Abstract
Embryo transfer (ET) in bovines was created with the purpose of increasing the pregnancy rate (PR) of animals with high genetic value; however, multiple factors have been found to affect the success of this reproductive biotechnology. These factors are frequently grouped in intrinsic and extrinsic factors. Thus, the objective of the present experiments was to assess the effect of intrinsic and extrinsic factors on the pregnancy rate under tropical conditions. To do this a total of 648 embryo transfer (ET) procedures were performed between January and December 2021. The intrinsic factors were size and location of the corpus luteum, body condition, genetic group, age and parity; while extrinsic factors were location of the farm, environmental comfort, season in which the ET was carried out, prevailing weather conditions, and the preservation, quality, and the development stage of embryos at the time of ET. A χi2 was used for analysis of main effects, and logistic regression analysis to calculate the probability of pregnancy and the association between intrinsic or extrinsic factors; additionally, a multivariate analysis of data clusters was used to find a linkage between the effects. While recipient female age had a negative effect (Odds ratio = 0.345—0.871) on PR (p < 0.05), being higher in younger cows, the rest of the intrinsic factors did not affect the PR. The significant (p < 0.05) extrinsic factors were THI category, season of year and type of embryo preservation, showing that the highest PR (p < 0.05) was obtained in the comfort THI category, during the winter season and using fresh embryos for transfer. The clustering analysis did not show any linkage between PR and intrinsic factors, while a linkage (p < 0.05) was found with season of the year and embryo preservation as extrinsic factors. It is concluded that age of the recipient cow and environmental conditions at the time of the embryo transfer are key factors to be considered for a successful pregnancy rate from in-vitro ET programs using dual-purpose cows under tropical conditions.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are not publicly available due to it belongs to the farms that kindly participated in the study, but are available from the corresponding author on reasonable request. Requests to access the datasets should be directed to BDM.
References
Abdulkadir, K., Gülnaz, M., Ebru, B., Baris, G., Abdülkadir, O., Hayrettin, o. & Ahmet, G. (2016). The effect of ovulatory follicle size at the time of insemination on pregnancy rate in lactating dairy cows. Turkish Journal of Veterinary & Animal Sciences. 40 (1), 68-74. https://doi.org/10.3906/vet-1506-59
Aguilar, A., Vendramini, J., Arthington, J., Sollenberger, L., Sánchez, J., da Silva, W, Valente, A. & Salvo, P. (2014). Stocking rate effects on ‘Jiggs’ bermudagrass pastures grazed by heifers receiving supplementation. Crop Science, 54(6), 2872-2879. DOI: https://doi.org/10.2135/cropsci2014.02.0135
Amundson, J.L., Mader, T.L., Rasby, R.J. & Hu, Q.S. (2006) Environmental effects on pregnancy rate in beef cattle. Journal Animal Science, 84, 3415–3420. DOI: https://doi.org/10.2527/jas.2005-611
Arrieta-González, A., Hernández-Beltrán, A., Barrientos-Morales, M., Martínez-Herrera, D. I., Cervantes-Acosta, P., Rodríguez-Andrade, A., & Dominguez-Mancera, B. (2022). Characterization and technological typification of bovine dual-purpose system of the Huasteca Veracruzana Mexico. Revista MVZ Cordoba, 27(2), 2022. https://doi.org/10.21897/rmvz.2444
Baruselli, P. S., Ferreira, R. M., Sales, J. N., Gimenes, L. U., Sá Filho, M. F., Martins, C. M., Rodrigues, C. A., & Bó, G. A. (2011). Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology, 76(9), 1583–1593. https://doi.org/10.1016/j.theriogenology.2011.06.006
Beck, H., Zimmermann, N., McVicar, T. et al. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Science Data 5, 180214 (2018). https://doi.org/10.1038/sdata.2018.214
Carnero S., Sylvia, Huanca L., Wilfredo, Cordero R., Aída, Vásquez E., Martha, & Huanca M., Teodosio. (2011). Transferencia embrionaria ipsilateral y contralateral a la posición del cuerpo lúteo y supervivencia embrionaria en llamas. Revista de Investigaciones Veterinarias del Perú, 22(2), 114–120. https://doi.org/10.15381/rivep.v22i2.278
Cruz Hernández, A., Hernández Garay, A., Chay Canul, A.J., Mendoza Pedroza, S.I., Ramírez Vera, S., Rojas García, Adelaido R., & Ventura Ríos, J. (2017). Componentes del rendimiento y valor nutritivo de Brachiaria humidicola cv Chetumal a diferentes estrategias de pastoreo. Revista Mexicana de Ciencias Agrícolas, 8(3), 599–610. https://doi.org/10.29312/remexca.v8i3.34
Cutini, A., Teruel, M. & Cabodevila, J. (2000) Factores que determinan el resultado de la transferencia no quirúrgica de embriones bovinos (Factors determining the results of non-surgical bovine embryo transference). Revista Taurus, 7(8), 35-47.
Duica A. A., Tovío L. N., y Grajales L. H. (2007). Factores que afectan la eficiencia reproductiva de la hembra receptora en un programa de trasplante de embriones bovinos. (Factors affecting reproductive efficiency of receiving cows in a bovine embryo transplant program) Revista Médica Veterinaria. (Bogotá); (14), 107–124,
Domínguez-Mancera, B., Hernández-Beltrán, A., Rodríguez-Andrade, A., Cervantes-Acosta, P., Barrientos-Morales M. and Pinos-Rodríguez, JM. (2017). Changes in livestock weather security index (Temperature Humidity Index, THI) during the period 1917-2016 in Veracruz, Mexico. Journal of Animal Research, 7(6), 983-991. https://doi.org/10.5958/2277-940x.2017.00149.8
Erdem, H., Karasahin, T., Alkan, H. et al. (2020). Effect of embryo quality and developmental stages on pregnancy rate during fresh embryo transfer in beef heifers. Tropical Animal Health and Production. 52, 2541–2547 https://doi.org/10.1007/s11250-020-02287-6
Fernandes, C. A., Palhao, M. P., Figueiredo, A. C., Ribeiro, J. R., Fonseca e Silva, F., & Viana, J. H. (2016). Weight gain potential affects pregnancy rates in bovine embryo recipients raised under pasture conditions. Tropical Animal Health and Production, 48(1), 103–107. https://doi.org/10.1007/s11250-015-0926-0
Ferraz, P. A., Burnley, C., Karanja, J., Viera-Neto, A., Santos, J. E., Chebel, R. C., & Galvão, K. N. (2016). Factors affecting the success of a large embryo transfer program in Holstein cattle in a commercial herd in the southeast region of the United States. Theriogenology, 86(7), 1834–1841. https://doi.org/10.1016/j.theriogenology.2016.05.032
Ferraz, P.A., Galvão, M.V., Soares, A.R., Coelho, M.C.L., dos Santos, T.C.B., & Ribeiro, A.L.F. (2017). The effect of the intensity of estrus expression on the follicular diameter and fertility of Nellore cows managed under a FTAI program. Ciencia Animal Brasileira, 18, 1-9. https://doi.org/10.1590/1809-6891v18e-37643
Filipiak, Y, Viqueira, M, & Bielli, A. (2016). Desarrollo y dinámica de los folículos ováricos desde la etapa fetal hasta la prepuberal en bovinos. Veterinaria (Montevideo), 52(202), 2.
Flores-Alca, V., Beltrán-Barriga, P. A., Mamani-Paredes, J., Canaza-Cayo, A.W. (2022). Transferencia de embriones en vacas brown swiss y evaluación de los terneros nacidos hasta el destete. Revista de Ciencias Agrarias - Journal of Agricultural Science. 8(2), 28–40.
Fuentes, S. (2015). Incremento del porcentaje de gestación en la transferencia de embriones bovinos de aptitud láctea mediante tratamientos hormonales de sincronización y postransferencia de la hembra receptora. Universidad de León, Facultad De Veterinaria Departamento De Sanidad Animal, España. https://doi.org/10.18002/10612/5984
García y González, Ethel C., Mendoza Medel, G., Pineda Burgos, Blanca C., Romero Rodríguez, Perla I., Hernández Ruiz, P.E., Vicente Pérez, R., Valencia Franco, E., & Ponce, J.L. (2019). Parity does not affect the reproductive response of Suizo Americano cows submitted to embryo transference in tropical areas of Guerrero. Cuban Journal of Agricultural Science, 53(2), 109-117.
Ghoribi, L., Hireche, S., and Chibat, M. (2012). Study of some reproductive parameters in bovine dairy farms in the east of Algeria. Livestock Research for Rural Development, 24 (2). http://www.lrrd.org/lrrd24/2/ghor24032.htm
Granados-Rivera, L.D., Quiroz-Valiente, J., Maldonado-Jáquez, J.A., Granados-Zurita, L., Díaz-Rivera, P., & Oliva-Hernández, J. (2018). Caracterización y tipificación del sistema doble propósito en la ganadería bovina del Distrito de Desarrollo Rural 151, Tabasco, México. Acta Universitaria, 28(6), 47–57. https://doi.org/10.15174/au.2018.1916
Hahn, G., Mader, T., Gaughan, J., Hu, Q. & Nienaber, J. (1999). Heat waves and their impacts on feedlot cattle. In: Proceedings, 15th International Society Biometeorology Congress, 11(1), 353–357.
Hasler J. F. (2001). Factors affecting frozen and fresh embryo transfer pregnancy rates in cattle. Theriogenology, 56(9), 1401–1415. https://doi.org/10.1016/s0093-691x(01)00643-4
Hernandez-Fonseca H. J., Perea F. P., Argudo D. E., Rosillo I. C. (2023). 124 Transfer of in vitro-produced hatched blastocyst as an alternative to increasing pregnancy rate in a commercial cattle farm in the tropics. Reproduction, Fertility and Development 35, 189-190. https://doi.org/10.1071/RDv35n2Ab124
Hernández, J., Lara, D., Vázquez, D. & Retureta, A. (2019) Unidad de producción bovina con transferencia de embriones en el sur de Veracruz. (Embryo transfer in a bovine production unit located in southern Veracruz state) Revista Biológico-Agropecuaria Tuxpan, 7(2), 222–232. https://doi.org/10.47808/revistabioagro.v7i2.113
Horrach Junco, M. N., Bertot Valdés, J. A., Vázquez Montes de Oca, R., & Garay Durba, M. (2020). Eficiencia reproductiva de sistemas vacunos en inseminación artificial. Tendencias actuales y perspectivas. Revista de Producción Animal, 32(3).
IETS. International Embryo Transfer. (1998). Manual of the International Embryo Transfer Society. Stringfellow DA., Seidel SM (eds). USA: Ed. Savoy. 170 p.
Jousan, F. D., & Hansen, P. J. (2004). Insulin-like growth factor-I as a survival factor for the bovine preimplantation embryo exposed to heat shock. Biology of Reproduction, 71(5), 1665–1670. https://doi.org/10.1095/biolreprod.104.032102
Kuwayama, M., Vajta, G., Ieda, S., & Kato, O. (2005). Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination. Reprod. BioMedicine online 11 (5): 608-614. https://doi.org/10.1016/S1472-6483(10)61169-8
López-García, G., Góngora-Orjuela, A., Díaz-González, F., & Rojas-Rodríguez, A. (2019). Evaluación del estado metabólico, el peso vivo y la condición corporal durante la gestación en vacas de carne en la Altillanura colombiana. ORINOQUIA, 23(2), 13–24. https://doi.org/10.22579/20112629.565
López-Quiñonez, E., Albarrán-Tamayo, F.I., Ramírez-Emiliano, J., Bañuelos-Hernández, B., & Cruz-Hernández, A. (2021). Índice de temperatura y humedad (THI) respaldado por el cortisol capilar en ganado lechero para la medición de estrés calórico crónico. Nova Scientia, 13(27), 00012. https://doi.org/10.21640/ns.v13i27.2811
López, F. (2006). Relación entre condición corporal y eficiencia reproductiva en vacas Holstein. Revista Biotecnología en el Sector Agropecuario y Agroindustrial, 4(1), 77-86.
Mapletoft R. J. (1986). Bovine Embryo Transfer. In: Current Therapy in Theriogenology, 2, 54-63.
Méndez- Cortés V., Mora-Flores, J.S., García-Salazar, J.A., Hernández-Mendo O., García-Mata R., and García-Sánchez R.C. (2019). Tipología de productores de ganado bovino en la zona norte de Veracruz. Tropical and Subtropical Agroecosystems 22: 305–314 https://doi.org/10.56369/tsaes.2723
Mellado, M., Sepúlveda, E., Macias-Cruz, U., Avendaño-Reyes, L., García, J. E., Veliz, F. G., & Rodríguez, A. (2014). Effects of month of breeding on reproductive efficiency of Holstein cows and heifers inseminated with sex-sorted or conventional semen in a hot environment. Tropical Animal Health and Production, 46(1), 265–269. https://doi.org/10.1007/s11250-013-0470-8
Menegassi, S., Barcellos, J., Dias, E., Koetz, C., Pereira, G., Peripolli, V., McManus, C., Andrighetto, C. & Lopes, F. (2015). Scrotal infrared digital thermography as a predictor of seasonal effects on sperm traits in Braford bulls. International Journal of Biometeorology, 59, 357-364. DOI: https://doi.org/10.1007/s00484-014-0847-z
Merton, J. S., de Roos, A. P., Mullaart, E., de Ruigh, L., Kaal, L., Vos, P. L., & Dieleman, S. J. (2003). Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology, 59(2), 651–674. https://doi.org/10.1016/s0093-691x(02)01246-3
Munar, C., Mujica, I., Martin, E., Irouleguy, J., Huter, S., Alonso, H., Arzeno, M., Goitia, O., Farnetano, N., & Anchordoqui, J. (2013). Factores que afectan la eficiencia de las receptoras en ganado lechero y de carne. Spermova, 3(1), 15–22. https://doi.org/10.18548/aspe
Narváez Bedoya, H.J. (2021). Efecto del ibuprofeno en el establecimiento de la gestación de embriones bovinos producidos in vitro. Revista de Investigaciones Veterinarias del Perú, 32(2), e17798. https://doi.org/10.15381/rivep.v32i2.17798
Nienabar, J. & Hahn, G. (2007). Livestock production system management responses to thermal challenges. International Journal of Biometeorology. 52, 149-157. https://doi.org/10.1007/s00484-007-0103-x
Odeón, M.M., & Romera, S.A. (2017). Estrés en ganado: causas y consecuencias. Revista Veterinaria, 28(1), 69–77. https://doi.org/10.30972/vet.2811556
Palma, G. (2008). Biotecnología de la Reproducción. 2° ed (Reproductive Biotechnology, 2nd edition). Mar del Plata: Producción Gráfica Integral. 669 p.
Parra, M. E. S., Parra, C. A. S., Álvarez, S. M., Garzón, D. A., García, G. S., Inga, C. T., & Lucero, A. G. (2018). Assessment of two Superovulation Protocols for Embryo Production in Holstein Cows. Revista de Producción Animal, 30(2), 54–58.
Pérez-Mora, A., Segura-Correa, J. C., & Peralta-Torres, J. A. (2020). Factors associated with pregnancy rate in fixed-time embryo transfer in cattle under humid-tropical conditions of México. Animal Reproduction, 17(2), e20200007. https://doi.org/10.1590/1984-3143-AR2020-0007
Poock, S. E., Lamberson, W. R., & Lucy, M. C. (2015). Effect of different gonadorelin (GnRH) products used for the first or resynchronized timed artificial insemination on pregnancy rates in postpartum dairy cows. Theriogenology, 84(4), 504–508. https://doi.org/10.1016/j.theriogenology.2015.04.002
Román, S. I., Ríos, A., Montaño, M., García, A., Vega, V. E., Sifuentes, A. M., Martínez, G., Vázquez, C., & Ruíz F. de J. (2015). Mejoramiento genético de los bovinos del trópico. En: E. González, J. L. Daválos, & O. Rodríguez. (Coords.) Estado del arte sobre investigación e innovación tecnológica en ganadería bovina tropical (pp. 99–152). D.F., México: Red de Investigación e Innovación Tecnológica para la Ganadería Bovina Tropical & Consejo Nacional de Ciencia y Tecnología.
Saizi, T., Mpayipheli, M. & Idowu, P. (2019). Heat tolerance level in dairy herds: a review on coping strategies to heat stress and ways of measuring heat tolerance. Journal of Animal Behavior and Biometeorology, 7, 39–51. https://doi.org/10.31893/2318-1265jabb.v7n2p39-51
SIAP, SAGARPA. (2022). Servicio de Información Agroalimentaria y Pesquera, Secretaría de Agricultura Ganadería y Desarrollo Rural, Pesca y Alimentación. http://www.pgn.org.mx/_programs/estadistica-bis.php. Fecha de consulta 21/07/2023.
Souissi, W., & Bouraoui, R. (2020). Relationship between body condition score, milk yield, reproduction, and biochemical parameters in dairy cows. Lactation in Farm Animals - Biology, Physiological Basis, Nutritional Requirements, and Modelization. https://doi.org/10.5772/intechopen.85343
StatSoft, Inc. (2011) STATISTICA (Data Analysis Software System), Version 10. http://www.statsoft.com
Stringfellow D. A. Givens M. D. & International Embryo Transfer Society. (2010). Manual of the international embryo transfer society: a procedural guide and general information for the use of embryo transfer technology emphasizing sanitary procedures (4th ed.). International Embryo Transfer Society.
Systat Software (2008). SigmaPlot V11, San Jose, CA. www.systatsoftware.com
Uribe-Velásquez, L. F., Oba, E., Brasil, L. H. de A., Sousa, F. N. de, & Wechsler, F. S.. (2001). Efeitos do estresse térmico nas concentrações plasmáticas de progesterona (P4) e estradiol 17-b (E2) e temperatura retal em cabras da raça Pardo Alpina. Revista Brasileira De Zootecnia, 30 (2), 388–393. https://doi.org/10.1590/S1516-35982001000200014
Vásquez Borja, S.D.C. (2018) Evaluación del método de transferencia embrionaria en novillas y vacas receptoras en una hacienda de producción bovina (trabajo de titulación). UTMACH, Unidad Académica de Ciencias Agropecuarias, Machala, Ecuador.
Verdoljak, J., Pereira, M., Gándara, L., Acosta, F., Fernández-López, C., & Martínez-González, J. (2018). Reproducción y mortalidad de razas bovinas en clima subtropical de Argentina. Abanico Veterinario, 8(1), 28–35. https://doi.org/10.21929/abavet2018.81.2
Zuchelli JM., Pinto Na., De Oliveira W., Cattelam J., Garcia G.H. (2019). Pregnancy rate of recipient cows after transfer of in vitro produced Nellore embryos. Rev. Caatinga, Mossoró. 32 (4), 1087 – 1091 https://doi.org/10.1590/1983-21252019v32n425rc
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
The authors confirm contribution to the paper as follows: Study conception and design: Alondra Zavaleta-Martínez, Manuel Barrientos-Morales, Victor Abasalon Medina, Antonio Hernández Beltran, Belisario Domínguez-Mancera; Data collection: Alondra Zavaleta-Martínez, Manuel Barrientos-Morales, Patricia Cervantes-Acosta; Analysis and interpretation of results: Alondra Zavaleta-Martínez, Belisario Domínguez-Mancera, Araceli Rodríguez-Andrade, Leonel Avendaño-Reyes; Draft manuscript preparation: Leonel Avendaño-Reyes, Antonio Hernández Beltran, Belisario Domínguez-Mancera. All authors reviewed the results and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflicts of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zavaleta-Martínez, A., Barrientos-Morales, M., Medina, V.A. et al. Evaluation of intrinsic and extrinsic factors affecting pregnancy rate in dual-purpose cows under tropical conditions. Trop Anim Health Prod 56, 163 (2024). https://doi.org/10.1007/s11250-024-04016-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-024-04016-9