Skip to main content Accessibility help
×
Home

Biofilms in chronic rhinosinusitis: what is new and where next?

  • Y Ramakrishnan (a1), R C Shields (a2), M R Elbadawey (a1) (a3) and J A Wilson (a1)

Abstract

Background:

Chronic rhinosinusitis is a common, heterogeneous condition. An effective means of mitigating disease in chronic rhinosinusitis patients remains elusive. A variety of causes have been implicated, with the biofilm theory gaining increasing prominence.

Objective:

This article reviews the literature on the role of biofilms in chronic rhinosinusitis, in terms of pathophysiology and with regard to avenues for future treatment.

Methods:

A systematic review of case series was performed using databases with independently developed search strategies, including Medline, Embase, Cumulative Index to Nursing and Allied Health Literature, Cochrane library, and Zetoc, in addition to conference proceedings and a manual search of literature, with the last search conducted on 18 January 2014. The search terms included the following, used in various combinations to maximise the yield of articles identified: ‘biofilms’, ‘chronic rhinosinusitis’, ‘DNase’, ‘extracellular DNA’ and ‘biofilm dispersal’.

Results:

The existing evidence lends further support for the role of biofilms (particularly the Staphylococcus aureus phenotype) in more severe, recalcitrant disease and poorer surgical outcomes.

Conclusion:

Multimodality treatment, with a shift in paradigm to incorporate anti-biofilm strategies, is likely to form the mainstay of future recalcitrant chronic rhinosinusitis management.

Copyright

Corresponding author

Address for correspondence: Dr Yujay Ramakrishnan, Department of Otolaryngology, Freeman Hospital, Newcastle upon Tyne NE7 7DN, UK E-mail: yujay.ramakrishnan@gmail.com

