Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0068
Animal Reproduction (AR)
Thematic Section: 40th Annual Meeting of the Association of Embryo Technology in Europe (AETE)

Embryo transfer: past, present, future – a personal perspective

Patrick Lonergan

Downloads: 0
Views: 183

Abstract

Embryo transfer is just one of a range of assisted reproductive technologies – often the last one in a sequence of others – that has revolutionised the cattle breeding industry. The number of in vitro-produced embryos transferred annually now surpasses the number derived by traditional superovulation by a factor of four. Although issues with cryotolerance of IVP embryos, embryo loss, and, in some cases, calf birth weight remain to be fully resolved, IVP embryos are likely here to stay as a tool for genetic improvement in dairy herds, offering increased flexibility in sire usage allowing multiple pregnancies from elite dam-bull combinations to be generated and the ability to produce more embryos per unit time than traditional superovulation. What follows is a short personal look back at the last 30 years; if you are looking for deep insights into the underlying biology regulating embryo development, this is not the place to look! Please refer to some of the excellent recent reviews and research papers cited herein.

Keywords

assisted reproductive technologies, bovine, IVF

References

Barnwell CV, Farin PW, Ashwell CM, Farmer WT, Galphin SP Jr, Farin CE. Differences in mRNA populations of short and long bovine conceptuses on Day 15 of gestation. Mol Reprod Dev. 2016;83(5):424-41. http://doi.org/10.1002/mrd.22640. PMid:27013032.

Berg DK, Ledgard A, Donnison M, McDonald R, Henderson HV, Meier S, Juengel JL, Burke CR. The first week following insemination is the period of major pregnancy failure in pasture-grazed dairy cows. J Dairy Sci. 2022;105(11):9253-70. http://doi.org/10.3168/jds.2021-21773. PMid:36153157.

Bernstein AD, Petropavlovski VV. Influence of non-electrolytes on viability of spermatozoa. Buleten Experimentalnoi Biologii i Medicini. 1937;III:17-28.

Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D. Collection, description and transfer of embryos from cattle 10--16 days after oestrus. J Reprod Fertil. 1980;59(1):205-16. http://doi.org/10.1530/jrf.0.0590205. PMid:7401037.

Carter F, Rings F, Mamo S, Holker M, Kuzmany A, Besenfelder U, Havlicek V, Mehta JP, Tesfaye D, Schellander K, Lonergan P. Effect of elevated circulating progesterone concentration on bovine blastocyst development and global transcriptome following endoscopic transfer of in vitro produced embryos to the bovine oviduct. Biol Reprod. 2010;83(5):707-19. http://doi.org/10.1095/biolreprod.109.082354. PMid:20631399.

Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche JF, Rizos D, Lonergan P. Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction. 2009;138(3):507-17. http://doi.org/10.1530/REP-09-0152. PMID: 19556439.

Crowe AD, Sánchez JM, Moore SG, McDonald M, McCabe MS, Randi F, Lonergan P, Butler ST. Incidence and timing of pregnancy loss following timed artificial insemination or timed embryo transfer with a fresh or frozen in vitro-produced embryo. J Dairy Sci. Forthcoming.

Crowe AD, Lonergan P, Butler ST. Invited review: use of assisted reproduction techniques to accelerate genetic gain and increase value of beef production in dairy herds. J Dairy Sci. 2021;104(12):12189-206. http://doi.org/10.3168/jds.2021-20281. PMid:34538485.

Crowe AD, Sánchez JM, Moore SG, McDonald M, Randi F, Santos A, Minela T, Branen J, Pursley JR, Lonergan P, Butler ST. Time to conceptus attachment and subsequent pregnancy loss in seasonal-calving pasture-based lactating dairy cows following timed artificial insemination with conventional or X-sorted semen or timed embryo transfer with frozen/thawed in vitro produced embryos. Reprod Fertil Dev. 2024a;36(1–2):149.

