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Vaginal microbial flora and outcome of pregnancy

  • Materno-fetal Medicine
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Abstract

Background

The vaginal microflora of a healthy asymptomatic woman consists of a wide variety of anaerobic and aerobic bacterial genera and species dominated by the facultative, microaerophilic, anaerobic genus Lactobacillus. The activity of Lactobacillus is essential to protect women from genital infections and to maintain the natural healthy balance of the vaginal flora. Increasing evidence associates abnormalities in vaginal flora during pregnancy with preterm labor and delivery with potential neonatal sequelae due to prematurity and poor perinatal outcome. Although this phenomenon is relatively common, even in populations of women at low risk for adverse events, the pathogenetic mechanism that leads to complications in pregnancy is still poorly understood.

Objective

This review summarizes the current knowledge and uncertainties in defining alterations of vaginal flora in non-pregnant adult women and during pregnancy, and, in particular, investigates the issue of bacterial vaginosis and aerobic vaginitis. This could help specialists to identify women amenable to treatment during pregnancy leading to the possibility to reduce the preterm birth rate, preterm premature rupture of membranes, chorioamnionitis, neonatal, puerperal and maternal–fetal infectious diseases.

Conclusions

Vaginal ecosystem study with the detection of pathogens is a key instrument in the prevention of preterm delivery, pPROM, chorioamnionitis, neonatal, puerperal and maternal-fetal infections.

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References

  1. Witkin SS, Linhares IM, Giraldo P (2007) Bacterial flora of the female genital tract. function and immune regulation 21(3):347–354

    Google Scholar 

  2. Lidbeck A, Nord CE (1993) Lactobacilli and the normal human anaerobic microflora. Clin Infect Dis 16(Suppl 4):S181–S187

    PubMed  Google Scholar 

  3. Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner-Hanssen P (1996) Hydrogen peroxide-producing Lactobacilli and acquisition of vaginal infections. J Infect Dis 174(5):1058–1063

    CAS  PubMed  Google Scholar 

  4. Zhou X, Bent SJ, Schneider MG et al (2004) Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology 150:2565–2573

    Article  CAS  PubMed  Google Scholar 

  5. Donders GGG (1999) Bacterial vaginosis in pregnancy: screen and treat? [editorial]. Eur J Obstet Gynecol Reprod Biol 83:1–4

    Article  CAS  PubMed  Google Scholar 

  6. Verhelst R, Verstraelen H, Claeys G et al (2004) Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae, Gardnerella vaginalis and bacterial vaginosis. BMC Microbiol 4:16–26

    Article  PubMed  Google Scholar 

  7. Fredricks DN, Fiedler TL, e Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353:1899–1911

    Article  CAS  PubMed  Google Scholar 

  8. Rodriguez JM, Collins MD, Sjoden B, Falsen E (1999) Characterization of a novel Atopobium isolate from the human vagina: description of Atopobium vaginae sp. Nov. Int J Syst Bacteriol 49:e1573–e1576

    Article  Google Scholar 

  9. Antonio MA, Hawes SE, Hillier SL (1999) The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 180:e1950–e1956

    Article  Google Scholar 

  10. Stevens-Simon C, Jamison J, McGregor JA, Douglas JM (1994) Racial variation in vaginal pH among healthy sexually active adolescents. Sex Transm Dis 21:e168–e172

    Article  Google Scholar 

  11. Royce RA, Jackson TP, Thorp JMJ et al (1999) Race/ethnicity, vaginal flora patterns, and pH during pregnancy. Sex Transm Dis 26:e96–e102

    Article  Google Scholar 

  12. Fiscella K, Klebanoff MA (2004) Are racial differences in vaginal pH explained by vaginal flora? Am J Obstet Gynecol 191:e747–e750

    Article  Google Scholar 

  13. Priestlley CFJ, Jones BM, Dhar J, Goodwin L (1997) What is normal vaginal flora? Genitourin Med 73:e23–e28

    Google Scholar 

  14. Eschenbach DA, Patton DL, Hooten TM et al (2001) Effects of vaginal intercourse with and without a condom on vaginal flora and vaginal epithelium. J Infect Dis 183:e913–e918

