Возможности преодоления неудач имплантации при бесплодии маточного генеза, обусловленных хроническим эндометритом

1. The World Health Organization. Infertility. Available at https://www.who.int/health-topics/infertility#tab=tab_1. Accessed: 07.09.2022.
2. Tamrakar SR, Bastakoti R. Determinants of Infertility in Couples. J Nepal Health Res Counc. 2019;17(1):85-9. DOI:10.33314/jnhrc.1827
3. Sallée C, Margueritte F, Marquet P, et al. Uterine Factor Infertility, a Systematic Review. J Clin Med. 2022;11(16):4907. DOI:10.3390/jcm11164907
4. Michels TC. Chronic endometritis. Am Fam Physician. 1995;52(1):217-22.
5. Kimura F, Takebayashi A, Ishida M, et al. Review: Chronic endometritis and its effect on reproduction. J Obstet Gynaecol Res. 2019;45(5):951-60. DOI:10.1111/jog.13937
6. Puente E, Alonso L, Laganà AS, et al. Chronic Endometritis: Old Problem, Novel Insights and Future Challenges. Int J Fertil Steril. 2020;13(4):250-6. DOI:10.22074/ijfs.2020.5779
7. Vitagliano A, Saccardi C, Litta P, Noventa M. Chronic endometritis: Really so relevant in repeated IVF failure? Am J Reprod Immunol. 2017;78(6). DOI:10.1111/aji.12758
8. Johnston-MacAnanny EB, Hartnett J, Engmann LL, et al. Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 2010;93(2):437-41. DOI:10.1016/j.fertnstert.2008.12.131
9. Vitagliano A, Noventa M, Gizzo S. Autoimmunity, systemic inflammation, and their correlation with repeated implantation failure and recurrent miscarriage: is chronic endometritis the missing piece of the jigsaw? Am J Reprod Immunol. 2017;77(1). DOI:10.1111/aji.12597
10. McQueen DB, Bernardi LA, Stephenson MD. Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil Steril. 2014;101(4):1026-30. DOI:10.1016/j.fertnstert.2013.12.031
11. Chen YQ, Fang RL, Luo YN, Luo CQ. 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. DOI:10.1186/s12905-016-0341-3
12. Аскар Е., Валиев Р.К., Рыбина А.Н., Ауелбекова А.К. Хронический эндометрит – современные представления, принципы ведения. Обзор литературы. Репродуктивная медицина. 2020;4(45):16-24 [Askar E, Valiev RK, Rybina AN, Auelbekova AK. Chronic endometritis – modern concepts, principles of maintenance. Literature review. Reproductive Medicine. 2020;4(45):16-24 (in Russian)]. DOI:10.37800/RM2020-1-31
13. Liu Y, Ko EY, Wong KK, et al. Endometrial microbiota in infertile women with and without chronic endometritis 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
14. 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;263:25-32. DOI:10.1016/j.ejogrb.2021.05.045
15. Tanaka SE, Sakuraba Y, Kitaya K, Ishikawa T. Differential Vaginal Microbiota Profiling in Lactic-Acid-Producing Bacteria between Infertile Women with and without Chronic Endometritis. Diagnostics. 2022;12(4):878. DOI:10.3390/diagnostics12040878
16. Lüll K, Saare M, Peters M, et al. Differences in microbial profile of endometrial fluid and tissue samples in women with in vitro fertilization failure are driven by Lactobacillus abundance. Acta Obstet Gynecol Scand. 2022;101(2):212-20. DOI:10.1111/aogs.14297
17. Cicinelli E, De Ziegler D, Nicoletti R, et al. Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis. Gynecol Obstet Invest. 2009;68(2):108-15. DOI:10.1159/000223819
18. Buzzaccarini G, Vitagliano A, Andrisani A, 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. DOI:10.1007/s10815-020-01955-8
19. 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 [Orazov MR, Mikhaleva LM, Ismayilzade SY, et al. Intrauterine synechiae and chronic endometritis – is there a causal relationship? Gynecology. 2022;24(2):144-9 (in Russian)]. DOI:10.26442/20795696.2022.2.201417
20. Huang W, Liu B, He 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. DOI:10.1016/j.jri.2020.103146
21. Cicinelli E, Haimovich S, De Ziegler D, et al. 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
22. Song D, Li TC, Zhang Y, et al. Correlation between hysteroscopy findings and chronic endometritis. Fertil Steril. 2019;111(4):772-9. DOI:10.1016/j.fertnstert.2018.12.007
23. 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 [Orazov MR, Silantieva ES, Orekhov RE, et al. Repeated Implantation Failures: Etiology And Physiotherapy Possibilities. Difficult Patient. 2020;18(8-9):20-4 (in Russian)]. 
DOI:10.24411/2074-1995-2020-10055
24. Зиновьева О.С., Мотовилова Т.М., Качалина Т.С., и др. Влияние сочетанной плацентарной терапии и инфракрасного спектра лазера на гемодинамические нарушения в гипопластичном эндометрии. Медицинский альманах. 2018;6(57):94-7 [Zinovieva OS, Motovilova TM, Kachalina TS, et al. Effect of combined placental therapy and infrared laser spectrum on hemodynamic disturbances in hypoplastic endometrium. Medical Almanac. 2018;6(57):94-7 (in Russian)]. DOI:10.21145/2499-9954-2018-6-94-97
25. Song D, He Y, Wang Y, 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. DOI:10.1016/j.fertnstert.2020.12.019
26. Cicinelli E, Resta L, Loizzi V, et al. Antibiotic therapy versus no treatment for chronic endometritis: a case-control study. Fertil Steril. 2021;115(6):1541-8. DOI:10.1016/j.fertnstert.2021.01.018
27. Gay C, Hamdaoui N, Pauly V, et al. Impact of antibiotic treatment for chronic endometritis on unexplained recurrent pregnancy loss. J Gynecol Obstet Hum Reprod. 2021;50(5):102034. DOI:10.1016/j.jogoh.2020.102034
28. 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 [Radzinsky VE, Orazov MR, Toktar LR, et al. The scattered puzzle effect: implantation disorders in chronic endometritis. Gynecology. 2020;22(6)93-100 (in Russian)]. 
DOI:10.26442/20795696.2020.6.200493
29. Duan H, Li X, Hao Y, et al. Risk of spontaneous abortion after antibiotic therapy for chronic endometritis before in vitro fertilization and intracytoplasmic sperm injection stimulation. Fertil Steril. 2022;118(2):337-46. DOI:10.1016/j.fertnstert.2022.04.026
30. 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. DOI:10.1007/s10815-022-02558-1
31. 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):1002-10.e2. DOI:10.1016/j.fertnstert.2019.01.006
32. de Ziegler D, Pirtea P, Ayoubi JM. Inflammation and uterine fibrosis: the possible role of chronic endometritis. Fertil Steril. 2019;111(5):890-1. DOI:10.1016/j.fertnstert.2019.02.005
33. Тапильская Н.И., Савичева А.М., Шалепо К.В., Копылова А.А. Опыт лечения хронического эндометрита. Гинекология. 2020;22(4):68-70 [Tapilskaya NI, Savicheva AM, Shalepo KV, Kopylova A.A. Experience in the treatment of chronic endometritis. Gynecology. 2020;22(4):68-70 (in Russian)]. DOI:10.26442/20795696.2020.4.200312
34. Балан В.Е., Журавель А.С. Возможности применения препаратов, содержащих гиалуроновую кислоту, в гинекологии. Эффективная фармакотерапия. 2014;23:50-4 [Balan VYe, Zhuravel AS. Opportunities for using hyaluronic acid-containing drugs in gynecology. Effektivnaia farmakoterapiia. 2014;23:50-4 (in Russian)].
35. Вартанян Э.В., Девятова Е.А., Цатурова К.А., Аглямова Д.Р. Роль системной терапии при бесплодии и неудачах реализации репродуктивной функции. Акушерство, гинекология и репродукция. 2018;12(1):5-16 [Vartanyan EV, Devyatova EA, Tsaturova KA, Aglyamova DR. Role of combined therapy in the treatment of patients with infertility and reproductive failures. Obstetrics, Gynecology and Reproduction. 2018;12(1):5-16 (in Russian)]. DOI:10.17749/2313-7347.2018.12.1.005-015

________________________________________________

1. The World Health Organization. Infertility. Available at https://www.who.int/health-topics/infertility#tab=tab_1. Accessed: 07.09.2022.
2. Tamrakar SR, Bastakoti R. Determinants of Infertility in Couples. J Nepal Health Res Counc. 2019;17(1):85-9. DOI:10.33314/jnhrc.1827
3. Sallée C, Margueritte F, Marquet P, et al. Uterine Factor Infertility, a Systematic Review. J Clin Med. 2022;11(16):4907. DOI:10.3390/jcm11164907
4. Michels TC. Chronic endometritis. Am Fam Physician. 1995;52(1):217-22.
5. Kimura F, Takebayashi A, Ishida M, et al. Review: Chronic endometritis and its effect on reproduction. J Obstet Gynaecol Res. 2019;45(5):951-60. DOI:10.1111/jog.13937
6. Puente E, Alonso L, Laganà AS, et al. Chronic Endometritis: Old Problem, Novel Insights and Future Challenges. Int J Fertil Steril. 2020;13(4):250-6. DOI:10.22074/ijfs.2020.5779
7. Vitagliano A, Saccardi C, Litta P, Noventa M. Chronic endometritis: Really so relevant in repeated IVF failure? Am J Reprod Immunol. 2017;78(6). DOI:10.1111/aji.12758
8. Johnston-MacAnanny EB, Hartnett J, Engmann LL, et al. Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 2010;93(2):437-41. DOI:10.1016/j.fertnstert.2008.12.131
9. Vitagliano A, Noventa M, Gizzo S. Autoimmunity, systemic inflammation, and their correlation with repeated implantation failure and recurrent miscarriage: is chronic endometritis the missing piece of the jigsaw? Am J Reprod Immunol. 2017;77(1). DOI:10.1111/aji.12597
10. McQueen DB, Bernardi LA, Stephenson MD. Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil Steril. 2014;101(4):1026-30. DOI:10.1016/j.fertnstert.2013.12.031
11. Chen YQ, Fang RL, Luo YN, Luo CQ. 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. DOI:10.1186/s12905-016-0341-3
12. Askar E, Valiev RK, Rybina AN, Auelbekova AK. Chronic endometritis – modern concepts, principles of maintenance. Literature review. Reproductive Medicine. 2020;4(45):16-24 (in Russian). DOI:10.37800/RM2020-1-31
13. Liu Y, Ko EY, Wong KK, et al. Endometrial microbiota in infertile women with and without chronic endometritis 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
14. 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;263:25-32. DOI:10.1016/j.ejogrb.2021.05.045
15. Tanaka SE, Sakuraba Y, Kitaya K, Ishikawa T. Differential Vaginal Microbiota Profiling in Lactic-Acid-Producing Bacteria between Infertile Women with and without Chronic Endometritis. Diagnostics. 2022;12(4):878. DOI:10.3390/diagnostics12040878
16. Lüll K, Saare M, Peters M, et al. Differences in microbial profile of endometrial fluid and tissue samples in women with in vitro fertilization failure are driven by Lactobacillus abundance. Acta Obstet Gynecol Scand. 2022;101(2):212-20. DOI:10.1111/aogs.14297
17. Cicinelli E, De Ziegler D, Nicoletti R, et al. Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis. Gynecol Obstet Invest. 2009;68(2):108-15. DOI:10.1159/000223819
18. Buzzaccarini G, Vitagliano A, Andrisani A, 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. DOI:10.1007/s10815-020-01955-8
19. Orazov MR, Mikhaleva LM, Ismayilzade SY, et al. Intrauterine synechiae and chronic endometritis – is there a causal relationship? Gynecology. 2022;24(2):144-9 (in Russian). DOI:10.26442/20795696.2022.2.201417
20. Huang W, Liu B, He 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. DOI:10.1016/j.jri.2020.103146
21. Cicinelli E, Haimovich S, De Ziegler D, et al. 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
22. Song D, Li TC, Zhang Y, et al. Correlation between hysteroscopy findings and chronic endometritis. Fertil Steril. 2019;111(4):772-9. DOI:10.1016/j.fertnstert.2018.12.007
23. Orazov MR, Silantieva ES, Orekhov RE, et al. Repeated Implantation Failures: Etiology And Physiotherapy Possibilities. Difficult Patient. 2020;18(8-9):20-4 (in Russian). 
DOI:10.24411/2074-1995-2020-10055
24. Zinovieva OS, Motovilova TM, Kachalina TS, et al. Effect of combined placental therapy and infrared laser spectrum on hemodynamic disturbances in hypoplastic endometrium. Medical Almanac. 2018;6(57):94-7 (in Russian). DOI:10.21145/2499-9954-2018-6-94-97
25. Song D, He Y, Wang Y, 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. DOI:10.1016/j.fertnstert.2020.12.019
26. Cicinelli E, Resta L, Loizzi V, et al. Antibiotic therapy versus no treatment for chronic endometritis: a case-control study. Fertil Steril. 2021;115(6):1541-8. DOI:10.1016/j.fertnstert.2021.01.018
27. Gay C, Hamdaoui N, Pauly V, et al. Impact of antibiotic treatment for chronic endometritis on unexplained recurrent pregnancy loss. J Gynecol Obstet Hum Reprod. 2021;50(5):102034. DOI:10.1016/j.jogoh.2020.102034
28. Radzinsky VE, Orazov MR, Toktar LR, et al. The scattered puzzle effect: implantation disorders in chronic endometritis. Gynecology. 2020;22(6)93-100 (in Russian). 
DOI:10.26442/20795696.2020.6.200493
29. Duan H, Li X, Hao Y, et al. Risk of spontaneous abortion after antibiotic therapy for chronic endometritis before in vitro fertilization and intracytoplasmic sperm injection stimulation. Fertil Steril. 2022;118(2):337-46. DOI:10.1016/j.fertnstert.2022.04.026
30. 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. DOI:10.1007/s10815-022-02558-1
31. 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):1002-10.e2. DOI:10.1016/j.fertnstert.2019.01.006
32. de Ziegler D, Pirtea P, Ayoubi JM. Inflammation and uterine fibrosis: the possible role of chronic endometritis. Fertil Steril. 2019;111(5):890-1. DOI:10.1016/j.fertnstert.2019.02.005
33. Тапильская Н.И., Савичева А.М., Шалепо К.В., Копылова А.А. Опыт лечения хронического эндометрита. Гинекология. 2020;22(4):68-70 [Tapilskaya NI, Savicheva AM, Shalepo KV, Kopylova A.A. Experience in the treatment of chronic endometritis. Gynecology. 2020;22(4):68-70 (in Russian)]. DOI:10.26442/20795696.2020.4.200312
34. Balan VYe, Zhuravel AS. Opportunities for using hyaluronic acid-containing drugs in gynecology. Effektivnaia farmakoterapiia. 2014;23:50-4 (in Russian).
35. Vartanyan EV, Devyatova EA, Tsaturova KA, Aglyamova DR. Role of combined therapy in the treatment of patients with infertility and reproductive failures. Obstetrics, Gynecology and Reproduction. 2018;12(1):5-16 (in Russian). DOI:10.17749/2313-7347.2018.12.1.005-015

К.В. Краснопольская1,2, Л.М. Михалева3, М.Р. Оразов*4, Е.Д. Долгов4

1 ГБУЗ МО «Московский областной научно-исследовательский институт акушерства и гинекологии», Москва, Россия;
2 ООО «ПРИОР КЛИНИКА», Москва, Россия;
3 ФГБНУ «Российский научный центр хирургии им. акад. Б.В. Петровского», Москва, Россия;
4 ФГАОУ ВО «Российский университет дружбы народов», Москва, Россия
*omekan@mail.ru

________________________________________________

Kseniya V. Krasnopolskaya1,2, Liudmila M. Mikhaleva3, Mekan R. Orazov*4, Evgeny D. Dolgov4

1 Moscow Regional Research Institute of Obstetrics and Gynecology, Moscow, Russia;
2 PRIOR CLINIC, Moscow, Russia;
3 Petrovsky National Research Center of Surgery, Moscow, Russia;
4 People’s Friendship University of Russia (RUDN University), Moscow, Russia
*omekan@mail.ru