Crowe AD, Sánchez JM, Moore SG, McDonald M, Rodrigues R, Morales MF, Orsi de Freitas L, Randi F, Furlong J, Browne JA, Rabaglino MB, Lonergan P, Butler ST. Fertility in seasonal-calving pasture-based lactating dairy cows following timed artificial insemination or timed embryo transfer with fresh or frozen in vitro-produced embryos. J Dairy Sci. 2024b;107(3):1788-804. http://doi.org/10.3168/jds.2023-23520. PMid:37806631.

Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O’Gaora P, Roche JF, Lonergan P, Crowe MA. Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biol Reprod. 2011b;84(2):266-78. http://doi.org/10.1095/biolreprod.110.085910. PMid:20881316.

Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O’Gaora P, Lonergan P, Roche JF. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod. 2009;81(4):784-94. http://doi.org/10.1095/biolreprod.108.074336. PMid:19553605.

Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O’Gaora P, Roche JF, Lonergan P. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod. 2011a;85(1):144-56. http://doi.org/10.1095/biolreprod.110.090019. PMid:21349821.

Forde N, Mehta JP, Minten M, Crowe MA, Roche JF, Spencer TE, Lonergan P. Effects of low progesterone on the endometrial transcriptome in cattle. Biol Reprod. 2012;87(5):124. http://doi.org/10.1095/biolreprod.112.103424. PMid:23018184.

Forde N, Spencer TE, Bazer FW, Song G, Roche JF, Lonergan P. Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol Genomics. 2010;41(1):53-62. http://doi.org/10.1152/physiolgenomics.00162.2009. PMid:19996158.

Gad A, Hoelker M, Besenfelder U, Havlicek V, Cinar U, Rings F, Held E, Dufort I, Sirard MA, Schellander K, Tesfaye D. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod. 2012;87(4):100. http://doi.org/10.1095/biolreprod.112.099697. PMid:22811576.

Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction. 2002;124(2):289-300. http://doi.org/10.1530/rep.0.1240289. PMid:12141942.

Hansen PJ. Review: Some challenges and unrealized opportunities toward widespread use of the in vitro-produced embryo in cattle production. Animal. 2023;17(Suppl 1):100745. http://doi.org/10.1016/j.animal.2023.100745. PMID: 37567654.

Hansen PJ. The incompletely fulfilled promise of embryo transfer in cattle-why aren’t pregnancy rates greater and what can we do about it? J Anim Sci. 2020;98(11):skaa288. http://doi.org/10.1093/jas/skaa288. PMid:33141879.

Heape W. Preliminary note on the transplantation and growth of mammalian ova within a uterine foster mother. Proc R Soc Lond. 1891;48(292-295):457-8. http://doi.org/10.1098/rspl.1890.0053.

Kubisch HM, Sirisathien S, Bosch P, Hernandez-Fonseca HJ, Clements G, Liukkonen JR, Brackett BG. Effects of developmental stage, embryonic interferon-tau secretion and recipient synchrony on pregnancy rate after transfer of in vitro produced bovine blastocysts. Reprod Domest Anim. 2004;39(2):120-4. http://doi.org/10.1111/j.1439-0531.2004.00491.x. PMid:15065994.

Larson MA, Kimura K, Kubisch HM, Roberts RM. Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-tau. Proc Natl Acad Sci USA. 2001;98(17):9677-82. http://doi.org/10.1073/pnas.171305398. PMid:11481449.

Lonergan P, Fair T. Maturation of Oocytes in Vitro. Annu Rev Anim Biosci. 2016;4(1):255-68. http://doi.org/10.1146/annurev-animal-022114-110822. PMid:26566159.

Lonergan P, Forde N, Spencer T. Role of progesterone in embryo development in cattle. Reprod Fertil Dev. 2016;28(1-2):66-74. http://doi.org/10.1071/RD15326. PMid:27062875.

Lonergan P, Monaghan P, Rizos D, Boland MP, Gordon I. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol Reprod Dev. 1994;37(1):48-53. http://doi.org/10.1002/mrd.1080370107. PMid:8129930.

Lonergan P, Rizos D, Gutierrez-Adán A, Moreira PM, Pintado B, de la Fuente J, Boland MP. Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod. 2003a;69(4):1424-31. http://doi.org/10.1095/biolreprod.103.018168. PMid:12826577.

Lonergan P, Rizos D, Kanka J, Nemcova L, Mbaye AM, Kingston M, Wade M, Duffy P, Boland MP. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction. 2003b;126(3):337-46. http://doi.org/10.1530/rep.0.1260337. PMid:12968941.

Lonergan P, Sánchez JM. Symposium review: progesterone effects on early embryo development in cattle. J Dairy Sci. 2020;103(9):8698-707. http://doi.org/10.3168/jds.2020-18583. PMid:32622590.

Lu KH, Gordon I, Chen HB, Gallagher M, McGovern H. Birth of twins after transfer of cattle embryos produced by in vitro techniques. Vet Rec. 1988;122(22):539-40. http://doi.org/10.1136/vr.122.22.539. PMid:3413923.

Lu KH, Gordon I, Gallagher M, McGovern H. Pregnancy established in cattle by transfer of embryos derived from in vitro fertilisation of oocytes matured in vitro. Vet Rec. 1987;121(11):259-60. http://doi.org/10.1136/vr.121.11.259. PMid:3686787.

Maillo V, Gaora PÓ, Forde N, Besenfelder U, Havlicek V, Burns GW, Spencer TE, Gutierrez-Adan A, Lonergan P, Rizos D. Oviduct-embryo interactions in cattle: two-way traffic or a one-way street? Biol Reprod. 2015;92(6):144. http://doi.org/10.1095/biolreprod.115.127969. PMid:25926440.

Maillo V, Rizos D, Besenfelder U, Havlicek V, Kelly AK, Garrett M, Lonergan P. Influence of lactation on metabolic characteristics and embryo development in postpartum Holstein dairy cows. J Dairy Sci. 2012;95(7):3865-76. http://doi.org/10.3168/jds.2011-5270. PMid:22720941.

Mamo S, Mehta JP, Forde N, McGettigan P, Lonergan P. Conceptus-endometrium crosstalk during maternal recognition of pregnancy in cattle. Biol Reprod. 2012;87(1):6, 1-9. http://doi.org/10.1095/biolreprod.112.099945. PMid:22517619.

Mamo S, Mehta JP, McGettigan P, Fair T, Spencer TE, Bazer FW, Lonergan P. RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol Reprod. 2011;85(6):1143-51. http://doi.org/10.1095/biolreprod.111.092643. PMid:21795669.

Passaro C, Tutt D, Bagés-Arnal S, Maicas C, Laguna-Barraza R, Gutierrez-Adán A, Browne JA, Rath D, Behura SK, Spencer TE, Fair T, Lonergan P. Global transcriptomic response of bovine endometrium to blastocyst-stage embryos. Reproduction. 2019;158(3):223-35. http://doi.org/10.1530/REP-19-0064. PMid:31247587.

Passaro C, Tutt D, Mathew DJ, Sanchez JM, Browne JA, Boe-Hansen GB, Fair T, Lonergan P. Blastocyst-induced changes in the bovine endometrial transcriptome. Reproduction. 2018;156(3):219-29. http://doi.org/10.1530/REP-18-0188. PMid:30021913.

Polge C, Smith A, Parkes A. Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature. 1949;164(4172):666. http://doi.org/10.1038/164666a0. PMid:18143360.

Ponsart C, Heyman Y, Thibier M. Celebrating 25 years: history of AETE [Internet]. 2009 [cited 2024 May 20]. Available from: www.aete.eu.

Rabaglino MB, Forde N, Besenfelder U, Havlicek V, Blum H, Graf A, Wolf E, Lonergan P. Maternal metabolic status and in-vitro culture conditions during embryonic genome activation deregulate the expression of energy-related genes in the bovine 16-cells embryo. PLoS One. 2023;18(8):e0290689. http://doi.org/10.1371/journal.pone.0290689. PMid:37624829.

