Selecting the most competent embryo

Biennial Review of Infertility: Volume 1

Volumn , Issue , 2009, Pages 143-169

  Ceyhan, S Temel ^a   Jackson, Katharine V ^a   Racowsky, Catherine ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Implan tation; Morphology scoring; Noninvasive embryo selection; Spectroscopic metabolomic profiling

Indexed keywords

EID: 77955577427     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-60327-392-3_10     Document Type: Chapter

References (185)

1. Boiso I, Veiga A, Edawards RG. Fundamentals of human embryonic growth in vitro and the selection of high-quality embryos for transfer. Reprod Biomed Online 2002;5(3):328-350.
2. Söderström-Anttila V, Vilska S. Five years of single embryo transfer with anonymous and non-anonymous oocyte donation. Reprod Biomed Online 2007;15(4):428-433. (Pubitemid 47565011)
3. Palermo G, Joris H, Devroey P. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 1992;340(8810):17-18.
4. Van Steirteghem A, Nagy Z, Joris H. High fertilization and implantation rates after intracytoplasmic sperm injection. Hum Reprod 1993;8(7):1061-1066. (Pubitemid 23204690)
5. Veeck LL. The morphologic estimation of mature oocytes and their preparation for insemination. In: Jones HW Jr, Jones GS, Hodgen GD, and Rosenwack Z, eds. In Vitro Fertilization-Norfolk. Baltimore: Williams & Wilkins, 1986:81.
6. Rattanachaiyanont M, Leader A, Léveillé MC. Lack of correlation between oocyte-corona-cumulus complex morphology and nuclear maturity of oocytes collected in stimulated cycles for intracytoplasmic sperm injection. Fertil Steril 1999;71(5):937-940. (Pubitemid 29206925)
7. Laufer N, Tarlatzis BC, DeCherney AH, Master JT, Haseltine FB, MacLusky N, Naftolin F. Asynchrony between human cumulus-corona cell complex and oocyte maturation after human menopausal gonadotropin treatment for in vitro fertilization. Fertil Steril 1984;42(3):366-372. (Pubitemid 14072153)
8. Khamsi F, Roberge S, Lacanna IC, Wong J, Yavas Y. Effects of granulosa cells, cumulus cells, and oocyte density on in vitro fertilization in women. Endocrine 1999;10(2):161-166. (Pubitemid 29295790)
9. Borini A, Lagalla C, Cattoli M, Sereni E, Sciajno R, Flamigni C, Coticchio G. Predictive factors for embryo implantation potential. Reprod Biomed Online 2005;10(5):653-668. (Pubitemid 40645550)
10. Balaban B, Urman B, Sertac A, Alatas C, Aksoy S, Mercan R. Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate after intracytoplasmic sperm injection. Hum Reprod 1998;13(12):3431-3433. (Pubitemid 29002637)
11. Balaban B, Urman B. Effect of oocyte morphology on embryo development and implantation. Reprod Biomed Online 2006;12(5):608-615. (Pubitemid 43674933)
12. Xia P. Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum Reprod 1997;12(8):1750-1755. (Pubitemid 27406092)
13. Mikkelsen AL, Lindenberg S. Morphology of in-vitro matured oocytes: impact on fertility potential and embryo quality. Hum Reprod 2001;16(8):1714-1718. (Pubitemid 32761757)
14. Rienzi L, Ubaldi F, Iacobelli M, Minasi M, Romano S, Ferrero S, Sapienza F, Baroni E, Litwicka K, Greco E. Significance of metaphase II human oocyte morphology on ICSI outcome. Fertil Steril 2008;90(5):1692-700, PMID: 18249393.
15. Garside WT, Loret de Mola J, Bucci JA, Tureck RW, Heyner S. Sequential analysis of zona thickness during in vitro culture of human zygotes: correlation with embryo quality, age, and implantation. Mol Reprod Dev 1997;47(1):99-104. (Pubitemid 27173055)
16. Loutradis D, Drakakis P, Kallianidis K, Milingos S, Dendrinos S, Michalas S. Oocyte morphology correlates with embryo quality and pregnancy rate after intracytoplasmic sperm injection. Fertil Steril 1999;72(2):240-244. (Pubitemid 29364616)
17. Serhal PF, Ranieri DM, Kinis A, Marchant S, Davies M, Khadum IM. Oocyte morphology predicts outcome of intracytoplasmic sperm injection. Hum Reprod 1997;12(6):1267-1270. (Pubitemid 27273558)
18. Kahraman S, Yakin K, Dönmez E, Samli H, Bahçe M, Cengiz G, Sertyel S, Samli M, Imirzalioglu N. Relationship between granular cytoplasm of oocytes and pregnancy outcome following intracytoplasmic sperm injection. Hum Reprod 2000;15(11):2390-2393.
19. De Sutter P, Dozortsev D, Qian C, Dhont M. Oocyte morphology does not correlate with fertilization rate and embryo quality after intracytoplasmic sperm injection. Hum Reprod 1996;11(3):595-597. (Pubitemid 26125266)
20. Eichhenlaub-Ritter U, Schmiady H, Kentenich H, Soewarto D. Recurrent failure in polar body formation and premature chromosome condensation in oocytes from a human patient: indicators of asynchrony in nuclear and cytoplasmic maturation. Human Reprod 1995;10(9):2343-2349.
