Molecular diagnosis of bacterial vaginosis: impact on IVF outcome

  • J. Mangot-Bertrand
  • F. Fenollar
  • F. Bretelle
  • M. Gamerre
  • D. Raoult
  • B. Courbiere


Bacterial vaginosis can increase obstetrical complications such as miscarriage, premature rupture of membranes and preterm delivery. The aim of our study was first to assess BV prevalence for infertile patients treated by in vitro fertilisation (IVF) using both the Nugent score and polymerase chain reaction (PCR), and then to assess the impact of BV on the pregnancy rate after IVF. Vaginal samples were obtained from women followed for IVF in our Assisted Reproduction Technology (ART) Unit between August 2010 and April 2011. For each patient, two techniques were performed to diagnose BV: Gram staining to assess the Nugent score and a quantitative molecular analysis using a specific real-time PCR assay. Two groups were studied: normal flora (BV−) and BV (BV+). The primary outcome measure was the implantation rate. The secondary outcomes were clinical pregnancy rate, early and late miscarriage, premature rupture of membranes, preterm delivery, mode of delivery and birthweight. A total of 307 patients were included. PCR revealed a prevalence of BV of 9.45 %. Among women who performed vaginal douching, 22.2 % were BV+, whereas 7.9 % of patients who did not douche were BV+ (p = 0.028). The embryo implantation rate was decreased between the BV− and BV+ groups (36.3 % vs. 27.6 %, p = 0.418), but it was not significant. Obstetrical outcomes did not present significant statistical differences among the groups. Vaginal douching significantly enhanced BV in women treated with IVF. We also observed a non-significant decrease of embryo implantation rate and clinical pregnancy rate for women treated by IVF.


