LI Maoping, CHANG Heng. Research Progress on the Correlation Between Microecological Flora and Endometriosis[J]. Medical Journal of Peking Union Medical College Hospital, 2025, 16(1): 184-191. DOI: 10.12290/xhyxzz.2024-0201
Citation: LI Maoping, CHANG Heng. Research Progress on the Correlation Between Microecological Flora and Endometriosis[J]. Medical Journal of Peking Union Medical College Hospital, 2025, 16(1): 184-191. DOI: 10.12290/xhyxzz.2024-0201

Research Progress on the Correlation Between Microecological Flora and Endometriosis

More Information
  • Corresponding author:

    CHANG Heng, E-mail: changheng3030@163.com

  • Received Date: March 28, 2024
  • Accepted Date: April 21, 2024
  • Available Online: May 09, 2024
  • Publish Date: May 08, 2024
  • Issue Publish Date: January 29, 2025
  • Microecological flora, an important part of the human microenvironment, changes with the changes in the internal and external environments of the human body, and plays an important role in maintaining human body's normal function. Endometriosis (EMs) is a common estrogen-dependent female disease chara-cterized by the growth of endometrial glands and mesenchyme outside the uterine cavity. Existing studies have shown that imbalance of intestinal and reproductive tract flora can trigger local immune-inflammatory responses and cause systemic immune-inflammatory responses through cytokines and metabolic pathways, which in turn participate in the progression of EMs. Thus, the diagnosis and treatment of EMs through microecological flora interventions is one of the hotspots research in this field. This article aims to review the research progress on the correlation between microbial dysbiosis and EMs, with the hope of providing more references for the treatment of EMs.

  • [1]
    He G M, Chen J B, Peng Z Q, et al. A study on the correlation between quality of life and unhealthy emotion among patients with endometriosis[J]. Front Psychol, 2022, 13: 830698. DOI: 10.3389/fpsyg.2022.830698
    [2]
    Le N, Cregger M, Fazleabas A, et al. Effects of endometriosis on immunity and mucosal microbial community dynamics in female olive baboons[J]. Sci Rep, 2022, 12(1): 1590. DOI: 10.1038/s41598-022-05499-y
    [3]
    Taylor H S, Kotlyar A M, Flores V A. Endometriosis is a chronic systemic disease: clinical challenges and novel innovations[J]. Lancet, 2021, 397(10276): 839-852. DOI: 10.1016/S0140-6736(21)00389-5
    [4]
    Chen S K, Gu Z Y, Zhang W, et al. Microbiome of the lower genital tract in Chinese women with endometriosis by 16s-rRNA sequencing technique: a pilot study[J]. Ann Transl Med, 2020, 8(21): 1440. DOI: 10.21037/atm-20-1309
    [5]
    Lin W C, Chang C Y Y, Hsu Y A, et al. Increased risk of endometriosis in patients with lower genital tract infection: a nationwide cohort study[J]. Medicine (Baltimore), 2016, 95(10): e2773. DOI: 10.1097/MD.0000000000002773
    [6]
    Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women[J]. Proc Natl Acad Sci U S A, 2011, 108(Suppl 1): 4680-4687.
    [7]
    Molina N M, Sola-Leyva A, Saez-Lara M J, et al. New opportunities for endometrial health by modifying uterine microbial composition: present or future?[J]. Biomolecules, 2020, 10(4): 593. DOI: 10.3390/biom10040593
    [8]
    Amro B, Ramirez Aristondo M E, Alsuwaidi S, et al. New understanding of diagnosis, treatment and prevention of endometriosis[J]. Int J Environ Res Public Health, 2022, 19(11): 6725. DOI: 10.3390/ijerph19116725
    [9]
    Leonardi M, Hicks C, El-Assaad F, et al. Endometriosis and the microbiome: a systematic review[J]. BJOG, 2020, 127(2): 239-249. DOI: 10.1111/1471-0528.15916
    [10]
    Khan K N, Fujishita A, Hiraki K, et al. Bacterial contamination hypothesis: a new concept in endometriosis[J]. Reprod Med Biol, 2018, 17(2): 125-133. DOI: 10.1002/rmb2.12083
    [11]
    Fan P Y, Li T. Unveil the pain of endometriosis: from the perspective of the nervous system[J]. Expert Rev Mol Med, 2022, 24: e36. DOI: 10.1017/erm.2022.26
    [12]
    Yano M, Matsuda A, Natsume T, et al. Pain-related behavior and brain activation in cynomolgus macaques with naturally occurring endometriosis[J]. Hum Reprod, 2019, 34(3): 469-478. DOI: 10.1093/humrep/dey383
    [13]
    Wang S J, Shang Y J, Pi Z Y, et al. Temporal changes of the oral and fecal microbiota after mild traumatic brain injury in rats by 16S rRNA sequencing[J]. Microorganisms, 2023, 11(6): 1452. DOI: 10.3390/microorganisms11061452
    [14]
    Slocum C, Kramer C, Genco C A. Immune dysregulation mediated by the oral microbiome: potential link to chronic inflammation and atherosclerosis[J]. J Intern Med, 2016, 280(1): 114-128. DOI: 10.1111/joim.12476
    [15]
    Hu J J, Li G J, Huang M M, et al. Analysis of microbiota reveals the underlying mechanism of PHF11 in the development of Enterococcus-regulated endometriotic cysts[J]. iScience, 2023, 26(11): 108158. DOI: 10.1016/j.isci.2023.108158
    [16]
    Dicks L M T. Gut bacteria and neurotransmitters[J]. Microorganisms, 2022, 10(9): 1838. DOI: 10.3390/microorganisms10091838
    [17]
    Wang J F, Li Z Z, Ma X L, et al. Translocation of vaginal microbiota is involved in impairment and protection of uterine health[J]. Nat Commun, 2021, 12(1): 4191. DOI: 10.1038/s41467-021-24516-8
    [18]
    Witkin S S, Linhares I M. Why do lactobacilli dominate the human vaginal microbiota?[J]. BJOG, 2017, 124(4): 606-611. DOI: 10.1111/1471-0528.14390
    [19]
    黄思霞. 不同分期子宫内膜异位症患者肠道微生物菌群的特征性研究[D]. 广州: 南方医科大学, 2023: 75.

    Huang S X. Characteristics of gut microbiota in patients with different stages of Endometriosis[D]. Guangzhou: Southern Medical University, 2023: 75.
    [20]
    Chadchan S B, Naik S K, Popli P, et al. Gut microbiota and microbiota-derived metabolites promotes endometriosis[J]. Cell Death Discov, 2023, 9(1): 28. DOI: 10.1038/s41420-023-01309-0
    [21]
    Baker J M, Al-Nakkash L, Herbst-Kralovetz M M. Estrogen-gut microbiome axis: physiological and clinical implications[J]. Maturitas, 2017, 103: 45-53. DOI: 10.1016/j.maturitas.2017.06.025
    [22]
    Pai A H Y, Wang Y W, Lu P C, et al. Gut microbiome-estrobolome profile in reproductive-age women with endometriosis[J]. Int J Mol Sci, 2023, 24(22): 16301. DOI: 10.3390/ijms242216301
    [23]
    Elkafas H, Walls M, Al-Hendy A, et al. Gut and genital tract microbiomes: dysbiosis and link to gynecological disorders[J]. Front Cell Infect Microbiol, 2022, 12: 1059825. DOI: 10.3389/fcimb.2022.1059825
    [24]
    Guo R, Chen L H, Xing C G, et al. Pain regulation by gut microbiota: molecular mechanisms and therapeutic potential[J]. Br J Anaesth, 2019, 123(5): 637-654. DOI: 10.1016/j.bja.2019.07.026
    [25]
    Ding X M, Zhou J, Zhao L, et al. Intestinal flora composition determines microglia activation and improves epileptic episode progress[J]. Front Cell Infect Microbiol, 2022, 12: 835217. DOI: 10.3389/fcimb.2022.835217
    [26]
    Saldova R. Cause of cancer and chronic inflammatory diseases and the implications for treatment[J]. Discov Med, 2016, 22(120): 105-119.
    [27]
    Zhai L X, Wu J Y, Lam Y Y, et al. Gut-microbial metabolites, probiotics and their roles in type 2 diabetes[J]. Int J Mol Sci, 2021, 22(23): 12846. DOI: 10.3390/ijms222312846
    [28]
    Shabbir U, Arshad M S, Sameen A, et al. Crosstalk between gut and brain in Alzheimer's disease: the role of gut microbiota modulation strategies[J]. Nutrients, 2021, 13(2): 690. DOI: 10.3390/nu13020690
    [29]
    Li M F, Yang H, Shao C Y, et al. Application of dominant gut microbiota promises to replace fecal microbiota transplantation as a new treatment for Alzheimer's disease[J]. Microorganisms, 2023, 11(12): 2854. DOI: 10.3390/microorganisms11122854
    [30]
    Feng C, Li A H, Yin C H, et al. Realgar alleviated neuroinflammation induced by high protein and high calorie diet in rats via the microbiota-gut-brain axis[J]. Nutrients, 2022, 14(19): 3958. DOI: 10.3390/nu14193958
    [31]
    Gao Y J, Ji R R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain[J]. Pharmacol Ther, 2010, 126(1): 56-68. DOI: 10.1016/j.pharmthera.2010.01.002
    [32]
    Fattori V, Franklin N S, Gonzalez-Cano R, et al. Nonsurg-ical mouse model of endometriosis-associated pain that responds to clinically active drugs[J]. Pain, 2020, 161(6): 1321-1331. DOI: 10.1097/j.pain.0000000000001832
    [33]
    Wei W X, Zhang X W, Tang H R, et al. Microbiota composition and distribution along the female reproductive tract of women with endometriosis[J]. Ann Clin Microbiol Antimicrob, 2020, 19(1): 15. DOI: 10.1186/s12941-020-00356-0
    [34]
    Mahajan G, Doherty E, To T, et al. Vaginal microbiome-host interactions modeled in a human vagina-on-a-chip[J]. Microbiome, 2022, 10(1): 201. DOI: 10.1186/s40168-022-01400-1
    [35]
    Gholiof M, Adamson-De Luca E, Wessels J M. The female reproductive tract microbiotas, inflammation, and gynecological conditions[J]. Front Reprod Health, 2022, 4: 963752. DOI: 10.3389/frph.2022.963752
    [36]
    Lu F L, Wei J, Zhong Y Y, et al. Antibiotic therapy and vaginal microbiota transplantation reduce endometriosis disease progression in female mice via NF-κB signaling pathway[J]. Front Med (Lausanne), 2022, 9: 831115.
    [37]
    Chao X P, Liu Y, Fan Q B, et al. The role of the vaginal microbiome in distinguishing female chronic pelvic pain caused by endometriosis/adenomyosis[J]. Ann Transl Med, 2021, 9(9): 771. DOI: 10.21037/atm-20-4586
    [38]
    Ustianowska K, Ustianowski Ł, Machaj F, et al. The role of the human microbiome in the pathogenesis of pain[J]. Int J Mol Sci, 2022, 23(21): 13267. DOI: 10.3390/ijms232113267
    [39]
    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[J]. Sci Rep, 2019, 9(1): 2204. DOI: 10.1038/s41598-019-39700-6
    [40]
    Salmeri N, Viganò P, Cavoretto P, et al. The kisspeptin system in and beyond reproduction: exploring intricate pathways and potential links between endometriosis and polycystic ovary syndrome[J]. Rev Endocr Metab Disord, 2024, 25(2): 239-257. DOI: 10.1007/s11154-023-09826-0
    [41]
    Khan K N, Fujishita A, Masumoto H, et al. Molecular detection of intrauterine microbial colonization in women with endometriosis[J]. Eur J Obstet Gynecol Reprod Biol, 2016, 199: 69-75. DOI: 10.1016/j.ejogrb.2016.01.040
    [42]
    Akiyama K, Nishioka K, Khan K N, et al. Molecular detection of microbial colonization in cervical mucus of women with and without endometriosis[J]. Am J Reprod Immunol, 2019, 82(2): e13147. DOI: 10.1111/aji.13147
    [43]
    Xu H, Zhao J, Lu J Q, et al. Ovarian endometrioma infiltrating neutrophils orchestrate immunosuppressive microenvironment[J]. J Ovarian Res, 2020, 13(1): 44. DOI: 10.1186/s13048-020-00642-7
    [44]
    Khan K N, Fujishita A, Koshiba A, et al. Biological differences between intrinsic and extrinsic adenomyosis with coexisting deep infiltrating endometriosis[J]. Reprod Biomed Online, 2019, 39(2): 343-353. DOI: 10.1016/j.rbmo.2019.03.210
    [45]
    Kulinska K I, Białas P, Dera-Szymanowska A, et al. The role of phoenixin in the proliferation and migration of ectopic epithelial cells in vitro[J]. Biochem Biophys Res Commun, 2023, 646: 44-49. DOI: 10.1016/j.bbrc.2023.01.056
    [46]
    Lee S R, Lee J C, Kim S H, et al. Altered composition of microbiota in women with ovarian endometrioma: microbiome analyses of extracellular vesicles in the peritoneal fluid[J]. Int J Mol Sci, 2021, 22(9): 4608. DOI: 10.3390/ijms22094608
    [47]
    Wang X M, Ma Z Y, Song N. Inflammatory cytokines IL-6, IL-10, IL-13, TNF-α and peritoneal fluid flora were associated with infertility in patients with endometriosis[J]. Eur Rev Med Pharmacol Sci, 2018, 22(9): 2513-2518.
    [48]
    Chang C Y Y, Chiang A J, Lai M T, et al. A more diverse cervical microbiome associates with better clinical outcomes in patients with endometriosis: a pilot study[J]. Biomedicines, 2022, 10(1): 174. DOI: 10.3390/biomedicines10010174
    [49]
    Nabiel Y, ELshahawy H, Mosbah A. Intrauterine bacterial colonization and endometrial microRNA-17-5p levels in association to endometriosis: a study in an Egyptian population[J]. Immunol Invest, 2020, 49(6): 611-621. DOI: 10.1080/08820139.2019.1693592
    [50]
    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[J]. Reprod Sci, 2020, 27(4): 1064-1073. DOI: 10.1007/s43032-019-00113-5
    [51]
    Rzewuska A M, Żybowska M, Sajkiewicz I, et al. Gonadotropin-releasing hormone antagonists-a new hope in endometriosis treatment?[J]. J Clin Med, 2023, 12(3): 1008. DOI: 10.3390/jcm12031008
    [52]
    Slate-Romano J J, Yano N, Zhao T C. Irisin reduces inflammatory signaling pathways in inflammation-mediated metabolic syndrome[J]. Mol Cell Endocrinol, 2022, 552: 111676. DOI: 10.1016/j.mce.2022.111676
    [53]
    Mazur-Bialy A I, Pocheć E, Zarawski M. Anti-inflammatory properties of irisin, mediator of physical activity, are connected with TLR4/MyD88 signaling pathway activation[J]. Int J Mol Sci, 2017, 18(4): 701. DOI: 10.3390/ijms18040701
    [54]
    Khan K N, Fujishita A, Kitajima M, et al. Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis[J]. Hum Reprod, 2014, 29(11): 2446-2456. DOI: 10.1093/humrep/deu222
    [55]
    Chadchan S B, Cheng M, Parnell L A, et al. Antibiotic therapy with metronidazole reduces endometriosis disease progression in mice: a potential role for gut microbiota[J]. Hum Reprod, 2019, 34(6): 1106-1116. DOI: 10.1093/humrep/dez041
    [56]
    Mancilla V J, Braden-Kuhle P N, Brice K N, et al. A synthetic formula amino acid diet leads to microbiome dysbiosis, reduced colon length, inflammation, and altered locomotor activity in C57BL/6J mice[J]. Microorganisms, 2023, 11(11): 2694. DOI: 10.3390/microorganisms11112694
    [57]
    Porpora M G, Brunelli R, Costa G, et al. A promise in the treatment of endometriosis: an observational cohort study on ovarian endometrioma reduction by N-acetylcysteine[J]. Evid Based Complement Alternat Med, 2013, 2013: 240702.
    [58]
    Sienko A, Cichosz A, Urban A, et al. The effect of two anti-inflammatory dietary components, omega-3 and resveratrol, on endometriosis[J]. Ginekol Pol, 2024, 95(7): 573-583. DOI: 10.5603/gpl.97573
    [59]
    Arablou T, Aryaeian N, Khodaverdi S, et al. The effects of resveratrol on the expression of VEGF, TGF-β, and MMP-9 in endometrial stromal cells of women with endometriosis[J]. Sci Rep, 2021, 11(1): 6054. DOI: 10.1038/s41598-021-85512-y
    [60]
    Qu Z H, Tian P J, Wang L L, et al. Dietary nucleotides promote neonatal rat microbiota-gut-brain axis development by affecting gut microbiota composition and metabolic function[J]. J Agric Food Chem, 2023, 71(49): 19622-19637. DOI: 10.1021/acs.jafc.3c07349
    [61]
    Hu Z Y, Zhao P H, Liao A M, et al. Fermented wheat germ alleviates depression-like behavior in rats with chronic and unpredictable mild stress[J]. Foods, 2023, 12(5): 920. DOI: 10.3390/foods12050920
    [62]
    Pferschy-Wenzig E M, Pausan M R, Ardjomand-Woelkart K, et al. Medicinal plants and their impact on the gut microbiome in mental health: a systematic review[J]. Nutrients, 2022, 14(10): 2111. DOI: 10.3390/nu14102111
    [63]
    Paredes S, Cantillo S, Candido K D, et al. An association of serotonin with pain disorders and its modulation by estrogens[J]. Int J Mol Sci, 2019, 20(22): 5729. DOI: 10.3390/ijms20225729
    [64]
    Chiantera V, Laganà A S, Basciani S, et al. A critical perspective on the supplementation of Akkermansia muciniphila: benefits and harms[J]. Life (Basel), 2023, 13(6): 1247.
    [65]
    Paladino L, Rappa F, Barone R, et al. NF-κB regulation and the chaperone system mediate restorative effects of the probiotic Lactobacillus fermentum LF31 in the small intestine and cerebellum of mice with ethanol-induced damage[J]. Biology (Basel), 2023, 12(11): 1394.
    [66]
    Xu R L, Zhang Y X, Chen S R, et al. The role of the probiotic Akkermansia muciniphila in brain functions: insights underpinning therapeutic potential[J]. Crit Rev Microbiol, 2023, 49(2): 151-176. DOI: 10.1080/1040841X.2022.2044286

Catalog

    Article Metrics

    Article views (261) PDF downloads (40) Cited by()
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return
    x Close Forever Close