Probiotic strategies for the treatment and prevention of bacterial vaginosis

Expert Opinion on Pharmacotherapy

Volumn 11, Issue 18, 2010, Pages 2985-2995

  MacPhee, Roderick A ^a   Hummelen, Ruben ^a,b   Bisanz, Jordan E ^a   Miller, Wayne L ^a   Reid, Gregor ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Bacterial vaginosis; Lactobacillus; Probiotics; Vaginal microbiota

Indexed keywords

AMOXICILLIN; CLINDAMYCIN; COTRIMOXAZOLE; METRONIDAZOLE; PROBIOTIC AGENT; TINIDAZOLE; YOGHURT;

CLINICAL TRIAL; DRUG MECHANISM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; NONHUMAN; REVIEW; SECONDARY PREVENTION; URINARY TRACT INFECTION; UROGENITAL TRACT INFECTION; VAGINA CANDIDIASIS; VAGINA FLORA; VAGINITIS;

ANIMALS; CLINICAL TRIALS AS TOPIC; FEMALE; HUMANS; LACTOBACILLUS; PROBIOTICS; RECURRENCE; VAGINA; VAGINOSIS, BACTERIAL;

EID: 78649239107     PISSN: 14656566     EISSN: None     Source Type: Journal    
DOI: 10.1517/14656566.2010.512004     Document Type: Review

References (68)

1. Antonio MA, Hawes SE, Hillier SL. The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 1999;180:1950-6
2. Zozaya-Hinchliffe M, Lillis R, Martin DH, Ferris MJ. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J Clin Microbiol 2010;48:1812-19 • Good paper using quantitative real-time PCR (qPCR) assays to facilitate assessments of bacterial abundance in vaginal specimens.
3. Hummelen R, Macklaim J, Fernandes A, et al. Deep sequencing of the vaginal microbiome in HIV patients. PLoS ONE 2010;5(8):e12078 •• New technique that has uncovered 4 clusters of bacteria associated with BV and 4 associated with healthy.
4. Christensen HR, Frokiaer H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002;168:171-8
5. Reid G, Dols J, Miller W. Targeting the vaginal microbiota with probiotics as a means to counteract infections. Curr Opin Clin Nutr Metab Care 2009;12:583-7 • Good review.
6. Schwebke JR, Richey CM, Weiss HL. Correlation of behaviors with microbiological changes in vaginal flora. J Infect Dis 1999;180:1632-6
7. Keane FE, Ison CA, Taylor-Robinson D. A longitudinal study of the vaginal flora over a menstrual cycle. Int J STD AIDS 1997;8:489-94
8. Valore EV, Park CH, Igreti SL, Ganz T. Antimicrobial components of vaginal fluid. Am J Obstet Gynecol 2002;187:561-8
9. 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(Suppl 6):13-8 • Imporant assessment of mechanisms of lactobacilli anti-infective properties.
10. Eschenbach DA, Thwin SS, Patton DL, et al. Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis 2000;30:901-7
11. Srinivasan S, Liu C, Mitchell CM, et al. Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 2010;5:e10197 •• Interesting insight into the composition of the vaginal microbiota.
12. Heinemann C, Reid G. Vaginal microbial diversity among postmenopausal women with and without hormone replacement therapy. Can J Microbiol 2005;51:777-81
13. 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
14. Zhou X, Brown CJ, Abdo Z, et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 2007;1:121-33
15. Hitti J, Nugent R, Boutain D, et al. Racial disparity in risk of preterm birth associated with lower genital tract infection. Paediatr Perinat Epidemiol 2007;21:330-7
16. Peipert JF, Lapane KL, Allsworth JE, et al. Bacterial vaginosis, race, and sexually transmitted infections: does race modify the association? Sex Transm Dis 2008;35:363-7 • Covers interesting concepts in why some women are more susceptible to infection.
17. Hillier SL. The complexity of microbial diversity in bacterial vaginosis. N Engl J Med 2005;353:1886-7
18. Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 2005;353:1899-911
19. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:297-301
20. Reid G, Burton J, Hammond J-A, Bruce AW. Nucleic acid based diagnosis of bacterial vaginosis and improved management using probiotic lactobacilli. J Med Food 2004;7:223-8
21. Bradshaw CS, Morton AN, Garland SM, et al. Evaluation of a point-of-care test, BVBlue, and clinical and laboratory criteria for diagnosis of bacterial vaginosis. J Clin Microbiol 2005;43:1304-8
22. Payne SC, Cromer PR, Stanek MK, Palmer AA. Evidence of African-American women's frustrations with chronic recurrent bacterial vaginosis. J Am Acad Nurse Pract 2010;22:101-8 • Notable quality of life discussion pointing out core problems with chronic BV.
23. Klebanoff MA, Schwebke JR, Zhang J, et al. Vulvovaginal symptoms in women with bacterial vaginosis. Obstet Gynecol 2004;104:267-72
24. Gomez LM, Sammel MD, Appleby DH, et al. Evidence of a gene-environment interaction that predisposes to spontaneous preterm birth: a role for asymptomatic bacterial vaginosis and DNA variants in genes that control the inflammatory response. Am J Obstet Gynecol 2010;202:386.e1-6 • Important correlation between aberrant microbiota and preterm birth.
25. Stock SJ, Duthie L, Tremaine T, et al. Elafin (SKALP/Trappin-2/proteinase inhibitor-3) is produced by the cervix in pregnancy and cervicovaginal levels are diminished in bacterial vaginosis. Reprod Sci 2009;16:1125-34
26. Iqbal SM, Ball TB, Levinson P, et al. Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition. AIDS 2009;23:1669-77 •• Identification of a factor that may put some women at higher risk of HIV.
27. Ness RB, Kip KE, Hillier SL, et al. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol 2005;162:585-90
28. Reid G, Cook RL, Bruce AW. Examination of strains of lactobacilli for properties which may influence bacterial interference in the urinary tract. J Urol 1987;138:330-5
29. Mastromarino P, Brigidi P, Macchia S, et al. Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets. J Appl Microbiol 2002;93:884-93
30. McLean NW, Rosenstein IJ. Characterisation and selection of a Lactobacillus species to re-colonise the vagina of women with recurrent bacterial vaginosis. J Med Microbiol 2000;49:543-52
31. Osset J, Bartolome RM, Garcia E, Andreu A. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J Infect Dis 2001;183:485-91
32. 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;27:251-6
33. Reid G, Bruce AW, Taylor M. Instillation of Lactobacillus and stimulation of indigenous organisms to prevent recurrence of urinary tract infections. Microecol Ther 1995;23:32-45
34. Gardiner GE, Heinemann C, Bruce AW, et al. Persistence of Lactobacillus fermentum RC-14 and Lactobacillus rhamnosus GR-1 but not L. rhamnosus GG in the human vagina as demonstrated by randomly amplified polymorphic DNA. Clin Diag Lab Immunol 2002;9:92-6
35. Kirjavainen PK, Laine RM, Carter D, et al. Expression of anti-microbial defense factors in vaginal mucosa following exposure to Lactobacillus rhamnosus GR-1. Int J Probiotics 2008;3:99-106
36. Burton JP, Cadieux P, Reid G. Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation. Appl Environ Microbiol 2003;69:97-101
37. McGroarty JA, Reid G. Detection of a Lactobacillus substance which inhibits Escherichia coli. Can J Microbiol 1988;34:974-8
38. Klebanoff SJ, Hillier SL, Eschenbach DA, Waltersdorph AM. Control of the microbial flora of the vagina by H2O2-generating lactobacilli. J Infect Dis 1991;164:94-100
