Compositional features of the gut microbiota in perimenopausal and postmenopausal women
Kurbanova P.F., Ermakova E.I., Priputnevich T.V.
Menopause is the final stage of a woman’s reproductive life characterized by the cessation of monthly menstrual periods due to a decline in ovarian activity. The average life expectancy of women today is estimated to be about three to four decades after menopause. The hormonal changes related to menopause can affect physical, emotional, mental and social well-being. This period is associated with an increased risk of metabolic disorders, such as insulin resistance and abdominal obesity, which in turn can lead to cardiovascular diseases. The gut microbiome changes with the onset of menopause and may impact women’s health indirectly. Estrogen deficiency leads to a decrease in the species diversity of the intestinal microbiome and loss of its sexual dimorphism. The gut microbiome of postmenopausal women becomes identical to the gut microbiome of men of the same age. The results of experimental studies have demonstrated that the use of hormone replacement therapy can positively affect the homeostasis of the gut microbiome and balance the processes associated with estrogen deficiency.
Conclusion: Hormone therapy prescribed to correct menopausal symptoms has been shown to have the potential to positively affect the homeostasis of the gut microbiota. However, the findings are mostly based on experimental work with a relatively small sample size. Therefore, it is necessary to conduct more large-scale studies aimed at examining the gut microbiome of peri- and postmenopausal women and its changes during hormone therapy.
Authors’ contributions: Kurbanova P.F. – collecting and processing the material, writing the text; Ermakova E.I.,
Priputnevich T.V. – editing the article.
Conflicts of interest: Authors declare lack of the possible conflicts of interest.
Funding: The study was carried out without sponsorship.
For citation: Kurbanova P.F., Ermakova E.I., Priputnevich T.V.
Compositional features of the gut microbiota in perimenopausal and postmenopausal women.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2024; (9): 56-61 (in Russian)
https://dx.doi.org/10.18565/aig.2024.194
Keywords
menopause
postmenopause
perimenopause
gut microbiome
sexual dimorphism of the gut microbiome
hormone replacement therapy
References
- Santoro N., Roeca C., Peters B.A., Neal-Perry G. The menopause transition: signs, symptoms, and management options. J. Clin. Endocrinol. Metab. 2021; 106(1): 1-15. https://dx.doi.org/10.1210/clinem/dgaa764
- Юренева С.В., Ермакова Е.И. Менопауза и климактерическое состояние у женщины. Акушерство и гинекология. 2018; 7: 32-8. [Yureneva S.V., Ermakova E.I. Menopause and menopausal status in a woman. Obstetrics and Gynecology. 2018; (7): 32-8. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.7.32-38.
- The NAMS 2017 Hormone Therapy Position Statement Advisory Panel. The 2017 hormone therapy position statement of the North American Menopause Society. Menopause. 2017; 24(7): 728-53. https://dx.doi.org/10.1097/GME.0000000000000921
- Baber R.J., Panay N., Fenton A.; IMS Writing Group. 2016 IMS Recommendations on women’s midlife health and menopause hormone therapy. Climacteric. 2016; 19(2): 109-50. https://dx.doi.org/10.3109/13697137.2015.1129166.
- Motlani V., Motlani G., Pamnani S., Sahu A., Acharya N. Endocrine changes in postmenopausal women: a comprehensive view. Cureus. 2023; 15(12): e51287. https://dx.doi.org/10.7759/cureus.51287.
- Marlatt K.L., Pitynski-Miller D.R., Gavin K.M., Moreau K.L., Melanson E.L., Santoro N. et al. Body composition and cardiometabolic health across the menopause transition. Obesity (Silver Spring). 2022; 30(1): 14-27. https://dx.doi.org/10.1002/oby.23289.
- Ambikairajah A., Walsh E., Tabatabaei-Jafari H., Cherbuin N. Fat mass changes during menopause: a metaanalysis. Am J Obstet Gynecol. 2019; 221(5): 393-409.e50. https://dx.doi.org/10.1016/j.ajog.2019.04.023.
- Kozakowski J., Gietka-Czernel M., Leszczyńska D., Majos A. Obesity in menopause - our negligence or an unfortunate inevitability? Prz. Menopauzalny. 2017; 16(2): 61-5. https://dx.doi.org/10.5114/pm.2017.68594.
