Skip to main content
SpringerLink
Log in

Relationship between biofilms and clinical features in patients with sinus fungal ball

  • Rhinology
  • Published:
European Archives of Oto-Rhino-Laryngology Aims and scope Submit manuscript

Abstract

The presence of bacterial biofilms (BBF) and fungal biofilms (FBF) is associated with greater disease severity in chronic rhinosinusitis. However, researches on biofilms in fungal rhinosinusitis are rare. This study investigated the relationship between biofilms and clinical features in patients with sinus fungal ball (SFB). Sixty-four SFB patients undergoing endoscopic sinus surgery and 21 controls were enrolled in this study. Mucosal samples from nasal sinuses were collected for biofilm detection under confocal scanning laser microscopy (CSLM). The general clinical data, Lund-Mackay computed tomography (CT) score, Lund-Kennedy endoscopy score, Global Osteitis Scoring Scale (GOSS) score, Sinonasal Outcome Test (SNOT)-22 score and visual analog scale (VAS) score were recorded. Associations between these parameters and biofilms were assessed. Under CSLM, the positive rates of BBF and FBF were 45.3 % (29/64) and 21.9 % (14/64), respectively in the SFB group but none in controls. When sub-classified according to biofilm status, the BBF-positive subgroup had significantly higher Lund-Mackay score and GOSS score than the BBF-negative one, but there were no differences in demographic characteristics, health-related quality-of-life and endoscopic inflammatory severity. BBF and FBF coexisted on the sinus mucosa of the patients with SFB. BBF was associated with more severe disease, but the distribution of FBF did not affect the severity of SFB.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Chakrabarti A, Denning DW, Ferguson BJ et al (2009) Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies. Laryngoscope 119:1809–1818

    Article  PubMed Central  PubMed  Google Scholar 

  2. Montone KT, Livolsi VA, Feldman MD, Palmer J, Chiu AG, Lanza DC, Kennedy DW, Loevner LA, Nachamkin I (2012) Fungal rhinosinusitis: a retrospective microbiologic and pathologic review of 400 patients at a single university medical center. Int J Otolaryngol 2012:684835

    Article  PubMed Central  PubMed  Google Scholar 

  3. Brook I (2011) Recovery of aerobic and anaerobic bacteria in sinus fungal ball. Otolaryngol Head Neck Surg 145:851–852

    Article  PubMed  Google Scholar 

  4. Wang JH, Lee BJ, Jang YJ (2010) Bacterial coinfection and antimicrobial resistance in patients with paranasal sinus fungus balls. Ann Otol Rhinol Laryngol 119:406–411

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Foreman A, Psaltis AJ, Tan LW, Wormald PJ (2009) Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy 23:556–561

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Foreman A, Boase S, Psaltis A, Wormald PJ (2012) Role of bacterial and fungal biofilms in chronic rhinosinusitis. Curr Allergy Asthma Rep 12:127–135

    Article  PubMed  Google Scholar 

  11. Singhal D, Foreman A, Jervis-Bardy J, Wormald PJ (2011) Staphylococcus aureus biofilms: nemesis of endoscopic sinus surgery. Laryngoscope 121:1578–1583

    Article  PubMed  Google Scholar 

  12. Tan NC, Foreman A, Jardeleza C, Douglas R, Tran H, Wormald PJ (2012) The multiplicity of staphylococcus aureus in chronic rhinosinusitis: correlating surface biofilm and intracellular residence. Laryngoscope 122:1655–1660

    Article  PubMed  Google Scholar 

  13. Li H, Wang D, Sun X, Hu L, Yu H, Wang J (2012) Relationship between bacterial biofilm and clinical features of patients with chronic rhinosinusitis. Eur Arch Otorhinolaryngol 269:155–163

    Article  PubMed  Google Scholar 

  14. Dong D, Yulin Z, Xiao W, Hongyan Z, Jia L, Yan X, Jia W (2014) Correlation between bacterial biofilms and osteitisin patients with chronic rhinosinusitis. Laryngoscope 124:1071–1077

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. deShazo RD, O’Brien M, Chapin K, Soto-Aguilar M, Swain R, Lyons M, Bryars WC Jr, Alsip S (1997) Criteria for the diagnosis of sinus mycetoma. J Allergy Clin Immunol 99:475–485

    Article  CAS  PubMed  Google Scholar 

  17. Healy DY, Leid JG, Sanderson AR, Hunsaker DH (2008) Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg 138:641–647

    Article  PubMed  Google Scholar 

  18. Dong D, Yulin Z, Yan X, Hongyan Z, Shitao Z, Jia W (2014) Enhanced expressions of lysozyme, SLPI and glycoprotein 340 in biofilm-associated chronic rhinosinusitis. Eur Arch Otorhinolaryngol 271:1563–1571

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. Georgalas C, Videler W, Freling N, Fokkens W (2010) Global osteitis scoring scale and chronic rhinosinusitis: a marker of revision surgery. Clin Otolaryngol 35:455–461

    Article  CAS  PubMed  Google Scholar 

  21. Georgalas C (2013) Osteitis and paranasal sinus inflammation: what we know and what we do not. Curr Opin Otolaryngol Head Neck Surg 21:45–49

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  23. Al-Mutairi D, Kilty SJ (2011) Bacterial biofilms and the pathophysiology of chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 11:18–23

    Article  PubMed  Google Scholar 

  24. Boase S, Jervis-Bardy J, Cleland E, Pant H, Tan L, Wormald PJ (2013) Bacterial-induced epithelial damage promotes fungal biofilm formation in a sheep model of sinusitis. Int Forum Allergy Rhinol 3:341–348

    Article  PubMed  Google Scholar 

  25. Cantero D, Cooksley C, Bassiouni A, Wormald PJ, Vreugde S (2013) Staphylococcus aureus biofilm activates the nucleotide-binding oligomerization domain containing 2 (Nod2) pathway and proinflammatory factors on a human sinonasal explant model. Int Forum Allergy Rhinol 3:877–884

    Article  PubMed  Google Scholar 

  26. Chen JC, Ho CY (2012) The significance of computed tomographic findings in the diagnosis of fungus ball in the paranasal sinuses. Am J Rhinol Allergy 26:117–119

    Article  CAS  PubMed  Google Scholar 

  27. Bowman J, Panizza B, Gandhi M (2007) Sphenoid sinus fungal balls. Ann Otol Rhinol Laryngol 116:514–519

    Article  PubMed  Google Scholar 

  28. Bassiouni A, Naidoo Y, Wormald PJ (2012) When fess fails: the inflammatory load hypothesis in refractory chronic rhinosinusitis. Laryngoscope 122:460–466

    Article  PubMed  Google Scholar 

  29. Singhal D, Psaltis AJ, Foreman A, Wormald PJ (2010) The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy 24:169–174

    Article  PubMed  Google Scholar 

  30. You H, Zhuge P, Li D, Shao L, Shi H, Du H (2011) Factors affecting bacterial biofilm expression in chronic rhinosinusitis and the influences on prognosis. Am J Otolaryngol 32:583–590

    Article  PubMed  Google Scholar 

  31. 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–S126

    Article  CAS  PubMed  Google Scholar 

  32. Loussert C, Schmitt C, Prevost MC, Balloy V, Fadel E, Philippe B, Kauffmann-Lacroix C, Latgé JP, Beauvais A (2010) In vivo biofilm composition of aspergillus fumigatus. Cell Microbiol 12:405–410

    Article  CAS  PubMed  Google Scholar 

  33. Foreman A, Wormald PJ (2010) Different biofilms, different disease? A clinical outcomes study. Laryngoscope 120:1701–1706

    Article  PubMed  Google Scholar 

  34. Bendouah Z, Barbeau J, Hamad WA, Desrosiers M (2006) 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 134:991–996

    Article  PubMed  Google Scholar 

  35. Ma L, Xu R, Shi J, Zhou W, Xu G, Jiang G, Li G, Chen Z (2013) Identification of fungi in fungal ball sinusitis: comparison between MUC5B immunohistochemical and grocott methenamine silver staining. Acta Otolaryngol 133:1181–1187

    Article  PubMed  Google Scholar 

  36. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME (2010) Microbial interactions and differential protein expression in Staphylococcus aureus—Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493–503

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Conflict of interest

All authors have no conflict of interest regarding this paper.

Author information

Authors and Affiliations

  1. Department of Radiology, The First Affiliated Hospital of Zhengzhou University, No. 1 Construction East Road, Zhengzhou, 450000, China

    Xiao Wang & Jingliang Cheng

  2. Department of Rhinology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450000, China

    Dong Dong & Yulin Zhao

  3. Department of Pathology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, 450000, China

    Xinjuan Fan

Authors
  1. Xiao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dong Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jingliang Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinjuan Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yulin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jingliang Cheng.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Dong, D., Cheng, J. et al. Relationship between biofilms and clinical features in patients with sinus fungal ball. Eur Arch Otorhinolaryngol 272, 2363–2369 (2015). https://doi.org/10.1007/s00405-014-3361-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-014-3361-3

Keywords

Search

Navigation