New ideas about the maternal gut microbiome as a source of fetal programming

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

New genetic technologies that have emerged and been introduced into practice over the past 20 years, including 16s rRNA sequencing, have significantly expanded our understanding of the microbial composition of the human body. The gut is one of the most densely populated microbial niches in the human body. Numerous studies have shown the relationship of the gut microbiome with various non-communicable diseases, including diabetes mellitus, obesity, allergies and even mental disorders. The perinatal period, as one of the most hormonally dependent ones in human ontogenesis, has a direct impact on the composition of the intestinal microbiota, just as the microbiota itself can be a precursor and etiological cause of pregnancy complications.

In this regard, the aim of this review article was to systematize data on the gut microbiota of the maternal body in normal and pathological pregnancy, as well as to analyze data on the interaction of the maternal gut microbiome with the fetal immune system.

The review presents data on changes in the maternal intestinal microbiome in normal pregnancy, during infertility, as well as in pregnancy complicated with obesity, gestational diabetes mellitus and preeclampsia. The review also shows how the maternal microbiome is able to “educate” the fetal immune system in utero, thereby preparing the child, who develops in a sterile womb, for extrauterine life surrounded by a large number of various microorganisms. These mechanisms include the direct effect of not only the microorganisms themselves, but also, even largely, their metabolites — primarily short-chain fatty acids.

All these presented data allow for concluding that the maternal microbiome is essentially a separate regulatory homeostatic system, along with the immune, endocrine and cardiovascular systems, which may determine the development of certain complications of pregnancy and shape the health of the unborn child. Interventions in the composition of the maternal gut microbiota may be a way to modulate the course of pregnancy and prevent major obstetric syndromes.

Full Text

Restricted Access

About the authors

Viktoria V. Barinova

Clinic of Professor Bushtyreva

Author for correspondence.
Email: victoria-barinova@yandex.ru
ORCID iD: 0000-0002-8584-7096
SPIN-code: 5068-0680
Scopus Author ID: 57216425249
ResearcherId: AAH-3314-2019

MD, Cand. Sci. (Med.)

Russian Federation, 58/7 Soborny Lane, Rostov-on-Don, 344010

Dmitry O. Ivanov

Saint Petersburg State Pediatric Medical University

Email: doivanov@yandex.ru
ORCID iD: 0000-0002-0060-4168
SPIN-code: 4437-9626

MD, Dr. Sci. (Med.), Professor

Russian Federation, Saint Petersburg

Irina O. Bushtyreva

Clinic of Professor Bushtyreva

Email: kio4@mail.ru
ORCID iD: 0000-0001-9296-2271
SPIN-code: 5009-1565

MD, Dr. Sci. (Med.), Professor

Russian Federation, 58/7 Soborny Lane, Rostov-on-Don, 344010

Tatiana L. Botasheva

Rostov State Medical University

Email: t_botasheva@mail.ru
SPIN-code: 3341-2928
Scopus Author ID: 55531205100
ResearcherId: HKE-0537-2023