- Paschou S.A., Athanasiadou K.I., Papanas N. Menopausal hormone therapy in women with type 2 diabetes mellitus: an updated review. Diabetes Ther. 2024; 15(4): 741-8. https://dx.doi.org/10.1007/s13300-024-01546-1.
- Рекомендации экспертов Всероссийского научного общества кардиологов по диагностике и лечению метаболического синдрома. Второй пересмотр. Практическая медицина. 2010; 5(44): 81-101. [Recommendations of experts of Russian Scientific Society of Cardiologists on diagnosis and treatment of metabolic syndrome. Second Revision. Practical Medicine. 2010; 5(44): 81-101. (in Russian)].
- Schreurs M.P.H., de Vos van Steenwijk P.J., Romano A., Dieleman S., Werner H.M.J. How the gut microbiome links to menopause and obesity, with possible implications for endometrial cancer development. J. Clin. Med. 2021; 10(13): 2916. https://dx.doi.org/10.3390/jcm10132916.
- Cani P.D. Human gut microbiome: hopes, threats and promises. Gut. 2018; 67(9): 1716-25. https://dx.doi.org/10.1136/gutjnl-2018-316723.
- Asadi A., Shadab Mehr N., Mohamadi M.H., Shokri F., Heidary M., Sadeghifard N. et al. Obesity and gut–microbiota–brain axis: A narrative review. J. Clin. Lab. Anal. 2022; 36(5): e24420. https://dx.doi.org/10.1002/jcla.24420.
- Fan Y., Pedersen O. Gut microbiota in human metabolic health and disease. Nat. Rev. Microbiol. 2021; 19(1): 55-71. https://dx.doi.org/10.1038/s41579-020-0433-9.
- Osadchiy V., Martin C.R., Mayer E.A. The gut–brain axis and the microbiome: mechanisms and clinical implications. Clin. Gastroenterol. Hepatol. 2019; 17(2): 322-32. https://dx.doi.org/10.1016/j.cgh.2018.10.002.
- Witkowski M., Weeks T.L., Hazen S.L. Gut microbiota and cardiovascular disease. Circ. Res. 2020; 127(4): 553-70. https://dx.doi.org/10.1161/CIRCRESAHA.120.316242.
- Табеева Г.И., Думановская М.Р., Чернуха Г.Е., Припутневич Т.В. Современные представления о микробиоте в гинекологии. Акушерство и гинекология. 2020; 2: 38-44. [Tabeeva G.I., Dumanovskaya M.R., Chernukha G.E., Priputnevich T.V. Current views on microbiota in gynecology. Obstetrics and Gynecology. 2020; (2): 38-44. (in Russian)]. https://dx.doi.org/10.18565/aig.2020.2.38-44.
- Чернуха Г.Е., Мирошина Е.Д., Припутневич Т.В. Синдром поликистозных яичников и микробиота кишечника. Акушерство и гинекология. 2021; 3: 36-43. [Chernukha G.E., Miroshina E.D., Priputnevich T.V. Polycystic ovary syndrome and gut microbiota. Obstetrics and Gynecology. 2021; (3): 36-43. (in Russian)]. https://dx.doi.org/10.18565/aig.2021.3.36-43.
- Alemany M. The roles of androgens in humans: biology, metabolic regulation and health. Int. J. Mol. Sci. 2022; 23(19): 11952. https://dx.doi.org/10.3390/ijms231911952.
- Yoon K., Kim N. Roles of sex hormones and gender in the gut microbiota. J. Neurogastroenterol. Motil. 2021; 27(3): 314-25. https://dx.doi.org/10.5056/jnm20208.
- Peters B.A., Santoro N., Kaplan R.C., Qi Q. Spotlight on the gut microbiome in menopause: current insights. Int. J. Womens Health. 2022; 14: 1059-72. https://dx.doi.org/10.2147/IJWH.S340491.
- Ervin S.M., Li H., Lim L., Roberts L.R., Liang X., Mani S. et al. Gut microbial β-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens. J. Biol. Chem. 2019; 294(49): 18586-99. https://dx.doi.org/10.1074/jbc.RA119.010950.
- Siddiqui R., Makhlouf Z., Alharbi A.M., Alfahemi H., Khan N.A. The gut microbiome and female health. Biology (Basel). 2022; 11(11): 1683. https://dx.doi.org/10.3390/biology11111683.
