Composition of the Vaginal Microbiota in Women of Reproductive Age - Sensitive and Specific Molecular Diagnosis of Bacterial Vaginosis Is Possible?

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Shipitsyna, Elena ^a   Roos, Annika ^b   Datcu, Raluca ^c   Hallén, Anders ^d   Fredlund, Hans ^e   Jensen, Jørgen S ^c   Engstrand, Lars ^b   Unemo, Magnus ^e  

^a D O OTT RESEARCH INSTITUTE OF OBSTETRICS   (Russian Federation)

^b KAROLINSKA INSTITUTE   (Sweden)

^c STATENS SERUM INSTITUT   (Denmark)

^d UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^e ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

16S RNA GENE; ADOLESCENT; ADULT; AMSEL CRITERIA; ARTICLE; ATOPOBIUM VAGINAE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIUM DETECTION; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; EGGERTHELLA; FEMALE; GARDNERELLA VAGINALIS; HUMAN; INTERMETHOD COMPARISON; LACTOBACILLUS; MAJOR CLINICAL STUDY; MEGASPHAERA; NONHUMAN; PREDICTION; PREVOTELLA; PYROSEQUENCING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SPECIES COMPOSITION; VAGINA FLORA; VAGINITIS;

ACTINOBACTERIA; ADOLESCENT; ADULT; CASE-CONTROL STUDIES; DNA, BACTERIAL; FEMALE; GARDNERELLA VAGINALIS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LACTOBACILLUS; MEGASPHAERA; METAGENOME; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; VAGINA; VAGINOSIS, BACTERIAL;

ATOPOBIUM VAGINAE; BACTERIA (MICROORGANISMS); EGGERTHELLA; GARDNERELLA VAGINALIS; LACTOBACILLUS; MEGASPHAERA; PREVOTELLA;

EID: 84876049369     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060670     Document Type: Article

References (61)

