT (1970) Aspergillosis. The spectrum of the disease in 98 patients. Medicine (Baltimore) 49:147–173
Younkin S, Evarts CM, Steigbigel RT (1984) Candida parapsilosis infection of a total hip-joint replacement: successful reimplantation after treatment with amphotericin B and 5-fluorocytosine. A case report. J Bone Joint Surg Am 66:142–143
Zhao X, Daniels KJ, Oh SH, Green CB, Yeater KM et al (2006) Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152:2287–2299
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Williams, C., Ramage, G. (2015). Fungal Biofilms in Human Disease. In: Donelli, G. (eds) Biofilm-based Healthcare-associated Infections. Advances in Experimental Medicine and Biology, vol 831. Springer, Cham. https://doi.org/10.1007/978-3-319-09782-4_2
Download citation
DOI: https://doi.org/10.1007/978-3-319-09782-4_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-09781-7
Online ISBN: 978-3-319-09782-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)