    Article  Google Scholar 

  15. Spiegel CA (1991) Bacterial vaginosis. Clin Microbiol Rev 4:485–502

    CAS  PubMed  Google Scholar 

  16. Forsum U, Holst E, Larsson PG, Vasquez A, Jacobsson T, Mattsby-Baltzer I (2005) Bacterial vaginosis—a microbiological and immunological enigma. APMIS 113:81–90

    Article  CAS  PubMed  Google Scholar 

  17. Amsel R, Totten PA, Spiegel CA, Chen K, Eshenbach DA, Holmes KK (1983) Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiological associations. Am J Med 74:14–22

    Article  CAS  PubMed  Google Scholar 

  18. Leopold S (1953) Heretofore undescribed organism isolated from the genitourinary system. U S Armed Forces Med J 4:263–266

    CAS  PubMed  Google Scholar 

  19. Gardner HL, Dukes CD (1954) New etiologic agent in nonspecific bacterial vaginitis. Science 120:853

    Article  CAS  PubMed  Google Scholar 

  20. Gardner HL, Dukes CD (1955) Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol 69:962–976

    CAS  PubMed  Google Scholar 

  21. Greenwood JR, Pickett MJ (1979) Salient features of Haemophilus vaginalis. J Clin Microbiol 9:200–204

    CAS  PubMed  Google Scholar 

  22. Piot P, van Dyck E, Goodfellow M, Falkow S (1980) A taxonomic study of Gardnerella vaginalis (Haemophilus vaginalis) Gardner and Dukes 1955. J Gen Microbiol 119:373–396

    CAS  PubMed  Google Scholar 

  23. Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S, Hale LP, Lochs H (2005) Adherent biofilms in bacterial vaginosis. Obstet Gynecol 106:1013–1023

    PubMed  Google Scholar 

  24. Swidsinski A, Mendling W, Loening-Baucke V, Swidsinski S, Dörffel Y, Scholze J, Lochs H, Verstraelen H (2008) An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. Am J Obstet Gynecol 198(97):e1–e6

    PubMed  Google Scholar 

  25. Aroutcheva AA, Simoes JA, Behbakht K, Faro S (2001) Gardnerella vaginalis isolated from patients with bacterial vaginosis and from patients with healthy vaginal ecosystems. Clin Infect Dis 33:1022–1027

    Article  CAS  PubMed  Google Scholar 

  26. Waites KB, Katz B, Schelonka RL (2005) Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev 18:757–789

    Article  PubMed  Google Scholar 

  27. Hay PE, Lamont RF, Taylor-Robinson et al (1994) Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. Br Med J 308:295–298

  28. Platz-Christensen J-J, Larsson P-G, Sundstrom E, Wiqvist N (1995) Detection of bacterial vaginosis in wet mount, Papanicolaou stained vaginal smears and in Gram stained smears. Acta Obstet Gynecol Scand 74:67–70

    Article  CAS  PubMed  Google Scholar 

  29. McDonald HM, O’Loughlin JA, Jolley PT et al (1994) Changes in vaginal flora during pregnancy and association with preterm birth. J Infect Dis 170:724–728

    CAS  PubMed  Google Scholar 

  30. Spiegel CA, Amsel R, Holmes KK (1983) Diagnosis of bacterial vaginosis by direct Gram stain of vaginal fluid. J Clin Microbiol 18:e170–e177

    Google Scholar 

  31. Kalinka J, Laudanski T, Hanke W, Wasiela M (2003) Do microbiological factors account for poor pregnancy outcome among unmarried pregnant women in Poland? Fetal Diagn Ther 18:e345–e352

    Article  Google Scholar 

  32. Donders GG, Veerecken A, Bosmans E, Dekersmaecker A, Salembier G, Spitz B (2002) Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. Br J Obstet Gynecol 109:34–43

