Quality control and standardization of embryo morphology scoring and viability markers

Reproductive BioMedicine Online

Volumn 31, Issue 4, 2015, Pages 459-471

  Lundin, Kersti ^a   Ahlström, Aisling ^a  

^a SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

embryo; human; IVF; quality control; validation

Indexed keywords

BIOLOGICAL MARKER; DNA; PROTEIN; RNA; TRANSCRIPTOME;

BLASTOCYST; CONFERENCE PAPER; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; ENDOMETRIUM; GENE EXPRESSION; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; METABOLITE; MORPHOLOGY; NIDATION; QUALITY CONTROL; STANDARDIZATION; TIME LAPSE IMAGING; ANATOMY AND HISTOLOGY; EMBRYOLOGY; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION PROFILING; GENETIC SCREENING; LIVE BIRTH; MAMMALIAN EMBRYO; METABOLISM; NEWBORN; PREGNANCY; STANDARDS; VALIDATION STUDY;

BIOMARKERS; EMBRYO CULTURE TECHNIQUES; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; EMBRYOLOGY; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION PROFILING; GENETIC TESTING; HUMANS; INFANT, NEWBORN; LIVE BIRTH; PREGNANCY; QUALITY CONTROL; TIME-LAPSE IMAGING;

EID: 84943580875     PISSN: 14726483     EISSN: 14726491     Source Type: Journal    
DOI: 10.1016/j.rbmo.2015.06.026     Document Type: Conference Paper

References (130)

1. T. Adriaenssens, S. Wathlet, I. Segers, G. Verheyen, A. De Vos, J. Van Der Elst, W. Coucke, P. Devroey, and J. Smitz Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics Hum. Reprod 25 2010 1259 1270
2. J. Aguilar, Y. Motato, M.J. Escriba, M. Ojeda, E. Munoz, and M. Meseguer The human first cell cycle: impact on implantation Reprod. Biomed. Online 28 2014 475 484
3. A. Ahlstrom, C. Westin, E. Reismer, M. Wikland, and T. Hardarson Trophectoderm morphology: an important parameter for predicting live birth after single blastocyst transfer Hum. Reprod 26 2011 3289 3296
4. A. Ahlstrom, M. Wikland, L. Rogberg, J.S. Barnett, M. Tucker, and T. Hardarson Cross-validation and predictive value of near-infrared spectroscopy algorithms for day-5 blastocyst transfer Reprod. Biomed. Online 22 2011 477 484
5. 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 26 2011 1270 1283
6. B. Aparicio, M. Cruz, and M. Meseguer Is morphokinetic analysis the answer? Reprod. Biomed. Online 27 2013 654 663
7. J.C. Arce, S. Ziebe, K. Lundin, R. Janssens, L. Helmgaard, and P. Sorensen Interobserver agreement and intraobserver reproducibility of embryo quality assessments Hum. Reprod 21 2006 2141 2148
8. S. Armstrong, N. Arroll, L.M. Cree, V. Jordan, and C. Farquhar Time-lapse systems for embryo incubation and assessment in assisted reproduction Cochrane Database Syst. Rev 2 2015 CD011320
9. S. Assou, D. Haouzi, K. Mahmoud, A. Aouacheria, Y. Guillemin, V. Pantesco, T. Reme, H. Dechaud, J. De Vos, and S. Hamamah A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study Mol. Hum. Reprod 14 2008 711 719
10. A. Azzarello, T. Hoest, and A.L. Mikkelsen The impact of pronuclei morphology and dynamicity on live birth outcome after time-lapse culture Hum. Reprod 27 2012 2649 2657
11. B. Balaban, B. Urman, A. Sertac, C. Alatas, S. Aksoy, and R. Mercan Blastocyst quality affects the success of blastocyst-stage embryo transfer Fertil. Steril 74 2000 282 287
12. B. Balaban, K. Yakin, and B. Urman Randomized comparison of two different blastocyst grading systems Fertil. Steril 85 2006 559 563
13. N. Basile, D. Morbeck, J. Garcia-Velasco, F. Bronet, and M. Meseguer Type of culture media does not affect embryo kinetics: a time-lapse analysis of sibling oocytes Hum. Reprod 28 2013 634 641