  1. 1.
    Livengood CH (2009) Bacterial vaginosis: an overview for 2009. Rev Obstet Gynecol 2:28–37PubMedGoogle Scholar
  2. 2.
    Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P (2003) Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol 189:139–147PubMedCrossRefGoogle Scholar
  3. 3.
    Fredricks DN, Fiedler TL, Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353:1899–1911PubMedCrossRefGoogle Scholar
  4. 4.
    Larsson PG, Forsum U (2005) Bacterial vaginosis—a disturbed bacterial flora and treatment enigma. APMIS 113:305–316, ReviewPubMedCrossRefGoogle Scholar
  5. 5.
    Allsworth JE, Peipert JF (2011) Severity of bacterial vaginosis and the risk of sexually transmitted infection. Am J Obstet Gynecol 205:113.e1–113.e6CrossRefGoogle Scholar
  6. 6.
    Guaschino S, Ricci E, Franchi M, Frate GD, Tibaldi C, Santo DD et al (2003) Treatment of asymptomatic bacterial vaginosis to prevent pre-term delivery: a randomised trial. Eur J Obstet Gynecol Reprod Biol 110:149–152PubMedCrossRefGoogle Scholar
  7. 7.
    Hogan VK, Culhane JF, Hitti J, Rauh VA, McCollum KF, Agnew KJ (2007) Relative performance of three methods for diagnosing bacterial vaginosis during pregnancy. Matern Child Health J 11:532–539PubMedCrossRefGoogle Scholar
  8. 8.
    Ralph SG, Rutherford AJ, Wilson JD (1999) Influence of bacterial vaginosis on conception and miscarriage in the first trimester: cohort study. BMJ 319:220–223PubMedCrossRefGoogle Scholar
  9. 9.
    Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J (1994) Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ 308:295–298PubMedCrossRefGoogle Scholar
  10. 10.
    McGregor JA, French JI, Parker R, Draper D, Patterson E, Jones W et al (1995) Prevention of premature birth by screening and treatment for common genital tract infections: results of a prospective controlled evaluation. Am J Obstet Gynecol 173:157–167PubMedCrossRefGoogle Scholar
  11. 11.
    Spiegel CA, Amsel R, Holmes KK (1983) Diagnosis of bacterial vaginosis by direct gram stain of vaginal fluid. J Clin Microbiol 18:170–177PubMedGoogle Scholar
  12. 12.
    Schwebke JR, Hillier SL, Sobel JD, McGregor JA, Sweet RL (1996) Validity of the vaginal gram stain for the diagnosis of bacterial vaginosis. Obstet Gynecol 88:573–576PubMedCrossRefGoogle Scholar
  13. 13.
    Landers DV, Wiesenfeld HC, Heine RP, Krohn MA, Hillier SL (2004) Predictive value of the clinical diagnosis of lower genital tract infection in women. Am J Obstet Gynecol 190:1004–1010PubMedCrossRefGoogle Scholar
  14. 14.
    Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29:297–301PubMedGoogle Scholar
  15. 15.
    Menard JP, Mazouni C, Salem-Cherif I, Fenollar F, Raoult D, Boubli L et al (2010) High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet Gynecol 115:134–140PubMedCrossRefGoogle Scholar
  16. 16.
    Menard JP, Fenollar F, Henry M, Bretelle F, Raoult D (2008) Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis 47:33–43PubMedCrossRefGoogle Scholar
  17. 17.
    Baker VL, Luke B, Brown MB, Alvero R, Frattarelli JL, Usadi R et al (2010) Multivariate analysis of factors affecting probability of pregnancy and live birth with in vitro fertilization: an analysis of the Society for Assisted Reproductive Technology Clinic Outcomes Reporting System. Fertil Steril 94:1410–1416PubMedCrossRefGoogle Scholar
  18. 18.
    Moore DE, Soules MR, Klein NA, Fujimoto VY, Agnew KJ, Eschenbach DA (2000) Bacteria in the transfer catheter tip influence the live-birth rate after in vitro fertilization. Fertil Steril 74:1118–1124PubMedCrossRefGoogle Scholar
  19. 19.
    van Os HC, Roozenburg BJ, Janssen-Caspers HA, Leerentveld RA, Scholtes MC, Zeilmaker GH et al (1992) Vaginal disinfection with povidon iodine and the outcome of in-vitro fertilization. Hum Reprod 7:349–350PubMedGoogle Scholar
  20. 20.
    Liversedge NH, Turner A, Horner PJ, Keay SD, Jenkins JM, Hull MG (1999) The influence of bacterial vaginosis on in-vitro fertilization and embryo implantation during assisted reproduction treatment. Hum Reprod 14:2411–2415PubMedCrossRefGoogle Scholar
  21. 21.
    Eckert LO, Moore DE, Patton DL, Agnew KJ, Eschenbach DA (2003) Relationship of vaginal bacteria and inflammation with conception and early pregnancy loss following in-vitro fertilization. Infect Dis Obstet Gynecol 11:11–17PubMedCrossRefGoogle Scholar
  22. 22.
    Daya S, Gunby JL (2004) Luteal phase support in assisted reproduction cycles. Cochrane Database Syst Rev (3):CD004830. Review. Update in: Cochrane Database Syst Rev. 2008;(3):CD004830Google Scholar
  23. 23.
    Menard JP, Mazouni C, Fenollar F, Raoult D, Boubli L, Bretelle F (2010) Diagnostic accuracy of quantitative real-time PCR assay versus clinical and Gram stain identification of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 29:1547–1552PubMedCrossRefGoogle Scholar
  24. 24.
    Martius J, Krohn MA, Hillier SL, Stamm WE, Holmes KK, Eschenbach DA (1988) Relationships of vaginal Lactobacillus species, cervical Chlamydia trachomatis, and bacterial vaginosis to preterm birth. Obstet Gynecol 71:89–95PubMedGoogle Scholar
  25. 25.
    Pastore LM, Royce RA, Jackson TP, Thorp JM Jr, Savitz DA, Kreaden US (1999) Association between bacterial vaginosis and fetal fibronectin at 24–29 weeks’ gestation. Obstet Gynecol 93:117–123PubMedCrossRefGoogle Scholar
  26. 26.
    Kekki M, Kurki T, Pelkonen J, Kurkinen-Räty M, Cacciatore B, Paavonen J (2001) Vaginal clindamycin in preventing preterm birth and peripartal infections in asymptomatic women with bacterial vaginosis: a randomized, controlled trial. Obstet Gynecol 97:643–648PubMedCrossRefGoogle Scholar
  27. 27.
    Eriksson K, Adolfsson A, Forsum U, Larsson PG (2010) The prevalence of BV in the population on the Åland Islands during a 15-year period. APMIS 118:903–908PubMedCrossRefGoogle Scholar
  28. 28.
    Gustafsson RJ, Ahrné S, Jeppsson B, Benoni C, Olsson C, Stjernquist M et al (2011) The Lactobacillus flora in vagina and rectum of fertile and postmenopausal healthy Swedish women. BMC Womens Health 25:11–17Google Scholar
  29. 29.
    Srinivasan S, Liu C, Mitchell CM, Fiedler TL, Thomas KK, Agnew KJ et al (2010) Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 5(4):e10197PubMedCrossRefGoogle Scholar
  30. 30.
    Fredricks DN (2011) Molecular methods to describe the spectrum and dynamics of the vaginal microbiota. Anaerobe 17:191–195PubMedCrossRefGoogle Scholar
  31. 31.
    Fanchin R, Harmas A, Benaoudia F, Lundkvist U, Olivennes F, Frydman R (1998) Microbial flora of the cervix assessed at the time of embryo transfer adversely affects in vitro fertilization outcome. Fertil Steril 70:866–870PubMedCrossRefGoogle Scholar
  32. 32.
    Donders GG, Bosmans E, Dekeersmaecker A, Vereecken A, Van Bulck B, Spitz B (2000) Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol 182:872–878PubMedCrossRefGoogle Scholar
  33. 33.
    Leitich H, Kiss H (2007) Asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 21:375–390PubMedCrossRefGoogle Scholar
  34. 34.
    Ness RB, Hillier SL, Richter HE, Soper DE, Stamm C, McGregor J et al (2002) Douching in relation to bacterial vaginosis, lactobacilli, and facultative bacteria in the vagina. Obstet Gynecol 100:765PubMedCrossRefGoogle Scholar
  35. 35.
    Mijac VD, Dukić SV, Opavski NZ, Dukić MK, Ranin LT (2006) Hydrogen peroxide producing lactobacilli in women with vaginal infections. Eur J Obstet Gynecol Reprod Biol 129:69–76PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • J. Mangot-Bertrand
    • 1
  • F. Fenollar
    • 2
  • F. Bretelle
    • 1
    • 2
  • M. Gamerre
    • 1
  • D. Raoult
    • 2
  • B. Courbiere
    • 1
    • 3
    • 4
  1. 1.Department of Gynaecology, Obstetrics, and ReproductionAP-HM La Conception & APHM NordMarseilleFrance
  2. 2.Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), UMR CNRS-IRD 6236—Faculté de Médecine de MarseilleUniversité de la MéditerranéeMarseilleFrance
  3. 3.Institut Méditerranéen de Biodiversité et d’Ecologie (IMBE, UMR CNRS 7263 - IRD 237) équipe BiogénotoxicologieSanté Humaine et Environnement, Aix-Marseille Université, Faculté de MédecineMarseilleFrance
  4. 4.FR CNRS 3098, Ecosystèmes Continentaux et Risques EnvironnementauxECCOREV Europôle de l’ArboisAix-en-ProvenceFrance

Personalised recommendations