The Association Between Vaginal Microbiota Dysbiosis, Bacterial Vaginosis, and Aerobic Vaginitis, and Adverse Pregnancy Outcomes of Women Living in Sub-Saharan Africa: A Systematic Review

Naomi C A Juliana, Meghan J M Suiters, Salwan Al-Nasiry, Servaas A Morré, Remco P H Peters, Elena Ambrosino, Naomi C A Juliana, Meghan J M Suiters, Salwan Al-Nasiry, Servaas A Morré, Remco P H Peters, Elena Ambrosino

Abstract

Background: Previous studies have described the association between dysbiosis of the vaginal microbiota (VMB) and related dysbiotic conditions, such as bacterial vaginosis (BV) and aerobic vaginitis (AV), and various adverse pregnancy outcomes. There is limited overview of this association from countries in sub-Saharan Africa (SSA), which bear a disproportionally high burden of both vaginal dysbiotic conditions and adverse pregnancy outcomes. This systematic review assesses the evidence on the association between VMB dysbiosis, BV, and AV, and late adverse pregnancy outcomes in women living in SSA. Methods: The Preferred Reporting Items for Systematic Review and Meta-Analysis Statement (PRISMA) guidelines were followed. Three databases [PubMed, Embase (Ovid), and Cochrane] were used to retrieve observational and intervention studies conducted in SSA that associated VMB dysbiosis, BV, or AV and preterm birth/labor/delivery, preterm rupture of membranes (PROM), low birthweight, small for gestational age, intrauterine growth restriction, intrauterine infection, intrauterine (fetal) death, stillbirth, perinatal death, or perinatal mortality. Results: Twelve studies out of 693 search records from five SSA countries were included. One study identified a positive association between VMB dysbiosis and low birthweight. Despite considerable differences in study design and outcome reporting, studies reported an association between BV and preterm birth (7/9), low birthweight (2/6), PROM (2/4), intrauterine infections (1/1), and small for gestational age (1/1). None of the retrieved studies found an association between BV and pregnancy loss (5/5) or intrauterine growth retardation (1/1). At least two studies support the association between BV and PROM, low birthweight, and preterm birth in Nigerian pregnant women. No reports were identified investigating the association between AV and late adverse pregnancy outcomes in SSA. Conclusion: Two of the included studies from SSA support the association between BV and PROM. The remaining studies show discrepancies in supporting an association between BV and preterm birth or low birthweight. None of the studies found an association between BV and pregnancy loss. As for the role of VMB dysbiosis, BV, and AV during pregnancy among SSA women, additional research is needed. These results provide useful evidence for prevention efforts to decrease vaginal dysbiosis and its contribution to adverse pregnancy outcomes in SSA.

Keywords: anaerobic vaginitis (AV); bacterial vaginosis (BV); microbiome; pregnancy outcomes; sub-saharan africa; systematic review; vaginal dysbiosis; vaginal microbiota (VMB).

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2020 Juliana, Suiters, Al-Nasiry, Morré, Peters and Ambrosino.

Figures

Figure 1
Figure 1
PRISMA based Flow diagram displaying the study selection (69).
Figure 2
Figure 2
Map of Africa depicting sub-Saharan countries (in gray) where the included studies were conducted (in red) and countries not considered within the sub-Saharan region (spotted). Map created with Mapchart (83).

References

    1. Mombo-Ngoma G, Mackanga JR, González R, Ouedraogo S, Kakolwa MA, Manego RZ, et al. . Young adolescent girls are at high risk for adverse pregnancy outcomes in sub-Saharan Africa: an observational multicountry study. BMJ Open. (2016) 6:e011783. 10.1136/bmjopen-2016-011783
    1. Kinney MV, Kerber KJ, Black RE, Cohen B, Nkrumah F, Coovadia H, et al. . Sub-Saharan Africa's mothers, newborns, and children: where and why do they die? PLoS Med. (2010) 7:e1000294. 10.1371/journal.pmed.1000294
