MOET Efficiency in a Spanish Herd of Japanese Black Heifers and Analysis of Environmental and Metabolic Determinants

  1. Vázquez-Mosquera, Juan M.
  2. Sebastián, Francisco
  3. Pesántez-Pacheco, Jose L.
  4. Fernández-Novo, Aitor
  5. Pérez-Solana, Maria Luz
  6. Pérez-Garnelo, Sonia Salomé
  7. Martínez, Daniel
  8. Pérez-Villalobos, Natividad
  9. Villagrá, Arantxa
  10. Astiz, Susana
  11. Bonet-Bo, Martin
  12. Gardón, Juan Carlos
  13. de Mercado, Eduardo
  1. 1 Universidad Complutense de Madrid
    info

    Universidad Complutense de Madrid

    Madrid, España

    ROR 02p0gd045

  2. 2 Universidad Europea de Madrid
    info

    Universidad Europea de Madrid

    Madrid, España

    ROR https://ror.org/04dp46240

  3. 3 Embriovet SL
  4. 4 Universidad de Cuenca
    info

    Universidad de Cuenca

    Cuenca, Ecuador

    ROR https://ror.org/04r23zn56

  5. 5 Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria
    info

    Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria

    Madrid, España

    ROR https://ror.org/011q66e29

  6. 6 Universidad Católica de Valencia San Vicente Mártir
    info

    Universidad Católica de Valencia San Vicente Mártir

    Valencia, España

    ROR https://ror.org/03d7a9c68

  7. 7 Instituto Valenciano de Investigaciones Agrarias
    info

    Instituto Valenciano de Investigaciones Agrarias

    Moncada i Reixac, España

    ROR https://ror.org/00kx3fw88

  8. 8 Cowvet SL
Revista:
Biology

ISSN: 2079-7737

Año de publicación: 2022

Volumen: 11

Número: 2

Páginas: 225

Tipo: Artículo

DOI: 10.3390/BIOLOGY11020225 GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Biology

Resumen

Embryo transfer procedures have been widely implemented in bovine all around the world. These techniques help to accelerate the increase in the genetic merit and to keep the level of inbreeding under control, which is especially important in breeds, such as Japanese Black cattle, in areas outside of Japan, where there are scarce individuals and few herds. Our study describes an adequate embryo productivity of Japanese Black heifers under Spanish management and environmental conditions, like that which has been previously reported, demonstrating the adequate adaptation capacity of these animals. No effect on embryo production or quality was found due to plasma metabolic parameters of the donors, suggesting an optimal nutritional and body conditioning of the donors’ herd. Pregnant recipients after embryo transfer showed significantly higher levels of cholesterol-related parameters, glucose, and urea, which may be related to higher availability of nutrients for the future pregnancy. Heat stress at embryo transfer negatively impacted conception rates as expected, while larger parity and ET number corresponded to numerically higher conception rates.

