Obstetric and Gynecological Diseases and Complications Resulting from Vaginal Dysbacteriosis

Abstract

Accurate knowledge of the composition and ecology of vaginal microbial environment of a healthy woman is necessary for the understanding of normal flora and how to reduce the risk for diseases. Vagina and its microflora form a balanced ecosystem in which dominated bacteria are vaginal lactobacilli. There are dynamic changes in this ecosystem having structure and composition depending on many factors. The term dysbacteriosis defines any movement outside the normal range for the given biotope of obligate and/or facultative microflora. Such a change in the quantity and quality of the respective microbial balance is fraught with danger and requires correction and recovery. The purpose of this overview is to examine obstetric and gynecological diseases that can cause vaginal impaired microbial balance. Vaginal dysbacteriosis is a cause, predecessor, and often also consequence of vaginal infections. In essence, any vaginal infection can be seen as dysbacteriosis, developed to the most severe extent. Here, there is a dominant microorganism other than lactic acid bacteria in the vagina (clinically manifested or not, respectively), depletion of defense mechanisms of the vagina associated with the shift of lactobacilli from their dominant role in the vaginal balance, decrease in their number and species diversity, and a resulting change in the healthy status of the vagina. Vaginal dysbacteriosis can be found in pathogenetic mechanism, whereby many obstetric and gynecological diseases develop. Most of these diseases lead directly to increased maternal and infant morbidity and mortality, so it is important to understand the reasons for them and the arrangements for their prevention.

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References

  1. 1.

    Kovachev S (2011) Vaginal ecosystem. Akush Ginekol 50(3):41–49

    CAS  Google Scholar 

  2. 2.

    Sobel JD (1999) Is there a protective role for vaginal flora? Curr Infect Dis Rep 1:379–383

    Article  PubMed  Google Scholar 

  3. 3.

    Donders GGG, Basmans E, Dekkersmaecker A, Verecken A, Bulck BV, Spitz B (2000) Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol 182:872–878

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Van De Wijgert JH, Mason PR, Gwanzura L, Mbizvo MT, Chirenje ZM, Iliff V, Shiboski S, Padian NS (2000) Intravaginal practices, vaginal flora disturbances and acquisition of sexually transmitted diseases in Zimbabwean women. J Infect Dis 181:587–594

    Article  Google Scholar 

  5. 5.

    Sewankambo N, Gray RH, Wawer MJ, Paxton L, McNaim D, Wabwire-Mangen F, Serwadda D, Li C, Kiwanuka N, Hillier SL, Rabe L, Gaydos CA, Quinn TC, Konde-Lule J (1997) HIV-1infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet 350:546–550

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, Chohan B, Mandaliya K, Ndinya-Achola JO, Bwayo J, Kreiss J (1999) Vaginal lactobacilli, microbial flora and risk of HIV type 1 and STD acquisition. J Infect Dis 180:1863–1868

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Schmid G, Markowitz L, Joesoef R, Koumans E (2000) Bacterial vaginosis and HIV infection. Sex Transm Inf 76:3–4

    CAS  Article  Google Scholar 

  8. 8.

    Knezevic A, Stepanovic S, Cypic M, Jevtovic D, Ranin J, Jovanovic T (2005) Reduced quantity and hydrogen-peroxide production of vaginal lactobacilli in HIV positive women. Biomed Pharmacother 59(9):521–523

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Charonis G, Larsson PG (2006) Use of pH/whiff test or Quick Vue Advanced pH and Amines test for the diagnosis of bacterial vaginosis and prevention of postabortion PID. Acta Obstet Gynecol Scand 85(7):837–843

    Article  PubMed  Google Scholar 

  10. 10.

    Ness RB, Soper DE, Holley RL, Peipert J, Randall H, Sweet RL, Sondheimer SJ, Hendrix SL, Hillier SL, Amortegui A, Trucco G, Bass DC (2001) PID Evaluation and Clinical Health (PEACH) Study Investigators. Douching and endometritis: results from the PID evaluation and clinical health (PEACH) study. Sex Transm Dis 28(4):240–245

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Lo E, Moore DE, Patton DL, Agnew KJ, Eschenbach DA (2003) Relationship of vaginal bacteria and inflamation with conception and early pregnancy loss following in-vitro fertilization. Infect Dis Obstet Gynecol 11(1):11–17

    Article  Google Scholar 

  12. 12.