- Mayneris-Perxachs J., Arnoriaga-Rodríguez M., Luque-Córdoba D., Priego-Capote F., Pérez-Brocal V., Moya A. et al. Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status. Microbiome. 2020; 8(1): 136. https://dx.doi.org/10.1186/s40168-020-00913-x.
- Santos-Marcos J.A., Rangel-Zuñiga O.A., Jimenez-Lucena R., Quintana-Navarro G.M., Garcia-Carpintero S., Malagon M.M. et al. Influence of gender and menopausal status on gut microbiota. Maturitas. 2018; 116: 43-53. https://dx.doi.org/10.1016/j.maturitas.2018.07.008.
- Peters B.A., Lin J., Qi Q., Usyk M., Isasi C.R., Mossavar-Rahmani Y. et al. Menopause is associated with an altered gut microbiome and estrobolome, with implications for adverse cardiometabolic risk in the Hispanic Community Health Study/Study of Latinos. mSystems. 2022; 7(3): e0027322. https://dx.doi.org/10.1128/msystems.00273-22.
- Zhao H., Chen J., Li X., Sun Q., Qin P., Wang Q. Compositional and functional features of the female premenopausal and postmenopausal gut microbiota. FEBS Lett. 2019; 593(18): 2655-64. https://dx.doi.org/10.1002/1873-3468.13527.
- Kaliannan K., Robertson R.C., Murphy K., Stanton C., Kang C., Wang B. et al. Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice. Microbiome. 2018; 6(1): 205. https://dx.doi.org/10.1186/s40168-018-0587-0.
- Meng Q., Ma M., Zhang W., Bi Y., Cheng P., Yu X. et al. The gut microbiota during the progression of atherosclerosis in the perimenopausal period shows specific compositional changes and significant correlations with circulating lipid metabolites. Gut Microbes. 2021; 13(1): 1-27. https://dx.doi.org/10.1080/19490976.2021.1880220.
- Dempsey E., Corr S.C. Lactobacillus spp. for gastrointestinal health: current and future perspectives. Front. Immunol. 2022; 13: 840245. https://dx.doi.org/10.3389/fimmu.2022.840245.
- Iljazovic A., Roy U., Gálvez E.J.C., Lesker T.R., Zhao B., Gronow A. et al. Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation. Mucosal. Immunol. 2021; 14(1): 113-124. https://dx.doi.org/10.1038/s41385-020-0296-4.
- Leite G., Barlow G.M., Parodi G., Pimentel M.L., Chang C., Hosseini A. et al. Duodenal microbiome changes in postmenopausal women: effects of hormone therapy and implications for cardiovascular risk. Menopause. 2022; 29(3):264-75. https://dx.doi.org/10.1097/GME.0000000000001917.
- Dothard M.I., Allard S.M., Gilbert J.A. The effects of hormone replacement therapy on the microbiomes of postmenopausal women. Climacteric. 2023; 26(3): 182-92. https://dx.doi.org/10.1080/13697137.2023.2173568.
- Huang J., Shan W., Li F., Wang Z., Cheng J., Lu F. et al. Fecal microbiota transplantation mitigates vaginal atrophy in ovariectomized mice. Aging (Albany NY). 2021; 13(5): 7589-607. https://dx.doi.org/10.18632/aging.202627.
Received 05.08.2024
Accepted 16.09.2024
About the Authors
Parvin F. Kurbanova, PhD student at the Department of Gynecological Endocrinology, Academician V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia,117997, Russia, Moscow, Academician Oparin str., 4, par0502@yandex.ru, https://orcid.org/0000-0002-2225-8067
Elena I. Ermakova, PhD, Senior Researcher at the Department of Gynecological Endocrinology, Academician V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia, 117997, Russia, Moscow, Academician Oparin str., 4, ermakova.health@mail.ru, https://orcid.org/0000-0002-6629-051X
Tatiana V. Priputnevich, Corresponding Member of the Russian Academy of Sciences, Dr. Med. Sci., Associate Professor, Head of the Institute of Microbiology,
Antimicrobial Therapy and Epidemiology, Academician V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia, 117997, Russia, Moscow, Academician Oparin str., 4, t_priputnevich@oparina4.ru, https://orcid.org/0000-0002-4126-9730
Similar Articles