    Google Scholar 

  33. Sobel JD (1994) Desquamative inflammatory vaginitis: a new subgroup of purulent vaginitis responsive to topical 2% clindamycin therapy. Am J Obstet Gynecol 171:1215–1220

    CAS  PubMed  Google Scholar 

  34. Donders GGG (1999) Microscopy of bacterial flora on fresh vaginal smears. Infect Dis Obstet Gynecol 7:126–127

    Article  CAS  PubMed  Google Scholar 

  35. Gardner HL (1968) Desquamative inflammatory vaginitis: a newly defined entity. Am J Obstet Gynecol 102:1102–1105

    CAS  PubMed  Google Scholar 

  36. Donders GGG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B (2002) Aerobic vaginitis: abnormal vaginal flora entity that is distinct from bacterial vaginosis. Br J Obstet Gynecol 109:1–10

    Google Scholar 

  37. Mattsby-Baltzer I, Platz-Christensen JJ, Hosseini N, Rosen P (1998) IL-1beta, IL-6, TNFalfa, fetal fibronectin and endotoxin in the lower genital tract of pregnant women with bacterial vaginosis. Acta Obstet Gynecol Scand 77:701–706

    Article  CAS  PubMed  Google Scholar 

  38. Imseis HM, Livengood HH, Shunior E, Durda P, Erikson M (1997) Characterisation of the inflammatory cytokines in the vagina during pregnancy and labour and with bacterial vaginosis. J Soc Gynecol Investig 4:90–92

    Article  CAS  PubMed  Google Scholar 

  39. Romero R, Yoon BH, Mazor M, Gomez R et al (1993) The diagnostic and prognostic value of amniotic fluid white blood cell count, glucose, IL-6, and Gram stain in patients with preterm labour and intact membranes. Am J Obstet Gynecol 169:805–816

    CAS  PubMed  Google Scholar 

  40. Chaisilwattana P, Monif GRG (1995) In vitro ability of the group B streptococci to inhibit gram-positive and gram-variable constituents of the bacterial flora of the female genital tract. Infect Dis Obstet Gynecol 3:91–97

    Article  CAS  PubMed  Google Scholar 

  41. Monif GRG (1999) Semiquantitative bacterial observations with group B streptococci. Infect Dis Obstet Gynecol 7:227–229

    Article  CAS  PubMed  Google Scholar 

  42. Honig E, Mouton JW, van der Meijden WI (1999) Can group B streptococci cause symptomatic vaginitis? Infect Dis Obstet Gynecol 7:206–209

    Article  CAS  PubMed  Google Scholar 

  43. Usui R, Ohkuchi S, Matsubara S, Izumi A, Watanabe T, Suzuki M (2000) Vaginal lactobacilli and preterm birth. J Perinat Med 30:458–466

    Article  Google Scholar 

  44. Waites KB, Katz B, Schelonka RL (2005) Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev 18:757–789

    Article  PubMed  Google Scholar 

  45. Donders GGG (2007) Definition and classification of abnormal vaginal flora. Best Pract Res Clin Obstet Gynaecol 21:355–373

    Article  PubMed  Google Scholar 

  46. Larsson P-G, Platz-Christensen JJ (1990) Enumeration of clue cells in rehydrated air-dried vaginal wet smears for the diagnosis of bacterial vaginosis. Obstet Gynecol 76:727–730

    CAS  PubMed  Google Scholar 

  47. Simhan HN, Caritis SN, Krohn MA, Martinez de Teada B, Landers DV, Hillier SL (2003) Decreased cervical proinflammatory cytokines permit subsequent upper genital tract infection during pregnancy. Am J Obstet Gynecol 189:560–567

    Article  CAS  PubMed  Google Scholar 

  48. Hillier SL, Martius, Krohn M, Kiviat N, Holmes KK, Eschenbach DA (1988) A case control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 319:972–978

  49. Leitch H, Kiss H (2006) asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 21:375–390

    Article  Google Scholar 

  50. Allsworth JE, Peipert JF (2007) Prevalence of bacterial vaginosis: 2001–2004 National Health and Nutrition Examination Survey Data. Obstet Gynecol 109:114–120

    PubMed  Google Scholar 

  51. Britton T, Dawn PM (2007) Risk factors for bacterial vaginosis during pregnancy among African American women. Am J Obstet Gynecol 197:477.e1–477.e8

    Article  Google Scholar 

  52. Mc Donald H, O’Loughlin JA, Jolley PT, Vigneswaran R, McDonald P (1994) Changes in vaginal flora during pregnancy and association with preterm birth. J Infect Dis 170:724–728

    CAS  Google Scholar 

  53. Fischbach F, Petersen E, Weissenbacher ER, Martius J, Hossman J, Mayer H (1993) Efficacy of clindamycin vaginal cream versus oral metronidazole I the treatment of bacterial vaginosis. Obstet Gynecol 82(3):405–410

    CAS  PubMed  Google Scholar 

  54. Waters TP, Denney JM, Mathew L, Goldenberg RL, Culhane JF (2008) Longitudinal trajectory of bacterial vaginosis during pregnancy. Am J Obstet Gynecol 199:431–435

    Google Scholar 

  55. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH (1995) Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med 333(26):1737–1742

    Article  CAS  PubMed  Google Scholar 

  56. Krohn MA, Thwin SS, Rabe LK, Brown Z, Hillier SL (1997) Vaginal colonization by Escherichia coli as a risk factor for very low birth weight delivery and other perinatal complications. J Infect Dis 175(3):606–610

    CAS  PubMed  Google Scholar 

  57. Newton ER (1993) Chorioamnionitis and intraamniotic infection. Clin Obstet Gynecol 36:795–808

    Article  CAS  PubMed  Google Scholar 

  58. Andrews WW, Goldenberg RL, Hauth C, Cliver SP, Conner M, Goepfert AR (2005) Endometrial microbial colonization and plasma cell endometritis after spontaneous or indicated preterm versus term delivery. Am J Obstet Gynecol 193(3 Pt 1):739–745

    Article  PubMed  Google Scholar 

  59. Cassell GH, Davis RO, Waites KB et al (1983) Isolation of Mycoplasma hominis and Ureaplasma urealyticum from amniotic fluid at 16–20 weeks of gestation: potential effect on outcome of pregnancy. Sex Transm Dis 10(4 Suppl):294–302

    CAS  PubMed  Google Scholar 

  60. Waites KB, Katz B, Schelonka RL (2005) Mycoplasmas and Ureaplasmas as neonatal pathogens. Clin Microbiol Rev 18:757–789

    Article  PubMed  Google Scholar 

  61. McDonald HM, Brocklehurst P, Gordon A (2007) Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst Rev 1:CD000262

  62. Morency AM, Buold E (2007) The effect of second-trimester antibiotic therapy on the rate of preterm birth. J Obstet Gynaecol Can 29:35–44

    PubMed  Google Scholar 

  63. Swadpanich U, Lumbiganon P, Prasertcharoensook W, Laopaiboon M (2008) Antenatal lower genital tract infection screening and treatment programs for preventing preterm delivery. Cochrane Database Syst Rev 2:CD006178

  64. Kenyon SL, Taylor D, Tarnow-Mordi W (2001) Broad-spectrum antibiotics for preterm, prelabour rupture of fetal membranes: the ORACLE I randomised trial. ORACLE Collaborative Group. Lancet 357(9261):979–988

    Article  CAS  PubMed  Google Scholar 

  65. Read JS, Klebanoff MA (1993) Sexual intercourse during pregnancy and preterm delivery: effects of vaginal microorganism. The Vaginal infection and Prematurity Study Group. Am J Obstet Gynecol 168(2):514–519

    CAS  PubMed  Google Scholar 

  66. Donders GGG, Van Bulck B, Caudron J et al (2000) Relationship of bacterial vaginosis and mycoplasmas to the risk of spontaneous abortion. Am J Obstet Gynecol 183:431–437

