What is the optimal means of preparing the endometrium in frozen-thawed embryo transfer cycles? A systematic review and meta-analysis

Human Reproduction Update

Volumn 19, Issue 5, 2013, Pages 458-470

  Groenewoud, Eva R ^a   Cantineau, Astrid E P ^a   Kollen, Boudewijn J ^a   Macklon, Nick S ^b   Cohlen, Ben J ^c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c ISALA HOSPITAL   (Netherlands)

Author keywords

Assisted reproduction techniques; Embryo transfer; Endometrium; Frozen thawed embryo transfer

Indexed keywords

GONADORELIN AGONIST;

ARTICLE; BIRTH RATE; CONSENSUS; EMBRYO TRANSFER; ENDOMETRIUM; FREEZE THAWING; HUMAN; LIVE BIRTH; LUTEAL PHASE; META ANALYSIS; PREGNANCY RATE; PRIORITY JOURNAL; RISK FACTOR; SUPPLEMENTATION; SYSTEMATIC REVIEW;

ASSISTED REPRODUCTION TECHNIQUES; EMBRYO TRANSFER; ENDOMETRIUM; FROZEN-THAWED EMBRYO TRANSFER;

CHORIONIC GONADOTROPIN; CORPUS LUTEUM HORMONES; CRYOPRESERVATION; EMBRYO TRANSFER; EMBRYO, MAMMALIAN; ENDOMETRIUM; FEMALE; FERTILIZATION IN VITRO; FREEZING; HUMANS; PREGNANCY; PREGNANCY RATE; SPERM INJECTIONS, INTRACYTOPLASMIC;

EID: 84882728244     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmt030     Document Type: Article

References (78)