21. Balakier H, Sojecki A, Motamedi G, Librach C. Timedependent capability of human oocytes for activation and pronuclear formation during metaphase II arrest. Hum Reprod 2004;19(4):982-987. (Pubitemid 38456066)
22. Hyun CS, Cha JH, Son WY, Yoon SH, Kim KA, Lim JH. Optimal ICSI timing after the first polar body extrusion in in vitro matured human oocytes. Hum Reprod 2007;22(7):1991-1995.
23. Ebner T, Yaman C, Moser M, Sommergruber M, Feichtinger O, Tews G. Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum Reprod 2000;15(2):427-430. (Pubitemid 30076725)
24. Fancsovits P, Tothne ZG, Murber A, Takacs FZ, Papp Z, Urbancek J. Correlation between first polar body morphology and further embryo development. Acta Biol Hung 2006;57(3):331-338. (Pubitemid 44583310)
25. Ciotti PM, Notarangelo L, Morselli-Labate AM, Felletti V, Porcu E, Venturoli S. First polar body morphology before ICSI is not related to embryo quality or pregnancy rate. Hum Reprod 2004;19(10):2334-2339. (Pubitemid 39406697)
26. Verlinsky Yury, Lerner S, Illkevitch N, Kuznetsov V, Kuznetsov I, Cieslak J, Kuliev A. Is there any predictive value of first polar body morphology for embryo genotype or developmental potential? Reprod Biomed Online 2003;7(3):336-341. (Pubitemid 37259289)
27. De Santis L, Cino I, Rabellotti E, Calzi F, Borini A, Coticchio G. Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod Biomed Online 2005;11(1):36-42. (Pubitemid 40960144)
28. Keefe D, Liu L, Wang W, Silva C. Imaging meiotic spindles by polarization light microscopy: principles and applications to IVF. Reprod Biomed Online 2003;7(1):24-29. (Pubitemid 36874402)
29. Oldenbourg R, Salmon ED, Tran PT. Birefringence of single and bundled microtubules. Biophys J 1998;74(1):645-654. (Pubitemid 28041793)
30. Liu L, Oldenbourg R, Trimarchi JR, Keefe DL. A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes. Nat Biotechnol 2000;18(2):223-225. (Pubitemid 30091187)
31. Wang WH, Meng L, Hackett RJ, Keefe DL. Developmental ability of human oocytes with or without birefringent spindles imaged by Polscope before insemination. Hum Reprod 2001;16(7):1464-1468. (Pubitemid 32640324)
32. 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. (Pubitemid 32112113)
33. Madaschi C, Carvalho de Souza Bonetti T, Paes de Almeida Ferreira Braga D, Pasqualotto F, Iaconelli A, Jr, Borges E, Jr. Spindle imaging: a marker for embryo development and implantation. Fertil Steril 2008;90(1):194-198. (Pubitemid 351885191)
34. Cohen Y, Malcov M, Schwartz T, Mey-Raz N, Carmon A, Cohen T, Lessing JB, Amit A, Azem F. Spindle imaging: a new marker for optimal timing of ICSI? Human Reprod 2004;19(3):649-654. (Pubitemid 38344530)
35. Moo JH, Hyun CS, Lee SW, Son WY, Yoon SH, Lim JH. Visualization of the metaphase II meiotic spindle in living human oocytes using the Polscope enables the prediction of embryonic developmental competence after ICSI. Human Reprod 2003;18(4):817-820.
36. Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 1996;11(10):2217-2222. (Pubitemid 26392017)
37. Shen Y, Betzendahl I, Tinneberg H, Eichenlaub-Ritter U. Enhanced polarizing microscopy as a new tool in aneuploidy research in oocytes. Mutat Res 2008;12:651(1-2):131-140.
38. Green D P L. Three-dimensional structure of the zona pellucida. Rev Reprod 1997;2(3):147-156. (Pubitemid 27416907)
39. Herrler A, Beier HM. Early embryonic coats: morphology, function, practical applications. An overview. Cells Tissues Organs 2000;166(2):233-246. (Pubitemid 30163559)
40. Cohen J, Inge KL, Suzman K, Wiker SG, Wright G. Videocinematography of fresh and cryopreserved embryos: a retrospective analysis of embryonic morphology and implantation. Fertil Steril 1989;51(5):820-827. (Pubitemid 19127855)
41. Garside WT, Loret de Mola JR, Bucci JA, Tureck RW, Heyner S. Sequential analysis of zona thickness during in vitro culture of human zygotes: correlation with embryo quality, age, and implantation. Mol Reprod Dev 1997;47(1):99-104. (Pubitemid 27173055)
42. Gabrielsen A, Lindenberg S, Petersen K. The impact of the zona pellucida thickness variation of human embryos on pregnancy outcome in relation to suboptimal embryo development. A prospective randomized controlled study. Hum Reprod 2001;16(10):2166-2170. (Pubitemid 32951912)
43. Shen Y, Stalf T, Mehnert C, Eichenlaub-Ritter, Tinneberg HR. High magnitude of light retardation by the zona pellucida is associated with conception cycles. Hum Reprod. 2005;20(6):1596-1606. (Pubitemid 40852254)
44. Tesarik J, Greco E. The probability of abnormal preimplantation development can be predicted by a single static observation on pronuclear stage morphology. Hum Reprod 1999;14(5):1318-1323. (Pubitemid 29224914)
45. Scott L, Alvero R, Leondires M, Miller B. The morphology of human pronuclear embryos is positively related to blastocyst development and implantation. Human Reprod 2000;15(11):2394-2403.
46. Balaban B, Urman B, Isklar A, Alatas C, Aksoy S, Mercan R, Mumcu A, Nunhglu A. The effects of pronuclear morphology on embryo quality parameters and blastocyst transfer outcome. Hum Reprod 2001;16(11):2357-2361. (Pubitemid 33054138)
47. Rienzi L, Ubaldi F, Iacobelli M, Ferrero S, Minasi MG, Martinez F, Tesarik J, Greco E. Day 3 embryo transfer with combined evaluation at the pronuclear and cleavage stages compares favourably with day 5 blastocyst transfer. Hum Reprod 2002;17(7):1852-1855. (Pubitemid 34790312)
48. Zollner U, Zollner KP, Hartl G, Dietl J, Steck T. The use of a detailed zygote score after IVF/ICSI to obtain good quality blastocysts: the German experience. Hum Reprod 2002;17(5):1327-1333. (Pubitemid 34537371)
49. Ludwig M, Schopper B, Al-Hasani S, Diedrich K. Clinical use of a pronuclear stage score following intracytoplasmic sperm injection: impact on pregnancy rates under the conditions of the German embryo protection law. Hum Reprod 2000;15(2):325-329. (Pubitemid 30076712)
50. Wittemer C, Bettahar-Lebugle K, Ohl J, Rongieres C, Nisand I, Gerlinger P. Zygote evaluation: an efficient tool for embryo selection. Hum Reprod 2000;15(12):2591-2597. (Pubitemid 32000518)
51. Montag M, van der Ven H. Evaluation of pronuclear morphology as the only selection criterion for further embryo culture and transfer: results of a prospective multicentre study. Hum Reprod 2001;16(11):2384-2389. (Pubitemid 33054142)
52. Zollner U, Zollner KP, Steck T, Dietl J. Pronuclear scoring: time for international standardization. J Reprod Med 2003(5);48:365-369. (Pubitemid 36613136)
53. Kahraman S, Kumtepe Y, Sertyel S, Donmez E, Benkhalifa M, Findikli N, Vanderzwalmen P. Pronuclear morphology scoring and chromosomal status of embryos in severe male infertility. Hum Reprod 2002;17(12):3193-3200. (Pubitemid 35469273)
54. Balaban B, Yakin K, Urman B, Isiklar A, Tesarik J. Pronuclear morphology predicts embryo development and chromosome constitution. Reprod Biomed Online 2004;8(6):695-700. (Pubitemid 38744951)
55. Gianarolli L, Magli MC, Ferrareti AP, Fortini D, Grieco N. Pronuclear morphology and chromosomal abnormalities as scoring criteria for embryo selection. Fertil Steril 2003;80(2):341-349. (Pubitemid 36959792)
56. Salumets A, Hydén-Granskog C, Suikkari AM, Tiitinen A, Tuuri T. The predictive value of pronuclear morphology of zygotes in the assessment of human embryo quality. Hum Reprod 2001;16(10):2177-2181. (Pubitemid 32951914)
57. Payne J, Raburn D, Couchman G, Price T, Jamison M, Walmer D. Relationship between pre-embryo pronuclear morphology (zygote score) and standard day 2 or 3 embryo morphology with regard to assisted reproductive technique outcomes. Fertil Steril 2005;84(4):900-909. (Pubitemid 41414579)
58. James AN, Hennessy S, Reggio B, Wiemer K, Larsen F, Cohen J. The limited importance of pronuclear scoring of human zygotes. Hum Reprod 2006;21(6):1599-1604. (Pubitemid 44445042)
59. Tesarik J, Kopecyn V. Development of human male pronucleus: ultrastructure and timing. Gamete Res 1989;24(2):135-149. (Pubitemid 19246495)
60. Nagy ZP, Janssenswillen C, Janssens R, De Vos A, Staessen C, Van de Velde H, Van Steirteghem AC. Timing of oocyte activation, pronucleus formation and cleavage in humans after intracytoplasmic sperm injection (ICSI) with testicular spermatozoa and after ICSI or in-vitro fertilizationn on sibling oocytes with ejaculated spermatozoa. Hum Reprod 1998;13(6):1606-1612. (Pubitemid 28310502)
61. Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum Reprod 2000;15(13):2621-2633. (Pubitemid 32000522)
62. Scott L. Pronuclear scoring as a predictor of embryo development. Reprod Biomed Online 2003;6(2):201-214. (Pubitemid 36857150)
63. Ebner T, Moser M, Sommergruber M, Gaiswinkler U, Wiesinger R, Puchner M, Tews G. Presence, but not type or degree of extension, of a cytoplasmic halo has a significant influence on preimplantation development and implantation behaviour. Hum Reprod 2003;18(11):2406-2412. (Pubitemid 37427824)
64. Stalf T, Herrero J, Mehnert C, Manolopoulos K, Lenhard A, Gips H. Influence of polarization effects in ooplasma and pronuclei on embryo quality and implantation in an IVF program. J Assist Reprod Genet 2002;19(8):355-362. (Pubitemid 34847950)
65. Balakier H, MacLusky NJ, Casper RF. Characterization of the first cell cycle in human zygotes: implications for cryopreservation. Fertil Steril 1993;59(2):359-365. (Pubitemid 23057790)
66. Trounson A, Mohr LR, Woos C, Leeton JF. Effect of delayed insemination on in-vitro fertilization, culture and transfer of human embryos. J Reprod Fertil 1982;64(2):285-294. (Pubitemid 12129819)
67. Terriou P, Giorgetti C, Hans E, Salzmann J, Charles O, Cignetti L, Avon C, Roulier R. Relationship between even early cleavage and day 2 embryo score and assessment of their predictive value for pregnancy. Reprod Biomed Online 2007;14(3):294-299. (Pubitemid 46463626)
68. Shoukir Y, Campana A, Farley T, Sakkas D. Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Hum Reprod 1997;12(7):1531-1536. (Pubitemid 27373211)
69. Guerif F, Le Gouge A, Giraudeau B, Poindron J, Bidault R, Gasnier O, Royere D. Limited value of morphological assessment at days 1 and 2 to predict blastocyst development potential: a prospective study based on 4042 embryos. Hum Reprod 2007;22(7):1973-1981. (Pubitemid 47062766)
70. Windt ML, Kruger TF, Coetzee K, Lombard CJ. Comparative analysis of pregnancy rates after the transfer of early dividing embryos versus slower dividing embryos. Hum Reprod 2004;19(5):1155-1162. (Pubitemid 38618498)
71. Lundin K, Bergh C, Hardarson T. Early embryo cleavage is a strong indicator of embryo quality in human IVF. Human Reprod 2001;16(12):2652-2657. (Pubitemid 34007486)
72. Hesters L, Prisant N, Fanchin R, Méndez Lozano D, Feyereisen E, Frydman R, Tachdjian G, Frydman N. Impact of early cleaved zygote morphology on embryo development and in vitro fertilization-embryo transfer outcome: a prospective study. Fertil Steril 2008;89(6):1677-1684.
73. Fenwick J, Platteau P, Murdoch AP, Herbert M. Time from insemination to first cleavage predits developmental competence of human preimplantation embryos in vitro. Human Reprod 2002;17(2):407-412. (Pubitemid 34168449)
74. Petersen CG, Mauri AL, Ferreira R, Baruffi R L R, Frango JG. Embryo selection by the first cleavage parameter between 25 and 27 hours after ICSI. J A Reprod Gen 2001;18(4):209-212. (Pubitemid 32574600)
75. Sundström P, Saldeen P. Early embryo cleavage and day 2 mononucleation after intracytoplasmatic sperm injection for predicting embryo implantation potential in single embryo transfer cycles. Fertil Steril 2008;89(2):475-477. (Pubitemid 351215388)
76. 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. (Pubitemid 11026998)
77. Giorgetti C, Terriou P, Auquier P, Hans E, Spach JL, Salzmann J, Roulier R. Embryo score to predict implantation after in-vitro fertilization: based on 957 single embryo transfers. Hum Reprod 1995;10(9):2427-2431.
78. Ziebe S, Petersen K, Lindenberg S, Andersen AG, Gabrielsen A, Andersen AN. Embryo morphology or cleavage stage: how to select the best embryos for transfer after in-vitro fertilization. Hum Reprod 1997;12(7):1545-1549. (Pubitemid 27373213)
79. Alikani M, Calderon G, Tomkin G, et al. Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro. Hum Reprod 2000;15(12):2634-2643. (Pubitemid 32000523)
80. Steer C, Mills C, Tan S, et al. The cumulative embryo score: a predictive embryo scoring technique to select the optimal number of embryos to transfer in an in-vitro fertilization and embryo transfer program. Hum Reprod 1992;7:117-119.
81. Puissant F, Van Rysselberge M, Barlow P, et al. Embryo scoring as a prognostic tool in IVF treatment. Hum Reprod 1987;2:705-708.
82. Carillo A, Lane B, Pridham D, et al. Improved clinical outcomes for in vitro fertilization with delay of embryo transfer from 48 to 72 hours after oocyte retrieval: use of glucose-and phosphate-free media. Fertil Steril 1998;69:329-334. (Pubitemid 28117114)
83. Racowsky C, Combelles C, Nureddin A, et al. Day 3 and day 5 morphological predictors of embryo viability. Reprod Biomed Online 2003;6:323-331. (Pubitemid 36849778)
84. Munne 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.
85. Jones G, Trounson A, Lolatgis N, et al. Factors affecting the success of human blastocyst development and pregnancy following in vitro fertilization and embryo transfer. Fertil Steril 1998;70:1022-1029. (Pubitemid 28546225)
86. Antczak M, Van Blerkom J. Temporal and spatial aspects of fragmentation in early human embryos: possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum Reprod 1999;14(2):429-447. (Pubitemid 29097399)
87. Alikani M, Cohen J, Tomkin G, Garrisi GJ, Mack C, Scott RT. Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertil Steril 1999;71(5):836-842. (Pubitemid 29206907)
88. Jurisicova A, Varmuza S, Casper RF. Programmed cell death and human embryo fragmentation. Mol Hum Reprod 1996;2(2):93-98. (Pubitemid 126715855)
89. Perez GI, Tao XJ, Tilly JL. Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Mol Hum Reprod 1999;5(5):414-420. (Pubitemid 29202197)
90. Pellestor F, Girardet A, Andréo B, Arnal F, Humeau C. Relationship between morphology and chromosomal constitution in human preimplantation embryo. Mol Reprod Dev 1994;39(2):141-146. (Pubitemid 24312154)
91. Munné S, Alikani M, Cohen J. Monospermic polyploidy and atypical embryo morphology. Hum Reprod 1994;9(3):506-510. (Pubitemid 24096408)
92. Sorimachi K, Naora H, Akimoto K, Niwa A, Naora H. Multinucleation and preservation of nucleolar integrity of macrophages. Cell Biol Int 1998;22(5):351-357. (Pubitemid 29149829)
93. Alikani M. The origins and consequences of fragmentation in mammalian eggs and embryos. In Human Preimplantation Embryo Selection. Elder K and Cohen J, eds. Informa Healthcare, London, UK, 2007:51-77.
