Effect of the Estrus Expression on Follicular and Luteal Morphofunctional Characteristics and Fertility in Bos indicus females Synchronized for FTAI
DOI:
https://doi.org/10.22456/1679-9216.107435Abstract
Background: Recent studies have been conducted with the aim of improving the fertility rates in the FTAI programs in beef females. The observation of the estrus expression constitutes an important indicator of fertility in zebu females. Therefore, this work has as an objective to evaluate the impact of the estrus expression on the follicular, luteal and fertility morphofunctional characteristics of Nelore females synchronized for FTAI.
Materials, Methods & Results: Sixty five lactating female Nelore (Bos taurus indicus) were used. On a random day, denominated day 0 (D0), the 65 Nelore females received a progesterone-releasing device associated to the application of 2.0 mg of estradiol benzoate intramuscularly (IM). On D9, the progesterone-releasing intravaginal devices were removed and was administered 500 μg of cloprostenol sodium IM; 0.6 mg of estradiol cypionate IM and 300 UI of Equine Chorionic Gonadotropin IM. At this point, the animals were marked with a marking stick for the determination of the estrus expression. On D11 of the synchronization protocol, the animals were characterized in two groups: without estrus expression (WO/ ESTRUS) and with estrus expression (W/ ESTRUS). The evaluation of the follicle diameter (FOLD), of the follicle wall area (FOLA), of the follicle wall vascularization (FOLV) and the percentage of vascularization in the area of the preovulatory follicle wall (%FOLV) were conducted on D11 using B-mode ultrasonography and color Doppler and then the artificial inseminations were performed. The evaluation of the corpus luteum diameter (CLD), the total area of the corpus luteum (CLA), of the area of vascularization of the corpus luteum (CLV), of the percentage of vascularization of the in the area of the corpus luteum (% CLV) and the collection of blood for the evaluation of the serum levels of progesterone were carried out on D24. The analysis of the serum progesterone concentration were performed by the chemiluminescence method using the Access immunoassay systems Progesterone, with a sensitivity of 0.1 ng/mL. The diagnosis of gestation was carried out by transrectal ultrasonography on D45. The animals of the WITH ESTRUS group presented superior FOLD, FOLA, FOV (P < 0.05) averages to those presented by the cows of the WITHOUT ESTRUS group. In relation to the luteal characteristics, in the WITH ESTRUS group the cows exhibited averages for CLD, CLA, CLV and P4 significantly higher than those of the WITHOUT ESTRUS group. However, the bovines of the WITH ESTRUS group presented a % CLV similar to the presented by the females of the WITHOUT ESTRUS group. As for the fertility rates, there was difference between the experimental groups WITH ESTRUS and WITHOUT ESTRUS.
Discussion: The present work demonstrated the impact of the estrus expression on the follicular morphological parameters, therefore in accordance with other studies. These authors show a relation between the estrus expression and levels of estradiol, which is directly related to the sperm transport in the female reproductive tract, oocyte maturation and fertilization directly affecting the fertility of females submitted to the FTAI program. Similarly, there was an interrelation between the estrus expression and the luteal morphological parameters, corroborating with the findings of some researches, where were verified higher luteal morphological parameters associated to higher conception rates in cows that demonstrated estrus behavior in the FTAI. Therefore, the estrus detection can be used as a tool to direct matings in synchronization protocols, promoting the identification of the animals with a higher probability of conception, owing to better follicular and luteal hemodynamic conditions.
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Acosta T.J., Ozawa T., Kobayashi S., Hayashi K., Ohtani M., Kraetzl W.D. & Miyamoto A. 2002. Periovulatory changes in the local release of vasoactive peptides, prostaglandin F2α, and steroid hormones from bovine mature follicles in vivo. Biology of Reproduction. 63(5): 1253-1261.
Acosta T.J., Hayashi K.G., Ohtani M. & Miyamoto A. 2003. Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows. Reproduction. 125 (5): 759-767.
Acosta T.J. & Miyamoto A. 2004. Vascular control of ovarian function: ovulation, corpus luteum formation and regression. Animal Reproduction Science. 82-83: 127-140.
Aslan S., Arslanbas D., Beindorff N. & Bollwein H. 2011. Effects of induction of ovulation with GnRH or hCG on follicular and luteal blood flow in Holstein–Friesian heifers. Reproduction in Domestic Animals. 46(5): 781-786.
