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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Consequences of assisted reproductive technologies for offspring function in cattle

Luiz G. Siqueira A C , Marcos V. G. Silva A , João C. Panetto A and João H. Viana B
+ Author Affiliations
- Author Affiliations

A Embrapa Gado de Leite, Juiz de Fora, MG, Brazil 36038-330.

B Embrapa Recursos Genéticos e Biotecnologia, Brasília, DF, Brazil 70770-917.

C Corresponding author. Email: luiz.siqueira@embrapa.br

Reproduction, Fertility and Development 32(2) 82-97 https://doi.org/10.1071/RD19278
Published: 2 December 2019

Abstract

Abnormal fetuses, neonates and adult offspring derived by assisted reproductive technologies (ART) have been reported in humans, rodents and domestic animals. The use of ART has also been associated with an increased likelihood of certain adult diseases. These abnormalities may arise as a result of an excess of or missing maternally derived molecules during in vitro culture, because the in vitro environment is artificial and suboptimal for embryo development. Nonetheless, the success of ART in overcoming infertility or improving livestock genetics is undeniable. Limitations of in vitro embryo production (IVEP) in cattle include lower rates of the establishment and maintenance of pregnancy and an increased incidence of neonatal morbidity and mortality. Moreover, recent studies demonstrated long-term effects of IVEP in cattle, including increased postnatal mortality, altered growth and a slight reduction in the performance of adult dairy cows. This review addresses the effects of an altered preimplantation environment on embryo and fetal programming and offspring development. We discuss cellular and molecular responses of the embryo to the maternal environment, how ART may disturb programming, the possible role of epigenetic effects as a mechanism for altered phenotypes and long-term effects of ART that manifest in postnatal life.

Additional keywords: epigenetics, in vitro embryo, postnatal, pregnancy, programming.


References

Adamson, G. D., de Mouzon, J., Chambers, G. M., Zegers-Hochschild, F., Mansour, R., Ishihara, O., Banker, M., and Dyer, S. (2018). International Committee for Monitoring Assisted Reproductive Technology: world report on assisted reproductive technology, 2011. Fertil. Steril. 110, 1067–1080.
International Committee for Monitoring Assisted Reproductive Technology: world report on assisted reproductive technology, 2011.Crossref | GoogleScholarGoogle Scholar | 30396551PubMed |

Aleyasin, A., Abediasl, Z., Nazari, A., and Sheikh, M. (2016). Granulocyte colony-stimulating factor in repeated IVF failure, a randomized trial. Reproduction 151, 637–642.
Granulocyte colony-stimulating factor in repeated IVF failure, a randomized trial.Crossref | GoogleScholarGoogle Scholar | 26980809PubMed |

Andersen, A. N., Goossens, V., Ferraretti, A. P., Bhattacharya, S., Felberbaum, R., de Mouzon, J., and Nygren, K. G. (2008). European IVF-monitoring (EIM) Consortium, European Society of Human Reproduction and Embryology (ESHRE). Assisted reproductive technology in Europe, 2004: results generated from European registers by ESHRE. Hum. Reprod. 23, 756–771.
European IVF-monitoring (EIM) Consortium, European Society of Human Reproduction and Embryology (ESHRE). Assisted reproductive technology in Europe, 2004: results generated from European registers by ESHRE.Crossref | GoogleScholarGoogle Scholar | 18281243PubMed |

Arat, S., Caputcu, A. T., Cevik, M., Akkoc, T., Cetinkaya, G., and Bagis, H. (2016). Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos. Zygote 24, 554–562.
Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos.Crossref | GoogleScholarGoogle Scholar | 26444069PubMed |

Barker, D. J. (1990). The fetal and infant origins of adult disease. BMJ 301, 1111.
The fetal and infant origins of adult disease.Crossref | GoogleScholarGoogle Scholar | 2252919PubMed |

Barker, D. J., and Osmond, C. (1986). Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 327, 1077–1081.
Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales.Crossref | GoogleScholarGoogle Scholar |

Barros, C. M., Satrapa, R. A., Castilho, A. C. S., Fontes, P. K., Razza, E. M., Ereno, R. L., and Nogueira, M. F. G. (2013). Effect of superstimulatory treatments on the expression of genes related to ovulatory capacity, oocyte competence and embryo development in cattle. Reprod. Fertil. Dev. 25, 17–25.
Effect of superstimulatory treatments on the expression of genes related to ovulatory capacity, oocyte competence and embryo development in cattle.Crossref | GoogleScholarGoogle Scholar |

Behboodi, E., Anderson, G. B., BonDurant, R. H., Cargill, S. L., Kreuscher, B. R., Medrano, J. F., and Murray, J. D. (1995). Birth of large calves that developed from in vitro-derived bovine embryos. Theriogenology 44, 227–232.
Birth of large calves that developed from in vitro-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 16727722PubMed |

Bertolini, M., Beam, S. W., Shim, H., Bertolini, L. R., Moyer, A. L., Famula, T. R., and Anderson, G. B. (2002a). Growth, development, and gene expression by in vivo- and in vitro-produced Day 7 and 16 bovine embryos. Mol. Reprod. Dev. 63, 318–328.
Growth, development, and gene expression by in vivo- and in vitro-produced Day 7 and 16 bovine embryos.Crossref | GoogleScholarGoogle Scholar | 12237947PubMed |

Bertolini, M., Mason, J. B., Beam, S. W., Carneiro, G. F., Sween, M. L., Kominek, D. J., Moyer, A. L., Famula, T. R., Sainz, R. D., and Anderson, G. B. (2002b). Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology 58, 973–994.
Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights.Crossref | GoogleScholarGoogle Scholar | 12212896PubMed |

Block, J., Fischer-Brown, A. E., Rodina, T. M., Ealy, A. D., and Hansen, P. J. (2007). The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation. Theriogenology 68, 153–161.
The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation.Crossref | GoogleScholarGoogle Scholar | 17532038PubMed |