    1. WHO WHO | Maternal and Perinatal Health. (2020). Available online at: (accessed March 11, 2020).
    1. Ramharter M, Grobusch MP, Kießling G, Adegnika AA, Möller U, Agnandji STM, et al. . Clinical and parasitological characteristics of puerperal malaria. J Infect Dis. (2005) 191:1005–9. 10.1086/427781
    1. Adegnika AA, Verweij JJ, Agnandji ST, Chai SK, Breitling LP, Ramharter M, et al. . Microscopic and sub-microscopic plasmodium falciparum infection, but not inflammation caused by infection, is associated with low birth weight. Am J Trop Med Hyg. (2006) 75:798–803. 10.4269/ajtmh.2006.75.798
    1. Morikawa E, Mudau M, Olivier D, De Vos L, Joseph Davey D, Price C, et al. . Acceptability and feasibility of integrating point-of-care diagnostic testing of sexually transmitted infections into a south African antenatal care program for hiv-infected pregnant women. Infect Dis Obstet Gynecol. (2018) 2018:3946862. :10.1155/2018/3946862
    1. Friberg IK, Kinney MV, Lawn JE, Kerber KJ, Odubanjo MO, Bergh A-M, et al. . Sub-saharan africa's mothers, newborns, and children: how many lives could be saved with targeted health interventions? PLoS Med. (2010) 7:e1000295. 10.1371/journal.pmed.1000295
    1. Guise JM, Mahon SM, Aickin M, Helfand M, Peipert JF, Westhoff C. Screening for bacterial vaginosis in pregnancy. Am J Prev Med. (2001) 20(Suppl. 3):63–72. 10.1016/s0749-3797(01)00257-4
    1. Kekki M, Kurki T, Kotomäki T, Sintonen H, Paavonen J. Cost-effectiveness of screening and treatment for bacterial vaginosis in early pregnancy among women at low risk for preterm birth. Acta Obstet Gynecol Scand. (2004) 83:27–36. 10.1111/j.1600-0412.2004.00262.x
    1. van de Wijgert JHHM, Jespers V. The global health impact of vaginal dysbiosis. Res Microbiol. (2017) 168:859–54. 10.1016/j.resmic.2017.02.003
    1. Marchesi JR, Ravel J. The vocabulary of microbiome research: a proposal. Microbiome. (2015) 3:31. 10.1186/s40168-015-0094-5
    1. Bayigga L, Kateete DP, Anderson DJ, Sekikubo M, Nakanjako D. Diversity of vaginal microbiota in sub-Saharan Africa and its effects on HIV transmission and prevention. Am J Obstet Gynecol. (2019) 220:155–66. 10.1016/j.ajog.2018.10.014
    1. Selle K, Klaenhammer TR. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev. (2013) 37:915–35. 10.1111/1574-6976.12021
    1. Al-Nasiry S, Ambrosino E, Schlaepfer M, Morré SA, Wieten L, Voncken JW, et al. . The Interplay between reproductive tract microbiota and immunological system in human reproduction. Front Immunol. (2020) 11:378. 10.3389/fimmu.2020.00378
    1. Borgdorff H, van der Veer C, van Houdt R, Alberts CJ, de Vries HJ, Bruisten SM, et al. . The association between ethnicity and vaginal microbiota composition in Amsterdam, the Netherlands. PLoS ONE. (2017) 12:e0181135. 10.1371/journal.pone.0181135
    1. Bilardi J, Walker S, McNair R, Mooney-Somers J, Temple-Smith M, Bellhouse C, et al. . Women's management of recurrent bacterial vaginosis and experiences of clinical care: a qualitative study. PLoS ONE. (2016) 11:e0151794. 10.1371/journal.pone.0151794
    1. Meis PJ, Goldenberg RL, Mercer B, Moawad A, Das A, McNellis D, et al. . The preterm prediction study: Significance of vaginal infections. Am J Obstet Gynecol. (1995) 173:1231–5. 10.1016/0002-9378(95)91360-2
    1. Kenyon C, Colebunders R, Crucitti T. The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol. (2013) 209:505–23. 10.1016/j.ajog.2013.05.006
    1. Onderdonk AB, Delaney ML, Fichorova RN. The human microbiome during bacterial vaginosis. Clin Microbiol Rev. (2016) 29:223–38. 10.1128/CMR.00075-15
    1. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al. . Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med. (1995) 333:1737–42. 10.1056/NEJM199512283332604
    1. Flynn CA, Helwig AL, Meurer LN. Bacterial vaginosis in pregnancy and the risk of prematurity a meta-analysis. J Fam Pract. (1999) 48:885–92.
    1. Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P. Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol. (2003) 189:139–47. 10.1067/mob.2003.339
    1. McGregor JA, French JI. Bacterial vaginosis in pregnancy. Obstet Gynecol Surv. (2000) 55:1–19. 10.1097/00006254-200005001-00001
    1. Donders GGG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG. (2002) 109:34–43. 10.1111/j.1471-0528.2002.00432.x
    1. Dermendjiev T, Pehlivanov B, Hadjieva K, Stanev S. Epidemiological, clinical and microbiological findings in women with aerobic vaginitis. Akush Ginekol. (2015) 54:4–8.
    1. Tansarli GS, Kostaras EK, Athanasiou S, Falagas ME. Prevalence and treatment of aerobic vaginitis among non-pregnant women: evaluation of the evidence for an underestimated clinical entity. Eur J Clin Microbiol Infect Dis. (2013) 32:977–84. 10.1007/s10096-013-1846-4
    1. Rumyantseva TA, Bellen G, Savochkina YA, Guschin AE, Donders GGG. Diagnosis of aerobic vaginitis by quantitative real-time PCR. Arch Gynecol Obstet. (2016) 294:109–14. 10.1007/s00404-015-4007-4
    1. Fan A, Yue Y, Geng N, Zhang H, Wang Y, Xue F. Aerobic vaginitis and mixed infections: comparison of clinical and laboratory findings. Arch Gynecol Obstet. (2013) 287:329–35. 10.1007/s00404-012-2571-4
    1. Donders GGG, Bellen G, Grinceviciene S, Ruban K, Vieira-Baptista P. Aerobic vaginitis: no longer a stranger. Res Microbiol. (2017) 168:845–58. 10.1016/j.resmic.2017.04.004
    1. Donders GGG, Bellen G, Rezeberga D. Aerobic vaginitis in pregnancy. BJOG. (2011) 118:1163–70. 10.1111/j.1471-0528.2011.03020.x
    1. Donders GG, Van Calsteren K, Bellen G, Reybrouck R, Van Den Bosch T, Riphagen I, et al. . Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG. (2009) 116:1315–24. 10.1111/j.1471-0528.2009.02237.x
    1. Hassan MF, Rund NMA, El-Tohamy O, Moussa M, Ali YZ, Moussa N, et al. . Does aerobic vaginitis have adverse pregnancy outcomes? prospective observational study. Infect Dis Obstet Gynecol. (2020) 2020:5842150. 10.1155/2020/5842150
    1. Freitas AC, Chaban B, Bocking A, Rocco M, Yang S, Hill JE, et al. . The vaginal microbiome of pregnant women is less rich and diverse, with lower prevalence of Mollicutes, compared to non-pregnant women. Sci Rep. (2017) 7:9212. 10.1038/s41598-017-07790-9
    1. Parry S, Strauss JF. Premature rupture of the fetal membranes. N Engl J Med. (1998) 338:663–70. 10.1056/NEJM199803053381006
    1. Larsson P-G, Platz-Christensen J-J, Dalaker K, Eriksson K, Fåhraeus L, Irminger K, et al. . Treatment with 2% clindamycin vaginal cream prior to first trimester surgical abortion to reduce signs of postoperative infection: a prospective, double-blinded, placebo-controlled, multicenter study. Acta Obstet Gynecol Scand. (2000) 79:390–6. 10.1080/j.1600-0412.2000.079005390.x
    1. Larsson PG, Platz-Christensen JJ, Thejls H, Forsum U, Påhlson C. Incidence of pelvic inflammatory disease after first-trimester legal abortion in women with bacterial vaginosis after treatment with metronidazole: a double-blind, randomized study. Am J Obstet Gynecol. (1992) 166:100–3. 10.1016/0002-9378(92)91838-2
    1. Donders GG, Van Bulck B, Caudron J, Londers L, Vereecken A, Spitz B. Relationship of bacterial vaginosis and mycoplasmas to the risk of spontaneous abortion. Am J Obstet Gynecol. (2000) 183:431–7. 10.1067/mob.2000.105738
    1. Ralph SG, Rutherford AJ, Wilson JD. Influence of bacterial vaginosis on conception and miscarriage in the first trimester: cohort study. Br Med J. (1999) 319:220–3. 10.1136/bmj.319.7204.220
    1. Llahí-Camp JM, Rai R, Ison C, Regan L, Taylor-Robinson D. Association of bacterial vaginosis with a history of second trimester miscarriage. Hum Reprod. (1996) 11:1575–8. 10.1093/oxfordjournals.humrep.a019440
    1. Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J. Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ. (1994) 308:295. 10.1136/bmj.308.6924.295
    1. Gibbs RS. Chorioamnionitis and bacterial vaginosis. Am J Obstet Gynecol. (1993) 169:460–2. 10.1016/0002-9378(93)90341-F
    1. Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA. A case–control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med. (1988) 319:972–8. 10.1056/NEJM198810133191503
    1. Stout MJ, Zhou Y, Wylie KM, Tarr PI, Macones GA, Tuuli MG. Early pregnancy vaginal microbiome trends and preterm birth. Am J Obstet Gynecol. (2017) 217:356.e1–356.e18. 10.1016/j.ajog.2017.05.030
    1. van de Wijgert JHHM. The vaginal microbiome and sexually transmitted infections are interlinked: consequences for treatment and prevention. PLoS Med. (2017) 14:e1002478. 10.1371/journal.pmed.1002478