94. Ebner T, Yaman C, Moser M, Sommergruber M, Pölz W, Tews G. Embryo fragmentation in vitro and its impact on treatment and pregnancy outcome. Fertil Steril 2001;76(2):281-285. (Pubitemid 32703815)
95. della Ragione T, Verheyen G, Papanikolaou EG, Van Landuyt L, Devroey P, Van Steirteghem A. Developmental stage on day-5 and fragmentation rate on day-3 can influence the implantation potential of top-quality blastocysts in IVF cycles with single embryo transfer. Reprod Biol Endocrinol 2007;5(2):1-8.
96. Stone B, Greene J, Vargyas J, Ringler G, Marrs R. Embryo fragmentation as a determinant of blastocyst development in vitro and pregnancy outcomes following embryo transfer. Am J Obstet Gynecol 2005;192(6):2014-2019.
97. Sathananthan H, Gunasheela S, Menezes J. Mechanics of human blastocyst hatching in vitro. Reprod Biomed Online 2003;7(2):228-234. (Pubitemid 37121072)
98. Rienzi L. Significance of morphological attributes of the early embryo. Reprod BioMed Online 2005;10(5):669-681. (Pubitemid 40645551)
99. Hardarson T, Hanson C, Sjogren A, Lundin K. Human embryos with unevenly sized blastomeres have lower pregnancy and implantation rates: indications for aneuploidy and multinucleation. Hum Reprod 2001;16:313-318. (Pubitemid 32149427)
100. Holte J, Berglund L, Milton K, Garello C, Gennarelli G, Revelli A, Bergh T. Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval. Hum Reprod 2007;22(2):548-557. (Pubitemid 46152580)
101. Van Royen E, Mangelschots K, Vercruyssen M, De Neubourg D, Valkenburg M, Ryckaert G, Gerris J. Multinucleation in cleavage stage embryos. Hum Reprod 2003;18(5):1062-1069. (Pubitemid 36592050)
102. Jackson KV, Ginsburg ES, Hornstein MD, Rein MS, Clarke RN. Multinucleation in normally fertilized embryos is associated with an accelerated ovulation induction response and lower implantation and pregnancy rates in in vitro fertilization-embryo transfer cycles. Fertil Steril 1998;70(1):60-66. (Pubitemid 28294623)
103. Saldeen P, Sundstrom P. Nuclear status of four-cell preembryos predicts implantation potential in in vitro fertilization treatment cycles. Fertil Steril 2005;84(3):584-589. (Pubitemid 41317714)
104. Kligman I, Benadiva C, Alikani M, Munne S. The presence of multinucleated blastomeres in human embryos is correlated with chromosomal abnormalities. Hum Reprod 1996;11:1492-1498. (Pubitemid 26335100)
105. Munne S, Cohen J. Unsuitability of multinucleated human blastomeres for preimplantation genetic diagnosis. Human Reprod 1993;8:1120-1125. (Pubitemid 23204702)
106. Moriwaki T, Suganuma N, Hayakawa M, Hibi H, Katsumata Y, Oguchi H, Furuhashi M. Embryo evaluation by analysing blastomere nuclei. Hum Reprod 2004;19(1):152-6. (Pubitemid 38072024)
107. Tao J, Tamis R, Fink K, et al. The neglected morula/compact stage embryo transfer. Hum Reprod 2002;17(6):1513-1518. (Pubitemid 34661800)
108. Nikas G, Ao A, Winston R M L, Handyside AH. Compaction and surface polarity in the human embryo in vitro. Biol Reprod 1996;55(1):32-37. (Pubitemid 26293138)
109. Desai N, Goldstein J, Rowland DY, Goldfarb MJ. 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.
110. Skiadas C, Jackson K, Racowsky C. Early compaction on day 3 may be associated with increased implantation potential. Fertil Steril 2006;86:1386-1391. (Pubitemid 44602038)
111. Feil D, Henshaw RC, Lane M. Day 4 embryo selection is equal to Day 5 using a new embryo scoring system validated in single embryo transfers. Hum Reprod 2008;23(7):1505-1510. (Pubitemid 351809692)
112. Steptoe PC, Edwards RG, Purdy JM. Human blastocyst grown culture. Nature 1971;229:132-133.
113. Bolton VN, Wren ME, Parsons JH. Pregnancies after in vitro fertilization and transfer of human blastocysts. Fertil Steril 1991;55(4):830-832.