14. A.E. Baxter Bendus, J.F. Mayer, S.K. Shipley, and W.H. Catherino Interobserver and intraobserver variation in day 3 embryo grading Fertil. Steril 86 2006 1608 1615
15. L. Botros, D. Sakkas, and E. Seli Metabolomics and its application for non-invasive embryo assessment in IVF Mol. Hum. Reprod 14 2008 679 690
16. P.J. Bridges, M. Jeoung, H. Kim, J.H. Kim, D.R. Lee, C. Ko, and D.J. Baker Methodology matters: IVF versus ICSI and embryonic gene expression Reprod. Biomed. Online 23 2011 234 244
17. D.R. Brison, F.D. Houghton, D. Falconer, S.A. Roberts, J. Hawkhead, P.G. Humpherson, B.A. Lieberman, and H.J. Leese Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover Hum. Reprod 19 2004 2319 2324
18. A. Campbell, S. Fishel, N. Bowman, S. Duffy, M. Sedler, and C.F. Hickman Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics Reprod. Biomed. Online 26 2013 477 485
19. A. Campbell, S. Fishel, N. Bowman, S. Duffy, M. Sedler, and S. Thornton Retrospective analysis of outcomes after IVF using an aneuploidy risk model derived from time-lapse imaging without PGS Reprod. Biomed. Online 27 2013 140 146
20. A. Capalbo, L. Rienzi, D. Cimadomo, R. Maggiulli, T. Elliott, G. Wright, Z.P. Nagy, and F.M. Ubaldi Correlation between standard blastocyst morphology, euploidy and implantation: an observational study in two centers involving 956 screened blastocysts Hum. Reprod 29 2014 1173 1181
21. J.A. Castilla, R. Ruiz De Assin, M.C. Gonzalvo, A. Clavero, J.P. Ramirez, F. Vergara, and L. Martinez External quality control for embryology laboratories Reprod. Biomed. Online 20 2010 68 74
22. A. Cervero, J.A. Horcajadas, F. Dominguez, A. Pellicer, and C. Simon Leptin system in embryo development and implantation: a protein in search of a function Reprod. Biomed. Online 10 2005 217 223
23. S. Chamayou, P. Patrizio, G. Storaci, V. Tomaselli, C. Alecci, C. Ragolia, C. Crescenzo, and A. Guglielmino The use of morphokinetic parameters to select all embryos with full capacity to implant J. Assist. Reprod. Genet 30 2013 703 710
24. S.L. Chavez, K.E. Loewke, Han J., F. Moussavi, P. Colls, S. Munne, B. Behr, and R.A. Reijo Pera Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage Nat Commun 3 2012 1251
25. Chen A.A., Tan L., V. Suraj, R. Reijo Pera, and Shen S. Biomarkers identified with time-lapse imaging: discovery, validation, and practical application Fertil. Steril 99 2013 1035 1043
26. Chen J.J., H.M. Hsueh, R.R. Delongchamp, Lin C.J., and C.A. Tsai Reproducibility of microarray data: a further analysis of microarray quality control (MAQC) data BMC Bioinform 8 2007 412
27. M. Cicconet, M. Gutwein, K.C. Gunsalus, and D. Geiger Label free cell-tracking and division detection based on 2D time-lapse images for lineage analysis of early embryo development Comput. Biol. Med 51 2014 24 34
28. F. Cillo, T.A. Brevini, S. Antonini, A. Paffoni, G. Ragni, and F. Gandolfi Association between human oocyte developmental competence and expression levels of some cumulus genes Reproduction 134 2007 645 650
29. H.N. Ciray, T. Aksoy, C. Goktas, B. Ozturk, and M. Bahceci Time-lapse evaluation of human embryo development in single versus sequential culture media - a sibling oocyte study J. Assist. Reprod. Genet 29 2012 891 900
30. H.N. Ciray, A. Campbell, I.E. Agerholm, J. Aguilar, S. Chamayou, M. Esbert, and S. Sayed Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group Hum. Reprod 29 2014 2650 2660
31. J. Conaghan, K. Hardy, A.H. Handyside, R.M. Winston, and H.J. Leese Selection criteria for human embryo transfer: a comparison of pyruvate uptake and morphology J. Assist. Reprod. Genet 10 1993 21 30
