Current understanding of the relationship between gut and vaginal microbiotas

Nikolaeva A.V., Kozlova A.A., Baranov I.I., Priputnevich T.V.

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of the Russian Federation, Moscow, Russia
The paper reviews publications devoted to cross-sectional studies of the composition of vaginal and gut microbiotas in order to assess the relationship between impaired intestinal microbiocenosis and dysbiotic processes in vaginal microbiocenosis. An analysis of the literature has shown that the change in the number of certain types of microorganisms in a particular biotope or the identification of species that are not peculiar to this habitat serves as a signal for adaptive or irreversible changes in the appropriate component of the microecosystem. These changes are known to be interrelated and occur simultaneously in several biotopes. Vaginal dysbiosis can result in a cascade of processes that disrupt balance in the female reproductive tract, causing various infectious and inflammatory processes. In this connection, gut and vaginal microbiotas as indicators of female reproductive health deserve the special attention of obstetricians and gynecologists today. A number of recent studies have identified a correlation between microbial communities in pregnant women and women whose pregnancy was complicated. Both the vaginal and gut microbiotas contribute to mother-to-infant Bifidobacterium transmission, and establishing the fact that the vaginal and gut bacteria represent the same population is an important step for future studies of maternal and neonatal health.
Conclusion: Data on the intestinal microflora serve as informative indicators of a woman's health, and the substantial changes in the composition of the intestinal microbiocenosis require adequate correction. The expediency of conducting studies in this area is confirmed.

Keywords

microbiota
vaginal microbiome
gut microbiota
opportunistic microorganisms
biotope
dysbiotic disorders
microbial colonization

References

  1. Рыбальченко О.В. Электронно-микроскопическое исследование межклеточных взаимодействий микроорганизмов различных таксономических групп. Микробиология. 2006; 75(4): 1-6. [Rybal'chenko O.V. Electron microscopic study of intercellular interactions of microorganisms of various taxonomic groups. Microbiology. 2006; 75(4): 1-6. (in Russian)]
  2. Бондаренко В.М., Мацулевич Т.В. Дисбактериоз кишечника как клинико-лабораторный синдром: современное состояние проблемы. М.: ГЭОТАР-Медиа; 2007. 300 с. [Bondarenko V.M, Maculevich T.V. Intestinal dysbiosis as a clinical and laboratory syndrome: the current state of the problem.] Moscow: GEOTAR-Media; 2007. 300 p. (in Russian)].
  3. O’Hara A.М., Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006; 7(7): 688-93. https://dx.doi.org/10.1038/sj.embor.7400731.
  4. Verda E.F., Collns S.M. Microbial-gut interactions in health and disease. Immune response s. Best Pract. Res. Clin. Gastroenterol. 2004; 18(2): 271-85. https://dx.doi.org/10.1016/j.bpg.2003.10.009.
  5. Pallen M.J. The human microbiome and hostpathogen interactions. In: K.E. Nelson, ed. Metagenomics of the human body. Springer; 2011: 43-61.
  6. Рудакова Е.Б., Мозговой С.И., Лазарева О.В. Бактериальный вагиноз. Лечащий врач. 2008; 6: 61-5. [Rudakova E.B., Mozgovoj S.I., Lazareva O.V. Bacterial vaginosis. The attending physician. 2008: 6: 61-5. (in Russian)].
  7. Цизина Е.А. Микрофлора влагалища женщин при бактериальном вагинозе. В кн.: Материалы международной заочной научной конференции «Новые задачи современной медицины». Пермь, январь 2012 г. Пермь: Меркурий; 2012: 38-40. [Cizina E.A. Microflora of the vagina of women with bacterial vaginosis. Materials of the international correspondence scientific conference "New tasks of modern Medicine". Perm, January 2012. Perm: Mercury; 2012: 38-40. (in Russian)].
  8. Costello E., Lauber C., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009; 326(5960): 1694-7. https://dx.doi.org/10.1126/science.1177486.
  9. Cribby S., Taylor M., Reid G. Vaginal microbiota and the use of probiotics. Interdiscip. Perspect. Infect. Dis. 2008; 2008: 256490. https://dx.doi.org/10.1155/2008/256490.
  10. de Vrese M., Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 2008; 111: 1-66. https://dx.doi.org/10.1093/ajcn/73.2.361s.
  11. Kinross J.M., von Roon A.C., Holmes E., Darzi A., Nicholson J.K. The human gut microbiome: implications for future health care. Curr. Gastroenterol. Rep. 2008; 10(4): 396-403. https://dx.doi.org/10.1007/s11894-008-0075-y.
  12. Попкова С.М., Ракова Е.Б., Кичигина Е.Л. Микроэкологические сочетания вагинального и кишечного биотопов у женщин с воспалительными заболеваниями нижнего этажа полового тракта. Международный междисциплинарный форум «Шейка матки и вульвовагинальные болезни». Москва, 14-17 ноября 2012 г. М.: StatusPraesens; 2012: 68-70. [Popkova S.M., Rakova E.B., Kichigina E.L. Microecological combinations of vaginal and intestinal biotopes in women with inflammatory diseases of the lower floor of the genital tract.] International Interdisciplinary Forum "Cervix and vulvovaginal diseases". Moscow, November 14–17, 2012. Moscow: Publishing House of the journal StatusPraesens; 2012: 68-70. (in Russian)].
  13. Попкова С.М., Ракова Е.Б., Храмова Е.Е., Данусевич И.Н. Микроэкологические сочетания вагинального и кишечного биотопов у женщин с воспалительными заболеваниями нижнего этажа полового тракта и девочек-подростков с дисфункцией яичников. Бюллетень СО РАМН. 2013; 33(4): 77-83. [Popkova S.M., Rakova E.B., Hramova E.E., Danusevich I.N. Microecological combinations of vaginal and intestinal biotopes in women with inflammatory diseases of the lower floor of the genital tract and adolescent girls with ovarian dysfunction. Bulletin of the SB RAMS. 2013; 33(4): 77-83. (in Russian)].
  14. Ворошилина Е.С., Тумбинская Л.В., Донников А.Е., Плотко Е.Э., Хаютин Л.В. Биоценоз влагалища с точки зрения количественной ПЦР: что есть норма? Акушерство и гинекология. 2011; 1: 57-65. [Voroshilina E.S., Donnikov A.E., Plotko E.E., Tumbinskaya L.V., Hajutin L.V. Vaginal biocenosis in terms of the quantitative polymerase chain reaction: what is the norm? Obstetrics and Gynecology. 2011; 1: 57-65. (in Russian)].
  15. Меджидова М.К., Зайдиева З.С., Вересова А.А. Микробиоценоз влагалища и факторы, влияющие на его состояние. Доступно по: http://www.remedium.ru/drugs/detail.php?ID=60978 [Medzhidova M.K., Zajdieva Z.S., Veresova A.A. Vaginal microbiocenosis and factors affecting its condition. (in Russian)]. http://www.remedium.ru/drugs/detail.php? ID=60978
  16. Antonio M.A., Rabe L.K., Hillier S.L. Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J. Infect. Dis. 2005; 192(3): 394-8. https://dx.doi.org/10.1086/430926.
  17. El Aila N. A., Tency I., Saerens B., De Backer E., Cools P., dos Santos Santiago G.L. et al. Strong correspondence in bacterial loads between the vagina and rectum of pregnant women. Res. Microbiol. 2011; 162(5): 506-13. https://dx.doi.org/10.1016/j.resmic.2011.04.004.
  18. Nuriel-Ohayon M., Neuman H., Koren O. Microbial changes during pregnancy, birth, and infancy. Front. Microbiol. 2016; 7: 1031. https://dx.doi.org/10.3389/fmicb.2016.01031.
  19. Koren O., Goodrich J.K., Cullender T.C., Spor A., Laitinen K., Bäckhed H.K. et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150(3): 470-80. https://dx.doi.org/10.1016/j.cell.2012.07.008.
  20. Aagaard K., Riehle K., Ma J., Segata N., Mistretta T.A., Coarfa C. et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PloS One. 2012; 7(6): e36466. https://dx.doi.org/10.1371/journal.pone.0036466.
  21. Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.S., McCulle S.L. et al. Vaginal microbiome of reproductive - age women. Proc. Natl. Acad. Sci. USA. 2011; 108(Suppl. 1): 4680-7. https://dx.doi.org/10.1073/pnas.1002611107.
  22. Prince A.L., Antony K.M., Ma J., Aagaard K.M. The microbiome and development: a mother’s perspective. Semin. Reprod. Med. 2014; 32: 14-22. https://dx.doi.org/10.1055/s-0033-1361818.
