Incomplete secretory remodeling of the extracellular matrix of the endometrium is associated with recrudescent reproductive losses
DOI:
https://doi.org/10.37800/RM.4.2023.43-51Keywords:
Endometrial biopsy, infertility, habitual miscarriage of pregnancy, histological examination of the endometriumAbstract
Relevance: Despite the progress made in understanding the physiology and pathophysiology of the human endometrium, insufficient progress has been made in integrating clinical tools for endometrial assessment in habitual miscarriage/primary infertility. It is difficult to reliably assess the quality of endometrial preparation, including secretory transformation, using clinical studies such as transvaginal ultrasound or hysteroscopic examination of the endometrial cavity and measuring proteins in blood plasma. Thus, information about the state of the endometrium obtained by clinical and instrumental methods is limited. Therefore, morphological examination of the endometrium remains relevant.
The study aimed to compare the histochemical pattern of the endometrium of the middle secretory phase with recurrent reproductive failures and physiological reproductive status to reveal the impact of the endometrial extracellular matrix incomplete secretory remodeling on reproductive losses.
Materials and Methods: This cross-sectional study included endometrial biopsies of the middle stage of the secretion phase (21 days of the cycle), aimed at morphological examination in the pathology department of the NAO «Medical University of Karaganda» clinic for the period from January 2020 to December 2022.
Results: The results of the study showed that in cases of reproductive function disorders, there are deviations in the histochemical pattern of the reticular fibers of the endometrial stroma.
Conclusion: We propose to use the method of histochemical assessment of the pattern of reticular fibers of the extracellular matrix of the endometrium to identify a group of women of fertile age at risk of reproductive failures.
References
Napso T, Yong HEJ, Lopez-Tello J, Sferruzzi-Perri AN. The Role of Placental Hormones in Mediating Maternal Adaptations to Support Pregnancy and Lactation. Front Physiol. 2018;9:1091.
https://doi.org/10.3389/fphys.2018.01091
Duzyj CM, Buhimschi IA, Laky CA, Cozzini G, Zhao G, Wehrum M, Buhimschi CS. Extravillous trophoblast invasion in placenta accreta is associated with differential local expression of angiogenic and growth factors: a cross-sectional study. BJOG. 2018;125(11):1441-1448.
https://doi.org/10.1111/1471-0528.15176
Vining KH, Mooney DJ. Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol. 2017;18(12):728-742.
https://doi.org/10.1038/nrm.2017.108
Karamanos NK, Theocharis AD, Piperigkou Z, Manou D, Passi A, Skandalis SS, Vynios DH, Orian-Rousseau V, Ricard-Blum S, Schmelzer CEH., Duca L, Durbeej M, Afratis NA, Troeberg L, Franchi M, Masola V, Onisto M. A guide to the composition and functions of the extracellular matrix. FEBS J. 2021;288(24):6850-6912.
https://doi.org/10.1111/febs.15776
Тихаева К.Ю., Рогова Л.Н., Ткаченко Л.В. Роль металлопротеиназ в обмене белков внеклеточного матрикса эндометрия в норме и при патологии. Пробл Репрод. 2020;26(4):22-29.
Tihaeva KJu, Rogova LN, Tkachenko LV. The role of metalloproteinases in the metabolism of endometrial extracellular matrix proteins in normal and pathological conditions. Probl Reprod. 2020;26(4):22-29. (In Russ.).
https://doi.org/10.17116/repro20202604122
Azkargorta M, Escobes I, Iloro I, Osinalde N, Corral B, Ibañez-Perez J, Exposito A, Prieto B, Elortza F, Matorras R. Differential proteomic analysis of endometrial fluid suggests increased inflammation and impaired glucose metabolism in non-implantative IVF cycles and pinpoints PYGB as a putative implantation marker. Hum Reprod. 2018;33(10):1898-1906.
https://doi.org/10.1093/humrep/dey274
Liu W, Tal R, Chao H, Liu M, Liu Y. Effect of local endometrial injury in proliferative vs. luteal phase on IVF outcomes in unselected sub-fertile women undergoing in vitro fertilization. Reprod Biol Endocrinol. 2017;15(1):75.
https://doi.org/10.1186/s12958-017-0296-8
He Q, Zhou Y, Zhou W, Mao C, Kang Q, Pan Y, Wang N, Zhong Y, Pan Z. Nomogram incorporating ultrasonic markers of endometrial receptivity to determine the embryo-endometrial synchrony after in vitro fertilization. Front Endocrinol (Lausanne). 2022;13:973306.
https://doi.org/10.3389/fendo.2022.973306
Huang C, Shen X, Shi Q, Shan H, Yan Y, Liu J, Kong N. Adverse impact of elevated serum progesterone and luteinizing hormone levels on the hCG trigger day on clinical pregnancy outcomes of modified natural frozen-thawed embryo transfer cycles. Front. Endocrinol. (Lausanne). 2022;13:1000047.
https://doi.org/10.3389/fendo.2022.1000047
Wu JL, Keller P, Kanchwala M, Xing C, Babayev SN, Carr BR, Bukulmez O, Word RA. Controlled Ovarian Stimulation Protocols Alter Endometrial Histomorphology and Gene Expression Profiles. Reprod Sci. 2020;27(3):895-904.
https://doi.org/10.1007/s43032-019-00093-6
Kalakota NR, George LC, Morelli SS, Douglas NC, Babwah AV. Towards an improved understanding of the effects of elevated progesterone levels on Human Endometrial Receptivity and Oocyte/Embryo Quality during Assisted Reproductive Technologies. Cells. 2022;11(9):1405.
https://doi.org/10.3390/cells11091405
Rubin SC, Abdulkadir M, Lewis J, Harutyunyan A, Hirani R, Grimes CL. Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications. J Pers Med. 2023;13(5):749.
https://doi.org/10.3390/jpm13050749
Jiang WJ, Sun ZG, Song JY. Premature timing of progesterone luteal phase support initiation did not negatively impact live birth rates in modified natural frozen thawed embryo transfer cycles. Heliyon. 2023;249(2):e13218.
https://doi.org/10.1016/j.heliyon.2023.e13218
Pittari D, Dalla Torre M, Borini E, Hummel B, Sawarkar R, Semino C, Van Anken E, Panina-Bordignon P, Sitia R, Anelli T. CREB3L1 and CREB3L2 control Golgi remodelling during decidualization of endometrial stromal cells. Front Cell Dev Biol. 2022;10:986997.
https://doi.org/10.3389/fcell.2022.986997
Danhof NA, Wang R, Van Wely M, Van der Veen F, Mol BWJ, Mochtar MH. IUI for unexplained infertility-a network meta-analysis. Hum Reprod Update. 2020;26(1):1-15.
https://doi.org/10.1093/humupd/dmz035
You S, Zhu Y, Li H, He F, Liu S, Yang X, Wang L, Zeng H, Dai J, Hu L. Recombinant humanized collagen remodels endometrial immune microenvironment of chronic endometritis through macrophage immunomodulation. Regen Biomater. 2023;10:d033. https://doi.org/10.1093/rb/rbad033
Cox DA, Helvering LM. Extracellular matrix integrity: a possible mechanism for differential clinical effects among selective estrogen receptor modulators and estrogens? Mol Cell Endocrinol. 2006;247(1-2):53-59.
https://doi.org/10.1016/j.mce.2005.12.020
Li T, Liao R, Chan C, Greenblatt EM. Deep learning analysis of endometrial histology as a promising tool to predict the chance of pregnancy after frozen embryo transfers. J Assist Reprod Genet. 2023;40(4):901-910.
https://doi.org/10.1007/s10815-023-02745-8
Navarro A, Bariani MV, Yang Q, Al-Hendy A. Understanding the Impact of Uterine Fibroids on Human Endometrium Function. Front Cell Dev Biol. 2021;9:633180.
https://doi.org/10.3389/fcell.2021.633180
Casarramona G, Lalmahomed T, Lemmen C, Eijkemans M, Broekmans F, Cantineau A, Drechsel K. The efficacy and safety of luteal phase support with progesterone following ovarian stimulation and intrauterine insemination: A systematic review and meta-analysis. Front Endocrinol. (Lausanne). 2022;13:960393.
https://doi.org/10.3389/fendo.2022.960393
Abcam. ab236473 Reticulum Stain Kit (Modified Gomori's). Version 1 [Internet]. Updated 2018 June 27; cited 2023 Aug 30. Available from:
Bajpai K, Acharya N, Prasad R, Wanjari MB. Endometrial Receptivity during the Preimplantation Period: A Narrative Review. Cureus. 2023;15(4):e37753.
https://doi.org/10.7759/cureus.37753
Quinn KE, Matson BC, Wetendorf M, Caron KM. Pinopodes: Recent advancements, current perspectives, and future directions. Mol. Cell. Endocrinol. 2020;501:110644.
https://doi.org/10.1016/j.mce.2019.110644
Zegers-Hochschild F, Adamson GD, Dyer S, Racowsky C, De Mouzon J, Sokol R, Rienzi L, Sunde A, Schmidt L, Cooke ID, Simpson JL, Van der Poel S. The International Glossary on Infertility and Fertility Care, 2017. Fertil Steril. 2017;108(3):393-406.
https://doi.org/10.1016/j.fertnstert.2017.06.005
Vander Borght M, Wyns C. Fertility and infertility: Definition and epidemiology. Clin Biochem. 2018;62:2-10.
https://doi.org/10.1016/j.clinbiochem.2018.03.012
Lampiasi N. Interactions between Macrophages and Mast Cells in the Female Reproductive System. Int J Mol Sci. 2022;23(10):5414.
https://doi.org/10.3390/ijms23105414
Okada H., Tsuzuki T., Murata H. Decidualization of the human endometrium. Reprod Med Biol. 2018;17(3):220-227.
https://doi.org/10.1002/rmb2.12088
Mesen TB, Young SL. Progesterone and the luteal phase: a requisite to reproduction. Obstet Gynecol Clin North Am. 2015;42(1):135-151.
https://doi.org/10.1016/j.ogc.2014.10.003
Ganer Herman H, Volodarsky-Perel A, Ton Nu TN, Machado-Gedeon A, Cui Y, Shaul J, Dahan MH. Pregnancy complications and placental histology following embryo transfer with a thinner endometrium. Hum Reprod. 2022;37(8):1739-1745.
https://doi.org/10.1093/humrep/deac148
Sacha C.R., Harris A.L., James K., Basnet K., Freret T.S., Yeh J., Kaimal A., Souter I., Roberts D.J. Placental pathology in live births conceived with in vitro fertilization after fresh and frozen embryo transfer. Am J Obstet Gynecol. 2020;222(4):360.e1-360.e16.
https://doi.org/10.1016/j.ajog.2019.09.047
Иceнoвa С.Ш., Бодыков Г.Ж. Ким В.Д., Каргабаева Ж.А., Казыбаева А.С., Кабыл Б.К. Анализ особенностей течения беременности и родов у пациенток с бесплодием в анамнезе после применения программ вспомогательных репродуктивных технологий (ВРТ). Репрод мед. 2019;3(40):45-49.
Issenova SSh, Bodykov GZh, Kim VD, Kargabaeva ZhA, Kazybaeva AS, Kabyl BK. Analysis of the characteristics of the course of pregnancy and childbirth in patients with a history of infertility after the use of assisted reproductive technologies (ART) programs. Reprod Med. 2019;3(40):45-49. (In Russ.).
https://doi.org./10.37800/RM.3.2019.45-49
Девятова Е.А., Вартанян Э.В., Цатурова К.А., Девятов И.М. Эндометриопатии и бесплодие. Репрод мед. 2022;1(50):60-67.
Devjatova EA, Vartanjan JeV, Caturova KA, Devjatov IM. Endometriopathy and infertility. Reprod Med. 2022;1(50):60-67. (In Russ.).
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