References

Hide All
1Gliklich, RE, Metson, R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngol Head Neck Surg 1995;113:104–9
2Hastan, D, Fokkens, WJ, Bachert, C, Newson, RB, Bislimovska, J, Bockelbrink, A et al. Chronic rhinosinusitis in Europe--an underestimated disease. A GA2LEN study. Allergy 2011;66:1216–23
3Lange, B, Holst, R, Thilsing, T, Baelum, J, Kjeldsen, A. Quality of life and associated factors in persons with chronic rhinosinusitis in the general population. Clin Otolaryngol 2013;38:474–80
4Wilson, KF, McMains, K, Orlandi, R. The association between allergy and chronic rhinosinusitis with and without nasal polyps: an evidence-based review with recommendations. Int Forum Allergy Rhinol 2014;2:93103
5European Academy of Allergology and Clinical Immunology. European position paper on rhinosinusitis and nasal polyps. Rhinol Suppl 2005;(18):187
6Benninger, MS, Ferguson, BJ, Hadley, JA, Hamilos, DL, Jacobs, M, Kennedy, DW et al. Adult chronic rhinosinusitis: definitions, diagnosis, epidemiology, and pathophysiology. Otolaryngol Head Neck Surg 2003;129:S132
7Gilbert, P, Das, J, Foley, I. Biofilm susceptibility to antimicrobials. Adv Dent Res 1997;11:160–7
8Marsh, PD. Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 2005;32(suppl 6):715
9Thornton, RB, Rigby, PJ, Wiertsema, SP, Filion, P, Langlands, J, Coates, HL et al. Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr 2011;11:94
10Dempsey, KE, Riggio, MP, Lennon, A, Hannah, VE, Ramage, G, Allan, D et al. Identification of bacteria on the surface of clinically infected and non-infected prosthetic hip joints removed during revision arthroplasties by 16S rRNA gene sequencing and by microbiological culture. Arthritis Res Ther 2007;9:R46
11Parsek, M, Singh, PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003;57:677701
12Cryer, J, Schipor, I, Perloff, JR, Palmer, JN. Evidence of bacterial biofilms in human chronic sinusitis. ORL J Otorhinolaryngol Relat Spec 2004;66:155–8
13Perloff, JR, Palmer, JN. Evidence of bacterial biofilms on frontal recess stents in patients with chronic rhinosinusitis. Am J Rhinol 2004;18:377–80
14Ramadan, HH, Sanclement, JA, Thomas, JG. Chronic rhinosinusitis and biofilms. Otolaryngol Head Neck Surg 2005;132:414–17
15Sanderson, AR, Leid, JG, Hunsaker, D. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope 2006;116:1121–6
16Singhal, D, Psaltis, AJ, Foreman, A, Wormald, PJ. The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy 2010;24:169–74
17Healy, DY, Leid, JG, Sanderson, AR, Hunsaker, DH. Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg 2008;138:641–7
18Bezerra, TF, Padua, FG, Gebrim, EM, Saldiva, PH, Voegels, RL. Biofilms in chronic rhinosinusitis with nasal polyps. Otolaryngol Head Neck Surg 2011;144:612–16
19Hochstim, CJ, Choi, JY, Lowe, D, Masood, R, Rice, DH. Biofilm detection with hematoxylin-eosin staining. Arch Otolaryngol Head Neck Surg 2010;136:453–6
20Foreman, A, Psaltis, AJ, Tan, LW, Wormald, PJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy 2009;23:556–61
21Psaltis, AJ, Ha, KR, Beule, AG, Tan, LW, Wormald, PJ. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 2007;117:1302–6
22Sanclement, JA, Webster, P, Thomas, J, Ramadan, HH. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope 2005;115:578–82
23Prince, AA, Steiger, JD, Khalid, AN, Dogrhamji, L, Reger, C, Eau Claire, S et al. Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol 2008;22:239–45
24Shields, RC, Mokhtar, N, Ford, M, Hall, MJ, Burgess, JG, ElBadawey, MR et al. Efficacy of a marine bacterial nuclease against biofilm forming microorganisms isolated from chronic rhinosinusitis. PLoS One 2013;8:e55339
25Stephenson, M, Mfuna, L, Dowd, SE, Wolcott, RD, Barbeau, J, Poisson, M et al. Molecular characterization of the polymicrobial flora in chronic rhinosinusitis. J Otolaryngol Head Neck Surg 2010;39:182–7
26Stressmann, FA, Rogers, GB, Chan, SW, Howarth, PH, Harries, PG, Bruce, KD et al. Characterization of bacterial community diversity in chronic rhinosinusitis infections using novel culture-independent techniques. Am J Rhinol Allergy 2011;25:e133–40
27Boase, 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;1:340–7
28Sachse, F, Becker, K, von Eiff, C, Metze, D, Rudack, C. Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy 2010;65:1430–7
29Ellington, JK, Harris, M, Hudson, MC, Vishin, S, Webb, LX, Sherertz, R. Intracellular Staphylococcus aureus and antibiotic resistance: implications for treatment of staphylococcal osteomyelitis. J Orthop Res 2006;24:8793
30Ellington, JK, Harris, M, Webb, L, Smith, B, Smith, T, Tan, K et al. Intracellular Staphylococcus aureus. A mechanism for the indolence of osteomyelitis. J Bone Joint Surg Br 2003;85:918–21
31Garzoni, C, Francois, P, Huyghe, A, Couzinet, S, Tapparel, C, Charbonnier, Y et al. A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 2007;8:171
32Bera, A, Herbert, S, Jakob, A, Vollmer, W, Götz, F. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 2005;55:778–87
33Wood, AJ, Fraser, JD, Swift, S, Patterson-Emanuelson, EA, Amirapu, S, Douglas, RG. Intramucosal bacterial microcolonies exist in chronic rhinosinusitis without inducing a local immune response. Am J Rhinol Allergy 2012;26:265–70
34Tan, NC, Foreman, A, Jardeleza, C, Douglas, R, Vreugde, S, Wormald, PJ. Intracellular Staphylococcus aureus: the Trojan horse of recalcitrant chronic rhinosinusitis? Int Forum Allergy Rhinol 2013;3:261–6
35Psaltis, AJ, Wormald, PJ, Ha, KR, Tan, LW. Reduced levels of lactoferrin in biofilm-associated chronic rhinosinusitis. Laryngoscope 2008;118:895901
36Psaltis, AJ, Bruhn, MA, Ooi, EH, Tan, LW, Wormald, PJ. Nasal mucosa expression of lactoferrin in patients with chronic rhinosinusitis. Laryngoscope 2007;117:2030–5
