Semin Reprod Med 2014; 32(02): 127-133
DOI: 10.1055/s-0033-1363554
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Limitations of Embryo Selection Methods

Kai Mee Wong
1   Center for Reproductive Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
,
Sjoerd Repping
1   Center for Reproductive Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
,
Sebastiaan Mastenbroek
1   Center for Reproductive Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
› Author Affiliations
Further Information

Publication History

Publication Date:
10 February 2014 (online)

Abstract

In in vitro fertilization (IVF), the selection of embryos for transfer is generally based on the morphology of the available embryos. However, not all embryos with good morphology implant and on average only one in four treatments are successful. This has driven a quest for alternative selection methods. The best known alternative selection method is preimplantation genetic screening (PGS), which has been used for over a decade before it was shown to be inferior to morphological selection. Now, new forms of PGS (performing biopsy at another stage of development and new methods for analysis) are emerging, just like alternative noninvasive embryo selection methods. However, the concept that better selection will lead to improved IVF results is not so certain anymore. Evidence is accumulating that all available embryos in an IVF cycle can be cryopreserved and transferred in subsequent cycles without impairing pregnancy rates or maybe even with an improvement in pregnancy rates. Embryo selection will then no longer be able to improve the live birth rate in IVF; it could even lower the live birth rate. Embryo selection will only be able to improve the time to pregnancy, if embryos with the highest implantation potential are transferred first.

 
  • References

  • 1 Steptoe PC, Edwards RG. Birth after the reimplantation of a human embryo. Lancet 1978; 2 (8085) 366
  • 2 Sullivan EA, Zegers-Hochschild F, Mansour R , et al. International Committee for Monitoring Assisted Reproductive Technologies (ICMART) world report: assisted reproductive technology 2004. Hum Reprod 2013; 28 (5) 1375-1390
  • 3 Rock J, Menkin MF. In vitro fertilization and cleavage of human ovarian eggs. Science 1944; 100 (2588) 105-107
  • 4 Edwards RG, Donahue RP, Baramki TA, Jones Jr HW. Preliminary attempts to fertilize human oocytes matured in vitro. Am J Obstet Gynecol 1966; 96 (2) 192-200
  • 5 Shettles LB. A morula stage of human ovum developed in vitro. Fertil Steril 1955; 6 (4) 287-289
  • 6 Steptoe PC, Edwards RG, Purdy JM. Human blastocysts grown in culture. Nature 1971; 229 (5280) 132-133
  • 7 Shettles LB. Human blastocyst grown in vitro in ovulation cervical mucus. Nature 1971; 229 (5283) 343
  • 8 Jones Jr HW, Jones GS, Andrews MC , et al. The program for in vitro fertilization at Norfolk. Fertil Steril 1982; 38 (1) 14-21
  • 9 Gleicher N, Barad D. The relative myth of elective single embryo transfer. Hum Reprod 2006; 21 (6) 1337-1344
  • 10 Gleicher N, Oleske DM, Tur-Kaspa I, Vidali A, Karande V. Reducing the risk of high-order multiple pregnancy after ovarian stimulation with gonadotropins. N Engl J Med 2000; 343 (1) 2-7
  • 11 The ESHRE Capri Workshop Group. Multiple gestation pregnancy. Hum Reprod 2000; 15 (8) 1856-1864
  • 12 Edwards RG, Purdy JM, Steptoe PC, Walters DE. The growth of human preimplantation embryos in vitro. Am J Obstet Gynecol 1981; 141 (4) 408-416
  • 13 Hill GA, Freeman M, Bastias MC , et al. The influence of oocyte maturity and embryo quality on pregnancy rate in a program for in vitro fertilization-embryo transfer. Fertil Steril 1989; 52 (5) 801-806
