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Yarmolinskaya M.I.

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology;
I.I. Mechnikov North-Western State Medical University

Adamyan L.V.

Moscow State Medical and Dental University named after A.I. Evdokimov

Endometriosis-associated pain and adhesions — new pathogenetic aspects and therapeutic approach

Authors:

Yarmolinskaya M.I., Adamyan L.V.

More about the authors

Journal: Russian Journal of Human Reproduction. 2023;29(2): 93‑100

Read: 3051 times


To cite this article:

Yarmolinskaya MI, Adamyan LV. Endometriosis-associated pain and adhesions — new pathogenetic aspects and therapeutic approach. Russian Journal of Human Reproduction. 2023;29(2):93‑100. (In Russ.)
https://doi.org/10.17116/repro20232902193

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References:

  1. Janša V, Klančič T, Pušić M, Klein M, Vrtačnik Bokal E, Ban Frangež H, Rižner TL. Proteomic analysis of peritoneal fluid identified COMP and TGFBI as new candidate biomarkers for endometriosis. Scientific Reports. 2021;11(1):20870. https://doi.org/10.1038/s41598-021-00299-2
  2. Endometrioz. Klinicheskie rekomendatsii. M.: Ministerstvo zdravooxraneniya Rossijskoj Federacii; 2020. Accessed March 11, 2023. (In Russ.). https://minzdrav.samregion.ru/wp-content/uploads/sites/28/2020/12/endometrioz.pdf?ysclid=lfgnra6oc3298261126
  3. Becker CM, Bokor A, Heikinheimo O, Horne A, Jansen F, Kiesel L, King K, Kvaskoff M, Nap A, Petersen K, Saridogan E, Tomassetti C, van Hanegem N, Vulliemoz N, Vermeulen N; ESHRE Endometriosis Guideline Group. ESHRE guideline: endometriosis. Human Reproduction Open. 2022(2):2022,hoac009. https://doi.org/10.1093/hropen/hoac009
  4. Zheng P, Zhang W, Leng J, Lang J. Research on central sensitization of endometriosis-associated pain: a systematic review of the literature. Pain Research. 2019(12):1447-1456. https://doi.org/10.2147/JPR.S197667
  5. Adamyan LV, Aznaurova YaB. Molecular aspects of endometriosis. Russian Journal of Human Reproduction. 2015;21(2):66-77. (In Russ.). https://doi.org/10.17116/repro201521266-77
  6. Koninckx PR, Ussia A, Adamyan L, Wattiez A, Gomel V, Martin DC. Pathogenesis of endometriosis: the genetic/epigenetic theory. Fertility and Sterility. 2019;111(2):327-340.  https://doi.org/10.1016/j.fertnstert.2018.10.013
  7. Koninckx PR, Gomel V, Ussia A, Adamyan L. Role of the peritoneal cavity in the prevention of postoperative adhesions, pain, and fatigue. Fertility and Sterility. 2016;106(5):998-1010. https://doi.org/10.1016/j.fertnstert.2016.08.012
  8. Guo SW. Fibrogenesis resulting from cyclic bleeding: the Holy Grail of the natural history of ectopic endometrium. Human Reproduction. 2018;33(3):353-356.  https://doi.org/10.1093/humrep/dey015
  9. Richter K, Konzack A, Pihlajaniemi T, Heljasvaara R, Kietzmann T. Redox-fibrosis: impact of TGFβ1 on ROS generators, mediators and functional consequences. Redox Biology. 2015;6:344-352.  https://doi.org/10.1016/j.redox.2015.08.015
  10. Anaf V, Simon P, Fayt I, Noel J. Smooth muscles are frequent components of endometriotic lesions. Human Reproduction. 2000;15(4): 767-771.  https://doi.org/10.1093/humrep/15.4.767
  11. Leyendecker G, Herbertz M, Kunz G, Mall G. Endometriosis results from the dislocation of basal endometrium. Human Reproduction. 2002;17(10):2725-2736. https://doi.org/10.1093/humrep/17.10.2725
  12. Guo SW, Ding D, Geng JG, Wang L, Liu X. P-selectin as a potential therapeutic target for endometriosis. Fertility and Sterility. 2015; 103(4):990-1000. https://doi.org/10.1016/j.fertnstert.2015.01.001
  13. Guo SW, Du Y, Liu X. Endometriosis-derived stromal cells secrete thrombin and thromboxane A2, inducing platelet activation. Reproductive Sciences. 2016;23(8):1044-1052. https://doi.org/10.1177/1933719116630428
  14. Ding D, Liu X, Duan J, Guo SW. Platelets are an unindicted culprit in the development of endometriosis: clinical and experimental evidence. Human Reproduction. 2015;30(4):812-832.  https://doi.org/10.1093/humrep/dev025
  15. Zhang Q, Duan J, Olson M, Fazleabas A, Guo SW. Cellular Changes Consistent with Epithelial-Mesenchymal Transition and Fibroblast-to-Myofibroblast Transdifferentiation in the Progression of Experimental Endometriosis in Baboons. Reproductive Sciences. 2016;23(10):1409-1421. https://doi.org/10.1177/1933719116641763
  16. Zhang Q, Duan J, Liu X, Guo SW. Platelets drive smooth muscle metaplasia and fibrogenesis in endometriosis through epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation. Molecular and Cellular Endocrinology. 2016;428:431.  https://doi.org/10.1016/j.mce.2016.03.015
  17. Shi LB, Zhou F, Zhu HY, Huang D, Jin XY, Li C, Dai Y, Pan YB, Zhang SY. Transforming growth factor beta1 from endometriomas promotes fibrosis in surrounding ovarian tissues via Smad2/3 signaling. Biology of Reproduction. 2017;97(6):873-882.  https://doi.org/10.1093/biolre/iox140
  18. Nie J, Zhao C, Laganà AS, Liu X, Guo SW. Identification of lesional attributes of dysmenorrhea severity and the serum antimüllerian hormone levels in women with ovarian endometriomas. Fertility and Sterility. 2022;118(1):191-202.  https://doi.org/10.1016/j.fertnstert.2022.04.016
  19. Guo SW, Ding D, Shen M, Liu X. Dating Endometriotic Ovarian Cysts Based on the Content of Cyst Fluid and its Potential Clinical Implications. Reproductive Sciences. 2015;22(7):873-883.  https://doi.org/10.1177/1933719115570907
  20. Burns KA, Thomas SY, Hamilton KJ, Young SL, Cook DN, Korach KS. Early endometriosis in females is directed by immune-mediated estrogen receptor alpha and IL-6 cross-talk. Endocrinology. 2018;159(1):103-118.  https://doi.org/10.1210/en.2017-00562
  21. Yarmolinskaya MI, Denisova VM. Immunomodulating therapy of endometriosis. Pharmateca. 2015;12(305):6-12. (In Russ.).
  22. Medikamentoznaya terapiya genital`nogo e`ndometrioza. Realii i perspektivy`. Rukovodstvo dlya vrachej. M.: GE`OTAR-Media; 2021. (In Russ).
  23. Capobianco A, Rovere-Querini P. Endometriosis, a disease of the macrophage. Frontiers in Immunology. 2013;4:9.  https://doi.org/10.3389/fimmu.2013.00009
  24. Ding D, Cai X, Zheng H, Guo SW, Liu X. Scutellarin Suppresses Platelet Aggregation and Stalls Lesional Progression in Mouse with Induced Endometriosis. Reproductive Sciences. 2019;26(11):1417-1428. https://doi.org/10.1177/1933719118817661
  25. Nie MF, Xie Q, Wu YH, He H, Zou LJ, She XL, Wu XQ. Serum and ectopic endometrium from women with endometriosis modulate macrophage M1/M2 polarization via the Smad2/Smad3 pathway. Journal of Immunology Research. 2018;6285813. https://doi.org/10.1155/2018/6285813
  26. Adamyan LV, Arslanyan KN, Loginova ON, Manukyan LM, Kharchenko EI. Immunological aspects of endometriosis: review of the literature. Lechaschiy vrach. 2020;(4):37. (In Russ.) https://doi.org/10.26295/OS.2020.29.10.007
  27. Symons LK, Miller JE, Kay VR, Marks RM, Liblik K, Koti M, Tayade C. The Immunopathophysiology of endometriosis. Trends in Molecular Medicine. 2018;24(9):748-762.  https://doi.org/10.1016/j.molmed.2018.07.004
  28. Duan J, Liu X, Wang H, Guo SW. The M2a macrophage subset may be critically involved in the fibrogenesis of endometriosis in mice. Reproductive Biomedicine Online. 2018;37(3):254-268.  https://doi.org/10.1016/j.rbmo.2018.05.017
  29. Novella-Maestre E, Herraiz S, Vila-Vives JM, Carda C, Ruiz-Sauri A, Pellicer A. Effect of antiangiogenic treatment on peritoneal endometriosis-associated nerve fibers. Fertility and Sterility. 2012; 98(5):1209-1217. https://doi.org/10.1016/j.fertnstert.2012.07.1103
  30. McKinnon B, Bersinger NA, Wotzkow C, Mueller MD. Endometriosis-associated nerve fibers, peritoneal fluid cytokine concentrations, and pain in endometriotic lesions from different locations. Fertility and Sterility. 2012;97(2):373-380.  https://doi.org/10.1016/j.fertnstert.2011.11.011
  31. Morotti M, Vincent K, Becker CM. Mechanisms of pain in endometriosis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2017;209:8-13.  https://doi.org/10.1016/j.ejogrb.2016.07.497
  32. Yu J, Francisco A, Patel BG, Cline JM, Zou E, Berga SL, Taylor RN. IL-1beta stimulates brain-derived neurotrophic factor production in eutopic endometriosis stromal cell cultures: a model for cytokine regulation of neuroangiogenesis. The American Journal of Pathology. 2018;188(10):2281-2292. https://doi.org/10.1016/j.ajpath.2018.06.011
  33. Peng B, Zhan H, Alotaibi F, Alkusayer GM, Bedaiwy MA, Yong PJ. Nerve growth factor is associated with sexual pain in women with endometriosis. Reproductive Sciences. 2018;25(4):540-549.  https://doi.org/10.1177/1933719117716778
  34. Howard FM. Endometriosis and mechanisms of pelvic pain. Journal of Minimally Invasive Gynecology. 2009;16(5):540-550.  https://doi.org/10.1016/j.jmig.2009.06.017
  35. Ding S, Zhu T, Tian Y, Xu P, Chen Z, Huang X, Zhang X. Role of brain-derived neurotrophic factor in endometriosis pain. Reproductive Sciences. 2018;25(7):1045-1057. https://doi.org/10.1177/1933719117732161
  36. Wang G, Tokushige N, Fraser IS. Nerve fibers and menstrual cycle in peritoneal endometriosis. Fertility and Sterility. 2011;95(8):2772-2774. https://doi.org/10.1016/j.fertnstert.2011.01.150
  37. Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Human Reproduction. 2009;24:827-834.  https://doi.org/10.1093/humrep/den464
  38. Arnold J, Barcena de Arellano ML, Rüster C, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Imbalance between sympathetic and sensory innervation in peritoneal endometriosis. Brain, Behavior, and Immunity. 2012;26(1):132-141.  https://doi.org/10.1016/j.bbi.2011.08.004
  39. Liang Y, Liu D, Yang F, Pan W, Zeng F, Wu J, Xie H, Li J, Yao S. Perineural invasion in endometriotic lesions contributes to endometriosis-associated pain. Journal of Pain Research. 2018;11:1999-2009. https://doi.org/10.2147/JPR.S168715
  40. Ianieri MM, Mautone D, Ceccaroni M. Recurrence in deep infiltrating endometriosis: a systematic review of the literature. Journal of Minimally Invasive Gynecology. 2018;25(5):786-793.  https://doi.org/10.1016/j.jmig.2017.12.025
  41. Kelm Junior AR, Lancellotti CL, Donadio N, Auge AP, Lima SM, Aoki T, Ribeiro PA. Nerve fibers in uterosacral ligaments of women with deep infiltrating endometriosis Journal of Reproductive Immunology. 2008;79(1):93-99.  https://doi.org/10.1016/j.jri.2008.08.004
  42. The LUNA Trial Collaboration. A randomised controlled trial to assess the efficacy of Laparoscopic Uterosacral Nerve Ablation (LUNA) in the treatment of chronic pelvic pain: The trial protocol [ISRCTN41196151]. BMC Womens Health. 2003;3(1):6.  https://doi.org/10.1186/1472-6874-3-6
  43. Khare VK, Martin DC, Eltorky MA. A comparative study of ovarian and pelvic wall-infiltrating endometriosis. The Journal of the American Association of Gynecologic Laparoscopists. 1996;3(2):235-239.  https://doi.org/10.1016/s1074-3804(96)80006-5
  44. Soni UK, Chadchan SB, Kumar V, Ubba V, Khan MTA, Vinod BSV, Konwar R, Bora HK, Rath SK, Sharma S, Jha RK. A high level of TGF-B1 promotes endometriosis development via cell migration, adhesiveness, colonization, and invasivenessdagger. Biology of Reproduction. 2019;100(4):917-938.  https://doi.org/10.1093/biolre/ioy242
  45. Young VJ, Ahmad SF, Duncan WC, Horne AW. The role of TGF-β in the pathophysiology of peritoneal endometriosis. Human Reproduction Update. 2017;23(5):548-559.  https://doi.org/10.1093/humupd/dmx016
  46. Coxon L, Horne AW, Vincent K. Pathophysiology of endometriosis-associated pain: a review of pelvic and central nervous system mechanisms. Best Practice and Research. Clinical Obstetrics and Gynaecology. 2018;51:53-67.  https://doi.org/10.1016/j.bpobgyn.2018.01.014
  47. Matsuzaki S, Darcha C, Pouly JL, Canis M. Effects of matrix stiffness on epithelial to mesenchymal transition-like processes of endometrial epithelial cells: Implications for the pathogenesis of endometriosis. Scientific Reports. 2017;7:44616. https://doi.org/10.1038/srep44616
  48. Liu X, Yan D, Guo SW. Sensory nerve-derived neuropeptides accelerate the development and fibrogenesis of endometriosis. Human Reproduction. 2019;34(3):452-468.  https://doi.org/10.1093/humrep/dey392
  49. De Wilde RL, Bakkum EA, Brölmann H. Consensus recommendations on adhesions (version 2014) for the ESGE Adhesions Research Working Group (European Society for Gynecological Endoscopy): an expert opinion. Archives of Gynecology and Obstetrics. 2014;290(3):581-582.  https://doi.org/10.1007/s00404-014-3312-7
  50. Yarmolinskaya MI, Selkov SA, Manuilova TYu., Bezhenar V.F., Rulev VV, Seljutin AV, Thazaplizheva SSh. The efficacy of the proteolytic medication longidaza in combined treatment of adhesions in patients with genital endometriosis. Immunologiya. 2015;36(2):116-121. (In Russ.).
  51. Yarmolinskaya MI. Cytokine profile of peritoneal fluid and peripheral blood in patients with pelvic endometriosis. Zhurnal akusherstva i zhenskix boleznej. 2008;3:30-34. (In Russ.).
  52. Yarmolinskaya MI, Radzinsky VE, Orazov MR, Korotkikh IN, Ziganshin OR, Eremina NA, Khobets VV. Evaluation of bovhyaluronidase azoxymer efficacy in combined treatment of patients with endometriosis based on the results of multicenter prospective non-interventional study (ISLAND). Ginekologiya. 2021;23(5):392-401. (In Russ.). https://doi.org/10.26442/20795696.2021.5.201211

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