MD, Dr. Sci. (Med.), Professor

Russian Federation, Rostov-on-Don

Ekaterina E. Artouz

Rostov State Medical University

Email: artouz-ekaterina@rambler.ru
ORCID iD: 0009-0000-1516-7362

студентка 6 курса лечебно-профилактического факультета

Russian Federation, Rostov-on-Don

References

  1. Burge MN, editor. Fungi in biological control systems. Manchester: Manchester University Press; 1988.
  2. Foster JA, Lyte M, Meyer E, et al. Gut microbiota and brain function: an evolving field in neuroscience. Int J Neuropsychopharmacol. 2016;19(5). doi: 10.1093/ijnp/pyv114
  3. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375(24):2369–2379. doi: 10.1056/NEJMra1600266
  4. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268–1273. doi: 10.1126/science.1223490
  5. Thaiss CA, Zmora N, Levy M, et al. The microbiome and innate immunity. Nature. 2016:535(7610);65–74. doi: 10.1038/nature18847
  6. Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535(7610):75–84. doi: 10.1038/nature18848
  7. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558(Pt 1):263–275. doi: 10.1113/jphysiol.2004.063388
  8. Diaz Heijtz R, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA. 2011;108(7):3047–3052. doi: 10.1073/pnas.1010529108
  9. Neufeld KA, Kang N, Bienenstock J, et al. Effects of intestinal microbiota on anxiety-like behavior. Commun Integr Biol. 2011;4(4):492–494. doi: 10.4161/cib.4.4.15702
  10. Nuriel-Ohayon M, Neuman H, Ziv O, et al. Progesterone increases bifidobacterium relative abundance during late pregnancy. Cell Rep. 2019;27(3):730–736.e3. doi: 10.1016/j.celrep.2019.03.075
  11. Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470–480. doi: 10.1016/j.cell.2012.07.008
  12. Li Y, Toothaker JM, Ben-Simon S, et al. In utero human intestine harbors unique metabolome, including bacterial metabolites. JCI Insight. 2020;5(21). doi: 10.1172/jci.insight.138751
  13. Gomez de Agüero M, Ganal-Vonarburg SC, Fuhrer T, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351(6279):1296–1302. doi: 10.1126/science.aad2571
  14. Vuillermin PJ, O’Hely M, Collier F, et al. Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring. Nat Commun. 2020;11(1):1452. doi: 10.1038/s41467-020-14552-1
  15. Goldberg MR, Mor H, Magid Neriya D, et al. Microbial signature in IgE-mediated food allergies. Genome Med. 2020;12(1):92. doi: 10.1186/s13073-020-00789-4
  16. Komiya S, Naito Y, Okada H, et al. Characterizing the gut microbiota in females with infertility and preliminary results of a water-soluble dietary fiber intervention study. J Clin Biochem Nutr. 2020;67(1):105–111. doi: 10.3164/jcbn.20-53
  17. Silva MSB, Giacobini P. Don’t trust your gut: when gut microbiota disrupt fertility. Cell Metab. 2019;30(4):616–618. doi: 10.1016/j.cmet.2019.09.005
  18. Collado MC, Isolauri E, Laitinen K, et al. Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am J Clin Nutr. 2010;92(5):1023–1030. doi: 10.3945/ajcn.2010.29877
  19. Santacruz A, Collado MC, García-Valdés L, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010;104(1):83–92. doi: 10.1017/S0007114510000176
  20. Collado MC, Isolauri E, Laitinen K, et al. Distinct composition of gut icrobiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008;88(4):894–899. doi: 10.1093/ajcn/88.4.894
  21. Penders J, Thijs C, Vink C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–521. doi: 10.1542/peds.2005-2824
  22. Stanislawski MA, Dabelea D, Wagner BD, et al. Gut Microbiota in the first 2 years of life and the association with body mass index at age 12 in a norwegian birth cohort. mBio. 2018;9(5). doi: 10.1128/mBio.01751-18
  23. Zacarías MF, Collado MC, Gómez-Gallego C, et al. Pregestational overweight and obesity are associated with differences in gut microbiota composition and systemic inflammation in the third trimester. PLoS One. 2018;13(7). doi: 10.1371/journal.pone.0200305
  24. Mokkala K, Houttu N, Vahlberg T, et al. Gut microbiota aberrations precede diagnosis of gestational diabetes mellitus. Acta Diabetol. 2017;54(12):1147–1149. doi: 10.1007/s00592-017-1056-0
  25. Hasain Z, Mokhtar NM, Kamaruddin NA, et al. Gut microbiota and gestational diabetes mellitus: a review of host-gut microbiota interactions and their therapeutic potential. Front Cell Infect Microbiol. 2020;10:188. doi: 10.3389/fcimb.2020.00188
