Changes in the bacterial microbiome of patients with chronic rhinosinusitis after endoscopic sinus surgery
Ravi Jain MBChB
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorMichael Hoggard BSc (hons)
School of Biological Sciences, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorKristi Biswas PhD
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorMelissa Zoing MNurs
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorYannan Jiang PhD
Department of Statistics, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorCorresponding Author
Richard Douglas MD FRACS
Department of Surgery, The University of Auckland, Auckland, New Zealand
Correspondence to: Richard Douglas, MD FRACS, Department of Surgery, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand; e-mail: [email protected]Search for more papers by this authorRavi Jain MBChB
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorMichael Hoggard BSc (hons)
School of Biological Sciences, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorKristi Biswas PhD
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorMelissa Zoing MNurs
Department of Surgery, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorYannan Jiang PhD
Department of Statistics, The University of Auckland, Auckland, New Zealand
Search for more papers by this authorCorresponding Author
Richard Douglas MD FRACS
Department of Surgery, The University of Auckland, Auckland, New Zealand
Correspondence to: Richard Douglas, MD FRACS, Department of Surgery, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand; e-mail: [email protected]Search for more papers by this authorFunding sources for the study: Garnett Passe and Rodney Williams Foundation.
Potential conflict of interest: None provided.
Presented at the ARS Meeting at the annual Combined Otolaryngology Spring Meetings (COSM) on May 18–22, 2016, in Chicago, IL.
Abstract
Background
Endoscopic sinus surgery (ESS) improves symptoms for many chronic rhinosinusitis (CRS) patients by enlarging the size of sinus ostia, improving mucociliary clearance, and facilitating access for topical therapies. However, the effect of surgery on the sinonasal microbiota remains poorly understood. This study examined changes in bacterial communities in CRS patients before and after surgery.
Methods
Swab samples were taken from the middle meatus of 23 patients undergoing ESS. Follow-up swabs were taken in clinic (mean 120 days postsurgery). Symptom scores and antibiotic use were recorded. Bacterial communities were characterized using 16s ribosomal RNA (rRNA) gene-targeted amplicon sequencing and bacterial abundance was measured using quantitative polymerase chain reaction (PCR). Coexisting asthma, aspirin sensitivity, antibiotic use, and presence of polyps were controlled for.
Results
Unpredictable shifts in bacterial community composition were seen postoperatively. ESS was associated with increased bacterial richness. Many taxa had changes in average relative abundance and prevalence. Staphylococcus was the only dominant taxa to increase significantly in relative abundance (p = 0.002). Changes in bacterial communities were driven more by intersubject variability (p = 0.007) than other study factors. Finegoldia, a minority taxon, was associated with a reduction in abundance following ESS, increases in patients with higher symptoms scores, and reductions in patients with reduced total bacterial burden.
Conclusion
This study documented changes in bacterial composition and abundance in the middle meatus following ESS. The complexity of these changes reflects the variability between patients. Modern molecular techniques highlight the currently limited knowledge of the impact of therapies on the microbiology of CRS.
References
- 1Al-Shemari H, Abou-Hamad W, Libman M, Desrosiers M. Bacteriology of the sinus cavities of asymptomatic individuals after endoscopic sinus surgery. J Otolaryngol. 2007; 36: 43–48.
- 2Yildirim A, Oh C, Erdem H, Kunt T. Bacteriology in patients with chronic sinusitis who have been medically and surgically treated. Ear Nose Throat J. 2004; 83: 836–838.
- 3Bhattacharyya N, Gopal HV. Microbiology of the ethmoid sinus following endoscopic sinus surgery. Ear Nose Throat J. 2002; 81: 458–461.
- 4Bhattacharyya N, Gopal HV, Lee KH. Bacterial infection after endoscopic sinus surgery: a controlled prospective study. Laryngoscope. 2004; 114: 765–767.
- 5Coffey CS, Sonnenburg RE, Melroy CT, Dubin MG, Senior BA. Endoscopically guided aerobic cultures in postsurgical patients with chronic rhinosinusitis. Am J Rhinol. 2006; 20: 72–76.
- 6Psaltis AJ, Ha KR, Beule AG, Tan LW, Wormald P-J. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope. 2007; 117: 1302–1306.
- 7Cleland EJ, Bassiouni A, Wormald P-J. The bacteriology of chronic rhinosinusitis and the pre-eminence of Staphylococcus aureus in revision patients. Int Forum Allergy Rhinol. 2013; 3: 642–646.
- 8Oncel S, Pinar E, Sener G, Calli C, Karagoz U. Evaluation of bacterial biofilms in chronic rhinosinusitis. J Otolaryngol Head Neck Surg. 2010; 39: 52–55.
- 9Bendouah Z, Barbeau J, Hamad WA, Desrosiers M. 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. 2006; 134: 991–996.
- 10Jervis-Bardy J, Foreman A, Field J, Wormald P-J. Impaired mucosal healing and infection associated with Staphylococcus aureus after endoscopic sinus surgery. Am J Rhinol Allergy. 2009; 23: 549–552.
- 11Feazel LM, Robertson CE, Ramakrishnan VR, Frank DN. Microbiome complexity and Staphylococcus aureus in chronic rhinosinusitis. Laryngoscope. 2012; 122: 467–472.
- 12Hauser LJ, Feazel LM, Ir D, et al. Sinus culture poorly predicts resident microbiota. Int Forum Allergy Rhinol. 2014; 5: 3–9.
- 13 NIH HMP Working Group, Peterson J, Garges S, Giovanni M, et al. The NIH Human Microbiome Project. Genome Res. 2009; 19: 2317–2323.
- 14Biswas K, Hoggard M, Jain R, Taylor MW, Douglas RG. The nasal microbiota in health and disease: variation within and between subjects. Front Microbiol. 2015; 9: 134.
- 15Wilson MT, Hamilos DL. The nasal and sinus microbiome in health and disease. Curr Allergy Asthma Rep. 2014; 14: 485–485.
- 16Ramakrishnan VR, Hauser LJ, Frank DN. The sinonasal bacterial microbiome in health and disease. Curr Opin Otolaryngol Head Neck Surg. 2016; 24: 20–25.
- 17Lee JT, Frank DN, Ramakrishnan V. Microbiome of the paranasal sinuses: update and literature review. Am J Rhinol Allergy. 2016; 30: 3–16.
- 18Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009; 77: 2367–2375.
- 19Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008; 6: e280.
- 20Quintanilla-Dieck L, Litvack JR, Mace JC, Smith TL. Comparison of disease-specific quality-of-life instruments in the assessment of chronic rhinosinusitis. Int Forum Allergy Rhinol. 2012; 2: 437–443.
- 21Wabnitz DAM, Nair S, Wormald PJ. Correlation between preoperative symptom scores, quality-of-life questionnaires, and staging with computed tomography in patients with chronic rhinosinusitis. Am J Rhinol. 2005; 19: 91–96.
- 22Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011; 5: 1571–1579.
- 23Edgar RC. Search and clustering orders of magnitude faster than blast. Bioinformatics. 2010; 26: 2460–2461.
- 24Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7: 335–336.
- 25Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73: 5261–5267.
- 26Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26: 266–267.
- 27DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72: 5069–5072.
- 28Price MN, Dehal PS, Arkin AP. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One. 2009; 5: e9490.
- 29Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71: 8228–8235.
- 30R Core Team. The R Project for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2015. https://www.r-project.org. Accessed September 5, 2016.
- 31Oksanen J, Blanchet FG, Kindt R, et al. Vegan Community Ecology Package. R package version 2.3. 2; 2015. https://cran.r-project.org/web/packages/vegan/index.html. Accessed September 5, 2016.
- 32Ramakrishnan VR, Hauser LJ, Feazel LM, Ir D, Robertson CE, Frank DN. Sinus microbiota varies among chronic rhinosinusitis phenotypes and predicts surgical outcome. J Allergy Clin Immunol. 2015; 136: 334-342.e1.
- 33Larson DA, Han JK. Microbiology of sinusitis: does allergy or endoscopic sinus surgery affect the microbiologic flora? Curr Opin Otolaryngol Head Neck Surg. 2011; 19: 199–203.
- 34Singhal D, Foreman A, Jervis-Bardy J, Bardy J-J, Wormald P-J. Staphylococcus aureus biofilms: nemesis of endoscopic sinus surgery. Laryngoscope. 2011; 121: 1578–1583.
- 35Cleland EJ, Bassiouni A, Vreugde S, Wormald P-J. The bacterial microbiome in chronic rhinosinusitis: richness, diversity, postoperative changes, and patient outcomes. Am J Rhinol Allergy. 2015; 30: 37–43.
- 36Hauser LJ, Ir D, Kingdom TT, Robertson CE, Frank DN, Ramakrishnan VR. Investigation of bacterial repopulation after sinus surgery and perioperative antibiotics. Int Forum Allergy Rhinol. 2015; 6: 34–40.
