urovestВестник урологииUrology Herald2308-6424Rostov State Medical University10.21886/2308-6424-2024-12-5-12-23urovest-954Research ArticleОРИГИНАЛЬНЫЕ СТАТЬИORIGINAL ARTICLESСостав и динамика мочепузырной, влагалищной и кишечной микробиоты в трёх триместрах беременности у здоровых женщинComposition and dynamics of bladder, vaginal and bowel microbiota during three trimesters in healthy pregnant womenhttps://orcid.org/0000-0002-4808-7024НабокаЮ. Л.NabokaYu. L.

Набока Юлия Лазаревна — д-р мед. наук, профессор.

Ростов-на-Дону

Yulia L. Naboka — Dr.Sc.(Med), Full Prof.

Rostov-on-Don

nagu22@mail.ruhttps://orcid.org/0000-0003-0995-7848ВоробьеваН. В.VorobyevaN. V.

Воробьева Наталья В.

Ростов-на-Дону

Natalia V. Vorobyeva.

Rostov-on-Don

nagu22@mail.ruhttps://orcid.org/0000-0003-2986-3099ГудимаИ. А.GudimaI. A.

Гудима Ирина Александровна — д-р мед. наук, доцент.

Ростов-на-Дону

Irina A. Gudima — Dr.Sc.(Med), Assoc. Prof. (Docent).

Rostov-on-Don

Nensi71@mail.ruhttps://orcid.org/0000-0002-4120-9180СинявскаяТ. Г.SinyavskayaT. G.

Синявская Татьяна Геннадьевна — канд. экон. наук, доцент.

Ростов-на-Дону

Tatiana G. Sinyavskaya — Cand.Sc. (Econ), Assoc.Prof. (Docent).

Rostov-on-Don

sin-ta@yandex.ruhttps://orcid.org/0000-0003-1958-9858ИсмаиловР. С.IsmailovR. S.

Исмаилов Руслан Самедович — канд. мед. наук.

Ростов-на-Дону

Ruslan S. Ismailov — Cand.Sc.(Med).

Rostov-on-Don

dr.ruslan.ismailov@gmail.comhttps://orcid.org/0000-0003-1304-5403НаберК. Г.NaberK. G.

Набер Курт Георг — доктор медицины, доктор философии, доцент.

Мюнхен

Kurt G. Naber — M.D., Ph.D., Assoc. Prof. of Urology.

Munich

kurt@nabers.dehttps://orcid.org/0000-0002-1710-0169КоганМ. И.KoganM. I.

Коган Михаил Иосифович — д-р мед. наук, профессор, заслуженный деятель науки РФ.

Ростов-на-Дону

Mikhail I. Kogan — Dr.Sc.(Med), Full Prof., Honored Scientist of the Russian Federation.

Rostov-on-Don

dept_kogan@mail.ruРостовский государственный медицинский университетРоссияRostov State Medical UniversityRussian FederationРостовский государственный экономический университет (РИНХ)РоссияRostov State University of Economics (RINH)Russian FederationТехнический университет МюнхенаГерманияTechnical University of MunichGermany2024281120241251223Copyright © Набока Ю.Л., Воробьева Н.В., Гудима И.А., Синявская Т.Г., Исмаилов Р.С., Набер К.Г., Коган М.И., 20242024Набока Ю.Л., Воробьева Н.В., Гудима И.А., Синявская Т.Г., Исмаилов Р.С., Набер К.Г., Коган М.И.Naboka Y.L., Vorobyeva N.V., Gudima I.A., Sinyavskaya T.G., Ismailov R.S., Naber K.G., Kogan M.I.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.urovest.ru/jour/article/view/954Введение

Введение. Динамика микробиоты основных биотопов во время беременности практически не изучена, хотя изменения в данных компартментах имеют важную роль как в функционировании женского организма, так и в развитии плода.

Цель исследования

Цель исследования. Изучить динамику и взаимосвязь изменений микробиоты мочевого пузыря, влагалища и кишечника у здоровых беременных женщин в течение трёх триместров (Т-1, 2, 3).

Материалы и методы

Материалы и методы. Дизайн исследования: одноцентровое сравнительное наблюдательное лонгитюдное исследование. Тридцать из 220 первородящих женщин были отобраны для скрининга в женской консультации в период с 2021 по 2022 год. У всех беременных женщин были взяты пробы в Т-1, 2, 3 для культурального исследования: пробы мочи из мочевого пузыря (средняя порция), мазки из заднего свода влагалища и фекальные массы. После предкультуральной подготовки образцы исследовали на расширенном наборе питательных сред (n = 13) в специальных условиях культивирования (аэробно-анаэробных). По результатам исследований оценивали частоты идентификации (ЧИД), величины микробной нагрузки (ВМН) и коэффициенты взаимной сопряжённости (КВС) микроорганизмов между различными биотопами.

Результаты

Результаты. Культуральное исследование выявило различные бактерии в каждом биотопе, исследованном во всех триместрах. В моче от Т1 до Т3 наблюдались аэробы и анаэробы с различными ЧИД, но ни один таксон не показал стабильного ЧИД. Во влагалище ЧИД бактерий были аналогичны в моче. Микробиота кишечника была наиболее стабильным биотопом, остававшимся практически неизменным в течение беременности. В моче и влагалище средние показатели ЧИД большинства аэробов и анаэробов не претерпели значительных изменений в течение беременности. В кишечнике ВМН были стабильно выше, чем в мазках из мочи и влагалища. По данным анализа КВС, биотопы мочевой пузырь — влагалище и мочевой пузырь — кишечник показали значительно большее количество взаимосвязей между микроорганизмами во всех Т. Заключение. Наблюдаемая структура микробиоты в течение всех Т ассоциируется с неосложнённым течением беременности. Эти результаты являются значимыми для изучения изменений микробиоты при осложнённой беременности.

Introduction

Introduction. The microbiota dynamics of the core biotopes during pregnancy are hardly studied, although changes in these compartments have an important role in both the functioning of the female organism and foetal development.

Objective

Objective. To study the dynamics and interactions of changes in bladder, vaginal and bowel microbiota in healthy pregnant women over three trimesters (TRI-1, 2, 3).

Materials & Methods

Materials & Methods. Study design: a single-centre comparative observational longitudinal study. Thirty out of first-time 220 pregnant women were selected for screening at the antenatal clinic from 2021 to 2022. All pregnant women underwent sampling at T-1, 2, 3: mid-stream bladder urine samples, posterior vaginal swabs and faecal masses were collected for culture study. After a special pre-culture preparation, samples were examined on an expanded set of nutrient media (n = 13) using special cultivation (aerobic-anaerobic) conditions. Based on the research results, identification frequencies (IDFs), microbial load values (MLVs) and microbial co-occurrence coefficients between the different biotopes were estimated.

Results

Results. Culture study revealed various bacteria in each biotope investigated during all TRIs. In the urine, aerobes and anaerobes were observed from TRI-1 to TRI-3 with different IDFs, but no taxa showed a stable IDFs. In the vagina, IDFs of bacteria were similar to urinary. The bowel microbiota was the most stable biotope remained almost unchanged during pregnancy. In the urine and vagina, mean MLVs of most aerobes and anaerobes did not change significantly throughout pregnancy. In the bowel, MLVs were consistently higher than in the urine and vaginal swabs. According to the co-occurrence analysis bladder-vagina and bladder-bowel biotopes showed significantly more interconnections between microorganisms in all TRIs.

Conclusion

Conclusion. The observed microbiota structure during all TRIs is associated with uncomplicated gestation. These results will be valuable for studying changes of microbiota in complicated pregnancies.