    Usui R, Ohkuchi A, Matsubara S, Izumi A, Watanabe T, Suzuki M, Minakami H (2002) Vaginal lactobacilli and preterm birth. J Perinat Med 30(6):458–466

    Article  PubMed  Google Scholar 

  13. 13.

    Verstraelen H, Verhelst R, Roelens K, Claeys G, Weyers S, De Backer E, Vaneechoutte M, Temmerman M (2007) Modified classification of Gram-stained vaginal smears to predict spontaneous preterm birth: a prospective cohort study. Am J Obstet Gynecol 196(6):528.e 1–6

    Article  Google Scholar 

  14. 14.

    Hyman RW, Fukushima M, Diamond L, Kumm J, Giudice L, Davis R (2005) Microbes on the human vaginal epithelium. Proc Natl Acad Sci U S A 102(22):7952–7957

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  15. 15.

    Маrdh PA (1991) The vaginal ecosystem. Am J Obstet Gynecol 165(5):1130–1134

    Google Scholar 

  16. 16.

    Моrse AS. (2010) Classification of bacteria. In Jawetz, Melnick, & Adelberg”s Medical Microbiology. 25th Edition: 42–51

  17. 17.

    Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108(1):4680–4687

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  18. 18.

    Cribby S, Taylor M, Reid G (2008) Vaginal microbiota and the use of probiotics. Hindawi Publishing Corporation. Interdiscip Perspect Infect Dis 4:256–490

    Google Scholar 

  19. 19.

    Lepargneur JP, Rousseau V (2002) Protective role of the Doderlain flora. J Gynecol Obstet Biol Reprod 31:485–494

    CAS  Google Scholar 

  20. 20.

    Redondo-Lopez V, Cook RL, Sobel JD (1990) Emerging role of lactobacilli in the control and maintainance of the vaginal bacterial microflora. Rev Infect Dis 12:856–872

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Döderlein A (1892) Scheidensekret und seine Bedeutung für das Puerperalfieber. Verlag von Eduard Besold, Leipzig

    Google Scholar 

  22. 22.

    Aroutcheva A, Gariti D, Simon M, Shotts S, Faro J, Simoes JA, Gurgius A, Faro S (2001) Defence factors of vaginal lactobacilli. Am J Obstet Gynecol 185(2):375–379

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Catanzaro J, Green L (1997) Microbial ecology and probiotics in human medicine. Alt Med Rev 2(4):296–305

    Google Scholar 

  24. 24.

    Dimitonova SP, Bakalov BV, Aleksandrova-Georgieva RN, Danova ST (2008) Phenotypic and molecular identification of lactobacilli isolated from vaginal secretions. J Microbiol Immunol Infect 41:469–477, 6

    CAS  PubMed  Google Scholar 

  25. 25.

    Stoyancheva GD, Danova ST, Boudakov IY (2006) Molecular identification of vaginal lactobacilli isolated from Bulgarian women. Antonie Van Leeuwenhock 90(3):201–210

    CAS  Article  Google Scholar 

  26. 26.

    Antonio MA, Hawes SE, Hillier SL (1999) The identification of vaginal lactobacillus species and the demographic and microbiologic characteristics of woman colonized by this species. J Infect Dis 180:1950–1956

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Vasquez A, Jakobsson T, Ahrne S, Forsum U, Molin G (2002) Vaginal lactobacillus flora of healthy Swedish woman. J Clin Microbiol 40:2746–2749

    PubMed Central  Article  PubMed  Google Scholar 

  28. 28.

    Zhou X, Bent SJ, Shneider MG, Davis CC, Islam MR, Forney LJ (2004) Characterization of vaginal microbial communities in adult healthy woman using cultivation-independent methods. J Microbial 150:2565–2573

    CAS  Google Scholar 

  29. 29.

    Burton JP, Cadieux PA, Reid G (2003) Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation. Appl Envir Microbiol 69(1):97–101

    CAS  Article  Google Scholar 

  30. 30.

    Reid G, Burton J, Hammond JA, Bruce AW (2004) Nucleic acid based diagnosis of bacterial vaginosis and improved management using probiotic lactobacilli. J Med Food 7:223–228

    Article  PubMed  Google Scholar 

  31. 31.

