Evolution of knowledge on ovarian physiology and its contribution to the widespread application of reproductive biotechnologies in South American cattle
Reuben J. Mapletoft, Gabriel A. Bó, Pietro S. Baruselli, Alejo Menchaca, Roberto Sartori
Abstract
As our understanding of ovarian function in cattle has improved, our ability to control it has also increased. Luteal function in cattle has been studied in detail, and prostaglandin F2α has been used for several years for the elective induction of luteal regression. More recently, follicle wave dynamics has been studied and protocols designed to induce follicular wave emergence and ovulation have reduced, and even eliminated, the need for estrus detection. The addition of progestin-releasing devices, estradiol, GnRH and equine chorionic gonadotropin (eCG) have provided opportunities for fixed-time AI (FTAI) and possibilities for increased pregnancy rates. In embryo transfer programs, these same treatments have eliminated the need for estrus detection, permitting fixed-time embryo transfer and the initiation of superstimulatory treatments without regard to day of the estrous cycle. Collectively, new treatment protocols have facilitated the application of assisted reproductive technologies, and this is especially true in South America. Over the last 20 years, the use of AI in South America has increased, due largely to the use of FTAI. There has been more than a 10-fold increase in the use of FTAI in Brazil with more than 11 million treatments in 2016, representing 85% of all AI. Similar trends are occurring in Argentina and Uruguay. Production of in vivo-derived (IVD) embryos has remained relatively stable over the years, but in vitro embryo production (IVP) has increased dramatically over the past 10 to 15 years, especially in Brazil where more than 300,000 IVP embryos were produced in 2010. World-wide, more than 666,000 bovine IVP embryos were produced in 2016, of which more than 57% were produced in South America. The use of assisted reproductive technologies has facilitated the dissemination of improved genetics and increased reproductive performance; other South American countries are now following suit.
Keywords
References
Adams GP. 1999. Comparative patterns of follicle development and selection in ruminants. J Reprod Fertil Suppl, 54:17-32.
Adams GP, Jaiswal R, Singh J, Malhi P. 2008. Progress in understanding ovarian follicular dynamics in cattle. Theriogenology, 69:72-80.
Bao B, Garverick HA. 1998. Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J Anim Sci, 76:1903-1921.
Baruselli PS. Reis EL, Marques MO, Nasser LF, Bó GA. 2004. The use of hormonal treatments to improve reproductive performance of anestrous beef cattle in tropical climates. Anim Reprod Sci, 82-83:479-486.
Baruselli PS, RM Ferreira, Filho MF, Nasser LFT, Rodrigues CA, Bó GA. 2010. Bovine embryo transfer recipient synchronization and management in tropical environments. Reprod Fertil Dev, 22:67-74.
Baruselli PS, Sa´ 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 Pietro Sampaio, Ferreira Roberta Machado, Colli Marcos Henrique Alcantara, Elliff Flávia Morag, Sá Filho Manoel Francisco, Vieira Lais, Gonzales de Freitas Bruno. 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.
Beal WB. 1999. Streamlining embryo transfer. In: Proceedings of the 18th Annual Convention AETA, Colorado Springs, CO, USA. Savoy, IL: AETA. pp.78-85.
Bergfelt DR, Lightfoot KC, Adams GP. 1994. Ovarian dynamics following ultrasound-guided transvaginal follicle ablation in heifers. Theriogenology. 42:895-907.
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.
Bisinotto RS, Ribeiro ES, Lima FS, Martinez N, Greco LF, Barbosa LFSP, Bueno PP, Scagion LFS, Thatcher WW, Santos JEP. 2013. Targeted progesterone supplementation improves fertility in lactating dairy cows without a corpus luteum at the initiation of the timed artificial insemination protocol. J Dairy Sci, 96:2214-2225.
Bó GA, Adams GP, Pierson RA, Mapletoft RJ. 1995. Exogenous control of follicular wave emergence in cattle. Theriogenology, 43:31-40.
Bó GA, Adams GP, Pierson RA, Mapletoft RJ. 1996. Effect of progestogen plus E-17 treatment on superovulatory response in beef cattle. Theriogenology, 45:897-910.
