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Real-time image and time-lapse technology to select the single blastocyst to transfer in assisted reproductive cycles

Published online by Cambridge University Press:  11 April 2023

Romualdo Sciorio Open the ORCID record for Romualdo Sciorio [Opens in a new window] ,
Gerard Campos ,
Simone Palini ,
Domenico Baldini  and
Ronny Janssens
Romualdo Sciorio*
Affiliation:
Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, 51 Little France Crescent, Old Dalkeith Road, Edinburgh, Scotland, EH16 4SA, UK
Gerard Campos
Affiliation:
Girexx Fertility Clinics, 17004, Girona, Spain
Simone Palini
Affiliation:
Physiopathology of Reproduction Unit, Cervesi Hospital, Via Ludwig Van Beethoven 1, Cattolica, Italy
Domenico Baldini
Affiliation:
IVF Center MomòFertilife Clinic, Bisceglie, Italy
Ronny Janssens
Affiliation:
BE-ART IVF, Kloosterstraat 76, 2880 Bornem, Belgium
*
Author for correspondence: Romualdo Sciorio. Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, 51 Little France Crescent, Old Dalkeith Road, Edinburgh, Scotland, EH16 4SA, UK. E-mail: sciorioromualdo@hotmail.com
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Abstract

The success of an assisted reproduction cycle should be the achievement of a healthy singleton live birth following the replacement of one embryo. Therefore, one of the most critical points for embryologists has been the selection criteria and how to choose the best embryo to transfer with high implantation potential. In this vein, morphological evaluation has been historically the method applied. However, this practice relies on a limited number of single observations and is associated with high operator variability. Recently, a major innovation in embryo culture has been the introduction of a new type of incubator with integrated time-lapse monitoring, which enables the embryologist to analyze the dynamic events of embryo development, from fertilization to blastocyst formation. This novel practice is quickly growing and has been implemented in many IVF clinics worldwide. Therefore, the main aim of this review is to illustrate the benefits of time-lapse technology in a modern embryology laboratory. In particular, we discuss the blastocyst collapse(s) event and morphometric blastocyst assessment and analyse their association with embryo viability and implantation potential.

Keywords

Blastocyst collapseEmbryo cultureMorphometric blastocyst assessmentPregnancy outcomeSingle-blastocyst transferTime-lapse technology
Type
Review Article
Information
Zygote , Volume 31 , Issue 3 , June 2023 , pp. 207 - 216
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Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Aguilar, J., Motato, Y., Escribá, M. J., Ojeda, M., Muñoz, E. and Meseguer, M. (2014). The human first cell cycle: Impact on implantation. Reproductive Biomedicine Online, 28(4), 475–484. doi: 10.1016/j.rbmo.2013.11.014 CrossRefGoogle ScholarPubMed
Ahlström, A., Westin, C., Reismer, E., Wikland, M. and Hardarson, T. (2011). Trophectoderm morphology: An important parameter for predicting live birth after single blastocyst transfer. Human Reproduction, 26(12), 3289–3296. doi: 10.1093/humrep/der325 CrossRefGoogle ScholarPubMed
Alegre, L., Del Gallego, R., Bori, L., Loewke, K., Maddah, M., Aparicio-Ruiz, B., Palma-Govea, A. P., Marcos, J. and Meseguer, M. (2021). Assessment of embryo implantation potential with a cloud-based automatic software. Reproductive Biomedicine Online, 42(1), 66–74. doi: 10.1016/j.rbmo.2020.09.032 CrossRefGoogle ScholarPubMed
Almagor, M., Harir, Y., Fieldust, S., Or, Y. and Shoham, Z. (2016). Ratio between inner cell mass diameter and blastocyst diameter is correlated with successful pregnancy outcomes of single blastocyst transfers. Fertility and Sterility, 106(6), 1386–1391. doi: 10.1016/j.fertnstert.2016.08.009 CrossRefGoogle ScholarPubMed
Aparicio-Ruiz, B., Basile, N., Pérez Albalá, S., Bronet, F., Remohí, J. and Meseguer, M. (2016). Automatic time-lapse instrument is superior to single-point morphology observation for selecting viable embryos: Retrospective study in oocyte donation. Fertility and Sterility, 106(6), 1379–1385.e10. doi: 10.1016/j.fertnstert.2016.07.1117 CrossRefGoogle ScholarPubMed
Apter, S., Ebner, T., Freour, T., Guns, Y., Kovacic, B., Le Clef, N., Marques, M., Meseguer, M., Montjean, D., Sfontouris, I., Sturmey, R. and Coticchio, G. (2020, March 19). Good practice recommendations for the use of time-lapse technology. Human Reproduction Open, 2020(2), hoaa008. doi: 10.1093/hropen/hoaa008 CrossRefGoogle ScholarPubMed
Arce, J. C., Ziebe, S., Lundin, K., Janssens, R., Helmgaard, L. and Sørensen, P. (2006). Interobserver agreement and intraobserver reproducibility of embryo quality assessments. Human Reproduction, 21(8), 2141–2148. doi: 10.1093/humrep/del106 CrossRefGoogle ScholarPubMed
Armstrong, S., Bhide, P., Jordan, V., Pacey, A., Marjoribanks, J. and Farquhar, C. (2019). Time-lapse systems for embryo incubation and assessment in assisted reproduction. Cochrane Database of Systematic Reviews, 5(5), CD011320. doi: 10.1002/14651858.CD011320.pub4 Google ScholarPubMed
Athayde Wirka, K., Chen, A. A., Conaghan, J., Ivani, K., Gvakharia, M., Behr, B., Suraj, V., Tan, L. and Shen, S. (2014). Atypical embryo phenotypes identified by time-lapse microscopy: High prevalence and association with embryo development. Fertility and Sterility, 101(6), 1637–48.e1. doi: 10.1016/j.fertnstert.2014.02.050 CrossRefGoogle ScholarPubMed
Baltz, J. M., Smith, S. S., Biggers, J. D. and Lechene, C. (1997). Intracellular ion concentrations and their maintenance by Na+/K+-ATPase in preimplantation mouse embryos. Zygote, 5(1), 1–9.CrossRefGoogle ScholarPubMed
Barrie, A., Homburg, R., McDowell, G., Brown, J., Kingsland, C. and Troup, S. (2017). Embryos cultured in a time-lapse system result in superior treatment outcomes: A strict matched pair analysis. Human Fertility, 20(3), 179–185. doi: 10.1080/14647273.2016.1258735.CrossRefGoogle Scholar
Basile, N., Nogales, M. C., Bronet, F., Florensa, M., Riqueiros, M., Rodrigo, L., García-Velasco, J. and Meseguer, M. (2014). Increasing the probability of selecting chromosomally normal embryos by time-lapse morphokinetics analysis. Fertility and Sterility, 101(3), 699–704. doi: 10.1016/j.fertnstert.2013.12.005 CrossRefGoogle ScholarPubMed
Basile, N., Vime, P., Florensa, M., Aparicio-Ruiz, B., Garcia-Velasco, J. A., Remohi, J. and Meseguer, M. (2015). The use of morphokinetics as a predictor of implantation: A multicentric study to define and validate an algorithm for embryo selection. Human Reproduction (Oxford, England), 30(2), 276–283.CrossRefGoogle ScholarPubMed
Biggers, J. D. (1998). Reflections on the culture of the preimplantation embryo. International Journal of Developmental Biology, 42(7), 879–884.Google ScholarPubMed
Bontekoe, S., Mantikou, E., van Wely, M., Seshadri, S., Repping, S. and Mastenbroek, S. (2012). Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database of Systematic Reviews, 7(7), CD008950. doi: 10.1002/14651858.CD008950.pub2 Google Scholar
Bori, L., Paya, E., Alegre, L., Viloria, T. A., Remohi, J. A., Naranjo, V. and Meseguer, M. (2020). Novel and conventional embryo parameters as input data for artificial neural networks: An artificial intelligence model applied for prediction of the implantation potential. Fertility and Sterility, 114(6), 1232–1241. doi: 10.1016/j.fertnstert.2020.08.023 CrossRefGoogle ScholarPubMed
Bormann, C. L., Kanakasabapathy, M. K., Thirumalaraju, P., Gupta, R., Pooniwala, R., Kandula, H., Hariton, E., Souter, I., Dimitriadis, I., Ramirez, L. B., Curchoe, C. L., Swain, J., Boehnlein, L. M. and Shafiee, H. (2020). Performance of a deep learning based neural network in the selection of human blastocysts for implantation. eLife, 9, e55301. doi: 10.7554/eLife.55301 CrossRefGoogle ScholarPubMed
Boueilh, T., Reignier, A., Barriere, P. and Freour, T. (2018). Time-lapse imaging systems in IVF laboratories: A French national survey. Journal of Assisted Reproduction and Genetics, 35(12), 2181–2186. doi: 10.1007/s10815-018-1302-6 CrossRefGoogle ScholarPubMed
Braude, P. (2013). Selecting the “best” embryos: Prospects for improvement. Reproductive Biomedicine Online, 27(6), 644–653. doi: 10.1016/j.rbmo.2013.08.009 CrossRefGoogle ScholarPubMed
Braude, P., Bolton, V. and Moore, S. (1988). Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature, 332(6163), 459–461. doi: 10.1038/332459a0 CrossRefGoogle ScholarPubMed
