Relationships between maternal hormone secretion and embryo development on day 5 of pregnancy in dairy cows

doi:10.1016/j.anireprosci.2004.12.007

Animal Reproduction Science

Volume 88, Issues 3–4, September 2005, Pages 179-189

https://doi.org/10.1016/j.anireprosci.2004.12.007 Get rights and content

Abstract

In cattle, increasing early embryonic losses are associated with inadequate progesterone concentrations within the first three weeks of pregnancy. The aim of this study was to investigate the complex relationship between early maternal progesterone concentration and embryo development early within the first week of pregnancy, specifically, on day 5 post-oestrus in dairy cows. Twenty Holstein–Friesian cows at the end of lactation were inseminated at oestrus (day 0) and on day 5 post-oestrus cows were slaughtered and the reproductive tract flushed to determine the presence and stage of embryo development. Three cows that had failed to synchronise correctly were excluded from analysis while in the remaining 17 cows 11 (65%) were pregnant with embryos at the morula (n = 3), 9–16 (n = 3) and 8-cell (n = 5) stages of development. No differences in day 5 plasma progesterone concentrations or corpus luteum (CL) size or progesterone content were observed between pregnant (n = 11) and non-pregnant (n = 6) cows. In cows with embryos beyond the 8-cell stage of development (n = 6) plasma progesterone concentration (P < 0.001) and CL weight (P < 0.01) were higher and plasma insulin concentrations lower (P < 0.001) than in cows with 8-cell embryos (n = 5). In addition there was a negative relationship between plasma progesterone and plasma insulin in pregnant cows (R² = 0.65; P < 0.005). In cows with an embryo present in the oviduct, oviductal glucose concentrations were lower (P < 0.05) than in cows with no embryo present. These results confirm progesterone is not only directly associated with embryo development, but that it may indirectly modulate embryo development via changes in the oviductal environment. In summary, the association between maternal progesterone concentration and embryo development exists as early as day 5 of pregnancy in dairy cows.

Introduction

Studies of the extent and timing of early embryo mortality in the dairy cow indicate that at least 25% of embryos are lost during the first three weeks of pregnancy (Sreenan and Diskin, 1986, Peters, 1996). Despite extensive research, the reasons for this phenomenon are still poorly understood. A number of factors have been implicated including poor oocyte quality, defects within the embryo, an inadequate maternal environment, asynchrony between embryo and mother and failure of the mother to respond appropriately to embryonic signals. Studies suggest the time at which the embryo enters the uterus (around days 4–5; Guillomot, 1995) to be critical, since embryo mortality has been found to occur by day 5 post-oestrus in the dairy cow (Ayalon, 1978, Wiebold, 1988).

During early pregnancy, progesterone influences the endometrial secretion of nutrients, growth factors, immunosuppressive agents, enzymes, ions and steroids that are essential for embryo development (Graham and Clarke, 1997) and a number of studies have demonstrated lower maternal progesterone concentrations during the first three weeks of pregnancy in those cows in which mating is unsuccessful (see Mann et al., 1999). Further studies have also established a link between lower maternal progesterone concentrations and reduced embryo development with poor development accompanied by both a delayed post-ovulatory plasma progesterone rise and reduced progesterone concentrations (Mann and Lamming, 2001). Other studies in beef cows have shown that administration of progesterone can advance embryo development (Garrett et al., 1988) further emphasising the importance of progesterone in the control of early embryo development. Consistent increases in pregnancy rate are only achieved when administration of progesterone to mated cows is initiated during the first week of pregnancy (Mann and Lamming, 1999). Furthermore, in a large field trial, Starbuck et al. (2001) identified a close relationship between the concentration of milk progesterone on day 5 after mating and the outcome of early pregnancy indicating that the post-ovulatory progesterone rise may be the critical factor of maternal progesterone secretion controlling early embryo development.

In dairy cows, a relationship has been established between maternal progesterone concentration on day 5 after mating and the degree of embryo development on day 16 of pregnancy (Mann and Lamming, 2001). The objective of the present study was to determine if a relationship between maternal progesterone and embryo development could be identified as early as day 5 of pregnancy.

Section snippets

Experimental protocol

The study was undertaken in 20 Holstein–Friesian cows of 1st to 9th parity (mean 3.7 ± 0.5) obtained from the University of Nottingham commercial herd between September and February in accordance with the Animals (Scientific Procedures) Act, 1986. All the cows were at the end of lactation, on average 374 ± 32 days post-partum.

Oestrous cycles were synchronised by two intramuscular injections of 50 μg of the prostaglandin F_2α analogue, Cloprostenol (Estrumate; Schering-Plough Animal Health Welwyn

Statistical analyses

Pregnant animals were defined as those animals in which an intact embryo was recovered at the expected stage of development while non-pregnant animals were those in which empty zona pellucidae, unfertilised oocytes or no embryonic structure was found. For all analyses, data from non-pregnant animals were always analysed both including and excluding those animals in which no embryonic structures were found. Unless stated, no difference between the two data sets was identified with respect to the

Ovulation and pregnancy rate

Twenty animals were initially synchronised, although three animals were excluded from all subsequent analysis as they failed to develop a functional CL and had undetectable plasma progesterone concentrations by day 5 post-oestrus. Of the remaining 17 cows, viable embryos (n = 15) were recovered from 11 cows (65%). These animals had embryos at the morula (n = 3 cows), 8–16 cell (n = 3 cows) and 8-cell (n = 5 cows) stages of development. Embryos at the morula stage of development were recovered from the

Discussion

In the present study, we have demonstrated a relationship between maternal progesterone concentration and the stage of early embryo development on day 5 of pregnancy in dairy cows. This extends the findings of an earlier study in which a relationship was established between maternal progesterone and the degree of embryo development on day 16 (Mann and Lamming, 2001).

The role of progesterone as the key hormone in the maintenance of pregnancy is well established. The time at which divergence in

Acknowledgements

This work was supported by a research grant from the Ministry of Agriculture, Fisheries and Food. MPG was supported by a studentship from MAFF.

References (42)

J. Chagas e Silva et al.
Embryo yield and plasma progesterone profiles in superovulated dairy cows and heifers
Anim. Reprod. Sci.
(2002)
J.J. Ireland et al.
Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum
J. Dairy Sci.
(1980)
S.F. Larson et al.
Reduced fertility associated with low progesterone postbreeding and increased milk urea nitrogen in lactating cows
J. Dairy Sci.
(1997)
G.M. Lindner et al.
Bovine embryo morphology and evaluation
Theriogenology
(1983)
G.E. Mann
Conception rates during experimentation in dairy cows
Vet. J.
(2001)
G.E. Mann et al.
Plasma oestradiol and progesterone during early pregnancy in the cow and the effects of treatment with Buserelin™
Anim. Reprod. Sci.
(1995)
J.G. Thompson
In vitro culture and embryo metabolism of cattle and sheep embryos: a decade of achievement
Anim. Reprod. Sci.
(2000)
J.S. Walton et al.
Relationships between time of day, estrous behaviour, and the preovulatory luteinizing hormone surge in Holstein cows after treatment with cloprostenol
J. Dairy Sci.
(1987)
D.G. Armstrong et al.
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.
(2001)
R. Augustin et al.
Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos
Mol. Reprod. Dev.
(2001)

N. Ayalon

A review of embryo mortality in cattle

J. Reprod. Fertil.

(1978)

T. Dominko et al.

Timing of meiotic progression in bovine oocytes and its effect on early embryo development

Mol. Reprod. Dev.

(1997)

R.E. Erb et al.

Profiles of reproductive hormones associated with fertile and nonfertile inseminations of dairy cows

Theriogenology

(1976)

J.E. Garrett et al.

Evidence for maternal regulation of early conceptus growth and development in beef cattle

J. Reprod. Fertil.

(1988)

J.D. Graham et al.

Physiological action of progesterone in target tissues

Endocr. Rev.

(1997)

M. Guillomot

Cellular interactions during implantation in domestic ruminants

J. Reprod. Fert. Suppl.

(1995)

P.J. Hansen

Embryonic mortality from the embryo's perspective

J. Anim. Sci.

(2001)

R.L. Krisher et al.

Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence

Mol. Reprod. Dev.

(1999)

A.S. Law et al.

Evidence for the action of bovine follicular fluid factor(s) other than inhibin in suppressing follicular development and delaying oestrus in heifers

J. Reprod. Fertil.

(1992)

Genstat 5 Release 4.1

(1997)

H.J. Leese et al.

Pyruvate and glucose uptake by mouse ova and preimplantation embryos

J. Reprod. Fertil.

(1984)

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¹: Present address: Department of Animal Sciences, University of Missouri, 920 East Campus Drive, Columbia, MO 65211, USA.

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Relationships between maternal hormone secretion and embryo development on day 5 of pregnancy in dairy cows

Abstract

Introduction

Section snippets

Experimental protocol

Statistical analyses

Ovulation and pregnancy rate

Discussion

Acknowledgements

Anim. Reprod. Sci.

J. Dairy Sci.

J. Dairy Sci.

Theriogenology

Vet. J.

Anim. Reprod. Sci.

Anim. Reprod. Sci.

J. Dairy Sci.

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.

Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos

Mol. Reprod. Dev.

A review of embryo mortality in cattle

J. Reprod. Fertil.

Timing of meiotic progression in bovine oocytes and its effect on early embryo development

Mol. Reprod. Dev.

Profiles of reproductive hormones associated with fertile and nonfertile inseminations of dairy cows

Theriogenology

Evidence for maternal regulation of early conceptus growth and development in beef cattle

J. Reprod. Fertil.

Physiological action of progesterone in target tissues

Endocr. Rev.

Cellular interactions during implantation in domestic ruminants

J. Reprod. Fert. Suppl.

Embryonic mortality from the embryo's perspective

J. Anim. Sci.

Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence

Mol. Reprod. Dev.

Evidence for the action of bovine follicular fluid factor(s) other than inhibin in suppressing follicular development and delaying oestrus in heifers

J. Reprod. Fertil.

Genstat 5 Release 4.1

Pyruvate and glucose uptake by mouse ova and preimplantation embryos

J. Reprod. Fertil.