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1 . 2023

Role of oral probiotic lactobacilli in maintaining vaginal microbiome homeostasis

Abstract

The vaginal microbiome is a dynamic ecosystem that includes a large number of different types of microorganisms, which are influenced by ethnicity of women, their residence in a certain geographical region, social status, dietary habits, personal hygiene, sexual behavior, etc. The vaginal microbiome changes throughout life from newborn to postmenopausal and largely determines a woman’s quality of life. The bases of the vaginal microbiome of a woman of reproductive age are lactobacillus. In case of violation of the physiological microbiocenosis of the vagina, an additional subsidy of lactobacilli is necessary. This literature review aims to evaluate the role of oral probiotic lactobacilli in maintaining the homeostasis of the female vaginal microbiome.

Keywords:vaginal microbiome; lactobacilli; homeostasis; oral probiotic lactobacilli

Funding. The study had no sponsor support.

Conflict of interest. The authors declare no conflict of interest.

For citation: Savicheva A.M., Budilovskaya O.V., Tapilskaya N.I. Role of oral probiotic lactobacilli in maintaining vaginal microbiome homeostasis. Akusherstvo i ginekologiya: novosti, mneniya, obuchenie [Obstetrics and Gynecology: News, Opinions, Training]. 2023; 11 (1): 33–42. DOI: https://doi.org/10.33029/2303-9698-2023-11-1-33-42 (in Russian)

References

1. Durán A.B., Fuentes-López A., de Salazar A., Plaza-Díaz J., García F. Reviewing the composition of vaginal microbiota: Inclusion of nutrition and probiotic factors in the maintenance of eubiosis. Nutrients. 2020; 12 (2): 419. DOI: https://doi.org/10.3390/nu12020419

2. Kira E.F. Bacterial vaginosis. Moscow: Meditsinskoe informatsionnoe agentstvo, 2012: 472 p. (in Russian)

3. Belizário J.E., Napolitano M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front Microbiol. 2015; 6: 1050.

4. Rizk M.G., Thackray V.G. Intersection of polycystic ovary syndrome and the gut microbiome. J Endocr Soc. 2020; 5 (2): bvaa177. PMID: 33381671.

5. Lee L.-H., Ser H.-L., Khan T.M., Gan K.-G., Goh B.-H., Ab Mutalib N.-S. Relationship between autism and gut microbiome: Current status and update. Gut. 2019; 68. DOI: https://doi.org/10.1136/gutjnl-2019-IDDFAbstracts.76

6. Pramanick R., Mayadeo N., Warke H., Begum S., Aich P., Aranha C. Vaginal microbiota of asymptomatic bacterial vaginosis and vulvovaginal candidiasis: Are they different from normal microbiota? Microb Pathog. 2019; 134: 103599. DOI: https://doi.org/10.1016/j.micpath.2019.103599 Epub 2019 Jun 15. PMID: 31212037.

7. Sinyakova A.A., Shipitsyna E.V., Budilovskaya O.V., Bolotskikh V.M., Savicheva A.M.. The efficiency of treatment of vaginal infections in women with a history of miscarriage. Zhurnal akusherstva i zhenskikh bolezney [Journal of Obstetrics and Women’s Diseases]. 2019; 68 (5): 63–74. DOI: https://doi.org/10.17816/JOWD68563-74 (in Russian)

8. Bautista C.T., Wurapa E., Sateren W.B., et al. Bacterial vaginosis: A synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections. Mil Med Res. 2016; 3: 4.

9. Edwards V.L., Smith S.B., McComb E.J., et al. The cervicovaginal microbiota host interaction modulates Chlamydia trachomatis infection. mBio. 2019; 10 (4): e01548-19.

10. Bradshaw C.S., Morton A.N., Hocking J., Garland S.M., Morris M.B., Moss L.M., 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 (11): 1478–86. DOI: https://doi.org/10.1086/503780

11. Arastehfar A., Kargar M.L., Mohammadi S.R., Roudbary M., Ghods N., Haghighi L., et al. A high rate of recurrent vulvovaginal candidiasis and therapeutic failure of azole derivatives among Iranian women. Front Microbiol. 2021; 12: 655069.

12. McDonald B., McCoy K.D. Maternal microbiota in pregnancy and early life. Science. 2019; 365: 984–5.

13. Rodriguez D.A., Peña Vélez R., Toro Monjaraz E.M., Ramirez Mayans J., MacDaragh Ryan P. The gut microbiota: A clinically impactful factor in patient health and disease. SN Compr Clin Med. 2019; 1: 188–99.

14. Prevention of early-onset neonatal group B streptococcal disease: Green-top guideline No. 36. BJOG. 2017; 124 (12): e280–305. DOI: https://doi.org/10.1111/1471-0528.14821

15. Khvan V.O., Shipitsyna E.V., Zatsiorskaya S.L., Grinenko G.V., Shalepo K.V., Savicheva A.M. Frequency and risk factors of colonization of pregnant women with group B streptococci. Zhurnal akusherstva i zhenskikh bolezney [Journal of Obstetrics and Women’s Diseases]. 2017; 66 (6): 44–58. DOI: https://doi.org/10.17816/JOWD66644-58 (in Russian)

16. Money D., Allen V.M. The prevention of early-onset neonatal group B streptococcal disease. J Obstet Gynaecol Can. 2013; 35 (10): 939–48. DOI: https://doi.org/10.1016/S1701-2163(15)30818-5

17. Sgayer I., Gur T., Glikman D., Rechnitzer H., Bornstein J., Wolf M.F. Routine uterine culture swab during cesarean section and its clinical correlations: A retrospective comparative study. Eur J Obstet Gynecol Reprod Biol. 2020; 249: 42–6. DOI: https://doi.org/10.1016/j.ejogrb.2020.04.011

18. Verani J.R., McGee L., Schrag S.J.; Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention (CDC). Prevention of Perinatal Group B Streptococcal Disease – revised guidelines from CDC, 2010. MMWR Recomm Rep. 2010; 59 (RR-10): 1–36.

19. Order of the Ministry of Health of the Russian Federation dated October 20, 2020 number 1130n «On approval of the Procedure for providing medical care in the profile “obstetrics and gynecology”». URL: https://mz19.ru/bnsi/detail.php?id=10199 (date of access February 18, 2022). (in Russian)

20. Clinical guidelines «Microbiological diagnosis of infections caused by group B streptococcus in pregnant women and newborns». Moscow, 2016. (in Russian)

21. Davis R.L., Hasselquist M.B., Cardenas V., Zerr D.M., Kramer J., Zavitkovsky A., et al. Introduction of the new Centers for Disease Control and Prevention group B streptococcal prevention guideline at a large West Coast health maintenance organization. Am J Obstet Gynecol. 2001; 184: 603–10.

22. Kolousova K.A., Shipitsyna E.V., Shalepo K.V., Savicheva A.M. Virulence and pathogenicity factors of S. agalactiae strains isolated from pregnant women and newborns. Zhurnal akusherstva i zhenskikh bolezney [Journal of Obstetrics and Women’s Diseases]. 2021; 70 (5): 15–22. DOI: https://doi.org/10.17816/JOWD75671 (in Russian)

23. Zimmermann P., Curtis N. Effect of intrapartum antibiotics on the intestinal microbiota of infants: A systematic review. Arch Dis Child Fetal Neonatal Ed. 2020; 105: 201–8.

24. Tapiainen T., Koivusaari P., Brinkac L., Lorenzi H., Salo J., Renko M., et al. Impact of intrapartum and postnatal antibiotics on the gut microbiome and emergence of antimicrobial resistance in infants. Sci Rep. 2019; 9: 10635.

25. Back E.E., O’Grady E.J., Back J.D. High rates of perinatal group B Streptococcus clindamycin and erythromycin resistance in an Upstate New York Hospital. Antimicrob Agents Chemother. 2012; 56: 739–42.

26. Spaetgens R. Perinatal antibiotic usage and changes in colonization and resistance rates of group B streptococcus and other pathogens. Obstet Gynecol. 2002; 100: 525–33.

27. Bruce A.W., Chadwick P., Hassan A., VanCott G.F. Recurrent urethritis in women. Can Med Assoc J. 1973; 108 (8): 973–6.

28. Shah T., Baloch Z., Shah Z., et al. The intestinal microbiota: Impacts of antibiotics therapy, colonization resistance, and diseases. Int J Mol Sci. 2021; 22 (12): 6597. PMID: 34202945.

29. Sanders M.E., Merenstein D., Merrifield C.A., Hutkins R. Probiotics for human use. Nutr Bull. 2018; 43 (3): 212–25.

30. Antonio M.A.D., Rabe L.K., Hillier S.L. Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J Infect Dis. 2005; 192 (3): 394–8. DOI: https://doi.org/10.1086/430926

31. Bastani P., Homayouni A., Tabrizian V.G., Ziyadi S. Dairy probiotic foods and bacterial vaginosis: A review on mechanism of action. In: E. Rigobelo (ed.). Probiotics. IntechOpen, 2012. DOI: https://doi.org/10.5772/50083

32. Leonova M.V. Probiotics in the treatment of vaginal infections: efficacy from the perspective of evidence-based medicine. Meditsinskiy sovet [Medical Council]. 2020; (13): 148–54. DOI: https://doi.org/10.21518/2079-701X-2020-13-148-154 (in Russian)

33. Libertucci J., Young V.B. The role of the microbiota in infectious diseases. Nat Microbiol. 2019; 4: 35–45. DOI: https://doi.org/10.1038/s41564-018-0278-4

34. Han Y., Ren Q.L. Does probiotics work for bacterial vaginosis and vulvovaginal candidiasis. Curr Opin Pharmacol. 2021; 61: 83–90. DOI: https://doi.org/10.1016/j.coph.2021.09.004

35. Leccese Terraf M.C., Mendoza L.M., Juárez Tomás M.S., et al. Phenotypic surface properties (aggregation, adhesion and biofilm formation) and presence of related genes in beneficial vaginal lactobacilli. J Appl Microbiol. 2014; 117 (6): 1761–72. DOI: https://doi.org/10.1111/jam.12642

36. Leccese Terraf M.C., Juarez Tomás M.S., Rault L., et al. In vitro effect of vaginal lactobacilli on the growth and adhesion abilities of uropathogenic Escherichia coli. Arch Microbiol. 2017; 199 (5): 767–74. DOI: https://doi.org/10.1007/s00203-016-1336-z

37. De Gregorio P.R., Maldonado N.C., Pingitore E.V., et al. Intravaginal administration of gelatine capsules containing freeze–dried autochthonous lactobacilli: A double–blind, randomised clinical trial of safety. Benef Microbes. 2020; 11 (1): 5–17. DOI: https://doi.org/10.3920/BM2019.0081

38. De Gregorio P.R., Tomás M.S.J., Terraf M.C.L., Nader–Macías M.E.F. In vitro and in vivo effects of beneficial vaginal lactobacilli on pathogens responsible for urogenital tract infections. J Med Microbiol. 2014; 63 (pt 5): 685–96. DOI: https://doi.org/10.1099/jmm.0.069401-0

39. Zheng J., Wittouck S., Salvetti E., Franz C.M.A.P., Harris H.M.B., Mattarelli P., et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol. 2020; 70 (4): 2782–858. DOI: https://doi.org/10.1099/ijsem.0.004107 Epub 2020 Apr 15. PMID: 32293557.