114. Gardner DK, Lane M, Calderon I, Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil Steril 1996;65(2):349-353. (Pubitemid 26043831)
115. Ménézo Y J R, Hamamah S, Hazout A, Dale B. Time to switch from co-culture to sequential defined media for transfer at the blastocyst stage. Hum Reprod 1998;13(8):2043-2044. (Pubitemid 28425081)
116. Biggers JD, Racowsky C. The development of fertilized human ova to the blastocyst stage in KSOM (AA) medium: is a two-step protocol necessary? Reprod Biomed Online 2002;5(2):133-140.
117. Summers MC, Biggers JD. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update 2003;9(6):557-582. (Pubitemid 38072148)
118. Behr B, Fisch J, Racowsky C, Miller K, Pool T, Milki A. Blastocyst-ET and monozygotic twinning. J Assist Reprod Genet 2000;17:349-351.
119. Skiadas CC, Missmer SA, Benson CB, Gee RE, Racowsky C. Risk factors associated with pregnancies containing a monochorionic pair following assisted reproductive technologies. Hum Reprod 2008;23(6):1366-1371. (Pubitemid 351770566)
120. Racowsky C, Jackson KV, Cekleniak NA, Fox JH, Hornstein MD, Ginsburg ES. The number of eight-cell embryos is a key determinant for selecting day 3 or day 5 transfer. Fertil Steril 2000;73(3):558-564. (Pubitemid 30109655)
121. Gardner DK, Schoolcraft WB, Wagley L, Schlenker T, Stevens J, Hesla J. A prospective randomized trial of blastocyst culture and transfer in in-vitro fertilization. Hum Reprod 1998;13(12):3434-3440. (Pubitemid 29002638)
122. Marek D, Langley M, Gardner DK, Confer N, Doody KM, Doody KJ. Introduction of blastocyst culture and transfer for all patients in an in vitro fertilization program. Fertil Steril 1999;72(6):1035-1040.
123. Schoolcraft WB, Gardner DK, Lane M, Schlenker T, Hamilton F, Meldrum DR. Blastocyst culture and transfer: analysis of results and parameters affecting outcome in two in vitro fertilization programs. Fertil Steril 1999;72(4):604-609. (Pubitemid 29475115)
124. Papanikolaou EG, D'haeseleer E, Verheyen G, Van de Velde H, Camus M, Van Steirteghem A, Devroey P, Tournaye H. Live birth rate is significantly higher after blastocyst transfer than after cleavage-stage embryo transfer when at least four embryos are available on day 3 of embryo culture. A randomized prospective study. Hum Reprod 2005;20(11):3198-3203. (Pubitemid 41662678)
125. Milki AA, Hinckley MD, Gebhardt J, Dasig D, Westpal L, Behr B. Accuracy of day 3 criteria for selecting the best embryos. Fertil Steril 2002;77(6):1191-1195. (Pubitemid 34626328)
126. 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. (Pubitemid 36827062)
127. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four-and eight-cell stages of preimplantation development. Nature 1988;332(6163):459-461. (Pubitemid 18090251)
128. Sakkas D. The use of blastocyst culture to avoid inheritance of an abnormal paternal genome after ICSI. Hum Reprod 1999;14(1):4-5. (Pubitemid 29046301)
129. Sandalinas M, Sadowy S, Alikani M, Calderon G, Cohen J, Munné S. Developmental ability of chromosomally abnormal human embryos to develop to the blastocyst stage. Hum Reprod 2001;16(9):1954-1958. (Pubitemid 32916228)
130. Shi W, Haaf T. Aberrant methylation patterns at the twocell stage as an indicator of early developmental failure. Mol Reprod Dev 2002;63:329-334.
131. Ertzeid G, Stroreng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod 2001;16(2):221-225. (Pubitemid 32149411)
132. Fanchin R, Ayoubi JM, Righini C, Olivennes F, Schönauer LM, Frydman R. Uterine contractility decreases at the time of blastocyst transfers. Hum Reprod 2001;16(6):1115-1119. (Pubitemid 32544679)
133. Bungum M, Bungum L, Humaidan P, Yding Andersaen C. Day 3 versus day 5 embryo transfer: a prospective randomized study. Reprod Biomed Online 2003;7(1):98-104. (Pubitemid 36874418)
134. Cruz JR, Dubey AK, Patel J, Peak D, Hartog B, Gindoff PR. Is blastocyst transfer useful as an alternative treatment for patients with multiple in vitro fertilization failures? Fertil Steril 1999;72(2):218-220. (Pubitemid 29364610)
135. Balaban B, Urman B, Alatas C, Mercan R, Aksoy S, Isiklar A. Blastocyst-stage transfer of poor-quality cleavage-stage embryos results in higher implantation rates. Fertil Steril 2001;75(3):514-518. (Pubitemid 32177777)
136. Gardner D, Lane M, Stevens J, Schlenker T, Schoolcraft WB. Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 2000;73(6):1155-1158. (Pubitemid 30336760)
137. Gardner DK, Stevens J, Sheehan CB, Schoolcraft W. Analysis of blastocyst morphology. In Human Preimplantation Embryo Selection. Elder K and Cohen J, eds. Informa Healthcare, London, UK, 2007:79-87.
138. Cummins JM, Breen TM, Harrison KL, Shwan JM, Wilson LM, Hennessey JF. A formula for scoring human embryo growth rates in in vitro fertilization: its value in predicting pregnancy and in comparison with visual estimates of embryo quality. J In Vitro Fert Embryo Transf 1986;3(5):284-295. (Pubitemid 17208120)
139. Skiadas CC, Racowsky C. Developmental rate, cumulative scoring, and embryo viability. In Human Preimplantation Embryo Selection. Elder K and Cohen J, eds. Informa Healthcare, London, UK, 2007:101-121.
140. Veeck LL. Atlas of the human oocyte and early conceptus. Vol 2 Baltimore: Williams and Wilkins, 1991:427-444.
141. Giorgetti C, Terriou P, Auquier P, Hans E, Spach JL, Salzmann J, Roulier R. Embryo score to predict implantation after in-vitro fertilization: based on 957 single embryo transfers. Hum Reprod 1995;10(9):2427-2431.
142. Van Royen E, Mangelschots K, De Neubourg D, Valkenburg M, Van de Meerssche M, Ryckaert G, Eestermans W, Gerris J. Characterization of a top quality embryo, a step towards single-embryo transfer. Hum Reprod 1999;14(9):2345-2349. (Pubitemid 29425427)
143. Van Royen E, Mangelschots K, De Neubourg D, Laureys I, Ryckaert G, Gerris J. Calculating the implantation potential of day 3 embryos in women younger than 38 years of age: a new model. Human Reprod 2001;16(2):326-332. (Pubitemid 32149429)
144. Terriou P, Sapin C, Giorgetti C, Hans E, Spach JL, Roulier R. Embryo score is a better predictor of pregnancy than the number of transferred embryos or female age. Fertil Steril 2001;75(3):525-531. (Pubitemid 32175667)
145. Scott L, Finn A, O'Leary T, McLellan S, Hill J. Morphologic parameters of early cleavage-stage embryos that correlate with fetal development and delivery: prospective and applied data for increased pregnancy rates. Human Reprod 2007;22(1):230-340.
146. Peterson CM, Reading JC, Hatasaka HH, Parker Jones K, Udoff LC, Adashi EY, Kuneck PH, Erickson LD, Malo JW, Campbell BF, Carrell D. Use of outcomes-based data in reducing high-order multiple pregnancies: the role of age, diagnosis, and embryo score. Fertil Steril 2004;81(6):1534-1541. (Pubitemid 38748995)
147. Fisch J, Sher G, Adamowicz M, et al. The graduated embryo score predicts the outcome of assisted reproductive technologies better than a single day 3 evaluation and achieves results associated with blastocyst transfer from day 3 embryo transfer. Fertil Steril 2003;80:1352-1358. (Pubitemid 37532448)
148. Sakkas D, Percival G, D'Arcy Y, Sharif K, Afnan M. Assessment of early cleaving in vitro fertilized human embryos at the 2-cell stage before transfer improves embryo selection. Fertil Steril 2001;76(6):1150-1156. (Pubitemid 33116379)
149. Carrell DT, Peterson CM, Jones KP, Hatasaka HH, Udoff LC, Cornwell CE, Thorp C, Kuneck P, Erickson L, Campbell B. A simplified coculture system using homologous, attached cumulus tissue results in improved human embryo morphology and pregnancy rates during in vitro fertilization. J Assist Reprod Genet 1999;16(7):344-349. (Pubitemid 29384073)
150. Sjöblom P, Menezes J, Cummins L, Mathiyalagan B, Costello MF. Prediction of embryo developmental potential and pregnancy based on early stage morphological characteristics. Fertility Sterility 2006;86(4):848-861. (Pubitemid 44485053)
151. Hunault CC, Eijkemans MJ, Pieters MH, te Velde ER, Habbema JD, Fauser BC, Macklon NS. Aprediction model for selecting patients undergoing in vitro fertilization for elective single embryo transfer. Fertil Steril 2002;77(4):725-732. (Pubitemid 34275352)
152. Hardarson T, Caisander G, Sjögren A, Hanson C, Hamberger L, Lundin K. A morphological and chromosomal study of blastocysts developing from morphologically suboptimal human pre-embryos compared with control blastocysts. Hum Reprod 2003;18(2):399-407. (Pubitemid 36236277)
153. Ciray H, Karagenc L, Ulug U, et al. Early cleavage morphology affects the quality and implantation potential of day 3 embryos. Fertil Steril 2006;85:358-365. (Pubitemid 43170908)
154. Lan KC, Huang FJ, Lin YC, Kung FT, Hsieh CH, Huang HW, Tan PH, Chang SY. The predictive value of using a combined Z-score and day 3 embryo morphology score in the assessment of embryo survival on day 5. Hum Reprod 2003;18(6):1299-1306. (Pubitemid 36740581)
155. Brison DR, Hollywood K, Arnesen R, Goodacre R. Predicting human embryo viability: the road to non-invasive analysis of the secretome using metabolic footprinting. Reprod Biomed Online 2007;15(3):296-302. (Pubitemid 47430369)
156. Villas-Bôas S, Mas S, Åkesson M, Smedsgaard J, Nielsen J. Mass spectrometry in metabolome analysis. Mass Spect Rev 2005;24(5):613-646. (Pubitemid 41621943)
157. Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update 2001;7(4):419-427. (Pubitemid 32655328)
158. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001;64(3):918-926. (Pubitemid 32174065)
159. Leese HJ, Sturmey RG, Baumann CG, McEvoy TG. Embryo viability and metabolism: obeying the quiet rules. Hum Reprod 2007;22(12):3047-3050. (Pubitemid 351696765)
160. Lane M, Gardner DK. Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod Fertil Dev 2005;17(3):371-378. (Pubitemid 40425691)
161. Hardy K, Hooper M A K, Handyside AH, Rutherford AJ, Winston R M L, Leese HJ. Non-invasive measurement of glucose and pyruvate uptake by individual human oocytes and preimplantation embryos. Hum Reprod 1989;4(2):188-191. (Pubitemid 19069936)
162. Gott AL, Hardy K, Winston R M L, 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. (Pubitemid 20111643)
163. 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. (Pubitemid 23136592)
164. Gardner D, 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. (Pubitemid 33116382)
165. 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.