Block, J., Bonilla, L., and Hansen, P. J. (2009). Effect of addition of hyaluronan to embryo culture medium on survival of bovine embryos in vitro following vitrification and establishment of pregnancy after transfer to recipients. Theriogenology 71, 1063–1071.
Effect of addition of hyaluronan to embryo culture medium on survival of bovine embryos in vitro following vitrification and establishment of pregnancy after transfer to recipients.Crossref | GoogleScholarGoogle Scholar | 19157530PubMed |

Bloise, E., Feuer, S. K., and Rinaudo, P. F. (2014). Comparative intrauterine development and placental function of ART concepti: implications for human reproductive medicine and animal breeding. Hum. Reprod. Update 20, 822–839.
Comparative intrauterine development and placental function of ART concepti: implications for human reproductive medicine and animal breeding.Crossref | GoogleScholarGoogle Scholar | 24947475PubMed |

Blondin, P., Farin, P. W., Crosier, A. E., Alexander, J. E., and Farin, C. E. (2000). In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer. Biol. Reprod. 62, 384–389.
In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer.Crossref | GoogleScholarGoogle Scholar | 10642577PubMed |

Blondin, P., Bousquet, D., Twagiramungu, H., Barnes, F., and Sirard, M. A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
Manipulation of follicular development to produce developmentally competent bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 11751261PubMed |

Boerjan, M. L., den Daas, J. H., and Dieleman, S. J. (2000). Embryonic origins of health: long-term effects of IVF in human and livestock. Theriogenology 53, 537–547.
Embryonic origins of health: long-term effects of IVF in human and livestock.Crossref | GoogleScholarGoogle Scholar | 10735048PubMed |

Bonilla, L., Block, J., Denicol, A. C., and Hansen, P. J. (2014). Consequences of transfer of an in vitro-produced embryo for the dam and resultant calf. J. Dairy Sci. 97, 229–239.
Consequences of transfer of an in vitro-produced embryo for the dam and resultant calf.Crossref | GoogleScholarGoogle Scholar | 24210495PubMed |

Burdge, G. C., and Lillycrop, K. A. (2010). Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu. Rev. Nutr. 30, 315–339.
Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease.Crossref | GoogleScholarGoogle Scholar | 20415585PubMed |

Burton, G. J., and Fowden, A. L. (2012). The placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, S23–S27.
The placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation.Crossref | GoogleScholarGoogle Scholar | 22154688PubMed |

Ceelen, M., van Weissenbruch, M. M., Vermeiden, J. P. W., van Leeuwen, F. E., and Delemarre-van de Waal, H. A. (2008). Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J. Clin. Endocrinol. Metab. 93, 1682–1688.
Cardiometabolic differences in children born after in vitro fertilization: follow-up study.Crossref | GoogleScholarGoogle Scholar | 18285409PubMed |

Chen, Z., Robbins, K. M., Wells, K. D., and Rivera, R. M. (2013). Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith–Wiedemann. Epigenetics 8, 591–601.
Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith–Wiedemann.Crossref | GoogleScholarGoogle Scholar | 23751783PubMed |

Chen, Z., Hagen, D. E., Elsik, C. G., Ji, T., Morris, C. J., Moon, L. E., and Rivera, R. M. (2015). Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction. Proc. Natl Acad. Sci. USA 112, 4618–4623.
Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 25825726PubMed |

Chen, Z., Hagen, D. E., Wang, J., Elsik, C. G., Ji, T., Siqueira, L. G., Hansen, P. J., and Rivera, R. M. (2016). Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing. Epigenetics 11, 501–516.
Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing.Crossref | GoogleScholarGoogle Scholar | 27245094PubMed |

Chu, T., Dufort, I., and Sirard, M. A. (2012). Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 77, 1928–1938.
Effect of ovarian stimulation on oocyte gene expression in cattle.Crossref | GoogleScholarGoogle Scholar | 22444561PubMed |

de Boo, H. A., and Harding, J. E. (2006). The developmental origins of adult disease (Barker) hypothesis. Aust. N. Z. J. Obstet. Gynaecol. 46, 4–14.
The developmental origins of adult disease (Barker) hypothesis.Crossref | GoogleScholarGoogle Scholar | 16441686PubMed |

de Moraes, A. A., and Hansen, P. J. (1997). Granulocyte–macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos. Biol. Reprod. 57, 1060–1065.
Granulocyte–macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 9369171PubMed |

de Moraes, A. A., Paula-Lopes, F. F., Chegini, N., and Hansen, P. J. (1999). Localization of granulocyte–macrophage colony-stimulating factor in the bovine reproductive tract. J. Reprod. Immunol. 42, 135–145.
Localization of granulocyte–macrophage colony-stimulating factor in the bovine reproductive tract.Crossref | GoogleScholarGoogle Scholar | 10221736PubMed |

de Waal, E., Mak, W., Calhoun, S., Stein, P., Ord, T., Krapp, C., Coutifaris, C., Schultz, R. M., and Bartolomei, M. S. (2014). In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol. Reprod. 90, 22.
In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 24337315PubMed |

Denicol, A. C., Block, J., Kelley, D. E., Pohler, K. G., Dobbs, K. B., Mortensen, C. J., Ortega, M. S., and Hansen, P. J. (2014). The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo. FASEB J. 28, 3975–3986.
The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 24858280PubMed |

Dobbs, K. B., Rodriguez, M., Sudano, M. J., Ortega, M. S., and Hansen, P. J. (2013). Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PLoS One 8, e66230.
Dynamics of DNA methylation during early development of the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar | 23799080PubMed |

Doherty, A. S., Mann, M. R. W., Tremblay, K. D., Bartolomei, M. S., and Schultz, R. M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–1535.
Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 10819752PubMed |

Donjacour, A., Liu, X., Lin, W., Simbulan, R., and Rinaudo, P. F. (2014). In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol. Reprod. 90, 80.
In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model.Crossref | GoogleScholarGoogle Scholar | 24621920PubMed |

Enright, B. P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F. A., Yang, X., and Boland, M. P. (2000). Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 54, 659–673.
Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 11101029PubMed |

Ertzeid, G., and Storeng, R. (2001). The impact of ovarian stimulation on implantation and fetal development in mice. Hum. Reprod. 16, 221–225.
The impact of ovarian stimulation on implantation and fetal development in mice.Crossref | GoogleScholarGoogle Scholar | 11157810PubMed |

Farin, P. W., and Farin, C. E. (1995). Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development. Biol. Reprod. 52, 676–682.
Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development.Crossref | GoogleScholarGoogle Scholar | 7756461PubMed |

Farin, P. W., Piedrahita, J. A., and Farin, C. E. (2006). Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178–191.
Errors in development of fetuses and placentas from in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 16266745PubMed |

Farin, C. E., Farmer, W. T., and Farin, P. W. (2010). Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod. Fertil. Dev. 22, 75–87.
Pregnancy recognition and abnormal offspring syndrome in cattle.Crossref | GoogleScholarGoogle Scholar | 20003848PubMed |

Fátima, L. A., Baruselli, P. S., Gimenes, L. U., Binelli, M., Rennó, F. P., Murphy, B. D., and Papa, P. C. (2013). Global gene expression in the bovine corpus luteum is altered after stimulatory and superovulatory treatments. Reprod. Fertil. Dev. 25, 998–1011.
Global gene expression in the bovine corpus luteum is altered after stimulatory and superovulatory treatments.Crossref | GoogleScholarGoogle Scholar | 23106933PubMed |

Fernández-Gonzalez, R., Moreira, P., Bilbao, A., Jiménez, A., Pérez-Crespo, M., Ramírez, M. A., Fonseca, F. R. D., Pintado, B., and Gutiérrez-Adán, A. (2004). Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc. Natl Acad. Sci. USA 101, 5880–5885.
Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior.Crossref | GoogleScholarGoogle Scholar | 15079084PubMed |

Feuer, S. K., Liu, X., Donjacour, A., Lin, W., Simbulan, R. K., Giritharan, G., Piane, L. D., Kolahi, K., Ameri, K., Maltepe, E., and Rinaudo, P. F. (2014a). Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology 155, 1956–1969.
Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis.Crossref | GoogleScholarGoogle Scholar | 24684304PubMed |

Feuer, S. K., Donjacour, A., Simbulan, R. K., Lin, W., Liu, X., Maltepe, E., and Rinaudo, P. F. (2014b). Sexually dimorphic effect of in vitro fertilization (IVF) on adult mouse fat and liver metabolomes. Endocrinology 155, 4554–4567.
Sexually dimorphic effect of in vitro fertilization (IVF) on adult mouse fat and liver metabolomes.Crossref | GoogleScholarGoogle Scholar | 25211591PubMed |

Fidanza, A., Toschi, P., Zacchini, F., Czernik, M., Palmieri, C., Scapolo, P., Modlinski, J. A., Loi, P., and Ptak, G. E. (2014). Impaired placental vasculogenesis compromises the growth of sheep embryos developed in vitro. Biol. Reprod. 91, 21.
Impaired placental vasculogenesis compromises the growth of sheep embryos developed in vitro.Crossref | GoogleScholarGoogle Scholar | 24855101PubMed |

Fields, S. D., Hansen, P. J., and Ealy, A. D. (2011). Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75, 1466–1475.
Fibroblast growth factor requirements for in vitro development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 21295834PubMed |

Fleming, T. P., Watkins, A. J., Sun, C., Velazquez, M. A., Smyth, N. R., and Eckert, J. J. (2015a). Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo’s potential, affecting adult health. Reprod. Fertil. Dev. 27, 684.
Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo’s potential, affecting adult health.Crossref | GoogleScholarGoogle Scholar | 25730413PubMed |

Fleming, T. P., Velazquez, M. A., and Eckert, J. J. (2015b). Embryos, DOHaD and David Barker. J. Dev. Orig. Health Dis. 6, 377–383.
Embryos, DOHaD and David Barker.Crossref | GoogleScholarGoogle Scholar | 25952250PubMed |

Fontes, P. K., Castilho, A. C. S., Razza, E. M., Ereno, R. L., Satrapa, R. A., and Barros, C. M. (2014). Prostaglandin receptors (EP2 and EP4) and angiotensin receptor (AGTR2) mRNA expression increases in the oviducts of Nelore cows submitted to ovarian superstimulation. Anim. Reprod. Sci. 151, 112–118.
Prostaglandin receptors (EP2 and EP4) and angiotensin receptor (AGTR2) mRNA expression increases in the oviducts of Nelore cows submitted to ovarian superstimulation.Crossref | GoogleScholarGoogle Scholar | 25459076PubMed |

Ford, S. P., and Long, N. M. (2012). Evidence for similar changes in offspring phenotype following either maternal undernutrition or overnutrition: potential impact on fetal epigenetic mechanisms. Reprod. Fertil. Dev. 24, 105–111.
Evidence for similar changes in offspring phenotype following either maternal undernutrition or overnutrition: potential impact on fetal epigenetic mechanisms.Crossref | GoogleScholarGoogle Scholar |

Gad, A., Besenfelder, U., Rings, F., Ghanem, N., Salilew-Wondim, D., Hossain, M. M., Tesfaye, D., Lonergan, P., Becker, A., Cinar, U., Schellander, K., Havlicek, V., and Hölker, M. (2011). Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction. Hum. Reprod. 26, 1693–1707.
Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 21531990PubMed |

Gardner, D. K., and Harvey, A. J. (2015). Blastocyst metabolism. Reprod. Fertil. Dev. 27, 638.
Blastocyst metabolism.Crossref | GoogleScholarGoogle Scholar | 25751298PubMed |

Gasson, J. C. (1991). Molecular physiology of granulocyte–macrophage colony-stimulating factor. Blood 77, 1131–1145.
| 2001448PubMed |

Giritharan, G., Talbi, S., Donjacour, A., Di Sebastiano, F., Dobson, A. T., and Rinaudo, P. F. (2007). Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction 134, 63–72.
Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 17641089PubMed |

Grazul-Bilska, A. T., Borowicz, P. P., Johnson, M. L., Minten, M. A., Bilski, J. J., Wroblewski, R., Redmer, D. A., and Reynolds, L. P. (2010). Placental development during early pregnancy in sheep: vascular growth and expression of angiogenic factors in maternal placenta. Reproduction 140, 165–174.
Placental development during early pregnancy in sheep: vascular growth and expression of angiogenic factors in maternal placenta.Crossref | GoogleScholarGoogle Scholar | 20400519PubMed |

