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Endometriosis is an inflammatory and estrogen-dependent condition, affecting approximately 6–10% of women in their reproductive years. The pathogenesis and histological findings are characterized by endometrial glandular and stromal tissue growing beyond the uterus. It is classified into three types: superficial, ovarian, and deep endometriosis. In addition to gynecological manifestations, many endometriosis patients experience gastrointestinal symptoms, indicating a potential association between gut health and the disease.
Study | N | Animal Species | Endometriosis Model | Sample | Technic | Aim and Conclusion |
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Bailey & Coe, 2002 [35] | 18 | Female Rhesus Monkeys (Macaca Mulatta) | Spontaneous occurring endometriosis, diagnosed with USG and MRI and confirmed by surgery and histology | Fecal samples | Coprocolture | Aim: demonstrate that monkeys have an altered profile of intestinal microflora, in particular altered Lactobacilli Conclusion: decreased Lactobacilli and increased gram-negative anaerobes and facultative anaerobes |
Yuan et al., 2018 [45] | Cases: 16 Controls: 20 |
C57BL6 mice | Induced: intraperitoneal injection of endometrial tissue from sacrificed donor mice | Fecal pellets | NGS Illumina: V4 16S rRNA | Aim: determine the changes in gut microbiota in a murine endometriosis model by 16S ribosomal-RNA gene sequencing Conclusion: Firmicutes/Bacteroidetes ratio was elevated in mice with endometriosis, indicating that endometriosis may induce dysbiosis |
Chadchan et al., 2019 [41] | Cases: 5 with endometriosis treated with vehicle and 4 with endometriosis and treated with broad spectrum antibiotics Controls: 5 |
C57BL/6 mice | Induced: autologous transplantation of endometrial tissue onto the peritoneal wall | Fecal pellets, peritoneal fluid, endometriotic lesions | NGS Illumina: V1-V9 16S rRNA | Aim: investigate if altering gut microbiota with antibiotic treatment has any impact on endometriosis progression Conclusion: oral antibiotic treatment is effective in reducing the progression of endometriosis and administering fecal material from mice with endometriosis via oral gavage restored both the growth of endometriotic lesions and inflammation |
Cao et al., 2020 [50] | Cases: 24 Controls: 8 |
Sprague Dawley rats | Induced: autologous transplantation of uterine tissue fragments onto the peritoneal wall | Fecal pellets | NGS Illumina: V3-V4 16S rRNA | Aim: investigate if letrozole and SFZYD can act on microbiota, inhibiting the progression of lesions Conclusion: Letrozole and SFZYD reduce the inflammatory response in both ectopic and eutopic endometrial tissues, which could be associated with the decrease in the Firmicutes/Bacteroidetes ratio. |
Ni et al., 2020 [51] | Cases: 16 Controls: 20 |
C57BL/6J mice | Induced: estrogen solution subcutaneous injection on days 1, 4, and 7, transplantation of endometrial fragments on day 8. Estrogen injection again on day 9, 11, and 14. After 3 weeks, mice were dissected to obtain faces from cecum. | Feces from cecum | NGS Illumina: V3-V4 16S rRNA | Aim: uncover the interaction between fecal metabolomics and gut microbiota in mice with endometriosis Conclusion: The abnormal fecal metabolites, particularly those related to secondary bile acid biosynthesis and the alpha-linolenic acid pathways, influenced by dysbiosis, may serve as distinctive features in mice with endometriosis and as potential markers for distinguishing the disease |
Study | N | Age (Years) | Endometriosis Diagnosis Type | Sample | Technic | Aim and Conclusion |
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Khan et al., 2016 [52] | Cases: 32 Controls: 32 In each group 16 in treatment with GnRHa |
21–52 | Surgery and histology | Endometrial swabs and cystic fluid | NGS Illumina: 16S rRNA | Aim: investigate microbial colonization in intrauterine environment and cystic fluid Conclusion: presence of sub-clinical infections in intrauterine environment and cystic fluid of ovarian endometriomas. Potential additional side effect of GnRHa treatment in promoting silent intrauterine and/or ovarian infections (abundance of Streptococcaceae, Staphylococaceae, Enterobacteriaceae and lowered Lactobacillae in GnRHa treated women) |
Akiyama et al., 2019 [53] | Cases: 30 Controls: 39 |
20–44 | Surgery and histology | Cervical Mucus | NGS Illumina: V5-V6 16S rRNA | Aim: investigating pattern of microbiota in the cervical mucus Conclusion: Enterobacteriaceae and Streptococcus were more commonly found in women with endometriosis |
Ata et al., 2019 [40] | Cases: 14 Controls: 14 |
18–45 | Surgery and histology (only stage 3–4) | Stool sample Vaginal and endocervical swabs |
NGS Illumina: V3- V4 16S rRNA | Aim: comparing gut, vaginal, and cervical microbiota in endometriosis vs. controls Conclusion: no differences in species level analysis, but they found a possible difference at genus level analysis |
Chen et al., 2020 [54] | Cases: 20 endometriosis, 19 adenomyosis and 7 adenomyosis-endometriosis Controls: 36 |
18–45 | Surgery, histology, transvaginal ultrasound, and MRI | Cervical swabs and posterior fornix swabs | NGS Illumina: V3-V4 16S rRNA | Aim: create a microbiota profile model for endometriosis and investigate and identify significant microbiota associated with endometriosis or adenomyosis conditions. Conclusion: Higher prevalence of Atopobium in endometriosis-adenomysosis group |
Hernandes et al., 2020 [42] | Cases: 10 Controls: 11 |
18–50 | Surgery and histology | Vaginal fluid, eutopic endometrium (collected by curettage), and endometrial lesion tissue samples (collected by surgery) | NGS Illumina: V3-V4 rRNA | Aim: Investigate and compare the microbiome profile Conclusion:
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Wei et al., 2020 [44] | Cases: 36 Controls: 14 |
23–44 | Surgery and histology | Lower reproductive tract swabs: lower third of the vagina, posterior vaginal fornix, cervical mucus Upper reproductive tract samples: surgery (endometrial and peritoneal lavage) |
NGS Ion Torrent PGM: V4-V5 16S rRNA | Aim: study the flora distribution and bacterial community across the upper and lower reproductive tract Conclusion: shift in microbiota distribution starting from the cervical samples (microbiota in cervical samples as an indicator for the risk of endometriosis) and progressively increasing upward the reproductive tract, decreased Lactobacillus in lower tract, enriched Sphingobium sp. and Pseudomonas viridiflava in endometrium and peritoneal fluid |
Khan et al., 2021 [48] | Cases: 53 (21 untreated, 11 GnRHa, 15 LVFX, 6 LVFX+ GnRHa) Controls: 47 (11 untreated, 12 GnRHa, 10 LVFX, 14 LVFX+ GnRHa |
18–51 | Surgery and histology | Endometrial samples | NGS Illumina: V5-V6 16S rRNA Immunohistochimical analysis: Ab against CD138, CD68, Ki-67, and CD31 |
Aim: demonstrate the hypothesis that antibiotic treatment with or without GnRHa may decrease intrauterine infection with consequent decrease in tissue inflammation, cell proliferation and angiogenesis in human endometriosis Conclusion: Decreased Gardnerella, Prevotella, Acidibactor, Atopobium, Megasphaera, and Bradyrhizobium in patients with endometriosis in treatment with LVFX or LVFX + GnRHa, reduced occurrence rate of chronic endometritis after GnRHa + LVFX treatment comparison to GnRHa treatment group and decreased CD68, Ki-67, and CD31 |