Role of the vaginal microbiota in preterm premature rupture of membranes


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Abstract

The authors have carried out a systems analysis of the information available in the current literature on the vaginal microbiome and the role of dysbiotic disorders in the genesis of premature rupture of membranes (PROM) when the length of pregnancy is 22-36 weeks and 6 days. The paper includes the data published over the past 10 years in the foreign and Russian literary sources found in Pubmed on this problem. It presents the results of some studies of the vaginal microbiome in pregnant women with PROM and the identification of predictors for this complication. The results of ongoing studies confirm that it is necessary to investigate the vaginal microbiota composition at early gestational ages; the timely diagnosis of the abnormal vaginal microbiota will be able to substantially reduce the frequency of obstetric and neonatal complications. Further investigations are required to identify the most significant microbiological predictors in order to determine pregnant women at high risk for PROM.

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About the authors

Gulnara E. Guseinova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology Ministry of Health of Russia

Email: marysca666@rambler.ru
graduate student in the Department 117997, Russia, Moscow, Akademika Oparina str. 4

Zulfiya S. Khodzhaeva

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology Ministry of Health of Russia

Email: zkhodjaeva@mail.ru
M.D., Professor, Head of High Risk Pregnancy Dept 117997, Russia, Moscow, Akademika Oparina str. 4

Vera V. Muravyeva

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology Ministry of Health of Russia

Email: v_muravieva@oparina4.ru
senior researcher, PhD in the Laboratory of microbiology, Departament of microbiology and clinical pharmacology 117997, Russia, Moscow, Akademika Oparina str. 4