беременностьмикробиота влагалищамикробиота мочевого пузырямикробиота кишечникаpregnancyvaginal microbiotabladder microbiotabowel microbiotaReferencesKoren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, Bäckhed F, Isolauri E, Salminen S, Ley RE. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470-480. DOI: 10.1016/j.cell.2012.07.008Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, Bäckhed F, Isolauri E, Salminen S, Ley RE. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470-480. DOI: 10.1016/j.cell.2012.07.008Di Simone N, Santamaria Ortiz A, Specchia M, Tersigni C, Villa P, Gasbarrini A, Scambia G, D’Ippolito S. Recent Insights on the Maternal Microbiota: Impact on Pregnancy Outcomes. Front Immunol. 2020;11:528202. DOI: 10.3389/fimmu.2020.528202Di Simone N, Santamaria Ortiz A, Specchia M, Tersigni C, Villa P, Gasbarrini A, Scambia G, D’Ippolito S. Recent Insights on the Maternal Microbiota: Impact on Pregnancy Outcomes. Front Immunol. 2020;11:528202. DOI: 10.3389/fimmu.2020.528202Yang H, Guo R, Li S, Liang F, Tian C, Zhao X, Long Y, Liu F, Jiang M, Zhang Y, Ma J, Peng M, Zhang S, Ye W, Gan Q, Zeng F, Mao S, Liang Q, Ma X, Han M, Gao F, Yang R, Zhang C, Xiao L, Qin J, Li S, Zhu C. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes. 2020;6(1):32. DOI: 10.1038/s41522-020-00142-yYang H, Guo R, Li S, Liang F, Tian C, Zhao X, Long Y, Liu F, Jiang M, Zhang Y, Ma J, Peng M, Zhang S, Ye W, Gan Q, Zeng F, Mao S, Liang Q, Ma X, Han M, Gao F, Yang R, Zhang C, Xiao L, Qin J, Li S, Zhu C. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes. 2020;6(1):32. DOI: 10.1038/s41522-020-00142-yLiang X, Wang R, Luo H, Liao Y, Chen X, Xiao X, Li L. The interplay between the gut microbiota and metabolism during the third trimester of pregnancy. Front Microbiol. 2022;13:1059227. DOI: 10.3389/fmicb.2022.1059227Liang X, Wang R, Luo H, Liao Y, Chen X, Xiao X, Li L. The interplay between the gut microbiota and metabolism during the third trimester of pregnancy. Front Microbiol. 2022;13:1059227. DOI: 10.3389/fmicb.2022.1059227Haddad EN, Nel NH, Petrick LM, Kerver JM, Comstock SS. Associations between the Gut Microbiota, Urinary Metabolites, and Diet in Women during the Third Trimester of Pregnancy. Curr Dev Nutr. 2022;7(4):100025. DOI: 10.1016/j.cdnut.2022.100025Haddad EN, Nel NH, Petrick LM, Kerver JM, Comstock SS. Associations between the Gut Microbiota, Urinary Metabolites, and Diet in Women during the Third Trimester of Pregnancy. Curr Dev Nutr. 2022;7(4):100025. DOI: 10.1016/j.cdnut.2022.100025García-Mantrana I, Selma-Royo M, González S, Parra-Llorca A, Martínez-Costa C, Collado MC. Distinct maternal microbiota clusters are associated with diet during pregnancy: impact on neonatal microbiota and infant growth during the first 18 months of life. Gut Microbes. 2020;11(4):962-978. DOI: 10.1080/19490976.2020.1730294García-Mantrana I, Selma-Royo M, González S, Parra-Llorca A, Martínez-Costa C, Collado MC. Distinct maternal microbiota clusters are associated with diet during pregnancy: impact on neonatal microbiota and infant growth during the first 18 months of life. Gut Microbes. 2020;11(4):962-978. DOI: 10.1080/19490976.2020.1730294Wang J, Zheng J, Shi W, Du N, Xu X, Zhang Y, Ji P, Zhang F, Jia Z, Wang Y, Zheng Z, Zhang H, Zhao F. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut. 2018;67(9):1614-1625. DOI: 10.1136/gutjnl-2018-315988Wang J, Zheng J, Shi W, Du N, Xu X, Zhang Y, Ji P, Zhang F, Jia Z, Wang Y, Zheng Z, Zhang H, Zhao F. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut. 2018;67(9):1614-1625. DOI: 10.1136/gutjnl-2018-315988Zheng W, Xu Q, Huang W, Yan Q, Chen Y, Zhang L, Tian Z, Liu T, Yuan X, Liu C, Luo J, Guo C, Song W, Zhang L, Liang X, Qin H, Li G. Gestational Diabetes Mellitus Is Associated with Reduced Dynamics of Gut Microbiota during the First Half of Pregnancy. mSystems. 2020;5(2):e00109-20. DOI: 10.1128/mSystems.00109-20Zheng W, Xu Q, Huang W, Yan Q, Chen Y, Zhang L, Tian Z, Liu T, Yuan X, Liu C, Luo J, Guo C, Song W, Zhang L, Liang X, Qin H, Li G. Gestational Diabetes Mellitus Is Associated with Reduced Dynamics of Gut Microbiota during the First Half of Pregnancy. mSystems. 2020;5(2):e00109-20. DOI: 10.1128/mSystems.00109-20Ma S, You Y, Huang L, Long S, Zhang J, Guo C, Zhang N, Wu X, Xiao Y, Tan H. Alterations in Gut Microbiota of Gestational Diabetes Patients During the First Trimester of Pregnancy. Front Cell Infect Microbiol. 