Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Oocyte competence in repeat-breeder heifers: effects of an optimized ovum pick-up schedule on expression of oestrus, follicular development and fertility

Renée Båge A D , Sudsaijai Petyim A , Birgitta Larsson A , Triin Hallap A B , Ann-Sofi Bergqvist A , Hans Gustafsson A C and Heriberto Rodríguez-Martínez A
+ Author Affiliations
- Author Affiliations

A Centre for Reproductive Biology in Uppsala (CRU), Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, PO Box 7039, SE-750 07 Uppsala, Sweden.

B Department of Reproductive Biology, Estonian Agricultural University, Tartu, Estonia.

C Swedish Dairy Association, Hållsta, SE-631 84 Eskilstuna, Sweden.

D To whom correspondence should be addressed. email: renee.bage@og.slu.se

Reproduction, Fertility and Development 15(2) 115-123 https://doi.org/10.1071/RD02094
Submitted: 7 November 2002  Accepted: 8 April 2003   Published: 8 April 2003

Abstract

Repeat-breeder heifers (RBH) have been shown to present reproductive perturbations during spontaneous cyclicity, which affects oestrus and ovulation. Some of these disturbances (e.g. deviating hormone patterns) are also present during and after cycles of twice-weekly ovum pick-up (OPU), performed according to an optimized schedule allowing normal oestrous cyclicity. In the present study, the effects of OPU on oocyte competence in in vitro maturation (IVM) and in vitro fertilization (IVF) have been evaluated, as were the effects on expression of oestrus and fertility in five RBH (≥4 artificial inseminations) and five virgin heifers (VH controls). In total, 269 RBH and 174 VH oocytes were scored for quality prior to IVM and IVF. The number of follicles available for puncture was higher in RBH, but the oocyte recovery rate after OPU was lower in RBH compared with VH controls and the recovered RBH oocytes were of lower quality, as judged by their appearance at retrieval. Confocal laser scanning and transmission electron microscopy of immature oocytes did not reveal any differences between RBH and VH control oocytes with respect to nuclear and mitochondrial status. However, after IVM, the cytoplasmic spatial reorganization of mitochondria and cortical granules was less advanced in RBH, which could contribute to the subfertility that defines the syndrome. Cleavage rates after IVF were similar in RBH and VH controls. Subsequent to the OPU period, in vivo fertility after controlled artificial insemination was comparable with field fertility rates in both RBH and VH.

Extra keywords: artificial insemination


Acknowledgments

The authors thank Mrs Å. Jansson and Mr H. Ekwall for excellent technical assistance and Mr P. Öhagen for valuable statistical help. The study received financial support from FORMAS and SLF, Stockholm.


References

Ahmad, N. , Schrick, F. N. , Butcher, R. L. , and Inskeep, E. K. (1995). Effect of persistent follicles on early embryonic losses in beef cows Biol. Reprod. 52, 1129–35.
PubMed |

Albihn, A. , Gustafsson, H. , Rodriguez-Martinez, H. , and Larsson, K. (1989). Development of day 7 bovine demi-embryos transferred into virgin and repeat-breeder heifers Anim. Reprod. Sci. 21, 161–76.
Crossref | GoogleScholarGoogle Scholar |

Albihn, A. , Gustafsson, H. , and Rodriguez-Martinez, H. (1991a). Maternal influence on the early development of asynchronously transferred bovine embryos Anim. Reprod. Sci. 24, 25–35.
Crossref | GoogleScholarGoogle Scholar |

Albihn, A. , Shamsuddin, M. , Qunshan, H. , and Kindahl, H. (1991b). Plasma levels of prostaglandin F2α metabolite and progesterone in repeat breeder heifers Acta Vet. Scand. 32, 361–71.
PubMed |

Assey, R. J. , Hyttel, P. , Greve, T. , and Purwantara, B. (1994). Oocyte morphology in dominant and subordinate follicles Mol. Reprod. Dev. 37, 335–44.
PubMed |

Austin, C. R. (1956). Cortical granules in hamster eggs Exp. Cell Res. 10, 533–40.
PubMed |

Ayalon, N. (1984). The repeat breeding problem. In Proceedings of the Xth International Congress of Animal Reproduction and Artificial Insemination IL, USA.  pp. 41–50. (Abstract.)

Båge, R. (2003). Fertility in Swedish red and white dairy heifers: relationship with progesterone concentrations at AI Reprod. Dom. Anim. 38,(in press)
Crossref | GoogleScholarGoogle Scholar |

Båge, R. , Bosu, W. T. K. , and Rodríguez-Martínez, H. (2001a). Ovarian follicle apoptosis at the onset of standing estrus in virgin and repeat breeder dairy heifers Theriogenology 56, 699–712.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Båge, R., Petyim, S., Larsson, B., Gustafsson, H., Forsberg, M., and  Rodríguez-Martínez, H. (2001b). Repeated OPU on day 0 to 12 of the cycle for the use of dairy heifers as both oocyte donors and embryo recipients. In Vienna, Austria. (Eds. H. Rodríguez-Martínez)  pp. 50. (Blackwell: Edinburgh, UK.) (Abstract.)

Båge, R. , Gustafsson, H. , Larsson, B. , Forsberg, M. , and Rodríguez-Martínez, H. (2002a). Repeat breeding in dairy heifers: follicular dynamics and oestrous cycle characteristics in relation to sexual hormone patterns Theriogenology 57, 2257–69.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Båge, R. , Masironi, B. , Sahlin, L. , and Rodríguez-Martínez, H. (2002b). Deviant peri-oestrual hormone patterns affect the uterine tube epithelium in repeat-breeder heifers Reprod. Fertil. Dev. 14, 461–9.
PubMed |

Bavister, B. D. , and Squirrel, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos Hum. Reprod. 15, 189–98.
Crossref | GoogleScholarGoogle Scholar |

Bruyas, J. F. , Fieni, F. , and Tainturier, D. (1993). Le syndrome ‘repeat breeding’: Analyse bibliographique, 1ere partie: étiologie Rev. Méd. Vét. 144, 385–98.


Clancy, B. , and Cauller, L. J. (1998). Reduction of background auto-fluorescence in brain sections following immersion in sodiumborohydride J. Neurosci. Methods 83, 97–102.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Crosignani, P. G. , Vegetti, W. , Colombo, M. , and Ragni, G. (2002). Resumption of fertility with diet in overweight women Reprod. Biomed. Online 5, 60–4.
PubMed |

de Loos, F. , van Maurik, P. , van Beneden, T. , and Kruip, T. A. (1992). Structural aspects of bovine oocyte maturation in vitro Mol. Reprod. Dev. 31, 208–14.
PubMed |

Dieleman, S. J. , Kruip, Th. A. M. , Fontijne, P. , de Jong, W. H. R. , and van der Weiden, G. C. (1983). Changes in estradiol, progesterone and testosterone concentrations in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone J. Endocrinol. 97, 31–42.
PubMed |

Dieleman, S. J. , Hendriksen, P. J. M. , Viuff, D. , Thomsen, P. D. , Hyttel, P. , Knijn, H. M. , Wrenzycki, C. , Kruip, T. A. M. , Niemann, H. , Gadella, B. M. , Bevers, M. M. , and Vos, P. L. A. M. (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos Theriogenology 57, 5–20.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Duchens, M. , Forsberg, M. , Gustafsson, H. , Edqvist, L.-E. , and Rodriguez-Martinez, H. (1995). Reproductive performance of heifers induced to oestrus asynchrony by suprabasal plasma progesterone levels Anim. Reprod. Sci. 39, 171–82.
Crossref | GoogleScholarGoogle Scholar |

Erickson, B. H. (1966). Development and senescence of the postnatal bovine ovary J. Anim. Sci. 25, 800–5.
PubMed |

Gustafsson, H. , and Plöen, L. (1986). The morphology of 16-day and 17-day old bovine blastocysts from virgin and repeat breeder heifers Anat. Histol. Embryol. 15, 277–87.
PubMed |

Gustafsson, H. , Larsson, K. , Kindahl, H. , and Madej, A. (1986). Sequential endocrine changes and behaviour during estrus and metestrus in repeat breeder and virgin heifers Anim. Reprod. Sci. 19, 261–73.
Crossref | GoogleScholarGoogle Scholar |

Hendriksen, P. J. , Vos, P. L. , Steenweg, W. N. , Bevers, M. M. , and Dieleman, S. J. (2000). Bovine follicular development and its effect on the in vitro competence of oocytes Theriogenology 1, 11–20.
Crossref | GoogleScholarGoogle Scholar |

Hyttel, P. , Greve, T. , and Callesen, H. (1989). Ultrastructural aspects of oocyte maturation and fertilization in cattle J. Reprod. Fertil. Suppl. 38, 35–47.
PubMed |

Hyttel, P. , Fair, T. , Callesen, H. , and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle Theriogenology 47, 23–32.
Crossref | GoogleScholarGoogle Scholar |

Ireland, J. J. , and Roche, J. F. (1982). Development of antral follicles in cattle after prostaglandin-induced luteolysis: changes in serum hormones, steroid in follicular fluid, and gonadotrophin receptors Endocrinology 111, 2077–86.
PubMed |

Kruip, T. A. M. , Cran, D. G. , van Beneden, T. H. , and Dieleman, S. J. (1983). Structural changes in bovine oocytes during final maturation in vivo  Gamete Res. 8, 29–47.


Linares, T. (1982). Embryonic development in repeat breeder heifers and virgin heifers seven days after insemination Anim. Reprod. Sci. 4, 189–98.
Crossref | GoogleScholarGoogle Scholar |

Linares, T. , King, W. A. , and Plöen, L. (1980). Observations on the early development of embryos from repeat breeder heifers Nord. Vet. Med. 32, 433–43.
PubMed |

Lonergan, P. , Khatir, K. , Carolan, C. , and Mermillod, P. (1997). Bovine blasocyst production in vitro after inhibition of oocyte meiotic resumption for 24 h J. Reprod. Fertil. 109, 355–65.
PubMed |

Lonergan, P. , Dinnyes, A. , Fair, T. , Yang, X. , and Boland, M. (2000). Bovine oocyte and embryo development following meiotic inhibition with butyrolactone I Mol. Reprod. Dev. 57, 204–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Marquant-Le Guienne, B. (1999). Atlas of the bovine oocyte AETE Newsletter 10, 6–8.


Mermillod, P. , Oussaid, B. , and Cognie, Y. (1999). Aspects of follicular and oocyte maturation that affect the developmental potential of embryos J. Reprod. Fertil. Suppl. 54, 449–60.
PubMed |

Mermillod, P. , Tomanek, M. , Marchal, R. , and Meijer, L. (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity Mol. Reprod. Dev. 55, 89–95.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Mihm, M. , Curran, N. , Hyttel, 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.
PubMed |

Moor, R. M. , Dai, Y. , Lee, C. , and Fulka, J. (1998). Oocyte maturation and embryonic failure Hum. Reprod. Update 4, 223–36.
PubMed |

Parrish, J. J. , Susko-Parrish, J. , Minner, M. A. , and First, N. L. (1988). Capacitation of bovine sperm by heparin Biol. Reprod. 38, 1171–80.
PubMed |

Petyim, S. , Båge, R. , Forsberg, M. , Rodríguez-Martínez, H. , and Larsson, B. (2000). The effect of repeated follicular puncture on ovarian function in dairy heifers J. Vet. Med. Assoc. 47, 627–40.
Crossref | GoogleScholarGoogle Scholar |

Petyim, S. , Båge, R. , Hallap, T. , Bergqvist, A.-S. , Rodríguez-Martínez, H. , and Larsson, B. (2003). Two different schemes of twice-weekly ovum pick-up in dairy heifers: effect on oocyte recovery and ovarian function Theriogenology 60, 175–88.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pieterse, M. C. , Kappen, K. A. , Kruip, Th. A. M. , Wurth, Y. A. , Van Beneden, Th. M. , Willemse, A. H. , and Taverne, M. A. M. (1991). Transvaginal ultrasound-guided follicular aspiration of bovine oocytes Theriogenology 35, 19–24.
Crossref | GoogleScholarGoogle Scholar |

Ponderato, N. , Crott, G. , Turini, P. , Duchi, R. , Galli, C. , and Lazzari, G. (2002). Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF Mol. Reprod. Dev. 62, 513–18.
Crossref | GoogleScholarGoogle Scholar | PubMed |

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

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, 234–48.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Spörndly, R. (1995). Fodertabeller för idisslare [Nutrition requirement for ruminants]. Speciella skrifter, Swedish University of Agricultural Sciences, Department of Animal Nutrition and Management, Report 235 (Swedish University of Agricultural Sciences: Uppsala, Sweden.)

Sreenan, J. M. , and Diskin, M. G. (1983). Early embryonic mortality in the cow: its relationship with progesterone concentration Vet. Rec. 112, 517–21.
PubMed |

Tagliaferro, P. , Tandler, C. J. , Ramos, A. J. , Pecci Saavedra, J. , and Brusco, A. (1997). Immunofluorescence and glutaraldehyde fixation. A new procedure based on the Schiff-quenching method J. Neurosci. Methods 77, 191–7.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Takenouchi, N. , Hirao, Y. , Kosuke, I. , Shimizu, M. , Geshi, M. , and Nagai, T. (2001). The effect of inhibin immunization on the results of ovum pick up in Japanese Black cow Proc. Ann. Meeting Jpn. Soc. Anim. Reprod. 1, 71.(Abstract.)


Tanaka, H. , Hishinuma, M. , Takahashi, Y. , and Kanagawa, H. (1994). Developmental competence of oocytes from the ovaries of repeat-breeding cows after in vitro fertilization J. Vet. Med. Sci. 56, 547–8.
PubMed |

Wang, W. , Hosoe, M. , Li, R. , and Shioya, Y. (1997). Development of the competence of bovine oocytes to release cortical granules and block polyspermy after meiotic maturation Dev. Growth. Differ. 39, 607–15.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wu, G. M. , Sun, Q. Y. , Mao, J. , Lai, L. , McCauley, T. C. , Park, K. W. , Prather, R. S. , Didion, B. A. , and Day, B. N. (2002). High developmental competence of pig oocytes after meiotic inhibition with a specific m-phase promoting factor kinase inhibitor, butyrolactone I Biol. Reprod. 67, 170–7.
PubMed |