Vaginal microbiome
Authors:
V. Buchta
Authors‘ workplace:
Ústav klinické mikrobiologie FN a LF UK, Hradec Králové, přednostka doc. MUDr. H. Žemličková, Ph. D.
Published in:
Ceska Gynekol 2018; 83(5): 371-379
Category:
Overview
Objective:
Presentation of complex information about the vaginal microbiota from historical view to current concepts with focus on latest findings on the structure and functioning of the vaginal microbiome.
Design:
Review article.
Setting:
Department of Clinical Microbiology, University Hospital and Faculty of Medicine in Hradci Králové, Charles University in Prague.
Methods:
Literature review using the databases (PubMed, Web of Science, Ovid, etc.) with keywords (vaginal microbiota/ microbiom; vaginal discharge; bacterial vaginosis; vulvovaginitis; vaginal Lactobacillus).
Results:
The vaginal microbiome is a specific compartment of the human microbiome. Unique conditions of the vagina are characterized by a few microbial species, usually lactobacilli, which are able to utilize glycogen, which is under control of estrogens. Lactobacilli and other fermentative bacteria together with vaginal epithelial cells produce lactic acid and are responsible for acidifying vaginal milieu. Lactic acid occurs in two isomeric forms, and their relative ratio is likely to give the vaginal microbiota a certain degree of stability and ability to withstand some infections. This microbiota is manifested by a low degree of diversity and by the high dynamics of changes of its composition under the influence of various exogenous and endogenous factors. Increase in diversity can be paradoxically associated with a dysbiosis such as bacterial vaginosis. Individual species of lactobacilli mainly Lactobacillus crispatus characterize the main community state types in the vagina. Apart from lactobacilli, healthy women may be colonized with a non-lactobacillary microbiota whose rate is dependent on ethnicity. Conclusion: The definition of vaginal microbiota cannot be only related to the presence or absence of individual microorganisms, although the incidence of some of them can be correlated with dysbiosis or eubiosis. The composition of microbiota is important, but it is only one of the basic attributes of normal vaginal microbiota, but not sufficient; that is the functional definition of vaginal microbiota in relation to its structure and dynamics, including the influence of ethnicity, physiological status of the vagina, and genetic disposition of woman.
Keywords:
vaginal microbiome, dysbiosis, community state types, Lactobacillus, lactic acid, pH, H2O2, sexual hormones, historical and recent concept
Sources
1. Aldunate, M., Srbinovski, D., Hearps, AC., et al. Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front Physiol, 2015, 6, p. 164. doi: 10.3389/fphys.2015.00164.
2. Al-Mushrif, S., Eley, A., Jones, BM. Inhibition of chemotaxis by organic acids from anaerobes may prevent a purulent response in bacterial vaginosis. J Med Microbiol, 2000, 49, p. 1023–1030.
3. Amsel, R., Totten, PA., Spiegel, CA., et al. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiological associations. Am J Med, 1983, 74, p. 14–22.
4. Austin, MN., Rabe, LK., Srinivasan, S., et al. Mageeibacillus indolicus gen. nov., sp. nov.: a novel bacterium isolated from the female genital tract. Anaerobe, 2015, 32, p. 37–42.
5. Beigi, RH., Wiesenfeld, HC., Hillier, SL., et al. Factors associated with absence of H2O2-producing Lactobacillus among women with bacterial vaginosis. J Infect Dis, 2005, 191(6), p. 924–949.
6. Brotman, RM., He, X., Gajer, P., et al. Association between cigarette smoking and the vaginal microbiota: a pilot study. BMC Infect Dis, 2014, 28, 14, p. 471. doi: 10.1186/1471-2334-14-471.
7. Brotman, RM., Bradford, LL., Conrad, M., et al. Association between Trichomonas vaginalis and vaginal bacterial community composition among reproductive-age women. Sex Transm Dis, 2012, 39(10), p. 807–812.
8. Buchta, V., Andrys, C., Bolehovska, R., et al. The role of Candida yeasts in vaginal microbiome in women with chronic vulvovaginal discomfort. J Internat Soc Microbiota, 2017, 4, p. 71 doi: 10.18143/JISM_v4i1.
9. Buve, A., Jespers, V., Crucitti, T., Fichorova, RN. The vaginal microbiota and susceptibility to HIV. AIDS, 2014, 28(16), p. 2333–2344.
10. Cardone, A., Zarcone, R., Borrelli, A., et al. Utilisation of H2O2 hydrogen peroxide in the treatment of recurrent bacterial vaginosis. Minerva Ginecol, 2003, 55(6), p. 483–492.
11. Cherpes, TL., Meyn, LA., Krohn, MA., et al. Association between acquisition of herpes simplex virus type2 in women and bacterial vaginosis. Clin Infect Dis, 2003, 37, p. 319–325.
12. Clemente, JC., Dominguez-Bello, MG. Safety of vaginal microbial transfer in infants delivered by caesarean, and expected health outcomes. BMJ, 2016, 31, 352, p. i1707. doi: 10.1136/bmj.i1707.
13. Dareng, EO., Ma, B., Famooto, AO., et al. Prevalent high-risk HPV infection and vaginal microbiota in Nigerian women. Epidemiol Infect, 2016, 144(1), p. 123–137.
14. Döderlein, A. Das scheidensekret und seine bedeutung fur puerperalfieber. Zentralblatt fur Bakteriology, 1892, 11, S. 699.
15. Donders, GG. Definition and classification of abnormal vaginal flora. Best Pract Res Clin Obstet Gynaecol, 2007, 21, p. 355–373.
16. El Aila, NA., Tency, I., Claeys, G., et al. Identification and genotyping of bacteria from paired vaginal and rectal samples from pregnant women indicates similarity between vaginal and rectal microflora. BMC Infect Dis, 2009 14, 9, p. 167.
17. Eschenbach, DA., Davick, PR., Williams, BL., et al. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J Clin Microbiol, 1989, 27, p. 251–256.
18. Falsen, E., Pascual, C., Sjödén, B., et al. Phenotypic and phylogenetic characterization of a novel Lactobacillus species from human sources: description of Lactobacillus iners sp. nov. Int J Syst Bacteriol, 1999, 49(Pt 1), p. 217–221.
19. Ferris, MJ., Masztal, A., Aldridge, KE., et al. Association of Atopobium vaginae, a recently described metronidazole resistant anaerobe, with bacterial vaginosis. BMC Infect Dis, 2004 13, 4, p. 5.
20. Ferris, MJ., Norori, J., Zozaya-Hinchliffe, M., Martin, DH. Cultivation independent analysis of changes in bacterial vaginosis flora following metronidazole treatment. J Clin Microbiol, 2007, 45, p. 1016–1018.
21. Fitzsimmons, N., Berry, DR. Inhibition of Candida albicans by Lactobacillus acidophilus: evidence for the involvement of a peroxidase system. Microbios, 1994, 80, p. 125–133.
22. France, MT., Mendes-Soares, H., Forney, LJ. Genomic comparisons of Lactobacillus crispatus and Lactobacillus iners reveal potential ecological drivers of community composition in the vagina. Appl Environ Microbiol, 2016, 82(24), p. 7063–7073.
23. Gajer, P., Brotman, RM., Bai, G., et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med, 2012, 4(132), p. 132.
24. Gardner, HL., Dukes, CD. New etiologic agent in non-specific bacterial vaginitis. Science, 1954, 120, p. 853.
25. Haggerty, CL., Totten, PA., Ferris, M., et al. Clinical characteristics of bacterial vaginosis among women testing positive for fastidious bacteria. Sex Transm Infect, 2009, 85(4), p. 242–248.
26. Hugenholtz, P., Goebel, BM., Pace, NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol, 1998, 180, p. 4765–4774.
27. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature, 2012, 486(7402), p. 207–214.
28. Ison, CA., Hay, PE. Validation of a simplified grading of Gram stained vaginal smears for use in genitourinary medicine clinics. Sex Transm Infect, 2002, 78, p. 413–415.
29. Keane, FE., Ison, CA., Taylor-Robinson, D. A longitudinal study of the vaginal flora over a menstrual cycle. Int. J.STD & AIDS, 1997, 8, p. 489–494.
30. Kestřánek, J., Jílek, P., Matula, V., et al. Jaký je aktuální stav diagnostiky vulvovaginálního dyskomfortu v České republice? Pilotní analýza. Čes Gynek, 2013, 78(6), s. 522–527.
31. Koucký, M., Malíčková, K., Hrdý, J., et al. Úloha mateřské imunity a mikrobiomu ženy v patogenezi předčasného porodu. Čes Gynek, 2017, 82(5), s. 407–410.
32. Kyongo, JK., Jespers, V., Goovaerts, O., et al. Searching for lower female genital tract soluble and cellular biomarkers: defining levels and predictors in a cohort of healthy Caucasian women. PLoS One, 2012, 7(8), p. e43951. doi: 10.1371/ journal.pone.0043951.
33. Lauer, E., Helming, C., Kandler, O. Heterogeneity of the species Lactobacillus acidophilus (Moro) Hansen and Mocquot as revealed by biochemical characteristics and DNA-DNA hybridization. Zentbl Bakteriol Microbiol Hyg Abt, 1980, 1, p. 150–168.
34. Leopold, S. Heretofore undescribed organism isolated from the genitourinary system. U S Armed Forces Med J, 1953, 4(2), p. 263–266.
35. Mašata, J., Jedličková, A., Poislová, M., et al. Současné možnosti diagnostiky vulvovaginálních infekcí. Čes Gynek, 2010, 75(2), s. 111–117.
36. Mašata, J., Poislová, M., Jedličková, A., et al. Modifikovaná klasifikace mikroskopického hodnocení poševních infekcí. Čes Gynek, 2010, 75(3), s. 199–208.
37. Menard, JP., Mazouni, C., Salem-Cherif, I., et al. High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet Gynecol, 2010, 115(1), p. 134–140.
38. Mendes-Soares, H., Krishnan, V., Settles, ML., et al. Fine-scale analysis of 16S rRNA sequences reveals a high level of taxonomic diversity among vaginal Atopobium spp. Pathog Dis, 2015, 73(4). pii: ftv020. doi: 10.1093/femspd/ftv020. Epub 2015 Mar 15.
39. Miller, L., Patton, DL., Meier, A., et al. Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol, 2000, 96(3), p. 431–439.
40. Mirmonsef, P., Hotton, AL., Gilbert, D., et al. Glycogen levels in undiluted genital fluid and their relationship to vaginal ph, estrogen, and progesterone. PLoS One, 2016, 19, 11(4), p. e0153553. doi: 10.1371/journal.pone.0153553.
41. Mitchell, C., Fredricks, D., Agnew, K., Hitti, J. Hydrogen peroxide-producing lactobacilli are associated with lower levels of vaginal interleukin-1β, independent of bacterial vaginosis. Sex Transm Dis, 2015, 42(7), p. 358–363.
42. Miura, H. Beiträge zum Studium über die Vaginasekrete. Mitt. Med. Akad. Kioto, 1928, 2, Heft 1, 1.
43. Nedovic, B., Posteraro, B., Leoncini, E., et al. Mannose-binding lectin codon 54 gene polymorphism and vulvovaginal candidiasis: a systematic review and meta-analysis. Biomed Res Int, 2014, p. 738298. doi: 10.1155/2014/738298.
44. Nugent, RP., Krohn, MA., Hillier, SL. Reliability of diagnosing bacterial vaginosis is improved by a standardised method of Gram‘s stain interpretation. J Clin Microbiol, 1991, 29, p. 297–301.
45. O‘Hanlon, DE., Moench, TR., Cone, RA. In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis, 2011, 11, p. 200.
46. O‘Hanlon, DE., Moench, TR., Cone, RA. Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS One, 2013, 8(11), p. e80074.
47. Petricevic, L., Domig, KJ., Nierscher, FJ., et al. Characterisation of the oral, vaginal and rectal Lactobacillus flora in healthy pregnant and postmenopausal women. Eur J Obstet Gynecol Reprod Biol, 2012, 160(1), p. 93–99.
48. Petricevic, L., Domig, KJ., Nierscher, FJ., et al. Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci Rep, 2014, 30, 4, p. 5136. doi: 10.1038/ srep05136.
49. Ravel, J., Brotman, RM., Gajer, P., et al. Daily temporal dynamics of vaginal microbiota before, during and after episodes of bacterial vaginosis. Microbiome, 2013, 2, 1(1), p. 29. doi: 10.1186/2049-2618-1-29.
50. Ravel, J., Gajer, P., Abdo, Z., et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A., 2011, 108, Suppl. 1, p. 4680–4687.
51. Reid, G. Probiotic and prebiotic applications for vaginal health. J AOAC Int, 2012, 95(1), p. 31–34.
52. Rodrigues, FS., Peixoto, S., Adami, F., et al. Proposal of a new cutoff for Nugent criteria in the diagnosis of bacterial vaginosis. J Microbiol Methods, 2015, 115, p. 144–146.
53. Rogosa, M., Sharpe, ME. Species differentiation of human vaginal lactobacilli. J Gen Microbiol, 1960, 23, p. 197–201.
54. Rosenstein, IJ., Fontaine, EA., Morgan, DJ., et al. Relationship between hydrogen peroxide-producing strains of lactobacilli and vaginosis-associated bacterial species in pregnant women. Eur J Clin Microbiol Infect Dis, 1997, 16(7), p. 517–522.
55. Santiago, GL., Tency, I., Verstraelen, H., et al. Longitudinal qPCR study of the dynamics of L. crispatus, L. iners, A. vaginae, (sialidase positive) G. vaginalis, and P. bivia in the vagina. PLoS One, 2012, 7(9), p. e45281. doi: 10.1371/ journal.pone.0045281.
56. Špaček, J., Kestřánek, J., Jílek, P., et al. Comparison of two long-term gestagen regimens in the management of recurrent vulvovaginal candidiasis: A pilot study. Mycoses, 2017, 60(4), p. 260–265. doi:10.1111/myc.12593.
57. Spear, GT., French, AL., Gilbert, D., et al. Human α-amylase present in lower-genital-tract mucosal fluid processes glycogen to support vaginal colonization by Lactobacillus. J Infect Dis, 2014, 210(7), p. 1019–1028.
58. Spiegel, CA., Amsel, R., Holmes, KK. Diagnosis of bacterial vaginosis by direct Gram-stain of vaginal fluid. J Clin Microbiol, 1983, 18, p. 170–177.
59. Srinivasan, S., Liu, C., Mitchell, CM., et al. Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One, 2010, 5(4), p. e10197.
60. Stoyancheva, G., Marzotto, M., Dellaglio, F., Torriani, S. Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains. Arch Microbiol, 2014, 196(9), p. 645–653.
61. Strus, M., Brzychczy-Włoch, M., Gosiewski, T., et al. The in vitro effect of hydrogen peroxide on vaginal microbial communities. FEMS Immunol Med Microbiol, 2006, 48(1), p. 56–63.
62. Swidsinski, A., Mendling, W., Loening-Baucke, V., et al. Adherent biofilms in bacterial vaginosis. Obstet Gynecol, 2005, 106(5, part 1), p. 1013–1023.
63. Thomas, S. Döderlein‘s bacillus: Lactobacillus acidophilus. J Infect Dis, 1928, 43, p. 218–227.
64. Vallor, AC., Antonio, MA., Hawes, SE., Hillier, SL. Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production. J Infect Dis, 2001, 184(11), p. 1431–1436.
65. van de Wijgert, JH., Borgdorff, H., Verhelst, R., et al. The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS One, 2014, 22, 9(8), p. e105998. doi: 10.1371/journal.pone.0105998.
66. van Houdt, R., Ma, B., Bruisten, SM., et al. Lactobacillus iners – dominated vaginal microbiota is associated with increased susceptibility to Chlamydia trachomatis infection in Dutch women: a case-control study. Sex Transm Infect, 2017, 25. pii: sextrans-2017-053133. doi: 10.1136/sextrans-2017-053133.
67. van Oostrum, N., De Sutter, P., Meys, J., Verstraelen, H. Risks associated with bacterial vaginosis in infertility patients: a systematic review and meta-analysis. Hum Reprod, 2013, 28, p. 1809–1815
68. Verstraelen, H., Verhelst, R., Claeys, G., et al. Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora. BMC Microbiol, 2009, 9, p. 116.
69. Weinstein, L. The bacterial flora of the human vagina. Yale J Biol Med, 1938, 10(3), p. 247–260.
70. White, S., Larsen, B. Candida albicans morphogenesis is influenced by estrogen. Cell Mol Life Sci, 1997, 53, p. 744–749.
71. Wira, CR., Fahey, JV., Ghosh, M., et al. Sex hormone regulation of innate immunity in the female reproductive tract: the role of epithelial cells in balancing reproductive potential with protection against sexually transmitted pathogens. Am J Reprod Immunol, 2010, 63(6), p. 544–565.
72. Witkin, SS., Mendes-Soares, H., Linhares, IM., et al. Influence of vaginal bacteria and D- and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. Mbio, 2013, 4(4). pii: e00460-13.
73. Yildirim, S., Yeoman, CJ., Janga, SC., et al. Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance. ISME J, 2014, 8(12), p. 2431–2444.
74. Záhumenský, J., Hederlingová, J., Pšenková, P. Význam materského mikrobiómu v tehotnosti. Čes Gynek, 2017, 82(3), p. 211–217.
Labels
Paediatric gynaecology Gynaecology and obstetrics Reproduction medicineArticle was published in
Czech Gynaecology
2018 Issue 5
Most read in this issue
- HCG level after embryo transfer as a prognostic indicator of pregnancy finished with delivery
- Vaginal microbiome
- Pelvic actinomycosis and IUD
- Eating disorders in pregnancy