Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle

Microbiome

Volumn 2, Issue 1, 2014, Pages

  Chaban, Bonnie ^c   Links, Matthew G ^c,d   Jayaprakash, Teenus P ^c   Wagner, Emily C ^a,b   Bourque, Danielle K ^b   Lohn, Zoe ^b   Albert, Arianne Y K ^b   van Schalkwyk, Julie ^a,b   Reid, Gregor ^e   Hemmingsen, Sean M ^c,f   Hill, Janet E ^c   Money, Deborah M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WOMEN S HEALTH RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^e LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^f NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Bifidobacteriales; Bifidobacterium; cpn60; Gardnerella; Lactobacillus; Menstrual cycle; Mollicutes; Mycoplasma; Ureaplasma; Vaginal bacteria; Vaginal microbiome

Indexed keywords

CHAPERONIN 60; RNA 16S;

ADULT; AMPLICON; ARTICLE; BIFIDOBACTERIUM BREVE; CANADIAN; FEMALE; GARDNERELLA VAGINALIS; HUMAN; LACTOBACILLUS CRISPATUS; LACTOBACILLUS JENSENII; MENSTRUAL CYCLE; MICROBIOME; MOLLICUTES; MYCOPLASMA HOMINIS; NORMAL HUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; UREAPLASMA PARVUM; UREAPLASMA UREALYTICUM; VAGINA FLORA;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIALES; BIFIDOBACTERIUM; BIFIDOBACTERIUM BREVE; GARDNERELLA; GARDNERELLA VAGINALIS; LACTOBACILLUS; LACTOBACILLUS CRISPATUS; LACTOBACILLUS INERS; LACTOBACILLUS JENSENII; MOLLICUTES; MYCOPLASMA; MYCOPLASMA HOMINIS; UREAPLASMA; UREAPLASMA PARVUM; UREAPLASMA UREALYTICUM;

EID: 84926461946     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/2049-2618-2-23     Document Type: Article

References (70)

1. Ma B, Forney LJ, Ravel J. Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol 2012, 66:371-389.
2. Cadieux PA, Burton J, Devillard E, Reid G. Lactobacillus by-products inhibit the growth and virulence of uropathogenic Escherichia coli. J Physiol Pharmacol 2009, 60:13-18.
3. Matu MN, Orinda GO, Njagi EN, Cohen CR, Bukusi EA. In vitro inhibitory activity of human vaginal lactobacilli against pathogenic bacteria associated with bacterial vaginosis in Kenyan women. Anaerobe 2010, 16:210-215.
4. Strus M, Brzychczy-Wloch M, Gosiewski T, Kochan P, Heczko PB. The in vitro effect of hydrogen peroxide on vaginal microbial communities. FEMS Immunol Med Microbiol 2006, 48:56-63.
5. 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, 11:200.
6. Reid G, McGroarty JA, Tomeczek L, Bruce AW. Identification and plasmid profiles of Lactobacillus species from the vagina of 100 healthy women. FEMS Immunol Med Microbiol 1996, 15:23-26.
7. Velraeds MMC, Vander Mei HC, Reid G, Busscher HJ. Physicochemical and biochemical characterization of biosurfactants released by Lactobacillus strains. Colloids Surf B Biointerfaces 1996, 8:51-61.
8. Vitali B, Pugliese C, Biagi E, Candela M, Turroni S, Bellen G, Donders GG, Brigidi P. Dynamics of vaginal bacterial communities in women developing bacterial vaginosis, candidiasis, or no infection, analyzed by PCR-denaturing gradient gel electrophoresis and real-time PCR. Appl Environ Microbiol 2007, 73:5731-5741.
9. Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P, Foster JA, Forney LJ. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 2007, 1:121-133.
10. Yamamoto T, Zhou X, Williams CJ, Hochwalt A, Forney LJ. Bacterial populations in the vaginas of healthy adolescent women. J Pediatr Adolesc Gynecol 2009, 22:11-18.
11. Zhou X, Hansmann MA, Davis CC, Suzuki H, Brown CJ, Schutte U, Pierson JD, Forney LJ. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol 2010, 58:169-181.
12. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011, 108:4680-4687.
13. Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, Abdo Z, Forney LJ, Ravel J. Temporal dynamics of the human vaginal microbiota. Sci Transl Med 2012, 4:132-152.
14. Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspõllu A, Väin E, Saarma I, Salumets A, Donders GG, Metsis M. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One 2013, 8:e54379.
15. Chan RC, Bruce AW, Reid G. Adherence of cervical, vaginal and distal urethral normal microbial flora to human uroepithelial cells and the inhibition of adherence of gram-negative uropathogens by competitive exclusion. J Urol 1984, 131:596-601.
16. Semmens JP, Wagner G. Estrogen deprivation and vaginal function in postmenopausal women. JAMA 1982, 248:445-448.
17. Wagner G, Ottesen B. Vaginal physiology during menstruation. Ann Intern Med 1982, 96:921-923.
18. Brenner RM, West NB. Hormonal regulation of the reproductive tract in female mammals. Annu Rev Physiol 1975, 37:273-302.
19. Bartlett JG, Onderdonk AB, Drude E, Goldstein C, Anderka M, Alpert S, McCormack WM. Quantitative bacteriology of the vaginal flora. J Infect Dis 1977, 136:271-277.
20. Sautter RL, Brown WJ. Sequential vaginal cultures from normal young women. J Clin Microbiol 1980, 11:479-484.
21. Wilks M, Tabaqchali S. Quantitative bacteriology of the vaginal flora during the menstrual cycle. J Med Microbiol 1987, 24:241-245.
22. Priestley CJ, Jones BM, Dhar J, Goodwin L. What is normal vaginal flora?. Genitourin Med 1997, 73:23-28.
23. Eschenbach DA, Thwin SS, Patton DL, Hooton TM, Stapleton AE, Agnew K, Winter C, Meier A, Stamm WE. Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis 2000, 30:901-907.
24. Srinivasan S, Liu C, Mitchell CM, Fiedler TL, Thomas KK, Agnew KJ, Marrazzo JM, Fredricks DN. Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 2010, 5:e10197.
25. Hickey RJ, Abdo Z, Zhou X, Nemeth K, Hansmann M, Osborn TW, Wang F, Forney LJ. Effects of tampons and menses on the composition and diversity of vaginal microbial communities over time. BJOG 2013, 120:695-704.
26. Hill JE, Fernando WM, Zello GA, Tyler RT, Dahl WJ, Van Kessel AG. Improvement of the representation of bifidobacteria in fecal microbiota metagenomic libraries by application of the cpn60 universal primer cocktail. Appl Environ Microbiol 2010, 76:4550-4552.
27. Links MG, Dumonceaux TJ, Hemmingsen SM, Hill JE. The chaperonin-60 universal target is a barcode for bacteria that enables de novo assembly of metagenomic sequence data. PLoS One 2012, 7:e49755.
28. Hill JE, Goh SH, Money DM, Doyle M, Li A, Crosby WL, Links M, Leung A, Chan D, Hemmingsen SM. Characterization of vaginal microflora of healthy, nonpregnant women by chaperonin-60 sequence-based methods. Am J Obstet Gynecol 2005, 193:682-692.
29. Schellenberg J, Links MG, Hill JE, Dumonceaux TJ, Peters GA, Tyler S, Ball TB, Severini A, Plummer FA. Pyrosequencing of the chaperonin-60 universal target as a tool for determining microbial community composition. Appl Environ Microbiol 2009, 75:2889-2898.
30. Schellenberg JJ, Links MG, Hill JE, Dumonceaux TJ, Kimani J, Jaoko W, Wachihi C, Mungai JN, Peters GA, Tyler S, Graham M, Severini A, Fowke KR, Ball TB, Plummer FA. Molecular definition of vaginal microbiota in East African commercial sex workers. Appl Environ Microbiol 2011, 77:4066-4074.
31. Paramel Jayaprakash T, Schellenberg JJ, Hill JE. Resolution and characterization of distinct cpn60-based subgroups of Gardnerella vaginalis in the vaginal microbiota. PLoS One 2012, 7:e43009.
32. Keane FE, Ison CA, Taylor-Robinson D. A longitudinal study of the vaginal flora over a menstrual cycle. Int J STD AIDS 1997, 8:489-494.
33. Thoma ME, Gray RH, Kiwanuka N, Aluma S, Wang MC, Sewankambo N, Wawer MJ. Longitudinal changes in vaginal microbiota composition assessed by Gram stain among never sexually active pre- and postmenarcheal adolescents in Rakai, Uganda. J Pediatr Adolesc Gynecol 2011, 24:42-47.
34. Brotman RM, Ravel J, Cone RA, Zenilman JM. Rapid fluctuation of the vaginal microbiota measured by Gram stain analysis. Sex Transm Infect 2010, 86:297-302.
35. Petignat P, Hankins C, Walmsley S, Money D, Provencher D, Pourreaux K, Kornegay J, Rouah F, Coutlee F. Self-sampling is associated with increased detection of human papillomavirus DNA in the genital tract of HIV-seropositive women. Clin Infect Dis 2005, 41:527-534.
36. Ogilvie GS, Patrick DM, Schulzer M, Sellors JW, Petric M, Chambers K, White R, FitzGerald JM. Diagnostic accuracy of self-collected vaginal specimens for human papillomavirus compared to clinician collected human papillomavirus specimens: a meta-analysis. Sex Transm Infect 2005, 81:207-212.
37. Chaban B, Albert A, Links MG, Gardy J, Tang P, Hill JE. Characterization of the upper respiratory tract microbiomes of patients with pandemic H1N1 influenza. PLoS One 2013, 8:e69559.
38. Menard JP, Fenollar F, Henry M, Bretelle F, Raoult D. Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis 2008, 47:33-43.
39. Dumonceaux TJ, Schellenberg J, Goleski V, Hill JE, Jaoko W, Kimani J, Money D, Ball TB, Plummer FA, Severini A. Multiplex detection of bacteria associated with normal microbiota and with bacterial vaginosis in vaginal swabs by use of oligonucleotide-coupled fluorescent microspheres. J Clin Microbiol 2009, 47:4067-4077.
40. van Kuppeveld FJ, van der Logt JT, Angulo AF, van Zoest MJ, Quint WG, Niesters HG, Galama JM, Melchers WJ. Genus- and species-specific identification of mycoplasmas by 16S rRNA amplification. Appl Environ Microbiol 1993, 59:655.
41. Watson HL, Blalock DK, Cassell GH. Variable antigens of Ureaplasma urealyticum containing both serovar-specific and serovar-cross-reactive epitopes. Infect Immun 1990, 58:3679-3688.
42. Hill JE, Town JR, Hemmingsen SM. Improved template representation in cpn60 polymerase chain reaction (PCR) product libraries generated from complex templates by application of a specific mixture of PCR primers. Environ Microbiol 2006, 8:741-746.
43. Schellenberg J, Links MG, Hill JE, Hemmingsen SM, Peters GA, Dumonceaux TJ. Pyrosequencing of chaperonin-60 (cpn60) amplicons as a means of determining microbial community composition. Methods Mol Biol 2011, 733:143-158.
44. Links MG, Chaban B, Hemmingsen SM, Muirhead K, Hill JE. mPUMA: a computational approach to microbiota analysis by de novo assembly of operational taxonomic units based on protein-coding barcode sequences. Microbiome 2013, 1:23.
45. Hill JE, Penny SL, Crowell KG, Goh SH, Hemmingsen SM. cpnDB: a chaperonin sequence database. Genome Res 2004, 14:1669-1675.
46. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7:335-336.
47. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biomed J 2008, 50:346-363.
48. Team RDC R: A Language and Environment for Statistical Computing 2012, Vienna, Austria: R Foundation for Statistical Computing, URL http://www.R-project.org/. ISBN 3-900051-07-0, Team RDC.
49. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. Vegan: Community Ecology Package. R package version 2.0-3 2012, http:CRAN.R-project.org/package=vegan.
50. Hennig C. fpc: Flexible Procedures For Clustering. R Package Version 2.1-6 2013, http://CRAN.R-project.org/package=fpc.
51. Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ. Understanding vaginal microbiome complexity from an ecological perspective. Transl Res 2012, 160:267-282.
52. Zhou J, Jiang YH, Deng Y, Shi Z, Zhou BY, Xue K, Wu L, He Z, Yang Y. Random sampling process leads to overestimation of beta-diversity of microbial communities. MBio 2013, 4:e00324-e00313.
53. Schlicht MJ, Lovrich SD, Sartin JS, Karpinsky P, Callister SM, Agger WA. High prevalence of genital mycoplasmas among sexually active young adults with urethritis or cervicitis symptoms in La Crosse, Wisconsin. J Clin Microbiol 2004, 42:4636-4640.
54. Taylor-Robinson D. Infections due to species of Mycoplasma and Ureaplasma: an update. Clin Infect Dis 1996, 23:671-682.
55. Waites KB, Katz B, Schelonka RL. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev 2005, 18:757-789.
56. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, Gloor GB, Reid G. Deep sequencing of the vaginal microbiota of women with HIV. PLoS One 2010, 5:e12078.
57. Tibaldi C, Cappello N, Latino MA, Masuelli G, Marini S, Benedetto C. Vaginal and endocervical microorganisms in symptomatic and asymptomatic non-pregnant females: risk factors and rates of occurrence. Clin Microbiol Infect 2009, 15:670-679.
58. McKechnie ML, Hillman RJ, Jones R, Lowe PC, Couldwell DL, Davies SC, King F, Kong F, Gilbert GL. The prevalence of urogenital micro-organisms detected by a multiplex PCR-reverse line blot assay in women attending three sexual health clinics in Sydney, Australia. J Med Microbiol 2011, 60:1010-1016.
59. Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA. The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 1993, 16:S273-S281.
60. Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Delanghe J, Van Simaey L, De Ganck C, Temmerman M, Vaneechoutte M. 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 2004, 4:16.
61. Santiago GL, Cools P, Verstraelen H, Trog M, Missine G, El Aila N, Verhelst R, Tency I, Claeys G, Temmerman M, Vaneechoutte M. Longitudinal study of the dynamics of vaginal microflora during two consecutive menstrual cycles. PLoS One 2011, 6:e28180.
62. Korshunov VM, Gudieva ZA, Efimov BA, Pikina AP, Smeianov VV, Reid G, Korshunova OV, Tiutiunnik VL, Stepin II. [The vaginal Bifidobacterium flora in women of reproductive age]. Zh Mikrobiol Epidemiol Immunobiol 1999, 4:74-78.
63. Sundquist A, Bigdeli S, Jalili R, Druzin ML, Waller S, Pullen KM, El-Sayed YY, Taslimi MM, Batzoglou S, Ronaghi M. Bacterial flora-typing with targeted, chip-based pyrosequencing. BMC Microbiol 2007, 7:108.
64. Burton JP, Dixon JL, Reid G. Detection of Bifidobacterium species and Gardnerella vaginalis in the vagina using PCR and denaturing gradient gel electrophoresis (DGGE). Int J Gynaecol Obstet 2003, 81:61-63.
65. Hyman RW, Fukushima M, Diamond L, Kumm J, Giudice LC, Davis RW. Microbes on the human vaginal epithelium. Proc Natl Acad Sci U S A 2005, 102:7952-7957.
66. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol 2007, 5:e177.
67. Sim K, Cox MJ, Wopereis H, Martin R, Knol J, Li MS, Cookson WO, Moffatt MF, Kroll JS. Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS One 2012, 7:e32543.
68. Oakley BB, Fiedler TL, Marrazzo JM, Fredricks DN. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl Environ Microbiol 2008, 74:4898-4909.
69. Perdigón G, Locascio M, Medici M, Pesce de Ruiz Holgado A, Oliver G. Interaction of bifidobacteria with the gut and their influence in the immune function. Biocell 2003, 27:1-9.
70. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 2013, 185:385-394.