2020;10:58. DOI: 10.3389/fcimb.2020.00058Ma S, You Y, Huang L, Long S, Zhang J, Guo C, Zhang N, Wu X, Xiao Y, Tan H. Alterations in Gut Microbiota of Gestational Diabetes Patients During the First Trimester of Pregnancy. Front Cell Infect Microbiol. 2020;10:58. DOI: 10.3389/fcimb.2020.00058Lv LJ, Li SH, Li SC, Zhong ZC, Duan HL, Tian C, Li H, He W, Chen MC, He TW, Wang YN, Zhou X, Yao L, Yin AH. Early-Onset Preeclampsia Is Associated With Gut Microbial Alterations in Antepartum and Postpartum Women. Front Cell Infect Microbiol. 2019;9:224. DOI: 10.3389/fcimb.2019.00224Lv LJ, Li SH, Li SC, Zhong ZC, Duan HL, Tian C, Li H, He W, Chen MC, He TW, Wang YN, Zhou X, Yao L, Yin AH. Early-Onset Preeclampsia Is Associated With Gut Microbial Alterations in Antepartum and Postpartum Women. Front Cell Infect Microbiol. 2019;9:224. DOI: 10.3389/fcimb.2019.00224Tersigni C, D’Ippolito S, Di Nicuolo F, Marana R, Valenza V, Masciullo V, Scaldaferri F, Malatacca F, de Waure C, Gasbarrini A, Scambia G, Di Simone N. Correction to: Recurrent pregnancy loss is associated to leaky gut: a novel pathogenic model of endometrium inflammation? J Transl Med. 2019;17(1):83. Erratum for: J Transl Med. 2018;16(1):102. DOI: 10.1186/s12967-019-1823-5.Tersigni C, D’Ippolito S, Di Nicuolo F, Marana R, Valenza V, Masciullo V, Scaldaferri F, Malatacca F, de Waure C, Gasbarrini A, Scambia G, Di Simone N. Correction to: Recurrent pregnancy loss is associated to leaky gut: a novel pathogenic model of endometrium inflammation? J Transl Med. 2019;17(1):83. Erratum for: J Transl Med. 2018;16(1):102. DOI: 10.1186/s12967-019-1823-5.D’Ippolito S, Tersigni C, Marana R, Di Nicuolo F, Gaglione R, Rossi ED, Castellani R, Scambia G, Di Simone N. Inflammosome in the human endometrium: further step in the evaluation of the “maternal side”. Fertil Steril. 2016;105(1):111-8.e1-4. DOI: 10.1016/j.fertnstert.2015.09.027D’Ippolito S, Tersigni C, Marana R, Di Nicuolo F, Gaglione R, Rossi ED, Castellani R, Scambia G, Di Simone N. Inflammosome in the human endometrium: further step in the evaluation of the “maternal side”. Fertil Steril. 2016;105(1):111-8.e1-4. DOI: 10.1016/j.fertnstert.2015.09.027Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108 Suppl 1(Suppl 1):4680-4687. DOI: 10.1073/pnas.1002611107Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108 Suppl 1(Suppl 1):4680-4687. DOI: 10.1073/pnas.1002611107Anahtar MN, Gootenberg DB, Mitchell CM, Kwon DS. Cervicovaginal Microbiota and Reproductive Health: The Virtue of Simplicity. Cell Host Microbe. 2018;23(2):159-168. DOI: 10.1016/j.chom.2018.01.013Anahtar MN, Gootenberg DB, Mitchell CM, Kwon DS. Cervicovaginal Microbiota and Reproductive Health: The Virtue of Simplicity. Cell Host Microbe. 2018;23(2):159-168. DOI: 10.1016/j.chom.2018.01.013Hyman RW, Fukushima M, Jiang H, Fung E, Rand L, Johnson B, Vo KC, Caughey AB, Hilton JF, Davis RW, Giudice LC. Diversity of the vaginal microbiome correlates with preterm birth. Reprod Sci. 2014;21(1):32-40. DOI: 10.1177/1933719113488838Hyman RW, Fukushima M, Jiang H, Fung E, Rand L, Johnson B, Vo KC, Caughey AB, Hilton JF, Davis RW, Giudice LC. Diversity of the vaginal microbiome correlates with preterm birth. Reprod Sci. 2014;21(1):32-40. DOI: 10.1177/1933719113488838Fettweis JM, Serrano MG, Brooks JP, Edwards DJ, Girerd PH, Parikh HI, Huang B, Arodz TJ, Edupuganti L, Glascock AL, Xu J, Jimenez NR, Vivadelli SC, Fong SS, Sheth NU, Jean S, Lee V, Bokhari YA, Lara AM, Mistry SD, Duckworth RA 3rd, Bradley SP, Koparde VN, Orenda XV, Milton SH, Rozycki SK, Matveyev AV, Wright ML, Huzurbazar SV, Jackson EM, Smirnova E, Korlach J, Tsai YC, Dickinson MR, Brooks JL, Drake JI, Chaffin DO, Sexton AL, Gravett MG, Rubens CE, Wijesooriya NR, Hendricks-Muñoz KD, Jefferson KK, Strauss JF 3rd, Buck GA. The vaginal microbiome and preterm birth. Nat Med. 2019;25(6):1012-1021. DOI: 10.1038/s41591-019-0450-2Fettweis JM, Serrano MG, Brooks JP, Edwards DJ, Girerd PH, Parikh HI, Huang B, Arodz TJ, Edupuganti L, Glascock AL, Xu J, Jimenez NR, Vivadelli SC, Fong SS, Sheth NU, Jean S, Lee V, Bokhari YA, Lara AM, Mistry SD, Duckworth RA 3rd, Bradley SP, Koparde VN, Orenda XV, Milton SH, Rozycki SK, Matveyev AV, Wright ML, Huzurbazar SV, Jackson EM, Smirnova E, Korlach J, Tsai YC, Dickinson MR, Brooks JL, Drake JI, Chaffin DO, Sexton AL, Gravett MG, Rubens CE, Wijesooriya NR, Hendricks-Muñoz KD, Jefferson KK, Strauss JF 3rd, Buck GA. The vaginal microbiome and preterm birth. Nat Med. 2019;25(6):1012-1021. DOI: 10.1038/s41591-019-0450-2Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 2015;6:81. DOI: 10.3389/fphys.2015.00081Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 2015;6:81. DOI: 10.3389/fphys.2015.00081Fettweis JM, Brooks JP, Serrano MG, Sheth NU, Girerd PH, Edwards DJ, Strauss JF, The Vaginal Microbiome Consortium, Jefferson KK, Buck GA. Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology (Reading). 2014;160(Pt 10):2272-2282. DOI: 10.1099/mic.0.081034-0Fettweis JM, Brooks JP, Serrano MG, Sheth NU, Girerd PH, Edwards DJ, Strauss JF, The Vaginal Microbiome Consortium, Jefferson KK, Buck GA. Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology (Reading). 2014;160(Pt 10):2272-2282. DOI: 10.1099/mic.0.081034-0Abdelmaksoud AA, Koparde VN, Sheth NU, Serrano MG, Glascock AL, Fettweis JM, Strauss JF, Buck GA, Jefferson KK. Comparison of Lactobacillus crispatus isolates from Lactobacillus-dominated vaginal microbiomes with isolates from microbiomes containing bacterial vaginosis-associated bacteria. Microbiology (Reading). 2016;162(3):466-475. DOI: 10.1099/mic.0.000238Abdelmaksoud AA, Koparde VN, Sheth NU, Serrano MG, Glascock AL, Fettweis JM, Strauss JF, Buck GA, Jefferson KK. Comparison of Lactobacillus crispatus isolates from Lactobacillus-dominated vaginal microbiomes with isolates from microbiomes containing bacterial vaginosis-associated bacteria. Microbiology (Reading). 2016;162(3):466-475. DOI: 10.1099/mic.0.000238Stout MJ, Zhou Y, Wylie KM, Tarr PI, Macones GA, Tuuli MG. Early pregnancy vaginal microbiome trends and preterm birth. Am J Obstet Gynecol. 2017;217(3):356.e1-356.e18. DOI: 10.1016/j.ajog.2017.05.030Stout MJ, Zhou Y, Wylie KM, Tarr PI, Macones GA, Tuuli MG. Early pregnancy vaginal microbiome trends and preterm birth. Am J Obstet Gynecol. 2017;217(3):356.e1-356.e18. DOI: 10.1016/j.ajog.2017.05.030Hu F, Sun X, Su Y, Huang M. The Dynamic Changes in the Composition and Diversity of Vaginal Microbiota in Women of Different Pregnancy Periods. Microorganisms. 2023;11(11):2686. DOI: 10.3390/microorganisms11112686Hu F, Sun X, Su Y, Huang M. The Dynamic Changes in the Composition and Diversity of Vaginal Microbiota in Women of Different Pregnancy Periods. Microorganisms. 2023;11(11):2686. DOI: 10.3390/microorganisms11112686Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C, Raza S, Rosenbaum S, Van den Veyver I, Milosavljevic A, Gevers D, Huttenhower C, Petrosino J, Versalovic J. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012;7(6):e36466. DOI: 10.1371/journal.pone.0036466Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C, Raza S, Rosenbaum S, Van den Veyver I, Milosavljevic A, Gevers D, Huttenhower C, Petrosino J, Versalovic J. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012;7(6):e36466. DOI: 10.1371/journal.pone.0036466Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, Galuppi M, Lamont RF, Chaemsaithong P, Miranda J, Chaiworapongsa T, Ravel J. Correction: The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):10. Erratum for: Microbiome. 2014;2(1):4. DOI: 10.1186/2049-2618-2-10Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, Galuppi M, Lamont RF, Chaemsaithong P, Miranda J, Chaiworapongsa T, Ravel J. Correction: The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):10. Erratum for: Microbiome. 2014;2(1):4. DOI: 10.1186/2049-2618-2-10MacIntyre DA, Chandiramani M, Lee YS, Kindinger L, Smith A, Angelopoulos N, Lehne B, Arulkumaran S, Brown R, Teoh TG, Holmes E, Nicoholson JK, Marchesi JR, Bennett PR. The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci Rep. 2015;5:8988. DOI: 10.1038/srep08988MacIntyre DA, Chandiramani M, Lee YS, Kindinger L, Smith A, Angelopoulos N, Lehne B, Arulkumaran S, Brown R, Teoh TG, Holmes E, Nicoholson JK, Marchesi JR, Bennett PR. The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci Rep. 2015;5:8988. DOI: 10.1038/srep08988Yeruva T, Rajkumar H, Donugama V. Vaginal lactobacilli profile in pregnant women with normal & abnormal vaginal flora. Indian J Med Res. 2017;146(4):534-540. DOI: 10.4103/ijmr.IJMR_774_16Yeruva T, Rajkumar H, Donugama V. Vaginal lactobacilli profile in pregnant women with normal & abnormal vaginal flora. Indian J Med Res. 2017;146(4):534-540. DOI: 10.4103/ijmr.IJMR_774_16Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI, Mendez K, Knight R, Clemente JC. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250-253. DOI: 10.1038/nm.4039Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI, Mendez K, Knight R, Clemente JC. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250-253. DOI: 10.1038/nm.4039Verma J, Bag S, Saha B, Kumar P, Ghosh TS, Dayal M, Senapati T, Mehra S, Dey P, Desigamani A, Kumar D, Rana P, Kumar B, Maiti TK, Sharma NC, Bhadra RK, Mutreja A, Nair GB, Ramamurthy T, Das B. Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. Proc Natl Acad Sci U S A. 2019;116(13):6226-6231. DOI: 10.1073/pnas.1900141116Verma J, Bag S, Saha B, Kumar P, Ghosh TS, Dayal M, Senapati T, Mehra S, Dey P, Desigamani A, Kumar D, Rana P, Kumar B, Maiti TK, Sharma NC, Bhadra RK, Mutreja A, Nair GB, Ramamurthy T, Das B. Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. Proc Natl Acad Sci U S A. 2019;116(13):6226-6231. DOI: 10.1073/pnas.1900141116Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA. The MaSuRCA genome assembler. Bioinformatics. 2013;29(21):2669-2677. DOI: 10.1093/bioinformatics/btt476Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA. The MaSuRCA genome assembler. Bioinformatics. 2013;29(21):2669-2677. DOI: 10.1093/bioinformatics/btt476Naser SM, Dawyndt P, Hoste B, Gevers D, Vandemeulebroecke K, Cleenwerck I, Vancanneyt M, Swings J. Identification of lactobacilli by pheS and rpoA gene sequence analyses. Int J Syst Evol Microbiol. 2007;57(Pt 12):2777-2789. DOI: 10.1099/ijs.0.64711-0Naser SM, Dawyndt P, Hoste B, Gevers D, Vandemeulebroecke K, Cleenwerck I, Vancanneyt M, Swings J. Identification of lactobacilli by pheS and rpoA gene sequence analyses. Int J Syst Evol Microbiol. 2007;57(Pt 12):2777-2789. DOI: 10.1099/ijs.0.64711-0Mehta O, Ghosh TS, Kothidar A, Gowtham MR, Mitra R, Kshetrapal P, Wadhwa N, Thiruvengadam R; GARBH-Ini study group; Nair GB, Bhatnagar S, Das B. Vaginal Microbiome of Pregnant Indian Women: Insights into the Genome of Dominant Lactobacillus Species. Microb Ecol. 2020;80(2):487-499. DOI: 10.1007/s00248-020-01501-0Mehta O, Ghosh TS, Kothidar A, Gowtham MR, Mitra R, Kshetrapal P, Wadhwa N, Thiruvengadam R; GARBH-Ini study group; Nair GB, Bhatnagar S, Das B. Vaginal Microbiome of Pregnant Indian Women: Insights into the Genome of Dominant Lactobacillus Species. Microb Ecol. 2020;80(2):487-499. DOI: 10.1007/s00248-020-01501-0DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DS, Wong RJ, Shaw G, Stevenson DK, Holmes SP, Relman DA. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A. 2015;112(35):11060-11065. DOI: 10.1073/pnas.1502875112DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DS, Wong RJ, Shaw G, Stevenson DK, Holmes SP, Relman DA. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A. 2015;112(35):11060-11065. DOI: 10.1073/pnas.1502875112Goltsman DSA, Sun CL, Proctor DM, DiGiulio DB, Robaczewska A, Thomas BC, Shaw GM, Stevenson DK, Holmes SP, Banfield JF, Relman DA. Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome. Genome Res. 2018;28(10):1467-1480. DOI: 10.1101/gr.236000.118Goltsman DSA, Sun CL, Proctor DM, DiGiulio DB, Robaczewska A, Thomas BC, Shaw GM, Stevenson DK, Holmes SP, Banfield JF, Relman DA. Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome. Genome Res. 2018;28(10):1467-1480. DOI: 10.1101/gr.236000.118Dobrut A, Gosiewski T, Pabian W, Bodaszewska-Lubas M, Ochonska D, Bulanda M, Brzychczy-Wloch M. The dynamics of vaginal and rectal Lactobacillus spp. flora in subsequent trimesters of pregnancy in healthy Polish women, assessed using the Sanger sequencing method. BMC Pregnancy Childbirth. 2018;18(1):350. DOI: 10.1186/s12884-018-1987-7Dobrut A, Gosiewski T, Pabian W, Bodaszewska-Lubas M, Ochonska D, Bulanda M, Brzychczy-Wloch M. The dynamics of vaginal and rectal Lactobacillus spp. flora in subsequent trimesters of pregnancy in healthy Polish women, assessed using the Sanger sequencing method. BMC Pregnancy Childbirth. 