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Aspergillus Biofilms in Human Disease

Part of the Advances in Experimental Medicine and Biology book series (AMIDPH,volume 931)

Abstract

The biofilm phenotype of Aspergillus species is an important and accepted clinical entity. While industrially these biofilms have been used extensively in important biofermentations, their role in clinical infection is less well defined. A recent flurry of activity has demonstrated that these interesting filamentous moulds have the capacity to form biofilms both in vitro and in vivo, and through various investigations have shown that these are exquisitely resistant to antifungal therapies through a range of adaptive resistance mechanisms independent of defined genetic changes. This review will explore the clinical importance of these biofilms and provide contemporary information with respect to their clinical management.

Keywords

  • Aspergillus biofilm
  • Filamentous moulds
  • Fungal infections
  • Aspergillosis
  • Antifungal drugs

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Fig. 1

References

  • Amin R, Dupuis A, Aaron SD et al (2010) The effect of chronic infection with Aspergillus fumigatus on lung function and hospitalization in patients with cystic fibrosis. Chest 137(1):171–176

    PubMed  CrossRef  Google Scholar 

  • Anaissie EJ, Stratton SL, Dignani MC 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

    PubMed  CrossRef  Google Scholar 

  • Bakaletz LO (2007) Bacterial biofilms in otitis media: evidence and relevance. Pediatr Infect Dis J 26:S17–S19

    PubMed  CrossRef  Google Scholar 

  • Bauernfeind A, Bertele RM, Harms K et al (1987) Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15:270–277

    CAS  PubMed  CrossRef  Google Scholar 

  • Beauvais A, Schmidt C, Guadagnini S et al (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9:1588–1600

    CAS  PubMed  CrossRef  Google Scholar 

  • Beauvais A, Fontaine T, Aimanianda V et al (2014) Aspergillus cell wall and biofilm. Mycopathologia 178:371–377

    PubMed  CrossRef  Google Scholar 

  • Boase S, Valentine R, Singhal D et al (2011) A sheep model to investigate the role of fungal biofilms in sinusitis: fungal and bacterial synergy. Int Forum Allergy Rhinol 1:340–347

    PubMed  CrossRef  Google Scholar 

  • Bom VL, de Castro PA, Winkelstroter LK et al (2015) The Aspergillus fumigatus sitA Phosphatase Homologue Is Important for Adhesion, Cell Wall Integrity, Biofilm Formation, and Virulence. Eukaryot Cell 14:728–744

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Bonhomme J, Chauvel M, Goyard S et al (2011) Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol Microbiol 80:995–1013

    CAS  PubMed  CrossRef  Google Scholar 

  • Branski LK, Al-Mousawi A, Rivero H et al (2009) Emerging infections in burns. Surg Infect (Larchmt) 10:389–397

    CrossRef  Google Scholar 

  • Bueid A, Howard SJ, Moore CB et al (2010) Azole antifungal resistance in Aspergillus fumigatus: 2008 and 2009. J Antimicrob Chemother 65:2116–2118

    CAS  PubMed  CrossRef  Google Scholar 

  • Bugli F, Posteraro B, Papi M et al (2013) In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother 57:1275–1282

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Cannon RD, Lamping E, Holmes AR et al (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22:291–321

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Cetrulo CL Jr, Leto Barone AA, Jordan 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

    PubMed  CrossRef  Google Scholar 

  • Chotirmall SH, O’Donoghue E, Bennett K et al (2010) Sputum Candida albicans presages FEV decline and hospital-treated exacerbations in cystic fibrosis. Chest 138:1186–1195

    PubMed  CrossRef  Google Scholar 

  • Cimon B, Zouhair R, Symoens F et al (2003) Aspergillus terreus in a cystic fibrosis clinic: environmental distribution and patient colonization pattern. J Hosp Infect 53:81–82

    CAS  PubMed  CrossRef  Google Scholar 

  • da Silva Ferreira ME, Capellaro JL, dos Reis ME et al (2004) In vitro evolution of itraconazole resistance in Aspergillus fumigatus involves multiple mechanisms of resistance. Antimicrob Agents Chemother 48:4405–4413

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Delhaes L, Monchy S, Frealle E et al (2012) The airway microbiota in cystic fibrosis: a complex fungal and bacterial community–implications for therapeutic management. PLoS ONE 7:e36313