Ribeiro ES, Monteiro APA, Bisinotto RS, Lima FS, Greco LF, Ealy AD, Thatcher WW, Santos JEP. Conceptus development and transcriptome at preimplantation stages in lactating dairy cows of distinct genetic groups and estrous cyclic statuses. J Dairy Sci. 2016;99(6):4761-77. http://doi.org/10.3168/jds.2015-10315. PMid:27016828.

Rizos D, Carter F, Besenfelder U, Havlicek V, Lonergan P. Contribution of the female reproductive tract to low fertility in postpartum lactating dairy cows. J Dairy Sci. 2010;93(3):1022-9. http://doi.org/10.3168/jds.2009-2605. PMid:20172222.

Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev. 2002;61(2):234-48. http://doi.org/10.1002/mrd.1153. PMid:11803560.

Rodríguez-Alonso B, Sánchez JM, Hamdi M, McDonald M, Havlicek V, Besenfelder U, Lonergan P, Rizos D. Asynchrony between the early embryo and the reproductive tract affects subsequent embryo development in cattle. Reprod Fertil Dev. 2020;32(6):564-71. http://doi.org/10.1071/RD19360. PMid:32209207.

Rostand J. Glycérine et résistance du sperme aux basses temperatures. C. R Acad. Sci. 1946;222:1524-5.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. Progesterone alters the bovine uterine fluid lipidome during the period of elongation. Reproduction. 2019b;157(4):399-411. http://doi.org/10.1530/REP-18-0615. PMid:30763281.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. The biochemistry surrounding bovine conceptus elongation. Biol Reprod. 2019c;101(2):328-37. http://doi.org/10.1093/biolre/ioz101. PMid:31181571.

Simintiras CA, Sánchez JM, McDonald M, Martins T, Binelli M, Lonergan P. Biochemical characterization of progesterone-induced alterations in bovine uterine fluid amino acid and carbohydrate composition during the conceptus elongation window. Biol Reprod. 2019a;100(3):672-85. http://doi.org/10.1093/biolre/ioy234. PMid:30388203.

Spencer TE, Forde N, Lonergan P. The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. J Dairy Sci. 2016;99(7):5941-50. http://doi.org/10.3168/jds.2015-10070. PMid:26387021.

Sponchiado M, Gomes NS, Fontes PK, Martins T, Del Collado M, Pastore AA, Pugliesi G, Nogueira MFG, Binelli M. Pre-hatching embryo-dependent and -independent programming of endometrial function in cattle. PLoS One. 2017;12(4):e0175954. http://doi.org/10.1371/journal.pone.0175954. PMid:28423001.

Talukder AK, Rabaglino MB, Browne JA, Charpigny G, Lonergan P. Dose- and time-dependent effects of interferon tau on bovine endometrial gene expression. Theriogenology. 2023;211:1-10. http://doi.org/10.1016/j.theriogenology.2023.07.033. PMID: 37549523.

Thibier M. The European Embryo Transfer industry in cattle – a challenge in 1984, a success in 2014 – and well supported by the AETE. In: Proceedings of the 30th Annual Meeting AETE, 12th – 13th September 2014, Dresden, Germany. Dresden: AETE; 2014. Available at: https://www.aete.eu/annual-meeting/previous-meetings/.

Viana JHM. 2022 Statistics of embryo production and transfer in domestic farm animals: the main trends for the world embryo industry still stand. Embryo Technology Newsletter. 2023;41(4):20-38.

Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PL, Melo LF, Ochoa JC, Santos JE, Sartori R. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology. 2016;86(1):239-53. http://doi.org/10.1016/j.theriogenology.2016.04.037. PMid:27238438.

Wrenzycki C, Herrmann D, Carnwath JW, Niemann H. Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol Reprod Dev. 1999;53(1):8-18. http://doi.org/10.1002/(SICI)1098-2795(199905)53:1<8::AID-MRD2>3.0.CO;2-K. PMid:10230812.
 


Submitted date:
05/20/2024

Accepted date:
06/14/2024

66bb9b42a953951d67769106 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections