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Bacterial vaginosis, aerobic vaginitis, vaginal inflammation and major Pap smear abnormalities

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Abstract

The purpose of this investigation was to evaluate the impact of the vaginal milieu on the presence of abnormal Pap smears and a positive human papilloma virus (HPV) test. A cross-sectional study was conducted between June 2014 and May 2015, evaluating the vaginal discharge by fresh wet mount microscopy and comparing these data with Pap smear findings. Wet mount slides were scored for bacterial vaginosis (BV), aerobic vaginitis (AV), presence of Candida and Trichomonas vaginalis. Cytologic evaluation was done on all Pap smears according to the Bethesda criteria. The cobas© HPV Test (Roche) was performed for HPV detection. A total of 622 cases were evaluated. The mean age of the patients was 41.6 ± 10.65 years (range 21–75). Eighty-three women (13.3 %) had a cytology result worse than low-grade squamous intraepithelial lesion (LSIL). When comparing this group with the one with normal or minor [atypical squamous cells of undetermined significance (ASC-US) or LSIL] Pap smear abnormalities, there were no differences in the presence of Candida (32.5 % vs. 33.2 %, p = 1.0), absence of lactobacilli (38.6 % vs. 32.5 %, p = 0.32) or BV (20.5 % vs. 13.2 %, p = 0.09). On the other hand, moderate or severe inflammation (msI) (41.0 % vs. 28.8 %, p = 0,04), moderate or severe AV (msAV) (16.9 % vs. 7.2 %, p = 0.009) and msAV/BV (37.3 % vs. 20.0 %, p = 0.001) were more common in women with such major cervical abnormalities. No significant association was found between deviations of the vaginal milieu and high-risk HPV infection. The presence of msI or msAV, but not BV, is independently associated with an increased risk of major cervical cytological abnormalities, but not with HPV infection.

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References

  1. Donders GGG, 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. http://www.ncbi.nlm.nih.gov/pubmed/11845812. Accessed May 15, 2015

    Article  PubMed  Google Scholar 

  2. Sobel JD (1994) Desquamative inflammatory vaginitis: a new subgroup of purulent vaginitis responsive to topical 2% clindamycin therapy. Am J Obstet Gynecol 171(5):1215–1220. http://www.ncbi.nlm.nih.gov/pubmed/7977522. Accessed June 29, 2015

    Article  CAS  PubMed  Google Scholar 

  3. Donders G, Bellen G, Rezeberga D (2011) Aerobic vaginitis in pregnancy. BJOG 118(10):1163–1170. doi:10.1111/j.1471-0528.2011.03020.x

    Article  PubMed  Google Scholar 

  4. Newbern EC, Foxman B, Leaman D, Sobel JD (2002) Desquamative inflammatory vaginitis: an exploratory case–control study. Ann Epidemiol 12(5):346–352. http://www.ncbi.nlm.nih.gov/pubmed/12062923. Accessed June 29, 2015

    Article  PubMed  Google Scholar 

  5. Han C, Wu W, Fan A et al (2015) Diagnostic and therapeutic advancements for aerobic vaginitis. Arch Gynecol Obstet 291(2):251–257. doi:10.1007/s00404-014-3525-9

    Article  PubMed  Google Scholar 

  6. Sangkomkamhang US, Lumbiganon P, Prasertcharoensuk W, Laopaiboon M (2015) Antenatal lower genital tract infection screening and treatment programs for preventing preterm delivery. Cochrane Database Syst Rev 2, CD006178. http://www.ncbi.nlm.nih.gov/pubmed/25922860. Accessed April 30, 2015

    PubMed  Google Scholar 

  7. Hauth JC, Macpherson C, Carey JC et al (2003) Early pregnancy threshold vaginal pH and Gram stain scores predictive of subsequent preterm birth in asymptomatic women. Am J Obstet Gynecol 188(3):831–835. http://www.ncbi.nlm.nih.gov/pubmed/12634666. Accessed June 29, 2015

    Article  PubMed  Google Scholar 

  8. Donders GGG (2007) Definition and classification of abnormal vaginal flora. Best Pract Res Clin Obstet Gynaecol 21(3):355–373. doi:10.1016/j.bpobgyn.2007.01.002

    Article  PubMed  Google Scholar 

  9. Donders GGG, Vereecken A, Bosmans E, Spitz B (2003) Vaginal cytokines in normal pregnancy. Am J Obstet Gynecol 189(5):1433–1438. http://www.ncbi.nlm.nih.gov/pubmed/14634582. Accessed June 29, 2015

    Article  CAS  PubMed  Google Scholar 

  10. Nenadić DB, Pavlović MD (2008) Cervical fluid cytokines in pregnant women: relation to vaginal wet mount findings and polymorphonuclear leukocyte counts. Eur J Obstet Gynecol Reprod Biol 140(2):165–170. doi:10.1016/j.ejogrb.2008.02.020

    Article  PubMed  Google Scholar 

  11. Donders GG, Van Calsteren K, Bellen G et al (2009) Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG 116(10):1315–1324. doi:10.1111/j.1471-0528.2009.02237.x

    Article  CAS  PubMed  Google Scholar 

  12. McDonald HM, O’Loughlin JA, Jolley P, Vigneswaran R, McDonald PJ (1991) Vaginal infection and preterm labour. Br J Obstet Gynaecol 98(5):427–435. http://www.ncbi.nlm.nih.gov/pubmed/2059587. Accessed June 30, 2015

    Article  CAS  PubMed  Google Scholar 

  13. Villaseca R, Ovalle A, Amaya F et al (2015) Vaginal infections in a family health clinic in the metropolitan region, Chile. Rev Chilena Infectol 32(1):30–36. doi:10.4067/S0716-10182015000200007

    Article  PubMed  Google Scholar 

  14. Tomusiak A, Heczko PB, Janeczko J, Adamski P, Pilarczyk-Zurek M, Strus M (2013) Bacterial infections of the lower genital tract in fertile and infertile women from the southeastern Poland. Ginekol Pol 84(5):352–358. http://www.ncbi.nlm.nih.gov/pubmed/23819400. Accessed June 29, 2015

    PubMed  Google Scholar 

  15. Bologno R, Díaz YM, Giraudo MC et al (2011) Importance of studying the balance of vaginal content (BAVACO) in the preventive control of sex workers. Rev Argent Microbiol 43(4):246–250. doi:10.1590/S0325-75412011000400002

    PubMed  Google Scholar 

  16. Tansarli GS, Kostaras EK, Athanasiou S, Falagas ME (2013) 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 32(8):977–984. doi:10.1007/s10096-013-1846-4

    Article  CAS  PubMed  Google Scholar 

  17. Donders G, De Wet HG, Hooft P, Desmyter J (1993) Lactobacilli in Papanicolaou smears, genital infections, and pregnancy. Am J Perinatol 10(5):358–361. doi:10.1055/s-2007-994761

    Article  CAS  PubMed  Google Scholar 

  18. Donders GG, Moerman P, De Wet GH, Hooft P, Goubau P (1991) The association between Chlamydia cervicitis, chorioamnionitis and neonatal complications. Arch Gynecol Obstet 249(2):79–85. http://www.ncbi.nlm.nih.gov/pubmed/1953055. Accessed June 30, 2015

    Article  CAS  PubMed  Google Scholar 

  19. Jahic M, Mulavdic M, Hadzimehmedovic A, Jahic E (2013) Association between aerobic vaginitis, bacterial vaginosis and squamous intraepithelial lesion of low grade. Med Arch 67(2):94–96. http://www.ncbi.nlm.nih.gov/pubmed/24341052. Accessed June 21, 2015

    Article  PubMed  Google Scholar 

  20. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F; WHO International Agency for Research on Cancer (2005) Carcinogenicity of human papillomaviruses. Lancet Oncol 6(4):204. http://www.ncbi.nlm.nih.gov/pubmed/15830458. Accessed July 1, 2015

    Article  PubMed  Google Scholar 

  21. Gillet E, Meys JF, Verstraelen H et al (2011) Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis 11(1):10. doi:10.1186/1471-2334-11-10

    Article  PubMed  PubMed Central  Google Scholar 

  22. Clarke MA, Rodriguez AC, Gage JC et al (2012) A large, population-based study of age-related associations between vaginal pH and human papillomavirus infection. BMC Infect Dis 12:33. doi:10.1186/1471-2334-12-33

    Article  PubMed  PubMed Central  Google Scholar 

  23. Donders GG, Vereecken A, Dekeersmaecker A, Van Bulck B, Spitz B (2000) Wet mount microscopy reflects functional vaginal lactobacillary flora better than Gram stain. J Clin Pathol 53(4):308–313. http://www.ncbi.nlm.nih.gov/pubmed/10823128. Accessed July 3, 2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Donders GGG, Larsson PG, Platz-Christensen JJ, Hallén A, van der Meijden W, Wölner-Hanssen P (2009) Variability in diagnosis of clue cells, lactobacillary grading and white blood cells in vaginal wet smears with conventional bright light and phase contrast microscopy. Eur J Obstet Gynecol Reprod Biol 145(1):109–112. doi:10.1016/j.ejogrb.2009.04.012

    Article  CAS  PubMed  Google Scholar 

  25. Donders GGG, Marconi C, Bellen G, Donders F, Michiels T (2015) Effect of short training on vaginal fluid microscopy (wet mount) learning. J Low Genit Tract Dis 19(2):165–169. doi:10.1097/LGT.0000000000000052

    Article  PubMed  Google Scholar 

  26. Nayar R, Wilbur DC (2015) The Pap test and Bethesda 2014. “The reports of my demise have been greatly exaggerated.” (after a quotation from Mark Twain). Acta Cytol 59(2):121–132. doi:10.1159/000381842

    Article  PubMed  Google Scholar 

  27. Gillet E, Meys JFA, Verstraelen H et al (2012) Association between bacterial vaginosis and cervical intraepithelial neoplasia: systematic review and meta-analysis. PLoS One 7(10), e45201. doi:10.1371/journal.pone.0045201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mikamo H, Sato Y, Hayasaki Y et al (1999) Intravaginal bacterial flora in patients with uterine cervical cancer. High incidence of detection of Gardnerella vaginalis. J Infect Chemother 5(2):82–85. doi:10.1007/s101569900002

    Article  PubMed  Google Scholar 

  29. Donders GG (1999) Bacterial vaginosis during pregnancy: screen and treat? Eur J Obstet Gynecol Reprod Biol 83(1):1–4. http://www.ncbi.nlm.nih.gov/pubmed/10221601. Accessed August 7, 2015

    Article  CAS  PubMed  Google Scholar 

  30. Fernandes JV, DE Medeiros Fernandes TAA, DE Azevedo JCV et al (2015) Link between chronic inflammation and human papillomavirus-induced carcinogenesis (Review). Oncol Lett 9(3):1015–1026. doi:10.3892/ol.2015.2884

    PubMed  PubMed Central  Google Scholar 

  31. Adefuye A, Sales K (2012) Regulation of inflammatory pathways in cancer and infectious disease of the cervix. Scientifica (Cairo) 2012, 548150. doi:10.6064/2012/548150

    Google Scholar 

  32. Boccardo E, Lepique AP, Villa LL (2010) The role of inflammation in HPV carcinogenesis. Carcinogenesis 31(11):1905–1912. doi:10.1093/carcin/bgq176

    Article  CAS  PubMed  Google Scholar 

  33. Behbakht K, Friedman J, Heimler I, Aroutcheva A, Simoes J, Faro S (2002) Role of the vaginal microbiological ecosystem and cytokine profile in the promotion of cervical dysplasia: a case–control study. Infect Dis Obstet Gynecol 10(4):181–186. doi:10.1155/S1064744902000200

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kemp TJ, Hildesheim A, García-Piñeres A et al (2010) Elevated systemic levels of inflammatory cytokines in older women with persistent cervical human papillomavirus infection. Cancer Epidemiol Biomarkers Prev 19(8):1954–1959. doi:10.1158/1055-9965.EPI-10-0184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Iwata T, Fujii T, Morii K et al (2015) Cytokine profile in cervical mucosa of Japanese patients with cervical intraepithelial neoplasia. Int J Clin Oncol 20(1):126–133. doi:10.1007/s10147-014-0680-8

    Article  CAS  PubMed  Google Scholar 

  36. Castle PE, Hillier SL, Rabe LK et al (2001) An association of cervical inflammation with high-grade cervical neoplasia in women infected with oncogenic human papillomavirus (HPV). Cancer Epidemiol Biomarkers Prev 10(10):1021–1027. http://www.ncbi.nlm.nih.gov/pubmed/11588127. Accessed July 5, 2015

    CAS  PubMed  Google Scholar 

  37. Marconi C, Donders GGG, Bellen G, Brown DR, Parada CMGL, Silva MG (2013) Sialidase activity in aerobic vaginitis is equal to levels during bacterial vaginosis. Eur J Obstet Gynecol Reprod Biol 167(2):205–209. doi:10.1016/j.ejogrb.2012.12.003

    Article  CAS  PubMed  Google Scholar 

  38. Friel G, Liu CS, Kolomeyevskaya NV et al (2015) Aspirin and acetaminophen use and the risk of cervical cancer. J Low Genit Tract Dis 19(3):189–193. doi:10.1097/LGT.0000000000000104

    Article  PubMed  PubMed Central  Google Scholar 

  39. Mitchell A, Newton JM, Brite K et al (2007) Cyclooxygenase 2 expression in cervical intraepithelial neoplasia and vulvar cancer. J Low Genit Tract Dis 11(2):80–85

    Article  PubMed  Google Scholar 

  40. Linhares IM, Summers PR, Larsen B, Giraldo PC, Witkin SS (2011) Contemporary perspectives on vaginal pH and lactobacilli. Am J Obstet Gynecol 204(2):120.e1–120.e5. doi:10.1016/j.ajog.2010.07.010

    Article  Google Scholar 

  41. Mead PB (1978) Cervical-vaginal flora of women with invasive cervical cancer. Obstet Gynecol 52(5):601–604. http://www.ncbi.nlm.nih.gov/pubmed/364358. Accessed August 7, 2015

    CAS  PubMed  Google Scholar 

  42. Pabich WL, Fihn SD, Stamm WE, Scholes D, Boyko EJ, Gupta K (2003) Prevalence and determinants of vaginal flora alterations in postmenopausal women. J Infect Dis 188(7):1054–1058. doi:10.1086/378203

    Article  PubMed  Google Scholar 

  43. Witkin SS, Linhares IM, Giraldo P (2007) Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol 21(3):347–354. doi:10.1016/j.bpobgyn.2006.12.004

    Article  PubMed  Google Scholar 

  44. Yang XL, Yang HX, Duan T et al (2009) Vaginal microflora and relevant factors in puerperium. Zhonghua Fu Chan Ke Za Zhi 44(7):496–499. http://www.ncbi.nlm.nih.gov/pubmed/19957547. Accessed August 7, 2015

    PubMed  Google Scholar 

  45. Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S (2015) Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol 6:81. doi:10.3389/fphys.2015.00081

    Article  PubMed  PubMed Central  Google Scholar 

  46. Donders GGG, Depuydt CE, Bogers J-P, Vereecken AJ (2013) Association of Trichomonas vaginalis and cytological abnormalities of the cervix in low risk women. PLoS One 8(12), e86266. doi:10.1371/journal.pone.0086266

    Article  PubMed  PubMed Central  Google Scholar 

  47. Güdücü N, Gönenç G, Işçi H, Yiğiter AB, Başsüllü N, Dünder I (2012) Clinical importance of detection of bacterial vaginosis, Trichomonas vaginalis, Candida albicans and actinomyces in papanicolaou smears. Clin Exp Obstet Gynecol 39(3):333–336. http://www.ncbi.nlm.nih.gov/pubmed/23157037. Accessed August 7, 2015

    PubMed  Google Scholar 

  48. Heller DS, Weiss G, Bittman S, Goldsmith L (2015) Does a diagnosis of atrophic vaginitis on Papanicolaou test signify the presence of inflammation? Menopause 22(8):814–815. doi:10.1097/GME.0000000000000393

    Article  PubMed  Google Scholar 

  49. Donders GGG, Berger J, Heuninckx H, Bellen G, Cornelis A (2011) Vaginal flora changes on Pap smears after insertion of levonorgestrel-releasing intrauterine device. Contraception 83(4):352–356. doi:10.1016/j.contraception.2010.08.007

    Article  CAS  PubMed  Google Scholar 

  50. Smith WL, Hedges SR, Mordechai E et al (2014) Cervical and vaginal flora specimens are highly concordant with respect to bacterial vaginosis-associated organisms and commensal lactobacillus species in women of reproductive age. J Clin Microbiol 52(8):3078–3081. doi:10.1128/JCM.00795-14

    Article  PubMed  PubMed Central  Google Scholar 

  51. Khatoon R, Jahan N, Ahmad S, Khan HM, Rabbani T (2015) Comparison of four diagnostic techniques for detection of Trichomonas vaginalis infection in females attending tertiary care hospital of North India. Indian J Pathol Microbiol 58(1):36–39. doi:10.4103/0377-4929.151172

    Article  PubMed  Google Scholar 

  52. Bro F (1989) The diagnosis of Candida vaginitis in general practice. Scand J Prim Health Care 7(1):19–22. http://www.ncbi.nlm.nih.gov/pubmed/2657952. Accessed August 10, 2015

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Gynecology and Obstetrics, Centro Hospitalar de São João, Alameda Prof. Hernâni Monteiro, 4200, Porto, Portugal

    P. Vieira-Baptista, J. Lima-Silva, C. Pinto & J. Beires

  2. LAP—Laboratório de Anatomia Patológica, Unilabs, Porto, Portugal

    C. Saldanha

  3. Faculty of Health Sciences, University of Beira Interior, Covilhã, Portugal

    J. Martinez-de-Oliveira

  4. Department of Children and Women’s Health, Centro Hospitalar da Cova da Beira, Covilhã, Portugal

    J. Martinez-de-Oliveira

  5. Department of Obstetrics and Gynecology, University Hospital Antwerp, Antwerp, Belgium

    G. Donders

  6. Femicare Clinical Research for Women, Tienen, Belgium

    G. Donders

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  1. P. Vieira-Baptista
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Correspondence to P. Vieira-Baptista.

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Vieira-Baptista, P., Lima-Silva, J., Pinto, C. et al. Bacterial vaginosis, aerobic vaginitis, vaginal inflammation and major Pap smear abnormalities. Eur J Clin Microbiol Infect Dis 35, 657–664 (2016). https://doi.org/10.1007/s10096-016-2584-1

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