The upper respiratory tract microbiome and its role in human health: biotopes and variability
https://doi.org/10.18093/0869-0189-2022-32-5-745-754
Abstract
Human respiratory tract is a complex system with a specific microbiological profile. Until recently, researchers were mostly interested in lung microbial communities associated with acute and chronic infections. The upper respiratory tract microbiota has gained attention during COVID-19 pandemic as it was proposed to be one of the factors affecting the course and the outcome of viral infections. The aim. In this review, we summarized the current knowledge about microbial communities in each section of the upper respiratory tract, considering the proposed barrier function of the respiratory microbiome. Conclusion. The facts provided in the first part of this review give a modern perspective on the structure of microbial communities of each part of the upper respiratory tract and factors that affect their variability.
About the Authors
E. V. Starikova
Federal Research & Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation
Competing Interests:
Russian Federation
Elizaveta V. Starikova, Researcher, Laboratory of Genomic Research and Computational Biology
ul. Malaya Pirogovskaya 1a, Moscow, 119435
Competing Interests:
The author declares no conflict of interests
Ju. S. Galeeva
Federal Research & Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation
Competing Interests:
Russian Federation
Yuliya S. Galeeva, Research Assistant at Laboratory of Genomic Research and Computational Biology
ul. Malaya Pirogovskaya 1a, Moscow, 119435
Competing Interests:
The author declares no conflict of interests
E. N. Ilina
Federal Research & Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation
Competing Interests:
Russian Federation
Elena N. Ilina, Doctor of Biology Science, Professor, Corresponding Member of Russian Academy of Sciences, Head of Laboratory of Genomic Studies and Computational Biology, Deputy Director for Science
ul. Malaya Pirogovskaya 1a, Moscow, 119435
Competing Interests:
The author declares no conflict of interests
References
1. Zhou Y., Mihindukulasuriya K.A., Gao H. et al. Exploration of bacterial community classes in major human habitats. Genome Biol. 2014; 15 (5): R66. https://doi.org/10.1186/gb-2014-15-5-r66.
2. Oh J., Byrd A.L., Deming C. et al. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014; 514 (7520): 59-64. https://doi.org/10.1038/nature13786.
3. Koskinen K., Reichert J.L., Hoier S. et al. The nasal microbiome mirrors and potentially shapes olfactory function. Sci. Rep. 2018; 8 (1): 1296. https://doi.org/10.1038/s41598-018-19438-3.
4. Tizzano M., Gulbransen B.D., Vandenbeuch A. et al. Nasal chemosensory cells use bitter taste signaling to detect irritants and bacterial signals. Proc. Natl. Acad. Sci. USA. 2010; 107 (7): 3210-3215. https://doi.org/10.1073/pnas.0911934107.
5. Lemon K.P., Klepac-Ceraj V., Schiffer H.K. et al. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. mBio. 2010; 1 (3): e00129-10. https://doi.org/10.1128/mBio.00129-10.
6. Ta L.D.H., Yap G.C., Tay C.J.X. et al. Establishment of the nasal microbiota in the first 18 months of life: Correlation with early-onset rhinitis and wheezing. J. Allergy Clin. Immunol. 2018; 142 (1): 86-95. https://doi.org/10.1016/j.jaci.2018.01.032.
7. Ahluwalia J., Borok J., Haddock E.S. et al. The microbiome in preadolescent acne: Assessment and prospective analysis of the influence of Benzoyl peroxide. Pediatr. Dermatol. 2019; 36 (2): 200-206. https://doi.org/10.1111/pde.13741.
8. Ramakrishnan V.R., Feazel L.M., Gitomer S.A. et al. The microbiome of the middle meatus in healthy adults. PLoS One. 2013; 8 (12): e85507. https://doi.org/10.1371/journal.pone.0085507.
9. Pausan M.R., Csorba C., Singer G. et al. Exploring the archaeome: detection of archaeal signatures in the human body. Front. Microbiology. 2019; 10: 2796. https://doi.org/10.3389/fmicb.2019.02796.
10. Abou-Hamad W., Matar N., Elias M. et al. Bacterial flora in normal adult maxillary sinuses. Am. J. Rhinol. Allergy. 2009; 23 (3): 261-263. https://doi.org/10.2500/ajra.2009.23.3317.
