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Malcolm, K. The Vaginal Microbiota. Encyclopedia. Available online: https://encyclopedia.pub/entry/11178 (accessed on 16 April 2024).
Malcolm K. The Vaginal Microbiota. Encyclopedia. Available at: https://encyclopedia.pub/entry/11178. Accessed April 16, 2024.
Malcolm, Karl. "The Vaginal Microbiota" Encyclopedia, https://encyclopedia.pub/entry/11178 (accessed April 16, 2024).
Malcolm, K. (2021, June 23). The Vaginal Microbiota. In Encyclopedia. https://encyclopedia.pub/entry/11178
Malcolm, Karl. "The Vaginal Microbiota." Encyclopedia. Web. 23 June, 2021.
The Vaginal Microbiota
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This entry is adapted from the peer-reviewed paper 10.3390/pharmaceutics13050751

The human vagina is a useful and accessible route for local and systemic administration of drugs, and particularly for clinical indications that are directly associated with women’s sexual and reproductive health. Spurred in part by progressive societal changes to attitudes, behaviors and stigmas around the human vagina, the past twenty years has witnessed increased interest among users, clinicians, and the pharmaceutical industry in developing and using vaginal products for therapeutic benefit.

controlled release drug delivery system silicone elastomer

1. Lactobacillus spp.

In humans, Lactobacillus spp. are the dominant microorganism in the healthy human vagina, found in a relative abundance of greater than 70%. Yet, lactobacilli are rarely found in greater than 1% abundance in the vaginal environment of other mammals [1]. Lactobacilli are Gram-positive, rod-shaped, anaerobic bacteria that produce lactic acid via their metabolic action on the various glycogen breakdown products found in the vagina and formed under the influence of estrogen. It is this lactic acid production that results in a healthy vaginal pH of ~4.2 [2][3]. Lactobacilli will adhere to vaginal epithelial cells, out-competing other microorganisms for surface real estate. They also produce soluble compounds, including bacteriocins, that are toxic to other bacterial species [4]. These attributes of lactobacilli contribute to their dominance in the human vagina and protect against infection with pathogenic microorganisms without themselves inducing inflammation [3]. However, studies have shown that not all lactobacilli are equal in this protective capacity. Lactobacillus crispatus, Lactobacillus gasseri, Lactobacillus iners, and Lactobacillus jensenii have been reported as the most frequently occurring species in the healthy vagina [5]. L. crispatus is associated with a strong protective and anti-inflammatory capabilities, whereas L. iners is easily displaced by other species, and is often associated with a dysbiotic environment. The picture is less clear for L. gasseri and L. jensenii, although these species appear to be less abundant in states of vaginal dysbiosis [6].

2. Gardnerella vaginalis

G. vaginalis, first described as Haemophilus vaginalis, a Gram-variable facultatively anaerobic rod, was proposed over half a century ago as the sole etiological agent of bacterial vaginosis (BV), the most common vaginal infection in women of reproductive age [7]. However, its presence in the vaginal microbiome of healthy women has since cast doubt on its virulence and role as a putative pathogen [8]. It has been detected at rates of 14% to 69% in asymptomatic women [9] and has been isolated as the dominant vaginal microorganism of almost all women with BV [10][11][12]. BV is associated with malodorous vaginal discharge, increased vaginal pH, and the presence of “clue cells” (vaginal epithelial cells with a heavy coating of bacteria, that can be observed microscopically in vaginal fluid). These clue cells are explained by the ability of G. vaginalis to form biofilms on the vaginal epithelium, providing convincing evidence for the role of the species in this condition [13]. However, its colonization in asymptomatic women, combined with phenotypic variability and limited taxonomic refinement, results in a somewhat complicated and incomplete understanding of the precise role of G. vaginalis within the vaginal microbiome.
G. vaginalis has been well known to display genotypic and phenotypic diversity with differing virulence potential, and at least four ‘clades’ (or subgroups) within the species are differentially associated with different clinical outcomes [14][15]. In recent years, biotyping and molecular methods have been applied to categorize these subgroups. In 2019, Vaneechoutte et al. formally proposed three new and distinct species based on whole-genome sequencing and biochemical analysis: Gardnerella piotii, Gardnerella swidsinskii, and Gardnerella leopoldii [13].
BV is also associated with increased risk of HIV infection and transmission [16][17][18][19]. Several factors are likely at play here, including decreased levels of hydrogen peroxide-producing lactobacilli, production of mucin-degrading enzymes, increased influx of HIV target cells, elevated levels of proinflammatory cytokines, elevated vaginal pH, and increased expression of HIV in the lower genital tract. Novel drug-releasing ring formulations to treat or prevent recurrence of BV, including multipurpose devices that simultaneously administer antiretrovirals, have been reported [20][21].

