Current understanding of the connection between endometriosis and intestinal microbiocenosis: a literature review

Marina S. Shelekhova , Anna N. Modorskaya , Angelina N. Fil'chakova , Yuliya V. Grudkova , Kirill P. Rayevskiy

Russian Medicine ›› 2024, Vol. 30 ›› Issue (2) : 181 -190.

PDF
Russian Medicine ›› 2024, Vol. 30 ›› Issue (2) : 181 -190. DOI: 10.17816/medjrf626841
Reviews
review-article

Current understanding of the connection between endometriosis and intestinal microbiocenosis: a literature review

Author information +
History +
PDF

Abstract

Endometriosis is a complex condition that affects at least 10% of women in their reproductive years worldwide. It is characterized by persistent pelvic pain, dysmenorrhea, impaired pelvic organ function, infertility, and psychological distress. Alarmingly, about 30% of patients experience a recurrence of the disease even after receiving full treatment. Given the urgent nature of this problem, extensive studies are regularly conducted to investigate the various factors that contribute to the development of endometriosis. One area of particular interest is the relationship between the condition and changes in the intestinal microflora.

Research suggests that endometriosis is primarily associated with a decrease in the number of Lactobacillus bacteria and an increase in the presence of potentially harmful flora, including Enterobacteriaceae, Bifidobacterium, Parabacteroides, Proteobacteria, Actinobacteria, Cyanobacteria, Saccharibacteria, Fusobacteria etc. Furthermore, there is a focus on the ratio of Firmicutes to Bacteroidetes. Such dysbiosis leads to abnormal cytokine expression and immune cell dysfunction, ultimately resulting in chronic inflammation. A correlation has been found between changes in the intestinal microflora in endometriosis and an increase in the levels of TNF-α, NF-κB, and IL-8. Additionally, the condition has been linked to factors related to apoptosis (Fas and Bax), proliferation (epidermal growth factor), and angiogenesis (VEGF).

Another significant aspect is the role of the intestinal microbiota in the breakdown of estrogen. Enzymes such as β-glucuronidase and β-glucosidase, secreted by the microbiota, contribute to the breakdown of estrogen and subsequently increase the levels of free estrogen in the bloodstream. This increase in free estrogen is believed to play a role in the development of endometriosis by promoting the proliferative activity of endometrial cells. It further confirms the significance of intestinal dysbiosis in the pathogenesis of the disease.

However, despite these findings, additional research is still required to fully understand the mechanisms behind the development of endometriosis.

Keywords

endometriosis / gut microbiota / disbiosis / microflora / inflammation / endometrium

Cite this article

Download citation ▾
Marina S. Shelekhova, Anna N. Modorskaya, Angelina N. Fil'chakova, Yuliya V. Grudkova, Kirill P. Rayevskiy. Current understanding of the connection between endometriosis and intestinal microbiocenosis: a literature review. Russian Medicine, 2024, 30(2): 181-190 DOI:10.17816/medjrf626841

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Mason BR, Chatterjee D, Menias CO, et al. Encyclopedia of endometriosis: a pictorial rad-path review. Abdom Radiol (NY). 2020;45(6):1587–1607. doi: 10.1007/s00261-019-02381-w

[2]

Mason B.R., Chatterjee D., Menias C.O., et al. Encyclopedia of endometriosis: a pictorial rad-path review // Abdom Radiol (NY). 2020. Vol. 45, N 6. P. 1587–1607. doi: 10.1007/s00261-019-02381-w

[3]

Zondervan KT, Becker CM, Missmer SA. Endometriosis. N Engl J Med. 2020;382(13):1244–1256. doi: 10.1056/NEJMra1810764

[4]

Zondervan K.T., Becker C.M., Missmer S.A. Endometriosis // N Engl J Med. 2020. Vol. 382, N 13. P. 1244–1256. doi: 10.1056/NEJMra1810764

[5]

Taylor HS, Kotlyar AM, Flores VA. Endometriosis is a chronic systemic disease: clinical challenges and novel innovations. Lancet. 2021;397(10276):839–852. doi: 10.1016/S0140-6736(21)00389-5

