Skip to main content

Advertisement

SpringerLink
Log in

Role of Bacterial and Fungal Biofilms in Chronic Rhinosinusitis

  • Sinusitis (ML Kowalski, Section Editor)
  • Published:
Current Allergy and Asthma Reports Aims and scope Submit manuscript

Abstract

Chronic rhinosinusitis (CRS) is a very common condition that remains poorly understood from a pathogenic standpoint. Recent interest has been sparked by a potential role for biofilms in this process, with a significant body of evidence implicating them in inciting sinonasal inflammation. Biofilms are clearly present on the sinus mucosa of CRS patients, and their presence there is associated with severe disease characteristics and surgical recalcitrance. We are beginning to understand the importance of the species within these biofilms, but there may be other as-yet-unidentified factors at play in influencing disease outcomes. Recent exciting research has emerged documenting the immune response to the presence of biofilms—research that will ultimately solidify the nature and extent of the contribution of biofilms in CRS pathogenesis. Future research should focus on evidence-based antibiofilm treatments with reference to efficacy and timing of treatment.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Gliklich RE, Metson R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngol Head Neck Surg. 1995;113:104–9.

    Article  PubMed  CAS  Google Scholar 

  2. Bhattacharyya N. The economic burden and symptom manifestations of chronic rhinosinusitis. Am J Rhinol. 2003;17:27–32.

    PubMed  Google Scholar 

  3. Blackwell DL, Collins JG, Coles R. Summary health statistics for U.S. adults: National Health Interview Survey, 1997. Vital Health Stat. 2002;10:1–109.

    Google Scholar 

  4. Collins JG. Prevalence of selected chronic conditions: United States, 1990–1992. Vital Health Stat. 1997;10:1–89.

    Google Scholar 

  5. Statistics ABo. National Health Survey: summary of results, Australia 2004–05. 2006; cat no. 4364.0.

  6. Van Zele T, Claeys S, Gevaert P, et al. Differentiation of chronic sinus diseases by measurement of inflammatory mediators. Allergy. 2006;61:1280–9.

    Article  PubMed  Google Scholar 

  7. Chiu AG. Osteitis in chronic rhinosinusitis. Otolaryngol Clin North Am. 2005;38:1237–42.

    Article  PubMed  Google Scholar 

  8. Lanza DC, Dhong HJ, Tantilipikorn P, et al. Fungus and chronic rhinosinusitis: from bench to clinical understanding. Ann Otol Rhinol Laryngol. 2006;196:27–34.

    Google Scholar 

  9. Bachert C, Zhang N, Patou J, et al. Role of staphylococcal superantigens in upper airway disease. Curr Opin Allergy Clin Immunol. 2008;8:34–8.

    Article  PubMed  CAS  Google Scholar 

  10. Kern RC, Conley DB, Walsh W, et al. Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis. Am J Rhinol. 2008;22:549–59.

    Article  PubMed  Google Scholar 

  11. Brook I. The role of bacteria in chronic rhinosinusitis. Otolaryngol Clin North Am. 2005;38:1171–92.

    Article  PubMed  Google Scholar 

  12. Wolcott RD, Ehrlich GD. Biofilms and chronic infections. JAMA. 2008;299:2682–4.

    Article  PubMed  CAS  Google Scholar 

  13. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.

    Article  PubMed  CAS  Google Scholar 

  14. Nobel Lectures, Physiology and Medicine 1901–1921. Amsterdam: Elsevier Publishing Company; 1967.

  15. Costerton JW, Lewandowski Z, Caldwell DE, et al. Microbial biofilms. Annu Rev Microbiol. 1995;49:711–45.

    Article  PubMed  CAS  Google Scholar 

  16. Potera C. Forging a link between biofilms and disease. Science. 1999;283:1837–9.

    Article  PubMed  CAS  Google Scholar 

  17. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–93.

    Article  PubMed  CAS  Google Scholar 

  18. de Beer D, Stoodley P, Roe F, Lewandowski Z. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng. 1994;43:1131–8.

    Article  PubMed  Google Scholar 

  19. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135–8.

