Features of the reproductive tract microbiota in patients with genital endometriosis. A literature review
- 作者: Kazymova O.E.1, Yarmolinskaya M.I.1,2, Savicheva A.M.1,3
-
隶属关系:
- The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott
- North-Western State Medical University named after I.I. Mechnikov
- Saint Petersburg State Pediatric Medical University
- 期: 卷 71, 编号 1 (2022)
- 页面: 129-139
- 栏目: Reviews
- ##submission.dateSubmitted##: 23.11.2021
- ##submission.dateAccepted##: 24.12.2021
- ##submission.datePublished##: 15.01.2022
- URL: https://journals.eco-vector.com/jowd/article/view/88921
- DOI: https://doi.org/10.17816/JOWD88921
- ID: 88921
如何引用文章
详细
BACKGROUND: Due to the widespread prevalence, steady growth and insufficient effectiveness of existing treatment regimens for external genital endometriosis, further study of the etiology and pathogenesis of the disease remains relevant. Inflammation is known to be one of the links in the pathogenesis of endometriosis; therefore, there is reason to believe that microorganisms are involved in the pathogenesis of this disease.
AIM: The aim of this study was to analyze the role of the reproductive tract microbiota in patients with endometriosis.
MATERIALS AND METHODS: This literature review was performed using systematic reviews, meta-analyses and experimental studies from such electronic databases as PubMed, CyberLeninka, and ScienceDirect published in the period from 1992 to 2021.
RESULTS AND CONCLUSIONS: In the review, we present the pathogenetic relationship between pelvic inflammatory diseases and endometriosis. The quantitatively and qualitatively altered microbiota composition of the reproductive tract, the genetic-epigenetic theory on the pathogenesis of endometriosis, which is based on mutations that accumulate directly under the influence of infectious agents, as well as the mechanisms of an abnormal immune response modeled by microorganisms, reflect the interconnection between the microbiota and the pathogenesis of endometriosis. Based on a number of studies, the relationship between the intestinal microbiota and the abdominal microbiome has been confirmed. Since endometriosis is the estrogen-dependent disease, of importance is the ability of the intestinal microbiota to produce β-glucuronidase, which is enhanced by gut microbial dysbiosis, thus possibly contributing to the progression of endometriosis. One of the important practical directions is the drug correction of dysbiotic conditions. The effectiveness of antibiotic therapy has been demonstrated by experimentally induced endometriosis model. Currently, there are very few highly specific methods for non-invasive diagnosis of the disease, therefore, the study of the reproductive tract and intestinal microflora of women with endometriosis is promising for the introduction of new laboratory diagnostic methods.
全文:
作者简介
Olga Kazymova
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott
编辑信件的主要联系方式.
Email: olia.merk@yandex.ru
ORCID iD: 0000-0003-3869-010X
SPIN 代码: 5986-3469
MD
俄罗斯联邦, 3, Mendeleevskaya Line, Saint Petersburg, 199034Maria Yarmolinskaya
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott; North-Western State Medical University named after I.I. Mechnikov
Email: m.yarmolinskaya@gmail.com
ORCID iD: 0000-0002-6551-4147
SPIN 代码: 3686-3605
Scopus 作者 ID: 7801562649
Researcher ID: P-2183-2014
MD, Dr. Sci. (Med.), Professor, Professor of the Russian Academy of Sciences
俄罗斯联邦, 3, Mendeleevskaya Line, Saint Petersburg, 199034; Saint PetersburgAlevtina Savicheva
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott; Saint Petersburg State Pediatric Medical University
Email: savitcheva@mail.ru
ORCID iD: 0000-0003-3870-5930
SPIN 代码: 8007-2630
Scopus 作者 ID: 6602838765
Researcher ID: P-6788-2015
MD, Dr. Sci. (Med.), Professor, Honored Scientist of the Russian Federation
俄罗斯联邦, 3, Mendeleevskaya Line, Saint Petersburg, 199034; Saint Petersburg参考
- Jarmolinskaja MI, Ajlamazjan JeK. Genital’nyj jendometrioz. Razlichnye grani problemy. Saint Petersburg: Jeko-Vektor; 2017.
