Skip to main content
SpringerLink
Log in

Clinical Characteristics of Biofilms in Patients with Chronic Rhinosinusitis: A Prospective Case–Control Study

  • Original Article
  • Published:
Indian Journal of Otolaryngology and Head & Neck Surgery Aims and scope Submit manuscript

Abstract

Recent studies have indicated that biofilms are involved in the pathogenesis of recurrent and recalcitrant chronic rhinosinusitis (CRS). The present study was performed to evaluate the presence of biofilms and to evaluate the relationships between the presence of biofilms and clinical features of CRS. A total of 33 patients were included in this study. Maxillary sinus mucosa from 26 CRS patients and the ethmoid mucosa from 7 patients undergoing septoplasty were collected. Biofilms were evaluated by scanning electron microscopy. Preoperative symptom scores, preoperative and intraoperative nasoendoscopic findings, and postoperative healing period were compared between the groups. Biofilms were detected in 14 (42.4 %) of the 33 patients. Biofilms were present in 13 (50 %) of the 26 patients in the CRS group, but in only one (14.3 %) of the seven patients in the control group. There were no significant differences in preoperative symptom scores or preoperative nasal Lund–Kennedy endoscopic scores between the groups. However, the average Lund–Mackay and intraoperative sinus Lund–Kennedy endoscopic scores were significantly higher in biofilm-positive than biofilm-negative patients (P < 0.05). In the follow-up period, the healing time was significantly longer in biofilm-positive than biofilm-negative patients (P < 0.05). This study suggested that the presence of bacterial biofilms may contribute to the pathogenesis of CRS and the clinical characteristics of CRS patients after endoscopic sinus surgery.

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

Similar content being viewed by others

References

  1. Benninger MS, Ferguson BJ, Hadley JA, Hamilos DL, Jacobs M, Kennedy DW et al (2003) Adult chronic rhinosinusitis: definitions, diagnosis, epidemiology, and pathophysiology. Otolaryngol Head Neck Surg 129:S1–S32

    Article  PubMed  Google Scholar 

  2. 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 

  3. Palmer JN (2005) Bacterial biofilms: do they play a role in chronic sinusitis? Otolaryngol Clin North Am 38:1193–1201

    Article  PubMed  Google Scholar 

  4. Sanderson AR, Leid JG, Hunsaker D (2006) Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope 116:1121–1126

    Article  PubMed  Google Scholar 

  5. Mladina R, Poje G, Vukovi K, Risti M, Musi S (2008) Biofilm in nasal polyps. Rhinology 46:302–307

    PubMed  Google Scholar 

  6. 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 

  7. Lund VJ, Mackay IS (1993) Staging in rhinosinusitis. Rhinology 107:183–184

    Google Scholar 

  8. Lund VJ, Kennedy DW (1995) Quantification for staging sinusitis. Ann Otol Rhinol Laryngol 104:17–21

    Google Scholar 

  9. Psaltis AJ, Ha KR, Beule AG, Tan LW, Wormald PJ (2007) Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 117:1302–1306

    Article  PubMed  Google Scholar 

  10. 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 

  11. Zhang Z, Han D, Zhang S, Han Y, Dai W, Fan E et al (2009) Biofilms and mucosal healing in postsurgical patients with chronic rhinosinusitis. Am J Rhinol Allergy 23:506–511

    Article  PubMed  Google Scholar 

  12. Sun Y, Zhou B, Wang CS, Huang Q, Zhang Q, Han YH et al (2012) Clinical and histopathologic features of biofilm-associated chronic rhinosinusitis with nasal polyps in Chinese patients. Chin Med J (Engl) 125:1104–1109

    Google Scholar 

  13. 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 

  14. 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(6):991–996

    Article  PubMed  Google Scholar 

  15. Polzehl D, Moeller P, Riechelmann H, Perner S (2006) Distinct features of chronic rhinosinusitis with and without nasal polyps. Allergy 61:1275–1279

    Article  CAS  PubMed  Google Scholar 

  16. Fokkens W, Lund V, Bachert C, Clement P, Helllings P, Holmstrom M et al (2005) EAACI position paper on rhinosinusitis and nasal polyps executive summary. Allergy 60:583–601

    Article  CAS  PubMed  Google Scholar 

  17. Bezerra TF, Padua FG, Gebrim EM, Saldiva PH, Voegels RL (2011) Biofilms in chronic rhinosinusitis with nasal polyps. Otolaryngol Head Neck Surg 144(4):612–616

    Article  PubMed  Google Scholar 

  18. Zhang Z, Kofonow JM, Finkelman BS, Doghramji L, Chiu AG, Kennedy DW, Cohen NA, Palmer JN (2011) Clinical factors associated with bacterial biofilm formation in chronic rhinosinusitis. Otolaryngol Head Neck Surg 144:457–462

