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The microbiology of chronic rhinosinusitis with and without nasal polyps

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

Abstract

Objective

To compare the microbiological features in middle meatus samples from chronic rhinosinusitis (CRS) patients with nasal polyps (CRSwNP) and those without nasal polyps (CRSsNP), and control subjects.

Methods

A total of 136 CRSwNP patients, 66 CRSsNP patients, and 49 control subjects who underwent endoscopic surgery in Beijing TongRen Hospital were enrolled between January 2014 and January 2016. Swab samples were obtained from the middle meatus during surgery and processed for the presence of aerobic and non-aerobic bacteria and fungi. Information on the allergic rhinitis, asthma, the percentage of eosinophils in peripheral blood, and the history of smoking and surgery was collected.

Results

The overall isolation rate for bacteria was 81.3% for the three groups, with the lowest in the CRSsNP group (77.3%) and the highest in the CRSwNP group (88.4%). There were no significant differences in isolation rates among the three groups (P = 0.349). The three most common bacterial species were: Coagulase-negative Staphylococcus (24.3%), Corynebacterium (19.9%), and Staphylococcus epidermidis (19.1%) in the CRSwNP group; S. epidermidis (21.2%), Corynebacterium (21.2%), Coagulase-negative staphylococcus (18.2%), and Staphylococcus aureus (13.6%) in the CRSsNP group; S. epidermidis (30.6%), Coagulase-negative Staphylococcus (28.6%), and S. aureus (14.3%) in the control group. For the bacterial species with high isolation rates, no significant difference in the microbial cultures was observed among the three groups; whereas in the CRSwNP group, a relatively high proportion of Citrobacter (5.9%, a bacterium with low isolation rate) was observed compared with the CRSsNP and control groups (all 0.0%). Furthermore, when samples were categorized into subgroups according to the percentage of eosinophils, some bacterial species showed different rates in the CRSwNP group (e.g., S. aureus, 3.3% in the subgroup with normal percentage of eosinophils, 17.2% in the subgroup with increased percentage of eosinophils, P = 0.011).

Conclusions

There were no significant differences in the microbiological features (except Citrobacter) in middle meatus samples from CRSwNP patients, CRSsNP patients, and control subjects. S. aureus may promote eosinophilic inflammatory response, while S. epidermidis may promote non-eosinophilic inflammatory response.

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References

  1. Kato A (2015) Immunopathology of chronic rhinosinusitis. Allergol Int 64(2):121–130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Akdis CA, Bachert C, Cingi C et al (2013) Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol 131(6):1479–1490

    Article  PubMed  PubMed Central  Google Scholar 

  3. Fokkens WJ, Lund VJ, Mullol J et al (2012) EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 50(1):1–12

    Article  PubMed  Google Scholar 

  4. McLoughlin RM, Mills KH (2011) Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma. J Allergy Clin Immunol 127(5):1097–1107

    Article  PubMed  CAS  Google Scholar 

  5. Frank DN, Pace NR (2008) Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24(1):4–10

    Article  PubMed  CAS  Google Scholar 

  6. Tabas I, Glass CK (2013) Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 339(6116):166–172

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Ramakrishnan VR, Feazel LM, Gitomer SA, Ir D, Robertson CE, Frank DN (2013) The microbiome of the middle meatus in healthy adults. PLoS ONE 8(12):e85507

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Abreu NA, Nagalingam NA, Song Y et al (2012) Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci Transl Med 4(151):151ra124–151ra124

    Article  CAS  Google Scholar 

  9. Yan M, Pamp SJ, Fukuyama J et al (2013) Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 14(6):631–640

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Boase S, Foreman A, Cleland E et al (2013) The microbiome of chronic rhinosinusitis: culture, molecular diagnostics and biofilm detection. BMC Infect Dis 13(1):210

    Article  PubMed  PubMed Central  Google Scholar 

  11. Feazel LM, Robertson CE, Ramakrishnan VR, Frank DN (2012) Microbiome complexity and Staphylococcus aureus in chronic rhinosinusitis. Laryngoscope 122(2):467–472

    Article  PubMed  PubMed Central  Google Scholar 

  12. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI (2007) The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449(7164):804

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Ivanov II, Atarashi K, Manel N et al (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139(3):485–498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Ivanov II, de Llanos Frutos R, Manel N et al (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4(4):337–349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Sudo N, Sawamura S-A, Tanaka K, Aiba Y, Kubo C, Koga Y (1997) The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 159(4):1739–1745

    PubMed  CAS  Google Scholar 

  16. Worbs T, Bode U, Yan S et al (2006) Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203(3):519–527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Atarashi K, Tanoue T, Shima T et al (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331(6015):337–341

    Article  PubMed  CAS  Google Scholar 

  18. Sze MA, Dimitriu PA, Hayashi S et al (2012) The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 185(10):1073–1080

    Article  PubMed  PubMed Central  Google Scholar 

  19. Marri PR, Stern DA, Wright AL, Billheimer D, Martinez FD (2013) Asthma-associated differences in microbial composition of induced sputum. J Allergy Clin Immunol 131(2):346–352. e343

    Article  PubMed  CAS  Google Scholar 

  20. Tomassen P, Zele TV, Zhang N et al (2011) Pathophysiology of chronic rhinosinusitis. Proc Am Thorac Soc 8(1):115–120

    Article  PubMed  CAS  Google Scholar 

  21. Ba L, Zhang N, Meng J et al (2011) The association between bacterial colonization and inflammatory pattern in Chinese chronic rhinosinusitis patients with nasal polyps. Allergy 66(10):1296–1303

