Rina U. Mitrelis , Liudmila M. Mikhaleva , Mekan R. Orazov , Sergey A. Mikhalev , Tatyana Yu. Kobyzeva
Abstract
Abnormal uterine bleeding (AUB), common in a cohort of women in the reproductive period, is undoubtedly an extremely important factor reducing quality of life. Persistent endometrial inflammation is a pathogenetic link associated with endometrial dysfunction. The article reflects the modern paradigm of etiology, pathogenesis and management of patients with AUB on the background of chronic endometritis according to the data of domestic and foreign literature.
Keywords: abnormal uterine bleeding, chronic endometritis, endometrial dysfunction.
About the Author
Rina U. Mitrelis 1 , Liudmila M. Mikhaleva 2 , Mekan R. Orazov 3 , Sergey A. Mikhalev 4 , Tatyana Yu. Kobyzeva 51 Research Institute of Human Morphology named after Academician A.P. Avtsyna – Russian Scientific Centre of Surgery named after Academi- cian B.V. Petrovsky, Moscow, Russia; OJSC "Treatment Centre", Moscow, Russia;
2 Research Institute of Human Morphology named after Academician A.P. Avtsyna – Russian Scientific Centre of Surgery named after Academi- cian B.V. Petrovsky, Moscow, Russia; Municipal Clinical Hospital No. 31 named after Academician G.M. Savelyeva of the M
3 People’s Friendship University of Russia (RUDN University), Moscow, Russia;
4 Municipal Clinical Hospital No. 31 named after Academician G.M. Savelyeva of the Moscow City Health Department, Moscow, Russia; Pirogov National Medical and Surgical Centre, Moscow, Russia;
5 Research Institute of Human Morphology named after Academician A.P. Avtsyna – Russian Scientific Centre of Surgery named after Academi- cian B.V. Petrovsky, Moscow, Russia;
References
1. Munro MG, Critchley HOD, Fraser IS. The two FIGO systems for normal and abnormal uterine bleeding symptoms and classification of causes of abnormal uterine bleeding in the reproductive years: 2018 revisions. International Journal of Gynecology and Obstetrics. 2018;143(3):393-408. DOI: 10.1002/ijgo.12666
2. Sun Y, Wang Y, Mao L et al. Prevalence of abnormal uterine bleeding according to new International Federation of Gynecology and Obstetrics classification in Chinese women of reproductive age: A cross-sectional study. Medicine (Baltimore). 2018;97(31):e11457. DOI: 10.1097/MD.0000000000011457
3. Kazemijaliseh H, Tehrani FR, Beh- boudi-Gandevani S et al. A Population-Based Study of the Prevalence of Abnormal Uterine Bleeding and its Related Factors among Iranian Reproductive-Age Women: An Updated Data. Archives of Iranian Medicine. 2017;20(9):558-63.
4. Lee JHS, Cheng EOL, Choi KM et al. Hong Kong College of Obstetricians and Gynaecologists guideline on investigations of premenopausal women with abnormal uterine bleeding. Hong Kong Medical Journal. 2020;26(6):520-5. DOI: 10.12809/hkmj208897
5. Lam C, Anderson B, Lopes V et al. Assessing Abnormal Uterine Bleeding: Are Physicians Taking a Meaningful Clinical History? Journal of Women’s Health. 2017;26(7):762-7. DOI: 10.1089/jwh.2016.6155
6. Maqbool R, Maqbool M, Zehravi M et al. Menstrual distress in females of reproductive age: a literature review. International Journal of Adolescent Medicine and Health. 2021;34(2):11-7. DOI: 10.1515/ijamh-2021-0081
7. A Clinicopathological Correlation of International Federation of Gynecology and Obstetrics’s PALM–COEIN Classification of Abnormal Uterine Bleeding. Journal of Mid-Life Health. 2019;10(3):147-52. DOI: 10.4103/jmh.JMH_128_18
8. Darville TJ. Pelvic Inflammatory Disease Due to Neisseria gonorrhoeae and Chlamydia trachomatis: Immune Evasion Mechanisms and Pathogenic Disease Pathways. Infect Dis. 2021;224(12 Suppl. 2):S39-S46. DOI: 10.1093/infdis/jiab031. PMID: 34396413
9. Chen Y, Zheng S, Zhao X et al. Unveiling the protective effects of BMSCs/anti-miR-124-3p exosomes on LPS-induced endometrial injury. Funct Integr Genomics. 2024;24(2):32. DOI: 10.1007/s10142-024-01303-4. PMID: 38363406
10. 2021 exceptional surveillance of heavy menstrual bleeding: assessment and management (NICE guideline NG88). London: National Institute for Health and Care Excellence (NICE); 2021.
