Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T21:57:55.588Z Has data issue: false hasContentIssue false
  • English
  • Français

Feeding frequency has diet-dependent effects on plasma hormone concentrations but does not affect oocyte quality in dairy heifers fed fibre- or starch-based diets

Published online by Cambridge University Press:  01 September 2008

J. A. Rooke ,
A. Ainslie ,
R. G. Watt ,
F. M. Alink ,
T. G. McEvoy ,
K. D. Sinclair ,
P. C. Garnsworthy  and
R. Webb
J. A. Rooke*
Affiliation:
Sustainable Livestock Systems, Scottish Agricultural College, Roslin Bio-Centre, Roslin, Midlothian EH25 9PS, UK
A. Ainslie
Affiliation:
Sustainable Livestock Systems, Scottish Agricultural College, Roslin Bio-Centre, Roslin, Midlothian EH25 9PS, UK
R. G. Watt
Affiliation:
Sustainable Livestock Systems, Scottish Agricultural College, Roslin Bio-Centre, Roslin, Midlothian EH25 9PS, UK
F. M. Alink
Affiliation:
Sustainable Livestock Systems, Scottish Agricultural College, Roslin Bio-Centre, Roslin, Midlothian EH25 9PS, UK
T. G. McEvoy
Affiliation:
Sustainable Livestock Systems, Scottish Agricultural College, Roslin Bio-Centre, Roslin, Midlothian EH25 9PS, UK
K. D. Sinclair
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
P. C. Garnsworthy
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
R. Webb
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
*
E-mail: john.rooke@sac.ac.uk
Get access

Abstract

The post-fertilisation developmental capacity of bovine oocytes recovered by ultrasound guided transvaginal follicular aspiration (ovum pick-up, OPU) is influenced by diet-induced changes in hormone and metabolite concentrations. The objectives of this experiment were first to determine whether post-prandial changes in hormone concentrations, induced by changing the frequency of feeding, influenced oocyte quality and second whether changes in plasma glucagon concentration were associated with oocyte quality. Using a 2 × 2 factorial design, Holstein heifers (six per treatment) were fed either fibre- or starch-based diets containing either 189 or 478 g starch/kg dry matter. The diets were offered in either two or four equal meals per day and supplied twice the maintenance energy requirement. Blood samples were obtained both at weekly intervals (three samples per heifer, collected before feeding) during the experiment and throughout an entire 24-h period (15 or 17 samples per heifer for twice or four times daily-fed heifers, respectively). Each heifer underwent six sessions of OPU (twice weekly) beginning 25 days after introduction of the diets. Oocyte quality was assessed by development to the blastocyst stage in synthetic oviductal fluid following in vitro fertilisation. Mean weekly plasma insulin concentrations did not differ between diets, but plasma glucagon concentrations were greatest when heifers were fed the starch-based diet twice daily compared with the other diets. When heifers were offered four meals per day, there were no meal-related changes in hormone concentrations. However, when heifers were offered two meals per day, plasma insulin concentration increased after feeding the starch-based, but not the fibre-based diet. Plasma glucagon concentration increased after meals when heifers were fed twice daily and the increase was substantially greater when the starch-based diet was fed. Treatments did not influence (overall mean with mean ± s.e.) ovarian follicle size distribution or oocyte recovery by OPU (6.2 ± 0.4 per heifer), the proportion of oocytes that cleaved following insemination (0.57 ± 0.030) or blastocyst yield (0.27 ± 0.027 of oocytes cleaved). In conclusion, by feeding diets differing in carbohydrate source at different frequencies of feeding, meal-related changes in plasma hormone profiles were altered significantly, but oocyte quality was not affected. Therefore effects of diet on oocyte quality appear not to be mediated by meal-related fluctuations in hormone concentrations.

Keywords

cowsoocyte qualitydietinsulinglucagon
Type
Full Paper
Information
animal , Volume 2 , Issue 9 , September 2008 , pp. 1361 - 1370
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acevedo, N, Ding, J, Cabrera, LM, Smith, GD 2006. Maternal hyperinsulinemia increases incidence of abnormal oocyte chromatin condensation and impairs oocyte developmental competence. Fertility and Sterility 86, S79.CrossRefGoogle Scholar
Adamiak, SJ, Mackie, K, Watt, RG, Webb, R, Sinclair, KD 2005. Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinaemia in cattle. Biology of Reproduction 73, 918–926.CrossRefGoogle ScholarPubMed
Adamiak, SJ, Powell, K, Rooke, JA, Webb, R, Sinclair, KD 2006. Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro. Reproduction 131, 247–258.CrossRefGoogle ScholarPubMed
Agricultural and Food Research Council 1993. Energy and Protein Requirements of Ruminants. An advisory manual prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK.Google Scholar
Armstrong, DG, Duclos, MJ, Goddard, C 1990. Biological activity of insulin-like growth factor-I purified from chicken serum. Domestic Animal Endocrinology 7, 383–393.CrossRefGoogle ScholarPubMed
Armstrong, DG, McEvoy, TG, Baxter, G, Robinson, JJ, Hogg, CO, Woad, KJ, Webb, R, Sinclair, KD 2001. Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system. Biology of Reproduction 64, 1624–1632.CrossRefGoogle ScholarPubMed
Armstrong, DG, Gong, JG, Webb, R 2003. Interactions between nutrition and ovarian activity in cattle: physiological, cellular and molecular mechanisms. In Reproduction in Domestic Ruminants V (ed. BK Campbell, R Webb, H Dobson and C Doberska), pp. 403–414. Society for Reproduction and Fertility, Cambridge, UK.Google Scholar
Bassett, JM 1975. Dietary and gastro-intestinal control of hormones regulating carbohydrate metabolism in ruminants. In Digestion and metabolism in the ruminant (ed. IW McDonald and ACI Warner), pp. 383–398. University of New England Publishing Unit, Armidale, Australia.Google Scholar
Blache, D, Tellam, RL, Chagas, LM, Blackberry, MA, Vercoe, PE, Martin, GB 2000. Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. Journal of Endocrinology 165, 625–637.CrossRefGoogle ScholarPubMed
Bradford, BJ, Gour, AD, Nash, AS, Allen, MS 2006. Propionate challenge tests have limited value for investigating bovine metabolism. Journal of Nutrition 136, 1915–1920.CrossRefGoogle ScholarPubMed
Chagas, LM, Bass, JJ, Blache, D, Burke, CR, Kay, JK, Lindsay, DR, Lucy, MC, Martin, GB, Meier, S, Rhodes, FM, Roche, JR, Thatcher, WW, Webb, R 2007. New perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing cows. Journal of Dairy Science 90, 4022–4032.CrossRefGoogle Scholar
Chamberlain, CS, Spicer, LJ 2001. Hormonal control of ovarian cell production of insulin-like growth factor binding proteins. Molecular and Cellular Endocrinology 182, 69–81.CrossRefGoogle ScholarPubMed
Chilliard, Y, Delavaud, C, Bonnet, M 2005. Leptin regulation in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domestic Animal Endocrinology 29, 3–22.CrossRefGoogle ScholarPubMed
Ehrhardt, RA, Slepetis, RM, Siegal-Willott, J, Van Amburgh, ME, Bell, AW, Boisclair, YR 2000. Development of a specific radioimmunoassay to measure physiological changes of circulating leptin in cattle and sheep. Journal of Endocrinology 166, 519–528.CrossRefGoogle ScholarPubMed
Fouladi-Nashta, AA, Gutierrez, CG, Gong, JG, Garnsworthy, PC, Webb, R 2007. Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biology of Reproduction 77, 9–17.CrossRefGoogle ScholarPubMed
French, N, Kennelly, JJ 1990. Effects of feeding frequency on ruminal parameters, plasma insulin, milk yield, and milk composition in Holstein cows. Journal of Dairy Science 73, 1857–1863.CrossRefGoogle ScholarPubMed
French, N, De Boer, G, Kennelly, JJ 1990. Effects of feeding frequency and exogenous somatotrophin on lipolysis, hormone profiles, and milk production in dairy cows. Journal of Dairy Science 73, 1552–1559.CrossRefGoogle ScholarPubMed
Genstat 2002. Release 6 Reference Manual. Oxford Science Publications. Clarendon Press, Oxford, UK.Google Scholar
Harmon, DL 1992. Impact of nutrition on pancreatic exocrine and endocrine secretion in ruminants: a review. Journal of Animal Science 70, 1290–1301.CrossRefGoogle ScholarPubMed
Kaneko, JJ 1989. Clinical biochemistry of domestic animals, 4th edition. Academic Press, London, UK.Google Scholar
Keane, MG, More O’Ferrall, GJ 1992. Comparison of Friesian, Canadian Hereford × Friesian and Simmental × Friesian steers for growth and carcass composition. Animal Production 55, 377–387.Google Scholar
Lents, CA, Wettemann, RP, White, FJ, Rubio, I, Ciccioli, NH, Spicer, LJ, Keisler, DH, Payton, ME 2005. Influence of nutrient intake and body fat on concentrations of insulin-like growth factor-I, insulin, thyroxine, and leptin in plasma of gestating beef cows. Journal of Animal Science 83, 586–596.CrossRefGoogle ScholarPubMed
Mann, GE, Green, MP, Sinclair, KD, Demmers, KJ, Fray, MD, Gutierrez, CG, Garnsworthy, PC, Webb, R 2003. Effects of circulating progesterone and insulin on early embryo development in beef heifers. Animal Reproduction Science 79, 71–79.CrossRefGoogle ScholarPubMed
McEvoy, TG, Robinson, JJ, Aitken, RP, Findlay, PA, Robertson, IS 1997. Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Animal Reproduction Science 47, 71–90.CrossRefGoogle ScholarPubMed
Morgan, CR, Lazerow, A 1963. Immunoassay of insulin: two antibody system. Plasma insulin levels in normal, subdiabetic and diabetic rats. Diabetes 12, 115–126.CrossRefGoogle Scholar
Nolan, R, O’Callaghan, D, Duby, RT, Lonergan, P, Boland, MP 1998. The influence of short-term nutrient changes on follicle growth and embryo production following superovulation in beef heifers. Theriogenology 50, 1263–1274.CrossRefGoogle ScholarPubMed
Owens, PC, Johnson, RJ, Campbell, RG, Ballard, FJ 1990. Growth hormone increases insulin-like growth factor-I (IGF-I) and decreases IGF-II in plasma of growing pigs. Journal of Endocrinology 124, 269–275.CrossRefGoogle ScholarPubMed
Robinson, JJ 1990. Nutrition in the reproduction of farm animals. Nutrition Research Reviews 3, 253–276.CrossRefGoogle ScholarPubMed
Sinclair, KD, Kuran, M, Gebbie, FE, Webb, R, McEvoy, TG 2000. Nitrogen metabolism and fertility in cattle. II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen. Journal of Animal Science 78, 2670–2680.CrossRefGoogle ScholarPubMed
Smith, DL, Stinefelt, BM, Blemings, KP, Wilson, ME 2006. Diet-induced alterations in progesterone clearance appear to be mediated by insulin signalling in hepatocytes. Journal of Animal Science 84, 1102–1109.CrossRefGoogle ScholarPubMed
Spicer, LJ, Chamberlain, CS 2000. Production of insulin-like growth factor-I by granulosa cells but not thecal cells is hormonally responsive in cattle. Journal of Animal Science 78, 2919–2926.CrossRefGoogle Scholar
Starr, JI, Horwitz, DL, Rubenstein, AH, Mako, ME 1979. Insulin, proinsulin and c-peptide. In Methods of hormone radioimmunoassay, 2nd edition (ed. BM Jaffer and HR Behman), pp. 613–633. Academic Press, London, UK.Google Scholar
Sutton, JD, Hart, IC, Morant, SV, Schuller, E, Simmonds, AD 1988. Feeding frequency for lactating cows: diurnal patterns of hormones and metabolites in peripheral blood in relation to milk-fat concentration. British Journal of Nutrition 60, 265–274.CrossRefGoogle ScholarPubMed
Taylor St, CS, Murray, JI 1991. Effect of feeding level, breed and milking potential on body tissues and organs of mature, non-lactating cows. Animal Production 53, 27–38.Google Scholar
Thorp, CL, Wylie, ARG, Steen, RWJ, Shaw, C, McEvoy, JD 2000. Effects of incremental changes in forage:concentrate ratio on plasma hormone and metabolite concentrations and products of rumen fermentation in fattening beef steers. Animal Science 71, 93–109.CrossRefGoogle Scholar
Webb, R, Garnsworthy, PC, Gong, JG, Armstrong, DG 2004. Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science 82 (Suppl. E), E63–E74.Google ScholarPubMed
Yaakub, H, O’Callaghan, D, Boland, MP 1999. Effect of roughage type and concentrate supplementation on follicle numbers and in vitro fertilisation and development of oocytes recovered from beef heifers. Animal Reproduction Science 55, 1–12.CrossRefGoogle ScholarPubMed