[6]

Taylor H.S., Kotlyar A.M., Flores V.A. Endometriosis is a chronic systemic disease: clinical challenges and novel innovations // Lancet. 2021. Vol. 397, N 10276. P. 839–852. doi: 10.1016/S0140-6736(21)00389-5

[7]

Arion K, Orr NL, Noga H, et al. A quantitative analysis of sleep quality in women with endometriosis. J Womens Health (Larchmt). 2020;29(9):1209–1215. doi: 10.1089/jwh.2019.8008

[8]

Arion K., Orr N.L., Noga H., et al. A quantitative analysis of sleep quality in women with endometriosis // J Womens Health (Larchmt). 2020. Vol. 29, N 9. P. 1209–1215. doi: 10.1089/jwh.2019.8008

[9]

Della Corte L, Di Filippo C, Gabrielli O, et al. The burden of endometriosis on women’s lifespan: a narrative overview on quality of life and psychosocial wellbeing. Int J Environ Res Public Health. 2020;17(13):4683. doi: 10.3390/ijerph17134683

[10]

Della Corte L., Di Filippo C., Gabrielli O., et al. The burden of endometriosis on women’s lifespan: a narrative overview on quality of life and psychosocial wellbeing // Int J Environ Res Public Health. 2020. Vol. 17, N 13. P. 4683. doi: 10.3390/ijerph17134683

[11]

Velho RV, Taube E, Sehouli J, Mechsner S. Neurogenic inflammation in the context of endometriosis-what do we know? Int J Mol Sci. 2021;22(23):13102. doi: 10.3390/ijms222313102

[12]

Velho R.V., Taube E., Sehouli J., Mechsner S. Neurogenic inflammation in the context of endometriosis-what do we know? // Int J Mol Sci. 2021. Vol. 22, N 23. P. 13102. doi: 10.3390/ijms222313102

[13]

Vannuccini S, Clemenza S, Rossi M, Petraglia F. Hormonal treatments for endometriosis: the endocrine background. Rev Endocr Metab Disord. 2022;23(3):333–355. doi: 10.1007/s11154-021-09666-w

[14]

Vannuccini S., Clemenza S., Rossi M., Petraglia F. Hormonal treatments for endometriosis: the endocrine background // Rev Endocr Metab Disord. 2022. Vol. 23, N 3. P. 333–355. doi: 10.1007/s11154-021-09666-w

[15]

Smolarz B, Szyłło K, Romanowicz H. Endometriosis: epidemiology, classification, pathogenesis, treatment and genetics (review of literature). Int J Mol Sci. 2021;22(19):10554. doi: 10.3390/ijms221910554

[16]

Smolarz B., Szyłło K., Romanowicz H. Endometriosis: epidemiology, classification, pathogenesis, treatment and genetics (review of literature) // Int J Mol Sci. 2021. Vol. 22, N 19. P. 10554. doi: 10.3390/ijms221910554

[17]

Dzhaynakbayev NT, Orakbay LZh, Imanbayeva ZhA, Bakayeva AZ. Epidemiological aspects of endometriosis at the present stage (literature review). Vestnik Kazahskogo nacional’nogo medicinskogo universiteta. 2020;(4):3–8. EDN: NJGWBO

[18]

Джайнакбаев Н.Т., Оракбай Л.Ж., Иманбаева Ж.А., Бакаева А.Ж. Эпидемиологические аспекты эндометриоза на современном этапе (обзор литературы) // Вестник Казахского национального медицинского университета. 2020. № 4. С. 3–8. EDN: NJGWBO

[19]

Chadchan SB, Naik SK, Popli P, et al. Gut microbiota and microbiota-derived metabolites promotes endometriosis. Cell Death Discov. 2023;9(1):28. doi: 10.1038/s41420-023-01309-0

[20]