Bó GA, Baruselli PS, Moreno D, Cutaia L, Caccia M, Tribulo R, Tribulo H, Mapletoft RJ. 2002. The control of follicular wave development for self-appointed embryo transfer programs in cattle. Theriogenology, 57:53-72.
Bó GA, Baruselli PS, Martinez MF. 2003. Pattern and manipulation of follicular development in Bos indicus cattle. Anim Reprod Sci, 78:307-326.
Bó GA, Carballo Guerrero D, Adams GP. 2008. Alternative approaches to setting up donor cows for superstimulation. Theriogenology, 69:81-87.
Bó G A, Peres LC, Cutaia LE, Pincinato D, Baruselli PS, Mapletoft RJ. 2012. Treatments for the synchronisation of bovine recipients for fixed-time embryo transfer and improvement of pregnancy rates. Reprod Fertil Dev, 24:272-277.
Bó GA, Baruselli PS, Mapletoft RJ. 2013. Synchronization techniques to increase the utilization of artificial insemination in beef and dairy cattle. Anim Reprod, 10:137-143.
Bó Gabriel A, Mapletoft Reuben J. 2014. Historical perspectives and recent research on superovulation in cattle. Theriogenology, 81:38-48.
Bó GA, de la Mata JJ, Baruselli PS, Menchaca A. 2016 Alternative programs for synchronizing and resynchronizing ovulation in beef cattle. Theriogenology, 86:388-396.
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.
Brusveen DJ, Cunha AP, Silva CD, Cunha PM, Sterry RA, Silva EPB, Guenther JN, Wiltbank MC. 2008. Altering the time of the second gonadotropin-releasing hormone injection and artificial insemination (AI) during Ovsynch affects pregnancies per AI in lactating dairy cows. J Dairy Sci, 91:1044-1052.
Colazo MG, Martínez MF, Kastelic JP, Mapletoft RJ. 2003. Effects of estradiol cypionate (ECP) on ovarian follicular dynamics, synchrony of ovulation, and fertility in CIDR-based, fixed-time AI programs in beef heifers. Theriogenology, 60:855-865.
Colazo MG, Martínez MF, Small JA, Kastelic JP, Burnley CA, Ward D. Mapletoft RJ. 2005. Effects of estradiol valerate on ovarian follicle dynamics and superovulatory response in progestin-treated cattle. Theriogenology, 63:1454-1468.
Colazo MG, Ambrose DJ. 2011. Neither duration of progesterone insert nor initial GnRH treatment affected pregnancy per timed-insemination in dairy heifers subjected to a Co-synch protocol. Theriogenology, 76:578-588.
Day ML. 2015. State of the art of GnRH-based timed AI in beef cattle. Anim Reprod, 12:473-478.
Folman Y, Kaim M, Herz Z, Rosenberg M. 1990. Comparison of methods for the synchronization of estrous cycles in dairy cows. 2. Effects of progesterone and parity on conception. J Dairy Sci, 73:2817-2825.
García Guerra A, Tribulo A, Yapura J, Adams GP, Singh J, Mapletoft RJ. 2015. Lengthened superstimulatory treatment in cows: evidence for rescue of follicles within a wave rather than continuous recruitment of new follicles. Theriogenology, 84:467-476.
Gimenes LU, Sá Filho MF, Carvalho NAT, Torres-Junor JRS, Souza AH, Madureira EH, Tricia LA, Sartorelli ES, Barros CM, Carvalho JBP, Mapletoft RJ, Baruselli PS. 2008. Follicle deviation and ovulatory capacity in Bos indicus heifers. Theriogenology, 69:852-858.
Ginther OJ, Kastelic JP, Knopf L. 1989a. Composition and characteristics of follicular waves during the bovine estrous cycle. Anim Reprod Sci, 20:187-200.
Ginther OJ, Knopf L, Kastelic JP. 1989b. Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J Reprod Fert, 87:223-230
Ginther OJ, Bergfelt DR, Beg MA, Kot K. 2001. Follicle selection in cattle: relationships among growth rate, diameter ranking, and capacity for dominance. Biol Reprod, 65:345-350.
