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European Archives of Oto-Rhino-Laryngology

, Volume 275, Issue 6, pp 1439–1447 | Cite as

The microbiology of chronic rhinosinusitis with and without nasal polyps

  • Hong-Zheng Wei
  • Yun-Chuan Li
  • Xiang-Dong Wang
  • Xin-Xin Lu
  • Chun-Hua Hu
  • Shuai He
  • Xin Liu
Rhinology

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.

Keywords

Microbiology Chronic rhinosinusitis Staphylococcus epidermidis Staphylococcus aureus 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Kato A (2015) Immunopathology of chronic rhinosinusitis. Allergol Int 64(2):121–130CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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):1479–1490CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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):1–12PubMedGoogle Scholar
  4. 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):1097–1107CrossRefPubMedGoogle Scholar
  5. 5.
    Frank DN, Pace NR (2008) Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24(1):4–10CrossRefPubMedGoogle Scholar
  6. 6.
    Tabas I, Glass CK (2013) Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 339(6116):166–172CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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):e85507CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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):151ra124–151ra124CrossRefGoogle Scholar
  9. 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):631–640CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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):210CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Feazel LM, Robertson CE, Ramakrishnan VR, Frank DN (2012) Microbiome complexity and Staphylococcus aureus in chronic rhinosinusitis. Laryngoscope 122(2):467–472CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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):804CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ivanov II, Atarashi K, Manel N et al (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139(3):485–498CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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):337–349CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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):1739–1745PubMedGoogle Scholar
  16. 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):519–527CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Atarashi K, Tanoue T, Shima T et al (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331(6015):337–341CrossRefPubMedGoogle Scholar
  18. 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):1073–1080CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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. e343CrossRefPubMedGoogle Scholar
  20. 20.
    Tomassen P, Zele TV, Zhang N et al (2011) Pathophysiology of chronic rhinosinusitis. Proc Am Thorac Soc 8(1):115–120CrossRefPubMedGoogle Scholar
  21. 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):1296–1303CrossRefPubMedGoogle Scholar
  22. 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, DCGoogle Scholar
  23. 23.
    Brook I (1989) Bacteriology of chronic maxillary sinusitis in adults. Ann Otol Rhinol Laryngol 98(6):426–428CrossRefPubMedGoogle Scholar
  24. 24.
    Rombaux P, Gigi J, Hamoir M, Eloy P, Bertrand B (2002) Bacteriology of chronic sinusitis: the bulla ethmoidalis content. Rhinology 40(1):18–23PubMedGoogle Scholar
  25. 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):131–136CrossRefPubMedGoogle Scholar
  26. 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):545–548Google Scholar
  27. 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):1251–1258CrossRefPubMedGoogle Scholar
  28. 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):1328–1338CrossRefPubMedGoogle Scholar
  29. 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):253–262CrossRefPubMedGoogle Scholar
  30. 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.e331CrossRefPubMedGoogle Scholar
  31. 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):1487–1495CrossRefPubMedGoogle Scholar
  32. 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–e373CrossRefPubMedGoogle Scholar
  33. 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):981–983CrossRefPubMedGoogle Scholar
  34. 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):461–465CrossRefPubMedGoogle Scholar
  35. 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):1430–1437CrossRefPubMedGoogle Scholar
  36. 36.
    Jiang RS, Hsu CY, Jang JW (1998) Bacteriology of the maxillary and ethmoid sinuses in chronic sinusitis. J Laryngol Otol 112(9):845–848PubMedGoogle Scholar
  37. 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):498–503CrossRefPubMedGoogle Scholar
  38. 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):650–653Google Scholar
  39. 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):e0141067CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Prince AA, Steiger JD, Khalid AN et al (2008) Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am J Rhinol 22(3):239–245CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Otolaryngology Head and Neck surgery, Beijing Tongren HospitalCMUBeijingChina
  2. 2.Department of Clinical Laboratory, Beijing Tongren HospitalCMUBeijingChina

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