Pronuclear and blastocyst morphology are associated age-dependently with embryo ploidy in in vitro fertilization cycles

References

• Ahlstrom, A., Westin, C., Reismer, E., Wikland, M., & Hardarson, T. (2011). Trophectoderm morphology: an important parameter for predicting live birth after single blastocyst transfer. Human Reproduction (Oxford, England), 26(12), 3289–3296. https://doi.org/https://doi.org/10.1093/humrep/der325
   PubMed Web of Science ®Google Scholar
• Alfarawati, S., Fragouli, E., Colls, P., Stevens, J., Gutiérrez-Mateo, C., Schoolcraft, W. B., Katz-Jaffe, M., & Wells, D. (2011). The relationship between blastocyst morphology, chromosomal abnormality, and embryo gender. Fertility and Sterility, 95(2), 520–524. https://doi.org/https://doi.org/10.1016/j.fertnstert.2010.04.003
   PubMed Web of Science ®Google Scholar
• Balaban, B., Urman, B., Isiklar, A., Alatas, C., Aksoy, S., Mercan, R., Mumcu, A., & Nuhoglu, A. (2001). The effect of pronuclear morphology on embryo quality parameters and blastocyst transfer outcome. Human Reproduction (Oxford, England), 16(11), 2357–2361. https://doi.org/https://doi.org/10.1093/humrep/16.11.2357
   PubMed Web of Science ®Google Scholar
• Balaban, B., Yakin, K., Urman, B., Isiklar, A., & Tesarik, J. (2004). Pronuclear morphology predicts embryo development and chromosome constitution. Reproductive Biomedicine Online, 8(6), 695–700. https://doi.org/https://doi.org/10.1016/S1472-6483(10)61651-3
   PubMed Web of Science ®Google Scholar
• Capalbo, A., Rienzi, L., Cimadomo, D., Maggiulli, R., Elliott, T., Wright, G., Nagy, Z. P., & Ubaldi, F. M. (2014). Correlation between standard blastocyst morphology, euploidy and implantation: an observational study in two centers involving 956 screened blastocysts. Human Reproduction (Oxford, England), 29(6), 1173–1181. https://doi.org/https://doi.org/10.1093/humrep/deu033
   PubMed Web of Science ®Google Scholar
• Capalbo, A., Romanelli, V., Patassini, C., Poli, M., Girardi, L., Giancani, A., Stoppa, M., Cimadomo, D., Ubaldi, F. M., & Rienzi, L. (2018). Diagnostic efficacy of blastocoel fluid and spent media as sources of DNA for preimplantation genetic testing in standard clinical conditions. Fertility and Sterility, 110(5), 870–879.e5. https://doi.org/https://doi.org/10.1016/j.fertnstert.2018.05.031
   PubMed Web of Science ®Google Scholar
• Chiang, T., Duncan, F. E., Schindler, K., Schultz, R. M., & Lampson, M. A. (2010). Report evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Current Biology: Cb, 20(17), 1522–1528. https://doi.org/https://doi.org/10.1016/j.cub.2010.06.069
   PubMed Web of Science ®Google Scholar
• Cimadomo, D., Soscia, D., Vaiarelli, A., Maggiulli, R., Capalbo, A., Ubaldi, F. M., & Rienzi, L. (2019). Looking past the appearance: a comprehensive description of the clinical contribution of poor-quality blastocysts to increase live birth rates during cycles with aneuploidy testing. Human Reproduction (Oxford, England), 34(7), 1206–1214. https://doi.org/https://doi.org/10.1093/humrep/dez078
   PubMed Web of Science ®Google Scholar
• Dahdouh, E. M., Balayla, J., & García-Velasco, J. A. (2015). Comprehensive chromosome screening improves embryo selection: A meta-analysis. Fertility and Sterility, 104(6), 1503–1512. https://doi.org/https://doi.org/10.1016/j.fertnstert.2015.08.038
