The importance of biodiversity of human microbiota and environment in the susceptibility to the development of bronchial asthma in children
https://doi.org/10.20538/1682-0363-2024-4-197-204
Abstract
Bronchial asthma (BA) remains one of the most common chronic respiratory diseases in childhood. BA develops with a combination of genetic predisposition and environmental factors. Epidemiological data on the development of BA emphasize the role of early-life microbiota in the formation of immune responses and susceptibility to the development of BA. In recent years, enough data has been accumulated to suggest that an imbalance in intestinal and airway microbiota during early life may predispose a child to the development of BA. In turn, the biodiversity of the environment influences the colonization of various biotopes in the human body by microorganisms. The study of the mechanisms of interaction between microbiota communities of the environment and humans will pave the way for the development of new strategies for the prevention of BA.
The aim of this review was to analyze current research aimed at assessing the importance of biodiversity of human microbiota and environment in the susceptibility to the development of BA in children.
Keywords
Supporting agencies: The study was funded by the Russian Science Foundation grant (“The role of microbiota in parasite–host interactions and its metabolic potential as a tool for bronchial asthma control”, agreement dated 01.08.22, No. 22-75-00078).
About the Authors
T. S. Sokolova
Siberian State Medical University
Russian Federation
Russian Federation
2, Moscow Trakt, Tomsk, 634050
V. N. Malchuk
Siberian State Medical University
Russian Federation
Russian Federation
2, Moscow Trakt, Tomsk, 634050
A. A. Nogai
Siberian State Medical University
Russian Federation
Russian Federation
2, Moscow Trakt, Tomsk, 634050
O. S. Fedorova
Siberian State Medical University
Russian Federation
Russian Federation
2, Moscow Trakt, Tomsk, 634050
L. M. Ogorodova
Siberian State Medical University
Russian Federation
Russian Federation
2, Moscow Trakt, Tomsk, 634050
References
1. Reddel H.K., Bacharier L.B., Bateman E.D., Brightling C.E., Brusselle G.G., Buhl R. et al. Global initiative for asthma strategy 2021: executive summary and rationale for key changes. Am. J. Respir. Crit .Care Med. 2022;205(1):17–35. DOI: 10.1164/rccm.202109-2205PP.
2. Haahtela T., Laatikainen T., Alenius H., Auvinen P., Fyhrquist N., Hanski I. et al. Hunt for the origin of allergy – comparing the Finnish and Russian Karelia. Clin. Exp. Allergy. 2015; 45(5):891–901. DOI: 10.1111/cea.12527.
3. Haahtela T., Holgate S., Pawankar R., Akdis C.A., Benjaponpitak S., Caraballo L. et al. The biodiversity hypothesis and allergic disease: world allergy organization position statement. World Allergy Organ J. 2013;6(1):3. DOI: 10.1186/1939- 4551-6-3.
4. Dang A.T., Marsland B.J. Microbes, metabolites, and the gut-lung axis. Mucosal Immunol. 2019;12(4):843–850. DOI: 10.1038/s41385-019-0160-6.
5. Smulders T., Van Der Schee M.P., Maitland-Van Der Zee A.H., Dikkers F.G., Van Drunen C.M. Influence of the gut and airway microbiome on asthma development and disease. Pediatr. Allergy Immunol. 2024;35(3):e14095. DOI: 10.1111/pai.14095.
6. Olszak T., An D., Zeissig S., Vera M.P., Richter J., Franke A. et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336(6080):489– 493. DOI: 10.1126/science.1219328.
7. Lynch S.V., Wood R.A., Boushey H., Bacharier L.B., Bloomberg G.R., Kattan M. et al. Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children. J. Allergy Clin. Immunol. 2014;134(3):593–601. e12. DOI: 10.1016/j.jaci.2014.04.018.
8. Strachan D.P. Hay fever, hygiene, and household size. BMJ. 1989;299(6710):1259–1260. DOI: 10.1136/bmj.299.6710.1259.
9. Rook G.A., Lowry C.A., Raison C.L. Microbial ‘Old Friends’, immunoregulation and stress resilience. Evol. Med. Public Health. 2013;2013(1):46–64. DOI: 10.1093/emph/eot004.
