Vaginal microbiota stability as a marker of successful outcomes of pregnancy

Cover Page


Cite item

Full Text

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

Abstract

Overcoming the problem of miscarriage still remains relevant today. Its' significant contribution to the structure of premature birth is due to the invasion of conditionally pathogenic microflora from the lower parts of the genital tract into the amniotic cavity. It can thus trigger an inflammatory reaction, causing early termination of pregnancy. The microbiota of the genital tract is characterized by the least diversity and high stability over time compared to any other location of the body. The dominance of certain types of lactobacilli in the vaginal biotope may be a marker of well-being, or a harbinger of termination of pregnancy. The aim of this review article is to summarize the current understanding of the vaginal microbiota during pregnancy in order to determine the relationship between its composition and stability throughout pregnancy, as well as the risk of early termination of pregnancy.

Full Text

Restricted Access

About the authors

Natalia R. Beliaeva

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Author for correspondence.
Email: natascha778@yandex.ru
ORCID iD: 0000-0002-4277-1474
SPIN-code: 4126-3035
Russian Federation, Saint Petersburg

Olga V. Budilovskaya

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: o.budilovskaya@gmail.com
ORCID iD: 0000-0001-7673-6274
Scopus Author ID: 12545757500
ResearcherId: K-1854-2018

MD, Cand. Sci. (Med.)

Russian Federation, Saint Petersburg

Alevtina M. Savicheva

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: savitcheva@mail.ru
ORCID iD: 0000-0003-3870-5930
SPIN-code: 8007-2630
ResearcherId: P-6788-2015

MD, Dr. Sci. (Med.), Professor, Honored Worker of Science of the Russian Federation

Russian Federation, Saint Petersburg

Natalia I. Tapilskaya

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: tapnatalia@yandex.ru
ORCID iD: 0000-0001-5309-0087
Scopus Author ID: 23013489000
ResearcherId: A-7504-2016

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

Russian Federation, Saint Petersburg

Igor Yu. Kogan

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: ikogan@mail.ru
ORCID iD: 0000-0002-7351-6900
SPIN-code: 6572-6450
Scopus Author ID: 56895765600
ResearcherId: P-4357-2017