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Denning DW (1998) Invasive aspergillosis. Clin Infect Dis 26:781–803

    CAS  PubMed  CrossRef  Google Scholar 

  • Denning DW, Tucker RM, Hanson LH et al (1989) Treatment of invasive aspergillosis with itraconazole. Am J Med 86:791–800

    CAS  PubMed  CrossRef  Google Scholar 

  • Denning DW, Cadranel J, Beigelman-Aubry C et al (2016) Chronic pulmonary aspergillosis: rationale and clinical guidelines for diagnosis and management. Eur Respir J 47:45–68

    PubMed  CrossRef  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Dowd SE, Delton Hanson J, Rees E et al (2011) Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care 20:40–47

    CAS  PubMed  CrossRef  Google Scholar 

  • Ebbens FA, Georgalas C, Fokkens WJ (2009a) The mold conundrum in chronic hyperplastic sinusitis. Curr Allergy Asthma Rep 9:114–120

    PubMed  CrossRef  Google Scholar 

  • Ebbens FA, Georgalas C, Fokkens WJ (2009b) Fungus as the cause of chronic rhinosinusitis: the case remains unproven. Curr Opin Otolaryngol Head Neck Surg 17:43–49

    PubMed  CrossRef  Google Scholar 

  • Escande W, Fayad G, Modine T 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

    PubMed  CrossRef  Google Scholar 

  • Fan Z, Li Z, Xu Z et al (2015) cspA influences biofilm formation and drug resistance in pathogenic fungus Aspergillus fumigatus. BioMed Res Int 2015:960357

    PubMed  PubMed Central  Google Scholar 

  • Fanning S, Mitchell AP (2012) Fungal biofilms. PLoS Pathog 8:e1002585

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Fanning S, Xu W, Solis N et al (2012) Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell 11:896–904

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Fazli M, Bjarnsholt T, Kirketerp-Moller K et al (2009) Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47:4084–4089

    PubMed  PubMed Central  CrossRef  Google Scholar 

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

    CAS  PubMed  CrossRef  Google Scholar 

  • Foreman A, Jervis-Bardy J, Wormald PJ (2011) Do biofilms contribute to the initiation and recalcitrance of chronic rhinosinusitis? Laryngoscope 121:1085–1091

    PubMed  CrossRef  Google Scholar 

  • Fraczek MG, Bromley M, Buied A et al (2013) The cdr1B efflux transporter is associated with non-cyp51a-mediated itraconazole resistance in Aspergillus fumigatus. J Antimicrob Chemother 68:1486–1496

    CAS  PubMed  CrossRef  Google Scholar 

  • Golmia R, Bello I, Marra A et al (2011) Aspergillus fumigatus joint infection: a review. Semin Arthritis Rheum 40:580–584

    PubMed  CrossRef  Google Scholar 

  • Goncalves SS, Souza AC, Chowdhary A et al (2016) Epidemiology and molecular mechanisms of antifungal resistance in Candida and Aspergillus. Mycoses. doi:10.1111/myc.12469

    PubMed  Google Scholar 

  • Gravelat FN, Doedt T, Chiang LY et al (2008) In vivo analysis of Aspergillus fumigatus developmental gene expression determined by real-time reverse transcription-PCR. Infect Immun 76:3632–3639

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Gravelat FN, Ejzykowicz DE, Chiang LY et al (2010) Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol 12:473–488

    CAS  PubMed  CrossRef  Google Scholar 

  • Grosjean P, Weber R (2007) Fungus balls of the paranasal sinuses: a review. Eur Arch Otorhinolaryngol 264:461–470

    PubMed  CrossRef  Google Scholar 

  • Gutierrez-Correa M, Ludena Y, Ramage G et al (2012) Recent advances on filamentous fungal biofilms for industrial uses. Appl Biochem Biotechnol 167:1235–1253

    CAS  PubMed  CrossRef  Google Scholar 

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

    CAS  PubMed  CrossRef  Google Scholar 

  • Hoiby N, Bjarnsholt T, Moser C et al (2015) ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clin Microbiol Infect 21:S1–S25

    PubMed  CrossRef  Google Scholar 

  • Howard SJ, Cerar D, Anderson MJ et al (2009) Frequency and evolution of Azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15:1068–1076

