Modern aspects of pathophysiology, diagnosis and treatment of chronic endometritis
Tabeeva G.I., Elovenko A.A., Dumanovskaya M.R., Asaturova A.V., Kuzemin A.A.
Chronic endometritis is a chronic inflammatory disease of the endometrium characterized by the presence of plasma cells in the endometrial stroma. The prevalence of this condition can vary, but its diagnosis presents significant challenges. These challenges are due to the non-specificity of its clinical symptoms, as well as the absence of unambiguous criteria for diagnosis. In addition, there is a lack of clinical guidelines in medical practice regarding the management of patients with this pathology. All these factors led to a detailed analysis of the currently available literature on chronic endometritis. This review provides key information that covers various aspects of this disease, including its etiology, pathogenesis, and approaches to diagnosis and treatment. The focus of this study is to examine the etiological factors of chronic endometritis. These include the colonization of various microorganisms and the release of endogenous molecules during endometrial trauma and ischemia. These factors lead to aberrant activation of innate immunity, alteration of immunocompetent cells, and increased production and release of inflammatory cytokines. The article presents the findings of studies conducted to evaluate the efficacy of various antibiotic regimens in the treatment of chronic endometritis. The results of other treatments, such as intrauterine infusion of autologous platelet-rich plasma and the use of lactoferrin, are also described. The review pays special attention to the current literature data on molecular biological markers (inflammasomes, extracellular vesicles, etc.) that play an important role in the pathogenesis of the disease. These markers have the potential to be promising tools for the diagnosis of chronic endometritis and the development of innovative therapeutic approaches in the future.
Conclusion: This review highlights the need to study chronic endometritis and its molecular mechanisms, which may open new horizons to improve the diagnosis and treatment of this pathological condition.
Authors’ contributions: Tabeeva G.I. – developing the concept and design of the review; Tabeeva G.I., Elovenko A.A. – writing the text; Dumanovskaya M.R., Asaturova A.V., Kuzemin A.A. – editing the article.
Conflicts of interest: The authors declare no possible conflicts of interest.
Funding: The study was carried out within the framework of State Assignment to the Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology (№122020900122-7).
For citation: Tabeeva G.I., Elovenko A.A., Dumanovskaya M.R., Asaturova A.V., Kuzemin A.A.
Modern aspects of pathophysiology, diagnosis and treatment of chronic endometritis.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2024; (11): 12-20 (in Russian)
https://dx.doi.org/10.18565/aig.2024.223
Keywords
References
- Vitagliano A., Saccardi C., Noventa M., Di 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): 103-112.e1. https://dx.doi.org/10.1016/j.fertnstert.2018.03.017.
- Зефирова Т.П., Садыкова Д.А., Дзамуков Р.А., Толибова Г.Х., Гусев В.И., Евсегнеева И.В. Новый взгляд на причины репродуктивных неудач у женщин с хроническим эндометритом. Акушерство и гинекология. 2024; 9: 156-62. [Zefirova T.P., Sadykova D.A., Dzamukov R.A., Tolibova G.Kh., Gusev V.I., Evsegneeva I.V. A new perspective on the causes of reproductive failure in women with chronic endometritis. Obstetrics and Gynecology. 2024; (9): 156-62. (in Russian)]. https://dx.doi.org/10.18565/aig.2024.237.
- Paavonen J., Aine R., Teisala K., Heinonen P.K., Punnonen R., Lehtinen M. et al. Chlamydial endometritis. J. Clin. Pathol. 1985; 38(7): 726-32. https://dx.doi.org/10.1136/jcp.38.7.726.
- Cicinelli E., Trojano G., Mastromauro M., Vimercati A., Marinaccio M., Mitola P.C. et al. Higher prevalence of chronic endometritis in women with endometriosis: a possible etiopathogenetic link. Fertil. Steril. 2017; 108(2):289-295.e1. https://dx.doi.org/10.1016/j.fertnstert.2017.05.016.
- Song D., Feng X., Zhang Q., Xia E., Xiao Y., Xie W. et al. Prevalence and confounders of chronic endometritis in premenopausal women with abnormal bleeding or reproductive failure. Reprod. Biomed. Online. 2018; 36(1): 78-83. https://dx.doi.org/10.1016/j.rbmo.2017.09.008.
- Kimura F., Takebayashi A., Ishida M., Nakamura A., Kitazawa J., Morimune A. et al. Review: chronic endometritis and its effect on reproduction. J. Obstet. Gynaecol. Res. 2019; 45(5): 951-60. https://dx.doi.org/10.1111/jog.13937.
- Тихончук Е.Ю., Асатурова А.В., Адамян Л.В. Частота выявления и структура патологических изменений эндометрия у женщин репродуктивного возраста с генитальным эндометриозом. Акушерство и гинекология. 2016; 12: 87-95. [Tikhonchuk E.Yu., Asaturova A.V., Adamyan L.V. The detection rate and the structure of pathological changes of the endometrium in women of reproductive age with endometriosis. Obstetrics and Gynecology. 2016; (12): 87-95. (in Russian)]. https://dx.doi.org/10.18565/aig.2016.12.87-95.
- Qu D., Liu Y., Zhou H., Wang Z. Chronic endometritis increases the recurrence of endometrial polyps in premenopausal women after hysteroscopic polypectomy. BMC Womens Health. 2023; 23(1): 88. https://dx.doi.org/10.1186/s12905-023-02232-3.
- Kabodmehri R., Etezadi A., Sharami S.H., Ghanaei M.M., Hosseinzadeh F., Heirati S.F.D. et al. The association between chronic endometritis and uterine fibroids. J. Family Med. Prim. Care. 2022; 11(2): 653-9. https://dx.doi.org/10.4103/jfmpc.jfmpc_1470_21.
- Fardini Y., Chung P., Dumm R., Joshi N., Han Y.W. Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect. Immun. 2010; 78(4): 1789-96. https://dx.doi.org/10.1128/IAI.01395-09.
- Chen C., Song X., Wei W., Zhong H., Dai J., Lan Z. et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat. Commun. 2017; 8(1): 875. https://dx.doi.org/10.1038/s41467-017-00901-0.
- Moreno I., Cicinelli E., Garcia-Grau I., Gonzalez-Monfort M., Bau D., Vilella F. et al. The diagnosis of chronic endometritis in infertile asymptomatic women: a comparative study of histology, microbial cultures, hysteroscopy, and molecular microbiology. Am. J. Obstet. Gynecol. 2018; 218(6): 602.e1-602.e16. https://dx.doi.org/10.1016/j.ajog.2018.02.012.
- D’lppolito S., Tersigni C., Marana R., Di Nicuolo F., Gaglione R., Rossi E.D. et al. Inflammosome in the human endometrium: further step in the evaluation of the “maternal side”. Fertil. Steril. 2016; 105(1): 111-8.e1-4. https://dx.doi.org/10.1016/j.fertnstert.2015.09.027.
- Puente E., Alonso L., Laganà A.S., Ghezzi F., Casarin J., Carugno J. Chronic endometritis: old problem, novel insights and future challenges. Int. J. Fertil. Steril. 2020; 13(4): 250-6. https://dx.doi.org/10.22074/ijfs.2020.5779.
- Тапильская Н.И., Будиловская О.В., Крысанова А.А., Толибова Г.Х., Копылова А.А., Цыпурдеева Н.Д., Гзгзян А.М., Савичева А.М., Коган И.Ю. Микробиота эндометрия женщин с хроническим эндометритом и идиопатическим бесплодием. Акушерство и гинекология. 2020; 4: 72-81. [Tapil’skaya N.I., Budilovskaya O.V., Krysanova A.A.,
- Tolibova G.Kh., Kopylova A.A., Tsypurdeeva N.D., Gzgzyan A.M., Savicheva A.M., Kogan I.Yu. Еndometrial microbiota of women with chronic endometritis and idiopathic infertility. Obstetrics and Gynecology. 2020; (4): 72-81. (in Russian)]. https://dx.doi.org/10.18565/aig.2020.4.72-81.
- Li Y., Yu S., Huang C., Lian R., Chen C., Liu S. et al. Evaluation of peripheral and uterine immune status of chronic endometritis in patients with recurrent reproductive failure. Fertil. Steril. 2020; 113(1): 187-196.e1. https://dx.doi.org/10.1016/j.fertnstert.2019.09.001.
- Маринкин И.О., Трунченко Н.В., Волчек А.В., Агеева Т.А., Никитенко Е.В., Макаров К.Ю., Кулешов В.М., Омигов В.В., Айдагулова С.В. Маркеры воспаления в нормальном и тонком эндометрии при хроническом эндометрите. Акушерство и гинекология. 2018; 2: 65-73. [Marinkin I.O., Trunchenko N.V., Volchek A.V., Ageeva T.A., Nikitenko E.V.,
- Makarov K.Yu., Kuleshov V.M., Omigov V.V., Aidagulova S.V. Inflammatory markers in the normal and thin endometrium in chronic endometritis. Obstetrics and Gynecology. 2018; (2): 65-73. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.2.65-73.
- Pirtea P., Cicinelli E., De Nola R., de Ziegler D., Ayoubi J.M. Endometrial causes of recurrent pregnancy losses: endometriosis, adenomyosis, and chronic endometritis. Fertil. Steril. 2021; 115(3): 546-60. https://dx.doi.org/10.1016/j.fertnstert.2020.12.010.
- Buzzaccarini G., Vitagliano A., Andrisani A., Santarsiero C.M., Cicinelli R., Nardelli C. et al. Chronic endometritis and altered embryo implantation: a unified pathophysiological theory from a literature systematic review. J. Assist. Reprod. Genet. 2020; 37(12): 2897-911. https://dx.doi.org/10.1007/s10815-020-01955-8.
- Mangan M.S.J., Olhava E.J., Roush W.R., Seidel H.M., Glick G.D., Latz E. Targeting the NLRP3 inflammasome in inflammatory diseases. Nat. Rev. Drug Discov. 2018; 17(8): 588-606. https://dx.doi.org/10.1038/nrd.2018.97.
- Табеева Г.И., Думановская М.Р., Асатурова А.В., Богданова И.М., Саная С.З., Трегубова А.В. Особенности регуляции и функции инфламмасом при воспалительных заболеваниях органов женской репродуктивной системы. Клиническая и экспериментальная морфология. 2020; 9(3): 12-20. [Tabeeva G.I., Dumanovskaya M.R., Asaturova A.V., Bogdanova I.M., Sanaya S.Z., Tregubova A.V. Features of regulation and function of inflammasomes in inflammatory diseases of the female reproductive system. Clinical and Experimental Morphology. 2020; 9(3): 12-20. (in Russian)]. https://dx.doi.org/10.31088/CEM2020.9.3.12-20.
- Han J.H., Park J., Kang T.B., Lee K.H. Regulation of Caspase-8 activity at the crossroads of pro-inflammation and anti-inflammation. Int. J. Mol. Sci. 2021; 22(7): 3318. https://dx.doi.org/10.3390/ijms22073318.
- Табеева Г.И., Трегубова А.В., Асатурова А.В., Думановская М.Р., Магнаева А.С., Сметник А.А., Павлович С.В. Экспрессия маркеров апоптоза NF-kB, Bcl2 и Caspase-8 в эндометрии при наружном генитальном эндометриозе и хроническом эндометрите. Гинекология. 2023; 25(2): 158-63. [Tabeeva G.I., Tregubova A.V., Asaturova A.V., Dumanovskaya M.R., Magnaeva A.S., Smetnik A.A., Pavlovich S.V. Expression of NF-kB, Bcl2 and Caspase-8 apoptosis markers in endometrium in external genital endometriosis and chronic endometritis: a retrospective study. Gynecology. 2023; 25(2): 158-63. (in Russian)]. https://dx.doi.org/10.26442/20795696.2023.2.202003.
- Shih A.J., Adelson R.P., Vashistha H., Khalili H., Nayyar A., Puran R. et al. Single-cell analysis of menstrual endometrial tissues defines phenotypes associated with endometriosis. BMC Med. 2022; 20(1): 315. https://dx.doi.org/10.1186/s12916-022-02500-3.
- Казачков Е.Л., Затворницкая А.В., Воропаева Е.Е., Казачкова Э.А., Щеголев А.И. Особенности пролиферативной и антипролиферативной активности клеток эндометрия при его гиперплазии в сочетании с хроническим эндометритом. Акушерство и гинекология. 2019; 8: 100-6. [Kazachkov E.L., Zatvornitskaya A.V., Voropaeva E.E., Kazachkova E.A., Shchegolev A.I. Characteristics of the proliferative and antiproliferative activities of the cells of the endometrium in its hyperplasia concurrent with chronic endometritis. Obstetrics and Gynecology. 2019; (8): 100-6 (in Russian)]. https://dx.doi.org/10.18565/aig.2019.8.100-106.
- Bouic P.J. Endometriosis and infertility: the hidden link between endometritis, hormonal imbalances and immune dysfunctions preventing implantation! JBRA Assist. Reprod. 2023; 27(2): 144-6. https://dx.doi.org/10.5935/1518-0557.20230015.
- Министерство здравоохранения Российской Федерации. Клинические рекомендации. Воспалительные болезни женских тазовых органов. 2024. [Ministry of Health of the Russian Federation. Clinical guidelines. Inflammatory diseases of the female pelvic organs. 2024. (in Russian)].
- Gilmore H., Fleischhacker D., Hecht J.L. Diagnosis of chronic endometritis in biopsies with stromal breakdown. Hum. Pathol. 2007; 38(4): 581-4. https://dx.doi.org/10.1016/j.humpath.2006.09.002.
- Espinós J.J., Fabregues F., Fontes J., García-Velasco J.A., Llácer J., Requena A. et al.; Spanish Infertility SWOT Group (SISG). Impact of chronic endometritis in infertility: a SWOT analysis. Reprod. Biomed. Online. 2021; 42(5): 939-51. https://dx.doi.org/10.1016/j.rbmo.2021.02.003.
- Kitaya K., Yasuo T. Immunohistochemistrical and clinicopathological characterization of chronic endometritis. Am. J. Reprod. Immunol. 2011; 66(5): 410-5. https://dx.doi.org/10.1111/j.1600-0897.2011.01051.x.
- Bouet P.E., El Hachem H., Monceau E., Gariépy G., Kadoch I.J., Sylvestre C. Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis. Fertil. Steril. 2016; 105(1): 106-10. https://dx.doi.org/10.1016/j.fertnstert.2015.09.025.
- Kitaya K., Yasuo T. Inter-observer and intra-observer variability in immunohistochemical detection of endometrial stromal plasmacytes in chronic endometritis. Exp. Ther. Med. 2013; 5(2): 485-8. https://dx.doi.org/10.3892/etm.2012.824.
- Li Y., Xu S., Yu S., Huang C., Lin S., Chen W. et al. Diagnosis of chronic endometritis: how many CD138+ cells/HPF in endometrial stroma affect pregnancy outcome of infertile women? Am. J. Reprod. Immunol. 2021; 85(5): e13369. https://dx.doi.org/10.1111/aji.13369.
- Huang W., Liu B., He Y., Xie Y., Liang T., Bi Y. et al. Variation of diagnostic criteria in women with chronic endometritis and its effect on reproductive outcomes: a systematic review and meta-analysis. J. Reprod. Immunol. 2020; 140: 103146. https://dx.doi.org/10.1016/j.jri.2020.103146.
- Santoro A., Travaglino A., Inzani F., Angelico G., Raffone A., Maruotti G.M. et al. The role of plasma cells as a marker of chronic endometritis: a systematic review and meta-analysis. Biomedicines. 2023; 11(6): 1714. https://dx.doi.org/10.3390/biomedicines11061714.
- Adegboyega P.A., Pei Y., McLarty J. Relationship between eosinophils and chronic endometritis. Hum. Pathol. 2010; 41(1): 33-7. https://dx.doi.org/10.1016/j.humpath.2009.07.008.
- Ryan E., Tolani A.T., Zhang J., Cruz G.I., Folkins A.K., Lathi R.B. The menstrual cycle phase impacts the detection of plasma cells and the diagnosis of chronic endometritis in endometrial biopsy specimens. Fertil. Steril. 2022; 118(4):787-94. https://dx.doi.org/10.1016/j.fertnstert.2022.07.011.
- Park H.J., Kim Y.S., Yoon T.K., Lee W.S. Chronic endometritis and infertility. Clin. Exp. Reprod. Med. 2016; 43(4): 185-92. https://dx.doi.org/10.5653/cerm.2016.43.4.185.
- Bayer-Garner I.B., Nickell J.A., Korourian S. Routine syndecan-1 immunohistochemistry aids in the diagnosis of chronic endometritis. Arch. Pathol. Lab. Med. 2004; 128(9): 1000-3. https://dx.doi.org/10.5858/2004-128-1000-RSIAIT.
- Асатурова А.В., Бадлаева А.С., Трегубова А.В., Табеева Г.И. Воспроизводимость диагностики хронического эндометрита до и после применения иммуногистохимического исследования плазматических клеток в эндометрии. Новости клинической цитологии России. 2023; 27(1): 5-10. [Asaturova A.V., Badlaeva A.S., Tregubova A.V., Tabeeva G.I. Reproducibility of diagnostics of chronic endometritis before and after the use of immunohistochemical examination of plasma cells in the endometrium. Russian News of Clinical Cytology. 2023; 27(1): 5-10. (in Russian)]. https://dx.doi.org/10.24412/1562-4943-2023-1-0001.
- Chen Y.Q., Fang R.L., Luo Y.N., Luo C.Q. Analysis of the diagnostic value of CD138 for chronic endometritis, the risk factors for the pathogenesis of chronic endometritis and the effect of chronic endometritis on pregnancy: a cohort study. BMC Womens Health. 2016; 16(1): 60. https://dx.doi.org/10.1186/s12905-016-0341-3.
- Cicinelli E., Haimovich S., De Ziegler D., Raz N., Ben-Tzur D., Andrisani A. et al.; International Working Group for Standardization of Chronic Endometritis Diagnosis. MUM-1 immunohistochemistry has high accuracy and reliability in the diagnosis of chronic endometritis: a multi-centre comparative study with CD-138 immunostaining. J. Assist. Reprod. Genet. 2022; 39(1): 219-26. https://dx.doi.org/10.1007/s10815-021-02356-1.
- Parks R.N., Kim C.J., Al-Safi Z.A., Armstrong A.A., Zore T., Moatamed N.A. Multiple myeloma 1 transcription factor is superior to CD138 as a marker of plasma cells in endometrium. Int. J. Surg. Pathol. 2019; 27(4): 372-9. https://dx.doi.org/10.1177/1066896918814307.
- Xiong Z., Zhang W., Liu S., Liu K., Wang J., Qin P. et al. The combination of CD138/MUM1 dual-staining and artificial intelligence for plasma cell counting in the diagnosis of chronic endometritis. Am. J. Reprod. Immunol. 2023; 89(3): e13671. https://dx.doi.org/10.1111/aji.13671.
- Асатурова А.В., Табеева Г.И., Магнаева А.С., Трегубова А.В. Диагностика хронического эндометрита с помощью оценки плазматических клеток в строме эндометрия: настоящее и будущее. Обзор литературы. Лаборатория и клиническая медицина. Фармация. 2023; 3(4): 49-57. [Asaturova A.V., Tabeeva G.I., Magnaeva A.S., Tregubova A.V. Chronic endoemtritis diagnosis with plasma cells detection: present and future. Review. Laboratory and Clinical Medicine. Pharmacy. 2023; 3(4): 49-57. (in Russian)]. https://dx.doi.org/10.14489/lcmp.2023.04.pp.049-057.
- Chen P., Chen P., Guo Y., Fang C., Li T. Interaction between chronic endometritis caused endometrial microbiota disorder and endometrial immune environment change in recurrent implantation failure. Front. Immunol. 2021; 12: 748447. https://dx.doi.org/10.3389/fimmu.2021.748447.
- Chen W., Wei K., He X., Wei J., Yang L., Li L. et al. Identification of uterine microbiota in infertile women receiving in vitro fertilization with and without chronic endometritis. Front. Cell Dev. Biol. 2021; 9: 693267. https://dx.doi.org/10.3389/fcell.2021.693267.
- Liang J., Li M., Zhang L., Yang Y., Jin X., Zhang Q. et al. Analysis of the microbiota composition in the genital tract of infertile patients with chronic endometritis or endometrial polyps. Front. Cell. Infect. Microbiol. 2023; 13: 1125640. https://dx.doi.org/10.3389/fcimb.2023.1125640.
- Molina N.M., Sola-Leyva A., Haahr T., Aghajanova L., Laudanski P., Castilla J.A. et al. Analysing endometrial microbiome: methodological considerations and recommendations for good practice. Hum. Reprod. 2021; 36(4): 859-79. https://dx.doi.org/10.1093/humrep/deab009.
- Tanaka S.E., Sakuraba Y., Kitaya K., Ishikawa T. Differential vaginal microbiota profiling in lactic-acid-producing bacteria between infertile women with and without chronic endometritis. Diagnostics (Basel). 2022; 12(4): 878. https://dx.doi.org/10.3390/diagnostics12040878.
- Демидов В.Н., Демидов Б.С., Марченко Л.А. Эхографические критерии хронического эндометрита. Ультразвуковая диагностика в акушерстве, гинекологии и педиатрии. 1993; 4: 21-7. [Demidov V.N., Demidov B.S., Marchenko L.A. Echographic criteria for chronic endometritis. Ultrasound Diagnosis in Obstetrics, Gynecology and Pediatrics. 1993; (4): 21-7.(in Russian)].
- Dalby J., Stoner B.P. Sexually transmitted infections: updates from the 2021 CDC Guidelines. Am. Fam. Physician. 2022; 105(5): 514-20.
- Kitaya K., Matsubayashi H., Takaya Y., Nishiyama R., Yamaguchi K., Takeuchi T. et al. Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. Am. J. Reprod. Immunol. 2017; 78(5): e12719. https://dx.doi.org/10.1111/aji.12719.
- Cicinelli E., Resta L., Loizzi V., Pinto V., Santarsiero C., Cicinelli R. et al. Antibiotic therapy versus no treatment for chronic endometritis: a case-control study. Fertil. Steril. 2021; 115(6): 1541-8. https://dx.doi.org/10.1016/j.fertnstert.2021.01.018.
- Luncan M., Huniadi A., Bimbo-Szuhai E., Botea M., Zaha I., Stefan L. et al. The effectiveness of intrauterine antibiotic infusion versus oral antibiotic therapy in the treatment of chronic endometritis in patients during IVF (in vitro fertilization) procedures. BMC Womens Health. 2022; 22(1): 529. https://dx.doi.org/10.1186/s12905-022-02128-8.
- Qu D., Yang M., Tong L., Yu X., Jing Q., Yang Y. et al. Combination of dydrogesterone and antibiotic versus antibiotic alone for chronic endometritis: a randomized controlled trial study. Reprod. Sci. 2021; 28(11): 3073-80. https://dx.doi.org/10.1007/s43032-021-00583-6.
- Vitagliano A., Saccardi C., Noventa M., Di 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): 103-112.e1. https://dx.doi.org/10.1016/j.fertnstert.2018.03.017.
- Li J., Li X., Ding J., Zhao J., Chen J., Guan F. et al. Analysis of pregnancy outcomes in patients with recurrent implantation failure complicated with chronic endometritis. Front. Cell Dev. Biol. 2023; 11: 1088586. https://dx.doi.org/10.3389/fcell.2023.1088586.
- Sfakianoudis K., Simopoulou M., Nitsos N., Lazaros L., Rapani A., Pantou A. et al. Successful implantation and live birth following autologous platelet-rich plasma treatment for a patient with recurrent implantation failure and chronic endometritis. In vivo. 2019; 33(2): 515-21. https://dx.doi.org/10.21873/invivo.11504.
- Nakamura A., Kimura F., Tsuji S., Hanada T., Takebayashi A., Takahashi A. et al. Bovine lactoferrin suppresses inflammatory cytokine expression in endometrial stromal cells in chronic endometritis. J. Reprod. Immunol. 2022; 154: 103761. https://dx.doi.org/10.1016/j.jri.2022.103761.
- You S., Zhu Y., Li H., He F., Liu S., Yang X. et al. Recombinant humanized collagen remodels endometrial immune microenvironment of chronic endometritis through macrophage immunomodulation. Regen. Biomater. 2023; 10: rbad033. https://dx.doi.org/10.1093/rb/rbad033.
- Wang B., Li L., Yu R. Exosomes from adipose-derived stem cells suppress the progression of chronic endometritis. Cell Transplant. 2023; 32: 9636897231173736. https://dx.doi.org/10.1177/09636897231173736.
- Xue J., Liu J., Xu B., Yu J., Zhang A., Qin L. et al. miR-21-5p inhibits inflammation injuries in LPS-treated H9c2 cells by regulating PDCD4. Am. J. Transl. Res. 2021; 13(10): 11450-60.
- Pan Y.Q., Li J., Li X.W., Li Y.C., Li J., Lin J.F. Effect of miR-21/TLR4/NF-κB pathway on myocardial apoptosis in rats with myocardial ischemia-reperfusion. Eur. Rev. Med. Pharmacol. Sci. 2018; 22(22): 7928-37. https://dx.doi.org/10.26355/eurrev_201811_16420.
- Zhao C., Li J., Cai H., Wu D., Tao S., Pi C. et al. An injectable hydrogel scaffold with IL-1β-activated MSC-derived exosomes for the treatment of endometritis. Biomater. Sci. 2023; 11(4): 1422-36. https://dx.doi.org/10.1039/d2bm01586b.
- Wu H., Dai A., Chen X., Yang H., Li X., Huang C. et al. Leonurine ameliorates the inflammatory responses in lipopolysaccharide-induced endometritis. Int. Immunopharmacol. 2018; 61: 156-61. https://dx.doi.org/10.1016/j.intimp.2018.06.002.
Received 06.09.2024
Accepted 29.10.2024
About the Authors
Gyuzyal I. Tabeeva, PhD, Senior Researcher, Department of Gynecological Endocrinology, V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, 4, Oparina str., Moscow, 117997, Russia, +7(903)199-72-82, g_tabeeva@oparina4.ru, https://orcid.org/0000-0003-1498-6520Alina A. Elovenko, Resident, V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia,
4, Oparina str., Moscow, 117997, Russia, alina.elovenko@gmail.com
Madina R. Dumanovskaya, PhD, Senior Researcher, Department of Gynecological Endocrinology, V.I. Kulakov National Medical Research Center of Obstetrics,
Gynecology and Perinatology, Ministry of Health of Russia, 4, Oparina str., Moscow, 117997, Russia, dumanovskaya@gmail.com, https://orcid.org/0000-0001-7286-6047
Alexandra V. Asaturova, Dr. Med. Sci., Head of the 1st Pathological Anatomy Department, V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, 4, Oparina str., Moscow, 117997, Russia, a_asaturova@oparina4.ru, https://orcid.org/0000-0001-8739-5209
Andrey A. Kuzemin, PhD, Head of the Day Hospital, V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, 4, Oparina str., Moscow, 117997, Russia, a_kuzemin@oparina4.ru, https://orcid.org/0000-0002-7559-0629
Corresponding author: Gyuzyal I. Tabeeva, g_tabeeva@oparina4.ru