- Khan KN, Fujishita A, Hiraki K, et al. Bacterial contamination hypothesis: a new concept in endometriosis. Reprod Med Biol. 2018;17(2):125−133. doi: 10.1002/rmb2.12083
- Laschke MW, Menger MD. The gut microbiota: a puppet master in the pathogenesis of endometriosis? Am J Obstet Gynecol. 2016;215(1):68.e1−4. doi: 10.1016/j.ajog.2016.02.036
- Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93−110.43.
- Jacobson L. Endometriosis with infection of the small pelvis. Nord Med. 1960;64:844−847.
- Jiang I, Yong PJ, Allaire C, Bedaiwy MA. Intricate connections between the microbiota and endometriosis. Int J Mol Sci. 2021;22(11):5644. doi: 10.3390/ijms22115644
- France MT, Ma B, Gajer P, et al. VALENCIA: a nearest centroid classification method for vaginal microbial communities based on composition. Microbiome. 2020;8(1):166. doi: 10.1186/s40168-020-00934-6
- Baker JM, Chase DM, Herbst-Kralovetz MM. Uterine microbiota: Residents, tourists, or invaders? Front Immunol. 2018;9:208. doi: 10.3389/fimmu.2018.00208
- Bedaiwy MA. Endometrial macrophages, endometriosis, and microbiota: time to unravel the complexity of the relationship. Fertil Steril. 2019;112(6):1049−1050. doi: 10.1016/j.fertnstert.2019.09.021
- 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
- Elizur SE, Lebovitz O, Weintraub AY, et al. Pelvic inflammatory disease in women with endometriosis is more severe than in those without. Aust NZJ Obstet Gynaecol. 2014;54(2):162−165. doi: 10.1111/ajo.12189
- Tai FW, Chang CY, Chiang JH, et al. Association of pelvic inflammatory disease with risk of endometriosis: A nationwide cohort study involving 141,460 individuals. J Clin Med. 2018;7(11):379. doi: 10.3390/jcm7110379
- Lin WC, Chang CY, Hsu YA, et al. Increased risk of endometriosis in patients with lower Genital tract infection: A nationwide cohort study. Medicine (Baltimore). 2016;95(10):e2773. doi: 10.1097/MD.0000000000002773
- Takebayashi A, Kimura F, Kishi Y, et al. The association between endometriosis and chronic endometritis. PLoS One. 2014;9(2):e88354. doi: 10.1371/journal.pone.0088354
- Cicinelli E, Trojano G, Mastromauro M, et al. Higher prevalence of chronic endometritis in women with endometriosis: a possible etiopathogenetic link. Fertil Steril. 2017;108(2):289−295.e1. doi: 10.1016/j.fertnstert.2017.05.016
- Tolibova GH, Tral’ TG, Jarmolinskaja MI, Cypurdeeva AA. Jendometrial’naja disfunkcija u pacientok s besplodiem, associirovannym s naruzhnym genital’nym jendometriozom. Journal of Obstetrics and Women’s Diseases. 2017;66(Suppl):84−85. (In Russ.)
- Koninckx PR, Ussia A, Adamyan L, et al. Pathogenesis of endometriosis: the genetic/epigenetic theory. Fertil Steril. 2019;111(2):327−340. doi: 10.1016/j.fertnstert.2018.10.013
- O’Day DH, Taylor RJ, Myre MA. Calmodulin and calmodulin binding proteins in dictyostelium: A primer. Int J Mol Sci. 2020;21(4):1210. doi: 10.3390/ijms21041210
- Zhang T, De Carolis C, Man GCW, et al. The link between immunity, autoimmunity and endometriosis: a literature update. Autoimmun Rev. 2018;17(10):945−955. doi: 10.1016/j.autrev.2018.03.017
- Scutiero G, Iannone P, Bernardi G, et al. Oxidative stress and endometriosis: A systematic review of the literature. Oxid Med Cell Longev. 2017;2017:7265238. doi: 10.1155/2017/7265238
- Bierne H, Hamon M, Cossart P. Epigenetics and bacterial infections. Cold Spring Harb Perspect Med. 2012;2(12):a010272. doi: 10.1101/cshperspect.a010272
- Milavetz BI, Balakrishnan L. Viral epigenetics. Methods Mol Biol. 2015;1238:569−596. doi: 10.1007/978-1-4939-1804-1_30
- Campos GB, Marques LM, Rezende IS, et al. Mycoplasma genitalium can modulate the local immune response in patients with endometriosis. Fertil Steril. 2018;109(3):549−560.e4. doi: 10.1016/j.fertnstert.2017.11.009
- Khan KN, Kitajima M, Inoue T, et al. 17β-estradiol and lipopolysaccharide additively promote pelvic inflammation and growth of endometriosis. Reprod Sci. 2015;22(5):585−594. doi: 10.1177/1933719114556487
- Sheldon IM, Owens SE, Turner ML. Innate immunity and the sensing of infection, damage and danger in the female genital tract. J Reprod Immunol. 2017;119:67−73. doi: 10.1016/j.jri.2016.07.002
- Laux-Biehlmann A, d’Hooghe T, Zollner TM. Menstruation pulls the trigger for inflammation and pain in endometriosis. Trends Pharmacol Sci. 2015;36(5):270−276. doi: 10.1016/j.tips.2015.03.004
- 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
- Pinto V, Matteo M, Tinelli R, et al. Altered uterine contractility in women with chronic endometritis. Fertil Steril. 2015;103(4):1049−1052. doi: 10.1016/j.fertnstert.2015.01.007
- Agostinis C, Mangogna A, Bossi F, et al. Uterine immunity and microbiota: A shifting paradigm. Front Immunol. 2019;10:2387. doi: 10.3389/fimmu.2019.02387
- Chen C, Song X, Wei W, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017;8(1):875. doi: 10.1038/s41467-017-00901-0
- Khan KN, Fujishita A, Masumoto H, et al. Molecular detection of intrauterine microbial colonization in women with endometriosis. Eur J Obstet Gynecol Reprod Biol. 2016;199:69−75. doi: 10.1016/j.ejogrb.2016.01.040
- Cregger MA, Braundmeier A, Lenz K, et al. Reproductive microbiomes: Using the microbiome as a novel diagnostic tool for endometriosis. Reproduct Immunol Open Access. 2017;2(3). doi: 10.21767/2476-1974.100036
- Khan KN, Kitajima M, Hiraki K, et al. Escherichia coli contamination of menstrual blood and effect of bacterial endotoxin on endometriosis. Fertil Steril. 2010;94(7):2860-3.e1−3. doi: 10.1016/j.fertnstert.2010.04.053
- 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
- Khan KN, Fujishita A, Kitajima M, et al. Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis†. Hum Reprod. 2014;29(11):2446−2456. doi: 10.1093/humrep/deu222
- Wei W, Zhang X, Tang H, et al. Microbiota composition and distribution along the female reproductive tract of women with endometriosis. Ann Clin Microbiol Antimicrob. 2020;19(1):15. doi: 10.1186/s12941-020-00356-0
- Wang XM, Ma ZY, Song N. Inflammatory cytokines IL-6, IL-10, IL-13, TNF-α and peritoneal fluid flora were associated with infertility in patients with endometriosis. Eur Rev Med Pharmacol Sci. 2018;22(9):2513−2518. doi: 10.26355/eurrev_201805_14899
