Bacterial-induced epithelial damage promotes fungal biofilm formation in a sheep model of sinusitis

International Forum of Allergy and Rhinology

Volumn 3, Issue 5, 2013, Pages 341-348

  Boase, Sam ^a   Jervis Bardy, Joshua ^a   Cleland, Edward ^a   Pant, Harshita ^a   Tan, Lorwai ^a   Wormald, Peter John ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Bacteria; Biofilms; Chronic rhinosinusitis; Cilia; Epithelial damage fungus; Fungal sinusitis

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; BIOFILM; CONFOCAL SCANNING LASER OPHTHALMOSCOPE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FRONTAL SINUS; FUNGUS; HAEMOPHILUS INFLUENZAE; INFLAMMATION; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SHEEP; SINUSITIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; BACTERIAL INFECTIONS; BACTERIAL TOXINS; BIOFILMS; CHRONIC DISEASE; CILIA; DISEASE MODELS, ANIMAL; HUMANS; NASAL MUCOSA; RESPIRATORY MUCOSA; RHINITIS; SHEEP; SINUSITIS;

EID: 84878195184     PISSN: 20426976     EISSN: 20426984     Source Type: Journal    
DOI: 10.1002/alr.21138     Document Type: Article

References (60)

1. Safirstein BH. Allergic bronchopulmonary aspergillosis with obstruction of the upper respiratory tract. Chest. 1976;70:788-790.
2. Millar J, Johnston A, Lamb D. Proceedings of the Scottish Thoracic Society and the Thoracic Society: allergic aspergillosis of the maxillary sinuses. Thorax. 1981;36:710.
3. Bent JP 3rd, Kuhn FA. Diagnosis of allergic fungal sinusitis. Otolaryngol Head Neck Surg. 1994;111:580-588.
4. Marple B, Newcomer M, Schwade N, Mabry R. Natural history of allergic fungal rhinosinusitis: a 4- to 10-year follow-up. Otolaryngol Head Neck Surg. 2002;127:361-366.
5. Marple BF. Allergic fungal rhinosinusitis: current theories and management strategies. Laryngoscope. 2001;111:1006-1019.
6. Kupferberg SB, Bent JP 3rd, Kuhn FA. Prognosis for allergic fungal sinusitis. Otolaryngol Head Neck Surg. 1997;117:35-41.
7. Lynch AS, Robertson GT. Bacterial and fungal biofilm infections. Ann Rev Med. 2008;59:415-428.
8. Cristobal R, Edmiston CE Jr, Runge-Samuelson CL, Owen HA, Firszt JB, Wackym PA. Fungal biofilm formation on cochlear implant hardware after antibiotic-induced fungal overgrowth within the middle ear. Pediatr Infect Dis J. 2004;23:774-778.
9. Healy DY, Leid JG, Sanderson AR, Hunsaker DH. Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2008;138:641-647.
10. Foreman A, Psaltis AJ, Tan LW, Wormald PJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy. 2009;23:556-561.
11. Boase S, Valentine R, Singhal D, Tan LW, Wormald PJ. A sheep model to investigate the role of fungal biofilms in sinusitis: fungal and bacterial synergy. Int Forum Allergy Rhinol. 2011;1:340-347.
12. Valentine R, Jervis-Bardy J, Psaltis A, Tan LW, Wormald PJ. Efficacy of using a hydrodebrider and of citric acid/zwitterionic surfactant on a Staphylococcus aureus bacterial biofilm in the sheep model of rhinosinusitis. Am J Rhinol Allergy. 2011;25:323-326.
13. Tamashiro E, Banks CA, Chen B, et al. In vivo effects of citric acid/zwitterionic surfactant cleansing solution on rabbit sinus mucosa. Am J Rhinol Allergy. 2009;23:597-601.
14. Singhal D, Baker L, Wormald PJ, Tan L. Aspergillus fumigatus biofilm on primary human sinonasal epithelial culture. Am J Rhinol Allergy. 2011;25:219-225.
15. Khalid A, Woodworth B, Prince A, et al. Physiologic alterations in the murine model after nasal fungal antigenic exposure. Otolaryngol Head Neck Surg. 2008;139:695-701.
16. Hogardt M, Trebesius K, Geiger AM, Hornef M, Rosenecker J, Heesemann J. Specific and rapid detection by fluorescent in situ hybridization of bacteria in clinical samples obtained from cystic fibrosis patients. J Clin Microbiol. 2000;38:818-825.
17. Ragab A, Clement P. The role of fungi in the airway of chronic rhinosinusitis patients. Curr Opin Allergy Clin Immunol. 2007;7:17-24.
18. Ebbens FA, Georgalas C, Fokkens WJ. Fungus as the cause of chronic rhinosinusitis: the case remains unproven. Curr Opin Otolaryngol Head Neck Surg. 2009;17:43-49.
19. Ponikau J, Sherris D, Kern E, et al. The diagnosis and incidence of allergic fungal sinusitis. Mayo Clin Proc. 1999;74:877-884.
20. Shin SH, Ponikau JU, Sherris DA, et al. Chronic rhinosinusitis: an enhanced immune response to ubiquitous airborne fungi. J Allergy Clin Immunol. 2004;114:1369-1375.
21. Ebbens FA, Georgalas C, Fokkens WJ. The mold conundrum in chronic hyperplastic sinusitis. Curr Allergy Asthma Rep. 2009;9:114-120.
22. Fokkens WJ, Ebbens F, van Drunen CM. Fungus: a role in pathophysiology of chronic rhinosinusitis, disease modifier, a treatment target, or no role at all? Immunol Allergy Clin North Am. 2009;29:677-688.
23. Ryan MW. Allergic fungal rhinosinusitis. Otolaryngol Clin North Am. 2011;44:697-710.
24. Galli J, Calo L, Ardito F, et al. Damage to ciliated epithelium in chronic rhinosinusitis: what is the role of bacterial biofilms? Ann Otol Rhinol Laryngol. 2008;117:902-908.
25. Palmer J. Bacterial biofilms in chronic rhinosinusitis. Ann Otol Rhinol Laryngol Suppl. 2006;196:35-39.
26. Bendouah Z, Barbeau J, Hamad WA, Desrosiers M. Biofilm formation by Staphylococcus aureus and Pseudomonas aeruginosa is associated with an unfavorable evolution after surgery for chronic sinusitis and nasal polyposis. Otolaryngol Head Neck Surg. 2006;134:991-996.
27. Singhal D, Foreman A, Bardy JJ, Wormald PJ. Staphylococcus aureus biofilms: Nemesis of endoscopic sinus surgery. Laryngoscope. 2011;121:1578-1583.
28. Foreman A, Wormald PJ. Different biofilms, different disease? A clinical outcomes study. Laryngoscope. 2010;120:1701-1706.
29. Wilson R, Roberts D, Cole P. Effect of bacterial products on human ciliary function in vitro. Thorax. 1985;40:125-131.
30. Mallants R, Jorissen M, Augustijns P. Beneficial effect of antibiotics on ciliary beat frequency of human nasal epithelial cells exposed to bacterial toxins. J Pharm Pharmacol. 2008;60:437-443.
31. Evans NM, Smith DD, Wicken AJ. Haemin and nicotinamide adenine dinucleotide requirements of Haemophilus influenzae and Haemophilus parainfluenzae. J Med Microbiol. 1974;7:359-365.
32. Turk DC. The pathogenicity of Haemophilus influenzae. J Med Microbiol. 1984;18:1-16.
33. Bragonzi A. Murine models of acute and chronic lung infection with cystic fibrosis pathogens. Int J Med Microbiol. 300:584-593.
34. Ehrlich GD, Veeh R, Wang X, et al. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA. 2002;287:1710-1715.
35. Tong HH, Blue LE, James MA, Chen YP, DeMaria TF. Evaluation of phase variation of nontypeable Haemophilus influenzae lipooligosaccharide during nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect Immun. 2000;68:4593-4597.
36. Fujihara K, Yamanaka N, Ogra PL, Bernstein JM, Hard R. Morphologic and motility changes of nasal cilia in primary culture caused by Haemophilus influenzae. Ann Otol Rhinol Laryngol. 1996;105:452-457.
37. Denny FW. Effect of a toxin produced by Haemophilus influenzae on ciliated respiratory epithelium. J Infect Dis. 1974;129:93-100.
38. Wilson R, Read R, Cole P. Interaction of Haemophilus influenzae with mucus, cilia, and respiratory epithelium. J Infect Dis. 1992;165:S100-S102.
39. Janson H, Carleãån B, Cervin A, et al. Effects on the ciliated epithelium of protein D-producing and - nonproducing nontypeable Haemophilus influenzae in nasopharyngeal tissue cultures. J Infect Dis. 1999;180:737-746.
40. Yeater KM, Chandra J, Cheng G, et al. Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology. 2007;153:2373-2385.
41. Murillo LA, Newport G, Lan CY, Habelitz S, Dungan J, Agabian NM. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell. 2005;4:1562-1573.
42. Thomas DP, Bachmann SP, Lopez-Ribot JL. Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics. 2006;6:5795-5804.
43. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. Our current understanding of fungal biofilms. Crit Rev Microbiol. 2009;35:340-355.
44. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol. 2001;183:5385-5394.
45. Blankenship JR, Mitchell AP. How to build a biofilm: a fungal perspective. Curr Opin Microbiol. 2006;9:588-594.
46. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8:881-890.
47. Ramage G, Rajendran R, Gutierrez-Correa M, Jones B, Williams C. Aspergillus biofilms: clinical and industrial significance. FEMS Microbiol Lett. 2011;324:89-97.
48. Shaw BD, Carroll GC, Hoch HC. Generality of the prerequisite of conidium attachment to a hydrophobic substratum as a signal for germination among Phyllosticta species. Mycologia. 2006;98:186-194.
49. Burge HA. Airborne allergenic fungi. Classification, nomenclature, and distribution. Immunol Allergy Clin North Am. 1989;9:307-319.
50. Chandra J, Mukherjee PK, Leidich SD, et al. Antifungal resistance of Candidal biofilms formed on denture acrylic in vitro. J Dent Res. 2001;80:903-908.
51. Huang HM, Cheng JJ, Liu CM, Lin KN. Mucosal healing and mucociliary transport change after endoscopic sinus surgery in children with chronic maxillary sinusitis. Int J Pediatr Otorhinolaryngol. 2006;70:1361-1367.
52. Bassiouny A, Atef AM, Raouf MA, Nasr SM, Nasr M, Ayad EE. Ultrastructural ciliary changes of maxillary sinus mucosa following functional endoscopic sinus surgery: an image analysis quantitative study. J Laryngol Otol. 2003;117:273-279.
53. Ikeda K, Oshima T, Furukawa M, et al. Restoration of the mucociliary clearance of the maxillary sinus after endoscopic sinus surgery. J Allergy Clin Immunol. 1997;99:48-52.
54. Tong YF, Sun XZ, Li DW. [Observation of maxillary mucosa restoration after the endoscopic sinus surgery operation of chronic sinusitis and nasal polyps]. Zhonghua Er Bi Yan Hou Ke Za Zhi. 2004;39:402-406. [Chinese]
55. Shaw CKL, Cowin A, Wormald PJ. A study of the normal temporal healing pattern and the mucociliary transport after endoscopic partial and full-thickness removal of nasal mucosa in sheep. Immunol Cell Biol. 2001;79:145-148.
56. Abdel-Hak B, Gunkel A, Kanonier G, Schrott-Fischer A, Ulmer H, Thumfart W. Ciliary beat frequency, olfaction and endoscopic sinus surgery. ORL J Otorhinolaryngol Relat Spec. 1998;60:202-205.
57. Schubert MS, Goetz DW. Evaluation and treatment of allergic fungal sinusitis. II. Treatment and follow-up. J Allergy Clin Immunol. 1998;102:395-402.
58. Ikram M, Abbas A, Suhail A, Onali MA, Akhtar S, Iqbal M. Management of allergic fungal sinusitis with postoperative oral and nasal steroids: a controlled study. Ear Nose Throat J. 2009;88:E8-E11.
59. Netea MG, Ferwerda G, van der Graaf CAA, Van der Meer JWM, Kullberg BJ. Recognition of fungal pathogens by toll-like receptors. Curr Pharm Des. 2006;12:4195-4201.
60. Weindl G, Naglik JR, Kaesler S, et al. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J Clin Invest. 2007;117:3664-3672.