166. Devreker F, Hardy K, Van den Bergh M, Vannin AS, Emiliani S, Englert Y. Noninvasive assessment of glucose and pyruvate uptake by human embryos after intracytoplasmic sperm injection and during the formation of pronuclei. Fertil Steril 2000;73(5):947-954. (Pubitemid 30227517)
167. Jones GM, Trounson AO, Vella PJ, Thouas GA, Lolatgis N, Wood C. Glucose metabolism of human morula and blastocyst-stage embryos and its relationship to viability after transfer. Reprod Biomed Online 2001;3(2):124-132.
168. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, Humpherson PG, Lieberman BA, Leese HJ. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 2004;19(10):2319- 2324. (Pubitemid 39406695)
169. Houghton FD, Hawkhead JA, Humpherson PG, Hogg JE, Balen AH, Rutherford AJ, Leese HJ. Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 2002;17(4):999-1005. (Pubitemid 34411137)
170. Noci I, Fuzzi B, Rizzo R, Melchiorri L, Criscuoli L, Dabizz S, Biagiotti R, Pellegrini S, Menicucci A, Baricordi OR. Embryonic soluble HLA-G as a marker of developmental potential in embryos. Hum Reprod 2005;20(1):138-146.
171. Desai N, Fillipovits J, Goldfarb J. Secretion of soluble HLA-G by day 3 human embryos associated with higher pregnancy and implantation rates: assay of culture media using a new ELISA kit. Reprod Biomed Online 2006;13(2):272-277. (Pubitemid 44207777)
172. Fuzzi B, Rizzo R, Criscuoli L, Noci I, Melchiorri L, Scarselli B, Bencini E, Menicucci A, Baricordi OR. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002;32(2):311-315. (Pubitemid 34173321)
173. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 1987;329(6139):512-518. (Pubitemid 17131094)
174. Roussev RG, Coulam CB. HLA-G and its role in implantation. J Assist Reprod Genet 2007;24(7):288-2953 Review.
175. Chu W, Fant ME, Geraghty DE, Hunt JS. Soluble HLA-G in human placentas: synthesis in trophoblasts and interferongamma-activated macrophages but not placental fibroblasts. Hum Immunol 1998;59(7):435-442. (Pubitemid 28332493)
176. Jurisicova A, Casper RF, MacLusky NJ, Mills GB, Librach CL. HLA-G expression during preimplantation human embryo development. Proc Natl Acad Sci U S A 1996;9;93(1):161-165. (Pubitemid 26038120)
177. Fisch J, Keskintepe L, Ginsburg M, Adamowicz M, Sher G. Graduated Embryo Score and soluble human leukocyte antigen-G expression improve assisted reproductive technology outcomes and suggest a basis for elective singleembryo transfer. Fertil Steril 2007;87(4):757-763. (Pubitemid 46550397)
178. Sageshima N, Shobu T, Awai K, Hashimoto H, Yamashita M, Takeda N, Odawara Y, Nakanishi M, Hatake K, Ishitani A. Soluble HLA-G is absent from human embryo cultures: a reassessment of sHLA-G detection methods. J Reprod Immunol 2007;75(1):11-22. (Pubitemid 47081190)
179. Sargent I, Swales A, Ledee N, Kozma N, Tabiasco J, Le Bouteiller P. sHLA-G production by human IVF embryos: can it be measured reliably? J Reprod Immunol 2007;75(2):128-132. (Pubitemid 47384861)
180. Bromer JG, Seli E. Assessment of embryo viability in assisted reproductive technology: shortcomings of current approaches and the emerging role of metabolomics. Curr Opin Obstet Gynecol 2008;20(3):234-241. (Pubitemid 351643510)
181. Raamsdonk LM, Teusink B, Broadhurst D, Zhang N, Hayes A, Walsh MC, Berden JA, Brindle KM, Kell DB, Rowland JJ, Westerhoff HV, van Dam K, Oliver SG. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 2001;19(1):45-50. (Pubitemid 32051955)
182. Hollywood K, Brison DR, Goodacre R. Metabolomics: current technologies and future trends. Proteomics 2006;6(17):4716-4723. (Pubitemid 44375842)
183. 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. (Pubitemid 350030104)
184. Vergouw CG, Botros LL, Roos P, Lens JW, Schats R, Hompes PG, Burns DH, Lambalk CB. Metabolomic profiling by near-infrared spectroscopy as a tool to assess embryo viability: a novel, non-invasive method for embryo selection. Human Reprod 2008;23(7):1499-1504. (Pubitemid 351809705)
185. Scott R, Seli E, Miller K, Sakkas D, Scott K, Burns DH. Noninvasive metabolomic profiling of human embryo culture media using Raman spectroscopy predicts embryonic reproductive potential: a prospective blinded pilot study. Fertil Steril 2008;90(1):77-83.