Referencias bibliográficas

  • Nomura, T.; Honda, T.; Mukai, F. Inbreeding and effective population size of Japanese Black Cattle. J. Anim. Sci. 2001, 79, 366–370.
  • Motoyama, M.; Sasaki, K.; Watanabe, A. Wagyu and the factors contributing to its beef quality: A japanese industry overview. Meat Sci. 2016, 120, 10–18.
  • Smith, S.B.; Lunt, D.K.; Chung, K.Y.; Choi, C.B.; Tume, R.K.; Zembayashi, M. Adiposity, fatty acid composition, and delta-9 desaturase activity during growth in beef cattle. Anim. Sci. J. 2006, 77, 478–486.
  • Nogi, T.; Honda, T.; Mukai, F.; Okagaki, T.; Oyama, K. Heritabilities and genetic correlations of fatty acid compositions in longissimus muscle lipid with carcass traits in Japanese Black Cattle. J. Anim. Sci. 2011, 89, 615–621.
  • Gotoh, T.; Albrecht, E.; Teuscher, F.; Kawabata, K.; Sakashita, K.; Iwamoto, H.; Wegner, J. Differences in muscle and fat accretion in Japanese Black and European Cattle. Meat Sci. 2009, 82, 300–308.
  • Trenkle, A.; Topel, D.G. Relationship of some endocrine measurements to growth and carcass composition of cattle. J. Anim. Sci. 1978, 46, 1604–1609.
  • Matsuzaki, M.; Takizawa, S.; Ogawa, M. Plasma Insulin, metabolite concentrations, and carcass characteristics of Japanese Black, Japanese Brown, and Holstein Steers. J. Anim. Sci. 1997, 75, 3287–3293.
  • Chen, G.; Koyama, K.; Yuan, X.; Lee, Y.; Zhou, Y.T.; O’Doherty, R.; Newgard, C.B.; Unger, R.H. Disappearance of body fat in normal rats induced by adenovirus-mediated leptin gene therapy. Proc. Natl. Acad. Sci. USA 1996, 93, 14795–14799.
  • Siegrist-Kaiser, C.A.; Pauli, V.; Juge-Aubry, C.E.; Boss, O.; Pernin, A.; Chin, W.W.; Cusin, I.; Rohner-Jeanrenaud, F.; Burger, A.G.; Zapf, J.; et al. Direct effects of leptin on brown and white adipose tissue. J. Clin. Investig. 1997, 100, 2858–2864.
  • Minokoshi, Y.; Kim, Y.-B.; Peroni, O.D.; Fryer, L.G.D.; Müller, C.; Carling, D.; Kahn, B.B. Leptin stimulates fatty-acid oxidation by activating amp-activated protein kinase. Nature 2002, 415, 339–343.
  • Corva, P.M.; Macedo, G.V.F.; Soria, L.A.; Mazzucco, J.P.; Motter, M.; Villarreal, E.L.; Schor, A.; Mezzadra, C.A.; Melucci, L.M.; Miquel, M.C. Effect of leptin gene polymorphisms on growth, slaughter and meat quality traits of grazing Brangus steers. Genet. Mol. Res. GMR 2009, 8, 105–116.
  • Silva, D.B.S.; Crispim, B.A.; Silva, L.E.; Oliveira, J.A.; Siqueira, F.; Seno, L.O.; Grisolia, A.B. Genetic variations in the leptin gene associated with growth and carcass traits in Nellore Cattle. Genet. Mol. Res. GMR 2014, 13, 3002–3012.
  • Tian, J.; Zhao, Z.; Zhang, L.; Zhang, Q.; Yu, Z.; Li, J.; Yang, R. Association of the leptin gene E2-169T>C and E3-299T>a mutations with carcass and meat quality traits of the Chinese Simmental-cross steers. Gene 2013, 518, 443–448.
  • Kawaguchi, F.; Okura, K.; Oyama, K.; Mannen, H.; Sasazaki, S. Identification of leptin gene polymorphisms associated with carcass traits and fatty acid composition in Japanese Black Cattle. Anim. Sci. J. Nihon Chikusan Gakkaiho 2017, 88, 433–438.
  • Buchanan, F.C.; Van Kessel, A.G.; Waldner, C.; Christensen, D.A.; Laarveld, B.; Schmutz, S.M. Hot Topic: An Association between a leptin single nucleotide polymorphism and milk and protein yield. J. Dairy Sci. 2003, 86, 3164–3166.
  • Glantz, M.; Månsson, H.L.; Stålhammar, H.; Paulsson, M. Effect of Polymorphisms in the leptin, leptin receptor and Acyl-CoA:Diacylglycerol Acyltransferase 1 (DGAT1) Genes and genetic polymorphism of milk proteins on bovine milk composition. J. Dairy Res. 2012, 79, 110–118.
  • Giblin, L.; Butler, S.T.; Kearney, B.M.; Waters, S.M.; Callanan, M.J.; Berry, D.P. Association of bovine leptin polymorphisms with energy output and energy storage traits in progeny tested Holstein-Friesian Dairy Cattle Sires. BMC Genet. 2010, 11, 73.
  • Fantuzzi, G.; Faggioni, R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. J. Leukoc. Biol. 2000, 68, 437–446.
  • Ingvartsen, K.L.; Boisclair, Y.R. Leptin and the regulation of food intake, energy homeostasis and immunity with special focus on periparturient ruminants. Domest. Anim. Endocrinol. 2001, 21, 215–250.
  • Yonekura, S.; Oka, A.; Noda, M.; Uozumi, N.; Yonezawa, T.; Katoh, K.; Obara, Y. Relationship between serum leptin concentrations and the marbling scores in Japanese Black cattle. Anim. Sci. J. 2002.
  • Kulcsár, M.; Jánosi, S.; Lehtolainen, T.; Kátai, L.; Delavaud, C.; Balogh, O.; Chilliard, Y.; Pyörälä, S.; Rudas, P.; Huszenicza, G. Feeding-Unrelated Factors Influencing the plasma leptin level in ruminants. Domest. Anim. Endocrinol. 2005, 29, 214–226.
  • Wu, B.; Zan, L. Enhance beef cattle improvement by embryo biotechnologies. Reprod. Domest. Anim. 2012, 47, 865–871.
  • Ferré, L.B.; Kjelland, M.E.; Strøbech, L.B.; Hyttel, P.; Mermillod, P.; Ross, P.J. Review: Recent advances in bovine in vitro embryo production: Reproductive biotechnology history and methods. Anim. Int. J. Anim. Biosci. 2020, 14, 991–1004.
  • Numabe, T.; Oikawa, T.; Kikuchi, T.; Horiuchi, T. Production efficiency of Japanese Black calves by transfer of bovine embryos produced in vitro. Theriogenology 2000, 54, 1409–1420.
