The role of the microbiome in pregnancy

Česká verzia

Authors: Hornová M.; Pařízek A.; Koucký M.
Authors place of work: Gynekologicko-porodnická klinika 1. LF UK a VFN v Praze
Published in the journal: Ceska Gynekol 2021; 86(6): 422-427
Category: Review Article
doi: https://doi.org/10.48095/cccg2021422

Summary

Objective: To provide a comprehensive overview of the available information on the maternal microbiome and its effect on pregnancy and preterm birth. Methods: Systematic review of available literature on the topic was done using the PubMed database. Conclusion: Etiology of preterm labor is multifactorial. Individual setting of humoral and cellular immune response is key; however, lately the focus has shifted to the role of the microbiome, especially the vaginal one. The role of additional microbiomes and the relationship between different compartments are the focus of intensive research. Mainly the differences in the maternal and neonatal microbiome depend on the method of delivery and administration of different antibiotics during pregnancy and labor. The uterine cavity is no longer thought to be without colonization and the formation of the fetal microbiome begins early in pregnancy.

Keywords:

Preterm labor – microbiome – antibiotics – microbial invasion of amniotic cavity – vaginal seeding

Zdroje

1. Gensollen T, Iyer SS, Kasper DL et al. How colonization by microbiota in early life shapes the immune system. Science 2016; 352 (6285): 539–544. doi: 10.1126/science.aad9378.

2. Kacerovský M, Kokrdová Z, Koucký M et al. Spontánní předčasný porod, doporučený postup České gynekologické a porodnické společnosti (ČGPS) a České lékařské společnosti Jana Evangelisty Purkyně (ČLS JEP). 2021 [online]. Dostupné z: http: //www.gynultrazvuk.cz/doporucene-postupy.

3. Koucký M, Malíčková K, Hrdý J et al. The role of maternal imunity and woman’s microbiome in the pathogenesis of preterm labor. Ceska Gynekol 2017; 82 (5): 407–410.

4. Gomez-Lopez N, StLouis D, Lehr MA et al. Immune cells in term and preterm labor. Cell Mol Immunol 2014; 11 (6): 571–581. doi: 10.1038/cmi.2014.46.

5. Tong M, Abrahams VM. Immunology of the placenta. Obstet Gynecol Clin North Am 2020; 47 (1): 49–63. doi: 10.1016/j.ogc.2019.10.006.

6. Regal JF, Gilbert JS, Burwick RM. The complement system and adverse pregnancy outcomes. Mol Immunol 2015; 67 (1): 56–70. doi: 10.1016/j.molimm.2015.02.030.

7. Green ES, Arck PC. Pathogenesis of preterm birth: bidirectional inflammation in mother and fetus. Semin Immunopathol 2020; 42 (4): 413–429. doi: 10.1007/s00281-020-00807-y.

8. Prince AL, Chu DM, Seferovic MD et al. The perinatal microbiome and pregnancy: moving beyond the vaginal microbiome. Cold Spring Harb Perspect Med 2015; 5 (6): a023051. doi: 10.1101/cshperspect.a023051.

9. Devaraj S, Hemarajata P, Versalovic J. The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 2013; 59 (4): 617–628. doi: 10.1373/clinchem.2012.187617.

10. Wang T, Cai G, Qiu Y et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 2012; 6 (2): 320–329. doi: 10.1038/ismej.2011.109.

11. Qin J, Li Y, Cai Z et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490 (7418): 55–60. doi: 10.1038/nature11450.

12. Prince AL, Ma J, Kannan PS et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am J Obstet Gynecol 2016; 214 (5): 627.e1–627.e16. doi: 10.1016/j.ajog.2016.01.193.

13. Tétu A, Guerby P, Rallu F et al. Mid-trimester microbial invasion of the amniotic cavity and the risk of preterm birth. J Matern Fetal Neonatal Med 2020: 1–4. doi: 10.1080/14767058.2020.1846704.

14. Rowlands S, Danielewski JA, Tabrizi SN et al. Microbial invasion of the amniotic cavity in mid- trimester pregnancies using molecular microbiology. Am J Obstet Gynecol 2017; 217 (1): 71.e1–71.e5. doi: 10.1016/j.ajog.2017.02.051.

15. Crha I, Ventruba P, Žáková J et al. Děložní mikrobiom jako faktor receptivity endometria. Ceska Gynekol 2019; 84 (1): 49–54.

16. Eisenhofer R, Minich JJ, Marotz C et al. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol 2019; 27 (2): 105–117. doi: 10.1016/j.tim.2018.11.003.

17. Bardos J, Fiorentino D, Longman RE et al. Immunological role of the maternal uterine microbiome in pregnancy: pregnancies pathologies and alterated microbiota. Front Immunol 2020; 10: 2823. doi: 10.3389/fimmu.2019.02823.

18. Baker JM, Chase DM, Herbst-Kralovetz MM. Uterine microbiota: residents, tourists, or invaders? Front Immunol 2018; 9: 208. doi: 10.3389/ fimmu.2018.00208.

19. Theis KR, Romero R, Winters AD et al. Does the human placenta delivered at term have a microbiota? Results of cultivation, quantitative real-time PCR, 16S rRNA gene sequencing, and metagenomics. Am J Obstet Gynecol 2019; 220 (3): 267.e1–267.e39. doi: 10.1016/j.ajog.2018.10.018.

20. Zhu L, Luo F, Hu W et al. Bacterial communities in the womb during healthy pregnancy. Front Microbiol 2018; 9: 2163. doi: 10.3389/fmicb.2018.02163.

21. Leiby JS, McCormick K, Sherrill-Mix S et al. Lack of detection of a human placenta microbiome in samples from preterm and term deliveries. Microbiome 2018; 6 (1): 196. doi: 10.1186/s40168-018-0575-4.

22. Ravel J, Gajer P, Abdo Z et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011; 108 (Suppl 1): 4680–4687. doi: 10.1073/pnas.1002611107.

23. Witkin SS. The vaginal microbiome, vaginal anti-microbial defence mechanisms and the clinical challenge of reducing infection-related preterm birth. BJOG 2015; 122 (2): 213–218. doi: 10.1111/1471-0528.13115.

24. Vinturache AE, Gyamfi-Bannerman C, Hwang J et al. Preterm Birth International Collaborative (PREBIC). Maternal microbiome – a pathway to preterm birth. Semin Fetal Neonatal Med 2016; 21 (2): 94–99. doi: 10.1016/j.siny.2016.02.004.

25. Mendling W. Vaginal microbiota. Adv Exp Med Biol 2016; 902: 83–93. doi: 10.1007/ 978-3-319-31248-4_6.

26. Brown RG, Al-Memar M, Marchesi JR et al. Establishment of vaginal microbiota composition in early pregnancy and its association with subsequent preterm prelabor rupture of the fetal membranes. Transl Res 2019; 207: 30–43. doi: 10.1016/j.trsl.2018.12.005.

27. Tabatabaei N, Eren AM, Barreiro LB et al. Vaginal microbiome in early pregnancy and subsequent risk of spontaneous preterm birth: a case-control study. BJOG 2019; 126 (3): 349–358. doi: 10.1111/1471-0528.15299.

28. Hyman RW, Fukushima M, Jiang H et al. Diversity of the vaginal microbiome correlates with preterm birth. Reprod Sci 2014; 21 (1): 32–40. doi: 10.1177/1933719113488838.

29. Stout MJ, Zhou Y, Wylie KM et al. Early pregnancy vaginal microbiome trends and preterm birth. Am J Obstet Gynecol 2017; 217 (3): 356.e1–356.e18. doi: 10.1016/j.ajog.2017.05.030.

30. Mls J, Stráník J, Kacerovský M. Lactobacillus iners-dominantní vaginální mikrobiota v těhotenství. Ceska Gynekol 2019; 84 (6): 463–467.

31. Kindinger LM, Bennett PR, Lee YS et al. The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome 2017; 5 (1): 6. doi: 10.1186/s40168-016-0223-9.

32. Elovitz MA, Gajer P, Riis V et al. Cervicovaginal microbiota and local immune response modulate the risk of spontaneous preterm delivery. Nat Commun 2019; 10 (1): 1305. doi: 10.1038/s41467-019-09285-9.

33. Mor G, Kwon JY. Trophoblast – microbiome interaction: a new paradigm on immune regulation. Am J Obstet Gynecol 2015; 213 (Suppl 4): S131–S137. doi: 10.1016/j.ajog.2015.06.039.

34. Záhumenský J, Hederlingová J, Pšenková P. Význam materského mikrobiómu v tehotnosti. Ceska gynekol 2017; 82 (3): 211–217.

35. Power ML, Quaglieri C, Schulkin J. Reproductive microbiomes: a new thread in the microbial network. Reprod Sci 2017; 24 (11): 1482–1492. doi: 10.1177/1933719117698577.

36. Chu DM, Seferovic M, Pace RM et al. The microbiome in preterm birth. Best Pract Res Clin Obstet Gynaecol 2018; 52: 103–113. doi: 10.1016/j.bpobgyn.2018.03.006.

37. Cobb CM, Kelly PJ, Williams KB et al. The oral microbiome and adverse pregnancy outcomes. Int J Womens Health 2017; 9: 551–559. doi: 10.2147/IJWH.S142730.

38. Connor KL, Chehoud C, Chan L et al. Reproductive Sciences. Maternal diet shapes the gut microbiome, impacting immune status in pregnancy. Vol. 21. USA, CA: Thousand Oaks 2014.

39. Atarashi K, Tanoue T, Shima T et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331 (6015): 337–341. doi: 10.1126/science.1198469.

40. Atarashi K, Tanoue T, Oshima K et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500 (7461): 232–236. doi: 10.1038/nature12331.

41. Lee N, Kim WU. Microbiota in T-cell homeostasis and inflammatory diseases. Exp Mol Med 2017; 49 (5): e340. doi: 10.1038/emm.2017.36.

42. Reyman M, van Houten MA, van Baarle D et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun 2019; 10 (1): 4997. doi: 10.1038/s41467-019-13014-7.

43. Dierikx TH, Visser DH, Benninga MA et al. The influence of prenatal and intrapartum antibiotics on intestinal microbiota colonisation in infants: a systematic review. J Infect 2020; 81 (2): 190–204. doi: 10.1016/j.jinf.2020.05.002.

44. Zimmermann P, Curtis N. Effect of intrapartum antibiotics on the intestinal microbiota of infants: a systematic review. Arch Dis Child Fetal Neonatal Ed 2020; 105 (2): 201–208. doi: 10.1136/archdischild-2018-316659.

45. Marrs T, Jo JH, Perkin MR et al. Gut microbiota development during infancy: impact of introducing allergenic foods. J Allergy Clin Immunol 2021; 147 (2): 613.e9–621.e9. doi: 10.1016/j.jaci.2020.09.042.

46. Galazzo G, van Best N, Bervoets L 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.

47. Zheng H, Liang H, Wang Y et al. Altered gut microbiota composition associated with Eczema in infants. PLoS One 2016; 11 (11): e0166026. doi: 10.1371/journal.pone.0166026.

48. Sordillo JE, Zhou Y, McGeachie MJ et al. Factors influencing the infant gut microbiome at age 3–6 months: findings from the ethnically diverse Vitamin D Antenatal Asthma Reduction Trial (VDAART). J Allergy Clin Immunol 2017; 139 (2): 482.e14–491.e14. doi: 10.1016/j.jaci.2016.08.045.

49. Gholizadeh P, Mahallei M, Pormohammad A et al. Microbial balance in the intestinal microbiota and its association with diabetes, obesity and allergic disease. Microb Pathog 2019; 127: 48–55. doi: 10.1016/j.micpath.2018.11.031.

50. Soderborg TK, Clark SE, Mulligan CE et al. The gut microbiota in infants of obese mothers increases inflammation and susceptibility to NAFLD. Nat Commun 2018; 9 (1): 4462. doi: 10.1038/s41467-018-06929-0.

51. Štefan M, Vojtěch J. Antibiotická terapie v graviditě. Ceska Gynekol 2018; 83 (1): 70–80.

52. Chu DM, Ma J, Prince AL et al. 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.

53. Aagaard KM. Mode of delivery and pondering potential sources of the neonatal microbiome. EBioMedicine 2020; 51: 102554. doi: 10.1016/j.ebiom.2019.11.015.

54. Limaye MA, Ratner AJ. ‚Vaginal seeding‘ after a caesarean section provides benefits to newborn children: AGAINST: Vaginal microbiome transfer – a medical procedure with clear risks and uncertain benefits. BJOG 2020; 127 (2): 302. doi: 10.1111/1471-0528.15977.

55. Cunnington AJ, Sim K, Deierl A et al. „Vaginal seeding“ of infants born by caesarean section. BMJ 2016; 352: i227. doi: 10.1136/bmj. i227.

56. Eschenbach DA. Vaginal seeding: more questions than answers. BJOG 2018; 125 (5): 537. doi: 10.1111/1471-0528.14815.