- Kobayashi H, Higashiura Y, Shigetomi H, et al. Pathogenesis of endometriosis: the role of initial infection and subsequent sterile inflammation (Review). Mol Med Rep. 2014;9(1):9−15. doi: 10.3892/mmr.2013.1755
- Wu QJ, Guo M, Lu ZM, et al. Detection of human papillomavirus-16 in ovarian malignancy. Br J Cancer. 2003;89(4):672−675. doi: 10.1038/sj.bjc.6601172
- Oppelt P, Renner SP, Strick R, al. Correlation of high-risk human papilloma viruses but not of herpes viruses or Chlamydia trachomatis with endometriosis lesions. Fertil Steril. 2010;93(6):1778−1786. doi: 10.1016/j.fertnstert.2008.12.061
- Heidarpour M, Derakhshan M, Derakhshan-Horeh M, et al. Prevalence of high-risk human papillomavirus infection in women with ovarian endometriosis. J Obstet Gynaecol Res. 2017;43(1):135−139. doi: 10.1111/jog.13188
- Vestergaard AL, Knudsen UB, Munk T, et al. Low prevalence of DNA viruses in the human endometrium and endometriosis. Arch Virol. 2010;155(5):695−703. doi: 10.1007/s00705-010-0643-y
- Rocha RM, Souza RP, Gimenes F, et al. The high-risk human papillomavirus continuum along the female reproductive tract and its relationship to infertility and endometriosis. Reprod Biomed Online. 2019;38(6):926−937. doi: 10.1016/j.rbmo.2018.11.032
- Akiyama K, Nishioka K, Khan KN, et al. Molecular detection of microbial colonization in cervical mucus of women with and without endometriosis. Am J Reprod Immunol. 2019;82(2):e13147. doi: 10.1111/aji.13147
- Chen S, Gu Z, Zhang W, et al. Microbiome of the lower genital tract in Chinese women with endometriosis by 16s-rRNA sequencing technique: a pilot study. Ann Transl Med. 2020;8(21):1440. doi: 10.21037/atm-20-1309
- Okamoto N, Uchida A, Takakura K, et al. Suppression by human placental protein 14 of natural killer cell activity. Am J Reprod Immunol. 1991;26(4):137−142. doi: 10.1111/j.1600-0897.1991.tb00713.x
- Kanzaki H, Wang HS, Kariya M, et al. Suppression of natural killer cell activity by sera from patients with endometriosis. Am J Obstet Gynecol. 1992;167(1):257−261. doi: 10.1016/s0002-9378(11)91670-6
- Lee SR, Lee JC, Kim SH, et al. Altered composition of microbiota in women with ovarian endometrioma: Microbiome analyses of extracellular vesicles in the peritoneal fluid. Int J Mol Sci. 2021;22(9):4608. doi: 10.3390/ijms22094608
- 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
- Jess T, Frisch M, Jørgensen KT, et al. Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study. Gut. 2012;61(9):1279−1283. doi: 10.1136/gutjnl-2011-301095
- 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
- Kitawaki J, Kado N, Ishihara H, et al. Endometriosis: the pathophysiology as an estrogen-dependent disease. J Steroid Biochem Mol Biol. 2002;83(1−5):149−155. doi: 10.1016/s0960-0760(02)00260-1
- Jones LA, Sun EW, Martin AM, et al. The ever-changing roles of serotonin. Int J Biochem Cell Biol. 2020;125:105776. doi: 10.1016/j.biocel.2020.105776
- Kalinkina OB, Tezikov YuV, Lipatov IS, et al. Study of urogenital tract and gut microbiota in women with stage III and IV ovarian endometriosis. Perm Medical Journal. 2020;37(1):14−21. doi: 10.17816/pmj37114-21
- 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
- Chadchan SB, Cheng M, Parnell LA, et al. Antibiotic therapy with metronidazole reduces endometriosis disease progression in mice: a potential role for gut microbiota. Hum Reprod. 2019;34(6):1106−1116. doi: 10.1093/humrep/dez041