  • Honda, T.; Nomura, T.; Mukai, F. Conservation of genetic diversity in the Japanese Black cattle population by the construction of partially isolated lines. J. Anim. Breed. Genet. Z. Tierz. Zucht. 2005, 122, 188–194.
  • Sasaki, Y.; Uematsu, M.; Kitahara, G.; Osawa, T. Reproductive performance of Japanese Black Cattle: Association with herd size, season, and parity in commercial cow-calf operations. Theriogenology 2016, 86, 2156–2161.
  • Irikura, N.; Uematsu, M.; Kitahara, G.; Osawa, T.; Sasaki, Y. Effects of service number on conception rate in Japanese Black Cattle. Reprod. Domest. Anim. 2018, 53, 34–39.
  • Kasimanickam, R.; Kasimanickam, V.; Kappes, A. Timed artificial insemination strategies with or without short-term natural service and pregnancy success in beef heifers. Theriogenology 2021, 166, 97–103.
  • White, S.S.; Kasimanickam, R.K.; Kasimanickam, V.R. Fertility after two doses of PGF2α concurrently or at 6-hour interval on the day of CIDR removal in 5-Day CO-Synch progesterone-based synchronization protocols in beef heifers. Theriogenology 2016, 86, 785–790.
  • Fernandez-Novo, A.; Santos-Lopez, S.; Pesantez-Pacheco, J.L.; Pérez-Villalobos, N.; Heras-Molina, A.; Gonzalez-Martin, J.V.; Astiz, S. Effects on synchronization and reproductive efficiency of delaying the removal of the intravaginal progesterone device by 24 h in the 5d Co-Synch protocol in heifers. Anim. Open Access J. 2021, 11, 849.
  • Konishi, M.; Aoyagi, Y.; Takedomi, T.; Itakura, H.; Itoh, T.; Yazawa, S. Production and transfer of IVF embryos from individual inhibin-immunized cows by ultrasound-guided transvaginal follicular aspiration. J. Vet. Med. Sci. 1996, 58, 893–896. [Google Scholar] [CrossRef] [PubMed] Livestock Improvement Association of Japan. Available online: http://liaj.or.jp/giken/gijutsubu/seieki/jyutai.htm (accessed on 18 December 2021).
  • Sao, K.; Fujita, T. Elucidation of genes involved in the conception rates of cows decrease. Bull. Oita Prefect. Anim. Ind. Exp. Stn. 2010, 39, 17–19. Nomura, T.; Honda, T.; Mukai, F. Inbreeding and effective population size of Japanese Black Cattle. J. Anim. Sci. 2001, 79, 366–370.
  • Motoyama, M.; Sasaki, K.; Watanabe, A. Wagyu and the factors contributing to its beef quality: A japanese industry overview. Meat Sci. 2016, 120, 10–18.
  • Smith, S.B.; Lunt, D.K.; Chung, K.Y.; Choi, C.B.; Tume, R.K.; Zembayashi, M. Adiposity, fatty acid composition, and delta-9 desaturase activity during growth in beef cattle. Anim. Sci. J. 2006, 77, 478–486.
  • Nogi, T.; Honda, T.; Mukai, F.; Okagaki, T.; Oyama, K. Heritabilities and genetic correlations of fatty acid compositions in longissimus muscle lipid with carcass traits in Japanese Black Cattle. J. Anim. Sci. 2011, 89, 615–621.
  • Gotoh, T.; Albrecht, E.; Teuscher, F.; Kawabata, K.; Sakashita, K.; Iwamoto, H.; Wegner, J. Differences in muscle and fat accretion in Japanese Black and European Cattle. Meat Sci. 2009, 82, 300–308.
  • Trenkle, A.; Topel, D.G. Relationship of some endocrine measurements to growth and carcass composition of cattle. J. Anim. Sci. 1978, 46, 1604–1609.
  • Matsuzaki, M.; Takizawa, S.; Ogawa, M. Plasma Insulin, metabolite concentrations, and carcass characteristics of Japanese Black, Japanese Brown, and Holstein Steers. J. Anim. Sci. 1997, 75, 3287–3293.
  • Chen, G.; Koyama, K.; Yuan, X.; Lee, Y.; Zhou, Y.T.; O’Doherty, R.; Newgard, C.B.; Unger, R.H. Disappearance of body fat in normal rats induced by adenovirus-mediated leptin gene therapy. Proc. Natl. Acad. Sci. USA 1996, 93, 14795–14799.
  • Siegrist-Kaiser, C.A.; Pauli, V.; Juge-Aubry, C.E.; Boss, O.; Pernin, A.; Chin, W.W.; Cusin, I.; Rohner-Jeanrenaud, F.; Burger, A.G.; Zapf, J.; et al. Direct effects of leptin on brown and white adipose tissue. J. Clin. Investig. 1997, 100, 2858–2864.
  • Minokoshi, Y.; Kim, Y.-B.; Peroni, O.D.; Fryer, L.G.D.; Müller, C.; Carling, D.; Kahn, B.B. Leptin stimulates fatty-acid oxidation by activating amp-activated protein kinase. Nature 2002, 415, 339–343.
  • Corva, P.M.; Macedo, G.V.F.; Soria, L.A.; Mazzucco, J.P.; Motter, M.; Villarreal, E.L.; Schor, A.; Mezzadra, C.A.; Melucci, L.M.; Miquel, M.C. Effect of leptin gene polymorphisms on growth, slaughter and meat quality traits of grazing Brangus steers. Genet. Mol. Res. GMR 2009, 8, 105–116.
  • Silva, D.B.S.; Crispim, B.A.; Silva, L.E.; Oliveira, J.A.; Siqueira, F.; Seno, L.O.; Grisolia, A.B. Genetic variations in the leptin gene associated with growth and carcass traits in Nellore Cattle. Genet. Mol. Res. GMR 2014, 13, 3002–3012.
  • Tian, J.; Zhao, Z.; Zhang, L.; Zhang, Q.; Yu, Z.; Li, J.; Yang, R. Association of the leptin gene E2-169T>C and E3-299T>a mutations with carcass and meat quality traits of the Chinese Simmental-cross steers. Gene 2013, 518, 443–448.
  • Kawaguchi, F.; Okura, K.; Oyama, K.; Mannen, H.; Sasazaki, S. Identification of leptin gene polymorphisms associated with carcass traits and fatty acid composition in Japanese Black Cattle. Anim. Sci. J. Nihon Chikusan Gakkaiho 2017, 88, 433–438.
