Skip to main content

Animal Infections: The Role of Fungal Biofilms

  • Chapter
  • First Online:
Recent Developments in Fungal Diseases of Laboratory Animals

Part of the book series: Fungal Biology ((FUNGBIO))

  • 383 Accesses

Abstract

A biofilm is defined as adherent microbial communities on biotic or abiotic surfaces surrounded by extracellular polymeric substances (EPS) matrix. Biofilm formation by bacteria is very common; however, the pathogenic filamentous fungi and yeast also form biofilms. The microbial biofilm protects microbes against harsh environments, host immune defence and antibiotics. The composition and architecture of the fungal biofilms attribute tolerance to antifungal agents and require up to 10–1000 times greater concentrations of antifungal agents than planktonic cells to eradicate biofilms. In mature biofilms, the cell metabolism is slow and demonstrates differential gene expressions compared to the counterpart planktonic cells; therefore, the common antifungal agents are ineffective on active growing cells. The mode of growth of biofilms increases the frequency of genetic exchange, which results in the origin of an antibiotic-resistant strain. Polymicrobial biofilms of bacteria and fungi is another huge challenge in which cooperation between different species has been detected. The microbial biofilm infections are persisters and resistant to antibiotic therapy. The formation of biofilm is regulated by a process called quorum sensing (cell-to-cell communication) mediated by small molecules (auto-inducers). In animals, various infectious diseases, such as otomycosis, dermatitis, stomatitis, onychomycosis, vulvovaginitis, urinary tract infection and respiratory tract infection, are caused by biofilms of Candida spp., Cryptococcus spp., Malassezia spp., Trichosporon spp., Fusarium spp., Scedosporium spp., Lomentospora prolificans and Coccidioides spp. Animal disease caused by fungi forming biofilms is a huge challenge in veterinary medicine. In this review chapter, we provide an overview of biofilm-related fungi diseases of animals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam B, Baillie GS, Douglas LJ (2002) Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344–349

    Article  PubMed  Google Scholar 

  • Aguilar-Romero F, Pérez-Romero N, Díaz-Aparicio E, Hernández-Castro R (2011) Bacterial biofilms: importance in animal diseases. In: Mendez-Vilas A (ed) In current research technology and education topics in applied microbiology and molecular biotechnology. http://microbiologia.org.mx/microbiosenlinea/capitulo04

    Google Scholar 

  • Ajesh K, Sreejith K (2012) Cryptococcus laurentii biofilms: structure, development and antifungal drug resistance. Mycopathologia 174:409–419

    Article  CAS  PubMed  Google Scholar 

  • Akins RA (2005) An update on antifungal targets and mechanisms of resistance in Candida albicans. Med Mycol 43:285–318

    Article  CAS  PubMed  Google Scholar 

  • Albertson GD, Niimi M, Cannon RD, Jenkinson HF (1996) Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob Agents Chemother 40:2835–2841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Dhaheri RS, Douglas LJ (2008) Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob Agents Chemother 52:1884–1887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Fattani MA, Douglas LJ (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55:999–1008

    Article  CAS  PubMed  Google Scholar 

  • Amorena B, Gracia E, Monzóna M, Leivab J, Oteizab C, Péreza M, Alabarta J, Hernández-Yagoc J (1999) Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J Antimicrob Chemother 44:43–55

    Article  CAS  PubMed  Google Scholar 

  • Anderson JB (2005) Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 3:547–556

    Article  CAS  PubMed  Google Scholar 

  • Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72:6023–6031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, Henry C, Paris S, Mallet A, Prevost MC, Latge JP (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9:1588–1600

    Article  CAS  PubMed  Google Scholar 

  • Beauvais A, Loussert C, Prevost MC, Verstrepen K, Latge JP (2009) Characterization of a biofilm-like extracellular matrix in FLO1-expressing Saccharomyces cerevisiae cells. FEMS Yeast Res 9:411–419

    Article  CAS  PubMed  Google Scholar 

  • Bizerra FC, Nakamura CV, de Poersch C, EstivaletSvidzinski TI, Borsato Quesada RM, Goldenberg S (2008) Characteristics of biofilm formation by Candida tropicalis and antifungal resistance. FEMS Yeast Res 8:442–450

    Article  CAS  PubMed  Google Scholar 

  • Blankenship JR, Mitchell AP (2006) How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9:588–594

