Increased antral follicle population and in vitro embryo production in pregnant Holstein
DOI:
https://doi.org/10.5433/1679-0359.2021v42n5p2851Keywords:
Antral follicle count, Dairy cattle, In vitro embryo production, Pregnancy.Abstract
This study used Holstein cattle to evaluate the following: I) the productive and reproductive characteristics of cows with low, intermediate and high antral follicle counts (AFCs) that were subjected to artificial insemination (AI) and comparison of AFC variability at the time of AI (nonpregnant) and at two time points during pregnancy (30 and 60 days), and II) whether the pregnancy status and different pregnancy periods in heifers improves the efficiency at in vitro embryo production (IVEP). In study I, 75 high-milk production cows with body condition scores (BCSs) of 2.75 to 4.75 and ages of 23 to 99 months were selected. On the day of estrus, AFCs (follicles bigger, smaller 3 mm), BCS, body weight, and diameters of the dominant follicle, ovaries and the corpus luteum were evaluated. Posteriorly, AFC was monitored in pregnant cows at 30 days (n = 35) and at 60 days for comparison of AFC before pregnancy versus different periods. In study II, heifers (n = 9) with BCS of 2.5 to 3.5 and ages of 10 to 16 months were selected for ovum pick-up and an IVEP program before AI (nonpregnant) as well as at 0 to 30, 31 to 60, and bigger 60 days of pregnancy. Statistical analysis was performed using PROC GLM and binary logistic regression model (P bigger, smaller 0.05). In study I, AFC was not associated with variations in productive and reproductive parameters. However, AFCs in the low group increased following pregnancy (AI: 14.82 ± 1.36, 30 days: 23.45 ± 2.31 and 60 days: 35.18 ± 3.17 follicles). AFCs increased from AI to 60 days in the intermediate group but did not vary among time points in the high group. AFCs varied among AFC groups in AI and at 30 days of pregnancy but not at 60 days. In study II, the mean of total oocytes (17.43 ± 4.52 vs. 41.67 ± 3.79) and viable oocytes (13.77 ± 3.63 vs. 30.56 ± 3.45) increased from AI (nonpregnant) to the first 30 days of pregnancy. The mean number of embryos produced increased during pregnancy and during the first 30 days of pregnancy (4.55 ± 0.75) compared to the nonpregnant period (1.39 ± 0.85). In conclusion, pregnancy positively influences AFC, and the greatest effect is noted in low count cows. In addition, the OPU at the time of pregnancy increased the efficiency of IVEP in heifers.Downloads
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References
Burns, D. S., Jimenez-Krassel, F., Ireland, J. L. H., Knight, P. G., & Ireland, J. J. (2005). Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle stimulating hormone concentrations. Biology of Reproduction, 73(1), 54-62. doi: 10.1095/biolreprod.104.036277
Center, K., Dixon, D., Looney, C., & Rorie, R. (2018). Anti-mullerian hormone and follicle counts as predictors of superovulatory response and embryo production in beef cattle. Advances in Reproductive Sciences, 6(1), 22-33. doi: 10.4236/arsci.2018.61003
Claes, A., Ball, B. A., Scoggin, K. E., Roser, J. F., Woodward, E. M., Davolli, G. M., Squires, E. L., Troedsson, M. H. T. (2017). The influence of age, antral follicle count and diestrous ovulations on estrous cycle characteristics of mares. Theriogenology, 97(15), 34-40. doi: 10.1016/j.theriogenology. 2017.04.019
Coad, J., & Dunstall, M. (2011). Anatomy and physiology for midwives (3nd ed.). London: Churchill Livingstone.
Cushman, R. A., Allan, M. F., Kuehn, L. A., Snelling, W. M., Cupp, A. S., & Freetly, H. C. (2009). Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: Investigation of influence of stage of the estrous cycle, age, and birth weight1, 2. Journal of Animal Science, 87(6), 1971-1980. doi: 10.2527/jas.2008-1728
Evans, A., Mossa, F., Walsh, S., Scheetz, D., Jimenez-Krassel, F., Ireland, J. L. H.,… Ireland, J. J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reproduction in Domestic Animals, 47(4), 31-37. doi: 10.1111/j.1439-05 31.2012.02052.x
Ferguson, J. D., Galligan, D. T., & Thomsen, N. (1994). Principal descriptors of body condition score in holstein cows. Journal of Dairy Science, 77(9), 2695-2703. doi: 10.3168/jds.S0022-0302(94)77212-X
Gonçalves, G. R., Morotti, F., Colombo, A. H. B., Bonato, D. V., Bizarro-Silva, C., Rosa, C. O.,… Seneda, M. M. (2020). Influence of age and ovarian antral follicle count on the reproductive characteristics of embryo donor mares. Veterinary Record, 186(17), 564-564. doi: 10.1136/vr.105526
Ireland, J., Ward, F., Jimenez-Krassel, F., Ireland, J. L. H., Smith, G. W., Lonergan, P., & Evans, A. C. O. (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. Human Reproduction, 22(6), 1687-1695. doi: 10.1093/humrep/dem071
Ireland, J. J., Smith, G. W., Scheetz, D., Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H.,… Evans, A. C. O. (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. Reproduction, Fertility and Development, 23(1), 1-14. doi: 10.1071/RD10226
Ireland, J. L. H., Scheetz, D., Jimenez-Krassel, F., Themmen, A. P. N., Ward, F., Lonergan, P.,… Ireland, J. J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biology of Reproduction, 79(6), 1219-1225. doi: 10.1095/biolreprod. 108.071670
Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H., Smith, G. W., Hou, X., Davis, J. S.,… Ireland, J. J. (2009). Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during estrous cycles in cattle. Biology of Reproduction, 80(6), 1272-1281. doi: 10.1095/biolreprod.108.075093
Jimenez-Krassel, F., Scheetz, D. M., Neuder, L. M., Ireland, J. L. H., Pursley, J. R., Smith, G. W.,… Ireland, J. J. (2015). Concentration of anti-Müllerian hormone in dairy heifers is positively associated with productive herd life. Journal of Dairy Science, 98(5), 3036-3045. doi: 10.3168/jds.2014-8130
Jimenez-Krassel, F., Scheetz, D. M., Neuder, L. M., Pursley, J. R., & Ireland, J. J. (2017). A single ultrasound determination of ≥25 follicles ≥3 mm in diameter in dairy heifers is predictive of a reduced productive herd life. Journal of Dairy Science, 100(6), 5019-5027. doi: 10.3168/jds.2016-12277
Lonergan, P., Rizos, D., Ward, F., & Boland, M. P. (2001). Factors influencing oocyte and embryo quality in cattle. Reproduction Nutrition Development, 41(5), 427-437. doi: 10.1051/rnd:2001142
Martinez, M. F., Sanderson, N., Quirke, L. D., Lawrence, S. B., & Juengel, J. L. (2016). Association between antral follicle count and reproductive measures in New Zealand lactating dairy cows maintained in a pasture-based production system. Theriogenology, 85(3), 466-475. doi: 10.1016/j.theriogenology.2015. 09.026
Meintjes, M., Bellow, M. S., Broussard, J. R., Paul, J. B., & Godke, R. A. (1995). Transvaginal aspiration of oocytes from hormone-treated pregnant beef cattle for in vitro fertilization. Journal of Animal Science, 73(4), 967-974. doi: 10.2527/1995.734967x
Monteiro, F. M., Batista, E. O. S., Vieira, L. M., Bayeux, B. M., Accorsi, M., Campanholi, S. P.,... Baruselli, P. S. (2017). Beef donor cows with high number of retrieved COC produce more in vitro embryos compared with cows with low number of COC after repeated ovum pick-up sessions. Theriogenology, 90(1), 54-58. doi: 10.1016/j.theriogenology.2016.11.002
Moraes, F. L. Z. de, Morotti, F., Costa, C. B., Lunardelli, P. A., & Seneda, M. M. (2019). Relationships between antral follicle count, body condition, and pregnancy rates after timed-AI in Bos indicus cattle. Theriogenology, 136(15), 10-14. doi: 10.1016/j.theriogenology.2019.06.024
Morotti, F., Moretti, R., Santos, G. M. G. dos, Silva-Santos, K. C., Ramos Cerqueira, P. H., & Seneda, M. M. (2018). Ovarian follicular dynamics and conception rate in Bos indicus cows with different antral follicle counts subjected to timed artificial insemination. Animal Reproduction Science, 188(1), 170-177. doi: 10.1016/j.anireprosci.2017.12.001
Mossa, F., Walsh, S. W., Butler, S. T., Berry, D. P., Carter, F., Lonergan, P.,… Evans, A. C. O. (2012). Low numbers of ovarian follicles ≥3 mm in diameter are associated with low fertility in dairy cows. Journal of Dairy Science, 95(5), 2355-2361. doi: 10.3168/jds.2011-4325
Nagai, K., Yanagawa, Y., Katagiri, S., & Nagano, M. (2016). The relationship between antral follicle count in a bovine ovary and developmental competence of in vitro-grown oocytes derived from early antral follicles. Biomedical Research, 37(1), 63-71. doi: 10.2220/biomedres.37.63
National Research Council (2001). Nutrient requirements of dairy cattle (7nd rev.). Washington, DC: National Academy Press.
Parrish, J. J., Krogenaes, A., & Susko-Parrish, J. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology, 44(6), 859-869. doi: 10.1016/0093-691X(95)00271-9
Pfeifer, L. F. M., Souza Leal, S. del C. B. de, Schneider, A., Schmitt, E., & Corrêa, M. N. (2012). Effect of the ovulatory follicle diameter and progesterone concentration on the pregnancy rate of fixed-time inseminated lactating beef cows. Revista Brasileira de Zootecnia, 41(4), 1004-1008. doi: 10.1590/S15 16-35982012000400024
Purcell, S. H., Seidel, G. E., McCue, P. M., & Squires, E. L. (2007). Aspiration of oocytes from transitional, cycling, and pregnant mares. Animal Reproduction Science, 100(3-4), 291-300. doi: 10.1016/j. anireprosci.2006.07.009
Rosa, C., Marinho, L., Rosa, P. da, Cesaro, M. de, Lunardelli, P., Silva-Santos, K.,... Seneda, M. (2018). Molecular characteristics of granulosa and cumulus cells and oocyte competence in Nelore cows with low and high numbers of antral follicles. Reproduction in Domestic Animals, 53(4), 921-929. doi: 10.11 11/rda.13189
Santos, G. M. G. dos, Silva-Santos, K. C., Barreiros, T. R. R., Morotti, F., Sanches, B. V., Moraes, F. L. Z. de.,... Seneda, M. M. (2016). High numbers of antral follicles are positively associated with in vitro embryo production but not the conception rate for FTAI in Nelore cattle. Animal Reproduction Science, 165(2), 17-21. doi: 10.1016/j.anireprosci.2015.11.024
Sartori, R., Guardieiro, M., Surjus, R., Melo, L., Prata, A., Ishiguro, M.,… Nascimento, A. (2013). Metabolic hormones and reproductive function in cattle. Animal Reproduction, 10(3), 199-205.
Silva-Santos, K., Santos, G., Koetz, C., Jr., Morotti, F., Siloto, L., Marcantonio, T.,... Seneda, M. (2014). Antral follicle populations and embryo production - in vitro and in vivo - of bos indicus-taurus donors from weaning to yearling ages. Reproduction in Domestic Animals, 49(2), 228-232. doi: 10.1111/rda.12 255
Spicer, L. J., Alpizar, E., & Echternkamp, S. E. (1993). Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and(or) insulin-like growth factor I production in vitro1. Journal of Animal Science, 71(5), 1232-1241. doi: 10.2527/1993.7151232x
Takuma, T., Sakai, S., Ichimaru, H., Jinnouchi, T., Kaedei, Y., Nagai, T., & Otoi, T. (2010). Effects of season and reproductive phase on the quality, quantity and developmental competence of oocytes aspirated from japanese black cows. Journal of Reproduction and Development, 56(1), 55-59. doi: 10. 1262/jrd.09-071h
Webb, R., Garnsworthy, P. C., Gong, J.-G., & Armstrong, D. G. (2004). Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science, 82(E-Suppl.), E63-74. doi: 10.2527/ 2004.8213_supplE63x
Williams, G. L., & Stanko, R. L. (2000). Dietary fats as reproductive nutraceuticals in beef cattle. Journal of Animal Science, 77(E-Suppl.), 1. doi: 10.2527/jas2000.77E-Suppl1n
Wright, J. (1998). Photomicrographic illustration of embryo codes. In S. M. Stringfellow, & D. A. Seidel (Eds.), Manual of the international embryo transfer society (3nd ed., pp. 167-170). Savory, IL, USA, International Embryo Transfer Society.
