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

Multiple factors affecting the efficiency of multiple ovulation and embryo transfer in sheep and goats

Antonio González-Bulnes A H , David T. Baird B , Bruce K. Campbell C , María J. Cocero A , Rosa M. García-García D , E. Keith Inskeep E , Antonio López-Sebastián A , Alan S. McNeilly F , Julián Santiago-Moreno A , Carlos J.H. Souza G and Almudena Veiga-López A
+ Author Affiliations
- Author Affiliations

A Departamento de Reproducción Animal, INIA Avda. Puerta de Hierro s/n, 28040-Madrid, Spain.

B Department of Obstetrics and Gynaecology, University of Edinburgh, Little France Crescent, Edinburgh EH16 4SB, UK.

C School of Human Development, University of Nottingham, QMC, Nottingham NG7 2UH, UK.

D Departamento de Ciencia y Tecnología Agroforestal, EUITA-UCLM, Ronda de Calatrava 7, 13071-Ciudad Real, Spain.

E Division of Animal and Veterinary Sciences, College of Agriculture, Forestry and Consumer Sciences, West Virginia University, Morgantown, WV 26506-6108, USA.

F MRC Human Reproductive Sciences Unit, Centre for Reproductive Biology, University of Edinburgh, Little France Crescent, Edinburgh EH16 4SB, UK.

G South Embrapa Cattle & Sheep Research Centre, Rodovia BR 153 km 595, Cx. Postal 242, Vila Industrial – Zona Rural, CEP 96401-970, Bagé, RS, Brazil.

H To whom correspondence should be addressed. email: bulnes@inia.es

Reproduction, Fertility and Development 16(4) 421-435 https://doi.org/10.1071/RD04033
Submitted: cfArticle2ecfc1997462761$funcRECEIVEDDATE@8783057  Accepted: 23 March 2004   Published: 6 July 2004

Abstract

This review offers an overview of the basic characteristics of in vivo embryo technologies, their current status, the main findings and the advances gained in recent years, and the outstanding subjects for increasing their efficiency. The use of superovulation and embryo transfer procedures remains affected by a high variability in the ovulatory response to hormonal treatment and by a low and variable number of transferable embryos and offspring obtained. This variability has been classically identified with both extrinsic (source, purity of gonadotrophins and protocol of administration) and intrinsic factors (breed, age, nutrition and reproductive status), which are reviewed in this paper. However, emerging data indicate that the main causes of variability are related to endocrine and ovarian factors, and so the number of studies and procedures addressing a better understanding and control of these factors may be increased in the future. The accomplishment of this objective, the improvement of procedures for embryo conservation and for the selection and management of recipient females, will allow further development and application of this technology.

Extra keywords: embryo cryopreservation, follicle dynamic, luteal function, superovulation.


Acknowledgments

We would like to thank the support from the administration, companies, breeders association and farmers of the authors’ different countries, the efforts from the staff of the different research centres and, last but not least, the help from all the sheep and goats (also those less convinced or even refusing) that made possible to achieve the information used in this review.


References

Abecia, J. A. , Lozano, J. M. , Forcada, F. , and Zarazaga, L. (1997). Effect of level of dietary energy and protein on embryo survival and progesterone production on day eight of pregnancy in Rasa Aragonesa ewes. Anim. Reprod. Sci. 48, 209–218.
CrossRef | PubMed |

Adams, G. P. (1999). Comparative patterns of follicle development and selection in ruminants. J. Reprod. Fertil. Suppl. 54, 17–32.
PubMed |

Alabart, J. L. , Folch, J. , Fernández-Arias, A. , Ramón, J. P. , Garbayo, A. , and Cocero, M. J. (1995). Screening of some variables influencing the results of embryo transfer in the ewe. I. Five-day-old embryos. Theriogenology 44, 1011–1026.
CrossRef |

Alabart, J. L. , Folch, J. , Fernández-Arias, A. , Ramon, J. P. , Garbayo, J. M. , and Cocero, M. J. (2003). Screening of some variables influencing the results of embryo transfer in the ewe. Part II: two-day-old embryos. Theriogenology 59, 1345–1356.
CrossRef | PubMed |

Armstrong, D. T. , and Evans, G. (1983). Factors affecting success of embryo transfer in sheep and goats. Theriogenology 19, 31–42.
CrossRef |

Armstrong, D. T. , Pfitzner, A. P. , Porter, K. J. , Warnes, G. M. , Janson, P. O. , and Seamark, R. F. (1982). Ovarian responses of anoestrous goats to stimulation with pregnant mare serum gonadotrophin. Anim. Reprod. Sci. 5, 15–23.
CrossRef |

Avdi, M. , Chemineau, P. , and Driancourt, M. A. (1997). Alterations in follicular maturation associated with within-breed variation in ovulation rate in Chios sheep. Anim. Reprod. Sci. 46, 223–235.
CrossRef | PubMed |

Baird, D. T. (1983). Factors regulating the growth of the preovulatory follicle in sheep and human. J. Reprod. Fertil. 69, 343–352.
CrossRef | PubMed |

Baird, D. T. , and McNeilly, A. S. (1981). Gonadotrophic control of follicular development and function during the oestrous cycle in the ewe. J. Reprod. Fertil Suppl 30, 129–133.


Baril, G. , and Vallet, J. C. (1990). Time of ovulation in dairy goats induced to superovulate with porcine follicle stimulating hormone and out of the breeding season. Theriogenology 34, 303–311.
CrossRef |

Baril, G., Brebion, P., and  Chesné, P. (1993). Manuel de Formation pour la Transplantation Embryonnaire Chez la Brebis et la Chevre 115 In Rome, Italy. In French

Baril, G. , Pougnard, J. L. , Freitas, V. J. F. , Leboeuf, B. , and Saumande, J. (1996). A new method for controlling the precise time of occurrence of the preovulatory gonadotropin surge in superovulated goats. Theriogenology 45, 697–706.
CrossRef |

Baril, G. , Traldi, A. L. , Cognie, Y. , Leboeuf, B. , Beckers, J. F. , and Mermillod, P. (2001). Successful direct transfer of vitrified sheep embryos. Theriogenology 56, 299–305.
CrossRef | PubMed |

Barnes, F. L. (2000). The effects of early uterine environment on the subsequent development of embryo and fetus. Theriogenology 19, 31–42.


Battye, K. M. , Fairclough, R. J. , Cameron, A. W. , and Trounson, A. O. (1988). Evidence for prostaglandin involvement in early luteal regression of the superovulated nanny goat (Capra hircus). J. Reprod. Fertil. 84, 425–430.
CrossRef | PubMed |

Bilton, R. J. , and Moore, N. W. (1976). In vitro culture, storage and transfer of goat embryos. Aust. J. Biol. Sci. 29, 125–129.
PubMed | | PubMed |

Bindon, B. M. , Piper, L. R. , Cahill, L. P. , Driancourt, M. A. , and O’Shea, T. (1986). Genetic and hormonal factors affecting superovulation. Theriogenology 25, 53–70.
CrossRef |

Binelli, M. , Hampton, J. , Buhi, W. C. , and Thatcher, W. W. (1999). Persistent dominant follicle alters pattern of oviductal secretory proteins from cows at estrus. Biol. Reprod. 61, 127–134.
PubMed |

Boland, M. P. , Goulding, D. , and Roche, J. F. (1991). Alternative gonadotrophins for superovulation in cattle. Theriogenology 35, 5–17.
CrossRef |

Brebion, P., and  Cognie, Y. (1989). Increased superovulation in the ewe following 14 days of GnRH agonist pretreatment. In ‘Proceedings of the 5th Meeting of the European Association of Embryo Transfer’. (European Association for Embryo Transfer: Lyon, France.)

Brebion, P., Belloc, J. P., and  Briois, M. (1990). Elite Lacaune ewes pretreated with a GnRH antagonist yield more usable embryos following pFSH. In ‘Proceedings of the 6th Meeting of the European Association of Embryo Transfer’. (European Association for Embryo Transfer: Lyon, France.) [Abstract]

Bungartz, L. , and Niemman, H. (1994). Assessment of the presence of a dominant follicle and selection of dairy cows suitable for superovulation by a single ultrasound examination. J. Reprod. Fertil. 101, 583–591.
CrossRef | PubMed |

Cahill, L. P. , Mariana, J. C. , and Mauleon, P. (1979). Total follicular population in ewes of high and low ovulation rate. J. Reprod. Fertil. 55, 27–36.
CrossRef | PubMed |

Campbell, B. K. , Scaramuzzi, R. J. , and Webb, R. (1995). Control of follicle development and selection in sheep and cattle. J. Reprod. Fertil. Suppl. 49, 335–350.
PubMed |

Campbell, B. K. , Dobson, H. , and Scaramuzzi, R. J. (1998). Ovarian function in ewes made hypogonadal with GnRH antagonist and stimulated with FSH in the presence or absence of low amplitude LH pulses. J. Endocrinol. 156, 213–222.
PubMed |

Casida, L. E. , Warwick, E. J. , and Meyer, R. A. (1944). Survival of multiple pregnancies induced in the ewe following treatment with pituitary gonadotrophins. J. Anim. Sci. 3, 22–28.


Chemineau, P. , Baril, G. , Leboeuf, B. , McMaurel, M. C. , and Cognie, Y. (1996). Recent advances in the control of goat reproduction. In ‘Proceedings of the 6th International Conference on Goats, July 1996’.   , 776–784.


Chupin, D., Cognie, Y., Combarnous, Y., Procureur, R. and  Saumande, J. (1987). Effect of purified LH and FSH on ovulation in the cow and ewe. In ‘Follicular growth and ovulation rate in farm animals’. (Eds. J. F. Roche and D. O'Callaghan)  pp. 63–71. (Martinus Nijhoff: The Hague, The Netherlands.)

Cocero, M. J. , Procureur, R. , De la Fuente, J. , and Chupin, D. (1988). Glycerol or ethylene glycol for embryo cryoprotection of deep frozen ewe embryos. Theriogenology 29, 238.
CrossRef |

Cocero, M. J. , Lopez-Sebastian, A. , Barragan, M. L. , and Picazo, R. A. (1996). Differences on post-thawing survival between ovine morulae and blastocysts cryopreserved with ethylene glycol or glycerol. Cryobiology 33, 502–507.
CrossRef | PubMed |

Cognie, Y. (1999). State of the art in sheep-goat embryo transfer. Theriogenology 51, 105–116.
CrossRef | PubMed |

Cognie, Y. , Baril, G. , Poulin, N. , and Mermillod, P. (2003). Current status of embryo technologies in sheep and goats. Theriogenology 59, 171–188.
CrossRef | PubMed |

Cox, S. F. , McMillan, W. H. , and Donnison, M. J. (1998). Establishment of a herd of cattle divergent potential pregnancy rate. Theriogenology 49, 242.
CrossRef |

Cran, D. G. (1983). Follicular development in the sheep after priming with PMSG. J. Reprod. Fertil. 67, 415–423.
CrossRef | PubMed |

Dattena, M., Isachenko, V., Alabart, J. L., Folch, J., Accardo, C. and  Cappai, P. (2001) Follicular development in the sheep after priming with PMSG. Proceedings of the 17th Meeting of the European Association of Embryo Transfer  114.

de Castro, T. , Rubianes, E. , Menchaca, A. , and Rivero, A. (1999). Ovarian dynamics, serum estradiol and progesterone concentrations during the interovulatory interval in goats. Theriogenology 52, 399–411.
CrossRef | PubMed |

De Smedt, V. , Crozet, N. , and Gall, L. (1994). Morphological and functional changes accompanying the acquisition of meiotic competence in ovarian goat oocyte. J. Exp. Zool. 269, 128–139.
PubMed | | PubMed |

Diedrich, K. , Diedrich, C. , Santos, E. , Zoll, C. , Al-Hasani, S. , Reissmann, T. , Krebs, D. , and Klingmuller, D. (1994). Suppression of the endogenous luteinizing hormone surge by the gonadotrophin-releasing hormone antagonist Cetrorelix during ovarian stimulation. Hum. Reprod. 9, 788–791.
PubMed |

Dingwall, W. S., McKelvey, W. A. C., Mylne, M. J. A., and  Simm, G. (1994). A protocol for MOET in Suffolk ewes. In ‘45th Annual Meeting of the European Association of Animal Production, Edinburgh. October 1994’.  pp. S2–4. (European Association of Animal Production: Edinburgh, UK.) [Abstract]

Donaldson, L. E. , and Perry, B. (1983). Embryo production in repeated superovulation of commercial donor cow. Theriogenology 20, 163–168.
CrossRef |

Doney, J. M. , Gunn, R. G. , Peart, J. N. , and Smith, W. F. (1981). Effect of body condition on paste type herbage intake, performance during lactation and subsequent ovulation rate in Scottish Blackface ewes. Anim. Prod. 33, 241–247.


Driancourt, M. A. (2001). Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction. Theriogenology 55, 1211–1239.
CrossRef | PubMed |

Driancourt, M. A. , and Avdi, M. (1993). Effect of the physiological stage of the ewe on the number of follicles ovulating following hCG injection. Anim. Reprod. Sci. 32, 227–236.
CrossRef |

Driancourt, M. A. , Fry, R. C. , Campbell, B. K. , and McNeilly, A. S. (1990a). Granulosa cell content and production of steroids, inhibin and follicular peptides by large follicles from a range of prolific and non-prolific breeds of sheep. J. Reprod. Fertil. 43, 230–231.


Driancourt, M. A. , Fry, R. C. , Campbell, B. K. , and McNeilly, A. S. (1990b). Granulosa cell content and production of steroids, inhibin and follicular peptides by large follicles from a range of prolific and non-prolific breeds of sheep. J. Reprod. Fertil. 43, 230–231.


Driancourt, M. A. , Webb, R. , and Fry, R. C. (1991). Does follicular dominance occur in ewes? J. Reprod. Fertil. 93, 63–70.
CrossRef | PubMed |

Dufour, J. J. , Cognie, Y. , Mermillod, P. , Mariana, J. C. , and Romain, R. F. (2000). Effects of the Booroola Fec gene on ovarian follicular populations in superovulated Romanov ewes pretreated with a GnRH antagonist. J. Reprod. Fertil. 118, 85–94.
CrossRef | PubMed |

El-Gayar, M. , and Holtz, W. (2001). Technical note: vitrification of goat embryos by the open pulled-straw method. J. Anim. Sci. 79, 2436–2438.
PubMed |

Evans, A. C. O. , Flynn, J. D. , Quinn, K. M. , Duffy, P. , Quinn, P. , Madgwick, S. , Crosby, T. F. , Boland, M. P. , and Beard, A. P. (2001). Ovulation of aged follicles does not affect embryo quality of fertility after a 14-day progestagen estrus synchronization protocol in ewes. Theriogenology 56, 923–936.
CrossRef | PubMed |

Evans, G. , and Armstrong, D. T. (1984). Reduction of sperm transport in ewes by superovulation treatments. J. Reprod. Fertil. 70, 47–53.
CrossRef | PubMed |

Fahning, M. L. , and Garcia, M. A. (1992). Status of cryopreservation of embryos from domestic animals. Cryobiology 29, 1–18.
PubMed |

Flynn, J. D. , Duffy, P. , Boland, M. P. , and Evans, A. C. O. (2000). Progestagen synchronization in the absence of a corpus luteum results in the ovulation of a persistent follicle in cyclic ewe lambs. Anim. Reprod. Sci. 62, 285–296.
CrossRef | PubMed |

Ford, S. P. , Weems, C. W. , Pitts, R. E. , Pexton, J. E. , Butcher, R. L. , and Inskeep, E. K. (1975). Effects of estradiol 17β and progesterone on prostaglandins F in sheep uteri and venous plasma. J. Anim. Sci. 41, 1407–1413.
PubMed |

Fortune, J. E. (1994). Ovarian follicular growth and development in mammals. Biol. Reprod. 50, 225–232.
PubMed |

García-García, R. M. (2003). Estudio de los efectos del cultivo y la congelación en la viabilidad de los embriones ovinos en estadios previos a la compactación (Study of the effects of culture and freezing on viability of preimplantational embryo stages). PhD Thesis. (: INIA: Madrid, Spain.) [In Spanish]

Gaston-Parry, O. , Heasman, K. , Nemorin, J. K. , and Robinson, T. J. (1988). A radioimmunoassay for fluorogestone acetate (FGA) and its application to the measurement of plasma FGA and progesterone in ewes treated with FGA-impregnated intravaginal sponges. Aust. J. Biol. Sci. 41, 57–67.
PubMed |

Gherardi, P. B. , and Lindsay, D. R. (1980). The effects of season on the ovulatory response of Merino ewes to serum from pregnant mares. J. Reprod. Fertil. 60, 425–429.
CrossRef | PubMed |

Ginther, O. J. , Knopf, L. , and Kastelic, L. P. (1989). Temporal associations among ovarian events in cattle during estrous cycles with two and three follicular waves. J. Reprod. Fertil. 87, 223–230.
CrossRef | PubMed |

Ginther, O. J. , and Kot, K. (1994). Follicular dynamics during the ovulatory season in goats. Theriogenology 42, 987–1001.
CrossRef |

González-Bulnes, A. , Osoro, K. , and López Sebastián, A. (1999a). Ultrasonographic assessment of the ovarian response in eCG-treated goats. Small Ruminant Res. 34, 65–69.
CrossRef |

González-Bulnes, A. , Santiago-Moreno, J. , Gómez-Brunet, A. , Inskeep, E. K. , Townsend, E. C. , and López-Sebastián, A. (1999b). Follicular dynamics during the oestrous cycle in dairy goats. Anim. Sci. 68, 547–554.


González-Bulnes, A. , Santiago-Moreno, J. , Cocero, M. J. , and López-Sebastián, A. (2000a). Effects of FSH commercial preparation and follicular status on follicular growth and superovulatory response in Spanish Merino ewes. Theriogenology 54, 1055–1064.
CrossRef | PubMed |

González-Bulnes, A. , Santiago-Moreno, J. , Gómez-Brunet, A. , and López-Sebastián, A. (2000b). Relationship between ultrasonographic assessment of the corpus luteum and plasma progesterone concentration during the oestrous cycle in monovular ewes. Reprod. Domest. Anim. 35, 65–68.
CrossRef |

González-Bulnes, A. , Santiago-Moreno, J. , García-García, R. M. , del Campo, A. , Gómez-Brunet, A. , and López-Sebastián, A. (2001). Origin of the preovulatory follicle in Mouflon sheep (Ovis gmelini musimon) and effect on the growth of remaining follicles during the follicular phase of oestrous cycle. Anim. Reprod. Sci. 65, 265–272.
CrossRef | PubMed |

González-Bulnes, A. , García-García, R. M. , Dominguez, V. , Santiago-Moreno, J. , López-Sebastián, A. , and Cocero, M. J. (2002a). Influence of physical ablation of dominant follicles on sheep superovulatory yields. Reprod. Domest. Anim. 37, 234.[Abstract]


González-Bulnes, A. , García-García, R. M. , Santiago-Moreno, J. , López-Sebastián, A. , and Cocero, M. (2002b). Effects of follicular status on superovulatory response in ewes is influenced by presence of corpus luteum at first FSH dosage. Theriogenology 58, 1607–1614.
CrossRef | PubMed |

González-Bulnes, A. , García-García, R. M. , Souza, C. J. H. , Santiago-Moreno, J. , López-Sebastián, A. , Cocero, M. J. , and Baird, D. T. (2002c). Patterns of follicular growth in superovulated ewes and influence on endocrine and ovarian response. Reprod. Domest. Anim. 37, 357–361.
CrossRef | PubMed | PubMed |

González-Bulnes, A. , Santiago-Moreno, J. , Cocero, M. J. , Souza, C. J. H. , Groome, N. P. , García-García, R. M. , López-Sebastián, A. , and Baird, D. T. (2002d). Measurement of inhibin A predicts the superovulatory response to exogenous FSH in sheep. Theriogenology 57, 1263–1272.
CrossRef | PubMed |

González-Bulnes, A. , Carrizosa, J. A. , Díaz-Delfa, C. , García-García, R. , Urrutia, B. , Santiago-Moreno, J. , Cocero, M. J. , and López-Sebastián, A. (2003a). Effects of ovarian follicular status on superovulatory response of dairy goats to FSH treatments. Small Ruminant Res. 48, 9–14.
CrossRef |

González-Bulnes, A. , García-García, R. M. , Castellanos, V. , Santiago-Moreno, J. , Ariznavarreta, C. , Domínguez, V. , López-Sebastián, A. , Tresguerres, J. A. F. , and Cocero, M. J. (2003b). Influence of maternal environment on the number of transferable embryos obtained in response to superovulatory FSH treatments in ewes. Reprod. Nutr. Dev. 43, 17–28.
CrossRef | PubMed | PubMed |

González-Bulnes, A. , García-García, R. M. , Santiago-Moreno, J. , Dominguez, V. , López-Sebastián, A. , and Cocero, M. J. (2003c). Reproductive season affects inhibitory effects from large follicles on superovulatory response in ewes. Theriogenology 60, 281–288.
CrossRef | PubMed |

González-Bulnes, A. , García-García, R. M. , Carrizosa, J. A. , Urrutia, B. , Souza, C. J. H. , Cocero, M. J. , López-Sebastián, A. , and McNeilly, A. S. (2004a). Plasma inhibin A determination at start superovulatory FSH treatments is predictive for embryo outcome in goats. Domest. Anim. Endocrinol. 26, 259–266.
CrossRef | PubMed | PubMed |

González-Bulnes, A. , Santiago-Moreno, J. , García-García, R. M. , Souza, C. J. H. , López-Sebastián, A. , and McNeilly, A. S. (2004b). Effect of GnRH antagonists treatment on gonadotrophin secretion, follicular development and inhibin a secretion in goats. Theriogenology 61, 977–985.
CrossRef | PubMed | PubMed |

González-Bulnes, A. , Souza, C. J. H. , Campbell, B. K. , and Baird, D. T. (in press). Systemic and intraovarian effects of dominant follicles on ovine follicular growth. Anim. Reprod. Sci. ,


Goodman, R. L. , and Karsh, F. J. (1980). Pulsatile secretion of luteinizing hormone: differential suppression by ovarian steroids. Endocrinology 107, 1286–1290.
PubMed |

Greve, T. , Callesen, H. , Hyttel, P. , Hoier, R. , and Assey, R. (1995). The effects of exogenous gonadotrophins on oocyte and embryo quality in cattle. Theriogenology 43, 41–50.
CrossRef |

Greyling, J. P. C. , Kotze, W. F. , Taylor, G. J. , Hagendijk, W. J. , and Cloete, F. (1994). Synchronization of oestrus in sheep: use of different dosages of progestagen outside the normal breeding season. S. Afr. J. Anim. Sci. 24, 33–37.


Hasler, J. F. , Bowen, R. A. , Nelson, L. D. , and Seidel, G. E. (1980). Serum progesterone concentrations in cows receiving embryo transfers. J. Reprod. Fertil. 58, 71–77.
CrossRef | PubMed |

Hawk, H. W. , and Conley, H. H. (1975). Involvement of the cervix in sperm transport failures in the reproductive tract of the ewe. J. Anim. Sci. 44, 638–644.


Hoffman, K. A. , Waller, S. L. , and Young, C. R. (1988). Once daily vs twice daily treatments with follicle stimulating hormone in ewes synchronized with different dosages of norgestomet. Theriogenology 29, 261.[Abstract]
CrossRef |

Inskeep, E. K. , Oloufa, M. M. , Pope, A. L. , and Casida, L. E. (1963). Functional capabilities of experimentally induced corpora lutea ewes. J. Anim. Sci. 22, 159–161.


Inskeep, E. K. , Howland, B. E. , Pope, A. L. , and Casida, L. E. (1964a). Some effects of progesterone on experimentally-induced corpora lutea in ewes. J. Anim. Sci. 23, 791–794.


Inskeep, E. K. , Howland, B. E. , Pope, A. L. , and Casida, L. E. (1964b). Ability of corpora lutea induced experimentally in progesterone-treated ewes to prevent subsequent ovulation. J. Anim. Sci. 23, 1172–1175.


Isachenko, V. , Alabart, J. L. , Dattena, M. , Nawroth, F. , and Cappai, P. , et al. (2003). New technology for vitrification and field (microscope-free) warming and transfer of small ruminant embryos. Theriogenology 59, 1209–1218.
CrossRef | PubMed |

Jabbour, H. N. , Ryan, J. P. , Evans, G. , and Maxwell, W. M. (1991). Effects of season, GnRH administration and lupin supplementation on the ovarian and endocrine responses of merino ewes treated with PMSG and FSH-P to induce superovulation. Reprod. Fertil. Dev. 3, 699–707.
PubMed |

Johnson, S. K. , Dailey, R. A. , Inskeep, E. K. , and Lewis, P. E. (1996). Effect of peripheral concentrations of progesterone on follicular growth and fertility in ewes. Domest. Anim. Endocrinol 13, 69–79.
CrossRef | PubMed |

Joseph, I. B. J. K. , Currie, W. D. , and Rawlings, N. C. (1992). Effects of time after ovariectomy, season and oestradiol on luteinizing hormone and follicle-stimulating hormone secretion in ovariectomized ewes. J. Reprod. Fertil. 94, 511–523.
CrossRef | PubMed |

Kafi, M. , and McGowan, M. R. (1997). Factors associated with variation in the superovulatory response in cattle. Anim. Reprod. Sci. 48, 137–157.
CrossRef | PubMed |

Kiessling, A. A. , Hughes, W. H. , and Blankevoort, M. R. (1986). Superovulation and embryo transfer in the dairy goat. J. Am. Vet. Med. Assoc. 188, 829–832.
PubMed |

Kojima, F. N. , Stumpf, T. T. , Cupp, A. S. , Werth, L. A. , Robertson, M. S. , Wolfe, M. W. , Kittok, R. J. , and Kinder, J. E. (1992). Exogenous progesterone and progestins as used in estrous synchrony do not mimic the corpus luteum in regulation in luteinizing hormone and 17β-estradiol in circulation of cows. Biol. Reprod. 47, 1009–1017.
PubMed |

Leibo, S. P. , Martino, A. , Kobayashi, S. , and Pollard, J. W. (1996). Stage dependent sensitivity of oocytes and embryos to low temperatures. Anim. Reprod. Sci. 42, 43–53.


Leyva, V. , Buckrell, B. C. , and Walton, J. S. (1998). Regulation of follicular activity and ovulation in ewes by exogenous progestagen. Theriogenology 50, 395–416.
CrossRef | PubMed |

Lindsell, C. E. , Rajkumar, K. , Manning, A. W. , Emery, S. K. , Mapletoft, R. J. , and Murphy, B. D. (1986). Variability in FSH : LH ratios among batches of commercially available gonadotrophins. Theriogenology 25, 167.[Abstract]
CrossRef |

López-Sebastián, A. , Cognie, Y. , Cocero, M. J. , De La Fuente, J. , and Poulin, N. (1990). Effect of season and duration of FSH treatment on embryo production in sheep. Theriogenology 34, 175–180.
CrossRef |

López-Sebastián, A. , González-Bulnes, A. , Santiago-Moreno, J. , Gómez-Brunet, A. , Townsend, E. C. , and Inskeep, E. K. (1997). Patterns of follicular development during the oestrous cycle in monovular Merino del Pais ewes. Anim. Reprod. Sci. 48, 279–291.
CrossRef | PubMed |

López-Sebastián, A. , González-Bulnes, A. , Santiago-Moreno, J. , Gómez-Brunet, A. , Townsend, E. C. , and Inskeep, E. K. (1999). Effects of follicular status at treatment on follicular development and ovulation in response to FSH in Spanish Merino ewes. Theriogenology 52, 505–514.
CrossRef | PubMed |

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.
PubMed |

Massip, A. (2001). Cryopreservation of embryos of farm animals. Reprod. Domest. Anim. 36, 49–55.
CrossRef | PubMed | PubMed |

Massip, A. , Van der Zwalmen, P. , Scheffen, B. , and Ectors, F. (1989). Some significant steps in the cryopreservation of mammalian embryos with a note on a vitrification procedure. Anim. Reprod. Sci. 19, 117–129.
CrossRef |

McNatty, K. P. , Lun, S. , Heath, D. A. , Ball, K. , Smith, P. , Hudson, N. L. , McDiarmid, J. , Gibb, M. , and Henderson, K. M. (1986). Differences in ovarian activity between Booroola x Merino ewes which are homozygous, heterozygous and non carriers of a major gene influencing their ovulation rate. J. Reprod. Fertil. 77, 193–205.
CrossRef | PubMed |

McNeilly, A. S. , and Fraser, H. M. (1987). Effect of gonadotrophin-releasing hormone agonist-induced suppression of LH and FSH on follicle growth and corpus luteum function in the ewe. J. Endocrinol. 115, 273–282.
PubMed |

McNeilly, A. S. , Picton, H. M. , Campbell, B. K. , and Baird, D. T. (1991). Gonadotrophic control of follicle growth in the ewe. J. Reprod. Fertil. Suppl. 43, 177–186.
PubMed |

Menchaca, A. , and Rubianes, E. (2002). Relation between progesterone concentrations during the early luteal phase and follicular dynamic in goats. Theriogenology 57, 1411–1419.
CrossRef | PubMed |

Mihm, M. , Baguisi, A. , Boland, M. P. , and Roche, J. F. (1994). Association between the duration of dominance of the ovulatory follicle and pregnancy rate in beef heifers. J. Reprod. Fertil. 102, 123–130.
CrossRef | PubMed |

Mihm, M. , Curran, N. , Hyttle, P. , Knight, P. G. , Boland, M. P. , and Roche, J. F. (1999). Effect of dominant follicle persistence on follicular fluid oestradiol and inhibin and on oocyte maturation in heifers. J. Reprod. Fertil. 116, 293–304.
CrossRef | PubMed |

Miller, K. F. , Nordheim, E. V. , and Ginther, O. J. (1981). Periodic fluctuations in FSH concentration during the ovine estrous cycle. Theriogenology 16, 669–679.
CrossRef |

Mitchell, L. M. , Dingwall, W. S. , Mylne, M. J. , Hunton, J. , Matthews, K. , Gebbie, F. E. , McCallum, G. J. , and McEvoy, T. G. (2002a). Season affects characteristics of the pre-ovulatory LH surge and embryo viability in superovulated ewes. Anim. Reprod. Sci. 74, 163–174.
CrossRef | PubMed |

Mitchell, L. M. , Silveira, M. , Mylne, M. J. , Matthews, K. , and Dingwall, W. S. (2002b). Seasonal differences in lamb birthweight do not arise from inherent differences in the oocyte and/or early embryo. Reprod. Fertil. Dev. 14, 207–213.
CrossRef | PubMed |

Monniaux, D. , Chupin, D. , and Saumande, J. (1983). Superovulatory response of cattle. Theriogenology 19, 55–81.
CrossRef |

Moore, N. W. , Rowson, L. E. A. , and Short, R. V. (1959). Egg transfer in sheep. Factors affecting the survival and development of transferred eggs. J. Reprod. Fertil. 1, 332–339.


Morand-Fehr, P. , and Boyazoglu, J. (1999). Present state and future outlook of the small ruminant sector. Small Ruminant Res. 34, 175–188.
CrossRef |

Murphy, B. D. , Mapletoft, R. J. , Manns, J. , and Humphrey, W. D. (1984). Variability in gonadotrophin preparation as a factor in the superovulatory response. Theriogenology 21, 117–125.
CrossRef |

Niemann, H. , Sacher, B. , and Elsaesser, F. (1985). Pregnancy rates relative to recipient plasma progesterone levels on the day of nonsurgical transfer of frozen/thawed bovine embryos. Theriogenology 23, 631–639.
CrossRef |

Niswender, G. D. , Schwall, R. H. , Fitz, T. A. , Farin, C. E. , and Sawyer, H. R. (1985). Regulation of luteal function in domestic ruminants: new concepts. Rec. Progr. Horm. Res. 41, 101–150.
PubMed |

Nöel, B. , Bister, J. L. , Pierquin, B. , and Paquay, R. (1994). Effects of FGA and PMSG on follicular growth and LH secretion in Suffolk ewes. Theriogenology 41, 719–727.
CrossRef |

Nuti, L. C. , Minhas, B. S. , Baker, W. C. , Capehart, J. S. , and Marrack, P. (1987). Superovulation and recovery of zygotes from Nubian and alpine dairy goats. Theriogenology 28, 481–488.
CrossRef |

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.
CrossRef | PubMed |

Oussaid, B. , Mariana, J. C. , Poulin, N. , Fontaine, J. , Lonergan, P. , Beckers, J. F. , and Cognie, Y. (1999). Reduction of the developmental competence of sheep oocytes by inhibition of LH pulses during the follicular phase with a GnRH antagonist. J. Reprod. Fertil. 117, 71–77.
CrossRef | PubMed |

Pendleton, R. J. , Youngs, C. R. , Rorie, R. W. , Pool, S. H. , Memon, M. A. , and Godke, R. A. (1992). Follicle stimulating hormone versus pregnant mare serum gonadotropin for superovulation of dairy goats. Small Ruminant Res. 8, 217–224.
CrossRef |

Picazo, R. A. , Cocero, M. J. , Barragan, M. L. , and Lopez-Sebastian, A. (1996). Effects of LH administration at the end of an FSH superovulatory regimen on ovulation rate and embryo production in three breeds of sheep. Theriogenology 45, 1065–1073.
CrossRef |

Picton, H. M. , Tsonis, C. G. , and McNeilly, A. S. (1990). The antagonistic effect of exogenous LH pulses on FSH-stimulated preovulatory follicle growth in ewes chronically treated with a gonadotrophin-releasing hormone agonist. J. Endocrinol. 127, 273–283.
PubMed |

Rall, W. F. (1987). Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology 24, 387–402.
PubMed |

Rall, W. F. (1992). Cryopreservation of oocytes and embryos: methods and applications. Anim. Reprod. Sci. 28, 237–245.
CrossRef |

Rall, W. F. , and Fahy, G. M. (1985). Ice free cryopreservation of mouse embryos at –196 degrees C by vitrification. Nature 313, 573–575.
PubMed |

Reissmann, T. , Felberbaum, R. , Diedrich, K. , Engel, J. , Comaru-Schally, A. M. , and Schally, A. V. (1995). Development and applications of luteinizing hormone-releasing hormone antagonists in the treatment of infertility: an overview. Hum. Reprod. 10, 1974–1981.
PubMed |

Remsen, L. G. , and Roussel, J. D. (1982). Pregnancy rates relating to plasma progesterone levels in recipient heifers at day of transfer. Theriogenology 18, 365–372.
CrossRef |

Revah, I. , and Butler, W. R. (1996). Prolonged dominance of follicles and reduced viability of bovine oocytes. J. Reprod. Fertil. 106, 39–47.
CrossRef | PubMed |

Rexroad, C. E. , and Powell, A. M. (1991). FSH injections and intrauterine insemination in protocols for superovulation of ewes. J. Anim. Sci. 69, 246–251.
PubMed |

Reynolds, L. P. , Killilea, S. D. , Grazul-Bilska, A. T. , and Redmer, D. A. (1994). Mitogenic factors of corpora lutea. Progr. Growth Factor Res. 5, 159–175.


Robinson, T. J. (1965). Use of progestagen-impregnated sponges inserted intravaginally or subcutaneously for the control of the oestrous cycle in the sheep. Nature 206, 39–41.
PubMed |

Robinson, T. J. (1967). ‘The Control of the Ovarian Cycle in the Sheep.’  pp. 237–244. (Sydney University Press: Sydney, Australia.)

Rowson, L. E. , and Moor, R. M. (1966). Embryo transfer in the sheep: the significance of synchronizing oestrus in the donor and recipient animal. J. Reprod. Fertil. 11, 207–212.
PubMed |

Rubianes, E. , and Menchaca, A. (2003). The pattern and manipulation of ovarian follicular growth in goats. Anim. Reprod. Sci. 78, 271–287.
CrossRef | PubMed |

Rubianes, E. , Ibarra, D. , Ungerfeld, R. , de Castro, T. , and Carbajal, B. (1995). Superovulatory response in anestrous ewes is affected by the presence of a large follicle. Theriogenology 43, 465–472.
CrossRef |

Rubianes, E. , de Castro, T. , and Carvajal, B. (1996). Effect of high progesterone levels during the growing phase of the dominant follicle of wave 1 in ultrasonographically monitored ewes. Can. J. Anim. Sci. 76, 473–475.


Rubianes, E. , Ungerfeld, R. , Viñoles, C. , Rivero, A. , and Adams, G. P. (1997). Ovarian response to gonadotropin treatment initiated relative to wave emergence in ultrasonographically monitored ewes. Theriogenology 47, 1479–1488.
CrossRef |

Saharrea, A. , Valencia, J. , Balcazar, A. , Mejia, O. , Cerbon, J. L. , Caballero, V. , and Zarco, L. (1998). Premature luteal regression in goats superovulated with PMSG: effect of hCG or GnRH administration during the early luteal phase. Theriogenology 50, 1039–1052.
CrossRef | PubMed |

Samartzi, F. , Boscos, C. , Vainas, E. , and Tsakalof, P. (1995). Superovulatory response of Chios sheep to PMSG during spring and autumn. Anim. Reprod. Sci. 39, 215–222.
CrossRef |

Santiago-Moreno, J. , González-Bulnes, A. , Gómez-Brunet, A. , Cocero, M. J. , del Campo, A. , García-García, R. M. , and López-Sebastián, A. (2001). Procedure for successful interspecific embryo transfer between mouflon (Ovis gmelini musimon) and Spanish Merino sheep (Ovis Aries). J. Zoo Wildl. Med. 32, 336–341.
PubMed |

Savio, J. D. , Thatcher, W. W. , Morris, G. R. , Entwistle, K. , Drost, M. , and Mattiacci, M. R. (1993). Effects of induction of low plasma progesterone concentrations with a progesterone-releasing intravaginal device on follicular turnover and fertility in cattle. J. Reprod. Fertil. 98, 77–84.
CrossRef | PubMed |

Scaramuzzi, R. J. , Downing, J. A. , Campbell, B. K. , and Cognie, Y. (1988). Control of fertility and fecundity of sheep by means of hormonal manipulation. Aust. J. Biol. Sci. 41, 37–45.
PubMed | | PubMed |

Scaramuzzi, R. J. , Adams, N. R. , Baird, D. T. , Campbell, B. K. , and Downing, J. A. , et al. (1993). A model for follicle selection and the determination of ovulation rate in ewes. Reprod. Fertil. Dev. 5, 459–478.
PubMed |

Schrick, F. N. , Surface, R. A. , Pritchard, J. Y. , Dailey, R. A. , Townsend, E. C. , and Inskeep, E. K. (1993). Ovarian structures during the estrous cycle and early pregnancy in ewes. Biol. Reprod. 49, 1133–1140.
PubMed |

Scudamore, C. L. , Robinson, J. J. , Aitken, R. P. , and Robertson, I. S. (1993). The effect of two different levels of progesterone priming on the response of ewes to superovulation. Theriogenology 39, 433–442.
CrossRef |

Sirois, J. , and Fortune, J. E. (1990). Lengthening the bovine estrous cycle with low levels of exogenous progesterone a model for studying ovarian follicular dominance. Endocrinology 127, 916–925.
PubMed |

Stock, A. E. , and Fortune, J. E. (1993). Ovarian follicular dominance in cattle: relationship between prolonged growth of the ovulatory follicle and endocrine parameters. Endocrinology 132, 1108–1114.
CrossRef | PubMed |

Stormshak, F. , Inskeep, E. K. , Lynn, J. E. , Pope, A. L. , and Casida, L. E. (1963). Progesterone levels in corpora lutea and ovarian effluent blood of the ewe. J. Anim. Sci. 22, 1021.


Taft, R. , Ahmad, N. , and Inskeep, E. K. (1996). Exogenous pulses of luteinizing hormone cause persistence of the largest bovine ovarian follicle. J. Anim. Sci. 74, 2985–2991.
PubMed |

Theriez, C. , Desvignes, A. , and Thimonier, S. (1971). Amelioration de la prolificite chez les ovins. Bull. Tech. Inf. Minn. 157, 1–7.


Thibier, M. (1996). Statistics of the ET industry around the world. IETS Newsletter 15, 10–13.


Thompson, J. G. E. , Simpson, A. C. , James, R. W. , and Tervit, H. R. (1990). The application of progesterone-containing CIDR devices to superovulated ewes. Theriogenology 33, 1297–1304.
CrossRef |

Torres, S. , and Sevellec, C. (1987). Repeated superovulation and surgical recovery of embryos in the ewe. Reprod. Nutr. Dev. 27, 859–863.
PubMed |

Torres, S. , Cognie, Y. , and Colas, G. (1987). Transfer of superovulated sheep embryos obtained with different FSH-P. Theriogenology 27, 407–419.
CrossRef |

Tsonis, C. G. , McNeilly, A. S. , and Baird, D. T. (1988). Inhibin secretion by the sheep ovary during the luteal and follicular phases of the oestrous cycle and following stimulation with FSH. J. Endocrinol. 117, 283–291.
PubMed |

Ungerfeld, R. , and Rubianes, E. (1999). Effectiveness of short-term progestogen primings for the induction of fertile oestrus with eCG in ewes during late seasonal anoestrus. J. Anim. Sci. 68, 349–353.


Vatja, G. , Booth, P. J. , Holm, P. , Greve, T. , and Callesen, H. (1997). Succesful vitrification of early stage bovine in vitro produced embryos with the open pulled straw (OPS) method. Cryo Letters 18, 191–195.


Viñoles, C. , Forsberg, M. , Banchero, G. , and Rubianes, E. (2001). Effect of long-term and short-term progestagen treatment on follicular development and pregnancy rate in cyclic ewes. Theriogenology 55, 993–1004.
CrossRef | PubMed |

Viñoles, C. , Meikle, A. , Forsberg, M. , and Rubianes, E. (1999). The effect of subluteal levels of exogenous progesterone on follicular dynamics and endocrine patterns during the early luteal phase of the ewe. Theriogenology 51, 1351–1361.
CrossRef | PubMed |

Walker, S. K. , Smith, D. H. , Frensham, A. , Ashman, R. J. , and Seamark, R. F. (1989). The use of synthetic gonadotropin releasing hormone treatment in the collection of sheep embryos. Theriogenology 31, 741–752.
CrossRef |

Wehrman, M. E. , Fike, K. E. , Melvin, E. J. , Kojima, F. N. , and Kinder, J. E. (1997). Development of a persistent ovarian follicle and associated elevated concentrations of 17β-estradiol preceding ovulation does not alter the pregnancy rate after embryo transfer in cattle. Theriogenology 47, 1413–1421.
CrossRef |

Wiemer, K. E. , Cassey, P. L. , McFarland, C. W. , and Godke, R. A. (1988). Superovulatory response of split-embryo twin heifers. Theriogenology 29, 328.
CrossRef |

Willadsen, S. M. , Polge, C. , Rowson, L. E. A. , and Moor, R. M. (1976). Deep freezing of sheep embryos. J. Reprod. Fertil. 46, 151–154.
CrossRef | PubMed |

Wilmut, I. (1972). The effect of cooling rate, warming rate, cryoprotective agent and stage of development on survival of mouse embryos during freezing and thawing. Life Sci. 11, 1071–1079.
CrossRef |

Wollen, T. S. , Schultz, R. H. , and Newkirk, H. L. (1985). Use and handling of drugs and biologicals in embryo transfer. Theriogenology 23, 31–43.
CrossRef |

Wright, R. W. , Bondioli, K. , Grammer, J. , Kuzan, F. , and Menino, A. (1981). FSH or FSH plus LH superovulation in ewes following estrus synchronization with medroxyprogesterone acetate pessaries. J. Anim. Sci. 52, 115–118.
PubMed |



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