11. Abreu N.A., Nagalingam N.A., Song Y. et al. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci. Transl. Med. 2012; 4 (151): 151ra124. https://doi.org/10.1126/scitranslmed.3003783.
12. Boase S., Foreman A., Cleland E. et al. The microbiome of chronic rhinosinusitis: culture, molecular diagnostics and biofilm detection. BMC Infect. Dis. 2013; 13: 210. https://doi.org/10.1186/1471-2334-13-210.
13. Koeller K., Herlemann D.P.R., Schuldt T. et al. Microbiome and culture based analysis of chronic rhinosinusitis compared to healthy sinus mucosa. Front. Microbiol. 2018; 9: 643. https://doi.org/10.3389/fmicb.2018.00643.
14. Cremers A.J., Zomer A.L., Gritzfeld J.F. et al. The adult nasopharyngeal microbiome as a determinant of pneumococcal acquisition. Microbiome. 2014; 2: 44. https://doi.org/10.1186/2049-2618-2-44.
15. De Boeck I., Wittouck S., Wuyts S. et al. Comparing the healthy nose and nasopharynx microbiota reveals continuity as well as niche-specificity. Front. Microbiol. 2017; 8: 2372. https://doi.org/10.3389/fmicb.2017.02372.
16. Watson R.L., de Koff E.M., Bogaert D. Characterising the respiratory microbiome. Eur. Respir. J. 2019; 53 (2): 1801711. https://doi.org/10.1183/13993003.01711-2018.
17. Castro-Nallar E., Bendall M.L., Pérez-Losada M. et al. Composition, taxonomy and functional diversity of the oropharynx microbiome in individuals with schizophrenia and controls. Peer. J. 2015; 3: e1140. https://doi.org/10.7717/peerj.1140.
18. van den Munckhof E.H.A., Hafkamp H.C., de Kluijver J. et al. Nasal microbiota dominated by Moraxella spp. is associated with respiratory health in the elderly population: a case control study. Respir. Res. 2020; 21 (1): 181. https://doi.org/10.1186/s12931-020-01443-8.
19. Chen Y., Xu C., Zhong C. et al. Temporal characteristics of the oropharyngeal and nasal microbiota structure in crewmembers stayed 180 days in the controlled ecological life support system. Front. Microbiol. 2020; 11: 617696. https://doi.org/10.3389/fmicb.2020.617696.
20. Vuononvirta J., Toivonen L., Gröndahl-Yli-Hannuksela K. et al. Nasopharyngeal bacterial colonization and gene polymorphisms of Mannose-binding lectin and Toll-like receptors 2 and 4 in infants. PLoS One. 2011; 6 (10): e26198. https://doi.org/10.1371/journal.pone.0026198.
21. Vuononvirta J., Peltola V., Mertsola J., He Q. Risk of repeated Moraxella catarrhalis colonization is increased in children with Toll-like receptor 4 Asp299Gly polymorphism. Pediatr. Infect. Dis. J. 2013; 32 (11): 1185-1188. https://doi.org/10.1097/INF.0b013e31829e6df2.
22. Nurjadi D., Heeg K., Weber A.N.R., Zanger P. Toll-like receptor 9 (TLR-9) promotor polymorphisms and gene expression are associated with persistent Staphylococcus aureus nasal carriage. Clin. Microbiol. Infect. 2018; 24 (11): 1210.e7-1210.e12. https://doi.org/10.1016/j.cmi.2018.02.014.
23. Vuononvirta J., Peltola V., Ilonen J. et al. The gene polymorphism of IL-17 G-152A is associated with increased colonization of Streptococcus pneumoniae in young finnish children. Pediatr. Infect. Dis. J. 2015; 34 (9): 928-932. https://doi.org/10.1097/INF.0000000000000691.
24. Igartua C., Davenport E.R., Gilad Y. et al. Host genetic variation in mucosal immunity pathways influences the upper airway microbiome. Microbiome. 2017; 5 (11): 16. https://doi.org/10.1186/s40168-016-0227-5.
25. Houpt E.R. Microbial inhabitants of humans: their ecology and role in health and disease. Clin. Infect. Dis. 2005; 41 (5): 768-768. https://doi.org/10.1086/432586.
26. Camarinha-Silva A., Jáuregui R., Pieper D.H., Wos-Oxley M.L. The temporal dynamics of bacterial communities across human anterior nares. Environ. Microbiol Rep. 2012; 4 (1): 126-132. https://doi.org/10.1111/j.1758-2229.2011.00313.x.
27. Wagner Mackenzie B., Chang K., Zoing M. et al. Longitudinal study of the bacterial and fungal microbiota in the human sinuses reveals seasonal and annual changes in diversity. Sci. Rep. 2019; 9 (1): 17416. https://doi.org/10.1038/s41598-019-53975-9.
28. Zhao H., Chen S., Yang F. et al. Alternation of nasopharyngeal microbiota in healthy youth is associated with environmental factors: implication for respiratory diseases. Int. J. Environ. Health Res. 2022; 32 (5): 952-962. https://doi.org/10.1080/09603123.2020.1810209.
29. Bogaert D., Keijser B., Huse S. et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS One. 2011; 6 (2): e17035. https://doi.org/10.1371/journal.pone.0017035.
30. Schoos A.M.M., Kragh M., Ahrens P. et al. Season of birth impacts the neonatal nasopharyngeal microbiota. Children (Basel). 2020; 7 (5): 45. https://doi.org/10.3390/children7050045.
31. Johnston J.R. Hazard prevention and control in the work environment: airborne dust. Protection of the human environment occupational health and environmental health. Series, Geneva, 1999, World Health Organization WHO/SDE/OEH/99.14: English only. Ann. Occup. Hyg. 2000; 44 (5): 405. https://doi.org/10.1093/annhyg/44.5.405.
32. Kreyling W.G., Hirn S., Möller W. et al. Air-blood barrier translocation of tracheally instilled gold nanoparticles inversely depends on particle size. ACS Nano. 2014; 8 (1): 222-233. https://doi.org/10.1021/nn403256v.
33. Kreyling W.G., Semmler-Behnke M., Takenaka S., Möller W. Differences in the biokinetics of inhaled nano- versus micrometer-sized particles. Acc. Chem. Res. 2013; 46 (3): 714-722. https://doi.org/10.1021/ar300043r.
34. Li X., Sun Y., An Y. et al. Air pollution during the winter period and respiratory tract microbial imbalance in a healthy young population in Northeastern China. Environ. Pollut. 2019; 246: 972-979. https://doi.org/10.1016/j.envpol.2018.12.083.
35. Qin T., Zhang F., Zhou H. et al. High-Level PM2.5/PM10 exposure is associated with alterations in the human pharyngeal microbiota composition. Front. Microbiol. 2019; 10: 54. https://doi.org/10.3389/fmicb.2019.00054.
36. Mariani J., Favero C., Spinazzè A. et al. Short-term particulate matter exposure influences nasal microbiota in a population of healthy subjects. Environ. Res. 2018; 162: 119-126. https://doi.org/10.1016/j.envres.2017.12.016.
37. Fajersztajn L., Veras M., Barrozo L.V., Saldiva P. Air pollution: a potentially modifiable risk factor for lung cancer. Nat. Rev. Cancer. 2013; 13 (9): 674-678. https://doi.org/10.1038/nrc3572.
38. Niu Y., Chen R., Wang C. et al. Ozone exposure leads to changes in airway permeability, microbiota and metabolome: a randomised, double-blind, crossover trial. Eur. Respir. J. 2020; 56 (3): 2000165. https://doi.org/10.1183/13993003.00165-2020.
39. Gupta S., Hjelmsø M.H., Lehtimäki J. et al. Environmental shaping of the bacterial and fungal community in infant bed dust and correlations with the airway microbiota. Microbiome. 2020; 8 (1): 115. https://doi.org/10.1186/s40168-020-00895-w.
40. Hanson B., Zhou Y., Bautista E.J. et al. Characterization of the bacterial and fungal microbiome in indoor dust and outdoor air samples: a pilot study. Env. Sci. Process. Impacts. 2016; 18 (6): 713-724. https://doi.org/10.1039/c5em00639b.
