Study of nucleation status in the second cell cycle of human embryo and its impact on implantation rate

Fertility and Sterility

Volumn 106, Issue 2, 2016, Pages 291-299.e2

  Aguilar, Jesus ^a   Rubio, Irene ^b   Muñoz, Elkin ^a   Pellicer, Antonio ^b   Meseguer, Marcos ^b  

^a IVI Vigo   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Embryo kinetic; multinucleation; reversibility; time lapse

Indexed keywords

ADULT; CELL CYCLE S PHASE; CELL NUCLEUS; COHORT ANALYSIS; CONFERENCE PAPER; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO CELL; EMBRYO CULTURE; FEMALE; HUMAN; HUMAN CELL; INTRACYTOPLASMIC SPERM INJECTION; KINETICS; MORPHOLOGY; NIDATION; OOCYTE DONATION; PRIORITY JOURNAL; REPRODUCTION; RETROSPECTIVE STUDY; BLASTOMA; COMPARATIVE STUDY; EMBRYO TRANSFER; MAMMALIAN EMBRYO; PHYSIOLOGY; PREGNANCY; PREGNANCY RATE; TREATMENT OUTCOME;

BLASTOMERES; CELL NUCLEUS; EMBRYO CULTURE TECHNIQUES; EMBRYO IMPLANTATION; EMBRYO TRANSFER; EMBRYO, MAMMALIAN; FEMALE; HUMANS; KINETICS; PREGNANCY; PREGNANCY RATE; RETROSPECTIVE STUDIES; S PHASE; SPERM INJECTIONS, INTRACYTOPLASMIC; TREATMENT OUTCOME;

EID: 84963945648     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2016.03.036     Document Type: Conference Paper

References (67)

