{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T17:20:09Z","timestamp":1790961609749,"version":"4.1.0"},"reference-count":113,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2024,6,30]],"date-time":"2024-06-30T00:00:00Z","timestamp":1719705600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Background\/Objectives: There are indications that the microbial composition of the maternal mucosal surfaces is associated with adverse events during pregnancy. The aim of this review is to investigate the link between vaginal microbiome alterations and gestational complication risk. Methods: This comprehensive literature review was performed using Medline and Scopus databases. The following search algorithm was used, \u201cPregnancy Complications\u201d [Mesh] AND (Vagin*), and after the literature screening, 44 studies were included in the final review. Results: The studies that were included investigated the association between vaginal microbial composition and preterm birth, miscarriage, preeclampsia, ectopic pregnancy, gestational diabetes mellitus, chorioamnionitis, and preterm premature rupture of membranes. In most of the studies, it was well established that increased microbial diversity is associated with these conditions. Also, the depletion of Lactobacillus species is linked to most of the gestational complications, while the increased relative abundance and especially Lactobacillus crispatus may exert a protective effect in favor of the pregnant woman. Several pathogenic taxa including Gardnerella, Prevotella, Sneathia, Bacterial Vaginosis-Associated Bacteria-2, Atopobium, and Megasphera seem to be correlated to higher maternal morbidity. Conclusions: Vaginal microbiome aberrations seem to have an association with pregnancy-related adverse events, but more high-quality homogenous studies are necessary to reliably verify this link.<\/jats:p>","DOI":"10.3390\/jcm13133875","type":"journal-article","created":{"date-parts":[[2024,7,1]],"date-time":"2024-07-01T09:06:07Z","timestamp":1719824767000},"page":"3875","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Vaginal Microbiome and Pregnancy Complications: A Review"],"prefix":"10.3390","volume":"13","author":[{"given":"Angeliki","family":"Gerede","sequence":"first","affiliation":[{"name":"Unit of Maternal-Fetal-Medicine, Department of Obstetrics and Gynecology, Medical School, Democritus University of Thrake, GR-68100 Alexandroupolis, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Konstantinos","family":"Nikolettos","sequence":"additional","affiliation":[{"name":"Unit of Maternal-Fetal-Medicine, Department of Obstetrics and Gynecology, Medical School, Democritus University of Thrake, GR-68100 Alexandroupolis, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3577-8782","authenticated-orcid":false,"given":"Eleftherios","family":"Vavoulidis","sequence":"additional","affiliation":[{"name":"Second Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, GR-54640 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chrysoula","family":"Margioula-Siarkou","sequence":"additional","affiliation":[{"name":"Second Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, GR-54640 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5564-0406","authenticated-orcid":false,"given":"Stamatios","family":"Petousis","sequence":"additional","affiliation":[{"name":"Second Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, GR-54640 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Giourga","sequence":"additional","affiliation":[{"name":"First Department of Obstetrics and Gynecology, Medical School, National and Kapodistrian University of Athens, GR-11528 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Panagiotis","family":"Fotinopoulos","sequence":"additional","affiliation":[{"name":"First Department of Obstetrics and Gynecology, Medical School, National and Kapodistrian University of Athens, GR-11528 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9821-1559","authenticated-orcid":false,"given":"Maria","family":"Salagianni","sequence":"additional","affiliation":[{"name":"First Department of Obstetrics and Gynecology, Medical School, National and Kapodistrian University of Athens, GR-11528 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sofoklis","family":"Stavros","sequence":"additional","affiliation":[{"name":"First Department of Obstetrics and Gynecology, Medical School, National and Kapodistrian University of Athens, GR-11528 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7144-2840","authenticated-orcid":false,"given":"Konstantinos","family":"Dinas","sequence":"additional","affiliation":[{"name":"Second Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, GR-54640 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikolaos","family":"Nikolettos","sequence":"additional","affiliation":[{"name":"Unit of Maternal-Fetal-Medicine, Department of Obstetrics and Gynecology, Medical School, Democritus University of Thrake, GR-68100 Alexandroupolis, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8899-3040","authenticated-orcid":false,"given":"Ekaterini","family":"Domali","sequence":"additional","affiliation":[{"name":"First Department of Obstetrics and Gynecology, Medical School, National and Kapodistrian University of Athens, GR-11528 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"533","DOI":"10.3111\/13696998.2015.1016229","article-title":"The prevalence of complications and healthcare costs during pregnancy","volume":"18","author":"Law","year":"2015","journal-title":"J. Med. Econ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"405.e1","DOI":"10.1016\/j.ajog.2018.07.002","article-title":"Contribution of hypertension to severe maternal morbidity","volume":"219","author":"Hitti","year":"2018","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1111\/ppe.12574","article-title":"Severe maternal morbidity surveillance: Monitoring pregnant women at high risk for prolonged hospitalisation and death","volume":"34","author":"Dzakpasu","year":"2020","journal-title":"Paediatr. Perinat. Epidemiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7189\/jogh.10.020429","article-title":"Applicability of the WHO maternal near-miss tool: A nationwide surveillance study in Suriname","volume":"10","author":"Verschueren","year":"2020","journal-title":"J. Glob. Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"548","DOI":"10.2471\/BLT.20.251371","article-title":"Maternal near-miss surveillance, Namibia","volume":"98","author":"Heemelaar","year":"2020","journal-title":"Bull. World Health Organ."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Galv\u00e3o, L.P.L., Alvim-Pereira, F., de Mendon\u00e7a, C.M.M., Menezes, F.E.F., G\u00f3is, K.A.D.N., Ribeiro, R.F., and Gurgel, R.Q. (2014). The prevalence of severe maternal morbidity and near miss and associated factors in Sergipe, Northeast Brazil. BMC Pregnancy Childbirth, 14.","DOI":"10.1186\/1471-2393-14-25"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/s12978-018-0527-2","article-title":"A global view of severe maternal morbidity: Moving beyond maternal mortality","volume":"15","author":"Geller","year":"2018","journal-title":"Reprod. Health"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e007903","DOI":"10.1136\/bmjopen-2015-007903","article-title":"Risk factors for maternal morbidity in Victoria, Australia: A population-based study","volume":"5","author":"Lindquist","year":"2015","journal-title":"BMJ Open"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Nik Hazlina, N.H., Norhayati, M.N., Shaiful Bahari, I., and Mohamed Kamil, H.R. (2022). The Prevalence and Risk Factors for Severe Maternal Morbidities: A Systematic Review and Meta-Analysis. Front. Med., 9.","DOI":"10.3389\/fmed.2022.861028"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e323","DOI":"10.1016\/S2214-109X(14)70227-X","article-title":"Global causes of maternal death: A WHO systematic analysis","volume":"2","author":"Say","year":"2014","journal-title":"Lancet Glob. Health"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"108642","DOI":"10.1016\/j.diabres.2020.108642","article-title":"Increasing prevalence of gestational diabetes mellitus when implementing the IADPSG criteria: A systematic review and meta-analysis","volume":"172","author":"Saeedi","year":"2021","journal-title":"Diabetes Res. Clin. Pract."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12884-021-03809-2","article-title":"Epidemiological trends of maternal hypertensive disorders of pregnancy at the global, regional, and national levels: A population-based study","volume":"21","author":"Wang","year":"2021","journal-title":"BMC Pregnancy Childbirth"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S46","DOI":"10.1016\/j.ijgo.2015.03.007","article-title":"Essential basic and emergency obstetric and newborn care: From education and training to service delivery and quality of care","volume":"130","author":"Otolorin","year":"2015","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_14","first-page":"297397","article-title":"Early prediction of preeclampsia","volume":"2014","author":"Poon","year":"2014","journal-title":"Obs. Gynecol. Int."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Stupak, A., and Kwa\u015bniewski, W. (2023). Evaluating Current Molecular Techniques and Evidence in Assessing Microbiome in Placenta-Related Health and Disorders in Pregnancy. Biomolecules, 13, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/37371491.","DOI":"10.3390\/biom13060911"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e12993","DOI":"10.1111\/aji.12993","article-title":"Microbiome in normal and pathological pregnancies: A literature overview","volume":"80","author":"Taddei","year":"2018","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Lv, L.-J., Li, S.-H., Li, S.-C., Zhong, Z.-C., Duan, H.-L., Tian, C., Li, H., He, W., Chen, M.C., and He, T. (2019). Early-Onset Preeclampsia Is Associated With Gut Microbial Alterations in Antepartum and Postpartum Women. Front. Cell Infect. Microbiol., 9, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/31297341.","DOI":"10.3389\/fcimb.2019.00224"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1007\/s00404-011-2012-9","article-title":"Simultaneous detection of periodontal pathogens in subgingival plaque and placenta of women with hypertension in pregnancy","volume":"285","author":"Swati","year":"2011","journal-title":"Arch. Gynecol. Obs."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1007\/s11908-999-0045-z","article-title":"Is there a protective role for vaginal flora?","volume":"1","author":"Sobel","year":"1999","journal-title":"Curr. Infect. Dis. Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1093\/humrep\/16.9.1809","article-title":"Origins of vaginal acidity: High d\/l lactate ratio is consistent with bacteria being the primary source","volume":"16","author":"Boskey","year":"2001","journal-title":"Hum. Reprod."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/j.1574-695X.2006.00124.x","article-title":"Selection and identification of anaerobic lactobacilli producing inhibitory compounds against vaginal pathogens","volume":"48","author":"Kaewsrichan","year":"2006","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.tim.2013.01.001","article-title":"The uses of race and ethnicity in human microbiome research","volume":"21","author":"Fortenberry","year":"2013","journal-title":"Trends Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T.-A., Coarfa, C., Raza, S., Rosenbaum, S., Van den Veyver, I., and Milosavljevic, A. (2012). A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE, 7, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/22719832.","DOI":"10.1371\/journal.pone.0036466"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1038\/s41591-019-0465-8","article-title":"Racioethnic diversity in the dynamics of the vaginal microbiome during pregnancy","volume":"25","author":"Serrano","year":"2019","journal-title":"Nat. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4680","DOI":"10.1073\/pnas.1002611107","article-title":"Vaginal microbiome of reproductive-age women","volume":"108","author":"Ravel","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9","DOI":"10.14715\/cmb\/2023.69.8.2","article-title":"Vaginal Microbiota Profile in first-trimester miscarriages cases","volume":"69","author":"Abdulla","year":"2023","journal-title":"Cell Mol. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1186\/s13643-016-0384-4","article-title":"Rayyan-a web and mobile app for systematic reviews","volume":"5","author":"Ouzzani","year":"2016","journal-title":"Syst. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1111\/1471-0528.15972","article-title":"The association between vaginal bacterial composition and miscarriage: A nested case-control study","volume":"127","author":"Bobdiwala","year":"2020","journal-title":"BJOG Int. J. Obstet. Gynaecol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.annepidem.2019.11.004","article-title":"Vaginal microbiome diversity and preterm birth: Results of a nested case-control study in Peru","volume":"41","author":"Blostein","year":"2020","journal-title":"Ann. Epidemiol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Brown, R.G., Marchesi, J.R., Lee, Y.S., Smith, A., Lehne, B., Kindinger, L.M., Terzidou, V., Holmes, E., Nicholson, J.K., and Bennett, P.R. (2018). Vaginal dysbiosis increases risk of preterm fetal membrane rupture, neonatal sepsis and is exacerbated by erythromycin. BMC Med., 16.","DOI":"10.1186\/s12916-017-0999-x"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2105","DOI":"10.1080\/01443615.2022.2033183","article-title":"Derangements of vaginal and cervical canal microbiota determined with real-time PCR in women with recurrent miscarriages","volume":"42","author":"Yurtcu","year":"2022","journal-title":"J. Obs. Gynaecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"9966","DOI":"10.1073\/pnas.1705899114","article-title":"Replication and refinement of a vaginal microbial signature of preterm birth in two racially distinct cohorts of US women","volume":"114","author":"Callahan","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"248","DOI":"10.4014\/jmb.1908.08016","article-title":"Vaginal Microbiota Profiles of Native Korean Women and Associations with High-Risk Pregnancy","volume":"30","author":"Chang","year":"2020","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1007\/s12020-018-1813-z","article-title":"Microbiome and its relation to gestational diabetes","volume":"64","author":"Cortez","year":"2018","journal-title":"Endocrine"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s42770-019-00118-x","article-title":"Defining microbial biomarkers for risk of preterm labor","volume":"51","author":"Dobbler","year":"2020","journal-title":"Braz. J. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Dunlop, A.L., Satten, G.A., Hu, Y.-J., Knight, A.K., Hill, C.C., Wright, M.L., Smith, A.K., Read, T.D., Pearce, B.D., and Corwin, E.J. (2021). Vaginal Microbiome Composition in Early Pregnancy and Risk of Spontaneous Preterm and Early Term Birth Among African American Women. Front. Cell Infect. Microbiol., 11, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/33996627.","DOI":"10.3389\/fcimb.2021.641005"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e23558","DOI":"10.1097\/MD.0000000000023558","article-title":"The alteration and potential relationship of vaginal microbiota and chemokines for unexplained recurrent spontaneous abortion","volume":"99","author":"Fan","year":"2020","journal-title":"Medicine"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Fettweis, J.M., Serrano, M.G., Sheth, N.U., Mayer, C.M., Glascock, A.L., Brooks, J.P., and Jefferson, K.K. (2012). Species-level classification of the vaginal microbiome. BMC Genom., 13.","DOI":"10.1186\/1471-2164-13-S8-S17"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Freitas, A.C., Bocking, A., Hill, J.E., Money, D.M., and Group, V.R. (2018). Increased richness and diversity of the vaginal microbiota and spontaneous preterm birth. Microbiome, 6, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/29954448.","DOI":"10.1186\/s40168-018-0502-8"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Gryaznova, M., Kozarenko, O., Smirnova, Y., Burakova, I., Syromyatnikov, M., Maslov, A., and Lebedeva, O. (2023). Cervical and Vaginal Microbiomes in Early Miscarriages and Ongoing Pregnancy with and without Dydrogesterone Usage. Int. J. Mol. Sci., 24, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/37762139.","DOI":"10.3390\/ijms241813836"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Gulavi, E., Mwendwa, F., Atandi, D.O., Okiro, P.O., Hall, M., Beiko, R.G., and Adam, R.D. (2022). Vaginal microbiota in women with spontaneous preterm labor versus those with term labor in Kenya: A case control study. BMC Microbiol., 22, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/36357861.","DOI":"10.1186\/s12866-022-02681-0"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"106458","DOI":"10.1016\/j.micpath.2023.106458","article-title":"Relationship between vaginal microbiota and chorioamnionitis: A prospective cohort study","volume":"186","author":"Guo","year":"2024","journal-title":"Microb. Pathog."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1177\/1933719113488838","article-title":"Diversity of the vaginal microbiome correlates with preterm birth","volume":"21","author":"Hyman","year":"2014","journal-title":"Reprod. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1080\/01443615.2021.1904851","article-title":"Alteration of vaginal microbiota in patients with recurrent miscarriage","volume":"42","author":"Jiao","year":"2021","journal-title":"J. Obs. Gynaecol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Kindinger, L.M., Bennett, P.R., Lee, Y.S., Marchesi, J.R., Smith, A., Cacciatore, S., Holmes, E., Nicholson, J.K., Teoh, T.G., and MacIntyre, D.A. (2017). The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome, 5, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/28103952.","DOI":"10.1186\/s40168-016-0223-9"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Kumar, M., Murugesan, S., Singh, P., Saadaoui, M., Elhag, D.A., Terranegra, A., Kabeer, B.S.A., Marr, A.K., Kino, T., and Brummaier, T. (2021). Vaginal Microbiota and Cytokine Levels Predict Preterm Delivery in Asian Women. Front. Cell. Infect. Microbiol., 11, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/33747983.","DOI":"10.3389\/fcimb.2021.639665"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4997","DOI":"10.1038\/s41467-023-40719-7","article-title":"Microdiversity of the vaginal microbiome is associated with preterm birth","volume":"14","author":"Liao","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"18249","DOI":"10.1038\/s41598-020-75534-3","article-title":"Severe preeclampsia is associated with a higher relative abundance of Prevotella bivia in the vaginal microbiota","volume":"10","author":"Lin","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e0046222","DOI":"10.1128\/spectrum.00462-22","article-title":"An Altered Microbiota in the Lower and Upper Female Reproductive Tract of Women with Recurrent Spontaneous Abortion","volume":"10","author":"Liu","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Ng, S., Chen, M., Kundu, S., Wang, X., Zhou, Z., Zheng, Z., Oing, W., Sheng, H., Wang, Y., and He, Y. (2021). Large-scale characterisation of the pregnancy vaginal microbiome and sialidase activity in a low-risk Chinese population. NPJ Biofilms Microbiomes, 7, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/34930922.","DOI":"10.1038\/s41522-021-00261-0"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e01261-20","DOI":"10.1128\/mSphere.01261-20","article-title":"Predominance of Atopobium vaginae at Midtrimester: A Potential Indicator of Preterm Birth Risk in a Nigerian Cohort","volume":"6","author":"Odogwu","year":"2021","journal-title":"mSphere"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"206.e1","DOI":"10.1016\/j.ajog.2020.08.034","article-title":"A specific bacterial DNA signature in the vagina of Australian women in midpregnancy predicts high risk of spontaneous preterm birth (the Predict1000 study)","volume":"224","author":"Payne","year":"2021","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"5136","DOI":"10.1038\/srep05136","article-title":"Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery","volume":"4","author":"Petricevic","year":"2014","journal-title":"Sci. Rep."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1016\/j.rbmo.2022.06.008","article-title":"Female reproductive tract microbiota and recurrent pregnancy loss: A nested case-control study","volume":"45","author":"Holster","year":"2022","journal-title":"Reprod. Biomed. Online"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Ruan, X.-F., Zhang, Y.-X., Chen, S., Liu, X.-R., Zhu, F.-F., Huang, Y.-X., Liu, X.-J., Luo, S.-P., Deng, G.-P., and Gao, J. (2021). Non-Lactobacillus-Dominated Vaginal Microbiota Is Associated With a Tubal Pregnancy in Symptomatic Chinese Women in the Early Stage of Pregnancy: A Nested Case-Control Study. Front. Cell. Infect. Microbiol., 11, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/34307190.","DOI":"10.3389\/fcimb.2021.659505"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1111\/jog.15086","article-title":"Is there an association between the vaginal microbiome and first trimester miscarriage? A prospective observational study","volume":"48","author":"Shahid","year":"2021","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1055\/s-0036-1581057","article-title":"The Gestational Vaginal Microbiome and Spontaneous Preterm Birth among Nulliparous African American Women","volume":"33","author":"Shin","year":"2016","journal-title":"Am. J. Perinatol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"356.e1","DOI":"10.1016\/j.ajog.2017.05.030","article-title":"Early pregnancy vaginal microbiome trends and preterm birth","volume":"217","author":"Stout","year":"2017","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1111\/aogs.14410","article-title":"The association between vaginal microbiota disorders and early missed abortion: A prospective study","volume":"101","author":"Sun","year":"2022","journal-title":"Acta Obs. Gynecol. Scand."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/1471-0528.15299","article-title":"Vaginal microbiome in early pregnancy and subsequent risk of spontaneous preterm birth: A case\u2013control study","volume":"126","author":"Tabatabaei","year":"2018","journal-title":"BJOG Int. J. Obstet. Amp; Gynaecol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1614","DOI":"10.1136\/gutjnl-2018-315988","article-title":"Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus","volume":"67","author":"Wang","year":"2018","journal-title":"Gut"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"189.e1","DOI":"10.1016\/j.ajog.2018.04.048","article-title":"The vaginal eukaryotic DNA virome and preterm birth","volume":"219","author":"Wylie","year":"2018","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1007\/s12275-023-00039-3","article-title":"Vaginal Microbiome Dysbiosis is Associated with the Different Cervical Disease Status","volume":"61","author":"Ma","year":"2023","journal-title":"J. Microbiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"860","DOI":"10.1093\/cid\/ciu966","article-title":"High Atopobium vaginae and Gardnerella vaginalis Vaginal Loads Are Associated With Preterm Birth","volume":"60","author":"Bretelle","year":"2015","journal-title":"Clin. Infect. Dis."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1038\/s41467-019-09285-9","article-title":"Cervicovaginal microbiota and local immune response modulate the risk of spontaneous preterm delivery","volume":"10","author":"Elovitz","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1016\/j.fertnstert.2007.01.035","article-title":"First trimester bacterial vaginosis, individual microorganism levels, and risk of second trimester pregnancy loss among urban women","volume":"88","author":"Nelson","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"S29","DOI":"10.1016\/j.ajog.2015.08.040","article-title":"Acute chorioamnionitis and funisitis: Definition, pathologic features, and clinical significance","volume":"213","author":"Kim","year":"2015","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Stafford, G.P., Parker, J.L., Amabebe, E., Kistler, J., Reynolds, S., Stern, V., Paley, M., and Anumba, D.O.C. (2017). Spontaneous Preterm Birth Is Associated with Differential Expression of Vaginal Metabolites by Lactobacilli-Dominated Microflora. Front. Physiol., 8, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/28878691.","DOI":"10.3389\/fphys.2017.00615"},{"key":"ref_69","first-page":"3307","article-title":"Alteration of vaginal microbiota in patients with unexplained recurrent miscarriage","volume":"17","author":"Zhang","year":"2019","journal-title":"Exp. Ther. Med."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1007\/s10096-013-1847-3","article-title":"Characterization of the vaginal fungal flora in pregnant diabetic women by 18S rRNA sequencing","volume":"32","author":"Zheng","year":"2013","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1016\/S0140-6736(23)00878-4","article-title":"National, regional, and global estimates of preterm birth in 2020, with trends from 2010: A systematic analysis","volume":"402","author":"Ohuma","year":"2023","journal-title":"Lancet"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e1398","DOI":"10.7717\/peerj.1398","article-title":"Persistent microbial dysbiosis in preterm premature rupture of membranes from onset until delivery","volume":"3","author":"Baldwin","year":"2015","journal-title":"PeerJ"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Aldunate, M., Srbinovski, D., Hearps, A.C., Latham, C.F., Ramsland, P.A., Gugasyan, R., Cone, R.A., and Tachedjian, G. (2015). Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front. Physiol., 6.","DOI":"10.3389\/fphys.2015.00164"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1086\/588661","article-title":"Molecular Quantification of Gardnerella vaginalis and Atopobium vaginae Loads to Predict Bacterial Vaginosis","volume":"47","author":"Menard","year":"2008","journal-title":"Clin. Infect. Dis."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1658","DOI":"10.1016\/S0140-6736(21)00682-6","article-title":"Miscarriage matters: The epidemiological, physical, psychological, and economic costs of early pregnancy loss","volume":"397","author":"Quenby","year":"2021","journal-title":"Lancet"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Larsen, E.C., Christiansen, O.B., Kolte, A.M., and Macklon, N. (2013). New insights into mechanisms behind miscarriage. BMC Med., 11, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/23803387.","DOI":"10.1186\/1741-7015-11-154"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.bpobgyn.2020.09.002","article-title":"Sporadic pregnancy loss and recurrent miscarriage","volume":"69","author":"Devall","year":"2020","journal-title":"Best. Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2682","DOI":"10.1007\/s10995-015-1790-2","article-title":"First Trimester Levels of BV-Associated Bacteria and Risk of Miscarriage Among Women Early in Pregnancy","volume":"19","author":"Nelson","year":"2015","journal-title":"Matern. Child. Health J."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Ponzo, V., Fedele, D., Goitre, I., Leone, F., Lezo, A., Monzeglio, C., Finocchiaro, C., Ghigo, E., and Bo, S. (2019). Diet-Gut Microbiota Interactions and Gestational Diabetes Mellitus (GDM). Nutrients, 11, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/30717458.","DOI":"10.3390\/nu11020330"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Hasain, Z., Mokhtar, N.M., Kamaruddin, N.A., Mohamed Ismail, N.A., Razalli, N.H., Gnanou, J.V., and Raja Ali, R.A. (2020). Gut Microbiota and Gestational Diabetes Mellitus: A Review of Host-Gut Microbiota Interactions and Their Therapeutic Potential. Front. Cell Infect. Microbiol., 10, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/32500037.","DOI":"10.3389\/fcimb.2020.00188"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1097\/AOG.0b013e3181a45b25","article-title":"Hypertensive Disorders and Severe Obstetric Morbidity in the United States","volume":"113","author":"Kuklina","year":"2009","journal-title":"Obstet. Gynecol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ejogrb.2013.05.005","article-title":"Global and regional estimates of preeclampsia and eclampsia: A systematic review","volume":"170","author":"Abalos","year":"2013","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3233\/NPM-17155","article-title":"Association between clinical chorioamnionitis and histological funisitis at term","volume":"12","author":"Suzuki","year":"2019","journal-title":"J. Neonatal Perinat. Med."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s10140-021-01974-7","article-title":"Ectopic pregnancy: A resident\u2019s guide to imaging findings and diagnostic pitfalls","volume":"29","author":"Houser","year":"2021","journal-title":"Emerg. Radiol."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Nunes, V., Cross, J., Speich, J.E., Morgan, D.R., Strauss 3rd, J.F., and Ramus, R.M. (2016). Fetal membrane imaging and the prediction of preterm birth: A systematic review, current issues, and future directions. BMC Pregnancy Childbirth, 16, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/27938341.","DOI":"10.1186\/s12884-016-1176-5"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Yan, C., Hong, F., Xin, G., Duan, S., Deng, X., and Xu, Y. (2022). Alterations in the vaginal microbiota of patients with preterm premature rupture of membranes. Front. Cell Infect. Microbiol., 12.","DOI":"10.3389\/fcimb.2022.858732"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"132ra52","DOI":"10.1126\/scitranslmed.3003605","article-title":"Temporal Dynamics of the Human Vaginal Microbiota","volume":"4","author":"Gajer","year":"2012","journal-title":"Sci. Transl. Med."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Amabebe, E., and Anumba, D.O.C. (2018). The Vaginal Microenvironment: The Physiologic Role of Lactobacilli. Front. Med., 5, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/29951482.","DOI":"10.3389\/fmed.2018.00181"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1097\/AOG.0000000000001932","article-title":"Vaginal Microbiome and Its Relationship to Behavior, Sexual Health, and Sexually Transmitted Diseases","volume":"129","author":"Lewis","year":"2017","journal-title":"Obstet. Gynecol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"5016810","DOI":"10.1155\/2019\/5016810","article-title":"Emergence of Vulvovaginal Candidiasis among Lebanese Pregnant Women: Prevalence, Risk Factors, and Species Distribution","volume":"2019","author":"Ghaddar","year":"2019","journal-title":"Infect. Dis. Obstet. Gynecol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"89","DOI":"10.17305\/bjbms.2010.2744","article-title":"Candida Albicans and non-albicans species as etiological agent of vaginitis in pregnant and nonpregnant women","volume":"10","year":"2010","journal-title":"Bosn. J. Basic. Med. Sci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.mycmed.2014.10.021","article-title":"Species spectrum and antifungal susceptibility profile of vaginal isolates of Candida in Kuwait","volume":"25","author":"Alfouzan","year":"2015","journal-title":"J. Mycol. Med."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/s11908-015-0462-0","article-title":"Vulvovaginal candidiasis in pregnancy","volume":"17","author":"Aguin","year":"2015","journal-title":"Curr. Infect. Dis. Rep."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Dias, S., Pheiffer, C., and Adam, S. (2023). The Maternal Microbiome and Gestational Diabetes Mellitus: Cause and Effect. Microorganisms, 11, Available online: https:\/\/www.mdpi.com\/2076-2607\/11\/9\/2217\/htm.","DOI":"10.3390\/microorganisms11092217"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Agnoletti, D., Piani, F., Cicero, A.F.G., and Borghi, C. (2022). The Gut Microbiota and Vascular Aging: A State-of-the-Art and Systematic Review of the Literature. J. Clin. Med., 11, Available online: https:\/\/www.mdpi.com\/2077-0383\/11\/12\/3557\/htm.","DOI":"10.3390\/jcm11123557"},{"key":"ref_96","first-page":"412","article-title":"Tumor necrosis factor-alpha, interleukin-6, and interleukin-10 levels are altered in preeclampsia: A systematic review and meta-analysis","volume":"70","author":"Lau","year":"2013","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"359","DOI":"10.12816\/0003256","article-title":"Recurrent Urinary Tract Infections Management in Women: A review","volume":"13","year":"2013","journal-title":"Sultan Qaboos Univ. Med. J."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1007\/s00404-013-2929-2","article-title":"Ectopic pregnancy: A review","volume":"288","author":"Rana","year":"2013","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_99","first-page":"844","article-title":"Risk factors for ectopic pregnancy: A case\u2013control study","volume":"19","author":"Moini","year":"2014","journal-title":"J. Res. Med. Sci."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"142.e1","DOI":"10.1016\/j.ajog.2010.08.061","article-title":"High sialidase levels increase preterm birth risk among women who are bacterial vaginosis-positive in early gestation","volume":"204","author":"Cauci","year":"2011","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.ajog.2018.11.1089","article-title":"Ecological dynamics of the vaginal microbiome in relation to health and disease","volume":"220","author":"Greenbaum","year":"2019","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.ejogrb.2019.12.005","article-title":"Female genital tract microbiota affecting the risk of preterm birth: What do we know so far? A review","volume":"245","author":"Tsonis","year":"2020","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"e00781-16","DOI":"10.1128\/mBio.00781-16","article-title":"Bacterial Hyaluronidase Promotes Ascending GBS Infection and Preterm Birth","volume":"7","author":"Vornhagen","year":"2016","journal-title":"mBio"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1067\/mob.2002.127454","article-title":"Vaginal hydrolytic enzymes, immunoglobulin A against Gardnerella vaginalis toxin, and risk of early preterm birth among women in preterm labor with bacterial vaginosis or intermediate flora","volume":"187","author":"Cauci","year":"2002","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_105","first-page":"27799","article-title":"Changes in vaginal microbiota following antimicrobial and probiotic therapy","volume":"26","author":"Macklaim","year":"2015","journal-title":"Microb. Ecol. Health Dis."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1097\/LGT.0b013e31829156ec","article-title":"Effects of Probiotics on the Recurrence of Bacterial Vaginosis","volume":"18","author":"Homayouni","year":"2014","journal-title":"J. Low. Genit. Tract. Dis."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/S1701-2163(16)34218-9","article-title":"Probiotic Safety in Pregnancy: A Systematic Review and Meta-analysis of Randomized Controlled Trials of Lactobacillus, Bifidobacterium, and Saccharomyces spp","volume":"31","author":"Dugoua","year":"2009","journal-title":"J. Obstet. Gynaecol. Can."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Zhu, B., Tao, Z., Edupuganti, L., Serrano, M.G., and Buck, G.A. (2022). Roles of the Microbiota of the Female Reproductive Tract in Gynecological and Reproductive Health. Microbiol. Mol. Biol. Rev., 86, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/36222685.","DOI":"10.1128\/mmbr.00181-21"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1038\/s41570-023-00463-4","article-title":"Metals to combat antimicrobial resistance","volume":"7","author":"Frei","year":"2023","journal-title":"Nat. Rev. Chem."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"2647","DOI":"10.1080\/17441692.2021.2003839","article-title":"Community engagement: The key to tackling Antimicrobial Resistance (AMR) across a One Health context?","volume":"17","author":"Mitchell","year":"2022","journal-title":"Glob. Public Health"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/nrd.2017.23","article-title":"Different drugs for bad bugs: Antivirulence strategies in the age of antibiotic resistance","volume":"16","author":"DIckey","year":"2017","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1057\/s41599-020-0478-4","article-title":"Phage therapy as a potential solution in the fight against AMR: Obstacles and possible futures","volume":"6","author":"Brives","year":"2020","journal-title":"Palgrave Commun."},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Salam, M.A., Al-Amin, M.Y., Salam, M.T., Pawar, J.S., Akhter, N., Rabaan, A.A., and Alqumber, M.A.A. (2023). Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. 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