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RESEARCH ARTICLE

A diet enriched in linoleic acid compromises the cryotolerance of embryos from superovulated beef heifers

Monique M. Guardieiro A , Grazieli M. Machado B , Michele R. Bastos C , Gerson B. Mourão A , Luiz H. D. Carrijo D , Margot A. N. Dode B , Jo L. M. R. Leroy E and Roberto Sartori A F
+ Author Affiliations
- Author Affiliations

A Departament of Animal Science, Luiz de Queiroz College of Agriculture (ESALQ), University of São Paulo, Av. Pádua Dias, 11, Piracicaba, SP 13418-900, Brazil.

B Embrapa Genetic Resources and Biotechnology, Parque Estação Biológica, Av. W5 Norte, Caixa Postal 02372, Brasília, DF 70770-900, Brazil.

C UNESP – University Estadual Paulista, Distrito Rubião Júnior, Botucatu, SP 18618-000, Brazil.

D Integral Nutrição Animal, GO 070 Km 8. 3, Goianira, GO 75370-000, Brazil.

E Gamete Research Center, Laboratory for Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium.

F Corresponding author. Email: robertosartori@usp.br

Reproduction, Fertility and Development 26(4) 511-520 https://doi.org/10.1071/RD12403
Submitted: 20 December 2012  Accepted: 13 March 2013   Published: 9 May 2013

Abstract

Dietary rumen-protected fat rich in linoleic acid may affect the superovulatory response and embryo yield; however, its effects on in vivo embryo cryotolerance are unknown in zebu cattle. The present study evaluated the production and cryotolerance after freezing or vitrification of embryos from Nelore heifers supplemented with rumen-protected polyunsaturated fatty acids (PUFA). Forty heifers kept in pasture were randomly distributed into two groups according to the type of feed supplement (F, supplement with rumen-protected PUFA, predominantly linoleic; C, control fat-free supplement with additional corn). Supplements were formulated to be isocaloric and isonitrogenous. Each heifer underwent both treatments in a crossover design with 70 days between replicates. After 50 days feeding, heifers were superovulated. Embryos were evaluated morphologically and vitrified or frozen. After thawing or warming, embryo development was evaluated in vitro. There was no difference between the F and C groups (P > 0.10) in terms of embryo production. Regardless of the cryopreservation method used, Group C embryos had a greater hatching rate after 72 h in vitro culture than Group F embryos (44.3 ± 4.2% (n = 148) vs 30.9 ± 4.0% (n = 137), respectively; P = 0.04). Moreover, vitrified and frozen embryos had similar hatching rates (P > 0.10). In conclusion, dietary rumen-protected PUFA rich in linoleic acid did not improve embryo production and compromised the cryotolerance of conventionally frozen or vitrified embryos from Nelore heifers.

Additional keywords: cryopreservation, fatty acid, nutrition.


References

Ahmad, N., Schrick, F. N., Butcher, R. L., and Inskeep, E. K. (1995). Effect of persistent follicles on early embryonic losses in beef cows. Biol. Reprod. 52, 1129–1135.
Effect of persistent follicles on early embryonic losses in beef cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltVCjs70%3D&md5=23e3526ed808670426d7a8f80bf603a2CAS | 7626713PubMed |

Al Darwich, A., Perreau, C., Petit, M. H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P., and Guignot, F. (2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKalpha phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat. 93, 30–36.
Effect of PUFA on embryo cryoresistance, gene expression and AMPKalpha phosphorylation in IVF-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvV2ht7Y%3D&md5=42ccd24f6aaef77676b590eb89734b61CAS | 20601073PubMed |

Arreseigor, C. J., Sisul, A., Arreseigor, A. E., and Stahringe, R. C. (1998). Effect of cryoprotectant, thawing method, embryo grade and breed on pregnancy rates of cryopreserved bovine embryos. Theriogenology 49, 160.
Effect of cryoprotectant, thawing method, embryo grade and breed on pregnancy rates of cryopreserved bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Block, J., Fischer-Brown, A. E., Rodina, T. M., Ealy, A. D., and Hansen, P. J. (2007). The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation. Theriogenology 68, 153–161.
The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFKgsL4%3D&md5=2ab0d183dee8c780bc548f9b1b80b4b7CAS | 17532038PubMed |