  • Buchanan, F.C.; Van Kessel, A.G.; Waldner, C.; Christensen, D.A.; Laarveld, B.; Schmutz, S.M. Hot Topic: An Association between a leptin single nucleotide polymorphism and milk and protein yield. J. Dairy Sci. 2003, 86, 3164–3166.
  • Glantz, M.; Månsson, H.L.; Stålhammar, H.; Paulsson, M. Effect of Polymorphisms in the leptin, leptin receptor and Acyl-CoA:Diacylglycerol Acyltransferase 1 (DGAT1) Genes and genetic polymorphism of milk proteins on bovine milk composition. J. Dairy Res. 2012, 79, 110–118.
  • Giblin, L.; Butler, S.T.; Kearney, B.M.; Waters, S.M.; Callanan, M.J.; Berry, D.P. Association of bovine leptin polymorphisms with energy output and energy storage traits in progeny tested Holstein-Friesian Dairy Cattle Sires. BMC Genet. 2010, 11, 73.
  • Fantuzzi, G.; Faggioni, R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. J. Leukoc. Biol. 2000, 68, 437–446.
  • Ingvartsen, K.L.; Boisclair, Y.R. Leptin and the regulation of food intake, energy homeostasis and immunity with special focus on periparturient ruminants. Domest. Anim. Endocrinol. 2001, 21, 215–250.
  • Yonekura, S.; Oka, A.; Noda, M.; Uozumi, N.; Yonezawa, T.; Katoh, K.; Obara, Y. Relationship between serum leptin concentrations and the marbling scores in Japanese Black cattle. Anim. Sci. J. 2002.
  • Kulcsár, M.; Jánosi, S.; Lehtolainen, T.; Kátai, L.; Delavaud, C.; Balogh, O.; Chilliard, Y.; Pyörälä, S.; Rudas, P.; Huszenicza, G. Feeding-Unrelated Factors Influencing the plasma leptin level in ruminants. Domest. Anim. Endocrinol. 2005, 29, 214–226.
  • Wu, B.; Zan, L. Enhance beef cattle improvement by embryo biotechnologies. Reprod. Domest. Anim. 2012, 47, 865–871.
  • Ferré, L.B.; Kjelland, M.E.; Strøbech, L.B.; Hyttel, P.; Mermillod, P.; Ross, P.J. Review: Recent advances in bovine in vitro embryo production: Reproductive biotechnology history and methods. Anim. Int. J. Anim. Biosci. 2020, 14, 991–1004.
  • Numabe, T.; Oikawa, T.; Kikuchi, T.; Horiuchi, T. Production efficiency of Japanese Black calves by transfer of bovine embryos produced in vitro. Theriogenology 2000, 54, 1409–1420.
  • Honda, T.; Nomura, T.; Mukai, F. Conservation of genetic diversity in the Japanese Black cattle population by the construction of partially isolated lines. J. Anim. Breed. Genet. Z. Tierz. Zucht. 2005, 122, 188–194.
  • Sasaki, Y.; Uematsu, M.; Kitahara, G.; Osawa, T. Reproductive performance of Japanese Black Cattle: Association with herd size, season, and parity in commercial cow-calf operations. Theriogenology 2016, 86, 2156–2161.
  • Irikura, N.; Uematsu, M.; Kitahara, G.; Osawa, T.; Sasaki, Y. Effects of service number on conception rate in Japanese Black Cattle. Reprod. Domest. Anim. 2018, 53, 34–39.
  • Kasimanickam, R.; Kasimanickam, V.; Kappes, A. Timed artificial insemination strategies with or without short-term natural service and pregnancy success in beef heifers. Theriogenology 2021, 166, 97–103.
  • White, S.S.; Kasimanickam, R.K.; Kasimanickam, V.R. Fertility after two doses of PGF2α concurrently or at 6-hour interval on the day of CIDR removal in 5-Day CO-Synch progesterone-based synchronization protocols in beef heifers. Theriogenology 2016, 86, 785–790.
  • Fernandez-Novo, A.; Santos-Lopez, S.; Pesantez-Pacheco, J.L.; Pérez-Villalobos, N.; Heras-Molina, A.; Gonzalez-Martin, J.V.; Astiz, S. Effects on synchronization and reproductive efficiency of delaying the removal of the intravaginal progesterone device by 24 h in the 5d Co-Synch protocol in heifers. Anim. Open Access J. 2021, 11, 849.
  • Konishi, M.; Aoyagi, Y.; Takedomi, T.; Itakura, H.; Itoh, T.; Yazawa, S. Production and transfer of IVF embryos from individual inhibin-immunized cows by ultrasound-guided transvaginal follicular aspiration. J. Vet. Med. Sci. 1996, 58, 893–896. [Google Scholar] [CrossRef] [PubMed] Livestock Improvement Association of Japan. Available online: http://liaj.or.jp/giken/gijutsubu/seieki/jyutai.htm (accessed on 18 December 2021).
  • Sao, K.; Fujita, T. Elucidation of genes involved in the conception rates of cows decrease. Bull. Oita Prefect. Anim. Ind. Exp. Stn. 2010, 39, 17–19.
  • Sutmoller, P.; Wrathall, A.E. A Quantitative assessment of the risk of transmission of foot-and-mouth disease, bluetongue and vesicular stomatitis by embryo transfer in cattle. Prev. Vet. Med. 1997, 32, 111–132.
  • Thibier, M. Embryo Transfer: A comparative biosecurity advantage in international movements of germplasm. Rev. Sci. Tech. Int. Off. Epizoot. 2011, 30, 177–188.
  • Baruselli, P.S.; Ferreira, R.M.; Vieira, L.M.; Souza, A.H.; Bó, G.A.; Rodrigues, C.A. Use of embryo transfer to alleviate infertility caused by heat stress. Theriogenology 2020, 155, 1–11.
  • Fernandez-Novo, A.; Pérez-Garnelo, S.S.; Villagrá, A.; Pérez-Villalobos, N.; Astiz, S. The effect of stress on reproduction and reproductive technologies in beef cattle-A review. Anim. Open Access J. 2020, 10, 2096.
  • Nishigai, M.; Kamomae, H.; Tanaka, T.; Kaneda, Y. Improvement of pregnancy rate in Japanese Black cows by administration of HCG to recipients of transferred frozen-thawed embryos. Theriogenology 2002, 58, 1597–1606.
  • Lukaszewska, J.; Hansel, W. Corpus luteum maintenance during early pregnancy in the cow. J. Reprod. Fertil. 1980, 59, 485–493.
  • Setiaji, A.; Oikawa, T. Genetics of heifer reproductive traits in Japanese Black Cattle. Asian-Australas. J. Anim. Sci. 2020, 33, 197–202.
  • Tanigawa, S.; Kondo, N.; Ogawa, Y.; Fujiura, T.; Shuqing, H.; Takao, Y.; Fukushima, M.; Watanabe, O.; Kohama, N. The relationship between serum vitamin A level of Japanese black cattle and light reflection on the pupil. In IEEE/SICE International Symposium on System Integration (SII); IEEE: Piscataway, NJ, USA, 2011; pp. 187–191.
  • AEMET. Available online: https://www.aemet.es/es/web/datos_abiertos/estadisticas/vigilancia_clima (accessed on 18 December 2021).
  • GMAO; NASA. Available online: https://gmao.gsfc.nasa.gov/reanalysis/MERRA-2/ (accessed on 18 December 2021). Wheather Spark. Available online: https://es.weatherspark.com/y/42909/Clima-promedio-en-Aliaga-Espa%C3%B1a-durante-todo-el-a%C3%B1o (accessed on 18 December 2021).
  • National Research Council. Nutrient Requirements of Beef Cattle: Seventh Revised Edition: Update 2000; The National Academies Press: Washington, DC, USA, 2000.
  • Stringfellow, D.A.; Givens, M.D.; International Embryo Transfer Society. Manual of the International Embryo Transfer Society: A Procedural Guide and General Information for the Use of Embryo Transfer Technology Emphasizing Sanitary Procedures; International Embryo Transfer Society; Savory, Ill.: Boulder, CO, USA, 2010.
  • Dochi, O. Direct transfer of frozen-thawed bovine embryos and its application in cattle reproduction management. J. Reprod. Dev. 2019, 65, 389–396.
  • Leibo, S.P. A one-step method for direct nonsurgical transfer of frozen-thawed bovine embryos. Theriogenology 1984, 21, 767–790.
  • Edmonson, A.J.; Lean, I.J.; Weaver, L.D.; Farver, T.; Webster, G. A body condition scoring chart for Holstein Dairy cows. J. Dairy Sci. 1989, 72, 68–78.
  • An, L.; Ling, P.P.; Zhu, X.; Liu, Y.; Zhang, F.; Ma, X.; Xu, B.; Wang, Y.; Du, Z.; Yang, L.; et al. Successful vitrification of in vivo embryos collected from superovulated Japanese Black cattle (Wagyu). Reprod. Domest. Anim. 2016, 51, 255–261.
  • American Embryo Transfer Association. Annual Survey of Members. Available online: https://www.aeta.org/survey.asp (accessed on 18 December 2021).
  • Phillips, P.E.; Jahnke, M.M. Embryo transfer (techniques, donors, and recipients). Vet. Clin. N. Am. Food Anim. Pract. 2016, 32, 365–385.
  • Shull, J.W. Managing the problem beef embryo donor. In Proceedings; Society for Theriogenology: Montgomery, AL, USA, 2009; pp. 283–288.
  • Mikkola, M.; Hasler, J.F.; Taponen, J. Factors affecting embryo production in superovulated Bos Taurus Cattle. Reprod. Fertil. Dev. 2019, 32, 104–124.
  • Zoda, A.; Urakawa, M.; Oono, Y.; Ogawa, S.; Satoh, M. Estimation of genetic parameters for superovulatory response traits in Japanese Black Cows. J. Anim. Sci. 2021, 99, skab265.
  • Watanabe, U.; Takagi, M.; Yamato, O.; Otoi, T.; Okamoto, K. Retrospective surveillance of metabolic parameters affecting reproductive performance of Japanese Black Breeding cows. J. Vet. Sci. 2014, 15, 283–288.
  • Sakatani, M.; Balboula, A.Z.; Yamanaka, K.; Takahashi, M. Effect of summer heat environment on body temperature, estrous cycles and blood antioxidant levels in Japanese Black cow. Anim. Sci. J. Nihon Chikusan Gakkaiho 2012, 83, 394–402.
  • Chebel, R.C.; Demétrio, D.G.B.; Metzger, J. Factors affecting success of embryo collection and transfer in large dairy herds. Theriogenology 2008, 69, 98–106.
  • Hansen, P.J.; Drost, M.; Rivera, R.M.; Paula-Lopes, F.F.; Al-Katanani, Y.M.; Krininger, C.E.; Chase, C.C. Adverse impact of heat stress on embryo production: Causes and strategies for mitigation. Theriogenology 2001, 55, 91–103.
  • Sartori, R.; Sartor-Bergfelt, R.; Mertens, S.A.; Guenther, J.N.; Parrish, J.J.; Wiltbank, M.C. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 2002, 85, 2803–2812.
  • Roth, Z. Physiology and Endocrinology Symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function. J. Anim. Sci. 2015, 93, 2034–2044.
  • De Rensis, F.; Lopez-Gatius, F.; García-Ispierto, I.; Morini, G.; Scaramuzzi, R.J. Causes of declining fertility in dairy cows during the warm season. Theriogenology 2017, 91, 145–153.
  • Takuma, T.; Sakai, S.; Ezoe, D.; Ichimaru, H.; Jinnouchi, T.; Kaedei, Y.; Nagai, T.; Otoi, T. Effects of season and reproductive phase on the quality, quantity and developmental competence of oocytes aspirated from Japanese Black cows. J. Reprod. Dev. 2010, 56, 55–59.
  • Kasimanickam, R.; Kasimanickam, V.; Kastelic, J.P.; Ramsey, K. Metabolic biomarkers, body condition, uterine inflammation and response to superovulation in lactating Holstein Cows. Theriogenology 2020, 146, 71–79.
  • Bender, R.W.; Hackbart, K.S.; Dresch, A.R.; Carvalho, P.D.; Vieira, L.M.; Crump, P.M.; Guenther, J.N.; Fricke, P.M.; Shaver, R.D.; Combs, D.K.; et al. Effects of acute feed restriction combined with targeted use of increasing luteinizing hormone content of follicle-stimulating hormone preparations on ovarian superstimulation, fertilization, and embryo quality in lactating dairy cows. J. Dairy Sci. 2014, 97, 764–778.
  • Yaakub, H.; O’Callaghan, D.; Boland, M.P. Effect of type and quantity of concentrates on superovulation and embryo yield in beef heifers. Theriogenology 1999, 51, 1259–1266.
  • Otomaru, K.; Shiga, H.; Kanome, J.; Yanagita, K. Blood biochemical values in Japanese Black Breeding cows in Kagoshima Prefecture, Japan. J. Vet. Med. Sci. 2015, 77, 1021–1023.
  • Bobe, G.; Young, J.W.; Beitz, D.C. Invited Review: Pathology, etiology, prevention, and treatment of fatty liver in dairy cows. J. Dairy Sci. 2004, 87, 3105–3124.
  • LeBlanc, S. Monitoring metabolic health of dairy cattle in the transition period. J. Reprod. Dev. 2010, 56, S29–S35.
  • Takahashi, M.; Sawada, K.; Kawate, N.; Inaba, T.; Tamada, H. Improvement of superovulatory response and pregnancy rate after transfer of embryos recovered from Japanese Black cows fed rumen bypass polyunsaturated fatty acids. J. Vet. Med. Sci. 2013, 75, 1485–1490.
  • Cerri, R.L.A.; Juchem, S.O.; Chebel, R.C.; Rutigliano, H.M.; Bruno, R.G.S.; Galvão, K.N.; Thatcher, W.W.; Santos, J.E.P. Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J. Dairy Sci. 2009, 92, 1520–1531.
  • Hussein, H.A.; Thurmann, J.-P.; Staufenbiel, R. 24-h variations of blood serum metabolites in high yielding dairy cows and calves. BMC Vet. Res. 2020, 16, 327.
  • Katoh, K.; Kouno, S.; Okazaki, A.; Suzuki, K.; Obara, Y. Interaction of GH polymorphism with body weight and endocrine functions in Japanese Black calves. Domest. Anim. Endocrinol. 2008, 34, 25–30.
  • Smith, G.D.; Jackson, L.M.; Foster, D.L. Leptin regulation of reproductive function and fertility. Theriogenology 2002, 57, 73–86.
  • Batista, A.M.; Gomes, W.A.; Carvalho, C.C.D.; Monteiro, P.L.J.; Silva, F.L.M.; Almeida, F.C.; Soares, P.C.; Carneiro, G.F.; Guerra, M.M.P. Effect of leptin on in vivo goat embryo production. Reprod. Domest. Anim. 2014, 49, 476–480.
  • Williams, G.L.; Amstalden, M.; Garcia, M.R.; Stanko, R.L.; Nizielski, S.E.; Morrison, C.D.; Keisler, D.H. Leptin and Its role in the central regulation of reproduction in cattle. Domest. Anim. Endocrinol. 2002, 23, 339–349.
  • Zieba, D.A.; Amstalden, M.; Williams, G.L. Regulatory roles of leptin in reproduction and metabolism: A comparative review. Domest. Anim. Endocrinol. 2005, 29, 166–185.
  • D’Occhio, M.J.; Baruselli, P.S.; Campanile, G. Influence of nutrition, body condition, and metabolic status on reproduction in female beef cattle: A review. Theriogenology 2019, 125, 277–284.
  • Nabenishi, H.; Sugino, F.; Konaka, R.; Yamazaki, A. Conception rate of Holstein and Japanese Black cattle following embryo transfer in southwestern Japan. Anim. Sci. J. Nihon Chikusan Gakkaiho 2018, 89, 1073–1078.
  • Rodrigues, M.; Bonotto, A.; Acosta, D.; Boligon, A.A.; Corrêa, M.N.; Brauner, C.C. Effect of oestrous synchrony between embryo donors and recipients, embryo quality and state on the pregnancy rate in beef cattle. Reprod. Domest. Anim. 2018, 53, 152–156.
  • Bó, G.A.; Cedeño, A.; Mapletoft, R.J. Strategies to increment in vivo and in vitro embryo production and transfer in cattle. Anim. Reprod. 2019, 16, 411–422.
  • Rocha, J.C.; Passalia, F.; Matos, F.D.; Maserati, M.P.; Alves, M.F.; de Almeida, T.G.; Cardoso, B.L.; Basso, A.C.; Nogueira, M.F.G. Methods for assessing the quality of mammalian embryos: How far we are from the gold standard? JBRA Assist. Reprod. 2016, 20, 150–158.
  • Hasler, J.F. The Holstein cow in embryo transfer today as compared to 20 years ago. Theriogenology 2006, 65, 4–16.
  • Gómez, E.; Muñoz, M.; Gatien, J.; Carrocera, S.; Martín-González, D.; Salvetti, P. Metabolomic identification of pregnancy-specific biomarkers in blood plasma of Bos Taurus beef cattle after transfer of in vitro produced embryos. J. Proteom. 2020, 225, 103883.
  • Forde, N.; Simintiras, C.A.; Sturmey, R.G.; Graf, A.; Wolf, E.; Blum, H.; Lonergan, P. Effect of lactation on conceptus-maternal interactions at the initiation of implantation in cattle: I. Effects on the conceptus transcriptome and amino acid composition of the uterine luminal fluid. Biol. Reprod. 2017, 97, 798–809.
  • Gomez, E.; Canela, N.; Herrero, P.; Cereto, A.; Gimeno, I.; Carrocera, S.; Martin-Gonzalez, D.; Murillo, A.; Muñoz, M. Metabolites secreted by bovine embryos in vitro predict pregnancies that the recipient plasma metabolome cannot, and vice versa. Metabolites 2021, 11, 162.
  • Sutmoller, P.; Wrathall, A.E. A Quantitative assessment of the risk of transmission of foot-and-mouth disease, bluetongue and vesicular stomatitis by embryo transfer in cattle. Prev. Vet. Med. 1997, 32, 111–132.
  • Thibier, M. Embryo Transfer: A comparative biosecurity advantage in international movements of germplasm. Rev. Sci. Tech. Int. Off. Epizoot. 2011, 30, 177–188.
  • Baruselli, P.S.; Ferreira, R.M.; Vieira, L.M.; Souza, A.H.; Bó, G.A.; Rodrigues, C.A. Use of embryo transfer to alleviate infertility caused by heat stress. Theriogenology 2020, 155, 1–11.
  • Fernandez-Novo, A.; Pérez-Garnelo, S.S.; Villagrá, A.; Pérez-Villalobos, N.; Astiz, S. The effect of stress on reproduction and reproductive technologies in beef cattle-A review. Anim. Open Access J. 2020, 10, 2096.
  • Nishigai, M.; Kamomae, H.; Tanaka, T.; Kaneda, Y. Improvement of pregnancy rate in Japanese Black cows by administration of HCG to recipients of transferred frozen-thawed embryos. Theriogenology 2002, 58, 1597–1606.
  • Lukaszewska, J.; Hansel, W. Corpus luteum maintenance during early pregnancy in the cow. J. Reprod. Fertil. 1980, 59, 485–493.
  • Setiaji, A.; Oikawa, T. Genetics of heifer reproductive traits in Japanese Black Cattle. Asian-Australas. J. Anim. Sci. 2020, 33, 197–202.
  • Tanigawa, S.; Kondo, N.; Ogawa, Y.; Fujiura, T.; Shuqing, H.; Takao, Y.; Fukushima, M.; Watanabe, O.; Kohama, N. The relationship between serum vitamin A level of Japanese black cattle and light reflection on the pupil. In IEEE/SICE International Symposium on System Integration (SII); IEEE: Piscataway, NJ, USA, 2011; pp. 187–191.
  • AEMET. Available online: https://www.aemet.es/es/web/datos_abiertos/estadisticas/vigilancia_clima (accessed on 18 December 2021). GMAO; NASA. Available online: https://gmao.gsfc.nasa.gov/reanalysis/MERRA-2/ (accessed on 18 December 2021). Wheather Spark. Available online: https://es.weatherspark.com/y/42909/Clima-promedio-en-Aliaga-Espa%C3%B1a-durante-todo-el-a%C3%B1o (accessed on 18 December 2021).
  • National Research Council. Nutrient Requirements of Beef Cattle: Seventh Revised Edition: Update 2000; The National Academies Press: Washington, DC, USA, 2000.
  • Stringfellow, D.A.; Givens, M.D.; International Embryo Transfer Society. Manual of the International Embryo Transfer Society: A Procedural Guide and General Information for the Use of Embryo Transfer Technology Emphasizing Sanitary Procedures; International Embryo Transfer Society; Savory, Ill.: Boulder, CO, USA, 2010.
  • Dochi, O. Direct transfer of frozen-thawed bovine embryos and its application in cattle reproduction management. J. Reprod. Dev. 2019, 65, 389–396.
  • Leibo, S.P. A one-step method for direct nonsurgical transfer of frozen-thawed bovine embryos. Theriogenology 1984, 21, 767–790.
  • Edmonson, A.J.; Lean, I.J.; Weaver, L.D.; Farver, T.; Webster, G. A body condition scoring chart for Holstein Dairy cows. J. Dairy Sci. 1989, 72, 68–78.
  • An, L.; Ling, P.P.; Zhu, X.; Liu, Y.; Zhang, F.; Ma, X.; Xu, B.; Wang, Y.; Du, Z.; Yang, L.; et al. Successful vitrification of in vivo embryos collected from superovulated Japanese Black cattle (Wagyu). Reprod. Domest. Anim. 2016, 51, 255–261.
  • American Embryo Transfer Association. Annual Survey of Members. Available online: https://www.aeta.org/survey.asp (accessed on 18 December 2021).
  • Phillips, P.E.; Jahnke, M.M. Embryo transfer (techniques, donors, and recipients). Vet. Clin. N. Am. Food Anim. Pract. 2016, 32, 365–385.
  • Shull, J.W. Managing the problem beef embryo donor. In Proceedings; Society for Theriogenology: Montgomery, AL, USA, 2009; pp. 283–288.
  • Mikkola, M.; Hasler, J.F.; Taponen, J. Factors affecting embryo production in superovulated Bos Taurus Cattle. Reprod. Fertil. Dev. 2019, 32, 104–124.
  • Zoda, A.; Urakawa, M.; Oono, Y.; Ogawa, S.; Satoh, M. Estimation of genetic parameters for superovulatory response traits in Japanese Black Cows. J. Anim. Sci. 2021, 99, skab265.
  • Watanabe, U.; Takagi, M.; Yamato, O.; Otoi, T.; Okamoto, K. Retrospective surveillance of metabolic parameters affecting reproductive performance of Japanese Black Breeding cows. J. Vet. Sci. 2014, 15, 283–288.
  • Sakatani, M.; Balboula, A.Z.; Yamanaka, K.; Takahashi, M. Effect of summer heat environment on body temperature, estrous cycles and blood antioxidant levels in Japanese Black cow. Anim. Sci. J. Nihon Chikusan Gakkaiho 2012, 83, 394–402.
  • Chebel, R.C.; Demétrio, D.G.B.; Metzger, J. Factors affecting success of embryo collection and transfer in large dairy herds. Theriogenology 2008, 69, 98–106.
  • Hansen, P.J.; Drost, M.; Rivera, R.M.; Paula-Lopes, F.F.; Al-Katanani, Y.M.; Krininger, C.E.; Chase, C.C. Adverse impact of heat stress on embryo production: Causes and strategies for mitigation. Theriogenology 2001, 55, 91–103.
  • Sartori, R.; Sartor-Bergfelt, R.; Mertens, S.A.; Guenther, J.N.; Parrish, J.J.; Wiltbank, M.C. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J. Dairy Sci. 2002, 85, 2803–2812.
  • Roth, Z. Physiology and Endocrinology Symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function. J. Anim. Sci. 2015, 93, 2034–2044.
  • De Rensis, F.; Lopez-Gatius, F.; García-Ispierto, I.; Morini, G.; Scaramuzzi, R.J. Causes of declining fertility in dairy cows during the warm season. Theriogenology 2017, 91, 145–153.
  • Takuma, T.; Sakai, S.; Ezoe, D.; Ichimaru, H.; Jinnouchi, T.; Kaedei, Y.; Nagai, T.; Otoi, T. Effects of season and reproductive phase on the quality, quantity and developmental competence of oocytes aspirated from Japanese Black cows. J. Reprod. Dev. 2010, 56, 55–59.
  • Kasimanickam, R.; Kasimanickam, V.; Kastelic, J.P.; Ramsey, K. Metabolic biomarkers, body condition, uterine inflammation and response to superovulation in lactating Holstein Cows. Theriogenology 2020, 146, 71–79.
  • Bender, R.W.; Hackbart, K.S.; Dresch, A.R.; Carvalho, P.D.; Vieira, L.M.; Crump, P.M.; Guenther, J.N.; Fricke, P.M.; Shaver, R.D.; Combs, D.K.; et al. Effects of acute feed restriction combined with targeted use of increasing luteinizing hormone content of follicle-stimulating hormone preparations on ovarian superstimulation, fertilization, and embryo quality in lactating dairy cows. J. Dairy Sci. 2014, 97, 764–778.
  • Yaakub, H.; O’Callaghan, D.; Boland, M.P. Effect of type and quantity of concentrates on superovulation and embryo yield in beef heifers. Theriogenology 1999, 51, 1259–1266.
  • Otomaru, K.; Shiga, H.; Kanome, J.; Yanagita, K. Blood biochemical values in Japanese Black Breeding cows in Kagoshima Prefecture, Japan. J. Vet. Med. Sci. 2015, 77, 1021–1023.
  • Bobe, G.; Young, J.W.; Beitz, D.C. Invited Review: Pathology, etiology, prevention, and treatment of fatty liver in dairy cows. J. Dairy Sci. 2004, 87, 3105–3124.
  • LeBlanc, S. Monitoring metabolic health of dairy cattle in the transition period. J. Reprod. Dev. 2010, 56, S29–S35.
  • Takahashi, M.; Sawada, K.; Kawate, N.; Inaba, T.; Tamada, H. Improvement of superovulatory response and pregnancy rate after transfer of embryos recovered from Japanese Black cows fed rumen bypass polyunsaturated fatty acids. J. Vet. Med. Sci. 2013, 75, 1485–1490.
  • Cerri, R.L.A.; Juchem, S.O.; Chebel, R.C.; Rutigliano, H.M.; Bruno, R.G.S.; Galvão, K.N.; Thatcher, W.W.; Santos, J.E.P. Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J. Dairy Sci. 2009, 92, 1520–1531.
  • Hussein, H.A.; Thurmann, J.-P.; Staufenbiel, R. 24-h variations of blood serum metabolites in high yielding dairy cows and calves. BMC Vet. Res. 2020, 16, 327.
  • Katoh, K.; Kouno, S.; Okazaki, A.; Suzuki, K.; Obara, Y. Interaction of GH polymorphism with body weight and endocrine functions in Japanese Black calves. Domest. Anim. Endocrinol. 2008, 34, 25–30.
  • Smith, G.D.; Jackson, L.M.; Foster, D.L. Leptin regulation of reproductive function and fertility. Theriogenology 2002, 57, 73–86.
  • Batista, A.M.; Gomes, W.A.; Carvalho, C.C.D.; Monteiro, P.L.J.; Silva, F.L.M.; Almeida, F.C.; Soares, P.C.; Carneiro, G.F.; Guerra, M.M.P. Effect of leptin on in vivo goat embryo production. Reprod. Domest. Anim. 2014, 49, 476–480.
  • Williams, G.L.; Amstalden, M.; Garcia, M.R.; Stanko, R.L.; Nizielski, S.E.; Morrison, C.D.; Keisler, D.H. Leptin and Its role in the central regulation of reproduction in cattle. Domest. Anim. Endocrinol. 2002, 23, 339–349.
  • Zieba, D.A.; Amstalden, M.; Williams, G.L. Regulatory roles of leptin in reproduction and metabolism: A comparative review. Domest. Anim. Endocrinol. 2005, 29, 166–185.
  • D’Occhio, M.J.; Baruselli, P.S.; Campanile, G. Influence of nutrition, body condition, and metabolic status on reproduction in female beef cattle: A review. Theriogenology 2019, 125, 277–284.
  • Nabenishi, H.; Sugino, F.; Konaka, R.; Yamazaki, A. Conception rate of Holstein and Japanese Black cattle following embryo transfer in southwestern Japan. Anim. Sci. J. Nihon Chikusan Gakkaiho 2018, 89, 1073–1078.
  • Rodrigues, M.; Bonotto, A.; Acosta, D.; Boligon, A.A.; Corrêa, M.N.; Brauner, C.C. Effect of oestrous synchrony between embryo donors and recipients, embryo quality and state on the pregnancy rate in beef cattle. Reprod. Domest. Anim. 2018, 53, 152–156.
  • Bó, G.A.; Cedeño, A.; Mapletoft, R.J. Strategies to increment in vivo and in vitro embryo production and transfer in cattle. Anim. Reprod. 2019, 16, 411–422.
  • Rocha, J.C.; Passalia, F.; Matos, F.D.; Maserati, M.P.; Alves, M.F.; de Almeida, T.G.; Cardoso, B.L.; Basso, A.C.; Nogueira, M.F.G. Methods for assessing the quality of mammalian embryos: How far we are from the gold standard? JBRA Assist. Reprod. 2016, 20, 150–158.
  • Hasler, J.F. The Holstein cow in embryo transfer today as compared to 20 years ago. Theriogenology 2006, 65, 4–16.
  • Gómez, E.; Muñoz, M.; Gatien, J.; Carrocera, S.; Martín-González, D.; Salvetti, P. Metabolomic identification of pregnancy-specific biomarkers in blood plasma of Bos Taurus beef cattle after transfer of in vitro produced embryos. J. Proteom. 2020, 225, 103883.
  • Forde, N.; Simintiras, C.A.; Sturmey, R.G.; Graf, A.; Wolf, E.; Blum, H.; Lonergan, P. Effect of lactation on conceptus-maternal interactions at the initiation of implantation in cattle: I. Effects on the conceptus transcriptome and amino acid composition of the uterine luminal fluid. Biol. Reprod. 2017, 97, 798–809.
  • Gomez, E.; Canela, N.; Herrero, P.; Cereto, A.; Gimeno, I.; Carrocera, S.; Martin-Gonzalez, D.; Murillo, A.; Muñoz, M. Metabolites secreted by bovine embryos in vitro predict pregnancies that the recipient plasma metabolome cannot, and vice versa. Metabolites 2021, 11, 162.