Microbiota of the nasal cavity. Part 3

REVIEWS

Keywords:
nasal cavity microbiota pathogenesis allergic rhinitis chronic rhinosinusitis neurodegenerative diseases probiotic correction of nasal cavity microbiota микробиота носовой полости патогенез аллергический ринит хронический риносинусит нейродегенеративные заболевания пробиотическая коррекция микробиоты носовой полости

Abstract

This review presents the results of studies that emphasise the importance of the nasal cavity microbiota in the context of various diseases. The composition of the microbiota in the nasal cavity of patients with asthma differs significantly from healthy individuals, with changes in the microbiome being closely related to asthma activity and alterations in glycerolipid metabolism. The microbiota plays an important role in the pathogenesis of allergic rhinitis, especially in the context of the Th2-mediated inflammatory response. Early colonisation by certain microbes may influence the risk of developing allergic reactions. The nasal microbiota may influence susceptibility to respiratory infections, including influenza and other viral diseases, by enhancing or attenuating inflammation. Pathogenic microbes in the nasal cavity can contribute to otitis media by migrating to the middle ear, causing inflammation and infection. There is a link between the nasal cavity microbiota and the development of neurodegenerative diseases, including Alzheimer’s disease, Parkinson’s disease and multiple sclerosis, through mechanisms involving chronic inflammation and molecular mimicry. The use of probiotics may hold promise in the treatment of various conditions including chronic rhinosinusitis, allergic rhinitis and as support in the treatment of respiratory infections by improving microbiota composition and maintaining immune balance.

Author Biographies

Anatoly I. Khavkin, Research and Clinical Institute of Childhood Ministry of Health of the Moscow Region; Belgorod State University

Dr. Sci. (Med.), Professor, Head of the Moscow state center of gastroenterology and hepatology of the Research Clinical Institute of Childhood, Ministry of Health of the Moscow Region; Professor, Department of Pediatrics, Medical Institute, Belgorod National Research University

Kirill M. Nikolaychuk, Novosibirsk National Research State University; N.N. Vorozhtsov Novosibirsk Institute of Organic Chemistry, Siberian Branch of the Russian Academy of Sciences

Associate of the Laboratory of Viral Protease Inhibitors, Novosibirsk Institute of Organic Chemistry, Siberian Branch of the Russian Academy of Sciences, Resident Neurologist of the First Year Center for Postgraduate Medical Education, Institute of Medicine and Medical Technologies, Novosibirsk State University

Ksenia M. Stavriyani, Consultative and Diagnostic Polyclinic No. 2

Physician

Polina Ya. Platonova, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Maria F. Novikova, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Artem S. Tumas, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Ekaterina E. Vergunova, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Dmitry A. Lukichev, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Danil A. Sergeev, Novosibirsk National Research State University

student of the Faculty of Medicine and Psychology

Evgenia V. Krylova, Novosibirsk National Research State University; Institute of Chemical Biology and Fundamental Medicine of the Siberian Branch of the Russian Academy of Sciences

Cand. Sci. (Med.), gastroenterologist, pediatrician, researcher of the institute of chemical, Institute of Chemical Biology and Fundamental Medicine of the SB RAS; Associate Professor of the Department of Obstetrics and Gynecology, Faculty of Medicine, Novosibirsk State University

References

1. Tai J., Han M.S., Kwak J., Kim T.H. Association Between Microbiota and Nasal Mucosal Diseases in terms of Immunity. Int J Mol Sci. 2021.22(9):4744. https://doi.org/10.3390/ijms22094744.

2. Fokkens W.J., Lund V.J., Hopkins C., Hellings P.W., Kern R., Reitsma S. et al. Epos2020: a major step forward. Rhinology. 2020.58(1):1. https://doi.org/10.4193/Rhin20.401.

3. Bauer A.M., Turner J.H. Personalized Medicine in Chronic Rhinosinusitis: Phenotypes, Endotypes, and Biomarkers. Immunol Allergy Clin North Am. 2020.40(2):281–293. https://doi.org/10.1016/j.iac.2019.12.007.

4. Kim Y.S., Han D., Mo J.H., Kim Y.M., Kim D.W., Choi H.G. et al. Antibiotic Dependent Relationships Between the Nasal Microbiome and Secreted Proteome in Nasal Polyps. Allergy Asthma Immunol Res. 2021.13(4):589–608. https://doi.org/10.4168/aair.2021.13.4.589.

5. Rom D., Bassiouni A., Eykman E., Liu Z., Paramasivan S., Alvarado R. et al. The Association Between Disease Severity and Microbiome in Chronic Rhinosinusitis. Laryngoscope. 2019.129(6):1265–1273. https://doi.org/10.1002/lary.27726.

6. Lee K., Tai J., Lee S.H., Kim T.H. Advances in the Knowledge of the Underlying Airway Remodeling Mechanisms in Chronic Rhinosinusitis Based on the Endotypes: A Review. Int J Mol Sci. 2021.22(2):910. https://doi.org/10.3390/ijms22020910.

7. Rawls M., Ellis A.K. The microbiome of the nose. Ann Allergy Asthma Immunol. 2019.122(1):17–24. https://doi.org/10.1016/j.anai.2018.05.009.

8. Dimitri Pinheiro S., Soares R., Barata P. The Microbiome of the Nose Friend or Foe? Allergy Rhinol (Providence). 2020.11:2152656720911605. https://doi.org/10.1177/2152656720911605.

9. Min J.Y., Tan B.K. Risk factors for chronic rhinosinusitis. Curr Opin Allergy Clin Immunol. 2015.15(1):1–13. https://doi.org/10.1097/Aci.0000000000000128.

10. Peace O., Rachakonda K., Kress M., Villalta F., Rachakonda G. Respiratory and Neurological Disease across Different Ethnic Groups Is Influenced by the Microbiome. Microorganisms. 2021.9(9):1965. https://doi.org/10.3390/microorganisms9091965.

11. Zhou Y., Jackson D., Bacharier L.B., Mauger D., Boushey H., Castro M. et al. The upper airway microbiota and loss of asthma control among asthmatic children. Nat Commun. 2019.10(1):5714. https://doi.org/10.1038/s41467-019-13698_x.

12. Teräsjärvi J.T., Toivonen L., Vuononvirta J., Mertsola J., Peltola V., He Q. Tlr4 Polymorphism, Nasopharyngeal Bacterial Colonization, and the Development of Childhood Asthma: A Prospective Birth Cohort Study in Finnish Children. Genes (Basel). 2020.11(7):768. https://doi.org/10.3390/genes11070768.

13. Toivonen L., Karppinen S., Schuez Havupalo L., Waris M., He Q., Hoffman K.L. et al. Longitudinal Changes in Early Nasal Microbiota and the Risk of Childhood Asthma. Pediatrics. 2020.146(4):e20200421. https://doi.org/10.1542/peds.2020-0421.

14. Espuela Ortiz A., Lorenzo Diaz F., Baez Ortega A., Eng C., Hernandez Pacheco N., Oh S.S. et al. Bacterial salivary microbiome associates with asthma among africanamerican children and young adults. Pediatr Pulmonol. 2019.54(12):1948–1956. https://doi.org/10.1002/ppul.24504.

15. Lee J.J., Kim S.H., Lee M.J., Kim B.K., Song W.J., Park H.W. et al. Different upper airway microbiome and their functional genes associated with asthma in young adults and elderly individuals. Allergy. 2019.74(4):709–719. https://doi.org/10.1111/all.13608.

16. Wu B.G., Sulaiman I., Wang J., Shen N., Clemente J.C., Li Y. et al. Severe Obstructive Sleep Apnea Is Associated with Alterations in the Nasal Microbiome and an Increase in Inflammation. Am J Respir Crit Care Med. 2019.199(1):99–109. https://doi.org/10.1164/rccm.201801_0119oc.

17. Meng Y., Wang C., Zhang L. Recent developments and highlights in allergic rhinitis. Allergy. 2019.74(12):2320–2328. https://doi.org/10.1111/all.14067.

18. van de Veen W., Akdis M. The use of biologics for immune modulation in allergic disease. J Clin Invest. 2019.129(4):1452–1462. https://doi.org/10.1172/JCi124607.

19. Lee K.H., Gordon A., Shedden K., Kuan G., Ng S., Balmaseda A. et al. The respiratory microbiome and susceptibility to influenza virus infection. PLo S One. 2019.14(1):e0207898. https://doi.org/10.1371/journal.pone.0207898.