MD, Dr. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences

Russian Federation, Saint Petersburg

References

  1. Gonçalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8(1):3–13. doi: 10.1002/mrdd.10008
  2. Goldenberg RL, Andrews WW, Hauth JC. Choriodecidual infection and preterm birth. Nutr Rev. 2002;60(5 Pt 2):S19–S25. doi: 10.1301/00296640260130696
  3. Rossiiskoe obshchestvo akusherov-ginekologov, Assotsiatsiya akusherskikh anesteziologov-reanimatologov. Prezhdevremennye rody. Klinicheskie rekomendatsii. (In Russ.) [cited 2023 Feb 12]. Available from: https://roag-portal.ru/recommendations_obstetrics
  4. Romero R, Gómez R, Chaiworapongsa T, et al. The role of infection in preterm labour and delivery. Paediatr Perinat Epidemiol. 2001;15(Suppl 2):41–56. doi: 10.1046/j.1365-3016.2001.00007.x
  5. Steel JH, Malatos S, Kennea N, et al. Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor. Pediatr Res. 2005;57(3):404–411. doi: 10.1203/01.PDR.0000153869.96337.90
  6. Carey JC, Klebanoff MA, Hauth JC, et al. Metronidazole to prevent preterm delivery in pregnant women with asymptomatic bacterial vaginosis. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. N Engl J Med. 2000;342:534–540.
  7. Kenyon SL, Taylor DJ, Tarnow-Mordi W; ORACLE Collaborative Group. Broad-spectrum antibiotics for spontaneous preterm labour: the ORACLE II randomised trial. ORACLE Collaborative Group. Lancet. 2001;357(9261):989–994. doi: 10.1016/s0140-6736(00)04234-3
  8. Flenady V, Hawley G, Stock OM, et al. Prophylactic antibiotics for inhibiting preterm labour with intact membranes. Cochrane Database Syst Rev. 2013;(12). doi: 10.1002/14651858.CD000246.pub2
  9. 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
  10. Shafquat A, Joice R, Simmons SL, et al. Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol. 2014;22(5):261–266. doi: 10.1016/j.tim.2014.01.011
  11. Bäckhed F, Fraser CM, Ringel Y, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12(5):611–622. doi: 10.1016/j.chom.2012.10.012
  12. Eschenbach DA, Thwin SS, Patton DL, et al. Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis. 2000;30(6):901–907. doi: 10.1086/313818
  13. Li K, Bihan M, Methé BA. Analyses of the stability and core taxonomic memberships of the human microbiome. PLoS One. 2013;8(5). doi: 10.1371/journal.pone.0063139
  14. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449(7164):811–818. doi: 10.1038/nature06245
  15. White BA, Creedon DJ, Nelson KE, et al. The vaginal microbiome in health and disease. Trends Endocrinol Metab. 2011;22(10):389–393. doi: 10.1016/j.tem.2011.06.001
  16. Patton DL, Thwin SS, Meier A, et al. Epithelial cell layer thickness and immune cell populations in the normal human vagina at different stages of the menstrual cycle. Am J Obstet Gynecol. 2000;183(4):967–973. doi: 10.1067/mob.2000.108857
  17. Miller L, Patton DL, Meier A, et al. Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol. 2000;96(3):431–439. doi: 10.1016/s0029-7844(00)00906-6
  18. Aldunate M, Tyssen D, Johnson A, et al. Vaginal concentrations of lactic acid potently inactivate HIV. J Antimicrob Chemother. 2013;68(9):2015–2025. doi: 10.1093/jac/dkt156
  19. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. doi: 10.1038/nature11234
  20. Voroshilina ES, Plotko EE, Islamidi DK, et al. Mikrobiotsenoz vlagalishcha s tochki zreniya PTsR v real’nom vremeni. Vozmozhnosti korrektsii disbioticheskikh narushenii vlagalishcha: uchebnoe posobie. Ekaterinburg; 2018. (In Russ.) [cited 2023 Feb 12]. Available from: https://www.g-mc.ru/application/files/6015/3958/3995/mikrobiocenoz_i_ego_korrekciya_2018.pdf
  21. Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4680–4687. doi: 10.1073/pnas.1002611107
  22. De Seta F, Campisciano G, Zanotta N, et al. The vaginal community state types microbiome-immune network as key factor for bacterial vaginosis and aerobic vaginitis. Front Microbiol. 2019;10. doi: 10.3389/fmicb.2019.02451
  23. van de Wijgert JH, Borgdorff H, Verhelst R, et al. The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS One. 2014;9(8). doi: 10.1371/journal.pone.0105998
  24. Witkin SS, Mendes-Soares H, Linhares IM, et al. Influence of vaginal bacteria and D- and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. mBio. 2013;4(4):e00460–e00413. doi: 10.1128/mBio.00460-13