Grazul-Bilska, A. T., Johnson, M. L., Borowicz, P. P., Baranko, L., Redmer, D. A., and Reynolds, L. P. (2013). Placental development during early pregnancy in sheep: effects of embryo origin on fetal and placental growth and global methylation. Theriogenology 79, 94–102.
Placental development during early pregnancy in sheep: effects of embryo origin on fetal and placental growth and global methylation.Crossref | GoogleScholarGoogle Scholar | 23117132PubMed |

Gutiérrez-Adán, A., Rizos, D., Fair, T., Moreira, P. N., Pintado, B., de la Fuente, J., Boland, M. P., and Lonergan, P. (2004). Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol. Reprod. Dev. 68, 441–448.
Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 15236328PubMed |

Hales, C. N., and Barker, D. J. (2001). The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5–20.
The thrifty phenotype hypothesis.Crossref | GoogleScholarGoogle Scholar | 11809615PubMed |

Hansen, M., Kurinczuk, J. J., Bower, C., and Webb, S. (2002). The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N. Engl. J. Med. 346, 725–730.
The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 11882727PubMed |

Hansen, P. J., Dobbs, K. B., and Denicol, A. C. (2014). Programming of the preimplantation embryo by the embryokine colony stimulating factor 2. Anim. Reprod. Sci. 149, 59–66.
Programming of the preimplantation embryo by the embryokine colony stimulating factor 2.Crossref | GoogleScholarGoogle Scholar | 24954585PubMed |

Hansen, P. J., Dobbs, K. B., Denicol, A. C., and Siqueira, L. G. B. (2016). Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell Tissue Res. 363, 237–247.
Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development.Crossref | GoogleScholarGoogle Scholar | 26391275PubMed |

Hasler, J. F. (2000). In-vitro production of cattle embryos: problems with pregnancies and parturition. Hum. Reprod. 15, 47–58.
In-vitro production of cattle embryos: problems with pregnancies and parturition.Crossref | GoogleScholarGoogle Scholar | 11263537PubMed |

Hiendleder, S., Wirtz, M., Mund, C., Klempt, M., Reichenbach, H.-D., Stojkovic, M., Weppert, M., Wenigerkind, H., Elmlinger, M., Lyko, F., Schmitz, O. J., and Wolf, E. (2006). Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses. Biol. Reprod. 75, 17–23.
Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses.Crossref | GoogleScholarGoogle Scholar | 16554415PubMed |

Holm, P., and Callesen, H. (1998). In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. Reprod. Nutr. Dev. 38, 579–594.
In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application.Crossref | GoogleScholarGoogle Scholar | 9932292PubMed |

Hori, N., Nagai, M., Hirayama, M., Hirai, T., Matsuda, K., Hayashi, M., Tanaka, T., Ozawa, T., and Horike, S. (2010). Aberrant CpG methylation of the imprinting control region KvDMR1 detected in assisted reproductive technology-produced calves and pathogenesis of large offspring syndrome. Anim. Reprod. Sci. 122, 303–31210.1016/J.ANIREPROSCI.2010.09.008

Inbar-Feigenberg, M., Choufani, S., Butcher, D. T., Roifman, M., and Weksberg, R. (2013). Basic concepts of epigenetics. Fertil. Steril. 99, 607–615.
Basic concepts of epigenetics.Crossref | GoogleScholarGoogle Scholar | 23357459PubMed |

Jackson, R. A., Gibson, K. A., Wu, Y. W., and Croughan, M. S. (2004). Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet. Gynecol. 103, 551–563.
Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 14990421PubMed |

Kane, M. T., Morgan, P. M., and Coonan, C. (1997). Peptide growth factors and preimplantation development. Hum. Reprod. Update 3, 137–157.
Peptide growth factors and preimplantation development.Crossref | GoogleScholarGoogle Scholar | 9286738PubMed |

Kannampuzha-Francis, J., Denicol, A. C., Loureiro, B., Kaniyamattam, K., Ortega, M. S., and Hansen, P. J. (2015). Exposure to colony stimulating factor 2 during preimplantation development increases postnatal growth in cattle. Mol. Reprod. Dev. 82, 892–897.
Exposure to colony stimulating factor 2 during preimplantation development increases postnatal growth in cattle.Crossref | GoogleScholarGoogle Scholar | 26227079PubMed |

Kannampuzha-Francis, J., Tribulo, P., and Hansen, P. J. (2017). Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on development of the bovine preimplantation embryo. Reprod. Fertil. Dev. 29, 1329–1339.
Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on development of the bovine preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 27185102PubMed |

Katari, S., Turan, N., Bibikova, M., Erinle, O., Chalian, R., Foster, M., Gaughan, J. P., Coutifaris, C., and Sapienza, C. (2009). DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum. Mol. Genet. 18, 3769–3778.
DNA methylation and gene expression differences in children conceived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 19605411PubMed |

Keverne, E. B. (2015). Genomic imprinting, action, and interaction of maternal and fetal genomes. Proc. Natl Acad. Sci. USA 112, 6834–6840.
Genomic imprinting, action, and interaction of maternal and fetal genomes.Crossref | GoogleScholarGoogle Scholar | 25404322PubMed |

Kojima, Y., Tam, O. H., and Tam, P. P. L. (2014). Timing of developmental events in the early mouse embryo. Semin. Cell Dev. Biol. 34, 65–75.
Timing of developmental events in the early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 24954643PubMed |

Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–23.
| 15471793PubMed |

Krisher, R. L., and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
Responses of oocytes and embryos to the culture environment.Crossref | GoogleScholarGoogle Scholar | 10732124PubMed |

Kruip, T. A. M., and den Daas, J. H. G. (1997). In vitro produced and cloned embryos: effects on pregnancy, parturition and offspring. Theriogenology 47, 43–52.
In vitro produced and cloned embryos: effects on pregnancy, parturition and offspring.Crossref | GoogleScholarGoogle Scholar |

Kwak, S. S., Jeung, S. H., Biswas, D., Jeon, Y. B., and Hyun, S. H. (2012). Effects of porcine granulocyte–macrophage colony-stimulating factor on porcine in vitro-fertilized embryos. Theriogenology 77, 1186–1197.
Effects of porcine granulocyte–macrophage colony-stimulating factor on porcine in vitro-fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 22153263PubMed |

Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., and Fleming, T. P. (2000). Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127, 4195–4202.
| 10976051PubMed |

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 |

Lim, D., Bowdin, S. C., Tee, L., Kirby, G. A., Blair, E., Fryer, A., Lam, W., Oley, C., Cole, T., Brueton, L. A., Reik, W., Macdonald, F., and Maher, E. R. (2009). Clinical and molecular genetic features of Beckwith–Wiedemann syndrome associated with assisted reproductive technologies. Hum. Reprod. 24, 741–747.
Clinical and molecular genetic features of Beckwith–Wiedemann syndrome associated with assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 19073614PubMed |

Lonergan, P., Fair, T., Corcoran, D., and Evans, A. C. O. (2006). Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology 65, 137–152.
Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos.Crossref | GoogleScholarGoogle Scholar | 16289260PubMed |

Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q. S., and Hansen, P. J. (2009). Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 19797121PubMed |

Lucas, E. (2013). Epigenetic effects on the embryo as a result of periconceptional environment and assisted reproduction technology. Reprod. Biomed. Online 27, 477–485.
Epigenetic effects on the embryo as a result of periconceptional environment and assisted reproduction technology.Crossref | GoogleScholarGoogle Scholar | 23933034PubMed |

Mainigi, M. A., Olalere, D., Burd, I., Sapienza, C., Bartolomei, M., and Coutifaris, C. (2014). Peri-implantation hormonal milieu: elucidating mechanisms of abnormal placentation and fetal growth. Biol. Reprod. 90, 26.
Peri-implantation hormonal milieu: elucidating mechanisms of abnormal placentation and fetal growth.Crossref | GoogleScholarGoogle Scholar | 24352558PubMed |

Market-Velker, B. A., Fernandes, A. D., and Mann, M. R. W. (2010a). Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol. Reprod. 83, 938–950.
Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance.Crossref | GoogleScholarGoogle Scholar | 20702853PubMed |

Market-Velker, B. A., Zhang, L., Magri, L. S., Bonvissuto, A. C., and Mann, M. R. W. (2010b). Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum. Mol. Genet. 19, 36–51.
Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner.Crossref | GoogleScholarGoogle Scholar | 19805400PubMed |

McEvoy, T. G., Sinclair, K. D., Broadbent, P. J., Goodhand, K. L., and Robinson, J. J. (1998). Post-natal growth and development of Simmental calves derived from in vivo or in vitro embryos. Reprod. Fertil. Dev. 10, 459–464.
Post-natal growth and development of Simmental calves derived from in vivo or in vitro embryos.Crossref | GoogleScholarGoogle Scholar | 10588375PubMed |

McHughes, C. E., Springer, G. K., Spate, L. D., Li, R., Woods, R., Green, M. P., Korte, S. W., Murphy, C. N., Green, J. A., and Prather, R. S. (2009). Identification and quantification of differentially represented transcripts in in vitro and in vivo derived preimplantation bovine embryos. Mol. Reprod. Dev. 76, 48–60.
Identification and quantification of differentially represented transcripts in in vitro and in vivo derived preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 18449894PubMed |

Miles, J. R., Farin, C. E., Rodriguez, K. F., Alexander, J. E., and Farin, P. W. (2004). Angiogenesis and morphometry of bovine placentas in late gestation from embryos produced in vivo or in vitro. Biol. Reprod. 71, 1919–1926.
Angiogenesis and morphometry of bovine placentas in late gestation from embryos produced in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 15286036PubMed |

Morstyn, G., and Burgess, A. W. (1988). Hemopoietic growth factors: a review. Cancer Res. 48, 5624–5637.
| 2458827PubMed |

Mundim, T. C. D., Ramos, A. F., Sartori, R., Dode, M. A. N., Melo, E. O., Gomes, L. F. S., Rumpf, R., and Franco, M. M. (2009). Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation. Genet Mol Res 8, 1398–1407.
Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation.Crossref | GoogleScholarGoogle Scholar |

Painter, R. C., de Rooij, S. R., Bossuyt, P. M., Simmers, T. A., Osmond, C., Barker, D. J., Bleker, O. P., and Roseboom, T. J. (2006). Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am. J. Clin. Nutr. 84, 322–327.
Early onset of coronary artery disease after prenatal exposure to the Dutch famine.Crossref | GoogleScholarGoogle Scholar | 16895878PubMed |

Palma, G. A., Müller, M., and Brem, G. (1997). Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro. J. Reprod. Fertil. 110, 347–353.
Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 9306989PubMed |

Paria, B. C., and Dey, S. K. (1990). Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc. Natl Acad. Sci. USA 87, 4756–4760.
Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors.Crossref | GoogleScholarGoogle Scholar | 2352946PubMed |

Pohler, K. G., Pereira, M. H. C., Lopes, F. R., Lawrence, J. C., Keisler, D. H., Smith, M. F., Vasconcelos, J. L. M., and Green, J. A. (2016). Circulating concentrations of bovine pregnancy-associated glycoproteins and late embryonic mortality in lactating dairy herds. J. Dairy Sci. 99, 1584–1594.
Circulating concentrations of bovine pregnancy-associated glycoproteins and late embryonic mortality in lactating dairy herds.Crossref | GoogleScholarGoogle Scholar | 26709163PubMed |

Pontes, J. H. F., Nonato-Junior, I., Sanches, B. V., Ereno-Junior, J. C., Uvo, S., Barreiros, T. R. R., Oliveira, J. A., Hasler, J. F., and Seneda, M. M. (2009). Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology 71, 690–697.
Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows.Crossref | GoogleScholarGoogle Scholar |

Ravelli, A. C., van der Meulen, J. H., Michels, R. P. J., Osmond, C., Barker, D. J., Hales, C. N., and Bleker, O. P. (1998). Glucose tolerance in adults after prenatal exposure to famine. Lancet 351, 173–177.
Glucose tolerance in adults after prenatal exposure to famine.Crossref | GoogleScholarGoogle Scholar | 9449872PubMed |

Reefhuis, J., Honein, M. A., Schieve, L. A., Correa, A., Hobbs, C. A., and Rasmussen, S. A. (2009). National Birth Defects Prevention Study. Assisted reproductive technology and major structural birth defects in the United States. Hum. Reprod. 24, 360–366.
National Birth Defects Prevention Study. Assisted reproductive technology and major structural birth defects in the United States.Crossref | GoogleScholarGoogle Scholar | 19010807PubMed |

Rérat, M., Zbinden, Y., Saner, R., Hammon, H., and Blum, J. W. (2005). In vitro embryo production: growth performance, feed efficiency, and hematological, metabolic, and endocrine status in calves. J. Dairy Sci. 88, 2579–2593.
In vitro embryo production: growth performance, feed efficiency, and hematological, metabolic, and endocrine status in calves.Crossref | GoogleScholarGoogle Scholar | 15956319PubMed |

Rexhaj, E., Paoloni-Giacobino, A., Rimoldi, S. F., Fuster, D. G., Anderegg, M., Somm, E., Bouillet, E., Allemann, Y., Sartori, C., and Scherrer, U. (2013). Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J. Clin. Invest. 123, 5052–5060.
Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span.Crossref | GoogleScholarGoogle Scholar | 24270419PubMed |

Rexhaj, E., von Arx, R., Cerny, D., Soria, R., Bouillet, E., Sartori, C., Scherrer, U., and Rimoldi, S. (2015). Assisted reproductive technologies-induced premature vascular ageing persists and evolves into arterial hypertension in adolescents. FASEB J. 29, 957.9.

Rimoldi, S. F., Sartori, C., Rexhaj, E., Cerny, D., Von Arx, R., Soria, R., Germond, M., Allemann, Y., and Scherrer, U. (2014). Vascular dysfunction in children conceived by assisted reproductive technologies: underlying mechanisms and future implications. Swiss Med. Wkly. 144, w13973.
Vascular dysfunction in children conceived by assisted reproductive technologies: underlying mechanisms and future implications.Crossref | GoogleScholarGoogle Scholar | 24964004PubMed |

Rinaudo, P., and Schultz, R. M. (2004). Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction 128, 301–311.
Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 15333781PubMed |

Rivera, R. M., and Ross, J. W. (2013). Epigenetics in fertilization and preimplantation embryo development. Prog. Biophys. Mol. Biol. 113, 423–432.
Epigenetics in fertilization and preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 23454467PubMed |

Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). 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. 61, 234–248.
Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 11803560PubMed |

Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., De La Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–243.
Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 12493719PubMed |

Rizos, D., Clemente, M., Bermejo-Alvarez, P., de La Fuente, J., Lonergan, P., and Gutiérrez-Adán, A. (2008). Consequences of in vitro culture conditions on embryo development and quality. Reprod. Domest. Anim. 43, 44–50.
Consequences of in vitro culture conditions on embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 18803756PubMed |

Robertson, S. A. (2007). GM-CSF regulation of embryo development and pregnancy. Cytokine Growth Factor Rev. 18, 287–298.
GM-CSF regulation of embryo development and pregnancy.Crossref | GoogleScholarGoogle Scholar | 17512774PubMed |

Robertson, S. A., Mayrhofer, G., and Seamark, R. F. (1992). Uterine epithelial cells synthesize granulocyte–macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice. Biol. Reprod. 46, 1069–1079.
Uterine epithelial cells synthesize granulocyte–macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice.Crossref | GoogleScholarGoogle Scholar | 1391304PubMed |

Roseboom, T. J., Van Der Meulen, J. H., Ravelli, A. C., Osmond, C., Barker, D. J., and Bleker, O. P. (2001). Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol. Cell. Endocrinol. 185, 93–98.
Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview.Crossref | GoogleScholarGoogle Scholar | 11738798PubMed |

Salilew-Wondim, D., Tesfaye, D., Hossain, M., Held, E., Rings, F., Tholen, E., Looft, C., Cinar, U., Schellander, K., and Hoelker, M. (2013). Aberrant placenta gene expression pattern in bovine pregnancies established after transfer of cloned or in vitro produced embryos. Physiol. Genomics 45, 28–46.
Aberrant placenta gene expression pattern in bovine pregnancies established after transfer of cloned or in vitro produced embryos.Crossref | GoogleScholarGoogle Scholar | 23092953PubMed |

Santos, F., and Dean, W. (2004). Epigenetic reprogramming during early development in mammals. Reproduction 127, 643–651.
Epigenetic reprogramming during early development in mammals.Crossref | GoogleScholarGoogle Scholar | 15175501PubMed |

Sartori, R., Prata, A. B., Figueiredo, A. C. S., Sanches, B. V., Pontes, G. C. S., Viana, J. H. M., Pontes, J. H., Vasconcelos, J. L. M., Pereira, M. H. C., Dode, M. A. N., Monteiro, P. L. J., and Baruselli, P. S. (2016). Update and overview of assisted reproductive technologies (ARTs) in Brazil. Anim. Reprod. 13, 300–312.
Update and overview of assisted reproductive technologies (ARTs) in Brazil.Crossref | GoogleScholarGoogle Scholar |

Sato, A., Otsu, E., Negishi, H., Utsunomiya, T., and Arima, T. (2007). Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum. Reprod. 22, 26–35.
Aberrant DNA methylation of imprinted loci in superovulated oocytes.Crossref | GoogleScholarGoogle Scholar | 16923747PubMed |

Scherrer, U., Rimoldi, S. F., Rexhaj, E., Stuber, T., Duplain, H., Garcin, S., Marchi, S. F., Nicod, P., Germond, M., Allemann, Y., and Sartori, C. (2012). Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation 125, 1890–1896.
Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 22434595PubMed |

Scherrer, U., Rexhaj, E., Allemann, Y., Sartori, C., and Rimoldi, S. F. (2015). Cardiovascular dysfunction in children conceived by assisted reproductive technologies. Eur. Heart J. 36, 1583–1589.
Cardiovascular dysfunction in children conceived by assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 25911649PubMed |

Schieve, L. A., Meikle, S. F., Ferre, C., Peterson, H. B., Jeng, G., and Wilcox, L. S. (2002). Low and very low birth weight in infants conceived with use of assisted reproductive technology. N. Engl. J. Med. 346, 731–737.
Low and very low birth weight in infants conceived with use of assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 11882728PubMed |

Schulz, L. C. (2010). The Dutch Hunger Winter and the developmental origins of health and disease. Proc. Natl Acad. Sci. USA 107, 16757–16758.
The Dutch Hunger Winter and the developmental origins of health and disease.Crossref | GoogleScholarGoogle Scholar | 20855592PubMed |

Sferruzzi-Perri, A. N., Macpherson, A. M., Roberts, C. T., and Robertson, S. A. (2009). Csf2 null mutation alters placental gene expression and trophoblast glycogen cell and giant cell abundance in mice. Biol. Reprod. 81, 207–221.
Csf2 null mutation alters placental gene expression and trophoblast glycogen cell and giant cell abundance in mice.Crossref | GoogleScholarGoogle Scholar | 19228596PubMed |

Sinclair, K. D., McEvoy, T. G., Maxfield, E. K., Maltin, C. A., Young, L. E., Wilmut, I., Broadbent, P. J., and Robinson, J. J. (1999). Aberrant fetal growth and development after in vitro culture of sheep zygotes. J. Reprod. Fertil. 116, 177–186.
Aberrant fetal growth and development after in vitro culture of sheep zygotes.Crossref | GoogleScholarGoogle Scholar | 10505068PubMed |

Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J. F., Rees, W. D., Maloney, C. A., Lea, R. G., Craigon, J., McEvoy, T. G., and Young, L. E. (2007). DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc. Natl Acad. Sci. USA 104, 19351–19356.
DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status.Crossref | GoogleScholarGoogle Scholar | 18042717PubMed |

Siqueira, L. G. B., Torres, C. A. A., Souza, E. D., Monteiro, P. L. J., Arashiro, E. K. N., Camargo, L. S. A., Fernandes, C. A. C., and Viana, J. H. M. (2009). Pregnancy rates and corpus luteum-related factors affecting pregnancy establishment in bovine recipients synchronized for fixed-time embryo transfer. Theriogenology 72, 949–958.
Pregnancy rates and corpus luteum-related factors affecting pregnancy establishment in bovine recipients synchronized for fixed-time embryo transfer.Crossref | GoogleScholarGoogle Scholar |

Siqueira, L. G. B., Dikmen, S., Ortega, M. S., and Hansen, P. J. (2017a). Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen. J. Dairy Sci. 100, 5899–5908.
Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen.Crossref | GoogleScholarGoogle Scholar |

Siqueira, L. G. B., Tribulo, P., Chen, Z., Denicol, A. C., Ortega, M. S., Negrón-Pérez, V. M., Kannampuzha-Francis, J., Pohler, K. G., Rivera, R. M., and Hansen, P. J. (2017b). Colony-stimulating factor 2 acts from Days 5 to 7 of development to modify programming of the bovine conceptus at Day 86 of gestation. Biol. Reprod. 96, 743–757.
Colony-stimulating factor 2 acts from Days 5 to 7 of development to modify programming of the bovine conceptus at Day 86 of gestation.Crossref | GoogleScholarGoogle Scholar |

Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 11327682PubMed |

Sirisathien, S., and Brackett, B. G. (2003). TUNEL analyses of bovine blastocysts after culture with EGF and IGF-I. Mol. Reprod. Dev. 65, 51–56.
TUNEL analyses of bovine blastocysts after culture with EGF and IGF-I.Crossref | GoogleScholarGoogle Scholar | 12658633PubMed |

Sirisathien, S., Hernandez-Fonseca, H. J., and Brackett, B. G. (2003). Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro. Anim. Reprod. Sci. 77, 21–32.
Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar | 12654525PubMed |

Sjöblom, C., Wikland, M., and Robertson, S. A. (1999). Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum. Reprod. 14, 3069–3076.
Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar | 10601098PubMed |

Sjöblom, C., Roberts, C. T., Wikland, M., and Robertson, S. A. (2005). Granulocyte–macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146, 2142–2153.
Granulocyte–macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis.Crossref | GoogleScholarGoogle Scholar | 15705781PubMed |

Sponchiado, M., Gonella-Diaza, A. M., Rocha, C. C., Turco, E. G. L., Pugliesi, G., Leroy, J. L. M. R., and Binelli, M. (2019). The pre-hatching bovine embryo transforms the uterine luminal metabolite composition in vivo. Sci. Rep. 9, 8354.
The pre-hatching bovine embryo transforms the uterine luminal metabolite composition in vivo.Crossref | GoogleScholarGoogle Scholar | 31175317PubMed |

Steptoe, P. C., and Edwards, R. G. (1978). Birth after the reimplantation of a human embryo. Lancet 2, 366.
Birth after the reimplantation of a human embryo.Crossref | GoogleScholarGoogle Scholar |

Thoma, M. E., Boulet, S., Martin, J. A., and Kissin, D. (2014). Births resulting from assisted reproductive technology: comparing birth certificate and National ART Surveillance System Data, 2011. Natl Vital Stat. Rep. 63, 1–11.
| 25493705PubMed |

Thomasen, J. R., Willam, A., Egger-Danner, C., and Sørensen, A. C. (2016). Reproductive technologies combine well with genomic selection in dairy breeding programs. J. Dairy Sci. 99, 1331–1340.
Reproductive technologies combine well with genomic selection in dairy breeding programs.Crossref | GoogleScholarGoogle Scholar | 26686703PubMed |

Thomason, M. E., Scheinost, D., Manning, J. H., Grove, L. E., Hect, J., Marshall, N., Hernandez-Andrade, E., Berman, S., Pappas, A., Yeo, L., Hassan, S. S., Constable, R. T., Ment, L. R., and Romero, R. (2017). Weak functional connectivity in the human fetal brain prior to preterm birth. Sci. Rep. 7, 39286.
Weak functional connectivity in the human fetal brain prior to preterm birth.Crossref | GoogleScholarGoogle Scholar | 28067865PubMed |

Thompson, J. G. (1997). Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod. Fertil. Dev. 9, 341–354.
Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants.Crossref | GoogleScholarGoogle Scholar | 9261882PubMed |

Tobi, E. W., Lumey, L. H., Talens, R. P., Kremer, D., Putter, H., Stein, A. D., Slagboom, P. E., and Heijmans, B. T. (2009). DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum. Mol. Genet. 18, 4046–4053.
DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific.Crossref | GoogleScholarGoogle Scholar | 19656776PubMed |

Tremellen, K. P., Seamark, R. F., and Robertson, S. A. (1998). Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol. Reprod. 58, 1217–1225.
Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus.Crossref | GoogleScholarGoogle Scholar | 9603256PubMed |

Tríbulo, P., Siqueira, L. G. B., Oliveira, L. J., Scheffler, T., and Hansen, P. J. (2018). Identification of potential embryokines in the bovine reproductive tract. J. Dairy Sci. 101, 690–704.
Identification of potential embryokines in the bovine reproductive tract.Crossref | GoogleScholarGoogle Scholar | 29128220PubMed |

Tríbulo, P., Balzano-Nogueira, L., Conesa, A., Siqueira, L. G., and Hansen, P. J. (2019). Changes in the uterine metabolome of the cow during the first 7 days after estrus. Mol. Reprod. Dev. 86, 75–87.
Changes in the uterine metabolome of the cow during the first 7 days after estrus.Crossref | GoogleScholarGoogle Scholar | 30383328PubMed |

Urrego, R., Rodriguez-Osorio, N., and Niemann, H. (2014). Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle. Epigenetics 9, 803–815.
Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle.Crossref | GoogleScholarGoogle Scholar | 24709985PubMed |

Valenzuela-Alcaraz, B., Crispi, F., Bijnens, B., Cruz-Lemini, M., Creus, M., Sitges, M., Bartrons, J., Civico, S., Balasch, J., and Gratacós, E. (2013). Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally. Circulation 128, 1442–1450.
Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally.Crossref | GoogleScholarGoogle Scholar | 23985787PubMed |

van Wagtendonk-de Leeuw, A. M., Aerts, B. J., and den Daas, J. H. (1998). Abnormal offspring following in vitro production of bovine preimplantation embryos: a field study. Theriogenology 49, 883–894.
Abnormal offspring following in vitro production of bovine preimplantation embryos: a field study.Crossref | GoogleScholarGoogle Scholar | 10732097PubMed |

Viana, J. H. M. (2018). 2017 Statistics of embryo production and transfer in domestic farm animals: is it a turning point? Embryo Transfer Newsl 36, 8–25.

Viana, J. H. M., Vargas, M. S. B., Siqueira, L. G. B., Camargo, L. S. A., Figueiredo, A. C. S., Fernandes, C. A. C., and Palhao, M. P. (2016). Efficacy of induction of luteolysis in superovulated cows is dependent on time of prostaglandin F2alpha analog treatment: effects on plasma progesterone and luteinizing hormone profiles. Theriogenology 86, 934–939.
Efficacy of induction of luteolysis in superovulated cows is dependent on time of prostaglandin F2alpha analog treatment: effects on plasma progesterone and luteinizing hormone profiles.Crossref | GoogleScholarGoogle Scholar |

Vigneault, C., McGraw, S., Massicotte, L., and Sirard, M. A. (2004). Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol. Reprod. 70, 1701–1709.
Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition.Crossref | GoogleScholarGoogle Scholar | 14960490PubMed |

Wang, J. X., Norman, R. J., and Wilcox, A. J. (2004). Incidence of spontaneous abortion among pregnancies produced by assisted reproductive technology. Hum. Reprod. 19, 272–277.
Incidence of spontaneous abortion among pregnancies produced by assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 14747166PubMed |

Watkins, A. J., Platt, D., Papenbrock, T., Wilkins, A., Eckert, J. J., Kwong, W. Y., Osmond, C., Hanson, M., and Fleming, T. P. (2007). Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc. Natl Acad. Sci. USA 104, 5449–5454.
Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure.Crossref | GoogleScholarGoogle Scholar | 17372207PubMed |

Watkins, A. J., Ursell, E., Panton, R., Papenbrock, T., Hollis, L., Cunningham, C., Wilkins, A., Perry, V. H., Sheth, B., Kwong, W. Y., Eckert, J. J., Wild, A. E., Hanson, M. A., Osmond, C., and Fleming, T. P. (2008). Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol. Reprod. 78, 299–306.
Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease.Crossref | GoogleScholarGoogle Scholar | 17989357PubMed |

Watkins, A. J., Lucas, E. S., Wilkins, A., Cagampang, F. R. A., and Fleming, T. P. (2011). Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS One 6, e28745.
Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age.Crossref | GoogleScholarGoogle Scholar | 22194901PubMed |

Young, L. E., Sinclair, K. D., and Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. Reprod. 3, 155–163.
Large offspring syndrome in cattle and sheep.Crossref | GoogleScholarGoogle Scholar | 9829550PubMed |

Zhang, Y., Cui, Y., Zhou, Z., Sha, J., Li, Y., and Liu, J. (2010). Altered global gene expressions of human placentae subjected to assisted reproductive technology treatments. Placenta 31, 251–258.
Altered global gene expressions of human placentae subjected to assisted reproductive technology treatments.Crossref | GoogleScholarGoogle Scholar | 20116094PubMed |

Ziebe, S., Loft, A., Povlsen, B. B., Erb, K., Agerholm, I., Aasted, M., Gabrielsen, A., Hnida, C., Zobel, D. P., Munding, B., Bendz, S. H., and Robertson, S. A. (2013). A randomized clinical trial to evaluate the effect of granulocyte–macrophage colony-stimulating factor (GM-CSF) in embryo culture medium for in vitro fertilization. Fertil. Steril. 99, 1600–1609.e2.
A randomized clinical trial to evaluate the effect of granulocyte–macrophage colony-stimulating factor (GM-CSF) in embryo culture medium for in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 23380186PubMed |