Hinshaw RH, Switzer ML, Mapletoft RJ, Bó GA. 2015. A comparison of 2 approaches for the use of GnRH to synchronize follicle wave emergence for superovulation. Reprod Fertil Dev, 27:263. (Abstract).
Ireland JJ, Ward F, Jimenez-Krassel F, Ireland JLH, 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.
Ireland JLH, Scheetz D, Jimenez-Krassel F, Themmen APN, Ward F, Lonergan P, Smith GW, Perez GI, Evans ACO, Ireland JJ. 2008. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod, 79:1219-1225.
Ireland JJ, Smith GW, Scheetz D, Jimenez-Krassel F, Folger JK, Ireland JL, Mossa F, Lonergan P, Evans AC. 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-Müllerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev, 23:1-14.
Kasimanickam RK, Firth P, Schuenemann GM, Whitlock BK, Gay JM, Moore DA, Hall JB, Whittier WD. 2014. Effect of the first GnRH and two doses of PGF2α in a 5-day progesterone-based CO-Synch protocol on heifer pregnancy. Theriogenology, 81:797-804.
Kastelic JP, Knopf L, Ginther OJ. 1990. Effect of day of prostaglandin F2 treatment on selection and development of the ovulatory follicle in heifers. Anim Reprod Sci, 23:169-180.
Kastelic JP, Ginther OJ. 1991. Factors affecting the origin of the ovulatory follicle in heifers with induced luteolysis. Anim Reprod Sci, 26:13-24.
Lamb GC, Stevenson JS, Kesler DJ, Garverick HA, Brown DR, Salfen BE. 2001. Inclusion of an intravaginal progesterone insert plus GnRH and prostaglandin F2α for ovulation control in postpartum suckled beef cows. J Anim Sci, 79:2253-2259.
Lima F, Ribeiro ES, Bisinotto RS, Greco RF, Martinez N, Amstalden M, Thatcher WW, Santos JEP. 2013. Hormonal manipulations in the 5-day timed artificial insemination protocol to optimize estrous cycle synchrony and fertility in dairy heifers. J Dairy Sci, 96:7054-7065.
Macmillan KL, Thatcher WW. 1991. Effects of an agonist of gonadotropin-releasing hormone on ovarian follicles in cattle. Biol Reprod, 45:883-889.
Mapletoft RJ, Martinez MF, Colazo MG, Kastelic JP. 2003. The use of controlled internal drug release devices for the regulation of bovine reproduction. J Anim Sci, 81(E Suppl 2):E28-E36.
Mapletoft RJ. 2013. History and perspectives on bovine embryo transfer. Anim Reprod, 10:168-173.
Martinez MF, Adams GP, Bergfelt D, Kastelic JP, Mapletoft RJ. 1999. Effect of LH or GnRH on the dominant follicle of the first follicular wave in heifers. Anim Reprod Sci, 57:23-33.
Martinez MF, Kastelic JP, Adams GP, Cook RB, Olson WO, Mapletoft RJ. 2002. The use of progestins in regimens for fixed-time artificial insemination in beef cattle. Theriogenology, 57:1049-59.
Martínez MF, Kastelic JP, Bó GA, Caccia M, Mapletoft RJ. 2005. Effects of oestradiol and some of its esters on gonadotrophin release and ovarian follicular dynamics in CIDR-treated beef cattle. Anim Reprod Sci, 86:37-52.
Martínez MF, Kastelic JP, Mapletoft RJ. 2007. Effects of estradiol on gonadotrophin release, estrus and ovulation in CIDR-treated beef cattle. Domest Anim Endo, 33:77-90.
Martins T, Talamoni JP, Sponchiado M, Maio JRG, Nogueira GP, Pugliesi G, Binelli M. 2017. Impact of estradiol cypionate prior to TAI and progesterone supplementation at initial diestrus on ovarian and fertility responses in beef cows. Theriogenology, 104:156-163.
Moreira F, de la Sota RL, Diaz T, Thatcher WW. 2000. Effect of day of the estrous cycle at the initiation of a timed artificial insemination protocol on reproductive responses in dairy heifers. J Anim Sci, 78:1568-1576.
Moreira F, Orlandi C, Risco CA, Schouten MJ, Lopes F, Thatcher WW. 2001. Effects of presynchronization and bovine somatotropin on pregnancy rates to a timed artificial insemination protocol in lactating dairy cows. J Dairy Sci, 84:1646-1659.
Nasser L, Adams GP, Bó GA, Mapletoft RJ. 1993. Ovarian superstimulatory response relative to follicular wave emergence in heifers. Theriogenology, 40:713-724.
Núñez-Olivera R, de Castro T, García-Pintos C, Bó GA, Piaggio J, Menchaca A. 2014. Ovulatory response and luteal function after eCG administration at the end of a progesterone and estradiol-based treatment in postpartum anestrous beef cattle. Anim Reprod Sci, 146:111-116.
Odde KG. 1990. A review of synchronization of estrus in postpartum cattle. J Anim Sci, 68:817-830.
Pereira MHC, Sanches CP, Guida TG, Rodrigues ADP, Aragon FL, Veras MB, Borges PT, Wiltbank MC, Vasconcelos JLM. 2013. Timing of prostaglandin F2α treatment in an estrogen-based protocol for timed artificial insemination or timed embryo transfer in lactating dairy cows. J Dairy Sci, 96:2837-2846.
Perry George. 2017. 2016 statistics of embryo collection and transfer in domestic animals. Embryo Technology Newsletter, 35(4):8-23.
Peterson C, Alkar A, Smith S, Kerr S, Hall JB, Moore D, Kasimanickam, R. 2011. Effects of one versus two doses of prostaglandin F2alpha on AI pregnancy rates in a 5-day progesterone-based, CO-Synch protocol in crossbred beef heifers. Theriogenology, 75:1536-1542.
Ponsart C, Le Bourhis D, Knijn H, Fritz S, Guyader-Joly C, Otter T, Lacaze S, Charreaux F, Schibler L, Dupassieux D, Mullaart E. 2014. Reproductive technologies and genomic selection in dairy cattle. Reprod Fert Dev, 26:12-21.
Pursley JR, Mee MO, Wiltbank MC. 1995. Synchronization of ovulation in dairy cows using PGF2 and GnRH. Theriogenology, 44:915-923.
Rabaglino MB, Risco C, Thatcher MJ, Kim IH, Santos JE, Thatcher WW. 2010. Application of one injection of prostaglandin F2α in the five-day Co-Synch + CIDR protocol for estrous synchronization and resynchronization of dairy heifers. J Dairy Sci, 93:1050-1058.
Revah I, Butler WR. 1996. Prolonged dominance of follicles and reduced viability of bovine oocytes. J Reprod Fertil, 106:39-47.
Rico C, Fabre S, Medigue C, Clemente ND, Clement F, Bontoux M, Touze J-L, Dupont M, Briant E, Remy B, Beckers J-F, Monniaux D. 2009. Anti-Mullerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod, 80:50-59.
Rodrigues CA, Teixeira AA, Ferreira RM, Ayres H, Mancilha RF, Souza AH, Baruselli PS. 2010. Effect of fixed-time embryo transfer on reproductive efficiency in high-producing repeat-breeder Holstein cows. Anim Reprod Sci, 118:110-117.
Sales JNS, Carvalho JBP, Crepaldi GA, Cipriano RS, Jacomini JO, Maio JRG, Souza JC, Nogueira GP, Baruselli PS. 2012. Effects of two estradiol esters (benzoate and cypionate) on the induction of synchronized ovulations in Bos indicus cows submitted to a timed artificial insemination protocol. Theriogenology, 78:510-516.
Sanches B V, Lunardelli PA, Tannura JH, Cardoso BL, Colombo Pereira MH, Gaitkoski D, Basso AC, Arnold DR, Seneda MM. 2016. A new direct transfer protocol for cryopreserved IVF embryos. Theriogenology, 85:1147-1151.
Sartorelli ES, Carvalho LM, Bergfelt DR, Ginther OJ, Barros CM. 2005. Morphological characterization of follicle deviation in Nelore (Bos indicus) heifers and cows. Theriogenology, 63:2382-2394.
Sartori R, Fricke PM, Ferreira JCP, Ginther OJ, Wiltbank MC. 2001. Follicular deviation and acquisition of ovulatory capacity in bovine follicles. Biol Reprod, 65:1403-1409.
Sartori R, Haughian JM, Shaver RD, Rosa GJM, Wiltbank MC. 2004. Comparison of ovarian function and circulating steroids in estrous cycles of Holstein heifers and lactating cows. J Dairy Sci, 87:905-920.
Sartori R, Barros CM. 2011. Reproductive cycles in Bos indicus cattle. Anim Reprod Sci, 124:244-250.
Sartori R, Gimenes LU, Monteiro Jr PLJ, Melo LF, Baruselli PS, Bastos MR. 2016a. Metabolic and endocrine differences between Bos taurus and Bos indicus females that impact the interaction of nutrition with reproduction. Theriogenology, 86:32-40.
Sartori R, Prata1 AB, Figueiredo ACS, Sanches BV, Pontes GCS, Viana JHM, Pontes JH, Vasconcelos JLM, Pereira MHC, Dode MAN, Monteiro Jr PLJ, Baruselli PS. 2016b. Update and overview on assisted reproductive technologies (ARTs) in Brazil. Anim Reprod, 13:300-312.
Savio JD, Thatcher WW, Morris GR, Entwistle K, Drost M, Mattiacci MR. 1993. Effects of induction of low plasma progesterone concentrations with a progesterone-releasing intravaginal device on follicular turnover and fertility in cattle. J Reprod Fertil, 98:77-84.
Seguin B. 1987. Control of the reproductive cycle in dairy cattle. Proc Ann Mtg Soc Therio, pp. 300-308.
Seguin B. 1997. Strategies for estrus control to improve dairy reproductive performance. Proc Ann Mtg Soc Therio, pp.320-331.
Selk GE, Fink MS, Peake CA. 1988. Estrus synchronization of cattle using eleven day or fourteen day prostaglandin protocols. Anim Sci Res Ag Expt Station, Oklahoma State Univ. MP, USA, 125:34-37.
Singh J, Dominguez M, Jaiswal R, Adams GP. 2004. A simple ultrasound test to predict superovulatory response in cattle. Theriogenology, 62:227-243.
Siqueira LGB, Dikmen S, Ortega MS, Hansen PJ. 2017. Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen. J Dairy Sci, 100:5899-5908.
Smith C. 1988. Applications of embryo transfer in animal breeding. Theriogenology, 29:203-212.
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.
Stevenson JS, Pursley JR, Garverick HA, Fricke PM, Kesler DJ, Ottobre JS, Wiltbank MC. 2006.Treatment of cycling and noncycling lactating dairy cows with progesterone during Ovsynch. J Dairy Sci, 89:2567-2578.
Stevenson JS. 2011. Alternative programs to presynchronize estrous cycles in dairy cattle before timed artificial insemination program. J Dairy Sci, 94:205-217.
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.
Vasconcelos JLM, Silcox RW, Pursley JR, Wiltbank MC. 1999. Synchronization rate, size of the ovulatory follicle, and pregnancy rate after synchronization of ovulation beginning on different days of the estrous cycle in lactating dairy cows. Theriogenology, 52:1067-1078.
Viana João Henrique Moreira, Cristina Silva Figueiredo Ana, Siqueira Luiz Gustavo Bruno. 2017. Brazilian embryo industry in context: pitfalls, lessons, and expectations for the future. Anim Reprod, 14:476-481.
Washburn SP, Silvia WJ, Brown CH, McDaniel BT, McAllister AJ. 2002. Trends in reproductive performance in Southeastern Holstein and Jersey DHI herds. J Dairy Sci, 85:244-251.
Wiltbank JN, Zimmerman DR, Ingalls JE, Rowden WW. 1965. Use of progestational compounds alone or in combination with estrogen for synchronization of estrus. J Anim Sci, 24:990-994.
Wiltbank MC. 1997. How information of hormonal regulation of the ovary has improved understanding of timed breeding programs. In: Proc Ann Mtg Soc Therio, Montreal, QC, Canada. Montgomery, AL: Society for Theriogenology, pp. 83-97.