32. J. Conaghan, Chen A.A., S.P. Willman, K. Ivani, P.E. Chenette, R. Boostanfar, V.L. Baker, G.D. Adamson, M.E. Abusief, M. Gvakharia, K.E. Loewke, and Shen S. Improving embryo selection using a computer-automated time-lapse image analysis test plus day 3 morphology: results from a prospective multicenter trial Fertil. Steril 100 2013 412 419 e5
33. M. Cruz, N. Garrido, B. Gadea, M. Munoz, I. Perez-Cano, and M. Meseguer Oocyte insemination techniques are related to alterations of embryo developmental timing in an oocyte donation model Reprod. Biomed. Online 27 2013 367 375
34. M. Dal Canto, G. Coticchio, M. Mignini Renzini, E. De Ponti, P.V. Novara, F. Brambillasca, R. Comi, and R. Fadini Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation Reprod. Biomed. Online 25 2012 474 480
35. A.T. Dobson, R. Raja, M.J. Abeyta, T. Taylor, Shen S., C. Haqq, and R.A. Pera The unique transcriptome through day 3 of human preimplantation development Hum. Mol. Genet 13 2004 1461 1470
36. A. Dokras, I.L. Sargent, R.L. Gardner, and D.H. Barlow Human trophectoderm biopsy and secretion of chorionic gonadotrophin Hum. Reprod 6 1991 1453 1459
37. A. Dokras, I.L. Sargent, and D.H. Barlow Human blastocyst grading: an indicator of developmental potential? Hum. Reprod 8 1993 2119 2127
38. F. Dominguez, B. Gadea, F.J. Esteban, J.A. Horcajadas, A. Pellicer, and C. Simon Comparative protein-profile analysis of implanted versus non-implanted human blastocysts Hum. Reprod 23 2008 1993 2000
39. E.G. Ergin, E. Caliskan, E. Yalcinkaya, Z. Oztel, K. Cokelez, A. Ozay, and H.M. Ozornek Frequency of embryo multinucleation detected by time-lapse system and its impact on pregnancy outcome Fertil. Steril 102 2014 1029 1033 e1
40. P. Feuerstein, V. Puard, C. Chevalier, R. Teusan, V. Cadoret, F. Guerif, R. Houlgatte, and D. Royere Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors PLoS ONE 7 2012 e40449
41. T. Freour, L. Dessolle, J. Lammers, S. Lattes, and P. Barriere Comparison of embryo morphokinetics after in vitro fertilization-intracytoplasmic sperm injection in smoking and nonsmoking women Fertil. Steril 99 2013 1944 1950
42. D.K. Gardner, and W.B. Schoolcraft In virto culture of human blastocyst R. Janson, D. Mortimer, Towards Reproductive Certainty: Infertility and Genetics Beyond 1999 1999 Parthenon Press Carnforth
43. D.K. Gardner, M. Lane, J. Stevens, T. Schlenker, and W.B. Schoolcraft Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer Fertil. Steril 73 2000 1155 1158
44. D.K. Gardner, M. Lane, J. Stevens, and W.B. Schoolcraft Noninvasive assessment of human embryo nutrient consumption as a measure of developmental potential Fertil. Steril 76 2001 1175 1180
45. D.K. Gardner, E. Surrey, D. Minjarez, A. Leitz, J. Stevens, and W.B. Schoolcraft Single blastocyst transfer: a prospective randomized trial Fertil. Steril 81 2004 551 555
46. R. Goodacre Making sense of the metabolome using evolutionary computation: seeing the wood with the trees J. Exp. Bot 56 2005 245 254
47. R. Goodacre, S. Vaidyanathan, W.B. Dunn, G.G. Harrigan, and D.B. Kell Metabolomics by numbers: acquiring and understanding global metabolite data Trends Biotechnol 22 2004 245 252
48. C.E.W. Gributs, and D.H. Burns Parsimonious calibration models for near-infrared spectroscopy using wavelets and scaling functions Chemometrics and Intelligent Lab. Systems 83 2006 44 53
49. M. Hamel, I. Dufort, C. Robert, C. Gravel, M.C. Leveille, A. Leader, and M.A. Sirard Identification of differentially expressed markers in human follicular cells associated with competent oocytes Hum. Reprod 23 2008 1118 1127