    Article  CAS  PubMed  Google Scholar 

  • Bonhomme J, d’Enfert C (2013) Candida albicans biofilms: building a heterogeneous, drug-tolerant environment. Curr Opin Microbiol 16:398–403

    Article  CAS  PubMed  Google Scholar 

  • Bueid A, Howard SJ, Moore CB, Richardson MD, Harrison E, Bowyer P (2010) Azole antifungal resistance in Aspergillus fumigatus: 2008 and 2009. J Antimicrob Chemother 65:2116–2118

    Article  CAS  PubMed  Google Scholar 

  • Bumroongthai K, Chetanachan P, Niyomtham W, Yurayart C, Prapasarakul N (2016) Biofilm production and antifungal susceptibility of co-cultured Malassezia pachydermatis and Candida parapsilosis isolated from canine seborrheic dermatitis. MedMycol 54:544–549

    CAS  Google Scholar 

  • Burkhart CN, Burkhart CG, Gupta AK (2002) Dermatophytoma: recalcitrance to treatment because of existence of fungal biofilm. J Am Acad Dermatol 47:629–631

    Article  PubMed  Google Scholar 

  • Cannizzo FT, Eraso E, Ezkurra PA, Villar-Vidal M, Bollo E, Castella G (2007) Biofilm development by clinical isolates of Malassezia pachydermatis. Med Mycol 45:357–361

    Article  PubMed  Google Scholar 

  • Cannon RD, Lamping E, Holmes AR, Niimi K, Tanabe K, Niimi M (2007) Candida albicans drug resistance another way to cope with stress. Microbiology 153:3211–3217

    Article  CAS  PubMed  Google Scholar 

  • Carlson E (1982) Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality. Infect Immun 38:921–924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183:5385–5394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng MF, Chiou CC, Liu YC, Wang HZ, Hsieh KS (2001) Cryptococcus laurentii fungemia in a premature neonate. J Clin Microbiol 39:1608–1611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costa-Orlandi CB, Magalhães GM, Oliveira MB, Taylor EL, Marques CR, de Resende-Stoianoff MA (2012) Prevalence of dermatomycosis in a Brazilian tertiary care hospital. Mycopathologia 174:489–497

    Article  PubMed  Google Scholar 

  • Costa-Orlandi CB, Sardi JCO, Pitangui NS, de Oliveira HC, Scorzoni L, Galeane MC, Mendes-Giannini MJS (2017) Fungal biofilms and polymicrobial diseases. J Fungi 3:22. https://doi.org/10.3390/jof3020022

    Article  CAS  Google Scholar 

  • Costerton JW, Cheng KJ, Gersey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    Article  CAS  PubMed  Google Scholar 

  • Cushion MT, Collins MS, Linke MJ (2009) Biofilm formation by Pneumocystis spp. Eukaryot Cell 8:197–206

    Article  CAS  PubMed  Google Scholar 

  • D’Antonio D, Parruti G, Pontieri E, Di Bonaventura G, Manzoli L, Sferra R (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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • De Beer D, Stoodley P, Lewandowski Z (1994) Liquid flow in heterogeneous biofilms. Biotechnol Bioeng 44:636–641

    Article  PubMed  Google Scholar 

  • De Carvalho FG, Silva DS, Hebling J, Spolidorio LC, Spolidorio DMP (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

    Article  PubMed  CAS  Google Scholar 

  • Di Bonaventura G, Pompilio A, Picciani C, Iezzi M, D’Antonio D, Piccolomini R (2006) Biofilm formation by the emerging fungal pathogen Trichosporon asahii: development, architecture, and antifungal resistance. Antimicrob Agents Chemother 50:3269–3276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falsetta ML, Klein MI, Colonne PM, Scott-Anne K, Gregoire S, Pai C (2014) Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes the virulence of plaque-biofilms in vivo. Infect Immun 82:1968–1981

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Finkel JS, Mitchell AP (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9:109–118

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Ramirez AI, Ramirez-Granillo A, Medina-Canales MG, Rodriguez-Tovar AV, Martinez-Rivera MA (2016) Analysis and description of the stages of Aspergillus fumigatus biofilm formation using scanning electron microscopy. BMC Microbiol 16:243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gregoire S, Xiao J, Silva BB, Gonzalez I, Agidi PS, Klein MI et al (2011) Role of glucosyltransferase B in interactions of Candida albicans with Streptococcus mutans and with an experimental pellicle on hydroxyapatite surfaces. Appl Environ Microbiol 77:6357–6367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harding MW, Marques LL, Howard RJ, Olson ME (2009) Can filamentous fungi form biofilms? Trends Microbiol 17:475–480

