The impact of the oral microbiome on women’s reproductive health
https://doi.org/10.18699/SSMJ20250402
Abstract
In this review, based on the analysis of specialized domestic and foreign literature allocated in the electronic libraries eLibrary and CyberLeninka, the database of medical and biological publications PubMed, a theoretical justification is presented for the problem of women’s reproductive health associated with species-specific transformation of the oral microbiome and changes in its taxonomic profile. Data on previously studied predictors affecting women’s reproductive function do not raise discussions. However, the role of the oral microbiome in the pathogenesis of reproductive dysfunction has not been fully studied. It is known that the oral microbiome consists of more than 700 species of bacteria, and its diversity can change under the influence of various factors, such as age, hormonal changes, diet and general health. These changes can have a significant impact on the overall physical condition of a woman and her somatic health. It has been proven that during pregnancy, an increase in the number of viable microorganisms is observed, which can have both positive and negative effects on the health of the mother and fetus. At the same time, imbalances in the oral microbiome can increase the risk of developing various dental diseases (gingivitis, periodontitis), as well as systemic diseases, which in turn can have a negative impact on reproductive health. Therefore, further study of the relationship between the oral microbiome and women’s reproductive function opens up new opportunities for its implementation and prediction of outcomes.
About the Authors
S. I. GazhvaRussian Federation
Svetlana I. Gazhva, doctor of medical sciences, professor
603005, Nizhny Novgorod, Mininа i Pozharskogo sq., 10/1
A. N. Sulima
Russian Federation
Anna N. Sulima, doctor of medical sciences, professor
295051, Simferopol, Lenina blvd., 5/7
V. A. Kucher
Russian Federation
Valeriya A. Kucher, candidate of medical sciences
603005, Nizhny Novgorod, Mininа i Pozharskogo sq., 10/1
References
1. Aggarwal N., Kitano S., Puah G.R.Y., Kittelmann S., Hwang I.Y., Chang M.W. Microbiome and human health: current understanding, engineering, and enabling technologies. Chem. Rev. 2023;123(1):31–72. doi: 10.1021/acs.chemrev.2c00431
2. Stepanova T.Yu., Timofeeva A.V. Oral human microbiome. Sovremennye problemy nauki i obrazovaniya = Modern Problems of Science and Education. 2016;(5):308–308. [In Russian].
3. Human Oral Microbiome Database. Available at: https://www.homd.org
4. Karakhalis L.Yu., Ivantsiv N.S., Li N.V. Periodontal diseases and adverse pregnancy outcomes. Doktor. Ru = Doctor.Ru. 2021;20(1):21–25. [In Russian]. doi: 10.31550/1727-2378-2021-20-1-21-25
5. Usova A.V., Mukhamedshina V.R., Usova A.V., Sokolov V.S., Kucherenko S.G. Influence of dental health on pregnancy outcomes: the role of periodontal disease in preterm labour. Mezhdunarodnyy nauchno-issledovatel’skiy zhurnal = International Research Journal. 2024;(11):46. [In Russian]. doi: 10.60797/IRJ.2024.149.24
6. Pobozh’eva L.V., Kopeckiy I.S. Role of biofilm in pathogenesis of inflammatory oral diseases and methods of it elimination. Lechebnoye delo = Medical Care. 2012;( 2):9–13. [In Russian].
7. Wade W.G. The oral microbiome in health and disease. Pharmacol. Res. 2013;69(1):137–143. doi: 10.1016/j.phrs.2012.11.006
8. Genco R.J., Grossi S.G., Ho A., Nishimura F., Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J. Periodontol. 2005;76(11 Suppl):2075–2084. doi: 10.1902/jop.2005.76.11-S.2075
9. Freestone P.P. Communication between bacteria and their hosts. Scientifica (Cairo). 2013;2013:361073. doi: 10.1155/2013/361073
10. Freestone P.P., Sandrini S.M., Haigh R.D., Lyte M. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol. 2008;16(2):55–64. doi: 10.1016/j.tim.2007.11.005
11. Lyte M. Microbial endocrinology. Host-microbiota neuroendocrine interactions influencing brain and behavior. Gut. Microbes. 2014;5(3):381–389. doi: 10.4161/gmic.28682
12. Lyte M. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog. 2013;9(11):1–3. doi: 10.1371/journal.ppat.1003726
13. Usenko D.V. Antibiotic-induced changes in the microbiome of the gastrointestinal tract and their correction. Russkiy meditsinskiy zhurnal = Russian Medical Journal. 2018; 26(2-2):96–99. [In Russian].
14. Nemtsveridze Ja.Je., Derbina L.R., Voronina N.A., Derbin K.D. The effect of antibiotics used in the treatment of urological infectious diseases on the state of the oral microbiome. Vestnik meditsinskogo instituta “REAVIZ”: reabilitatsiya, vrach i zdorov’ye = Bulletin of the Medical Institute “REAVIZ”: Rehabilitation, Physician and Health. 2022;(2):338–339. [In Russian].