1. 1 Montag, M., Toth, B., Strowitzki, T., New approaches to embryo selection. Reprod Biomed Online 27 (2013), 539–546.
2. 2 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.
3. 3 Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Reprod Biomed Online 22 (2011), 632–646.
4. 4 Cohen, J., Alikani, M., Bisignano, A., Past performance of assisted reproduction technologies as a model to predict future progress: a proposed addendum to Moore's law. Reprod Biomed Online 25 (2012), 585–590.
5. 5 Meseguer, M., Rubio, I., Cruz, M., Basile, N., Marcos, J., Requena, A., Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 98 (2012), 1481–1489.
6. 6 Blandau, R.J., Rmery, R.E., The attachment cone of the guinea pig blastocyst as observed under time-lapse cinematography. Fertil Steril 8 (1957), 570–585.
7. 7 Adachi, Y., Takeshita, C., Wakatsuki, Y., Iwata, K., Kato, Y., Ueno, Y., et al. Analysis of physiological process in early stage of human embryos after ICSI using time-lapse cinematography. J Mamm Ova Res 22 (2005), 64–70.
8. 8 Lemmen, J.G., Agerholm, I., Ziebe, S., Kinetic markers of human embryo quality using time-lapse recordings of IVF/ICSI-fertilized oocytes. Reprod Biomed Online 17 (2008), 385–391.
9. 9 Mio, Y., Maeda, K., Time-lapse cinematography of dynamic changes occurring during in vitro development of human embryos. Am J Obstet Gynecol 199 (2008), 661–665.
10. 10 Pribenszky, C., Losonczi, E., Molnar, M., Lang, Z., Matyas, S., Rajczy, K., et al. Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reprod Biomed Online 20 (2010), 371–379.
11. 11 Scott, L., Ramsing, N.B., Oocyte and embryo respiration rate measurements in a clinical setting—potential to improve embryo selection?. Clin Embryol 10 (2007), 5–9.
12. 12 Herrero, J., Meseguer, M., Selection of high potential embryos using time-lapse imaging: the era of morphokinetics. Fertil Steril 99 (2013), 1030–1034.
13. 13 Wong, C.C., Loewke, K.E., Bossert, N.L., Behr, B., De Jonge, C.J., Baer, T.M., et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 28 (2010), 1115–1121.
14. 14 Cruz, M., Garrido, N., Herrero, J., Perez-Cano, I., Munoz, M., Meseguer, M., Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod Biomed Online 25 (2012), 371–381.
15. 15 Meseguer, M., Herrero, J., Tejera, A., Hilligsøe, K.M., Ramsing, N.B., Remohí, J., The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 26 (2011), 2568–2571.
16. 16 Aguilar, J., Motato, Y., Escribá, M.J., Ojeda, M., Muñoz, E., Meseguer, M., The human first cell cycle: impact on implantation. Reprod Biomed Online 28 (2014), 475–484.
17. 17 Campbell, A., Fishel, S., Duffy, S., Bowman, N., Sedler, M., Thornton, S., Retrospective analysis of outcome after IVF using an aneuploidy risk model derived from time-lapse imaging without PGS. Reprod Biomed Online 27 (2013), 140–146.
18. 18 Chamayou, S., Patrizio, P., Storaci, G., Tomaselli, V., Alecci, C., Ragolia, C., et al. The use of morphokinetic parameters to select all embryos with full capacity to implant. J Assist Reprod Genet 30 (2013), 703–710.
19. 19 Basile, N., Vime, P., Florensa, M., Aparicio Ruiz, B., García Velasco, J.A., Remohí, J., et al. The use of morphokinetics as a predictor of implantation: a multicentric study to define and validate an algorithm for embryo selection. Hum Reprod 30 (2014), 276–283.
20. 20 Chavez, S.L., Loewke, K.E., Han, J., Moussavi, F., Colls, P., Munne, S., et al. Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat Commun, 13, 2012, 1251.
21. 21 Campbell, A., Hickman, C.F.L., Duffy, S., Bowman, N., Sedler, M., Fishel, S., Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics. Reprod Biomed Online 26 (2013), 477–485.
22. 22 Freour, T., Lammers, J., Splingart, C., Lattes, S., Barriere, P., Is there a difference in morphokinetics according to ovarian reserve?. Fertil Steril, 98, 2012, S115.
23. 23 Muñoz, M., Cruz, M., Humaidan, P., Garrido, N., Perz-Cano, I., Meseguer, M., 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.
24. 24 Leibenthron, J., Montag, M., Koster, M., Toth, B., Reinsberg, J., Van der Ven, H., Influence of age and AMH on early embryo development realised by time-lapse imaging. Hum Reprod 27:Suppl 2 (2012), 162–205.
25. 25 Hampl, R., Stepan, M., Variability in timing of human embryos cleavage monitored by time-lapse system in relation to patient age. Ceska Gynekol 78 (2013), 531–536.
26. 26 Bellver, J., Mifsud, A., Grau, N., Privitera, L., Meseguer, M., Similar morphokinetic patterns in embryos derived from obese and normoweight infertile women: a time-lapse study. Hum Reprod 28 (2013), 794–800.
27. 27 Freour, T., Dessolle, L., Lammers, J., Lattes, S., Barriere, P., Comparison of embryo morphokinetics after in vitro fertilization-intracytoplasmic sperm injection in smoking and non-smoking women. Fertil Steril 99 (2013), 1944–1950.
28. 28 Ciray, H.N., Aksoy, T., Goktas, C., Ozturk, B., Bahceci, M., 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.
29. 29 Basile, N., Morbeck, D., Garcia-Velasco, J., Bronet, F., Meseguer, M., Type of culture media does not affect embryo kinetics: a time-lapse analysis of sibling oocytes. Hum Reprod 28 (2013), 634–641.
30. 30 Terada, Y., Ugajin, T., Hasegawa, H., Nabeshima, H., Yaegashi, N., Different embryonic development after blastomere biopsy for preimplantation genetic diagnosis, observed by time-lapse imaging. Fertil Steril 92 (2009), 1470–1471.
31. 31 Kirkegaard, K., Hindkjaer, J.J., Ingerslev, H.J., Human embryonic development after blastomere removal: a time-lapse analysis. Hum Reprod 27 (2012), 97–105.
32. 32 Kroener, L., Ambartsumyan, G.G., Briton-Jones, C.C., Dumesic, D.D., Surrey, M.M., Munne, S.S., et al. The effect of timing of embryonic progression on chromosomal abnormality. Fertil Steril 98 (2012), 876–880.
33. 33 Cruz, M., Garrido, N., Gadea, B., Munoz, M., Perez-Cano, I., Meseguer, M., Oocyte insemination techniques are related to alterations of embryo developmental timing in an oocyte donation model. Reprod Biomed Online 27 (2013), 367–375.
34. 34 Garcia, L.M., Martinez, M.M., Navaro, M.B., Cano, I.P., Cantero, M.M., Meseguer, M., Does semen cryopreservation have influence on embryo kinetics?. Fertil Steril, 98, 2012, S164.
35. 35 Hertig, A.T., Rock, J., Adams, E.C., et al. On the preimplantation multinuclear blastomeres analysed by FISH stages of the human ovum: a description of four normal and four abnormal specimens ranging from the second and fifth day of development. Contrib Embryol 35 (1954), 201–220.
36. 36 Lopata, A., Kohlman, D., Johnston, I., The fine structure of normal and abnormal human embryos developed in culture. Beier, H.M., Lindner, H.R., (eds.) Fertilization of the human egg in vitro, 1983, Springer Verlag, Berlin, 182–210.
37. 37 Plachot, M., Mandelbaum, J., Cohen, J., Debache, C., Pigeau, P., Junca, A.M., Sequential use of clomiphene citrate, human menopausal gonadotropin, and human chorionic gonadotrophin in human in vitro fertilization. I. Follicular growth and oocytes suitability. Fertil Steril 43 (1985), 255–262.
38. 38 Hardy, K., Winston, R.M., Handyside, A.H., Binucleate blastomeres in preimplantation human embryos in vitro: failure of cytokinesis during early cleavage. J Reprod Fertil 98 (1993), 549–558.
39. 39 Munné, S., Cohen, J., Unsuitability of multinucleated human blastomeres for preimplantation genetic diagnosis. Hum Reprod 8 (1993), 1120–1125.
40. 40 Munné, S., Grifo, J., Cohen, J., Weier, H.U., Chromosome abnormalities in human arrested preimplantation embryos: a multiple-probe FISH study. Am J Hum Genet 55 (1994), 150–159.
41. 41 Pickering, G.D., Taylor, A., Johnson, M.H., Braude, P.R., An analysis of multinucleated blastomere formation in human embryos. Hum Reprod 10 (1995), 1912–1922.
42. 42 Kligman, I., Benadiva, C., Alikani, M., Munné, S., The presence of multinucleated blastomeres in human embryos is correlated with chromosomal abnormalities. Hum Reprod 11 (1996), 1492–1498.
43. 43 Laverge, H., De Sutter, P., Verschraegen-Spae, M.R., De Paepe, A., Dhont, M., Triple colour fluorescent in-situ hybridization for chromosomes X, Y and 1 on spare human embryos. Hum Reprod 12 (1997), 809–814.
44. 44 De La Fuente, R., King, W.A., Developmental consequences of karyokinesis without cytokinesis during the first mitotic cell cycle of bovine parthenotes. Biol Reprod 58 (1998), 952–962.
45. 45 Chatzimeletiou, K., Morrison, E.E., Prapas, N., Prapas, Y., Handyside, A.H., Spindle abnormalities in normally developing and arrested human preimplantation embryos in vitro identified by confocal laser scanning microscopy. Hum Reprod 20 (2005), 672–682.
46. 46 Van Royen, E., Mangelschots, K., Vercruyssen, M., de Neubourg, D., Valkenburg, M., Ryckaert, G., et al. Multinucleation in cleavage stage embryos. Hum Reprod 18 (2003), 1062–1069.