    1. van de Wijgert JHHM, Verwijs MC, Gill AC, Borgdorff H, van der Veer C, Mayaud P. Pathobionts in the vaginal microbiota: individual participant data meta-analysis of three sequencing studies. Front Cell Infect Microbiol. (2020) 10:129. 10.3389/fcimb.2020.00129
    1. Son KA, Kim M, Kim YM, Kim SH, Choi SJ, Oh SY, et al. . Prevalence of vaginal microorganisms among pregnant women according to trimester and association with preterm birth. Obstet Gynecol Sci. (2018) 61:38–47. 10.5468/ogs.2018.61.1.38
    1. Kindinger LM, Bennett PR, Lee YS, Marchesi JR, Smith A, Cacciatore S, et al. . The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome. (2017) 5:6. 10.1186/s40168-016-0223-9
    1. Koedooder R, Mackens S, Budding A, Fares D, Blockeel C, Laven J, et al. . Identification and evaluation of the microbiome in the female and male reproductive tracts. Hum Reprod. (2019) 25:298–325. 10.1093/humupd/dmy048
    1. Kong Y, Liu Z, Shang Q, Gao Y, Li X, Zheng C, et al. . The disordered vaginal microbiota is a potential indicator for a higher failure of in vitro fertilization. Front Med. (2020) 7:217. 10.3389/fmed.2020.00217
    1. Singer M, Borg M, Ouburg S, Morré SA. The relation of the vaginal microbiota to early pregnancy development during in vitro fertilization treatment—a meta-analysis. J Gynecol Obstet Hum Reprod. (2019) 48:223–29. 10.1016/j.jogoh.2019.01.007
    1. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, et al. . Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci USA. (2015) 112:11060–5. 10.1073/pnas.1502875112
    1. Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Bieda J, et al. . 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. 10.1186/2049-2618-2-18
    1. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, et al. . Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. (2011) 108:4680–7. 10.1073/pnas.1002611107
    1. Abdool Karim SS, Baxter C, Passmore JS, McKinnon LR, Williams BL. The genital tract and rectal microbiomes: their role in HIV susceptibility and prevention in women. J Int AIDS Soc. (2019) 22:e25300. 10.1002/jia2.25300
    1. Serrano MG, Parikh HI, Brooks JP, Edwards DJ, Arodz TJ, Edupuganti L, et al. . Racioethnic diversity in the dynamics of the vaginal microbiome during pregnancy. Nat Med. (2019) 25:1001–11. 10.1038/s41591-019-0465-8
    1. Simhan HN, Bodnar LM, Krohn MA. Paternal race and bacterial vaginosis during the first trimester of pregnancy. Am J Obstet Gynecol. (2008) 198:196.e1–4. 10.1016/j.ajog.2007.09.006
    1. Moher D, Liberati A, Tetzlaff J, Altman D, The PRISMA group preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. (2009) 6:e1000097 10.1371/journal.pmed1000097
    1. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. (1991) 29:297–301.
    1. Spiegel CA, Amsel R, Holmes KK. Diagnosis of bacterial vaginosis by direct gram stain of vaginal fluid. J Clin Microbiol. (1983) 18:170–7. 10.1128/JCM.18.1.170-177.1983
    1. Amsel R, Totten PA, Spiegel CA, Chen KCS, Eschenbach D, Holmes KK. Nonspecific vaginitis. diagnostic criteria and microbial and epidemiologic associations. Am J Med. (1983) 74:14–22. 10.1016/0002-9343(83)91137-3
    1. Tempera G, Furneri PM. Management of aerobic vaginitis. Gynecol Obstet Invest. (2010) 70:244–9. 10.1159/000314013
    1. World Bank Sub-Saharan Africa | Data. (2020). Available online at: (accessed January 10, 2020).
    1. Altman D. Practical Statistics for Medical Research. London: Chapman and Hall; (1991).
    1. Pagano M, Cole KG. Principles of Biostatistics. 2nd Edn Belmont, CA: Brooks/Cole; (2000).
    1. Sheskin DJ. Handbook of Parametric and Nonparametric Statistical Procedures. 3rd Edn Boca Raton, FL: Chapman & Hall /CRC; (2004).
    1. Aromataris E, Munn Z. (Editors). Joanna Briggs Institute Reviewer's Manual. (2017). Available online at: (accessed January 10, 2020).
    1. Melo G, Dutra KL, Rodrigues Filho R, Ortega AOL, Porporatti AL, Dick B, et al. . Association between psychotropic medications and presence of sleep bruxism: a systematic review. J Oral Rehabil. (2018) 45:545–54. 10.1111/joor.12633
    1. Goplen CM, Verbeek W, Kang SH, Jones CA, Voaklander DC, Churchill TA, et al. . Preoperative opioid use is associated with worse patient outcomes after total joint arthroplasty: a systematic review and meta-analysis. BMC Musculoskelet Disord. (2019) 20:234. 10.1186/s12891-019-2619-8
    1. Mwatelah R, McKinnon LR, Baxter C, Abdool Karim Q, Abdool Karim SS. Mechanisms of sexually transmitted infection-induced inflammation in women: implications for HIV risk. J Int AIDS Soc. (2019) 22:e25346. 10.1002/jia2.25346
    1. Nakubulwa S, Kaye DK, Bwanga F, Tumwesigye NM, Mirembe FM. Genital infections and risk of premature rupture of membranes in Mulago Hospital, Uganda: a case control study. BMC Res Notes. (2015) 8:573. 10.1186/s13104-015-1545-6
    1. Warr AJ, Pintye J, Kinuthia J, Drake AL, Unger JA, McClelland RS, et al. . Sexually transmitted infections during pregnancy and subsequent risk of stillbirth and infant mortality in Kenya: a prospective study. Sex Transm Infect. (2019) 95:60–6. 10.1136/sextrans-2018-053597
    1. Aduloju OP, Akintayo AA, Aduloju T. Prevalence of bacterial vaginosis in pregnancy in a tertiary health institution, South Western Nigeria. Pan Afr Med J. (2019) 33:9. 10.11604/pamj.2019.33.9.17926
    1. Shayo PA, Kihunrwa A, Massinde AN, Mirambo M, Rumanyika R, Ngwalida N, et al. . Prevalence of bacterial vaginosis and associated factors among pregnant women attending at Bugando Medical Center, Mwanza, Tanzania. Tanzan J Health Res. (2012) 14:175–82. 10.4314/thrb.v14i3.3
    1. Govender L, Hoosen AA, Moodley J, Moodley P, Sturm AW. Bacterial vaginosis and associated infections in pregnancy. Int J Gynecol Obstet. (1996) 55:23–8. 10.1016/0020-7292(96)02744-0
    1. Watson-Jones D, Weiss HA, Changalucha JM, Todd J, Gumodoka B, Bulmer J, et al. . Adverse birth outcomes in United Republic of Tanzania - Impact and prevention of maternal risk factors. Bull World Health Organ. (2007) 85:9–18. 10.2471/BLT.06.033258
    1. Odendaal HJ, Popov I, Schoeman J, Smith M, Grové D. Preterm labour - Is bacterial vaginosis involved? South African Med J. (2002) 92:231–4.
    1. Afolabi BB, Moses OE, Oduyebo OO. Bacterial vaginosis and pregnancy outcome in Lagos, Nigeria. Open Forum Infect Dis. (2016) 3:ofw030. 10.1093/ofid/ofw030
    1. Schoeman J, Steyn PS, Odendaal HJ, Grové D. Bacterial vaginosis diagnosed at the first antenatal visit better predicts preterm labour than diagnosis later in pregnancy. J Obstet Gynaecol. (2005) 25:751–3. 10.1080/01443610500314660
    1. Slyker JA, Patterson J, Ambler G, Richardson BA, Maleche-Obimbo E, Bosire R, et al. . Correlates and outcomes of preterm birth, low birth weight, and small for gestational age in HIV-exposed uninfected infants. BMC Pregnancy Childbirth. (2014) 14:7. 10.1186/1471-2393-14-7
    1. Aderoba A, Olokor O, Olagbuji B, Ande A, Okonkwo C, Ojide C. Bacterial vaginosis in spontaneous preterm and term birth: a case–control study. Trop J Obstet Gynaecol. (2016) 33:297 10.4103/0189-5117.199820
    1. Medley N, Vogel JP, Care A, Alfirevic Z. Interventions during pregnancy to prevent preterm birth: an overview of cochrane systematic reviews. Cochrane Database Syst Rev. (2018) 11:CD012505. 10.1002/14651858.CD012505.pub2
    1. Steyn PS, Odendaal HJ, Schoeman J, Stander C, Fanie N, Grové D. A randomised, double-blind placebo-controlled trial of ascorbic acid supplementation for the prevention of preterm labour. J Obstet Gynaecol. (2003) 23:150–5. 10.1080/014436103000074673
    1. Mapchart Mapchart Africa Countries. Available online at: (accessed December 21, 2019).
    1. Donders G, De Wet HG, Hooft P, Desmyter J. Lactobacilli in papanicolaou smears, genital infections, and pregnancy. Am J Perinatol. (1993) 10:358–61. 10.1055/s-2007-994761
    1. Watson-Jones D, HW-B of the W . Adverse Birth Outcomes in United Republic of Tanzania: Impact and Prevention of Maternal Risk factors. SciELO Public Heal. (2007). Available online at: (accessed March 23, 2020).
    1. Peelen MJ, Luef BM, Lamont RF, de Milliano I, Jensen JS, Limpens J, et al. . The influence of the vaginal microbiota on preterm birth: a systematic review and recommendations for a minimum dataset for future research. Placenta. (2019) 79:30–9. 10.1016/j.placenta.2019.03.011
    1. Jespers V, Kyongo J, Joseph S, Hardy L, Cools P, Crucitti T, et al. . A longitudinal analysis of the vaginal microbiota and vaginal immune mediators in women from sub-Saharan Africa. Sci Rep. (2017) 7:11974. 10.1038/s41598-017-12198-6
    1. Anahtar MN, Byrne EH, Doherty KE, Bowman BA, Yamamoto HS, Soumillon M, et al. . Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. (2015) 42:965–76. 10.1016/j.immuni.2015.04.019
    1. Fettweis JM, Serrano MG, Brooks JP, Edwards DJ, Girerd PH, Parikh HI, et al. . The vaginal microbiome and preterm birth. Nat Med. (2019) 25:1012–21. 10.1038/s41591-019-0450-2
    1. Torcia MG. Interplay among vaginal microbiome, immune response and sexually transmitted viral infections. Int J Mol Sci. (2019) 20:266. 10.3390/ijms20020266
    1. Nadkarni MA, Martin FE, Hunter N, Jacques NA. Methods for optimizing DNA extraction before quantifying oral bacterial numbers by real-time PCR. FEMS Microbiol Lett. (2009) 296:45–51. 10.1111/j.1574-6968.2009.01629.x
    1. Hiergeist A, Gläsner J, Reischl U, Gessner A. Analyses of intestinal microbiota: culture versus sequencing. ILAR J. (2015) 56:228–40. 10.1093/ilar/ilv017
    1. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, Gloor GB, et al. . Deep sequencing of the vaginal microbiota of women with HIV. PLoS ONE. (2010) 5:e12078. 10.1371/journal.pone.0012078
    1. Thorsen P, Vogel I, Olsen J, Jeune B, Westergaard JG, Jacobsson B, et al. . Bacterial vaginosis in early pregnancy is associated with low birth weight and small for gestational age, but not with spontaneous preterm birth: a population-based study on Danish women. J Matern Neonatal Med. (2006) 19:1–7. 10.1080/14767050500361604
    1. Rosenberg RE, Ahmed ASMNU, Ahmed S, Saha SK, Chowdhury MAKA, Black RE, et al. . Determining gestational age in a low-resource setting: Validity of last menstrual period. J Heal Popul Nutr. (2009) 27:332–38. 10.3329/jhpn.v27i3.3375
    1. Hutcheon J, Platt R. The missing data problem in birth weight percentiles and thresholds for “small-for-gestational-age.” Am J Epidemiol. (2008) 167:786–92. 10.1093/aje/kwm327
    1. Sheehy O, Santos F, Ferreira E, Bérard A. The use of metronidazole during pregnancy: a review of evidence. Curr Drug Saf. (2015) 10:170–9. 10.2174/157488631002150515124548
    1. McGregor JA, French JI, Seo K. Premature rupture of membranes and bacterial vaginosis. Am J Obstet Gynecol. (1993) 169:463–6. 10.1016/0002-9378(93)90342-G
    1. Onwughara CE, Moodley D, Valashiya N, Sebitloane M. Preterm prelabour rupture of membranes (PPROM) and pregnancy outcomes in association with HIV-1 infection in KwaZulu-Natal, South Africa. BMC Pregnancy Childbirth. (2020) 20:204. 10.1186/s12884-020-02911-1
    1. Wiraguna AAGP, Rusyati LMM, Vijayamurthy IDAV. Bacterial vaginosis as a risk factor of preterm premature rupture of membrane (PPROM). Bali Dermatol Venereol J. (2019) 1:13 10.15562/bdv.v1i2.13
    1. Tchirikov M, Schlabritz-Loutsevitch N, Maher J, Buchmann J, Naberezhnev Y, Winarno AS, et al. . Mid-trimester preterm premature rupture of membranes (PPROM): etiology, diagnosis, classification, international recommendations of treatment options and outcome. J Perinat Med. (2018) 46:465–88. 10.1515/jpm-2017-0027
    1. Rzanek-Głowacka J, Pieta-Dolińska A, Zieba K, Oszukowski P. Is the mother's bacterial vaginosis with PROM a significant factor for intrauterine infection of the fetus in preterm labor before 32 weeks of gestation. Ginekol Pol. (2003) 74:1262–8.