Chadchan S.B., Naik S.K., Popli P., et al. Gut microbiota and microbiota-derived metabolites promotes endometriosis // Cell Death Discov. 2023. Vol. 9, N 1. P. 28. doi: 10.1038/s41420-023-01309-0

[21]

Ni Z, Ding J, Zhao Q, et al. Alpha-linolenic acid regulates the gut microbiota and the inflammatory environment in a mouse model of endometriosis. Am J Reprod Immunol. 2021;86(4):e13471. doi: 10.1111/aji.13471

[22]

Ni Z., Ding J., Zhao Q., et al. Alpha-linolenic acid regulates the gut microbiota and the inflammatory environment in a mouse model of endometriosis // Am J Reprod Immunol. 2021. Vol. 86, N 4. P. e13471. doi: 10.1111/aji.13471

[23]

Aliyeva FT, Bryunin DV, Aliyeva FT. Features of clinical manifestations after surgical interventions in patients with recurrent external genital endometriosis. Meditsinskie novosti. 2021;(12): 81–83. EDN: IKIWRM

[24]

Алиева Ф.Т., Брюнин Д.В., Алиева Ф.Т. Особенности клинических проявлений после перенесенных оперативных вмешательств при рецидивирующем наружном генитальном эндометриозе // Медицинские новости. 2021. № 12. С. 81–83. EDN: IKIWRM

[25]

Gumenyuk LN, Zemlyanaya IA, Rami A, et al. Gut microbiota alterations and their association with IL6, IL8 and TNFα levels in patients with external genital endometriosis. Bulletin of RSMU. 2023;(3):10–16. doi: 10.24075/vrgmu.2023.018

[26]

Гуменюк Л.Н., Земляная И.А., Рами А., и др. Изменения микробиоты кишечника и их связь с показателями IL6, IL8 и TNFα у пациенток с наружным генитальным эндометриозом // Вестник РГМУ. 2023. № 3. С. 10–16. doi: 10.24075/vrgmu.2023.018

[27]

Pontes CFR, Chamié LP, de Aguiar M, et al. Deep endometriosis: clinical and epidemiological findings of diagnosed women according to the criteria of the International Deep Endometriosis Analysis (IDEA) group. J Hum Growth Dev. 2022;32(2):223–231. doi: 10.36311/jhgd.v32.13312

[28]

Pontes C.F.R., Chamié L.P., de Aguiar M., et al. Deep endometriosis: clinical and epidemiological findings of diagnosed women according to the criteria of the International Deep Endometriosis Analysis (IDEA) group // J Hum Growth Dev. 2022. Vol. 32, N 2. P. 223–231. doi: 10.36311/jhgd.v32.13312

[29]

Artymuk NV, Zotova OA, Vaulina EN. Endometriomas: the effectiveness of combination treatment. Gynecology. 2021;23(6): 536–541. EDN: FCKQLA doi: 10.26442/20795696.2021.6.201173

[30]

Артымук Н.В., Зотова О.А., Ваулина Е.Н. Эндометриомы: эффективность комбинированного лечения // Гинекология. 2021. T. 23, № 6. С. 536–541. EDN: FCKQLA doi: 10.26442/20795696.2021.6.201173

[31]

Li Y, Wang K, Ding J, et al. Influence of the gut microbiota on endometriosis: potential role of chenodeoxycholic acid and its derivatives. Front Pharmacol. 2022;13:954684. doi: 10.3389/fphar.2022.954684

[32]

Li Y., Wang K., Ding J., et al. Influence of the gut microbiota on endometriosis: potential role of chenodeoxycholic acid and its derivatives // Front Pharmacol. 2022. Vol. 13. P. 954684. doi: 10.3389/fphar.2022.954684

[33]

Kupina AD, Petrov YuA, Ozdoeva IM. Enteric and vaginal microbiocenosis and implications for female reproductive health. Doctor.Ru. 2021;20(1):73–77. EDN: NUSAFQ doi: 10.31550/1727-2378-2021-20-1-73-77

[34]

