Bacterial vaginosis as a factor associated with adverse pregnancy outcomes

Abstract

Bacterial vaginosis is the most common disease of the genitals and affects 20–70% of women. This non-inflammatory syndrome is characterized by dysbiosis of the vaginal microbiota and is accompanied by a decrease in the number of lactobacilli. Bacterial vaginosis in 60% of pregnant women is asymptomatic, but can lead to obstetric complications such as late miscarriage, premature birth, fetal growth restriction, premature rupture of membranes, choriominionitis, postpartum endometritis, and sepsis. The clinical picture of bacterial vaginosis in pregnant women is the same as in non-pregnant women, namely homogeneous whitish-gray discharge from the genital tract, often with an unpleasant “fishy” smell, rarely itching and/or burning in the genital area and urethra, as well as soreness during urination (dysuria), with no signs of an inflammation detected in the genitals. Diagnosis of bacterial vaginosis in pregnant women, as well as in non-pregnant women, is based on the use of clinical and laboratory methods. Multiplex tests based on the nucleic acid amplification method, such as real-time polymerase chain reaction, are very popular for the diagnosis of bacterial vaginosis in this country. The Femoflor-16 Reagent Kit (DNA Technology CJSC, Moscow, Russia) is designed to detect the DNA of opportunistic microorganisms, lactobacilli DNA and human genomic DNA (as a control for taking biological material). Examination of pregnant women, especially in case of complaints of vaginal discharge, should be carried out when registering for pregnancy in order to start treatment early and prevent adverse pregnancy outcomes for the mother and fetus. Biofilms formed by microorganisms in bacterial vaginosis, especially G. vaginalis, limit the penetration of antibacterial agents to bacteria, their concentration being lower than therapeutic one, which leads to ineffective treatment. There remain many unexplored issues related to changes in the epidemiology of bacterial vaginosis, an increase in the frequency of relapses against the background of increasing resistance of microorganisms associated with bacterial vaginosis to antibiotics, and the development of agents that affect bacterial films.

Keywords

bacterial vaginosis / premature birth / premature rupture of membranes / complications of pregnancy / biofilms / bacterial films

References

[1] Dibo M, Ventimiglia MS, Valeff N, et al. An overview of the role of probiotics in pregnancy-associated pathologies with a special focus on preterm birth. J Reprod Immunol. 2022;150. DOI: 10.1016/j.jri.2022.103493

[2] Dibo M., Ventimiglia M.S., Valeff N., et al. An overview of the role of probiotics in pregnancy-associated pathologies with a special focus on preterm birth // J. Reprod. Immunol. 2022. Vol. 150. DOI: 10.1016/j.jri.2022.103493

[3] Rossiyskoe obshchestvo dermatovenerologov i kosmetologov. Bakterial’nyy vaginoz. Klinicheskie rekomendatsii. 2022. (In Russ.) [cited 2023 Jul 16]. Available from: https://cr.minzdrav.gov.ru/recomend/206_2

[4] Российское общество дерматовенерологов и косметологов. Бактериальный вагиноз. Клинические рекомендации. 2022 [дата обращения 16.07.2023]. Доступ по ссылке: https://cr.minzdrav.gov.ru/recomend/206_2

[5] Barrow RY, Ahmed F, Bolan GA, et al. Recommendations for providing quality sexually transmitted diseases clinical services, 2020. MMWR Recomm Rep. 2020;68(5):1–20. DOI: 10.15585/mmwr.rr6805a1

[6] Barrow R.Y., Ahmed F., Bolan G.A., et al. Recommendations for providing quality sexually transmitted diseases clinical services, 2020 // MMWR Recomm Rep. 2020. Vol. 68. No. 5. P. 1–20. DOI: 10.15585/mmwr.rr6805a1

[7] Gardner HL, Dukes CD. Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol. 1955;69(5):962–76. DOI: 10.1016/0002-9378(55)90095-8

[8] Gardner H.L., Dukes C.D. Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis // Am. J. Obstet. Gynecol. 1955. Vol. 69. No. 5. P. 962–976. DOI: 10.1016/0002-9378(55)90095-8

[9] Diop K, Dufour JC, Levasseur A, et al. Exhaustive repertoire of human vaginal microbiota. Hum Microbiome J. 2019;11. DOI: 10.1016/j.humic.2018.11.002

[10] Diop K., Dufour J.C., Levasseur A., et al. Exhaustive repertoire of human vaginal microbiota // Hum. Microbiome J. 2019. Vol. 11. DOI: 10.1016/j.humic.2018.11.002.