2018;18(1):350. DOI: 10.1186/s12884-018-1987-7Jacobs KM, Thomas-White KJ, Hilt EE, Wolfe AJ, Waters TP. Microorganisms Identified in the Maternal Bladder: Discovery of the Maternal Bladder Microbiota. AJP Rep. 2017;7(3):e188-e196. DOI: 10.1055/s-0037-1606860Jacobs KM, Thomas-White KJ, Hilt EE, Wolfe AJ, Waters TP. Microorganisms Identified in the Maternal Bladder: Discovery of the Maternal Bladder Microbiota. AJP Rep. 2017;7(3):e188-e196. DOI: 10.1055/s-0037-1606860Ollberding NJ, Völgyi E, Macaluso M, Kumar R, Morrow C, Tylavsky FA, Piyathilake CJ. Urinary Microbiota Associated with Preterm Birth: Results from the Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) Study. PLoS One. 2016;11(9):e0162302. DOI: 10.1371/journal.pone.0162302Ollberding NJ, Völgyi E, Macaluso M, Kumar R, Morrow C, Tylavsky FA, Piyathilake CJ. Urinary Microbiota Associated with Preterm Birth: Results from the Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) Study. PLoS One. 2016;11(9):e0162302. DOI: 10.1371/journal.pone.0162302Abbai NS, Reddy T, Ramjee G. Prevalent bacterial vaginosis infection – a risk factor for incident sexually transmitted infections in women in Durban, South Africa. Int J STD AIDS. 2016;27(14):1283-1288. DOI: 10.1177/0956462415616038Abbai NS, Reddy T, Ramjee G. Prevalent bacterial vaginosis infection – a risk factor for incident sexually transmitted infections in women in Durban, South Africa. Int J STD AIDS. 2016;27(14):1283-1288. DOI: 10.1177/0956462415616038Abd El Aziz MA, Sharifipour F, Abedi P, Jahanfar S, Judge HM. Secnidazole for treatment of bacterial vaginosis: a systematic review. BMC Womens Health. 2019;19(1):121. DOI: 10.1186/s12905-019-0822-2Abd El Aziz MA, Sharifipour F, Abedi P, Jahanfar S, Judge HM. Secnidazole for treatment of bacterial vaginosis: a systematic review. BMC Womens Health. 2019;19(1):121. DOI: 10.1186/s12905-019-0822-2Aghaizu A, Reid F, Kerry S, Hay PE, Mallinson H, Jensen JS, Kerry S, Kerry S, Oakeshott P. Frequency and risk factors for incident and redetected Chlamydia trachomatis infection in sexually active, young, multi-ethnic women: a community based cohort study. Sex Transm Infect. 2014;90(7):524-528. DOI: 10.1136/sextrans-2014-051607Aghaizu A, Reid F, Kerry S, Hay PE, Mallinson H, Jensen JS, Kerry S, Kerry S, Oakeshott P. Frequency and risk factors for incident and redetected Chlamydia trachomatis infection in sexually active, young, multi-ethnic women: a community based cohort study. Sex Transm Infect. 2014;90(7):524-528. DOI: 10.1136/sextrans-2014-051607Ahmed A, Earl J, Retchless A, Hillier SL, Rabe LK, Cherpes TL, Powell E, Janto B, Eutsey R, Hiller NL, Boissy R, Dahlgren ME, Hall BG, Costerton JW, Post JC, Hu FZ, Ehrlich GD. Comparative genomic analyses of 17 clinical isolates of Gardnerella vaginalis provide evidence of multiple genetically isolated clades consistent with subspeciation into genovars. J Bacteriol. 2012;194(15):3922-3937. DOI: 10.1128/JB.00056-12Ahmed A, Earl J, Retchless A, Hillier SL, Rabe LK, Cherpes TL, Powell E, Janto B, Eutsey R, Hiller NL, Boissy R, Dahlgren ME, Hall BG, Costerton JW, Post JC, Hu FZ, Ehrlich GD. Comparative genomic analyses of 17 clinical isolates of Gardnerella vaginalis provide evidence of multiple genetically isolated clades consistent with subspeciation into genovars. J Bacteriol. 2012;194(15):3922-3937. DOI: 10.1128/JB.00056-12Ahrens P, Andersen LO, Lilje B, Johannesen TB, Dahl EG, Baig S, Jensen JS, Falk L. Changes in the vaginal microbiota following antibiotic treatment for Mycoplasma genitalium, Chlamydia trachomatis and bacterial vaginosis. PLoS One. 2020;15(7):e0236036. DOI: 10.1371/journal.pone.0236036Ahrens P, Andersen LO, Lilje B, Johannesen TB, Dahl EG, Baig S, Jensen JS, Falk L. Changes in the vaginal microbiota following antibiotic treatment for Mycoplasma genitalium, Chlamydia trachomatis and bacterial vaginosis. PLoS One. 2020;15(7):e0236036. DOI: 10.1371/journal.pone.0236036Algburi A, Volski A, Chikindas ML. Natural antimicrobials subtilosin and lauramide arginine ethyl ester synergize with conventional antibiotics clindamycin and metronidazole against biofilms of Gardnerella vaginalis but not against biofilms of healthy vaginal lactobacilli. Pathog Dis. 2015;73(5):ftv018. DOI: 10.1093/femspd/ftv018Algburi A, Volski A, Chikindas ML. Natural antimicrobials subtilosin and lauramide arginine ethyl ester synergize with conventional antibiotics clindamycin and metronidazole against biofilms of Gardnerella vaginalis but not against biofilms of healthy vaginal lactobacilli. Pathog Dis. 2015;73(5):ftv018. DOI: 10.1093/femspd/ftv018Набока Ю.Л., Гудима И.А., Коган М.И., Черницкая М.Л. Микробный спектр мочи молодых здоровых женщин. Урология. 2010;(5):7-10. eLIBRARY ID: 15242297; EDN: MVOFTXNaboka Yu.L., Gudima I.A., Kogan M.I., Chernitskaya M.L. Bacterial spectrum of the urine in young healthy women. Urologiia. 2010;(5):7-10. (In Russian) eLIBRARY ID: 15242297; EDN: MVOFTXKogan MI, Naboka YL, Ibishev KS, Gudima IA, Naber KG. Human urine is not sterile — shift of paradigm. Urol Int. 2015;94(4):445-452. DOI: 10.1159/000369631Kogan MI, Naboka YL, Ibishev KS, Gudima IA, Naber KG. Human urine is not sterile — shift of paradigm. Urol Int. 2015;94(4):445-452. DOI: 10.1159/000369631Wolfe AJ, Brubaker L. “Sterile Urine” and the Presence of Bacteria. Eur Urol. 2015;68(2):173-174. DOI: 10.1016/j.eururo.2015.02.041Wolfe AJ, Brubaker L. “Sterile Urine” and the Presence of Bacteria. Eur Urol. 2015;68(2):173-174. DOI: 10.1016/j.eururo.2015.02.041Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, Fitzgerald M, Mueller ER, Schreckenberger P, Dong Q, Nelson DE, Brubaker L. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50(4):1376-1383. DOI: 10.1128/JCM.05852-11Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, Fitzgerald M, Mueller ER, Schreckenberger P, Dong Q, Nelson DE, Brubaker L. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50(4):1376-1383. DOI: 10.1128/JCM.05852-11Hooton TM, Roberts PL, Cox ME, Stapleton AE. Voided midstream urine culture and acute cystitis in premenopausal women. N Engl J Med. 2013;369(20):1883-1891 DOI: 10.1056/NEJMoa1302186Hooton TM, Roberts PL, Cox ME, Stapleton AE. Voided midstream urine culture and acute cystitis in premenopausal women. N Engl J Med. 2013;369(20):1883-1891 DOI: 10.1056/NEJMoa1302186Коган М.И., Набока Ю.Л., Гудима И.А., Воробьева Н.В. Асимптоматическая бактериурия у беременных — нормальное состояние мочи здоровой женщины. Урология. 2022;(6):5-8. DOI: 10.18565/urology.2022.6.5-8Kogan M.I., Naboka Y.L., Gudima I.A., Vorovb’eva N.V. Asymptomatic bacteriuria in pregnant women — the normal condition of healthy women urine. Urologiia. 2022;(6):5-8. (In Russian). DOI: 10.18565/urology.2022.6.5-8Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain inter-pretation. J Clin Microbiol. 1991;29(2):297-301. DOI: 10.1128/jcm.29.2.297-301.1991Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain inter-pretation. J Clin Microbiol. 1991;29(2):297-301. DOI: 10.1128/jcm.29.2.297-301.1991Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, Brubaker L, Gai X, Wolfe AJ, Schreckenberger PC. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol. 2014;52(3):871-876. DOI: 10.1128/JCM.02876-13Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, Brubaker L, Gai X, Wolfe AJ, Schreckenberger PC. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol. 2014;52(3):871-876. DOI: 10.1128/JCM.02876-13Guadamuro L, Dohrmann AB, Tebbe CC, Mayo B, Delgado S. Bacterial communities and metabolic activity of faecal cultures from equol producer and non-producer menopausal women under treatment with soy isoflavones. BMC Microbiol. 2017;17(1):93. DOI: 10.1186/s12866-017-1001-yGuadamuro L, Dohrmann AB, Tebbe CC, Mayo B, Delgado S. Bacterial communities and metabolic activity of faecal cultures from equol producer and non-producer menopausal women under treatment with soy isoflavones. BMC Microbiol. 2017;17(1):93. DOI: 10.1186/s12866-017-1001-yRomero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Bieda J, Chaemsaithong P, Miranda J, Chaiworapongsa T, Ravel J. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome. 2014;2:18. DOI: 10.1186/2049-2618-2-18Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Bieda J, Chaemsaithong P, Miranda J, Chaiworapongsa T, Ravel J. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome. 2014;2:18. DOI: 10.1186/2049-2618-2-18Callahan BJ, DiGiulio DB, Goltsman DSA, Sun CL, Costello EK, Jeganathan P, Biggio JR, Wong RJ, Druzin ML, Shaw GM, Stevenson DK, Holmes SP, Relman DA. Replication and refinement of a vaginal microbial signature of preterm birth in two racially distinct cohorts of US women. Proc Natl Acad Sci U S A. 2017;114(37):9966-9971. DOI: 10.1073/pnas.1705899114Callahan BJ, DiGiulio DB, Goltsman DSA, Sun CL, Costello EK, Jeganathan P, Biggio JR, Wong RJ, Druzin ML, Shaw GM, Stevenson DK, Holmes SP, Relman DA. Replication and refinement of a vaginal microbial signature of preterm birth in two racially distinct cohorts of US women. Proc Natl Acad Sci U S A. 2017;114(37):9966-9971. DOI: 10.1073/pnas.1705899114

The authors declare that there are no conflicts of interest present.