20. Toivonen L., Hasegawa K., Waris M., Ajami N.J., Petrosino J.F., Camargo C.A.Jr. et al. Early nasal microbiota and acute respiratory infections during the first years of life. Thorax. 2019.74(6):592–599. https://doi.org/10.1136/thoraxjnl-2018-212629.

21. Tsang T.K., Lee K.H., Foxman B., Balmaseda A., Gresh L., Sanchez N. et al. Association Between the Respiratory Microbiome and Susceptibility to Influenza Virus Infection. Clin Infect Dis. 2020.71(5):1195–1203. https://doi.org/10.1093/cid/ciz968.

22. Toivonen L., Camargo C.A. Jr., Gern J.E., Bochkov Y.A., Mansbach J.M., Piedra P.A. et al. Association between rhinovirus species and nasopharyngeal microbiota in infants with severe bronchiolitis. J Allergy Clin Immunol. 2019.143(5):1925–1928.e7. https://doi.org/10.1016/j.jaci.2018.

23. Mansbach J.M., Hasegawa K., Piedra P.A., Avadhanula V., Petrosino J.F., Sullivan A.F. et al. Haemophilus Dominant Nasopharyngeal Microbiota Is Associated With Delayed Clearance of Respiratory Syncytial Virus in Infants Hospitalized for Bronchiolitis. J Infect Dis. 2019.219(11):1804–1808. https://doi.org/10.1093/infdis/jiy741.

24. Rueca M., Fontana A., Bartolini B., Piselli P., Mazzarelli A., Copetti M. et al. Investigation of Nasal/Oropharyngeal Microbial Community of Covid-19 Patients by 16S r Dna Sequencing. Int J Environ Res Public Health. 2021.18(4):2174. https://doi.org/10.3390/ijerph18042174.

25. Rosas Salazar C., Kimura K.S., Shilts M.H., Strickland B.A., Freeman M.H., Wessinger B.C. et al. Sars Co V-2 infection and viral load are associated with the upper respiratory tract microbiome. J Allergy Clin Immunol. 2021.147(4):1226–1233.e2. https://doi.org/10.1016/j.jaci.2021.02.001.

26. Ko J.Y., Danielson M.L., Town M., Derado G., Greenlund K.J., Kirley P.D., et al. Covid NET Surveillance Team. Risk Factors for Coronavirus Disease 2019 (Covid-19)-Associated Hospitalization: Covid-19-Associated Hospitalization Surveillance Network and Behavioral Risk Factor Surveillance System. Clin Infect Dis. 2021.72(11):e695_e703. https://doi.org/10.1093/cid/ciaa1419.

27. Sze S., Pan D., Nevill C.R., Gray L.J., Martin C.A., Nazareth J. et al. Ethnicity and clinical outcomes in Covid-19: A systematic review and meta analysis. E Clinical Medicine. 2020.29:100630. https://doi.org/10.1016/j.eclinm.2020.100630.

28. Xu R., Liu P., Zhang T., Wu Q., Zeng M., Ma Y. et al. Progressive deterioration of the upper respiratory tract and the gut microbiomes in children during the early infection stages of Covid-19. J Genet Genomics. 2021.48(9):803–814. https://doi.org/10.1016/j.jgg.2021.05.004.

29. Xu R., Lu R., Zhang T., Wu Q., Cai W., Han X. et al. Temporal association between human upper respiratory and gut bacterial microbiomes during the course of Covid-19 in adults. Commun Biol. 2021.4(1):240. https://doi.org/10.1038/s42003-021-01796_w.

30. Walker R.E., Walker C.G., Camargo C.A. Jr., Bartley J., Flint D., Thompson J.M.D. et al. Nasal microbial composition and chronic otitis media with effusion: A case control study. Plos One. 2019.14(2):e0212473. https://doi.org/10.1371/journal.pone.0212473.

31. Lindberg H., Colliander C., Nise L., Dahlqvist J., Knight A. Are Farming and Animal Exposure Risk Factors for the Development of Granulomatosis With Polyangiitis? Environmental Risk Factors Revisited: A Case control Study. J Rheumatol. 2021.48(6):894–897. https://doi.org/10.3899/jrheum.200210.

32. Totté J.E.E., Pardo L.M., Fieten K.B., Vos M.C., van den Broek T.J., Schuren F.H.J. et al. Nasal and skin microbiomes are associated with disease severity in paediatric atopic dermatitis. Br J Dermatol. 2019.181(4):796–804. https://doi.org/10.1111/bjd.17755.