Atkins J.A., Smith M.F., Wells K.J. & Geary T.W. 2010. Factors affecting preovulatory follicle diameter and ovulation rate after gonadotropin-releasing hormone in postpartum beef cows. Part I: Cycling cows. Journal of Animal Science. 88(7): 2300-2310.
Baruselli P.S., Catussi B.L.C., Abreu L.A., Elliff F.M., Silva L.G., Batista E.S. & Crepaldi G.A. 2019. Evolução e perspectivas da inseminação artificial em bovinos. Revista Brasileira de Reprodução Animal. 43(2): 308-314.
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Colazo M.G., Behrouzi A., Ambrose D.J. & Mapletoft R.J. 2015. Diameter of the ovulatory follicle at timed artificial insemination as a predictor of pregnancy status in lactating dairy cows subjected to GnRH-based protocols. Theriogenology. 84(3): 377-383.
Colazo M.G., Whittaker P., Macmillan K., Bignell D., Boender G., De Carvalho Guimaraes R. & Mapletoft R.J. 2018. Evaluation of a modified GnRH-based timed-AI protocol associated with estrus detection in beef heifers inseminated with sex-selected or conventional semen. Theriogenology. 118: 90-95.
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Cooke R.F., Pohler K.G., Vasconcelos J.L.M. & Cerri R.L.A. 2019. Estrous expression during a fixed-time artificial insemination protocol enhances development and interferon-tau messenger RNA expression in conceptuses from Bos indicus beef cows. Animal. 13(11): 2569-2575.
Dantas F.G., Zechiel K.E., Reese S.T., Araújo G., Rhinehart J.D. & Pohler K.G. 2016. Keys to maximizing reproductive efficiency in a beef herd. Disponível em: .
De Tarso S.G.S., Gastal G.D.A., Bashir S.T., Gastal M.O., Apgar G.A. & Gastal E.L. 2017. Follicle vascularity coordinates corpus luteum blood flow and progesterone production. Reproduction, Fertility and Development. 29(3): 448-457.
Edwards S.A.A., Bo G.A., Chandra K.A., Atkinson P.C. & Mcgowan M.R. 2015. Comparison of the pregnancy rates and costs per calf born after fixed-time artificial insemination or artificial insemination after estrus detection in Bos indicus heifers. Theriogenology. 83(1): 114-120.
Ferraz P.A., Loiola M.V.G., Rodrigues A.S., Lima M.C.C., Bittencourt T.C.B.S.C. & Ribeiro Filho A.L. 2017. The effect of the intensity of estrus expression on the follicular diameter and fertility of nellore cows managed under a FTAI program. Ciência Animal Brasileira. 18: 1-9.
Forde N., Mcgettigan P.A., Mehta J.P., O'hara L., Mamo S., Bazer F.W. & Lonergan P. 2014. Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle. Reproduction. 147(5): 575-587.
Gentry Jr G.T., Walker R.S. & Gentry L.R. 2016. Impacts of incorporation of follicle stimulating hormone into an estrous synchronization protocol for timed artificial insemination of crossbred beef cattle. Animal Reproduction Science. 168: 19-25.
Hassan M., Arshad U., Bilal M., Sattar A., Avais M., Bollwein H. & Ahmad N. 2018. Luteal blood flew measured by Doppler ultrasonography during the first three weeks after artificial insemination in pregnant and non-pregnant Bos indicus dairy cows. Journal of Reproduction and Development. 65(1): 29-36.
Herzog K., Brockhan-Lüdemann M., Kaske M., Beindorff N., Paul V., Niemann H. & Bollwein H. 2010. Luteal blood flow is a more appropriate indicator for luteal function during the bovine estrous cycle than luteal size. Theriogenology. 73(5): 691-697.
Kasimanickam R.K., Kasimanickam V.R., Oldham J. & Whitmore M. 2020. Cyclicity, estrus expression and pregnancy rates in beef heifers with different reproductive tract scores following progesterone supplementation. Theriogenology. 145: 39-47.
Larimore E.L., Amundson O.L., Bridges G.A., Mcneel A.K., Cushman R.A. & Perry G.A. 2016. Changes in ovarian function associated with circulating concentrations of estradiol before a GnRH-induced ovulation in beef cows. Domestic Animal Endocrinology. 57: 71-79.
Lüttgenau J., Beindorff N., Ulbrich S.E., Kastelic J.P. & Bollwein H. 2011. Low plasma progesterone concentrations are accompanied by reduced luteal blood flow and increased size of the dominant follicle in dairy cows. Theriogenology. 76(1): 12-22.
Madsen C.A., Perry G.A., Mogck C.L., Daly R.F., Macneil M.D. & Geary T.W. 2015. Effects of preovulatory estradiol on embryo survival and pregnancy establishment in beef cows. Animal Reproduction Science. 158: 96-103.
Madureira A.M.L., Silper B.F., Burnett T.A., Polsky L., Cruppe L.H., Veira D.M. & Cerri R.L.A. 2015. Factors affecting expression of estrus measured by activity monitors and conception risk of lactating dairy cows. Journal of Dairy Science. 98(10): 7003-7014.
Madureira A.M.L., Polsky L.B., Burnett T.A., Silper B.F., Soriano S., Sica A.F. & Cerri R.L.A. 2019. Intensity of estrus following an estradiol-progesterone-based ovulation synchronization protocol influences fertility outcomes. Journal of Dairy Science. 102(4): 3598-3608.
Miyamoto A., Shirasuna K., Hayashi K.G., Kamada D., Awashima C., Kaneko E., Acosta T.J. & Matsui M.A. 2006. Potential use of color ultrasound as a tool for reproductive management: New observations using color ultrasound scanning that were not possible with imaging only in black and white. Journal of Reproduction and Development. 52(1): 153-160.
Murdoch W.J. & Van Kirk E.A. 1998. Luteal dysfunction in ewes induced to ovulate early in the follicular phase. Endocrinology. 139: 3480-3484.
Nogueira E., Silva M.R., Silva J.C.B., Abreu U.P.G., Anache N.A., Silva K.C., Cardoso C.J.T., Sutovsky P. & Rodrigues W.B. 2019. Timed artificial insemination plus heat I: effect of estrus expression scores on pregnancy of cows subjected to progesterone-estradiol-based protocols. Animal. 13(10): 2305-2312.
Pereira M.H.C., Wiltbank M.C. & Vasconcelos J.L.M. 2016. Expression of estrus improves fertility and decreases pregnancy losses in lactating dairy cows that receive artificial insemination or embryo transfer. Journal Dairy Science. 99(3): 2237-2247.
Perry G.A., Smith M.F., Roberts A.J., Macneil M.D. & Greary T.W. 2007. Relationship between size of the ovulatory follicle and pregnancy success in beef heifeirs. Journal Animal Science. 85: 684-689.
Perry G.A., Swanson O.L., Larimore E.L., Perry B.L., Djira G.D. & Cushman R.A. 2014. Relationship of follicle size and concentrations of estradiol among cows exhibiting or not exhibiting estrus during a fixed-time AI protocol. Domestic Animal Endocrinology. 48: 15-20.
Pfeifer L.F.M., Moreira E.M., Silva G.M., Souza V.L., Nunes V.R.R., Andrade J.S., Neves P.M.A. & Ferreira R. 2020. Effect of estradiol cypionate on estrus expression and pregnancy in timed artificially inseminated beef cows. Livestock Science. 231: 1-5.
Pinaffi F.L., Santos É.S., Silva M.G.D., Maturana Filho M., Madureira E.H. & Silva L.A. 2015. Follicle and corpus luteum size and vascularity as predictors of fertility at the time of artificial insemination and embryo transfer in beef cattle. Pesquisa Veterinária Brasileira. 35(5): 470-476.
Pohler K.G., Geary T.W., Atkins J.A., Perry G.A., Jinks E.M. & Smith M. F. 2012. Follicular determinants of pregnancy establishment and maintenance. Cell and Tissue Research. 349(3): 649-664.
Ribeiro Filho A.D.L., Ferraz P.A., Rodrigues A.S., Bittencourt T.C.B.D.S.C., Loiola M.V.G. & Chalhoub M. 2013. Diâmetro do folículo no momento da inseminação artificial em tempo fixo e taxa de concepção em vacas Nelore. Ciência Animal Brasileira. 14(4): 501-507.
Richardson B.N., Hill S.L., Stevenson J.S., Djira G.D. & Perry G.A. 2016. Expression of estrus before fixed-time AI affects conception rates and factors that impact expression of estrus and the repeatability of expression of estrus in sequential breeding seasons. Animal Reproduction Science. 166: 133-140.
