Chronic endometritis and assisted reproduction: a systematic review and meta-analysis

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Assoc. Med. Bras. 69 (10) • 2023 • https://doi.org/10.1590/1806-9282.20230792 link copy Chronic endometritis and assisted reproduction: a systematic review and meta-analysis Authorship SCIMAGO INSTITUTIONS RANKINGS INTRODUCTION Chronic endometritis (CE) is defined as a localized inflammation signaled by the infiltration of bacteria in the endometrial stroma. It has adverse implications in human reproduction, including recurrent implantation failure (RIF) and recurrent miscarriage 1 – 3 . Chronic endometritis can be asymptomatic, and it can cause several changes in the uterus, namely, pain, bleeding, leukorrhea, and other complications. Its prevalence significantly varies and is dependent on several factors, including inflammation of the uterus and the presence of infectious bacteria in the endometrial stroma. The incidence ranges from 10% to approximately 57% according to several studies 4 – 10 . A brief summary of the pathophysiology of CE would include not only various bacteria that influence the entire endometrial microenvironment but also cytokine secretions that can induce leukocyte recruitment, which in turn influences the conditions (e.g., vascularity, uterine contractility, and endometrial function) for successful implantation after in vitro fertilization (IVF) 11 , 12 . Women with chronic endometritis have fertilization difficulties in assisted reproduction; therefore, treating the pathology is essential for improving the results of infertility and assisted reproduction treatments 13 – 15 . The objective of this study was to carry out a systematic review and meta-analysis of the literature on the subject of chronic endometritis and reproductive outcomes. METHODS For the systematic reviews, we used examples and guidelines by Arya et al. 16 , Hennessy et al. 17 , Berstock et al. 18 , and Page et al. 19 . The meta-analysis was conducted in accordance with the study by Dettori et al. 20 . Search strategy To identify the studies for inclusion in this review, we selected articles indexed in PubMed, Google Scholar, and SciELO and published from January 2012 to February 2023. First, we chose keywords from the related articles and used MeSH international data lines to find more related keywords with closer meanings, which included (“endometritis”) [MeSH Terms] [All Fields] AND (“assisted reproductive technologies”) [MeSH Terms] OR (“Infertility”) [MeSH Terms] [All Fields]. The search was carried out in the three databases. In PubMed, we found 91 articles with titles and abstracts worth reading. From SciELO, we extracted 15 articles, and from Google Scholar, we retrieved 47 ( Figure 1 ). Figure 1 Flowchart of the study. This review was conducted according to the recommendations established by Preferred Reporting Items for Systematic Reviews and Meta-Analysis Page et al. 19 . Inclusion and exclusion criteria Studies were included if they met the following criteria: English or Spanish or Portuguese language, in vitro models, theme relevance, and objectives consistent with those of this study (see the flowchart in Figure 1 ). There were 14 articles that met the inclusion criteria ( Figure 1 ). The eligibility steps shown in Figure 1 were independently tracked by two different authors (ECAV and JMSJ). In case of a disagreement or contradiction, a third author (MS) stepped in and repeated the search strategy. Five meta-analyses were conducted comparing women diagnosed with chronic endometritis (group CE) and control women (women without the presence of the disease) (group NO CE). Statistical analysis For descriptive statistics, the means, standard deviations, mean differences, and odds ratios with 95% of confidence interval were calculated. Meta-analysis was carried out with the Review Manager 5.4.1 software program (Cochrane Collaboration, Oxford, UK). For the values of 95%CI and “test for overall effect size,” values of p≤0.05 were assumed for significant differences 20 . RESULTS Results of meta-analyses The live birth rates of the two study groups were significantly different (p=0.004), meaning that women with no chronic endometritis had a higher rate of live births ( Figure 2 ). In other words, women who underwent IVF and were treated for their endometritis, thus falling into the NO CE group (without endometritis), had a higher rate of healthy live births than pregnant women with endometritis. Figure 2 Comparison of the meta-analysis with the outcome live birth rate. The clinical pregnancy rates of the two groups also differed statistically (p≤0.00001), that is, the group of women without endometritis had a higher pregnancy rate than women with inflammatory endometrium who availed themselves of assisted reproduction techniques ( Figure 3 ). Women with chronic endometritis had a higher rate of miscarriage and were statistically significant (p=0.0002) than the control participants. Hence, women with endometritis were found to have a greater number of miscarriages than women without comorbidity. As for maternal age, there was no statistical difference between the groups (p=0.66). Figure 3 Meta-analyses comparing the group of women with chronic endometritis by the number of participants unit (events and total) with the group of women without chronic endometritis with respect to the clinical pregnancy rate. All studies selected for this systematic review were at risk for bias and the details are shown in Supplementary Figure 1 . It was demonstrated that close to half of the seven domains recommended for analysis by Cochrane had an unclear risk of bias, that is, the study did not mention whether the risk of bias was present or not in the work; therefore, we regarded the lack of analysis of the risk of bias as a limitation of the study 21 . DISCUSSION The main findings were that women without endometritis have improved rates of clinical pregnancy and live birth. Our meta-analysis showed a significant improvement in the rates of live birth and clinical pregnancy in the group without chronic endometritis to be consistent with the literature. In the study by Cicinelli et al. 22 , the live birth rate was 60% in the group treated with a CE antibiotic compared with 13% in the group that went untreated after the IVF procedures, and the clinical pregnancy rate doubled when comparing the CE and the NO CE groups 22 . Other studies that corroborate our results include Yang et al. 23 and McQueen et al. 24 . More recent studies in the literature have also yielded similar results, including three meta-analyses, three analyses on women who suffered from RIF, and one study on a woman with recurrent pregnancy loss 3 , 25 – 27 . Mitter et al. 28 observed long-term recurrent pregnancy loss, including miscarriage, and found that women with chronic endometritis, whom they observed for years, were more likely to have such losses. Despite the limitations imposed by the small number of studies and events and the lack of heterogeneity, the results of our meta-analyses showed that the NO CE group had fewer miscarriages. In short, our results are in line with the literature in that CE therapy improves clinical pregnancy rate and the course of pregnancy of patients seeking IVF. Various studies are limited by methodological problems and lack of randomization 29 , 30 . Strengths and limitations of the study The strength of this study definitely lies in the positive results of the meta-analyses of the live birth and pregnancy rates. A limitation of this study is that, from the perspective of Cochrane’s methodology of the seven domains of risk of bias, which we followed, the authors’ analyses in most studies were incomplete, for they did not clarify whether there were any of those particular risks. In addition, the number of studies and the overall number of events and participants in the meta-analyses we performed were small. CONCLUSION Our study showed that women who do not have chronic endometritis have better reproductive outcomes such as better rates of live birth and clinical pregnancy. Funding: none. REFERENCES 1 Kitaya K, Takeuchi T, Mizuta S, Matsubayashi H, Ishikawa T. Endometritis: new time, new concepts. 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Available from: www.handbook.cochrane.org » www.handbook.cochrane.org 22 Cicinelli E, Matteo M, Tinelli R, Lepera A, Alfonso R, Indraccolo U, et al. Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy. Hum Reprod. 2015;30(2):323-30. https://doi.org/10.1093/humrep/deu292 » https://doi.org/10.1093/humrep/deu292 23 Yang R, Du X, Wang Y, Song X, Yang Y, Qiao J. The hysteroscopy and histological diagnosis and treatment value of chronic endometritis in recurrent implantation failure patients. Arch Gynecol Obstet. 2014;289(6):1363-9. https://doi.org/10.1007/s00404-013-3131-2 » https://doi.org/10.1007/s00404-013-3131-2 24 McQueen DB, Perfetto CO, Hazard FK, Lathi RB. Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss. Fertil Steril. 2015;104(4):927-31. https://doi.org/10.1016/j.fertnstert.2015.06.044 » https://doi.org/10.1016/j.fertnstert.2015.06.044 25 Vitagliano A, Saccardi C, Noventa M, Spiezio Sardo A, Saccone G, Cicinelli E, et al. Effects of chronic endometritis therapy on in vitro fertilization outcome in women with repeated implantation failure: a systematic review and meta-analysis. Fertil Steril. 2018;110(1):103-12.e1. https://doi.org/10.1016/j.fertnstert.2018.03.017 » https://doi.org/10.1016/j.fertnstert.2018.03.017 26 Cheng X, Huang Z, Xiao Z, Bai Y. Does antibiotic therapy for chronic endometritis improve clinical outcomes of patients with recurrent implantation failure in subsequent IVF cycles? A systematic review and meta-analysis. J Assist Reprod Genet. 2022;39(8):1797-813. https://doi.org/10.1007/s10815-022-02558-1 » https://doi.org/10.1007/s10815-022-02558-1 27 Li S, Zheng PS, Ma HM, Feng Q, Zhang YR, Li QS, et al. Systematic review of subsequent pregnancy outcomes in couples with parental abnormal chromosomal karyotypes and recurrent pregnancy loss. Fertil Steril. 2022;118(5):906-14. https://doi.org/10.1016/j.fertnstert.2022.08.008 » https://doi.org/10.1016/j.fertnstert.2022.08.008 28 Mitter VR, Meier S, Rau TT, Gillon T, Mueller MD, Zwahlen M, et al. Treatment following hysteroscopy and endometrial diagnostic biopsy increases the chance for live birth in women with chronic endometritis. Am J Reprod Immunol. 2021;86(5):e13482. https://doi.org/10.1111/aji.13482 » https://doi.org/10.1111/aji.13482 29 Song D, He Y, Wang Y, Liu Z, Xia E, Huang X, et al. Impact of antibiotic therapy on the rate of negative test results for chronic endometritis: a prospective randomized control trial. Fertil Steril. 2021;115(6):1549-56. https://doi.org/10.1016/j.fertnstert.2020.12.019 » https://doi.org/10.1016/j.fertnstert.2020.12.019 30 Cicinelli E, Cicinelli R, Vitagliano A. Antibiotic therapy for chronic endometritis and its reproductive implications: a step forward, with some uncertainties. Fertil Steril. 2021;115(6):1445-6. https://doi.org/10.1016/j.fertnstert.2021.03.025 » https://doi.org/10.1016/j.fertnstert.2021.03.025 Publication Dates Publication in this collection 13 Oct 2023 Date of issue 2023 History Received 23 June 2023 Accepted 09 July 2023 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Authorship .author-card { border-bottom: 1px solid #ccc; padding: 1rem 0; } .author-card:last-child { border-bottom: 0px; } .author-name { font-weight: 600; } .orcid-button { padding-left: 2.5rem; } .modal-body { padding-bottom: 3rem; } .orcid-button::before { content: ""; position: absolute; background-image: url(https://ds.scielo.org/img/logo-orcid.svg); background-repeat: no-repeat; background-size: 1.5em auto; background-position: .5em center; display: block; width: 60px; height: 60px; top: -10px; left: 0; } person Eduardo Carvalho de Arruda Veiga * Conceptualization · Formal Analysis · Investigation · Methodology · Validation · Visualization · Writing – original draft · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. school Universidade de São Paulo, Hospital das Clínicas, Faculdade de Medicina de Ribeirão Preto, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Universidade de São Paulo Brazil São Paulo, SP, Brazil Universidade de São Paulo, Hospital das Clínicas, Faculdade de Medicina de Ribeirão Preto, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. 0000-0002-0167-861X person Jose Maria Soares Junior Methodology · Validation · Visualization · Writing – original draft · Writing – review & editing school Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. Universidade de São Paulo Brazil Sao Paulo, Brazil Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. 0000-0003-0774-9404 person Marise Samama Visualization · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. school Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Universidade Federal de São Paulo Brazil São Paulo, SP, Brazil Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. 0000-0002-3732-1057 person Fabio Ikeda Visualization · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. 0009-0003-9644-7797 person Luciana Semião Francisco Validation · Visualization · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. 0009-0001-1025-9193 person Amanda Sartor Validation · Visualization · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. school Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Universidade Federal de São Paulo Brazil São Paulo, SP, Brazil Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. 0000-0002-0367-8787 person Lorena Ana Mercedes Lara Urbanetz Visualization · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. school Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. Universidade de São Paulo Brazil Sao Paulo, Brazil Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. 0000-0003-3572-6680 person Edmund Chada Baracat Visualization · Writing – review & editing school Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. Universidade de São Paulo Brazil Sao Paulo, Brazil Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. 0000-0003-0111-9030 person Joji Ueno Conceptualization · Formal Analysis · Investigation · Methodology · Validation · Visualization · Writing – original draft · Writing – review & editing school GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. 0000-0002-5469-3688 person * Corresponding author: email [email protected] Conflicts of interest: the authors declare there is no conflicts of interest. SCIMAGO INSTITUTIONS RANKINGS GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo Brazil São Paulo, SP, Brazil GERA Instituto de Ensino e Pesquisa de Medicina Reprodutiva de São Paulo – São Paulo (SP), Brazil. Universidade de São Paulo, Hospital das Clínicas, Faculdade de Medicina de Ribeirão Preto, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Universidade de São Paulo Brazil São Paulo, SP, Brazil Universidade de São Paulo, Hospital das Clínicas, Faculdade de Medicina de Ribeirão Preto, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. Universidade de São Paulo Brazil Sao Paulo, Brazil Laboratório de Ginecologia Estrutural e Molecular (LIM-58), Disciplina de Ginecologia, Departamento de Obstetrícia e Ginecologia, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – Sao Paulo, Brazil. Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Universidade Federal de São Paulo Brazil São Paulo, SP, Brazil Universidade Federal de São Paulo, Escola Paulista de Medicina, Departamento de Obstetrícia e Ginecologia – São Paulo (SP), Brazil. Figures Figures (3) Thumbnail Figure 1 Flowchart of the study. Thumbnail Figure 2 Comparison of the meta-analysis with the outcome live birth rate. Thumbnail Figure 3 Meta-analyses comparing the group of women with chronic endometritis by the number of participants unit (events and total) with the group of women without chronic endometritis with respect to the clinical pregnancy rate. image Figure 1 Flowchart of the study. open_in_new image Figure 2 Comparison of the meta-analysis with the outcome live birth rate. open_in_new image Figure 3 Meta-analyses comparing the group of women with chronic endometritis by the number of participants unit (events and total) with the group of women without chronic endometritis with respect to the clinical pregnancy rate. open_in_new How to cite link copy function currentDate() { var today = new Date(); var months = ['January', 'February', 'March', 'April', 'May', 'June', 'July', 'August', 'September', 'October', 'November', 'December'] today.setTime(today.getTime()); return today.getDate() + " " + months[today.getMonth()] + " " + today.getFullYear(); } var citation = 'Veiga, Eduardo Carvalho de Arruda et al. Chronic endometritis and assisted reproduction: a systematic review and meta-analysis. Revista da Associação Médica Brasileira [online]. 2023, v. 69, n. 10 [Accessed CURRENTDATE], e20230792. Available from: . Epub 13 Oct 2023. ISSN 1806-9282. https://doi.org/10.1590/1806-9282.20230792.'.replace('CURRENTDATE', currentDate()); document.getElementById('citation').innerHTML = citation; document.getElementById('citationCut').value = citation.replace('<', ' "); more_horiz Ferramentas do artigo file_download PDFs show_chart Metrics image Figuras e tabelas translate Versions and translations link How to cite this article article Related articles location_on Associação Médica Brasileira R. 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