References

  1. Howson C.P., Kinney M.V., Lawn J.E., eds. March of Dimes, PMNCH, Save the Children, WHO. Born Too Soon: The Global Action Report on Preterm Birth. World Health Organization. Geneva, 2012. Available from: http://www.who.int/pmnch/media/news/2012/201204_born-toosoon-report.pdf
  2. Simhan H.N., Canavan T.P. Preterm premature rupture of membranes: diagnosis, evaluation and management strategies. BJOG. 2005; 112(Suppl 1): 32-7. doi: 10.1111/j.1471-0528.2005.00582.x
  3. Waters T.P., Mercer B.M. The management of preterm premature rupture of the membranes near the limit of fetal viability. Am J Obstet Gynecol. 2009; 201(3): 230-40. doi: 10.1016/j.ajog.2009.06.049.
  4. Crane J.M.G., Magee L.A., Lee T., Synnes A., von Dadelszen P, Dahlgren L., et al. Maternal and perinatal outcomes of pregnancies delivered at 23weeks’ gestation. J Obstet Gynaecol Can. 2015; 37: 214-24. http://dx.doi.org/10.1016/S1701-2163(15)30307-8
  5. Goldenberg R.L., Culhane J.F., Iams J.D., Romero R. Epidemiology and causes of preterm birth. Lancet. 2008; 371(9606): 75-84. doi: 10.1016/S0140-6736(08)60074-4.
  6. Mercer B.M. Preterm premature rupture of the membranes. Obstet Gynecol. 2003; 101: 178-93. doi: 10.1016/s0029-7844(02)02366-9
  7. Manuck T.A., Varner M.W. Neonatal and early childhood out-comes following early vs. later preterm premature rupture of membranes. Am J Obstet Gynecol. 2014; 211: 308.e1-6. doi: 10.1016/j.ajog.2014.05.030
  8. Soylu H., Jefferies A., Diambomba Y., Windrim R., Shah P.S. Rupture of membranes before the age of viability and birth after the age of viability: comparison of outcomes in a matched cohort study. J Perinatol. 2010; 30: 645-9. doi: 10.1038/jp.2010.11
  9. Brumbaugh J.E., Colaizy T.T., Nuangchamnong N., et al. Neonatal Survival after Prolonged Preterm Premature Rupture of Membranes before 24 Weeks of Gestation. Obstet Gynecol. 2014; 124(5): 992-8. doi: 10.1097/aog.0000000000000511
  10. Roberts D., Vause S., Martin W., Green P., Walkinshaw S., Bricker L., Beardsmore C., Shaw B.N., McKay A., Skotny G., Williamson P., Alfirevic Z. Amnioinfusion in preterm premature rupture of membranes (AMIPROM): a randomised controlled trial of amnioinfusion versus expectant management in very early preterm premature rupture of membranes - a pilot study. Health Technol Assess. 2014; 18(21): 1-135. doi: 10.3310/hta18210.
  11. Ryckman K.K., Simhan H.N., Krohn M.A., Williams S.M. Predicting risk of bacterial vaginosis: the role of race, smoking and corticotropin-releasing hormone-related genes. Mol Hum Reprod. 2009; 15(2): 131-7. doi: 10.1093/molehr/gan081
  12. Brotman R.M. Vaginal microbiome and sexually transmitted infections: an epidemiologic perspective. J Clin Invest. 2011; 121(12): 4610-7. doi: 10.1172/JCI57172.
  13. Ma B., Forney L.J., Ravel J. Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol. 2012; 66: 371-89. doi: 10.1146/annurev-micro-092611-150157.
  14. Hickey R.J., Zhou X., Pierson J.D., Ravel J., Forney L.J. Understanding vaginal microbiome complexity from an ecological perspective. Transl Res. 2012; 160: 267-82. doi: 10.1016/j.trsl.2012.02.008.
  15. Romero R., Hassan S.S., Gajer P., Tarca A.L, Fadrosh D.W., Nikita L., Galuppi M., Lamont R.F., Chaemsaithong P., Miranda J., Chaiworapongsa T., Ravel J. 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.
  16. Shiraishi T., Fukuda K., Morotomi N., Imamura Y., Mishima J., Imai S, et al. Influence of menstruation on the microbiota of healthy women’s labia minora as analyzed using a 16S rRNA gene-based clone library method. Jpn J Infect Dis. 2011; 64: 76-80. PMID: 21266747
  17. Kyongo J.K., Jespers V., Goovaerts O., Michiels J., Menten J., Fichorova R.N., et al. Searching for lower female genital tract soluble and cellular biomarkers: defining levels and predictors in a cohort of healthy Caucasian women. PloS One. 2012; 7: e43951. doi: 10.1371/journal.pone.0043951.
  18. Mitchell C.M., Fredricks D.N., Winer R.L., Koutsky L. Effect of sexual debut on vaginal microbiota in a cohort of young women. Obstet Gynecol. 2012; 120: 1306-13. http://dx.doi.org/10.1097/aog.0b013e31827075ac
  19. Gajer P., Brotman R.M., Bai G., Sakamoto J., Schutte U.M., Zhong X., et al. Temporal dynamics of the human vaginal microbiota. SciTransl Med. 2012; 4(132):132ra152. doi: 10.1126/scitranslmed.3003605.
  20. Romero R, Hassan S., Gajer P., Tarca A.L., Fadrosh D.W., Bieda J., Chaemsaithong P., Miranda J., Chaiworapongsa T., Rave J. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal deliveryat term. Microbiome. 2014; 2 (18): 1-15. http://dx.doi.org/10.1186/2049-2618-2-18
  21. Donders G.G., Van Calsteren K., Bellen G., et al. Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG. 2009; 116(10): 1315-24. doi: 10.1111/j.1471-0528.2009.02237.x.
  22. Macklaim J.M., Gloor G.B., Anukam K. C., et al. At the crossroads of vaginal health and disease, the ge- nome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci USA. 2011;108(1):4688-95. doi: 10.1073/pnas.1000086107.
  23. Ravel J., Gajer P., Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011;108: 4680-7. doi: 10.1073/pnas.1002611107.
  24. Petricevic L Domig K Nierscher F.J, et al. Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci Rep. 2014; 4: 51362. doi: 10.1038/srep05136.
  25. Sobel J.D. Bacterial Vaginosis. Annu Rev Med. 2000; 51: 349-56. doi: 10.1146/annurev.med.51.1.349
  26. Анкирская А.С., Муравьева В.В. Интегральная оценка состояния микробиоты влагалища, диагностика оппортунистических вагинитов. Медицинская технология. М.: ФГБУ «НЦ АГиП им. В.И. Кулакова» Минздравсоцразвития России, 2011.
  27. Ворошилина Е.В., Тумбинская Л.В., Донников А.Е., Плотко Е.Э., Хаютин Л.В. Биоценоз влагалища с точки зрения количественной ПЦР: изменения и коррекция во время беременности. Инфекции в гинекологии. 2010; 68(3): 108-111.
  28. Липова Е.В., Болдырева М.Н., Трофимов Д.Ю., Витвицкая Ю.Г. Фемофлор. Урогенитальные инфекции, обусловленные условно-патогенной биотой у женщин репродуктивного возраста (Клинико-лабораторная диагностика). Пособие для врачей. М.: ДНК-Технология. 2009. 30 с.
  29. 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. doi: 10.1371/journal.pone.0036466.
  30. MacIntyre D.A., Chandiramani M., Lee Y.S., Kindinger L. Smith A., Angelopoulos N., et al. The vaginal microbiome during pregnancy and the postpartum period in a European population. SciRep. 2015; 5: 8988. doi: 10.1038/srep08988.
  31. 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: 10. doi: 10.1186/2049-2618-2-10.
  32. Reid G., Younes J.A., Van der Mei H.C., Gloor G.B., Knight R., Busscher H.J. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol. 2011; 9(1): 27-38. doi: 10.1038/nrmicro2473.
  33. Vitali B., Cruciani F., Picone G., Parolin C., Donders G., Laghi L. Vaginal microbiome and metabolome highlight specific signatures of bacterial vaginosis. Eur J Clin Microbiol Infect Dis. 2015; 34(12): 2367e2376. http://dx.doi.org/10.1007/s10096-015-2490-y.
  34. DiGiulio D.B., Callhan B.J., McMurdie P.J., Costello E.K., Lyell D.J., Robaczewska A., Sun C.L., Goltsman D.S.A., Wong R.J., Shaw G., Stevenson D.K., Holmes S.P., Relman D.A. Temporal and spacial variation of the humanmicrobiota during pregnancy. Proc Natl Acad Sci U S A. 2015; 112(35): 11060-5. doi: 10.1073/pnas.1502875112.
  35. Hyman R.W., Fukushima M., Jiang H., et al. Diversity of the vaginal microbiomecorrelates with preterm birth. Reprod Sci. 2013; 21(1): 32e40. http://dx.doi.org/10.1177/1933719113488838
  36. Lamont R.F., Sobel J.D., Akins R.A., Hassan S.S., Chaiworapongsa T., Kusanovic J.P., Romero R. The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG. 2011; 118(5): 533-49. doi: 10.1111/j.1471-0528.2010.02840.x
  37. Tibaldi C., Cappello N., Latino M.A., Polarolo G., Masuelli G., Cavallo F., Benedetto C. Maternal risk factors for abnormal vaginal microbiota during pregnancy. Int J Gynaecol Obstet 2016; 133: 89-93. http://doi.wiley.com/10.1016/j.ijgo.2015.07.035
  38. Vinturache A.E., Gyamfi-Bannerman C., Hwang J., Mysorekar I.U., Jacobsson B.; Preterm Birth International Collaborative (PREBIC). Maternal microbiome -A pathway to preterm birth. Semin Fetal Neonatal Med. 2016; 21: 94-9. http:// dx.doi.org/10.1016/j.siny.2016.02.004
  39. Denney J.M., Culhane J.F. Bacterial vaginosis: a problematic infection from both a perinatal and neonatal perspective. Semin Fetal Neonatal Med. 2009; 14: 200-3. doi: 10.1016/j.siny.2009.01.008.
  40. Karat C., Madhivanan P., Krupp K., Poornima S., Jayanthi N.V., Suguna J.S., Mathai E. The clinical and microbiological correlates of premature rupture of membranes. Indian J Med Microbiol. 2006; 24: 283-5. doi: 10.4103/02550857.29388
  41. Tempera G., Furneri P.M. Management of aerobic vaginitis. Gynecol Obstet Invest. 2010; 70: 244-9. doi: 10.1159/000314013.
  42. Lamont R.F. Advances in the prevention of infection-related preterm birth. Front Immunol. 2015; 6: 566. doi: 10.3389/fimmu.2015.00566
  43. Romero R., Espinoza J., Kusanovic J.P., et al. The preterm parturition syndrome. BJOG. 2006; 113(Suppl3): 17-42. doi: 10.1111/j.1471-0528.2006.01120.x
  44. Ghartey J.P., Smith B.C., Chen Z., Buckley N., Lo Y., Ratner A.J., Herold B.C., Burk R.D. Lactobacillus crispatus Dominant Vaginal Microbiome Is Associated with Inhibitory Activity of Female Genital Tract Secretions against Escherichia coli. PLoS One. 2014; 9(5): e96659. doi: 10.1371/journal.pone.0096659.
  45. Дятлова Л.И. Особенности микробиоценоза влагалища при преждевременном разрыве околоплодных мембран при сроках гестации 22-34 недели. Международный журнал экспериментального образования. 2015; 3-46: 502-6.
  46. Brown R., Kindinger L., Lee Y., Marchesi J.R., Bennett P., MacIntyre D. Role of the vaginal microbiome in preterm prelabour rupture of the membranes: an observational study. Lancet. 2016; 387(special issue): S22. https://doi.org/10.1016/S0140-6736(16)00409-8
  47. Fortner K.B., Grotegut C.A., Ransom C.E., Bentley R.C., Feng L., Lan L., et al. Bacteria localization and chorion thinning among preterm premature rupture of membranes. PloS One. 2014; 9: e83338. http://dx.plos.org/10.1371/journal. pone.0083338
  48. Goldenberg R.L., Culhane J.F., Iams J.D., Romero R. Epidemiology and causes of preterm birth. Lancet. 2008; 371: 75-84. doi: 10.1016/S0140-6736(08)60074-4.
  49. Saigal S., Doyle L.W. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008; 371: 261-9. doi: 10.1016/S0140-6736(08)60136-1.
  50. Paramel Jayaprakash T., Wagner E.C., van Schalkwyk J., Albert A.Y.K., Hill J.E., Money D.M., et al. High Diversity and Variability in the Vaginal Microbiome in Women following Preterm Premature Rupture of Membranes (PPROM): A Prospective Cohort Study. PLoS One. 2016; 11(11): e0166794. https://doi.org/10.1371/journal.pone.0166794
  51. Genovese C., Corsello S., Nicolosi D., Aidala V., Falcidia E., Tempera G. Alterations of the vaginal microbiota in the third trimester of pregnancy and pPROM. Eur Rev Med Pharmacol Sci. 2016; 20(16): 3336-43. PMID: 27608890
  52. Brown R.G., Marchesi J.R., Lee Y.S., Smith A., Lehne B., Kindinger L.M., Terzidou V., Holmes E., Nicholson J.K., Bennett P.R., MacIntyre D.A. Vaginal dysbiosis increases risk of preterm fetal membrane rupture, neonatal sepsis and is exacerbated by erythromycin. BMC Med. 2018; 16(1): 9. doi: 10.1186/s12916-017-0999-x.
  53. Brown R.G., Al-Memar M., Marchesi J.R., Lee Y.S, Smith A., Chan D., Lews H., Kindinger L., Terzidou V., Bourne T., Bennett P.R., MacIntyre D. A. 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. http://dx.doi.org/10.1016/j.trsl.2018.12.005
  54. Ходжаева З.С., Припутневич Т.В., Муравьева В.В., Гусейнова Г.Э., Горина К.А., Мишина Н.Д. Оценка состава и стабильности микробиоты влагалища у беременных в процессе динамического наблюдения. Акушерство и гинекология. 2019; 7: 30-8. http://dx.doi.org/10.18565/aig.2019.7/30-38
  55. Li-Nan Zeng, Lingli Zhang ,Jing Shi, Liling Gu, W.endie Grogan, Mary M. Gargano, Chen Chen The primary microbial pathogens associated with premature rupture of the membranes in China: A systematic review. Taiwan J Obstet Gynecol. 2014; 53(4): 443-51. http://dx.doi.org/10.1016/j.tjog.2014.02.003
  56. Liu L., Oza S., Hogan D., Perin J., Rudan I., Lawn J.E., et al. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet. 2015; 385(9966): 430-40. doi: 10.1016/S0140-6736(14)61698-6.
  57. Linehan L.A., Walsh J., Morris A., Kenny L., O’Donoghue K., Dempsey E., et al. Neonatal and maternal outcomes following midtrimester preterm premature rupture of the membranes: a retrospective cohort study. BMC Pregnancy Childbirth. 2016; 16: 25. doi: 10.1186/s12884-016-0813-3.
  58. Gomez R., Romero R., Nien J.K., Medina.L, Carstens M., Kim Y.M., et al. Antibiotic administration to patients with preterm premature rupture of membranes does not eradicate intra-amniotic infection. J Matern Fetal Neonatal Med. 2007; 20: 167-73. doi: 10.1080/14767050601135485
  59. Gezer A., Parafit-Yalciner E., Guralp O., Yedigoz V., Altinok T., Madazli R. Neonatal morbidity mortality outcomes in preterm premature rupture of membranes. J Obstet Gynaecol. 2013; 33: 38-42. doi: 10.3109/01443615.2012.729620.
  60. MukhtarF., Hameed A.B., Greenfield Sh., Billimek J. Perinatal Outcomes of Previable Preterm Premature Rupture of Membranes. J Gyn Obs Bul. 2018; 2(1): 1-11. doi: https://doi.org/10.24218/jgob.2018.08.
  61. Korzeniewski S.J., Romero R., Cortez J., Pappas A., Schwartz A.G., Kim C.J., et al. A “multi-hit” model of neonatal white matter injury: cumulative contributions of chronic placental inflammation, acute fetal inflammation and postnatal inflammatory events. J Perinat Med. 2014; 42: 731-43. doi: 10.1515/jpm-2014-0250
  62. Garcia-Munoz R.F, Galan Henriquez G., Figueras Aloy J., Garcia-Alix P.A. Outcomes of very-low-birth-weight infants exposed to maternal clinical chorioamnionitis: a multicentre study. Neonatology. 2014; 106: 229-34. doi: 10.1159/000363127
  63. Soylu, H., Jefferies, A., Diambomba, Y., et al. Rupture of membranes before the age of viability and birth after the age of viability: comparison of outcomes in a matched cohort study. J Perinatol. 2010; 30: 645-9. doi: 10.1038/jp.2010.11
  64. Staude B., Oehmke F., Lauer T., Behnke J., Gopel W., Schloter M., Schulz H., Krauss-Etschmann S., Ehrhardt H. The Microbiome and Preterm Birth: A Change in Paradigm with Profound Implications for Pathophysiologic Concepts and Novel Therapeutic Strategies. Biomed Res Int. 2018; 2018: 7218187. doi: 10.1155/2018/7218187

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