Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T14:55:34.024Z Has data issue: false hasContentIssue false
  • English
  • Français

The consequences of metabolic changes in high-yielding dairy cows on oocyte and embryo quality*

Published online by Cambridge University Press:  01 August 2008

J. L. M. R. Leroy ,
A. Van Soom ,
G. Opsomer  and
P. E. J. Bols
J. L. M. R. Leroy*
Affiliation:
Laboratory for Veterinary Physiology, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium
A. Van Soom
Affiliation:
Department of Reproduction, Fertility and Herd Health; Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
G. Opsomer
Affiliation:
Department of Reproduction, Fertility and Herd Health; Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
P. E. J. Bols
Affiliation:
Laboratory for Veterinary Physiology, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium
*
E-mail: jo.leroy@ua.ac.be
Get access

Abstract

Unsatisfactory reproductive performance in dairy cows, such as reduced conception rates, in addition to an increased incidence of early embryonic mortality, is reported worldwide and has been associated with a period of negative energy balance (NEB) early post partum. Typically, NEB is associated with biochemical changes such as high non-esterified fatty acid (NEFA), high β-hydroxybutyrate (β-OHB) and low glucose concentrations. The concentrations of these and other metabolites in the follicular fluid (FF) of high-yielding dairy cows during NEB were determined and extensively analyzed, and then were replicated in in vitro maturation models to investigate their effect on oocyte quality. The results showed that typical metabolic changes during NEB are well reflected in the FF of the dominant follicle. However, the oocyte seems to be relatively isolated from extremely elevated NEFA or very low glucose concentrations in the blood. Nevertheless, the in vitro maturation models revealed that NEB-associated high NEFA and low glucose levels in the FF are indeed toxic to the oocyte, resulting in deficient oocyte maturation and developmental competence. Induced apoptosis and necrosis in the cumulus cells was particularly obvious. Furthermore, maturation in saturated free fatty acid-rich media had a carry-over effect on embryo quality, leading to reduced cryotolerance of day 7 embryos. Only β-OHB showed an additive toxic effect in moderately hypoglycemic maturation conditions. These in vitro maturation models, based on in vivo observations, suggest that a period of NEB may hamper the fertility of high-yielding dairy cows through increased NEFA and decreased glucose concentrations in the FF directly affecting oocyte quality. In addition to oocyte quality, these results also demonstrate that embryo quality is reduced following an NEB episode. This important observation may be linked to the typical diet provided to stimulate milk yield, or to physiological adaptations sustaining the high milk production. Research into this phenomenon is ongoing.

Keywords

high-yielding dairy cowfertilityoocyteembryometabolism
Type
Full Paper
Information
animal , Volume 2 , Issue 8 , August 2008 , pp. 1120 - 1127
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.)

Footnotes

*

This invited paper was presented at BSAS meeting ‘Fertility in Dairy Cows – bridging the gaps’ 30–31 August 2007, Liverpool Hope University.

References

Abe, H, Hoshi, H 2003. Evaluation of bovine embryos produced in high performance serum-free media. Journal of Reproduction and Development 49, 193–202.Google Scholar
Abe, H, Yamashita, S, Itoh, T, Satoh, T, Hoshi, H 1999. Ultrastructure of bovine embryos developed from in vitro – matured and – fertilized oocytes: comparative morphological evaluation of embryos cultured either in serum-free medium or in serum-supplemented medium. Molecular Reproduction and Development 53, 325–335.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Argov, N, Arav, A, Sklan, D 2004. Number of oocytes obtained from cows by OPU in early, but not late lactation increased with plasma insulin and estradiol concentrations and expression of mRNA of the FSH receptor in granulosa cells. Theriogenology 61, 947–962.CrossRefGoogle Scholar
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
Bagavandoss, P, Midgley, AR, Wicha, M 1983. Developmental changes in the ovarian follicular basal lamina detected by immunofluorescence and electron microscopy. Journal of Histochemistry and Cytochemistry 31, 633–640.CrossRefGoogle ScholarPubMed
Baird, GD 1982. Primary ketosis in the high-producing dairy cows: clinical and subclinical disorders, treatment, prevention and outlook. Journal of Dairy Science 65, 1–10.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S, Kastelic, JP 2003. Factors affecting embryo survival and strategies to reduce embryonic mortality in cattle. Canadian Journal of Animal Science 83, 659–671.CrossRefGoogle Scholar
Bilodeau-Goeseels, S, Panich, P 2002. Effects of quality on development and transcriptional activity in early bovine embryos. Animal Reproduction Science 71, 143–155.CrossRefGoogle ScholarPubMed
Boland, MP, Lonergan, P, O’Callaghan, D 2001. Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 55, 1323–1340.CrossRefGoogle ScholarPubMed
Bols, PEJ, Vandenheede, JMM, Van Soom, A, de Kruif, A 1995. Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system. Theriogenology 43, 677–687.CrossRefGoogle ScholarPubMed
Bousquet, D, Bouchard, E, DuTremblay, D 2004. Decreasing fertility in dairy cows: myth or reality? Le Médecin Vétérinaire du Québec 34, 59–61.Google Scholar
Brevini, TAL, Cillo, F, Antonini, S, Gandolfi, F 2005. Effects of endocrine disruptors on the oocyte and embryos of farm animals. Reproduction in Domestic Animals 40, 291–299.CrossRefGoogle ScholarPubMed
Britt, JH 1992. Impacts of early postpartum metabolism on follicular development and fertility. Proceedings of the Annual Convention – American Association of Bovine Practitioners 24, 39–43.Google Scholar
Britt JH 1994. Follicular development and fertility: potential impacts of negative energy balance. Proceedings of the National Reproduction Symposium, Pittsburgh, PA, USA, pp. 103–112.Google Scholar
Butler, WR 1998. Effect of protein nutrition on ovarian and uterine physiology in dairy cattle. Journal of Dairy Science 81, 2533–2539.CrossRefGoogle ScholarPubMed
Butler, WR 2003. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livestock Production Science 83, 211–218.CrossRefGoogle Scholar
Cetica, P, Pintos, L, Dalvit, G, Beconi, M 2002. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.CrossRefGoogle ScholarPubMed
Chilliard, Y, Bocquier, F, Doreau, M 1998. Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction. Reproduction, Nutrition, Development 38, 131–152.CrossRefGoogle ScholarPubMed
Chung, BH, Tallis, GA, Cho, BH, Segrest, JP, Henkin, Y 1995. Lipolysis-induced partitioning of free fatty acids to lipoproteins: effect on the biological properties of free fatty acids. Journal of Lipid Research 36, 1956–1970.CrossRefGoogle ScholarPubMed
Cnop, M, Hannaert, JC, Hoorens, A, Eizirik, DL, Pipeleers, DG 2001. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 50, 1771–1777.CrossRefGoogle ScholarPubMed
Comin, A, Gerin, D, Cappa, A, Marchi, V, Renaville, R, Motta, M, Fazzini, U, Prandi, A 2002. The effect of an acute energy deficit on the hormone profile of dominant follicles in dairy cows. Theriogenology 58, 899–910.CrossRefGoogle ScholarPubMed
Cortvrindt, R, Smitz, J 2001. In vitro follicle growth: achievements in mammalian species. Reproduction in Domestic Animals 36, 3–9.CrossRefGoogle ScholarPubMed
De Wit, AAC, Cesar, MLF, Kruip, TAM 2001. Effect of urea during in vitro maturation on nuclear maturation and embryo development of bovine cumulus-oocyte-complexes. Journal of Dairy Science 84, 1800–1804.CrossRefGoogle ScholarPubMed
Ducker, MJ, Morant, SV, Fisher, WJ, Haggett, RA 1985. Nutrition and reproductive performance of dairy cattle. Animal Production 41, 13–22.Google Scholar
Duffield, T 2000. Subclinical ketosis in lactating dairy cattle. Veterinary Clinics of North America: Food Animal Practice 16, 231–253.Google ScholarPubMed
Dunne, LD, Diskin, MG, Boland, MP, O’Farrell, KJ, Sreenan, JM 1999. The effect of pre- and post-insemination plane of nutrition on embryo survival in beef heifers. Animal Science 69, 411–417.CrossRefGoogle Scholar
Edwards, RG 1974. Follicular fluid. Journal of Reproduction and Fertility 37, 189–219.CrossRefGoogle ScholarPubMed
Elrod, CC, Butler, WR 1993. Reduction of fertility and alteration of uterine pH in heifers fed excess ruminally degradable protein. Journal of Animal Science 71, 694–701.CrossRefGoogle ScholarPubMed
Fedorcsak, P, Storeng, R, Dale, PO, Tanbo, T, Abyholm, T 2000. Obesity is a risk factor for early pregnancy loss after IVF or ICSI. Acta Obstetricia et Gynecologica Scandinavica 79, 43–48.CrossRefGoogle ScholarPubMed
Fedorcsak, P, Dale, PO, Storeng, R, Ertzeid, G, Bjercke, S, Oldereid, N, Omland, AK, Abyholm, T, Tanbo, T 2004. Impact of overweight and underweight on assisted reproduction treatment. Human Reproduction 19, 2523–2528.Google Scholar
Folch, J, Lees, M, Sloane Stanley, GH 1957. A simple method for the isolation and purification of total lipids from animal tissue. Journal of Biological Chemistry 226, 497–509.CrossRefGoogle Scholar
Gosden, RG, Hunter, RHF, Telfer, E, Torrance, C, Brown, N 1988. Physiological factors underlying the formation of ovarian follicular fluid. Journal of Reproduction and Fertility 82, 813–825.CrossRefGoogle ScholarPubMed
Gutierrez, CG, Ralph, JH, Telfer, EE, Wilmut, I, Webb, R 2000. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biology of Reproduction 62, 1322–1328.CrossRefGoogle ScholarPubMed
Gwazdauskas, FC, Kendrick, KW, Pryor, AW, Bailey, TL 2000. Impact of follicular aspiration on folliculogenesis as influenced by dietary energy and stage of lactation. Journal of Dairy Science 83, 1625–1634.CrossRefGoogle ScholarPubMed
Hammon, DS, Holyoak, GR, Dhiman, TR 2005. Association between blood plasma urea nitrogen levels and reproductive fluid urea nitrogen and ammonia concentrations in early lactation dairy cows. Animal Reproduction Science 86, 195–204.CrossRefGoogle ScholarPubMed
Hansen, PJ, Soto, P, Natzke, RP 2004. Mastitis and fertility in cattle – possible involvement of inflammation or immune activation in embryonic mortality. American Journal of Reproductive Immunology 51, 294–301.CrossRefGoogle ScholarPubMed
Hashimoto, S, Minami, N, Yamada, M, Imai, H 2000. Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilisation: relevance to intracellular reactive oxygen species and glutathione contents. Molecular Reproduction and Development 56, 520–526.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Hayhurst C, Firth M, Christie MF and Royal MD 2007. Estimation of genetic variation in embryo quality: is there potential with the inherent ability to produce high quality embryos? Proceedings of the International Conference ‘Fertility in Dairy Cows, bridging the gaps’, 30–31 August 2007, Liverpool Hope University, UK [Abstract].Google Scholar
Herdt, TH 2000. Ruminant adaptation to negative energy balance. Veterinary Clinics of North America: Food Animal Practice 16, 215–230.Google ScholarPubMed
Hirabara, SM, de Oliveira Carvalho, CR, Mendonça, JR, Piltcher Haber, E, Fernandes, LC, Curi, R 2003. Palmitate acutely raises glycogen synthesis in rat soleus muscle by a mechanism that requires its metabolization (Randle cycle). FEBS Letters 541, 109–114.Google Scholar
Hoeben, D, Heyneman, R, Burvenich, C 1997. Elevated levels of beta-hydroxybutyric acid in periparturient cows and in vitro effect on respiratory burst activity of bovine neutrophils. Veterinary Immunology and Immunopathology 58, 165–170.Google Scholar
Hoeben, D, Monfardini, E, Opsomer, G, Burvenich, C, Dosogne, H, De Kruif, A, Beckers, JF 2000. Chemiluminescence of bovine polymorphonuclear leucocytes during the periparturient period and relation with metabolic markers and bovine pregnancy-associated glycoprotein. Journal of Dairy Research 67, 249–259.Google Scholar
Homa, ST, Brown, CA 1992. Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes. Journal of Reproduction and Fertility 94, 153–160.Google Scholar
Huszenicza, G, Janosi, S, Kulcsar, M, Korodi, P, Reiczigel, J, Katai, L, Peters, AR, De Rensis, F 2005. Effects of clinical mastitis on ovarian function in post-partum dairy cows. Reproduction in Domestic Animals 40, 199–204.CrossRefGoogle ScholarPubMed
Iwata, H, Inoue, J, Kimura, K, Kuge, T, Kuwayama, T, Monji, Y 2006. Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes. Animal Reproduction Science 91, 215–223.Google Scholar
Jorritsma, R, Groot, MW, Vos, PL, Kruip, TA, Wensing, T, Noordhuizen, JP 2003. Acute fasting in heifers as a model for assessing the relationship between plasma and follicular fluid NEFA concentrations. Theriogenology 60, 151–161.CrossRefGoogle Scholar
Jorritsma, R, Cesar, ML, Hermans, JT, Kruitwagen, CLJJ, Vos, PLAM, Kruip, TAM 2004. Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Animal Reproduction Science 81, 225–235.CrossRefGoogle ScholarPubMed
Kendrick, KW, Bailey, TL, Garst, AS, Pryor, AW, Ahmadzadeh, A, Akers, RM, Eyestone, WE, Pearson, RE, Gwasdauskas, FC 1999. Effects of energy balance on hormones, ovarian activity, and recovered oocytes in lactating Holstein cows using transvaginal follicular aspiration. Journal of Dairy Science 82, 1731–1740.CrossRefGoogle ScholarPubMed
Kenny, DA, Humpherson, PG, Leese, HJ, Morris, DG, Tomos, AD, Diskin, MG, Sreenan, JM 2002. Effect of elevated systemic concentrations of ammonia and urea on the metabolite and ionic composition of oviductal fluid in cattle. Biology of Reproduction 66, 1797–1804.Google Scholar
Krisher, RL, Bavister, BD 1998. Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.Google Scholar
Kruip TAM, Van Beek H, De Wit A and Postma A 1995. Quality of bovine oocytes in dairy cows post partum: consequences for embryo production in vivo and in vitro. Proceedings of the 11th conference of the ESET, 8–9 September 1995, Hannover, Germany, pp. 113–119.Google Scholar
Lacetera, N, Scalia, D, Bernabucci, U, Ronchi, B, Pirazzi, D, Nardone, A 2005. Lymphocyte function in overconditioned cows around parturition. Journal of Dairy Science 88, 2010–2016.Google Scholar
Leroy, JLMR, Vanholder, T, Delanghe, JR, Opsomer, G, Van Soom, A, Bols, PE, de Kruif, A 2004a. Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Animal Reproduction Science 80, 201–211.Google Scholar
Leroy, JLMR, Vanholder, T, Delanghe, JR, Opsomer, G, Van Soom, A, Bols, PE, Dewulf, J, de Kruif, A 2004b. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 62, 1131–1143.CrossRefGoogle ScholarPubMed
Leroy, JLMR, Vanholder, T, Mateusen, B, Christophe, A, Opsomer, G, de Kruif, A, Genicot, G, Van Soom, A 2005a. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.Google Scholar
Leroy, JLMR, Opsomer, G, De Vliegher, S, Vanholder, T, Goossens, L, Geldhof, A, Bols, PEJ, de Kruif, A, Van Soom, A 2005b. Comparison of embryo quality in high-yielding dairy cows, in dairy heifers and in beef cows. Theriogenology 64, 2022–2036.CrossRefGoogle ScholarPubMed
Leroy, JLMR, Genicot, G, Donnay, I, Van Soom, A 2005c. Evaluation of the lipid content in bovine oocytes and embryos with Nile red: a practical approach. Reproduction in Domestic Animals 40, 76–78.CrossRefGoogle ScholarPubMed
Leroy, JLMR, Vanholder, T, Opsomer, G, Van Soom, A, de Kruif, A 2006. The in vitro development of bovine oocytes after maturation in glucose and β-hydroxybutyrate concentrations associated with negative energy balance in dairy cows. Reproduction in Domestic Animals 41, 119–123.Google Scholar
Leroy JLMR, Van Soom A, Opsomer G, Goovaerts IGF and Bols PEJ 2008. Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high yielding dairy cows – Review. Reproduction in Domestic Animals, in press. Doi: 10.1111/j.1439-0531.2007.00961.CrossRefGoogle Scholar
Loeffler, SH, de Vries, MJ, Schukken, YH 1999. The effects of timing of disease occurrence, milk yield, and body condition on fertility of dairy cows. Journal of Dairy Science 82, 2589–2604.Google Scholar
Lozano, JM, Lonergan, P, Boland, MP, 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, 543–553.Google Scholar
Lu, ZH, Mu, Y, Wang, BA, Li, XL, Lu, JM, Li, JY, Pan, CY, Yanase, T, Nawata, H 2003. Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cells. Biochemical and Biophysical Research Communications 303, 1002–1007.Google Scholar
Lucy, MC 2001. Reproductive loss in high-producing dairy cattle: where will it end? Journal of Dairy Science 84, 1277–1293.CrossRefGoogle ScholarPubMed
Lucy, MC 2003. Mechanisms linking nutrition and reproduction in postpartum cows. Reproduction Supplement 61, 415–427.Google ScholarPubMed
Maedler, K, Spinas, GA, Dyntar, D, Moritz, W, Kaiser, N, Donath, MY 2001. Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 50, 69–76.Google Scholar
Mann, GE, Lamming, GE 2001. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121, 175–180.CrossRefGoogle ScholarPubMed
McEvoy, TG, Robinson, JJ, Aitken, RP, Findlay, PA, Palmer, RM, Robertson, IS 1995. Dietary-induced suppression of pre-ovulatory progesterone concentrations in superovulated ewes impairs the subsequent in vivo and in vitro development of their ova. Animal Reproduction Science 39, 89–107.Google Scholar
Moallem, U, Folman, Y, Bor, A, Arav, A, Sklan, D 1999. Effect of calcium soaps of fatty acids and administration of somatotropin on milk production, preovulatory follicular development, and plasma and follicular fluid lipid composition in high yielding dairy cows. Journal of Dairy Science 82, 2358–2368.CrossRefGoogle ScholarPubMed
Mu, YM, Yanase, T, Nishi, Y, Tanaka, A, Saito, M, Jin, CH, Mukasa, C, Okabe, T, Nomura, M, Goto, K, Nawata, H 2001. Saturated FFAs, palmitic acid and stearic acid induce apoptosis in human granulosa cells. Endocrinology 142, 3590–3597.CrossRefGoogle ScholarPubMed
O’Callaghan, D, Boland, MP 1999. Nutritional effects on ovulation. Animal Science 68, 299–314.CrossRefGoogle Scholar
Ocon, OM, Hansen, PJ 2003. Disruption of bovine oocytes and preimplantation embryos by urea and acidic pH. Journal of Dairy Science 86, 1194–1200.CrossRefGoogle ScholarPubMed
Opsomer, G, Coryn, M, Deluyker, H, de Kruif, A 1998. An analysis of ovarian dysfunction in high yielding dairy cows after calving based on progesterone profiles. Reproduction in Domestic Animals 33, 193–204.Google Scholar
Pasquali, R, Pelusi, C, Genghini, S, Cacciari, M, Gambineri, A 2003. Obesity and reproductive disorders in women. Human Reproduction Update 9, 359–372.Google Scholar
Rajala-Schultz, PJ, Gröhn, YT 2001. Comparison of economically optimized culling recommendations and actual culling decisions of Finnish Ayrshire cows. Preventive Veterinary Medicine 49, 29–39.Google Scholar
Reis, A, Rooke, JA, McCallum, GJ, Ewen, M, Staines, ME, Lomax, MA, McEvoy, TG 2003. Fatty acid content of polar and neutral lipids from bovine blastocysts produced in vitro in the presence or absence of serum. Reproduction, Abstract Series 30, 57–58 [abstract].Google Scholar
Rizos, D, Ward, F, Duffy, P, Boland, MP, 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. Molecular Reproduction and Development 61, 234–248.CrossRefGoogle ScholarPubMed
Rizos, D, Gutierrez-Adan, A, Perez-Garnelo, S, De La Fuente, J, Boland, MP, Lonergan, P 2003. Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biology of Reproduction 68, 236–243.Google Scholar
Rooke, JA, Ewen, M, Reis, A, McEvoy, TG 2006. Comparison of the fatty acid contents of bovine follicular fluid, granulose cells and cumulus enclosed or denuded oocytes. Reproduction in Domestic Animals 41, 306.Google Scholar
Royal, M, Mann, GE, Flint, APF 2000. Strategies for reversing the trend towards subfertility in dairy cattle. The Veterinary Journal 160, 53–60.CrossRefGoogle ScholarPubMed
Sartorelli, P, Paltrinieri, S, Comazzi, S 2000. Non-specific immunity and ketone bodies. II. In vitro studies on adherence and superoxide anion production in ovine neutrophils. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 47, 1–8.CrossRefGoogle Scholar
Sartori, R, Sartor-Bergfelt, R, Mertens, SA, Guenther, JN, Parrish, JJ, Wiltbank, MC 2002. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. Journal of Dairy Science 85, 2803–2812.Google Scholar
Sata, R, Tsujii, H, Abe, H, Yamashita, S, Hoshi, H 1999. Fatty acid composition of bovine embryos cultured in serum-free and serum containing medium during early embryonic development. The Journal of Reproduction and Development 45, 97–103.CrossRefGoogle Scholar
Sato, H, Matsumoto, M, Hanasaka, S 1999. Relations between plasma acetate, 3-hydroxybutyrate, FFA, glucose levels and energy nutrition in lactating dairy cows. Journal of Veterinary Medical Science 61, 447–451.Google Scholar
Shehab-El-Deen MA, Leroy JLMR, Maes D and Van Soom A 2008. Cryotolerance of Bovine Blastocysts is affected by Oocyte Maturation in Media Containing Palmitic or Stearic Acid. Reproduction in Domestic Animals, in press.Google Scholar
Shimabukuro, M, Zhou, YT, Levi, M, Unger, RH 1998. Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proceedings of the National Academy of Sciences of the United States of America 95, 2498–2502.Google Scholar
Sinclair, KD, Sinclair, LA, Robinson, JJ 2000. Nitrogen metabolism and fertility in cattle: I. Adaptive changes in intake and metabolism to diets differing in their rate of energy and nitrogen release in the rumen. Journal of Animal Science 78, 2659–2669.Google Scholar
Snijders, SE, Dillon, P, O’Callaghan, D, Boland, MP 2000. Effect of genetic merit, milk yield, body condition and lactation number on in vitro oocyte development in dairy cows. Theriogenology 53, 981–989.Google Scholar
Sutton-McDowall, ML, Gilchrist, RB, Thompson, JG 2004. Cumulus expansion and glucose utilization by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.Google Scholar
Tanghe, S, Van Soom, A, Nauwynck, H, Coryn, M, de Kruif, A 2002. Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Molecular Reproduction and Development 61, 414–424.CrossRefGoogle ScholarPubMed
Vanholder, T, Leroy, JLMR, Van Soom, A, Opsomer, G, Maes, D, Coryn, M, de Kruif, A 2005. Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Animal Reproduction Science 87, 33–44.Google Scholar
Walters, AH, Bailey, TL, Pearson, RE, Gwazdauskas, FC 2002. Parity-related changes in bovine follicle and oocyte populations, oocyte quality, and hormones to 90 days postpartum. Journal of Dairy Science 85, 824–832.CrossRefGoogle ScholarPubMed
Wehrman, ME, Welsh, TH, Williams, GL 1991. Diet-induced hyperlipidemia in cattle modifies the intrafollicular cholesterol environment, modulates ovarian follicular dynamics, and hastens the onset of postpartum luteal activity. Biology of Reproduction 45, 514–522.CrossRefGoogle ScholarPubMed
Wiltbank, MC, Sartori, R, Sangsritavong, S, Lopez, H, Haughian, JM, Fricke, PM, Gumen, A 2001. Novel effects of nutrition on reproduction in lactating dairy cows. Journal of Dairy Science 84 (Suppl.), 32 [abstract].Google Scholar
Wise, T 1987. Biochemical analysis of bovine follicular fluid: albumin, total protein, lysosomal enzymes, ions, steroids and ascorbic acid content in relation to follicular size, rank, atresia classification and day of estrous cycle. Journal of Animal Science 64, 1153–1169.Google Scholar
Wrenzycki, C, De Sousa, P, Overström, EW, Duby, RT, Herrmann, D, Watson, AJ, Niemann, H, O’Callaghan, D, Boland, MP 2000. Effects of superovulated heifer diet type and quantity on relative mRNA abundances and pyruvate metabolism in recovered embryos. Journal of Reproduction and Fertility 118, 69–78.Google Scholar
Zamboni, L 1974. Fine morphology of the follicle cell-oocyte association. Biology of Reproduction 10, 125–149.Google Scholar