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Jayshree RS, Shafiulla M, George J 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

    CAS  PubMed  CrossRef  Google Scholar 

  • Jeloka TK, Shrividya S, Wagholikar G et al (2011) Catheter outflow obstruction due to an aspergilloma. Perit Dial Int 31:211–212

    CAS  PubMed  Google Scholar 

  • Karkas A, Rtail R, Reyt E et al (2013) Sphenoid sinus fungus ball. Eur Arch Otorhinolaryngol 270:893–898

    PubMed  CrossRef  Google Scholar 

  • Keir J, Pedelty L, Swift AC et al (2011) Biofilms in chronic rhinosinusitis: systematic review and suggestions for future research. J Laryngol Otol 125:331–337

    CAS  PubMed  CrossRef  Google Scholar 

  • Krappmann S, Ramage G (2013) A sticky situation: extracellular DNA shapes Aspergillus fumigatus biofilms. Front Microbiol 4:159

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Langer P, Kassim RA, Macari GS et al (2003) Aspergillus infection after total knee arthroplasty. Am J Orthop 32:402–404

    PubMed  Google Scholar 

  • Leclair LW, Hogan DA (2010) Mixed bacterial-fungal infections in the CF respiratory tract. Med Mycol 48:S125–S132

    PubMed  CrossRef  Google Scholar 

  • Leroux S, Ullmann AJ (2013) Management and diagnostic guidelines for fungal diseases in infectious diseases and clinical microbiology: critical appraisal. Clin Microbiol Infect 19:1115–1121

    CAS  PubMed  CrossRef  Google Scholar 

  • Lutz L, Pereira DC, Paiva RM et al (2012) Macrolides decrease the minimal inhibitory concentration of anti-pseudomonal agents against Pseudomonas aeruginosa from cystic fibrosis patients in biofilm. BMC Microbiol 12:196

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Maertens J, Marchetti O, Herbrecht R et al (2011) European guidelines for antifungal management in leukemia and hematopoietic stem cell transplant recipients: summary of the ECIL 3–2009 update. Bone Marrow Transplant 46:709–718

    CAS  PubMed  CrossRef  Google Scholar 

  • Martin TJ, Kerschner JE, Flanary VA (2005) Fungal causes of otitis externa and tympanostomy tube otorrhea. Int J Pediatr Otorhinolaryngol 69:1503–1508

    PubMed  CrossRef  Google Scholar 

  • Mellado E, Garcia-Effron G, Alcazar-Fuoli L et al (2007) A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alterations. Antimicrob Agents Chemother 51:1897–1904

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Meneau I, Sanglard D et al (2005) Azole and fungicide resistance in clinical and environmental Aspergillus fumigatus isolates. Med Mycol 43:S307–S311

    CAS  PubMed  CrossRef  Google Scholar 

  • Moree WJ, Phelan VV, Wu CH et al (2012) Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc Natl Acad Sci U S A 109:13811–13816

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Morschhauser J (2010) Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol 47:94–106

    PubMed  CrossRef  CAS  Google Scholar 

  • Mosquera J, Denning DW (2002) Azole cross-resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 46:556–557

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Mowat E, Butcher J, Lang S et al (2007) Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol 56:1205–1212

    CAS  PubMed  CrossRef  Google Scholar 

  • Mowat E, Lang S, Williams C et al (2008a) Phase-dependent antifungal activity against Aspergillus fumigatus developing multicellular filamentous biofilms. J Antimicrob Chemother 62:1281–1284

    CAS  PubMed  CrossRef  Google Scholar 

  • Mowat E, Williams C, Jones B et al (2008b) The characteristics of Aspergillus fumigatus mycetoma development: is this a biofilm? Med Mycol 47:S120–S126

    PubMed  CrossRef  CAS  Google Scholar 

  • Mowat E, Rajendran R, Williams C et al (2010) Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett 313:96–102

    CAS  PubMed  CrossRef  Google Scholar 

  • Nascimento AM, Goldman GH, Park S et al (2003) Multiple resistance mechanisms among Aspergillus fumigatus mutants with high-level resistance to itraconazole. Antimicrob Agents Chemother 47:1719–1726

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Nett JE, Sanchez H, Cain MT et al (2010) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202:171–175

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Nierman WC, Pain A, Anderson MJ et al (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156

    CAS  PubMed  CrossRef  Google Scholar 

  • Nobile CJ, Mitchell AP et al (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8:1382–1391

    CAS  PubMed  CrossRef  Google Scholar 

  • Odds F (1988) Candida and candidosis, 2nd edn. Bailliere Tindall, London

    Google Scholar 

  • O’Donnell LE, Millhouse E, Sherry L et al (2015) Polymicrobial Candida biofilms: friends and foe in the oral cavity. FEMS Yeast Res 15:pii: fov077

    CrossRef  Google Scholar 

  • Oren I, Rowe JM, Sprecher H et al (2006) A prospective randomized trial of itraconazole vs fluconazole for the prevention of fungal infections in patients with acute leukemia and hematopoietic stem cell transplant recipients. Bone Marrow Transplant 38:127–134

    CAS  PubMed  CrossRef  Google Scholar 

  • Peters BM, Jabra-Rizk MA, O’May GA et al (2012) Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25:193–213

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Pihet M, Carrere J, Cimon B et al (2009) Occurrence and relevance of filamentous fungi in respiratory secretions of patients with cystic fibrosis--a review. Med Mycol 47:387–397

    PubMed  CrossRef  Google Scholar 

  • Raad II, Hanna HA, Boktour M et al (2008) Novel antifungal agents as salvage therapy for invasive aspergillosis in patients with hematologic malignancies: posaconazole compared with high-dose lipid formulations of amphotericin B alone or in combination with caspofungin. Leukemia 22:496–503

    CAS  PubMed  CrossRef  Google Scholar 

  • Rajendran R, Mowat E, McCulloch E et al (2011) Azole resistance of Aspergillus fumigatus biofilms is partly associated with efflux pump activity. Antimicrob Agents Chemother 55:2092–2097

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

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

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Rajendran R, Mowat E, Jones B et al (2015) Prior in vitro exposure to voriconazole confers resistance to amphotericin B in Aspergillus fumigatus biofilms. Int J Antimicrob Agents 46:342–345

    CAS  PubMed  CrossRef  Google Scholar 

  • Ramage G, Williams C (2013) The clinical importance of fungal biofilms. Adv Appl Microbiol 84:27–83

    CAS  PubMed  CrossRef  Google Scholar 

  • Ramage G, VandeWalle K, Lopez-Ribot JL et al (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

    CAS  PubMed  CrossRef  Google Scholar 

  • Ramage G, Mowat E, Jones B et al (2009) Our current understanding of fungal biofilms. Crit Rev Microbiol 35:340–355

    CAS  PubMed  CrossRef  Google Scholar 

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

    CAS  PubMed  CrossRef  Google Scholar 

  • Ramage G, Rajendran R, Sherry L et al (2012) Fungal biofilm resistance. Int J Microbiol 2012:528521

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Richardson M (2009) The ecology of the Zygomycetes and its impact on environmental exposure. Clin Microbiol Infect 15:2–9

    PubMed  CrossRef  Google Scholar 

  • Robbins N, Uppuluri P, Nett J et al (2011) Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog 7:e1002257

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Rosenblatt WB, Pollock A (1997) Aspergillus flavus cultured from a saline-filled implant. Plast Reconstr Surg 99:1470–1472

    CAS  PubMed  CrossRef  Google Scholar 

  • Rowe SM, Miller S, Sorscher EJ (2005) Mechanisms of disease: cystic fibrosis. New Engl J Med 352:1992–2001

    CAS  PubMed  CrossRef  Google Scholar 

  • Sambatakou H, Dupont B, Lode H et al (2006) Voriconazole treatment for subacute invasive and chronic pulmonary aspergillosis. Am J Med 119(527):e517–e524

    Google Scholar 

  • Sato FR, Sawazaki R, Berretta D et al (2010) Aspergillosis of the maxillary sinus associated with a zygomatic implant. J Am Dent Assoc 141:1231–1235

    PubMed  CrossRef  Google Scholar 

  • Sayed SI, Datta S, Deore N et al (2012) Prevention of voice prosthesis biofilms: current scenario and future trends in prolonging prosthesis lifetime. J Indian Med Assoc 110(175–178):180