Campbell, A., Fishel, S., Bowman, N., Duffy, S., Sedler, M. and Thornton, S. (2013). Retrospective analysis of outcomes after IVF using an aneuploidy risk model derived from time-lapse imaging without PGS. Reproductive Biomedicine Online, 27(2), 140–146. doi: 10.1016/j.rbmo.2013.04.013 CrossRefGoogle ScholarPubMed
Chavez-Badiola, A., Flores-Saiffe-Farías, A., Mendizabal-Ruiz, G., Drakeley, A. J. and Cohen, J. (2020). Embryo Ranking Intelligent Classification Algorithm (ERICA): Artificial intelligence clinical assistant predicting embryo ploidy and implantation. Reproductive Biomedicine Online, 41(4), 585–593. doi: 10.1016/j.rbmo.2020.07.003 CrossRefGoogle ScholarPubMed
Chawla, M., Fakih, M., Shunnar, A., Bayram, A., Hellani, A., Perumal, V., Divakaran, J. and Budak, E. (2015). Morphokinetic analysis of cleavage stage embryos and its relationship to aneuploidy in a retrospective time-lapse imaging study. Journal of Assisted Reproduction and Genetics, 32(1), 69–75. doi: 10.1007/s10815-014-0372-3 CrossRefGoogle Scholar
Chen, A. A., Tan, L., Suraj, V., Reijo Pera, R. R. and Shen, S. (2013). Biomarkers identified with time-lapse imaging: Discovery, validation, and practical application. Fertility and Sterility, 99(4), 1035–1043. doi: 10.1016/j.fertnstert.2013.01.143 CrossRefGoogle ScholarPubMed
Chimote, N. M., Chimote, N. N., Nath, N. M. and Mehta, B. N. (2013, July 6). Transfer of spontaneously hatching or hatched blastocyst yields better pregnancy rates than expanded blastocyst transfer. Journal of Human Reproductive Sciences, 6(3), 183–188. doi: 10.4103/0974-1208.121420 CrossRefGoogle ScholarPubMed
Conaghan, J., Chen, A. A., Willman, S. P., Ivani, K., Chenette, P. E., Boostanfar, R., Baker, V. L., Adamson, G. D., Abusief, M. E., Gvakharia, M., Loewke, K. E. and Shen, S. (2013). Improving embryo selection using a computer-automated time-lapse image analysis test plus day 3 morphology: Results from a prospective multicenter trial. Fertility and Sterility, 100(2), 412–9.e5. doi: 10.1016/j.fertnstert.2013.04.021 CrossRefGoogle ScholarPubMed
Coticchio, G., Lagalla, C., Sturmey, R., Pennetta, F. and Borini, A. (2019). The enigmatic morula: Mechanisms of development, cell fate determination, self-correction and implications for ART. Human Reproduction Update, 25(4), 422–438. doi: 10.1093/humupd/dmz008 CrossRefGoogle ScholarPubMed
Coticchio, G., Mignini Renzini, M., Novara, P. V., Lain, M., De Ponti, E., Turchi, D., Fadini, R. and Dal Canto, M. (2018). Focused time-lapse analysis reveals novel aspects of human fertilization and suggests new parameters of embryo viability. Human Reproduction, 33(1), 23–31. doi: 10.1093/humrep/dex344 CrossRefGoogle ScholarPubMed
Coticchio, G., Ezoe, K., Lagalla, C., Shimazaki, K., Ohata, K., Ninomiya, M., Wakabayashi, N., Okimura, T., Uchiyama, K., Kato, K. and Borini, A. (2021, March 18). Perturbations of morphogenesis at the compaction stage affect blastocyst implantation and live birth rates. Human Reproduction, 36(4), 918–928. doi: 10.1093/humrep/deab011 CrossRefGoogle ScholarPubMed
Cruz, M., Garrido, N., Herrero, J., Pérez-Cano, I., Muñoz, M. and Meseguer, M. (2012). Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reproductive Biomedicine Online, 25(4), 371–381. doi: 10.1016/j.rbmo.2012.06.017 CrossRefGoogle ScholarPubMed
Dal Canto, M., Coticchio, G., Mignini Renzini, M., De Ponti, E., Novara, P. V., Brambillasca, F., Comi, R. and Fadini, R. (2012). Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation. Reproductive Biomedicine Online, 25(5), 474–480. doi: 10.1016/j.rbmo.2012.07.016 CrossRefGoogle ScholarPubMed
Dal Canto, M., Bartolacci, A., Turchi, D., Pignataro, D., Lain, M., De Ponti, E., Brigante, C., Mignini Renzini, M. and Buratini, J. (2021). Faster fertilization and cleavage kinetics reflect competence to achieve a live birth after intracytoplasmic sperm injection, but this association fades with maternal age. Fertility and Sterility, 115(3), 665–672. doi: 10.1016/j.fertnstert.2020.06.023.CrossRefGoogle ScholarPubMed
Danuser, G. (2011). Computer vision in cell biology. Cell, 147(5), 973–978. doi: 10.1016/j.cell.2011.11.001 CrossRefGoogle ScholarPubMed
De Vos, A., Van Landuyt, L., Santos-Ribeiro, S., Camus, M., Van de Velde, H., Tournaye, H. and Verheyen, G. (2016). Cumulative live birth rates after fresh and vitrified cleavage-stage versus blastocyst-stage embryo transfer in the first treatment cycle. Human Reproduction, 31(11), 2442–2449. doi: 10.1093/humrep/dew219 CrossRefGoogle ScholarPubMed