11. Hapangama DK, Bulmer JN. Pathophysiology of heavy menstrual bleeding. Women’s Health. 2015;12(1):3-13 DOI: 10.2217/whe.15.81
12. Uglietti A, Buggio L, Farella M et al. The risk of malignancy in uterine polyps: A systematic review and meta-analysis. European Journal of Obstetrics, Gynecology and Reproductive Biology. 2019;237:48-56. DOI: 10.1016/j.ejogrb.2019.04.009
13. Peres GF, Spadoto-Dias D, Bueloni-Dias FN et al. Immunohistochemical expression of hormone receptors, Ki-67, endoglin (CD105), claudins 3 and 4, MMP-2 and -9 in endometrial polyps and endometrial cancer type I. OncoTargets and Therapy. 2018;11:3949-58. DOI: 10.2147/ OTT.S160014
14. Harmsen MJ, Wong CFC, Mijatovic V. Role of angiogenesis in adenomyosis associated abnormal uterine bleeding and subfertility: a systematic review. Human Reproduction Update. 2019;25(5):647-71. DOI: 10.1093/humupd/dmz024
15. Stratopoulou CA, Donnez J, Dolmans MM. Origin and Pathogenic Mechanisms of Uter- ine Adenomyosis: What Is Known So Far. Reproductive Sciences. 2021; 28:2087-97. DOI: 10.1007/s43032-020-00361-w
16. Bazot M, Darai E. Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertility and Sterility. 2018;109(3):389-97. DOI: 10.1016/j.fertnstert.2018.01.024
17. Taylor HS, Kotlyar AM, Flores VA. Endometriosis is a chronic systemic disease: Clinical challenges and novel innovations. The Lancet. 2021;397(10276):839-52. DOI: 10.1016/S0140-6736(21)00389-5
18. Wray S, Prendergast C. The Myometrium: From Excitation to Contractions and Labour. Advances in Experimental Medicine and Biology. 2019;1124:233-63. DOI: 10.1007/978-981-13-5895-1_10
19. Lax SF. New features in the 2014 WHO classification of uterine neoplasms. Der Pathologe. 2016;37(6):500-11. DOI: 10.1007/s00292-016-0230-4
20. Ragni MV, Machin N, Malec LM et al. Von Willebrand factor for menorrhagia: a survey and literature review. Haemophilia. 2016;22(3): 397-402. DOI: 10.1111/hae.12898
21. Crosbie EJ, Kitson SJ, McAlpine JN et al. Endometrial cancer. Lancet. 2022;399(10333):1412-28. DOI: 10.1016/S0140-6736(22)00323-3
22. Archer DF. Vascular dysfunction as a cause of endometrial bleeding. Gynecological Endocrinology. 2012;28(9):688-93. DOI: 10.3109/09513590.2011.588848
23. Eworuke E, Hou L, Zhang R et al. Risk of Severe Abnormal Uterine Bleeding Associated with Rivaroxaban Compared with Apixaban, Dabigatran and Warfarin. Drug Safety. 2021;44(7):753-73. DOI: 10.1007/s40264-021-01072-0
24. Сухих Г.Т., Шуршалина А.В. Хронический эндометрит. М.: ГЭОТАР-Медиа, 2013. Sukhoi G.T., Shurshalina A.V. Chronic endometritis. Moscow: GEOTAR-Media, 2013 (in Russian).
25. Михалева Л.М., Болтовская М.Н., Михалев С.А. и др. Клинико-морфологические аспекты эндометриальной дисфункции, обусловленной хроническим эндометритом. Архив патологии. 2017;79(6):22-29. Mikhaleva L.M., Boltovskaya M.N., Mikhalev S.A. et al. Endometrial dysfunction caused by chronic endometritis: сlinical and morphological aspects. Arkhiv Patologii. 2017;79(6):22-9. DOI: 10.17116/ patol201779622-29 (in Russian).
26. Михалева Л.М., Михалев С.А., Савельева Г.М. и др. Хронический эндометрит – показание для прегравидарной подготовки. Клиническая практика. 2018;9(2):36-41. Mikhaleva L.M., Mikhalev S.A., Savelyeva G.M., etc. Chronic endometritis is an indication for pregravidar preparation. Clinical practice. 2018;9(2):36-41. (in Russian).
27. Kushnir VA, Solouki S, Sarig-Meth T et al. Systemic inflammation and autoimmunity in women with chronic endometritis. Am J Reprod Immunol. 2016;75(6):672-7. DOI: 10.1111/aji.12508
28. Радзинский В.Е., Петров Ю.А., Калинина Е.А. и др. Патогенетические особенности макротипов хронического эндометрита. Казанский медицинский журнал. 2017;98(1):27-34. Radzinskii VE, Petrov YuA, Kalinina EA et al. Pathogenetic features of the macrotypes of chronic endometritis. Kazanskii meditsinskii zhurnal. 2017; 98(1):27-34. DOI: 10.17750/kmj2017-27 (in Russian).
29. Радзинский В.Е., Ордиянц И.М., Добрецова Т.А. Эндометрий в огне. Острое и хроническое воспаление эндометрия: от новых взглядов к новым стратегиям StatusPraesens. Гинекология, акушерство, бесплодный брак. 2016;2(31):126-32. Radzinsky V.E., Ordiyants I.M., Dobretsova T.A. The endometrium is on fire. Acute and chronic endometrial inflammation: from new perspectives to new strategies of Status Praesens. Gynecology, obstetrics, infertile marriage. 2016;2(31):126-32 (in Russian).
30. Радзинский В.Е., Петров Ю.А., Калинина Е.А. и др. Патогенетические особенности макротипов хронического эндометрита. Казанский медицинский журнал. 2017;98(1):27-34. Radzinsky V.E., Petrov Yu.A., Kalinina E.A. et al. Pathogenetic features of macrotypes of chronic endometritis. Kazan Medical Journal. 2017;98(1):27-34 (in Russian).
31. Оразов М.Р., Михалева Л.М., Семенов П.А. и др. Эффективность лечения хронического эндометрита у женщин с неудачами имплантации в анамнезе. Трудный пациент. 2020;18(8-9):7-12. . DOI: 10.24411/2074-1995-2020-10053 Orazov M.R., Mikhaleva L.M., Semenov P.A. et al. The effectiveness of treatment of chronic endometritis in women with a history of implantation failures. A difficult patient. 2020;18(8-9):7-12. . DOI: 10.24411/2074-1995-2020-10053 (in Russian).
32. Полина М.Л., Радзинский В.Е., Михалева Л.М. и др. Иммунологические аспекты нарушений имплантации при маточной форме бесплодия. Акушерство и гинекология: новости, мнения, обучение. 2023;11(Спецвыпуск):6-17. DOI: 10.33029/2303-9698-2023-11-suppl-6-17 Polina M.L., Radzinsky V.E., Mikhaleva L.M. et al. Immunological aspects of implantation disorders in uterine infertility. Obstetrics and gynecology: news, opinions, training. 2023;11(Special Edition):6-17. DOI: 10.33029/2303-9698-2023-11-suppl-6-17 (in Russian).
33. Стюшин А.М., Семенченко И.Б. Особенности патогенеза при хроническом эндометрите. В сборнике: Актуальные вопросы акушерства и гинекологии. Сборник материалов внутривузовской научно-практической конференции. Ростов-на-Дону, 2023. Styushin A.M., Semenchenko I.B. Features of pathogenesis in chronic endometritis. In: Topical issues of obstetrics and gynecology. Anthology of materials of the intra-university scientific and practical conference. Rostov-on-Don, 2023. (in Russian).
34. Данилюк С.В., Кирия Д.Г., Долгая О.В., Олейник А.Е. Патогистологические и иммуногистохимические особенности эндометрия при хроническом эндометрите у женщин с бесплодием. Вестник проблем биологии и медицины. 2020;4(158):13-7. Danilyuk S.V., Kiria D.G., Dolgaya O.V., Oleinik A.E. Pathohistological and immunohistochemical features of the endometrium in chronic endometritis in women with infertility. Bulletin of problems of Biology and Medicine. 2020;4(158):13-7 (in Russian).
35. Оразов М.Р., Токтар Л.Р., Михалева Л.М. и др. Хронический эндометрит и дисфункция эндометрия – есть ли причинно-следственная связь? Акушерство и гинекология. Новости. Мнения. Обучение. 2020;8(S3):61-9. Orazov M.R., Toktar L.R., Mikhaleva L.M. et al. Chronic endometritis and endometrial dysfunction – is there a causal relationship? Obstetrics and gynecology. News. Opinions. Training. 2020;8(S3):61-9 (in Russian).
36. Оразов М.Р., Михалева Л.М., Исмаилзаде С.Я. и др. Внутриматочные синехии и хронический эндометрит – есть ли причинно-следственная связь? Гинекология. 2022;24(2):144-9. DOI: 10.26442/20795696.2022.2.201417 Orazov M.R., Mikhaleva L.M., Ismailzade S.Ya. et al. Intrauterine synechiae and chronic endometritis – is there a causal relationship? Gynecology. 2022;24(2):144-9. DOI: 10.26442/20795696.2022.2. 201417 (in Russian).
37. Радзинский В.Е., Оразов М.Р., Токтар Л.Р. и др. Вклад хронического эндометрита в нарушения репродуктивной системы у пациенток с повторными неудачами имплантации. Гинекология. 2021;23(1):102-6. DOI: 10.26442/20795696.2021.1.200671 Radzinsky V.E., Orazov M.R., Toktar L.R. et al. The contribution of chronic endometritis to reproductive system disorders in patients with repeated implantation failures. Gynecology. 2021;23(1):102-6. DOI: 10.26442/20795696.2021.1.200671 (in Russian).
38. Сорокин Ю.А., Гизингер О.А., Радзинский В.Е. Клинико-иммунологическое обоснование ультразвуковой кавитации в комплексном лечении бесплодия при хроническом эндометрите. Гинекология. 2022;24(5):355-61. Sorokin Yu.A., Giesinger O.A., Radzinsky V.E. Clinical and immunological substantiation of ultrasonic cavitation in the complex treatment of infertility in chronic endometritis. Gynecology. 2022;24(5):355-61 (in Russian).
39. Оразов М.Р., Волкова С.В., Безуглова Т.В. Хронический эндометрит и неудачи имплантации: как не упустить последний шанс? Трудный пациент. 2022;20(1):17-21. Orazov M.R., Volkova S.V., Bezuglova T.V. Chronic endometritis and implantation failures: how not to miss the last chance? A difficult patient. 2022;20(1):17-21 (in Russian).
40. Сндоян А.В., Ермаков А.Н. Иммунологическая перестройка при хроническом воспалении слизистой оболочки матки. Молодой ученый. 2016;22.1(126.1):39-43. URL: https://moluch.ru/archive/ 126/35012/ Sndoyan A.V., Ermakov A.N. Immunological restructuring in chronic inflammation of the uterine mucosa. A young scientist. 2016;22.1(126.1):39-43. URL: https://moluch.ru/archive/126/35012/ (in Russian).
41. Полина М.Л., Михалева Л.М., Витязева И.И. и др. Взаимосвязь типа микробиоты и ммунных ресурсов эндометрия бесплодных женщин в фазу имплантационного окна. Якутский медицинский журнал. 2023;82(2):8-13. Polina M.L., Mikhaleva L.M., Vityazeva I.I. et al. The relationship between the type of microbiota and the immune resources of the endometrium of infertile women during the implantation window phase. Yakut Medical Journal. 2023;82(2):8-13 (in Russian).
42. Оразов М.Р., Михалева Л.М., Семенов П.А. и др. Хронический эндометрит и контраверсии антибактериальной терапии. Трудный пациент. 2020;18(10):41-6. Orazov M.R., Mikhaleva L.M., Semenov P.A. et al. Chronic endometritis and contraversions of antibacterial therapy. A difficult patient. 2020;18(10):41-6 (in Russian).
43. Михалев С.А., Бабиченко И.И., Шахпазян Н.К. и др. Роль урогенитальной инфекции в развитии спонтанных преждевременных родов. Проблемы репродукции. 2019;25(2):88-94. DOI:10.17116/repro20192502188 Mikhalev S.A., Babichenko I.I., Shakhpazyan N.K. et al. The role of urogenital infection in the development of spontaneous premature birth. Reproduction problems. 2019;25(2):88-94. DOI:10.17116/repro20192502188 (in Russian).
44. Оразов М.Р., Локшин В.Н., Силантьева Е.С. и др. Морфологические и молекулярно-биологические детерминанты повторных неудач имплантации. Вестник национальной академии наук республики Казахстан. 2020;3(385):15. DOI: 10.32014/2020.2518-1467.63 Orazov M.R., Lokshin V.N., Silantieva E.S. et al. Morphological and molecular biological determinants of repeated implantation failures. Bulletin of the National Academy of Sciences of the Republic of Kazakhstan. 2020;3(385):15. DOI: 10.32014/2020.2518-1467.63 (in Russian).
45. Михалева Л.М., Оразов М.Р., Силантьева Е.С. и др. Повторные неудачи имплантации. Патогенез иммунологических нарушений в эндометрии. Доктор.Ру. 2022;21(1):21-6. DOI: 10.31550/1727-2378-2022-21-1-21-26(RCI WoS) Mikhaleva L.M., Orazov M.R., Silantieva E.S. et al. Repeated implantation failures. The pathogenesis of immunological disorders in the endometrium. Doctor.Ru. 2022;21(1):21-6. DOI: 10.31550/1727-2378-2022-21-1-21-26(RCI WoS) (in Russian).
46. Радзинский В.Е., Михалева Л.М., Оразов М.Р. и др. Рецептивность эндометрия пациенток с повторными неудачами имплантации. Доктор.Ру. 2022;21(1):27-33. DOI: 10.31550/1727-2378-2022-21-1-27-33(RCI WoS) Radzinsky V.E., Mikhaleva L.M., Orazov M.R. et al. Endometrial receptivity in patients with repeated implantation failures. Doctor.Ru. 2022;21(1):27-33. DOI: 10.31550/1727-2378-2022-21-1-27-33(RCI WoS) (in Russian).
47. Радзинский В.Е., Оразов М.Р., Токтар Л.Р. и др. Эффект «разбросанных пазлов»: имплантационные нарушения при хроническом эндометрите. Гинекология. 2020;22(6):93-100. DOI: 10.26442/ 20795696.2020.6.200493 Radzinsky V.E., Orazov M.R., Toktar L.R. et al. The effect of «scattered puzzles»: implantation disorders in chronic endometritis. Gynecology. 2020;22(6):93-100. DOI: 10.26442/20795696.2020.6.200493 (in Russian).
48. Cicinelli E, Haimovich S, De Ziegler D 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. DOI: 10.1007/s10815-021-02356-1. PMID: 34791588
49. Кузнецова И.В., Землина Н.С., Мусина Р.А. et al. Применение аутологичных мезенхимальных стволовых клеток с целью восстановления эндометрия у пациенток со сниженной фертильностью. Вопросы гинекологии, акушерства и перинатологии. 2019;18(60):34-40. Kuznetsova I.V., Zemlina N.S., Musina R.A. et al. The use of autologous mesenchymal stem cells to restore the endometrium in patients with reduced fertility. Issues of gynecology, obstetrics and perinatology. 2019;18(60):34-40 (in Russian).
50. Краснопольская К.В., Михалева Л.М., Оразов М.Р., Долгов Е.Д. Возможности преодоления неудач имплантации при бесплодии маточного генеза, обусловленных хроническим эндометритом. Гинекология. 2022;24(5):400-7. Krasnopolskaya K.V., Mikhaleva L.M., Orazov M.R., Dolgov E.D. The possibilities of overcoming implantation failures in infertility of uterine genesis caused by chronic endometritis. Gynecology. 2022;24(5):400-7 (in Russian).
51. Оразов М.Р., Орехов Р.Е., Камиллова Д.П. и др. Тайны патогенеза повторных неудач имплантации. Трудный пациент. 2020;18(4). DOI: 10.24411/2074-1995-2020-10030 Orazov M.R., Orekhov R.E., Kamilova D.P. et al. Secrets of the pathogenesis of repeated implantation failures. A difficult patient. 2020;18(4). DOI: 10.24411/2074-1995-2020-10030 (in Russian).
52. Оразов М.Р., Михалева Л.М., Семенов П.А. Хронический эндометрит: патогенез, диагностика, лечение и его связь с бесплодием. Клиническая и экспериментальная морфология. 2020;9(2):16-25. DOI:10.31088/CEM2020.9.2 Orazov M.R., Mikhaleva L.M., Semenov P.A. Chronic endometritis: pathogenesis, diagnosis, treatment and its connection with infertility. Clinical and experimental morphology. 2020;9(2):16-25. DOI:10.31088/ CEM2020.9.2 (in Russian).
53. Оразов М.Р., Радзинский В.Е., Волкова С.В. и др. Хронический эндометрит у женщин с эндометриоз-ассоциированным бесплодием. Гинекология. 2020;22(3):15-20. DOI: 10.26442/20795696.2020.3.200174 Orazov M.R., Radzinsky V.E., Volkova S.V. et al. Chronic endometritis in women with endometriosis-associated infertility. Gynecology. 2020;22(3):15-20. DOI: 10.26442/20795696.2020.3.200174 (in Russian).
54. Оразов М.Р., Краснопольская К.В., Силантьева Е.С. и др. «Проблемный» эндометрий как фактор бесплодия: поиск путей преодоления продолжается. Трудный пациент. 2020;18(8-9):13-9. DOI: 10.24411/2074-1995-2020-10054 Orazov M.R., Krasnopolskaya K.V., Silantieva E.S. et al. «Problematic» endometrium as a factor of infertility: the search for ways to overcome it continues. A difficult patient. 2020;18(8-9):13-9. DOI: 10.24411/2074-1995-2020-10054 (in Russian).
55. Оразов М.Р., Силантьева Е.С., Орехов Р.Е. и др. Повторные неудачи имплантации: этиология и возможности физиотерапии. Трудный пациент. 2020;18(8-9):20-4. DOI: 10.24411/2074-1995-2020-10055 Orazov M.R., Silantieva E.S., Orekhov R.E. et al. Repeated implantation failures: etiology and possibilities of physiotherapy. A difficult patient. 2020;18(8-9):20-4. DOI: 10.24411/2074-1995-2020-10055 (in Russian).
56. Оразов М.Р., Краснопольская К.В., Силантьева Е.С. и др. Эффективность альтернативных методов лечения бесплодия маточного генеза. Гинекология. 2021;23(1):92-6. DOI: 10.26442/20795696. 2021.1.200672 Orazov M.R., Krasnopolskaya K.V., Silantieva E.S. et al. The effectiveness of alternative methods of treatment of infertility of uterine origin. Gynecology. 2021;23(1):92-6. DOI: 10.26442/20795696.2021.1. 200672 (in Russian).
57. Радзинский В.Е., Оразов М.Р., Михалева Л.М. и др. Предикторы неудач ЭКО при имплантационной несостоятельности эндометрия. Трудный пациент. 2021;19(1):23-6. DOI: 10.24412/2074-1995-2021-1-18-22 Radzinsky V.E., Orazov M.R., Mikhaleva L.M. et al. Predictors of IVF failures in endometrial implantation failure. A difficult patient. 2021;19(1):23-6. DOI: 10.24412/2074-1995-2021-1-18-22 (in Russian).
58. Оразов М.Р., Михалёва Л.М., Силантьева Е.С., Орехов Р.Е. Хронический эндометрит у пациенток с повторными неудачами имплантации: эпидемиология, этиология, патогенез и преодоление бесплодия. Репродуктивная медицина. 2021;47(2):31-40. DOI: 10.37800/RM2021-2-3 Orazov M.R., Mikhaleva L.M., Silantieva E.S., Orekhov R.E. Chronic endometritis in patients with repeated implantation failures: epidemiology, etiology, pathogenesis and overcoming infertility. Reproductive medicine. 2021;47(2):31-40. DOI: 10.37800/RM2021-2-3 (in Russian).
59. Liu Z, Liu X, Li F et al. Overexpression of hypoxia-inducible factor 1alpha and excessive vascularization in the peri-implantation endometrium of infertile women with chronicendometritis. Front Endocrinol (Lausanne). 2022;13:1001437. DOI: 10.3389/fendo.2022.1001437. eCollection 2022. PMID: 36531509
60. Yasuo T, Kitaya K. Challenges in Clinical Diagnosis and Management of Chronic Endometritis. Diagnostics (Basel). 2022;12(11):2711. DOI: 10.3390/diagnostics12112711. PMID: 36359553
61. McQueen DB, Maniar KP, Hutchinson A et al. Redefining chronic endometritis: the importance of endometrial stromal changes. Fertil Steril. 2021;116(3):855-61. DOI: 10.1016/j.fertnstert.2021.04.036. PMID: 34120737
62. Cicinelli E, Vitagliano A, Loizzi V et al. Altered Gene Expression Encoding Cytochines, Grow Factors and Cell Cycle Regulators in the Endometrium of Women with Chronic Endometritis. Diagnostics (Basel). 2021;11(3):471. DOI: 10.3390/diagnostics11030471. PMID: 33800186
63. Germic N, Frangez Z, Yousefi S, Simon H.U. Regulation of the innate immune system by autophagy: neutrophils, eosinophils, mast cells, NK cells. Cell Death Differ. 2019;26(4):703-14.
64. Lawrence SM, Corriden R, Nizet V. How Neutrophils Meet Their End. Trends Immunol. 2020;41(6):531-44.
65. Brostjan C, Oehler R. The role of neutrophil death in chronic inflammation and cancer. Cell Death Discov. 2020;6: 26. DOI: 10.1038/s41420-020-0255-6
66. Щепеткин И.А., Буданова О.П., Малышев И.Ю., Аточин Д.Н. Молекулярные механизмы апоптоза нейтрофилов (обзор литературы). Патогенез. 2018;16(4):5-18. Schepetkin I.A., Budanova O.P., Malyshev I.Yu., Atochin D.N. Molecular mechanisms of neutrophil apoptosis (review). Patogenez/Pathogenesis. 2018;16(4):5-18 (in Russian).
67. Kourtzelis I, Hajishengallis G, Chavakis T. Phagocytosis of Apoptotic Cells in Resolution of Inflammation. Front Immunol. 2020;11:553. DOI: 10.3389/fimmu.2020.00553
68. Liew PX, Kubes P. The Neutrophil’s Role During Health and Disease. Physiol Rev. 2019;99(2):1223–48.
69. Schett G, Neurath MF. Resolution of chronic inflammatory disease: universal and tissue-specific concepts. Nat Commun. 2018;9(1):3261. DOI: 10.1038/s41467-018-05800-6
70. Kumar S, Dikshit M. Metabolic Insight of Neutrophils in Health and Disease. Front Immunol. 2019;10:2099. DOI: 10.3389/fimmu.2019.02099
71. Оздоева И.М-Б., Петров Ю.А. хронический эндометрит: изменения основных звеньев иммунитета. Международный журнал прикладных и фундаментальных исследований. 2020;(4):26-30; URL: https://applied-research.ru/ru/article/view?id=13050 Ozdoeva I.M.-B., Petrov Yu.A. chronic endometritis: changes in the main links of immunity. International Journal of Applied and Fundamental Research. 2020;(4):26-30; URL: https://applied-research.ru/ru/article/view?id=13050 (in Russian).
72. Yang G, Zhang Q, Tan J et al. HMGB1 induces macrophage pyroptosis in chronic endometritis. Int Immunopharmacol. 2023;123:110706. DOI: 10.1016/j.intimp.2023.110706. Epub 2023 Aug 2. PMID: 37541110
73. Оразов М.Р., Краснопольская К.В., Силантьева Е.С. и др. Эффективность альтернативных методов лечения бесплодия маточного генеза. Гинекология. 2021;23(1):92-6. Orazov M.R., Krasnopolskaya K.V., Silantieva E.S. et al. The effectiveness of alternative methods of treatment of infertility of uterine origin. Gynecology. 2021;23(1):92-6 (in Russian).
74. Sharkey AM, Smith SK. The endometrium as a cause of implantation failure. Best Practice and Research Clinical Obstetrics Gynecology. 2015;17(2):289-307.
75. Лызикова Ю.А. Выбор тактики лечения хронического эндометрита на основании иммуногистохимического и микробиологического исследований эндометрия. Вестник смоленской государственной медицинской академии. 2019;18(2):122-7. Lyzikova Yu.A. The choice of tactics for the treatment of chronic endometritis based on immunohistochemical and microbiological studies of the endometrium. Bulletin of the Smolensk State Medical Academy. 2019;18(2):122-7 (in Russian).
76. Газизова Г.Х., Ящук А.Г., Масленников А.В. и др. Морфологические особенности эндометрия у пациенток с хроническим эндометритом атрофической формы и нарушения гемодинамики. Архив акушерства и гинекологии им. В.Ф. Снегирева. 2022;9(4):231-7. Gazizova G.H., Yaschuk A.G., Maslennikov A.V. et al. Morphological features of the endometrium in patients with chronic atrophic endometritis and hemodynamic disorders. Archive of Obstetrics and Gynecology named after V.F. Snegirev. 2022;9(4):231-7 (in Russian).
77. Hosseini S, Abbasi H, Salehpour S et al. Prevalence of chronic endometritis in infertile women undergoing hysteroscopy and its association with intrauterine abnormalities: A Cross-Sectional study. JBRA Assist Reprod. 2024;Mar 28. DOI: 10.5935/1518-0557.20240011
76. Li JW, Xv H, Wan RT. Bibliometric analysis of the global trends in immune-related recurrent pregnancy loss research over the last two decades. J Obstet Gynaecol Res. 2024;Mar 11. DOI: 10.1111/jog.15907.
79. Blazheva S, Pachkova S, Bodurska T et al. Unlocking the Uterine Code: Microbiota, Immune Cells, and Therapy for Recurrent Reproductive Failure. Microorganisms. 2024; Mar 9;12(3):547. DOI: 10.3390/microorganisms12030547
80. Hiraoka T, Osuga Y, Hirota Y. Current perspectives on endometrial receptivity: A comprehensive overview of etiology and treatment. J Obstet Gynaecol Res. 2023;49(10):2397-409. DOI: 10.1111/jog.15759. Epub 2023 Aug 1. PMID: 37527810
81. Ryan E, Tolani AT, Zhang J et al. 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. DOI: 10.1016/j.fertnstert.2022.07.011. PMID: 36182264
82. Kuroda K, Yamanaka A, Takamizawa S et al. Prevalence of and risk factors for chronic endometritis in patients with intrauterine disorders after hysteroscopic surgery. Fertil Steril. 2022;118(3):568-75. DOI: 10.1016/j.fertnstert.2022.05.029. Epub 2022 Jun 17. PMID: 35718544
83. Zeng S, Liu X, Liu D, Song W. Research update for the immune microenvironment of chronic endometritis. J Reprod Immunol. 2022;152:103637. DOI: 10.1016/j.jri.2022.103637. PMID: 35576684
84. Margulies SL, Flores V, Parkash V, Pal L. Chronic endometritis: A prevalent yet poorly understood entity. Int J Gynaecol Obstet. 2022;158(1):194-200. DOI: 10.1002/ijgo.13962. PMID: 34605024
85. Tsonis O, Gkrozou F, Dimitriou E, Paschopoulos M. Hysteroscopic detection of chronic endometritis: Evaluating proposed hysteroscopic features suggestive of chronic endometritis. J Gynecol Obstet Hum Reprod. 2021;50(9):102182. DOI: 10.1016/j.jogoh.2021.102182. PMID: 34111625
86. Ticconi C, Di Simone N, Campagnolo L, Fazleabas A. Clinical consequences of defective decidualization. Tissue Cell. 2021;72:101586. DOI: 10.1016/j.tice.2021.101586. PMID: 34217128
87. Guo L, Gu F, Tan J et al. Multiple endometrial polyps is associated with higher risk of chronicendometritis in reproductive-aged women. J Obstet Gynaecol Res. 2021;47(1):389-96. DOI: 10.1111/jog.14541. PMID: 33300233
88. Saxtorph MH, Hallager T, Persson G et al. Assessing endometrial receptivity after recurrent implantation failure: a prospective controlled cohort study. Reprod Biomed Online. 2020;41(6):998-1006. DOI: 10.1016/j.rbmo.2020.08.015. PMID: 32978074
89. Mlodzik N, Lukaszuk K, Sieg W et al. Endometrial microbiota – do they mean more than we have expected? Ginekol Pol. 2020;91(1):45-8. DOI: 10.5603/GP.2020.0010. PMID: 32039468
90. Zargar M, Ghafourian M, Nikbakht R et al. Evaluating Chronic Endometritis in Women with Recurrent Implantation Failure and Recurrent Pregnancy Loss by Hysteroscopy and Immunohistochemistry. J Minim Invasive Gynecol. 2020;27(1):116-21. DOI: 10.1016/j.jmig.2019. 02.016.PMID: 30851430
91. Yoneda E, Kim S, Tomita K et al. Evaluation of Lipopolysaccharide and Interleukin-6 as Useful Screening Tool for Chronic Endometritis. Int J Mol Sci. 2024;25(4):2017. DOI: 10.3390/ijms25042017. PMID: 38396694
92. Hue HJ, Choi H, Lee HK et al. Prevalence and confounders of chronic endometritis diagnosed using CD138in patients with recurrent implantation failure. Clin Exp Reprod Med. 2024. DOI: 10.5653/cerm. 2023.06170. Online ahead of print. PMID: 38263588
93. Retracted: Investigation of the Relationship between Chronic EndometritisManifestations under Hysteroscope and CD138 Expression. And Biomechanics AB.Appl Bionics Biomech. 2023 Dec 20;2023:9896519. DOI: 10.1155/2023/9896519. eCollection 2023. PMID: 38152755
94. Yang G, Zhang Q, Tan J et al. HMGB1 induces macrophage pyroptosis in chronic endometritis. Int Immunopharmacol. 2023;123:110706. DOI: 10.1016/j.intimp.2023.110706. PMID: 37541110
95. Takimoto K, Yamada H, Shimada S et al. Chronic Endometritis and Uterine Endometrium Microbiota in Recurrent Implantation Failure and Recurrent Pregnancy Loss. Biomedicines. 2023;11(9):2391. DOI: 10.3390/biomedicines11092391. PMID: 37760832
96. Oshina K, Kuroda K, Nakabayashi K et al. Gene expression signatures associated with chronic endometritis revealed by RNA sequencing. Front Med (Lausanne). 2023;10:1185284. DOI: 10.3389/fmed.2023.1185284. eCollection 2023. PMID: 37547609
97. Kuroda K, Ishiyama S, Shiobara K et al. Therapeutic efficacy of gentle endometrial curettage on antibiotic-resistant chronic endometritis in infertile women. Reprod Med Biol. 2023;22(1):e12525. DOI: 10.1002/rmb2.12525. eCollection 2023 Jan-Dec. PMID: 37409240
98. Tian Y, Zeng Q, Cheng Y et al. Follicular helper T lymphocytes in the endometria of patients with reproductive failure: Association with pregnancy outcomes and inflammatory status of the endometria. Am J Reprod Immunol. 2023;90(1):e13708. DOI: 10.1111/aji.13708. PMID: 37095737
99. Gu J, Sun Q, Qi Y et al. The effect of chronic endometritis and treatment on patients with unexplained infertility. BMC Womens Health. 2023;23(1):345. DOI: 10.1186/s12905-023-02499-6. PMID: 37391747
100. Mihara M, Yasuo T, Kitaya K. Precision Medicine for Chronic Endometritis: Computer-Aided Diagnosis Using Deep Learning Model. Diagnostics (Basel). 2023;13(5):936. DOI: 10.3390/diagnostics 13050936. PMID: 36900079
101. Goto T, Goto S, Ozawa F et al. The association between chronic deciduitis and recurrent pregnancy loss. J Reprod Immunol. 2023;156:103824. DOI: 10.1016/j.jri.2023.103824. PMID: 36773493
102. Xiang R, Li M, Gu Z et al. Chronic endometritis positively correlates with the aggravation of intrauterine adhesions but has limited effects on reproductive prognosis with antibiotic application. Int J Gynaecol Obstet. 2023;160(3):986-92. DOI: 10.1002/ijgo.14434. PMID: 36049892
103. Wu X, Niu S, Zhao T. Establishment and verification of hysteroscopic scoring system for chronicendometritis in infertile patients. Zhejiang Da Xue Xue Bao Yi Xue Ban. 2023;52(1):46-53. DOI: 10.3724/zdxbyxb-2022-0513. PMID: 37283117
104. Li J, Li X, Ding J et al. Analysis of pregnancy outcomes in patients with recurrent implantation failure complicated with chronic endometritis. Front Cell Dev Biol. 2023;11:1088586. DOI: 10.3389/fcell.2023. 1088586. eCollection 2023. PMID: 36861040
105. Li Y, Xu Y, Yu S et al. Chronic endometritis impairs embryo implantation in patients with repeated implantation failure: A retrospective study. Taiwan J Obstet Gynecol. 2022;61(6):984-8. DOI: 10.1016/ j.tjog.2021.01.034. PMID: 36428002
106. Murtinger M, Wirleitner B, Spitzer D et al. Diagnosing chronic endometritis: when simplification fails to clarify. Hum Reprod Open. 2022 Jun 7;2022(3):hoac023. DOI: 10.1093/hropen/hoac023. eCollection 2022. PMID: 35722504
107. Mitter VR, Meier S, Rau TT 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. DOI: 10.1111/aji.13482. Epub 2021 Aug 9. PMID: 34218478
108. Li J, Song D, Feng X et al. The association of chronic endometritis with mid-trimester loss due to cervical incompetence and the outcome of laparoscopic cervical cerclage. Arch Gynecol Obstet. 2021;304(5):1345-51. DOI: 10.1007/s00404-021-06029-3. PMID: 33811545
109. Lozano FM, Bernabeu A, Lledo B et al. Characterization of the vaginal and endometrial microbiome in patients with chronic endometritis. Eur J Obstet Gynecol Reprod Biol. 2021 Aug;263:25-32. DOI: 10.1016/j.ejogrb.2021.05.045. PMID: 34144490
110. Kitaya K, Ishikawa T. Chronic endometritis: simple can be harder than complex? Fertil Steril. 2021;115(6):1443-4. DOI: 10.1016/j.fertnstert.2021.03.023
111. Li Y, Xu S, Yu S 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. DOI: 10.1111/aji.13369. PMID: 33152123
112. Ishida M, Takebayashi A, Kimura F et al. Induction of the epithelial-mesenchymal transition in the endometrium by chronic endometritis in infertile patients. PLoS One. 2021;16(4):e0249775. DOI: 10.1371/journal.pone.0249775. eCollection 2021. PMID: 33826645
113. Kitazawa J, Kimura F, Nakamura A et al. Alteration in endometrial helper T-cell subgroups in chronic endometritis. Am J Reprod Immunol. 2021;85(3):e13372. DOI: 10.1111/aji.13372. PMID: 33155317
114. Chiokadze M, Bär C, Pastuschek J et al. Beyond Uterine Natural Killer Cell Numbers in Unexplained Recurrent Pregnancy Loss: Combined Analysis of CD45, CD56, CD16, CD57, and CD138. Diagnostics (Basel). 2020 Aug 29;10(9):650. DOI: 10.3390/diagnostics10090650. PMID: 32872526
115. Liu H, Song J, Zhang F et al. A New Hysteroscopic Scoring System for Diagnosing Chronic Endometritis. Minim Invasive Gynecol. 2020;27(5):1127-32. DOI: 10.1016/j.jmig.2019.08.035. PMID: 32240839
116. Kuroda K, Horikawa T, Moriyama A et al. Impact of chronic endometritis on endometrial receptivity analysis results and pregnancy outcomes. Immun Inflamm Dis. 2020 Dec;8(4):650-8. DOI: 10.1002/iid3. 354. PMID: 32969185
117. Rimmer MP, Fishwick K, Henderson I et al. Quantifying CD138+ cells in the endometrium to assess chronic endometritisin women at risk of recurrent pregnancy loss: A prospective cohort study and rapid review. Obstet Gynaecol Res. 2021;47(2):689-97. DOI: 10.1111/jog.14585. PMID: 33274569
118. Kaku S, Kubo T, Kimura F et al. Relationship of chronic endometritis with chronic deciduitis in cases of miscarriage. BMC Womens Health. 2020;20(1):114. DOI: 10.1186/s12905-020-00982-y. PMID: 32487112
119. Chen X, Liu Y, Zhao Y et al. Association between chronic endometritis and uterine natural killer cell density in women with recurrent miscarriage: clinical implications. J Obstet Gynaecol Res. 2020;46(6):858-63. DOI: 10.1111/jog.14250. PMID: 32189458
120. Liu Y, Ko EY, Wong KK et al. Endometrial microbiota in infertile women with and without chronicendometritis as diagnosed using a quantitative and reference range-based method. Fertil Steril. 2019;112(4):707-17.e1. DOI: 10.1016/j.fertnstert.2019.05.015. PMID: 31327470
121. Liu L, Yang H, Guo Y et al. The impact of chronic endometritis on endometrial fibrosis and reproductive prognosis in patients with moderate and severe intrauterine adhesions: a prospective cohort study. Fertil Steril. 2019;111(5):1002-1010.e2. DOI: 10.1016/j.fertnstert.2019.01.006
122. Cao W, Fu X, Zhou J et al. The effect of the female genital tract and gut microbiome on reproductive dysfunction. Biosci Trends. 2024;17(6):458-74. DOI: 10.5582/bst.2023.01133. PMID: 38104979
123. HogenEsch E, Hojjati R, Komorowski A, et al. J Chronic endometritis: screening, treatment, and pregnancy outcomes in an academic fertility center. Assist Reprod Genet. 2023;40(10):2463-71. DOI: 10.1007/s10815-023-02902-z. PMID: 37558906
124. Liang J, Li M, Zhang L 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 May 22;13:1125640. DOI: 10.3389/fcimb.2023.1125640. eCollection 2023. PMID: 37284497
125. Margulies SL, Flores V, Parkash V, Pal L. Chronic endometritis: A prevalent yet poorly understood entity. Int J Gynaecol Obstet. 2022;158(1):194-200. DOI: 10.1002/ijgo.13962. PMID: 34605024
126. Molina NM, Sola-Leyva A, Saez-Lara MJ et al. New Opportunities for Endometrial Health by Modifying Uterine Microbial Composition: Present or Future? Biomolecules. 2020;10(4):593. DOI: 10.3390/biom10040593. PMID: 32290428
127. Endometritis. Taylor M, Jenkins SM, Pillarisetty LS.2023 Oct 26. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024; Jan. PMID: 31985918
128. Zhang Z, Li T, Xu L et al. Extracellular superoxide produced by Enterococcus faecalis reduces endometrial receptivity via inflammatory injury. Am J Reprod Immunol. 2021 Oct;86(4):e13453. DOI: 10.1111/aji.13453. Epub 2021 May 24. PMID: 33991362
For citation:Mitrelis R.Y., Mikhaleva L.M., Orazov M.R., Mikhalev S.A., Kobyzeva T.Yu..Chronic endometritis in the development of abnormal uterine bleeding, endometrial dysfunction and other reproductive disorders (literature review). Clinical review for general practice. 2024; 5 (3): 27–38. (In Russ.). DOI: 10.47407/kr2023.5.3.00371
All accepted articles publish licensed under a Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.