33. van Mierlo M.M.F., Pasmans S.G.M.A., Totté J.E.E., de Wit J., Herpers B.L., Vos M.C. et al. Temporal Variation in Staphylococcus aureus Protein A Genotypes from Nose and Skin in Atopic Dermatitis Patients. Dermatology. 2021.237(4):506–512. https://doi.org/.1159/000515235.

34. Brunner P.M., Guttman Yassky E. Racial differences in atopic dermatitis. Ann Allergy Asthma Immunol. 2019.122(5):449–455. https://doi.org/10.1016/j.anai.2018.11.015.

35. Chen L., Li J., Zhu W., Kuang Y., Liu T., Zhang W. et al. Skin and Gut Microbiome in Psoriasis: Gaining Insight Into the Pathophysiology of It and Finding Novel Therapeutic Strategies. Front Microbiol. 2020.11:589726. https://doi.org/10.3389/fmicb.2020.589726.

36. Kamiya K., Kishimoto M., Sugai J., Komine M., Ohtsuki M. Risk Factors for the Development of Psoriasis. Int J Mol Sci. 2019.20(18):4347. https://doi.org/10.3390/ijms20184347.

37. Harrass S., Yi C., Chen H. Chronic Rhinosinusitis and Alzheimer’s Disease A Possible Role for the Nasal Microbiome in Causing Neurodegeneration in the Elderly. Int J Mol Sci. 2021.22(20):11207. https://doi.org/10.3390/ijms222011207.

38. Lotz S.K., Blackhurst B.M., Reagin K.L., Funk K.E. Microbial Infections Are a Risk Factor for Neurodegenerative Diseases. Front Cell Neurosci. 2021.15:691136. https://doi.org/10.3389/fncel.2021.691136.

39. Subramaniapillai S., Almey A., Natasha Rajah M., Einstein G. Sex and gender differences in cognitive and brain reserve: Implications for Alzheimer’s disease in women. Front Neuroendocrinol. 2021.60:100879. https://doi.org/10.1016/j.yfrne.2020.100879.

40. Gilsanz P., Lee C., Corrada M.M., Kawas C.H., Quesenberry C.P. Jr., Whitmer R.A. Reproductive period and risk of dementia in a diverse cohort of health care members. Neurology. 2019.92(17):e2005_e2014. https://doi.org/10.1212/Wnl.0000000000007326.

41. Jung H.J., Lee J.Y., Choi Y.S., Choi H.G., Wee J.H. Chronic rhinosinusitis and progression of cognitive impairment in dementia. Eur Ann Otorhinolaryngol Head Neck Dis. 2021.138(3):147–151. https://doi.org/10.1016/j.anorl.2020.05.017.

42. Jafari A., de Lima Xavier L., Bernstein J.D., Simonyan K., Bleier B.S. Association of Sinonasal Inflammation With Functional Brain Connectivity. Jama Otolaryngol Head Neck Surg. 2021.147(6):534–543. https://doi.org/10.1001/jamaoto.2021.0204.

43. Wee J.H., Yoo D.M., Byun S.H., Hong S.J., Park M.W., Choi H.G. Association between neurodegenerative dementia and chronic rhinosinusitis: A nested case control study using a national health screening cohort. Medicine (Baltimore). 2020.99(36):e22141. https://doi.org/10.1097/Md.0000000000022141.

44. Kaur D., Sharma V., Deshmukh R. Activation of microglia and astrocytes: a roadway to neuroinflammation and Alzheimer’s disease. Inflammopharmacology. 2019.27(4):663–677. https://doi.org/10.1007/s10787-019-00580_x.

45. Imamura F., Ito A., La Fever B.J. Subpopulations of Projection Neurons in the Olfactory Bulb. Front Neural Circuits. 2020.14:561822. https://doi.org/10.3389/fncir.2020.561822.

46. Yoo S.J., Son G., Bae J., Kim S.Y., Yoo Y.K., Park D. et al. Longitudinal profiling of oligomeric Aβ in human nasal discharge reflecting cognitive decline in probable Alzheimer’s disease. Sci Rep. 2020.10(1):11234. https://doi.org/10.1038/s41598-020-68148-2.

47. Rowan N.R., Schlosser R.J., Storck K.A., Ganjaei K.G., Soler Z.M. The impact of medical therapy on cognitive dysfunction in chronic rhinosinusitis. Int Forum Allergy Rhinol. 2019.9(7):738–745. https://doi.org/10.1002/alr.22323.