    Article  PubMed  Google Scholar 

  19. Prince AA, Steiger JD, Khalid AN, Dogrhamji L, Reger C, Eau Claire S et al (2008) Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol 22:239–245

    Article  PubMed  Google Scholar 

  20. Xiong GY, Chen HH, Wang SQ, Xie XX, Lin W, Shen Q (2010) Relationship between bacterial biofilms and chronic rhinosinusitis by scanning electron microscopic study. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 45:19–23

    PubMed  Google Scholar 

  21. Cryer J, Schipor I, Perloff JR, Palmer JN (2004) Evidence of bacterial biofilms in human chronic sinusitis. ORL J Otorhinolaryngol Relat Spec 66:155–158

    Article  PubMed  Google Scholar 

  22. Ramadan HH, Sanclement JA, Thomas JG (2005) Chronic rhinosinusitis and biofilms. Otolaryngol Head Neck Surg 132:414–417

    Article  PubMed  Google Scholar 

  23. Ferguson BJ, Stolz DB (2005) Demonstration of biofilm in human bacterial chronic rhinosinusitis. Am J Rhinol 19:452–457

    PubMed  Google Scholar 

  24. Sanclement JA, Webster P, Thomas J, Ramadan HH (2005) Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope 115:578–582

    Article  PubMed  Google Scholar 

  25. Lawrence JR, Neu TR (1999) Confocal laser scanning microscopy for analysis of microbial biofilms. Methods Enzymol 310:131–144

    Article  CAS  PubMed  Google Scholar 

  26. Mladina R, Skitarelic N, Music S, Ristic M (2010) A biofilm exists on healthy mucosa of the paranasal sinuses: a prospectively performed, blinded, scanning electron microscope study. Clin Otolaryngol 35:104–110

    Article  CAS  PubMed  Google Scholar 

  27. Hochstim CJ, Masood R, Rice DH (2010) Biofilm and persistent inflammation in endoscopic sinus surgery. Otolaryngol Head Neck Surg 143:697–698

    Article  PubMed  Google Scholar 

  28. 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 

  29. Cohen M, Kofonow J, Nayak JV, Palmer JN, Chiu AG, Leid JG et al (2009) Biofilms in chronic rhinosinusitis: a review. Am J Rhinol Allergy 23:255–260

    Article  PubMed  Google Scholar 

  30. Jefferson KK, Goldmann DA, Pier GB (2005) Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob Agents Chemother 49:2467–2473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  32. Singhal D, Foreman A, Jervis-Bardy J, Wormald PJ (2011) Staphylococcus aureus biofilms: nemesis of endoscopic sinus surgery. Laryngoscope 121(7):1578–1583

    Article  PubMed  Google Scholar 

  33. Chiu AG, Palmer JN, Woodworth BA, Doghramji L, Cohen MB, Prince A, Cohen NA (2008) Baby shampoo nasal irrigations for the symptomatic post-functional endoscopic sinus surgery patient. Am J Rhinol 22(1):34–37

    Article  PubMed  Google Scholar 

  34. Alandejani T, Marsan J, Ferris W, Slinger R, Chan F (2009) Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngol Head Neck Surg 41(1):114–118

    Article  Google Scholar 

  35. Hai PV, Lidstone C, Wallwork B (2010) The effect of endoscopic sinus surgery on bacterial biofilms in chronic rhinosinusitis. Otolaryngol Head Neck Surg 142:S27–S32

    Article  PubMed  Google Scholar 

  36. Wozniak DJ, Keyser R (2004) Effects of subinhibitory concentrations of macrolide antibiotics on Pseudomonas aeruginosa. Chest 125(2):62S–69S

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant of the Korean Health Technology R&D Project, Ministry of Health & Welfare, Republic of Korea (A100785).

Author information

Authors and Affiliations

  1. Department of Otolaryngology-Head & Neck Surgery, Gachon University, Gil Medical Center, 1198, 405-760, Guwaldong Namdong-gu, Incheon, Korea

    Joo Hyun Jung, Heung Eog Cha, Il Gyu Kang & Seon Tae Kim

Authors
  1. Joo Hyun Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heung Eog Cha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Il Gyu Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seon Tae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seon Tae Kim.

Additional information

The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see: http://www.textcheck.com/certificate/jMbiEZ

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jung, J.H., Cha, H.E., Kang, I.G. et al. Clinical Characteristics of Biofilms in Patients with Chronic Rhinosinusitis: A Prospective Case–Control Study. Indian J Otolaryngol Head Neck Surg 67, 1–6 (2015). https://doi.org/10.1007/s12070-014-0707-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12070-014-0707-5

Keywords

Search

Navigation