[11] Bitew A, Abebaw Y, Bekele D, et al. Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. Int J Microbiol. 2017;2017. DOI: 10.1155/2017/4919404

[12] Bitew A., Abebaw Y., Bekele D., et al. Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection // Int. J. Microbiol. 2017. Vol. 2017. DOI: 10.1155/2017/4919404

[13] Onderdonk AB, Delaney ML, Fichorova RN. The human microbiome during bacterial vaginosis. Clin Microbiol Rev. 2016;29:223–238. DOI: 10.1128/CMR.00075-15

[14] Onderdonk A.B., Delaney M.L., Fichorova R.N. The human microbiome during bacterial vaginosis // Clin. Microbiol. Rev. 2016. Vol. 29. P. 223–238. DOI: 10.1128/CMR.00075-15

[15] Hillier SL, Nougent RP, Eschenbach DA, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995;333(26):1737–1742. DOI: 10.1056/NEJM199512283332604

[16] Hillier S.L., Nugent R.P., Eschenbach D.A., et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The vaginal infections and prematurity study group // N. Engl. J. Med. 1995. Vol. 333. No. 26. P. 1737–1742. DOI: 10.1056/NEJM199512283332604

[17] Ugwumadu A, Manyonda I, Reid F, et al. Effect of early oral clindamycin on late miscarriage and preterm delivery in asymptomatic women with abnormal vaginal flora and bacterial vaginosis: a randomised controlled trial. Lancet. 2003;361(9362):983–988. DOI: 10.1016/S0140-6736(03)12823-1

[18] Ugwumadu A., Manyonda I., Reid F., et al. Effect of early oral clindamycin on late miscarriage and preterm delivery in asymptomatic women with abnormal vaginal flora and bacterial vaginosis: a randomised controlled trial // Lancet. 2003. Vol. 361. No. 9362. P. 983–988. DOI: 10.1016/S0140-6736(03)12823-1

[19] Ralph SG, Rutherford AJ, Wilson JD. Influence of bacterial vaginosis on conception and miscarriage in the first trimester: cohort study. BMJ. 1999;319(7204):220–223. DOI: 10.1136/bmj.319.7204.220

[20] Ralph S.G., Rutherford A.J., Wilson J.D. Influence of bacterial vaginosis on conception and miscarriage in the first trimester: cohort study // BMJ. 1999. Vol. 319. No. 7204. P. 220–223. DOI: 10.1136/bmj.319.7204.220

[21] Muzny CA, Schwebke JR. Biofilms: an underappreciated mechanism of treatment failure and recurrence in vaginal infections. Clin Infect Dis. 2015;61(4):601–606. DOI: 10.1093/cid/civ353

[22] Muzny C.A., Schwebke J.R. Biofilms: an underappreciated mechanism of treatment failure and recurrence in vaginal infections // Clin. Infect. Dis. 2015. Vol. 61. No. 4. P. 601–606. DOI: 10.1093/cid/civ353

[23] Dikke GB. Bacterial vaginosis: novel aspects of etiology, pathogenesis, and selection of therapeutic strategy. Russian Journal of Woman and Child Health. 2019;2(4):307–313. (In Russ.) DOI: 10.32364/2618-8430-2019-2-4-307-313

[24] Дикке Г.Б. Бактериальный вагиноз: новые аспекты этиопатогенеза и выбора терапевтических стратегий // РМЖ. Мать и дитя. 2019. Т. 2. № 4. С. 307–313. DOI: 10.32364/2618-8430-2019-2-4-307-313

[25] Cox C, Watt AP, McKenna JP, et al. Mycoplasma hominis and Gardnerella vaginalis display a significant synergistic relationship in bacterial vaginosis. Eur J Clin Microbiol Infect Dis. 2016;35(3):481–487. DOI: 10.1007/s10096-015-2564-x

[26] Cox C., Watt A.P., McKenna J.P., et al. Mycoplasma hominis and Gardnerella vaginalis display a significant synergistic relationship in bacterial vaginosis // Eur. J. Clin. Microbiol. Infect. Dis. 2016. Vol. 35. No. 3. P. 481–487. DOI: 10.1007/s10096-015-2564-x

[27] Swidsinski A, Mendling W, Loening-Baucke V, et al. Adherent biofilms in bacterial vaginosis. Obstet Gynecol. 2005;106(5):1013–1023. DOI: 10.1097/01.AOG.0000183594.45524.d2

[28] Swidsinski A., Mendling W., Loening-Baucke V., et al. Adherent biofilms in bacterial vaginosis // Obstet. Gynecol. 2005. Vol. 106. No. 5. P. 1013–1023. DOI: 10.1097/01.AOG.0000183594.45524.d2

[29] Hardy L, Jespers V, Abdellati S, et al. A fruitful alliance: the synergy between Atopobium vaginae and Gardnerella vaginalis in bacterial vaginosis-associated biofilm. Sex Transm Infect. 2016;92(7):487–491. DOI: 10.1136/sextrans-2015-052475

[30] Hardy L., Jespers V., Abdellati S., et al. A fruitful alliance: the synergy between Atopobium vaginae and Gardnerella vaginalis in bacterial vaginosis-associated biofilm // Sex. Transm. Infect. 2016. Vol. 92. No. 7. P. 487–491. DOI: 10.1136/sextrans-2015-052475

[31] Moi H, Fredlund H, Törnqvist E, et al. Mobiluncus species in bacterial vaginosis: aspects of pathogenesis. APMIS. 1991;99(11):1049–1054. DOI: 10.1111/j.1699-0463.1991.tb01298.x

[32] Moi H., Fredlund H., Törnqvist E., et al. Mobiluncus species in bacterial vaginosis: aspects of pathogenesis // APMIS. 1991. Vol. 99. No. 11. P. 1049–1054. DOI: 10.1111/j.1699-0463.1991.tb01298.x

[33] Dabee S, Passmore JS, Heffron R, et al. The complex link between the female genital microbiota, genital infections, and inflammation. Infect Immun. 2021;89(5). DOI: 10.1128/IAI.00487-20

[34] Dabee S., Passmore J.S., Heffron R., et al. The complex link between the female genital microbiota, genital infections, and inflammation // Infect. Immun. 2021. Vol. 89. No. 5. DOI: 10.1128/IAI.00487-20

[35] Doerflinger SY, Throop AL, Herbst-Kralovetz MM. Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner. J Infect Dis. 2014;209(12):1989–1999. DOI: 10.1093/infdis/jiu004

[36] Doerflinger S.Y., Throop A.L., Herbst-Kralovetz M.M. Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner // J. Infect. Dis. 2014. Vol. 209. No. 12. P. 1989–1999. DOI: 10.1093/infdis/jiu004

[37] Mendling W, Shazly MAE, Zhang L. The role of lactic acid in the management of bacterial vaginosis: a systematic literature review. Future Pharmacol. 2022;2(3):198–213. DOI: 10.3390/futurepharmacol2030014

[38] Mendling W., Shazly M.A.E., Zhang L. The role of lactic acid in the management of bacterial vaginosis: a systematic literature review // Future Pharm. 2022. Vol. 2. No. 3. P. 198–213. DOI: 10.3390/futurepharmacol2030014

[39] Coudray MS, Madhivanan P. Bacterial vaginosis – a brief synopsis of the literature. Eur J Obstet Gynecol Reprod Biol. 2020;245:143–148. DOI: 10.1016/j.ejogrb.2019.12.035

[40] Coudray M.S., Madhivanan P. Bacterial vaginosis – A brief synopsis of the literature // Eur. J. Obstet. Gynecol. Reprod. Biol. 2020. Vol. 245. P. 143–148. DOI: 10.1016/j.ejogrb.2019.12.035

[41] Savicheva AM, Shipitsyna EV. Bakterial’nyy vaginoz i be remennost’ (obzor literatury). Gynecology. 2012;14(3):38–43. (In Russ.)