- 37Tan NC-W, Foreman A, Jardeleza C, Douglas R, Vreugde S, Wormald P-J. Intracellular Staphylococcus aureus: the Trojan horse of recalcitrant chronic rhinosinusitis? Int Forum Allergy Rhinol. 2013; 3: 261–266.
- 38Tuchscherr L, Medina E, Hussain M, et al. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med. 2011; 3: 129–141.
- 39Chavakis T, Preissner KT, Herrmann M. The anti-inflammatory activities of Staphylococcus aureus. Trends Immunol. 2007; 28: 408–418.
- 40Yu R-L, Dong Z. Proinflammatory impact of Staphylococcus aureus enterotoxin B on human nasal epithelial cells and inhibition by dexamethasone. Am J Rhinol Allergy. 2009; 23: 15–20.
- 41Stow NW, Douglas R, Tantilipikorn P, Lacroix JS. Superantigens. Otolaryngol Clin North Am. 2010; 43: 489–502.
- 42Damgaard C, Magnussen K, Enevold C, et al. Viable bacteria associated with red blood cells and plasma in freshly drawn blood donations. PLoS One. 2015; 10: e0120826.
- 43Nelson RA. The immune-adherence phenomenon; an immunologically specific reaction between microorganisms and erythrocytes leading to enhanced phagocytosis. Science. 1953; 118: 733–737.
- 44Belstrøm D, Holmstrup P, Damgaard C, et al. The atherogenic bacterium Porphyromonas gingivalis evades circulating phagocytes by adhering to erythrocytes. Infect Immun. 2011; 79: 1559–1565.
- 45de Goffau MC, Yang X, van Dijl JM, Harmsen HJM. Bacterial pleomorphism and competition in a relative humidity gradient. Environ Microbiol. 2009; 11: 809–822.
- 46Shafiur Rahman M. Handbook of Food Preservation. 2nd ed. Boca Raton: CRC Press; 2007.
10.1201/9781420017373 Google Scholar
- 47Choi KJ, Jang DW, Ellison MD, Frank-Ito DO. Characterizing airflow profile in the postoperative maxillary sinus by using computational fluid dynamics modeling: a pilot study. Am J Rhinol Allergy. 2016; 30: 29–36.
- 48Zhu JH, Lim KM, Thong KTM, Wang DY, Lee HP. Assessment of airflow ventilation in human nasal cavity and maxillary sinus before and after targeted sinonasal surgery: a numerical case study. Respir Physiol Neurobiol. 2014; 194: 29–36.
- 49Frank DO, Zanation AM, Dhandha VH, et al. Quantification of airflow into the maxillary sinuses before and after functional endoscopic sinus surgery. Int Forum Allergy Rhinol. 2013; 3: 834–840.
- 50Stewart I, Schluter PJ, Shaw GR. Cyanobacterial lipopolysaccharides and human health - a review. Environ Health. 2006; 5: 7.
- 51Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102: 11070–11075.
- 52Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol. 2010; 192: 5002-5017.
- 53Aurora R, Chatterjee D, Hentzleman J, Prasad G, Sindwani R, Sanford T. Contrasting the microbiomes from healthy volunteers and patients with chronic rhinosinusitis. JAMA Otolaryngol Head Neck Surg. 2013; 139: 1328–1338.
- 54Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One. 2010; 5: e10598.
- 55Murdoch DA. Gram-positive anaerobic cocci. Clin Microbiol Rev. 1998; 11: 81–120.
- 56Bourgault AM, Rosenblatt JE, Fitzgerald RH. Peptococcus magnus: a significant human pathogen. Ann Intern Med. 1980; 93: 244–248.
- 57Brook I. Microbiology of nosocomial sinusitis in mechanically ventilated children. Arch Otolaryngol Head Neck Surg. 1998; 124: 35–38.
- 58Murphy EC, Mörgelin M, Reinhardt DP, Olin AI, Björck L, Frick I-M. Identification of molecular mechanisms used by Finegoldia magna to penetrate and colonize human skin. Mol Microbiol. 2014; 94: 403–417.
- 59Pynnonen MA, Venkatraman G, Davis GE. Macrolide therapy for chronic rhinosinusitis: a meta-analysis. Otolaryngol Head Neck Surg. 2013; 148: 366–373.
- 60Bachert C, Hamilos DL. Are antibiotics useful for chronic rhinosinusitis? J Allergy Clin Immunol Pract. 2016; 4: 629–638.
- 61Jervis-Bardy J, Boase S, Psaltis A, Foreman A, Wormald P-J. A randomized trial of mupirocin sinonasal rinses versus saline in surgically recalcitrant staphylococcal chronic rhinosinusitis. Laryngoscope. 2012; 122: 2148–2153.