37Galli, J, Calò, L, Ardito, F, Imperiali, M, Bassotti, E, Passali, GC et al. Damage to ciliated epithelium in chronic rhinosinusitis: what is the role of bacterial biofilms? Ann Otol Rhinol Laryngol 2008;117:902–8
38Lane, AP, Truong-Tran, QA, Schleimer, RP. Altered expression of genes associated with innate immunity and inflammation in recalcitrant rhinosinusitis with polyps. Am J Rhinol 2006;20:138–44
39Hekiert, AM, Kofonow, JM, Doghramji, L, Kennedy, DW, Chiu, AG, Palmer, JN et al. Biofilms correlate with TH1 inflammation in the sinonasal tissue of patients with chronic rhinosinusitis. Otolaryngol Head Neck Surg 2009;141:448–53
40Foreman, A, Holtappels, G, Psaltis, AJ, Jervis-Bardy, J, Field, J, Wormald, PJ et al. Adaptive immune responses in Staphylococcus aureus biofilm-associated chronic rhinosinusitis. Allergy 2011;66:1449–56
41Arjomandi, H, Gilde, J, Zhu, S, Delaney, S, Hochstim, C, Mazhar, K et al. Relationship of eosinophils and plasma cells to biofilm in chronic rhinosinusitis. Am J Rhinol Allergy 2013;27:e8590
42Jardeleza, C, Miljkovic, D, Baker, L, Boase, S, Tan, NC, Koblar, SA et al. Inflammasome gene expression alterations in Staphylococcus aureus biofilm-associated chronic rhinosinusitis. Rhinology 2013;51:315–22
43Dong, D, Yulin, Z, Xiao, W, Hongyan, Z, Jia, L, Yan, X et al. Correlation between bacterial biofilms and osteitis in patients with chronic rhinosinusitis. Laryngoscope 2014;5:1071–7
44Vergara-Irigaray, M, Maira-Litrán, T, Merino, N, Pier, GB, Penadés, JR, Lasa, I. Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology 2008;154(Pt 3):865–77
45Izano, EA, Amarante, MA, Kher, WB, Kaplan, JB. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 2008;74:470–6
46Cerca, N, Jefferson, KK, Maira-Litrán, T, Pier, DB, Kelly-Quintos, C, Goldmann, DA et al. Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun 2007;75:3406–13
47Goldstein-Daruech, N, Cope, EK, Zhao, KQ, Vukovic, K, Kofonow, JM, Doghramji, L et al. Tobacco smoke mediated induction of sinonasal microbial biofilms. PLoS One 2011;6:e15700
48Perloff, JR, Palmer, JN. Evidence of bacterial biofilms in a rabbit model of sinusitis. Am J Rhinol 2005;19:16
49Psaltis, AJ, Weitzel, EK, Ha, KR, Wormald, PJ. The effect of bacterial biofilms on post-sinus surgical outcomes. Am J Rhinol 2008;22:16
50Foreman, A, Wormald, PJ. Different biofilms, different disease? A clinical outcomes study. Laryngoscope 2010;120:1701–6
51Davies, DG, Parsek, MR, Pearson, JP, Iglewski, BH, Costerton, JW, Greenberg, EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998;280:295–8
52Chiu, AG, Palmer, JN, Woodworth, BA, Doghramji, L, Cohen, MB, Prince, A et al. Baby shampoo nasal irrigations for the symptomatic post-functional endoscopic sinus surgery patient. Am J Rhinol 2008;22:34–7
53Valentine, 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;25:323–6
54Kaplan, JB, LoVetri, K, Cardona, ST, Madhyastha, S, Sadovskaya, I, Jabbouri, S et al. Recombinant human DNase I decreases biofilm and increases antimicrobial susceptibility in staphylococci. J Antibiot (Tokyo) 2012;65:73–7
55Kaplan, JB. Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs 2009;32:545–54
56Lamppa, JW, Griswold, KE. Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother 2013;57:137–45
57Steinberger, RE, Holden, PA. Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 2005;71:5404–10
58Dominiak, DM, Nielsen, JL, Nielsen, PH. Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 2011;13:710–21
59Martins, M, Uppuluri, P, Thomas, DP, Cleary, IA, Henriques, M, Lopez-Ribot, JL et al. Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 2010;169:323–31
60Vilain, S, Pretorius, JM, Theron, J, Brözel, VS. DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 2009;75:2861–8
61Molin, S, Tolker-Nielsen, T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 2003;14:255–61
62Jakubovics, NS, Shields, RC, Rajarajan, N, Burgess, JG. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 2013;57:467–75
63Shakir, A, Elbadawey, MR, Shields, RC, Jakubovics, NS, Burgess, JG. Removal of biofilms from tracheoesophageal speech valves using a novel marine microbial deoxyribonuclease. Otolaryngol Head Neck Surg 2012;147:509–14
64Alandejani, T, Marsan, J, Ferris, W, Slinger, R, Chan, F. Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngol Head Neck Surg 2009;141:114–18
65Paramasivan, S, Drilling, AJ, Jardeleza, C, Jervis-Bardy, J, Vreugde, S, Wormald, PJ. Methylglyoxal-augmented manuka honey as a topical anti-Staphylococcus aureus biofilm agent: safety and efficacy in an in vivo model. Int Forum Allergy Rhinol 2014;3:187–95
66Goggin, R, Jardeleza, C, Wormald, PJ, Vreugde, S. Colloidal silver: a novel treatment for Staphylococcus aureus biofilms? Int Forum Allergy Rhinol 2014;3:171–5
67Foreman, A, Jervis-Bardy, J, Boase, SJ, Tan, L, Wormald, PJ. Noninvasive Staphylococcus aureus biofilm determination in chronic rhinosinusitis by detecting the exopolysaccharide matrix component poly-N-acetylglucosamine. Int Forum Allergy Rhinol 2013;3:83–8
68Comstat 2 home page. In: http://www.comstat.dk/ [5 June 2015]
69Heydorn, A, Nielsen, AT, Hentzer, M, Sternberg, C, Givskov, M, Ersbøll, BK et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 2000;146(Pt 10):2395–407
70Singhal, D, Boase, S, Field, J, Jardeleza, C, Foreman, A, Wormald, PJ. Quantitative analysis of in vivo mucosal bacterial biofilms. Int Forum Allergy Rhinol 2012;2:5762

Keywords

Biofilms in chronic rhinosinusitis: what is new and where next?

  • Y Ramakrishnan (a1), R C Shields (a2), M R Elbadawey (a1) (a3) and J A Wilson (a1)

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed