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Mycoplasma hominis and Gardnerella vaginalis display a significant synergistic relationship in bacterial vaginosis

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Abstract

Gardnerella vaginalis plays an important role in bacterial vaginosis (BV,) while the role of genital Mollicutes is less obvious. The diagnosis of BV by use of the current Gram stain Nugent score is also suboptimal for defining the role of Mollicutes that lack a cell wall. Since bacterial load and diversity is an important prerequisite for BV, real-time quantitative polymerase chain reaction (qPCR) assays enable these to be assessed. The purpose of this study was to define the role of genital Mollicutes and potential patterns of synergy with G. vaginalis in women with BV. Vaginal swabs from 130 women categorised by Nugent score as BV (n = 28), intermediate (n = 22) and non-BV (n = 80) were tested against four qPCR TaqMan assays targeting G. vaginalis, Mycoplasma hominis, M. genitalium, Ureaplasma urealyticum and U. parvum. Statistical analyses were used to compare bacterial prevalence and load between the three groups of women. Mycoplasma hominis and G. vaginalis co-infection was significantly more common in BV (60.7 %) compared to intermediate (36.4 %) and non-BV (8.8 %) Nugent scores (p < 0.001). Significantly higher loads of M. hominis (p = 0.001) and G. vaginalis (p < 0.001) were detected in women with BV and the respective loads in M. hominis and G. vaginalis co-infections displayed a significant positive correlation (p < 0.001; r = 0.60). No significant associations were seen with the other Mollicutes. The findings strengthen the evidence of a role for M. hominis in BV and a potential synergy with G. vaginalis. This synergy could be an important trigger of the condition and sexual contact the conduit for the transmission of an otherwise commensal bacterium that could initiate it.

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References

  1. Mania-Pramanik J, Kerkar SC, Salvi VS (2009) Bacterial vaginosis: a cause of infertility? Int J STD AIDS 20(11):778–781

    Article  CAS  PubMed  Google Scholar 

  2. Oakeshott P, Hay P, Hay S, Steinke F, Rink E, Kerry S (2002) Association between bacterial vaginosis or chlamydial infection and miscarriage before 16 weeks’ gestation: prospective community based cohort study. BMJ (Clin Res Ed) 325(7376):1334

    Article  Google Scholar 

  3. 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(3):375–390

    Article  PubMed  Google Scholar 

  4. Balashov SV, Mordechai E, Adelson ME, Gygax SE (2014) Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR. J Med Microbiol 63(Pt 2):162–175

    Article  CAS  PubMed  Google Scholar 

  5. Fredricks DN, Fiedler TL, Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353(18):1899–1911

    Article  CAS  PubMed  Google Scholar 

  6. Lamont RF, Sobel JD, Akins RA, Hassan SS, Chaiworapongsa T, Kusanovic JP, Romero R (2011) The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG: Int J Obstet Gynaecol 118(5):533–549

    Article  CAS  Google Scholar 

  7. Cox C, McKenna JP, Watt AP, Coyle PV (2015) New assay for Gardnerella vaginalis loads correlates with Nugent scores and has potential in the diagnosis of bacterial vaginosis. J Med Microbiol 64(9):978–984. doi:10.1099/jmm.0.000118

    Article  PubMed  Google Scholar 

  8. Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y, Li L, Nelson KE, Xia Y, Xiang C (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11:488

    Article  PubMed Central  PubMed  Google Scholar 

  9. Haggerty CL, Totten PA, Ferris M, Martin DH, Hoferka S, Astete SG, Ondondo R, Norori J, Ness RB (2009) Clinical characteristics of bacterial vaginosis among women testing positive for fastidious bacteria. Sex Transm Infect 85(4):242–248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Africa CW, Nel J, Stemmet M (2014) Anaerobes and bacterial vaginosis in pregnancy: virulence factors contributing to vaginal colonisation. Int J Environ Res Public Health 11(7):6979–7000

    Article  PubMed Central  PubMed  Google Scholar 

  11. Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S, Hale LP, Lochs H (2005) Adherent biofilms in bacterial vaginosis. Obstet Gynecol 106(5 Pt 1):1013–1023

    Article  PubMed  Google Scholar 

  12. Swidsinski A, Doerffel Y, Loening-Baucke V, Swidsinski S, Verstraelen H, Vaneechoutte M, Lemm V, Schilling J, Mendling W (2010) Gardnerella biofilm involves females and males and is transmitted sexually. Gynecol Obstet Invest 70(4):256–263

    Article  PubMed  Google Scholar 

  13. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, Ferris MJ (2011) Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS One 6(10):e26732

