Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Dietary propylene glycol and in vitro embryo production after ovum pick-up in heifers with different anti-Müllerian hormone profiles

G. Gamarra A B , C. Ponsart A , S. Lacaze B , B. Le Guienne A , P. Humblot C , M.-C. Deloche A , D. Monniaux D E F G and A. A. Ponter H I J
+ Author Affiliations
- Author Affiliations

A UNCEIA Département Recherche et Développement, 13 rue Jouet, F-94704 Maisons-Alfort, France.

B MIDATEST, Domine de Sensacq cedex 55A, F-64230 Denguin, France.

C Division of Reproduction, Department of Clinical Sciences, Faculty of Veterinary Medicine and Agricultural Sciences, Swedish University of Agricultural Sciences, PO Box 7054, SE 75007 Uppsala, Sweden.

D INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France.

E CNRS, UMR7247, F-37380 Nouzilly, France.

F Université François Rabelais de Tours, F-37041 Tours, France.

G IFCE, F-37380 Nouzilly, France.

H Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, UMR 1198 Biologie du Développement et Reproduction, F-94704 Maisons-Alfort, France.

I INRA, UMR 1198 Biologie du Développement et Reproduction, Domaine de Vilvert, F-78350 Jouy-en-Josas, France.

J Corresponding author. Email: aponter@vet-alfort.fr

Reproduction, Fertility and Development 27(8) 1249-1261 https://doi.org/10.1071/RD14091
Submitted: 11 March 2014  Accepted: 11 May 2014   Published: 24 July 2014

Abstract

Rapid genetic improvement in cattle requires the production of high numbers of embryos of excellent quality. Increasing circulating insulin and/or glucose concentrations improves ovarian follicular growth, which may improve the response to superovulation. The measurement of anti-Müllerian hormone (AMH) can help predict an animal’s response to superovulation treatment. The aim of the present study was to investigate whether increasing circulating insulin concentrations, through propylene glycol (PG) drenches, could improve in vitro embryo production in oestrus-synchronised superovulated heifers with different AMH profiles. Holstein heifers were grouped according to pre-experimental AMH concentrations as low (L) or high (H). The PG drench increased circulating insulin and glucose concentrations and reduced β-hydroxybutyrate and urea concentrations compared with the control group. AMH was a good predictor of follicle and oocyte numbers at ovum pick-up (OPU), and of oocyte and embryo quality (AMH H > AMH L). PG in the AMH H group increased the number of follicles and blastocyst quality above that in the control group, but did not improve these parameters in the AMH L group. These results indicate that short-term oral PG supplementation modifies an animal’s metabolic milieu and is effective in improving in vitro embryo production, after superovulation–OPU, more markedly in heifers with high rather than low AMH concentrations.

Additional keywords: cattle fertility, follicle growth, insulin, insulin-like growth factor 1, oocyte quality, superovulation.


References

Adamiak, S. J., Mackie, K., Watt, R. G., Webb, R., and Sinclair, K. D. (2005). Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle. Biol. Reprod. 73, 918–926.
Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktb7L&md5=1acdbeaa6e0e0af212ed88a019a2f8b4CAS | 15972884PubMed |

Armstrong, D. G., and Webb, R. (1997). Ovarian follicular dominance: the role of intraovarian growth factors and novel proteins. Rev. Reprod. 2, 139–146.
Ovarian follicular dominance: the role of intraovarian growth factors and novel proteins.Crossref | GoogleScholarGoogle Scholar | 9414477PubMed |

Armstrong, D. G., Mc Evoy, T. G., Baxter, G., Robinson, J. J., Hogg, C. O., and Woad, K. J. (2001). Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system. Biol. Reprod. 64, 1624–1632.
Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgsbY%3D&md5=8fd773bb014c8de60a005967f197730aCAS | 11369588PubMed |

Balogh, O. G., Fébel, H., Huszenicza, G., Kulcsár, M., Abonyi-Tóth, Z., Endrődi, T., and Gábor, G. (2012). Seasonal fertility differences in synchronised dairy cows: ultrasonic, metabolic and endocrine findings. Acta Vet. Hung. 60, 131–143.
Seasonal fertility differences in synchronised dairy cows: ultrasonic, metabolic and endocrine findings.Crossref | GoogleScholarGoogle Scholar | 22366138PubMed |

Barnouin, J., Chillard, Y., Chacornac, J. P., and Lefaivre, R. (1986). Microdosage automatisé sans déprotéïnisation du 3-hydroxy-butyrate plasmatique chez les bovins. Ann. Rech. Vet. 17, 129–139.
| 1:CAS:528:DyaL28XltFWhtrY%3D&md5=2ddebb6701846501244ca037d90318c7CAS | 3777808PubMed |

Bazin, S. (1984). ‘In Grille de notation de l’état d’engraissement des vaches Pie noires’. (Technipel: Paris.)

Blondin, P., Coenen, K., Guilbault, L. A., and Sirard, M. A. (1997). In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47, 1061–1075.
In vitro production of bovine embryos: developmental competence is acquired before maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVyjug%3D%3D&md5=a9b07d4873ec013f8ce60bded0f6e19cCAS | 16728056PubMed |

Boland, M. P., Lonergan, P., and O’Callaghan, D. (2001). Effect of nutrition on endocrine parameters, ovarian physiology and oocyte and embryo development. Theriogenology 55, 1323–1340.
Effect of nutrition on endocrine parameters, ovarian physiology and oocyte and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSis70%3D&md5=e7b866275be8ad2b3676466115ea7b5dCAS | 11327687PubMed |

Bols, P. E. J., Vandenheede, J. M. M., Van Soom, A., and de Kruif, A. (1995). Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system. Theriogenology 43, 677–687.
Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVCitA%3D%3D&md5=23a8ba91cfc3432ffd30ac75df9c691bCAS |

Burgwald-Balstad, L. A., Caton, J. S., Burke, V. I., and Olson, K. C. (1995). Influence of forage level and naloxone injection on feed intake, digestion, and plasma hormone and metabolite concentrations in dairy heifers. J. Anim. Sci. 73, 2677–2686.
| 1:CAS:528:DyaK2MXotFWqurY%3D&md5=c377253e5117a8e442a72009c7e3020fCAS | 8582858PubMed |

Butler, A. A., and Le Roith, D. (2001). Control of growth by the somatropic axis: GH and the IGF’s have related and independent roles. Annu. Rev. Physiol. 63, 141–164.
Control of growth by the somatropic axis: GH and the IGF’s have related and independent roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKmtL4%3D&md5=d06acbda954bb81bd991808e0dab0227CAS | 11181952PubMed |

Callesen, H., Løvendahl, P., Bak, A., and Greve, T. (1995). Factors affecting the developmental stage of embryos recovered on Day 7 from superovulated dairy cattle. J. Anim. Sci. 73, 1539–1543.
| 1:CAS:528:DyaK2MXmtV2isrw%3D&md5=542f88e527818fd9ed0b47bbcf17d0f4CAS | 7673046PubMed |

Christensen, J. O., Grummer, R. R., Rasmussen, F. E., and Bertics, S. J. (1997). Effect of method of delivery of propylene glycol on plasma metabolites of feed-restricted cattle. J. Dairy Sci. 80, 563–568.
Effect of method of delivery of propylene glycol on plasma metabolites of feed-restricted cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXit1yru7s%3D&md5=d8a5ad4a64c296c88d1d75b713300203CAS | 9098807PubMed |

Ferlay, A., and Chilliard, Y. (1999). Effects of the infusion of non-selective beta-, and selective beta1- or beta2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers. Reprod. Nutr. Dev. 39, 409–421.
Effects of the infusion of non-selective beta-, and selective beta1- or beta2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsFeksL0%3D&md5=21e1bd8243baf73321e3cada8bdc7292CAS | 10493147PubMed |

Freret, S., Grimard, B., Ponter, A. A., Joly, C., Ponsart, C., and Humblot, P. (2006). Reduction of body-weight gain enhances in vitro embryo production in overfed superovulated dairy heifers. Reproduction 131, 783–794.
Reduction of body-weight gain enhances in vitro embryo production in overfed superovulated dairy heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jt7o%3D&md5=ae76ffb051cc293dd9235a9ad2abfc52CAS | 16595729PubMed |

Gamarra, G., Ponsart, C., Lacaze, S., Marquant-Leguienne, B., Deloche, M.-C., Monniaux, D., and Ponter, A. A. (2014). Short term dietary propylene glycol supplementation affects circulating metabolic hormones, progesterone concentrations and follicular growth in dairy heifers. Livest. Sci. 162, 240–251.

Garnsworthy, P. C., Fouladi-Nashta, A. A., Mann, G. E., Sinclair, K. D., and Webb, R. (2009). Effect of dietary-induced changes in plasma insulin concentrations during the early post partum period on pregnancy rate in dairy cows. Reproduction 137, 759–768.
Effect of dietary-induced changes in plasma insulin concentrations during the early post partum period on pregnancy rate in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2nur4%3D&md5=223ec55e737aacebb8eff6846ec6e757CAS | 19129370PubMed |

Gong, J.-G. (2002). Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Domest. Anim. Endocrinol. 23, 229–241.
Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Wktbw%3D&md5=2258d0ab4d112d56625a1b2b0bfc988dCAS | 12142240PubMed |

Gong, J.-G., McBride, D., Bramley, T. A., and Webb, R. (1993). Effects of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on the proliferation of bovine granulosa cells in vitro. J. Endocrinol. 139, 67–75.
Effects of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on the proliferation of bovine granulosa cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitl2gtg%3D%3D&md5=b67d3303f07341b8c883fcf6385d10fbCAS | 8254295PubMed |

Greer, R. C., Staigmiller, R. B., and Parrish, J. J. (1992). Female traits, ovary and follicle characteristics, and the conditional probability of normal oocyte development after superovulation of beef cows. J. Anim. Sci. 70, 263–272.
| 1:STN:280:DyaK383lvFegsA%3D%3D&md5=f8ce6b252855d9121ef316f8283e3f97CAS | 1582913PubMed |

Grummer, R. R., Winkler, J. C., Bertics, S. J., and Studer, V. A. (1994). Effect of propylene glycol dosage during feed restriction on metabolites in blood of prepartum Holstein heifers. J. Dairy Sci. 77, 3618–3623.
Effect of propylene glycol dosage during feed restriction on metabolites in blood of prepartum Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivVyhsLg%3D&md5=42ac847b3daf2ffb6d4c699ff69148cdCAS | 7699140PubMed |

Gutiérrez, C. G., Campbell, B. K., and Webb, R. (1997). Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics. Biol. Reprod. 56, 608–616.
Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics.Crossref | GoogleScholarGoogle Scholar | 9047004PubMed |

Guyader-Joly, C., Ponchon, S., Durand, M., Heyman, Y., Renard, J. P., and Ménézo, Y. (1999). Effect of lecithin on in vitro and in vivo survival of in vitro produced bovine blastocysts after cryopreservation. Theriogenology 52, 1193–1202.
Effect of lecithin on in vitro and in vivo survival of in vitro produced bovine blastocysts after cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVKrtw%3D%3D&md5=4c04eec7d5bdae46c55502652fd7fc99CAS | 10735097PubMed |

Hidalgo, C. O., Gomez, E., Prieto, L., Duque, P., Goyache, F., Fernandez, L., Fernandez, I., Facal, N., and Diez, C. (2004). Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer. Theriogenology 62, 664–676.
Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltF2rsrc%3D&md5=10cffa5eaf0d659cbaf1b35aa5054ed4CAS | 15226021PubMed |

Humblot, P., Holm, P., Lonergan, P., Wrenzycki, C., Lequarré, A. S., Guyader-Joly, C., Herrmann, D., Lopes, A., Rizos, D., Niemann, H., and Callesen, H. (2005). Effect of stage of follicular growth during superovulation on developmental competence of bovine oocytes. Theriogenology 63, 1149–1166.
Effect of stage of follicular growth during superovulation on developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2Fot1Kltg%3D%3D&md5=dced378849bd569d3e5eb76f8713ea64CAS | 15710200PubMed |

Ireland, J. L. H., Scheetz, D., Jimenez-Krassel, F., Themmen, A. P., Ward, F., Lonergan, P., Smith, G. W., Perez, G. I., Evans, A. C. O., and Ireland, J. J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 79, 1219–1225.
Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCltL3M&md5=00a89418176dcda4a7306a002175afbaCAS |

Ireland, J. J., Zielak-Steciwko, A. E., Jimenez-Krassel, F., Folger, J., Bettegowda, A., Scheetz, D., Walsh, S., Mossa, F., Knight, P. G., Smith, G. W., Lonergan, P., and Evans, A. O. C. (2009). Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol. Reprod. 80, 954–964.
Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVajsr4%3D&md5=3cf069a1cfc3432fd6fd3497341a100bCAS | 19164170PubMed |

Jepson, M. M., Bates, P. C., and Millward, D. J. (1988). The role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein in the rat. Br. J. Nutr. 59, 397–415.
The role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktFOlsbY%3D&md5=7208fb6caac4396720950cad9a9b77d1CAS | 3293661PubMed |

Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H., Smith, G. W., Hou, X., Davis, J. S., Lonergan, P., Evans, A. C. O., and Ireland, J. J. (2009). Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during estrous cycles in cattle. Biol. Reprod. 80, 1272–1281.
Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during estrous cycles in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGmsb4%3D&md5=d11aa1c11cf249924f4673b78a3bce61CAS | 19211804PubMed |

Johnson, R. B. (1954). The treatment of ketosis with glycerol and propylene glycol. Cornell Vet. 44, 6–21.
| 1:STN:280:DyaG2c%2FkvVCltQ%3D%3D&md5=28be10af12d9304e422cf130e6449fc4CAS | 13127379PubMed |

Kristensen, N. B., and Raun, B. M. L. (2007). Ruminal and intermediary metabolism of propylene glycol in lactating Holstein cows. J. Dairy Sci. 90, 4707–4717.
Ruminal and intermediary metabolism of propylene glycol in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWlsrbN&md5=2cc2512292c5e73f48068647376ae093CAS | 17881693PubMed |

La Marca, A., and Volpe, A. (2006). Anti-Müllerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin. Endocrinol. (Oxf.) 64, 603–610.
Anti-Müllerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVylsrk%3D&md5=294d3c32e9e0c6bd03bf3bc96717e2efCAS | 16712660PubMed |

Lalman, D. L., Williams, J. E., Hess, B. W., Thomas, M. G., and Keisler, D. H. (2000). Effect of dietary energy on milk production and metabolic hormones in thin, primiparous beef heifers. J. Anim. Sci. 78, 530–538.
| 1:CAS:528:DC%2BD3cXisVSht7c%3D&md5=255f2e70e852374ce649d0fb7c117a7eCAS | 10764058PubMed |

Leiva, T., Cooke, R. F., Aboin, A. C., Soares, H. F., Barbosa, M., Madureira, A. M. L., Borges, M. A. F., and Vasconcelos, J. L. M. (2013). Effects of propiogenic ingredients on serum concentration of insulin and progesterone in non-lactating cows. Livest. Sci. 153, 165–172.
Effects of propiogenic ingredients on serum concentration of insulin and progesterone in non-lactating cows.Crossref | GoogleScholarGoogle Scholar |

Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=64880f331903999a2453ed9a0169b013CAS | 16183866PubMed |

Lozano, J. M., Lonergan, P., Boland, M. P., and O’Callaghan, D. (2003). Influence of nutrition on the effectiveness of superovulation programmes in ewes: effect on oocyte quality and post-fertilization development. Reproduction 125, 543–553.
Influence of nutrition on the effectiveness of superovulation programmes in ewes: effect on oocyte quality and post-fertilization development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOqtL0%3D&md5=b60340fdb0f76c9d3f1b393ef83fbf4aCAS | 12683925PubMed |

Majerus, V., De Roover, R., Etienne, D., Kaidi, S., Massip, A., Dessy, F., and Donnay, I. (1999). Embryo production by ovum pick up in unstimulated calves before and after puberty. Theriogenology 52, 1169–1179.
Embryo production by ovum pick up in unstimulated calves before and after puberty.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFaksg%3D%3D&md5=908a6ca9081ae937802490d5a4542db4CAS | 10735095PubMed |

Mantovani, R., Enright, W. J., Keane, M. G., Roche, J. F., and Bolan, M. P. (1993). Effect of nutrition and dose of follicle stimulating hormone (FSH) on superovulatory response in beef heifers. In ‘Proceedings of the 9th AETE Meeting, Lyon, France’. (Ed. Fondation Marcel Merieux.) p. 234. (European Embryo Transfer Association: Paris, France.) [Abstract]

Maplesden, D. C. (1954). Propylene glycol in the treatment of ketosis. Can. J. Comp. Med. Vet. Sci. 18, 287–293.
| 1:STN:280:DC%2BD2svjs1KjsA%3D%3D&md5=ed4449af13d7ac944d8315dd81444282CAS | 17648745PubMed |

Marquant-Le Guienne, B. (1998). Petit atlas de l’ovocyte bovin. Elevage Insémin. 288, 24–30.

McEvoy, T. G., Robinson, J. J., Aitken, R. P., Findlay, P. A., Palmer, R. M., and Robertson, I. S. (1995). Dietary-induced suppression of preovulatory progesterone concentrations in superovulated ewes impairs the subsequent in vivo and in vitro development of their ova. Anim. Reprod. Sci. 39, 89–107.
Dietary-induced suppression of preovulatory progesterone concentrations in superovulated ewes impairs the subsequent in vivo and in vitro development of their ova.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsF2mtrc%3D&md5=cd4d9273d131b6b064871ad1bb23e203CAS |

Miyoshi, S., Pate, J. L., and Palmquist, D. L. (2001). Effects of propylene glycol drenching on energy balance, plasma glucose, plasma insulin, ovarian function and conception in dairy cows. Anim. Reprod. Sci. 68, 29–43.
Effects of propylene glycol drenching on energy balance, plasma glucose, plasma insulin, ovarian function and conception in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlOqsr4%3D&md5=c9caebbf5259045973b4b0129c460430CAS | 11600272PubMed |

Monniaux, D., di Clemente, N., Touzé, J. L., Belville, C., Rico, C., Bontoux, M., Picard, J. Y., and Fabre, S. (2008). Intrafollicular steroids and anti-Müllerian hormone during normal and cystic ovarian follicular development in the cow. Biol. Reprod. 79, 387–396.
Intrafollicular steroids and anti-Müllerian hormone during normal and cystic ovarian follicular development in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWmsb0%3D&md5=397d0815da87931accddf4f095628f25CAS | 18448844PubMed |

Monniaux, D., Barbey, S., Rico, C., Fabre, S., Gallard, Y., and Larroque, H. (2010). Anti-Müllerian hormone: a predictive marker of embryo production in cattle? Reprod. Fertil. Dev. 22, 1083–1091.
Anti-Müllerian hormone: a predictive marker of embryo production in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOgu7vE&md5=39ec10c00877b66ac2b66553f5d282c3CAS | 20797346PubMed |

Morgan, L. M., Hampton, S. M., Tredger, J. A., Cramb, R., and Marks, (1988). Modifications of gastric inhibitory polypeptide (GIP) secretion in man by a high-fat diet. Br. J. Nutr. 59, 373–380.
Modifications of gastric inhibitory polypeptide (GIP) secretion in man by a high-fat diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkt1aju78%3D&md5=6125d15ca51f7307d49bb4435ee600b2CAS | 3293660PubMed |

Mossa, F., Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H., Smith, G. W., Lonergan, P., Evans, A. C. O., and Ireland, J. J. (2010). Evidence that high variation in antral follicle count during follicular waves is linked to alterations in ovarian androgen production in cattle. Reproduction 140, 713–720.
Evidence that high variation in antral follicle count during follicular waves is linked to alterations in ovarian androgen production in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfE&md5=9fe840d5e929494ea5bde14ff4d90cf3CAS | 20699380PubMed |

Nielsen, N. I., and Ingvartsen, K. L. (2004). Propylene glycol for dairy cows. A review of the metabolism of propylene glycol and its effects on physiological parameters, feed intake, milk production and risk of ketosis. Anim. Feed Sci. Technol. 115, 191–213.
Propylene glycol for dairy cows. A review of the metabolism of propylene glycol and its effects on physiological parameters, feed intake, milk production and risk of ketosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVels78%3D&md5=9f34263b952ff75c12eae97e13e99d08CAS |

O’Callaghan, D., Yaakub, H., Hyttel, P., Spicer, L. J., and Boland, M. P. (2000). Effect of nutrition and superovulation on oocyte morphology, follicular fluid composition and systemic hormone concentrations in ewes. J. Reprod. Fertil. 118, 303–313.
| 1:CAS:528:DC%2BD3cXitlCqurw%3D&md5=09664c2595e5dc491b2828b978787c8eCAS | 10864794PubMed |

Papadopoulos, S., Lonergan, P., and Gath, Papadopoulos, S., Lonergan, P., and Gath, (2001). Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep. Theriogenology 55, 1059–1069.
Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Srurw%3D&md5=ed8509a37a66d463f5aa18b1c0dd0676CAS | 11322234PubMed |

Parr, R. A., Davis, I. F., Miles, M. A., and Squires, T. J. (1993). Liver blood flow and metabolic clearance rate of progesterone in sheep. Res. Vet. Sci. 55, 311–316.
Liver blood flow and metabolic clearance rate of progesterone in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht1Ghsb4%3D&md5=7bc863b944e6c8e97d52e66802d65961CAS | 8284494PubMed |

Rico, C., Fabre, S., Médigue, C., di Clemente, N., Clément, F., Touze, J., Dupont, M., Briant, E., Remy, E., Beckers, J. F., and Monniaux, D. (2009). Anti-Müllerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol. Reprod. 80, 50–59.
Anti-Müllerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFKq&md5=74a76fc500cf0dd7c7f3f110762fe1d6CAS | 18784351PubMed |

Rico, C., Drouilhet, L., Salvetti, P., Dalbiès-Tran, R., Jarrier, P., Touzé, J.-L., Pillet, E., Ponsart, C., Fabre, S., and Monniaux, D. (2012). Determination of anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reprod. Fertil. Dev. 24, 932–944.
Determination of anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Grs7vI&md5=3bc5acd1c02ad604c17869ef5a0807c2CAS | 22935154PubMed |

Rizos, D., Kenny, D. A., Griffin, W., Quinn, K., Duffy, P., Mulligan, F. J., Roche, J. F., Boland, M. P., and Lonergan, P. (2008). The effect of feeding propylene glycol to dairy cows during the early postpartum period on follicular dynamics and on metabolic parameters related to fertility. Theriogenology 69, 688–699.
The effect of feeding propylene glycol to dairy cows during the early postpartum period on follicular dynamics and on metabolic parameters related to fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVWhsL4%3D&md5=257199d378d06b035b09089d28e48484CAS | 18262261PubMed |

Sangsritavong, S., Combs, D. K., Sartori, R., and Wiltbank, M. C. (2002). High feed intake increases blood flow and metabolism of progesterone and estradiol-17β in dairy cattle. J. Dairy Sci. 85, 2831–2842.
High feed intake increases blood flow and metabolism of progesterone and estradiol-17β in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlagsbc%3D&md5=570d3bd250e10df638e2b3c1d2ae8d2fCAS | 12487450PubMed |

Santos, J. E., Cerri, L., and Sartori, R. (2008). Nutritional management of the donor cow. Theriogenology 69, 88–97.
Nutritional management of the donor cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nE&md5=47ded9b79f4cb99e142f725646857870CAS | 17959235PubMed |

SAS Institute. (2000). ‘SAS/STAT Software: User’s Guide, Release 8.0.’ (Cary, NC: SAS Institute Inc.)

Scaramuzzi, R. J., Campbell, B. K., Downing, J. A., Kendall, N. R., Khalid, M., Muñoz-Gutiérrez, M., and Somchit, A. (2006). A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reprod. Nutr. Dev. 46, 339–354.
A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOnsrzF&md5=ad00f912a50cfc1af95df0bc26913776CAS | 16824444PubMed |

Scheetz, D., Folger, J. K., Smith, G. W., and Ireland, J. J. (2012). Granulosa cells are refractory to FSH action in individuals with a low antral follicle count. Reprod. Fertil. Dev. 24, 327–336.
Granulosa cells are refractory to FSH action in individuals with a low antral follicle count.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Oitbs%3D&md5=11ca7fb9c59afe3aedfa47cb2f9ac578CAS | 22281079PubMed |

Seneda, M. M., Esper, C., Mansano, J., Ademir de Oliveira, J., and Vantini, R. (2001). Relationship between follicle size and ultrasound-guided transvaginal oocyte recovery. Anim. Reprod. Sci. 67, 37–43.
Relationship between follicle size and ultrasound-guided transvaginal oocyte recovery.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzksFSisA%3D%3D&md5=32e5e6c60fcf4a4ba55302e4e9720162CAS | 11408112PubMed |

Sirard, M. A., and Blondin, P. (1996). Oocyte maturation and IVF in cattle. Anim. Reprod. Sci. 42, 417–426.
Oocyte maturation and IVF in cattle.Crossref | GoogleScholarGoogle Scholar |

Starzl, T. E., Francavilla, A., Halgrimson, C. G., Francavilla, F. R., Porter, K. A., Brown, T. H., and Putnam, C. W. (1973). The origin, hormonal nature, and action of hepatotrophic substances in portal blood. Surg. Gynecol. Obstet. 137, 179–199.
| 1:CAS:528:DyaE3sXkvFSjurk%3D&md5=72035b538a2faa9bfafecc2b5ed286c8CAS | 4353133PubMed |

Vanholder, T., Leroy, J. L., Soom, A. vs, Opsomer, G., Maes, D., Coryn, M., and de Kruif, A. (2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 87, 33–44.
Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktVOju74%3D&md5=7c943fa70094277dfbeb69bda96db314CAS | 15885439PubMed |

Vasconcelos, J. L. M., Sangsritavong, S., Tsai, S. J., and Wiltbank, M. C. (2003). Acute reduction in serum progesterone concentrations after feed intake in dairy cows. Theriogenology 60, 795–807.
Acute reduction in serum progesterone concentrations after feed intake in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVejtrw%3D&md5=c0daf859b69fafec97c280d813c76a4eCAS |

Webb, R., Campbell, B. K., Garverick, H. A., Gong, J.-G., Gutierrez, C. G., and Armstrong, D. G. (1999). Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. Suppl. 54, 33–48.
| 1:CAS:528:DyaK1MXnslSisbg%3D&md5=a161e6262c4b1a26a07a18664854151dCAS | 10692843PubMed |

Webb, R., Garnsworthy, P. C., Gong, J.-G., and Armstrong, D. G. (2004). Control of follicular growth: local interactions and nutritional influences. J. Anim. Sci. 82, E63–E74.
| 15471816PubMed |

Yelich, J. vs, Wettemann, R. P., Marston, T. T., and Spicer, L. J. (1996). Luteinizing hormone, growth hormone, insulin-like growth factor-I, insulin and metabolites before puberty in heifers fed to gain at two rates. Domest. Anim. Endocrinol. 13, 325–338.
Luteinizing hormone, growth hormone, insulin-like growth factor-I, insulin and metabolites before puberty in heifers fed to gain at two rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVGmurc%3D&md5=354e181d656e3d9d4d3e42e5b541ec9aCAS |