Dietary fat supplementation and the consequences for oocyte and embryo quality: Hype or significant benefit for dairy cow reproduction?

Reproduction in Domestic Animals

Volumn 49, Issue 3, 2014, Pages 353-361

  Leroy, J L M R ^a   Sturmey, R G ^b   Van Hoeck, V ^a   De Bie, J ^a   Mckeegan, P J ^b   Bols, P E J ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOS;

FAT INTAKE; LIPID;

ADMINISTRATION AND DOSAGE; ANIMAL; ANIMAL EMBRYO; ANIMAL FOOD; BOVINAE; CHEMISTRY; DAIRYING; DIET; EMBRYOLOGY; ENERGY METABOLISM; FAT INTAKE; FEMALE; GROWTH, DEVELOPMENT AND AGING; OOCYTE; OVARY; OVARY FOLLICLE; PHYSIOLOGY; PROCEDURES; REPRODUCTION; TRENDS; UTERUS; VETERINARY;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CATTLE; DAIRYING; DIET; DIETARY FATS; EMBRYO, MAMMALIAN; ENERGY METABOLISM; FEMALE; LIPIDS; OOCYTES; OVARIAN FOLLICLE; OVARY; REPRODUCTION; UTERUS;

EID: 84899917946     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/rda.12308     Document Type: Article

References (121)

1. Aardema H, Vos PL, Lolicato F, Roelen BA, Knijn HM, Vaandrager AB, Helms JB, Gadella BM, 2011: Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod 85, 62-69.
2. 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 hyperinsulinemia in cattle. Biol Reprod 73, 918-926.
3. 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.
4. Andersen JB, Ridder C, Larsen T, 2008: Priming the cow for mobilization in the periparturient period: effects of supplementing the dry cow with saturated fat or linseed. J Dairy Sci 91, 1029-1043.
5. Armstrong DG, Gong JG, Webb R, 2002: Interactions between nutrition and ovarian activity in cattle: physiological, cellular and molecular mechanisms. Reproduction 61, 403-414.
6. Ashworth CJ, Toma LM, Hunter MG, 2009: Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B Biol Sci 364, 3351-3361.
7. Awasthi H, Saravia F, Rodriguez-Martinez H, Bage R, 2010: Do cytoplasmic lipid droplets accumulate in immature oocytes from over-conditioned repeat breeder dairy heifers? Reprod Domest Anim 45, E194-E198.
8. Ballou MA, Gomes RC, Juchem SO, DePeters EJ, 2009: Effects of dietary supplemental fish oil during the peripartum period on blood metabolites and hepatic fatty acid compositions and total triacylglycerol concentrations of multiparous Holstein cows. J Dairy Sci 92, 657-669.
9. Barceló-Fimbres M, Seidel GE, 2011: Cross-validation of techniques for measuring lipid content of bovine oocytes and blastocysts. Theriogenology 75, 434-444.
10. Bauman DE, Perfield JW II, Harvatine KJ, Baumgard LH, 2008: Regulation of fat synthesis by conjugated linoleic acid: lactation and the ruminant model. J Nutr 138, 403-409.
11. Beam SW, Butler WR, 1997: Energy balance and ovarian follicle development prior to the first ovulation postpartum in dairy cows receiving three levels of dietary fat. Biol Reprod 56, 133-142.
12. Bilan PJ, Samokhvalov V, Koshkina A, Schertzer JD, Samaan MC, Klip A, 2009: Direct and macrophage-mediated actions of fatty acids causing insulin resistance in muscle cells. Arch Physiol Biochem 115, 176-190.
13. Bilby TR, Block J, do Amaral BC, Sa O, Silvestre FT, Hansen PJ, Staples CR, Thatcher WW, 2006a: Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer. J Dairy Sci 89, 3891-3903.
14. Bilby TR, Guzeloglu A, MacLaren LA, Staples CR, Thatcher WW, 2006b: Pregnancy, bovine somatotropin, and dietary n-3 fatty acids in lactating dairy cows: II. Endometrial gene expression related to maintenance of pregnancy. J Dairy Sci 89, 3375-3385.
15. Bilodeau-Goeseels S, Kastelic JF, 2003: Factors affecting embryo survival and strategies to reduce embryonic mortality in cattle. Can J Anim Sci 83, 659-671.
16. Bousquet D, Bouchard E, DuTremblay D, 2004: Decreasing fertility in dairy cows: myth or reality? Le Médecin Vétérinaire du Québec 34, 59-61.
17. Brickner AE, Pires JAA, Gressley TF, Grummer RR, 2009: Effects of abomasal lipid infusion on liver triglyceride accumulation and adipose lipolysis during fatty liver induction in dairy cows. J Dairy Sci 92, 4954-4961.
18. Butler WR, 2003: Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livest Prod Sci 83, 211-218.
19. Canfield RW, Sniffen CJ, Butler WR, 1990: Effects of excess degradable protein on postpartum reproduction and energy-balance in dairy-cattle. J Dairy Sci 73, 2342-2349.
20. Castaneda-Gutierrez E, Benefield BC, de Veth MJ, Santos NR, Gilbert RO, Butler WR, Bauman DE, 2007: Evaluation of the mechanism of action of conjugated linoleic acid isomers on reproduction in dairy cows(1). J Dairy Sci 90, 4253-4264.
21. Cerri RLA, Juchem SO, Chebel RC, Rutigliano HM, Bruno RGS, Galvao KN, Thatcher WW, Santos JEP, 2009: Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J Dairy Sci 92, 1520-1531.
22. Cheng Z, Robinson RS, Pushpakumara PGA, Mansbridge RJ, Wathes DC, 2001: Effect of dietary polyunsaturated fatty acids on uterine prostaglandin synthesis in the cow. J Endocrinol 171, 463-473.
23. Childs S, Hennessy AA, Sreenan JM, Wathes DC, Cheng Z, Stanton C, Diskin MG, Kenny DA, 2008a: Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology 70, 595-611.
24. Childs S, Lynch CO, Hennessy AA, Stanton C, Wathes DC, Sreenan JM, Diskin MG, Kenny DA, 2008b: Effect of dietary enrichment with either n-3 or n-6 fatty acids on systemic metabolite and hormone concentration and ovarian function in heifers. Animal 2, 883-893.
25. 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.
26. DeFrain JM, Hippen AR, Kalscheur KF, Patton RS, 2005: Effects of feeding propionate and calcium salts of long-chain fatty acids on transition dairy cow performance. J Dairy Sci 88, 983-993.
27. Douglas GN, Overton TR, Bateman HG, Dann HM, Drackley JK, 2006: Prepartal plane of nutrition, regardless of dietary energy source, affects periparturient metabolism and dry matter intake in Holstein cows. J Dairy Sci 89, 2141-2157.
28. Dubuc J, Duffield TF, Leslie KE, Walton JS, LeBlanc SJ, 2012: Risk factors and effects of postpartum anovulation in dairy cows. J Dairy Sci 95, 1845-1854.
29. Ducker MJ, Morant SV, Fisher WJ, Haggett RA, 1985: Nutrition and reproductive-performance of dairy-cattle. 2. Prediction of reproductive-performance in 1st lactation dairy heifers subjected to controlled nutritional regimes. Anim Prod 41, 13-22.
30. Ferguson EM, Leese HJ, 1999: Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil 116, 373-378.
31. 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. Biol Reprod 77, 9-17.
32. Fouladi-Nashta AA, Wonnacott KE, Gutierrez CG, Gong JG, Sinclair KD, Garnsworthy PC, Webb R, 2009: Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids. Reproduction 138, 771-781.
33. Garnsworthy PC, 2004: The environmental impact of fertility in dairy cows: a modelling approach to predict methane and ammonia emissions. Anim Feed Sci Technol 112, 211-223.
34. Garnsworthy PC, Lock A, Mann GE, Sinclair KD, Webb R, 2008: Nutrition, metabolism, and fertility in dairy cows: 2. Dietary fatty acids and ovarian function. J Dairy Sci 91, 3824-3833.
35. Garnsworthy PC, Fouladi-Nashta AA, Mann GE, Sinclair KD, Webb R, 2009: Effect of dietary-induced changes in plasma insulin concentrations during the early post partum period on pregnancy rate in dairy cows. Reproduction 137, 759-768.
36. Genicot G, Leroy J, Van Soom A, Donnay I, 2005: The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian oocytes. Theriogenology 63, 1181-1194.
37. González-Serrano AF, Pirro V, Ferreira CR, Oliveri P, Eberlin LS, Heinzmann J, Lucas-Hahn A, Niemann H, Cooks RG, 2013: Desorption electrospray ionization mass spectrometry reveals lipid metabolism of individual oocytes and embryos. PLoS ONE 8, e74981.
38. Grummer RR, 1995: Impact of changes in organic nutrient metabolism on feeding the transition dairy-cow. J Anim Sci 73, 2820-2833.
39. Grummer RR, Hoffman PC, Luck ML, Bertics SJ, 1995: Effect of prepartum and postpartum dietary energy on growth and lactation of primiparous cows. J Dairy Sci 78, 172-180.
40. Guardieiro M, Machado G, Bastos M, Mourão G, Carrijo L, Dode M, Leroy J, Sartori R, 2013: Diet enriched in linoleic acid compromises cryotolerance of embryos from superovulated beef heifers. Reprod Fertil Dev (in press). doi: 10.1071/RD12403.
41. Haggarty P, Wood M, Ferguson E, Hoad G, Srikantharajah A, Milne E, Hamilton M, Bhattacharya S, 2006: Fatty acid metabolism in human preimplantation embryos. Hum Reprod 21, 766-773.
42. Hammiche F, Vujkovic M, Wijburg W, de Vries JHM, Macklon NS, Laven JSE, Steegers-Theunissen RPM, 2011: Increased preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology. Fertil Steril 95, 1820-1823.
43. Hinckley T, Clark RM, Bushmich SL, Milvae RA, 1996: Long chain polyunsaturated fatty acids and bovine luteal cell function. Biol Reprod 55, 445-449.
44. 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. J Reprod Fertil 94, 153-160.
45. Hostens M, Fievez V, Vlaeminck B, Buyse J, Leroy J, Piepers S, De Vliegher S, Opsomer G, 2011: The effect of marine algae in the ration of high-yielding dairy cows during transition on metabolic parameters in serum and follicular fluid around parturition. J Dairy Sci 94, 4603-4615.
46. Hughes J, Kwong WY, Li DF, Salter AM, Lea RG, Sinclair KD, 2011: Effects of omega-3 and-6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism. Reproduction 141, 105-118.
47. Inchaisri C, Jorritsma R, Vos PLAM, van der Weijden GC, Hogeveen H, 2011: Analysis of the economically optimal voluntary waiting period for first insemination. J Dairy Sci 94, 3811-3823.
48. Jacobsen SC, Brons C, Bork-Jensen J, Ribel-Madsen R, Yang B, Lara E, Hall E, Calvanese V, Nilsson E, Jorgensen SW, Mandrup S, Ling C, Fernandez AF, Fraga MF, Poulsen P, Vaag A, 2012: Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men. Diabetologia 55, 3341-3349.
49. Janovick NA, Drackley JK, 2010: Prepartum dietary management of energy intake affects postpartum intake and lactation performance by primiparous and multiparous Holstein cows. J Dairy Sci 93, 3086-3102.
50. Jorritsma R, Cesar ML, Hermans JT, Kruitwagen CL, Vos PL, Kruip TA, 2004: Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim Reprod Sci 81, 225-235.
51. Jungheim ES, Macones GA, Odem RR, Patterson BW, Lanzendorf SE, Ratts VS, Moley KH, 2011: Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil Steril 95, 1970-1974.
52. Kim JY, Kinoshita M, Ohnishi M, Fukui Y, 2001: Lipid and fatty acid analysis of fresh and frozen-thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131-138.
53. van Knegsel ATM, van den Branda H, Dijkstra J, Tamminga S, Kemp B, 2005: Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reprod Nutr Dev 45, 665-688.
54. van Knegsel ATM, van den Brand H, Dijkstra J, van Straalen WM, Heetkamp MJW, Tamminga S, Kemp B, 2007: Dietary energy source in dairy cows in early lactation: energy partitioning and milk composition. J Dairy Sci 90, 1467-1476.
55. van Knegsel AT, van der Drift SG, Čermáková J, Kemp B, 2013: Effects of shortening the dry period of dairy cows on milk production, energy balance, health, and fertility: a systematic review. Vet J 198, 707-713.
56. Lammoglia MA, Willard ST, Oldham JR, Randel RD, 1996: Effects of dietary fat and season on steroid hormonal profiles before parturition and on hormonal, cholesterol, triglycerides, follicular patterns, and postpartum reproduction in Brahman cows. J Anim Sci 74, 2253-2262.
57. Lapa M, Marques CC, Alves SP, Vasques MI, Baptista MC, Carvalhais I, Silva Pereira M, Horta AE, Bessa RJ, Pereira RM, 2011: Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod Domest Anim 46, 904-910.
58. Leese HJ, Barton AM, 1984: Pyruvate and glucose-uptake by mouse ova and preimplantation embryos. J Reprod Fertil 72, 9-13.
59. Leese HJ, Gray SM, 1985: Vascular perfusion - a novel means of studying oviduct function. Am J Physiol 248, E624-E632.
60. Leese HJ, Hugentobler SA, Gray SM, Morris DG, Sturmey RG, Whitear S-L, Sreenan JM, 2008: Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev 20, 1-8.
61. Leroy J, de Kruif A, 2006: Reduced reproductive performance in high producing dairy cows: is there actually a problem? Vlaams Diergeneeskd Tijdschr 75, 55-60.
62. Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A, 2005: 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.
63. Leroy J, Opsomer G, Van Soom A, Goovaerts IGF, Bols PEJ, 2008a: Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I the importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows*. Reprod Domest Anim 43, 612-622.
64. Leroy J, Van Soom A, Opsomer G, Goovaerts IGF, Bols PEJ, 2008b: 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*. Reprod Domest Anim 43, 623-632.
65. Leroy J, Vanholder T, Van Knegsel ATM, Garcia-Ispierto I, Bols PEJ, 2008c: Nutrient prioritization in dairy cows early postpartum: mismatch between metabolism and fertility? Reprod Domest Anim 43, 96-103.
66. Leroy JL, Van Hoeck V, Clemente M, Rizos D, Gutierrez-Adan A, Van Soom A, Uytterhoeven M, Bols PE, 2010: The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum Reprod 25, 768-778.
67. Leroy J, Rizos D, Sturmey R, Bossaert P, Gutierrez-Adan A, Van Hoeck V, Valckx S, Bols PEJ, 2012: Intrafollicular conditions as a major link between maternal metabolism and oocyte quality: a focus on dairy cow fertility. Reprod Fertil Dev 24, 1-12.
68. Lucy MC, 2001: Adsa Foundation Scholar Award - Reproductive loss in high-producing dairy cattle: where will it end? J Dairy Sci 84, 1277-1293.
69. Lucy MC, Staples CR, Michel FM, Thatcher WW, Bolt DJ, 1991: Effect of feeding calcium soaps to early postpartum dairy-cows on plasma prostaglandin-F2-alpha luteinizing-hormone, and follicular-growth. J Dairy Sci 74, 483-489.
70. 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.
71. Marei WF, Wathes DC, Fouladi-Nashta AA, 2009: The effect of linolenic acid on bovine oocyte maturation and development. Biol Reprod 81, 1064-1072.
72. Marei WF, Wathes DC, Fouladi-Nashta AA, 2010: Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979-988.
73. Mattos R, Staples CR, Williams J, Amorocho A, McGuire MA, Thatcher WW, 2002: Uterine, ovarian, and production responses of lactating dairy cows to increasing dietary concentrations of menhaden fish meal. J Dairy Sci 85, 755-764.
74. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JSM, Speake BK, 2000: Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 118, 163-170.
75. McKeegan PJ, Sturmey RG, 2012: The role of fatty acids in oocyte and early embryo development. Reprod Fertil Dev 24, 59-67.
76. McNamara S, Murphy JJ, Rath M, O'Mara FP, 2003: Effects of different transition diets on energy balance, blood metabolites and reproductive performance in dairy cows. Livest Prod Sci 84, 195-206.
77. Moallem U, Katz M, Arieli A, Lehrer H, 2007: Effects of peripartum propylene glycol or fats differing in fatty acid profiles on feed intake, production, and plasma metabolites in dairy cows. J Dairy Sci 90, 3846-3856.
78. Murakami K, Chan SY, Routtenberg A, 1986: Protein-kinase-C activation by cis-fatty acid in the absence of Ca-2+ and phospholipids. J Biol Chem 261, 5424-5429.
79. Nishizuka Y, 1988: The molecular heterogeneity of protein kinase-C and its implications for cellular-regulation. Nature 334, 661-665.
80. Oba M, Miyashita S, Nishii R, Koiwa M, Koyama H, Ambrose DJ, Dochi O, 2013: Short communication: effects of serum obtained from dairy cows with low or high body condition score on in vitro embryo development. J Dairy Sci 96, 1668-1671.
81. Odens LJ, Burgos R, Innocenti M, VanBaale MJ, Baumgard LH, 2007: Effects of varying doses of supplemental conjugated linoleic acid on production and energetic variables during the transition period. J Dairy Sci 90, 293-305.
82. 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. Reprod Domest Anim 33, 193-204.
83. Pereira RM, Baptista MC, Vasques MI, Horta AEM, Portugal PV, Bessa RJB, Silva JCe, Pereira MS, Marques CC, 2007: Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t, 12c CLA). Anim Reprod Sci 98, 293-301.
84. Petit HV, Germiquet C, Lebel D, 2004: Effect of feeding whole, unprocessed sunflower seeds and flaxseed on milk production, milk composition, and prostaglandin secretion in dairy cows. J Dairy Sci 87, 3889-3898.
85. Petit HV, Cavalieri FB, Santos GTD, Morgan J, Sharpe P, 2008: Quality of embryos produced from dairy cows fed whole flaxseed and the success of embryo transfer. J Dairy Sci 91, 1786-1790.
86. Pires JAA, Souza AH, Grummer RR, 2007: Induction of hyperlipidemia by intravenous infusion of tallow emulsion causes insulin resistance in Holstein cows. J Dairy Sci 90, 2735-2744.
87. Ponter AA, Guyader-Joly C, Nuttinck F, Grimard B, Humblot P, 2012: Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio. Theriogenology 78, 632-645.
88. Rabiee AR, Lean IJ, Gooden JM, Miller BG, 1997: Short-term studies of ovarian metabolism in the ewe. Anim Reprod Sci 47, 43-58.
89. Rabiee AR, Breinhild K, Scott W, Golder HM, Block E, Lean IJ, 2012: Effect of fat additions to diets of dairy cattle on milk production and components: a meta-analysis and meta-regression. J Dairy Sci 95, 3225-3247.
90. Robinson RS, Pushpakumara PGA, Cheng Z, Peters AR, Abayasekara DRE, Wathes DC, 2002: Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124, 119-131.
91. Robker RL, Akison LK, Bennett BD, Thrupp PN, Chura LR, Russell DL, Lane M, Norman RJ, 2009: Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab 94, 1533-1540.
92. Roche JF, 2006: The effect of nutritional management of the dairy cow on reproductive efficiency. Anim Reprod Sci 96, 282-296.
93. Ryan DP, Spoon RA, Williams GL, 1992: Ovarian follicular characteristics, embryo recovery, and embryo viability in heifers fed high-fat diets and treated with follicle-stimulating-hormone. J Anim Sci 70, 3505-3513.
94. Santos JEP, Bilby TR, Thatcher WW, Staples CR, Silvestre FT, 2008: Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod Domest Anim 43, 23-30.
95. Santos JEP, Rutigliano HM, Sa Filho MF, 2009: Risk factors for resumption of postpartum estrous cycles and embryonic survival in lactating dairy cows. Anim Reprod Sci 110, 207-221.
96. Santos JEP, Bisinotto RS, Ribeiro ES, Lima FS, Greco LF, Staples CR, Thatcher WW. 2010: Applying nutrition and physiology to improve reproduction in dairy cattle. In: Lucy MC, Pate JL, Smith MF, Spencer TE (eds), Reproduction in Domestic Ruminants VII. Society of Reproduction and Fertility No. 67. Nottingham University Press, Loughborough, pp. 387-403.
97. Sata R, Tsujii H, Abe H, Yamashita S, Hosshi H, 1999: Fatty acid composition of bovine embryo cultured in serum free and serum containing medium during early embryonic development. J Reprod Dev 45, 97-103.
98. Shehab-El-Deen MAMM, Leroy JLMR, Fadel MS, Saleh SYA, Maes D, Van Soom A, 2010: Biochemical changes in the follicular fluid of the dominant follicle of high producing dairy cows exposed to heat stress early post-partum. Anim Reprod Sci 117, 189-200.
99. Silvestre FT, Carvalho TSM, Francisco N, Santos JEP, Staples CR, Jenkins TC, Thatcher WW, 2011: Effects of differential supplementation of fatty acids during the peripartum and breeding periods of Holstein cows: I. Uterine and metabolic responses, reproduction, and lactation. J Dairy Sci 94, 189-204.
100. Smith DG, Sturmey RG, 2013: Parallels between embryo and cancer cell metabolism. Biochem Soc Trans 41, 664-669.
101. Staples CR, Burke JM, Thatcher WW, 1998: Influence of supplemental fats on reproductive tissues and performance of lactating cows. J Dairy Sci 81, 856-871.
102. Stinshoff H, Wilkening S, Hanstedt A, Bollwein H, Wrenzycki C, 2013: Dimethylsulfoxide and conjugated linoleic acids affect bovine embryo development in vitro. Reprod Fertil Dev (in press). doi: 10.1071/RD12372.
103. Sturmey RG, Reis A, Leese HJ, McEvoy TG, 2009: Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim 44(Suppl 3), 50-58.
104. Thangavelu G, Colazo MG, Ambrose DJ, Oba M, Okine EK, Dyck MK, 2007: Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 68, 949-957.
105. Thatcher WW, Bilby TR, Bartolome JA, Silvestre F, Staples CR, Santos JEP, 2006: Strategies for improving fertility in the modern dairy cow. Theriogenology 65, 30-44.
106. Thatcher W, Santos JEP, Staples CR, 2011: Dietary manipulations to improve embryonic survival in cattle. Theriogenology 76, 1619-1631.
107. Tsujii H, Matsuoka Y, Obata R, Hossain MS, Takagi Y, 2009: Fatty acid composition of lipids in day 7-13 blastocysts, serum and uterine fluid of rabbits. Reprod Med Biol 8, 107-112.
108. Valckx SDM, De Pauw I, De Neubourg D, Inion I, Berth M, Fransen E, Bols PEJ, Leroy J, 2012: BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum Reprod 27, 3531-3539.
109. Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, Bols PE, Leroy JL, 2011: Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS ONE 6, e23183.
110. Van Hoeck V, Leroy JLMR, Arias-Alvarez M, Rizos D, Gutierrez-Adan A, Schnorbusch K, Bols PEJ, Leese HJ, Sturmey RG, 2013: Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33-44.
111. Vanholder T, Opsomer G, de Kruif A, 2006: Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review. Reprod Nutr Dev 46, 105-119.
112. Vasconcelos JLM, Sartori R, Oliveira HN, Guenther JG, Wiltbank MC, 2001: Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology 56, 307-314.
113. Wakefield SL, Lane M, Schulz SJ, Hebart ML, Thompson JG, Mitchell M, 2008: Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am J Physiol 294, E425-E434.
114. Walsh SW, Williams EJ, Evans ACO, 2011: A review of the causes of poor fertility in high milk producing dairy cows. Anim Reprod Sci 123, 127-138.
115. Wathes DC, Abayasekara DRE, Aitken RJ, 2007: Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77, 190-201.
116. Wonnacott KE, Kwong WY, Hughes J, Salter AM, Lea RG, Garnsworthy PC, Sinclair KD, 2010: Dietary omega-3 and-6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57-69.
117. Wullepit N, Hostens M, Ginneberge C, Fievez V, Opsomer G, Fremaut D, De Smet S, 2012: Influence of a marine algae supplementation on the oxidative status of plasma in dairy cows during the periparturient period. Prev Vet Med 103, 298-303.
118. Yang X, Wu LL, Chura LR, Liang X, Lane M, Norman RJ, Robker RL, 2012: Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes. Fertil Steril 97, 1438-1443.
119. Zachut M, Arieli A, Lehrer H, Argov N, Moallem U, 2008: Dietary unsaturated fatty acids influence preovulatory follicle characteristics in dairy cows. Reproduction 135, 683-692.
120. Zachut M, Dekel I, Lehrer H, Arieli A, Arav A, Livshitz L, Yakoby S, Moallem U, 2010: Effects of dietary fats differing in n-6:n-3 ratio fed to high-yielding dairy cows on fatty acid composition of ovarian compartments, follicular status, and oocyte quality. J Dairy Sci 93, 529-545.
121. Zeron Y, Sklan D, Arav A, 2002: Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol Reprod Dev 61, 271-278.