    Marelli G, Papaelo E, Ferrari A (2004) Lactobacilli for prevention of urogenital infections: a review. Eur Rev Med Pharmacol Sci 8:87–95

    CAS  PubMed  Google Scholar 

  32. 32.

    Todorova M, Buzalov S, Stoianov S (2002) Microbiological investigation of the vaginal flora during pregnancy. Akush Ginekol 41(1):11–14

    Google Scholar 

  33. 33.

    Vitali B, Pugliese C, Biagi E et al (2007) Dynamics of vaginal bacterial communities in women developing bacterial vaginosis, candidias, or no infection, analyzed by PCR-DGGE and real-time PCR. Appl Environ Microbiol 73(18):5731–5741

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  34. 34.

    Bornstein J, Lakovsky Y, Lavi I et al (2001) The classic approach to diagnosis of vulvovaginits: a critical analysis. Infect Dis Obstet Gynecol 9:105–111

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  35. 35.

    Schwiertz A, Taras D, Rusch K, Rusch V (2006) Throwing the dice for the diagnosis of vaginal complaints? Ann Clin Microbiol Antimicrob 5–4:1–7

    Google Scholar 

  36. 36.

    Grimes DA (1986) Deaths due to sexually transmitted diseases. The forgotten component of reproductive mortality. JAMA 255(13):1727–1729

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Division of STD Prevention (DSTDP). Centers for Disease Control and Prevention. Pelvic Inflammatory Disease (PID) - CDC Fact Sheet. www.cdc.gov/std

  38. 38.

    Sivalingam N, Vanitha NS, Loh KY (2007) Managing pelvic inflammatory disease. Med J Malaysia 62(5):425–427

    CAS  PubMed  Google Scholar 

  39. 39.

    Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, Rice P, Richter HE (2005) A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol 162(6):585–590

    Article  PubMed  Google Scholar 

  40. 40.

    Shopova E (2002) Pelvic inflammatory disease—microbial findings. Akush Ginekol 41(5):28–33

    CAS  Google Scholar 

  41. 41.

    Haggerty CL, Hillier SL, Bass DC, Ness RB (2004) Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin Infect Dis 39(7):990–995

    Article  PubMed  Google Scholar 

  42. 42.

    Kaul R, Nagelkerke NJ, Kimani J, Ngugi E, Bwayo JJ, Macdonald KS, Rebbaprgada A, Fonck K, Temmerman M, Ronald AR, Moses S; Kibera HIV Study Group (2007) Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis 196(11):1692–1697

    Article  Google Scholar 

  43. 43.

    Schwebke JR (2005) Abnormal vaginal flora as a biological risk factor for acquisition of HIV infection and sexually transmitted diseases. J Infect Dis 192(8):1315–1317

    Article  PubMed  Google Scholar 

  44. 44.

    Martens MG. (2004) Postoperative infections. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 601–612.

  45. 45.

    Faro C, Faro S (2008) Postoperative pelvic infections. Infect Dis Clin North Am 22(4):653–663

    Article  PubMed  Google Scholar 

  46. 46.

    Park TK, Flock M, Schulz KF, Grimes DA (1985) Preventing febrile complications of suction curettage abortion. Am J Obstet Gynecol 152(3):252–255

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Monif GRG, Baker DA. (2004) Infectious complications associated with legal termination of pregnancy. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 477–481

  48. 48.

    Monif GRG, Baker DA. (2004) Postpartum endometritis/endomyometritis. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 465–470.

  49. 49.

    Duff PW, Ledger W. (2004) Septic shock. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 482–488.

  50. 50.

    Cauci S, Culhane JF, Di Santolo M, McCollum K (2008) Among pregnant women with bacterial vaginosis, the hydrolytic enzymes sialidase and prolidase are positively associated with interleukin-1 beta. Am J Obstet Gynecol 198(1):132. e1–7

    Article  PubMed  Google Scholar 

  51. 51.

    Lee JW, Shin JG, Kim EH, Kang HE, Jim IB, Kim JY, Loo HG, Woo HJ (2004) Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci 5:41–48

    PubMed  Google Scholar 

  52. 52.

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

    Article  Google Scholar 

  53. 53.

    Styriak I, Nemcova R, Chang YH, jung A (2003) Binding of extracellular matrix molecules by probiotic bacteria. Lett Appl Microbiol 37:329–333

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Verbruggen BS, Boon ME, Boon LM (2006) Dysbacteriosis and squamous (pre) neoplasia of immigrants and Dutch women as established in population-based cervical screening. Diagn Cytopathol 34(5):377–381

    Article  PubMed  Google Scholar 

  55. 55.

    Engberts MK, Verbruggen BS, Boon ME, van Haaften M, Heintz AP (2007) Candida and dysbacteriosis: a cytologic, population-based study of 100,605 asymptomatic women concerning cervical carcinogenesis. Cancer 111(5):269–274

    Article  PubMed  Google Scholar 

  56. 56.

    Chancey CJ, Khanna KV, Seegers JF, Zhang GW, Hildreth J, Langan A, Markham RB (2006) Lactobacilli- expressed single-chain variable fragment (scFv) specific for intercellular adhesion molecule 1(ICAM-1) blocks cell-associated HIV-1 transmissionacross a cervical epithelial monolayer. J Immunol 176(9):5627–5636

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Monif GRG, Baker DA. (2004) Understanding the bacteriology of the female genital tract. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 3–7

  58. 58.

    Cauci S (2004) Vaginal immunity in bacterial vaginosis. Curr Infect Dis Rep 6(6):450–456

    Article  PubMed  Google Scholar 

  59. 59.

    Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL (2003) Bacterial vaginosis is a strong predictor of Neisseria gonorrhoae and Chlamydia trachomatis infection. Clin Infect Dis 36(5):663–668

    Article  PubMed  Google Scholar 

  60. 60.

    Reid G, Burton J, Devillard E (2004) The rationale for probiotics in female urogenital healthcare. Med Gen Med 6(1):49

    Google Scholar 

  61. 61.

    Brumbaugh AR, Mobley HLT (2012) Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine. Expert Rev Vaccines 11(6):663–676

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  62. 62.

    Reid G, Bruce AW, Fraser N, Heinemann C, Owen J, Henning B (2001) Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol 30(1):49–52

    CAS  Article  PubMed  Google Scholar 

  63. 63.

    Reid G, Bruce AW (2001) Selection of Lactobacillus strains for urogenital probiotic applications. J Infect Dis 183(S1):S77–S80

    Article  PubMed  Google Scholar 

  64. 64.

    Reid G, Bruce AW (2006) Probiotics to prevent urinary tract infections: the rationale and evidence. World J Urol 24(1):28–32

    Article  PubMed  Google Scholar 

  65. 65.

    Stapleton AE, Au-Yeung M, Hooton TM, Fredricks DN, Roberts PL, Czaja CA, Yarova-Yarovaya Y, Fiedler T, Cox M, Stamm WE (2011) Randomized, placebo-controlled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin Infect Dis 52(10):1212–1217

    PubMed Central  Article  PubMed  Google Scholar 

  66. 66.

    Lee JW, Lee JH, Sung SH, Lee SJ (2013) Preventive effects of Lactobacillus mixture on experimental E. coli urinary tract infection in infant rats. Yonsei Med J 54(2):489–493

    PubMed Central  Article  PubMed  Google Scholar 

  67. 67.

    Monif GRG, Baker DA. (2004) Urinary tract infections in pregnancy. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 511–522

  68. 68.

    Kirjavainen PV, Pautler S, Baroja ML, Anukam K, Crowley K, Carter K, Reid G (2009) Abnormal immunological profile and vaginal microbiota in women prone to urinary tract infections. Clin Vaccine Immunol 16(1):29–36

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  69. 69.

    Marrazzo JM, Wiesenfeld HC, Murray PJ, Busse B, Meyn L, Krohn M, Hillier SL (2006) Risk factors for cervicitis among women with bacterial vaginosis. J Infect Dis 193(5):617–624

    Article  PubMed  Google Scholar 

  70. 70.

    Simhan NH, Caritis SN, Krohn MA, Martinez de Tejada B, Landers DV, Hillier SL (2003) Decreased cervical proinflammatory cytokines permit subsequent upper genital tract infection during pregnancy. Am J Obstet Gynecol 189(2):560–567

    CAS  Article  PubMed  Google Scholar 

  71. 71.

    Marrazzo JM, Martin DH (2007) Management of women with cervicitis. Clin Infect Dis 44:s102–s110

    Article  PubMed  Google Scholar 

  72. 72.