    Article  PubMed  CAS  Google Scholar 

  20. Ehrlich GD, Veeh R, Wang X, et al. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA. 2002;287:1710–5.

    Article  PubMed  Google Scholar 

  21. Chole RA, Faddis BT. Evidence for microbial biofilms in cholesteatomas. Arch Otolaryngol Head Neck Surg. 2002;128:1129–33.

    PubMed  Google Scholar 

  22. Chole RA, Faddis BT. Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol Head Neck Surg. 2003;129:634–6.

    Article  PubMed  Google Scholar 

  23. Antonelli PJ, Lee JC, Burne RA. Bacterial biofilms may contribute to persistent cochlear implant infection. Otol Neurotol. 2004;25:953–7.

    Article  PubMed  Google Scholar 

  24. Post JC. Direct evidence of bacterial biofilms in otitis media. Laryngoscope. 2001;111:2083–94.

    Article  PubMed  CAS  Google Scholar 

  25. Perkins J, Mouzakes J, Pereira R, Manning S. Bacterial biofilm presence in pediatric tracheotomy tubes. Arch Otolaryngol Head Neck Surg. 2004;130:339–43.

    Article  PubMed  Google Scholar 

  26. Cryer J, Schipor I, Perloff JR, Palmer JN. Evidence of bacterial biofilms in human chronic sinusitis. ORL J Otorhinolaryngol Relat Spec. 2004;66:155–8.

    Article  PubMed  Google Scholar 

  27. Sanclement JA, Webster P, Thomas J, Ramadan HH. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope. 2005;115:578–82.

    Article  PubMed  Google Scholar 

  28. Ferguson BJ, Stolz DB. Demonstration of biofilm in human bacterial chronic rhinosinusitis. Am J Rhinol. 2005;19:452–7.

    PubMed  Google Scholar 

  29. Psaltis AJ, Ha KR, Beule AG, et al. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope. 2007;117:1302–6.

    Article  PubMed  Google Scholar 

  30. Bezerra TF, Padua FG, Gebrim EM, et al. Biofilms in chronic rhinosinusitis with nasal polyps. Otolaryngol Head Neck Surg. 2011;144:612–6.

    Article  PubMed  Google Scholar 

  31. Mladina R, Skitarelic N, Music S, Ristic M. A biofilm exists on healthy mucosa of the paranasal sinuses: a prospectively performed, blinded, scanning electron microscope study. Clin Otolaryngol. 2010;35:104–10.

    Article  PubMed  CAS  Google Scholar 

  32. Healy DY, Leid JG, Sanderson AR, Hunsaker DH. Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2008;138:641–7.

    Article  PubMed  Google Scholar 

  33. Sanderson AR, Leid JG, Hunsaker D. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope. 2006;116:1121–6.

    Article  PubMed  Google Scholar 

  34. Ha KR, Psaltis AJ, Tan L, Wormald PJ. A sheep model for the study of biofilms in rhinosinusitis. Am J Rhinol. 2007;21:339–45.

    Article  PubMed  Google Scholar 

  35. Ramadan HH, Sanclement JA, Thomas JG. Chronic rhinosinusitis and biofilms. Otolaryngol Head Neck Surg. 2005;132:414–7.

    Article  PubMed  Google Scholar 

  36. Foreman A, Psaltis AJ, Tan LW, Wormald PJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy. 2009;23:556–61.

    Article  PubMed  Google Scholar 

  37. Zernotti ME, Angel Villegas N, Roques Revol M, et al. Evidence of bacterial biofilms in nasal polyposis. J Investig Allergol Clin Immunol. 2010;20:380–5.

    PubMed  CAS  Google Scholar 

  38. • Stephenson MF, Mfuna L, Dowd SE et al. Molecular characterization of the polymicrobial flora in chronic rhinosinusitis. J Otolaryngol Head Neck Surg. 2010;39:182–187. This was the first report using novel molecular detection techniques to provide insights into the diverse bacterial communities present in the sinuses. It will represent the gold standard for future bacterial detection in CRS.

    PubMed  Google Scholar 

  39. Stressmann FA, Rogers GB, Chan SW, et al. Characterization of bacterial community diversity in chronic rhinosinusitis infections using novel culture-independent techniques. Am J Rhinol Allergy. 2011;25:e133–40.

    Article  PubMed  Google Scholar 

  40. Foreman A, Singhal D, Psaltis AJ, Wormald PJ. Targeted imaging modality selection for bacterial biofilms in chronic rhinosinusitis. Laryngoscope. 120:427–431.

  41. Ebbens FA, Georgalas C, Fokkens WJ. The mold conundrum in chronic hyperplastic sinusitis. Curr Allergy Asthma Rep. 2009;9:114–20.

    Article  PubMed  Google Scholar 

  42. Singhal D, Baker L, Wormald PJ, Tan L. Aspergillus fumigatus biofilm on primary human sinonasal epithelial culture. Am J Rhinol Allergy. 2011;25:219–25.

    Article  PubMed  Google Scholar 

  43. Hochstim CJ, Choi JY, Lowe D et al. Biofilm detection with hematoxylin-eosin staining. Arch Otolaryngol Head Neck Surg. 136:453–456.

  44. Boase S, Valentine R, Singhal D et al. A sheep model to investigate the role of fungal biofilms in sinusitis: fungal and bacterial synergy. Int Forum Allergy Rhinol. 2011;1:340–7.

    Google Scholar 

  45. Foreman A, Wormald PJ. Different biofilms, different disease? A clinical outcomes study. Laryngoscope. 120:1701–1706.

  46. Singhal D, Foreman A, Bardy JJ, Wormald PJ. Staphylococcus aureus biofilms: nemesis of endoscopic sinus surgery. Laryngoscope. 2011;121:1578–83.

    Article  PubMed  Google Scholar 

  47. Psaltis AJ, Weitzel EK, Ha KR, Wormald PJ. The effect of bacterial biofilms on post-sinus surgical outcomes. Am J Rhinol. 2008;22:1–6.

    Article  PubMed  Google Scholar 

  48. Singhal D, Psaltis AJ, Foreman A, Wormald PJ. The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy. 24:169–174.

  49. You H, Zhuge P, Li D, et al. Factors affecting bacterial biofilm expression in chronic rhinosinusitis and the influences on prognosis. Am J Otolaryngol. 2011.

  50. Zhang Z, Kofonow JM, Finkelman BS, et al. Clinical factors associated with bacterial biofilm formation in chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2011;144:457–62.

    Article  PubMed  Google Scholar 

  51. Hochstim CJ, Masood R, Rice DH. Biofilm and persistent inflammation in endoscopic sinus surgery. Otolaryngol Head Neck Surg. 2010;143:697–8.

    Article  PubMed  Google Scholar 

  52. 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;134:991–6.

    Article  PubMed  Google Scholar 

  53. Psaltis AJ, Wormald PJ, Ha KR, Tan LW. Reduced levels of lactoferrin in biofilm-associated chronic rhinosinusitis. Laryngoscope. 2008;118:895–901.

    Article  PubMed  CAS  Google Scholar 

  54. Tan L, Psaltis A, Baker LM, et al. Aberrant mucin glycoprotein patterns of chronic rhinosinusitis patients with bacterial biofilms. Am J Rhinol Allergy. 2010;24:319–24.

    Article  PubMed  Google Scholar 

  55. 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;117:902–8.

    PubMed  Google Scholar 

  56. Wood AJ, Fraser J, Swift S, et al. Are biofilms associated with an inflammatory response in chronic rhinosinusitis? Int Forum Allergy Rhinol. 2011;1:335–9.

    Google Scholar 

  57. Hekiert AM, Kofonow JM, Doghramji L, et al. Biofilms correlate with TH1 inflammation in the sinonasal tissue of patients with chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2009;141:448–53.

    Article  PubMed  Google Scholar 

  58. • Foreman A, Holtappels G, Psaltis AJ, et al. Adaptive immune responses in Staphylococcus aureus biofilm-associated chronic rhinosinusitis. Allergy. 2011;66:1449–1456. This study solidifies biofilms in CRS pathogenesis and provides new targets for research and therapy by associating S. aureus biofilms with a Th2 skewing of the host adaptive immune response, dependent on and independent of the superantigen pathway.