  • 14 Desai NN, Goldstein J, Rowland DY, Goldfarb JM. Morphological evaluation of human embryos and derivation of an embryo quality scoring system specific for day 3 embryos: a preliminary study. Hum Reprod 2000; 15 (10) 2190-2196
  • 15 Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 2011; 26 (6) 1270-1283
  • 16 Ferraretti AP, Goossens V, de Mouzon J , et al; European IVF-monitoring (EIM); Consortium for European Society of Human Reproduction and Embryology (ESHRE). Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE. Hum Reprod 2012; 27 (9) 2571-2584
  • 17 CDC. Centres for Disease Control and Prevention. Reproductive health. Assisted reproductive technology. 2010 ART National Summary Report. Available at: http://www.cdc.gov/art/ART2010/PDFs/ART_2010_National_Summary_Report.pdf . Accessed on December 23, 2013
  • 18 Ebner T, Moser M, Sommergruber M, Tews G. Selection based on morphological assessment of oocytes and embryos at different stages of preimplantation development: a review. Hum Reprod Update 2003; 9 (3) 251-262
  • 19 Machtinger R, Racowsky C. Morphological systems of human embryo assessment and clinical evidence. Reprod Biomed Online 2013; 26 (3) 210-221
  • 20 Wong CC, Loewke KE, Bossert NL , et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 2010; 28 (10) 1115-1121
  • 21 Meseguer M, Herrero J, Tejera A, Hilligsøe KM, Ramsing NB, Remohí J. The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 2011; 26 (10) 2658-2671
  • 22 Hashimoto S, Kato N, Saeki K, Morimoto Y. Selection of high-potential embryos by culture in poly(dimethylsiloxane) microwells and time-lapse imaging. Fertil Steril 2012; 97 (2) 332-337
  • 23 Kirkegaard K, Hindkjaer JJ, Grøndahl ML, Kesmodel US, Ingerslev HJ. A randomized clinical trial comparing embryo culture in a conventional incubator with a time-lapse incubator. J Assist Reprod Genet 2012; 29 (6) 565-572
  • 24 van Echten-Arends J, Mastenbroek S, Sikkema-Raddatz B , et al. Chromosomal mosaicism in human preimplantation embryos: a systematic review. Hum Reprod Update 2011; 17 (5) 620-627
  • 25 Verlinsky Y, Cieslak J, Freidine M , et al. Pregnancies following pre-conception diagnosis of common aneuploidies by fluorescent in-situ hybridization. Hum Reprod 1995; 10 (7) 1923-1927
  • 26 Harper JC, Wilton L, Traeger-Synodinos J , et al; The ESHRE PGD Consortium. The ESHRE PGD Consortium: 10 years of data collection. Hum Reprod Update 2012; 18 (3) 234-247
  • 27 Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001; 2 (4) 280-291
  • 28 Lintsen AM, Eijkemans MJ, Hunault CC , et al. Predicting ongoing pregnancy chances after IVF and ICSI: a national prospective study. Hum Reprod 2007; 22 (9) 2455-2462
  • 29 Munné S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril 1995; 64 (2) 382-391
  • 30 Márquez C, Sandalinas M, Bahçe M, Alikani M, Munné S. Chromosome abnormalities in 1255 cleavage-stage human embryos. Reprod Biomed Online 2000; 1 (1) 17-26
  • 31 Silber S, Escudero T, Lenahan K, Abdelhadi I, Kilani Z, Munné S. Chromosomal abnormalities in embryos derived from testicular sperm extraction. Fertil Steril 2003; 79 (1) 30-38
  • 32 Werlin L, Rodi I, DeCherney A, Marello E, Hill D, Munné S. Preimplantation genetic diagnosis as both a therapeutic and diagnostic tool in assisted reproductive technology. Fertil Steril 2003; 80 (2) 467-468
  • 33 Munné S, Sandalinas M, Magli C, Gianaroli L, Cohen J, Warburton D. Increased rate of aneuploid embryos in young women with previous aneuploid conceptions. Prenat Diagn 2004; 24 (8) 638-643
  • 34 Kahraman S, Benkhalifa M, Donmez E , et al. The results of aneuploidy screening in 276 couples undergoing assisted reproductive techniques. Prenat Diagn 2004; 24 (4) 307-311
  • 35 Wilding M, Forman R, Hogewind G , et al. Preimplantation genetic diagnosis for the treatment of failed in vitro fertilization-embryo transfer and habitual abortion. Fertil Steril 2004; 81 (5) 1302-1307
  • 36 Platteau P, Staessen C, Michiels A, Van Steirteghem A, Liebaers I, Devroey P. Preimplantation genetic diagnosis for aneuploidy screening in patients with unexplained recurrent miscarriages. Fertil Steril 2005; 83 (2) 393-397 , quiz 525–526
  • 37 Rubio C, Pehlivan T, Rodrigo L, Simón C, Remohí J, Pellicer A. Embryo aneuploidy screening for unexplained recurrent miscarriage: a minireview. Am J Reprod Immunol 2005; 53 (4) 159-165
  • 38 Baart EB, Martini E, van den Berg I , et al. Preimplantation genetic screening reveals a high incidence of aneuploidy and mosaicism in embryos from young women undergoing IVF. Hum Reprod 2006; 21 (1) 223-233
  • 39 Staessen C, Verpoest W, Donoso P , et al. Preimplantation genetic screening does not improve delivery rate in women under the age of 36 following single-embryo transfer. Hum Reprod 2008; 23 (12) 2818-2825
  • 40 Gianaroli L, Magli MC, Ferraretti AP, Munné S. Preimplantation diagnosis for aneuploidies in patients undergoing in vitro fertilization with a poor prognosis: identification of the categories for which it should be proposed. Fertil Steril 1999; 72 (5) 837-844
  • 41 Munné S, Magli C, Cohen J , et al. Positive outcome after preimplantation diagnosis of aneuploidy in human embryos. Hum Reprod 1999; 14 (9) 2191-2199
  • 42 Obasaju M, Kadam A, Biancardi T, Sultan K, Fateh M, Munné S. Pregnancies from single normal embryo transfer in women older than 40 years. Reprod Biomed Online 2001; 2 (2) 98-101
  • 43 Munné S, Sandalinas M, Escudero T , et al. Improved implantation after preimplantation genetic diagnosis of aneuploidy. Reprod Biomed Online 2003; 7 (1) 91-97
  • 44 Montag M, van der Ven K, Dorn C, van der Ven H. Outcome of laser-assisted polar body biopsy and aneuploidy testing. Reprod Biomed Online 2004; 9 (4) 425-429
  • 45 Mastenbroek S, Twisk M, van der Veen F, Repping S. Preimplantation genetic screening: a systematic review and meta-analysis of RCTs. Hum Reprod Update 2011; 17 (4) 454-466
  • 46 Twisk M, Mastenbroek S, van Wely M, Heineman MJ, Van der Veen F, Repping S. Preimplantation genetic screening for abnormal number of chromosomes (aneuploidies) in in vitro fertilisation or intracytoplasmic sperm injection. Cochrane Database Syst Rev 2006; (1) CD005291
  • 47 Mastenbroek S, Scriven P, Twisk M, Viville S, Van der Veen F, Repping S. What next for preimplantation genetic screening? More randomized controlled trials needed?. Hum Reprod 2008; 23 (12) 2626-2628
  • 48 De Vos A, Van Steirteghem A. Aspects of biopsy procedures prior to preimplantation genetic diagnosis. Prenat Diagn 2001; 21 (9) 767-780
  • 49 Cohen J, Wells D, Munné S. Removal of 2 cells from cleavage stage embryos is likely to reduce the efficacy of chromosomal tests that are used to enhance implantation rates. Fertil Steril 2007; 87 (3) 496-503
  • 50 Goossens V, De Rycke M, De Vos A , et al. Diagnostic efficiency, embryonic development and clinical outcome after the biopsy of one or two blastomeres for preimplantation genetic diagnosis. Hum Reprod 2008; 23 (3) 481-492
  • 51 De Vos A, Staessen C, De Rycke M , et al. Impact of cleavage-stage embryo biopsy in view of PGD on human blastocyst implantation: a prospective cohort of single embryo transfers. Hum Reprod 2009; 24 (12) 2988-2996
  • 52 Scriven PN, Bossuyt PM. Diagnostic accuracy: theoretical models for preimplantation genetic testing of a single nucleus using the fluorescence in situ hybridization technique. Hum Reprod 2010; 25 (10) 2622-2628