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Seth AK, Geringer MR, Hong SJ et al (2012) In vivo modeling of biofilm-infected wounds: a review. J Surg Res 178:330–338

    PubMed  CrossRef  Google Scholar 

  • Shopova I, Bruns S, Thywissen A et al (2013) Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus. Front Microbiol 4:141

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Short DP, O’Donnell K, Zhang N et al (2011) Widespread occurrence of diverse human pathogenic types of the fungus Fusarium detected in plumbing drains. J Clin Microbiol 49:4264–4272

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Sibley CD, Duan K, Fischer C et al (2008a) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4:e1000184

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Sibley CD, Parkins MD, Rabin HR 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

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Singh PK, Schaefer AL, Parsek MR et al (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764

    CAS  PubMed  CrossRef  Google Scholar 

  • Singhal D, Baker L, Wormald PJ et al (2011) Aspergillus fumigatus biofilm on primary human sinonasal epithelial culture. Am J Rhinol Allergy 25:219–225

    PubMed  CrossRef  Google Scholar 

  • Siqueira VM, Oliveira HM, Santos C et al (2011) Filamentous fungi in drinking water, particularly in relation to biofilm formation. Int J Environ Res Public Health 8:456–469

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Smith K, Rajendran R, Kerr S et al (2015) Aspergillus fumigatus enhances elastase production in Pseudomonas aeruginosa co-cultures. Med Mycol 53:645–655

    PubMed  CrossRef  Google Scholar 

  • Snelders E, van der Lee HA, Kuijpers J et al (2008) Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med 5:e219

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Snelders E, Karawajczyk A, Schaftenaar G et al (2010) Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrob Agents Chemother 54:2425–2430

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Sudfeld CR, Dasenbrook EC, Merz WG et al (2010) Prevalence and risk factors for recovery of filamentous fungi in individuals with cystic fibrosis. J Cyst Fibros Off J Eur Cyst Fibros Soc 9:110–116

    CrossRef  Google Scholar 

  • Tondervik A, Sletta H, Klinkenberg G et al (2014) Alginate oligosaccharides inhibit fungal cell growth and potentiate the activity of antifungals against Candida and Aspergillus spp. PLoS ONE 9:e112518

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Ullmann AJ, Cornely OA, Donnelly JP et al (2012) ESCMID* guideline for the diagnosis and management of Candida diseases 2012: developing European guidelines in clinical microbiology and infectious diseases. Clin Microbiol Infect 18:1–8

    CAS  PubMed  CrossRef  Google Scholar 

  • Uppuluri P, Chaturvedi AK, Srinivasan A et al (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6:e1000828

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Walsh TJ, Anaissie EJ, Denning DW et al (2008) Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 46:327–360

    CAS  PubMed  CrossRef  Google Scholar 

  • Warkentien T, Rodriguez C, Lloyd B et al (2012) Invasive mold infections following combat-related injuries. Clin Infect Dis 55:1441–1449

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Williams C, Ramage G (2015) Fungal biofilms in human disease. Adv Exp Med Biol 831:11–27

    PubMed  CrossRef  Google Scholar 

  • Winkelstroter LK, Bom VL, de Castro PA et al (2015) High osmolarity glycerol response PtcB phosphatase is important for Aspergillus fumigatus virulence. Mol Microbiol 96:42–54

    PubMed  CrossRef  CAS  Google Scholar 

  • Wolcott RD, Gontcharova V, Sun Y et al (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

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Yao M, Messner AH (2001) Fungal malignant otitis externa due to Scedosporium apiospermum. Ann Otol Rhinol Laryngol 110:377–380

    CAS  PubMed  CrossRef  Google Scholar 

  • Young RC, Bennett JE, Vogel CL et al (1970) Aspergillosis. The spectrum of the disease in 98 patients. Medicine (Baltimore) 49:147–173

    CAS  CrossRef  Google Scholar 

  • Zhao X, Daniels KJ, Oh SH et al (2006) Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152:2287–2299

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

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Williams, C., Rajendran, R., Ramage, G. (2016). Aspergillus Biofilms in Human Disease. In: Imbert, C. (eds) Fungal Biofilms and related infections. Advances in Experimental Medicine and Biology(), vol 931. Springer, Cham. https://doi.org/10.1007/5584_2016_4

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