40. Melkumyan A.R., Priputnevich T.V. Vaginal lactobacilli: current approaches to species identification and to the study of their role in the microbial community. Akusherstvo i ginekologiya [Obstetrics and Gynecology]. 2013; (7): 18–23. (in Russian)

41. Reid G. The scientific basis for probiotic strains of Lactobacillus. Appl Environ Microbiol. 1999; 65 (9): 3763–6. PMID: 10473372

42. Santos C.M.A., Pires M.C.V., Leao T.L., Hernandez Z.P., Rodriguez M.L., Martins A.K.S., et al. Selection of Lactobacillus strains as potential probiotics for vaginitis treatment. Microbiology. 2016; 162 (7): 1195–207. DOI: https://doi.org/10.1099/mic.0.000302

43. Mogha K.V., Prajapati J.B. Probiotics for treating bacterial vaginosis. Rev Med Microbiol. 2016; 27 (3): 87–94. DOI: https://doi.org/10.1097/MRM.0000000000000080

44. Reid G. Probiotics: definition, scope and mechanisms of action. Best Pract Res Clin Gastroenterol. 2016; 30 (1): 17–25. DOI: https://doi.org/10.1016/j.bpg.2015.12.001

45. Bertuccini L., Russo R., Iosi F., Superti F. Effects of Lactobacillus rhamnosus and Lactobacillus acidophilus on bacterial vaginal pathogens. Int J Immunopathol Pharmacol. 2017; 30 (2): 163–67. DOI: https://doi.org/10.1177/0394632017697987

46. De Alberti D., Russo R., Terruzzi F., Nobile V., Ouwehand A.C. Lactobacilli vaginal colonisation after oral consumption of Respecta® complex: A randomised controlled pilot study. Arch Gynecol Obstet. 2015; 292: 861–7.

47. Mezzasalma V., Manfrini E., Ferri E., Boccarusso M., Di Gennaro P., Schiano I., et al. Orally administered multispecies probiotic formulations to prevent uro-genital infections: A randomized placebo-controlled pilot study. Arch Gynecol Obstet. 2017; 295: 163–72.

48. Jang S.E., Jeong J.J., Choi S.Y., Kim H., Han M.J., Kim D.H. Lactobacillus rhamnosus HN001 and Lactobacillus acidophilus GLA-14 attenuate Gardnerella vaginalis-infected bacterial vaginosis in mice. Nutrients. 2017; 9 (6): 531. DOI: https://doi.org/10.3390/nu9060531 PMID: 28545241; PMCID: PMC5490510.

49. Russo R., Karadja E., De Seta F. Evidence-based mixture containing Lactobacillus strains and lactoferrin to prevent recurrent bacterial vaginosis: A double blind, placebo controlled, randomised clinical trial. Benef Microbes. 2019; 10 (1): 19–26. DOI: https://doi.org/10.3920/BM2018.0075 Epub 2018 Dec 10. PMID: 30525953.

50. Russo R., Superti F., Karadja E., De Seta F. Randomised clinical trial in women with Recurrent Vulvovaginal Candidiasis: Efficacy of probiotics and lactoferrin as maintenance treatment. Mycoses. 2019; 62 (4): 328–35. DOI: https://doi.org/10.1111/myc.12883 Epub 2019 Feb 20. PMID: 30565745.

51. McMillan A., Rulisa S., Gloor G.B., Macklaim J.M., Sumarah M., Reid G. Pilot assessment of probiotics for pregnant women in Rwanda. PLoS One. 2018; 13 (6): e0195081. DOI: https://doi.org/10.1371/journal.pone.0195081

52. Ho M., Chang Y.Y., Chang W.C., et al. Oral Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 to reduce Group B Streptococcus colonization in pregnant women: A randomized controlled trial. Taiwan J Obstet Gynecol. 2016; 55 (4): 515–8. DOI: https://doi.org/10.1016/j.tjog.2016.06.003

53. Menichini D., Chiossi G., Monari F., De Seta F., Facchinetti F. Supplementation of probiotics in pregnant women targeting Group B Streptococcus colonization: A systematic review and meta-analysis. Nutrients. 2022; 14 (21): 4520. DOI: https://doi.org/10.3390/nu14214520 Epub 2022 Oct 27.

54. Rosen G.H., Randis T.M., Desai P.V., Sapra K.J., Ma B., Gajer P., et al. Group B Streptococcus and the vaginal microbiota. J Infect Dis. 2017; 216: 744–51.

55. Tachedjian G., Aldunate M., Bradshaw C.S., Cone R.A. The role of lactic acid production by probiotic Lactobacillus species in vaginal health. Res Microbiol. 2017; 168: 782–92.

56. Petrova M.I., Imholz N.C.E., Verhoeven T.L.A., Balzarini J., Van Damme E.J.M., Schols D., et al. Lectin-like molecules of Lactobacillus rhamnosus GG inhibit pathogenic Escherichia coli and Salmonella biofilm formation. PLoS One. 2016; 11: e0161337.

57. Sheyholislami H., Connor K.L. Are Probiotics and prebiotics safe for use during pregnancy and lactation? A systematic review and meta-analysis. Nutrients. 2021; 13: 2382.

58. Kolesayeva Zh.Yu., Kucherenko M.A., Martikaynen Z.M., Tarasova M.A., Savicheva A.M. Correction of vaginal microbiocenosis of puerperas. Zhurnal akusherstva i zhenskikh bolezney [Journal of Obstetrics and Women’s Diseases]. 2011; LX (4): 55–61.

59. Allonsius C.N., Vandenheuvel D., Oerlemans E.F.M., Petrova M.I., Donders G.G.G., Cos P., et al. Inhibition of Candida albicans morphogenesis by chitinase from Lactobacillus rhamnosus GG. Sci Rep. 2019; 9 (1): 2900.

60. Martinez R.C., Franceschini S.A., Patta M.C., et al. Improved treatment of vulvovaginal candidiasis with fluconazole plus probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14. Lett Appl Microbiol. 2009; 48 (3): 269–74. DOI: https://doi.org/10.1111/j.1472-765X.2008.02477.x

61. Saunders S., Bocking A., Challis J., Reid G. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Colloids Surf B Biointerfaces. 2007; 55 (2): 138–42. DOI: https://doi.org/10.1016/j.colsurfb.2006.11.040

62. McMillan A., Dell M., Zellar M.P., Cribby S., Martz S., Hong E., et al. Disruption of urogenital biofilms by Lactobacilli. Colloids Surf B Biointerfaces. 2011; 86 (1): 58–64. DOI: https://doi.org/10.1016/j.colsurfb.2011.03.016

63. Chieng W.K., Abdul Jalal M.I., Bedi J.S., et al. Probiotics, a promising therapy to reduce the recurrence of bacterial vaginosis in women? A systematic review and meta-analysis of randomized controlled trials. Front Nutr. 2022; 9: 938838. DOI: https://doi.org/10.3389/fnut.2022.938838 Epub 2022 Sep 20.

64. Savicheva A.M., Tapil’skaya N.I., Krysanova A.A., Budilovskaya O.V., Khusnutdinova T.A., Shalepo K.V. Long-term results of two-stage treatment of bacterial vaginosis using antiseptics and probiotics. Akusherstvo i ginekologiya: novosti, mneniya, obuchenie [Obstetrics and Gynecology: News, Opinions, Training]. 2021; 9 (4): 19–28. DOI: https://doi.org/10.33029/2303-9698-2021-9-4-19-28 (in Russian)

65. Vujic G., Jajac Knez A., Despot Stefanovic V., Kuzmic Vrbanovic V. Efficacy of orally applied probiotic capsules for bacterial vaginosis and other vaginal infections: A double-blind, randomized, placebo-controlled study. Eur J Obstet Gynecol Reprod Biol. 2013; 168 (1): 75–9. DOI: https://doi.org/10.1016/j.ejogrb.2012.12.031

66. Chen R., Li R., Qing W., Zhang Y., Zhou Z., Hou Y., et al. Probiotics are a good choice for the treatment of bacterial vaginosis: A meta-analysis of randomized controlled trial. Reprod Health. 2022; 19 (1): 137. DOI: https://doi.org/10.1186/s12978-022-01449-z PMID: 35698149; PMCID: PMC9195231.

67. Joseph R.J., Ser H.L., Kuai Y.H., Tan L.T., Arasoo V.J.T., Letchumanan V., et al. Finding a balance in the vaginal microbiome: How do we treat and prevent the occurrence of bacterial vaginosis? Antibiotics (Basel). 2021; 10 (6): 719. DOI: https://doi.org/10.3390/antibiotics10060719

68. Huang H., Song L., Zhao W. Effects of probiotics for the treatment of bacterial vaginosis in adult women: A meta-analysis of randomized clinical trials. Arch Gynecol Obstet. 2014; 289: 1225–34. DOI: https://doi.org/10.1007/s00404-013-3117-0

69. Jeng H.S., Yan T.R., Chen J.Y. Treating vaginitis with probiotics in non-pregnant females: A systematic review and meta-analysis. Exp Ther Med. 2020; 20: 3749–65. DOI: https://doi.org/10.3892/etm.2020.9090

70. Petricevic L., Unger F.M., 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 (1): 54–7. DOI: https://doi.org/10.1016/j.ejogrb.2008.06.003

71. Reid G. The development of probiotics for women’s health. Can J Microbiol. 2017; 63 (4): 269–77. DOI: https://doi.org/10.1139/cjm-2016-0733

72. Reid G., Bruce A.W. Urogenital infections in women – can probiotics help? Postgrad Med J. 2003; 79: 428–32.

73. Potgieter M., Bester J., Kell D.B., Pretorius E. The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol Rev. 2015; 39 (4): 567–91. DOI: https://doi.org/10.1093/femsre/fuv013

74. Wiest R., Lawson M., Geuking M. Pathological bacterial translocation in liver cirrhosis. J Hepatol. 2014; 60: 197–209.

75. Venkatesh M., Mukherjee S., Wang H., et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity. 2014; 41: 296–310.

76. Zhang Y., Lyu J., Ge L., Huang L., Peng Z., Liang Y., et al. Probiotic Lacticaseibacillus rhamnosus GR-1 and Limosilactobacillus reuteri RC-14 as an adjunctive treatment for bacterial vaginosis do not increase the cure rate in a Chinese cohort: A prospective, parallel-group, randomized, controlled study. Front Cell Infect Microbiol. 2021; 11: 669901. DOI: https://doi.org/10.3389/fcimb.2021.669901 PMID: 34295831; PMCID: PMC8291149.

77. Bradshaw C.S., Pirotta M., De Guingand D., et al. Efficacy of oral metronidazole with vaginal clindamycin or vaginal probiotic for bacterial vaginosis: Randomised placebo-controlled double-blind trial. PLoS One. 2012; 7 (4): e34540. DOI: https://doi.org/10.1371/journal.pone.0034540

78. Wijgert J., Verwijs M. Lactobacilli-containing vaginal probiotics to cure or prevent bacterial or fungal vaginal dysbiosis: A systematic review and recommendations for future trial designs. BJOG. 2020; 127: 287–99.

79. Farr A., Sustr V., Kiss H., et al. Oral probiotics to reduce vaginal group B streptococcal colonization in late pregnancy. Sci Rep. 2020; 10 (1): 19745. DOI: https://doi.org/10.1038/s41598-020-76896-4

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CHIEF EDITORS
CHIEF EDITOR
Sukhikh Gennadii Tikhonovich
Academician of the Russian Academy of Medical Sciences, V.I. Kulakov Obstetrics, Gynecology and Perinatology National Medical Research Center of Ministry of Healthсаre of the Russian Federation, Moscow
CHIEF EDITOR
Kurtser Mark Arkadievich
Academician of the Russian Academy of Sciences, MD, Professor, Head of the Obstetrics and Gynecology Subdepartment of the Pediatric Department, N.I. Pirogov Russian National Scientific Research Medical University, Ministry of Health of the Russian Federation
CHIEF EDITOR
Radzinsky Viktor Evseevich
Corresponding Member of the Russian Academy of Sciences, MD, Professor, Head of the Subdepartment of Obstetrics and Gynecology with a Course of Perinatology of the Medical Department in the Russian People?s Friendship University

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