  26. Crusell MKW, Hansen TH, Nielsen T, et al. Gestational diabetes is associated with change in the gut microbiota composition in third trimester of pregnancy and postpartum. Microbiome. 2018;6(1):89. doi: 10.1186/s40168-018-0472-x
  27. Fugmann M, Breier M, Rottenkolber M, et al. The stool microbiota of insulin resistant women with recent gestational diabetes, a high risk group for type 2 diabetes. Sci Rep. 2015;5. doi: 10.1038/srep13212
  28. Hasan S, Aho V, Pereira P, et al. Gut microbiome in gestational diabetes: a cross-sectional study of mothers and offspring 5 years postpartum. Acta Obstet Gynecol Scand. 2018;97(1):38–46. doi: 10.1111/aogs.13252
  29. Wang J, Zheng J, Shi W, et al. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut. 2018;67(9):1614–1625. doi: 10.1136/gutjnl-2018-315988
  30. Liu J, Yang H, Yin Z, et al. Remodeling of the gut microbiota and structural shifts in Preeclampsia patients in South China. Eur J Clin Microbiol Infect Dis. 2017;36(4):713–719. doi: 10.1007/s10096-016-2853-z
  31. Chen X, Li P, Liu M, et al. Gut dysbiosis induces the development of pre-eclampsia through bacterial translocation. Gut. 2020;69(3):513–522. doi: 10.1136/gutjnl-2019-319101
  32. Wu Z, Ge M, Liu J, et al. The gut microbiota composition and metabolites are different in women with hypertensive disorders of pregnancy and normotension: a pilot study. J Obstet Gynaecol Res. 2024;50(3):334–341. doi: 10.1111/jog.15844
  33. Mishra A, Lai GC, Yao LJ, et al. Microbial exposure during early human development primes fetal immune cells. Cell. 2021;184(13):3394–3409.e20. doi: 10.1016/j.cell.2021.04.039
  34. McGovern N, Shin A, Low G, et al. Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature. 2017;546(7660):662–666. doi: 10.1038/nature22795
  35. Rackaityte E, Halkias J, Fukui EM, et al. Viable bacterial colonization is highly limited in the human intestine in utero. Nat Med. 2020;26(4):599–607. doi: 10.1038/s41591-020-0761-3
  36. Lewis RM, Baskaran H, Green J, et al. 3D visualization of trans-syncytial nanopores provides a pathway for paracellular diffusion across the human placental syncytiotrophoblast. iScience. 2022;25(12). doi: 10.1016/j.isci.2022.105453
  37. Alsharairi NA, Li L. Gut microbiota, inflammation, and probiotic supplementation in fetal growth restriction-a comprehensive review of human and animal studies. Life. 2023;13(12):2239. doi: 10.3390/life13122239
  38. Song X, Sun X, Oh SF, et al. Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis. Nature. 2020;577(7790):410–415. doi: 10.1038/s41586-019-1865-0
  39. De Angelis M, Montemurno E, Piccolo M, et al. Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS One. 2014;9(6). doi: 10.1371/journal.pone.0099006
  40. Di Pierro F, Sinatra F, Cester M, et al. Effect of L. crispatus M247 administration on pregnancy outcomes in women undergoing IVF: a controlled, retrospective, observational, and open-label study. Microorganisms. 2023;11(11):2796. doi: 10.3390/microorganisms11112796
  41. Xie Q, Cui D, Zhu Q, et al. Supplementing maternal diet with milk oligosaccharides and probiotics helps develop the immune system and intestinal flora of offsprings. Food Sci Nutr. 202311(11):6868–6877. doi: 10.1002/fsn3.3579
  42. Nachum Z, Perlitz Y, Shavit LY, et al. The effect of oral probiotics on glycemic control of women with gestational diabetes mellitus-a multicenter, randomized, double-blind, placebo-controlled trial. Am J Obstet Gynecol MFM. 2024;6(1). doi: 10.1016/j.ajogmf.2023.101224
  43. Barinova VV, Bushtyreva IO, Kuznetsova NB, et al. Experience of using vaginal autoprobiotics in a patient with spontaneous triplet pregnancy with recurrent vaginal anaerobic dysbiosis. Obstetrics and Gynecology. 2023;(10):184–192. EDN: AFYTWF doi: 10.18565/aig.2023.6

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Figure. Changes in the intestinal microbiota in normal and pathological pregnancy

Download (287KB)

Copyright (c) 2024 Eсо-Vector



СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 66759 от 08.08.2016 г. 
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия Эл № 77 - 6389
от 15.07.2002 г.



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies