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Morphometric and morphokinetic differences in the sperm- and oocyte-originated pronuclei of male and female human zygotes: a time-lapse study

  • Embryo Biology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

To study the morphometric and morphokinetic profiles of pronuclei (PN) between male and female human zygotes.

Method(s)

This retrospective cohort study included 94 consecutive autologous single day 5 transfer cycles leading to a singleton live birth. All oocytes were placed in the EmbryoScope + incubator post-sperm injection with all annotations performed retrospectively by one embryologist (L-SO). Timing parameters included 2nd polar body extrusion (tPB2), sperm-originated PN (tSPNa) or oocyte-originated PN (tOPNa) appearance, and PN fading (tPNF). Morphometrics were evaluated at 8 (stage 1), 4 (stage 2), and 0 h before PNF (stage 3), measuring PN area (um2), PN juxtaposition, and nucleolar precursor bodies (NPB) arrangement.

Results

Male zygotes had longer time intervals of tPB2_tSPNa than female zygotes (4.8 ± 0.2 vs 4.2 ± 0.1 h, OR = 1.442, 95% CI 1.009–2.061, p = 0.044). SPN increased in size from stage 1 through 2 to 3 (435.3 ± 7.2, 506.7 ± 8.0, and 556.3 ± 8.9 um2, p = 0.000) and OPN did similarly (399.0 ± 6.1, 464.3 ± 6.7, and 513.8 ± 6.5 um2, p = 0.000), with SPN being significantly larger than OPN at each stage (p < 0.05 respectively). More male than female zygotes reached central PN juxtaposition at stage 1 (76.7% vs 51.0%, p = 0.010), stage 2 (97.7% vs 86.3%, p = 0.048), and stage 3 (97.7% vs 86.3%, p = 0.048). More OPN showed aligned NPBs than in SPN at stage 1 only (44.7% vs 28.7%, p = 0.023).

Conclusion(s)

Embryos with different sexes display different morphokinetic and morphometric features at the zygotic stage. Embryo selection using such parameters may lead to unbalanced sex ratio in resulting offspring.

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References

  1. Alpha Scientists in Reproductive M, Embryology ESIGo.The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 2011; 26:1270–1283.

  2. Cutting R. Single embryo transfer for all. Best Pract Res Clin Obstet Gynaecol. 2018;53:30–7.

    Article  PubMed Central  Google Scholar 

  3. McLernon DJ, Harrild K, Bergh C, Davies MJ, de Neubourg D, Dumoulin JC, et al. Clinical effectiveness of elective single versus double embryo transfer: meta-analysis of individual patient data from randomised trials. BMJ. 2010;341:c6945.

    Article  CAS  PubMed Central  Google Scholar 

  4. Gardner DK, Schoolcraft WB, Wagley L, Schlenker T, Stevens J, Hesla J. A prospective randomized trial of blastocyst culture and transfer in in-vitro fertilization. Hum Reprod. 1998;13:3434–40.

    Article  CAS  PubMed Central  Google Scholar 

  5. Kemper JM, Wang R, Rolnik DL, Mol BW. Preimplantation genetic testing for aneuploidy: are we examining the correct outcomes? Hum Reprod. 2020;35:2408–12.

    Article  PubMed Central  Google Scholar 

  6. Dar S, Lazer T, Shah PS, Librach CL. Neonatal outcomes among singleton births after blastocyst versus cleavage stage embryo transfer: a systematic review and meta-analysis. Hum Reprod Update. 2014;20:439–48.

    Article  CAS  PubMed Central  Google Scholar 

  7. Castillo CM, Harper J, Roberts SA, O’Neill HC, Johnstone ED, Brison DR. The impact of selected embryo culture conditions on ART treatment cycle outcomes: a UK national study. Hum Reprod Open 2020;2020:hoz031.

  8. Mani S, Mainigi M. Embryo culture conditions and the epigenome. Semin Reprod Med. 2018;36:211–20.

    Article  CAS  PubMed Central  Google Scholar 

  9. Martins WP, Nastri CO, Rienzi L, van der Poel SZ, Gracia C, Racowsky C. Blastocyst vs cleavage-stage embryo transfer: systematic review and meta-analysis of reproductive outcomes. Ultrasound Obstet Gynecol. 2017;49:583–91.

    Article  CAS  PubMed Central  Google Scholar 

  10. Glujovsky D, Farquhar C, Quinteiro Retamar AM, Alvarez Sedo CR, Blake D. Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev. 2016:CD002118.

  11. Liu Y, Chapple V, Feenan K, Roberts P, Matson P. 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. Fertil Steril. 2015;103:1485-1491.e1481.

    Article  Google Scholar 

  12. -.Time-lapse deselection model for human day 3 in vitro fertilization embryos: the combination of qualitative and quantitative measures of embryo growth. Fertil Steril. 2016;105:656–662 e651.

  13. Liu Y, Chapple V, Roberts P, Matson P. Prevalence, consequence, and significance of reverse cleavage by human embryos viewed with the use of the Embryoscope time-lapse video system. Fertil Steril. 2014;102:1295-1300.e1292.

    Article  Google Scholar 

  14. Barberet J, Bruno C, Valot E, Antunes-Nunes C, Jonval L, Chammas J, et al. Can novel early non-invasive biomarkers of embryo quality be identified with time-lapse imaging to predict live birth? Hum Reprod. 2019;34:1439–49.

    Article  CAS  PubMed Central  Google Scholar 

  15. Otsuki J, Iwasaki T, Enatsu N, Katada Y, Furuhashi K, Shiotani M. Noninvasive embryo selection: kinetic analysis of female and male pronuclear development to predict embryo quality and potential to produce live birth. Fertil Steril. 2019;112:874–81.

    Article  CAS  Google Scholar 

  16. Coticchio G, Mignini Renzini M, Novara PV, Lain M, De Ponti E, Turchi D, et al. Focused time-lapse analysis reveals novel aspects of human fertilization and suggests new parameters of embryo viability. Hum Reprod. 2018;33:23–31.

    Article  CAS  PubMed Central  Google Scholar 

  17. Inoue T, Taguchi S, Uemura M, Tsujimoto Y, Miyazaki K, Yamashita Y. Migration speed of nucleolus precursor bodies in human male pronuclei: a novel parameter for predicting live birth. J Assist Reprod Genet. 2021;38:1725–36.

    Article  Google Scholar 

  18. Otsuki J, Iwasaki T, Tsuji Y, Katada Y, Sato H, Tsutsumi Y, et al. 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. Reprod Med Biol. 2017;16:200–5.

    Article  CAS  PubMed Central  Google Scholar 

  19. Bronet F, Nogales MC, Martinez E, Ariza M, Rubio C, Garcia-Velasco JA et al.Is there a relationship between time-lapse parameters and embryo sex? Fertil Steril 2015; 103: 396–401 e392.

  20. Watson K, Korman I, Liu Y, Zander-Fox D. Live birth in a complete zona-free patient: a case report. J Assist Reprod Genet. 2021;38:1109–13.

    Article  PubMed Central  Google Scholar 

  21. Gardner DK, Schoolcraft WB. Culture and transfer of human blastocysts. Curr Opin Obstet Gynecol. 1999;11:307–11.

    Article  CAS  PubMed Central  Google Scholar 

  22. Ciray HN, Campbell A, Agerholm IE, 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. 2014;29:2650–60.

    Article  Google Scholar 

  23. Bodri D, Kawachiya S, Sugimoto T, Yao Serna J, Kato R, Matsumoto T. Time-lapse variables and embryo gender: a retrospective analysis of 81 live births obtained following minimal stimulation and single embryo transfer. J Assist Reprod Genet. 2016;33:589–96.

    Article  PubMed Central  Google Scholar 

  24. Huang B, Ren X, Zhu L, Wu L, Tan H, Guo N, et al. Is differences in embryo morphokinetic development significantly associated with human embryo sex?dagger. Biol Reprod. 2019;100:618–23.

    Article  PubMed Central  Google Scholar 

  25. Serdarogullari M, Findikli N, Goktas C, Sahin O, Ulug U, Yagmur E, et al. Comparison of gender-specific human embryo development characteristics by time-lapse technology. Reprod Biomed Online. 2014;29:193–9.

    Article  PubMed Central  Google Scholar 

  26. Payne D, Flaherty SP, Barry MF, Matthews CD. Preliminary observations on polar body extrusion and pronuclear formation in human oocytes using time-lapse video cinematography. Hum Reprod. 1997;12:532–41.

    Article  CAS  PubMed Central  Google Scholar 

  27. Aguilar J, Motato Y, Escriba MJ, Ojeda M, Munoz E, Meseguer M. The human first cell cycle: impact on implantation. Reprod Biomed Online. 2014;28:475–84.

    Article  PubMed Central  Google Scholar 

  28. Liu Y, Chapple V, Feenan K, Roberts P, Matson P. Time-lapse videography of human embryos: using pronuclear fading rather than insemination in IVF and ICSI cycles removes inconsistencies in time to reach early cleavage milestones. Reprod Biol. 2015;15:122–5.

    Article  PubMed Central  Google Scholar 

  29. Gamiz P, Rubio C, de los Santos MJ, Mercader A, Simon C, Remohi J et al.The effect of pronuclear morphology on early development and chromosomal abnormalities in cleavage-stage embryos. Hum Reprod 2003; 18: 2413–2419.

  30. Tesarik J, Greco E. The probability of abnormal preimplantation development can be predicted by a single static observation on pronuclear stage morphology. Hum Reprod. 1999;14:1318–23.

    Article  CAS  Google Scholar 

  31. Coticchio G, Borini A, Albertini DF. The slippery slope antedating syngamy: pronuclear activity in preparation for the first cleavage. J Assist Reprod Genet. 2021;38:1721–3.

    Article  Google Scholar 

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Authors and Affiliations

  1. Monash IVF Gold Coast, 2 Short Street, Southport, QLD, L34215, Australia

    Lee-Sarose Orevich, Kate Watson, Kee Ong, Irving Korman & Yanhe Liu

  2. Monash IVF Auchenflower, Auchenflower, QLD, Australia

    Ross Turner & Yanhe Liu

  3. Monash IVF Rockhampton, Rockhampton, QLD, Australia

    David Shaker & Yanhe Liu

  4. Rural Clinical School, University of Queensland, Brisbane, QLD, Australia

    David Shaker

  5. School of Human Sciences, University of Western Australia, Crawley, WA, Australia

    Yanhe Liu

  6. School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA, Australia

    Yanhe Liu

  7. School of Health Sciences and Medicine, Bond University, Robina, QLD, Australia

    Yanhe Liu

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  1. Lee-Sarose Orevich
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  2. Kate Watson
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Correspondence to Lee-Sarose Orevich.

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Orevich, LS., Watson, K., Ong, K. et al. Morphometric and morphokinetic differences in the sperm- and oocyte-originated pronuclei of male and female human zygotes: a time-lapse study. J Assist Reprod Genet 39, 97–106 (2022). https://doi.org/10.1007/s10815-021-02366-z

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  • DOI: https://doi.org/10.1007/s10815-021-02366-z

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