The role of the intestinal microbiome in the development of allergies in children

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Abstract

To date, a clear correlation has been revealed between disorders of the intestinal microbiota in childhood and immune and metabolic disorders in the later period. Experimental data, confirming the long-term health benefits caused by the intestinal microbiota of infants, indicate the participation of the intestinal microbiota of children in modulating risk factors associated with a specific state of adult health, which justifies the expediency of developing strategies for influencing the development, composition and activity of the intestinal microbiome of infants using probiotics and/or prebiotics, synbiotics and postbiotics.

The composition of the intestinal microbiome of a child depends on its gestational age, method of delivery, type of feeding, environmental conditions and plays a vital role throughout a person’s life.

The intrauterine and neonatal periods represent critical stages in the formation of the child’s microbiome, the violation of which is associated with the development of various pathological conditions in the child’s body, including allergic ones, while early correction of intestinal microbial communities can serve as a basis for preventing allergic sensitization.

The review article presents an analysis of current data on the role of the intestinal microbiota in the development of atopic diseases in children and discusses the possibilities of preventive and therapeutic use of nutraceuticals with pro-, pre- and postbiotic effects, their effects on the development, composition and activity of the intestinal microbiome in children with atopias.

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About the authors

Natalia V. Kolesnikova

Kuban State Medical University

Author for correspondence.
Email: nvk24071954@mail.ru
ORCID iD: 0000-0002-9773-3408
SPIN-code: 9685-7584