    Article  CAS  PubMed  Google Scholar 

  • Harriott MM, Noverr MC (2009) Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother September 53:3914–3922

    Article  CAS  Google Scholar 

  • Henriques M, Azeredo J, Oliveira R (2006) Candida albicans and Candida dubliniensis: comparison of biofilm formation in terms of biomass and activity. Br J Biomed Sci 63:5–11

    Article  CAS  PubMed  Google Scholar 

  • Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R et al (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67:2982–2992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imamura Y, Chandra J, Mukherjee PK, Lattif AA, Szczotka-Flynn LB, Pearlman E, Lass JH, O’Donnell K, Ghannoum MA (2008) Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob Agents Chemother 52:171–182

    Article  CAS  PubMed  Google Scholar 

  • Ingram CW, Haywood HB 3rd, Morris VM, Allen RL, Perfect JR (1993) Cryptococcal ventricular-peritoneal shunt infection: clinical and epidemiological evaluation of two closely associated cases. Infect Control Hosp Epidemiol 14:719–722

    Article  CAS  PubMed  Google Scholar 

  • Iturrieta-Gonzalez IA, Padovan AC, Bizerra FC, Hahn RC, Colombo AL (2014) Multiple species of trichosporon produce biofilms highly resistant to triazoles and amphotericin B. PLoS One 9:e109553

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jadhav VJ, Pal M (2013) Human and domestic animal infections caused by Candida albicans. J Mycopathol Res 551:243–249

    Google Scholar 

  • Jefferson KK (2004) What drives bacteria to produce a biofilm? FEMS Microbiol Lett 236:163–173

    Article  CAS  PubMed  Google Scholar 

  • Kaur S, Singh S (2014) Biofilm formation by Aspergillus fumigatus. Med Mycol 52:2–9

    CAS  PubMed  Google Scholar 

  • Khawcharoenporn T, Apisarnthanarak A, Kiratisin P, Mundy LM, Bailey TC (2006) Evaluation of Cryptococcus laurentii meningitis in a patient with HIV infection: a case report and review of the literature. Hawaii Med J 65:260–263

    PubMed  Google Scholar 

  • Khawcharoenporn T, Apisarnthanarak A, Mundy LM (2007) Non-neoformans cryptococcal infections: a systematic review. Infection 35:51–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khot PD, Suci PA, Miller RL, Nelson RD, Tyler BJ (2006) A small subpopulation of blastospores in Candida albicans biofilms exhibit resistance to amphotericin B associated with differential regulation of ergosterol and beta-1,6-glucan pathway genes. Antimicrob Agents Chemother 50:3708–3716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klotz SA, Chasin BS, Powell B, Gaur NK, Lipke PN (2007) Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn Microbiol Infect Dis 59:401–406

    Article  CAS  PubMed  Google Scholar 

  • Kojic EM, Darouiche RO (2004) Candida infections of medical devices. Clin Microbiol Rev 17:255–267

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumamoto CA (2005) A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci U S A 102:5576–5581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaFleur MD, Kumamoto CA, Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50:3839–3846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (1991) Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis K (2010) Persister cells. Annu Rev Micro 64:357–372

    Article  CAS  Google Scholar 

  • Lopez-Ribot JL, McAtee RK, Perea S, Kirkpatrick WR, Rinaldi MG, Patterson TF (1999) Multiple resistant phenotypes of Candida albicans coexist during episodes of oropharyngeal candidiasis in human immunodeficiency virus-infected patients. Antimicrob Agents Chemother 43:1621–1630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malik R, Alderton B, Finlaison D et al (2002) Cryptococcosis in ferrets: a diverse spectrum of clinical disease. Aust Vet J 80:749–755

    Article  CAS  PubMed  Google Scholar 

  • Marcos-Zambrano LJ, Gomez-Perosanz M, Escribano P, Zaragoza O, Bouza E, Guinea J (2016) Biofilm production and antibiofilm activity of echinocandins and liposomal amphotericin B in echinocandin-resistant yeast species. Antimicrob Agents Chemother 60:3579–3586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsh PD (1999) Microbiologic aspects of dental plaque and dental caries. Dent Clin N Am 43:599–614

