Role of the vaginal microbiota in preterm premature rupture of membranes

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 pregnan-cies 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. Charac- terisation of the vaginal Lactobacillus microbiota as- sociated 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. [Ankirskaya A.S., Murav’eva V.V. Integral’naya otsenka sostoyaniya mikrobioty vlagalishcha, diagnostika opportunisticheskikh vaginitov. Meditsinskaya tekhnologiya. M.: FGBU «NTs AGiP im. V. I. Kulakova» Minzdravsotsrazvitiya Rossii, 2011. 20 c. (in Russian)].
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. [Voroshilina Ye.V., Tumbinskaya L.V.,Donnikov A.Ye., Plotko Ye.E., Khayutin L.V. Biotsenoz vlagalishcha s tochki zreniya kolichestvennoy PTSR: izmeneniya i korrektsiya vo vremya beremennosti. Infektsii v ginekologii. 2010; 68(3): 108–111.(in Russian)].
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. [Lipova Ye.V., Boldyreva M.N., Trofimov D.Yu., Vitvitskaya Yu.G. Femoflor. Urogenital’nyye infektsii, obuslovlennyye uslovno-patogennoy biotoy u zhenshchin reproduktivnogo vozrasta (Kliniko-laboratornaya diagnostika). Posobiye dlya vrachey. M.: DNK-Tekhnologiya. 2009. 30 s.(in Russian)]
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 GynaecolObstet 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: 10.4103/0255-0857.29388
41. Tempera G., Furneri P.M. Management of aerobic vaginitis. Gynecol Obstet Invest. 2010; 70: 244–9. oi: 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. [Dyatlova L.I. Features vaginal microbiocenosis for rupture of membranes of 22–34 weeks. Mezhdunarodnyy zhurnal eksperimental’nogo obrazovaniya. 2015; 3–46: 502–6. (in Russian)].eLIBRARY ID: 23372652
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. [Khodzhaeva Z.S., Priputnevich T.V., Murav’eva V.V., Guseinova G.E., Gorina K.A., Mishina N.D. The composition and stability of the vaginal microbiota in pregnant women during dynamic observation. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2019; (7): 30–8 (in Russian)]. http://dx.doi.org/10.18565/aig.2019.7/30-38
55. Li-Nan Zeng, Ling-li Zhang ,Jing Shi , Li-ling 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. Mukhtar F., Hameed A.B., Greenfield Sh., Billimek J. Perinatal Outcomes of Pre-viable 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., Göpel 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

Received 19.06.2019

Accepted 21.06.2019