1. Adams SM, Terry V, Hosie MJ, Gayer N, Murphy CR. Endometrial response to IVF hormonal manipulation: comparative analysis of menopausal, down regulated and natural cycles. Reprod Biol Endocrinol 2004;2:21.
2. Alama P. Higher ongoing pregnancy rates in blastocyst transfer of frozen-thawed embryos in natural cycles than in hormone replacement therapy cycles. Fertil Steril 2007;88:s161.
3. Al Shawaf T, Yang D, Al Magid Y, Seaton A, Iketubosin F, Craft I. Ultrasonic monitoring during replacement of frozen/thawed embryos in natural and hormone replacement cycles. Hum Reprod 1993;8:2068-2074.
4. Andersen AG, Als-Nielsen B, Hornnes PJ, Franch Andersen L. Time interval from human chorionic gonadotrophin (HCG) injection to follicular rupture. Hum Reprod 1995;10:3202-3205.
5. Belaisch-Allart J. Clinical management of a frozen-thawed embryo transfer cycle. Abstracts of the 10th Annual Meeting of the ESHRE Brussels 1994;356:138-139.
6. Bjuresten K, Landgren BM, Hovatta O, Stavreus-Evers A. Luteal phase progesterone increases live birth rate after frozen embryo transfer. Fertil Steril 2011;95:534-537.
7. Cattoli M. Arandomized prospective studyon cryopreserved-thawedembryo transfer: natural versus homrone replacement cycles. Abstracts of the 10th Annual Meeting of the ESHRE Brussels 1994;356:139.
8. Chang EM, Han JE, Kim YS, Lyu SW, Lee WS, Yoon TK. Use of the natural cycle and vitrification thawed blastocyst transfer results in better in-vitro fertilization outcomes: cycle regimens of vitrification thawed blastocyst transfer. J Assist Reprod Genet 2011;28:369-374. 468 Groenewoud et al.
9. Chen SL, He JX, Song HD, Li SZ, Liu XN, Li H, Xing FQ. Comparison of clinical outcomes of four protocols for frozen-thawed embryo transfer cycle. Nan Fang Yi Ke Da Xue Xue Bao 2007;27:303-306.
10. Dal Prato L, Borini A, Cattoli M, Bonu MA, Sciajno R, Flamigni C. Endometrial preparation for frozen-thawed embryo transfer with or without pretreatment with gonadotropin-releasing hormone agonist. Fertil Steril 2002;77:956-960.
11. de Ziegler D, Cornel C, Bergeron C, Hazout A, Bouchard P, Frydman R. Controlled preparation of the endometrium with exogenous estradiol and progesterone in women having functioning ovaries. Fertil Steril 1991;56:851-855.
12. Diniz D. New reproductive technologies, ethics and gender: the legislative process in Brazil. Dev World Bioeth 2002;2:144-158.
13. Dolan P. Natural cycles and estrogen/progestone induced cycles produce an equallly reeptive endometrium for implantation of cryopreserved embryos. Hum Reprod (Oxford, England) 1991;s16.
14. Dor J, Rudak E, Davidson A, Levran D, Ben Rafael Z, Mashiach S. Endocrine and biological factors influencing implantation of human embryos following cryopreservation. Gynecol Endocrinol 1991;5:203-211.
15. El Bahja D, Hertz P, Schweitzer T, Lestrade F, Ragage JP. Frozen embryo transfer protocol: Does spontaneous cycle give good results? Gynecol Obstet Fertil 2012.
16. El Toukhy T, Taylor A, Khalaf Y, Al Darazi K, Rowell P, Seed P, Braude P. Pituitary suppression in ultrasound-monitored frozen embryo replacement cycles. A randomised study. Hum Reprod 2004;19:874-879.
17. El-Toukhy T, Coomarasamy A, Khairy M, Sunkara K, Seed P, Khalaf Y, Braude P. The relationship between endometrial thickness and outcome of medicated frozen embryo replacement cycles. Fertil Steril 2008;89:832-839.
18. Fatemi HM, Kyrou D, Bourgain C, Van den AE, Griesinger G, Devroey P. Cryopreserved-thawed human embryo transfer: spontaneous natural cycle is superior to human chorionic gonadotropin-induced natural cycle. Fertil Steril 2010; 94:2054-2058.
19. Fineschi V, Neri M, Turillazzi E. The newItalian law on assisted reproduction technology (Law 40/2004). J Med Ethics 2005;31:536-539.
20. Frydman R, Testart J, Feinstein MC, Roger M. Interrelationship of plasma and urinary luteinizing hormone preovulatory surge. J Steroid Biochem 1984;20: 617-619.
21. Gelbaya TA, Nardo LG, Hunter HR, Fitzgerald CT, Horne G, Pease EE, Brison DR, Lieberman BA. Cryopreserved-thawed embryo transfer in natural or down-regulated hormonally controlled cycles: a retrospective study. Fertil Steril 2006;85:603-609.
22. Ghobara T, Vandekerckhove P. Cycle regimens for frozen-thawed embryo transfer. Cochrane Database Syst Rev 2008;CD003414.
23. Givens CR, Markun LC, Ryan IP, Chenette PE, Herbert CM, Schriock ED. Outcomes of natural cycles versus programmedcycles for 1677 frozen-thawed embryo transfers. Reprod Biomed Online 2009;19:380-384.
24. Glujovsky D, Pesce R, Fiszbajn G, Sueldo C, Hart RJ, Ciapponi A. Endometrial preparation for women undergoing embryo transfer with frozen embryos or embryos derived from donor oocytes. Cochrane Database Syst Rev 2010; CD006359. doi:CD006359.
25. Gonzales J. Natural cycle and hormonal replacement in FET: implantation and pregnancy rates. Abstract Book of the 48th Meeting of the American Fertility Society, 1992, p. s42.
26. Gordts S, Campo R, Puttemans P, Brosens I, Valkenburg M, Norre J, Renier M, Coeman D, Gordts S. Belgian legislation and the effect of elective single embryo transfer on IVF outcome. Reprod Biomed Online 2005;10:436-441.
27. Griesinger G, Weig M, Schroer A, Diedrich K, Kolibianakis EM. Mid-cycle serum levels of endogenous LH are not associated with the likelihood of pregnancy in artificial frozen-thawed embryo transfer cycles without pituitary suppression. Hum Reprod 2007;22:2589-2593.
28. Groenewoud ER, Kollen BJ, Macklon NS, Cohlen BJ. Spontaneous LH surges prior to HCG administration in unstimulated-cycle frozen-thawed embryo transfer do not influence pregnancy rates. Reprod Biomed Online 2012;24:191-196.
29. Guermandi E, VegettiW, Bianchi MM, Uglietti A, Ragni G, Crosignani P. Reliability of ovulation tests in infertile women. Obstet Gynecol 2001;97:92-96.
30. Hancke K, More S, Kreienberg R, Weiss JM. Patients undergoing frozen-thawed embryo transfer have similar live birth rates in spontaneous and artificial cycles. J Assist Reprod Genet 2012;29:403-407.
31. Harper MJ. The implantation window. Baillieres Clin Obstet Gynaecol 1992;6:351-371.
32. Hill MJ, Miller KA, Frattarelli JL. A GnRH agonist and exogenous hormone stimulation protocol has a higher live-birth rate than a natural endogenous hormone protocol for frozen-thawed blastocyst-stage embryo transfer cycles: an analysis of 1391 cycles. Fertil Steril 2010;93:416-422.
33. HoffJD, Quigley ME, Yen SS. Hormonal dynamics at midcycle: a reevaluation. J Clin Endocrinol Metab 1983;57:792-796.
34. Jaroudi KA, Hamilton CJ, Willemsen WN, Sieck UV, Roca G. Artificial endometrial stimulation for frozen embryo replacement. Fertil Steril 1991;55:835-837.
35. JOINT SOGC-CFAS. Guidelines for the number of embryos to transfer following in vitro fertilization No. 182, September 2006. Int J Gynaecol Obstet 2008; 102:203-216.
36. Kawamura T. Clinical outcomes of two different endometrial preparation methods for cryopreserved embryo transfer in patients with a normal menstrual cycle. Reproductive medicine and Biology 2007;6:53-57.
37. Konc J, Kanyo K, Varga E, Kriston R, Cseh S. The effect of cycle regimen used for endometrium preparation on the outcome of day 3 frozen embryo transfer cycle. Fertil Steril 2010;94:767-768.
38. Kumbak B, Erden HF, Tosun S, Akbas H, Ulug U, Bahceci M. Outcome of assisted reproduction treatment in patients with endometrial thickness less than 7 mm. Reprod Biomed Online 2009;18:79-84.
39. Kyrou D, Fatemi HM, Popovic-Todorovic B, Van den Abbeel E, Camus M, Devroey P. Vaginal progesterone supplementation has no effect on ongoing pregnancy rate in hCG-induced natural frozen-thawed embryo transfer cycles. Eur J Obstet Gynecol Reprod Biol 2010;150:175-179.