39. Patterson JL, Girerd PH, Karjane NW, Jefferson KK. Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Am J Obstet Gynecol 2007;197:170 e171-7
40. Saunders S, Bocking A, Challis J, Reid G. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Coll Surf B Biointerfaces 2007;55:138-42
41. Morelli L, Zonenenschain D, Del Piano M, Cognein P. Utilization of the intestinal tract as a delivery system for urogenital probiotics. J Clin Gastroenterol 2004;38:S107-10
42. Reid G, Bruce AW, Fraser N, et al. Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol 2001;30:49-52
43. Reid G, Charbonneau D, Erb J, et al. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol 2003;35:131-4
44. Antonio MA, Rabe LK, Hillier SL. Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J Infect Dis 2005;192:394-8 • Documentation of the importance of lactobacilli transfer from rectum to vagina.
45. Bradshaw CS, Morton AN, Hocking J, et al. High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J Infect Dis 2006;193:1478-86
46. Oduyebo OO, Anorlu RI, Ogunsola FT. The effects of antimicrobial therapy on bacterial vaginosis in non-pregnant women. Cochrane Database Syst Rev 2009;3:CD006055 • Interesting summary of antibiotic treatment of BV.
47. Mastromarino P, Macchia S, Meggiorini L, et al. Effectiveness of Lactobacillus-containing vaginal tablets in the treatment of symptomatic bacterial vaginosis. Clin Microbiol Infect 2009;15:67-74 • A more recent development of a vaginal probiotic.
48. Hallen A, Jarstrand C, Pahlson C. Treatment of bacterial vaginosis with lactobacilli. Sex Transm Dis 1992;19:146-8
49. Rossi A, Rossi T, Bertini M, Caccia G. The use of Lactobacillus rhamnosus in the therapy of bacterial vaginosis. Evaluation of clinical efficacy in a population of 40 women treated for 24 months. Arch Gynecol Obstet 2010;281:1065-9 • A more recent development of a vaginal probiotic.
50. Anukam KC, Osazuwa E, Osemene GI, et al. Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect 2006;8:2772-6
51. Anukam K, Osazuwa E, Ahonkhai I, et al. Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial. Microbes Infect 2006;8:1450-4 •• First study showing efficacy of combined probiotic and antibiotic therapy.
52. Martinez RC, Franceschini SA, Patta MC, et al. Improved cure of bacterial vaginosis with single dose of tinidazole (2g) and Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: a randomized, double-blind, placebo-controlled trial. Can J Microbiol 2009;55:133-8 • Confirmation that probiotic lactobacilli can improve cure of BV.
53. Larsson PG, Stray-Pedersen B, Ryttig KR, Larsen S. Human lactobacilli as supplementation of clindamycin to patients with bacterial vaginosis reduce the recurrence rate; a 6-month, double-blind, randomized, placebo-controlled study. BMC Womens Health 2008;8:3
54. Eriksson K, Carlsson B, Forsum U, Larsson PG. A double-blind treatment study of bacterial vaginosis with normal vaginal lactobacilli after an open treatment with vaginal clindamycin ovules. Acta Derm Venereol 2005;85:42-6
55. Petricevic L, Witt A. The role of Lactobacillus casei rhamnosus Lcr35 in restoring the normal vaginal flora after antibiotic treatment of bacterial vaginosis. BJOG 2008;115:1369-74
56. Shalev E, Battino S, Weiner E, et al. Ingestion of yogurt containing Lactobacillus acidophilus compared with pasteurized yogurt as prophylaxis for recurrent candidal vaginitis and bacterial vaginosis. Arch Fam Med 1996;5:593-6
57. Marcone V, Calzolari E, Bertini M. Effectiveness of vaginal administration of Lactobacillus rhamnosus following conventional metronidazole therapy: how to lower the rate of bacterial vaginosis recurrences. New Microbiol 2008;31:429-33
58. Petricevic L, Unger FM, Viernstein H, Kiss H. Randomized, double-blind, placebo-controlled study of oral lactobacilli to improve the vaginal flora of postmenopausal women. Eur J Obstet Gynecol Reprod Biol 2008;141:54-7 • Evidence for probiotics to improve vaginal health in postmenopausal women.
59. Beereport MAJ, Ter Riet M, Nys S, et al. Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 versus trimethoprim-sulfamethoxazole (TMP/SMX) in the prevention of recurrent urinary tract infections (rUTIs) in postmenopausal women: a randomized double-blind non-inferiority trial. ICAAC 2009; abstract identifier: L1-1656a •• Although not yet published in full, this is an exciting development that shows lactobacilli as effective as antibiotic in preventing infection.
60. Allsworth JE, Peipert JF. Prevalence of bacterial vaginosis: 2001-2004 National Health and Nutrition Examination Survey data. Obstet Gynecol 2007;109:114-20 • Excellent survey showing high prevalence of BV.
61. Hemmerling A, Harrison W, Schroeder A, et al. Phase 1 dose-ranging safety trial of Lactobacillus crispatus CTV-05 for the prevention of bacterial vaginosis. Sex Transm Dis 2009;36:564-9
62. Antonio MA, Meyn LA, Murray PJ, et al. Vaginal colonization by probiotic Lactobacillus crispatus CTV-05 is decreased by sexual activity and endogenous lactobacilli. J Infect Dis 2009;199:1506-13 •• Very interesting observations about factors that can influence the ability of exogenous lactobacilli to confer benefits on the host.
63. Anukam KC, Osazuwa EO, Reid G, Katsivo MN. Receptivity for probiotic products among premenopausal female students in an African university. Sex Transm Dis 2004;31:460-4
64. Marrazzo JM, Cook RL, Wiesenfeld HC, et al. Women's satisfaction with an intravaginal Lactobacillus capsule for the treatment of bacterial vaginosis. J Womens Health (Larchmt) 2006;15:1053-60
65. Bruce AW, Chadwick P, Hassan A, VanCott GF. Recurrent urethritis in women. Can Med Assoc J 1973;108:973-6
66. Chang TL, Chang CH, Simpson DA, et al. Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4. Proc Natl Acad Sci USA 2003;100:11672-7
67. Liu JJ, Reid G, Jiang Y, et al. Expression of HIV-inactivating proteins by recombinant human vaginal probiotic Lactobacillus reuteri RC-14. Cell Microbiol 2007;9:120-30
68. Vangelista L, Secchi M, Liu X, et al. Engineering of Lactobacillus jensenii to secrete RANTES and a CCR5 antagonist analogue as live HIV-1 blockers. Antimicrob Agents Chemother 2010;54(7):2994-3001 • A new lactobacilli recombinant strain that may help prevent HIV infection.