48. Kuang L., Hashimoto K., Huang E.J., Gentry M.S., Zhu H. Frontotemporal dementia non sense mutation of progranulin rescued by aminoglycosides. Hum Mol Genet. 2020.29(4):624–634. https://doi.org/10.1093/hmg/ddz280.

49. Gioacchini F.M., Ferlito S., Ralli M., Scarpa A., La Mantia I., Re M. et al. Nasal Microbiota and Neuroinflammation: Relationship between Nasal Flora and Multiple Sclerosis Onset/Progression. Life (Basel). 2022.12(12):2043. https://doi.org/10.3390/life12122043.

50. Zhao Y., Chen J., Hao Y., Wang B., Wang Y., Liu Q. et al. Predicting the recurrence of chronic rhinosinusitis with nasal polyps using nasal microbiota. Allergy. 2022.77(2):540–549. https://doi.org/10.1111/all.15168.

51. Di Stadio A., Costantini C., Renga G., Pariano M., Ricci G., Romani L. The Microbiota/Host Immune System Interaction in the Nose to Protect from Covid-19. Life (Basel). 2020.10(12):345. https://doi.org/10.3390/life10120345.

52. Loosen S.H., Doege C., Meuth S.G., Luedde T., Kostev K., Roderburg C. Infectious mononucleosis is associated with an increased incidence of multiple sclerosis: Results from a cohort study of 32,116 outpatients in Germany. Front Immunol. 2022.13:937583. https://doi.org/10.3389/fimmu.2022.937583.

53. Di Stadio A., Romani L., Bernitsas E. Could Sars Cov2 affect Ms progression? Mult Scler Relat Disord. 2020.46:102540. https://doi.org/10.1016/j.msard.2020.102540.

54. Thangaleela S., Sivamaruthi B.S., Kesika P., Bharathi M., Chaiyasut C. Nasal Microbiota, Olfactory Health, Neurological Disorders and Aging A Review. Microorganisms. 2022.10(7):1405. https://doi.org/10.3390/microorganisms10071405.

55. Thangaleela S., Sivamaruthi B.S., Kesika P., Bharathi M., Kunaviktikul W., Klunklin A. et al. Essential Oils, Phytoncides, Aromachology, and Aromatherapy — A Review. Appl Sci. 2022.12(9):4495. https://doi.org/10.3390/app12094495.

56. Bell J.S., Spencer J.I., Yates R.L., Yee S.A., Jacobs B.M., De Luca G.C. Invited Review: From nose to gut — the role of the microbiome in neurological disease. Neuropathol Appl Neurobiol. 2019.45(3):195–215. https://doi.org/10.1111/nan.12520.

57. Elgamal Z., Singh P., Geraghty P. The Upper Airway Microbiota, Environmental Exposures, Inflammation, and Disease. Medicina (Kaunas). 2021.57(8):823. https://doi.org/10.3390/medicina57080823.

58. Siu J., Shrestha K., Inthavong K., Shang Y., Douglas R. Particle deposition in the paranasal sinuses following endoscopic sinus surgery. Comput Biol Med. 2020.116:103573. https://doi.org/10.1016/j.compbiomed.2019.103573.

59. Spacova I., Petrova M.I., Fremau A., Pollaris L., Vanoirbeek J., Ceuppens J.L. et al. Intranasal administration of probiotic Lactobacillus rhamnosus GG prevents birch pollen induced allergic asthma in a murine model. Allergy. 2019.74(1):100–110. https://doi.org/10.1111/all.13502.

60. Hardy B.L., Dickey S.W., Plaut R.D., Riggins D.P., Stibitz S., Otto M. et al. Corynebacterium pseudodiphtheriticum Exploits Staphylococcus aureus Virulence Components in a Novel Polymicrobial Defense Strategy. m Bio. 2019.10(1):e02491–18. https://doi.org/10.1128/mbio.02491_18.

61. De Grandi R., Drago L., Bidossi A., Bottagisio M., Gelardi M., De Vecchi E. Putative Microbial Population Shifts Attributable to Nasal Administration of Streptococcus salivarius 24SMBc and Streptococcus oralis 89a. Probiotics Antimicrob Proteins. 2019.11(4):1219–1226. https://doi.org/10.1007/s12602-018-9488-6.