  23. Mysorekar I.U., Cao B. Microbiome in parturition and preterm birth. Semin. Reprod. Med. 2014; 32: 50-5. https://dx.doi.org/10.1055/s-0033-1361830.
  24. Romero R., Hassan S.S., Gajer P., Tarca A.L., Fadrosh D.W., Nikita L. 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. https://dx.doi.org/10.1186/2049-2618-2-4.
  25. Щербаков П.Л., Нижевич А.А., Логиновская В.В., Щербакова М.Ю., Кудрявцева Л.В., Митрохин С.Д., Нуртдинова Н.М., Очилова Р.А. Микроэкология кишечника у детей и ее нарушения. Фарматека. 2007; 14: 28-34. [Shcherbakov P.L., Nizhevich A.A., Loginovskaya V.V. et al. Microecology of the intestine in children and its disorders. Farmateka. 2007; 14: 28-34. (in Russian)].
  26. Никитенко В.И., Ткаченко Е.И., Стадников А.А. Транслокация бактерий из желудочно-кишечного тракта – естественный защитный механизм. Экспериментальная и клиническая гастроэнтерология. 2004; 1: 48. [Nikitenko V.I., Tkachenko E.I., Stadnikov A.A. et al. Translocation of bacteria from the gastrointestinal tract is a natural defense mechanism. Experimental and clinical gastroenterology. Experimental and clinical gastroenterology. 2004; 1: 48. (in Russian)].
  27. Funkhouser L.J., Bordenstein S.R. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 2013; 11(8): e1001631. https://dx.doi.org/10.1371/journal.pbio.1001631.
  28. Muglia L., Katz M. The enigma of spontaneous preterm birth. N. Engl. J. Med. 2010; 362(6): 529-35. https://dx.doi.org/10.1056/NEJMra0904308.
  29. Onderdonk A.B., Hecht J.L., McElrath T.F., Delaney M.L., Allred E.N., Leviton A.; ELGAN Study Investigators. Colonization of second-trimester placenta parenchyma. Am. J. Obstet. Gynecol. 2008; 199(1): 51-2. https://dx.doi.org/10.1016/j.ajog.2007.11.068.
  30. Li M., Wang M., Donovan S.M. Early development of the gut microbiome and immune-mediated childhood disorders. Semin. Reprod. Med. 2014; 32(1): 74-86. https://dx.doi.org/10.1055/s-0033-1361825.
  31. Jimenez E., Marin M.L., Martin R., Odriozola J.M., Olivares M., Xaus J. et al. Is meconium from healthy newborns actually sterile? Res. Microbiol. 2008; 159(3): 187-93. https://dx.doi.org/10.1016/j.resmic.2007.12.007.
  32. DiGiulio D.B. Diversity of microbes in amniotic fluid. Semin. Fetal Neonatal Med. 2012; 17: 2-11. https://dx.doi.org/10.1016/j.siny.2011.10.001.
  33. DiGiulio D.B., Romero R., Amogan H.P. et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008; 3(8): e3056. https://dx.doi.org/10.1371/journal.pone.0003056.
  34. Satokari R., Gronroos T., Laitinen K., Salminen S., Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett. Appl. Microbiol. 2009; 48(1): 8-12. https://dx.doi.org/10.1111/j.1472-765X.2008.02475.x.
  35. Pettker C.M., Buhimschi I.A., Magloire L.K., Sfakianaki A.K., Hamar B.D., Buhimschi C.S. Value of placental microbial evaluation in diagnosing intra-amniotic infection. Obstet. Gynecol. 2007; 109(3): 739-49. https://dx.doi.org/10.1097/01.AOG.0000255663.47512.23.
  36. Moles L., Gomez M., Heilig H., Bustos G., Fuentes S., de Vos W. et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One. 2013; 8(6): e66986. https://dx.doi.org/10.1371/journal.pone.0066986.
  37. Thum C., Cookson A.L., Otter D.E., McNabb W.C., Hodgkinson A.J., Dyer J., Roy N.C. Can nutritional modulation of maternal intestinal microbiota influence the development of the infant gastrointestinal tract? J. Nutr. 2012; 142(11): 1921-8. https://dx.doi.org/10.3945/jn.112.166231.
  38. Wagner C.L., Taylor S.N., Johnson D. Host factors in amniotic fluid and breast milk that contribute to gut maturation. Clin. Rev. Allergy Immunol. 2008; 34(2): 191-204. https://dx.doi.org/10.1007/s12016-007-8032-3.
  39. Bi L.W., Yan B.L., Yang Q.Y., Li M.M., Cui H.L. Which is the best probiotic treatment strategy to prevent the necrotizing enterocolitis in premature infants: A network meta-analysis revealing the efficacy and safety. Medicine (Baltimore). 2019; 98(41): e17521. https://dx.doi.org/10.1097/MD.0000000000017521.
  40. Gre J., Berg M., Soll R. Maternal probiotic supplementation for prevention of morbidity and mortality in preterm infants. Cochrane Database Syst. Rev. 2018; (12): CD012519. https://dx.doi.org/10.1002/14651858.CD012519.pub2.
  41. Кира Е.Ф. Бактериальный вагиноз. М.: МИА; 2012. 472с. [Kira E.F. Bacterial vaginosis. M.: MIA. 2012. 472p. (in Russian)].
  42. Greenbaum S., Greenbaum G., Moran-Gilad J., Weintraub A.Y. Ecological dynamics of the vaginal microbiome in relation to health and disease. Am. J. Obstet. Gynecol. 2019; 220(4): 324-35. https://dx.doi.org/10.1016/j.ajog.2018.11.1089.
  43. Afrakhteh M., Mahdavi A. Bacterial vaginosis and urinary tract infection. Iran. J. Obstet. Gynecol. Infertil. 2006; 9(1): 108-13.
  44. Falagas M.E., Betsi G.I., Tokas T., Athanasiou S. Probiotics for prevention of recurrent urinary tract infections in women: a review of the evidence from microbiological and clinical studies. Drugs. 2006; 66(9): 1253-61. https://dx.doi.org/10.2165/00003495-200666090-00007.
  45. Годовалов А.П., Карпунина Н.С., Карпунина Т.И. Микробиота кишечника и влагалища женщин со вторичным бесплодием и заболеваниями желудочно- кишечного тракта. Экспериментальная и клиническая гастроэнтерология. 2016; 130(6): 109-13. [Godovalov A.P., Karpunina N.S., Karpunina T.I. Microbiota of the intestine and vagina of women with secondary infertility and diseases of the gastrointestinal tract. Experimental and clinical gastroenterology. 2016; 6: 109-13. (in Russian)]..
  46. Жук С.И., Ночвина Е.А. Современный подход к коррекции нарушений овариально-менструального цикла. Здоровье женщины. 2006; 1: 92-5. [Zhuk S.I., Nochvina E.A. Modern approach to correction of ovarian-menstrual cycle disorders. Women's health. 2006; 1(25): 92-5. (in Russian)].
  47. Падруль М.М., Меззи Х., Олина А.А. Применение бактериофага в лечении хронического эндометрита. Материалы V Российского форума «Мать и дитя». М.: 2003; 287 c. [Padrul’ M.M., Mezzi Kh., Olina A.A. The use of bacteriophage in the treatment of chronic endometritis. Materials of the V Russian Forum "Mother and Child". Moscow: 2003; 287 p. [in Russian].