Dr. Sci. (Biol.), Professor

Russian Federation, Krasnodar

Evgeniy A. Kokov

Kuban State Medical University

Email: Kokovea@gmail.ru
ORCID iD: 0000-0001-5239-0846
SPIN-code: 3476-5062

MD, Cand. Sci. (Med.), Assistant Professor

Russian Federation, Krasnodar

Ludmila N. Kokova

Kuban State Medical University

Email: kokovaln@gmail.com
ORCID iD: 0000-0001-8995-5572
SPIN-code: 1415-3290

MD, Cand. Sci. (Med.), Assistant Professor

Russian Federation, Krasnodar

Ella V. Churyukina

Kuban State Medical University; Rostov State Medical University

Email: echuryukina@mail.ru
ORCID iD: 0000-0001-6407-6117
SPIN-code: 8220-1439

MD, Cand. Sci. (Med.), Assistant Professor

Russian Federation, Krasnodar; Rostov on Don

References

  1. Smirnova GI, Mankute GR. Intestinal microbiota and atopic dermatitis in children. Russ Pediatric J. 2015;18(6):46–53. (In Russ).
  2. Maksimova OV, Gervazieva VB, Zverev VV. Gut microbiota and allergic diseases. J Microbiol Epidemiol Immunobiol. 2014;(3):49–60. (In Russ).
  3. Sanchez-Borges M, Martin BL, Muraro AM, et al. The importance of allergic diseases for public health: iCAALL statement. World Allergy Authority J. 2018;11(1):8. doi: 10.1186/s40413-018-0187-2
  4. Ferreira MA, Wong JM, Baurecht H, et al. Eleven loci with new reproducible genetic associations with the risk of allergic diseases. J Allergy Wedge Immunal. 2019;143(2):691–699. doi: 10.1016/j.jaci.2018.03.012
  5. Bernard A, Nickmiller M, Dumont H. Respiratory tract epithelial defects and risks of allergic diseases: Multiple associations identified in the study of biomarkers among adolescents. Am J Respir Crit Care Med. 2015;191(6):714–717. doi: 10.1164/ rcm.201409-1748LE
  6. Han P, Gu JQ, Li LS, et al. The association between intestinal bacteria and allergic diseases-cause or consequence? Front Call Infect Microbiol. 2021;(11):650893. doi: 10.3389/fcimb.2021.650893
  7. Van Niemwegen FA, Penders J, Stobbering EE, et al. Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J Allergy Clin Immunol. 2011;128(5):948–955. doi: 10.1016/j.jaci.2011.07.027
  8. Lozupone KA, Stombaugh А, Gordon JI, et al. Diversity, stability and stability of the human gut microbiota. Nature. 2012;489(7415):220–230. doi: 10.1038/nature11550
  9. Schlaeppi K, Bulgarelli D. The plant microbiome at work. Mol Plant Microbe Interact. 2015;28(3):212–217. doi: 10.1094/MPMI-10-14-0334-FI
  10. Bokulich NA, Chang J, Battaglia T, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82. doi: 10.1126/scitranslmed.aad7121.
  11. Urcell LK, Clemente JK, Radeоut JR, et al. The interpersonal and intrapersonal diversity of human-associated microbiota in key body sites. J Allergy Clin Immunol. 2012;129(5):1204–1208. doi: 10.1016/j.jaci.2012.03.010
  12. Di Costanzo M, Carucci L, Berni C, Biasucci G. Gut microbiome modulation for preventing and treating pediatric food allergies. Int J Mol Sci. 2020;21(15):5275. doi: 10.3390/ijms21155275
  13. Frolova ЕV, Gmoshinsky IV, Lysikov YA, et al. Diagnosis of pediatric allergic enteropathy. Pediatria. Journal named after G.N. Speransky. 2001;80(2):19–22. (In Russ).
  14. Milani C, Duranti S, Bottacini F, et al. The first microbial colonizers of the human gut: Composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol Rev. 2017;81(4): e00036-17. doi: 10.1128/MMBR.00036-17
  15. Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol. 2014;(5):258. doi: 10.3389/fmicb.2014.00258
  16. Younge N, McCann JR, Ballard J, et al. Fetal exposure to the maternal microbiota in humans and mice. JCI Insight. 2019;4(19):e127806. doi: 10.1172/jci.insight.127806
  17. Biasucci G, Rubin M, Riboni S, et al. The method of delivery affects the bacterial community in the intestines of the newborn. Early Hum Dev. 2010;86(Suppl 1):S13–S15. doi: 10.1016/j.earlhumdev.2010.01.004
  18. Bager P, Wohlfahrt J, Westergaard T. Caesarean delivery and the risk of atopy and allergic diseases: Meta-analysis. Clin Exp Allergy. 2008;38(4):634–642. doi: 10.1111/j.1365-2222.2008.02939.x
  19. De Meij TG, Budding AE, de Groot EF, et al. Composition and stability of intestinal microbiota of healthy children within a Dutch population. FASEB J. 2016;30(4):1512–1522. doi: 10.1096/fj.15-278622