    1. Genc MR, Onderdonk A. Endogenous bacterial flora in pregnant women and the influence of maternal genetic variation. BJOG. (2011) 118:154–63. 10.1111/j.1471-0528.2010.02772.x
    1. Witkin SS, Linhares IM, Giraldo P. Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol. (2007) 21:347–54. 10.1016/j.bpobgyn.2006.12.004
    1. Redelinghuys MJ, Ehlers MM, Dreyer AW, Kock MM. Normal flora and bacterial vaginosis in pregnancy: an overview. Crit Rev Microbiol. (2015) 42:352–63. 10.3109/1040841X.2014.954522
    1. Nelson D, Bellamy S, Nachamkin I. sterility RN-F and, 2007 undefined. First Trimester Bacterial Vaginosis, Individual Microorganism Levels, and Risk of Second Trimester Pregnancy Loss Among Urban Women. Elsevier; Available online at: (accessed May 9, 2020).
    1. Donati L, Di Vico A, Nucci M, Quagliozzi L, Spagnuolo T, Labianca A, et al. . Vaginal microbial flora and outcome of pregnancy. Arch Gynecol Obstet. (2010) 281:589–600. 10.1007/s00404-009-1318-3
    1. Murphy K, Mitchell CM. The interplay of host immunity, environment and the risk of bacterial vaginosis and associated reproductive health outcomes. J Infect Dis. (2016) 214:S29–35. 10.1093/infdis/jiw140
    1. Denney J. Medicine JC-S in F and N, 2009 undefined. Bacterial Vaginosis: a Problematic Infection From Both a Perinatal and Neonatal Perspective. Elsevier (2009). Available online at: (accessed May 9, 2020).
    1. Murphy K. Diseases CM-TJ of Infectious, 2016 Undefined. The Interplay of Host Immunity, Environment and the Risk of Bacterial Vaginosis and Associated Reproductive Health Outcomes. (2016). Available online at: (accessed May 9, 2020)
    1. Macones G, Parry S, Elkousy M, Clothier B, Ural S, Strauss JF III. A polymorphism in the promoter region of TNF bacterial vaginosis: preliminary evidence of gene-environment interaction in the etiology of spontaneous. Am J Obstet Gynecol. (2004) 190:1504–8. 10.1016/j.ajog.2004.01.001
    1. Nelson DB, Bellamy S, Nachamkin I, Ness RB, Macones GA, Allen-Taylor L. First trimester bacterial vaginosis, individual microorganism levels, and risk of second trimester pregnancy loss among urban women. Fertil Steril. (2007) 88:1396–403. 10.1016/j.fertnstert.2007.01.035
    1. McGregor JA, French JI, Parker R, Draper D, Patterson E, Jones W, et al. . Prevention of premature birth by screening and treatment for common genital tract infections: results of a prospective controlled evaluation. Am J Obstet Gynecol. (1995) 173:157–67. 10.1016/0002-9378(95)90184-1
    1. Hay PE. Bacterial vaginosis and miscarriage. Curr Opin Infect Dis. (2004) 17:41–4. 10.1097/00001432-200402000-00008
    1. Shahgheibi S, Seied-Al-Shohadaie F, Seied-Al-Shohadaie A, Ghaderi E. Complications of bacterial vaginosis in pregnancy. Pakistan J Med Sci. (2009) 25:953–56.
    1. Kaambo E, Africa CWJ. The threat of aerobic vaginitis to pregnancy and neonatal morbidity. Afr J Reprod Health. (2017) 21:108–18. 10.29063/ajrh2017/v21i2.12
    1. Africa C, Kaambo E, Stemmet M. Opportunistic vaginal infections implicated in the risk for adverse pregnancy outcomes. In: 11th International Symposium on Antimicrobial Agents and Resistance (ISAAR) and 3rd International Interscience Conference on Infection and Chemotherapy (ICIC) (Busan: ), S84.
    1. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, et al. . A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus beijerinck 1901 and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol. (2020) 70:2782–858. 10.1099/ijsem.0.004107
    1. Zheng J, Ruan L, Sun M, Gänzle M. A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology downloaded from. Appl Env Microbiol. (2015) 81:2020. 10.1128/AEM.02116-15
    1. Castro J, Jefferson KK, Cerca N. Genetic heterogeneity and taxonomic diversity among Gardnerella species. Trends Microbiol. (2020) 28:202–11. 10.1016/j.tim.2019.10.002
    1. Yano J, Noverr MC, Fidel PL. Cytokines in the host response to Candida vaginitis: identifying a role for non-classical immune mediators, S100 alarmins. Cytokine. (2012) 58:118–28. 10.1016/j.cyto.2011.11.021
    1. Africa CWJ, Nel J, Stemmet M. Anaerobes and bacterial vaginosis in pregnancy: Virulence factors contributing to vaginal colonisation. Int J Environ Res Public Health. (2014) 11:6979–7000. 10.3390/ijerph110706979
    1. Van De Wijgert JHHM, Borgdorff H, Verhelst R, Crucitti T, Francis S, Verstraelen H, et al. . The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS ONE. (2014) 9:e0105998. 10.1371/journal.pone.0105998
    1. Virtanen S, Rantsi T, Virtanen A, Kervinen K, Nieminen P, Kalliala I, et al. . Vaginal microbiota composition correlates between pap smear microscopy and next generation sequencing and associates to socioeconomic status. Sci Rep. (2019) 9:7750. 10.1038/s41598-019-44157-8
    1. Fettweis JM, Paul Brooks J, Serrano MG, Sheth NU, Girerd PH, Edwards DJ, et al. . Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology. (2014) 160:2272–82. 10.1099/mic.0.081034-0
    1. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. (2008) 371:75–84. 10.1016/S0140-6736(08)60074-4
    1. Moosa Y, Kwon D, de Oliveira T, Wong EB. Determinants of vaginal microbiota composition. Front Cell Infect Microbiol. (2020) 10:467. 10.3389/fcimb.2020.00467
    1. Mason-Jones AJ, Sinclair D, Mathews C, Kagee A, Hillman A, Lombard C. School-based interventions for preventing HIV, sexually transmitted infections, and pregnancy in adolescents. Cochrane Database Syst Rev. (2016) 2016:CD006417. 10.1002/14651858.CD006417.pub3
    1. Kazeem A, Jensen L, Stokes CS. School attendance in nigeria: understanding the impact and intersection of gender, Urban-Rural residence, and socioeconomic status. Comp Educ Rev. (2010) 54:295–319. 10.1086/652139
    1. ISSC, IDS UNESCO World Social Science Report 2016 Challenging Inequalities: Pathways to a Just World. Paris: (2016). Available online at: (accessed September 22, 2020).
    1. UNESCO (United Nations Educational S CO EFA Global Monitoring Report 2008 Overcoming Inequality: Why Governance Matters. Paris and London: (2008) Available online at: (accessed September 22, 2020).
    1. Gueye A, Speizer IS, Corroon M, Okigbo CC. Belief in family planning myths at the individual and community levels and modern contraceptive use in Urban Africa. Int Perspect Sex Reprod Health. (2015) 41:191–9. 10.1363/4119115
    1. Mullick S, Watson-Jones D, Beksinska M, Mabey D. Sexually transmitted infections in pregnancy: Prevalence, impact on pregnancy outcomes, and approach to treatment in developing countries. Sex Transm Infect. (2005) 81:294–302. 10.1136/sti.2002.004077
    1. Bisanz JE, Enos MK, PrayGod G, Seney S, Macklaim JM, Chilton S, et al. . Microbiota at multiple body sites during pregnancy in a rural tanzanian population and effects of Moringa-supplemented probiotic yogurt. Appl Environ Microbiol. (2015) 81:4965–75. 10.1128/AEM.00780-15
    1. McMillan A, Rulisa S, Gloor GB, Macklaim JM, Sumarah M, Reid G. Pilot assessment of probiotics for pregnant women in Rwanda. PLoS ONE. (2018) 13:e0195081. 10.1371/journal.pone.0195081
    1. Price JT, Vwalika B, Hobbs M, Nelson JAE, Stringer EM, Zou F, et al. . Highly diverse anaerobe-predominant vaginal microbiota among HIV-infected pregnant women in Zambia. PLoS ONE. (2019) 14:e0223128. 10.1371/journal.pone.0223128
    1. Schwebke JR, Hillier SL, Sobel JD, McGregor JA, Sweet RL. Validity of the vaginal gram stain for the diagnosis of bacterial vaginosis. Obstet Gynecol. (1996) 88:573–6. 10.1016/0029-7844(96)00233-5
    1. Marrazzo JM, Martin DH, Watts DH, Schulte J, Sobel JD, Hillier SL, et al. . Bacterial vaginosis: Identifying research gaps proceedings of a workshop sponsored by DHHS/NIH/NIAID. Sex Transm Dis. (2010) 37:732–44. 10.1097/OLQ.0b013e3181fbbc95

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