Received 26.03.2021

Accepted 05.05.2021

About the Authors

Anastasia V. Nikolaeva, Ph.D., Chief physician, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology,
Ministry of Healthcare of Russian Federation, +7(916)653-43-09, a_nikolaeva@oparina4.ru, 117997, Russia, Moscow, Ac. Oparina str., 4.
Anastasia A. Kozlova, graduate student of 1st obstetric physiological department, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology
and Perinatology, Ministry of Healthcare of Russian Federation, +7(926)656-19-49, aakozlova.box@gmail.com, 117997, Russia, Moscow, Ac. Oparina str., 4.
Igor I. Baranov, Dr. Med. Sci., Professor, Head of the Department of Scientific and Educational Programs, Academician V.I. Kulakov National Medical Research Center
for Obstetrics, Gynecology and Perinatology, Ministry of Healthcare of Russian Federation, i_baranov@oparina4.ru, https://orcid.org/0000-0002-9813-2823, 117997, Russia, Moscow, Ac. Oparina str., 4.
Tatiana V. Priputnevich, Head of the Department of Microbiology, Clinical Pharmacology and Epidemiology, Academician V.I. Kulakov National Medical Research Center
for Obstetrics, Gynecology and Perinatology, Ministry of Healthcare of Russian Federation, +7(910)414-56-16, priput1@gmail.com, 117997, Russia, Moscow,
Ac. Oparina str., 4.

Authors' contributions: Kozlova A.A., Nikolaeva A.V. – choosing a research topic; Kozlova A.A., Nikolaeva A.V., Priputnevich T.V. – search for literary data; Kozlova A.A. – writing the manuscript of the article; Priputnevich T.V., Baranov I.I. – writing and editing the article.
Conflicts of interest: The authors declare that there are no conflicts of interest.
Funding: There has been no funding for the preparation of the article for publication.

For citation: Nikolaeva A.V., Kozlova A.A., Baranov I.I., Priputnevich T.V. Current understanding of the relationship between gut and vaginal microbiotas.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2021; 9: 5-11 (in Russian)
https://dx.doi.org/10.18565/aig.2021.9.5-11

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.