50. M. Hamel, I. Dufort, C. Robert, M.C. Leveille, A. Leader, and M.A. Sirard Identification of follicular marker genes as pregnancy predictors for human IVF: new evidence for the involvement of luteinization process Mol. Hum. Reprod 16 2010 548 556
51. R. Hampl, and M. Stepan [Variability in timing of human embryos cleavage monitored by time-lapse system in relation to patient age]. Ceska Gynekol 78 2013 531 536
52. T. Hardarson, C. Lofman, G. Coull, A. Sjogren, L. Hamberger, and R.G. Edwards Internalization of cellular fragments in a human embryo: time-lapse recordings Reprod. Biomed. Online 5 2002 36 38
53. T. Hardarson, G. Caisander, A. Sjogren, C. Hanson, L. Hamberger, and K. Lundin A morphological and chromosomal study of blastocysts developing from morphologically suboptimal human pre-embryos compared with control blastocysts Hum. Reprod 18 2003 399 407
54. T. Hardarson, A. Ahlstrom, L. Rogberg, L. Botros, T. Hillensjo, G. Westlander, D. Sakkas, and M. Wikland Non-invasive metabolomic profiling of Day 2 and 5 embryo culture medium: a prospective randomized trial Hum. Reprod 27 2012 89 96
55. K. Hardy, M.A. Hooper, A.H. Handyside, A.J. Rutherford, R.M. Winston, and H.J. Leese Non-invasive measurement of glucose and pyruvate uptake by individual human oocytes and preimplantation embryos Hum. Reprod 4 1989 188 191
56. J. Herrero, A. Tejera, C. Albert, C. Vidal, M.J. De Los Santos, and M. Meseguer A time to look back: analysis of morphokinetic characteristics of human embryo development Fertil. Steril 100 2013 1602 1609 e1-4
57. M.J. Hill, K.S. Richter, R.J. Heitmann, J.R. Graham, M.J. Tucker, A.H. Decherney, P.E. Browne, and E.D. Levens Trophectoderm grade predicts outcomes of single-blastocyst transfers Fertil. Steril 99 2013 1283 1289 e1
58. D. Hlinka, B. Kalatova, I. Uhrinova, S. Dolinska, J. Rutarova, J. Rezacova, S. Lazarovska, and M. Dudas Time-lapse cleavage rating predicts human embryo viability Physiol. Res 61 2012 513 525
59. J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh 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 22 2007 548 557
60. F.D. Houghton, J.A. Hawkhead, P.G. Humpherson, J.E. Hogg, A.H. Balen, A.J. Rutherford, and H.J. Leese Non-invasive amino acid turnover predicts human embryo developmental capacity Hum. Reprod 17 2002 999 1005
61. J.P. Ioannidis, D.B. Allison, C.A. Ball, I. Coulibaly, Cui X., A.C. Culhane, M. Falchi, C. Furlanello, L. Game, G. Jurman, J. Mangion, T. Mehta, M. Nitzberg, G.P. Page, E. Petretto, and V. Van Noort Repeatability of published microarray gene expression analyses Nat. Genet 41 2009 149 155
62. G.M. Jones, A.O. Trounson, P.J. Vella, G.A. Thouas, N. Lolatgis, and C. Wood Glucose metabolism of human morula and blastocyst-stage embryos and its relationship to viability after transfer Reprod. Biomed. Online 3 2001 124 132
63. G.M. Jones, D.S. Cram, Song B., G. Kokkali, K. Pantos, and A.O. Trounson Novel strategy with potential to identify developmentally competent IVF blastocysts Hum. Reprod 23 2008 1748 1759
64. T. Kanai, T. Fujii, N. Unno, T. Yamashita, H. Hyodo, A. Miki, Y. Hamai, S. Kozuma, and Y. Taketani Human leukocyte antigen-G-expressing cells differently modulate the release of cytokines from mononuclear cells present in the decidua versus peripheral blood Am. J. Reprod. Immunol 45 2001 94 99
65. D.J. Kaser, and C. Racowsky Clinical outcomes following selection of human preimplantation embryos with time-lapse monitoring: a systematic review Hum. Reprod. Update 20 2014 617 631
66. K. Kirkegaard, I.E. Agerholm, and H.J. Ingerslev Time-lapse monitoring as a tool for clinical embryo assessment Hum. Reprod 27 2012 1277 1285
67. K. Kirkegaard, U.S. Kesmodel, J.J. Hindkjaer, and H.J. Ingerslev Time-lapse parameters as predictors of blastocyst development and pregnancy outcome in embryos from good prognosis patients: a prospective cohort study Hum. Reprod 28 2013 2643 2651
68. K. Kirkegaard, A. Campbell, I. Agerholm, U. Bentin-Ley, A. Gabrielsen, J. Kirk, S. Sayed, and H.J. Ingerslev Limitations of a time-lapse blastocyst prediction model: a large multicentre outcome analysis Reprod. Biomed. Online 29 2014 156 158
69. K. Knez, T. Tomazevic, E. Vrtacnik-Bokal, and I. Virant-Klun Developmental dynamics of IMSI-derived embryos: a time-lapse prospective study Reprod. Biomed. Online 27 2013 161 171
70. J.G. Lemmen, I. Agerholm, and S. Ziebe Kinetic markers of human embryo quality using time-lapse recordings of IVF/ICSI-fertilized oocytes Reprod. Biomed. Online 17 2008 385 391
71. P. Lonergan, T. Fair, D. Corcoran, and A.C.O. Evans Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos Theriogenology 65 2006 137 152
72. B. Luke, M.B. Brown, J.E. Stern, S.K. Jindal, C. Racowsky, and G.D. Ball Using the Society for Assisted Reproductive Technology Clinic Outcome System morphological measures to predict live birth after assisted reproductive technology Fertil. Steril 102 2014 1338 1344
73. M.C. Magli, L. Gianaroli, and A.P. Ferraretti Chromosomal abnormalities in embryos Mol. Cell. Endocrinol 183 Suppl. 1 2001 S29 S34
74. M.C. Magli, L. Gianaroli, A.P. Ferraretti, M. Lappi, A. Ruberti, and V. Farfalli Embryo morphology and development are dependent on the chromosomal complement Fertil. Steril 87 2007 534 541
75. L.M. Mains, L. Christenson, Yang B., A.E. Sparks, S. Mathur, and B.J. Van Voorhis Identification of apolipoprotein A1 in the human embryonic secretome Fertil. Steril 96 2011 422 427 e2
76. R. Marchal-Bras-Goncalves, N. Rouas-Freiss, F. Connan, J. Choppin, J. Dausset, E.D. Carosella, M. Kirszenbaum, and J. Guillet A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity Transplant. Proc 33 2001 2355 2359
77. G.A. Maston, S.K. Evans, and M.R. Green Transcriptional regulatory elements in the human genome Annu. Rev. Genomics Hum. Genet 7 2006 29 59
78. Y. Menezo, K. Elder, and S. Viville Soluble HLA-G release by the human embryo: an interesting artefact? Reprod. Biomed. Online 13 2006 763 764
79. M. Meseguer, J. Herrero, A. Tejera, K.M. Hilligsoe, N.B. Ramsing, and J. Remohi The use of morphokinetics as a predictor of embryo implantation Hum. Reprod 26 2011 2658 2671
80. M. Montag, J. Liebenthron, and M. Koster Which morphological scoring system is relevant in human embryo development? Placenta 32 Suppl. 3 2011 S252 S256
81. S. Munne, Chen S., P. Colls, J. Garrisi, Zheng X., N. Cekleniak, M. Lenzi, P. Hughes, J. Fischer, M. Garrisi, G. Tomkin, and J. Cohen Maternal age, morphology, development and chromosome abnormalities in over 6000 cleavage-stage embryos Reprod. Biomed. Online 14 2007 628 634
82. M. Munoz, M. Cruz, P. Humaidan, N. Garrido, I. Perez-Cano, and M. Meseguer The type of GnRH analogue used during controlled ovarian stimulation influences early embryo developmental kinetics: a time-lapse study Eur. J. Obstet. Gynecol. Reprod. Biol 168 2013 167 172
83. C. Nezhat, M. Lewis, S. Kotikela, A. Veeraswamy, L. Saadat, and B. Hajhosseini Robotic versus standard laparoscopy for the treatment of endometriosis Fertil. Steril 94 2010 2758 2760