15. Scannapieco F.A. Role of oral bacteria in respiratory infection. J. Periodontol. 1999;70(7):793–802. doi: 10.1902/jop.1999.70.7.793
16. Seymour G.J., Ford P.J., Cullinan M.P., Leishman S., Yamazaki K. Relationship between periodontal infections and systemic disease. Clin. Microbiol. Infect. 2007;13(Suppl 4):3–10. doi: 10.1111/j.1469-0691.2007.01798.x
17. Katola V.M., Komogortseva V.E. The role of the oral microbiome in the development of inflammation and somatic pathology. Byulleten’ fiziologii i patologii dykhaniya = Bulletin of Physiology and Pathology of Respiration. 2018;(68):117–121. [In Russian]. doi: 10.12737/article_5b1a069e8a9318.69578013
18. Salimov O.R., Rikhsieva D.U. Changes in the microflora of the oral cavity in women during lactation. Integrative Dentistry and Maxillofacial Surgery. 2022;1(2):210–213. [In Russian]. doi: 10.57231/j.idmfs.2022.1.2.034
19. Thomas C., Minty M., Vinel A., Canceill T., Loubières P., Burcelin R., Kaddech M., Blasco-Baque V., Laurencin-Dalicieux S. Oral microbiota: a major player in the diagnosis of systemic diseases. Diagnostics (Basel). 2021;11(8):1376. doi: 10.3390/diagnostics11081376
20. Gazhva S.I., Ibragimova Yu.Sh., Gazhva Yu.V., Ryabova V.M., Teterin A.I., Yakovlev D.N., Kalinkin K.I., Krasnokutskaya N.S. Technologies for early diagnosis of oral mucosal diseases. Stomatologiya = Stomatology. 2021;100(6-2):37–42. [In Russian]. doi: 10.17116/stomat202110006237
21. Razumova S.N., Moroz A.F. Microflora of oral cavity in women with normal and complicated pregnancy. Vestnik Rossiyskogo universiteta druzhby narodov. Seriya: Meditsina = RUDN Journal of Medicine. 2002;(1):73–78. [In Russian].
22. Neuman H., Koren O. The pregnancy microbiome. Nestle Nutr. Inst. Workshop Ser. 2017;88:1–9. doi: 10.1159/000455207
23. Saadaoui M., Singh P., Al Khodor S. Oral microbiome and pregnancy: A bidirectional relationship. J. Reprod. Immunol. 2021;145:103293. doi: 10.1016/j.jri.2021.103293
24. Gazhva S.I., Ibragimova Yu.Sh., Solovieva I.V., Ryabova V.M., Belova I.V., Tochilina A.G., Aivazyan V.V., Knyashchuk E.A. Comprehensive rehabilitation of patients with chronic generalized periodontitis associated with comorbid pathology. Mezhdunarodnyy nauchno-issledovatel’skiy zhurnal = International Research Journal. 2023;(5):41. [In Russian]. doi: 10.23670/IRJ.2023.131.54
25. Biagi E., Candela M., Turroni S., Garagnani P., Franceschi C., Brigidi P. Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol. Res. 2013;69(1):11–20. doi: 10.1016/j.phrs.2012.10.005
26. Nuriel-Ohayon M., Neuman H., Koren O. Microbial changes during pregnancy, birth, and infancy. Front. Microbiol. 2016;7:1031. doi: 10.3389/fmicb.2016.01031
27. Gabidullina R.I., Bagirli R.R., Sharapova A.M., Galimyanova E.I. Effects of combined oral contraceptives on vaginal microbiota. Prakticheskaya meditsina = Practical Medicine. 2018;(6):106–110. [In Russian]. doi: 10.32000/2072-1757-2018-16-6-106-110
28. Yamazaki A., Ogura K., Minami K., Ogai K., Horiguchi T., Okamoto S., Mukai K. Oral microbiome changes associated with the menstrual cycle in healthy young adult females. Front. Cell. Infect. Microbiol. 2023;13:1119602. doi: 10.3389/fcimb.2023.1119602
29. Balan U., Gonsalves N., Jose M., Girish K.L. Symptomatic changes of oral mucosa during normal hormonal turnover in healthy young menstruating female. J. Contemp. Dent. Pract. 2012;13(2):178–181. doi: 10.5005/jp-journals-10024-1117
30. Baser U., Cekici A., Tanrikulu-Kucuk S., Kantarci A., Ademoglu E., Yalcin F. Gingival inflammation and interleukin-1 beta and tumor necrosis factor-alpha levels in gingival crevicular fluid during the menstrual cycle. J. Periodontol. 2009;80(12):1983–1990. doi: 10.1902/jop.2009.090076
31. Khosravisamani M., Maliji G., Seyfi S., Azadmehr A., Abd Nikfarjam B., Madadi S., Jafari S. Effect of the menstrual cycle on inflammatory cytokines in the periodontium. J. Periodontal. Res. 2014;49(6):770– 776. doi: 10.1111/jre.12161
32. Machtei E.E., Mahler D., Sanduri H., Peled M. The effect of menstrual cycle on periodontal health. J. Periodontol. 2004;75(3):408–412. doi: 10.1902/jop.2004.75.3.408
33. Fujiwara N., Tsuruda K., Iwamoto Y., Kato F., Odaki T., Yamane N., Hori Y., Harashima Y., Sakoda A., Tagaya A., … Noguchi M. Significant increase of oral bacteria in the early pregnancy period in Japanese women. J. Invest. Clin. Dent. 2017;8(1):e12189. doi: 10.1111/jicd.12189
34. Balan P., Chong Y.S., Umashankar S., Swarup S., Loke W.M., Lopez V., He H.G., Seneviratne C.J. Keystone species in pregnancy gingivitis: a snapshot of oral microbiome during pregnancy and postpartum Period. Front. Microbiol. 2018;9:2360. doi: 10.3389/fmicb.2018.02360
35. Lin W., Jiang W., Hu X., Gao L., Ai D., Pan H., Niu C., Yuan K., Zhou X., Xu C., Huang Z. Ecological shifts of supragingival microbiota in association with pregnancy. Front. Cell. Infect. Microbiol. 2018;8:24. doi: 10.3389/fcimb.2018.00024
36. Massoni R.S.S., Aranha A.M.F., Matos F.Z., Guedes O.A., Borges Á.H., Miotto M., Porto A.N. Correlation of periodontal and microbiological evaluations, with serum levels of estradiol and progesterone, during different trimesters of gestation. Sci. Rep. 2019;9(1):11762. doi: 10.1038/s41598-019-48288-w
37. Muramatsu Y., Takaesu Y. Oral health status related to subgingival bacterial flora and sex hormones in saliva during pregnancy. Bull. Tokyo Dent. Coll. 1994;35(3):139–151.
38. Dubrovskaya M.V., Eremin O.V., Savina E.A., Ivashchenko Yu.Yu., Minasyan A.M. Risk factors in the formation of periodontal diseases in pregnant women. Saratovskiy nauchno-meditsinskiy zhurnal = Saratov Journal of Medical Scientific Research. 2013;9(3):383– 386. [In Russian].
39. Yokoyama M., Hinode D., Yoshioka M., Fukui M., Tanabe S., Grenier D., Ito H.O. Relationship between Campylobacter rectus and periodontal status during pregnancy. Oral Microbiol. Immunol. 2008;23(1):55– 59. doi: 10.1111/j.1399-302X.2007.00391.x
40. Aliev T.Ya., Zeynalov G.A. Features of microbiological contamination of the oral cavity during physiological and pathological pregnancy. Meditsinskie novosti = Medical News. 2019;(8):63–64. [In Russian].
41. Order of the Ministry of Health of Russia dated 10.20.2020 No 1130n “On approval of the Procedure for the provision of medical care in the profile of “obstetrics and gynecology””. Available at: https://base.garant.ru/74840123/ [In Russian].
42. Russian Society of Obstetricians and Gynecologists. Clinical guidelines “Normal pregnancy”. Available at: clck.ru/3MG7TR [In Russian].
43. Kravtsova E.I., Kutsenko I.I., Borovikov I.O., Batmen S.K. Nutrition and nutritional support during pregnancy. Russkiy meditsinskiy zhurnal. Mat’ i ditya = Russian Medical Journal. Mother and Child. 2020;3(4):233–241. [In Russian]. doi: 10.32364/2618-8430-2020-3-4-233-241
44. Maltseva L.I., Vasilyeva E.N., Denisova T.G., Gerasimova L.I. Provision with vitamin D and correction of its deficit during pregnancy. Prakticheskaya meditsina = Practical Medicine. 2017;(5):18–21. [In Russian].
45. Tabeeva G.I., Dumanovskaya M.R., Chernukha G.E., Priputnevich T.V. Current views on microbiota in gynecology. Akusherstvo i ginekologiya = Obstetrics and Gynecology. 2020;(2):38–44. [In Russian]. doi: 10.18565/aig.2020.2.38-44
46. Pashkova G.S. The influence of the oral microbiome on the course of pregnancy. Possibilities of gentle correction of dysbiosis. Status Praesens. Ginekologiya, akusherstvo, besplodnyj brak = Status Praesens. Gynecology, obstetrics, infertile marriage. 2018;(1):59–63. [In Russian].
47. Erchick D.J., Khatry S.K., Agrawal N.K., Katz J., LeClerq S.C., Rai B., Reynolds M.A., Mullany L.C. Risk of preterm birth associated with maternal gingival inflammation and oral hygiene behaviours in rural Nepal: a community-based, prospective cohort study. BMJ Open. 2020;10(8):e036515. doi: 10.1136/bmjopen-2019-036515
48. Sulima A.N., Bulyuk V.V., Mitrofanova O.A. Postmenopausal osteoporosis. Akusherstvo i ginekologiya = Obstetrics and Gynecology. 2023;(9):52–59. [In Russian]. doi: 10.18565/aig.2023.103