Castro Neto, A. S., Sanches, B. V., Binelli, M., Seneda, M. M., Perri, S. H., and Garcia, J. F. (2005). Improvement in embryo recovery using double uterine flushing. Theriogenology 63, 1249–1255.
Improvement in embryo recovery using double uterine flushing.Crossref | GoogleScholarGoogle Scholar |

Cerri, R. L., Juchem, S. O., Chebel, R. C., Rutigliano, H. M., Bruno, R. G., Galvão, K. N., Thatcher, W. W., and Santos, J. E. (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.
Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFamt78%3D&md5=c95fa45c7df55d8786362fd64cc811feCAS | 19307633PubMed |

Childs, S., Carter, F., Lynch, C. O., Sreenan, J. M., Lonergan, P., Hennessy, A. A., and Kenny, D. A. (2008). Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA). Theriogenology 70, 992–1003.
Embryo yield and quality following dietary supplementation of beef heifers with n-3 polyunsaturated fatty acids (PUFA).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVKmsLjN&md5=5e437f217359e25b229e376abee72335CAS | 18692227PubMed |

Clandinin, M. T., Cheema, S., Field, C. J., Garg, M. L., Venkatraman, J., and Clandinin, T. R. (1991). Dietary fat: exogenous determination of membrane structure and cell function. FASEB J. 5, 2761–2769.
| 1:CAS:528:DyaK3MXmsFCku7s%3D&md5=e4bd15fe95e609566bbcdda2dd7fe052CAS | 1916101PubMed |

Cuello, C., Berthelot, F., Martinat-Botté, F., Guillouet, P., Furstoss, V., Boisseau, C., Manceau, P., Locatelli, A., and Martínez, E. A. (2004). Transfer of vitrified blastocysts from one or two superovulated Large White Hyperprolific donors to Meishan recipients: reproductive parameters at Day 30 of pregnancy. Theriogenology 61, 843–850.
Transfer of vitrified blastocysts from one or two superovulated Large White Hyperprolific donors to Meishan recipients: reproductive parameters at Day 30 of pregnancy.Crossref | GoogleScholarGoogle Scholar | 14757470PubMed |

Dattena, M., Ptak, G., Loi, P., and Cappai, P. (2000). Survival and viability of vitrified in vitro and in vivo produced ovine blastocysts. Theriogenology 53, 1511–1519.
Survival and viability of vitrified in vitro and in vivo produced ovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvislCqtA%3D%3D&md5=909abb0dc4b3cb0724e44bc551d23aabCAS | 10883839PubMed |

Dobrinsky, J. R. (2002). Advancements in cryopreservation of domestic animal embryos. Theriogenology 57, 285–302.
Advancements in cryopreservation of domestic animal embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyltg%3D%3D&md5=0e55e6b0a55dd16d88a885c30f6b923aCAS | 11775976PubMed |

El-Gayar, M., Gauly, M., and Holtz, W. (2008). One-step dilution of open-pulled-straw (OPS)-vitrified mouse blastocysts in sucrose-free medium. Cryobiology 57, 191–194.
One-step dilution of open-pulled-straw (OPS)-vitrified mouse blastocysts in sucrose-free medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVChtbzF&md5=c215a710566d32017948f0dcea372641CAS | 18761335PubMed |

Fenwick, M. A., Llewellyn, S., Fitzpatrick, R., Kenny, D. A., Murphy, J. J., Patton, J., and Wathes, D. C. (2008). Negative energy balance in dairy cows is associated with specific changes in IGF-binding protein expression in the oviduct. Reproduction 135, 63–75.
Negative energy balance in dairy cows is associated with specific changes in IGF-binding protein expression in the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1CksLg%3D&md5=1c7cd40376f2b78a9d4d9a93949574c4CAS | 18159084PubMed |

Fouladi-Nashta, A. A., Wonnacott, K. E., Gutierrez, C. G., Gong, J. G., Sinclair, K. D., Garnsworthy, P. C., and 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.
Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsValt7rI&md5=b84caa07cf603abe195ecf8316fe8ba5CAS | 19633135PubMed |

Gong, J. G. (2002). Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Domest. Anim. Endocrinol. 23, 229–241.
Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Wktbw%3D&md5=b2975ade37cf540202fb1e498399ad45CAS | 12142240PubMed |

Green, M. P., Spate, L. D., Parks, T. E., Kimura, K., Murphy, C. N., Williams, J. E., Kerley, M. S., Green, J. A., Keisler, D. H., and Roberts, R. M. (2008). Nutritional skewing of conceptus sex in sheep: effects of a maternal diet enriched in rumen-protected polyunsaturated fatty acids (PUFA). Reprod. Biol. Endocrinol. 6, 21.
Nutritional skewing of conceptus sex in sheep: effects of a maternal diet enriched in rumen-protected polyunsaturated fatty acids (PUFA).Crossref | GoogleScholarGoogle Scholar | 18541015PubMed |

Green, R. E., Santos, B. F., Sicherle, C. C., Landim-Alvarenga, F. C., and Bicudo, S. D. (2009). Viability of OPS vitrified sheep embryos after direct transfer. Reprod. Domest. Anim. 44, 406–410.
Viability of OPS vitrified sheep embryos after direct transfer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrisFWjtQ%3D%3D&md5=4920e5bd1cc3a452272a680417f69e3eCAS | 18954390PubMed |

Guignot, F., Bouttier, A., Baril, G., Salvetti, P., Pignon, P., Beckers, J. F., Touzé, J. L., Cognié, J., Traldi, A. S., Cognié, Y., and Mermillod, P. (2006). Improved vitrification method allowing direct transfer of goat embryos. Theriogenology 66, 1004–1011.
Improved vitrification method allowing direct transfer of goat embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vot1Sjuw%3D%3D&md5=d99a9af523cf2878d0e0fa44766961efCAS | 16581117PubMed |

Hochi, S., Kimura, K., and Hanada, A. (1999). Effect of linoleic acid–albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae. Theriogenology 52, 497–504.
Effect of linoleic acid–albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlyhuro%3D&md5=d57c71f7efdb7303785cebb6f84633fdCAS | 10734383PubMed |

Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.
High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=bda1bd1463ad693633a4028a58f68438CAS | 10734366PubMed |

Homa, S. T., and Brown, C. A. (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.
Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhslWjtLs%3D&md5=27e486642bc2d550ee87c062159d60adCAS | 1552477PubMed |

Houghton, P. L., Lemenager, R. P., Hendrix, K. S., Moss, G. E., and Stewart, T. S. (1990). Effects of body composition, pre- and postpartum energy intake and stage of production of energy utilization by beef cows. J. Anim. Sci. 68, 1447–1456.
| 1:STN:280:DyaK3czgslGqsw%3D%3D&md5=cddb551edea4e77e8429925b69eaf951CAS | 2365655PubMed |

Hughes, J., Kwong, W. Y., Li, D., Salter, A. M., Lea, R. G., and Sinclair, K. D. (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.
Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7k%3D&md5=bd778f01a703a4d505bea0cc50be4ba0CAS | 21045166PubMed |

Jousan, F. D., and Hansen, P. J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–196.
Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2rtQ%3D%3D&md5=079a87cf85105ead308a33d95a6f6605CAS | 16955404PubMed |

Jousan, F. D., Oliveira, L. J., and Hansen, P. J. (2008). Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-i prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Reprod. Dev. 75, 681–688.
Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-i prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFClu7k%3D&md5=70ded0aaaadc18151f3080d62b20862cCAS | 18161856PubMed |

Kim, J. Y., Kinoshita, M., Ohnishi, M., and Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–138.
Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=6d42e5e8c6e9d20f2606eb2e6c9c4b01CAS | 11425337PubMed |

Kojima, T., Zeniya, Y., Aoyama, T., Kondo, A., and Yoshino, J. (1997). Dietary administration of fatty acids-enriched mold dried cell containing γ-linolenic acid to female pigs improves ovulation rate and embryo quality in summer. J. Reprod. Dev. 43, 121–127.
Dietary administration of fatty acids-enriched mold dried cell containing γ-linolenic acid to female pigs improves ovulation rate and embryo quality in summer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltlWkurw%3D&md5=f492a3072d1c95b2b1c14d8775eac976CAS |

Kong, I. K., Lee, S. I., Cho, S. G., Cho, S. K., and Park, C. S. (2000). Comparison of open pulled straw (OPS) vs glass micropipette (GMP) vitrification in mouse blastocysts. Theriogenology 53, 1817–1826.
Comparison of open pulled straw (OPS) vs glass micropipette (GMP) vitrification in mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvpsFenuw%3D%3D&md5=192325f7ac30f81d5d5632952cd5d2e7CAS | 10968424PubMed |