40. Lee S, Kwon H, Kim J, Lee J, Jung Y, Jung J, Ko HS. Comparison of clinical outcome of frozen-thawed embryo transfer cycles between natural and artificial (hormone-treated) cycles. Hum Reprod 2008;23(Suppl. 1):i1-i230, i217.
41. Lee VC, Li RH, Ng EH, Yeung WS, Ho PC. Luteal phase support does not improve the clinical pregnancy rate of natural cycle frozen-thawed embryo transfer: a retrospective analysis. Eur J Obstet Gynecol Reprod Biol 2013.
42. Lelaidier C, de Ziegler D, Gaetano J, Hazout A, Fernandez H, Frydman R. Controlled preparation of the endometrium with exogenous oestradiol and progesterone: a novel regimen not using a gonadotrophin-releasing hormone agonist. Hum Reprod 1992;7:1353-1356.
43. Lelaidier C, de Ziegler D, Freitas S, Olivennes F, Hazout A, Frydman R. Endometrium preparation with exogenous estradiol and progesterone for the transfer of cryopreserved blastocysts. Fertil Steril 1995;63:919-921.
44. Le Lannou D, Griveau JF, Laurent MC, Gueho A, Veron E, Morcel K. Contribution of embryo cryopreservation to elective single embryo transfer in IVF-ICSI. Reprod Biomed Online 2006;13:368-375.
45. Loh SK, Leong NK. Factors affecting success in an embryo cryopreservation programme. Ann Acad Med Singapore 1999;28:260-265.
46. Ma WG, Song H, Das SK, Paria BC, Dey SK. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA 2003;100:2963-2968.
47. Miller PB, Soules MR. The usefulness of a urinary LH kit for ovulation prediction during menstrual cycles of normal women. Obstet Gynecol 1996;87:13-17.
48. Min JK, Hughes E, Young D, Gysler M, Hemmings R, Cheung AP, Goodrow GJ, Senikas V, Wong BC, Sierra S et al. Elective single embryo transfer following in vitro fertilization. J Obstet Gynaecol Can 2010;32:363-377.
49. Morozov V, Ruman J, Kenigsberg D, Moodie G, Brenner S. Natural cycle cryo-thaw transfer may improve pregnancy outcome. J Assist Reprod Genet 2007;24:119-123.
50. Muasher SJ, KruithoffC, Simonetti S, Oehninger S, Acosta AA, Jones GS. Controlled preparation of the endometrium with exogenous steroids for the transfer of frozen-thawed pre-embryos in patients with anovulatory or irregular cycles. Hum Reprod 1991;6:443-445.
51. Nawroth F, Ludwig M. What is the 'ideal' duration of progesterone supplementation before the transfer of cryopreserved-thawed embryos in estrogen/progesterone replacement protocols? Hum Reprod 2005;20:1127-1134.
52. O'Connor KA, Brindle E, Miller RC, Shofer JB, Ferrell RJ, Klein NA, Soules MR, Holman DJ, Mansfield PK, Wood JW. Ovulation detection methods for urinary hormones: precision, daily and intermittent sampling and a combined hierarchical method. Hum Reprod 2006;21:1442-1452.
53. Oehninger S, Toner JP, Veeck LL, Brzyski RG, Acosta AA, Muasher SJ. Performance of cryopreserved pre-embryos obtained in in vitro fertilization cycles with or without a gonadotropin-releasing hormone agonist. Fertil Steril 1992;57:620-625.
54. Oehninger S, Mayer J, Muasher S. Impact of different clinical variables on pregnancy outcome following embryo cryopreservation. Mol Cell Endocrinol 2000;169:73-77.
55. Park SJ, Goldsmith LT, Skurnick JH, Wojtczuk A, Weiss G. Characteristics of the urinary luteinizing hormone surge in young ovulatory women. Fertil Steril 2007;88:684-690. Endometrium preparation in frozen-thawed embryo transfer 469
56. Pattinson HA, Greene CA, Fleetham J, Anderson-Sykes SJ. Exogenous control of the cycle simplifies-thawed embryo transfer and results in a pregnancy rate similar to that for natural cycles. Fertil Steril 1992;58:627-629.
57. Paulson RJ. Hormonal induction of endometrial receptivity. Fertil Steril 2011;96:530-535.
58. Perrier D'Hauterive S, Berndt S, Tsampalas M, Charlet-Renard C, Dubois M, Bourgain C, Hazout A, Foidart JM, Geenen V. Dialogue between blastocyst hCG and endometrial LH/hCG receptor: which role in implantation? Gynecol Obstet Invest 2007;64:156-160.
59. Queenan JT Jr, Veeck LL, Seltman HJ, Muasher SJ. Transfer of cryopreserved-thawed pre-embryos in a natural cycle or a programmed cycle with exogenous hormonal replacement yields similar pregnancy results. Fertil Steril 1994;62:545-550.
60. Queenan JT Jr, Ramey JW, Seltman HJ, Eure L, Veeck LL, Muasher SJ. Transfer of cryopreserved-thawed pre-embryos in a cycle using exogenous steroids without prior gonadotrophin-releasing hormone agonist suppression yields favourable pregnancy results. Hum Reprod 1997;12:1176-1180.
61. 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;87:53-59.
62. Sathanandan M, Macnamee MC, Rainsbury P, Wick K, Brinsden P, Edwards RG. Replacement of frozen-thawed embryos in artificial and natural cycles: a prospective semi-randomized study. Hum Reprod 1991;6:685-687.
63. Schmidt CL, de Ziegler D, Gagliardi CL, Mellon RW, Taney FH, Kuhar MJ, Colon JM, Weiss G. Transfer of cryopreserved-thawed embryos: the natural cycle versus controlled preparation of the endometrium with gonadotropin-releasing hormone agonist and exogenous estradiol and progesterone (GEEP). Fertil Steril 1989; 52:609-616.
64. Simon A, Hurwitz A, Zentner BS, Bdolah Y, Laufer N. Transfer of frozen-thawed embryos in artificially prepared cycles with and without prior gonadotrophinreleasing hormone agonist suppression: a prospective randomized study. Hum Reprod 1998;13:2712-2717.
65. Simon A, Hurwitz A, Pharhat M, Revel A, Zentner BS, Laufer N. A flexible protocol for artificial preparation of the endometrium without prior gonadotropin-releasing hormone agonist suppression in women with functioning ovaries undergoing frozen-thawed embryo transfer cycles. Fertil Steril 1999;71:609-613.
66. Skovmand K. First-ever fertilisation bill passed in Denmark. Lancet 1997;349:1678. Spandorfer S. Blastocyst frozen embryo transfer (FET): comparison of outcome
67. Spandorfer S. Blastocyst frozen embryo transfer (FET): comparison of outcome with replacement in natural or programmed/medicated cycle. Fertil Steril 2004; 82:s154.
68. Tabibzadeh S. Molecular control of the implantation window. Hum Reprod Update 1998;4:465-471.
69. Tanos V, Friedler S, Zajicek G, Neiger M, Lewin A, Schenker JG. The impact of endometrial preparation on implantation following cryopreserved-thawedembryo transfer. Gynecol Obstet Invest 1996;41:227-231.
70. Thompson JG. A mixed bag: a perspective on the regulation of IVF in Australia. Hum Fertil (Camb) 2005;8:69-70.
71. Tomax C, Alsbjerg B, Martikainen H, Humaidan P. Pregnancy loss after frozen-embryo transfer-a comparison of three protocols. Fertil Steril 2012;98:1165-1169.
72. van der Linden M, Buckingham K, Farquhar C, Kremer JA, Metwally M. Luteal phase support for assisted reproduction cycles. Cochrane Database Syst Rev 2011; CD009154.
73. Wada I, Matson PL, Troup SA, Hughes S, Buck P, Lieberman BA. Outcome of treatment subsequent to the elective cryopreservation of all embryos fromwomenat risk of the ovarian hyperstimulation syndrome. Hum Reprod 1992;7:962-966.
74. Weissman A, Levin D, Ravhon A, Eran H, Golan A, Levran D. What is the preferred method for timing natural cycle frozen-thawed embryo transfer? Reprod Biomed Online 2009;19:66-71.
75. Weissman A, Horowitz E, Ravhon A, Steinfeld Z, MutzafiR, Golan A, Levran D. Spontaneous ovulation versus HCG triggering for timing natural-cycle frozen- thawed embryo transfer: a randomized study. Reprod Biomed Online 2011; 23:484-489.
76. Xiao Z, Zhou X, Xu W, Yang J, Xie Q. Natural cycle is superior to hormone replacement therapy cycle for vitrificated-preserved frozen-thawed embryo transfer. Syst Biol Reprod Med 2011;58:107-112.
77. Yishia D. Do we need to artificially prepare the endometrium for frozen embryo transfer in normal cycling women? A controlled study. Fertil Steril 2001;76:s112.
78. Zimmermann G, Ackermann W, Alexander H. Epithelial human chorionic gonadotropin is expressed and produced in human secretory endometrium during the normal menstrual cycle. Biol Reprod 2009;80:1053-1065.