Zeng, Z., Liu, F., & Li, S. (2017). Metabolic adaptations in pregnancy: a review. Annals of Nutrition and Metabolism, 70(1), 59-65. doi: 10.1159/000459633
Zhang, Y., Xu, Y., Xue, Q., Shang, J., Yang, X., Shan, X.,… Zeng, C. (2019). Discordance between antral follicle counts and anti-Müllerian hormone levels in women undergoing in vitro fertilization. Reproductive Biology and Endocrinology, 17(1), 51-51. doi: 10.1186/s12958-019-0497-4
Center, K., Dixon, D., Looney, C., & Rorie, R. (2018). Anti-mullerian hormone and follicle counts as predictors of superovulatory response and embryo production in beef cattle. Advances in Reproductive Sciences, 6(1), 22-33. doi: 10.4236/arsci.2018.61003
Claes, A., Ball, B. A., Scoggin, K. E., Roser, J. F., Woodward, E. M., Davolli, G. M., Squires, E. L., Troedsson, M. H. T. (2017). The influence of age, antral follicle count and diestrous ovulations on estrous cycle characteristics of mares. Theriogenology, 97(15), 34-40. doi: 10.1016/j.theriogenology. 2017.04.019
Coad, J., & Dunstall, M. (2011). Anatomy and physiology for midwives (3nd ed.). London: Churchill Livingstone.
Cushman, R. A., Allan, M. F., Kuehn, L. A., Snelling, W. M., Cupp, A. S., & Freetly, H. C. (2009). Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: Investigation of influence of stage of the estrous cycle, age, and birth weight1, 2. Journal of Animal Science, 87(6), 1971-1980. doi: 10.2527/jas.2008-1728
Evans, A., Mossa, F., Walsh, S., Scheetz, D., Jimenez-Krassel, F., Ireland, J. L. H.,… Ireland, J. J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reproduction in Domestic Animals, 47(4), 31-37. doi: 10.1111/j.1439-05 31.2012.02052.x
Ferguson, J. D., Galligan, D. T., & Thomsen, N. (1994). Principal descriptors of body condition score in holstein cows. Journal of Dairy Science, 77(9), 2695-2703. doi: 10.3168/jds.S0022-0302(94)77212-X
Gonçalves, G. R., Morotti, F., Colombo, A. H. B., Bonato, D. V., Bizarro-Silva, C., Rosa, C. O.,… Seneda, M. M. (2020). Influence of age and ovarian antral follicle count on the reproductive characteristics of embryo donor mares. Veterinary Record, 186(17), 564-564. doi: 10.1136/vr.105526
Ireland, J., Ward, F., Jimenez-Krassel, F., Ireland, J. L. H., Smith, G. W., Lonergan, P., & Evans, A. C. O. (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. Human Reproduction, 22(6), 1687-1695. doi: 10.1093/humrep/dem071
Ireland, J. J., Smith, G. W., Scheetz, D., Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H.,… Evans, A. C. O. (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. Reproduction, Fertility and Development, 23(1), 1-14. doi: 10.1071/RD10226
Ireland, J. L. H., Scheetz, D., Jimenez-Krassel, F., Themmen, A. P. N., Ward, F., Lonergan, P.,… Ireland, J. J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biology of Reproduction, 79(6), 1219-1225. doi: 10.1095/biolreprod. 108.071670
Jimenez-Krassel, F., Folger, J. K., Ireland, J. L. H., Smith, G. W., Hou, X., Davis, J. S.,… Ireland, J. J. (2009). Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during estrous cycles in cattle. Biology of Reproduction, 80(6), 1272-1281. doi: 10.1095/biolreprod.108.075093
Jimenez-Krassel, F., Scheetz, D. M., Neuder, L. M., Ireland, J. L. H., Pursley, J. R., Smith, G. W.,… Ireland, J. J. (2015). Concentration of anti-Müllerian hormone in dairy heifers is positively associated with productive herd life. Journal of Dairy Science, 98(5), 3036-3045. doi: 10.3168/jds.2014-8130
Jimenez-Krassel, F., Scheetz, D. M., Neuder, L. M., Pursley, J. R., & Ireland, J. J. (2017). A single ultrasound determination of ≥25 follicles ≥3 mm in diameter in dairy heifers is predictive of a reduced productive herd life. Journal of Dairy Science, 100(6), 5019-5027. doi: 10.3168/jds.2016-12277
Lonergan, P., Rizos, D., Ward, F., & Boland, M. P. (2001). Factors influencing oocyte and embryo quality in cattle. Reproduction Nutrition Development, 41(5), 427-437. doi: 10.1051/rnd:2001142
