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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Speed of in vitro embryo development affects the likelihood of foaling and the foal sex ratio*

A. Claes https://orcid.org/0000-0003-2209-7598 A D , J. Cuervo-Arango https://orcid.org/0000-0002-6939-017X A , S. Colleoni B , G. Lazzari B C , C. Galli B C and T. A. Stout https://orcid.org/0000-0001-5321-8095 A
+ Author Affiliations
- Author Affiliations

A Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 112, 3584 CM Utrecht, The Netherlands.

B Avantea, Laboratory of Reproductive Technologies, Via Porcellasco, 7/F, 26100 Cremona CR, Italy.

C Fondazione Avantea, Via Cabrini, 12 26100 Cremona CR, Italy.

D Corresponding author. Email: a.claes@uu.nl

Reproduction, Fertility and Development 32(5) 468-473 https://doi.org/10.1071/RD19298
Submitted: 24 July 2019  Accepted: 19 November 2019   Published: 10 February 2020

Abstract

The success of in vitro embryo production (IVEP) in horses has increased considerably during recent years, but little is known about the effect of the speed of in vitro embryo development. Blastocysts (n = 390) were produced by intracytoplasmic sperm injection of IVM oocytes from warmblood mares, cryopreserved, thawed and transferred into recipient mares on Days 3, 4, 5 or 6 after ovulation. The time required for in vitro-produced (IVP) embryos to reach the blastocyst stage was recorded (Day 7 vs Day 8). The likelihood of foaling was affected by the speed of in vitro embryo development and recipient day after ovulation at transfer. The odds ratio for foaling was ~0.63 for transfer of Day 8 (46%) compared with Day 7 (56%) IVP blastocysts. The highest likelihood of pregnancy (72%) and foaling (60%) was observed when IVP blastocysts were transferred to recipient mares on Day 4 after ovulation. Finally, the sex (colt : filly) ratio was higher after transfer of Day 7 (71% : 29%) than Day 8 (54% : 46%) IVP blastocysts, suggesting that the speed of embryo development is sex dependent. In conclusion, the speed of in vitro embryo development in our IVEP system affects the likelihood of foaling and the sex of the foal.

Graphical Abstract Image

Additional keywords: equine, intracytoplasmic sperm injection (ICSI), in vitro embryo production (IVEP), pregnancy.


References

Agca, Y., Monson, R. L., Northey, D. L., Abas Mazni, O., Schaefer, D. M., and Rutledge, J. J. (1998). Transfer of fresh and cryopreserved IVP bovine embryos: normal calving, birth weight and gestation lengths. Theriogenology 50, 147–162.
Transfer of fresh and cryopreserved IVP bovine embryos: normal calving, birth weight and gestation lengths.Crossref | GoogleScholarGoogle Scholar | 10734482PubMed |

Alomar, M., Tasiaux, H., Remacle, S., George, F., Paul, D., and Donnay, I. (2008). Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls. Anim. Reprod. Sci. 107, 48–61.
Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls.Crossref | GoogleScholarGoogle Scholar | 17629423PubMed |

Avery, B., Madison, V., and Greve, T. (1991). Sex and development in bovine in-vitro fertilized embryos. Theriogenology 35, 953–963.
Sex and development in bovine in-vitro fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 16726963PubMed |

Barash, O. O., Ivani, K. A., Willman, S. P., Rosenbluth, E. M., Wachs, D. S., Hinckley, M. D., Pittenger Reid, S., and Weckstein, L. N. (2017). Association between growth dynamics, morphological parameters, the chromosomal status of the blastocysts, and clinical outcomes in IVF PGS cycles with single embryo transfer. J. Assist. Reprod. Genet. 34, 1007–1016.
Association between growth dynamics, morphological parameters, the chromosomal status of the blastocysts, and clinical outcomes in IVF PGS cycles with single embryo transfer.Crossref | GoogleScholarGoogle Scholar | 28560610PubMed |

Carnevale, E. M., and Sessions, D. R. (2012). in vitro production of equine embryos. J. Equine Vet. Sci. 32, 367–371.
in vitro production of equine embryos.Crossref | GoogleScholarGoogle Scholar |

Chen, J., Albini, D., and Jain, J. K. (2014). Human embryonic aneuploidy delays blastocyst formation and development. Fertil. Steril. 102, e206.
Human embryonic aneuploidy delays blastocyst formation and development.Crossref | GoogleScholarGoogle Scholar | 25256925PubMed |

Claes, A., Galli, C., Colleoni, S., Necchi, D., Lazzari, G., Deelen, C., Beitsma, M., and Stout, T. A. (2016). Factors influencing oocyte recovery and in-vitro production of equine embryos in a commercial OPU/ICSI program. J. Equine Vet. Sci. 41, 68–69.
Factors influencing oocyte recovery and in-vitro production of equine embryos in a commercial OPU/ICSI program.Crossref | GoogleScholarGoogle Scholar |

Claes, A., Cuervo-Arango, J., van den Broek, J., Galli, C., Colleoni, S., Lazzari, G., Deelen, C., Beitsma, M., and Stout, T. A. (2019). Factors affecting the likelihood of pregnancy and embryonic loss after transfer of cryopreserved in vitro produced equine embryos. Equine Vet. J. 51, 446–450.
Factors affecting the likelihood of pregnancy and embryonic loss after transfer of cryopreserved in vitro produced equine embryos.Crossref | GoogleScholarGoogle Scholar | 30269336PubMed |

Colleoni, S., Lagutina, I., Lazzari, G., Rodriguez-Martinez, H., Galli, C., and Morrell, J. M. (2011). New methods for selecting stallion spermatozoa for assisted reproduction. J. Equine Vet. Sci. 31, 536–541.
New methods for selecting stallion spermatozoa for assisted reproduction.Crossref | GoogleScholarGoogle Scholar |

Cuervo-Arango, J., Claes, A., and Stout, T. A. (2018a). Effect of embryo transfer technique on the likelihood of pregnancy in the mare: a comparison of conventional and Wilsher’s forceps-assisted transfer. Vet. Rec. 183, 323.
Effect of embryo transfer technique on the likelihood of pregnancy in the mare: a comparison of conventional and Wilsher’s forceps-assisted transfer.Crossref | GoogleScholarGoogle Scholar | 29798842PubMed |

Cuervo-Arango, J., Claes, A., and Stout, T. A. (2018b). Effect of embryo–recipient synchrony on post-ET survival of in vivo and in vitro-produced equine embryos. J. Equine Vet. Sci. 66, 163–164.
Effect of embryo–recipient synchrony on post-ET survival of in vivo and in vitro-produced equine embryos.Crossref | GoogleScholarGoogle Scholar |

Galli, C., Duchi, R., Colleoni, S., Lagutina, I., and Lazzari, G. (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81, 138–151.
Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice.Crossref | GoogleScholarGoogle Scholar | 24274418PubMed |

Gutiérrez-Adán, A., Granados, J., Pintado, B., and Fuente, D. L. (2001). Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod. Fertil. Dev. 13, 361–365.
Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 11833931PubMed |

Gutiérrez-Adán, A., White, C. R., Van Soom, A., and Mann, R. (2015). Why we should not select the faster embryo: lessons from mice and cattle. Reprod. Fertil. Dev. 27, 765–775.
Why we should not select the faster embryo: lessons from mice and cattle.Crossref | GoogleScholarGoogle Scholar | 25209560PubMed |

Kimura, K., Spate, L. D., Green, M. P., and Roberts, R. M. (2005). Effects of d-glucose concentration, d-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol. Reprod. Dev. 72, 201–207.
Effects of d-glucose concentration, d-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 15968626PubMed |

Kuhl, J., Stock, K. F., Wulf, M., and Aurich, C. (2015). Maternal lineage of warmblood mares contributes to variation of gestation length and bias of foal sex ratio. PLoS One 10, e0139358.
Maternal lineage of warmblood mares contributes to variation of gestation length and bias of foal sex ratio.Crossref | GoogleScholarGoogle Scholar | 26436555PubMed |

Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.Crossref | GoogleScholarGoogle Scholar | 12193383PubMed |

Lewin, A., Schenker, J., Safran, A., Zigelman, N., Avrech, O., Abramov, Y., Friedler, S., and Reubinoff, B. E. (1994). Embryo growth rate in vitro as an indicator of embryo quality in IVF cycles. J. Assist. Reprod. Genet. 11, 500–503.
Embryo growth rate in vitro as an indicator of embryo quality in IVF cycles.Crossref | GoogleScholarGoogle Scholar | 7663105PubMed |

Lundin, K., Bergh, C., and Hardarson, T. (2001). Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum. Reprod. 16, 2652–2657.
Early embryo cleavage is a strong indicator of embryo quality in human IVF.Crossref | GoogleScholarGoogle Scholar | 11726590PubMed |

Marei, W. F. A., Khalil, W. A., Pushpakumara, A. P. G., El-Harairy, M. A., Abo El-Atta, A. M. A., Wathes, D. C., and Fouladi-Nashta, A. (2018). Polyunsaturated fatty acids influence offspring sex ratio in cows. Int. J. Vet. Sci. Med. 6, S36–S40.
Polyunsaturated fatty acids influence offspring sex ratio in cows.Crossref | GoogleScholarGoogle Scholar |

McCue, P. M., Ferris, R. A., Stokes, J., Hatzel, J., Trundell, D., and Carnevale, E. M. (2016). Pregnancy rate and pregnancy loss after transfer of in vivo or in vitro derived equine embryos. J. Equine Vet. Sci. 41, 70.
Pregnancy rate and pregnancy loss after transfer of in vivo or in vitro derived equine embryos.Crossref | GoogleScholarGoogle Scholar |

Peippo, J., Kurkilahti, M., and Bredbacka, P. (2001). Developmental kinetics of in vitro produced bovine embryos: the effect of sex, glucose and exposure to time-lapse environment. Zygote 9, 105–113.
Developmental kinetics of in vitro produced bovine embryos: the effect of sex, glucose and exposure to time-lapse environment.Crossref | GoogleScholarGoogle Scholar | 11358318PubMed |

Peippo, J., Farazmand, A., Kurkilahti, M., Markkula, M., Basrur, P. K., and King, W. A. (2002). Sex-chromosome linked gene expression in in-vitro produced bovine embryos. Mol. Hum. Reprod. 8, 923–929.
Sex-chromosome linked gene expression in in-vitro produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 12356942PubMed |

Reichenbach, H. D., Liebrich, J., Berg, U., and Brem, G. (1992). Pregnancy rates and births after unilateral transfer of bovine embryos produced in vitro. J. Reprod. Fertil. 95, 363–370.
Pregnancy rates and births after unilateral transfer of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1517994PubMed |

Shah, J., Vanijgul, C., Chauhan, S., Dunn, R. D., and Wun, W. A. (2016). Comparison of aneuploid rates among Day 5, 6, and 7 biopsied blastocysts. Fertil. Steril. 106, e26.
Comparison of aneuploid rates among Day 5, 6, and 7 biopsied blastocysts.Crossref | GoogleScholarGoogle Scholar |

Taylor, T. H., Patrick, J. L., Gitlin, S. A., Wilson, J. M., Crain, J. L., and Griffin, D. K. (2014). Comparison of aneuploidy, pregnancy and live birth rates between Day 5 and Day 6 blastocysts. Reprod. Biomed. Online 29, 305–310.
Comparison of aneuploidy, pregnancy and live birth rates between Day 5 and Day 6 blastocysts.Crossref | GoogleScholarGoogle Scholar | 25043891PubMed |

van Soom, A., Ysebaert, M., and de Kruif, A. (1997). Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol. Reprod. Dev. 47, 47–56.
Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 9110314PubMed |

Xu, K. P., Yadav, B. R., King, W. A., and Betteridge, K. J. (1992). Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol. Reprod. Dev. 31, 249–252.
Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1571158PubMed |