    Galinsky R, Polglase GR, Hooper SB, Black MJ, Moss TJ (2013) The consequences of chorioamnionitis: preterm birth and effects on development. J Pregnancy 2013:412831

    PubMed Central  Article  PubMed  Google Scholar 

  73. 73.

    Ugwumadu A, Manyonda I, Reid F, Hay P (2003) Effect of early clindamycin on late miscarriage and preterm delivery in asymptomatic women with abnormal vaginal flora and bacterial vaginosis: a randomized controlled trial. Lancet 361(9362):983–988

    CAS  Article  PubMed  Google Scholar 

  74. 74.

    Lajos GJ, Passini Junior R, Nomura ML, Amaral E, Pereira BG, Milanez H, Parpinelli MA (2008) Cervical bacterial colonization in women with preterm labor or premature rupture of membranes. Rev Bras Ginecol Obstet 30(8):393–399

    Article  PubMed  Google Scholar 

  75. 75.

    Klebanoff MA, Hillier SL, Nugent RP, MacPherson CA, Hauth JC, Carey JC, Harper M, Wapner RJ, Trout W, Moawad A, Leveno KJ, Miodovnik M, Sibai BM, Vandorsten JP, Dombrowski MP, O'Sullivan MJ, Varner M, Langer O (2005) National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Is bacterial vaginosis a stronger risk factor for preterm birth when it is diagnosed earlier in gestation? Am J Obstet Gynecol 192(2):470–477

    Article  PubMed  Google Scholar 

  76. 76.

    Goldenberg RL, Andrews WW, Hauth JC (2002) Choriodecidual infection and preterm birth. Nutr Rev 60(5pt2):19–25

    Article  Google Scholar 

  77. 77.

    Svare JA, Schmidt H, Hansen BB, Lose G (2007) Bacterial vaginosis in cohort of Danish pregnant women: prevalence and relationship with preterm delivery, low birthweight and perinatal infections. BJOG 114(4):510–511

    Google Scholar 

  78. 78.

    Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B (2002) Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG 109(1):34–43

    Article  PubMed  Google Scholar 

  79. 79.

    Monif GRG, Baker DA (2004) Candida albicans, In Infectious diseases in obstetrics and gynecology, 5th edn. The Parthenon Publishing Group, New York, NY, pp 405–421

    Google Scholar 

  80. 80.

    Hay P, Czeizel AE (2007) Asymptomatic trichomonas and candida colonization and pregnancy outcome. Best Pract Res Clin Obstet Gynecol 21(3):403–409

    Article  Google Scholar 

  81. 81.

    Kim YH, Kim CH, Cho MK, Na JH, Song TB, Oh JS (2006) Hydrogen peroxide-producing lactobacilli in the vaginal flora of pregnant women with preterm labor with intact membranes. Int J Gynecol Obstet 93(1):22–27

    Article  Google Scholar 

  82. 82.

    Saling E, Schreiber M (2005) The lactobacilli-protection system of pregnant women-efficient prevention of premature births by early detection of disturbances. Z Gebutshilfe Neonatol 209(4):128–134

    CAS  Article  Google Scholar 

  83. 83.

    Wilks M, Wiggins R, Whiley A, Hennessy E, Warwick S, Porter H, Corfield A, Miller M (2004) Identification and H2O2 production of vaginal lactobacilli from pregnant woman at high risk of preterm birth and relation with outcome. J Clin Microbiol 42(2):713–717

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  84. 84.

    Garland SM, Ni Chuileannain F, Satzke C, Robins-Browne R (2002) Mechanisms, organisms and markers of infection in pregnancy. J Reprod Immunol 57(1–2):169–183

    CAS  Article  PubMed  Google Scholar 

  85. 85.

    Park JS, Park CW, Lockwood CJ, Norwitz ER (2005) Role of cytokines in preterm labor and birth. Minerva Ginecol 57(4):349–366

    CAS  PubMed  Google Scholar 

  86. 86.

    Sakai M, Ishiyama A, Tabata M, Sasaki Y, Yoneda S, Shiozaki A, Saito S (2004) Relationship between cervical mucus interleukin-8 concentracions and vaginal bacteria in pregnancy. Am J Reprod Immunol 52(2):106–112

    Article  PubMed  Google Scholar 

  87. 87.

