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

Plasma anti-Müllerian hormone concentration as a predictive endocrine marker for selection of donor lambs to improve success in juvenile in vitro embryo transfer programs

Hayley McGrice https://orcid.org/0000-0003-2003-6812 A C , Jennifer M. Kelly B , David O. Kleemann B , Karen L. Kind A , Alissa J. Hampton A , Patrick Hannemann A , Simon K. Walker B and William H. E. J. van Wettere A
+ Author Affiliations
- Author Affiliations

A School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy Campus, Roseworthy, SA 5371, Australia.

B South Australian Research and Development Institute, Turretfield Research Centre, Rosedale, SA 5350, Australia.

C Corresponding author. Email: hayley.mcgrice@adelaide.edu.au

Reproduction, Fertility and Development 32(4) 383-391 https://doi.org/10.1071/RD18498
Submitted: 6 December 2018  Accepted: 17 July 2019   Published: 13 November 2019

Abstract

The use of juvenile in vitro embryo transfer (JIVET) is limited by variation between prepubertal lambs in ovarian response to exogenous gonadotrophins. In cattle, anti-Müllerian hormone (AMH) is a predictive endocrine marker of antral follicle count. In this study we measured plasma AMH concentrations in lambs at 3 and 5 weeks of age and determined associations between AMH concentrations and ovarian response to gonadotrophins and in vitro blastocyst production at 6–8 weeks of age in a JIVET program. At 5 weeks, AMH (n = 38) was positively correlated with surface antral follicle count (r = 0.87, P < 0.001), blastocysts produced (r = 0.92, P < 0.001) and blastocysts produced as a proportion of oocytes collected (r = 0.44, P < 0.01) or cleaved (r = 0.43, P < 0.01). Similar associations were observed between AMH at 3 weeks (n = 30) and follicle number (r = 0.70, P < 0.05) and blastocysts produced (r = 0.87, P < 0.05). Lambs with high (>2.2 ng mL−1) compared with medium (0.4–2.2 ng mL−1) and low (<0.4 ng mL−1) AMH at 5 weeks had more antral follicles (mean (± s.e.m.) 118.7 ± 13.9 vs 68.2 ± 8.1 and 30.4 ± 12.3 respectively; P < 0.05) and more blastocysts produced (mean (± s.e.m.) 54.9 ± 6.9 vs 18.9 ± 4.0 and 7.5 ± 6.1 respectively; P < 0.05). These results suggest that AMH concentration at 5 weeks of age can be used to select donor lambs which enhance the success of JIVET programs.

Additional keywords: ewe lambs, sheep.


References

Baldrighi, J. M., Sa, M. F., Batista, E. O. S., Lopes, R. N. V. R., Visintin, J. A., Baruselli, P. S., and Assumpcao, M. E. O. A. (2014). Anti-Mullerian hormone concentration and antral ovarian follicle population in Murrah heifers compared to Holstein and gyr kept under the same management. Reprod. Domest. Anim. 49, 1015–1020.
Anti-Mullerian hormone concentration and antral ovarian follicle population in Murrah heifers compared to Holstein and gyr kept under the same management.Crossref | GoogleScholarGoogle Scholar | 25291989PubMed |

Baruselli, P. S., Batista, E. O. S., Vieira, L. M., and Souza, A. H. (2015). Relationship between follicle population, AMH concentration and fertility in cattle. Anim. Reprod. 12, 487–497.

Batista, E. O., Macedo, G. G., Sala, R. V., Ortolan, M. D., Sa Filho, M. F., Del Valle, T. A., Jesus, E. F., Lopes, R. N., Renno, F. P., and Baruselli, P. S. (2014). Plasma antimullerian hormone as a predictor of ovarian antral follicular population in Bos indicus (Nelore) and Bos taurus (Holstein) heifers. Reprod. Domest. Anim. 49, 448–452.
Plasma antimullerian hormone as a predictor of ovarian antral follicular population in Bos indicus (Nelore) and Bos taurus (Holstein) heifers.Crossref | GoogleScholarGoogle Scholar | 24689827PubMed |

Batista, E. O. S., Guerreiro, B. M., Freitas, B. G., Silva, J. C. B., Vieira, L. M., Ferreira, R. M., Rezende, R. G., Basso, A. C., Lopes, R. N. V. R., Renno, F. P., Souza, A. H., and Baruselli, P. S. (2016). Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bos taurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production. Domest. Anim. Endocrinol. 54, 1–9.
Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bos taurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production.Crossref | GoogleScholarGoogle Scholar |

Campbell, B. K., Clinton, M., and Webb, R. (2012). The role of anti-Mullerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology 153, 4533–4543.
The role of anti-Mullerian hormone (AMH) during follicle development in a monovulatory species (sheep).Crossref | GoogleScholarGoogle Scholar | 22778215PubMed |

El-Sheikh Ali, H., Kitahara, G., Takahashi, T., Mido, S., Sadawy, M., Kobayashi, I., Hemmi, K., and Osawa, T. (2017). Plasma anti-Müllerian hormone profile in heifers from birth through puberty and relationship with puberty onset. Biol. Reprod. 97, 153–161.
Plasma anti-Müllerian hormone profile in heifers from birth through puberty and relationship with puberty onset.Crossref | GoogleScholarGoogle Scholar | 28859283PubMed |

Guerreiro, B. M., Batista, E. O. S., Vieira, L. M., Sa, M. F., Rodrigues, C. A., Netto, A. C., Silveira, C. R. A., Bayeux, B. M., Dias, E. A. R., Monteiro, F. M., Accorsi, M., Lopes, R. N. V. R., and Baruselli, P. S. (2014). Plasma anti-Mullerian hormone: an endocrine marker for in vitro embryo production from Bos taurus and Bos indicus donors. Domest. Anim. Endocrinol. 49, 96–104.
Plasma anti-Mullerian hormone: an endocrine marker for in vitro embryo production from Bos taurus and Bos indicus donors.Crossref | GoogleScholarGoogle Scholar | 25136816PubMed |

Kelly, J. M., Kleemann, D. O., and Walker, S. K. (2005). Enhanced efficiency in the production of offspring from 4-to 8-week-old lambs. Theriogenology 63, 1876–1890.
Enhanced efficiency in the production of offspring from 4-to 8-week-old lambs.Crossref | GoogleScholarGoogle Scholar | 15823345PubMed |

Kelly, J. M., Kleemann, D. O., and Walker, S. K. (2014) JIVET technology and marker assisted selection (MAS) in Merino sheep. In ‘Reproduction in Domestic Ruminants VII. Proceedings of the 9th International Ruminant Reproduction Symposium, Obihiro, Japan’. (Eds J. L. Juengel, A. Miyamoto and C. Price.) p. 584. (Context Products Ltd: Leicestershire, England.) [Abstract]

Kelly, J. M., Kleemann, D. O., Maxwell, W. C., and Walker, S. K. (2007). Effect of GnRH treatment on the maturation and in vitro development of oocytes collected from 4-to 6-week-old merino lambs. Reprod. Fertil. Dev. 19, 947–953.
Effect of GnRH treatment on the maturation and in vitro development of oocytes collected from 4-to 6-week-old merino lambs.Crossref | GoogleScholarGoogle Scholar | 18076826PubMed |

Kennedy, J. P., Worthington, C. A., and Cole, E. R. (1974). Postnatal-development of ovary and uterus of merino lamb. J. Reprod. Fertil. 36, 282.
Postnatal-development of ovary and uterus of merino lamb.Crossref | GoogleScholarGoogle Scholar | 4819311PubMed |

Kereilwe, O., Pandey, K., Borromeo, V., and Kadokawa, H. (2018). Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion. Reprod. Fertil. Dev. 30, 1192–1203.
Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion.Crossref | GoogleScholarGoogle Scholar | 29533759PubMed |

Lahoz, B., Alabart, J. L., Monniaux, D., Fabre, S., Jarrier, P., Cocero, M. J., and Folch, J. (2012a). Determination of anti-Mullerian hormone plasma concentration can help to select donor sheep for laparoscopic ovum pick-up. Reprod. Domest. Anim. 47, 492–492.

Lahoz, B., Alabart, J. L., Monniaux, D., Mermillod, P., and Folch, J. (2012b). Anti-Mullerian hormone plasma concentration in prepubertal ewe lambs as a predictor of their fertility at a young age. BMC Vet. Res. 8, 118.
Anti-Mullerian hormone plasma concentration in prepubertal ewe lambs as a predictor of their fertility at a young age.Crossref | GoogleScholarGoogle Scholar | 22824005PubMed |

Lahoz, B., Alabart, J. L., Cocero, M. J., Monniaux, D., Echegoyen, E., Sanchez, P., and Folch, J. (2014). Anti-Mullerian hormone concentration in sheep and its dependence of age and independence of BMP15 genotype: an endocrine predictor to select the best donors for embryo biotechnologies. Theriogenology 81, 347–357.
Anti-Mullerian hormone concentration in sheep and its dependence of age and independence of BMP15 genotype: an endocrine predictor to select the best donors for embryo biotechnologies.Crossref | GoogleScholarGoogle Scholar | 24268018PubMed |

Monniaux, D., Barbey, S., Rico, C., Fabre, S., Gallard, Y., and Larroque, H. (2010). Anti-Mullerian hormone: a predictive marker of embryo production in cattle? Reprod. Fertil. Dev. 22, 1083–1091.
Anti-Mullerian hormone: a predictive marker of embryo production in cattle?Crossref | GoogleScholarGoogle Scholar | 20797346PubMed |

Monniaux, D., Baril, G., Laine, A. L., Jarrier, P., Poulin, N., Cognie, J., and Fabre, S. (2011). Anti-Mullerian hormone as a predictive endocrine marker for embryo production in the goat. Reproduction 142, 845–854.
Anti-Mullerian hormone as a predictive endocrine marker for embryo production in the goat.Crossref | GoogleScholarGoogle Scholar | 21930684PubMed |

Monniaux, D., Drouilhet, L., Rico, C., Estienne, A., Jarrier, P., Touze, J. L., Sapa, J., Phocas, F., Dupont, J., Dalbies-Tran, R., and Fabre, S. (2012). Regulation of anti-Mullerian hormone production in domestic animals. Reprod. Fertil. Dev. 25, 1–16.
Regulation of anti-Mullerian hormone production in domestic animals.Crossref | GoogleScholarGoogle Scholar | 23244824PubMed |

Morton, K. M. (2008). Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes. Reprod. Domest. Anim. 43, 137–143.
Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes.Crossref | GoogleScholarGoogle Scholar | 18638115PubMed |

Morton, K. M., Catt, S. L., Maxwell, W. M. C., and Evans, G. (2005). In vitro and in vivo developmental capabilities and kinetics of in vitro development of in vitro matured oocytes from adult, unstimulated and hormone-stimulated prepubertal ewes. Theriogenology 64, 1320–1332.
In vitro and in vivo developmental capabilities and kinetics of in vitro development of in vitro matured oocytes from adult, unstimulated and hormone-stimulated prepubertal ewes.Crossref | GoogleScholarGoogle Scholar | 16139608PubMed |

National Health and Medical Research Council (NHMRC) (2013) Australian code for the care and use of animals for scientific purposes, 8th edition. (NHMRC: Canberra.)

Paramio, M. T., and Izquierdo, D. (2014). Current status of in vitro embryo production in sheep and goats. Reprod. Domest. Anim. 49, 37–48.
Current status of in vitro embryo production in sheep and goats.Crossref | GoogleScholarGoogle Scholar | 25277431PubMed |

Pinto, P. H. N., Balaro, M. F. A., Souza-Fabjan, J. M. G., dos Santos Ribeiro, L., Bragança, G. M., Leite, C. R., Arashiro, E. K. N., de Moraes Silva, K., Da Fonseca, J. F., and Brandão, F. Z. (2018). Anti-Müllerian hormone and antral follicle count are more effective for selecting ewes with good potential for in vivo embryo production than the presence of FecGE mutation or eCG pre-selection tests. Theriogenology 113, 146–152.
Anti-Müllerian hormone and antral follicle count are more effective for selecting ewes with good potential for in vivo embryo production than the presence of FecGE mutation or eCG pre-selection tests.Crossref | GoogleScholarGoogle Scholar |

Ptak, G., Loi, P., Dattena, M., Tischner, M., and Cappai, P. (1999). Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes. Biol. Reprod. 61, 1568–1574.
Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes.Crossref | GoogleScholarGoogle Scholar | 10570004PubMed |

Ptak, G., Tischner, M., Bernabo, N., and Loi, P. (2003). Donor-dependent developmental competence of oocytes from lambs subjected to repeated hormonal stimulation. Biol. Reprod. 69, 278–285.
Donor-dependent developmental competence of oocytes from lambs subjected to repeated hormonal stimulation.Crossref | GoogleScholarGoogle Scholar | 12606346PubMed |

Rico, C., Fabre, S., Medigue, C., di Clemente, N., Clement, F., Bontoux, M., Touze, J. L., Dupont, M., Briant, E., Remy, B., Beckers, J. F., and Monniaux, D. (2009). Anti-Mullerian 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-Mullerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow.Crossref | GoogleScholarGoogle Scholar | 18784351PubMed |

Rico, C., Drouilhet, L., Salvetti, P., Dalbies-Tran, R., Jarrier, P., Touze, J. L., Pillet, E., Ponsart, C., Fabre, S., and Monniaux, D. (2012). Determination of anti-Mullerian 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-Mullerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm.Crossref | GoogleScholarGoogle Scholar | 22935154PubMed |

Torres-Rovira, L., Gonzalez-Bulnes, A., Succu, S., Spezzigu, A., Manca, M. E., Leoni, G. G., Sanna, M., Pirino, S., Gallus, M., Naitana, S., and Berlinguer, F. (2014). Predictive value of antral follicle count and anti-Mullerian hormone for follicle and oocyte developmental competence during the early prepubertal period in a sheep model. Reprod. Fertil. Dev. 26, 1094–1106.
Predictive value of antral follicle count and anti-Mullerian hormone for follicle and oocyte developmental competence during the early prepubertal period in a sheep model.Crossref | GoogleScholarGoogle Scholar | 24008140PubMed |

Torres-Rovira, L., Succu, S., Pasciu, V., Manca, M. E., Gonzalez-Bulnes, A., Leoni, G. G., Pennino, M. G., Spezzigu, A., Gallus, M., Dattena, M., Monniaux, D., Naitana, S., and Berlinguer, F. (2016). Postnatal pituitary and follicular activation: a revisited hypothesis in a sheep model. Reproduction 151, 215–225.
Postnatal pituitary and follicular activation: a revisited hypothesis in a sheep model.Crossref | GoogleScholarGoogle Scholar | 26621920PubMed |

Veiga-Lopez, A., Ye, W., and Padmanabhan, V. (2012). Developmental programming: prenatal testosterone excess disrupts anti-Mullerian hormone expression in preantral and antral follicles. Fertil. Steril. 97, 748–756.
Developmental programming: prenatal testosterone excess disrupts anti-Mullerian hormone expression in preantral and antral follicles.Crossref | GoogleScholarGoogle Scholar | 22245531PubMed |

Vernunft, A., Schwerhoff, M., Viergutz, T., Diederich, M., and Kuwer, A. (2015). Anti-Muellerian hormone levels in plasma of Holstein–Friesian heifers as a predictive parameter for ovum pick-up and embryo production outcomes. J. Reprod. Dev. 61, 74–79.
Anti-Muellerian hormone levels in plasma of Holstein–Friesian heifers as a predictive parameter for ovum pick-up and embryo production outcomes.Crossref | GoogleScholarGoogle Scholar | 25482112PubMed |

Walker, S. K., Hill, J., Kleemann, D., and Nancarrow, C. (1996). Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol. Reprod. 55, 703–708.
Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations.Crossref | GoogleScholarGoogle Scholar | 8862790PubMed |