   PubMed Web of Science ®Google Scholar
• Ebner, T., Moser, M., & Tews, G. (2004). Developmental potential of human pronuclear zygotes in relation to their pronuclear orientation. Human Reproduction (Oxford, England), 19(8), 1925–1926. https://doi.org/https://doi.org/10.1093/humrep/deh331
   PubMed Web of Science ®Google Scholar
• Ebner, T., Tritscher, K., Mayer, R. B., Oppelt, P., Duba, H.-C., Maurer, M., Schappacher-Tilp, G., Petek, E., & Shebl, O. (2016). Quantitative and qualitative trophectoderm grading allows for prediction of live birth and gender. Journal of Assisted Reproduction and Genetics, 33(1), 49–57. https://doi.org/https://doi.org/10.1007/s10815-015-0609-9
   PubMed Web of Science ®Google Scholar
• Edirisinghe, W. R., Jemmott, R., Smith, C., & Allan, J. (2005). Association of pronuclear Z score with rates of aneuploidy in in vitro-fertilised embryos. Reproduction, Fertility and Development, 17(5), 529. https://doi.org/https://doi.org/10.1071/RD04065
   PubMed Web of Science ®Google Scholar
• Feichtinger, M., Vaccari, E., Carli, L., Wallner, E., Mädel, U., Figl, K., Palini, S., & Feichtinger, W. (2017). Non-invasive preimplantation genetic screening using array comparative genomic hybridization on spent culture media: a proof-of-concept pilot study. Reproductive BioMedicine Online, 34(6), 583–589. https://doi.org/https://doi.org/10.1016/j.rbmo.2017.03.015
   PubMed Web of Science ®Google Scholar
• Fragouli, E., Alfarawati, S., Spath, K., Babariya, D., Tarozzi, N., Borini, A., & Wells, D. (2017). Analysis of implantation and ongoing pregnancy rates following the transfer of mosaic diploid-aneuploid blastocysts. Human Genetics, 136(7), 805–819. https://doi.org/https://doi.org/10.1007/s00439-017-1797-4
   PubMed Web of Science ®Google Scholar
• Fragouli, E., Munné, S., & Wells, D. (2019). The cytogenetic constitution of human blastocysts: insights from comprehensive chromosome screening strategies. Human Reproduction Update, 25(1), 15–33. https://doi.org/https://doi.org/10.1093/humupd/dmy036
   PubMed Web of Science ®Google Scholar
• Fulka, H., Kyogoku, H., Zatsepina, O., Langerova, A., & Fulka, J. (2015). Can nucleoli be markers of developmental potential in human zygotes? Trends in Molecular Medicine, 21(11), 663–610. https://doi.org/https://doi.org/10.1016/j.molmed.2015.09.005
   PubMed Web of Science ®Google Scholar
• Gamiz, P., Rubio, C., de los Santos, M. J., Mercader, A., Simón, C., Remohí, J., & Pellicer, A. (2003). The effect of pronuclear morphology on early development and chromosomal abnormalities in cleavage-stage embryos. Human Reproduction (Oxford England), 18(11), 2413–2419. https://doi.org/https://doi.org/10.1093/humrep/deg458
   PubMed Web of Science ®Google Scholar
• Gardner, D. K., Lane, M., Stevens, J., Schlenker, T., & Schoolcraft, W. B. (2000). Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertility and Sterility, 73(6), 1155–1158. https://doi.org/https://doi.org/10.1016/S0015-0282(00)00518-5
   PubMed Web of Science ®Google Scholar
• Gianaroli, L., Magli, M. C., Ferraretti, A. P., Fortini, D., & Grieco, N. (2003). Pronuclear morphology and chromosomal abnormalities as scoring criteria for embryo selection. Fertility and Sterility, 80(2), 341–349. https://doi.org/https://doi.org/10.1016/S0015-0282(03)00596-X
