Free glycogen in vaginal fluids is associated with Lactobacillus colonization and low vaginal pH

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Mirmonsef, Paria ^a   Hotton, Anna L ^b   Gilbert, Douglas ^a   Burgad, Derick ^a   Landay, Alan ^a   Weber, Kathleen M ^b   Cohen, Mardge ^b   Ravel, Jacques ^c   Spear, Gregory T ^a  

^a RUSH UNIVERSITY   (United States)

^b CORE Center Cook County Health and Hospital System ^*  (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN; RNA 16S;

ADULT; AFRICAN AMERICAN; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM IDENTIFICATION; BODY MASS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; LACTOBACILLUS; LACTOBACILLUS CRISPATUS; LACTOBACILLUS JENSENII; MICROFLORA; NONHUMAN; ORAL CONTRACEPTIVE USE; PH; POPULATION ABUNDANCE; PYROSEQUENCING; TRICHOMONAS; VAGINA DISCHARGE; VAGINA PH; ADOLESCENT; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEXUAL BEHAVIOR; VAGINA; VAGINITIS; YOUNG ADULT;

ADOLESCENT; ADULT; BASE SEQUENCE; FEMALE; GLYCOGEN; HUMANS; HYDROGEN-ION CONCENTRATION; LACTOBACILLUS; MICROBIOTA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEXUAL BEHAVIOR; VAGINA; VAGINOSIS, BACTERIAL; YOUNG ADULT;

EID: 84904512056     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102467     Document Type: Article

References (64)

1. Antonio MA, Hawes SE, Hillier SL (1999) The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 180: 1950-1956.
2. Giorgi A, Torriani S, Dellaglio F, Bo G, Stola E, et al. (1987) Identification of vaginal lactobacilli from asymptomatic women. Microbiologica 10: 377-384.
3. Song YL, Kato N, Matsumiya Y, Liu CX, Kato H, et al. (1999) Identification of and hydrogen peroxide production by fecal and vaginal lactobacilli isolated from Japanese women and newborn infants. J Clin Microbiol 37: 3062-3064. (Pubitemid 29391944)
4. Wilks M, Wiggins R, Whiley A, Hennessy E, Warwick S, et al. (2004) Identification and H(2)O(2) production of vaginal lactobacilli from pregnant women at high risk of preterm birth and relation with outcome. J Clin Microbiol 42: 713-717. (Pubitemid 38222651)
5. Boskey ER, Cone RA, Whaley KJ, Moench TR (2001) Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod 16: 1809-1813. (Pubitemid 32916204)
6. Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA (1999) Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 67: 5170-5175. (Pubitemid 29455288)
7. Pybus V, Onderdonk AB (1999) Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect 1: 285-292.
8. Paavonen J (1983) Physiology and ecology of the vagina. Scand J Infect Dis Suppl 40: 31-35.
9. Aroutcheva A, Gariti D, Simon M, Shott S, Faro J, et al. (2001) Defense factors of vaginal lactobacilli. Am J Obstet Gynecol 185: 375-379. (Pubitemid 32769439)
10. Dover SE, Aroutcheva AA, Faro S, Chikindas ML (2008) Natural Antimicrobials and Their Role in Vaginal Health: A Short Review. Int J Probiotics Prebiotics 3: 219-230.
11. Sobel JD (1997) Vaginitis. N Engl J Med 337: 1896-1903.
12. Danielsson D, Teigen PK, Moi H (2011) The genital econiche: focus on microbiota and bacterial vaginosis. Ann N Y Acad Sci 1230: 48-58.
13. Marrazzo JM (2011) Interpreting the epidemiology and natural history of bacterial vaginosis: are we still confused? Anaerobe 17: 186-190.
14. Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS (2008) Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 22: 1493-1501.
15. Kaul R, Nagelkerke NJ, Kimani J, Ngugi E, Bwayo JJ, et al. (2007) Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis 196: 1692-1697. (Pubitemid 351411969)
16. 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. (Pubitemid 36976487)
17. Allsworth JE, Lewis VA, Peipert JF (2008) Viral sexually transmitted infections and bacterial vaginosis: 2001-2004 National Health and Nutrition Examination Survey data. Sex Transm Dis 35: 791-796.
18. Cherpes TL, Melan MA, Kant JA, Cosentino LA, Meyn LA, et al. (2005) Genital tract shedding of herpes simplex virus type 2 in women: effects of hormonal contraception, bacterial vaginosis, and vaginal group B Streptococcus colonization. Clin Infect Dis 40: 1422-1428. (Pubitemid 40628629)
19. Sha BE, Zariffard MR, Wang QJ, Chen HY, Bremer J, et al. (2005) Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis. J Infect Dis 191: 25-32. (Pubitemid 40041396)
20. Cu-Uvin S, Hogan JW, Caliendo AM, Harwell J, Mayer KH, et al. (2001) Association between bacterial vaginosis and expression of human immunodeficiency virus type 1 RNA in the female genital tract. Clin Infect Dis 33: 894-896. (Pubitemid 32831848)
21. Galvin SR, Cohen MS (2004) The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2: 33-42. (Pubitemid 39490046)
22. 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. (Pubitemid 26391004)
23. Haggerty CL, Hillier SL, Bass DC, Ness RB (2004) Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin Infect Dis 39: 990-995. (Pubitemid 39313455)
24. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, et al. (1995) Association between bacterial vaginosis and preterm delivery of a low-birthweight infant. The Vaginal Infections and Prematurity Study Group [see comments]. N Engl J Med 333: 1737-1742.
25. Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, et al. (2003) Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol 189: 139-147. (Pubitemid 36886539)
26. Eschenbach DA, Davick PR, Williams BL, Klebanoff SJ, Young-Smith K, et al. (1989) Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J Clin Microbiol 27: 251-256. (Pubitemid 19041152)
27. Hillier SL, Krohn MA, Klebanoff SJ, Eschenbach DA (1992) The relationship of hydrogen peroxide-producing lactobacilli to bacterial vaginosis and genital microflora in pregnant women. Obstet Gynecol 79: 369-373.
28. Martinez RC, Franceschini SA, Patta MC, Quintana SM, Nunes AC, et al. (2008) Analysis of vaginal lactobacilli from healthy and infected Brazilian women. Appl Environ Microbiol 74: 4539-4542. (Pubitemid 352031037)
29. Verstraelen H, Verhelst R, Claeys G, De Backer E, Temmerman M, et al. (2009) 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 9: 116.
30. Cruickshank R SA (1934) The biology of the vagina in the human subject. II: The bacterial flora and secretion of the vagina in relation to glycogen in the vaginal epithelium. J Obstet Gynecol Br Emp 41: 208-226.
31. Cruickshank R (1934) The conversion of the glycogen of the vagina into lactic acid. The Journal of Pathology and Bacteriology 39: 213-219.
32. Thoma ME, Gray RH, Kiwanuka N, Aluma S, Wang MC, et al. (2011) 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 24: 42-47.
33. Miller L, Patton DL, Meier A, Thwin SS, Hooton TM, et al. (2000) Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol 96: 431-439.
34. Gregoire AT, Parakkal PF (1972) Glycogen content in the vaginal tissue of normally cycling and estrogen and progesterone-treated rhesus monkeys. Biol Reprod 7: 9-14.
35. Stewart-Tull D (1964) Evidence that vaginal lactobacilli do not ferment glycogen. Am J Obstet Gynecol 88: 676-679.
36. Rogosa M, Sharpe ME (1960) Species differentiation of human vaginal lactobacilli. J Gen Microbiol 23: 197-201.
37. Wylie JG, Henderson A (1969) Identity and glycogen-fermenting ability of lactobacilli isolated from the vagina of pregnant women. J Med Microbiol 2: 363-366.
38. Martin R, Soberon N, Vaneechoutte M, Florez AB, Vazquez F, et al. (2008) Characterization of indigenous vaginal lactobacilli from healthy women as probiotic candidates. Int Microbiol 11: 261-266.
39. 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. (Pubitemid 13221599)
40. Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, et al. (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med 4: 132ra152.
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
42. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
43. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267. (Pubitemid 47326658)
44. Matsen FA, Kodner RB, Armbrust EV (2010) pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11: 538.
45. Newson R (2006) Confidence Intervals for Rank Statistics: Somers' D and Extensions. Stata Journal 6: 309-334.
46. Hosmer DW LS, Sturdivant R (2013) Applied Logistic Regression. Hoboken: Wiley & Sons, Inc.
47. Farage M, Maibach H (2006) Lifetime changes in the vulva and vagina. Arch Gynecol Obstet 273: 195-202. (Pubitemid 43004689)
48. O'Hanlon DE, Moench TR, Cone RA (2011) In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 11: 200.
49. Cohen CR, Lingappa JR, Baeten JM, Ngayo MO, Spiegel CA, et al. (2012) Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS Med 9: e1001251.
50. Gregoire AT, Kandil O, Ledger WJ (1971) The glycogen content of human vaginal epithelial tissue. Fertil Steril 22: 64-68.
51. Ayre WB (1950) The glycogen-estrogen relationship in the vaginal tract. J Clin Endocrinol Metab 11: 103-110.
52. Willson J, Goforth ML (1942) Effects of an excess of ingested carbohydrate upon the glycogen content of vaginal epithelium. J Clin Endocrinol Metab 2: 223-225.
53. Rakoff AE FL, Goldstein L. (1944) The biologic characteristics of the normal vagina. Am J Obstet Gynecol 47: 467.
54. Nelson LR, Bulun SE (2001) Estrogen production and action. J Am Acad Dermatol 45: S116-124. (Pubitemid 32783340)
55. Mitchell CM ML, Westerberg K, Astronomo R, Smythe K, Gardella C, Mack M, Magaret A, Patton D, Agnew K, McElrath MJ, Hladik F, Eschenbach D. (2014) Long-term effect of depot medroxyprogesterone acetate on vaginal microbiota, epithelial thickness and HIV target cells. J Infect Dis.
56. Owen JA, Jr. (1975) Physiology of the menstrual cycle. Am J Clin Nutr 28: 333-338.
57. Macklaim JM, Fernandes AD, Di Bella JM, Hammond JA, Reid G, et al. (2013) Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome 1: 12.
58. Moore MC, Coate KC, Winnick JJ, An Z, Cherrington AD (2012) Regulation of hepatic glucose uptake and storage in vivo. Adv Nutr 3: 286-294.
59. Nielsen J, Ortenblad N (2013) Physiological aspects of the subcellular localization of glycogen in skeletal muscle. Appl Physiol Nutr Metab 38: 91-99.
60. Belec L, Meillet D, Levy M, Georges A, Tevi-Benissan C, et al. (1995) Dilution assessment of cervicovaginal secretions obtained by vaginal washing for immunological assays. Clin Diagn Lab Immunol 2: 57-61.
61. 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 Suppl 1: 4680-4687.
62. Ma B, Forney LJ, Ravel J (2012) Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol 66: 371-389.
63. Spear GT, Gilbert D, Landay AL, Zariffard R, French AL, et al. (2011) Pyrosequencing of the genital microbiotas of HIV-seropositive and -seronegative women reveals Lactobacillus iners as the predominant Lactobacillus Species. Appl Environ Microbiol 77: 378-381.
64. Schellenberg J, Links MG, Hill JE, Dumonceaux TJ, Peters GA, et al. (2009) Pyrosequencing of the chaperonin-60 universal target as a tool for determining microbial community composition. Appl Environ Microbiol 75: 2889-2898.