  20. Hill CJ, Lynch DB, Murphy K, et al. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome. 2017;5(1):4. doi: 10.1186/s40168-016-0213-y
  21. Kong X, Xu W, Anton S, et al. Gut microbiome developmental patterns in early life of preterm infants: Impacts of feeding and gender. PLoS One. 2016;11(4):e0152751. doi: 10.1371/journal.pone.0152751
  22. Collado MC, Cerenada M, Neu J, et al. Factors influencing gastrointestinal tract and microbiota immune interaction in preterm infants. Pediatr Res. 2015;77(6):726–731. doi: 10.1038/ave.2015.54
  23. Ward RE, Ninonuevo M, Mills DA, et al. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl Environ Microbiol. 2006;72(6):4497–4499. doi: 10.1128/AEM.02515-05
  24. Genia S, Turker M, Hazel T, et al. Human milk oligosaccharides inhibit Candida albicans invasion of human premature intestinal epithelial cells. J Nutr. 2015;145(9):1992–1998. doi: 10.3945/jn.115.214940
  25. Avershina E, Lundgard K, Sekelja M, et al. Transition from infant: To adult-like gut microbiota. Environ Microbiol. 2016;18:2226–2236. doi: 10.1111/1462-2920.13248
  26. O’Sullivan A, Farber M, Smilowitz JT. The influence of early infant-feeding practices on the intestinal microbiome and body composition in infants. Nutr Metab Insights. 2015;8(Suppl 1):1–9. doi: 10.4137/NMI.S29530
  27. Wang S, Wei Y, Liu L, Li A. Association between breastmilk microbiota and food allergy in infants. Front Call Infect Microbiol. 2022;11(7):770913. doi: 10.3389/fcimb.2021.770913
  28. Pravdin P, Jordan F, Priami S, Morine MJ. The role of breast-feeding in infant immune system: A systems perspective on the intestinal microbiome. Microbiome. 2015;(3):41. doi: 10.1186/s40168-015-0104-7
  29. Adlerbert I, Strahan DP, Matricardi PM, et al. Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol. 2007;120(2):343–350. doi: 10.1016/j.jaci.2007.05.018
  30. Laursen MF, Zahariassen G, Ball MI, et al. Having older siblings is associated with gut microbiota development during early childhood. IUD Microbiol. 2015;(15):154. doi: 10.1186/s12866-015-0477-6
  31. Bonder MJ, Kurilshchikov A, Tigchelaar EF, et al. The effect of host genetics on the gut microbiome. Nat Genet. 2016;48(11): 1407–1412. doi: 10.1038/ng.3663
  32. Honda K, Takeda K. Regulatory mechanisms of immune responses to intestinal bacteria. Mucosal Immunol. 2009;2(3): 187–196. doi: 10.1038/mi.2009.8
  33. Nikolaeva IV, Caregorodcev D, Shajhieva GS. The formation of the intestinal microbiota of the child and the factors influencing this process. Russ Bulletin Perinatol Pediatrics. 2018;63:(3):13–18. (In Russ). doi: 10.21508/1027-4065-2018-63-3-13-18
  34. Rabe H, Lundell AC, Sjoberg F, et al. Neonatal gut colonization by Bifidobacterium is associated with higher childhood cytokine responses. Intestinal Microbes. 2020;12(1):1–14. doi: 10.1080/19490976.2020.1847628
  35. Selma-Royo M, Arroyo CM, Garcia-Mantrana I, et al. Perinatal environment shapes microbiota colonization and infant growth: Impact on host response and intestinal function. Microbiome. 2020;8(1):1–19. doi: 10.1186/s40168-020-00940-8
  36. Makarova SG, Namazova-Baranova LS, Ereshko OA, et al. Intestinal microbiota and allergy. Pro- and prebiotics in the prevention and treatment of allergic diseases. Pediatric Pharmacol. 2019;16(1):7–18. (In Russ).
  37. Johnson SS, Ownby DR. The infant gut bacterial microbiota and risk of pediatric asthma and allergic diseases. Translation Res. 2017;(179):60–70. doi: 10.1016/j.trsl.2016.06.010
  38. Sun L, Liu V, Zhang LJ. The role of toll-like receptors in skin host defense, psoriasis, and atopic dermatitis. J Immunal Res. 2019;2019:1824624. doi: 10.1155/2019/1824624
  39. Jo R, Yama K, Aita Y, et al. Comparison of oral microbiome profiles in 18-month-old infants and their parents. Sci Rep. 2021;11(1):861. doi: 10.1038/s41598-020-78295-1
  40. 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
  41. Ismail IH, Oppedisano F, Joseph SJ, et al. Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants. Pediatr Allergy Immunol. 2012;23(7):674–681. doi: 10.1111/j.1399-3038.2012.01328.x
  42. Azad MB, Kozyrsky AL. Perinatal programming of asthma: The role of the gut microbiota. Klin Def Immunal. 2012;2012:932072. doi: 10.1155/2012/932072
  43. Arrieta MC, Stiemsma LT, Dimitriu PA, 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
  44. Abrahamson TR, Jacobson HE, Anderson AF, et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Alergie La Clin Exp. 2014;44(6):842–850. doi: 10.1111 / cea.12253
  45. Azad MB, Konya T, Gutman DS, et al. Infant gut microbiota and food sensitization: Associations in the first year of life. Clin Exp Allergy. 2015;45(3):632–643. doi: 10.1111/cea.12487
  46. Savage JH, Lee-Sarwar KA, Sordello J, et al. A prospective microbiome-wide association study of food sensitization and food allergy in early childhood. Allergy. 2018;73(1):145–152. doi: 10.1111/all.13232
  47. Netrebenko OK, Kornienko EA. Intestinal microbiota and probiotics during pregnancy. Pediatria. Journal named after G.N. Speransky. 2012;91(6):87–95. (In Russ).
  48. Kurosh A, Luna RA, Balderas M, et al. Fecal microbiome signatures are different in food-allergic children compared to siblings and healthy children. Pediatrician. Allergy Immunal. 2018;29(5): 545–554. doi: 10.1111/pai.12904
  49. Kanoni BR, Sangwan N, Stefka A, et al. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2016;10(3):742–750. doi: 10.1038/ismej.2015.151
  50. Thule UJ, Kumagai H, Jumbo E, et al. Probiotics prevent sensitization to oral antigen and subsequent increase in intestinal tightness. Permeability in juvenile and young adult rats. Microorganisms. 2019;7(10):463. doi: 10.3390/microorganisms 7100463
  51. Hardy H, Harris J, Lyon E, et al. Probiotics, prebiotics and immunomodulation of gut mucosal defences: Homeostasis and immunopathology. Nutrients. 2013;5(6):1869–1912. doi: 10.3390/nu5061869
  52. Torii A, Tori S, Fujiwara S, et al. Lactobacillus Acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol Int. 2007;56(3):293–301. doi: 10.2332/allergolint.O-06-459
  53. Gibson GR, Atkins R, Sanders ME, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nats Reverend Gastroenterologist Hepatol. 2017;14(8):491–502. doi: 10.1038/nrgastro.2017.75
  54. Kuytunen M. Probiotics and prebiotics in preventing food allergy and eczema. Curr Opin Allergy Clin Immunol. 2013;13(3):280–286. doi: 10.1097/ACI.0b013e328360ed66
  55. Markovyak P, Slizevska K. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients. 2017;9(9):1021. doi: 10.3390/nu9091021
  56. Candy DE, Van Ampting MT, Oude Nijhuis MM, et al. A synbiotic-containing amino-acid-based formula improves gut microbiota in non-IgE-mediated allergic infants. Pediatrician Res. 2018;83(3): 677–686. doi: 10.1038/ave.2017.270
  57. Fiocchi A, Pawankar R, Cuello-Garcia C, et al. World allergy organization-mcmaster university guidelines for allergic disease prevention (GLAD-P): Probiotics. World Allergy Authority J. 2015; 8(1):4. doi: 10.1186/s40413-015-0055-2
  58. Esposito S, Patria MF, Spena S, et al. Impact of genetic polymorphisms on paediatric atopic dermatitis. Int J Immunopathol Pharmacol. 2015;28(3):286–295. doi: 10.1177/0394632015591997
  59. Hamayuni RA, Maleki AL, Kafel SH, Abbasi A. Postbiotics: A novel strategy in food allergy treatment. Crit Rev Food Sci Nutr. 2021;61(3):492–499. doi: 10.1080/10408398.2020.1738333
  60. Guryanova SV, Borisova OU, Kolesnikova NV, et al. The effect of muramylpeptide on the microbial composition of the oral microflora. Immunology. 2019;40(6):34–40. (In Russ).
  61. Kokov EА, Kolesnikova NV, Klokova LN, Andronova TM. Clinical efficacy of immunotherapy in the treatment of atopic dermatitis in children. Russ Med J. 2019;(3):11–14. (In Russ).
  62. Kolesnikova NV, Kozlov IG, Guryanova SV, et al. Clinical and immunological efficacy and prospects of using muramyldipeptides in the treatment of atopic diseases. Med Immunol. 2016;18(1):15–20. (In Russ).

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2. Fig. 1. Prenatal, neonatal and postnatal factors of modulation of the intestinal microbiome in children [14].

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