10. Stokholm J., Thorsen J., Chawes B.L., Schjørring S., Krogfelt K.A., Bønnelykke K. et al. Cesarean section changes neonatal gut colonization. J. Allergy Clin. Immunol. 2016;138(3):881–889.e2. DOI: 10.1016/j.jaci.2016.01.028.
11. Christensen E.D., Hjelmsø M.H., Thorsen J., Shah S., Redgwell T., Poulsen C.E. et al. The developing airway and gut microbiota in early life is influenced by age of older siblings. Microbiome. 2022;10(1):106. DOI: 10.1186/s40168-022-01305-z.
12. Depner M., Taft D.H., Kirjavainen P.V., Kalanetra K.M., Karvonen A.M., Peschel S. et al. Maturation of the gut microbiome during the first year of life contributes to the protective farm effect on childhood asthma. Nat. Med. 2020;26(11):1766– 1775. DOI: 10.1038/s41591-020-1095-x.
13. Von Mutius E., Vercelli D. Farm living: effects on childhood asthma and allergy. Nat. Rev. Immunol. 2010;10(12):861–868. DOI: 10.1038/nri2871.
14. Stein M.M., Hrusch C.L., Gozdz J., Igartua C., Pivniouk V., Murray S.E. et al. Innate immunity and asthma risk in amish and hutterite farm children. N. Engl. J. Med. 2016; 375(5):411– 421. DOI: 10.1056/NEJMoa1508749.
15. Strieker S., Weinmann T., Gerlich J., von Mutius E., Nowak D., Radon K. et al. Farm living and allergic rhinitis from childhood to young adulthood: Prospective results of the GABRIEL study. J. Allergy Clin. Immunol. 2022;150(5):1209–1215. e2. DOI: 10.1016/j.jaci.2022.05.027.
16. Bassis C.M., Erb-Downward J.R., Dickson R.P., Freeman C.M., Schmidt T.M., Young V.B. et al. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. mBio. 2015;6(2):e00037. DOI: 10.1128/mBio.00037-15.
17. Hilty M., Burke C., Pedro H., Cardenas P., Bush A., Bossley C. et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010;5(1):e8578. DOI: 10.1371/journal.pone.0008578.
18. Thorsen J., Rasmussen M.A., Waage J., Mortensen M., Brejnrod A., Bønnelykke K. et al. Infant airway microbiota and topical immune perturbations in the origins of childhood asthma. Nat Commun. 2019 Nov 1; 10(1):5001. DOI: 10.1038/s41467-019-12989-7.
19. Tang H.H.F., Lang A., Teo S.M., Judd L.M., Gangnon R., Evans M.D. et al. Developmental patterns in the nasopharyngeal microbiome during infancy are associated with asthma risk. J Allergy Clin. Immunol. 2021;47(5):1683–1691. DOI: 10.1016/j.jaci.2020.10.009.
20. Thorsen J., Li X.J., Peng S., Sunde R.B., Shah S.A., Bhattacharyya M. et al. The airway microbiota of neonates colonized with asthma-associated pathogenic bacteria. Nat. Commun. 2023;14(1):6668. DOI: 10.1038/s41467-023-42309-z.
21. 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. DOI: 10.1542/peds.2020-0421.
22. Teo S.M., Mok D., Pham K., Kusel M., Serralha M., Troy N. et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 2015;17(5):704–715. DOI: 10.1016/j.chom.2015.03.008.
23. Zhu Z., Camargo C.A. Jr., Raita Y., Freishtat R.J., Fujiogi M., Hahn A. et al. Nasopharyngeal airway dual-transcriptome of infants with severe bronchiolitis and risk of childhood asthma: A multicenter prospective study. J. Allergy Clin. Immunol. 2022;150(4):806–816. DOI: 10.1016/j.jaci.2022.04.017.
24. Bataineh M.T., Hamoudi R.A., Dash N.R., Ramakrishnan R.K., Almasalmeh M.A., Sharif H.A. et al. Altered respiratory microbiota composition and functionality associated with asthma early in life. BMC Infect. Dis. 2020;20(1):697. DOI: 10.1186/s12879-020-05427-3.
25. Bar K., Żebrowska P., Łaczmański Ł., Sozańska B. Airway bacterial biodiversity in exhaled breath condensates of asthmatic children-does it differ from the healthy ones? J. Clin. Med. 2022;11(22):6774. DOI: 10.3390/jcm11226774.
26. Weinstock G.M. Genomic approaches to studying the human microbiota. Nature. 2012;489(7415):250–256. DOI: 10.1038/nature11553.
27. Enaud R., Prevel R., Ciarlo E., Beaufils F., Wieërs G., Guery B. et al. The gut-lung axis in health and respiratory diseases: a place for inter-organ and inter-kingdom crosstalks. Front. Cell Infect. Microbiol. 2020;10:9. DOI: 10.3389/fcimb.2020.00009.
28. Wypych T.P., Wickramasinghe L.C., Marsland B.J. The influence of the microbiome on respiratory health. Nat. Immunol. 2019;20(10):1279–1290. DOI: 10.1038/s41590-019-0451-9.
29. Zhong C., Guo J., Tan T., Wang H., Lin L., Gao D. et al. Increased food diversity in the first year of life is inversely associated with allergic outcomes in the second year. Pediatr. Allergy Immunol. 2022;33(1):e13707. DOI: 10.1111/pai.13707.
30. Frei R., Ferstl R., Roduit C., Ziegler M., Schiavi E., Barcik W. et al. Exposure to nonmicrobial N-glycolylneuraminic acid protects farmers’ children against airway inflammation and colitis. J. Allergy Clin. Immunol. 2018;141(1):382–390.e7. DOI: 10.1016/j.jaci.2017.04.051.
31. Rook G.A., Adams V., Hunt J., Palmer R., Martinelli R., Brunet L.R. Mycobacteria and other environmental organisms as immunomodulators for immunoregulatory disorders. Springer Semin. Immunopathol. 2004;25(3-4):237–255. DOI: 10.1007/s00281-003-0148-9.
32. Abrahamsson T.R., Jakobsson H.E., Andersson A.F., Björkstén B., Engstrand L., Jenmalm M.C. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy. 2014;44(6):842–850. DOI: 10.1111/cea.12253.
33. Patrick D.M., Sbihi H., Dai D.L.Y., Al Mamun A., Rasali D., Rose C. et al. Decreasing antibiotic use, the gut microbiota, and asthma incidence in children: evidence from population-based and prospective cohort studies. Lancet Respir. Med. 2020;8(11):1094–1105. DOI: 10.1016/S2213- 2600(20)30052-7.
34. Galazzo G., van Best N., Bervoets L., Dapaah I.O., Savelkoul P.H., Hornef M.W. et al. Development of the microbiota and associations with birth mode, diet, and atopic disorders in a longitudinal analysis of stool samples, collected from infancy through early childhood. Gastroenterology. 2020;158(6):1584-1596. DOI: 10.1053/j.gastro.2020.01.024.
35. Stokholm J., Blaser M.J., Thorsen J., Rasmussen M.A., Waage J., Vinding R.K. et al. Maturation of the gut microbiome and risk of asthma in childhood. Nat. Commun. 2018;9(1):141. DOI: 10.1038/s41467-017-02573-2.
36. Chiu C.Y., Cheng M.L., Chiang M.H., Kuo Y.L., Tsai M.H., Chiu C.C. et al. Gut microbial-derived butyrate is inversely associated with IgE responses to allergens in childhood asthma. Pediatr. Allergy Immunol. 2019;30(7):689–697. DOI: 10.1111/pai.13096.
37. Lee-Sarwar K., Dedrick S., Momeni B., Kelly R.S., Zeiger R.S., O’Connor G.T. et al. Association of the gut microbiome and metabolome with wheeze frequency in childhood asthma. J. Allergy Clin. Immunol. 2022;150(2):325–336. DOI: 10.1016/j.jaci.2022.02.005.
38. Arrieta M.C., Stiemsma L.T., Dimitriu P.A., Thorson L., Russell S., Yurist-Doutsch S. et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 2015;7(307):307ra152. DOI: 10.1126/scitranslmed.aab2271.
39. Fujimura K.E., Sitarik A.R., Havstad S., Lin D.L, Levan S., Fadrosh D. et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat. Med. 2016; 22(10):1187–1191. DOI: 10.1038/nm.4176.
40. Thavagnanam S., Fleming J., Bromley A., Shields M.D., Cardwell C.R. A meta-analysis of the association between Caesarean section and childhood asthma. Clin. Exp. Allergy. 2008;38(4):629–633. DOI: 10.1111/j.1365-2222.2007.02780.x.
41. Chu D.M., Ma J., Prince A.L., Antony K.M., Seferovic M.D., Aagaard K.M. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat. Med. 2017;23(3):314–326. DOI: 10.1038/nm.4272.
42. Laursen M.F., Zachariassen G., Bahl M.I., Bergström A., Høst A., Michaelsen K.F. et al. Having older siblings is associated with gut microbiota development during early childhood. BMC Microbiol. 201515:154. DOI: 10.1186/s12866-015-0477-6.
43. Kirjavainen P.V., Karvonen A.M., Adams R.I., Täubel M., Roponen M., Tuoresmäki P. et al. Farm-like indoor microbiota in non-farm homes protects children from asthma development. Nat. Med. 2019;25(7):1089–1095. DOI: 10.1038/s41591-019-0469-4.
44. Ege M.J., Mayer M., Normand A.C., Genuneit J., Cookson W.O., Braun-Fahrländer C. et al. Exposure to environmental microorganisms and childhood asthma. N. Engl. J. Med. 2011;364(8):701–709. DOI: 10.1056/NEJMoa1007302.
45. Keller A., Groot J., Clippet-Jensen C., Pinot de Moira A., Pedersen M., Sigsgaard T. et al. Exposure to different residential indoor characteristics during childhood and asthma in adolescence: a latent class analysis of the Danish National Birth Cohort. Eur. J. Epidemiol. 2024;39(1):51–65. DOI: 10.1007/s10654-023-01051-y.
46. Schuijs M.J., Willart M.A., Vergote K., Gras D., Deswarte K., Ege M.J. et al. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science. 20154;349(6252):11061110. DOI: 10.1126/science. aac6623.
47. Gupta S., Hjelmsø M.H., Lehtimäki J., Li X., Mortensen M.S., Russel J. et al. 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. DOI: 10.1186/s40168-020-00895-w.
48. Lehtimäki J., Gupta S., Hjelmsø M., Shah S., Thorsen J., Rasmussen M.A. et al. Fungi and bacteria in the beds of rural and urban infants correlate with later risk of atopic diseases. Clin. Exp. Allergy. 2023;53(12):1268–1278. DOI: 10.1111/cea.14414.
49. Karvonen A.M., Kirjavainen P.V., Täubel M., Jayaprakash B., Adams R.I., Sordillo J.E. et al. Indoor bacterial microbiota and development of asthma by 10.5 years of age. J. Allergy Clin. Immunol. 2019;144(5):1402–1410. DOI: 10.1016/j.jaci.2019.07.035.
50. O’Connor G.T., Lynch S.V., Bloomberg G.R., Kattan M., Wood R.A., Gergen P.J. et al. Early-life home environment and risk of asthma among inner-city children. J. Allergy Clin. Immunol. 2018;141(4):1468–1475. DOI: 10.1016/j.jaci.2017.06.040.
51. Dannemiller K.C., Mendell M.J., Macher J.M., Kumagai K., Bradman A., Holland N. et al. Next-generation DNA sequencing reveals that low fungal diversity in house dust is associated with childhood asthma development. Indoor Air. 2014;24(3):236–247. DOI: 10.1111/ina.12072.
52. Dannemiller K.C., Gent J.F., Leaderer B.P., Peccia J. Indoor microbial communities: Influence on asthma severity in atopic and nonatopic children. J. Allergy Clin. Immunol. 2016;138(1):76–83.e1. DOI: 10.1016/j.jaci.2015.11.027.
53. Von Mutius E., Smits H.H. Primary prevention of asthma: from risk and protective factors to targeted strategies for prevention. Lancet. 2020;396(10254):854–866. DOI: 10.1016/S0140-6736(20)31861-4.
Review
For citations:
Sokolova T.S., Malchuk V.N., Nogai A.A., Fedorova O.S., Ogorodova L.M. The importance of biodiversity of human microbiota and environment in the susceptibility to the development of bronchial asthma in children. Bulletin of Siberian Medicine. 2024;23(4):197-204. https://doi.org/10.20538/1682-0363-2024-4-197-204
Views:
162
Email this article 