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

Published online by Cambridge University Press:  29 June 2015

Y Ramakrishnan ,
R C Shields ,
M R Elbadawey  and
J A Wilson
Y Ramakrishnan*
Affiliation:
Department of Otolaryngology, Freeman Hospital, Newcastle upon Tyne, UK
R C Shields
Affiliation:
School of Dental Sciences, Newcastle University, UK
M R Elbadawey
Affiliation:
Department of Otolaryngology, Freeman Hospital, Newcastle upon Tyne, UK Department of Otolaryngology, Tanta University, Egypt
J A Wilson
Affiliation:
Department of Otolaryngology, Freeman Hospital, Newcastle upon Tyne, UK
*
Address for correspondence: Dr Yujay Ramakrishnan, Department of Otolaryngology, Freeman Hospital, Newcastle upon Tyne NE7 7DN, UK E-mail: [email protected]
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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.

Keywords

BiofilmSinusitisDeoxyribonucleases
Type
Review Articles
Information
The Journal of Laryngology & Otology , Volume 129 , Issue 8 , August 2015 , pp. 744 - 751
Copyright
Copyright © JLO (1984) Limited 2015 

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References

1Gliklich, RE, Metson, R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngol Head Neck Surg 1995;113:104–9CrossRefGoogle ScholarPubMed
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;66:1216–23CrossRefGoogle ScholarPubMed
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;38:474–80CrossRefGoogle ScholarPubMed
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;2:93–103CrossRefGoogle Scholar
5European Academy of Allergology and Clinical Immunology. European position paper on rhinosinusitis and nasal polyps. Rhinol Suppl 2005;(18):1–87Google Scholar
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:S1–32CrossRefGoogle ScholarPubMed
7Gilbert, P, Das, J, Foley, I. Biofilm susceptibility to antimicrobials. Adv Dent Res 1997;11:160–7CrossRefGoogle ScholarPubMed
8Marsh, PD. Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 2005;32(suppl 6):7–15CrossRefGoogle ScholarPubMed
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;11:94CrossRefGoogle ScholarPubMed
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:R46CrossRefGoogle ScholarPubMed
11Parsek, M, Singh, PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003;57:677–701CrossRefGoogle ScholarPubMed
12Cryer, J, Schipor, I, Perloff, JR, Palmer, JN. Evidence of bacterial biofilms in human chronic sinusitis. ORL J Otorhinolaryngol Relat Spec 2004;66:155–8CrossRefGoogle ScholarPubMed
13Perloff, JR, Palmer, JN. Evidence of bacterial biofilms on frontal recess stents in patients with chronic rhinosinusitis. Am J Rhinol 2004;18:377–80CrossRefGoogle ScholarPubMed
14Ramadan, HH, Sanclement, JA, Thomas, JG. Chronic rhinosinusitis and biofilms. Otolaryngol Head Neck Surg 2005;132:414–17CrossRefGoogle ScholarPubMed
15Sanderson, AR, Leid, JG, Hunsaker, D. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope 2006;116:1121–6CrossRefGoogle ScholarPubMed
16Singhal, D, Psaltis, AJ, Foreman, A, Wormald, PJ. The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy 2010;24:169–74CrossRefGoogle ScholarPubMed
17Healy, DY, Leid, JG, Sanderson, AR, Hunsaker, DH. Biofilms with fungi in chronic rhinosinusitis. Otolaryngol Head Neck Surg 2008;138:641–7CrossRefGoogle ScholarPubMed
18Bezerra, TF, Padua, FG, Gebrim, EM, Saldiva, PH, Voegels, RL. Biofilms in chronic rhinosinusitis with nasal polyps. Otolaryngol Head Neck Surg 2011;144:612–16CrossRefGoogle ScholarPubMed
19Hochstim, CJ, Choi, JY, Lowe, D, Masood, R, Rice, DH. Biofilm detection with hematoxylin-eosin staining. Arch Otolaryngol Head Neck Surg 2010;136:453–6CrossRefGoogle ScholarPubMed
20Foreman, A, Psaltis, AJ, Tan, LW, Wormald, PJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Am J Rhinol Allergy 2009;23:556–61CrossRefGoogle ScholarPubMed
21Psaltis, AJ, Ha, KR, Beule, AG, Tan, LW, Wormald, PJ. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 2007;117:1302–6CrossRefGoogle ScholarPubMed
22Sanclement, JA, Webster, P, Thomas, J, Ramadan, HH. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope 2005;115:578–82CrossRefGoogle ScholarPubMed
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;22:239–45CrossRefGoogle ScholarPubMed
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:e55339CrossRefGoogle ScholarPubMed
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;39:182–7Google ScholarPubMed
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:e133–40CrossRefGoogle ScholarPubMed
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;1:340–7CrossRefGoogle ScholarPubMed
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;65:1430–7CrossRefGoogle ScholarPubMed
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;24:87–93CrossRefGoogle ScholarPubMed
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;85:918–21CrossRefGoogle ScholarPubMed
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;8:171CrossRefGoogle ScholarPubMed
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;55:778–87CrossRefGoogle ScholarPubMed
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;26:265–70CrossRefGoogle ScholarPubMed
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;3:261–6CrossRefGoogle ScholarPubMed
35Psaltis, AJ, Wormald, PJ, Ha, KR, Tan, LW. Reduced levels of lactoferrin in biofilm-associated chronic rhinosinusitis. Laryngoscope 2008;118:895–901CrossRefGoogle ScholarPubMed
36Psaltis, AJ, Bruhn, MA, Ooi, EH, Tan, LW, Wormald, PJ. Nasal mucosa expression of lactoferrin in patients with chronic rhinosinusitis. Laryngoscope 2007;117:2030–5CrossRefGoogle ScholarPubMed
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;117:902–8CrossRefGoogle ScholarPubMed
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;20:138–44CrossRefGoogle ScholarPubMed
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;141:448–53CrossRefGoogle ScholarPubMed
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;66:1449–56CrossRefGoogle ScholarPubMed
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:e85–90CrossRefGoogle ScholarPubMed
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;51:315–22CrossRefGoogle ScholarPubMed
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;5:1071–7CrossRefGoogle Scholar
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):865–77CrossRefGoogle Scholar
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;74:470–6CrossRefGoogle ScholarPubMed
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;75:3406–13CrossRefGoogle Scholar
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:e15700CrossRefGoogle ScholarPubMed
48Perloff, JR, Palmer, JN. Evidence of bacterial biofilms in a rabbit model of sinusitis. Am J Rhinol 2005;19:1–6CrossRefGoogle Scholar
49Psaltis, AJ, Weitzel, EK, Ha, KR, Wormald, PJ. The effect of bacterial biofilms on post-sinus surgical outcomes. Am J Rhinol 2008;22:1–6CrossRefGoogle ScholarPubMed
50Foreman, A, Wormald, PJ. Different biofilms, different disease? A clinical outcomes study. Laryngoscope 2010;120:1701–6CrossRefGoogle ScholarPubMed
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;280:295–8CrossRefGoogle ScholarPubMed
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;22:34–7CrossRefGoogle ScholarPubMed
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;25:323–6CrossRefGoogle ScholarPubMed
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;65:73–7CrossRefGoogle ScholarPubMed
55Kaplan, JB. Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs 2009;32:545–54CrossRefGoogle ScholarPubMed
56Lamppa, JW, Griswold, KE. Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother 2013;57:137–45CrossRefGoogle ScholarPubMed
57Steinberger, RE, Holden, PA. Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 2005;71:5404–10CrossRefGoogle ScholarPubMed
58Dominiak, DM, Nielsen, JL, Nielsen, PH. Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 2011;13:710–21CrossRefGoogle ScholarPubMed
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;169:323–31CrossRefGoogle ScholarPubMed
60Vilain, S, Pretorius, JM, Theron, J, Brözel, VS. DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 2009;75:2861–8CrossRefGoogle ScholarPubMed
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;14:255–61CrossRefGoogle ScholarPubMed
62Jakubovics, NS, Shields, RC, Rajarajan, N, Burgess, JG. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 2013;57:467–75CrossRefGoogle ScholarPubMed
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;147:509–14CrossRefGoogle ScholarPubMed
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;141:114–18CrossRefGoogle ScholarPubMed
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;3:187–95CrossRefGoogle Scholar
66Goggin, R, Jardeleza, C, Wormald, PJ, Vreugde, S. Colloidal silver: a novel treatment for Staphylococcus aureus biofilms? Int Forum Allergy Rhinol 2014;3:171–5CrossRefGoogle Scholar
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;3:83–8CrossRefGoogle ScholarPubMed
68Comstat 2 home page. In: http://www.comstat.dk/ [5 June 2015]Google Scholar
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):2395–407CrossRefGoogle ScholarPubMed
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;2:57–62CrossRefGoogle ScholarPubMed