47. 47 Balakier, H., Cadesky, K., The frequency and developmental capability of human embryos containing multinucleated blastomeres. Hum Reprod 12 (1997), 800–804.
48. 48 Jackson, K.V., Ginsburg, E.S., Hornstein, M.D., Rein, M.S., Clarke, R.N., 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 70 (1998), 60–66.
49. 49 Alikani, M., Calderon, G., Tomkin, G., Garrisi, J., Kokot, M., Cohen, J., Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro. Hum Reprod 1 (2000), 2634–2643.
50. 50 Pelinck, M.J., De Vos, M., Dekens, M., Van der Elst, J., De Sutter, P., Dhont, M., Embryos cultured in vitro with multinucleated blastomeres have poor implantation potential in human in-vitro fertilization and intracytoplasmic sperm injection. Hum Reprod 13 (1998), 960–963.
51. 51 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 16 (2001), 313–318.
52. 52 Staessen, C., Van Steirteghem, A., The genetic constitution of multinuclear blastomeres and their derivative daughter blastomeres. Hum Reprod 13 (1998), 1625–1631.
53. 53 Alikani, M., Cohen, J., Tomkin, G., Garrisi, G.J., Mack, C., Scott, R.T., Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertil Steril 71 (1999), 836–842.
54. 54 Knopman, J., Krey, L.C., Lee, J., Fino, M.E., Novetsky, A.P., Noyes, N., Monozygotic twinning: an eight-year experience at a large IVF center. Fertil Steril 94 (2010), 502–510.
55. 55 Portela, S., Fernandez, I., Lopez, T., Martinez, B., Aguilar, J., Munoz, E., Patients with müllerian anomalies have lower embryo implantation in oocyte donation. Fertil Steril, 96, 2011, S277.
56. 56 Garrido, N., Zuzuarregui, J.L., Meseguer, M., Simon, C., Remohi, J., Pellicer, A., Sperm and oocyte donor selection and management: experience of a 10 year follow-up of more than 2100 candidates. Hum Reprod 17 (2002), 3142–3148.
57. 57 Meseguer, M., Santiso, R., Garrido, N., Garcia-Herrero, S., Remohi, J., Fernandez, J.L., Effect of sperm DNA fragmentation on pregnancy outcome depends on oocyte quality. Fertil Steril 95 (2011), 124–128.
58. 58 Melo, M., Bellver, J., Garrido, N., Meseguer, M., Pellicer, A., Remohi, J., A prospective, randomized, controlled trial comparing three different gonadotropin regimens in oocyte donors: ovarian response, in-vitro fertilization outcome, and analysis of cost minimization. Fertil Steril 94 (2010), 958–964.
59. 59 Meseguer, M., Martinez-Conejero, J.A., O'Connor, J.E., Pellicer, A., Remohi, J., Garrido, N., The significance of sperm DNA oxidation in embryo development and reproductive outcome in an oocyte donation program: a new model to study a male infertility prognostic factor. Fertil Steril 89 (2008), 1191–1199.
60. 60 Ciray, N., Campbell, A., Agerholm, I., Aguilar, J., Chamayou, S., Esbert, M., et al. Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group. Hum Reprod 29 (2014), 2650–2660.
61. 61 Cobo, A., Meseguer, M., Remohi, J., Pellicer, A., Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod 25 (2010), 2239–2246.
62. 62 Yakin, K., Balaban, B., Urman, B., Impact of the presence of one or more multinucleated blastomeres on the developmental potential of the embryo to the blastocyst stage. Fertil Steril 83 (2005), 243–245.
63. 63 Ergin, E.G., Calişkan, E., Yalçinkaya, E., Oztel, Z., Cökelez, K., Ozay, A., et al. Frequency of embryo multinucleation detected by time-lapse system and its impact on pregnancy outcome. Fertil Steril 102 (2014), 1029–1034.
64. 64 Meriano, J., Clark, C., Cadesky, K., Laskin, C.A., Binucleated and micronucleated blastomeres in embryos derived from human assisted reproduction cycles. Reprod Biomed Online 9 (2004), 511–520.
65. 65 Asociación para el Estudio de la Biología de la Reproducción. Cuadernos de Embriología Clínica. Criterios ASEBIR de valoración morfológica de oocitos, embriones tempranos y blastocistos humanos. 3rd ed., 2015, ASEBIR, Madrid.
66. 66 Fauque, P., Audureau, E., Leandri, R., Delaroche, L., Assouline, S., Epelboin, S., et al. Is the nuclear status of an embryo an independent factor to predict its ability to develop to term?. Fertil Steril 99 (2013), 1299–1304.
67. 67 Rubio, I., Galan, A., Larreategui, Z., Ayerdi, F., Bellver, J., Herrero, J., et al. Clinical validation of embryo culture and selection by morphokinetic analysis: a randomized, controlled trial of the EmbryoScope. Fertil Steril 102 (2014), 1287–1294.