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Muzny CA, Schwebke JR (2015) Accuracy of self-report of sexual activity among adolescent girls: implications for interpretation of vaginal flora patterns. mBio 6(3):e00819. doi:10.1128/mBio.00819-15

    Article  PubMed Central  PubMed  Google Scholar 

  15. Swidsinski A, Loening-Baucke V, Swidsinski S, Verstraelen H (2015) Polymicrobial Gardnerella biofilm resists repeated intravaginal antiseptic treatment in a subset of women with bacterial vaginosis: a preliminary report. Arch Gynecol Obstet 291(3):605–609

    Article  CAS  PubMed  Google Scholar 

  16. Swidsinski A, Verstraelen H, Loening-Baucke V, Swidsinski S, Mendling W, Halwani Z (2013) Presence of a polymicrobial endometrial biofilm in patients with bacterial vaginosis. PLoS One 8(1):e53997

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Patterson JL, Girerd PH, Karjane NW, Jefferson KK (2007) Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Am J Obstet Gynecol 197(2):170.e1–170.e7

    Article  Google Scholar 

  18. 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(2):297–301

    PubMed Central  CAS  PubMed  Google Scholar 

  19. Mohammadzadeh F, Dolatian M, Jorjani M, Alavi Majd H (2014) Diagnostic value of Amsel’s clinical criteria for diagnosis of bacterial vaginosis. Glob J Health Sci 7(3):8–14

    PubMed  Google Scholar 

  20. Rodrigues FS, Peixoto S, Adami F, da Costa Aguiar Alves B, de Sousa Gehrke F, Azzalis LA, de Campos Junqueira VB, Fonseca FL (2015) Proposal of a new cutoff for Nugent criteria in the diagnosis of bacterial vaginosis. J Microbiol Methods 115:144–146

    Article  PubMed  Google Scholar 

  21. 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(1):33–43

    Article  CAS  PubMed  Google Scholar 

  22. Begum N, Muazzam N, Shamsuzzaman SM, Chowdhury A, Rashid A, Islam D (2010) Diagnosis of bacterial vaginosis by Acridine orange staining and its comparison to conventional methods and association of Gardnerella vaginalis with bacterial vaginosis. Bangladesh J Med Microbiol 4(1):37–42

    Google Scholar 

  23. Oakeshott P, Aghaizu A, Hay P, Reid F, Kerry S, Atherton H, Simms I, Taylor-Robinson D, Dohn B, Jensen JS (2010) Is Mycoplasma genitalium in women the “New Chlamydia?” a community-based prospective cohort study. Clin Infect Dis: Off Publ Infect Dis Soc Am 51(10):1160–1166

    Article  Google Scholar 

  24. Owen MK, Clenney TL (2004) Management of vaginitis. Am Fam Physician 70(11):2125–2132

    PubMed  Google Scholar 

  25. Lawton BA, Rose SB, Bromhead C, Gaitanos LA, MacDonald EJ, Lund KA (2008) High prevalence of Mycoplasma genitalium in women presenting for termination of pregnancy. Contraception 77(4):294–298

    Article  PubMed  Google Scholar 

  26. Manhart LE, Holmes KK, Hughes JP, Houston LS, Totten PA (2007) Mycoplasma genitalium among young adults in the United States: an emerging sexually transmitted infection. Am J Public Health 97(6):1118–1125

    Article  PubMed Central  PubMed  Google Scholar 

  27. Keane FE, Thomas BJ, Gilroy CB, Renton A, Taylor-Robinson D (2000) The association of Chlamydia trachomatis and Mycoplasma genitalium with non-gonococcal urethritis: observations on heterosexual men and their female partners. Int J STD AIDS 11(7):435–439

    Article  CAS  PubMed  Google Scholar 

  28. Lee SE, Romero R, Kim EC, Yoon BH (2009) A high Nugent score but not a positive culture for genital mycoplasmas is a risk factor for spontaneous preterm birth. J Matern Fetal Neonatal Med: Off J Eur Assoc Perinat Med Fed Asia Ocean Perinatal Soc Int Soc Perinat Obstetricians 22(3):212–217

    Article  Google Scholar 

  29. Rosenstein IJ, Morgan DJ, Sheehan M, Lamont RF, Taylor-Robinson D (1996) Bacterial vaginosis in pregnancy: distribution of bacterial species in different gram-stain categories of the vaginal flora. J Med Microbiol 45(2):120–126

    Article  CAS  PubMed  Google Scholar 

  30. Thorsen E, Aanderud L, Aasen TB (1998) Effects of a standard hyperbaric oxygen treatment protocol on pulmonary function. Eur Respir J 12(6):1442–1445

    Article  CAS  PubMed  Google Scholar 

  31. Vancutsem E, Soetens O, Breugelmans M, Foulon W, Naessens A (2011) Modified real-time PCR for detecting, differentiating, and quantifying Ureaplasma urealyticum and Ureaplasma parvum. J Mol Diagn: JMD 13(2):206–212

    Article  PubMed Central  PubMed  Google Scholar 

  32. Chalker VJ, Jordan K, Ali T, Ison C (2009) Real-time PCR detection of the mg219 gene of unknown function of Mycoplasma genitalium in men with and without non-gonococcal urethritis and their female partners in England. J Med Microbiol 58(Pt 7):895–899

    Article  CAS  PubMed  Google Scholar 

  33. Pascual A, Jaton K, Ninet B, Bille J, Greub G (2010) New diagnostic real-time PCR for specific detection of mycoplasma hominis DNA. Int J Microbiol. doi:10.1155/2010/317512

    PubMed Central  PubMed  Google Scholar 

  34. Hay P, Ugwumadu A (2009) Detecting and treating common sexually transmitted diseases. Best Pract Res Clin Obstet Gynaecol 23(5):647–660

    Article  PubMed  Google Scholar 

  35. Liu CM, Hungate BA, Tobian AA, Ravel J, Prodger JL, Serwadda D, Kigozi G, Galiwango RM, Nalugoda F, Keim P, Wawer MJ, Price LB, Gray RH (2015) Penile microbiota and female partner bacterial vaginosis in Rakai, Uganda. mBio 6(3):e00589. doi:10.1128/mBio.00589-15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Liu CM, Hungate BA, Tobian AA, Serwadda D, Ravel J, Lester R, Kigozi G, Aziz M, Galiwango RM, Nalugoda F, Contente-Cuomo TL, Wawer MJ, Keim P, Gray RH, Price LB (2013) Male circumcision significantly reduces prevalence and load of genital anaerobic bacteria. mBio 4(2):e00076

    Article  PubMed Central  PubMed  Google Scholar 

  37. Fethers K, Marks C, Mindel A, Estcourt CS (2000) Sexually transmitted infections and risk behaviours in women who have sex with women. Sex Transm Infect 76(5):345–349

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Bradshaw CS, Walker SM, Vodstrcil LA, Bilardi JE, Law M, Hocking JS, Fethers KA, Fehler G, Petersen S, Tabrizi SN, Chen MY, Garland SM, Fairley CK (2014) The influence of behaviors and relationships on the vaginal microbiota of women and their female partners: the WOW Health Study. J Infect Dis 209(10):1562–1572

    Article  PubMed  Google Scholar 

  39. Marrazzo JM, Antonio M, Agnew K, Hillier SL (2009) Distribution of genital Lactobacillus strains shared by female sex partners. J Infect Dis 199(5):680–683

    Article  PubMed Central  PubMed  Google Scholar 

  40. Schwebke JR, Desmond R (2007) Natural history of asymptomatic bacterial vaginosis in a high-risk group of women. Sex Transm Dis 34(11):876–877

    Article  PubMed  Google Scholar 

  41. Verstraelen H, Verhelst R, Vaneechoutte M, Temmerman M (2010) The epidemiology of bacterial vaginosis in relation to sexual behaviour. BMC Infect Dis 10:81

    Article  PubMed Central  PubMed  Google Scholar 

  42. Gray RH, Kigozi G, Serwadda D, Makumbi F, Nalugoda F, Watya S, Moulton L, Chen MZ, Sewankambo NK, Kiwanuka N, Sempijja V, Lutalo T, Kagayii J, Wabwire-Mangen F, Ridzon R, Bacon M, Wawer MJ (2009) The effects of male circumcision on female partners’ genital tract symptoms and vaginal infections in a randomized trial in Rakai, Uganda. Am J Obstet Gynecol 200(1):42.e1-42.e7

    PubMed Central  Google Scholar 

  43. Castro J, Alves P, Sousa C, Cereija T, França Â, Jefferson KK, Cerca N (2015) Using an in-vitro biofilm model to assess the virulence potential of bacterial vaginosis or non-bacterial vaginosis Gardnerella vaginalis isolates. Sci Rep 5:11640

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the support of Randox Laboratories Ltd, who sponsored Ciara Cox and also thank Innovate UK for co-funding this study.

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Correspondence to C. Cox.

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Cox, C., Watt, A.P., McKenna, J.P. et al. Mycoplasma hominis and Gardnerella vaginalis display a significant synergistic relationship in bacterial vaginosis. Eur J Clin Microbiol Infect Dis 35, 481–487 (2016). https://doi.org/10.1007/s10096-015-2564-x

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