Skip to main content
SpringerLink
Log in

The presence of CD209 expressing dendritic cells correlates with biofilm positivity in chronic rhinosinusitis with nasal polyposis

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

Abstract

Biofilm-positive cases of chronic rhinosinusitis with nasal polyposis (CRSwNP) may form a separate clinical entity, which is characterized by high recurrence rates and resistance against different therapeutic strategies. This can be explained by a special immunologic phenotype. Biofilm existence has been supposed to correlate with increased amount of dendritic cells that are responsible for antigen presentation in CRSwNP. A total of 20 patients with CRSwNP undergoing endoscopic sinus surgery (ESS) were analyzed. The negative control group consisted of ten patients undergoing septoplasty without CRSwNP. Three series of individual nasal polyps and control specimens were processed to hematoxylin–eosin (HE) and Gram staining and to CD209-specific immunofluorescent assay, respectively. Biofilm was detected in 13 of 20 patients (65 %) with CRSwNP and in none of the ten negative controls. The subepithelial layer of biofilm-positive nasal polyps displayed a statistically significant (p < 0.001) increase in the numbers of CD209-expressing dendritic cells compared to biofilm-negative specimens. It was found that biofilm detectability showed strong correlation to the architecture of respiratory mucosa and to the dominant inflammatory cell type of the subepithelial layer. Persisting bacterial biofilms may affect the type of antigen presentation and consecutive immune reactions in the subepithelial layer of nasal mucosa. This phenomenon may result in different inflammatory pathways with specific cytokine profile compared to biofilm-negative cases. Co-existence of bacterial biofilms and dominant pattern of dendritic cells suggest a biofilm-associated immunologic phenotype in CRSwNP. This can explain the mucosal changes, functional disorders and therapy resistance featuring CRSwNP.

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
Fig. 4

Similar content being viewed by others

References

  1. Meltzer EO, Hamilos DL (2011) Rhinosinusitis diagnosis and management for the clinician: a synopsis of recent consensus guidelines. Mayo Clin Proc 86:427–443

    Article  PubMed  Google Scholar 

  2. Marple BF, Stankiewicz JA, Baroody FM, Chow JM, Conley DB, Corey JP, Ferguson BJ, Kern RC, Lusk RP, Naclerio RM, Orlandi RR (2009) American Academy of Otolaryngic Allergy Working Group on Chronic Rhinosinusitis. Diagnosis and management of chronic rhinosinusitis in adults. Postgrad Med 121:121–139

    Article  PubMed  Google Scholar 

  3. 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 

  4. Eloy P, Poirrier AL, De Dorlodot C, Van Zele T, Watelet JB, Bertrand B (2011) Actual concepts in rhinosinusitis: a review of clinical presentations, inflammatory pathways, cytokine profiles, remodeling, and management. Curr Allergy Asthma Rep 11:146–162

    Article  PubMed  CAS  Google Scholar 

  5. Otto BA, Wenzel SE (2008) The role of cytokines in chronic rhinosinusitis with nasal polyps. Curr Opin Otolaryngol Head Neck Surg 16:270–274

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  7. Zernotti ME, Angel Villegas N, Roques Revol M, Baena-Cagnani CE, Arce Miranda JE, Paredes ME, Albesa I, Paraje MG (2010) Evidence of bacterial biofilms in nasal polyposis. J Investig Allergol Clin Immunol 5:380–385

    Google Scholar 

  8. Galli J, Calò L, Ardito F, Imperiali M, Bassotti E, Passali GC, La Torre G, Paludetti G, Fadda G (2008) Damage to ciliated epithelium in chronic rhinosinusitis: what is the role of bacterial biofilms? Ann Otol Rhinol Laryngol 117:902–908

    PubMed  Google Scholar 

  9. Tóth L, Csomor P, Sziklai I, Karosi T (2011) Biofilm detection in chronic rhinosinusitis by combined application of hematoxylin–eosin and gram staining. Eur Arch Otorhinolaryngol 268:1455–1462

    Article  PubMed  Google Scholar 

  10. Hekiert AM, Kofonow JM, Doghramji L, Kennedy DW, Chiu AG, Palmer JN, Leid JG, Cohen NA (2009) Biofilms correlate with TH1 inflammation in the sinonasal tissue of patients with chronic rhinosinusitis. Otolaryngol Head Neck Surg 141:448–453

    Article  PubMed  Google Scholar 

  11. Reizis B (2012) Classical dendritic cells as a unique immune cell lineage. J Exp Med 209:1053–1056

    Article  PubMed  CAS  Google Scholar 

  12. Joffre OP, Segura E, Savina A, Amigorena S (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12:557–569

    Article  PubMed  CAS  Google Scholar 

  13. Guermonprez P, Valladeau J, Zitvogel L, Théry C, Amigorena S (2002) Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol 20:621–667

    Article  PubMed  CAS  Google Scholar 

  14. Ortiz M, Kaessmann H, Zhang K, Bashirova A, Carrington M, Quintana-Murci L, Telenti A (2008) The evolutionary history of the CD209 (DC-SIGN) family in humans and non-human primates. Genes Immun 9:483–492

    Article  PubMed  CAS  Google Scholar 

  15. McGreal E, Miller J, Gordon S (2005) Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr Opin Immunol 17:18–24

    Article  PubMed  CAS  Google Scholar 

  16. Sultan B, May LA, Lane AP (2011) The role of TNF-α in inflammatory olfactory loss. Laryngoscope 121:2481–2486

    Article  PubMed  CAS  Google Scholar 

  17. Lennard CM, Mann EA, Sun LL, Chang AS, Bolger WE (2000) Interleukin-1 beta, interleukin-5, interleukin-6, interleukin-8, and tumor necrosis factor-alpha in chronic sinusitis: response to systemic corticosteroids. Am J Rhinol 14:367–373

    Article  PubMed  CAS  Google Scholar 

  18. 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 

  19. Bottari B, Ercolini D, Gatti M, Neviani E (2006) Application of FISH technology for microbiological analysis: current state and prospects. Appl Microbiol Biotechnol 73:485–494

    Article  PubMed  CAS  Google Scholar 

  20. Neu TR, Manz B, Volke F, Dynes JJ, Hitchcock AP, Lawrence JR (2010) Advanced imaging techniques for assessment of structure, composition and function in biofilm systems. FEMS Microbiol Ecol 72:1–21

    Article  PubMed  CAS  Google Scholar 

  21. Yea SS, Yang YI, Park SK, Jang WH, Lee SS, Seog DH, Park YH, Chun JH (2006) Interleukin-4 C-590T polymorphism is associated with protection against nasal polyps in a Korean population. Am J Rhinol 20:550–553

    Article  PubMed  Google Scholar 

  22. Yamamoto M, Kiyono H, Kweon MN, Yamamoto S, Fujihashi K, Kurazono H, Imaoka K, Bluethmann H, Takahashi I, Takeda Y, Azuma M, McGhee JR (2000) Enterotoxin adjuvants have direct effects on T cells and antigen-presenting cells that result in either interleukin-4-dependent or -independent immune responses. J Infect Dis 182:180–190

    Article  PubMed  CAS  Google Scholar 

  23. Mfuna Endam L, Cormier C, Bossé Y, Filali-Mouhim A, Desrosiers M (2010) Association of IL1A, IL1B, and TNF gene polymorphisms with chronic rhinosinusitis with and without nasal polyposis: a replication study. Arch Otolaryngol Head Neck Surg 136:187–192

    Article  PubMed  Google Scholar 

  24. Kirsche H, Niederführ A, Deutschle T, Fuchs C, Riechelmann H (2010) Ratio of myeloid and plasmacytoid dendritic cells and TH2 skew in CRS with nasal polyps. Allergy 65:24–31

    Article  PubMed  CAS  Google Scholar 

  25. Liu T, Xie C, Chen X, Zhao F, Liu AM, Cho DB, Chong J, Yang PC (2010) Role of muscarinic receptor activation in regulating immune cell activity in nasal mucosa. Allergy 65:969–977

    Article  PubMed  CAS  Google Scholar 

  26. Nonaka M, Fukumoto A, Ogihara N, Sakanushi A, Pawankar R, Yagi T (2010) Synergistic induction of thymic stromal lymphopoietin by tumor necrosis factor alpha and Th2 cytokine in nasal polyp fibroblasts. Am J Rhinol Allergy 24:e14–e18

    Article  PubMed  Google Scholar 

  27. Nonaka M, Ogihara N, Fukumoto A, Sakanushi A, Kusama K, Pawankar R, Yagi T (2010) Nasal polyp fibroblasts produce MIP-3alpha in response to toll-like receptor ligands and cytokine stimulation. Rhinology 48:41–46

    PubMed  Google Scholar 

  28. Mulligan JK, Bleier BS, O’Connell B, Mulligan RM, Wagner C, Schlosser RJ (2011) Vitamin D3 correlates inversely with systemic dendritic cell numbers and bone erosion in chronic rhinosinusitis with nasal polyps and allergic fungal rhinosinusitis. Clin Exp Immunol 164:312–320

    Article  PubMed  CAS  Google Scholar 

  29. Poposki JA, Uzzaman A, Nagarkar DR, Chustz RT, Peters AT, Suh LA, Carter R, Norton J, Harris KE, Grammer LC, Tan BK, Chandra RK, Conley DB, Kern RC, Schleimer RP, Kato A (2011) Increased expression of the chemokine CCL23 in eosinophilic chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol 128:73–81

    Article  PubMed  CAS  Google Scholar 

  30. Ayers CM, Schlosser RJ, O’Connell BP, Atkinson C, Mulligan RM, Casey SE, Bleier BS, Wang EW, Sansoni ER, Kuhlen JL, Mulligan JK (2011) Increased presence of dendritic cells and dendritic cell chemokines in the sinus mucosa of chronic rhinosinusitis with nasal polyps and allergic fungal rhinosinusitis. Int Forum Allergy Rhinol 1:296–302

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the grant of Research Fund of the European Union (TÁMOP 4.2.1.B).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Otolaryngology and Head and Neck Surgery, University of Debrecen, Medical and Health Science Center, Debrecen, Nagyerdei Krt. 98, 4032, Hungary

    Tamás Karosi, Péter Csomor & István Sziklai

  2. Department of Anatomy, Histology and Embryology, University of Debrecen, Medical and Health Science Center, Debrecen, Hungary

    Zoltán Hegyi

Authors
  1. Tamás Karosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Péter Csomor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zoltán Hegyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. István Sziklai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tamás Karosi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karosi, T., Csomor, P., Hegyi, Z. et al. The presence of CD209 expressing dendritic cells correlates with biofilm positivity in chronic rhinosinusitis with nasal polyposis. Eur Arch Otorhinolaryngol 270, 2455–2463 (2013). https://doi.org/10.1007/s00405-013-2372-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-013-2372-9

Keywords

Search

Navigation