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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of extending the length of pro-oestrus in an oestradiol- and progesterone-based oestrus synchronisation program on ovarian function, uterine environment and pregnancy establishment in beef heifers

J. J. de la Mata A B , R. Núñez-Olivera C , F. Cuadro C , D. Bosolasco C , V. de Brun D , A. Meikle D , G. A. Bó E F and A. Menchaca C G
+ Author Affiliations
- Author Affiliations

A Reproducción y Biotecnología Bovina, de la Mata-Veterinarios, Av. S. Marzo 245, PC 6300, Santa Rosa, La Pampa, Argentina.

B Facultad de Agronomía, Universidad Nacional de La Pampa, Ruta 35 Km 334, PC 6300, Santa Rosa, La Pampa, Argentina.

C Instituto de Reproducción Animal Uruguay, Fundación IRAUy, Cno. Cruz del Sur 2250, PC 12200, Montevideo, Uruguay.

D Facultad de Veterinaria, Lasplaces 1550, PC 11600, Montevideo, Uruguay.

E Instituto de Reproducción Animal Córdoba, Pozo del Tigre, PC 5145, Córdoba, Argentina.

F Instituto A. P. de Ciencias Basicas y Aplicadas, Universidad Nacional de Villa María, O. Ferreyra 411, PC 5963, Villa del Rosario, Córdoba, Argentina.

G Corresponding author. Email: menchaca.alejo@gmail.com

Reproduction, Fertility and Development 30(11) 1541-1552 https://doi.org/10.1071/RD17473
Submitted: 4 November 2017  Accepted: 25 April 2018   Published: 21 May 2018

Abstract

The aim of the present study was to investigate the effects of a strategy for extending pro-oestrus (the interval between luteolysis and ovulation) in an oestrus synchronisation protocol (named J-Synch) in beef heifers on follicular growth, sexual steroid concentrations, the oestrogen receptor ERα and progesterone receptors (PR) in the uterus, insulin-like growth factor (IGF) 1 and pregnancy rates. In Experiment 1, heifers treated with the new J-Synch protocol had a longer pro-oestrus period than those treated with the conventional protocol (mean (± s.e.m.) 93.7 ± 12.9 vs 65.0 ± 13.7 h respectively; P < 0.05). The rate of dominant follicle growth from the time of progesterone device removal to ovulation was greater in heifers in the J-Synch than conventional group (P < 0.05). Luteal area and serum progesterone concentrations were greater in the J-Synch Group (P < 0.05) for the 12 days after ovulation. Progesterone receptor (PGR) staining on Day 6 after ovulation in the uterine stroma was lower in the J-Synch than conventional group (P < 0.05), and the expression of PR gene (PGR) and IGF1 gene tended to be lower in J-Synch-treated heifers (P < 0.1). In Experiment 2 (n = 2349), the pregnancy rate 30–35 days after fixed-time AI (FTAI) was greater for heifers in the J-Synch than conventional group (56.1% vs 50.7% respectively). In conclusion, our strategy for extending pro-oestrus (i.e. the J-Synch protocol) significantly improves pregnancy establishment in beef heifers. This improvement was related to an increased rate of growth of the dominant ovulatory follicle, greater progesterone concentrations during the ensuing luteal phase and different uterine patterns of PGR and IGF1, which may have favoured embryo development and pregnancy establishment.

Additional keywords: artificial insemination, corpus luteum, endometrium, follicle.


References

Araújo, E. R., Sponchiado, M., Pugliesi, G., Van Hoeck, V., Mesquita, F. S., Membrive, C. M. B., and Binelli, M. (2016). Spatio-specific regulation of endocrine-responsive gene transcription by periovulatory endocrine profiles in the bovine reproductive tract. Reprod. Fertil. Dev. 28, 1533–1544.
Spatio-specific regulation of endocrine-responsive gene transcription by periovulatory endocrine profiles in the bovine reproductive tract.Crossref | GoogleScholarGoogle Scholar |

Astessiano, A. L., Pérez-Clariget, R., Quintans, G., Soca, P., and Carriquiry, M. (2012). Effects of a short-term increase in the nutritional plane before the mating period on metabolic and endocrine parameters, hepatic gene expression of insulin receptors and components of the somatotropic axis in growing Holstein heifers. J. Anim. Physiol. Anim. Nutr. (Berl.) 96, 535–544.
Effects of a short-term increase in the nutritional plane before the mating period on metabolic and endocrine parameters, hepatic gene expression of insulin receptors and components of the somatotropic axis in growing Holstein heifers.Crossref | GoogleScholarGoogle Scholar |

Binelli, M., Pugliesi, G., Hoeck, V. V., Sponchiado, M., Ramos, R. S., Oliveira, M. L., França, M. R., D’Alexandri, F. L., Mesquita, F. S., and Membrive, C. M. B. (2014). The role of proestrus on fertility and postovulatory uterine function in the cow. Anim. Reprod. 11, 246–253.

