Reproductive outcomes after different treatment and secondary prevention options for Asherman syndrome

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Asherman syndrome is characterized by the appearance of clinical symptoms of pain syndrome, as well as menstrual and reproductive dysfunction, which develop as a result of obliteration of the uterine cavity and/or cervical canal by connective tissue synechiae. It is believed that the leading cause of Asherman syndrome is mechanical damage to the basal layer of the endometrium due to intrauterine interventions performed during pregnancy, the postpartum period, or in the detection of uterine cavity pathologies. They lead to impaired cervico-uterine-tubal sperm transport, fibrotic changes in the endometrium, and resistance to hormonal stimulation.

The primary surgical treatment for Asherman syndrome is hysteroscopic adhesiolysis. It is known that this type of surgical intervention is associated with high risks of synechiae reformation, complicated course of gestation and unsatisfactory reproductive outcomes. For this reason, in the postoperative period, it is advisable to carry out preventive measures aimed at restoring female reproductive function. Most of the currently available methods of secondary prevention have no effect on the pregnancy rate and live birth rate. Low efficacy of the complex therapy creates a need to search for new alternative approaches to the treatment of Asherman syndrome and to develop tactics for postoperative management of patients. Cell therapy with mesenchymal stem cells is of particular interest.

This literature review examines the relationship between various treatment and secondary prevention options for Asherman syndrome and their impact on improving reproductive outcomes.

Full Text

Restricted Access

About the authors

Kamil R. Bakhtiyarov

I.M. Sechenov First Moscow State Medical University

Email: doctorbah@mail.ru
ORCID iD: 0000-0001-7114-4050
SPIN-code: 4820-1340

MD, Dr. Sci. (Medicine)

Russian Federation, Moscow

Irina V. Ignatko

I.M. Sechenov First Moscow State Medical University

Email: ignatko_i_v@staff.sechenov.ru
ORCID iD: 0000-0002-9945-3848
SPIN-code: 8073-1817

MD, Dr. Sci. (Medicine), Professor, Corresponding Member of the Russian Academy of Sciences

Russian Federation, Moscow

Alina S. Zueva

I.M. Sechenov First Moscow State Medical University

Author for correspondence.
Email: alina-zueva02@mail.ru
ORCID iD: 0009-0001-9755-2201
SPIN-code: 6190-4779
Russian Federation, Moscow

Tatyana D. Kapyrina

I.M. Sechenov First Moscow State Medical University

Email: tatya-kapyri@yandex.ru
ORCID iD: 0009-0004-7414-2471
SPIN-code: 8659-5885

MD

Russian Federation, Moscow

References

  1. Khirieva PM, Adamyan LV, Martynov SA. Modern methods of prevention and treatment of intrauterine synechiae (literature review). Gynecology. 2016;8(5):32–36. EDN: XQRZXZ doi: 10.26442/2079-5696_18.5.32-36
  2. Njagi P, Groot W, Arsenijevic J, et al. Financial costs of assisted reproductive technology for patients in low- and middle-income countries: a systematic review. Hum Reprod Open. 2023;2023(2):hoad007. doi: 10.1093/hropen/hoad007
  3. Makarenko TA, Nikiforova DE, Ulyanova IO. Intrauterine synechiae: features of surgical treatment and prevention of relapses. Medical Council. 2018;(7):146–151. EDN: YWRKYF doi: 10.21518/2079-701X-2018-7-146-151
  4. Orazov MR, Mikhaleva LM, Ismailzade SYa. Risk factors for intrauterine adhesions in women of reproductive age. Medical Herald of the South of Russia. 2022;13 (2):86–90. (In Russ.) EDN: EXXYBF doi: 10.21886/2219-8075-2022-13-2-86-90
  5. Arutyunova EE, Buralkina NA, Chuprynin VD, et al. Pathogenetic rationale and experience with the use of anti-speckling gel in patients with intrauterine synechiae after surgical hysteroscopy. Medical Council. 2018(13):160–164. EDN: RZRRAD doi: 10.21518/2079-701X-2018-13-160-164
  6. Bespalova AG, Popov AA, Fedorov AA, et al. Intrauterine synechiae in the reproductive age: a comprehensive approach to solving the problem. Russian Bulletin of Obstetrician-Gynecologist. 2021;21(2):62–67. EDN: JWDKJF doi: 10.17116/rosakush20212102162
  7. Khan Z. Etiology, risk factors, and management of Asherman Syndrome. Obstet Gynecol. 2023;142(3):543–554. doi: 10.1097/AOG.0000000000005309
  8. Dreisler E, Kjer JJ. Asherman’s syndrome: current perspectives on diagnosis and management. Int J Womens Health. 2019;20;11:191–198. doi: 10.2147/IJWH.S165474
  9. Freedman MF, Schlaff WD. Avoiding Asherman’s syndrome: refining our approach to uterine evacuation. Fertil Steril. 2021;116(4):961–962. doi: 10.1016/j.fertnstert.2021.06.037
  10. Drobyazko PA, Aksenova AA. Comprehensive prevention of Asherman syndrome in intrauterine surgery. clinical examples. International Research Journal. 2023;6:61. EDN: LGTVFG doi: 10.23670/IRJ.2023.132.4
  11. March CM. Management of Asherman’s syndrome. Reprod Biomed Online. 2011;23(1):63–76. doi: 10.1016/j.rbmo.2010.11.018
  12. Wang ZN, Wang MS, Xi X. Clinical evidence of positive correlation between intrauterine adhesions and chronic endometritis: a retrospective study. Eur Rev Med Pharmacol Sci. 2023;27(10):4601–4607. doi: 10.26355/eurrev_202305_32467
  13. 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
  14. 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):986–992. doi: 10.1002/ijgo.14434
  15. Liu Z, Kong Y, Gao Y, et al. Revealing the interaction between intrauterine adhesion and vaginal microbiota using highthroughput sequencing. Mol Med Rep. 2019;19:4167–4174. doi: 10.3892/mmr.2019.10092
  16. Qiu T, Liu L, Zhou H, et al. Analysis of endometrial microbiota in intrauterine adhesion by high-throughput sequencing. Ann Transl Med. 2021;9(3):195. doi: 10.21037/atm-20-2813
  17. Manchanda R, Rathore A, Carugno J, et al. Classification systems of Asherman’s syndrome. An old problem with new directions. Minim Invasive Ther Allied Technol. 2021;30(5):304–310. doi: 10.1080/13645706.2021.1893190
  18. Lee WL, Liu CH, Cheng M, et al. Focus on the primary prevention of intrauterine adhesions: current concept and vision. Int J Mol Sci. 2021;22(10):5175. doi: 10.3390/ijms22105175
  19. Hooker AB, de Leeuw RA, Emanuel MH, et al. The link between intrauterine adhesions and impaired reproductive performance: a systematic review of the literature. BMC Pregnancy Childbirth. 2022;22(1):837. doi: 10.1186/s12884-022-05164-2
  20. AAGL Elevating Gynecologic Surgery. AAGL practice report: practice guidelines on intrauterine adhesions developed in collaboration with the European Society of Gynaecological Endoscopy (ESGE). J Minim Invasive Gynecol. 2017;24(5):695–705. doi: 10.1016/j.jmig.2016.11.008
  21. Di Guardo F, Della Corte L, Vilos GA, et al. Evaluation and treatment of infertile women with Asherman syndrome: an updated review focusing on the role of hysteroscopy. Reprod Biomed Online. 2020;41(1):55–61. doi: 10.1016/j.rbmo.2020.03.021
  22. Yang L, Wang L, Chen Y, et al. Cold scissors versus electrosurgery for hysteroscopic adhesiolysis: a meta-analysis. Medicine. 2021;100(17):e25676. doi: 10.1097/MD.0000000000025676
  23. Makarenko TA, Nikiforova DE. Current options in the treatment of Asherman syndrome. Russian Medical Journal. 2016;24(15):1001–1004. EDN: WYYOBT
  24. Thomson AJ, Abbott JA, Kingston A, et al. Fluoroscopically guided synechiolysis for patients with Asherman’s syndrome: menstrual and fertility outcomes. Fertil Steril. 2007;87(2):405–410. doi: 10.1016/j.fertnstert.2006.06.035
  25. Morales B, Movilla P, Wang J, et al. Patient-reported menstrual and obstetric outcomes following hysteroscopic adhesiolysisfor Asherman syndrome. FS Rep. 2021;2(1):118–125. doi: 10.1016/j.xfre.2021.01.002
  26. Baradwan S, Alharbi D, Bashir MS, et al. Short and long-term reproductive outcomes after hysteroscopic adhesiolysis for infertile women. JBRA Assist Reprod. 2023;27(2):191–196. doi: 10.5935/1518-0557.20220016
  27. Siferih M, Gebre T, Hunduma F, et al. Review of Asherman syndrome and its hysteroscopic treatment outcomes: experience in a low-resource setting. BMC Women’s Health. 2024;4(1):99. doi: 10.1186/s12905-024-02944-0
  28. Hansen BB, Nøhr B. Surgical treatment of Asherman syndrome and reproductive outcome. Dan Med J. 2022;69(3):A09210736.
  29. Hanstede MMF, van der Meij E, Veersema S, et al. Live births after Asherman syndrome treatment. Fertil Steril. 2021;116(4):1181–1187. doi: 10.1016/j.fertnstert.2021.05.099
  30. Guo EJ, Wah Chung JP, Li TC. Reproductive outcomes after surgical treatment of Asherman syndrome: a systematic review. Best Pract Res Clin Obstet Gynaecol. 2019;59:98–114. doi: 10.1016/j.bpobgyn.2018.12.009
  31. Xu W, Zhang Y, Yang Y, et al. Effect of early second-look hysteroscopy on reproductive outcomes after hysteroscopic adhesiolysis in patients with intrauterine adhesion, a retrospective study in China. Int J Surg. 2018;50:49–54. doi: 10.1016/j.ijsu.2017.11.040
  32. Yu D, Li TC, Xia E, et al. Factors affecting reproductive outcome of hysteroscopic adhesiolysis for Asherman’s syndrome. Fertil Steril. 2008;89(3):715–722. doi: 10.1016/j.fertnstert.2007.03.070
  33. Sebbag L, Even M, Fay S, et al. Early second-look hysteroscopy: prevention and treatment of intrauterine post-surgical adhesions. Front Surg. 2019;6:50. doi: 10.3389/fsurg.2019.00050
  34. Orhue AA, Aziken ME, Igbefoh JO. A comparison of two adjunctive treatments for intrauterine adhesions following lysis. Int J Gynaecol Obstet. 2003;82(1):49–56. doi: 10.1016/s0020-7292(03)00030-4
  35. Wang Y, Zhao Y, Ge Y, et al. Reproductive outcomes and reproductive tract microbiota shift in women with moderate-to-severe intrauterine adhesions following 30-day post-hysteroscopic placement of balloon stents or intrauterine contraceptive devices: a randomized controlled trial. EClinicalMedicine. 2022;43:101200. doi: 10.1016/j.eclinm.2021.101200
  36. Zhuang LL, Wang K, Shen HL, et al. A comparison of special intrauterine balloons and intrauterine contraceptive devices in the treatment of intrauterine adhesions. Arch Gynecol Obstet. 2023;307(6):1873–1882. doi: 10.1007/s00404-023-06993-y
  37. Cai H, Qiao L, Song K, He Y. Oxidized, regenerated cellulose adhesion barrier plus intrauterine device prevents recurrence after adhesiolysis for moderate to severe intrauterine adhesions. J Minim Invasive Gynecol. 2017;24(1):80–88. doi: 10.1016/j.jmig.2016.09.021
  38. Torres-De La Roche LA, Campo R, Devassy R, et al. Adhesions and anti-adhesion systems highlights. Facts Views Vis Obgyn. 2019;11(2):137–149.
  39. Orazov MR, Mikhaleva LM, Silant’eva ES, et al. Efficacy of hyaluronic acid-based anti-speckling gels in the antiretroviral therapy of intrauterine synechiae. Difficult patient. 2021;19(6):26–31. EDN: ABTJOB doi: 10.224412/2074-1005-2021-6-26-31
  40. Dou Y, Yu T, Li Z, et al. Short- and long-term outcomes of postoperative intrauterine application of hyaluronic acid gel: a meta-analysis of randomized controlled trials. J Minim Invasive Gynecol. 2022;29(8):934–942. doi: 10.1016/j.jmig.2022.05.006
  41. Thubert T, Dussaux C, Demoulin G, et al. Influence of auto-cross-linked hyaluronic acid gel on pregnancy rate and hysteroscopic outcomes following surgical removal of intra-uterine adhesions. Eur J Obstet Gynecol Reprod Biol. 2015;193:65–69. doi: 10.1016/j.ejogrb.2015.06.025
  42. Zhou Q, Shi X, Saravelos S, et al. Auto-cross-linked hyaluronic acid gel for prevention of intrauterine adhesions after hysteroscopic adhesiolysis: a randomized controlled trial. J Minim Invasive Gynecol. 2021;28(2):307–313. doi: 10.1016/j.jmig.2020.06.030
  43. Fei Z, Bin Z, Xin X, et al. Meta-analysis on the use of hyaluronic acid gel to prevent recurrence of intrauterine adhesion after hysteroscopic adhesiolysis. Taiwan J Obstet Gynecol. 2019;58(6):731–736. doi: 10.1016/j.tjog.2019.09.002
  44. Trinh TT, Nguyen KD, Pham HV, et al. Effectiveness of hyaluronic acid gel and intrauterine devices in prevention of intrauterine adhesions after hysteroscopic adhesiolysis in infertile women. J Minim Invasive Gynecol. 2022;29(2):284–290. doi: 10.1016/j.jmig.2021.08.010
  45. Hanstede MMF, van Stralen KJ, Molkenboer JFM, et al. Hormonal support in women with Asherman syndrome does not lead to better outcomes: a randomized trial. Reprod Med Biol. 2023;22(1):e12526. doi: 10.1002/rmb2.12526
  46. Yang L, Ma N, Song D, et al. The Effect of estrogen in the prevention of adhesion reformation after hysteroscopic adhesiolysis: a prospective randomized control trial. J Minim Invasive Gynecol. 2022;29(7):871–878. doi: 10.1016/j.jmig.2022.04.004
  47. Guo T, Zeng N, Yang J, et al. The clinical effects of antibiotic prophylaxis for hysteroscopic procedures: a meta-analysis. Medicine (Baltimore). 2019;98(34):e16964. doi: 10.1097/MD.0000000000016964
  48. Liu F, Hu S, Wang S, et al. Cell and biomaterial-based approaches to uterus regeneration. Regen Biomater. 2019;6(3):141–148. doi: 10.1093/rb/rbz021
  49. Sukhikh GT, Chernukha GE, Tabeeva GI, et al. Current possibilities of cell therapy for Asherman’s syndrome. Obstetrics and Gynecology. 2018;5:20–28. EDN: XOSMUX doi: 10.18565/aig.2018.5.20-28
  50. Benor A, Gay S, DeCherney AJ. An update on stem cell therapy for Asherman syndrome. J Assist Reprod Genet. 2020;37:1511–1529. doi: 10.1007/s10815-020-01801-x
  51. Novikova PV, Domnina AP. Possibility of using stem cells of bone marrow origin for the treatment of Asherman’s syndrome in experiments. Journal of Obstetrics and Women’s Diseases. 2016;65(S1):68–69. EDN: YHVHKZ
  52. Tersoglio AE, Tersoglio S, Salatino DR, et al. Regenerative therapy by endometrial mesenchymal stem cells in thin endometrium with repeated implantation failure. A novel strategy. JBRA Assist Reprod. 2020;24(2):118–27. doi: 10.5935/1518-0557.20190061
  53. Ma H, Liu M, Li Y, et al. Intrauterine transplantation of autologous menstrual blood stem cells increases endometrial thickness and pregnancy potential in patients with refractory intrauterine adhesion. J Obstet Gynaecol Res. 2020;46(11):2347–2355. doi: 10.1111/jog.14449
  54. Saad-Naguib MH., Kenfack Y, Sherman LS, et al. Impaired receptivity of thin endometrium: therapeutic potential of mesenchymal stem cells. Front Endocrinol (Lausanne). 2024;14:1268990. doi: 10.3389/fendo.2023.1268990
  55. Kim JH, Park M, Paek JY, et al. Intrauterine infusion of human platelet-rich plasma improves endometrial regeneration and pregnancy outcomes in a murine model of Asherman’s syndrome. Front Physiol. 2020;11:105. doi: 10.3389/fphys.2020.00105.
  56. Tsygankova OYu, Kropmaer KP, Kravchenko EN. Experience with the use of platelet-containing autoplasm in the treatment of uterine synechiae. Mother and baby in Kuzbass. 2020;2(81):32–37. EDN: EAPYPU doi: 10.24411/2686-7338-2020-10019
  57. Tang R, Xiao X, He Y, et al. Clinical evaluation of autologous platelet-rich plasma therapy for intrauterine adhesions: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2023;14:1183209. doi: 10.3389/fendo.2023.1183209
  58. Tang R, Zhang W, Xiao X, et al. Intrauterine interventions options for preventing recurrence after hysteroscopic adhesiolysis: a systematic review and network meta-analysis of randomized controlled trials. Arch Gynecol Obstet. 2024;309(5):1847–1861. doi: 10.1007/s00404-024-07460-y
  59. Wang Z, Yang M, Mao L, et al. Efficacy and safety of autologous platelet-rich fibrin for the treatment of infertility with intrauterine adhesions. J Obstet Gynaecol Res. 2021;47(11):3883–3894. doi: 10.1111/jog.14964
  60. Wang S, Duan H, Li B, et al. Efficacy of freeze-dried amnion grafts on cytokines in uterine exudates following hysteroscopic adhesiolysis of severe intrauterine adhesions. Int J Gen Med. 2022;15:1703–1713. doi: 10.2147/IJGM.S333836
  61. Zheng F, Zhu B, Liu Y, et al. Meta-analysis of the use of amniotic membrane to prevent recurrence of intrauterine adhesion after hysteroscopic adhesiolysis. Int J Gynaecol Obstet. 2018;143(2):145–149. doi: 10.1002/ijgo.12635
  62. Jones BP, Vali S, Saso S, Garcia-Dominguez X, et al. Endometrial autotransplantation in rabbits: Potential for fertility restoration in severe Asherman’s syndrome. Eur J Obstet Gynecol Reprod Biol. 2020;248:14–23. doi: 10.1016/j.ejogrb.2020.03.011

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Eсо-Vector



СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 66759 от 08.08.2016 г. 
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия Эл № 77 - 6389
от 15.07.2002 г.