Features of the microbiota of placenta in full-term pregnancy

Cover Page

Cite item

Full Text

Abstract

Objective: to study the microbial landscape of the placenta in full-term pregnancy and intact fetal membranes.

Materials and methods. 19 pregnant women in the gestational age of 37-41 weeks with intact membranes underwent elective cesarean section at Samara City Clinical Hospital No. 1 named after N.I. Pirogov. Their placental tissues were collected and RT-PCR tests for Lactobacillus spp., Enterobacteriaceae, Streptococcus spp., Staphylococcus spp., Gardnerella vaginalis / Prevotella bivia / Porphyromonas spp., Eubacterium spp., Sneathia spp. / Leptotrihia spp. / Fusobacterium spp, Megasphaera spp. / Veillonella spp. / Dialister spp., Lachnobacterium spp. / Clostridium spp., Mobiluncus spp. / Corynebacterium spp., Peptostreptococcus spp., Atopobiumvaginae, Mycoplasma hominis, Ureaplasma (urealyticum + parvum), Candida spp., Mycoplasma henitalium were performed.

Results. In case of physiological full-term pregnancy the total bacterial mass can be 103.9-103.7 GE/sample on the placenta, it is a normal variant. Sterile placentas were found in 21.1% of cases. “Unknown” microorganisms were revealed in 52.6% of cases, they were unidentified by the standard panel “Femoflor-16”. In other cases Enterobacteriaceae spp. (102.6 GE/sample) were found in the placental tissues in patients with intact fetal membrane. The presence of Lactobacillus spp. in the placental tissues with intact membranes is not typical.

Conclusion. RT-PCR test allow to reveal a small amount of bacterial mass in the placental tissue in case of physiological full-term pregnancy, in which the representatives of Enterobacteriaceae spp. are often time detected.

About the authors

Alina A. Bezrukova

Samara State Medical University

Author for correspondence.
Email: bezzrukovaa@yandex.ru

assistant of the Department of Food Hygiene with a Course of Hygiene for Children and Adolescents

Russian Federation, Samara

Natalya V. Spiridonova

Samara State Medical University

Email: nvspiridonova@mail.ru

Doctor of Medical Sciences, Professor, Head of the Department of Obstetrics and Gynecology, IPE

Russian Federation, Samara

Maria A. Kaganova

Samara State Medical University

Email: mkaganova@yandex.ru

Candidate of Medical Sciences, Associate Professor, Department of Оbstetrics and Gynecology, IPE

Russian Federation, Samara

Darya A. Galkina

Samara City Clinical Hospital No. 1 named after N.I. Pirogov

Email: darya.golubeva.1992@mail.ru

MD, Obstetrician-Gynecologist

Russian Federation, Samara

References

  1. Болдырева М.Н., Липова Е.В., Алексеев Л.П. и др. Характеристика биоты урогенитального тракта у женщин репродуктивного возраста методом ПЦР в реальном времени // Журнал акушерства и женских болезней. – 2009. – Т. 58. – № 6. – С. 36–42. [Boldyreva MN, Lipova EV, Alexeev LP, et al. Features of urogenital tract’s biota determined by means of real-time pcr among women of reproductive age. Journal of obstetrics and women’s diseases. 2009;58(6):36–42. (In Russ.)]
  2. Ворошилина Е.С., Тумбинская Л.В., Донников А.Е. и др. Биоценоз влагалища с точки зрения количественной полимеразной цепной реакции: что есть норма? // Акушерство и гинекология. – 2011. – № 1. – С. 57–65. [Voroshilina ES, Tumbinskaya LV, Donnikov AE, et al. Vaginal biocenosis in the context of view of quantitative polymerase chain reaction: what is its norm? Obstetrics and gynecology. 2011;(1):57–65. (In Russ.)]
  3. Попова Е.Н., Гордеев И.Г. Современные представления о микробиоме человека. Микробиота / под ред. Е.Л. Никонова, Е.Н. Попова. – М.: Медиа Сфера, 2019. – С. 5–19. [Popova EN, Gordeev IG. Sovremennye predstavleniya o mikrobiome cheloveka. Mikrobiota. Ed. by E.L. Nikonova, E.N. Popova. Moscow: Media Sfera; 2019. P. 5–19. (In Russ.)]
  4. Сухих Г.Т., Прилепская В.Н., Трофимов Д.Ю. и др. Применение метода полимеразной цепной реакции в реальном времени для оценки микробиоценоза урогенитального тракта у женщин (тест фемофлор): медицинская технология. – М., 2011. – 36 с. [Sukhikh GT, Prilepskaya VN, Trofimov DYu, et al. Primeneniye metoda polimeraznoy tsepnoy reaktsii v realnom vremeni dlya otsenki mikrobiotsenoza urogenitalnogo trakta u zhenshchin (test femoflor): meditsinskaya tekhnologiya. Moscow, 2011. 36 p. (In Russ.)]
  5. Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014;(6):237ra265. https://doi.org/10.1126/scitranslmed.3008599.
  6. Ansbacher R, Boyson WA, Morris JA. Sterility of the uterine cavity. Am J Obstet Gynecol. 1967;99:394–396. https://doi.org/10.1016/S0002-9378(16)34549-5.
  7. Bagga R, Arora P. Genital micro-organisms in pregnancy. Front. Public Health. 2020;(8):225. https://doi.org/10.3389/fpubh.2020.00225.
  8. Mitchell CM, Haick A, Nkwopara, et al. Colonization of the upper genital tract by vaginal bacterial species in non-pregnant women. Am J Obstet Gynecol. 2015;212(5):611.e1–611.e9. https://doi.org/10.1016/ j.ajog.2014.11.043.
  9. Cobb CM, Kelly PJ, Williams KB, et al. The oral microbiome and adverse pregnancy outcomes. Int J Womens Health. 2017;(9):551–559. https://doi.org/10.2147/IJWH.S142730.
  10. Chen HJ, Gur TL. Intrauterine microbiota: Missing, or the missing link? Trends Neurosci. 2019;42:402–413. https://doi.org/10.1016/j.tins.2019.03.008.
  11. Cherouny PH, Pankuch GA, Botti JJ. Occult intraamniotic infection at the time of midtrimester genetic amniocentesis: A reassessment. Infect Dis Obstet Gynecol. 1994;2:136–139. https://doi.org/10.1155/S1064744994000530.
  12. Collado MC, Rautava S, Aakko J, et al. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;6:23129. https://doi.org/10.1038/srep23129.
  13. Fernandez H, Montuclard B, Guibert M. Does intraamniotic infection in the early phase of the second trimester really exist? Am J Obstet Gynecol. 1996;175:1077–1078.
  14. Fox C, Eichelberger K. Maternal microbiome and pregnancy outcomes. Fertil Steril. 2015;104(6):1358–1363. https://doi.org/10.1016/j.fertnstert.2015.09.037.
  15. Gervasi MT, Romero R, Bracalente G, et al. Midtrimester amniotic fluid concentrations of interleukin-6 and interferon-gamma-inducible protein-10: Evidence for heterogeneity of intra-amniotic inflammation and associations with spontaneous early (32 weeks) preterm delivery. J Perinat Med. 2012;(4):329–343. https://doi.org/10.1515/jpm-2012-0034.
  16. Goffau MC, Lager S, Sovio U, et al. Human placenta has no microbiome but can contain potential pathogens. Nature. 2019;(572):1–21. https://doi.org/10.1038/s41586-019-1451-5.
  17. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med. 2000;(342):1500–1507. https://doi.org/10.1056/NEJM200005183422007.
  18. Han YW, Shen T, Chung P, et al. Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol. 2009;(47):38–47. https://doi.org/10.1128/JCM.01206-08.