41. Shan Y., Guo J., Fan W. et al. Modern urbanization has reshaped the bacterial microbiome profiles of house dust in domestic environments. World Allergy Organ. J. 2020; 13 (8): 100452. https://doi.org/10.1016/j.waojou.2020.100452.
42. Fujimura K.E., Johnson C.C., Ownby D.R. et al. Man’s best friend? The effect of pet ownership on house dust microbial communities. J. Allergy Clin. Immunol. 2010; 126 (2): 410-2, 412.e1-3. https://doi.org/10.1016/j.jaci.2010.05.042.
43. Dannemiller K.C., Gent J.F., Leaderer B.P., Peccia J. Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. Indoor Air. 2016; 26 (2): 179-192. https://doi.org/10.1111/ina.12205.
44. Sharpe R.A., Bearman N., Thornton C.R. et al. Indoor fungal diversity and asthma: a meta-analysis and systematic review of risk factors. J. Allergy Clin. Immunol. 2015; 135 (1): 110-122. https://doi.org/10.1016/j.jaci.2014.07.002.
45. Ciaccio C.E., Barnes C., Kennedy K. et al. Home dust microbiota is disordered in homes of low-income asthmatic children. J. Asthma. 2015; 52 (9): 873-880. https://doi.org/10.3109/02770903.2015.1028076.
46. Fu X., Norbäck D., Yuan Q. et al. Indoor microbiome, environmental characteristics and asthma among junior high school students in Johor Bahru, Malaysia. Environ. Int. 2020; 138: 105664. https://doi.org/10.1016/j.envint.2020.105664.
47. Prasetyo A., Sadhana U., Budiman J. Nasal mucociliary clearance in smokers: a systematic review. Int. Arch. Otorhinolaryngol. 2021; 25 (1): e160-169. https://doi.org/10.1055/s-0040-1702965.
48. Sapkota A.R., Berger S., Vogel T.M. Human pathogens abundant in the bacterial metagenome of cigarettes. Environ. Health Perspect. 2010; 118 (3): 351-356. https://doi.org/10.1289/ehp.0901201.
49. Arcavi L., Benowitz N.L. Cigarette smoking and infection. Arch. Int. Med. 2004; 164 (20): 2206-2216. https://doi.org/10.1001/archinte.164.20.2206.
50. Brook I., Gober A.E. Recovery of potential pathogens and interfering bacteria in the nasopharynx of smokers and nonsmokers. Chest. 2005; 127 (6): 2072-2075. https://doi.org/10.1378/chest.127.6.2072.
51. Charlson E.S., Chen J., Custers-Allen R. et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One. 2010; 5 (12): e15216. https://doi.org/10.1371/journal.pone.0015216.
52. Turek E.M., Cox M.J., Hunter M. et al. Airway microbial communities, smoking and asthma in a general population sample. EBioMedicine. 2021; 71: 103538. https://doi.org/10.1016/j.ebiom.2021.103538.
53. Bugova G., Janickova M., Uhliarova B. et al. The effect of passive smoking on bacterial colonisation of the upper airways and selected laboratory parameters in children. Acta Otorhinolaryngol. Ital. 2018; 38 (5): 431-438. https://doi.org/10.14639/0392-100X-1573.
54. Greenberg D., Givon-Lavi N., Broides A. et al. The contribution of smoking and exposure to tobacco smoke to Streptococcus pneumoniae and Haemophilus influenzae carriage in children and their mothers. Clin. Infect. Dis. 2006; 42 (7): 897-903. https://doi.org/10.1086/500935.
55. Douglas P., Robertson S., Gay R. et al. A systematic review of the public health risks of bioaerosols from intensive farming. Int. J. Hyg. Environ. Health. 2018; 221 (2): 134-173. https://doi.org/10.1016/j.ijheh.2017.10.019.
56. Gilbert Y., Duchaine C. Bioaerosols in industrial environments: a review. J. Environmental Eng. Sci. 2014; 9 (1): 4-19. https://doi.org/10.1680/jees.2014.9.1.4.
57. Kraemer J.G., Ramette A., Aebi S. et al. Influence of pig farming on the human nasal microbiota: key role of airborne microbial communities. Appl. Environ. Microbiol. 2018; 84 (6): e02470-17. https://doi.org/10.1128/AEM.02470-17.