Купина А.Д., Петров Ю.А., Оздоева И.М. Кишечный и влагалищный микробиоценоз и его влияние на репродуктивное здоровье женщины // Доктор.Ру. 2021. T. 20, № 1. С. 73–77. EDN: NUSAFQ doi: 10.31550/1727-2378-2021-20-1-73-77

[35]

Svensson A, Brunkwall L, Roth B, et al. Associations between endometriosis and gut microbiota. Reprod Sci. 2021;28(8):2367–2377. doi: 10.1007/s43032-021-00506-5

[36]

Svensson A., Brunkwall L., Roth B., et al. Associations between endometriosis and gut microbiota // Reprod Sci. 2021. Vol. 28, N 8. P. 2367–2377. doi: 10.1007/s43032-021-00506-5

[37]

Kotiv KhB, Gorodnova TV, Lavrinovich OE, Berlev IV. Malignant endometriosis-associated ovarian and extraovarian neoplasia (review of literature). Tumors of Female Reproductive System. 2022;18(4):127–137. EDN: SZXSKI doi: 10.17650/1994-4098-2022-18-4-127-137

[38]

Котив Х.Б., Городнова Т.В., Лавринович О.Е., Берлев И.В. Малигнизированные эндометриозассоциированные овариальные и экстраовариальные неоплазии: обзор литературы // Опухоли женской репродуктивной системы. 2022. Т. 18, № 4. С. 127–137. EDN: SZXSKI doi: 10.17650/1994-4098-2022-18-4-127-137

[39]

Bairamova NN, Protasova AE, Raskin GA, et al. Distribution of malignant neoplasms among patients with endometriosis: an epidemiological study. Journal of Obstetrics and Women’s Diseases. 2018;67(6):5–12. EDN: VSVSOK doi: 10.17816/JOWD6765-12

[40]

Байрамова Н.Н., Протасова А.Э., Раскин Г.А., и др. Структура злокачественных новообразований у больных эндометриозом: данные эпидемиологического исследования // Журнал акушерства и женских болезней. 2018. Т. 67, № 6. С. 5–12. EDN: VSVSOK doi: 10.17816/JOWD6765-12

[41]

Rolla E. Endometriosis: advances and controversies in classification, pathogenesis, diagnosis, and treatment. F1000Res. 2019;8:F1000 Faculty Rev-529. doi: 10.12688/f1000research.14817.1

[42]

Rolla E. Endometriosis: advances and controversies in classification, pathogenesis, diagnosis, and treatment // F1000Res. 2019. Vol. 8. P. F1000 Faculty Rev-529. doi: 10.12688/f1000research.14817.1

[43]

Yovich JL, Rowlands PK, Lingham S, et al. Pathogenesis of endometriosis: look no further than John Sampson. Reprod Biomed Online. 2020;40(1):7–11. doi: 10.1016/j.rbmo.2019.10.007

[44]

Yovich J.L., Rowlands P.K., Lingham S., et al. Pathogenesis of endometriosis: Look no further than John Sampson // Reprod Biomed Online. 2020. Vol. 40, N 1. P. 7–11. doi: 10.1016/j.rbmo.2019.10.007

[45]

Saunders PTK, Horne AW. Endometriosis: etiology, pathobiology, and therapeutic prospects. Cell. 2021;184(11):2807–2824. doi: 10.1016/j.cell.2021.04.041

[46]

Saunders P.T.K., Horne A.W. Endometriosis: etiology, pathobiology, and therapeutic prospects // Cell. 2021. Vol. 184, N 11. P. 2807–2824. doi: 10.1016/j.cell.2021.04.041

[47]

García-Peñarrubia P, Ruiz-Alcaraz AJ, Martínez-Esparza M, et al. Hypothetical roadmap towards endometriosis: prenatal endocrine-disrupting chemical pollutant exposure, anogenital distance, gut-genital microbiota and subclinical infections. Hum Reprod Update. 2020;26(2):214–246. doi: 10.1093/humupd/dmz044

[48]

García-Peñarrubia P., Ruiz-Alcaraz A.J., Martínez-Esparza M., et al. Hypothetical roadmap towards endometriosis: prenatal endocrine-disrupting chemical pollutant exposure, anogenital distance, gut-genital microbiota and subclinical infections // Hum Reprod Update. 2020. Vol. 26, N 2 P. 214–246. doi: 10.1093/humupd/dmz044

[49]

Symons LK, Miller JE, Kay VR, et al. The immunopathophysiology of endometriosis. Trends Mol Med. 2018;24(9):748–762. doi: 10.1016/j.molmed.2018.07.004

[50]

Symons L.K., Miller J.E., Kay V.R., et al. The immunopathophysiology of endometriosis // Trends Mol Med. 2018. Vol. 24, N 9. P. 748–762. doi: 10.1016/j.molmed.2018.07.004

[51]

Bulun SE, Yilmaz BD, Sison C, et al. Endometriosis. Endocr Rev. 2019;40(4):1048–1079. doi: 10.1210/er.2018-00242

[52]

Bulun S.E., Yilmaz B.D., Sison C., et al. Endometriosis // Endocr Rev. 2019. Vol. 40, N 4. P. 1048–1079. doi: 10.1210/er.2018-00242

[53]

Fung JN, Montgomery GW. Genetics of endometriosis: state of the art on genetic risk factors for endometriosis. Best Pract Res Clin Obstet Gynaecol. 2018;50:61–71. doi: 10.1016/j.bpobgyn.2018.01.012

[54]

Fung J.N., Montgomery G.W. Genetics of endometriosis: state of the art on genetic risk factors for endometriosis // Best Pract Res Clin Obstet Gynaecol. 2018. Vol. 50. P. 61–71. doi: 10.1016/j.bpobgyn.2018.01.012

[55]

Vennberg Karlsson J, Patel H, Premberg A. Experiences of health after dietary changes in endometriosis: a qualitative interview study. BMJ open. 2020;10(2):e032321. doi: 10.1136/bmjopen-2019-032321

[56]

Vennberg Karlsson J., Patel H., Premberg A. Experiences of health after dietary changes in endometriosis: a qualitative interview study // BMJ open. 2020. Vol. 10, N 2. P. e032321. doi: 10.1136/bmjopen-2019-032321

[57]

Koller D, Pathak GA, Wendt FR, et al. Epidemiologic and genetic associations of endometriosis with depression, anxiety, and eating disorders. JAMA Netw Open. 2023;6(1):e2251214. doi: 10.1001/jamanetworkopen.2022.51214

[58]

Koller D., Pathak G.A., Wendt F.R., et al. Epidemiologic and genetic associations of endometriosis with depression, anxiety, and eating disorders // JAMA Netw Open. 2023. Vol. 6, N 1. P. e2251214. doi: 10.1001/jamanetworkopen.2022.51214

[59]

Salliss ME, Farland LV, Mahnert ND, Herbst-Kralovetz MM. The role of gut and genital microbiota and the estrobolome in endometriosis, infertility and chronic pelvic pain. Hum Reprod Update. 2021;28(1):92–131. doi: 10.1093/humupd/dmab035

[60]

Salliss M.E., Farland L.V., Mahnert N.D., Herbst-Kralovetz M.M. The role of gut and genital microbiota and the estrobolome in endometriosis, infertility and chronic pelvic pain // Hum Reprod Update. 2021. Vol. 28, N 1. P. 92–131. doi: 10.1093/humupd/dmab035

[61]

Huang L, Liu B, Liu Z, et al. Gut microbiota exceeds cervical microbiota for early diagnosis of endometriosis. Front Cell Infect Microbiol. 2021;11:788836. doi: 10.3389/fcimb.2021.788836

[62]

Huang L., Liu B., Liu Z., et al. Gut microbiota exceeds cervical microbiota for early diagnosis of endometriosis // Front Cell Infect Microbiol. 2021. Vol. 11. P. 788836. doi: 10.3389/fcimb.2021.788836

[63]

