Gut microbiota dysontogeniya in infants as a factor in the development of atopy
Irina A. Belyaeva,
Elena P. Bombardirova,
Leyla S. Namazova-Baranova,
Elena A. Vishneva,
Pavel E. Sadchikov https://doi.org/10.15690/pf.v16i2.2005
Abstract
The article describes the modern views on the relationship between altered development of gut microbiota in infants and the risk of developing atopic diseases (atopic dermatitis and bronchial asthma). The studies of genetic susceptibility to atopy and the influence of epigenetic mechanisms involved in the regulation of gene expression responsible for the hyperproduction of immunoglobulin E are discussed. The characteristics of the microbiota of infants with already developed atopic diseases and children at risk of atopy are analyzed. In infants who subsequently developed atopy, the composition of gut microbiota at the birth is characterized by a reduced abundance of bifidobacteria and high content of potentially pathogenic microorganisms. The triggering role of active metabolites of altered microbiota on the differentiation of T-regulatory cells has been established. A preventive effect of optimal breastfeeding has been confirmed: meta-analyzes of recent studies indicate a link between the duration of breastfeeding and a decrease in the frequency of bronchial asthma. The microbiota of breast milk contributes to the proper development of the infant’s microbiota, determines its diversity and immunomodulating action. On the basis of the conducted research, methods of targeted correction of the intestinal microbiota in children with risk of atopy can be developed.
Supporting agencies: Not specified
About the Authors
Irina A. Belyaeva
Pirogov Russian National Research Medical University; Morozov Children’s City Clinical Hospital
Russian Federation
Moscow.
Russian Federation
Moscow.
Elena P. Bombardirova
National Medical Research Center for Children’s Health
Russian Federation
Moscow.
Russian Federation
Moscow.
Leyla S. Namazova-Baranova
Pirogov Russian National Research Medical University; Central Clinical Hospital of the Russian Academy of Sciences
Russian Federation
Moscow.
Russian Federation
Moscow.
Elena A. Vishneva
Pirogov Russian National Research Medical University; National Medical Research Center for Children’s Health; Central Clinical Hospital of the Russian Academy of Sciences
Russian Federation
Moscow.
Russian Federation
Moscow.
Pavel E. Sadchikov
Pirogov Russian National Research Medical University
Russian Federation
Moscow.
Russian Federation
Moscow.
References
1. Sly RM. Changing prevalence of allergic rhinitis and asthma. Ann Allergy Asthma Immunol. 1999;82(3):233–248. doi: 10.1016/s1081-1206(10)62603-8.
2. Osnovy klinicheskoj immunologii i allergologii. Ed by LS Namazova-Baranova, LV Gankovskaya, RYa Meshkova. Moscow: Pediatr»; 2016. 152 p. (In Russ).
3. Namazova-Baranova LS, Snovskaya MA, Mitushin IL, et al. Peculiarities of allergy diagnosis in children. Annals of the Russian Academy of Medical Sciences. 2017;72(1):33–41. (In Russ). doi: 10.15690/vramn799.
4. Peng C, Van Meel ER, Cardenas A, et al. Epigenome-wide association study reveals methylation pathways associated with childhood allergic sensitization. Epigenetics. 2019;14(5):445–466. doi: 10.1080/15592294.2019.1590085.
5. Esteller M. (Ed). Epigenetics in biology and medicine. Taylor & Francis Group; 2009. 316 p.
6. Tatochenko VK. Bolezni organov dykhaniya u detej: prakticheskoe rukovodstvo. Moscow: Pediatr”; 2012. 480 p. (In Russ).
7. Belyaeva IA, Bombardirova EP, Mitish MD, et al. Ontogenesis and dysontogenesis of the gut microbiota in young children: a trigger mechanism of child health disorders. Current Pediatrics. 2017;16(1):29–38. (In Russ). doi: 10.15690/vsp.v16i1.1692.
8. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148(6):1258–1270. doi: 10.1016/j.cell.2012.01.035.
9. McGuire AL, Colgrove J, Whitney SN, et al. Ethical, legal, and social considerations in conducting the Human Microbiome Project. Genome Res. 2008;18(12):1861–1864. doi: 10.1101/gr.081653.108.
10. Antony KM, Ma J, Mitchell KB, et al. The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol. 2015;212(5):653.e1–16. doi: 10.1016/j.ajog.2014.12.041.
11. Pelzer E, Gomez-Arango LF, Barrett HL, Nitert MD. Review: maternal health and the placental microbiome. Placenta. 2017;54:30–37. doi: 10.1016/j.placenta.2016.12.003.
12. Chu DM, Antony KM, Ma J, et al. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. 2016;8(1):77. doi: 10.1186/s13073-016-0330-z.
13. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci US A. 2010;107(26):11971-11975. doi: 10.1073/pnas.1002601107.
14. Fouhy F, Watkins C, Hill CJ, et al. Perinatal factors affect the gut microbiota up to four years after birth. Nature Communications. 2019;10:1517. doi: 10.1038/s41467-019-09252-4.
15. Rutayisire E, Huang K, Liu Y Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review. BMC Gastroenterol. 2016;16(1):86. doi: 10.1186/s12876-016-0498-0.
16. Matsuyama M, Gomez-Arango LF, Fukuma NM, et al. Breastfeeding: a key modulator of gut microbiota characteristics in late infancy. J Dev Orig Health Dis. 2019;10(2):206-213. doi: 10.1017/S2040174418000624.
17. Laursen MF, Bahl MI, Michaelsen KF, Licht TR. First foods and gut microbes. Front Microbiol. 2017;8:356. doi: 10.3389/fmicb.2017.00356.
18. Vangay P Ward T, Gerber JS, Knights D. Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe. 2015;17(5):553-564. doi:10.1016/j.chom.2015.04.006.
19. Isolauri E. Microbiota and obesity. Nestle Nutr Inst Workshop Ser. 2017;88:95-105. doi: 10.1159/000455217.
20. Wen L, DuffyA. Factors influencingthe gut microbiota, inflammation, and type 2 diabetes. J Nutr. 2017;147(7):1468S-1475S. doi: 10.3945/jn.116.240754.
21. Kappel BA, Lehrke M. [Microbiome, diabetes and heart: a novel link? (Article in German).] Herz. 2019;44(3):223-230. doi: 10.1007/s00059-019-4791-x.
22. Legatzki A, Rosler B, von Mutius E. Microbiome diversity and asthma and allergy risk. Curr Allergy Asthma Rep. 2014;14(10):466. doi: 10.1007/s11882-014-0466-0.
23. Kang YB, Cai Y Zhang H. Gut microbiota and allergy/asthma: from pathogenesis to new therapeutic strategies. Allergol Immunopathol (Madr). 2017;45(3):305-309. doi: 10.1016/j.aller.2016.08.004.
24. Fujimura KE, Lynch SV. Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe. 2015;17(5):592-602. doi: 10.1016/j.chom.2015.04.007.
25. Kalliomaki M, Kirjavainen P Eerola E, et al. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107(1):129-134. doi:10.1067/mai.2001.111237.
26. Fujimura KE, Sitarik AR, Havstad S, 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.
27. Fujimura KE, Lynch SV. Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe. 2015;17(5):592-602. doi: 10.1016/j.chom.2015.04.007.
28. Oddy WH. Breastfeeding, childhood asthma, and allergic disease. Ann Nutr Metab. 2017;70 Suppl 2:26-36. doi: 10.1159/000457920.
29. Matheson M, Allen KJ, Tang ML. Understanding the evidence for and against the role of breastfeeding in allergy prevention. Clin Exp Allergy. 2012;42(6):827-851. doi: 10.1111/j.1365-2222.2011.03925.x.
30. Gungor D, Nadaud P, LaPergola CC, et al. Infant milk-feeding practices and food allergies, allergic rhinitis, atopic dermatitis, and asthma throughout the life span: a systematic review. Am J Clin Nutr. 2019;109(Suppl 7):772S-799S. doi: 10.1093/ajcn/nqy283.
31. Lodge CJ, Tan DJ, Lau MX, et al. Breastfeeding and asthma and allergies: a systematic review and meta-analysis. Acta Paediatr. 2015;104(467):38-53. doi: 10.1111/apa.13132.
32. Bener A, Ehlayel MS, Alsowaidi S, Sabbah A. Role of breast feeding in primary prevention of asthma and allergic diseases in a traditional society. Eur Ann Allergy Clin Immunol. 2007;39(10):337-343.
33. Tanaka K, Miyake Y, Sasaki S. Association between breastfeeding and allergic disorders in Japanese children. Int J Tuberc Lung Dis. 2010;14(4):513-518.
34. Bion V, Lockett GA, Soto-Ramirez N, et al. Evaluating the efficacy of breastfeeding guidelines on long-term outcomes for allergic disease. Allergy. 2016;71(5):661-670. doi: 10.1111/all.12833.
35. Heinrich J. Modulation of allergy risk by breast feeding. Curr Opin Clin Nutr Metab Care. 2017;20(3):217-221. doi: 10.1097/MCO.0000000000000366.
36. Silvers KM, Frampton CM, Wickens K, et al.; New Zealand Asthma and Allergy Cohort Study Group. Breastfeeding protects against adverse respiratory outcomes at 15 months of age. Matern Child Nutr. 2009;5(3):243-250. doi: 10.1111/j.1740-8709.2008.00169.x.
37. Scholtens S, Wijga AH, Brunekreef B, et al. Breastfeeding, parental allergy and asthma in children followed for eight years: the PIAMA birth cohort study. Thorax. 2009;64(7):604-609. doi: 10.1136/thx.2007.094938.
38. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013;60(1):49-74. doi:10.1016/j.pcl.2012.10.002.
39. Morita Y, Campos-Alberto E, Yamaide F, et al. TGF-p concentration in breast milk is associated with the development of eczema in infants. Front Pediatr. 2018;6:162. doi: 10.3389/fped.2018.00162.
40. Ando T, Hatsushika K, Wako M, et al. Orally administered TGF-beta is biologically active in the intestinal mucosa and enhances oral tolerance. J Allergy Clin Immunol. 2007;120(4):916-923. doi: 10.1016/j.jaci.2007.05.023.
41. Rajani PS, Seppo AE, Jarvinen KM. Immunologically active components in human milk and development of atopic disease, with emphasis on food allergy, in the pediatric population. Front Pediatr. 2018;6:218. doi: 10.3389/fped.2018.00218.
42. Fitzstevens JL, Smith KC, Hagadorn JI, et al. Systematic review of the human milk microbiota. Nutr Clin Pract. 2017;32(3):354-364. doi: 10.1177/0884533616670150.
43. Wang M, Karlsson C, Olsson C, et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol. 2008;121(1):129-134. doi: 10.1016/j.jaci.2007.09.011.
44. Ojo-Okunola A, Nicol M, du Toit E. Human breast milk bacteriome in health and disease. Nutrients. 2018;10(11):1643. doi: 10.3390/nu10111643.
45. Martin R, Olivares M, Marin ML, et al. Probiotic potential of 3 Lactobacilli strains isolated from breast milk. J Hum Lact. 2005;21(1):8-17. doi: 10.1177/0890334404272393.
46. Jost T, Lacroix C, Braegger CP, et al. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2014;16(9):2891-2904. doi: 10.1111/1462-2920.12238.
47. Martin R, Langa S, Reviriego C, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr. 2003;143(6):754-758. doi: 10.1016/j.jpeds.2003.09.028.
48. Fouhy F, Ross RP Fitzgerald GF, et al. Composition of the early intestinal microbiota: Knowledge, knowledge gaps and the use of high-throughput sequencing to address these gaps. Gut Microbes. 2012;3(3):203-220. doi: 10.4161/gmic.20169.
49. Cabrera-Rubio R, Collado MC, Laitinen K, et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96(3):544-551. doi: 10.3945/ajcn.112.037382.
50. Drago L, Toscano M, De Grandi R, et al. Microbiota network and mathematic microbe mutualism in colostrum and mature milk collected in two different geographic areas: Italy versus Burundi. ISME J. 2017;11(4):875-884. doi: 10.1038/ismej.2016.183.
51. Martin R, Langa S, Reviriego C, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr. 2003;143(6):754-758. doi: 10.1016/j.jpeds.2003.09.028.
52. Cabrera-Rubio R, Collado MC, Laitinen K, et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96:544-551. doi: 10.3945/ajcn.112.037382
53. Zhou X, Voigt A, Paveglio S, et al. Similar bacterial signatures in intestinal tissues, milk, and dendritic cells of lactating mice suggest a possible entero-mammary pathway. Gastroenterology. 2017;152(5):S172. doi: 10.1016/s0016-5085(17)30893-4.
54. Soto A, Martin V, Jimenez E, et al. Lactobacilli and bifidobacteria in human breastmilk: Influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr. 2014;59(1):78-88. doi: 10.1097/MPG.0000000000000347.
55. Kumar H, du Toit E, Kulkarni A, et al. Distinct patterns in human milk microbiota and fatty acid profiles across specific geographic locations. Front Microbiol. 2016;7:1619. doi: 10.3389/fmicb.2016.01619.
56. Gronlund MM, Gueimonde M, Laitinen K, et al. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the bifidobacterium microbiota in infants at risk of allergic disease. Clin Exp Allergy. 2007;37:1764-1772. doi: 10.1111/j.1365-2222.2007.02849.x.
57. Solis G, de los Reyes-Gavilan CG, Fernandez N, et al. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe. 2010;16(3):307-310. doi: 10.1016/j.anaerobe.2010.02.004.
58. Perez-Cano FJ, Dong H, Yaqoob P. In vitro immunomodulatory activity of lactobacillus fermentum cect5716 and lactobacillus salivarius cect5713: two probiotic strains isolated from human breast milk. Immunobiology. 2010;215(12):996-1004. doi: 10.1016/j.imbio.2010.01.004.
59. Lara-Villoslada F, Olivares M, Sierra S, et al. Beneficial effects of probiotic bacteria isolated from breast milk. Br J Nutr. 2007;98(1):S96-S100. doi: 10.1017/S0007114507832910.
60. Kirjavainen PV, Apostolou E, Arvola T, et al. Characterizing the composition of intestinal microflora as a prospective treatment target in infant allergic disease. FEMS Immunol Med Microbiol. 2001;32(1):1-7. doi: 10.1111/j.1574-695X.2001.tb00526.x.
61. Belyaeva IA, Mitish MD, Katosova LK. Effektivnost' ispol'zovaniya probiotikov u nedonoshennykh detei. Russkii meditsinskii zhurnal. 2009;17(15):1000-1004. (In Russ).
62. Madonini ER. Probiotics and allergies: myth or reality? Eur Ann Allergy Clin Immunol. 2014;46(6):196-200.
63. Wang HT, Anvari S, Anagnostou K. The role of probiotics in preventing allergic disease. Children (Basel). 2019;6(2):24. doi: 10.3390/children6020024.
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For citations:
Belyaeva I.A., Bombardirova E.P., Namazova-Baranova L.S., Vishneva E.A., Sadchikov P.E. Gut microbiota dysontogeniya in infants as a factor in the development of atopy. Pediatric pharmacology. 2019;16(2):91-96. (In Russ.) https://doi.org/10.15690/pf.v16i2.2005
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