Allergy Asthma Respir Dis.  2016 Nov;4(6):399-405. 10.4168/aard.2016.4.6.399.

Microbiome of the upper airway focusing on chronic rhinosinusitis and allergic rhinitis

• Hong SN
• Park P
• Cho SH
• Kim DY

• KMID: 2361254
• DOI: http://doi.org/10.4168/aard.2016.4.6.399

Abstract

The human microbiome is a collection of microbial species and their associated genomes that live on and in the body. Recent advances in molecular biology methods have revolutionized microbiome analysis techniques. Studies of the airway microbiome have illustrated that the paranasal sinuses are not sterile in the healthy state. Because human airways are in constant contact with the external environment and their mucosal surfaces are colonized with microorganisms, it is assumed that the local microbiota might influence immune homeostasis as well. Chronic rhinosinusitis and allergic rhinitis are the most common chronic airway diseases that yield a significant amount of socioeconomic burden. Despite the problematic nature of the diseases, a thorough understanding of their cause and pathogenesis is still lacking. At present, bacteria are believed to play a pathogenetic role in the propagation of inflammation and it is necessary to establish the relationship between the microbiome and inflammatory patterns to find their clinical reflections and also their possible causal relationship. Such investigations may elucidate the path to therapeutic approaches in correcting an imbalanced microbiome. In this review, we summarized recent typical studies dealing with the upper airway microbiome and discuss their clinical significance focusing on chronic rhinosinusitis and allergic rhinitis.

Keyword

Airway; Microbiome; Chronic rhinosinusitis; Allergic rhinitis; Metagenomics

MeSH Terms

Bacteria
Colon
Genome
Homeostasis
Humans
Inflammation
Metagenomics
Microbiota*
Molecular Biology
Paranasal Sinuses
Rhinitis, Allergic*

Figure

• 

  Fig. 1 Bacterial community diversity between chronic rhinosinusitis (CRS) and healthy subjects. Diversity index represented by Inverse-Simpson (A), Shannon-Wiener (B) demonstrate that the bacterial diversity of CRS patients are significantly lowever than the healthy counterparts.

• 

  Fig. 2 Bacterial genera that differ in relative abundance between patient subsets. Multiple genus-level alteration was observed between nonasthmatic (A) and asthmatic (B) patients with chronic rhinosinusitis.

Reference

1. Zoetendal EG, Collier CT, Koike S, Mackie RI, Gaskins HR. Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr. 2004; 134:465–472.

2. Weinstock GM. Genomic approaches to studying the human microbiota. Nature. 2012; 489:250–256.

3. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006; 312:1355–1359.

4. Mullard A. Microbiology: the inside story. Nature. 2008; 453:578–580.

5. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006; 124:837–848.

6. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012; 148:1258–1270.

7. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012; 13:260–270.

8. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011; 473:174–180.

9. Morgan XC, Huttenhower C. Chapter 12: Human microbiome analysis. PLoS Comput Biol. 2012; 8:e1002808.

10. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008; 4:337–349.

11. Gliklich RE, Metson R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngol Head Neck Surg. 1995; 113:104–109.

12. Mattos JL, Woodard CR, Payne SC. Trends in common rhinologic illnesses: analysis of U.S. healthcare surveys 1995-2007. Int Forum Allergy Rhinol. 2011; 1:3–12.

13. Asher MI, Montefort S, Björkstén B, Lai CK, Strachan DP, Weiland SK, et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet. 2006; 368:733–743.

14. Krouse JH. The unified airway: conceptual framework. Otolaryngol Clin North Am. 2008; 41:257–266.

15. Ramakrishnan VR, Ferril GR, Suh JD, Woodson T, Green TJ, Kingdom TT. Upper and lower airways associations in patients with chronic rhinosinusitis and bronchiectasis. Int Forum Allergy Rhinol. 2013; 3:921–927.

16. Godoy JM, Godoy AN, Ribalta G, Largo I. Bacterial pattern in chronic sinusitis and cystic fibrosis. Otolaryngol Head Neck Surg. 2011; 145:673–676.

17. Goleva E, Jackson LP, Harris JK, Robertson CE, Sutherland ER, Hall CF, et al. The effects of airway microbiome on corticosteroid responsiveness in asthma. Am J Respir Crit Care Med. 2013; 188:1193–1201.

18. Marri PR, Stern DA, Wright AL, Billheimer D, Martinez FD. Asthma-associated differences in microbial composition of induced sputum. J Allergy Clin Immunol. 2013; 131:346–352.e1-3.

19. Ling Z, Liu X, Luo Y, Yuan L, Nelson KE, Wang Y, et al. Pyrosequencing analysis of the human microbiota of healthy Chinese undergraduates. BMC Genomics. 2013; 14:390.

20. Biswas 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.

21. Choi EB, Hong SW, Kim DK, Jeon SG, Kim KR, Cho SH, et al. Decreased diversity of nasal microbiota and their secreted extracellular vesicles in patients with chronic rhinosinusitis based on a metagenomic analysis. Allergy. 2014; 69:517–526.

22. Ramakrishnan 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.

23. Ramakrishnan VR, Frank DN. Impact of cigarette smoking on the middle meatus microbiome in health and chronic rhinosinusitis. Int Forum Allergy Rhinol. 2015; 5:981–989.

24. Merkley MA, Bice TC, Grier A, Strohl AM, Man LX, Gill SR. The effect of antibiotics on the microbiome in acute exacerbations of chronic rhinosinusitis. Int Forum Allergy Rhinol. 2015; 5:884–893.

25. Bassiouni A, Cleland EJ, Psaltis AJ, Vreugde S, Wormald PJ. Sinonasal microbiome sampling: a comparison of techniques. PLoS One. 2015; 10:e0123216.

26. Choi CH, Poroyko V, Watanabe S, Jiang D, Lane J, deTineo M, et al. Seasonal allergic rhinitis affects sinonasal microbiota. Am J Rhinol Allergy. 2014; 28:281–286.

27. Jung WH, Croll D, Cho JH, Kim YR, Lee YW. Analysis of the nasal vestibule mycobiome in patients with allergic rhinitis. Mycoses. 2015; 58:167–172.

28. Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One. 2010; 5:e15216.

29. Ramakrishnan VR, Feazel LM, Gitomer SA, Ir D, Robertson CE, Frank DN. The microbiome of the middle meatus in healthy adults. PLoS One. 2013; 8:e85507.

30. Yan M, Pamp SJ, Fukuyama J, Hwang PH, Cho DY, Holmes S, et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe. 2013; 14:631–640.

31. Bachert C, Van Bruaene N, Toskala E, Zhang N, Olze H, Scadding G, et al. Important research questions in allergy and related diseases: 3-chronic rhinosinusitis and nasal polyposis - a GALEN study. Allergy. 2009; 64:520–533.

32. Fokkens W, Lund V, Mullol J. European Position Paper on Rhinosinusitis and Nasal Polyps Group. EP3OS 2007: European position paper on rhinosinusitis and nasal polyps 2007. A summary for otorhinolaryngologists. Rhinology. 2007; 45:97–101.

33. Fokkens WJ, Lund VJ, Mullol J, Bachert C, Alobid I, Baroody F, et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology. 2012; 50:1–12.

34. Kumar R, Eipers P, Little RB, Crowley M, Crossman DK, Lefkowitz EJ, et al. Getting started with microbiome analysis: sample acquisition to bioinformatics. Curr Protoc Hum Genet. 2014; 82:18.8.1–18.8.29.

35. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013; 368:407–415.