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Blastocyst collapse as an embryo marker of low implantation potential: a time-lapse multicentre study

Published online by Cambridge University Press:  13 January 2020

Romualdo Sciorio Open the ORCID record for Romualdo Sciorio [Opens in a new window] ,
Raquel Herrer Saura ,
K. Joo Thong ,
Marga Esbert Algam ,
Susan Jane Pickering  and
Marcos Meseguer
Romualdo Sciorio*
Affiliation:
Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, UK
Raquel Herrer Saura
Affiliation:
IVIRMA Zaragoza, Poetisa María Zambrano, 31, 50018, Zaragoza, Spain
K. Joo Thong
Affiliation:
Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, UK
Marga Esbert Algam
Affiliation:
IVIRMA Barcelona, Ronda Gral. Mitre, 17, 08017Barcelona, Spain
Susan Jane Pickering
Affiliation:
Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, UK
Marcos Meseguer
Affiliation:
IVIRMA Valencia, Valencia, Spain
*
Author for correspondence: Romualdo Sciorio. Edinburgh Assisted Conception Programme, Edinburgh Fertility and Reproductive Endocrine Centre (EFREC), Royal Infirmary of Edinburgh, UK. E-mail: [email protected]
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Summary

Spontaneous blastocyst collapse during in vitro embryo development has been suggested as a novel marker of embryo quality. Therefore, the aim of this multicentre study was to carry out a retrospective multicentre analysis to investigate the correlation between blastocyst collapse and pregnancy outcome. Here, 1297 intracytoplasmic sperm injection (ICSI)/in vitro fertilization (IVF) fresh cycles, with an elective single blastocyst transfer (eSET) were included in this study. Embryos were cultured individually in 6.0% CO2, 5.0% O2, 89.0% N2, using single step medium (GTLTM VitroLife, Sweden) or sequential medium (CookTM, Cook Medical, Australia) and selected for transfer using standard morphological criteria. With the use of time-lapse monitoring (TLM), blastocysts were analyzed by measuring the maximum volume reduction and defined as having collapsed, if there was ≥ 50% volume reduction from the expanded blastocyst and the collapse event. Following embryo replacement, each blastocyst was retrospectively allocated to one of two groups (collapsed or not collapsed). Here, 259 blastocysts collapsed once or more during development (19.9%) and the remaining 1038 either contracted minimally or not collapsed (80.1%). A significantly higher ongoing pregnancy rate (OPR) of 51.9% (95% CI 48.9–59.9%) was observed when blastocysts that had not collapsed were replaced compared with cycles in which collapsed blastocysts were transferred 37.5% (95% CI 31.6–43.4%). This study suggests that human blastocysts that collapse spontaneously during development are less likely to implant and generate a pregnancy compared with embryos that do not. Although this is a retrospective study, the results demonstrated the utility of collapse episodes as new marker of embryo selection following eSET at blastocyst stage.

