Strategies to increment in vivo and in vitro embryo production and transfer in cattle
Knowledge of follicular wave dynamics obtained through the use of real-time ultrasonography and the development of the means by which follicular wave dynamics can be controlled have provided practical approaches for the in vivo and in vitro production and transfer of embryos in cattle. The elective control of follicular wave emergence and ovulation has had a great impact on the application of on-farm embryo transfer, especially when large groups of donors need to be superstimulated at the same time. Although estradiol and progestins have been used for many years, practitioners in countries where estradiol cannot be used have turned to alternative treatments, such as mechanical follicle ablation or the administration of GnRH for the synchronization of follicle wave emergence. In vitro embryo production also benefits from the synchronization of follicle wave emergence prior to Cumulus Oocyte Complexes (COCs) recovery. As Bos indicus cattle have high antral follicle population, large numbers of oocytes can be obtained by ovum pick-up (OPU) without superstimulation. However, synchronization of follicular wave emergence and superstimulation is necessary to obtain high numbers of COCs by OPU and blastocysts following in vitro fertilization in Bos taurus donors. Finally, embryos can now be transferred in commercial beef or dairy herds using efficacious synchronization and resynchronization protocols that are easily implemented by farm personnel. These technologies can also be used to resolve reproductive problems such as the reduced fertility observed during summer heat stress and/or in repeat-breeder cows in commercial dairy herds.
Ambrose JD, Drost RL, Monson RL, Rutledge JJ, Leibfried-Rutledge ML, Thatcher MJ, Kassa T, Binelli M, Hansen PJ, Chenoweth PJ, Thatcher WW. 1999. Efficacy of timed embryo transfer with fresh and frozen in vitro-produced embryos to increase pregnancy rates in heat-stressed dairy cattle. J Dairy Sci, 82:2369-2376.
Barajas JL, Cedeño A, Andrada S, Ortega J., Oviedo JM., Tribulo A, Tribulo R, Tribulo H, Bó GA. 2019. Embryo production using follicle stimulating hormone (FSH) or FSH + equine chorionic gonadotropin in beef donors. Reprod Fertil Dev, 31:223. (Abstract).
Barros CM, Satrapa RA, Castilho ACS, Fontes PK, Razza EM, Ereno RL, Nogueira MFG. 2012. Effect of superstimulatory treatments on the expression of genes related to ovulatory capacity, oocyte competence and embryo development in cattle. Reprod Fertil Dev, 25:17-25.
Baruselli PS, Ferreira RM, Sales JNS, Gimenes LU, Sá Filho MF, Martins CM, Rodrigues CA, Bó GA. 2011. Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology, 76:1583-1593.
Baruselli PS, Sá Filho MF, Ferreira RM, Sales JNS, Gimenes LU, Vieira LM, Mendanha MF, Bó GA. 2012. Manipulation of follicle development to ensure optimal oocyte quality and conception rates in cattle. Reprod Dom Anim, 47(Suppl. 4):134-141.
Baruselli PS, Batista EOS, Vieira LM, Ferreira RM, Guerreiro BG, Bayeux BM, Sales JNS, Souza A, Gimenes L. 2016. Factors that interfere with oocyte quality for in vitro production of cattle embryos: effects of different developmental & reproductive stages. Anim Reprod, 13:264-272.
Baruselli PS, Ferreira RM, Colli MHA, Elliff FM, Sá Filho MF, Vieira L, Gonzales de Freitas B. 2017. Timed artificial insemination: current challenges and recent advances in reproductive efficiency in beef and dairy herds in Brazil. Anim Reprod, 14:558-571.
Batista EOS, Macedo GG, Sala RV, Ortolan MDDV, Sa Filho MF, Del Valle TA, Jesus EF, Lopes RNVR, Renno FP, Baruselli PS. 2014. Plasma antimullerian hormone as a predictor of ovarian antral follicular population in Bos indicus (Nelore) and Bos taurus (Holstein) heifers. Reprod Dom Anim, 49:448-452.
Bergfelt DR, Bó GA, Mapletoft RJ, Adams GP. 1997. Superovulatory response following ablation-induced follicular wave emergence at random stages of the estrous cycle in cattle. Anim Reprod Sci, 49:1-12.
Bernal B, Revol J, Oviedo JM, Tribulo A, Tribulo H, Moreira G, Bó GA. 2016. Influence of breed and season on in vitro embryo production. Reprod Fertil Dev 28, 255-255. (Abstract).
Block J, Bonilla L, Hansen PJ. 2010. Efficacy of in vitro embryo transfer in lactating dairy cows using fresh or vitrified embryos produced in a novel embryo culture medium. J Dairy Sci, 93:5234-5242.
Blondin P, Vigneault C, Nivet AL, Sirard MA. 2012. Improving oocyte quality in cows and heifers - What have we learned so far? Anim Reprod, 9:281-289.
Bó GA, Adams GP, Pierson RA, Mapletoft RJ. 1996. Effect of progestogen plus E-17ß treatment on superovulatory response in beef cattle. Theriogenology, 45:897-910.
Bó GA., Baruselli PS, Moreno D, Cutaia L, Caccia M, Tríbulo R, Tríbulo H, Mapletoft R.J. 2002a. The control of follicular wave development for self-pointed embryo transfer programs in cattle. Theriogenology, 57:53-72.
Bó GA, Cutaia L, Tríbulo R. 2002b. Tratamientos hormonales para inseminación artificial a tiempo fijo en bovinos para carne: algunas experiencias realizadas en Argentina. Segunda parte. Taurus, 15:17-32.
Bó GA, Carballo Guerrero D, Adams GP. 2008. Alternative approaches to setting up donor cows for superstimulation. Theriogenology, 69:81-7.
Bó GA, Baruselli PS, Mapletoft RJ. 2012a. Increasing pregnancies following synchronization of bovine recipients. Anim Reprod, 9:312-317.
Bó GA, Peres LC, Cutaia LE, Pincinato D, Baruselli PS, Mapletoft RJ. 2012b. Treatments for the synchronization of bovine recipients for fixed-time embryo transfer and improvement of pregnancy rates. Reprod Fertil Dev, 24:272-277.
Bó GA, Mapletoft RJ. 2014. Historical perspectives and recent research on superovulation in cattle. Theriogenology, 81:38-48.
Bó GA, Cedeño A. 2018. Expression of estrus as a relevant factor in fixed-time embryo transfer programs using estradiol/progesterone-based protocols in cattle. Anim Reprod, 15:224-230.
Bridges GA, Helser LA, Grum DE, Mussard ML, Gasser CL, Day ML. 2008. Decreasing the interval between GnRH and PGF2α from 7 to 5 days and lengthening proestrus increases timed-AI pregnancy rates in beef cows. Theriogenology, 69:843-851.
Caccia M, Tríbulo R, Tríbulo H, Bó GA. 2000. Effect of eCG pretreatment on superovulatory response in CIDR-B treated beef cattle. Theriogenology, 53:495. (Abstract).
Cifuentes E, Quevedo L, Hoyos A, Carballo D, Piccardi M, Bó GA. 2009. Efecto de la aplicación de eCG en vacas donantes de embriones superovuladas con Folltropin-V. VIII Simposio Internacional de Reproducción Bovina, Córdoba, Argentina, 26, 27 y 28 de Septiembre 2009, pp.7-9 (Abstract).
Cirit Ü, Özmen MF, Küçükaslan I, Köse M, Çınar EM. Kutsal HG, Çınarc EM. 2019. Effect of the interval from follicle aspiration to initiation of lengthened FSH treatment on follicular superstimulatory and superovulatory responses and embryo production in lactating Simmental cows. Theriogenology, 128:218-224.
Davis RL, Arteaga A, Hasler JF. 2012. Addition of equine chorionic gonadotropin to a traditional follicle stimulating hormone protocol for superovulation of Bos taurus beef cows. Reprod Fertil Dev, 24:224-225. (Abstract).
Dias FCF, Dadarwal D, Adams GP, Mrigank H, Mapletoft RJ, Singh J. 2013a. Length of the follicular growing phase and oocyte competence in beef heifers. Theriogenology, 79:1177-1183.
Dias FCF, Khan MIR, Sirard MA, Adams GP, Singh J. 2013b. Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reproduction, 146:181-191.
Dochi O, Takahashi K, Hirai T, Hayakawa H, Tanisawa M, Yamamoto Y, Koyama H. 2008. The use of embryo transfers to produce pregnancies in repeat-breeding dairy cattle. Theriogenology, 69:124-128.
García Guerra A, Tribulo A, Yapura J, Singh J, Mapletoft RJ. 2012. Lengthening the superstimulatory treatment protocol increases ovarian response and number of transferable embryos in beef cows. Theriogenology, 78:353-60.
Hinshaw RH. 1999. Formulating ET contracts. In “Proceedings Annual Meeting Soc. for Theriogenology”, Nashville, USA. Society for Theriogenology: USA. pp.399-404.
Ireland JJ, Ward F, Jimenez-Krassel F, Ireland JL, Smith GW, Lonergan P, Evans ACO. 2007. Follicle numbers are highly repeatable within individual animals but are inversely correlated with FSH concentrations and the proportion of good-quality embryos after ovarian stimulation in cattle. Hum Reprod, 22:1687-1695.
Lima WM, Vieira AD, Thaller Neto A, Mezzalira A, Matos RC, Gregory RM. 2007. Improved superovulatory response in beef cattle following ovarian follicular ablation using a simplified transvaginal device. Anim Reprod Sci,100:364-370.
Menchaca A, Dutra S, Carrau JM, Sapriza F, Salazar J, de la Mata JJ, Bó GA. 2015. Improvement of pregnancy rate by using the 6-day J-Synch protocol in recipient cows transferred with in vitro produced embryos. Anim Reprod, 12, 651. (Abstract).
Menchaca A, Dutra S, Carrau JM, Sapriza F, Bó GA. 2016. Improvements of the 423 new J-Synch protocol used for fixed-time embryo transfer (FTET) in recipients transferred with in vitro produced embryos. In: International Congress on Animal Reproduction (ICAR 2016), 18 th, Tours, France, pp.506. (Abstract).
Ireland JJ, Smith GW, Scheetz D, Jimenez-Krassel F, Folger JK, Ireland JLH, Mossa F, Lonergan P, Evans ACO. 2011. Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Mullerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev, 23:1-14.
Ferreira RM, Ayres H, Chiaratti MR, Rodrigues CA, Freitas BG, Meirelles F., Rodrigues CA, Baruselli PS. 2010. Heat stress and embryo production in high-producing dairy cows. Acta Scientiae Veterinariae, pp. s277-s315.
Ferreira RM, Ayres H, Chiaratti, MR, Ferraz ML, Araújo AB, Rodrigues CA, Watanabe YF, Vireque AA, Joaquim DC, Smith LC, Meirelles FV, Baruselli PS. 2011. The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. J Dairy Sci, 94:2383-2392.
Martins CM, Reis PO, Vieira JH, Soares JG, Vieira LM, Sa Filho MF, Baruselli PS. 2014. Effect of association of FTET and TAI in reproductive programs of Nelore females. Anim Reprod, 11:347. (Abstract).
Mapletoft RJ, Bó GA. 2016. Bovine embryo transfer. In: International Veterinary Information Service (Ed.). IVIS Reviews in Veterinary Medicine. Ithaca: International Veterinary Information Service. (www.ivis.org; Document No. R0104.1106S).
Mattos MC, Bastos MR, Guardieiro MM, Carvalho JO, Franco MM, Mourão GB, Barros CM, 2011. Improvement of embryo production by the replacement of the last two doses of porcine follicle-stimulating hormone with equine chorionic gonadotropin in Sindhi donors. Anim Reprod Sci, 125:119-123.
Monniaux D, Drouilhet L, Rico C, Estienne A, Jarrier P, Touzé JL, Sapa J, Phocas F, Dupont J, Dalbies-Tran R, Fabre S. 2013. Regulation of anti-Mullerian hormone production in domestic animals. Reprod Fertil Dev, 25:1-16.
Murphy BD. 2012. Equine chorionic gonadotropin: an enigmatic but essential tool. Anim Reprod, 9:223-230.
Oliveira ACS, Mattos MCC, Bastos MR, Trinca LA, Razza EM, Satrapa RA, Sartori R, Barros CM. 2014. Efficiency of superstimulatory protocol P-36 associated with the administration of eCH and LH in Nelore cows. Theriogenology, 82:715-719.
Oliveira LH, Sanches CP, Seddon AS, Veras MB, Lima FA, Monteiro PLJ Jr, Wiltbank MC, Sartori R. 2016. Short communication: Follicle superstimulation before ovum pick-up for in vitro embryo production in Holstein cows. J Dairy Sci, 99:9307-9312.
Ongaratto FL, Tribulo A, Ramos M, Rodríguez P, Bó GA. 2011. Oocyte recovery rates and in vitro blastocyst production in cattle treated with a single injection of folltropin-v diluted in a slow-release formulation. Repro Fert Dev, 23 (1): 202-203
Ongaratto FL, Rodriguez VP, Tribulo A, Bó GA. 2015. Effect of follicle wave synchronization and gonadotropin treatments on the number and quality of cumulus-oocyte complex obtained by ultrasound-guided ovum pick-up in beef cattle. Anim Reprod, 12:876-883.
Ongaratto FL, Cedeño AV, Rodriguez VP, Tribulo A, Bó GA. 2019. Effect of FSH treatment on cumulus oocyte complex recovery by ovum pick up and in vitro embryo production in beef donor cows. Anim Prod Sci, (Submitted).
Pellegrino CA, Morotti F, Untura RM, Pontes JH, Pellegrino MF, Campolina JP, Seneda MM, Barbosa FA, Henry M. 2016. Use of sexed sorted semen for fixed-time artificial insemination or fixed-time embryo transfer of in vitro-produced embryos in cattle. Theriogenology, 86:888-893.
Pontes JHF, Nonato-Junior I, Sanches BV, Ereno-Junior JC, Uvo S, Barreiros TRR, Oliveira JA, Hasler JF, Seneda MM. 2009. Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology, 71:690-697.
Pontes JH, Silva KC, Basso AC, Rigo AG, Ferreira CR, Santos GM, Sanches BV, Porcionato JP, Vieira PH, Faifer FS, Sterza FA, Schenk JL, Seneda MM. 2010. Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm. Theriogenology, 74:1349-1355.
Putney DJ, Drost M, Thatcher WW. 1989. Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology, 31:765-78.
Rasmussen S, Block J, Seidel GE Jr, Brink Z, McSweeney K, Farin PW, Bonilla L, Hansen PJ. 2013. Pregnancy rates of lactating cows after transfer of in vitro produced embryos using X-sorted sperm. Theriogenology, 79:453-461.
Reano I, Carballo D, Tribulo A, Tribulo P, Balla E, Bó GA. 2009. Efecto de la adición de eCG a los tratamientos superovulatorios con Folltropin-V en la producción de embriones de donantes de embriones. In: VIII Simposio Internacional de Reproducción Animal-IRAC, 10th to 12th July de 2009, Córdoba. Argentina, pp.54. (Abstract).
Rezende RG, Freitas BG, Mingoti RD, Colli MHA, Carvalho JBP, Sá Filho MF, Motta JCL, Macedo GG, Baruselli PS. 2016. Follicular dynamics of Nelore cows submitted to resynchronization 14 days after TAI using injectable P4 for synchronization of follicular wave. Anim Reprod, 13:375. (Abstract).
Rico C, Drouilhet L, Salvetti P, Dalbie`s-Tran R, Jarrier P, Touze´ J-L, Pillet E, Ponsart C, Fabre S, Monniaux D. 2012. Determination of anti-Mullerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reprod Fertil Dev, 24:932-944.
Rodrigues CA, Ayres H, Nichi M, Bó GA, Baruselli PS. 2004. Artificial insemination and embryo transfer pregnancy rates in high production Holstein breeding under tropical conditions. Anim Reprod, 14:396. (Abstract).
Rodrigues CA, Ayres H, Ferreira RM, Teixeira AA, Mancilha RF, Oliveira MEF, Souza AH, Baruselli PS. 2007a. Conception rate after artificial insemination and embryo transfer in high producing holstein cows. Acta Sci Vet, 33:1254. (Abstract).