Della Ragione, T., Verheyen, G., Papanikolaou, E. G., Van Landuyt, L., Devroey, P. and Van Steirteghem, A. (2007). 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. Reproductive Biology and Endocrinology: RB&E, 5, 2. doi: 10.1186/1477-7827-5-2 CrossRefGoogle ScholarPubMed
Desai, N., Ploskonka, S., Goodman, L. R., Austin, C., Goldberg, J. and Falcone, T. (2014). Analysis of embryo morphokinetics, multinucleation and cleavage anomalies using continuous time-lapse monitoring in blastocyst transfer cycles. Reproductive Biology and Endocrinology: RB&E, 12, 54. doi: 10.1186/1477-7827-12-54 CrossRefGoogle ScholarPubMed
Dolinko, A. V., Farland, L. V., Kaser, D. J., Missmer, S. A. and Racowsky, C. (2017). National survey on use of time-lapse imaging systems in IVF laboratories. Journal of Assisted Reproduction and Genetics, 34(9), 1167–1172. doi: 10.1007/s10815-017-0964-9 CrossRefGoogle ScholarPubMed
ESHRE Guideline Group on Good Practice in IVF Labs, De los Santos, M. J., Apter, S., Coticchio, G., Debrock, S., Lundin, K., Plancha, C. E., Prados, F., Rienzi, L., Verheyen, G., Woodward, B. and Vermeulen, N. (2015). Revised guidelines for good practice in IVF laboratories (2015). Human Reproduction (Oxford, England), 31(4), 685–686. doi: 10.1093/humrep/dew016 Google Scholar
European IVF-Monitoring Consortium (EIM), European Society of Human Reproduction and Embryology (ESHRE), Kupka, M. S., D’Hooghe, T., Ferraretti, A. P., de Mouzon, J., Erb, K., Castilla, J. A., Calhaz-Jorge, C., De Geyter, C.h and Goossens, V. (2016). Assisted reproductive technology in Europe, 2011: results generated from European registers by ESHRE. Human Reproduction (Oxford, England), 31(2), 233–248. doi: 10.1093/humrep/dev319 Google ScholarPubMed
Ezoe, K., Ohata, K., Morita, H., Ueno, S., Miki, T., Okimura, T., Uchiyama, K., Yabuuchi, A., Kobayashi, T., Montag, M. and Kato, K. (2019). Prolonged blastomere movement induced by the delay of pronuclear fading and first cell division adversely affects pregnancy outcomes after fresh embryo transfer on day 2: A time-lapse study. Reproductive Biomedicine Online, 38(5), 659–668. doi: 10.1016/j.rbmo.2018.12.014 CrossRefGoogle ScholarPubMed
Fadon, P., Gallegos, E., Jalota, S., Muriel, L. and Diaz-Garcia, C. (2021). Time-lapse systems: A comprehensive analysis on effectiveness. Seminars in Reproductive Medicine, 39(5–6), e12–e18. doi: 10.1055/s-0041-1742149 Google ScholarPubMed
Fischer, B. and Bavister, B. D. (1993). Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. Journal of Reproduction and Fertility, 99(2), 673–679. doi: 10.1530/jrf.0.0990673 CrossRefGoogle ScholarPubMed
Freeman, M. R., Hinds, M. S., Howard, K. G., Howard, J. M. and Hill, G. A. (2019). Guidance for elective single-embryo transfer should be applied to frozen embryo transfer cycles. Journal of Assisted Reproduction and Genetics, 36(5), 939–946. doi: 10.1007/s10815-019-01433-w CrossRefGoogle ScholarPubMed
Fréour, T., Dessolle, L., Lammers, J., Lattes, S. and Barrière, P. (2013). Comparison of embryo morphokinetics after in vitro fertilization-intracytoplasmic sperm injection in smoking and nonsmoking women. Fertility and Sterility, 99(7), 1944–1950. doi: 10.1016/j.fertnstert.2013.01.136 CrossRefGoogle ScholarPubMed
Gardner, D. K., Kuramoto, T., Tanaka, M., Mitzumoto, S., Montag, M. and Yoshida, A. (2020). Prospective randomized multicentre comparison on sibling oocytes comparing G-Series media system with antioxidants versus standard G-Series media system. Reproductive Biomedicine Online, 40(5), 637–644. doi: 10.1016/j.rbmo.2020.01.026 CrossRefGoogle ScholarPubMed
Gardner, D. K., Lane, M., Stevens, J., Schlenker, T. and Schoolcraft, W. B. (2000). Blastocyst score affects implantation and pregnancy outcome: Towards a single blastocyst transfer. Fertility and Sterility, 73(6), 1155–1158. doi: 10.1016/s0015-0282(00)00518-5 CrossRefGoogle ScholarPubMed
Gardner, D. K. and Schoolcraft, W. B. (1999). Culture and transfer of human blastocysts. Current Opinion in Obstetrics and Gynecology, 11(3), 307–311 doi: 10.1097/00001703-199906000-00013 CrossRefGoogle ScholarPubMed
Glujovsky, D., Farquhar, C., Quinteiro Retamar, A. M., Alvarez Sedo, C. R. and Blake, D. (2016, June 30). Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database of Systematic Reviews, 6(6), CD002118. doi: 10.1002/14651858.CD002118.pub5 Google Scholar
Gonzales, D. S., Jones, J. M., Pinyopummintr, T., Carnevale, E. M., Ginther, O. J., Shapiro, S. S. and Bavister, B. D. (1996). Trophectoderm projections: A potential means for locomotion, attachment and implantation of bovine, equine and human blastocysts. Human Reproduction, 11(12), 2739–2745. doi: 10.1093/oxfordjournals.humrep.a019201 CrossRefGoogle ScholarPubMed
Hashimoto, S., Kato, N., Saeki, K. and Morimoto, Y. (2012). Selection of high-potential embryos by culture in poly(dimethylsiloxane) microwells and time-lapse imaging. Fertility and Sterility, 97(2), 332–337. doi: 10.1016/j.fertnstert.2011.11.042 CrossRefGoogle ScholarPubMed
Hashimoto, S., Nakano, T., Yamagata, K., Inoue, M., Morimoto, Y. and Nakaoka, Y. (2016). Multinucleation per se is not always sufficient as a marker of abnormality to decide against transferring human embryos. Fertility and Sterility, 106(1), 133–139.e6. doi: 10.1016/j.fertnstert.2016.03.025 CrossRefGoogle Scholar
Hill, M. J., Richter, K. S., Heitmann, R. J., Graham, J. R., Tucker, M. J., DeCherney, A. H., Browne, P. E. and Levens, E. D. (2013). Trophectoderm grade predicts outcomes of single-blastocyst transfers. Fertility and Sterility, 99(5), 1283–1289.e1. doi: 10.1016/j.fertnstert.2012.12.003 CrossRefGoogle ScholarPubMed
Hlinka, D., Kaľatová, B., Uhrinová, I., Dolinská, S., Rutarová, J., Rezáčová, J., Lazarovská, S. and Dudáš, M. (2012). Time-lapse cleavage rating predicts human embryo viability. Physiological Research, 61(5), 513–525. doi: 10.33549/physiolres.932287 CrossRefGoogle ScholarPubMed
Huang, T. T. F., Chinn, K., Kosasa, T., Ahn, H. J. and Kessel, B. (2016). Morphokinetics of human blastocyst expansion in vitro . Reproductive Biomedicine Online, 33(6), 659–667. doi: 10.1016/j.rbmo.2016.08.020 CrossRefGoogle ScholarPubMed
Iwata, K., Yumoto, K., Sugishima, M., Mizoguchi, C., Kai, Y., Iba, Y. and Mio, Y. (2014). Analysis of compaction initiation in human embryos by using time-lapse cinematography. Journal of Assisted Reproduction and Genetics, 31(4), 421–426. doi: 10.1007/s10815-014-0195-2 CrossRefGoogle ScholarPubMed
Khosravi, P., Kazemi, E., Zhan, Q., Malmsten, J. E., Toschi, M., Zisimopoulos, P., Sigaras, A., Lavery, S., Cooper, L. A. D., Hickman, C., Meseguer, M., Rosenwaks, Z., Elemento, O., Zaninovic, N. and Hajirasouliha, I. (2019). Deep learning enables robust assessment and selection of human blastocysts after in vitro fertilization. npj Digital Medicine, 2, 21. doi: 10.1038/s41746-019-0096-y CrossRefGoogle ScholarPubMed
Kij, B., Kochan, J., Fryc, K., Niżański, W., Prochowska, S., Gabryś, J., Nowak, A. and Bugno-Poniewierska, M. (2020). The frequency of collapse as a predictor of feline blastocyst quality. Theriogenology, 157, 372–377. doi: 10.1016/j.theriogenology.2020.08.008 CrossRefGoogle ScholarPubMed
Kirkegaard, K., Agerholm, I. E. and Ingerslev, H. J. (2012). Time-lapse monitoring as a tool for clinical embryo assessment. Human Reproduction, 27(5), 1277–1285. doi: 10.1093/humrep/des079 CrossRefGoogle ScholarPubMed
Kirkegaard, K., Kesmodel, U. S., Hindkjær, J. J. and Ingerslev, H. J. (2013). Time-lapse parameters as predictors of blastocyst development and pregnancy outcome in embryos from good prognosis patients: A prospective cohort study. Human Reproduction, 28(10), 2643–2651. doi: 10.1093/humrep/det300 CrossRefGoogle ScholarPubMed
Kovacs, P. and Lieman, H. J. (2019). Which embryo selection method should be offered to the patients? Journal of Assisted Reproduction and Genetics, 36(4), 603–605. doi: 10.1007/s10815-019-01443-8 CrossRefGoogle ScholarPubMed
Kresowik, J. D., Sparks, A. E. and Van Voorhis, B. J. (2012). Clinical factors associated with live birth after single embryo transfer. Fertility and Sterility, 98(5), 1152–1156. doi: 10.1016/j.fertnstert.2012.07.1141 CrossRefGoogle ScholarPubMed
Lewis, W. H. and Gregory, P. W. (1929). Cinematographs of living developing rabbit-eggs. Science, 69(1782), 226–229. doi: 10.1126/science.69.1782.226-a CrossRefGoogle ScholarPubMed
Liao, Q., Zhang, Q., Feng, X., Huang, H., Xu, H., Tian, B., Liu, J., Yu, Q., Guo, N., Liu, Q., Huang, B., Ma, D., Ai, J., Xu, S. and Li, K. (2021, March 26). Development of deep learning algorithms for predicting blastocyst formation and quality by time-lapse monitoring. Communications Biology, 4(1), 415. doi: 10.1038/s42003-021-01937-1 CrossRefGoogle ScholarPubMed
Liu, Y., Chapple, V., Feenan, K., Roberts, P. and Matson, P. (2015). Clinical significance of intercellular contact at the four-cell stage of human embryos, and the use of abnormal cleavage patterns to identify embryos with low implantation potential: A time-lapse study. Fertility and Sterility, 103(6), 1485–91.e1. doi: 10.1016/j.fertnstert.2015.03.017 CrossRefGoogle ScholarPubMed
Manna, C., Nanni, L., Lumini, A. and Pappalardo, S. (2013). Artificial intelligence techniques for embryo and oocyte classification. Reproductive Biomedicine Online, 26(1), 42–49. doi: 10.1016/j.rbmo.2012.09.015 CrossRefGoogle ScholarPubMed
Marcos, J., Pérez-Albalá, S., Mifsud, A., Molla, M., Landeras, J. and Meseguer, M. (2015). Collapse of blastocysts is strongly related to lower implantation success: A time-lapse study. Human Reproduction, 30(11), 2501–2508. doi: 10.1093/humrep/dev216 CrossRefGoogle ScholarPubMed
Meintjes, M., Chantilis, S. J., Douglas, J. D., Rodriguez, A. J., Guerami, A. R., Bookout, D. M., Barnett, B. D. and Madden, J. D. (2009). A controlled randomized trial evaluating the effect of lowered incubator oxygen tension on live births in a predominantly blastocyst transfer program. Human Reproduction, 24(2), 300–307. doi: 10.1093/humrep/den368 CrossRefGoogle Scholar
Meseguer, M., Herrero, J., Tejera, A., Hilligsøe, K. M., Ramsing, N. B. and Remohí, J. (2011). The use of morphokinetics as a predictor of embryo implantation. Human Reproduction, 26(10), 2658–2671. doi: 10.1093/humrep/der256 CrossRefGoogle ScholarPubMed
Meseguer, M., Rubio, I., Cruz, M., Basile, N., Marcos, J. and Requena, A. (2012). Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: A retrospective cohort study. Fertility and Sterility, 98(6), 1481–9.e10. doi: 10.1016/j.fertnstert.2012.08.016 CrossRefGoogle Scholar
Mio, Y. and Maeda, K. (2008). Time-lapse cinematography of dynamic changes occurring during in vitro development of human embryos. American Journal of Obstetrics and Gynecology, 199(6), 660.e1–660.e5. doi: 10.1016/j.ajog.2008.07.023 CrossRefGoogle ScholarPubMed
Mizobe, Y., Oya, N., Iwakiri, R., Yoshida, N., Sato, Y., Miyoshi, K., Tokunaga, M. and Ezono, Y. (2016). Effects of early cleavage patterns of human embryos on subsequent in vitro development and implantation. Fertility and Sterility, 106(2), 348–353.e2. doi: 10.1016/j.fertnstert.2016.04.020 CrossRefGoogle ScholarPubMed
Motato, Y., de Los Santos, M. J., Escriba, M. J., Ruiz, B. A., Remohí, J. and Meseguer, M. (2016). Morphokinetic analysis and embryonic prediction for blastocyst formation through an integrated time-lapse system. Fertility and Sterility, 105(2), 376–84.e9–384. doi: 10.1016/j.fertnstert.2015.11.001 CrossRefGoogle ScholarPubMed
Niederberger, C., Pellicer, A., Cohen, J., Gardner, D. K., Palermo, G. D., O’Neill, C. L., Chow, S., Rosenwaks, Z., Cobo, A., Swain, J. E., Schoolcraft, W. B., Frydman, R., Bishop, L. A., Aharon, D., Gordon, C., New, E., Decherney, A., Tan, S. L., Paulson, R. J., et al. (2018). Forty years of IVF. Fertility and Sterility, 110(2), 185–324.e5. doi: 10.1016/j.fertnstert.2018.06.005 CrossRefGoogle ScholarPubMed
Niimura, S. (2003). Time-lapse videomicrographic analyses of contractions in mouse blastocysts. Journal of Reproduction and Development, 49(6), 413–423. doi: 10.1262/jrd.49.413 CrossRefGoogle ScholarPubMed
Otsuki, J., Iwasaki, T., Tsuji, Y., Katada, Y., Sato, H., Tsutsumi, Y., Hatano, K., Furuhashi, K., Matsumoto, Y., Kokeguchi, S. and Shiotani, M. (2017). Potential of zygotes to produce live births can be identified by the size of the male and female pronuclei just before their membranes break down. Reproductive Medicine and Biology, 16(2), 200–205. doi: 10.1002/rmb2.12032 CrossRefGoogle ScholarPubMed
Payne, D., Flaherty, S. P., Barry, M. F. and Matthews, C. D. (1997). Preliminary observations on polar body extrusion and pronuclear formation in human oocytes using time-lapse video cinematography. Human Reproduction, 12(3), 532–541. doi: 10.1093/humrep/12.3.532 CrossRefGoogle ScholarPubMed
Revelli, A., Canosa, S., Carosso, A., Filippini, C., Paschero, C., Gennarelli, G., Delle Piane, L. and Benedetto, C. (2019, August 9). Impact of the addition of Early Embryo Viability Assessment to morphological evaluation on the accuracy of embryo selection on day 3 or day 5: A retrospective analysis. Journal of Ovarian Research, 12(1), 73. doi: 10.1186/s13048-019-0547-8 CrossRefGoogle ScholarPubMed
Rubio, I., Kuhlmann, R., Agerholm, I., Kirk, J., Herrero, J., Escribá, M. J., Bellver, J. and Meseguer, M. (2012). Limited implantation success of direct-cleaved human zygotes: A time-lapse study. Fertility and Sterility, 98(6), 1458–1463. doi: 10.1016/j.fertnstert.2012.07.1135 CrossRefGoogle ScholarPubMed
Sciorio, R. and Smith, G. D. (2019). Embryo culture at a reduced oxygen concentration of 5%: A mini review. Zygote, 27(6), 355–361. doi: 10.1017/S0967199419000522 CrossRefGoogle Scholar
Sciorio, R., Thong, J. K. and Pickering, S. J. (2018). Comparison of the development of human embryos cultured in either an embryoscope or benchtop incubator. Journal of Assisted Reproduction and Genetics, 35(3), 515–522. doi: 10.1007/s10815-017-1100-6 CrossRefGoogle ScholarPubMed
Sciorio, R., Herrer Saura, R., Thong, K. J., Esbert Algam, M., Pickering, S. J. and Meseguer, M. (2020a). Blastocyst collapse as an embryo marker of low implantation potential: A time-lapse multicentre study. Zygote, 28(2), 139–147. doi: 10.1017/S0967199419000819 CrossRefGoogle Scholar
Sciorio, R., Thong, K. J. and Pickering, S. J. (2020b). Spontaneous blastocyst collapse as an embryo marker of low pregnancy outcome: A time-lapse study. JBRA Assisted Reproduction, 24(1), 34–40. doi: 10.5935/1518-0557.20190044 Google ScholarPubMed
Sciorio, R., Thong, D., Thong, K. J. and Pickering, S. J. (2021). Clinical pregnancy is significantly associated with the blastocyst width and area: A time-lapse study. Journal of Assisted Reproduction and Genetics, 38(4), 847–855. doi: 10.1007/s10815-021-02071-x CrossRefGoogle ScholarPubMed
Sciorio, R., Tramontano, L., Rapalini, E., Bellaminutti, S., Bulletti, F. M., D’Amato, A., Manna, C., Palagiano, A., Bulletti, C. and Esteves, S. C. (2023). Risk of genetic and epigenetic alteration in children conceived following ART: Is it time to return to nature whenever possible? Clinical Genetics, 103(2), 133–145. doi: 10.1111/cge.14232 CrossRefGoogle ScholarPubMed
Steptoe, P. C. and Edwards, R. G. (1978). Birth after the reimplantation of a human embryo. Lancet, 2(8085), 366. doi: 10.1016/s0140-6736(78)92957-4 CrossRefGoogle ScholarPubMed
Storr, A., Venetis, C. A., Cooke, S., Kilani, S. and Ledger, W. (2017). Inter-observer and intra-observer agreement between embryologists during selection of a single Day 5 embryo for transfer: A multicenter study. Human Reproduction, 32(2), 307–314. doi: 10.1093/humrep/dew330 CrossRefGoogle ScholarPubMed
Subira, J., Craig, J., Turner, K., Bevan, A., Ohuma, E., McVeigh, E., Child, T. and Fatum, M. (2016). Grade of the inner cell mass, but not trophectoderm, predicts live birth in fresh blastocyst single transfers. Human Fertility, 19(4), 254–261. doi: 10.1080/14647273.2016.1223357 CrossRefGoogle Scholar
Sullivan, E. A., Wang, Y. A., Hayward, I., Chambers, G. M., Illingworth, P., McBain, J. and Norman, R. J. (2012). Single embryo transfer reduces the risk of perinatal mortality, a population study. Human Reproduction, 27(12), 3609–3615. doi: 10.1093/humrep/des315 CrossRefGoogle ScholarPubMed
Sundvall, L., Ingerslev, H. J., Breth Knudsen, U. and Kirkegaard, K. (2013). Inter- and intra-observer variability of time-lapse annotations. Human Reproduction, 28(12), 3215–3221. doi: 10.1093/humrep/det366 CrossRefGoogle ScholarPubMed
Swain, J. E. (2013). Could time-lapse embryo imaging reduce the need for biopsy and PGS? Journal of Assisted Reproduction and Genetics, 30(8), 1081–1090. doi: 10.1007/s10815-013-0048-4 CrossRefGoogle ScholarPubMed
Thompson, S. M., Onwubalili, N., Brown, K., Jindal, S. K. and McGovern, P. G. (2013). Blastocyst expansion score and trophectoderm morphology strongly predict successful clinical pregnancy and live birth following elective single embryo blastocyst transfer (eSET): A national study. Journal of Assisted Reproduction and Genetics, 30(12), 1577–1581. doi: 10.1007/s10815-013-0100-4 CrossRefGoogle Scholar
