New ideas about the maternal gut microbiome as a source of fetal programming
- Authors: Barinova V.V.1, Ivanov D.O.2, Bushtyreva I.O.1, Botasheva T.L.3, Artouz E.E.3
-
Affiliations:
- Clinic of Professor Bushtyreva
- Saint Petersburg State Pediatric Medical University
- Rostov State Medical University
- Issue: Vol 73, No 2 (2024)
- Pages: 109-118
- Section: Reviews
- URL: https://journals.rcsi.science/jowd/article/view/259258
- DOI: https://doi.org/10.17816/JOWD625424
- ID: 259258
Cite item
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
##article.viewOnOriginalSite##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, 344010Dmitry 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 PetersburgIrina 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, 344010Tatiana 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-DonEkaterina 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-DonReferences
- Burge MN, editor. Fungi in biological control systems. Manchester: Manchester University Press; 1988.
- 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
- 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
- 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
- Thaiss CA, Zmora N, Levy M, et al. The microbiome and innate immunity. Nature. 2016:535(7610);65–74. doi: 10.1038/nature18847
- Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535(7610):75–84. doi: 10.1038/nature18848
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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