Rodrigues CA, Ayres H, Ferreira RM, Teixeira AA, Mancilha RF, Oliveira MEF, Souza AH, Baruselli PS. 2007b. Comparison of pregnancy rates after artificial insemination or embryo transfer in high producing repeat breeder Holstein cows. Acta Sci Vet, 35:1255. (Abstract).
Rodrigues CA, Teixeira AA, Ferreira RM, Ayres H, Mancilha RF, Souza AH, Baruselli P.S. 2010. Effect of fixed-time embryo transfer on reproductive efficiency in high-producing repeat-breeder Holstein cows. Anim Reprod Sci, 118:110-117.
Rodrigues CA, Ferreira RM, Vieira LM, Ranieri AL, Silva PRL, Baruselli PS. 2011. How FTAI and FTET impact reproductive efficiency of Brazilian dairy herds. Acta Sci Vet, 39:3-13.
Sartori R, Guardieiro MM, Barros CM, Bastos MR, Machado GM, Leme LO, Rumpf R. 2009. Lack of improvement on embryo production by the replacement of the last two doses of pFSH by eCG in superovulated Nelore heifers. Reprod Fertil Dev, 21:245. (Abstract).
Sala RV, Carrenho-Sala LC, Fosado M, Tosta LC, Tosta RD, Stoll M, Moreno JF, Monteiro BM, Baruselli PS, Garcia-Guera A, Wiltbank M. 2016. Comparison of methods for synchronizing recipients of in vitro produced embryos. Reprod Fertil Dev, 28:185-185. (Abstract).
Son DS, Choe CY, Cho SR, Choi SH, Kim HJ, Hur TY, Jung YG, Kang HG, Kim IM. 2007. A CIDR-based timed embryo transfer protocol increases the pregnancy rate of lactating repeat breeder dairy cows. J Reprod Dev, 53:1313-18.
Souza AH, Carvalho PD, Rozner AE, Vieira LM, Hackbart KS, Bender RW, Dresch AR, Verstegen JP, Shaver RD, Wiltbank MC. 2014. Relationship between circulating anti-Müllerian hormone (AMH) and superovulatory response of high producing dairy cows. J Dairy Sci, 98:169-178.
Surjus RS, Prata AB, Borsato M, Mattos FC, Martins da Silveira MC, Mourão GB, Pires AV, Wiltbank MC, Sartori R. 2014. In vivo embryo production in cows superovulated 1 or 2 days after ovum pick-up. Reprod Fertil Dev, 26:527-532.
Viana J. 2018. 2017 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter, 36:8-25.
Vieira LM, Rodrigues CA, Castro Netto A, Guerreiro BM, Silveira CRA, Moreira RJC, Sá Filho MA, Bó GA, Mapletoft RJ, Baruselli PS. 2014. Superstimulation prior to the ovum pick-up to improve in vitro embryo production in lactating and non-lactating Holstein cows. Theriogenology, 82:318-324.
Vieira LM, Rodrigues CA, Castro Netto A, Guerreiro BM, Silveira CRA, Freitas BG, Bragança LGM, Marques KNG, Sá Filho MF, Bó GA, Mapletoft RJ, Baruselli PS. 2015. Efficacy of a single intramuscular injection of porcine FSH in hyaluronan prior to ovum pick-up in Holstein cattle. Theriogenology, 84:1-10.
Stewart BM, Block J, Morelli P, Navarette AE, Amstalden M, Bonilla L, Hansen PJ, Bilby TR. 2011. Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen. J Dairy Sci, 94:3437-3445.
Watanabe Y, Souza H, Mingoti RD, Ferreira R, Batista EOS, Dayan A, Watanabe O, Meirelles FV, Nogueira MFG, Ferraz JBS, Baruselli PS. 2017. Number of oocytes retrieved per donor during OPU and its relationship with in vitro embryo production and field fertility following embryo transfer. Anim Reprod, 14(3):635-644.
Wheeler MB, Rutledge JJ, Fischer-Brown A, VanEtten T, Malusky S, Beebe DJ. 2006. Application of sexed semen technology to in vitro embryo production in cattle. Theriogenology, 65:219-227.