[42] Савичева А.М., Шипицына Е.В. Бактериальный вагиноз и беременность (обзор литературы) // Гинекология. 2012. Т. 14. № 3. C. 38–43.

[43] Amsel R, Totten PA, Spiegel CA, et al. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med. 1983;74(1):14–22. DOI: 10.1016/0002-9343(83)91112-9

[44] Amsel R., Totten P.A., Spiegel C.A., et al. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations // Am. J. Med. 1983. Vol. 74. No. 1. P. 14–22. DOI: 10.1016/0002-9343(83)91112-9

[45] Forsum U, Jakobsson T, Larsson PG, et al. An international study of the interobserver variation between interpretations of vaginal smear criteria of bacterial vaginosis. APMIS. 2002;110(11):811–818. DOI: 10.1034/j.1600-0463.2002.1101107.x

[46] Forsum U., Jakobsson T., Larsson P.G., et al. An international study of the interobserver variation between interpretations of vaginal smear criteria of bacterial vaginosis // APMIS. 2002;110(11):811–818. DOI: 10.1034/j.1600-0463.2002.1101107.x

[47] Nazarova VV, Shipitsyna EV, Gerasimova EN, et al. Criteria for diagnosis of bacterial vaginosis using the test Femoflor-16. Journal of Obstetrics and Women’s Diseases. 2017;66(4):57–67. (In Russ.) DOI: 10.17816/JOWD66457-67

[48] Назарова В.В., Шипицына Е.В., Герасимова Е.Н., и др. Критерии диагностики бактериального вагиноза с использованием теста Фемофлор-16 // Журнал акушерства и женских болезней. 2017. № 4. С. 57–67. DOI: 10.17816/JOWD66457-67

[49] Rumyantseva T, Shipitsyna E, Guschin A, et al. Evaluation and subsequent optimizations of the quantitative AmpliSens Florocenosis/Bacterial vaginosis-FRT multiplex real-time PCR assay for diagnosis of bacterial vaginosis. APMIS. 2016;124(12):1099–1108. DOI: 10.1111/apm.12608

[50] Rumyantseva T., Shipitsyna E., Guschin A., et al. Evaluation and subsequent optimizations of the quantitative AmpliSens Florocenosis/Bacterial vaginosis-FRT multiplex real-time PCR assay for diagnosis of bacterial vaginosis // APMIS. 2016. Vol. 124. No. 12. P. 1099–1108. DOI: 10.1111/apm.12608

[51] Shalepo KV, Nazarova VV, Menukhova YN, et al. Assessment of current methods of laboratory diagnosis of bacterial vaginosis. Journal of Obstetrics and Women’s Diseases. 2014;63(1):26–32. (In Russ.) DOI: 10.17816/JOWD63126-32

[52] Шалепо К.В., Назарова В.В., Менухова Ю.Н., и др. Оценка современных методов лабораторной диагностики бактериального вагиноза // Журнал акушерства и женских болезней. 2014. Т. 63. № 1. C. 26–32. DOI: 10.17816/JOWD63126-32

[53] Savicheva AM. Modern ideas about the laboratory diagnosis of reproductively significant infections in women of reproductive age. Expert opinion. Issues of Practical Colposcopy Genital Infections. 2022;(3):34–39. (In Russ.) DOI: 10.46393/27826392_2022_3_34