    CAS  PubMed  Google Scholar 

  • Martinez LR, Casadevall A (2006) Susceptibility of Cryptococcus neoformans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 50:1021–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez LR, Mihu MR, Han G, Frases S, Cordero RJ, Casadevall A, Friedman AJ, Friedman JM, Nosanchuk JD (2010) The use of chitosan to damage Cryptococcus neoformans biofilms. Biomaterials 31:669–679

    Article  CAS  PubMed  Google Scholar 

  • Mello TP, Aor A, Goncalves DS, Seabra SH, Branquinha MH, Santos AL (2016) Assessment of biofilm formation by Scedosporium apiospermum, S. aurantiacum, S. minutisporum and Lomentospora prolificans. Biofouling 32:737–749

    Article  CAS  PubMed  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annurev Micro 55:165–199

    Article  CAS  Google Scholar 

  • Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA (2003) Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 71:4333–4340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee PK, Chandra J, Yu C, Sun Y, Pearlman E, Ghannoum MA (2012) Characterization of Fusarium keratitis outbreak isolates: contribution of biofilms to antimicrobial resistance and pathogenesis. Investig Ophthalmol Vis Sci 53:4450–4457

    Article  CAS  Google Scholar 

  • Müller FM, Seidler M, Beauvais A (2011) Aspergillus fumigatus biofilms in the clinical setting. Med Mycol 49:S96–S100

    Article  PubMed  Google Scholar 

  • Nett JE, Lepak AJ, Marchillo K, Andes DR (2009) Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 200:307–313

    Article  CAS  PubMed  Google Scholar 

  • Niimi M, Firth NA, Cannon RD (2010) Antifungal drug resistance of oral fungi. Odontology 98:15–25

    Article  CAS  PubMed  Google Scholar 

  • Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A et al (2009) Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7:e1000133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peiqian L, Xiaoming P, Huifang S, Jingxin Z, Ning H, Birun L (2013) Biofilm formation by Fusarium oxysporum f. sp. cucumerinum and susceptibility to environmental stress. FEMS Microbiol Lett 350:138–145

    Article  PubMed  CAS  Google Scholar 

  • Pereira-Cenci T, Deng DM, Kraneveld EA, Manders EMM, Del Bel Cury AA, ten Cate JM et al (2008) The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch Oral Biol 53:755–764

    Article  CAS  PubMed  Google Scholar 

  • Pettit RK, Repp KK, Hazen KC (2010) Temperature affects the susceptibility of Cryptococcus neoformans biofilms to antifungal agents. Med Mycol 48:421–426

    Article  CAS  PubMed  Google Scholar 

  • Piddock LJ (2006) Multidrug-resistance efflux pumps – not just for resistance. Nat Rev Microbiol 4:629–636

    Article  CAS  PubMed  Google Scholar 

  • Pires RH, Santo s JM, Zaia JE, Martins CH, Mendes-Giannini MJ (2011) Candida parapsilosis complex water isolates from a haemodialysis unit: biofilm production and in vitro evaluation of the use of clinical antifungals. Memórias Inst Oswaldo Cruz 106:646–654

    Article  CAS  Google Scholar 

  • Pitangui NS, Sardi JC, Silva JF, Benaducci T, Moraes da Silva RA, Rodriguez-Arellanes G, Taylor ML, Mendes-Giannini MJ, Fusco-Almeida AM (2012) Adhesion of Histoplasma capsulatum to pneumocytes and biofilm formation on an abiotic surface. Biofouling 28:711–718

    Article  CAS  PubMed  Google Scholar 

  • Rajendran R, Williams C, Lappin DF, Millington O, Martins M, Ramage G (2013) Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot Cell 12:420–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramage G, Saville SP, Thomas DP, Lopez-Ribot JL (2005) Candida biofilms: an update. Eukaryot Cell 4:633–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J (2009) Our current understanding of fungal biofilms. Crit Rev Microbiol 35:340–355

    Article  CAS  PubMed  Google Scholar 

  • Ramage G, Rajendran R, Gutierrez-Correa M, Jones B, Williams C (2011) Aspergillus biofilms: clinical and industrial significance. FEMS Microbiol Lett 324:89–97