1. Morris M, Nicoll A, Simms I, Wilson J, Catchpole M, (2001) Bacterial vaginosis: a public health review. Br J Obstet Gynaecol 108: 439-450.
2. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, et al. (1995) Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med 333: 1737-1742.
3. Silver HM, Sperling RS, St Clair PJ, Gibbs RS, (1989) Evidence relating bacterial vaginosis to intraamniotic infection. Am J Obstet Gynecol 161: 808-812.
4. Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, et al. (1988) A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 319: 972-978.
5. Sweet RL, (1995) Role of bacterial vaginosis in pelvic inflammatory disease. Clin Infect Dis 20: S271-S275.
6. Hillier SL, Kiviat NB, Hawes SE, Hasselquist MB, Hanssen PW, et al. (1996) Role of bacterial vaginosis-associated microorganisms in endometritis. Am J Obstet Gynecol 175: 435-441.
7. Wiesenfeld H, Hillier S, Krohn M, Amortegui AJ, Heine RP, et al. (2002) Lower genital tract infection and endometritis: insight into subclinical pelvic inflammatory disease. Obstet Gynecol 100: 456-463.
8. Haggerty CL, Hillier SL, Bass DC, Ness RB, (2004) Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin Infect Dis 39: 990-995.
9. Schwebke JR, Schulien MB, Zajackowski M, (1995) Pilot study to evaluate the appropriate management of patients with coexistent bacterial vaginosis and cervicitis. Infect Dis Obstet Gynecol 3: 119-122.
10. Schwebke JR, Weiss HL, (2002) Interrelationships of bacterial vaginosis and cervical inflammation. Sex Transm Dis 29: 59-64.
11. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL, (2003) Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis 36: 663-668.
12. Allsworth JE, Peipert JF, (2011) Severity of bacterial vaginosis and the risk of sexually transmitted infection. Am J Obstet Gynecol 205: 113.e1-113.e6.
13. Cherpes TL, Meyn LA, Krohn MA, Lurie JG, Hillier SL, (2003) Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis 37: 319-325.
14. Myer L, Kuhn L, Stein ZA, Wright TC Jr, Denny L, (2005) Intravaginal practices, bacterial vaginosis, and women's susceptibility to HIV infection: epidemiological evidence and biological mechanisms. Lancet Infect Dis 5: 786-794.
15. Eschenbach DA, (1993) Bacterial vaginosis and anaerobes in obstetric-gynecologic infection. Clin Infect Dis 16: S282-S287.
16. Spiegel CA, (2002) Bacterial vaginosis. Rev Med Microbiol 13: 43-51.
17. Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Delanghe J, et al. (2004) Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae, Gardnerella vaginalis and bacterial vaginosis. BMC Microbiol 4: 16.
18. Fredricks DN, Fiedler TL, Marrazzo JM, (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353: 1899-1911.
19. Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM, (2007) Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol 45: 3270-3276.
20. Oakley BB, Fiedler TL, Marrazzo JM, Fredricks DN, (2008) Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl Environ Microbiol 74: 4898-909.
21. Ling Z, Kong J, Liu F, Zhu H, Chen X, et al. (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11: 488.
22. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, et al. (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108: S4680-S4687.
23. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, et al. (2012) Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS ONE 7: e37818.
24. Verstraelen H, Verhelst R, Claeys G, Temmerman M, Vaneechoutte M, (2004) Culture-independent analysis of vaginal microflora: the unrecognized association of Atopobium vaginae with bacterial vaginosis. Am J Obstet Gynecol 191: 1130-1132.
25. Zozaya-Hinchliffe M, Martin DH, Ferris MJ, (2008) Prevalence and abundance of uncultivated Megasphaera-like bacteria in the human vaginal environment. Appl Environ Microbiol 74: 1656-1659.
26. Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, et al. (1983) Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 74: 14-22.
27. 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.
28. 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.
29. Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Van Simaey L, et al. (2005) 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 5: 61.
30. Donders GG, (1999) Microscopy of bacterial flora on fresh vaginal smears. Infect Dis Obstet Gynecol 7: 12.
31. 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: 33-43.
32. Lamont RF, Sobel JD, Akins RA, Hassan SS, Chaiworapongsa T, et al. (2011) The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG 118: 533-549.
33. Obata-Yasuoka M, Ba-Thein W, Hamada H, Hayashi H, (2002) A multiplex polymerase chain reaction-based diagnostic method for bacterial vaginosis. Obstet Gynecol 100: 759-764.
34. Goffinet F, Maillard F, Mihoubi N, Kayem G, Papiernik E, et al. (2003) Bacterial vaginosis: prevalence and predictive value for premature delivery and neonatal infection in women with preterm labour and intact membranes. Eur J Obstet Gynecol Reprod Biol 108: 146-151.
35. Donders GG, (2007) Definition and classification of abnormal vaginal flora. Best Pract Res Clin Obstet Gynaecol 21: 355-373.
36. Zariffard MR, Saifuddin M, Sha BE, Spear GT, (2002) Detection of bacterial vaginosis-related organisms by real-time PCR for Lactobacilli, Gardnerella vaginalis and Mycoplasma hominis. FEMS Immunol Med Microbiol 34: 277-281.
37. Sha BE, Chen HY, Wang QJ, Zariffard MR, Cohen MH, et al. (2005) Utility of Amsel criteria, Nugent score, and quantitative PCR for Gardnerella vaginalis, Mycoplasma hominis, and Lactobacillus spp for diagnosis of bacterial vaginosis in human immunodeficiency virus-infected women. J Clin Microbiol 43: 4607-4612.
38. Cartwright CP, Lembke BD, Ramachandran K, Body BA, Nye MB, et al. (2012) Development and validation of a semi-quantitative, multi-target, PCR assay for the diagnosis of bacterial vaginosis. J Clin Microbiol 50: 2321-2329.
39. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, et al. (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3: e2836.
40. Maidak BL, Cole JR, Lilburn TG, Parker CT Jr, Saxman PR, et al. (2000) The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28: 173-174.
41. Fethers K, Twin J, Fairley CK, Fowkes FJ, Garland SM, et al. (2012) Bacterial vaginosis (BV) candidate bacteria: associations with BV and behavioural practices in sexually-experienced and inexperienced women. PLoS ONE 7: e30633.
42. Fredricks DN, Fiedler TL, Thomas KK, Mitchell CM, Marrazzo JM, (2009) Changes in vaginal bacterial concentrations with intravaginal metronidazole therapy for bacterial vaginosis as assessed by quantitative PCR. J Clin Microbiol 47: 721-726.
43. De Backer E, Verhelst R, Verstraelen H, Alqumber MA, Burton JP, et al. (2007) Quantitative determination by real-time PCR of four vaginal Lactobacillus species, Gardnerella vaginalis and Atopobium vaginae indicates an inverse relationship between L. gasseri and L. iners. BMC Microbiol 7: 115.
44. Zozaya-Hinchliffe M, Lillis R, Martin DH, Ferris MJ, (2010) Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J Clin Microbiol 48: 1812-1819.
45. Fleiss JL (1981) The measurement of interrater agreement. In: Fleiss JL, editor. Statistical Methods for Rates and Proportions. New York: John Wiley. 212-236.
46. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, et al. (2010) Deep sequencing of the vaginal microbiota of women with HIV. PLoS ONE 5: e12078.
47. Tamrakar R, Yamada T, Furuta I, Cho K, Morikawa M, et al. (2007) Association between Lactobacillus species and bacterial vaginosis-related bacteria, and bacterial vaginosis scores in pregnant Japanese women. BMC Infect Dis 7: 128.
48. Bradshaw CS, Tabrizi SN, Fairley CK, Morton AN, Rudland E, et al. (2006) The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J Infect Dis 194: 828-836.
49. Spear GT, Sikaroodi M, Zariffard MR, Landay AL, French AL, et al. (2008) Comparison of the diversity of the vaginal microbiota in HIV-infected and HIV-uninfected women with or without bacterial vaginosis. J Infect Dis 198: 1131-1140.
50. Klebanoff SJ, Hillier SL, Eschenbach DA, Waltersdorph AM, (1991) Control of the microbial flora of the vagina by H2O2-generating lactobacilli. J Infect Dis 164: 94-100.
51. Pavlova SI, Kilic AO, Kilic SS, So JS, Nader-Macias ME, et al. (2002) Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences. J Appl Microbiol 92: 451-459.
52. Vasquez A, Jakobsson T, Ahrne S, Forsum U, Molin G, (2002) Vaginal lactobacillus flora of healthy Swedish women. J Clin Microbiol 40: 2746-2749.
53. Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, et al. (2007) Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 1: 121-133.
54. Zhou X, Hansmann MA, Davis CC, Suzuki H, Brown CJ, et al. (2010) The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol 58: 169-181.
55. Verstraelen H, Verhelst R, Claeys G, De Backer E, Temmerman M, et al. (2009) Longitudinal analysis of the vaginal microora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microora. BMC Microbiol 9: 116.
56. Shi Y, Chen L, Tong J, Xu C, (2009) Preliminary characterization of vaginal microbiota in healthy Chinese women using cultivation-independent methods. J Obstet Gynaecol Res 35: 525-532.
57. Ferris MJ, Norori J, Zozaya-Hinchliffe M, Martin DH, (2007) Cultivation independent analysis of changes in bacterial vaginosis flora following metronidazole treatment. J Clin Microbiol 45: 1016-1018.
58. 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 vaginalflora. J Med Microbiol 45: 120-126.
59. Santiago GL, Deschaght P, El Aila N, Kiama TN, Verstraelen H, et al. (2011) Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am J Obstet Gynecol 204: 450.e1-7.
60. Santiago GL, Tency I, Verstraelen H, Verhelst R, Trog M, et al. (2012) 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 7: e45281.
61. Menard JP, Fenollar F, Raoult D, Boubli L, Bretelle F, (2012) Self-collected vaginal swabs for the quantitative real-time polymerase chain reaction assay of Atopobium vaginae and Gardnerella vaginalis and the diagnosis of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 31: 513-518.