Togashi, K., Kumagai, J., Sato, E., Shirasawa, H., Shimoda, Y., Makino, K., Sato, W., Kumazawa, Y., Omori, Y. and Terada, Y. (2015). Dysfunction in gap junction intercellular communication induces aberrant behavior of the inner cell mass and frequent collapses of expanded blastocysts in mouse embryos. Journal of Assisted Reproduction and Genetics, 32(6), 969–976. doi: 10.1007/s10815-015-0479-1 CrossRefGoogle ScholarPubMed
Tran, D., Cooke, S., Illingworth, P. J. and Gardner, D. K. (2019, June 4). Deep learning as a predictive tool for fetal heart pregnancy following time-lapse incubation and blastocyst transfer. Human Reproduction, 34(6), 1011–1018. doi: 10.1093/humrep/dez064 CrossRefGoogle ScholarPubMed
Valeri, C., Pappalardo, S., De Felici, M. and Manna, C. (2011). Correlation of oocyte morphometry parameters with woman’s age. Journal of Assisted Reproduction and Genetics, 28(6), 545–552. doi: 10.1007/s10815-011-9555-3 CrossRefGoogle ScholarPubMed
Van den Abbeel, E., Balaban, B., Ziebe, S., Lundin, K., Cuesta, M. J., Klein, B. M., Helmgaard, L. and Arce, J. C. (2013). Association between blastocyst morphology and outcome of single-blastocyst transfer. Reproductive Biomedicine Online, 27(4), 353–361. doi: 10.1016/j.rbmo.2013.07.006 CrossRefGoogle ScholarPubMed
Van der Weiden, R. M. (2013). Trophectoderm morphology grading reflects interactions between embryo and endometrium. Fertility and Sterility, 100(4), e23. doi: 10.1016/j.fertnstert.2013.07.1986 CrossRefGoogle ScholarPubMed
Vega, M., Zaghi, S., Buyuk, E. and Jindal, S. (2018). Not all twins are monozygotic after elective single embryo transfer: Analysis of 32,600 elective single embryo transfer cycles as reported to the Society for Assisted Reproductive Technology. Fertility and Sterility, 109(1), 118–122. doi: 10.1016/j.fertnstert.2017.10.003 CrossRefGoogle Scholar
Wale, P. L. and Gardner, D. K. (2012). Oxygen regulates amino acid turnover and carbohydrate uptake during the preimplantation period of mouse embryo development. Biology of Reproduction, 87(1), 21–28. doi: 10.1095/biolreprod.112.100552 CrossRefGoogle ScholarPubMed
Wale, P. L. and Gardner, D. K. (2016). The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction. Human Reproduction Update, 22(1), 2–22. doi: 10.1093/humupd/dmv034 CrossRefGoogle ScholarPubMed
Wong, C. C., Loewke, K. E., Bossert, N. L., Behr, B., De Jonge, C. J., Baer, T. M. and Reijo Pera, R. A. (2010). Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nature Biotechnology, 28(10), 1115–1121. doi: 10.1038/nbt.1686 CrossRefGoogle Scholar
Yoon, H. J., Yoon, S. H., Son, W. Y., Im, K. S. and Lim, J. H. (2001). High implantation and pregnancy rates with transfer of human hatching day 6 blastocysts. Fertility and Sterility, 75(4), 832–833. doi: 10.1016/s0015-0282(00)01797-0 CrossRefGoogle ScholarPubMed
Zaninovic, N., Irani, M. and Meseguer, M. (2017). Assessment of embryo morphology and developmental dynamics by time-lapse microscopy: Is there a relation to implantation and ploidy? Fertility and Sterility, 108(5), 722–729. doi: 10.1016/j.fertnstert.2017.10.002 CrossRefGoogle Scholar
Zaninovic, N., Nohales, M., Zhan, Q., de Los Santos, Z. M. J., Sierra, J., Rosenwaks, Z. and Meseguer, M. (2019). A comparison of morphokinetic markers predicting blastocyst formation and implantation potential from two large clinical data sets. Journal of Assisted Reproduction and Genetics, 36(4), 637–646. doi: 10.1007/s10815-018-1396-x CrossRefGoogle ScholarPubMed
Zhang, J. Q., Li, X. L., Peng, Y., Guo, X., Heng, B. C. and Tong, G. Q. (2010). Reduction in exposure of human embryos outside the incubator enhances embryo quality and blastulation rate. Reproductive Biomedicine Online, 20(4), 510–515. doi: 10.1016/j.rbmo.2009.12.027 CrossRefGoogle ScholarPubMed
Zhang, X. D., Zhang, Q., Han, W., Liu, W. W., Shen, X. L., Yao, G. D., Shi, S. L., Hu, L. L., Wang, S. S., Wang, J. X., Zhou, J. J., Kang, W. W., Zhang, H. D., Luo, C., Yu, Q., Liu, R. Z., Sun, Y. P., Sun, H. X., Wang, X. H., et al. (2022). Comparison of embryo implantation potential between time-lapse incubators and standard incubators: A randomized controlled study. Reproductive Biomedicine Online, 45(5), 858–866. doi: 10.1016/j.rbmo.2022.06.017 CrossRefGoogle ScholarPubMed