58. Mbareche H., Veillette M., Pilote J. et al. Bioaerosols play a major role in the nasopharyngeal microbiota content in agricultural environment. Int. J. Environ. Res. Public Health. 2019; 16 (8): 1375. https://doi.org/10.3390/ijerph16081375.
59. Wardyn S.E., Forshey B.M., Farina S.A. et al. Swine farming is a risk factor for Infection with and high prevalence of carriage of multidrug-resistant Staphylococcus aureus. Clin. Infect. Dis. 2015; 61 (1): 59-66. https://doi.org/10.1093/cid/civ234.
60. Arends J.P., Hartwig N., Rudolphy M., Zanen H.C. Carrier rate of Streptococcus suis capsular type 2 in palatine tonsils of slaughtered pigs. J. Clin. Microbiol. 1984; 20 (5): 945-947. https://doi.org/10.1128/jcm.20.5.945-947.1984.
61. Gottschalk M., Segura M. The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet. Microbiol. 2000; 76 (3): 259-272. https://doi.org/10.1016/S0378-1135(00)00250-9.
62. Yongkiettrakul S., Maneerat K., Arechanajan B. et al. Antimicrobial susceptibility of Streptococcus suis isolated from diseased pigs, asymptomatic pigs, and human patients in Thailand. BMC Vet. Res. 2019; 15 (1): 5. https://doi.org/10.1186/s12917-018-1732-5.
63. Gottschalk M., Xu J., Calzas C., Segura M. Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol. 2010; 5 (3): 371-391. https://doi.org/10.2217/fmb.10.2.
64. Shukla S.K., Ye Z., Sandberg S. et al. The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci. PLoS One. 2017; 12 (8): e0183898. https://doi.org/10.1371/journal.pone.0183898.
65. Kraemer J.G., Aebi S., Hilty M., Oppliger A. Nasal microbiota composition dynamics after occupational change in animal farmers suggest major shifts. Sci. Total Environ. 2021; 782: 146842. https://doi.org/10.1016/j.scitotenv.2021.146842.
66. Wipler J., Čermáková Z., Hanzálek T. et al. [Sharing bacterial microbiota between owners and their pets (dogs, cats)]. Klin. Mikrobiol. Infekc. Lek. 2017; 23 (2): 48-57. Available at: https://europepmc.org/article/med/28903168 (in Czech).
67. Misic A.M., Davis M.F., Tyldsley A.S. et al. The shared microbiota of humans and companion animals as evaluated from Staphylococcus carriage sites. Microbiome. 2015; 3: 2. https://doi.org/10.1186/s40168-014-0052-7.
68. Jourdain S., Smeesters P.R., Denis O. et al. Differences in nasopharyngeal bacterial carriage in preschool children from different socio-economic origins. Clin. Microbiol. Infect. 2011; 17 (6): 907-914. https://doi.org/10.1111/j.1469-0691.2010.03410.x.
69. Maleki A., Mirnaseri Z., Kouhsari E. et al. Asymptomatic carriers of Neisseria meningitidis and Moraxella catarrhalis in healthy children. New Microbes New Infect. 2020; 36: 100691. https://doi.org/10.1016/j.nmni.2020.100691
70. Conyn-van Spaendonck M.A., Reintjes R., Spanjaard L. et al. Meningococcal carriage in relation to an outbreak of invasive disease due to Neisseria meningitidis serogroup C in the Netherlands. J. Infect. 1999; 39 (1): 42-48. https://doi.org/10.1016/s0163-4453(99)90101-9.
71. Principi N., Marchisio P., Schito G.C., Mannelli S. Risk factors for carriage of respiratory pathogens in the nasopharynx of healthy children. Ascanius Project Collaborative Group Pediatr. Infect. Dis. J. 1999; 18 (6): 517-523. https://doi.org/10.1097/00006454-199906000-00008.
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Starikova E.V., Galeeva J.S., Ilina E.N. The upper respiratory tract microbiome and its role in human health: biotopes and variability. PULMONOLOGIYA. 2022;32(5):745-754. (In Russ.) https://doi.org/10.18093/0869-0189-2022-32-5-745-754
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