Keywords

Embryo cultureEmbryoScope time-lapse monitoringOngoing pregnancy rateSingle blastocyst transferSpontaneous blastocyst collapse
Type
Research Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 139 - 147
Copyright
© Cambridge University Press 2020

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References

Alikani, M, Calderon, G, Tomkin, G, Garrisi, J, Kokot, M and Cohen, J (2000) Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro. Hum Reprod 15, 2634–43.CrossRefGoogle ScholarPubMed
Aparicio-Ruiz, B, Basile, N, Perez-Albala, S, Bronet, F, Remohí, J and Meseguer, M (2016) Automatic time-lapse instrument is superior to singlepoint morphology observation for selecting viable embryos: retrospective study in oocyte donation. Fertil Steril 106, 1379, 1385.e10.CrossRefGoogle Scholar
Baltz, JM, Smith, SS, Biggers, JD and Lechene, C (1997) Intracellular ion concentrations and their maintenance by Na+/K+-ATPase in preimplantation mouse embryos. Zygote 5, 1–9.CrossRefGoogle ScholarPubMed
Basile, N, Morbeck, D, García-Velasco, J, Bronet, F and Meseguer, M (2013) Type of culture media does not affect embryo kinetics: a time-lapse analysis of sibling oocytes. Hum Reprod 28, 634–41.CrossRefGoogle Scholar
Basile, N, Nogales Mdel, C, Bronet, F, Florensa, M, Riqueiros, M, Rodrigo, L, Garcia-Velasco, J and Meseguer, M (2014) Increasing the probability of selecting chromosomally normal embryos by time-lapse morphokinetics analysis. Fertil Steril 101, 699–704.CrossRefGoogle ScholarPubMed
Bellver, J, Ayllon, Y, Ferrando, M, Melo, M, Goyri, E, Pellicer, A, Remohí, J and Meseguer, M (2010) Female obesity impairs in vitro fertilization outcome without affecting embryo quality. Fertil Steril 93, 447–54.CrossRefGoogle ScholarPubMed
Biggers, JD (1998) Reflections on the culture of the preimplantation embryo. Int J Dev Biol 42, 879–84.Google ScholarPubMed
Biggers, JD and Summers, MC (2008) Choosing a culture medium: making informed choices. Fertil Steril 90, 473–83.CrossRefGoogle ScholarPubMed
Biggers, JD, Bell, JE and Benos, DJ (1988) Mammalian blastocyst: transport functions in a developing epithelium. Am J Physiol 255, C419–32.CrossRefGoogle Scholar
Blake, D, Farquhar, CN, Johnson, N and Proctor, M (2007) Cleavage stage versus blastocyst stage embryo transfer in assisted conception. Cochrane Database Syst Rev 4, CD002118.Google Scholar
Bodri, D, Sugimoto, T, Yao Serna, J, Kawachiya, S, Kato, R and Matsumoto, T (2016) Blastocyst collapse is not an independent predictor of reduced live birth: a time-lapse study. Fertil Steril 105, 1476–83.CrossRefGoogle Scholar
Bourne, H, Edgar, DH and Baker, HWG (2004) Sperm preparation techniques. In: Gardner, DK, Weissman, A, Howles, CM and Shoham, Z (eds). Textbook of Assisted Reproductive Techniques: Laboratory and Clinical Perspectives 2nd edn. USA: Informa Healthcare, pp. 79–91.Google Scholar
Braude, P (2013) Selecting the ‘best’ embryos: prospects for improvement. Reprod Biomed Online 27, 644–53.CrossRefGoogle ScholarPubMed
Campbell, A (2014) Non-invasive techniques: embryo selection by time-lapse imaging. In: Montag, M. (ed.), A Practical Guide to Selecting Gametes and Embryos. CRC Press, Boca Raton, FL, USA, pp. 177–89.CrossRefGoogle Scholar
Campbell, A, Fishel, S, Bowman, N, Duffy, S, Sedler, M and Hickman, CF (2013) Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics. Reprod Biomed Online 26, 477–85.CrossRefGoogle ScholarPubMed
Cole, RJ (1967) Cinemicrographic observations on the trophoblast and zona pellucida of the mouse blastocyst. J Embryol Exp Morphol 17, 481–90.Google ScholarPubMed
Cruz, M, Garrido, N, Herrero, J, Perez-Cano, I, Munoz, M and Meseguer, M (2012) Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod Biomed Online 25, 371–81.CrossRefGoogle ScholarPubMed
Cutting, R, Morroll, D, Roberts, SA, Pickering, SJ, Rutherford, A; BFS and ACE (2008) Elective single embryo transfer: guidelines for practice. British Fertility Society and Association of Clinical Embryologists. Hum Fertil (Camb.) 11, 131–46.CrossRefGoogle Scholar
Dal Canto, M, Coticchio, G, Mignini-Renzini, M, De Ponti, E, Novara, PV, Brambillasca, F, Comi, R and Fadini, R (2012) Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation. Reprod Biomed Online 25, 474–80.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. Hum Reprod 31, 2442–9.CrossRefGoogle ScholarPubMed
Ducibella, T (1977) Surface changes of the developing trophoblast cell. In Development in Mammals (ed. Johnson, MH), pp. 5–31. Amsterdam, New York, Oxford: North-Holland Publishing Co.Google Scholar
Ducibella, T, Albertini, DF, Anderson, E and Biggers, JD (1975) The preimplantation mammalian embryo: characterization of intercellular junctions and their appearance during development. Dev Biol 45, 231–50.CrossRefGoogle ScholarPubMed
Eckert, JJ and Fleming, TP (2008) Tight junction biogenesis during early development. Biochim Biophys Acta 1778, 717–28.CrossRefGoogle ScholarPubMed
Erbach, GT, Biggers, JD, Manning, PC and Nowak, RA (2013) Localization of parathyroid hormone-related protein in the preimplantation mouse embryo is associated with events of blastocyst hatching. J Assist Reprod Genet 30, 1009–15.CrossRefGoogle ScholarPubMed
Fishel, S, Campbell, A, Montgomery, S, Smith, R, Nice, L, Duffy, S, Jenner, L, Berrisford, K, Kellam, L, Smith, R, D’Cruz, Iet al (2017) Live births after embryo selection using morphokinetics versus conventional morphology: a retrospective analysis. Reprod Biomed Online 35, 407–16.CrossRefGoogle ScholarPubMed
Fleming, TP, Sheth, B and Fesenko, I. (2001) Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci 6, D1000–7.CrossRefGoogle ScholarPubMed
Gardner, DK and Kelley, RL (2017) Impact of the IVF laboratory environment on human preimplantation embryo phenotype. J Dev Orig Health Dis 8, 418–35.CrossRefGoogle ScholarPubMed
Gardner, DK and Schoolcraft, WB (1999) Culture and transfer of human blastocysts. Curr Opin Obstet Gynecol 11, 307–11.CrossRefGoogle ScholarPubMed
Gerris, J, de Neubourg, D, Mangelschots, K, van Royen, E, Vercruyssen, M, Barudy-Vasquez, J, Valkenburg, M and Ryckaert, G (2002) Elective single day 3 embryo transfer halves the twinning rate without decrease in the ongoing pregnancy rate of an IVF/ICSI programme. Hum Reprod 17, 2626–31.CrossRefGoogle ScholarPubMed
Glass, RH, Lin, TP and Florence, J (1973) Mouse blastocyst re-expansion following puncture and treatment with inhibitors. J Reprod Fertil 35, 533–6.CrossRefGoogle ScholarPubMed
Glujovsky, D, Farquhar, C, Quinteiro Retamar, AM, Alvarez Sedo, CR and Blake, D (2016) Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev 6, CD002118.Google Scholar
Gonzales, DS and Bavister, BD (1995) Zona pellucida escape by hamster blastocysts in vitro is delayed and morphologically different compared with zona escape in vivo. Biol Reprod 52, 470–80.CrossRefGoogle ScholarPubMed
Gonzales, DS, Jones, JM, Pinyopummintr, T, Carnevale, EM, Ginther, OJ, Shapiro, SS and Bavister, BD (1996) Trophectoderm projections: a potential means for locomotion, attachment and implantation of bovine, equine, and human blastocysts. Hum Reprod 11, 2739–45.CrossRefGoogle ScholarPubMed
Harton, G, Tan, L, Chian, M, Suraj, V, Shen, S and Larman, MG (2016) Euploid blastocysts that experience more collapses are less likely to result in live birth: a quantitative and automated analysis of time-lapse cinematography. Abstract ESHRE 2016 O-222.Google Scholar
Hastings, RA and Enders, AC (1975) Junctional complexes in the preimplantation rabbit embryo. Anatom Rec 181, 17–34.CrossRefGoogle ScholarPubMed
Houghton, FD (2005) Role of gap junctions during early embryo development. Reproduction 129, 129–35.CrossRefGoogle ScholarPubMed
Huang, TT, Chinn, K, Kosasa, T, Ahn, HJ and Kessel, B (2016) Morphokinetics of human blastocyst expansion in vitro. Reprod Biomed Online 33, 659–67.CrossRefGoogle ScholarPubMed
Huang, ZP, Yu, H, Yang, ZM, Shen, WX, Wang, J and Shen, QX (2004) Uterine expression of implantation serine proteinase 2 during the implantation period and in vivo inhibitory effect of its antibody on embryo implantation in mice. Reprod Fertil Dev 16, 379–84.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. J Assist Reprod Genet 31, 421–6.CrossRefGoogle ScholarPubMed
Johnston, J, Gusmano, MK and Patrizio, P (2014) Preterm births, multiples, and fertility treatment: recommendations for changes to policy and clinical practices. Fertil Steril 102, 36–9.CrossRefGoogle ScholarPubMed
Lane, M and Gardner, DK (2007) Embryo culture medium: which is the best? Best Pract Res Clin Obstet Gynaecol 21, 83–100.CrossRefGoogle ScholarPubMed
Lemmen, JG, Agerholm, I and Ziebe, S (2008) Kinetic markers of human embryo quality using time-lapse recordings of IVF/ICSI-fertilized oocytes. Reprod Biomed Online 17, 385–91.CrossRefGoogle ScholarPubMed
Lewis, WH and Gregory, PW (1929) Cinematographs of living developing rabbit eggs. Science 69, 226–9.CrossRefGoogle ScholarPubMed
Marcos, J, Perez-Albala, 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. Hum Reprod 30, 2501–8.CrossRefGoogle ScholarPubMed
Marikawa, Y and Alarcon, VB (2012) Creation of trophectoderm, the first epithelium, in mouse preimplantation development. Results Probl Cell Differ 55, 165–84.CrossRefGoogle ScholarPubMed
Massip, A and Mulnard, J (1980) Time-lapse cinematographic analysis of hatching of normal and frozen–thawed cow blastocysts. J Reprod Fertil 58, 475–8.CrossRefGoogle ScholarPubMed
Massip, A, Mulnard, J, Vanderzwalmen, P, Hanzen, C and Ectors, F (1982) The behaviour of cow blastocyst in vitro: cinematographic and morphometric analysis. J Anat 134(Pt 2), 399–405.Google ScholarPubMed
Meseguer, M, Santiso, R, Garrido, N, García-Herrero, S, Remohí, J and Fernandez, JL (2011a) Effect of sperm DNA fragmentation on pregnancy outcome depends on oocyte quality. Fertil Steril 95, 124–8.CrossRefGoogle ScholarPubMed
Meseguer, M, Herrero, J, Tejera, A, Hilligsoe, KM, Ramsing, NB and Remohí, J (2011b) The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 26, 2658–71.CrossRefGoogle ScholarPubMed
Motato, Y, de los Santos, MJ, Escriba, MJ, Ruiz, BA, Remohí, J and Meseguer, M (2016) Morphokinetic analysis and embryonic prediction for blastocyst formation through an integrated time-lapse system. Fertil Steril 105, 376–84.CrossRefGoogle ScholarPubMed
Niimura, S (2003) Time-lapse videomicrographic analyses of contractions in mouse blastocysts. J Reprod Dev 49, 413–23.CrossRefGoogle ScholarPubMed
O’Sullivan, CM, Liu, SY, Rancourt, SL and Rancourt, DE (2001) Regulation of the trypsin-related proteinase ISP2 by progesterone in endometrial gland epithelium during implantation in mice. Reproduction 122, 235–44.CrossRefGoogle Scholar
Renard, JP, Philippson, A and Menezo, Y (1980) In-vitro uptake of glucose by bovine blastocysts. J Reprod Fertil 58, 161–4.CrossRefGoogle ScholarPubMed
Sciorio, R, Thong, JK and Pickering, SJ (2018) Comparison of the development of human embryos cultured in either an EmbryoScope or benchtop incubator. J Assist Reprod Genet 35, 515–22.CrossRefGoogle ScholarPubMed
Seshagiri, PB, Sen Roy, S, Sireesha, G and Rao, RP (2009) Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immun 83, 79–84.CrossRefGoogle ScholarPubMed
Sharma, N, Liu, S, Tang, L, Irwin, J, Meng, G and Rancourt, DE (2006) Implantation serine proteinases heterodimerize and are critical in hatching and implantation. BMC Dev Biol 6, 61.CrossRefGoogle ScholarPubMed
Sharma, N, Fahr, J, Renaux, B, Saifeddine, M, Kumar, R, Nishikawa, S, Mihara, K, Ramachandran, R, Hollenberg, MD and Rancourt, DE (2013) Implantation serine proteinase 2 is a monomeric enzyme with mixed serine proteolytic activity and can silence signalling via proteinase activated receptors. Biochem Cell Biol 91, 487–97.CrossRefGoogle ScholarPubMed
Sireesha, GV, Mason, RW, Hassanein, M, Tonack, S, Navarrete Santos, A, Fischer, B and Seshagiri, PB (2008) Role of cathepsins in blastocyst hatching in the golden hamster. Mol Hum Reprod 14, 337–46.CrossRefGoogle ScholarPubMed
Steptoe, P and Edwards, RG (1978) Birth after the reimplantation of a human embryo. Lancet 2, 366.CrossRefGoogle ScholarPubMed
Sun, ZG, Shi, HJ, Gu, Z, Wang, J and Shen, QX (2007) A single intrauterine injection of the serine protease inhibitor 4-(2-aminoethyl)benzenesulfonylfluoride hydrochloride reversibly inhibits embryo implantation in mice. Contraception 76, 250–5.CrossRefGoogle ScholarPubMed
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. J Assist Reprod Genet 32, 969–76.CrossRefGoogle ScholarPubMed
van Montfoort, AP, Dumoulin, JC, Land, JA, Coonen, E, Derhaag, JG and Evers, JL (2005) Elective single embryo transfer (eSET) policy in the first three IVF/ICSI treatment cycles. Hum Reprod 20, 433–6.CrossRefGoogle ScholarPubMed
Vilska, S, Tiitinen, A, Hyden-Granskog, C and Hovatta, O (1999) Elective transfer of one embryo results in an acceptable pregnancy rate and eliminates the risk of multiple birth. Hum Reprod 14, 2392–5.CrossRefGoogle Scholar
Wang, SX (2011) The past, present and future of embryo selection in in vitro fertilization: Frontiers in Reproductive Conference. Yale J Biol Med 84, 487–90.Google ScholarPubMed
Watson, AJ, Natale, DR and Barcroft, LC (2004) Molecular regulation of blastocyst formation. Anim Reprod Sci 82–83, 583–92.CrossRefGoogle ScholarPubMed
Wong, CC, Loewke, KE, Bossert, NL, Behr, B, De Jonge, CJ, Baer, TM and Reijo Pera, RA (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 28, 1115–21.CrossRefGoogle ScholarPubMed
Wordinger, RJ and Brinster, RL (1976) Influence of reduced glucose levels on the in vitro hatching, attachment and trophoblast outgrowth of the mouse blastocyst. Dev Biol 53, 294–6.CrossRefGoogle ScholarPubMed
Yamanaka, Y, Ralston, A, Stephenson, RO and Rossant, J (2006) Cell and molecular regulation of the mouse blastocyst. Dev Dyn 235, 2301–14.CrossRefGoogle ScholarPubMed
Zhang, JQ, Li, XL, Peng, Y, Guo, X, Heng, BC and Tong, GQ (2010) Reduction in exposure of human embryos outside the incubator enhances embryo quality and blastulation rate. Reprod Biomed Online 20, 510–5.CrossRefGoogle ScholarPubMed
Zhao, Y, Brezina, P, Hsu, CC, Garcia, J, Brinsden, PR and Wallach, E (2011) In vitro fertilization: four decades of reflections and promises. Biochim Biophys Acta 1810, 843–52.CrossRefGoogle ScholarPubMed