What is the contribution of embryo-endometrial asynchrony to implantation failure?

Journal of Assisted Reproduction and Genetics

Volumn 33, Issue 11, 2016, Pages 1419-1430

  Teh, Wan Tinn ^a,b   McBain, John ^b   Rogers, Peter ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL WOMEN'S HOSPITAL   (Australia)

Author keywords

Embryo; Endometrium; Implantation; Synchrony; Uterine receptivity

Indexed keywords

MOLECULAR MARKER;

EMBRYO DEVELOPMENT; ENDOMETRIUM; GENOMICS; HORMONAL REGULATION; HUMAN; IN VITRO FERTILIZATION; INFERTILITY THERAPY; LUTEINIZATION; NIDATION; NONHUMAN; OVARY HYPERSTIMULATION; PREGNANCY; PRIORITY JOURNAL; REVIEW; UTERUS; BLASTOCYST; CYTOLOGY; EMBRYO TRANSFER; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY;

BLASTOCYST; EMBRYO IMPLANTATION; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; FERTILIZATION IN VITRO; HUMANS; PREGNANCY; UTERUS;

EID: 84982801659     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-016-0773-6     Document Type: Review

References (110)

1. Lessey BA, Killam AP, Metzger DA, Haney AF, Greene GL, McCarty KS. Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metab. 1988;67:334–40.
2. Kodaman PH, Taylor HS. Hormonal regulation of implantation. Obstet Gynecol Clin N Am. 2004;31:745–66.
3. Young SL. Oestrogen and progesterone action on endometrium: a translational approach to understanding endometrial receptivity. Reprod BioMed Online. 2013;27:497–505.
4. Fritz MA, Westfahl PK, Graham RL. The effect of luteal phase estrogen antagonism on endometrial development and luteal function in women. J Clin Endocrinol Metab. 1987;65:1006–13.
5. Lutjen P, Trounson A, Leeton J, Findlay J, Wood C, Renou P. The establishment and maintenance of pregnancy using in vitro fertilization and embryo donation in a patient with primary ovarian failure. Nature. 1984;307:174–5.
6. Paulson RJ. Hormonal induction of endometrial receptivity. Fertil Steril. 2011;96:530–5.
7. Navot D, Laufer N, Kopolovic J, Rabinowitz R, Birkenfeld A, Lewin A, et al. Artificially induced endometrial cycles and establishment of pregnancies in the absence of ovaries. N Engl J Med. 1986;314:806–11.
8. Remohí J, Gutiérrez A, Cano F, Ruiz A, Simón C, Pellicer A. Long oestradiol replacement in an oocyte donation programme. Hum Reprod. 1995;10:1387–91.
9. Sauer MV, Miles RA, Dahmoush L, Paulson RJ, Press M, Moyer D. Evaluating the effect of age on endometrial responsiveness to hormone replacement therapy: a histologic ultrasonographic, and tissue receptor analysis. J Assist Reprod Genet. 1993;10:47–52.
10. Hofmann GE, Thie J, Scott RT, Navot D. Endometrial thickness is predictive of histologic endometrial maturation in women undergoing hormone replacement for ovum donation. Fertil Steril. 1996;66:380–3.
11. Sherman MI, Wudl LW. The implanting mouse blastocyst. In: Poste G, Nicholson GL, editors. The cell surface in embryogenesis and development. Amsterdam: Elsevier; 1976. p. 81–125.
12. Zhang S, Lin H, Kong S, Wang S, Wang H, Wang H, et al. Physiological and molecular determinants of embryo implantation. Mol Asp Med. 2013;34:939–80.
13. Næslund G, Lundkvist Ö, Nilsson BO. Transmission electron microscopy of mouse blastocysts activated and growth-arrested in vivo and in vitro. Anat Embryol. 1980;159:33–48.
14. Psychoyos A. Uterine receptivity for nidation. Ann N Y Acad Sci. 1986;476:36–42.
15. Macpherson AM, Rogers PA, Beaton LA. Vascular response in a non-uterine site to implantation-stage embryos following interspecies transfers between the rat, mouse, and guinea-pig. Cell Tissue Res. 1989;258:417–23.
16. Runner MN. Development of mouse eggs in the anterior chamber of the eye. Anat Rec. 1947;98:1–17.
17. Rogers PAW, Macpherson AM, Beaton LA. Vascular response in a non-uterine site to implantation-stage embryos in the rat and guinea-pig: in vivo and ultrastructural studies. Cell Tissue Res. 1988;254:217–24.
18. Fawcett DW. The development of mouse ova under the capsule of the kidney. Anat Rec. 1950;108:71–91.
19. Kirby DR. The development of mouse blastocysts transplanted to the scrotal and cryptorchid testis. J Anat. 1963;97:119–30.
20. Kirby DR. Development of the mouse blastocyst transplanted to the spleen. J Reprod Fertil. 1963;5:1–12.
21. Dahab A, Aburass R, Shawkat W, Babgi R, Essa O, Mujallid R. Full-term extrauterine abdominal pregnancy: a case report. J Med Case Rep. 2011;5:531–1.
22. Mpogoro F, Gumodoka B, Kihunrwa A, Massinde A. Managing a live advanced abdominal twin pregnancy. Ann Med Health Sci Res. 2013;3:113–5.
23. Lundkvist Ö, Nilsson BO. Endometrial ultrastructure in the early uterine response to blastocysts and artificial deciduogenic stimuli in rats. Cell Tissue Res. 1982;225:355–64.
24. Lawson R. Research applications of embryo transfer in sheep and goats. In: Betteridge K, editor. Embryo transfer in farm animals, vol. 16. Ottawa: Canada Department of Agriculture; 1977. p. 72–8.
25. Garrett JE, Geisert RD, Zavy MT, Morgan GL. Evidence for maternal regulation of early conceptus growth and development in beef cattle. J Reprod Fertil. 1988;84:437–46.
26. Teklenburg G, Salker M, Molokhia M, Lavery S, Trew G, Aojanepong T, et al. Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation. PLoS One. 2010;5:e10258–8.
27. Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999;340:1796–9.
28. Rogers PA. Oocyte donation. In: Wood C, Trounson A, editors. Clinical in vitro fertilization and embryo transfer. Berlin: Springer; 1988. p. 143.
29. Rogers PA, Murphy CR. Uterine receptivity for implantation: human studies. In: Yoshinaga K, editor. Blastocyst implantation. Serono Symposia: Adams Publishing Group; 1989. p. 231–8.
30. Navot D, Scott RT, Droesch K, Veeck LL, Liu HC, Rosenwaks Z. The window of embryo transfer and the efficiency of human conception in vitro. Fertil Steril. 1991;55:114–8.
31. Mandelbaum J, Junca AM, Plachot M, Cohen J, Alvarez S, Cornet D, et al. The implantation window in humans after fresh or frozen-thawed embryo transfers. In: Maschiach S, Ben-Rafel Z, Laufer N, Schenker JG, editors. Advances in assisted reproductive technologies. New York: Plenum; 1990. p. 729–35.
32. Ubaldi F, Bourgain C, Tournaye H, Smitz J, Van Steirteghem A, Devroey P. Endometrial evaluation by aspiration biopsy on the day of oocyte retrieval in the embryo transfer cycles in patients with serum progesterone rise during the follicular phase. Fertil Steril. 1997;67:521–6.
33. Kolibianakis E, Bourgain C, Albano C, Osmanagaoglu K, Smitz J, Van Steirteghem A, et al. Effect of ovarian stimulation with recombinant follicle-stimulating hormone, gonadotropin releasing hormone antagonists, and human chorionic gonadotropin on endometrial maturation on the day of oocyte pick-up. Fertil Steril. 2002;78:1025–9.
34. Van Vaerenbergh I, Van Lommel L, Ghislain V, In’t Veld P, Schuit F, Fatemi HM, et al. In GnRH antagonist/rec-FSH stimulated cycles, advanced endometrial maturation on the day of oocyte retrieval correlates with altered gene expression. Hum Reprod. 2009;24:1085–91.
35. Imbar T, Hurwitz A. Synchronization between endometrial and embryonic age is not absolutely crucial for implantation. Fertil Steril. 2004;82:472–4.
36. Shapiro BS, Daneshmand ST, Garner FC, Aguirre M, Ross R. Contrasting patterns in in vitro fertilization pregnancy rates among fresh autologous, fresh oocyte donor, and cryopreserved cycles with the use of day 5 or day 6 blastocysts may reflect differences in embryo-endometrium synchrony. Fertil Steril. 2008;89:20–6.
37. Mirkin S, Nikas G, Hsiu JG, Diaz J, Oehninger S. Gene expression profiles and structural/functional features of the peri-implantation endometrium in natural and gonadotropin-stimulated cycles. J Clin Endocrinol Metab. 2004;89:5742–52.
38. Kolb BA, Paulson RJ. The luteal phase of cycles utilizing controlled ovarian hyperstimulation and the possible impact of this hyperstimulation on embryo implantation. Am J Obstet Gynecol. 1997;176:1262–9.
39. Noyes R, Hertig A, Rock J. Dating the endometrial biopsy. Fertil Steril. 1950;1:21.
40. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol. 1975;122:262–3.
41. Gibson M, Badger GJ, Byrn F, Lee KR, Korson R, Trainer TD. Error in histologic dating of secretory endometrium: variance component analysis. Fertil Steril. 1991;56:242–7.
42. Medicine TPCotASfR. Optimal evaluation of the infertile female. Fertil Steril. 2006;86:S264–7.
43. Noyes RW, Haman JO. Accuracy of endometrial dating; correlation of endometrial dating with basal body temperature and menses. Fertil Steril. 1953;4:504–17.
44. Duggan MA, Brashert P, Ostor A, Scurry J, Billson V, Kneafsey P, et al. The accuracy and interobserver reproducibility of endometrial dating. Pathology. 2001;33:292–7.
45. Deligdisch L. Hormonal pathology of the endometrium. Mod Pathol 0000; 13:285–294.
46. Sher G, Herbert C, Maassarani G, Jacobs MH. Assessment of the late proliferative phase endometrium by ultrasonography in patients undergoing in-vitro fertilization and embryo transfer (IVF/ET). Hum Reprod. 1991;6:232–7.
47. Bustillo M, Krysa LW, Coulam CB. Implantation: uterine receptivity in an oocyte donation programme. Hum Reprod. 1995;10:442–5.
48. Fanchin R, Righini C, Ayoubi J-M, Olivennes F, de Ziegler D, Frydman R. New look at endometrial echogenicity: objective computer-assisted measurements predict endometrial receptivity in in vitro fertilization–embryo transfer. Fertil Steril. 2000;74:274–81.
49. Glissant A, de Mouzon J, Frydman R. Ultrasound study of the endometrium during in vitro fertilization cycles. Fertil Steril. 1985;44:786–90.
50. Gonen Y, Casper RF. Prediction of implantation by the sonographic appearance of the endometrium during controlled ovarian stimulation for in vitro fertilization (IVF). J In Vitro Fert Embryo Transf. 1990;7:146–52.
51. Check JH, Nowroozi K, Choe J, Lurie D, Dietterich C. The effect of endometrial thickness and echo pattern on in vitro fertilization outcome in donor oocyte-embryo transfer cycle. Fertil Steril. 1993;59:72–5.
52. Richter KS, Bugge KR, Bromer JG, Levy MJ. Relationship between endometrial thickness and embryo implantation, based on 1,294 cycles of in vitro fertilization with transfer of two blastocyst-stage embryos. Fertil Steril. 2007;87:53–9.
53. Fleischer AC, Herbert CM, Sacks GA, Wentz AC, Entman SS, James Jr AE. Sonography of the endometrium during conception and nonconception cycles of in vitro fertilization and embryo transfer. Fertil Steril. 1986;46:442–7.
54. Khalifa E, Brzyski RG, Oehninger S, Acosta AA, Muasher SJ. Sonographic appearance of the endometrium: the predictive value for the outcome of in-vitro fertilization in stimulated cycles. Hum Reprod. 1992;7:677–80.
55. Momeni M, Rahbar MH, Kovanci E. A meta-analysis of the relationship between endometrial thickness and outcome of in vitro fertilization cycles. J Hum Reprod Sci. 2011;4:130–7.
56. Li T-C, Nuttall L, Klentzeris L, Cooke ID. How well does ultrasonographic measurement of endometrial thickness predict the results of histological dating? Hum Reprod. 1992;7:1–5.
57. Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update. 2006;12:731–46.
58. Robertson M, Ritz J. Biology and clinical relevance of human natural killer cells. Blood 1990;76;2421–38.
59. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod. 1991;6:791–8.
60. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. 2006;12:1065–74.
61. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med. 2003;198:1201–12.
62. Quenby S, Bates M, Doig T, Brewster J, Lewis-Jones DI, Johnson PM, et al. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum Reprod. 1999;14:2386–91.
63. Seshadri S, Sunkara SK. Natural killer cells in female infertility and recurrent miscarriage: a systematic review and meta-analysis. Hum Reprod Update. 2014;20:429–38.
64. Lessey BA, Castelbaum AJ, Wolf L, Greene W, Paulson M, Meyer WR, et al. Use of integrins to date the endometrium. Fertil Steril. 2000;73:779–87.
65. Casals G, Ordi J, Creus M, Fábregues F, Carmona F, Casamitjana R, et al. Expression pattern of osteopontin and αvβ3 integrin during the implantation window in infertile patients with early stages of endometriosis. Hum Reprod. 2012;27:805–13.
66. Gonzalez RR, Palomino A, Boric A, Vega M, Devoto L. A quantitative evaluation of α1, α4, αV and β3 endometrial integrins of fertile and unexplained infertile women during the menstrual cycle. A flow cytometric appraisal. Hum Reprod. 1999;14:2485–92.
67. Ordi J, Creus M, Casamitjana R, Cardesa A, Vanrell J, Balasch J. Endometrial pinopode and alphavbeta3 integrin expression is not impaired in infertile patients with endometriosis. J Assist Reprod Genet. 2003;20:465–73.
68. Coughlan C, Sinagra M, Ledger W, Li TC, Laird S. Endometrial integrin expression in women with recurrent implantation failure after in vitro fertilization and its relationship to pregnancy outcome. Fertil Steril. 2013;100:825–30. e822.
69. Ordi J, Creus M, Quintó L, Casamitjana R, Cardesa A, Balasch J. Within-subject between-cycle variability of histological dating, αvβ3 integrin expression, and pinopod formation in the human endometrium. J Clin Endocrinol Metab. 2003;88:2119–25.
70. Dimitriadis E, Nie G, Hannan NJ, Paiva P, Salamonsen LA. Local regulation of implantation at the human fetal-maternal interface. Int J Dev Biol. 2010;54:313–22.
71. Aghajanova L, Altmäe S, Bjuresten K, Hovatta O, Landgren B-M, Stavreus-Evers A. Disturbances in the LIF pathway in the endometrium among women with unexplained infertility. Fertil Steril. 2009;91:2602–10.
72. Hambartsoumian E. Endometrial leukemia inhibitory factor (LIF) as a possible cause of unexplained infertility and multiple failures of implantation. Am J Reprod Immunol. 1998;39:137–43.
73. Laird SM, Tuckerman EM, Dalton CF, Dunphy BC, Li TC, Zhang X. The production of leukaemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture. Hum Reprod. 1997;12:569–74.
74. Lédée-Bataille N, Laprée-Delage G, Taupin J-L, Dubanchet S, Frydman R, Chaouat G. Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Hum Reprod. 2002;17:213–8.
75. Steck T, Giess R, Suetterlin MW, Bolland M, Wiest S, Poehls UG, et al. Leukaemia inhibitory factor (LIF) gene mutations in women with unexplained infertility and recurrent failure of implantation after IVF and embryo transfer. Eur J Obstet Gynecol Reprod Biol. 2004;112:69–73.
76. Brinsden PR, Alam V, de Moustier B, Engrand P. Recombinant human leukemia inhibitory factor does not improve implantation and pregnancy outcomes after assisted reproductive techniques in women with recurrent unexplained implantation failure. Fertil Steril. 2009;91:1445–7.
77. Koot YEM, Teklenburg G, Salker MS, Brosens JJ, Macklon NS. Molecular aspects of implantation failure. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2012;1822:1943–50.
78. Ponnampalam AP, Weston GC, Trajstman AC, Susil B, Rogers PA. Molecular classification of human endometrial cycle stages by transcriptional profiling. Mol Hum Reprod. 2004;10:879–93.
79. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006;147:1097–121.
80. Borthwick JM, Charnock-Jones DS, Tom BD, Hull ML, Teirney R, Phillips SC, et al. Determination of the transcript profile of human endometrium. Mol Hum Reprod. 2003;9:19–33.
81. Carson DD, Lagow E, Thathiah A, Al-Shami R, Farach-Carson MC, Vernon M, et al. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol Hum Reprod. 2002;8:871–9.
82. Horcajadas JA, Riesewijk A, Martı́n J, Cervero A, Mosselman S, Pellicer A, et al. Global gene expression profiling of human endometrial receptivity. J Reprod Immunol. 2004;63:41–9.
83. Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology. 2002;143:2119–38.
84. Kuokkanen S, Chen B, Ojalvo L, Benard L, Santoro N, Pollard JW. Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium. Biol Reprod. 2010;82:791–801.
85. Mirkin S, Arslan M, Churikov D, Corica A, Diaz JI, Williams S, et al. In search of candidate genes critically expressed in the human endometrium during the window of implantation. Hum Reprod. 2005;20:2104–17.
86. Riesewijk A, Martin J, van Os R, Horcajadas JA, Polman J, Pellicer A, et al. Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology. Mol Hum Reprod. 2003;9:253–64.
87. Díaz-Gimeno P, Horcajadas JA, Martínez-Conejero JA, Esteban FJ, Alamá P, Pellicer A, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011;95:50–60. e15.
88. Díaz-Gimeno P, Ruiz-Alonso M, Blesa D, Bosch N, Martínez-Conejero JA, Alamá P, et al. The accuracy and reproducibility of the endometrial receptivity array is superior to histology as a diagnostic method for endometrial receptivity. Fertil Steril. 2013;99:508–17.
89. Noci I, Borri P, Coccia ME, Criscuoli L, Scarselli G, Messeri G, et al. Hormonal patterns, steroid receptors and morphological pictures of endometrium in hyperstimulated IVF cycles. Eur J Obstet Gynecol Reprod Biol. 1997;75:215–20.
90. Lass A, Peat D, Avery S, Brinsden P. Histological evaluation of endometrium on the day of oocyte retrieval after gonadotrophin-releasing hormone agonist-follicle stimulating hormone ovulation induction for in-vitro fertilization. Hum Reprod. 1998;13:3203–5.
91. Meyer WR, Novotny DB, Fritz MA, Beyler SA, Wolf LJ, Lessey BA. Effect of exogenous gonadotropins on endometrial maturation in oocyte donors. Fertil Steril. 1999;71:109–14.
92. Bourgain C, Ubaldi F, Tavaniotou A, Smitz J, Van Steirteghem AC, Devroey P. Endometrial hormone receptors and proliferation index in the periovulatory phase of stimulated embryo transfer cycles in comparison with natural cycles and relation to clinical pregnancy outcome. Fertil Steril. 2002;78:237–44.
93. Seif MW, Pearson JM, Ibrahim ZHZ, Buckley CH, Aplin JD, Buck P, et al. Endometrium in in-vitro fertilization cycles: morphological and functional differentiation in the implantation phase. Hum Reprod. 1992;7:6–11.
94. Evans J, Hannan NJ, Hincks C, Rombauts LJF, Salamonsen LA. Defective soil for a fertile seed? Altered endometrial development is detrimental to pregnancy success. PLoS One. 2012;7, e53098.
95. Papanikolaou EG, Bourgain C, Kolibianakis E, Tournaye H, Devroey P. 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. 2005;20:1541–7.
96. Chai J, Lee K-F, Ng EHY, Yeung WSB, Ho P-C. Ovarian stimulation modulates steroid receptor expression and spheroid attachment in peri-implantation endometria: studies on natural and stimulated cycles. Fertil Steril. 2011;96:764–8.
97. Liu Y, Lee K-F, Ng EHY, Yeung WSB, Ho P-C. Gene expression profiling of human peri-implantation endometria between natural and stimulated cycles. Fertil Steril. 2008;90:2152–64.
98. Pandey S, Shetty A, Hamilton M, Bhattacharya S, Maheshwari A. Obstetric and perinatal outcomes in singleton pregnancies resulting from IVF/ICSI: a systematic review and meta-analysis. Hum Reprod Update. 2012;18:485–503.
99. Shih W, Rushford DD, Bourne H, Garrett C, McBain JC, Healy DL, et al. Factors affecting low birthweight after assisted reproduction technology: difference between transfer of fresh and cryopreserved embryos suggests an adverse effect of oocyte collection. Hum Reprod. 2008;23:1644–53.
100. Healy DL, Breheny S, Halliday J, Jaques A, Rushford D, Garrett C, et al. Prevalence and risk factors for obstetric haemorrhage in 6730 singleton births after assisted reproductive technology in Victoria Australia. Hum Reprod. 2010;25:265–74.
101. Maheshwari A, Pandey S, Shetty A, Hamilton M, Bhattacharya S. Obstetric and perinatal outcomes in singleton pregnancies resulting from the transfer of frozen thawed versus fresh embryos generated through in vitro fertilization treatment: a systematic review and meta-analysis. Fertil Steril. 2012;98:368–77. e369.
102. Evans J, Hannan NJ, Edgell TA, Vollenhoven BJ, Lutjen PJ, Osianlis T, et al. Fresh versus frozen embryo transfer: backing clinical decisions with scientific and clinical evidence. Hum Reprod Update. 2014.
103. Barker DJ. Fetal origins of coronary heart disease. BMJ. 1995;311:171–4.
104. Blumenfeld Z. Why more is less and less is more when it comes to ovarian stimulation. J Assist Reprod Genet. 2015;32:1713–9.
105. Bosch E, Valencia I, Escudero E, Crespo J, Simón C, Remohí J, et al. Premature luteinization during gonadotropin-releasing hormone antagonist cycles and its relationship with in vitro fertilization outcome. Fertil Steril. 2003;80:1444–9.
106. Griesinger G, Mannaerts B, Andersen CY, Witjes H, Kolibianakis EM, Gordon K. Progesterone elevation does not compromise pregnancy rates in high responders: a pooled analysis of in vitro fertilization patients treated with recombinant follicle-stimulating hormone/gonadotropin-releasing hormone antagonist in six trials. Fertil Steril. 2013.
107. Venetis CA, Kolibianakis EM, Bosdou JK, Tarlatzis BC. Progesterone elevation and probability of pregnancy after IVF: a systematic review and meta-analysis of over 60 000 cycles. Hum Reprod Update. 2013;19:433–57.
108. Bosch E, Labarta E, Crespo J, Simón C, Remohí J, Jenkins J, et al. Circulating progesterone levels and ongoing pregnancy rates in controlled ovarian stimulation cycles for in vitro fertilization: analysis of over 4000 cycles. Hum Reprod. 2010;25:2092–100.
109. Labarta E, Martínez-Conejero JA, Alamá P, Horcajadas JA, Pellicer A, Simón C, 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. 2011;26:1813–25.
110. Van Vaerenbergh I, Fatemi HM, Blockeel C, Van Lommel L, In’t Veld P, Schuit F, et al. Progesterone rise on HCG day in GnRH antagonist/rFSH stimulated cycles affects endometrial gene expression. Reprod BioMed Online. 2011;22:263–71.