    Article  PubMed  CAS  Google Scholar 

  59. Bachert C, Zhang N, van Zele T, et al. Staphylococcus aureus enterotoxins as immune stimulants in chronic rhinosinusitis. Clin Allergy Immunol. 2007;20:163–75.

    PubMed  CAS  Google Scholar 

  60. Seiberling KA, Grammer L, Kern RC. Chronic rhinosinusitis and superantigens. Otolaryngol Clin North Am. 2005;38:1215–36. ix.

    Article  PubMed  Google Scholar 

  61. Zhang N, Gevaert P, van Zele T, et al. An update on the impact of Staphylococcus aureus enterotoxins in chronic sinusitis with nasal polyposis. Rhinology. 2005;43:162–8.

    PubMed  CAS  Google Scholar 

  62. Berglundh T, Donati M. Aspects of adaptive host response in periodontitis. J Clin Periodontol. 2005;32 Suppl 6:87–107.

    Article  PubMed  CAS  Google Scholar 

  63. Cullinan MP, Hamlet SM, Westerman B, et al. Acquisition and loss of Porphyromonas gingivalis, Actinobacillus actinomycetemcomitans and Prevotella intermedia over a 5-year period: effect of a triclosan/copolymer dentifrice. J Clin Periodontol. 2003;30:532–41.

    Article  PubMed  CAS  Google Scholar 

  64. Mulligan RM, Atkinson C, Vertegel AA, et al. Cigarette smoke extract stimulates interleukin-8 production in human airway epithelium and is attenuated by superoxide dismutase in vitro. Am J Rhinol Allergy. 2009;23:e1–4.

    Article  PubMed  Google Scholar 

  65. • Goldstein-Daruech N, Cope EK, Zhao KQ, et al. Tobacco smoke mediated induction of sinonasal microbial biofilms. PLoS One. 2011;6:e15700. This is a novel paper documenting the effect of cigarette smoke on the sinus microbiome, in particular demonstrating its impact on the biofilm mode of bacterial growth.

    Article  PubMed  CAS  Google Scholar 

  66. Zhang Z, Han D, Zhang S, et al. Biofilms and mucosal healing in postsurgical patients with chronic rhinosinusitis. Am J Rhinol Allergy. 2009;23:506–11.

    Article  PubMed  Google Scholar 

  67. Le T, Psaltis A, Tan LW, Wormald PJ. The efficacy of topical antibiofilm agents in a sheep model of rhinosinusitis. Am J Rhinol. 2008;22:560–7.

    Article  PubMed  Google Scholar 

  68. Heydorn A, Nielsen AT, Hentzer M, et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology. 2000;146(Pt 10):2395–407.

    PubMed  CAS  Google Scholar 

  69. Singhal D, Boase S, Field J et al. Quantitative analysis of in vivo mucosal bacterial biofilms. Int Forum Allergy Immunol. 2011;In press.

Download references

Disclosure

Dr. Wormald receives royalties from Medtronic and serves as a consultant for NeilMed Pharmaceuticals.

Drs. Foreman, Boase, and Psaltis reported no potential conflicts of interest relevant to this article.

Author information

Authors and Affiliations

  1. Department of Otorhinolaryngology, Head, and Neck Surgery, The Queen Elizabeth Hospital, 28 Woodville Road, Woodville, South Australia, 5011, Australia

    Andrew Foreman, Sam Boase, Alkis Psaltis & Peter-John Wormald

Authors
  1. Andrew Foreman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sam Boase
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alkis Psaltis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter-John Wormald
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter-John Wormald.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Foreman, A., Boase, S., Psaltis, A. et al. Role of Bacterial and Fungal Biofilms in Chronic Rhinosinusitis. Curr Allergy Asthma Rep 12, 127–135 (2012). https://doi.org/10.1007/s11882-012-0246-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11882-012-0246-7

Keywords

Search

Navigation