  19. Tuominen H, Rautava S, Syrjänen S, et al. HPV infection and bacterial microbiota in the placenta, uterine cervix and oral mucosa. Sci Rep. 2018;8(1):9787. https://doi.org/10.1038/s41598-018-27980-3.
  20. Ren H, Du M. Role of maternal periodontitis in preterm birth. Front Immunol. 2017;(8):139. https://doi.org/10.3389/fimmu.2017.00139.
  21. Theis KR, Romero R, Greenberg JM, et al. No consistent evidence for microbiota in murine placental and fetal tissues. mSphere. 2020;5(1):e00933-19. https://doi.org/10.1128/mSphere.00933-19.
  22. 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. J Matern Fetal Neonatal Med. 2019;29:1–16. https://doi.org/10.1016/ j.ajog.2018.10.018.
  23. Lauder AP, Roche AM, Sherrill-Mix S, et al. Comparison of placenta samples with contamination controls does not provide evidence for a distinct placenta microbiota. Microbiome. 2016;(4):29. https://doi.org/10.1186/s40168-016-0172-3.
  24. 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):196. https://doi.org/10.1186/s40168-018-0575-4.
  25. Lihong Zhu, Fei Luo, Wenjing Hu, et al. Bacterial communities in the womb during healthy pregnancy. Front Microbiol. 2018;(9):2163. https://doi.org/10.3389/fmicb.2018.02163.
  26. Lim ES, Rodriguez C, Holtz LR. Amniotic fluid from healthy term pregnancies does not harbor a detectable microbial community. Microbiome. 2018;(6):87. https://doi.org/10.1186/s40168-018-0475-7.
  27. Sanz M, Kornman K. Periodontitis and adverse pregnancy outcomes: Consensus report of the joint EFP/AAP workshop on periodontitis and systemic diseases. J Periodontol. 2013;84(4 Suppl.):164–169. https://doi.org/ 10.1902/jop.2013. 1340016.
  28. Martinez KA, Romano-Keeler J, Zackular JP, et al. Bacterial DNA is present in the fetal intestine and overlaps with that in the placenta in mice. PLoS One. 2018;13(5):e0197439. https://doi.org/10.1371/journal.pone.0197439.
  29. Neuman H, Koren O. The pregnancy microbiome. Nestle Nutr Inst Workshop Ser. 2017;(88):1–9. https://doi.org/10.1159/000455207.
  30. Parnell LA, Briggs CM, Cao B, et al. Microbial communities in placentas from term normal pregnancy exhibit spatially variable profiles. Sci Rep. 2017;(7):11200. https://doi.org/10.1038/s41598-017-11514-4.
  31. Pelzer E, Gomez-Arango LF, Barrett HL, et al. Maternal health and the placental microbiome. Placenta. 2017;54:30–37. https://doi.org/10.1016/j.placenta.2016.12.003.
  32. Peterson J, Garges S, Giovanni M, et al. The NIH human microbiome project. Genome Res. 2009;(12):2317–2323. https://doi.org/10.1101/gr.096651.109.
  33. 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. https://doi.org/10.1016/j.ajog.2016.01.193.
  34. Romero R. Prenatal medicine: The child is the father of the man. J Matern Fetal Neonatal Med. 2009;(22):636–639. https://doi.org/ 10.1080/14767050902784171.
  35. Satokari R, Gronroos T, Laitinen K, et al. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol. 2009;48(1):8–12. https://doi.org/10.1111/j.1472-765X.2008.02475.x.
  36. Solt I. The human microbiome and the great obstetrical syndromes: A new frontier in maternal-fetal medicine. Best Pract Res Clin Obstet Gynaecol. 2015;29(2):165–175. https://doi.org/10.1016/j.bpobgyn.2014.04.024.
  37. 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):404–411. https://doi.org/10.1203/01.PDR.0000153869.96 337.90.
  38. Stout MJ, Conlon B, Landeau M, et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol. 2013;208(3):226.e1–7. https://doi.org/ 10.1016/j.ajog.2013.01.018.
  39. Vanterpool SF, Been JV, Houben ML, et al. Porphyromonas gingivalis within placental villous mesenchyme and umbilical cord stroma is associated with adverse pregnancy outcome. PLoS One. 2016;11(1):e0146157. https://doi.org/10.1371/journal.pone.0146157.
  40. Wang YL, Liou JD, Pan WL. Association between maternal periodontal disease and preterm delivery and low birth weight. Taiwan J Obstet Gynecol. 2013;52(1):71–76. https://doi.org/10.1016/j.tjog.2013. 01.011.
  41. Younes JA, Lievens E, Hummelen R, et al. Women and their microbes: The unexpected friendship. Trends Microbiol. 2017;26(1):16–32. https://doi.org/10.1016/ j.tim.2017.07.008.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure. Detection rate of microorganisms in the placental tissues in full-term pregnancy

Download (47KB)
Indexing metadata

Copyright (c) 2020 Bezrukova A.A., Spiridonova N.V., Kaganova M.A., Galkina D.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).