84. I. Noci, B. Fuzzi, R. Rizzo, L. Melchiorri, L. Criscuoli, S. Dabizzi, R. Biagiotti, S. Pellegrini, A. Menicucci, and O.R. Baricordi Embryonic soluble HLA-G as a marker of developmental potential in embryos Hum. Reprod 20 2005 138 146
85. J.C. Parks, B.R. McCallie, A.M. Janesch, W.B. Schoolcraft, and M.G. Katz-Jaffe Blastocyst gene expression correlates with implantation potential Fertil. Steril 95 2011 1367 1372
86. G. Paternot, S. Debrock, T. D'Hooghe, and C. Spiessens Computer-assisted embryo selection: a benefit in the evaluation of embryo quality? Reprod. Biomed. Online 23 2011 347 354
87. G. Paternot, A.M. Wetzels, F. Thonon, A. Vansteenbrugge, D. Willemen, J. Devroe, S. Debrock, T.M. D'Hooghe, and C. Spiessens Intra- and interobserver analysis in the morphological assessment of early stage embryos during an IVF procedure: a multicentre study Reprod. Biol. Endocrinol 9 2011 127
88. C. Racowsky, L. Ohno-Machado, J. Kim, and J.D. Biggers Is there an advantage in scoring early embryos on more than one day? Hum. Reprod 24 2009 2104 2113
89. C. Racowsky, J.E. Stern, W.E. Gibbons, B. Behr, K.O. Pomeroy, and J.D. Biggers National collection of embryo morphology data into Society for Assisted Reproductive Technology Clinic Outcomes Reporting System: associations among day 3 cell number, fragmentation and blastomere asymmetry, and live birth rate Fertil. Steril 95 2011 1985 1989
90. A. Radonic, S. Thulke, I.M. Mackay, O. Landt, W. Siegert, and A. Nitsche Guideline to reference gene selection for quantitative real-time PCR Biochem. Biophys. Res. Commun 313 2004 856 862
91. S. Rajagopalan, and Long E.O. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells J. Exp. Med 189 1999 1093 1100
92. A. Rhenman, L. Berglund, T. Brodin, M. Olovsson, K. Milton, N. Hadziosmanovic, and J. Holte Which set of embryo variables is most predictive for live birth? A prospective study in 6252 single embryo transfers to construct an embryo score for the ranking and selection of embryos Hum. Reprod 30 2015 28 36
93. K.S. Richter, D.C. Harris, S.T. Daneshmand, and B.S. Shapiro Quantitative grading of a human blastocyst: optimal inner cell mass size and shape Fertil. Steril 76 2001 1157 1167
94. W.E. Roudebush, J.D. Wininger, A.E. Jones, G. Wright, A.A. Toledo, H.I. Kort, J.B. Massey, and D.B. Shapiro Embryonic platelet-activating factor: an indicator of embryo viability Hum. Reprod 17 2002 1306 1310
95. I. Rubio, A. Galan, Z. Larreategui, F. Ayerdi, J. Bellver, J. Herrero, and M. Meseguer Clinical validation of embryo culture and selection by morphokinetic analysis: a randomized, controlled trial of the EmbryoScope Fertil. Steril 102 2014 1287 1294 e5
96. R. Ruiz De Assin, A. Clavero, M.C. Gonzalvo, J.P. Ramirez, S. Zamora, A. Fernandez, L. Martinez, and J.A. Castilla Comparison of methods to determine the assigned value in an external quality control programme for embryo evaluation Reprod. Biomed. Online 19 2009 824 829
97. R. Ruiz De Assin, A. Clavero, M.C. Gonzalvo, A. Rosales, S. Zamora, L. Martinez, J. Mozas, and J.A. Castilla Reducing inter-observer variability in embryo evaluation by means of training courses J. Assist. Reprod. Genet 28 2011 1129 1133
98. N. Sageshima, T. Shobu, K. Awai, H. Hashimoto, M. Yamashita, N. Takeda, Y. Odawara, M. Nakanishi, K. Hatake, and A. Ishitani Soluble HLA-G is absent from human embryo cultures: a reassessment of sHLA-G detection methods J. Reprod. Immunol 75 2007 11 22
99. D. Sakkas Embryo selection using metabolomics Methods Mol. Biol 1154 2014 533 540
100. D. Sakkas, and D. Gardner Evaluation of embryo quality: new strategies to facilitate single embryo transfer D.K. Gardner, A. Weissman, C.H. Howles, Z. Shohan, Textbook of Assisted Reproductive Technologies 2008 Informa Healthcare London 241 252
101. E. Sapey, D. Bayley, A. Ahmad, P. Newbold, N. Snell, and R.A. Stockley Inter-relationships between inflammatory markers in patients with stable COPD with bronchitis: intra-patient and inter-patient variability Thorax 63 2008 493 499
102. R. Scott, E. Seli, K. Miller, D. Sakkas, K. Scott, and D.H. Burns Noninvasive metabolomic profiling of human embryo culture media using Raman spectroscopy predicts embryonic reproductive potential: a prospective blinded pilot study Fertil. Steril 90 2008 77 83
103. E. Seli, D. Sakkas, R. Scott, S.C. Kwok, S.M. Rosendahl, and D.H. Burns 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 88 2007 1350 1357
104. B.S. Shapiro, S.T. Daneshmand, F.C. Garner, M. Aguirre, and R. Ross 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 89 2008 20 26
105. B.S. Shapiro, S.T. Daneshmand, F.C. Garner, M. Aguirre, and S. Thomas Large blastocyst diameter, early blastulation, and low preovulatory serum progesterone are dominant predictors of clinical pregnancy in fresh autologous cycles Fertil. Steril 90 2008 302 309
106. G. Sher, L. Keskintepe, J.D. Fisch, B.A. Acacio, P. Ahlering, J. Batzofin, and M. Ginsburg Soluble human leukocyte antigen G expression in phase I culture media at 46 h after fertilization predicts pregnancy and implantation from day 3 embryo transfer Fertil. Steril 83 2005 1410 1413
107. V. Shulaev Metabolomics technology and bioinformatics Brief. Bioinform 7 2006 128 139
108. R.G. Sturmey, D.R. Brison, and H.J. Leese Symposium: innovative techniques in human embryo viability assessment. Assessing embryo viability by measurement of amino acid turnover Reprod. Biomed. Online 17 2008 486 496
109. C. Stylianou, D. Critchlow, D.R. Brison, and S.A. Roberts Embryo morphology as a predictor of IVF success: an evaluation of the proposed UK ACE grading scheme for cleavage stage embryos Hum. Fertil. (Camb.) 15 2012 11 17
110. L. Sundvall, H.J. Ingerslev, U. Breth Knudsen, and K. Kirkegaard Inter- and intra-observer variability of time-lapse annotations Hum. Reprod 28 2013 3215 3221
111. J. Tabiasco, S. Perrier D'Hauterive, F. Thonon, J. Parinaud, R. Leandri, J.M. Foidart, G. Chaouat, C. Munaut, R. Lombroso, J. Selva, M. Bergere, I. Hammoud, N. Kozma, M. Aguerre-Girr, A.K. Swales, I.L. Sargent, P. Le Bouteiller, and N. Ledee Soluble HLA-G in IVF/ICSI embryo culture supernatants does not always predict implantation success: a multicentre study Reprod. Biomed. Online 18 2009 374 381
112. J. Van Blerkom Translocation of the subplasmalemmal cytoplasm in human blastomeres: possible effects on the distribution and inheritance of regulatory domains Reprod. Biomed. Online 14 2007 191 200
113. E. Van Den Abbeel, B. Balaban, S. Ziebe, K. Lundin, M.J. Cuesta, B.M. Klein, L. Helmgaard, and J.C. Arce Association between blastocyst morphology and outcome of single-blastocyst transfer Reprod. Biomed. Online 27 2013 353 361
114. M. Van Den Bergh, F. Devreker, S. Emiliani, and Y. Englert Glycolytic activity: a possible tool for human blastocyst selection Reprod BioMedicine Online 3 2001 8
115. L. Van Loendersloot, M. Van Wely, F. Van Der Veen, P. Bossuyt, and S. Repping Selection of embryos for transfer in IVF: ranking embryos based on their implantation potential using morphological scoring Reprod. Biomed. Online 29 2014 222 230
116. A.P. Van Montfoort, J.P. Geraedts, J.C. Dumoulin, A.P. Stassen, J.L. Evers, and T.A. Ayoubi Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis Mol. Hum. Reprod 14 2008 157 168
117. E. Van Royen, K. Mangelschots, D. De Neubourg, I. Laureys, G. Ryckaert, and J. Gerris Calculating the implantation potential of day 3 embryos in women younger than 38 years of age: a new model Hum. Reprod 16 2001 326 332
118. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol 3 2002 RESEARCH0034
119. C.G. Vergouw, L.L. Botros, P. Roos, J.W. Lens, R. Schats, P.G. Hompes, D.H. Burns, and C.B. Lambalk Metabolomic profiling by near-infrared spectroscopy as a tool to assess embryo viability: a novel, non-invasive method for embryo selection Hum. Reprod 23 2008 1499 1504
120. C.G. Vergouw, D.C. Kieslinger, E.H. Kostelijk, L.L. Botros, R. Schats, P.G. Hompes, D. Sakkas, and C.B. Lambalk 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 27 2012 2304 2311
121. C.G. Vergouw, M.W. Heymans, T. Hardarson, I.A. Sfontouris, K.A. Economou, A. Ahlstrom, L. Rogberg, T.G. Lainas, D. Sakkas, D.C. Kieslinger, E.H. Kostelijk, P.G. Hompes, R. Schats, and C.B. Lambalk No evidence that embryo selection by near-infrared spectroscopy in addition to morphology is able to improve live birth rates: results from an individual patient data meta-analysis Hum. Reprod 29 2014 455 461
122. M.D. Vermilyea, Tan L., J.T. Anthony, J. Conaghan, K. Ivani, M. Gvakharia, R. Boostanfar, V.L. Baker, V. Suraj, Chen A.A., M. Mainigi, C. Coutifaris, and Shen S. Computer-automated time-lapse analysis results correlate with embryo implantation and clinical pregnancy: a blinded, multi-centre study Reprod. Biomed. Online 29 2014 729 736
123. M. Vernon, J.E. Stern, G.D. Ball, D. Wininger, J. Mayer, and C. Racowsky Utility of the national embryo morphology data collection by the Society for Assisted Reproductive Technologies (SART): correlation between day-3 morphology grade and live-birth outcome Fertil. Steril 95 2011 2761 2763
124. S. Wathlet, T. Adriaenssens, I. Segers, G. Verheyen, H. Van de Velde, W. Coucke, R. Ron El, P. Devroey, and J. Smitz Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients Hum. Reprod 26 2011 1035 1051
125. D. Wells, M.G. Bermudez, N. Steuerwald, A.R. Thornhill, D.L. Walker, H. Malter, J.D. Delhanty, and J. Cohen Expression of genes regulating chromosome segregation, the cell cycle and apoptosis during human preimplantation development Hum. Reprod 20 2005 1339 1348
126. M.L. Wissing, M.R. Bjerge, A.I. Olesen, T. Hoest, and A.L. Mikkelsen Impact of PCOS on early embryo cleavage kinetics Reprod. Biomed. Online 28 2014 508 514
127. C. Wong, Chen A.A., B. Behr, and Shen S. Time-lapse microscopy and image analysis in basic and clinical embryo development research Reprod. Biomed. Online 26 2013 120 129
128. Yang Z., Zhang J., S.A. Salem, Liu X., Kuang Y., R.D. Salem, and Liu J. Selection of competent blastocysts for transfer by combining time-lapse monitoring and array CGH testing for patients undergoing preimplantation genetic screening: a prospective study with sibling oocytes BMC Med. Genomics 7 2014 38
129. Zhang X., N. Jafari, R.B. Barnes, E. Confino, M. Milad, and R.R. Kazer Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality Fertil. Steril 83 Suppl. 1 2005 1169 1179
130. S. Ziebe, K. Lundin, A. Loft, C. Bergh, A. Nyboe Andersen, U. Selleskog, D. Nielsen, C. Grondahl, H. Kim, and J.C. Arce FISH analysis for chromosomes 13, 16, 18, 21, 22, X and Y in all blastomeres of IVF pre-embryos from 144 randomly selected donated human oocytes and impact on pre-embryo morphology Hum. Reprod 18 2003 2575 2581