Clinical view of the ineffectiveness of IVF problem with endometrial receptivity

П. Н. Веропотвелян, И. С. Цехмистренко

Abstract


Objective: To review the literature for studying the mechanisms of influence of superovulation on the receptivity of the endometrium in vitro fertilization (IVF), which is largely due not only to the quality of the embryo, but with the condition of the endometrium, its maturity and readiness for implantation.

Given the fact that with each subsequent attempt likelihood of a positive outcome of IVF decreases endometrial maturation process optimization, training of “implantation window”, as well as support the development of pregnancy in the early stages of its development represents an important aspect of improving the effectiveness of ART.

Successful implantation endometrium maturation, including the formation and readiness pinopody embryo must be accurately synchronized in time and space (an “implantation window”), which corresponds to 19–21 days menstrual cycle.

Materials and methods: In the course of acquaintance with the publication presents the morphological characteristics of the endometrium in stimulated cycles. Presents current views on endometrial receptivity and the molecular mechanisms regulation of implantation.

Results: The features of the expression of estrogen and progesterone receptors, as well as other markers of endometrial receptivity (pinopodii, leukemia inhibitory factor, integrins) in natural and stimulated cycles. Patients with a history of failure of implantation prior to IVF ART program is necessary to analyze all inducers affecting the endometrium, endometrial morphological landscape, E2 receptor expression and progesterone pinopodii, integrins, molecular and genetic aspects of the endometrium in stimulated cycles.

Conclusion: The analysis of numerous publications showing an adverse effect on superovulation endometrial receptivity in assisted reproduction programs. Undetermined noninvasive markers to assess the receptivity of the endometrium, including in stimulated cycles. Not evaluated linically significant endometrial threshold level of progesterone on the day of ovulation trigger and insufficiently studied the possible mechanisms of the effect of a premature increase of progesterone on the outcomes of IVF. Therefore, further study and development of the best approaches for the prevention and correction of the negative impact of ovarian stimulation function on the endometrium in assisted reproduction programs.


Keywords


IVF; premature luteinization stimulated cycle; endometrial receptivity; receptors estradiol; progesterone receptors; integrins; pinopodii; leukemia inhibitory factor expression of Noja

References


Haouzi, D., Assou, S., Mahmoud, K., et al. “Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients.” Hum Reprod 24.6 (2009): 1436–45.

Horcajadas, J.A., Pellicer, A., Simon, C. “Wide genomic analysis of human endometrial receptivity: new times, new apportunities.” Hum Reprod Update 13.1 (2007): 77–86.

Acosta, A.A., Elberger, L., Borghi, M., et al. “Endometrial dating and determination of the window of implantation in healthy fertile women.” Fertil Steril 73.4 (2000): 788–98.

Diamond, M.P., Kruger, M., Santoro, N., et al. “Endometrial shedding effect on conception and live birth in women with polycystic ovary syndrome.” Obstet Gynecol 119 (2012): 902–8.

Gonen, Y., Casper, R.F. “Sonographic determination of a possible adverse effect of clomiphene citrate on endometrial growth.” Hum Reprod 5 (1990): 670–4.

Palomino, W.A., Fuentes, A., González, R.R., et al. “Differential expression of endometrial integrins and progesterone receptor during the window of implantation in normo-ovulatory women treated with clomiphene citrate.” Fertil Steril 83 (2005): 587–93.

Ruiz-Alonso, M., Blesa, D., Simón, C. “The genomics of the human endometrium.” Biochim Biophys Acta 1822 (2012): 1931–42.

Garrido-Gómez, T., Ruiz-Alonso, M., Blesa, D., et al. “Profiling the gene signature of endometrial receptivity: clinical results.” Fertil Steril 99 (2013): 1078–85.

Van Vaerenbergh, I., Fatemi, H.M., Blockeel, C., et al. “Progesterone rise on HCG day in GnRH antagonist/rFSH stimulated cycles affects endometrial gene expression.” Reprod Biomed Online 22.3 (2011): 263–71.

Vitielle, D., Kodaman, P.H., Taylor, H.S. “HOX genes in implantation.” Semin Reprod Med 25.6 (2007): 431–6.

Mityurina, E.V., Perminova, S.G., Demura, T.A., Gallyamova, E.M. “Endometrial receptivity in an in-vitro fertilization program.” Obstet Gynecol 2 (2014): 14-20.

Taylor, H.S., Daftery, G.S., Selam, B. “Endometrial HOXA 10 expression after controlled ovarian hyperstimulation with recombinant follicle-stimulating hormone.” Fertil Steril 80.2 (2003): 839–43.

Edwards, R.G. “Human implantation: the last barrier in assisted reproduction technologies?” Reprod Biomed Online 13.6 (2006): 887–904.

Ferraretti, A., Goossens, V., Bhattacharya, S., et al. Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE. Preliminary results. In: European Society of Human Reproduction and Embriology: 29th Annual Meeting. London, United Kingdom, Jul 7–10 2013.

Dunson, D.B., Colombo, B., Baird, D.D. “Changes with age in the level and duration of fertility in the menstrual cycle.” Hum Reprod 17 (2002): 1399–403.

Tavaniotou, A., Smitz, J., Bourgain, C., Devroey, P. “Ovulation induction disrupts phase function.” Ann NY Acad Sci 943 (2001): 55–63.

Lessey, B.A. “The role of the endometrium during embryo implantation.” Hum Reprod 15 (2000): 39–50.

Bourgain, C., Devroey, P. “The endometrium in stimulated cycles for IVF.” Hum Reprod Update 9.6 (2003): 515–22.

Evans, J., Hannan, N.J., Hincks, C., et al. “Defective soil for a fertile seed? Altered endometrial development is detrimental to pregnancy success.” PLoS One 7.12 (2012): e53098.

Noyes, R.W., Hertig, A.T., Rock, J. “Dating of endometrial biopsy.” Am J Obstet Gynecol 122 (1975): 262–3.

Lessey, B. “Endometrial integrins and the establishment of uterine receptivity.” Hum Reprod 13.3 (1998): 247–58.

Check, J.H., Nowroozi, K., Chase, J., et al. “Comparison of pregnancy rates following in vitro fertilizationembryo transfer between the donors and recipients in a donor oocyte program.” J Assist Reprod Genet 9.3 (1992): 248–50.

Shapiro, B.S., Daneshmand, S.T., Garner, F.C., et al. “Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: a prospective randomized trial comparing fresh and frozen-thawed embryo transfer in normal responders.” Fertil Steril 96.2 (2011): 344–8.

Rackow, B.W., Kliman, H.J., Taylor, H.S. “GnRH antagonists may affect endometrial receptivity.” Fertil Steril 89 (2008): 1234–9.

Van der Gaast, M.H., Classen-Linke, I., Krusche, C.A., et al. “Impact of ovarian stimulation on mid-luteal endometrial tissue and secretion markers of receptivity.” Reprod Biomed Online 17.4 (2008): 553–63.

Levi, A.J., Drews, M.R., Bergh, P.A., et al. “Controlled ovarian hyperstimulation does not adversely affect endometrial receptivity in IVF cycles.” Fertil Steril 76.4 (2001): 670–4.

Ubaldi, F., Bourgain, C., Tournaye, H., et al. “Endometrial evaluation by aspiration biopsy on the day of oocyte retrival in the embryo transfer cycle in patients with serum progesterone rise during the follicular phase.” Fertil Steril 67.3 (1997): 521–6.

Kolibianakis, E., Bourgain, C., Albano, C., et al. “Effect of ovarian stimulation with recombinant folliclestimulating hormone, gonadotropin releasing hormone antagonist, and human chorionic gonadotropin on endometrial maturation on the day of oocyte pick-up.” Fertil Steril 78.5 (2002): 1025–9.

Tarlatzis, B.C., Fauser, B.C., Kolibianakis, E.M., et al. “GnRH antagonists in ovarian stimulation for IVF.” Hum Reprod Update 12.4 (2006): 333–40.

Simon, C., Oberyé, J., Bellver, J., et al. “Similar endometrial development in oocyte donors treated with either high- or standard dose GnRH antagonist compared to treatment with a GnRH agonist or in natural cycles.” Hum Reprod 20.12 (2005): 3318–27.

Elnashar, A.M. “Progesterone rise on day of HCG administration (premature luteinization) in IVF: an overdue update.” J Assist Reprod Genet 27.4 (2010): 149–55.

Melo, M.A., Meseguer, M., Garrido, N., et al. “The significance of premature luteinization in an oocytedonation programme.” Hum Reprod 21.6 (2006): 1503–7.

Venetis, C.A., Kolibianakis, E.M., Papanikolaou, E., et al. “Is progesterone elevation on the day of human chorionic gonadotropin administration associated with the probability of pregnancy in in vitro fertilization? A systematic review and meta-analysis.” Hum Reprod Update 13.4 (2007): 343–55.

Nikas, G. “Cell-surface morphological events relevant to human implantation.” Hum Reprod 14.2 (1999): 7–44.

Bentin-Ley, U., Sjögren, A., Nilsson, L., et al. “Presence of uterine pinopodes at the embryo-endometrial interface during human implantation in vitro.” Hum Reprod 14 (1999): 515–20.

Nikas, G. “Pinopodes as markers of endometrial receptivity in clinical practice.” Hum Reprod 14.2 (1999): 99–106.

Quinn, С., Ryan, E., Claessens, E.A., et al. “The presence of pinopodes in the human endometrium does not delineate the implantation window.” Fertil Steril 87 (2007): 1015–21.

Lessey, B., Ilesanmi, A., Sun, J., et al. “Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception, and infertility.” Am J Reprod Immunol 35 (1996): 195–204.

Thomas, K., Thomson, A.J., Sephton, V., et al. “The effect of gonadotrophic stimulation on integrin expression in the endometrium.” Hum Reprod 17 (2002): 63–8.

Lessey, B.A. “Assessment of endometrial receptivity.” Fertil Steril 96.3 (2011): 522–9.

Noyes, R.W., Hertig, A.J., Rock, J. “Dating the endometrial biopsy.” Fertil Steril 1 (1950): 3–25.

Saadat, P., Boostanfar, R., Slater, C., et al. “Accelerated endometrial maturation in the luteal phase of cycles utilizing controlled ovarian hyperstimulation: impact of gonadotropin-releasing hormone agonists versus antagonists.” Fertil Steril 82.1 (2004): 167–71.

Lass, A., Peat, D., Avery, S., Brinsden, P. “Histological evaluation of endometrium on the day of oocyte retrieval after gonadotropin – releasing hormone agonistfollicle stimulating hormone ovulation induction in-vitro fertilization.” Hum Reprod 13.11 (1998): 3203–5.

Papanikolaou, E.G., Bourgain, C., Kolibianakis, E., et al. “Steroid receptor expression in late follicular phase endometrium in GnRH antagonist IVF cycles is already altered, indicating initiation of early luteal phase transformation in the absence of secretory changes.” Hum Reprod 20.6 (2005): 1541–7.

Gemzell-Danielsson, K., Bygdeman, M. “Effects of Progestogens on Endometrial Maturation in the Implantation Phase.” Ernst Schering Res Found Workshop 52 (2005): 119–38.

Garcia, E., Bouchard, P., De Brux, J., et al. “Use of immunocytochemistry of progesterone and estrogen receptors for endometrial dating.” J Clin Endocrinol Metab 67.1 (1988): 80–7.

Chai, J., Lee, K.F., Ng, E.H., et al. “Ovarian stimulation modulates steroid receptor expression and spheroid attachment in peri-implantation endometria: studies on natural and stimulated cycles.” Fertil Steril 96.3 (2011): 764–8.

Kyrou, D., Kolibianakis, E.M., Venetis, C.A., et al. “Steroid receptor expression in human endometrium during the follicular phase of stimulated cycles.” Hum Reprod 24.11 (2009): 2931–5.

Hadi, F.H., Chantler, E., Anderson, E., et al. “Ovulation induction and endometrial steroid receptors.” Hum Reprod 9.12 (1994): 2405–10.

Lessey, B.A., Holoch, K.J., Franasiak, J., et al. “Prospective assessment of med – secretory endometrial LIF and β3 integrin expression as a predictor of pregnancy outcome and endometriosis in unexplained infertility. European Society of Human Reproduction and Embryology: 28th Annual Meeting. Istanbul-Turkey, Jul 1–4, 2012.” Hum Reprod 27.1 (2012): 80.

Pan, Y.M., Shi, Y.F., Chen, H.Z. “Expression of estrogen receptor, progesterone receptor and leukemia inhibitory factor on endometrium during different ovarian stimulation protocols in mice.” Zhejiang Da Xue Xue Bao Yi Xue Ban 37.3 (2008): 300–3.

Mirkin, S., Nikas, G., Hsiu, J.D., et al. “Gene expression profiles and structural/functional features of the peri-implantation endometrium in natural and gonadotropin-stimulated cycles.” J Clin Endocrinol Metab 89.11 (2004): 5742–52.

Van Vaerenbergh, I., Van Lommel, L., Ghislain, V., et al. “In GnRH antagonist/rec-FSH stimulated cycles, advanced endometrial maturation on the day of oocyte retrieval correlates with altered expression.” Hum Reprod 24.5 (2009): 1085–91.

Li, R., Qiao, J., Wang, L., et al. “MicroRNA array and microarray evaluation of endometrial receptivity in patients with high serum progesterone levels on the day of hCG administration.” Reprod Biol Endocrinol 9 (2011): 29.

Labarta, E., Martínez-Conejero, J.A., Alamá, P., et al. “Endometrial receptivity is affected in women with high circulating progesterone levels at the end of the follicular phase: a functional genomics analysis.” Hum Reprod 26.7 (2011): 1813–25.

Nikzad, H., et al. “Expression of galectin-8 on human endometrium: Molecular and cellular aspects.” Iran J Reprod Med (2013).


GOST Style Citations


1. Haouzi, D., Assou, S., Mahmoud, K., et al. “Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients.” Hum Reprod 24.6 (2009): 1436–45.

2. Horcajadas, J.A., Pellicer, A., Simon, C. “Wide genomic analysis of human endometrial receptivity: new times, new apportunities.” Hum Reprod Update 13.1 (2007): 77–86.

3. Acosta, A.A., Elberger, L., Borghi, M., et al. “Endometrial dating and determination of the window of implantation in healthy fertile women.” Fertil Steril 73.4 (2000): 788–98.

4. Diamond, M.P., Kruger, M., Santoro, N., et al. “Endometrial shedding effect on conception and live birth in women with polycystic ovary syndrome.” Obstet Gynecol 119 (2012): 902–8.

5. Gonen, Y., Casper, R.F. “Sonographic determination of a possible adverse effect of clomiphene citrate on endometrial growth.” Hum Reprod 5 (1990): 670–4.

6. Palomino, W.A., Fuentes, A., González, R.R., et al. “Differential expression of endometrial integrins and progesterone receptor during the window of implantation in normo-ovulatory women treated with clomiphene citrate.” Fertil Steril 83 (2005): 587–93.

7. Ruiz-Alonso, M., Blesa, D., Simón, C. “The genomics of the human endometrium.” Biochim Biophys Acta 1822 (2012): 1931–42.

8. Garrido-Gómez, T., Ruiz-Alonso, M., Blesa, D., et al. “Profiling the gene signature of endometrial receptivity: clinical results.” Fertil Steril 99 (2013): 1078–85.

9. Van Vaerenbergh, I., Fatemi, H.M., Blockeel, C., et al. “Progesterone rise on HCG day in GnRH antagonist/rFSH stimulated cycles affects endometrial gene expression.” Reprod Biomed Online 22.3 (2011): 263–71.

10. Vitielle, D., Kodaman, P.H., Taylor, H.S. “HOX genes in implantation.” Semin Reprod Med 25.6 (2007): 431–6.

11. Mityurina, E.V., Perminova, S.G., Demura, T.A., Gallyamova, E.M. “Endometrial receptivity in an in-vitro fertilization program.” Obstet Gynecol 2 (2014): 14-20.

12. Taylor, H.S., Daftery, G.S., Selam, B. “Endometrial HOXA 10 expression after controlled ovarian hyperstimulation with recombinant follicle-stimulating hormone.” Fertil Steril 80.2 (2003): 839–43.

13. Edwards, R.G. “Human implantation: the last barrier in assisted reproduction technologies?” Reprod Biomed Online 13.6 (2006): 887–904.

14. Ferraretti, A., Goossens, V., Bhattacharya, S., et al. Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE. Preliminary results. In: European Society of Human Reproduction and Embriology: 29th Annual Meeting. London, United Kingdom, Jul 7–10 2013.

15. Dunson, D.B., Colombo, B., Baird, D.D. “Changes with age in the level and duration of fertility in the menstrual cycle.” Hum Reprod 17 (2002): 1399–403.

16. Tavaniotou, A., Smitz, J., Bourgain, C., Devroey, P. “Ovulation induction disrupts phase function.” Ann NY Acad Sci 943 (2001): 55–63.

17. Lessey, B.A. “The role of the endometrium during embryo implantation.” Hum Reprod 15 (2000): 39–50.

18. Bourgain, C., Devroey, P. “The endometrium in stimulated cycles for IVF.” Hum Reprod Update 9.6 (2003): 515–22.

19. Evans, J., Hannan, N.J., Hincks, C., et al. “Defective soil for a fertile seed? Altered endometrial development is detrimental to pregnancy success.” PLoS One 7.12 (2012): e53098.

20. Noyes, R.W., Hertig, A.T., Rock, J. “Dating of endometrial biopsy.” Am J Obstet Gynecol 122 (1975): 262–3.

21. Lessey, B. “Endometrial integrins and the establishment of uterine receptivity.” Hum Reprod 13.3 (1998): 247–58.

22. Check, J.H., Nowroozi, K., Chase, J., et al. “Comparison of pregnancy rates following in vitro fertilizationembryo transfer between the donors and recipients in a donor oocyte program.” J Assist Reprod Genet 9.3 (1992): 248–50.

23. Shapiro, B.S., Daneshmand, S.T., Garner, F.C., et al. “Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: a prospective randomized trial comparing fresh and frozen-thawed embryo transfer in normal responders.” Fertil Steril 96.2 (2011): 344–8.

24. Rackow, B.W., Kliman, H.J., Taylor, H.S. “GnRH antagonists may affect endometrial receptivity.” Fertil Steril 89 (2008): 1234–9.

25. Van der Gaast, M.H., Classen-Linke, I., Krusche, C.A., et al. “Impact of ovarian stimulation on mid-luteal endometrial tissue and secretion markers of receptivity.” Reprod Biomed Online 17.4 (2008): 553–63.

26. Levi, A.J., Drews, M.R., Bergh, P.A., et al. “Controlled ovarian hyperstimulation does not adversely affect endometrial receptivity in IVF cycles.” Fertil Steril 76.4 (2001): 670–4.

27. Ubaldi, F., Bourgain, C., Tournaye, H., et al. “Endometrial evaluation by aspiration biopsy on the day of oocyte retrival in the embryo transfer cycle in patients with serum progesterone rise during the follicular phase.” Fertil Steril 67.3 (1997): 521–6.

28. Kolibianakis, E., Bourgain, C., Albano, C., et al. “Effect of ovarian stimulation with recombinant folliclestimulating hormone, gonadotropin releasing hormone antagonist, and human chorionic gonadotropin on endometrial maturation on the day of oocyte pick-up.” Fertil Steril 78.5 (2002): 1025–9.

29. Tarlatzis, B.C., Fauser, B.C., Kolibianakis, E.M., et al. “GnRH antagonists in ovarian stimulation for IVF.” Hum Reprod Update 12.4 (2006): 333–40.

30. Simon, C., Oberyé, J., Bellver, J., et al. “Similar endometrial development in oocyte donors treated with either high- or standard dose GnRH antagonist compared to treatment with a GnRH agonist or in natural cycles.” Hum Reprod 20.12 (2005): 3318–27.

31. Elnashar, A.M. “Progesterone rise on day of HCG administration (premature luteinization) in IVF: an overdue update.” J Assist Reprod Genet 27.4 (2010): 149–55.

32. Melo, M.A., Meseguer, M., Garrido, N., et al. “The significance of premature luteinization in an oocytedonation programme.” Hum Reprod 21.6 (2006): 1503–7.

33. Venetis, C.A., Kolibianakis, E.M., Papanikolaou, E., et al. “Is progesterone elevation on the day of human chorionic gonadotropin administration associated with the probability of pregnancy in in vitro fertilization? A systematic review and meta-analysis.” Hum Reprod Update 13.4 (2007): 343–55.

34. Nikas, G. “Cell-surface morphological events relevant to human implantation.” Hum Reprod 14.2 (1999): 7–44.

35. Bentin-Ley, U., Sjögren, A., Nilsson, L., et al. “Presence of uterine pinopodes at the embryo-endometrial interface during human implantation in vitro.” Hum Reprod 14 (1999): 515–20.

36. Nikas, G. “Pinopodes as markers of endometrial receptivity in clinical practice.” Hum Reprod 14.2 (1999): 99–106.

37. Quinn, С., Ryan, E., Claessens, E.A., et al. “The presence of pinopodes in the human endometrium does not delineate the implantation window.” Fertil Steril 87 (2007): 1015–21.

38. Lessey, B., Ilesanmi, A., Sun, J., et al. “Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception, and infertility.” Am J Reprod Immunol 35 (1996): 195–204.

39. Thomas, K., Thomson, A.J., Sephton, V., et al. “The effect of gonadotrophic stimulation on integrin expression in the endometrium.” Hum Reprod 17 (2002): 63–8.

40. Lessey, B.A. “Assessment of endometrial receptivity.” Fertil Steril 96.3 (2011): 522–9.

41. Noyes, R.W., Hertig, A.J., Rock, J. “Dating the endometrial biopsy.” Fertil Steril 1 (1950): 3–25.

42. Saadat, P., Boostanfar, R., Slater, C., et al. “Accelerated endometrial maturation in the luteal phase of cycles utilizing controlled ovarian hyperstimulation: impact of gonadotropin-releasing hormone agonists versus antagonists.” Fertil Steril 82.1 (2004): 167–71.

43. Lass, A., Peat, D., Avery, S., Brinsden, P. “Histological evaluation of endometrium on the day of oocyte retrieval after gonadotropin – releasing hormone agonistfollicle stimulating hormone ovulation induction in-vitro fertilization.” Hum Reprod 13.11 (1998): 3203–5.

44. Papanikolaou, E.G., Bourgain, C., Kolibianakis, E., et al. “Steroid receptor expression in late follicular phase endometrium in GnRH antagonist IVF cycles is already altered, indicating initiation of early luteal phase transformation in the absence of secretory changes.” Hum Reprod 20.6 (2005): 1541–7.

45. Gemzell-Danielsson, K., Bygdeman, M. “Effects of Progestogens on Endometrial Maturation in the Implantation Phase.” Ernst Schering Res Found Workshop 52 (2005): 119–38.

46. Garcia, E., Bouchard, P., De Brux, J., et al. “Use of immunocytochemistry of progesterone and estrogen receptors for endometrial dating.” J Clin Endocrinol Metab 67.1 (1988): 80–7.

47. Chai, J., Lee, K.F., Ng, E.H., et al. “Ovarian stimulation modulates steroid receptor expression and spheroid attachment in peri-implantation endometria: studies on natural and stimulated cycles.” Fertil Steril 96.3 (2011): 764–8.

48. Kyrou, D., Kolibianakis, E.M., Venetis, C.A., et al. “Steroid receptor expression in human endometrium during the follicular phase of stimulated cycles.” Hum Reprod 24.11 (2009): 2931–5.

49. Hadi, F.H., Chantler, E., Anderson, E., et al. “Ovulation induction and endometrial steroid receptors.” Hum Reprod 9.12 (1994): 2405–10.

50. Lessey, B.A., Holoch, K.J., Franasiak, J., et al. “Prospective assessment of med – secretory endometrial LIF and β3 integrin expression as a predictor of pregnancy outcome and endometriosis in unexplained infertility. European Society of Human Reproduction and Embryology: 28th Annual Meeting. Istanbul-Turkey, Jul 1–4, 2012.” Hum Reprod 27.1 (2012): 80.

51. Pan, Y.M., Shi, Y.F., Chen, H.Z. “Expression of estrogen receptor, progesterone receptor and leukemia inhibitory factor on endometrium during different ovarian stimulation protocols in mice.” Zhejiang Da Xue Xue Bao Yi Xue Ban 37.3 (2008): 300–3.

52. Mirkin, S., Nikas, G., Hsiu, J.D., et al. “Gene expression profiles and structural/functional features of the peri-implantation endometrium in natural and gonadotropin-stimulated cycles.” J Clin Endocrinol Metab 89.11 (2004): 5742–52.

53. Van Vaerenbergh, I., Van Lommel, L., Ghislain, V., et al. “In GnRH antagonist/rec-FSH stimulated cycles, advanced endometrial maturation on the day of oocyte retrieval correlates with altered expression.” Hum Reprod 24.5 (2009): 1085–91.

54. Li, R., Qiao, J., Wang, L., et al. “MicroRNA array and microarray evaluation of endometrial receptivity in patients with high serum progesterone levels on the day of hCG administration.” Reprod Biol Endocrinol 9 (2011): 29.

55. Labarta, E., Martínez-Conejero, J.A., Alamá, P., et al. “Endometrial receptivity is affected in women with high circulating progesterone levels at the end of the follicular phase: a functional genomics analysis.” Hum Reprod 26.7 (2011): 1813–25.

56. Nikzad, H., et al. “Expression of galectin-8 on human endometrium: Molecular and cellular aspects.” Iran J Reprod Med (2013).





DOI: http://dx.doi.org/10.18370/2309-4117.2017.33.32-39

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