  • 53 Wilton L, Voullaire L, Sargeant P, Williamson R, McBain J. Preimplantation aneuploidy screening using comparative genomic hybridization or fluorescence in situ hybridization of embryos from patients with recurrent implantation failure. Fertil Steril 2003; 80 (4) 860-868
  • 54 Vanneste E, Voet T, Le Caignec C , et al. Chromosome instability is common in human cleavage-stage embryos. Nat Med 2009; 15 (5) 577-583
  • 55 Munné S, Dailey T, Sultan KM, Grifo J, Cohen J. The use of first polar bodies for preimplantation diagnosis of aneuploidy. Hum Reprod 1995; 10 (4) 1014-1020
  • 56 McArthur SJ, Leigh D, Marshall JT, de Boer KA, Jansen RP. Pregnancies and live births after trophectoderm biopsy and preimplantation genetic testing of human blastocysts. Fertil Steril 2005; 84 (6) 1628-1636
  • 57 Fragouli E, Alfarawati S, Daphnis DD , et al. Cytogenetic analysis of human blastocysts with the use of FISH, CGH and aCGH: scientific data and technical evaluation. Hum Reprod 2011; 26 (2) 480-490
  • 58 Scott Jr RT, Ferry K, Su J, Tao X, Scott K, Treff NR. Comprehensive chromosome screening is highly predictive of the reproductive potential of human embryos: a prospective, blinded, nonselection study. Fertil Steril 2012; 97 (4) 870-875
  • 59 Voullaire L, Slater H, Williamson R, Wilton L. Chromosome analysis of blastomeres from human embryos by using comparative genomic hybridization. Hum Genet 2000; 106 (2) 210-217
  • 60 Fragouli E, Lenzi M, Ross R, Katz-Jaffe M, Schoolcraft WB, Wells D. Comprehensive molecular cytogenetic analysis of the human blastocyst stage. Hum Reprod 2008; 23 (11) 2596-2608
  • 61 Wells D, Delhanty JD. Comprehensive chromosomal analysis of human preimplantation embryos using whole genome amplification and single cell comparative genomic hybridization. Mol Hum Reprod 2000; 6 (11) 1055-1062
  • 62 Handyside AH, Robinson MD, Simpson RJ , et al. Isothermal whole genome amplification from single and small numbers of cells: a new era for preimplantation genetic diagnosis of inherited disease. Mol Hum Reprod 2004; 10 (10) 767-772
  • 63 Le Caignec C, Spits C, Sermon K , et al. Single-cell chromosomal imbalances detection by array CGH. Nucleic Acids Res 2006; 34 (9) e68
  • 64 Spits C, Le Caignec C, De Rycke M , et al. Whole-genome multiple displacement amplification from single cells. Nat Protoc 2006; 1 (4) 1965-1970
  • 65 Iwamoto K, Bundo M, Ueda J , et al. Detection of chromosomal structural alterations in single cells by SNP arrays: a systematic survey of amplification bias and optimized workflow. PLoS ONE 2007; 2 (12) e1306
  • 66 Forman EJ, Hong KH, Ferry KM , et al. In vitro fertilization with single euploid blastocyst transfer: a randomized controlled trial. Fertil Steril 2013; 100 (1) 100 , e1
  • 67 Capalbo A, Bono S, Spizzichino L , et al. Sequential comprehensive chromosome analysis on polar bodies, blastomeres and trophoblast: insights into female meiotic errors and chromosomal segregation in the preimplantation window of embryo development. Hum Reprod 2013; 28 (2) 509-518
  • 68 Harper J, Sermon K, Geraedts J , et al. What next for preimplantation genetic screening?. Hum Reprod 2008; 23 (3) 478-480
  • 69 Geraedts J, Collins J, Gianaroli L , et al. What next for preimplantation genetic screening? A polar body approach!. Hum Reprod 2010; 25 (3) 575-577
  • 70 Geraedts J, Montag M, Magli MC , et al. Polar body array CGH for prediction of the status of the corresponding oocyte. Part I: clinical results. Hum Reprod 2011; 26 (11) 3173-3180
  • 71 Gleicher N, Barad DH. A review of, and commentary on, the ongoing second clinical introduction of preimplantation genetic screening (PGS) to routine IVF practice. J Assist Reprod Genet 2012; 29 (11) 1159-1166
  • 72 Montag M, Schimming T, Köster M , et al. Oocyte zona birefringence intensity is associated with embryonic implantation potential in ICSI cycles. Reprod Biomed Online 2008; 16 (2) 239-244
  • 73 Wang WH, Meng L, Hackett RJ, Odenbourg R, Keefe DL. The spindle observation and its relationship with fertilization after intracytoplasmic sperm injection in living human oocytes. Fertil Steril 2001; 75 (2) 348-353
  • 74 Molinari E, Evangelista F, Racca C, Cagnazzo C, Revelli A. Polarized light microscopy-detectable structures of human oocytes and embryos are related to the likelihood of conception in IVF. J Assist Reprod Genet 2012; 29 (10) 1117-1122
  • 75 Tejera A, Herrero J, de Los Santos MJ, Garrido N, Ramsing N, Meseguer M. Oxygen consumption is a quality marker for human oocyte competence conditioned by ovarian stimulation regimens. Fertil Steril 2011; 96 (3) 618-623 , e2
  • 76 Tejera A, Herrero J, Viloria T, Romero JL, Gamiz P, Meseguer M. Time-dependent O2 consumption patterns determined optimal time ranges for selecting viable human embryos. Fertil Steril 2012; 98 (4) 849-857 , e1–e3
  • 77 Hardy K, Hooper MA, Handyside AH, Rutherford AJ, Winston RM, Leese HJ. Non-invasive measurement of glucose and pyruvate uptake by individual human oocytes and preimplantation embryos. Hum Reprod 1989; 4 (2) 188-191
  • 78 Gott AL, Hardy K, Winston RM, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod 1990; 5 (1) 104-108
  • 79 Gardner DK, Lane M, Stevens J, Schoolcraft WB. Noninvasive assessment of human embryo nutrient consumption as a measure of developmental potential. Fertil Steril 2001; 76 (6) 1175-1180
  • 80 Conaghan J, Handyside AH, Winston RM, Leese HJ. Effects of pyruvate and glucose on the development of human preimplantation embryos in vitro. J Reprod Fertil 1993; 99 (1) 87-95
  • 81 Conaghan J, Hardy K, Handyside AH, Winston RM, Leese HJ. Selection criteria for human embryo transfer: a comparison of pyruvate uptake and morphology. J Assist Reprod Genet 1993; 10 (1) 21-30
  • 82 Turner K, Martin KL, Woodward BJ, Lenton EA, Leese HJ. Comparison of pyruvate uptake by embryos derived from conception and non-conception natural cycles. Hum Reprod 1994; 9 (12) 2362-2366
  • 83 Houghton FD, Hawkhead JA, Humpherson PG , et al. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 2002; 17 (4) 999-1005
  • 84 Brison DR, Houghton FD, Falconer D , et al. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 2004; 19 (10) 2319-2324
  • 85 Seli E, Botros L, Sakkas D, Burns DH. Noninvasive metabolomic profiling of embryo culture media using proton nuclear magnetic resonance correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril 2008; 90 (6) 2183-2189
  • 86 Katz-Jaffe MG, Gardner DK, Schoolcraft WB. Proteomic analysis of individual human embryos to identify novel biomarkers of development and viability. Fertil Steril 2006; 85 (1) 101-107
  • 87 Nel-Themaat L, Nagy ZP. A review of the promises and pitfalls of oocyte and embryo metabolomics. Placenta 2011; 32 (Suppl. 03) S257-S263
  • 88 Seli E, Sakkas D, Scott R, Kwok SC, Rosendahl SM, Burns DH. Noninvasive metabolomic profiling of embryo culture media using Raman and near-infrared spectroscopy correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril 2007; 88 (5) 1350-1357
  • 89 Vergouw CG, Botros LL, Roos P , et al. Metabolomic profiling by near-infrared spectroscopy as a tool to assess embryo viability: a novel, non-invasive method for embryo selection. Hum Reprod 2008; 23 (7) 1499-1504
  • 90 Vergouw CG, Kieslinger DC, Kostelijk EH , et al. Day 3 embryo selection by metabolomic profiling of culture medium with near-infrared spectroscopy as an adjunct to morphology: a randomized controlled trial. Hum Reprod 2012; 27 (8) 2304-2311