  25. Aroutcheva A, Gariti D, Simon M, et al. Defense factors of vaginal lactobacilli. Am J Obstet Gynecol. 2001;185(2):375–379. doi: 10.1067/mob.2001.115867
  26. Sgibnev AV, Kremleva EA. Vaginal protection by H2O2-producing lactobacilli. Jundishapur J Microbiol. 2015;8(10). doi: 10.5812/jjm.22913
  27. Parolin C, Croatti V, Laghi L, et al. Lactobacillus biofilms influence anti-candida activity. Front Microbiol. 2021;12. doi: 10.3389/fmicb.2021.750368
  28. Donia MS, Cimermancic P, Schulze CJ, et al. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell. 2014;158(6):1402–1414. doi: 10.1016/j.cell.2014.08.032
  29. Ma B, Forney LJ, Ravel J. Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol. 2012;66:371–389. doi: 10.1146/annurev-micro-092611-150157
  30. Gajer P, Brotman RM, Bai G, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 2012;4(132). doi: 10.1126/scitranslmed.3003605
  31. Kim H, Kim T, Kang J, et al. Is Lactobacillus gram-positive? A case study of lactobacillus iners. Microorganisms. 2020;8(7):969. doi: 10.3390/microorganisms8070969
  32. Kwak W, Han YH, Seol D, et al. Complete genome of lactobacillus iners KY using flongle provides insight into the genetic background of optimal adaption to vaginal econiche. Front Microbiol. 2020;11:1048. doi: 10.3389/fmicb.2020.01048
  33. Witkin SS, Linhares IM, Bongiovanni AM, et al. Unique alterations in infection-induced immune activation during pregnancy. BJOG. 2011;118(2):145–153. doi: 10.1111/j.1471-0528.2010.02773.x
  34. Aagaard K, Riehle K, Ma J, et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012;7(6). doi: 10.1371/journal.pone.0036466
  35. Romero R, Hassan SS, Gajer P, et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):4. doi: 10.1186/2049-2618-2-4
  36. Bennett PR, Brown RG, MacIntyre DA. Vaginal microbiome in preterm rupture of membranes. Obstet Gynecol Clin North Am. 2020;47(4):503–521. doi: 10.1016/j.ogc.2020.08.001
  37. Ruhljada NN, Taits AN, Romanova LA, et al. Bacterial vaginosis as a risk factor for preterm birth. Pediatrician (St. Petersburg). 2019;10(4):97–101. doi: 10.17816/PED10497-101
  38. Dadayeva DG, Sosnina AK, Tral TG, et al. Placental inflammatory changes and their association with the vaginal microbiota before delivery. Journal of Obstetrics and Women’s Diseases. 2021;70(1):59–68. (In Russ.) doi: 10.17816/JOWD52962
  39. Ganu RS, Ma J, Aagaard KM. The role of microbial communities in parturition: is there evidence of association with preterm birth and perinatal morbidity and mortality? Am J Perinatol. 2013;30(8):613–624. doi: 10.1055/s-0032-1329693
  40. 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
  41. Petricevic L, Domig KJ, Nierscher FJ, et al. Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci Rep. 2014;4:5136. doi: 10.1038/srep05136
  42. Sinyakova AA, Shipitsyna EV, Budilovskaya OV, et al. Anamnestic and microbiological predictors of miscarriage. Journal of Obstetrics and Women’s Diseases. 2019; 68(2):59–70. (In Russ.) doi: 10.17816/JOWD68259-70
  43. Vaneechoutte M. Lactobacillus iners, the unusual suspect. Res Microbiol. 2017;168(9–10):826–836. doi: 10.1016/j.resmic.2017.09.003
  44. 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
  45. Dunstan PK, Johnson CR. Linking richness, community variability, and invasion resistance with patch size. Ecology. 2006;87(11):2842–2850. doi: 10.1890/0012-9658(2006)87[2842:lrcvai]2.0.co;2
  46. Zhang F, Zhang T, Ma Y, et al. Alteration of vaginal microbiota in patients with unexplained recurrent miscarriage. Exp Ther Med. 2019;17(5):3307–3316. doi: 10.3892/etm.2019.7337
  47. DiGiulio DB, Callahan BJ, McMurdie PJ, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci USA. 2015;112(35):11060–11065. doi: 10.1073/pnas.1502875112
  48. 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
  49. Bohbot JM, Daraï E, Bretelle F, et al. Efficacy and safety of vaginally administered lyophilized Lactobacillus crispatus IP 174178 in the prevention of bacterial vaginosis recurrence. J Gynecol Obstet Hum Reprod. 2018;47(2):81–86. doi: 10.1016/j.jogoh.2017.11.005

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2023 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