    Google Scholar 

  67. Edwards RK, Ferguson KJ, Duff P (2006) The interleukin-l beta +3953 single nucleotide polymorphism: cervical protein concentration and preterm delivery risk. Am J Reprod Immunol 55:259–264

    Google Scholar 

  68. Goffinet F, Maillard F, Mihoubi N et al (2003) Bacterial vaginosis: prevalence and predictive value for premature delivery and neonatal infection in women with preterm labour and intact membranes. Eur J Obstet Gynecol Reprod Biol 108:146–151

    Google Scholar 

  69. Guerra P, Ghi T, Quarta S et al (2006) Pregnancy outcome alter early detection of bacterial vaginosis. Eur J Obstet Gynecol Reprod Biol 128:40–45

    Google Scholar 

  70. Oakeshott P, Kerry S, Hay S, Hay P (2004) Bacterial vaginosis and preterm birth: a prospective community-based cohort study. Br J Gen Pract 54:119–122

    Google Scholar 

  71. Andrews WW, Sibai BM, Thom EA et al (2003) Randomized clinical trial of metronidazole plus erythromycin to prevent spontaneous preterm delivery in fetal fibronectin-positive women. Obstet Gynecol 101:847–855

    Google Scholar 

  72. Daskalakis G, Papapanagiotou A, Mesogitis S et al (2006) Bacterial vaginosis and group B streptococcal colonization and preterm delivery in a low-risk population. Fetal Diagn Ther 21:172–176

    Google Scholar 

  73. De Seta F, Sartore A, Piccoli M et al (2005) Bacterial vaginosis and preterm delivery: an open question. J Reprod Med 50:313–318

    Google Scholar 

  74. Genc MR, Witkin SS, Delaney ML et al (2004) A disproportionate increase in IL-1beta over IL-1ra in the cervicovaginal secretions of pregnant women with altered vaginal microflora correlates with preterm birth. Am J Obstet Gynecol 190:1191–1197

    Google Scholar 

  75. Goyal R, Sharma P, Kaur I et al (2004) Bacterial vaginosis and vaginal anaerobes in preterm labour. J Indian Med Assoc 102:548–553

    Google Scholar 

  76. Kalinka J, Sobala W, Wasiela M, Brzezinska-Blaszczyk E (2005) Decreased proinflammatory cytokines in cervicovaginal fluid, as measured in midgestation, are associated with preterm delivery. Am J Reprod Immunol 54:70–76

    Google Scholar 

  77. Kiss H, Petricevic L, Husslein P (2004) Prospective randomised controlled trial of an infection screening programme to reduce the rate of preterrn delivery. BMJ 329:371

    Google Scholar 

  78. Purwar M, Ughade S, Bhagat B et al (2001) Bacterial vaginosis in early pregnancy and adverse pregnancy outcome. J Obstet Gynaecol Res 27:175–181

    Google Scholar 

  79. Thorsen P, Vogel I, Olsen J et al (2006) 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 Matem Fetal Neonatal Med 19:1–7

    Google Scholar 

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Acknowledgment

The authors would like to thank Tracie Dornbusch for revising the manuscript.

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Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Catholic University of Sacred Heart, Largo A. Gemelli 8, 00168, Rome, Italy

    Laura Donati, Augusto Di Vico, Marta Nucci, Lorena Quagliozzi, Terryann Spagnuolo, Antonietta Labianca, Marina Bracaglia, Francesca Ianniello, Alessandro Caruso & Giancarlo Paradisi

  2. Department of Obstetrics and Gynecology, Catholic University of Sacred Heart, Via Servilio IV 4, 00178, Rome, Italy

    Giancarlo Paradisi

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  1. Laura Donati
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  2. Augusto Di Vico
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  3. Marta Nucci
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Correspondence to Giancarlo Paradisi.

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Donati, L., Di Vico, A., Nucci, M. et al. Vaginal microbial flora and outcome of pregnancy. Arch Gynecol Obstet 281, 589–600 (2010). https://doi.org/10.1007/s00404-009-1318-3

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