Bisinotto, R. S., and Santos, J. E. P. (2012). The use of endocrine treatments to improve pregnancy rates in cattle. Reprod. Fertil. Dev. 24, 258–266.
The use of endocrine treatments to improve pregnancy rates in cattle.Crossref | GoogleScholarGoogle Scholar |

Bó, G. A., Peres, L. C., Cutaia, L. E., Pincinato, D., Baruselli, P. S., and Mapletoft, R. J. (2012). Treatments for the synchronisation of bovine recipients for fixed-time embryo transfer and improvement of pregnancy rates. Reprod. Fertil. Dev. 24, 272–277.
Treatments for the synchronisation of bovine recipients for fixed-time embryo transfer and improvement of pregnancy rates.Crossref | GoogleScholarGoogle Scholar |

Bó, G. A., Baruselli, P. S., and Mapletoft, R. J. (2013). Synchronization techniques to increase the utilization of artificial insemination in beef and dairy cattle. Anim. Reprod. 10, 137–142.

Bó, G. A., de la Mata, J. J., Baruselli, P. S., and Menchaca, A. (2016). Alternative programs for synchronizing and resynchronizing ovulation in beef cattle. Theriogenology 86, 388–396.
Alternative programs for synchronizing and resynchronizing ovulation in beef cattle.Crossref | GoogleScholarGoogle Scholar |

Boos, A., Meyer, W., Schwarz, R., and Grunert, E. (1996). Immunohistochemical assessment of estrogen receptor and progesterone receptor distribution in biopsy samples of the endometrium collected throughout the estrus cycle. Anim. Reprod. Sci. 44, 11–21.
Immunohistochemical assessment of estrogen receptor and progesterone receptor distribution in biopsy samples of the endometrium collected throughout the estrus cycle.Crossref | GoogleScholarGoogle Scholar |

Bridges, G. A., Helser, L. A., Grum, D. E., Mussard, M. L., Gasser, C. L., and Day, M. L. (2008). Decreasing the interval between GnRH and PGF2α from 7 to 5 days and lengthening proestrus increases timed-AI pregnancy rates in beef cows. Theriogenology 69, 843–851.
Decreasing the interval between GnRH and PGF from 7 to 5 days and lengthening proestrus increases timed-AI pregnancy rates in beef cows.Crossref | GoogleScholarGoogle Scholar |

Bridges, G. A., Mussard, M. L., Burke, C. R., and Day, M. L. (2010). Influence of the length of proestrus on fertility and endocrine function in female cattle. Anim. Reprod. Sci. 117, 208–215.
Influence of the length of proestrus on fertility and endocrine function in female cattle.Crossref | GoogleScholarGoogle Scholar |

Bridges, G. A., Mussard, M. L., Pate, J. L., Ott, T. L., Hansen, T. R., and Day, M. L. (2012). Impact of preovulatory estradiol concentrations on conceptus development and uterine gene expression. Anim. Reprod. Sci. 133, 16–26.
Impact of preovulatory estradiol concentrations on conceptus development and uterine gene expression.Crossref | GoogleScholarGoogle Scholar |

Bridges, G. A., Day, M. L., Geary, T. W., and Cruppe, L. H. (2013). Deficiencies in the uterine environment and failure to support embryonic development. J. Anim. Sci. 91, 3002–3013.
Deficiencies in the uterine environment and failure to support embryonic development.Crossref | GoogleScholarGoogle Scholar |

Bridges, G. A., Mussard, M. L., Hesler, L. A., and Day, M. L. (2014). Comparison of follicular dynamics and hormone concentrations between the 7-day and 5-day CO-Synch + CIDR program in primiparous beef cows. Theriogenology 81, 632–638.
Comparison of follicular dynamics and hormone concentrations between the 7-day and 5-day CO-Synch + CIDR program in primiparous beef cows.Crossref | GoogleScholarGoogle Scholar |

Carter, F., Forde, N., Duffy, P., Wade, M., Fair, T., Crowe, M. A., Evans, A. C. O., Kenny, D. A., Roche, J. F., and Lonergan, P. (2008). Effect of increasing progesterone from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod. Fertil. Dev. 20, 368–375.
Effect of increasing progesterone from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers.Crossref | GoogleScholarGoogle Scholar |

Day, M. L. (2015). State of the art of GnRH-based timed AI in beef cattle. Anim. Reprod. 79, 1–4.

de Brun, V., Carriquiry, M., Meikle, A., Forcada, F., Casal, A., and Sosa, C. (2015). Periconceptional undernutrition modifies endocrine profiles and hepatic gene expression in sheep. J. Anim. Physiol. Anim. Nutr. (Berl.) 99, 710–718.
Periconceptional undernutrition modifies endocrine profiles and hepatic gene expression in sheep.Crossref | GoogleScholarGoogle Scholar |

de la Mata, J. J., and Bó, G. A. (2012). Sincronización de celos y ovulación utilizando protocolos de benzoato de estradiol y GnRH en períodos reducidos de inserción de un dispositivo con progesterona en vaquillonas para carne. Taurus 55, 17–23.

Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., and Robledo, C. W. (2017). InfoStat versión 2017. (Grupo InfoStat, FCA, Universidad Nacional de Córdoba: Córdoba, Argentina.) Available at http://www.infostat.com.ar [verified 1 May 2017].

Diskin, M. G., Walters, S. M., Parr, M. H., and Kenny, D. A. (2016). Pregnancy losses in cattle: potential for improvement. Reprod. Fertil. Dev. 28, 83–93.
Pregnancy losses in cattle: potential for improvement.Crossref | GoogleScholarGoogle Scholar |

Forde, N., and Lonergan, P. (2012). Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle? J. Reprod. Dev. 58, 189–195.
Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle?Crossref | GoogleScholarGoogle Scholar |

Forde, N., Carter, F., Fair, T., Crowe, M. A., Evans, A. C. O., Spencer, T. E., Bazer, F. W., McBride, R., Boland, M. P., O’Gaora, P., Lonergan, P., and Roche, J. F. (2009). Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol. Reprod. 81, 784–794.
Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle.Crossref | GoogleScholarGoogle Scholar |

Forde, N., Beltman, M. E., Duffy, G. B., Duffy, P., Mehta, J. P., O’Gaora, P., Roche, J. F., Lonergan, P., and Crowe, M. A. (2011). Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for the conceptus elongation. Biol. Reprod. 84, 266–278.
Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for the conceptus elongation.Crossref | GoogleScholarGoogle Scholar |

Guzeloglu, A., Bilby, T. R., Meikle, A., Kamimura, S., Kowalski, A., Michel, F., MacLaren, L. A., and Tatcher, W. W. (2004). Pregnancy and bovine somatotropin in nonlactating dairy cows. II. Endometrial gene expression related to maintenance of pregnancy. J. Dairy Sci. 87, 3268–3279.
Pregnancy and bovine somatotropin in nonlactating dairy cows. II. Endometrial gene expression related to maintenance of pregnancy.Crossref | GoogleScholarGoogle Scholar |

Herd, D. B., and Sprott, L. R. (1986). ‘Body Condition, Nutrition and Reproduction of Beef Cows.’ (Texas Agricultural Extension Service, Texas A&M University: Texas.)

Iner-Jensen, N., and McCracken, J. A. (1981). The transfer of progesterone in the ovarian vascular pedicle of the sheep. Endocrinology 109, 685–690.
The transfer of progesterone in the ovarian vascular pedicle of the sheep.Crossref | GoogleScholarGoogle Scholar |

Inskeep, E. K. (2004). Preovulatory, postovulatory, and postmaternal recognition effects of concentrations of progesterone on embryonic survival in the cow. J. Anim. Sci. 82, E24–E39.
Preovulatory, postovulatory, and postmaternal recognition effects of concentrations of progesterone on embryonic survival in the cow.Crossref | GoogleScholarGoogle Scholar |

Kastelic, J. P., Bergfelt, D. R., and Ginther, O. J. (1990). Relationship between ultrasonic assessment of the corpus luteum and plasma progesterone concentration in heifers. Theriogenology 33, 1269–1278.
Relationship between ultrasonic assessment of the corpus luteum and plasma progesterone concentration in heifers.Crossref | GoogleScholarGoogle Scholar |

Kerbler, T. L., Buhr, M. M., Jordan, L. T., Leslie, K. E., and Walton, J. S. (1997). Relationship between maternal plasma progesterone concentration and interferon-tau synthesis by the conceptus in cattle. Theriogenology 47, 703–714.
Relationship between maternal plasma progesterone concentration and interferon-tau synthesis by the conceptus in cattle.Crossref | GoogleScholarGoogle Scholar |

Kimmins, S., and MacLaren, L. A. (2001). Oestrous cycle and pregnancy effects on the distribution of oestrogen and progesterone receptors in bovine endometrium. Placenta 22, 742–748.
Oestrous cycle and pregnancy effects on the distribution of oestrogen and progesterone receptors in bovine endometrium.Crossref | GoogleScholarGoogle Scholar |

Knopf, L., Kastelic, J. P., Schallenberger, E., and Ginther, O. J. (1989). Ovarian follicular dynamics in heifers: test of two wave hypothesis by ultrasonically monitoring individual follicles. Domest. Anim. Endocrinol. 6, 111–119.
Ovarian follicular dynamics in heifers: test of two wave hypothesis by ultrasonically monitoring individual follicles.Crossref | GoogleScholarGoogle Scholar |

Larimore, E. L., Amundson, O. L., Bird, S. L., Funnell, B. J., Kruse, S. G., Bridges, G. A., and Perry, G. A. (2015). Influence of estrus at fixed-time artificial insemination on early embryonic development in beef cattle. J. Anim. Sci. 93, 2806–2812.
Influence of estrus at fixed-time artificial insemination on early embryonic development in beef cattle.Crossref | GoogleScholarGoogle Scholar |

Lonergan, P., Forde, N., and Spencer, T. (2016). Role of progesterone in embryo development in cattle. Reprod. Fertil. Dev. 28, 66–74.
Role of progesterone in embryo development in cattle.Crossref | GoogleScholarGoogle Scholar |

Madsen, C. A., Perry, G. A., Mogck, C. L., Daly, R. F., MacNeil, M. D., and Geary, T. W. (2015). Effects of preovulatory estradiol on embryo survival and pregnancy establishment in beef cows. Anim. Reprod. Sci. 158, 96–103.
Effects of preovulatory estradiol on embryo survival and pregnancy establishment in beef cows.Crossref | GoogleScholarGoogle Scholar |

Mann, G. E. (2009). Corpus luteum size and plasma progesterone concentrations in cows. Anim. Reprod. Sci. 115, 296–299.
Corpus luteum size and plasma progesterone concentrations in cows.Crossref | GoogleScholarGoogle Scholar |

McNeill, R. E., Sreenan, J. M., Diskin, M. G., Cairns, M. T., Fitzpatrick, R., Smith, T. J., and Morris, D. G. (2006). Effect of systemic progesterone concentration on the expression of progesterone-responsive genes in the bovine endometrium during early luteal phase. Reprod. Fertil. Dev. 18, 573–583.
Effect of systemic progesterone concentration on the expression of progesterone-responsive genes in the bovine endometrium during early luteal phase.Crossref | GoogleScholarGoogle Scholar |

Meikle, A., Sahlin, L., Ferraris, A., Masironi, B., Blanc, J. E., Rodríguez-Irazoqui, M., Rodríguez-Piñón, M., Kindahl, H., and Forsber, M. (2001). Endometrial mRNA expression of oestrogen receptor α and insulin-like growth factor-I (IGF-I) throughout the bovine oestrous cycle. Anim. Reprod. Sci. 68, 45–56.
Endometrial mRNA expression of oestrogen receptor α and insulin-like growth factor-I (IGF-I) throughout the bovine oestrous cycle.Crossref | GoogleScholarGoogle Scholar |

Menchaca, A., Dutra, S., Carrau, J. M., Sapriza, F., Salazar, J., and Bó, G. A. (2016). Improvements of the new J-Synch protocol used for fixed time embryo transfer (FTET) in beef cattle recipients transferred with in vitro produced embryos. In ‘Proceeding of the 18th International Congress on Animal Reproduction (ICAR)’, 26–30 June 2016, Tours. (Eds P. Mermillod.) p. 506 [Abstract]. (ICAR: 2016.)

Mesquita, F. S., Pugliese, G., Scolari, S. C., França, M. R., Ramos, R. S., Oliveira, M., Papa, M. C., Meirelles, M. M., Silva, L. A., Nogueira, G. P., Membrive, C. M. B., and Binelli, M. (2014). Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows. Theriogenology 81, 861–869.
Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows.Crossref | GoogleScholarGoogle Scholar |

Moreno, D., Cutaia, L., Villata, L., Otisi, F., and Bó, G. A. (2001). Follicle wave emergence in beef cows treated with progesterone releasing devices, estradiol y progesterone. Theriogenology 55, 408.

Okumu, L. A., Forde, N., Fahey, A. G., Fitzpatrick, E., Roche, J. F., Crowe, M. A., and Lonergan, P. (2010). The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. Reproduction 140, 143–153.
The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus.Crossref | GoogleScholarGoogle Scholar |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar |

Ré, M., de la Mata, J. J., and Bó, G. A. (2014). Synchronization of ovulation in dairy heifers using a shortened estradiol-based protocol that provides for a lengthened proestrus. Reprod. Fertil. Dev. 26, 118.
Synchronization of ovulation in dairy heifers using a shortened estradiol-based protocol that provides for a lengthened proestrus.Crossref | GoogleScholarGoogle Scholar |

Santos, J. E. P., Narciso, C. D., Rivera, F., Tatcher, W. W., and Chebel, R. C. (2010). Effect of reducing the period of follicle dominance in a timed artificial insemination protocol on reproduction of dairy cows. J. Dairy Sci. 93, 2976–2988.
Effect of reducing the period of follicle dominance in a timed artificial insemination protocol on reproduction of dairy cows.Crossref | GoogleScholarGoogle Scholar |

Sosa, C., Abecia, J. A., Carriquiry, M., Vázquez, M. I., Fernández-Foren, A., Talmon, M., Forcada, F., and Meikle, A. (2009). Effect of undernutrition on the uterine environment during maternal recognition of pregnancy in sheep. Reprod. Fertil. Dev. 21, 869–881.
Effect of undernutrition on the uterine environment during maternal recognition of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |

Sosa, C., Carriquiry, M., Chalar, C., Crespi, D., Sanguinetti, C., Cavestany, D., and Meikle, A. (2010). Endometrial expression of leptin receptor and members of the growth hormone–insulin-like growth factor system throughout the estrous. Anim. Reprod. Sci. 122, 208–214.
Endometrial expression of leptin receptor and members of the growth hormone–insulin-like growth factor system throughout the estrous.Crossref | GoogleScholarGoogle Scholar |

Spencer, T. E., Johnson, G. A., Bazer, F. W., Burghardt, R. C., and Palmarini, M. (2007). Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod. Fertil. Dev. 19, 65–78.
Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses.Crossref | GoogleScholarGoogle Scholar |

Spencer, T. E., Forde, N., and Lonergan, P. (2017). Insights into conceptus elongation and establishment of pregnancy in ruminants. Reprod. Fertil. Dev. 29, 84–100.
Insights into conceptus elongation and establishment of pregnancy in ruminants.Crossref | GoogleScholarGoogle Scholar |

Uslenghi, G., Vater, A., Rodíguez Aguilar, S., Vabodevila, J., and Callejas, S. (2016). Effect of estradiol cypionate and GnRH treatment on plasma estradiol-17β concentrations, synchronization of ovulation and on pregnancy rates in suckled beef cows treated with FTAI-based protocols. Reprod. Domest. Anim. 51, 693–699.
Effect of estradiol cypionate and GnRH treatment on plasma estradiol-17β concentrations, synchronization of ovulation and on pregnancy rates in suckled beef cows treated with FTAI-based protocols.Crossref | GoogleScholarGoogle Scholar |

Vasconcelos, J. L. M., Sartori, R., Oliveira, H. N., Guenther, J. G., and Wiltbank, M. C. (2001). Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology 56, 307–314.
Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate.Crossref | GoogleScholarGoogle Scholar |

Wijayagunawardane, M. P. B., Miyamoto, A., Cerbito, W. A., Acosta, T. J., Takagi, M., and Sato, K. (1998). Local distribution of oviductal estradiol, progesterone, prostaglandins, oxytocin ad endothelin-1 in the cyclic cow. Theriogenology 49, 607–618.
Local distribution of oviductal estradiol, progesterone, prostaglandins, oxytocin ad endothelin-1 in the cyclic cow.Crossref | GoogleScholarGoogle Scholar |