  • 91 Hardarson T, Ahlström A, Rogberg L , et al. Non-invasive metabolomic profiling of Day 2 and 5 embryo culture medium: a prospective randomized trial. Hum Reprod 2012; 27 (1) 89-96
  • 92 Katz-Jaffe MG, Gardner DK. Symposium: innovative techniques in human embryo viability assessment. Can proteomics help to shape the future of human assisted conception?. Reprod Biomed Online 2008; 17 (4) 497-501
  • 93 Edgar DH, Bourne H, Speirs AL, McBain JC. A quantitative analysis of the impact of cryopreservation on the implantation potential of human early cleavage stage embryos. Hum Reprod 2000; 15 (1) 175-179
  • 94 Wang JX, Yap YY, Matthews CD. Frozen-thawed embryo transfer: influence of clinical factors on implantation rate and risk of multiple conception. Hum Reprod 2001; 16 (11) 2316-2319
  • 95 Shaw JM, Jones GM. Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum Reprod Update 2003; 9 (6) 583-605
  • 96 Zhang J, Chang L, Sone Y, Silber S. Minimal ovarian stimulation (mini-IVF) for IVF utilizing vitrification and cryopreserved embryo transfer. Reprod Biomed Online 2010; 21 (4) 485-495
  • 97 Youssry M, Ozmen B, Zohni K, Diedrich K, Al-Hasani S. Current aspects of blastocyst cryopreservation. Reprod Biomed Online 2008; 16 (2) 311-320
  • 98 Liebermann J, Nawroth F, Isachenko V, Isachenko E, Rahimi G, Tucker MJ. Potential importance of vitrification in reproductive medicine. Biol Reprod 2002; 67 (6) 1671-1680
  • 99 Kolibianakis EM, Venetis CA, Tarlatzis BC. Cryopreservation of human embryos by vitrification or slow freezing: which one is better?. Curr Opin Obstet Gynecol 2009; 21 (3) 270-274
  • 100 Loutradi KE, Kolibianakis EM, Venetis CA , et al. Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil Steril 2008; 90 (1) 186-193
  • 101 AbdelHafez FF, Desai N, Abou-Setta AM, Falcone T, Goldfarb J. Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod Biomed Online 2010; 20 (2) 209-222
  • 102 Paulson RJ, Sauer MV, Lobo RA. Embryo implantation after human in vitro fertilization: importance of endometrial receptivity. Fertil Steril 1990; 53 (5) 870-874
  • 103 Check JH, Choe JK, Katsoff D, Summers-Chase D, Wilson C. Controlled ovarian hyperstimulation adversely affects implantation following in vitro fertilization-embryo transfer. J Assist Reprod Genet 1999; 16 (8) 416-420
  • 104 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 (1) 20-26
  • 105 Krikun G, Schatz F, Taylor R , et al. Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. J Clin Endocrinol Metab 2005; 90 (3) 1812-1818
  • 106 Liu Y, Lee KF, Ng EH, Yeung WS, Ho PC. Gene expression profiling of human peri-implantation endometria between natural and stimulated cycles. Fertil Steril 2008; 90 (6) 2152-2164
  • 107 D'Angelo A, Amso N. Embryo freezing for preventing ovarian hyperstimulation syndrome. Cochrane Database Syst Rev 2007; (3) CD002806
  • 108 Check JH, O'Shaughnessy A, Lurie D, Fisher C, Adelson HG. Evaluation of the mechanism for higher pregnancy rates in donor oocyte recipients by comparison of fresh with frozen embryo transfer pregnancy rates in a shared oocyte programme. Hum Reprod 1995; 10 (11) 3022-3027
  • 109 Aflatoonian A, Oskouian H, Ahmadi S, Oskouian L. Can fresh embryo transfers be replaced by cryopreserved-thawed embryo transfers in assisted reproductive cycles? A randomized controlled trial. J Assist Reprod Genet 2010; 27 (7) 357-363
  • 110 Shapiro BS, Daneshmand ST, Garner FC, Aguirre M, Hudson C, Thomas S. 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 2011; 96 (2) 344-348
  • 111 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 (2) 368-377 , e1–e9