    Article  PubMed  CAS  Google Scholar 

  22. Versalovic J, Carroll KC, Funke G, Jorgensen JH, Landry ML, Warnock DW (2011) Manual of clinical microbiology, 10th edn. American Society of Microbiology, Washington, DC

    Google Scholar 

  23. Brook I (1989) Bacteriology of chronic maxillary sinusitis in adults. Ann Otol Rhinol Laryngol 98(6):426–428

    Article  PubMed  CAS  Google Scholar 

  24. Rombaux P, Gigi J, Hamoir M, Eloy P, Bertrand B (2002) Bacteriology of chronic sinusitis: the bulla ethmoidalis content. Rhinology 40(1):18–23

    PubMed  Google Scholar 

  25. Niederfuhr A, Kirsche H, Riechelmann H, Wellinghausen N (2009) The bacteriology of chronic rhinosinusitis with and without nasal polyps. Arch Otolaryngol Head Neck Surg 135(2):131–136

    Article  PubMed  Google Scholar 

  26. Liu Z, Gao QX, Cui YH, Tao YL (1998) Bacteriological study of chronic maxillary sinusitis in adults and observation of susceptibility to antibiotics. J Clin Otorhinolaryngol 12(12):545–548

    CAS  Google Scholar 

  27. Liu Q, Lu X, Bo M, Qing H, Wang X, Zhang L (2014) The microbiology of chronic rhinosinusitis with and without nasal polyps. Acta Otolaryngol 134(12):1251–1258

    Article  PubMed  CAS  Google Scholar 

  28. Aurora R, Chatterjee D, Hentzleman J, Prasad G, Sindwani R, Sanford T (2013) Contrasting the microbiomes from healthy volunteers and patients with chronic rhinosinusitis. JAMA Otolaryngol Head Neck Surg 139(12):1328–1338

    Article  PubMed  Google Scholar 

  29. Smeekens SP, Huttenhower C, Riza A et al (2014) Skin microbiome imbalance in patients with STAT1/STAT3 defects impairs innate host defense responses. J Innate Immun 6(3):253–262

    Article  PubMed  CAS  Google Scholar 

  30. Ramakrishnan VR, Hauser LJ, Feazel LM, Ir D, Robertson CE, Frank DN (2015) Sinus microbiota varies among chronic rhinosinusitis phenotypes and predicts surgical outcome. J Allergy Clin Immunol 136(2):334–342.e331

    Article  PubMed  Google Scholar 

  31. Bisgaard H, Hermansen MN, Buchvald F et al (2007) Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 357(15):1487–1495

    Article  PubMed  CAS  Google Scholar 

  32. Huang YJ, Nelson CE, Brodie EL et al (2011) Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol 127(2):372–381.e371–e373

    Article  PubMed  Google Scholar 

  33. Van Zele T, Gevaert P, Watelet JB et al (2004) Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis. J Allergy Clin Immunol 114(4):981–983

    Article  PubMed  CAS  Google Scholar 

  34. Corriveau MN, Zhang N, Holtappels G, Van Roy N, Bachert C (2009) Detection of Staphylococcus aureus in nasal tissue with peptide nucleic acid-fluorescence in situ hybridization. Am J Rhinol Allergy 23(5):461–465

    Article  PubMed  Google Scholar 

  35. Sachse F, Becker K, von Eiff C, Metze D, Rudack C (2010) Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy 65(11):1430–1437

    Article  PubMed  CAS  Google Scholar 

  36. Jiang RS, Hsu CY, Jang JW (1998) Bacteriology of the maxillary and ethmoid sinuses in chronic sinusitis. J Laryngol Otol 112(9):845–848

    PubMed  CAS  Google Scholar 

  37. Hu Y, Cao PP, Liang GT, Cui YH, Liu Z (2012) Diagnostic significance of blood eosinophil count in eosinophilic chronic rhinosinusitis with nasal polyps in Chinese adults. Laryngoscope 122(3):498–503

    Article  PubMed  Google Scholar 

  38. Wang MJ, Zhou B, Li YC, Huang Q (2013) The role of peripheral blood eosinophil percentage in classification of chronic rhinosinusitis with nasal polyps. Chin J Otorhinolaryngol Head Neck Surg 48(8):650–653

    Google Scholar 

  39. Laborel-Preneron E, Bianchi P, Boralevi F et al (2015) Effects of the Staphylococcus aureus and Staphylococcus epidermidis secretomes isolated from the skin microbiota of atopic children on CD4 + T cell activation. PLoS ONE 10(10):e0141067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Prince AA, Steiger JD, Khalid AN et al (2008) Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol 22(3):239–245

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Otolaryngology Head and Neck surgery, Beijing Tongren Hospital, CMU, No. 1 Dongjiao Folk Lane, Dongcheng District, Beijing, 100730, China

    Hong-Zheng Wei, Yun-Chuan Li, Xiang-Dong Wang, Chun-Hua Hu, Shuai He & Xin Liu

  2. Department of Clinical Laboratory, Beijing Tongren Hospital, CMU, Beijing, 100730, China

    Xin-Xin Lu

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  1. Hong-Zheng Wei
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Correspondence to Yun-Chuan Li.

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Wei, HZ., Li, YC., Wang, XD. et al. The microbiology of chronic rhinosinusitis with and without nasal polyps. Eur Arch Otorhinolaryngol 275, 1439–1447 (2018). https://doi.org/10.1007/s00405-018-4931-6

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  • DOI: https://doi.org/10.1007/s00405-018-4931-6

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