Rodrigues A.D., Cooke R.F., Cipriano R.S., Silva L.G.T., Cerri R.L.A., Cruppe L.H., Meneghetti M., Pohler K.G. & Vasconcelos J.L.M. 2018. Impacts of estrus expression and intensity during a timed-AI protocol on variables associated with fertility and pregnancy success in Bos indicus-influenced beef cows. Journal Animal Science. 96(1): 236-249.
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Thomas J.M., Poock S.E., Ellersieck M.R., Smith M.F. & Patterson D.J. 2014. Delayed insemination of non-estrous heifers and cows when using conventional semen in timed artificial 1 Abdelnaby E.A., El-Maaty A.M.A., Ragab R.S. & Seida A.A. 2018. Dynamics of uterine and ovarian arteries flow velocity waveforms and their relation to follicular and luteal growth and blood flow vascularization during the estrous cycle in Friesian cows. Theriogenology. 121: 112-121.
Acosta T.J., Ozawa T., Kobayashi S., Hayashi K., Ohtani M., Kraetzl W.D. & Miyamoto A. 2002. Periovulatory changes in the local release of vasoactive peptides, prostaglandin F2α, and steroid hormones from bovine mature follicles in vivo. Biology of Reproduction. 63(5): 1253-1261.
Acosta T.J., Hayashi K.G., Ohtani M. & Miyamoto A. 2003. Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows. Reproduction. 125 (5): 759-767.
Acosta T.J. & Miyamoto A. 2004. Vascular control of ovarian function: ovulation, corpus luteum formation and regression. Animal Reproduction Science. 82-83: 127-140.
Aslan S., Arslanbas D., Beindorff N. & Bollwein H. 2011. Effects of induction of ovulation with GnRH or hCG on follicular and luteal blood flow in Holstein–Friesian heifers. Reproduction in Domestic Animals. 46(5): 781-786.
Atkins J.A., Smith M.F., Wells K.J. & Geary T.W. 2010. Factors affecting preovulatory follicle diameter and ovulation rate after gonadotropin-releasing hormone in postpartum beef cows. Part I: Cycling cows. Journal of Animal Science. 88(7): 2300-2310.
Baruselli P.S., Catussi B.L.C., Abreu L.A., Elliff F.M., Silva L.G., Batista E.S. & Crepaldi G.A. 2019. Evolução e perspectivas da inseminação artificial em bovinos. Revista Brasileira de Reprodução Animal. 43(2): 308-314.
Beindorff N., Nagai K., Shirasuna K., Herzog K., Hoeffmann K., Sasak M., Bollwein H. & Miyamoto A. 2010. Vascular Changes in the Corpus Luteum During Early Pregnancy in the Cow. Journal of Reproduction and Development. 56(2): 263-270.
Bó G.A., Huguenine E., Mata J.J.L., Núñez-Olivera R., Baruselli P.S. & Menchaca A. 2018. Programs for fixed-time artificial insemination in South American beef cattle. Animal Reproduction. 15(Suppl 1): 952-962.
Bollwein H., Heppelmann M. & Lüttgenau J. 2016. Ultrasonographic Doppler use for female reproduction management. Veterinary Clinics: Food Animal Practice. 32(1): 149-164.
Bridges G.A., Mussard M.L., Pate J.L., Ott T.L., Hansen T.R. & Day M.L. 2012. Impact of preovulatory estradiol concentrations on conceptus development and uterine gene expression. Animal Reproduction Science. 133(1-2): 16-26.
Caunce S.L., Dadarwal D., Adams G.P., Brar P. & Singh J. 2019. An objective volumetric method for assessment of ovarian follicular and luteal vascular flow using colour Doppler ultrasonography. Theriogenology. 138: 66-76.
Cavalieri J., Gaina C. & Hepworth G. 2018. Randomised controlled trial of the effect of concentration of progesterone before artificial insemination on fertility inovulatory and anovulatory Bos indicus cattle. Australian Veterinary Journal. 96(9): 346-355.
Colazo M.G., Behrouzi A., Ambrose D.J. & Mapletoft R.J. 2015. Diameter of the ovulatory follicle at timed artificial insemination as a predictor of pregnancy status in lactating dairy cows subjected to GnRH-based protocols. Theriogenology. 84(3): 377-383.
Colazo M.G., Whittaker P., Macmillan K., Bignell D., Boender G., De Carvalho Guimaraes R. & Mapletoft R.J. 2018. Evaluation of a modified GnRH-based timed-AI protocol associated with estrus detection in beef heifers inseminated with sex-selected or conventional semen. Theriogenology. 118: 90-95.
Colégio Brasileiro de Reprodução Animal. 2013. Manual para exame andrológico e avaliação de sêmen animal. 3.ed. Belo Horizonte: CBRA, 104p.
Cooke R.F., Pohler K.G., Vasconcelos J.L.M. & Cerri R.L.A. 2019. Estrous expression during a fixed-time artificial insemination protocol enhances development and interferon-tau messenger RNA expression in conceptuses from Bos indicus beef cows. Animal. 13(11): 2569-2575.
Dantas F.G., Zechiel K.E., Reese S.T., Araújo G., Rhinehart J.D. & Pohler K.G. 2016. Keys to maximizing reproductive efficiency in a beef herd. Disponível em: .
De Tarso S.G.S., Gastal G.D.A., Bashir S.T., Gastal M.O., Apgar G.A. & Gastal E.L. 2017. Follicle vascularity coordinates corpus luteum blood flow and progesterone production. Reproduction, Fertility and Development. 29(3): 448-457.
Edwards S.A.A., Bo G.A., Chandra K.A., Atkinson P.C. & Mcgowan M.R. 2015. Comparison of the pregnancy rates and costs per calf born after fixed-time artificial insemination or artificial insemination after estrus detection in Bos indicus heifers. Theriogenology. 83(1): 114-120.
Ferraz P.A., Loiola M.V.G., Rodrigues A.S., Lima M.C.C., Bittencourt T.C.B.S.C. & Ribeiro Filho A.L. 2017. The effect of the intensity of estrus expression on the follicular diameter and fertility of nellore cows managed under a FTAI program. Ciência Animal Brasileira. 18: 1-9.
Forde N., Mcgettigan P.A., Mehta J.P., O'hara L., Mamo S., Bazer F.W. & Lonergan P. 2014. Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle. Reproduction. 147(5): 575-587.
Gentry Jr G.T., Walker R.S. & Gentry L.R. 2016. Impacts of incorporation of follicle stimulating hormone into an estrous synchronization protocol for timed artificial insemination of crossbred beef cattle. Animal Reproduction Science. 168: 19-25.
Hassan M., Arshad U., Bilal M., Sattar A., Avais M., Bollwein H. & Ahmad N. 2018. Luteal blood flew measured by Doppler ultrasonography during the first three weeks after artificial insemination in pregnant and non-pregnant Bos indicus dairy cows. Journal of Reproduction and Development. 65(1): 29-36.
Herzog K., Brockhan-Lüdemann M., Kaske M., Beindorff N., Paul V., Niemann H. & Bollwein H. 2010. Luteal blood flow is a more appropriate indicator for luteal function during the bovine estrous cycle than luteal size. Theriogenology. 73(5): 691-697.
Kasimanickam R.K., Kasimanickam V.R., Oldham J. & Whitmore M. 2020. Cyclicity, estrus expression and pregnancy rates in beef heifers with different reproductive tract scores following progesterone supplementation. Theriogenology. 145: 39-47.
Larimore E.L., Amundson O.L., Bridges G.A., Mcneel A.K., Cushman R.A. & Perry G.A. 2016. Changes in ovarian function associated with circulating concentrations of estradiol before a GnRH-induced ovulation in beef cows. Domestic Animal Endocrinology. 57: 71-79.
Lüttgenau J., Beindorff N., Ulbrich S.E., Kastelic J.P. & Bollwein H. 2011. Low plasma progesterone concentrations are accompanied by reduced luteal blood flow and increased size of the dominant follicle in dairy cows. Theriogenology. 76(1): 12-22.
Madsen C.A., Perry G.A., Mogck C.L., Daly R.F., Macneil M.D. & Geary T.W. 2015. Effects of preovulatory estradiol on embryo survival and pregnancy establishment in beef cows. Animal Reproduction Science. 158: 96-103.
Madureira A.M.L., Silper B.F., Burnett T.A., Polsky L., Cruppe L.H., Veira D.M. & Cerri R.L.A. 2015. Factors affecting expression of estrus measured by activity monitors and conception risk of lactating dairy cows. Journal of Dairy Science. 98(10): 7003-7014.
Madureira A.M.L., Polsky L.B., Burnett T.A., Silper B.F., Soriano S., Sica A.F. & Cerri R.L.A. 2019. Intensity of estrus following an estradiol-progesterone-based ovulation synchronization protocol influences fertility outcomes. Journal of Dairy Science. 102(4): 3598-3608.
Miyamoto A., Shirasuna K., Hayashi K.G., Kamada D., Awashima C., Kaneko E., Acosta T.J. & Matsui M.A. 2006. Potential use of color ultrasound as a tool for reproductive management: New observations using color ultrasound scanning that were not possible with imaging only in black and white. Journal of Reproduction and Development. 52(1): 153-160.
Murdoch W.J. & Van Kirk E.A. 1998. Luteal dysfunction in ewes induced to ovulate early in the follicular phase. Endocrinology. 139: 3480-3484.
Nogueira E., Silva M.R., Silva J.C.B., Abreu U.P.G., Anache N.A., Silva K.C., Cardoso C.J.T., Sutovsky P. & Rodrigues W.B. 2019. Timed artificial insemination plus heat I: effect of estrus expression scores on pregnancy of cows subjected to progesterone-estradiol-based protocols. Animal. 13(10): 2305-2312.
Pereira M.H.C., Wiltbank M.C. & Vasconcelos J.L.M. 2016. Expression of estrus improves fertility and decreases pregnancy losses in lactating dairy cows that receive artificial insemination or embryo transfer. Journal Dairy Science. 99(3): 2237-2247.
Perry G.A., Smith M.F., Roberts A.J., Macneil M.D. & Greary T.W. 2007. Relationship between size of the ovulatory follicle and pregnancy success in beef heifeirs. Journal Animal Science. 85: 684-689.
Perry G.A., Swanson O.L., Larimore E.L., Perry B.L., Djira G.D. & Cushman R.A. 2014. Relationship of follicle size and concentrations of estradiol among cows exhibiting or not exhibiting estrus during a fixed-time AI protocol. Domestic Animal Endocrinology. 48: 15-20.
Pfeifer L.F.M., Moreira E.M., Silva G.M., Souza V.L., Nunes V.R.R., Andrade J.S., Neves P.M.A. & Ferreira R. 2020. Effect of estradiol cypionate on estrus expression and pregnancy in timed artificially inseminated beef cows. Livestock Science. 231: 1-5.
Pinaffi F.L., Santos É.S., Silva M.G.D., Maturana Filho M., Madureira E.H. & Silva L.A. 2015. Follicle and corpus luteum size and vascularity as predictors of fertility at the time of artificial insemination and embryo transfer in beef cattle. Pesquisa Veterinária Brasileira. 35(5): 470-476.
Pohler K.G., Geary T.W., Atkins J.A., Perry G.A., Jinks E.M. & Smith M. F. 2012. Follicular determinants of pregnancy establishment and maintenance. Cell and Tissue Research. 349(3): 649-664.
Ribeiro Filho A.D.L., Ferraz P.A., Rodrigues A.S., Bittencourt T.C.B.D.S.C., Loiola M.V.G. & Chalhoub M. 2013. Diâmetro do folículo no momento da inseminação artificial em tempo fixo e taxa de concepção em vacas Nelore. Ciência Animal Brasileira. 14(4): 501-507.
Richardson B.N., Hill S.L., Stevenson J.S., Djira G.D. & Perry G.A. 2016. Expression of estrus before fixed-time AI affects conception rates and factors that impact expression of estrus and the repeatability of expression of estrus in sequential breeding seasons. Animal Reproduction Science. 166: 133-140.
Rodrigues A.D., Cooke R.F., Cipriano R.S., Silva L.G.T., Cerri R.L.A., Cruppe L.H., Meneghetti M., Pohler K.G. & Vasconcelos J.L.M. 2018. Impacts of estrus expression and intensity during a timed-AI protocol on variables associated with fertility and pregnancy success in Bos indicus-influenced beef cows. Journal Animal Science. 96(1): 236-249.
Sá Filho M.F., Torres-Júnior J.R.S., Penteado L., Gimenes L.U., Ferreira R.M., Ayres H., Castro e Paula L.A., Sales J.N.S. & Baruselli P.S. 2010. Equine chorionic gonadotropin improves the efficacy of a progestin-based fixed-time artificial insemination protocol in Nelore (Bos indicus) heifers. Animal Reproduction Science. 118: 182-187.
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