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Undernutrition affects embryo quality of superovulated ewes

Published online by Cambridge University Press:  09 October 2013

J.A. Abecia ,
F. Forcada ,
I. Palacín ,
L. Sánchez-Prieto ,
C. Sosa ,
A. Fernández-Foren  and
A. Meikle
J.A. Abecia*
Affiliation:
Dept Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Miguel Servet 177, 500013, Zaragoza, Spain.
F. Forcada
Affiliation:
Dept Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
I. Palacín
Affiliation:
Dept Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
L. Sánchez-Prieto
Affiliation:
Dept Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
C. Sosa
Affiliation:
Dept de Anatomía Patológica, Medicina Legal y Forense y Toxicología, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
A. Fernández-Foren
Affiliation:
Laboratorio de Técnicas Nucleares, Universidad de la República, Montevideo, Uruguay.
A. Meikle
Affiliation:
Laboratorio de Técnicas Nucleares, Universidad de la República, Montevideo, Uruguay.
*
All correspondence to: José-Alfonso Abecia. Dept Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Facultad de Veterinaria, Miguel Servet 177, 500013, Zaragoza, Spain. Tel: +34 876554159. e-mail: [email protected]
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Summary

To determine the effect of undernutrition on embryo production and quality in superovulated sheep, 45 ewes were allocated into two groups to be fed diets that provided 1.5 (control, C; n = 20) or 0.5 (low nutrition, L; n = 25) times daily requirements for maintenance, from oestrous synchronization with intravaginal sponges to embryo collection. Embryos were collected 7 days after the onset of oestrus (day 0). Low nutrition resulted in lower live weight and body condition at embryo collection (P < 0.05). Diet (P < 0.01) and day of sampling (P < 0.001) significantly affected plasma non-esterified fatty acid (NEFA) and insulin concentrations. Plasma leptin concentrations decreased on day 7 only in L ewes. A significant effect of dietary treatment (P < 0.05) and day (P < 0.0001) was observed on plasma insulin-like growth factor (IGF)-I concentrations. The number of recovered oocytes and embryos did not differ between the groups (L: 15.4 ± 0.4; C: 12.4 ± 0.4). Recovery rate was lower (P < 0.05) in the L (60%) than in the C group (73%). The total number of embryos and number of viable-transferable embryos (5.0 ± 0.3 and 3.4 ± 0.3 embryos, respectively) of the L group were lower (P < 0.1) when compared with controls (8.4 ± 0.4 and 6.2 ± 0.4 embryos, respectively). Undernutrition during the period of superovulation and early embryonic development reduced total and viable number of embryos. These effects might be mediated by disruption of endocrine homeostasis, oviduct environment and/or oocyte quality.

Keywords

EmbryoSheepSuperovulationUndernutrition
Type
Research Article
Information
Zygote , Volume 23 , Issue 1 , February 2015 , pp. 116 - 124
Copyright
Copyright © Cambridge University Press 2013 

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References

Abecia, J.A., Rhind, S.M., Bramley, T.A. & McMillen, S.R. (1995). Steroid production and LH receptor concentrations of ovarian follicles and corpora lutea and associated rates of ova wastage in ewes given high and low levels of food intake before and after mating. Anim. Sci. 60, 57–62.Google Scholar
Abecia, J.A., Lozano, J.M. & Forcada, F. (1999). A preliminary study on the effects of dietary energy and melatonin on the ex vivo production of progesterone and prostaglandin F-2 alpha by the corpora lutea and endometrial tissue of ewes. Vet. Res. Comm. 23, 115–21.CrossRefGoogle Scholar
Abecia, J.A., Sosa, C., Forcada, F. & Meikle, A. (2006). The effect of undernutrition on the establishment of pregnancy in the ewe. Reprod. Nutr. Dev. 46, 367–78.Google Scholar
Agricultural and Food Research Council (1993). Energy and Protein Requirements of Ruminants. An Advisor Manual Prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK.Google Scholar
Armstrong, D.T. & Evans, G. (1983). Factors influencing success of embryo transfer in sheep and goats. Theriogenology 19, 31–42.CrossRefGoogle Scholar
Ashworth, C.J., Toma, L.M. & Hunter, M.G. (2009). Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Phil. Trans. R. Soc. B 364, 3351–61CrossRefGoogle ScholarPubMed
Blache, D., Chagas, L.M., Blackberry, M.A., Vercoe, P.E. & Martin, G.B. (2000). Metabolic factors affecting the reproductive axis in male sheep. J. Reprod. Fertil. 120, 1–11.Google Scholar
Boland, M.P., Lonergan, P. & O'Callaghan, D. (2001). Effect of nutrition on endocrine parameters, ovarian physiology & oocyte and embryo development. Theriogenology 55, 1323–40.CrossRefGoogle ScholarPubMed
Borowczyk, E.J.S., Caton, D.A., Redmer, J.J., Bilski, R.M., Weigl, K.A., Vonnahme, P.P., Borowicz, J.D., Kirsch, K.C., Kraft, L.P., Reynolds, & Grazul-Bilska, A.T. (2006). Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 84, 1593–9.Google Scholar
Butler, S.T., Marr, A.L., Pelton, S.H., Radcliff, R.P. & Lucy, M.C. (2003). Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. J. Endocrinol. 176, 205–17.CrossRefGoogle ScholarPubMed
Chilliard, Y., Delavaud, C. & Bonnet, M. (2005). Leptin expression in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domes. Anim. Endocrinol. 29, 3–22.CrossRefGoogle ScholarPubMed
Cognié, Y., Baril, G., Poulin, N. & Mermillod, P. (2003). Current status of embryo technologies in sheep and goat. Theriogenology 59, 171–88.CrossRefGoogle ScholarPubMed
Edey, T.N. (1968). Body weight and ovulation rate in sheep. Proc. Aust. Soc. Anim. Prod. 7, 188–91.Google Scholar
Elsasser, T.H., Klasing, K.C., Filipov, N. & Thompson, F. (2000). The metabolic consequences of stress: targets for stress and priorities of nutrient use. In The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. (eds Moberg, G.P. & Mench, J.A.) pp. 77–110. CAB International, Oxon, UK.Google Scholar
Fernández-Foren, A., Abecia, J.A., Vázquez, M.I., Forcada, F., Sartore, I., Carriquiry, M., Meikle, A. & Sosa, C. (2011). Food restriction in sheep: endocrine-metabolic response according to the level of body reserves. ITEA 107, 257–71.Google Scholar
Findlay, J.K. & Cumming, I.A (1976). FSH in the ewe: effects of season, live weight and plane of nutrition on plasma FSH and ovulation rate. Biol. Reprod. 15, 335–42.CrossRefGoogle ScholarPubMed
Forcada, F. & Abecia, J.A. (2006). The effect of nutrition on the seasonality of reproduction in ewes. Reprod. Nutr. Develop. 46, 355–65.CrossRefGoogle ScholarPubMed
Forcada, F., Abecia, J.A. & Sierra, I. (1992). Seasonal changes in oestrous activity and ovulation rate in Rasa Aragonesa ewes maintained at two different body condition levels. Small Rumin. Res. 8, 313–24.CrossRefGoogle Scholar
Forcada, F., Abecia, J.A., Lozano, J.M. & Zúñiga, O. (2000) Repeated superovulation of high-prolificacy Rasa Aragonesa ewes before culling as an inexpensive way to obtain high-quality embryos. Livest. Prod. Sci. 66, 263–9.CrossRefGoogle Scholar
Forcada, F., Ait-Amer-Meziane, M., Abecia, J.A., Maurel, M.C., Cebrián-Pérez, J.A., Muiño-Blanco, T., Asenjo, B., Vázquez, M.I. & Casao, A. (2011). Repeated superovulation using a simplified FSH/eCG treatment for in vivo embryo production in sheep. Theriogenology 75, 769–76.CrossRefGoogle ScholarPubMed
Geisert, R.D., Lee, C.Y., Simmen, F.A., Zavy, M.T., Fliss, A.E., Bazer, F.W. & Simmen, R.C.M. (1991). Expression of messenger RNAs encoding insulin-like growth factor-I, -II and insulin-like growth factor binding protein-2 in bovine endometrium during the estrous cycle and early pregnancy. Biol. Reprod. 45, 975–83.Google Scholar
Herrid, M., Nguyen, V.N., Hinch, G. & McFarlane, J.R. (2006). Leptin has concentration and stage-dependent effects on embryonic development in vitro. Reproduction 132, 247–56.CrossRefGoogle ScholarPubMed
Kakar, M.A., Maddocks, S., Lorime, M.F., Kleemann, D.O., Rudiger, S.R., Hartwich, K.M. & Walker, S.K. (2005). The effect of peri-conception nutrition on embryo quality in the superovulated ewe. Theriogenology 64, 1090–1103.Google Scholar
Kawamura, K., Sato, N., Fukuda, J., Kodama, H., Kumagai, J., Tanikawa, H., Nakamura, A. & Tanaka, T. (2002). Leptin promotes the development of mouse preimplantation embryos in vitro. Endocrinology 145, 1922–31.CrossRefGoogle Scholar
Kaye, P.L. (1997). Preimplantation growth factor physiology. Rev. Reprod. 2, 121–127.Google Scholar
Lozano, J.M., Abecia, J.A., Forcada, F., Zarazaga, L. & Alfaro, B. (1998). Effect of undernutrition on the distribution of progesterone in the uterus of ewes during the luteal phase of the oestrous cycle. Theriogenology 49, 539–46.Google Scholar
Lozano, J.M., Lonergan, P., Boland, M.P. & 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, 543–53.CrossRefGoogle ScholarPubMed
McEvoy, T.G., Robinson, J.J., Aitken, R.P., Findlay, P.A., Palmer, R.M. & Robertson, I.S. (1995). Dietary-induced suppression of preovulatory progesterone concentrations in superovulated ewes impairs the subsequent in-vivo and in-vitro development of their ova. Anim. Reprod. Sci. 39, 89–107.Google Scholar
Meikle, A., Sahlin, L., Ferraris, A., Masironi, B., Blanc, J.E., Rodríguez-Irazoqui, M., Rodríguez-Piñon, M., Kindahl, H. & Forsberg, M. (2001). Endometrial mRNA expression of estrogen and progesterone receptors and insuline-like growth factor-I (IGF-I) throughout the bovine estrous cycle. Anim. Reprod. Sci. 68, 45–56.Google Scholar
Muñoz-Gutiérrez, M., Findlay, P.A., Adam, C.L., Wax, G., Campbell, B.K., Kendall, N.R., Khalid, M., Forsberg, M. & Scaramuzzi, R.J. (2005). The ovarian expression of mRNAs for aromatase, IGF-I receptor, IGF-binding protein-2, -4 and -5, leptin and leptin receptor in cycling ewes after three days of leptin infusion. Reproduction 130, 1–14.Google Scholar
O'Callaghan, D., Yaakub, H., Hyttel, P., Spicer, L.J. & 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, 303–13.Google Scholar
Parr, R.A., Davis, I.F., Fairclough, R.J. & Miles, M.A. (1987). Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep. J. Reprod. Fertil. 80, 317–20.CrossRefGoogle ScholarPubMed
Parr, R.A., Davis, I.F., Miles, M.A. & Squires, T.J. (1993). Feed intake affects metabolic clearance rate of progesterone in sheep. Res. Vet. Sci. 55, 306–10.CrossRefGoogle ScholarPubMed
Peura, T.T., Kleemann, D.O., Rudiger, S.R., Nattrass, G.S., McLaughlan, C.J. & Walker, S.K. (2003). Effect of nutrition of oocyte donor on the outcomes of somatic cell nuclear transfer in the sheep. Biol. Reprod. 68, 45–50.CrossRefGoogle ScholarPubMed
Pisani, L.F., Antonini, S., Pocar, P., Ferrari, S., Brevini, T.A.L., Rhind, S.M. & Gandolfi, F. (2008). Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303–12.CrossRefGoogle ScholarPubMed
Rhind, S.M., McKelvey, W.A.C., McMillen, S., Gunn, R.G. & Elston, D.A. (1989). Effect of restricted food-intake, before and/or after mating, on the reproductive-performance of greyface ewes. Anim. Prod. 48, 149–55.Google Scholar
Rhoads, R.P., Kim, J.W., Leury, B.J., Baumgard, L.H., Segoale, N., Frank, S.J., Bauman, D.E. & Boisclair, Y.R. (2004). Insulin increases the abundance of the growth hormone receptor in liver and adipose tissue of periparturient cows. J. Nutr. 134, 1020–7.CrossRefGoogle Scholar
Russel, A.J.F., Doney, J.M. & Gunn, R.G. (1969). Subjective assessment of body fat in live sheep. J. Agric. Sci. 72, 451–4.Google Scholar
Ryan, J.P., Hunton, J.R. & Maxwell, W.M.C. (1991) Increased production of sheep embryos following superovulation of Merino ewes with a combination of pregnant mare serum gonadotrophin and follicle stimulating hormone. Reprod. Fertil. Dev. 3, 551–80.Google Scholar
Simonetti, L., Forcada, F., Rivera, O.E., Carou, N., Alberio, R.H., Abecia, J.A. & Palacin, I. (2008). Simplified superovulatory treatments in Corriedale ewes. Anim. Reprod. Sci. 104, 227–37.CrossRefGoogle ScholarPubMed
Smith, G.D., Jackson, L.M., Foster, D.L. (2002). Leptin regulation of reproductive function and fertility. Theriogenology 57, 73–86.Google Scholar
Sosa, C., Abecia, J.A., Forcada, F., Vinoles, C., Tasende, C., Valares, J.A., Palacin, I., Martin, G.B. & Meikle, A. (2006). Effect of undernutrition on uterine progesterone and oestrogen receptors and on endocrine profiles during the ovine oestrous cycle. Reprod. Fertil. Dev. 18, 447–58.Google Scholar
Sosa, C., Abecia, J.A., Carriquiry, M., Forcada, F., Martin, G.B., Palacin, I. & Meikle, A. (2009). Early pregnancy alters the metabolic responses to restricted nutrition in sheep. Domest. Anim. Endocrinol. 36, 13–23.Google Scholar
Sosa, C., Carriquiry, M., Chalar, C., Crespi, D., Sanguinetti, C., Cavestany, D. & Meikle, A. (2010a). Endometrial expression of members of the growth hormone – insulin-like growth factor system throughout the estrous cycle in heifers. Anim. Reprod. Sci. 122, 208–14.Google Scholar
Sosa, C., Gonzalez-Bulnes, A., Abecia, J.A., Forcada, F. & Meikle, A. (2010b). Short-term undernutrition affects final development of ovulatory follicles in sheep synchronized for ovulation. Reprod. Domest. Anim. 45, 1033–8.Google Scholar
Staigmiller, R.B., Short, R.E., Bellows, R.A. & Carr, J.B. (1979). Effect of nutrition on response to exogenous FSH in beef-cattle. J. Anim. Sci. 48, 1182–90.Google Scholar
Stevenson, K.R., Gilmour, R.S. & Wathes, D.C. (1994). Localization of insulin-like growth factor-I (IGF-I) and -II messenger ribonucleic acid and type 1 IGF receptors in the ovine uterus during the estrous cycle and early pregnancy. Endocrinology 134, 1655–64.Google Scholar
Swain, J.E., Bormann, C.L. & Krisher, R.L. (2001). Effects of leptin on porcine oocyte maturation and embryo in vitro. Biol. Reprod. 1, 212.Google Scholar
Van Hoeck, V., Sturmey, R.G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H.J., Bols, P.E. & Leroy, J.L. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS ONE 6, e23183CrossRefGoogle ScholarPubMed
Viñoles, C., Martin, G.B., Forsberg, M., Cajarville, C. & Meikle, A. (2004). Effect of short-term nutritional supplementation on leptin and IGF-I concentrations in Corriedale ewes. Reprod. Fertil. Dev. 16, 526.Google Scholar
Webb, R., Garnsworthy, P.C., Gong, J.G. & Armstrong, D.G. (2004). Control of follicular growth: Local interactions and nutritional influences. J. Anim. Sci. 82, 63–74.Google Scholar
Winterberger-Torres, S. & Sevellec, C. (1987). Atlas of the Early Development of the Sheep Embryo. INRA, Paris, France.Google Scholar