   PubMed Web of Science ®Google Scholar
• Gianaroli, L., Magli, M. C., Ferraretti, A. P., Lappi, M., Borghi, E., & Ermini, B. (2007). Oocyte euploidy, pronuclear zygote morphology and embryo chromosomal complement. Human Reproduction (Oxford, England), 22(1), 241–249. https://doi.org/https://doi.org/10.1093/humrep/del334
   PubMed Web of Science ®Google Scholar
• Gianaroli, L., Magli, M. C., Pomante, A., Crivello, A. M., Cafueri, G., Valerio, M., & Ferraretti, A. P. (2014). Blastocentesis: a source of DNA for preimplantation genetic testing. Results from a pilot study. Fertility and Sterility, 102(6), 1692–1699.e6. https://doi.org/https://doi.org/10.1016/j.fertnstert.2014.08.021
   PubMed Web of Science ®Google Scholar
• Greco, E., Minasi, M. G., & Fiorentino, F. (2015). Healthy Babies after Intrauterine Transfer of Mosaic Aneuploid Blastocysts. The New England Journal of Medicine, 373(21), 2089–2090. https://doi.org/https://doi.org/10.1056/NEJMc1500421
   PubMed Web of Science ®Google Scholar
• Hill, M. J., Richter, K. S., Heitmann, R. J., Graham, J. R., Tucker, M. J., DeCherney, A. H., Browne, P. E., & Levens, E. D. (2013). Trophectoderm grade predicts outcomes of single-blastocyst transfers. Fertility and Sterility, 99(5), 1283–1289.e1. https://doi.org/https://doi.org/10.1016/j.fertnstert.2012.12.003
   PubMed Web of Science ®Google Scholar
• Huang, J., Yan, L., Lu, S., Zhao, N., & Qiao, J. (2017). Re-analysis of aneuploidy blastocysts with an inner cell mass and different regional trophectoderm cells. Journal of Assisted Reproduction and Genetics, 34(4), 487–493. https://doi.org/https://doi.org/10.1007/s10815-017-0875-9
   PubMed Web of Science ®Google Scholar
• Kahraman, S., Kumtepe, Y., Sertyel, S., Dönmez, E., Benkhalifa, M., Findiki, N., & Vanderzwalmen, P. (2002). Pronuclear morphology scoring and chromosomal status of embryos in severe male infertility. Human Reproduction (Oxford, England), 17(12), 3193–3200. https://doi.org/https://doi.org/10.1093/humrep/17.12.3193
   PubMed Web of Science ®Google Scholar
• Lai, H. H., Chuang, T. H., Wong, L. K., Lee, M. J., Hsieh, C. L., Wang, H. L., & Chen, S. U. (2017). Identification of mosaic and segmental aneuploidies by next-generation sequencing in preimplantation genetic screening can improve clinical outcomes compared to array-comparative genomic hybridization. Molecular Cytogenetics, 10(1), 14 https://doi.org/https://doi.org/10.1186/s13039-017-0315-7
   PubMedGoogle Scholar
• Magli, M. C., Albanese, C., Crippa, A., Tabanelli, C., Ferraretti, A. P., & Gianaroli, L. (2019). Deoxyribonucleic acid detection in blastocoelic fluid: a new predictor of embryo ploidy and viable pregnancy. Fertility and Sterility, 111(1), 77–85. https://doi.org/https://doi.org/10.1016/j.fertnstert.2018.09.016
   PubMed Web of Science ®Google Scholar
• Maille, L., Bergere, M., Lemoine, E., Camier, B., Prevost, J., Bourdrel, J., Hammoud, I., Selva, J., & Vialard, F. (2009). Pronuclear morphology differs between women more than 38 and women less than 30 years of age. Reproductive BioMedicine Online, 18(3), 367–373. https://doi.org/https://doi.org/10.1016/S1472-6483(10)60095-8
   PubMed Web of Science ®Google Scholar
• McCoy, R. C. (2017). Mosaicism in preimplantation human embryos: when chromosomal abnormalities are the norm. Trends in Genetics, 33(7), 448–463. https://doi.org/https://doi.org/10.1016/j.tig.2017.04.001
   PubMed Web of Science ®Google Scholar
• Minasi, M. G., Colasante, A., Riccio, T., Ruberti, A., Casciani, V., Scarselli, F., Spinella, F., Fiorentino, F., Varricchio, M. T., & Greco, E. (2016). Correlation between aneuploidy, standard morphology evaluation and morphokinetic development in 1730 biopsied blastocysts: a consecutive case series study. Human Reproduction (Oxford, England), 31(10), 2245–2254. https://doi.org/https://doi.org/10.1093/humrep/dew183
   PubMed Web of Science ®Google Scholar
• Morbeck, D. E. (2017). Blastocyst culture in the Era of PGS and FreezeAlls: Is a 'C' a failing grade? Human Reproduction Open, 2017(3), hox017. https://doi.org/https://doi.org/10.1093/hropen/hox017
   PubMedGoogle Scholar
• Munné, S., & Cohen, J. (1998). Chromosome abnormalities in human embryos. Human Reproduction Update, 4(6), 842–855. https://doi.org/https://doi.org/10.1093/humupd/4.6.842
   PubMed Web of Science ®Google Scholar
• Neal, S. A., Franasiak, J. M., Forman, E. J., Werner, M. D., Taylor, D., Treff, N. R., & Scott, R. T. (2014). High relative deoxyribonucleic acid content of trophectoderm biopsy adversely affects pregnancy outcomes. Fertility and Sterility, 102(3), e176–e177. https://doi.org/https://doi.org/10.1016/j.fertnstert.2016.11.013
   Web of Science ®Google Scholar
• Neal, S. A., Morin, S. J., Franasiak, J. M., Goodman, L. R., Juneau, C. R., Forman, E. J., Werner, M. D., & Scott, R. T. (2018). Preimplantation genetic testing for aneuploidy is cost-effective, shortens treatment time, and reduces the risk of failed embryo transfer and clinical miscarriage. Fertility and Sterility, 110(5), 896–904. https://doi.org/https://doi.org/10.1016/j.fertnstert.2018.06.021
   PubMed Web of Science ®Google Scholar
• Ozgur, K., Berkkanoglu, M., Bulut, H., Didem, G., Yoruk, A., & Candurmaz, N. N. (2019). Single best euploid versus single best unknown-ploidy blastocyst frozen embryo transfers: a randomized controlled trial. Journal of Assisted Reproduction and Genetics, 36(4), 629–636. https://doi.org/https://doi.org/10.1007/s10815-018-01399-1
   PubMed Web of Science ®Google Scholar
• Popovic, M., Dheedene, A., Christodoulou, C., Taelman, J., Dhaenens, L., Van Nieuwerburgh, F., Deforce, D., Van den Abbeel, E., De Sutter, P., Menten, B., & Heindryckx, B. (2018). Chromosomal mosaicism in human blastocysts: the ultimate challenge of preimplantation genetic testing? Human Reproduction (Oxford, England), 33(7), 1342–1354. https://doi.org/https://doi.org/10.1093/humrep/dey106
   PubMed Web of Science ®Google Scholar
• Popovic, M., Dhaenens, L., Boel, A., Menten, B., & Heindryckx, B. (2020). Chromosomal mosaicism in human blastocysts: the ultimate diagnostic dilemma. Human Reproduction Update, 26(3), 313–334. https://doi.org/https://doi.org/10.1093/humupd/dmz050
   PubMed Web of Science ®Google Scholar
• Qi, S., Liang, L., Xian, Y., Liu, J., & Wang, W. (2014). Arrested human embryos are more likely to have abnormal chromosomes than developing embryos from women of advanced maternal age. Journal of Ovarian Research, 7(1), 65. https://doi.org/https://doi.org/10.1186/1757-2215-7-65
   PubMedGoogle Scholar
• Reignier, A., Lammers, J., Barriere, P., & Freour, T. (2018). Can time-lapse parameters predict embryo ploidy? A systematic review. Reproductive Biomedicine Online, 36(4), 380–387. https://doi.org/https://doi.org/10.1016/j.rbmo.2018.01.001
   PubMed Web of Science ®Google Scholar
• Rubio, C., Rienzi, L., Navarro-Sánchez, L., Cimadomo, D., García-Pascual, C. M., Albricci, L., Soscia, D., Valbuena, D., Capalbo, A., Ubaldi, F., & Simón, C. (2019). Embryonic cell-free DNA versus trophectoderm biopsy for aneuploidy testing: concordance rate and clinical implications. Fertility and Sterility, 112(3), 510–519. https://doi.org/https://doi.org/10.1016/j.fertnstert.2019.04.038
   PubMed Web of Science ®Google Scholar
• Sadowy, S., Tomkin, G., Munné, S., Ferrara-Congedo, T., & Cohen, J. (1998). Impaired development of zygotes with uneven pronuclear size. Zygote (Cambridge, England), 6(2), 137–141. https://doi.org/https://doi.org/10.1017/s0967199498000057
   PubMed Web of Science ®Google Scholar
• Scott, L. (2003). Pronuclear scoring as a predictor of embryo development. Reproductive Biomedicine Online, 6(2), 201–214. https://doi.org/https://doi.org/10.1016/S1472-6483(10)61711-7
   PubMedGoogle Scholar
• Scott, L., Alvero, R., Leondires, M., & Miller, B. (2000). The morphology of human pronuclear embryos is positively related to blastocyst development and implantation. Human Reproduction (Oxford, England), 15(11), 2394–2403. https://doi.org/https://doi.org/10.1093/humrep/15.11.2394
   PubMed Web of Science ®Google Scholar
• Scott, R. T., Taylor, D., Treff, N. R., Tao, X., Ferry, K. M., & Forman, E. J. (2012). Single embryo transfer with comprehensive chromosome screening results in improved ongoing pregnancy rates and decreased miscarriage rates. Human Reproduction (Oxford, England), 27(4), 1217–1222. https://doi.org/https://doi.org/10.1093/humrep/des020
   PubMed Web of Science ®Google Scholar
• Shamonki, M. I., Jin, H., Haimowitz, Z., & Liu, L. (2016). Proof of concept: preimplantation genetic screening without embryo biopsy through analysis of cell-free DNA in spent embryo culture media. Fertility and Sterility, 106(6), 1312–1318. https://doi.org/https://doi.org/10.1016/j.fertnstert.2016.07.1112
   PubMed Web of Science ®Google Scholar
• Sigalos, G. Α., Triantafyllidou, O., & Vlahos, N. F. (2016). Novel embryo selection techniques to increase embryo implantation in IVF attempts. Archives of Gynecology and Obstetrics, 294(6), 1117–1124. https://doi.org/https://doi.org/10.1007/s00404-016-4196-5
   PubMed Web of Science ®Google Scholar
• Tesarik, J., & Greco, E. (1999). The probability of abnormal preimplantation development can be predicted by a single static observation on pronuclear stage morphology. Human Reproduction (Oxford, England), 14(5), 1318–1323. https://doi.org/https://doi.org/10.1093/humrep/14.5.1318
   PubMed Web of Science ®Google Scholar
• Thompson, S. M., Onwubalili, N., Brown, K., Jindal, S. K., & 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. https://doi.org/https://doi.org/10.1007/s10815-013-0100-4
   PubMed Web of Science ®Google Scholar
• Tšuiko, O., Zhigalina, D. I., Jatsenko, T., Skryabin, N. A., Kanbekova, O. R., Artyukhova, V. G., Svetlakov, A. V., Teearu, K., Trošin, A., Salumets, A., Kurg, A., & Lebedev, I. N. (2018). Karyotype of the blastocoel fluid demonstrates low concordance with both trophectoderm and inner cell mass. Fertility and Sterility, 109(6), 1127–1134.e1. https://doi.org/https://doi.org/10.1016/j.fertnstert.2018.02.008
   PubMed Web of Science ®Google Scholar
• Vera-Rodriguez, M., Diez-Juan, A., Jimenez-Almazan, J., Martinez, S., Navarro, R., Peinado, V., Mercader, A., Meseguer, M., Blesa, D., Moreno, I., Valbuena, D., Rubio, C., & Simon, C. (2018). Origin and composition of cell-free DNA in spent medium from human embryo culture during preimplantation development. Human Reproduction (Oxford, England), 33(4), 745–756. https://doi.org/https://doi.org/10.1093/humrep/dey028
   PubMed Web of Science ®Google Scholar
• Victor, A. R., Tyndall, J. C., Brake, A. J., Lepkowsky, L. T., Murphy, A. E., Griffin, D. K., McCoy, R. C., Barnes, F. L., Zouves, C. G., & Viotti, M. (2019). One hundred mosaic embryos transferred prospectively in a single clinic: exploring when and why they result in healthy pregnancies. Fertility and Sterility, 111(2), 280–293. https://doi.org/https://doi.org/10.1016/j.fertnstert.2018.10.019
   PubMed Web of Science ®Google Scholar
• Wang, A., Kort, J., Behr, B., & Westphal, L. M. (2018). Euploidy in relation to blastocyst sex and morphology. Journal of Assisted Reproduction and Genetics, 35(9), 1565–1572. https://doi.org/https://doi.org/10.1007/s10815-018-1262-x
   PubMed Web of Science ®Google Scholar
• Wang, H., Qin, J., Liang, D., Xia, J., Tan, H., & Sheng, X. (2015). Pregnancy-related complications and adverse pregnancy outcomes in multiple pregnancies resulting from assisted reproductive technology: a meta-analysis of cohort studies. Fertility and Sterility, 103(6), 1492–1508.e7. https://doi.org/https://doi.org/10.1016/j.fertnstert.2015.03.018
   PubMed Web of Science ®Google Scholar
• Xu, J., Fang, R., Chen, L., Chen, D., Xiao, J., Yang, W., Wang, H., Song, X., Ma, T., Bo, S., Shi, C., Ren, J., Huang, L., Cai, L.-Y., Yao, B., Xie, X. S., & Lu, S. (2016). Noninvasive chromosome screening of human embryos by genome sequencing of embryo culture medium for in vitro fertilization. Proceedings of the National Academy of Sciences of the United States of America, 113(42), 11907–11912. https://doi.org/https://doi.org/10.1073/pnas.1613294113
   PubMed Web of Science ®Google Scholar
• Zhang, S., Luo, K., Cheng, D., Tan, Y., Lu, C., He, H., Gu, Y., Lu, G., Gong, F., & Lin, G. (2016). Number of biopsied trophectoderm cells is likely to affect the implantation potential of blastocysts with poor trophectoderm quality. Fertility and Sterility, 105(5), 1222–1227.e4. https://doi.org/https://doi.org/10.1016/j.fertnstert.2016.01.011
   PubMed Web of Science ®Google Scholar
• Ziebe, S., Petersen, K., Lindenberg, S., Andersen, A. G., Gabrielsen, A., & Andersen, A. N. (1997). Embryo morphology or cleavage stage: how to select the best embryos for transfer after in-vitro fertilization. Human Reproduction (Oxford, England), 12(7), 1545–1549. https://doi.org/https://doi.org/10.1093/humrep/12.7.1545
   PubMed Web of Science ®Google Scholar