    Menon R, Fortunato SJ (2007) Infection and the role of inflammation in preterm premature rupture of the membranes. Best Pract Res Clin Obstet Gynecol 21(3):467–478

    Article  Google Scholar 

  88. 88.

    Monif GRG, Baker DA. (2004) Chorioamnionitis. In Infectious diseases in obstetrics and gynecology. 5th edition. The Parthenon Publishing Group, New York, NY, p 451–461

  89. 89.

    Rezeberga D, Lazdane G, Kroica J, Sokolova L, Donders GG (2008) Placental histological inflammation and reproductive tract infections in a low risk pregnant population in Latvia. Acta Obstet Gynecol Scand 87(3):360–365

    Article  PubMed  Google Scholar 

  90. 90.

    Maharaj D (2007) Purperal pyrexia: a review. Part I. Obstet Gynecol Surv 62(6):393–399

    Article  PubMed  Google Scholar 

  91. 91.

    Lapinsky SE (2013) Obstetric infections. Crit Care Clin 29(3):509–520

    Article  PubMed  Google Scholar 

  92. 92.

    Demirezen S (2003) Bacterial vaginosis: general overview. Mikrobiyol Bul 37(1):99–104

    PubMed  Google Scholar 

  93. 93.

    Romanik M, Martirosian G (2004) Frequency, diagnostic criteria and consequences of bacterial vaginosis in pregnant women. Przegl Epidemiol 58(3):547–553

    PubMed  Google Scholar 

  94. 94.

    Amsel R, Totten PA, Spiegel CA, Chen KCS, Eschenbach D, Holmes KK (1983) Non-specific vaginitis: diagnostic and microbial and epidemiological associations. Am J Med 74:14–22

    CAS  Article  PubMed  Google Scholar 

  95. 95.

    Gardner HL, Burnhill MS. (2004) Infectious vulvovaginitis. In Infectious diseases in obstetrics and gynecology 5th edition; 531–554.

  96. 96.

    Gardner HL, Burnhill BS, Boon ME, Boon LM (2006) Dysbacteriosis and squamous (pre)neoplasia of immigrants and Dutch women as established in population-based cervical screening. Diagn Cytopathol 34(5):377–381

    Article  Google Scholar 

  97. 97.

    Verbruggen BS, Boon ME, Melkerl P, van Haaften M, Heintz AP (2006) Microscopic diagnosis of dysbacteriosis in stained vaginal smears in clinical practice. Diagn Cytopathol 34(10):686–691

    Article  PubMed  Google Scholar 

  98. 98.

    Ison CA, Hay PE (2002) Validation of a simplified grading of Gram stained vaginal smears for use in genitourinary medicine clinics. Sex Transm Infect 78:413–415

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  99. 99.

    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 29:297–301

    PubMed Central  CAS  PubMed  Google Scholar 

  100. 100.

    Ryan KJ, Ray CG. (2010) Principles of laboratory diagnosis of infectious diseases. In Sherris Medical Microbiology. 5th edition: 59–89

  101. 101.

    Dunkelburg WE Jr (1965) Diagnosis of Hemophilus vaginalis vaginitis by Gram-stained smears. Am J Obstet Gynecol 91–998

  102. 102.

    Spiegel CA, Amsel R, Holmes KK (1983) Diagnosis of bacterial vaginosis by direct Gram stain of vaginal fluid. J Clin Microbiol 18:170–177

    PubMed Central  CAS  PubMed  Google Scholar 

  103. 103.

    Keane F, Ison CA, Noble H, Estcourt C (2006) Bacterial vaginosis. Sex Transm Infect 82(4):16–18

    Google Scholar 

  104. 104.

    Devillard E, Burton J, Reid G (2005) Complexity of vaginal microflora as analyzed by PCR denaturing gradient gel electrophoresis in a patient with recurrent bacterial vaginosis. Infect Dis Obstet Gynecol 13(1):25–30

    PubMed Central  CAS  Article  PubMed  Google Scholar 

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Kovachev, S.M. Obstetric and Gynecological Diseases and Complications Resulting from Vaginal Dysbacteriosis. Microb Ecol 68, 173–184 (2014). https://doi.org/10.1007/s00248-014-0414-5

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Keywords

  • Human Immunodeficiency Virus
  • Lactobacillus
  • Cervical Intraepithelial Neoplasia
  • Bacterial Vaginosis
  • Pelvic Inflammatory Disease