    Article  CAS  PubMed  Google Scholar 

  • Ramage G, Milligan S, Lappin DF, Sherry L, Sweeney P, Williams C et al (2012) Antifungal, cytotoxic, and immunomodulatory properties of tea tree oil and its derivative components: potential role in management of oral candidosis in cancer patients. Front Microbiol 3:220

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanglard D, Ischer F, Monod M, Bille J (1997) Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 143:405–416

    Article  CAS  PubMed  Google Scholar 

  • Sardi Jde C, Pitangui Nde S, Voltan AR, Braz JD, Machado MP, Fusco Almeida AM, Mendes Giannini MJ (2015) In vitro Paracoccidioides brasiliensis biofilm and gene expression of adhesins and hydrolytic enzymes. Virulence 6:642–651

    Article  PubMed  CAS  Google Scholar 

  • Scorzoni L, de PaulaeSilva ACA, Marcos CM, Assato PA, de Melo WCMA, de Oliveira HC, Costa-Orlandi CB, Mendes-Giannini MJS, Fusco-Almeida AM (2017) Antifungal therapy: new advances in the understanding and treatment of mycosis. Front Microbiol 8:36

    Article  PubMed  PubMed Central  Google Scholar 

  • Shankar EM, Kumarasamy N, Bella D et al (2006) Pneumonia and pleural effusion due to Cryptococcus laurentii in a clinically proven case of AIDS. Can Respir J 13:275–278

    Article  PubMed  PubMed Central  Google Scholar 

  • Shapiro RS, Robbins N, Cowen LE (2011) Regulatory circuitry governing fungal development, drug resistance and disease. Microbiol Mol Biol Rev 75:213–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47:681–689

    Article  CAS  PubMed  Google Scholar 

  • Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2011) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36:288–305

    Article  PubMed  CAS  Google Scholar 

  • Singh R, Shivaprakash MR, Chakrabarti A (2011) Biofilm formation by zygomycetes: quantification, structure and matrix composition. Microbiology 157:2611–2618

    Article  CAS  PubMed  Google Scholar 

  • Steinbach WJ, Reedy JL, Cramer RA Jr, Perfect JR, Heitman J (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5:418–430

    Article  CAS  PubMed  Google Scholar 

  • Sykes JE, Sturges BK, Cannon MS et al (2010) Clinical signs, imaging features, neuropathology, and outcome in cats and dogs with central nervous system cryptococcosis from California. J Vet Intern Med 24:1427–1438

    Article  CAS  PubMed  Google Scholar 

  • Thein Z, Seneviratne C, Samaranayake Y, Samaranayake L (2009) Community lifestyle of Candida in mixed biofilms: a mini review. Mycoses 52:467–475

    Article  CAS  PubMed  Google Scholar 

  • Tre-Hardy M, Vanderbist F, Traore H, Devleeschouwer MJ (2008) In vitro activity of antibiotic combinations against Pseudomonas aeruginosa biofilm and planktonic cultures. Int J Antimicrob Agents 31:329–336

    Article  CAS  PubMed  Google Scholar 

  • Tsui C, Kong EF, Jabra-Rizk MA (2016) Pathogenesis of Candida albicans biofilm. Pathog Dis 74:ftw018

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Weitzman I, Summerbell RC (1995) The dermatophytes. Clin Microbiol Rev 8:240–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams C, Rajendran R, Ramage G (2016) Aspergillus biofilms in human disease. Adv Exp Med Biol 931:1–11

    Article  PubMed  Google Scholar 

  • Wosten HA (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Moon Y, Li L, Rustchenko E, Wakabayashi H, Zhao X et al (2016) Candida albicans carriage in children with severe early childhood caries (S-ECC) and maternal relatedness. PLoS One 11:e0164242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xie Z, Thompson A, Sobue T, Kashleva H, Xu H, Vasilakos J et al (2012) Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. J Infect Dis 206:1936–1945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Jenkinson HF, Dongari-Bagtzoglou A (2014) Innocent until proven guilty: mechanisms and roles of Streptococcus–Candida interactions in oral health and disease. Mol Oral Microbiol 29:99–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yadav, M.K., Malvi, Y. (2019). Animal Infections: The Role of Fungal Biofilms. In: Gupta, A., Singh, N. (eds) Recent Developments in Fungal Diseases of Laboratory Animals. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-030-18586-2_10

Download citation

Publish with us

Policies and ethics