3. Atopobium vaginae and Prevotella spp.

Another species strongly associated with BV is the strict anaerobe Atopobium vaginae, which is resistant to metronidazole and may explain why some women suffer from recurrent BV after treatment with this antibiotic. Studies have reported that A. vaginae is present in up to 86% of BV samples [22]. The anaerobic species Prevotella spp. is also negatively associated with vaginal health [23]; it has been suggested that colonization with Prevotella—the most heritable vaginal bacteria—is strongly associated with host genetics [24]. Women with abundant Prevotella in their vagina have higher levels of pro-inflammatory cytokines and increased activation of Toll-like receptors leading to downstream signaling for immune surveillance [24]. Interestingly, there is a strong association between obesity and greater abundance of both gut and vaginal Prevotella compared to individuals with BMIs in the healthy range [24][25].

4. Candida albicans

Candida albicans is a polymorphic fungus and a member of the normal human microbiome, residing for the most part harmlessly in the oropharynx, gastrointestinal tract, on the skin, and in the vagina of 20–30% of healthy women [26]. The yeast form (blastoconidia) is typically associated with asymptomatic colonization and transmission, while the hyphal (mycelial) form contributes to adherence and mucosal invasion seen in symptomatic disease [27]. During the switching from a commensal to a vaginal pathogen, Candida spp. will also produce a range of extracellular enzymes (including proteases, phospholipases, and hemolysins) that are implicated in adherence to and invasion of vaginal epithelial cells [26]. Another important virulence factor is the ability of Candida spp. to form biofilms that attach irreversibly to both biotic and abiotic surfaces; this trait is highly dependent on yeast to hyphal morphogenesis [26][28]. Vulvovaginal candidiasis (VVC) is defined as symptoms of inflammation caused by an overgrowth of Candida spp., particularly C. albicans, without other infectious etiologies [22]. It is estimated that approximately 75% of all women suffer from VVC at least once in their lifetime [29] and it is a common side effect of treatment with broad spectrum antibiotics, with the eradication of commensal bacteria allowing C. albicans to dominate the vaginal microbiota [30].

References

  1. Miller, E.A.; Beasley, D.A.E.; Dunn, R.R.; Archie, E.A. Lactobacilli dominance and vaginal pH: Why is the human vaginal microbiome unique? Front. Microbiol. 2016, 7, 1–13.
  2. Greenbaum, S.; Greenbaum, G.; Moran-Gilad, J.; Weintruab, A.Y. Ecological dynamics of the vaginal microbiome in relation to health and disease. Am. J. Obstet. Gynecol. 2019, 220, 324–335.
  3. Witkin, S.; Linhares, I. Why do lactobacilli dominate the human vaginal microbiota? BJOG Int. J. Obstet. Gynaecol. 2017, 124, 606–611.
  4. Aroutcheva, A.; Gariti, D.; Simon, M.; Shott, S.; Faro, J.; Simoes, J.A.; Gurguis, A.; Faro, S. Defense factors of vaginal lactobacilli. Am. J. Obstet. Gynecol. 2001, 185, 375–379.
  5. Vásquez, A.; Jakobsson, T.; Ahrné, S.; Forsum, U.; Molin, G. Vaginal lactobacillus flora of healthy Swedish women. J. Clin. Microbiol. 2002, 40, 2746–2749.
  6. Van de Wijgert, J.H.H.M.; Jespers, V. The global health impact of vaginal dysbiosis. Res. Microbiol. 2017, 168, 859–864.
  7. Gardner, H.L.; Dukes, C.D. Haemophilus vaginalis vaginitis. Am. J. Obstet. Gynecol. 1955, 69, 962–976.
  8. Castro, J.; Machado, D.; Cerca, N. Unveiling the role of Gardnerella vaginalis in polymicrobial Bacterial Vaginosis biofilms: The impact of other vaginal pathogens living as neighbors. ISME J. 2019, 13, 1306–1317.
  9. Mikamo, H.; Sato, Y.; Hayasaki, Y.; Hua, Y.X.; Tamaya, T. Vaginal microflora in healthy women with Gardnerella vaginalis. J. Infect. Chemother. 2000, 6, 173–177.
  10. Fredricks, D.N.; Fiedler, T.L.; Thomas, K.K.; Oakley, B.B.; Marrazzo, J.M. Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J. Clin. Microbiol. 2007, 45, 3270–3276.
  11. Zozaya-Hinchliffe, M.; Lillis, R.; Martin, D.H.; Ferris, M.J. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J. Clin. Microbiol. 2010, 48, 1812–1819.
  12. Janulaitiene, M.; Paliulyte, V.; Grinceviciene, S.; Zakareviciene, J.; Vladisauskiene, A.; Marcinkute, A.; Pleckaityte, M. Prevalence and distribution of Gardnerella vaginalis subgroups in women with and without bacterial vaginosis. BMC Infect. Dis. 2017, 17, 394.
  13. Vaneechoutte, M.; Guschin, A.; Van Simaey, L.; Gansemans, Y.; Van Nieuwerburgh, F.; Cools, P. Emended description of Gardnerella vaginalis and description of Gardnerella leopoldii sp. nov., Gardnerella piotii sp. nov. and Gardnerella swidsinskii sp. nov., with delineation of 13 genomic species within the genus Gardnerella. Int. J. Syst. Evol. Microbiol. 2019, 69, 679–687.
  14. Hill, J.E.; Albert, A.Y.K. Resolution and Cooccurrence Patterns of Gardnerella leopoldii, G. swidsinskii, G. piotii, and G. vaginalis within the Vaginal Microbiome. Infect. Immun. 2019, 87.
  15. Janulaitiene, M.; Gegzna, V.; Baranauskiene, L.; Bulavaitė, A.; Simanavicius, M.; Pleckaityte, M. Phenotypic characterization of Gardnerella vaginalis subgroups suggests differences in their virulence potential. PLoS ONE 2018, 13, e0200625.
  16. McKinnon, L.R.; Achilles, S.L.; Bradshaw, C.S.; Burgener, A.; Crucitti, T.; Fredricks, D.N.; Jaspan, H.B.; Kaul, R.; Kaushic, C.; Klatt, N.; et al. The evolving facets of bacterial vaginosis: Implications for HIV transmission. AIDS Res. Hum. Retrovir. 2019, 35, 219–228.
  17. Atashili, J.; Poole, C.; Ndumbe, P.M.; Adimora, A.A.; Smith, J.S. Bacterial vaginosis and HIV acquisition: A meta-analysis of published studies. AIDS 2008, 22, 1493–1501.
  18. Low, N.; Chersich, M.F.; Schmidlin, K.; Egger, M.; Francis, S.C.; van de Wijgert, J.H.H.M.; Hayes, R.J.; Baeten, J.M.; Brown, J.; Delany-Moretlwe, S.; et al. Intravaginal practices, bacterial vaginosis, and HIV infection in women: Individual participant data meta-analysis. PLoS Med. 2011, 8, e1000416.
  19. Cohen, C.R.; Lingappa, J.R.; Baeten, J.M.; Ngayo, M.O.; Spiegel, C.A.; Hong, T.; Donnell, D.; Celum, C.; Kapiga, S.; Delany, S.; et al. Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: A prospective cohort analysis among african couples. PLoS Med. 2012, 9, e1001251.
  20. Verstraete, G.; Vandenbussche, L.; Kasmi, S.; Nuhn, L.; Brouckaert, D.; Van Renterghem, J.; Grymonpré, W.; Vanhoorne, V.; Coenye, T.; De Geest, B.G.G.; et al. Thermoplastic polyurethane-based intravaginal rings for prophylaxis and treatment of (recurrent) bacterial vaginosis. Int. J. Pharm. 2017, 529, 218–226.
  21. Pathak, M.; Turner, M.; Palmer, C.; Coombes, A.G. Evaluation of polycaprolactone matrices for the intravaginal delivery of metronidazole in the treatment of bacterial vaginosis. J. Biomater. Appl. 2014, 29, 354–363.
  22. Verhelst, R.; Verstraelen, H.; Claeys, G.; Verschraegen, G.; Van Simaey, L.; De Ganck, C.; De Backer, E.; Temmerman, M.; Vaneechoutte, M. Comparison between Gram stain and culture for the characterization of vaginal microflora: Definition of a distinct grade that resembles grade I microflora and revised categorization of grade I microflora. BMC Microbiol. 2005, 5, 61.
  23. Onderdonk, A.B.; Delaney, M.L.; Fichorova, R.N. The Human Microbiome during Bacterial Vaginosis. Clin. Microbiol. Rev. 2016, 29, 223–238.
  24. Si, J.; You, H.J.; Yu, J.; Sung, J.; Ko, G. Prevotella as a hub for vaginal microbiota under the influence of host genetics and their association with obesity. Cell Host Microbe 2017, 21, 97–105.
  25. Castaner, O.; Goday, A.; Park, Y.-M.; Lee, S.-H.; Magkos, F.; Shiow, S.-A.T.E.; Schröder, H. The gut microbiome profile in obesity: A systematic review. Int. J. Endocrinol. 2018, 2018, 1–9.
  26. Cauchie, M.; Desmet, S.; Lagrou, K. Candida and its dual lifestyle as a commensal and a pathogen. Res. Microbiol. 2017.
  27. Bradford, L.L.; Ravel, J. The vaginal mycobiome: A contemporary perspective on fungi in women’s health and diseases. Virulence 2017, 8, 342–351.
  28. Harriott, M.M.; Lilly, E.A.; Rodriguez, T.E.; Fidel, P.L.; Noverr, M.C. Candida albicans forms biofilms on the vaginal mucosa. Microbiology 2010, 156, 3635–3644.
  29. Mayer, F.L.; Wilson, D.; Hube, B. Candida albicans pathogenicity mechanisms. Virulence 2013, 4, 119–128.
  30. Liu, M.-B.; Xu, S.-R.; He, Y.; Deng, G.-H.; Sheng, H.-F.; Huang, X.-M.; Ouyang, C.-Y.; Zhou, H.-W. Diverse vaginal microbiomes in reproductive-age women with vulvovaginal candidiasis. PLoS ONE 2013, 8, e79812.
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