Morphokinetic prediction of embryo viability in cattle

Satoshi Sugimura; Tatsuma Yao; Satoko Matoba; Kazuo Yamagata; Kei Imai

doi:10.1071/RD24139

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Morphokinetic prediction of embryo viability in cattle

Satoshi Sugimura ^A ^* , Tatsuma Yao ^B ^C , Satoko Matoba ^D , Kazuo Yamagata ^B and Kei Imai ^E

+ Author Affiliations

- Author Affiliations

^A Department of Biological Production, Tokyo University of Agriculture and Technology, Tokyo, Japan.

^B Faculty of Biology-Oriented Science and Technology (BOST), Kindai University, Wakayama, Japan.

^C Research and Development Center, Fuso Pharmaceutical Industries, Ltd., Osaka, Japan.

^D National Livestock Breeding Center, Fukushima, Japan.

^E Department of Sustainable Agriculture, Rakuno Gakuen University, Hokkaido, Japan.

^* Correspondence to: satoshis@cc.tuat.ac.jp

Reproduction, Fertility and Development 37, RD24139 https://doi.org/10.1071/RD24139

Abstract

Conventionally, bovine in vitro-produced (IVP) embryos for transfer are morphologically evaluated at day 7–8 of embryo culture, as recommended by the International Embryo Technology Society (IETS). However, this method is subjective, relying on the percentage of degenerated cells and developmental stage, leading to variability depending on the operator. In contrast, we have implemented a novel selection system for bovine IVP blastocysts using time-lapse monitoring in specially developed microwell culture dishes (LinKID micro25). This approach allows for continuous tracking of individual embryo development. Additionally, we have advanced live-cell imaging technology to observe nuclear and chromosomal dynamics during early embryogenesis, identifying prognostic factors indicative of viability post-transfer. Integrating these factors has significantly improved conception rates compared to conventional morphological evaluation. This review discusses morphokinetics relevant to viability and our innovative selection system, which enable accurate prediction of embryo viability after transfer in cattle.

Keywords: bovine, embryo, first cleavage, in vitro production, live-cell imaging, morphokinetics, time-lapse monitoring, viability prediction.

References

Angel-Velez D, De Coster T, Azari-Dolatabad N, Fernández-Montoro A, Benedetti C, Pavani K, Van Soom A, Bogado Pascottini O, Smits K (2023) Embryo morphokinetics derived from fresh and vitrified bovine oocytes predict blastocyst development and nuclear abnormalities. Scientific Reports 13(1), 4765.
| Crossref | Google Scholar |

Bamford T, Barrie A, Montgomery S, Dhillon-Smith R, Campbell A, Easter C, Coomarasamy A (2022) Morphological and morphokinetic associations with aneuploidy: a systematic review and meta-analysis. Human Reproduction Update 28(5), 656-686.
| Crossref | Google Scholar | PubMed |

Bo GA, Mapletoft RJ (2013) Evaluation and classification of bovine embryos. Animal Reproduction 10, 344-348.
| Google Scholar |

Bolton H, Graham SJL, Van der Aa N, Kumar P, Theunis K, Fernandez Gallardo E, Voet T, Zernicka-Goetz M (2016) Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential. Nature Communications 7, 11165.
| Crossref | Google Scholar | PubMed |

De Coster T, Masset H, Tšuiko O, Catteeuw M, Zhao Y, Dierckxsens N, Aparicio AL, Dimitriadou E, Debrock S, Peeraer K, de Ruijter-Villani M, Smits K, Van Soom A, Vermeesch JR (2022) Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts. Genome Biology 23(1), 201.
| Crossref | Google Scholar | PubMed |

Destouni A, Zamani Esteki M, Catteeuw M, Tšuiko O, Dimitriadou E, Smits K, Kurg A, Salumets A, Van Soom A, Voet T, Vermeesch JR (2016) Zygotes segregate entire parental genomes in distinct blastomere lineages causing cleavage-stage chimerism and mixoploidy. Genome Research 26(5), 567-578.
| Crossref | Google Scholar | PubMed |

Farin PW, Britt JH, Shaw DW, Slenning BD (1995) Agreement among evaluators of bovine embryos produced in vivo or in vitro. Theriogenology 44(3), 339-349.
| Crossref | Google Scholar | PubMed |

Fenwick J, Platteau P, Murdoch AP, Herbert M (2002) Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro. Human Reproduction 17(2), 407-412.
| Crossref | Google Scholar |

Ferry L, Mermillod P, Massip A, Dessy F (1994) Bovine embryos cultured in serum-poor oviduct-conditioned medium need cooperation to reach the blastocyst stage. Theriogenology 42(3), 445-453.
| Crossref | Google Scholar | PubMed |

Fujita T, Umeki H, Shimura H, Kugumiya K, Shiga K (2006) Effect of group culture and embryo-culture conditioned medium on development of bovine embryos. Journal of Reproduction and Development 52(1), 137-142.
| Crossref | Google Scholar | PubMed |

Gjørret JO, Knijn HM, Dieleman SJ, Avery B, Larsson LI, Maddox-Hyttel P (2003) Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biology of Reproduction 69(4), 1193-1200.
| Crossref | Google Scholar | PubMed |

Gopichandran N, Leese HJ (2006) The effect of paracrine/autocrine interactions on the in vitro culture of bovine preimplantation embryos. Reproduction 131(2), 269-277.
| Crossref | Google Scholar | PubMed |

Han YM, Wang WH, Abeydeera LR, Petersen AL, Kim JH, Murphy C, Day BN, Prather RS (1999) Pronuclear location before the first cell division determines ploidy of polyspermic pig embryos. Biology of Reproduction 61(5), 1340-1346.
| Crossref | Google Scholar | PubMed |

Hardarson T, Hanson C, Sjögren A, Lundin K (2001) Human embryos with unevenly sized blastomeres have lower pregnancy and implantation rates: indications for aneuploidy and multinucleation. Human Reproduction 16(2), 313-318.
| Crossref | Google Scholar | PubMed |

Hare WC, Singh EL, Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D, Bilton RJ, Trounson AO (1980) Chromosomal analysis of 159 bovine embryos collected 12 to 18 days after estrus. Canadian Journal of Genetics and Cytology 22(4), 615-626.
| Crossref | Google Scholar | PubMed |

Hengstschläger M (2023) Artificial intelligence as a door opener for a new era of human reproduction. Human Reproduction Open 2023(4), hoad043.
| Crossref | Google Scholar |

Hoelker M, Rings F, Lund Q, Ghanem N, Phatsara C, Griese J, Schellander K, Tesfaye D (2009) Effect of the microenvironment and embryo density on developmental characteristics and gene expression profile of bovine preimplantative embryos cultured in vitro. Reproduction 137(3), 415-425.
| Crossref | Google Scholar | PubMed |

Holm P, Booth PJ, Callesen H (2002) Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 123(4), 553-565.
| Crossref | Google Scholar | PubMed |

Khurana NK, Niemann H (2000) Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 54(5), 741-756.
| Crossref | Google Scholar | PubMed |

Koo DB, Kang YK, Choi YH, Park JS, Kim HN, Oh KB, Son DS, Park H, Lee KK, Han YM (2002) Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biology of Reproduction 67(2), 487-492.
| Crossref | Google Scholar | PubMed |

Koyama H, Suzuki H, Yang X, Jiang S, Foote RH (1994) Analysis of polarity of bovine and rabbit embryos by scanning electron microscopy. Biology of Reproduction 50(1), 163-170.
| Crossref | Google Scholar | PubMed |

Larson MA, Kubisch HM (1999) The effects of group size on development and interferon-tau secretion by in-vitro fertilized and cultured bovine blastocysts. Human Reproduction 14(8), 2075-2079.
| Crossref | Google Scholar | PubMed |

Lequarre AS, Marchandise J, Moreau B, Massip A, Donnay I (2003) Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition. Biology of Reproduction 69(5), 1707-1713.
| Crossref | Google Scholar | PubMed |

Liu Y, Chapple V, Roberts P, Matson P (2014) Prevalence, consequence, and significance of reverse cleavage by human embryos viewed with the use of the Embryoscope time-lapse video system. Fertility and Sterility 102(5), 1295-1300.e1292.
| Crossref | Google Scholar |

Lonergan P, Khatir H, Piumi F, Rieger D, Humblot P, Boland MP (1999) Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. Journal of Reproduction and Fertility 117(1), 159-167.
| Crossref | Google Scholar | PubMed |

Magata F (2023) Time-lapse monitoring technologies for the selection of bovine in vitro fertilized embryos with high implantation potential. Journal of Reproduction and Development 69(2), 57-64.
| Crossref | Google Scholar | PubMed |

Magli MC, Gianaroli L, Ferraretti AP, Lappi M, Ruberti A, Farfalli V (2007) Embryo morphology and development are dependent on the chromosomal complement. Fertility and Sterility 87(3), 534-541.
| Crossref | Google Scholar | PubMed |

Mashiko D, Ikeda Z, Yao T, Tokoro M, Fukunaga N, Asada Y, Yamagata K (2020) Chromosome segregation error during early cleavage in mouse pre-implantation embryo does not necessarily cause developmental failure after blastocyst stage. Scientific Reports 10(1), 854.
| Crossref | Google Scholar | PubMed |

Massip A, Mulnard J, Vanderzwalmen P, Hanzen C, Ectors F (1982) The behaviour of cow blastocyst in vitro: cinematographic and morphometric analysis. Journal of Anatomy 134(Pt 2), 399-405.
| Google Scholar | PubMed |

Matoba S, Fair T, Lonergan P (2010) Maturation, fertilisation and culture of bovine oocytes and embryos in an individually identifiable manner: a tool for studying oocyte developmental competence. Reproduction, Fertility and Development 22(5), 839-851.
| Crossref | Google Scholar | PubMed |

McCoy RC, Demko ZP, Ryan A, Banjevic M, Hill M, Sigurjonsson S, Rabinowitz M, Petrov DA (2015) Evidence of selection against complex mitotic-origin aneuploidy during preimplantation development. PLoS Genetics 11(10), e1005601.
| Crossref | Google Scholar | PubMed |

Mohan M, Hurst AG, Malayer JR (2004) Global gene expression analysis comparing bovine blastocysts flushed on day 7 or produced in vitro. Molecular Reproduction and Development 68(3), 288-298.
| Crossref | Google Scholar | PubMed |

Nagai H, Okada M, Nagai Y, Sakuraba Y, Okae H, Suzuki R, Sugimura S (2021) Abnormal cleavage is involved in the self-correction of bovine preimplantation embryos. Biochemical and Biophysical Research Communications 562, 76-82.
| Crossref | Google Scholar | PubMed |

Rabaglino MB, Salilew-Wondim D, Zolini A, Tesfaye D, Hoelker M, Lonergan P, Hansen PJ (2023) Machine-learning methods applied to integrated transcriptomic data from bovine blastocysts and elongating conceptuses to identify genes predictive of embryonic competence. FASEB Journal 37(3), e22809.
| Crossref | Google Scholar | PubMed |

Shoukir Y, Campana A, Farley T, Sakkas D (1997) Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Human Reproduction 12(7), 1531-1536.
| Crossref | Google Scholar | PubMed |

Stokes PJ, Abeydeera LR, Leese HJ (2005) Development of porcine embryos in vivo and in vitro; evidence for embryo ‘cross talk’ in vitro. Developmental Biology 284(1), 62-71.
| Crossref | Google Scholar | PubMed |

Stringfellow DA, Givens SM (2010) ‘Manusal of the international embryo transfer society,’ 4th edn. (International Embryo Transfer)

Sugimura S, Akai T, Somfai T, Hirayama M, Aikawa Y, Ohtake M, Hattori H, Kobayashi S, Hashiyada Y, Konishi K, Imai K (2010) Time-lapse cinematography-compatible polystyrene-based microwell culture system: a novel tool for tracking the development of individual bovine embryos. Biology of Reproduction 83(6), 970-978.
| Crossref | Google Scholar | PubMed |

Sugimura S, Akai T, Hashiyada Y, Somfai T, Inaba Y, Hirayama M, Yamanouchi T, Matsuda H, Kobayashi S, Aikawa Y, Ohtake M, Kobayashi E, Konishi K, Imai K (2012) Promising system for selecting healthy in vitro-fertilized embryos in cattle. PLoS ONE 7(5), e36627.
| Crossref | Google Scholar | PubMed |

Sugimura S, Akai T, Hashiyada Y, Aikawa Y, Ohtake M, Matsuda H, Kobayashi S, Kobayashi E, Konishi K, Imai K (2013) Effect of embryo density on in vitro development and gene expression in bovine in vitro-fertilized embryos cultured in a microwell system. Journal of Reproduction and Development 59(2), 115-122.
| Crossref | Google Scholar | PubMed |

Sugimura S, Akai T, Imai K (2017) Selection of viable in vitro-fertilized bovine embryos using time-lapse monitoring in microwell culture dishes. Journal of Reproduction and Development 63(4), 353-357.
| Crossref | Google Scholar | PubMed |

Suzuki R, Yao T, Okada M, Nagai H, Khurchabilig A, Kobayashi J, Yamagata K, Sugimura S (2023) Direct cleavage during the first mitosis is a sign of abnormal fertilization in cattle. Theriogenology 200, 96-105.
| Crossref | Google Scholar | PubMed |

Tšuiko O, Catteeuw M, Zamani Esteki M, Destouni A, Bogado Pascottini O, Besenfelder U, Havlicek V, Smits K, Kurg A, Salumets A, D’Hooghe T, Voet T, Van Soom A, Robert Vermeesch J (2017) Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos. Hum Reprod 32(11), 2348-2357.
| Crossref | Google Scholar | PubMed |

Vajta G, Peura TT, Holm P, Páldi A, Greve T, Trounson AO, Callesen H (2000) New method for culture of zona-included or zona-free embryos: the Well of the Well (WOW) system. Molecular Reproduction and Development 55(3), 256-264.
| Crossref | Google Scholar | PubMed |

Vanneste E, Voet T, Melotte C, Debrock S, Sermon K, Staessen C, Liebaers I, Fryns JP, D’Hooghe T, Vermeesch JR (2009) What next for preimplantation genetic screening? High mitotic chromosome instability rate provides the biological basis for the low success rate. Human Reproduction 24(11), 2679-2682.
| Crossref | Google Scholar | PubMed |

Viuff D, Rickords L, Offenberg H, Hyttel P, Avery B, Greve T, Olsaker I, Williams JL, Callesen H, Thomsen PD (1999) A high proportion of bovine blastocysts produced in vitro are mixoploid. Biology of Reproduction 60(6), 1273-1278.
| Crossref | Google Scholar | PubMed |

Vutyavanich T, Saeng-Anan U, Sirisukkasem S, Piromlertamorn W (2011) Effect of embryo density and microdrop volume on the blastocyst development of mouse two-cell embryos. Fertility and Sterility 95(4), 1435-1439.
| Crossref | Google Scholar | PubMed |

Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, Reijo Pera RA (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nature Biotechnology 28(10), 1115-1121.
| Crossref | Google Scholar | PubMed |

Yang M, Rito T, Metzger J, Naftaly J, Soman R, Hu J, Albertini DF, Barad DH, Brivanlou AH, Gleicher N (2021) Depletion of aneuploid cells in human embryos and gastruloids. Nature Cell Biology 23(4), 314-321.
| Crossref | Google Scholar | PubMed |

Yang T, Yuan X, Xue Q, Sun L, Xu T, Chen Y, Shi D, Li X (2023) Comparison of symmetrical and asymmetrical cleavage 2-cell embryos of porcine by Smart-seq2. Theriogenology 210, 221-226.
| Crossref | Google Scholar | PubMed |

Yao T, Suzuki R, Furuta N, Suzuki Y, Kabe K, Tokoro M, Sugawara A, Yajima A, Nagasawa T, Matoba S, Yamagata K, Sugimura S (2018) Live-cell imaging of nuclear-chromosomal dynamics in bovine in vitro fertilised embryos. Scientific Reports 8(1), 7460.
| Crossref | Google Scholar | PubMed |

Yao T, Ueda A, Khurchabilig A, Mashiko D, Tokoro M, Nagai H, Sho T, Matoba S, Yamagata K, Sugimura S (2022) Micronucleus formation during early cleavage division is a potential hallmark of preimplantation embryonic loss in cattle. Biochemical and Biophysical Research Communications 617(Pt 2), 25-32.
| Crossref | Google Scholar | PubMed |

Zhan Q, Ye Z, Clarke R, Rosenwaks Z, Zaninovic N (2016) Direct unequal cleavages: embryo developmental competence, genetic constitution and clinical outcome. PLoS ONE 11(12), e0166398.
| Crossref | Google Scholar | PubMed |

Ziebe S, Petersen K, Lindenberg S, Andersen AG, Gabrielsen A, Andersen AN (1997) Embryo morphology or cleavage stage: how to select the best embryos for transfer after in-vitro fertilization. Human Reproduction 12(7), 1545-1549.
| Crossref | Google Scholar | PubMed |