Kurzawa, R., Głabowski, W., Baczkowski, T., and Brelik, P. (2002). Evaluation of mouse preimplantation embryos exposed to oxidative stress cultured with insulin-like growth factor I and II, epidermal growth factor, insulin, transferrin and selenium. Reprod. Biol. 2, 143–162.
| 14666155PubMed |

Lapa, M., Marques, C. C., Alves, S. P., Vasques, M. I., Baptista, M. C., Carvalhais, I., Silva Pereira, M., Horta, A. E., Bessa, R. J., and Pereira, R. M. (2011). Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reprod. Domest. Anim. 46, 904–910.
Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlemtrvM&md5=48f88517ebf95b5a2de109e2752456a1CAS | 21366717PubMed |

Leroy, J., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. J. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–778.
The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFeitr8%3D&md5=893630a90ef1fdd49f741c379d4317e9CAS | 20007613PubMed |

Leroy, J. L. M. R., Rizos, D., Sturmey, R., Bossaert, P., Gutierrez-Adan, A., Van Hoeck, V., Valckx, S., and Bols, P. E. J. (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.
Intrafollicular conditions as a major link between maternal metabolism and oocyte quality: a focus on dairy cow fertility.Crossref | GoogleScholarGoogle Scholar |

Lopatářová, M., Čech, S., Havlíček, V., and Holý, L. (2002). Effect of vitrification in open pulled straws on survival of bovine embryos from superovulated cows. Acta Vet. 71, 93–99.
Effect of vitrification in open pulled straws on survival of bovine embryos from superovulated cows.Crossref | GoogleScholarGoogle Scholar |

Lopatarova, M., Cech, S., Holy, L., and Dolezel, R. (2006). The effect of vitrification in open pulled straws on pregnancy rates after transfer of in vivo produced bovine embryos. Vet. Med. (Praha) 51, 454–460.

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2009). The effect of linolenic acid on bovine oocyte maturation and development. Biol. Reprod. 81, 1064–1072.
The effect of linolenic acid on bovine oocyte maturation and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vL&md5=723304df9e34ac8a15a75e7fa3a466afCAS | 19587335PubMed |

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2010). Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979–988.
Impact of linoleic acid on bovine oocyte maturation and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns12qsLY%3D&md5=4ae3e076f816f501fab3be94536e7b5dCAS | 20215338PubMed |

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2012). Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reprod. Fertil. Dev. 24, 679–690.
Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvFehu74%3D&md5=6f3825ae289b74959e0d0f7d0edc040fCAS | 22697118PubMed |

Mattos, M. C. C., Bastos, M. R., Oliveira, A. C. S., Gonçalves, J. R., Lima, L. G., Sousa, R. V., Pires, A. V., Mourão, G. B., and Sartori, R. (2010). Cryotolerance of morulae and blastocysts produced in vivo in Bos indicus. In ‘Proceedings of the 24th Reunião Anual da SBTE’, 19 August 2010. (Ed. Universidade Federal do Rio Grande do Sul) p. 815. (Acta Scientiae Veterinariae: Porto de Galinhas.)

McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S., and Speake, B. K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.
| 1:CAS:528:DC%2BD3cXpsl2msA%3D%3D&md5=4fed7c6456c743c05e762cdd8a760c46CAS | 10793638PubMed |

Miller, R. R., Cornett, C. L., Waterhouse, K. E., and Farstad, W. (2005). Comparative aspects of sperm membrane fatty acid composition in silver (Vulpes vulpes) and blue (Alopex lagopus) foxes, and their relationship to cell cryopreservation. Cryobiology 51, 66–75.
Comparative aspects of sperm membrane fatty acid composition in silver (Vulpes vulpes) and blue (Alopex lagopus) foxes, and their relationship to cell cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVGgu7s%3D&md5=3f27a3e584d4cffdfb4225f4016fb75eCAS | 16040024PubMed |

Nelder, J. A., and Wedderburn, R. W. M. (1972). Generalized linear models. J. R. Stat. Soc. [Ser. A] 135, 370–384.
Generalized linear models.Crossref | GoogleScholarGoogle Scholar |

Nogueira, M. F., Fragnito, P. S., Trinca, L. A., and Barros, C. M. (2007). The effect of type of vaginal insert and dose of pLH on embryo production, following fixed-time AI in a progestin-based superstimulatory protocol in Nelore cattle. Theriogenology 67, 655–660.
The effect of type of vaginal insert and dose of pLH on embryo production, following fixed-time AI in a progestin-based superstimulatory protocol in Nelore cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitl2jtw%3D%3D&md5=0c18f3b5bdd65d052a73997c67a462edCAS | 17109947PubMed |

Nonogaki, T., Noda, Y., Goto, Y., Kishi, J., and Mori, T. (1994). Developmental blockage of mouse embryos caused by fatty acids. J. Assist. Reprod. Genet. 11, 482–488.
Developmental blockage of mouse embryos caused by fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzlvFOjug%3D%3D&md5=a341ede5eeb1da4ed60e28ac7f43ef85CAS | 7633171PubMed |

Papadopoulos, S., Rizos, D., Duffy, P., Wade, M., Quinn, K., Boland, M. P., and Lonergan, P. (2002). Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo or in vitro produced ovine blastocysts. Anim. Reprod. Sci. 74, 35–44.
Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo or in vitro produced ovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nitFKqtw%3D%3D&md5=b8e3b8247051daec6dd24ce448dd7b7bCAS | 12379373PubMed |

Parrish, J. J., Krogenaes, A., and Susko-Parrish, J. L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–869.
Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVGgug%3D%3D&md5=162b4ec4dddf4398e84b8c88373cce16CAS | 16727781PubMed |

Pereira, R. M., Baptista, M. C., Vasques, M. I., Horta, A. E., Portugal, P. V., Bessa, R. J., Silva, J. C., Pereira, M. S., and Marques, C. C. (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.
Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Gnu7k%3D&md5=916ed2b7ffe9c3122930bf95b0bf4851CAS | 16644149PubMed |

Pereira, R. M., Carvalhais, I., Pimenta, J., Baptista, M. C., Vasques, M. I., Horta, A. E., Santos, I. C., Marques, M. R., Reis, A., Pereira, M. S., and Marques, C. C. (2008). Biopsied and vitrified bovine embryos viability is improved by trans10, cis12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim. Reprod. Sci. 106, 322–332.
Biopsied and vitrified bovine embryos viability is improved by trans10, cis12 conjugated linoleic acid supplementation during in vitro embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1yku78%3D&md5=5c94148b55c533ef88869522107e8134CAS | 17580103PubMed |

Petit, H. V., and Twagiramungu, H. (2006). Conception rate and reproductive function of dairy cows fed different fat sources. Theriogenology 66, 1316–1324.
Conception rate and reproductive function of dairy cows fed different fat sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotleqtrw%3D&md5=c0fcce3734502c4859a3928d4424753eCAS | 16735061PubMed |

Petit, H. V., Cavalieri, F. B., Santos, G. T., Morgan, J., and 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.
Quality of embryos produced from dairy cows fed whole flaxseed and the success of embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlWmtLw%3D&md5=9475cbc2772475bdbd24eb56a496cde7CAS | 18420609PubMed |

Reis, A., Rooke, J. A., McCallum, G. J., Staines, M. E., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003). Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro. Reprod. Fertil. Dev. 15, 275–284.
Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Cgur0%3D&md5=e779e7e142fe560e5295d479c49ee5c8CAS | 14588185PubMed |

Ryan, D. P., Spoon, R. A., and Williams, G. L. (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.
| 1:CAS:528:DyaK3sXnvF2mtw%3D%3D&md5=bacab10cf2906ac454cef7b7171d6a0aCAS | 1459913PubMed |

Sartori, R., Sartor-Bergfelt, R., Mertens, S. A., Guenther, J. N., Parrish, J. J., and Wiltbank, M. C. (2002). Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 85, 2803–2812.
Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlagsbg%3D&md5=91c878ff9dc9444345cad681e5af9344CAS | 12487447PubMed |

Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–235.
Modifying oocytes and embryos to improve their cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gitr3O&md5=1ee2b82b3cc1990aa34534dcdbf370b5CAS | 16263160PubMed |

Souza, A. H., Sartori, R., Guenther, J. N., Caraviello, D., Monson, R., and Wiltbank, M. C. (2007). Effect of semen source and dose of FSH on superovulatory response and embryo production in Holstein heifers. Anim. Reprod. 4, 70–76.

Stringfellow, D. A., and Seidel, S. M. (1998). ‘Manual of the International Embryo Transfer Society. 3rd edn.’ (IETS: Savoy, IL).

Stroud, B., and Callesen, H. (2012). IETS statement on worldwide ET statistics for 2010. Anim. Reprod. 9, 210–216.

Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–58.
Role of fatty acids in energy provision during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 19660080PubMed |

Sudano, M. J., Santos, V. G., Tata, A., Ferreira, C. R., Paschoal, D. M., Machado, R., Buratini, J., Eberlin, M. N., and Landim-Alvarenga, F. D. (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol. Reprod. 87, 130.
Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts.Crossref | GoogleScholarGoogle Scholar | 23053436PubMed |

Thangavelu, G., Colazo, M. G., Ambrose, D. J., Oba, M., Okine, E. K., and Dyck, M. K. (2007). Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 68, 949–957.
Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOgsb7N&md5=f509d0762f73048a26bb6257da9663bdCAS | 17850856PubMed |

Tominaga, K., Hamada, Y., Yabuue, T., and Ariyoshi, T. (2000). Effect of linoleic acid–albumin on post-thaw survival of in vitro-produced bovine embryos at the 16-cell stage. J. Vet. Med. Sci. 62, 465–467.
Effect of linoleic acid–albumin on post-thaw survival of in vitro-produced bovine embryos at the 16-cell stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvVWht78%3D&md5=4a993618153c1d93e3948355f64fbe10CAS | 10823739PubMed |

Vajta, G., Holm, P., Kuwayama, M., Booth, P. J., Jacobsen, H., Greve, T., and Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–58.
Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVGrs7g%3D&md5=49d4e9194babffb16608d70dd43f2acdCAS | 9712317PubMed |

Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E., and Leroy, J. L. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183.
Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=f70186f2c08e5bed5699f82fa441a304CAS | 21858021PubMed |

Van Wagtendonk-De Leeuw, A. M., Den Daas, J. H., Kruip, T. A., and Rall, W. F. (1995). Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos. Cryobiology 32, 157–167.
Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3mt1Cnsw%3D%3D&md5=d3f8119b1a4c8a6924b343182e82bea1CAS | 7743817PubMed |

Viana, J. H. M., and Camargo, L. S. A. (2007). Bovine embryo production in Brazil: a new scenario. Acta Sci. Vet. 35, 915–924.

Visintin, J. A., Martins, J. F., Bevilacqua, E. M., Mello, M. R., Nicácio, A. C., and Assumpção, M. E. (2002). Cryopreservation of Bos taurus vs Bos indicus embryos: are they really different? Theriogenology 57, 345–359.
Cryopreservation of Bos taurus vs Bos indicus embryos: are they really different?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyltQ%3D%3D&md5=94742106496923b1df027e615b5cb3efCAS | 11775979PubMed |

Wakefield, S. L., Lane, M., Schulz, S. J., Hebart, M. L., Thompson, J. G., and 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. Endocrinol. Metab. 294, E425–E434.
Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1ykur0%3D&md5=0f92a8e9d399562d498728f084fb714eCAS | 18073322PubMed |

Walter, B. M. T., and Sampaio, A. B. (1998). ‘A vegetação da fazenda Sucupira.’ (Embrapa Recursos Genéticos e Biotecnologia: Brasília.)

Wathes, D. C., Abayasekara, D. R., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190–201.
Polyunsaturated fatty acids in male and female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OnsL0%3D&md5=b77e4058f3c434369b914d92796196b9CAS | 17442851PubMed |

Wonnacott, K. E., Kwong, W. Y., Hughes, J., Salter, A. M., Lea, R. G., Garnsworthy, P. C., and Sinclair, K. D. (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.
Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWnug%3D%3D&md5=ee5da977df022e2e461fccec56508526CAS | 19789173PubMed |

Zeron, Y., Ocheretny, A., Kedar, O., Borochov, A., Sklan, D., and Arav, A. (2001). Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447–454.
Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFWjsrg%3D&md5=0836178746a69bb3c92908db878e2399CAS | 11226071PubMed |

Zeron, Y., Sklan, D., and Arav, A. (2002). Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev. 61, 271–278.
Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Ghsw%3D%3D&md5=f9ddc9499baf2c0a465a61683aab42fdCAS | 11803563PubMed |