[54] Савичева А.М. Современные представления о лабораторной диагностике репродуктивно значимых инфекций у женщин репродуктивного возраста. Мнение эксперта // Вопросы практической кольпоскопии. Генитальные инфекции. 2022. № 3. С. 34–39. DOI: 10.46393/27826392_2022_3_34

[55] Muzny CA, Kardas P. A narrative review of current challenges in the diagnosis and management of bacterial vaginosis. Sex Transm Dis. 2020;47(7):441–446. DOI: 10.1097/OLQ.0000000000001178

[56] Muzny C.A., Kardas P. A narrative review of current challenges in the diagnosis and management of bacterial vaginosis // Sex. Transm. Dis. 2020. Vol. 47. No. 7. P. 441–446. DOI: 10.1097/OLQ.0000000000001178

[57] Brocklehurst P, Gordon A, Heatley E, et al. Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst Rev. 2013;(1). DOI: 10.1002/14651858.CD000262.pub4

[58] Brocklehurst P., Gordon A., Heatley E., et al. Antibiotics for treating bacterial vaginosis in pregnancy // Cochrane Database Syst. Rev. 2013. No. 1. DOI: 10.1002/14651858.CD000262.pub4

[59] Bacterial Vaginosis. Sexually Transmitted Infections Treatment Guidelines, 2021 [cited 2023 Aug 21]. Available from: https://www.cdc.gov/std/treatment-guidelines/bv.htm

[60] Bacterial vaginosis. Sexually transmitted infections treatment guidelines, 2021 [дата обращения 21.08.2023]. Доступ по ссылке: https://www.cdc.gov/std/treatment-guidelines/bv.htm

[61] Siniakova AA, Shipitsyna EV, Budilovskaya OV, et al. The efficiency of treatment of vaginal infections in women with a history of miscarriage. Journal of Obstetrics and Women’s Diseases. 2019;68(5):63–74. (In Russ.) DOI: 10.17816/JOWD68563-74

[62] Синякова А.А., Шипицына Е.В., Будиловская О.В., и др. Оценка эффективности лечения вагинальных инфекций у пациенток с невынашиванием беременности в анамнезе // Журнал акушерства и женских болезней. 2019. Т. 68. № 5. C. 63–74. DOI: 10.17816/JOWD68563-74

[63] Karapetyan TE, Lomova NA, Yusubova VR, et al. Bacterial vaginosis in pregnancy: a current view on diagnosis and therapy (literature review). Gynecology. 2019;21(5):30–34. (In Russ.) DOI: 10.26442/20795696.2019.5.190667

[64] Карапетян Т.Э., Ломова Н.А., Юсубова В.Р., и др. Бактериальный вагиноз при беременности: современный взгляд на диагностику и терапию (обзор литературы) // Гинекология. 2019. Т. 21. № 5. C. 30–34. DOI: 10.26442/20795696.2019.5.190667

[65] Leitich H, Kiss H. Asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol. 2007;21(3):375–390. DOI: 10.1016/j.bpobgyn.2006.12.005

[66] Leitich H., Kiss H. Asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome // Best. Pract. Res. Clin. Obstet. Gynaecol. 2007. Vol. 21. No. 3. P. 375–390. DOI: 10.1016/j.bpobgyn.2006.12.005

[67] Ijeoma CC, Nyengidiki TK, Bassey G, et al. Oral Clindamycin and Metronidazole in the treatment of bacterial vaginosis in pregnant black women: comparison of efficacy and pregnancy outcome. Clinical Journal of Obstetrics and Gynecology. 2020. DOI: 10.29328/journal.cjog.1001040

[68] Ijeoma C.C., Nyengidiki T.K., Bassey G., et al. Oral clindamycin and metronidazole in the treatment of bacterial vaginosis in pregnant black women: comparison of efficacy and pregnancy outcome // Clin. J. Obstet. Gynecol. 2020. Vol. 6. No. 1. P. 001–006. DOI: 10.29328/journal.cjog.1001040

[69] Thulkar J, Kriplani A, Agarwal N. A comparative study of oral single dose of metronidazole, tinidazole, secnidazole and ornidazole in bacterial vaginosis. Indian J Pharmacol. 2012;44(2):243–245. DOI: 10.4103/0253-7613.93859