Talwar C, Singh V, Kommagani R. The gut microbiota: a double-edged sword in endometriosis. Biol Reprod. 2022;107(4):881–901. doi: 10.1093/biolre/ioac147

[64]

Talwar C., Singh V., Kommagani R. The gut microbiota: a double-edged sword in endometriosis // Biol Reprod. 2022. Vol. 107, N 4. P. 881–901. doi: 10.1093/biolre/ioac147

[65]

Farooqi T, Bhuyan DJ, Low M, et al. Cannabis and endometriosis: the roles of the gut microbiota and the endocannabinoid system. J Clin Med. 2023;12(22):7071. doi: 10.3390/jcm12227071

[66]

Farooqi T., Bhuyan D.J., Low M., et al. Cannabis and endometriosis: the roles of the gut microbiota and the endocannabinoid system // J Clin Med. 2023. Vol. 12, N 22. P. 7071. doi: 10.3390/jcm12227071

[67]

Hantschel J, Weis S, Schäfer KH, et al. Effect of endometriosis on the fecal bacteriota composition of mice during the acute phase of lesion formation. PLoS One. 2019;14(12):e0226835. doi: 10.1371/journal.pone.0226835

[68]

Hantschel J., Weis S., Schäfer K.H., et al. Effect of endometriosis on the fecal bacteriota composition of mice during the acute phase of lesion formation // PLoS One. 2019. Vol. 14, N 12. P. e0226835. doi: 10.1371/journal.pone.0226835

[69]

Perrotta AR, Borrelli GM, Martins CO, et al. The vaginal microbiome as a tool to predict rASRM stage of disease in endometriosis: a pilot study. Reprod Sci. 2020;27(4):1064–1073. doi: 10.1007/s43032-019-00113-5

[70]

Perrotta A.R., Borrelli G.M., Martins C.O., et al. The vaginal microbiome as a tool to predict rASRM stage of disease in endometriosis: a pilot study // Reprod Sci. 2020. Vol. 27, N 4. P. 1064–1073. doi: 10.1007/s43032-019-00113-5

[71]

Yuan M, Li D, Zhang Z, et al. Endometriosis induces gut microbiota alterations in mice. Hum Reprod. 2018;33(4):607–616. doi: 10.1093/humrep/dex372

[72]

Yuan M., Li D., Zhang Z., et al. Endometriosis induces gut microbiota alterations in mice // Hum Reprod. 2018. Vol. 33, N 4. P. 607–616. doi: 10.1093/humrep/dex372

[73]

Ni Z, Sun S, Bi Y, et al. Correlation of fecal metabolomics and gut microbiota in mice with endometriosis. Am J Reprod Immunol. 2020;84(6):e13307. doi: 10.1111/aji.13307

[74]

Ni Z., Sun S., Bi Y., et al. Correlation of fecal metabolomics and gut microbiota in mice with endometriosis // Am J Reprod Immunol. 2020. Vol. 84, N 6. P. e13307. doi: 10.1111/aji.13307

[75]

Ata B, Yildiz S, Turkgeldi E, et al. The endobiota study: comparison of vaginal, cervical and gut microbiota between women with stage 3/4 endometriosis and healthy controls. Sci Rep. 2019;9(1):2204. doi: 10.1038/s41598-019-39700-6

[76]

Ata B., Yildiz S., Turkgeldi E., et al. The endobiota study: comparison of vaginal, cervical and gut microbiota between women with stage 3/4 endometriosis and healthy controls // Sci Rep. 2019. Vol. 9, N 1. P. 2204. doi: 10.1038/s41598-019-39700-6

[77]

Shan J, Ni Z, Cheng W, et al. Gut microbiota imbalance and its correlations with hormone and inflammatory factors in patients with stage 3/4 endometriosis. Arch Gynecol Obstet. 2021;304(5): 1363–1373. doi: 10.1007/s00404-021-06057-z

[78]

Shan J., Ni Z., Cheng W., et al. Gut microbiota imbalance and its correlations with hormone and inflammatory factors in patients with stage 3/4 endometriosis // Arch Gynecol Obstet. 2021. Vol. 304, N 5. P. 1363–1373. doi: 10.1007/s00404-021-06057-z

[79]

Chadchan SB, Popli P, Ambati CR, et al. Gut microbiota-derived short-chain fatty acids protect against the progression of endometriosis. Life Sci Alliance. 2021;4(12):e202101224. doi: 10.26508/lsa.202101224

[80]

Chadchan S.B., Popli P., Ambati C.R., et al. Gut microbiota-derived short-chain fatty acids protect against the progression of endometriosis // Life Sci Alliance. 2021. Vol. 4, N 12. P. e202101224. doi: 10.26508/lsa.202101224

[81]

Cao Y, Jiang C, Jia Y, et al. Letrozole and the traditional chinese medicine, shaofu zhuyu decoction, reduce endometriotic disease progression in rats: a potential role for gut microbiota. Evid Based Complement Alternat Med. 2020;3687498. doi: 10.1155/2020/3687498

[82]

Cao Y., Jiang C., Jia Y., et al. Letrozole and the traditional chinese medicine, shaofu zhuyu decoction, reduce endometriotic disease progression in rats: a potential role for gut microbiota // Evid Based Complement Alternat Med. 2020. P. 3687498. doi: 10.1155/2020/3687498

[83]

Merrheim J, Villegas J, Van Wassenhove J, et al. Estrogen, estrogen-like molecules and autoimmune diseases. Autoimmun Rev. 2020;19(3):102468. doi: 10.1016/j.autrev.2020.102468

[84]

Merrheim J., Villegas J., Van Wassenhove J., et al. Estrogen, estrogen-like molecules and autoimmune diseases // Autoimmun Rev. 2020. Vol. 19, N 3. P. 102468. doi: 10.1016/j.autrev.2020.102468

[85]

Leonardi M, Hicks C, El-Assaad F, et al. Endometriosis and the microbiome: a systematic review. BJOG. 2020;127(2):239–249. doi: 10.1111/1471-0528.15916

[86]

Leonardi M., Hicks C., El-Assaad F., et al. Endometriosis and the microbiome: a systematic review // BJOG. 2020. Vol. 127, N 2. P. 239–249. doi: 10.1111/1471-0528.15916

[87]

Qi X, Yun C, Pang Y, Qiao J. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes. 2021;13(1):1–21. doi: 10.1080/19490976.2021.1894070

[88]

Qi X., Yun C., Pang Y., Qiao J. The impact of the gut microbiota on the reproductive and metabolic endocrine system // Gut Microbes. 2021. Vol. 13, N 1. P. 1–21. doi: 10.1080/19490976.2021.1894070

[89]

Ramírez-Pavez TN, Martínez-Esparza M, Ruiz-Alcaraz AJ, et al. The role of peritoneal macrophages in endometriosis. Int J Mol Sci. 2021;22(19):10792. doi: 10.3390/ijms221910792

[90]

Ramírez-Pavez T.N., Martínez-Esparza M., Ruiz-Alcaraz A.J., et al. The role of peritoneal macrophages in endometriosis // Int J Mol Sci. 2021. Vol. 22, N 19. P. 10792. doi: 10.3390/ijms221910792

[91]

Machairiotis N, Vasilakaki S, Thomakos N. Inflammatory mediators and pain in endometriosis: a systematic review. Biomedicines. 2021;9(1):54. doi: 10.3390/biomedicines9010054

[92]

Machairiotis N., Vasilakaki S., Thomakos N. Inflammatory mediators and pain in endometriosis: a systematic review // Biomedicines. 2021. Vol. 9, N 1. P. 54. doi: 10.3390/biomedicines9010054

[93]

Zhou WJ, Yang HL, Shao J, et al. Anti-inflammatory cytokines in endometriosis. Cell Mol Life Sci. 2019;76(11):2111–2132. doi: 10.1007/s00018-019-03056-x

[94]

Zhou W.J., Yang H.L., Shao J., et al. Anti-inflammatory cytokines in endometriosis // Cell Mol Life Sci. 2019. Vol. 76, N 11. P. 2111–2132. doi: 10.1007/s00018-019-03056-x

[95]

Quaranta G, Sanguinetti M, Masucci L. Fecal microbiota transplantation: a potential tool for treatment of human female reproductive tract diseases. Front Immunol. 2019;10:2653. doi: 10.3389/fimmu.2019.02653

[96]

Quaranta G., Sanguinetti M., Masucci L. Fecal microbiota transplantation: a potential tool for treatment of human female reproductive tract diseases // Front Immunol. 2019. Vol. 10. P. 2653. doi: 10.3389/fimmu.2019.02653

[97]

Artymuk NV, Bezhenar’ VF, Berlim JuD. Jendometrioz. Patogenez, diagnostika, lechenie. SO Dubrovina, VF Bezhenar’, editors. Moscow: GJeOTAR-Media; 2020. 352 p. (In Russ). EDN: JWNYNM

[98]

Артымук Н.В., Беженарь В.Ф., Берлим Ю.Д. Эндометриоз. Патогенез, диагностика, лечение / под ред. С.О. Дубровиной, В.Ф. Беженаря. Москва: ГЭОТАР-Медиа, 2020. 352 с. EDN: JWNYNM

[99]

Ang QY, Alexander M, Newman JC, et al. Ketogenic diets alter the gut microbiome resulting in decreased intestinal Th17 cells. Cell. 2020;181(6):1263–1275.e16. doi: 10.1016/j.cell.2020.04.027

[100]

Ang Q.Y., Alexander M., Newman J.C., et al. Ketogenic diets alter the gut microbiome resulting in decreased intestinal Th17 cells // Cell. 2020. Vol. 181, N 6. P. 1263–1275. doi: 10.1016/j.cell.2020.04.027

[101]

Agostinis C, Zorzet S, Balduit A, et al. The inflammatory feed-forward loop triggered by the complement component C3 as a potential target in endometriosis. Front Immunol. 2021;12:693118. doi: 10.3389/fimmu.2021.693118

[102]

Agostinis C., Zorzet S., Balduit A., et al. The inflammatory feed-forward loop triggered by the complement component C3 as a potential target in endometriosis // Front Immunol. 2021. Vol. 12. P. 693118. doi: 10.3389/fimmu.2021.693118

[103]

Ervin SM, Li H, Lim L, et al. Gut microbial β-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens. J Biol Chem. 2019;294(49):18586–18599. doi: 10.1074/jbc.RA119.010950

[104]

Ervin S.M., Li H., Lim L., et al. Gut microbial β-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens // J Biol Chem. 2019. Vol. 294, N 49. P. 18586–18599. doi: 10.1074/jbc.RA119.010950

[105]

Cai J, Sun L, Gonzalez FJ. Gut microbiota-derived bile acids in intestinal immunity, inflammation, and tumorigenesis. Cell Host Microbe. 2022;30(3):289–300. doi: 10.1016/j.chom.2022.02.004

[106]

Cai J., Sun L., Gonzalez F.J. Gut microbiota-derived bile acids in intestinal immunity, inflammation, and tumorigenesis // Cell Host Microbe. 2022. Vol. 30, N 3. P. 289–300. doi: 10.1016/j.chom.2022.02.004

[107]

Taniguchi F, Ota I, Iba Y, et al. The efficacy and safety of dydrogesterone for treatment of dysmenorrhea: an open-label multicenter clinical study. J Obstet Gynaecol Res. 2019;45(1): 168–175. doi: 10.1111/jog.13807

[108]

Taniguchi F., Ota I., Iba Y., et al. The efficacy and safety of dydrogesterone for treatment of dysmenorrhea: an open-label multicenter clinical study // J Obstet Gynaecol Res. 2019. Vol. 45, N 1. P. 168–175. doi: 10.1111/jog.13807

RIGHTS & PERMISSIONS

Eco-Vector

AI Summary AI Mindmap
PDF

156

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/