[70] Thulkar J., Kriplani A., Agarwal N. A comparative study of oral single dose of metronidazole, tinidazole, secnidazole and ornidazole in bacterial vaginosis // Indian J. Pharmacol. 2012. Vol. 44. No. 2. P. 243–245. DOI: 10.4103/0253-7613.93859

[71] Ajiji P, Uzunali A, Ripoche E, et al. Investigating the efficacy and safety of metronidazole during pregnancy; A systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol X. 2021;11. DOI: 10.1016/j.eurox.2021.100128

[72] Ajiji P., Uzunali A., Ripoche E., et al. Investigating the efficacy and safety of metronidazole during pregnancy; A systematic review and meta-analysis // Eur. J. Obstet. Gynecol. Reprod. Biol. X. 2021. Vol. 11. DOI: 10.1016/j.eurox.2021.100128

[73] Sherrard J, Wilson J, Donders G, et al. European (IUSTI/WHO) International Union against sexually transmitted infections (IUSTI) World Health Organisation (WHO) guideline on the management of vaginal discharge. Int J STD AIDS. 2018;29(13):1258–1272. DOI: 10.1177/0956462418785451.

[74] Sherrard J., Wilson J., Donders G., et al. European (IUSTI/WHO) International Union against sexually transmitted infections (IUSTI) World Health Organisation (WHO) guideline on the management of vaginal discharge // Int. J. STD AIDS. 2018. Vol. 29. No. 13. P. 1258–1272. DOI: 10.1177/0956462418785451

[75] Bradshaw CS, 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). DOI: 10.1371/journal.pone.0034540

[76] 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. Vol. 7. No. 4. DOI: 10.1371/journal.pone.0034540

[77] Lamont RF, Keelan JA, Larsson PG, et al. The treatment of bacterial vaginosis in pregnancy with clindamycin to reduce the risk of infection-related preterm birth: a response to the Danish Society of Obstetrics and Gynecology guideline group’s clinical recommendations. Acta Obstet Gynecol Scand. 2017;96(2):139–143. DOI: 10.1111/aogs.13065

[78] Lamont R.F., Keelan J.A., Larsson P.G., et al. The treatment of bacterial vaginosis in pregnancy with clindamycin to reduce the risk of infection-related preterm birth: a response to the Danish Society of Obstetrics and Gynecology guideline group’s clinical recommendations // Acta. Obstet. Gynecol. Scand. 2017. Vol. 96. No. 2. P. 139–143. DOI: 10.1111/aogs.13065

[79] Haahr T, Ersbøll AS, Karlsen MA, et al. Treatment of bacterial vaginosis in pregnancy in order to reduce the risk of spontaneous preterm delivery – a clinical recommendation. Acta Obstet Gynecol Scand. 2016;95(8):850–860. DOI: 10.1111/aogs.12933

[80] Haahr T., Ersbøll A.S., Karlsen M.A., et al. Treatment of bacterial vaginosis in pregnancy in order to reduce the risk of spontaneous preterm delivery – a clinical recommendation // Acta. Obstet. Gynecol. Scand. 2016. Vol. 95. No. 8. P. 850–860. DOI: 10.1111/aogs.12933

[81] Mendling W, Palmeira-de-Oliveira A, Biber S, et al. An update on the role of Atopobium vaginae in bacterial vaginosis: what to consider when choosing a treatment? A mini review. Arch Gynecol Obstet. 2019;300(1):1–6. DOI: 10.1007/s00404-019-05142-8

[82] Mendling W., Palmeira-de-Oliveira A., Biber S., et al. An update on the role of Atopobium vaginae in bacterial vaginosis: what to consider when choosing a treatment? A mini review // Arch. Gynecol. Obstet. 2019. Vol. 300. No. 1. P. 1–6. DOI: 10.1007/s00404-019-05142-8

[83] Bagnall P, Rizzolo D. Bacterial vaginosis: a practical review. JAAPA. 2017;30(12):15–21. DOI: 10.1097/01.JAA.0000526770.60197.fa

[84] Bagnall P., Rizzolo D. Bacterial vaginosis: a practical review // JAAPA. 2017. Vol. 30. No. 12. P. 15–21. DOI: 10.1097/01.JAA.0000526770.60197.fa

[85] Paladine HL, Desai UA. Vaginitis: diagnosis and treatment. Am Fam Physician. 2018;97(5):321–329.

[86] Paladine H.L., Desai U.A. Vaginitis: diagnosis and treatment // Am. Fam. Physician. 2018. Vol. 97. No. 5. P. 321–329.

[87] Savicheva AM, Shalepo KV, Nazarova VV, et al. Sravnitel’noe kontroliruemoe randomizirovannoe issledovanie otsenki effektivnosti dvukhetapnogo lecheniya bakterial’nogo vaginoza. Gynecology. 2013;15(5):12–15. (In Russ.)

[88] Савичева А.М., Шалепо К.В., Назарова В.В., и др. Сравнительное контролируемое рандомизированное исследование оценки эффективности двухэтапного лечения бактериального вагиноза // Гинекология. 2013. Т. 15. № 5. C. 12–15.

[89] Duckworth DH, Gulig PA. Bacteriophages: potential treatment for bacterial infections. BioDrugs. 2002;16(1):57–62. DOI: 10.2165/00063030-200216010-00006

[90] Duckworth D.H., Gulig P.A. Bacteriophages: potential treatment for bacterial infections // BioDrugs. 2002. Vol. 16. No. 1. P. 57–62. DOI: 10.2165/00063030-200216010-00006

[91] Swidsinski A, Mendling W, Loening-Baucke V, et al. An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. Am J Obstet Gynecol. 2008;198(1). DOI: 10.1016/j.ajog.2007.06.039.

[92] Swidsinski A., Mendling W., Loening-Baucke V., et al. An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole // Am. J. Obstet. Gynecol. 2008. Vol. 198. No. 1. DOI: 10.1016/j.ajog.2007.06.039

[93] Wang Z, He Y, Zheng Y. Probiotics for the treatment of bacterial vaginosis: a meta-analysis. Int J Environ Res Public Health. 2019;16(20). DOI: 10.3390/ijerph16203859

[94] Wang Z., He Y., Zheng Y. Probiotics for the treatment of bacterial vaginosis: a meta-analysis // Int. J. Environ. Res. Public. Health. 2019. Vol. 16. No. 20. DOI: 10.3390/ijerph16203859

[95] Chen R, Li R, Qing W, 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: 10.1186/s12978-022-01449-z

[96] Chen R., Li R., Qing W., et al. Probiotics are a good choice for the treatment of bacterial vaginosis: a meta-analysis of randomized controlled trial // Reprod. Health. 2022. Vol. 19. No. 1. P. 137. DOI: 10.1186/s12978-022-01449-z

[97] Chapman DK, Bartlett J, Powell J, et al. Bacterial vaginosis screening and treatment in pregnant women. J Midwifery Womens Health. 2016;61(5):628–631. DOI: 10.1111/jmwh.12475

[98] Chapman D.K., Bartlett J., Powell J., et al. Bacterial vaginosis screening and treatment in pregnant women // J. Midwifery Womens Health. 2016. Vol. 61. No. 5. P. 628–631. DOI: 10.1111/jmwh.12475

[99] Sousa LGV, Pereira SA, Cerca N. Fighting polymicrobial biofilms in bacterial vaginosis. Microb Biotechnol. 2023;16(7):1423–1437. DOI: 10.1111/1751-7915.14261

[100] Sousa L.G.V., Pereira S.A., Cerca N. Fighting polymicrobial biofilms in bacterial vaginosis // Microb. Biotechnol. 2023. Vol. 16. No. 7. P. 1423–1437. DOI: 10.1111/1751-7915.14261

RIGHTS & PERMISSIONS

Eсо-Vector