Martinez, M. F., Sanderson, N., Quirke, L. D., Lawrence, S. B., & Juengel, J. L. (2016). Association between antral follicle count and reproductive measures in New Zealand lactating dairy cows maintained in a pasture-based production system. Theriogenology, 85(3), 466-475. doi: 10.1016/j.theriogenology.2015. 09.026
Meintjes, M., Bellow, M. S., Broussard, J. R., Paul, J. B., & Godke, R. A. (1995). Transvaginal aspiration of oocytes from hormone-treated pregnant beef cattle for in vitro fertilization. Journal of Animal Science, 73(4), 967-974. doi: 10.2527/1995.734967x
Monteiro, F. M., Batista, E. O. S., Vieira, L. M., Bayeux, B. M., Accorsi, M., Campanholi, S. P.,... Baruselli, P. S. (2017). Beef donor cows with high number of retrieved COC produce more in vitro embryos compared with cows with low number of COC after repeated ovum pick-up sessions. Theriogenology, 90(1), 54-58. doi: 10.1016/j.theriogenology.2016.11.002
Moraes, F. L. Z. de, Morotti, F., Costa, C. B., Lunardelli, P. A., & Seneda, M. M. (2019). Relationships between antral follicle count, body condition, and pregnancy rates after timed-AI in Bos indicus cattle. Theriogenology, 136(15), 10-14. doi: 10.1016/j.theriogenology.2019.06.024
Morotti, F., Moretti, R., Santos, G. M. G. dos, Silva-Santos, K. C., Ramos Cerqueira, P. H., & Seneda, M. M. (2018). Ovarian follicular dynamics and conception rate in Bos indicus cows with different antral follicle counts subjected to timed artificial insemination. Animal Reproduction Science, 188(1), 170-177. doi: 10.1016/j.anireprosci.2017.12.001
Mossa, F., Walsh, S. W., Butler, S. T., Berry, D. P., Carter, F., Lonergan, P.,… Evans, A. C. O. (2012). Low numbers of ovarian follicles ≥3 mm in diameter are associated with low fertility in dairy cows. Journal of Dairy Science, 95(5), 2355-2361. doi: 10.3168/jds.2011-4325
Nagai, K., Yanagawa, Y., Katagiri, S., & Nagano, M. (2016). The relationship between antral follicle count in a bovine ovary and developmental competence of in vitro-grown oocytes derived from early antral follicles. Biomedical Research, 37(1), 63-71. doi: 10.2220/biomedres.37.63
National Research Council (2001). Nutrient requirements of dairy cattle (7nd rev.). Washington, DC: National Academy Press.
Parrish, J. J., Krogenaes, A., & Susko-Parrish, J. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology, 44(6), 859-869. doi: 10.1016/0093-691X(95)00271-9
Pfeifer, L. F. M., Souza Leal, S. del C. B. de, Schneider, A., Schmitt, E., & Corrêa, M. N. (2012). Effect of the ovulatory follicle diameter and progesterone concentration on the pregnancy rate of fixed-time inseminated lactating beef cows. Revista Brasileira de Zootecnia, 41(4), 1004-1008. doi: 10.1590/S15 16-35982012000400024
Purcell, S. H., Seidel, G. E., McCue, P. M., & Squires, E. L. (2007). Aspiration of oocytes from transitional, cycling, and pregnant mares. Animal Reproduction Science, 100(3-4), 291-300. doi: 10.1016/j. anireprosci.2006.07.009
Rosa, C., Marinho, L., Rosa, P. da, Cesaro, M. de, Lunardelli, P., Silva-Santos, K.,... Seneda, M. (2018). Molecular characteristics of granulosa and cumulus cells and oocyte competence in Nelore cows with low and high numbers of antral follicles. Reproduction in Domestic Animals, 53(4), 921-929. doi: 10.11 11/rda.13189
Santos, G. M. G. dos, Silva-Santos, K. C., Barreiros, T. R. R., Morotti, F., Sanches, B. V., Moraes, F. L. Z. de.,... Seneda, M. M. (2016). High numbers of antral follicles are positively associated with in vitro embryo production but not the conception rate for FTAI in Nelore cattle. Animal Reproduction Science, 165(2), 17-21. doi: 10.1016/j.anireprosci.2015.11.024
Sartori, R., Guardieiro, M., Surjus, R., Melo, L., Prata, A., Ishiguro, M.,… Nascimento, A. (2013). Metabolic hormones and reproductive function in cattle. Animal Reproduction, 10(3), 199-205.
Silva-Santos, K., Santos, G., Koetz, C., Jr., Morotti, F., Siloto, L., Marcantonio, T.,... Seneda, M. (2014). Antral follicle populations and embryo production - in vitro and in vivo - of bos indicus-taurus donors from weaning to yearling ages. Reproduction in Domestic Animals, 49(2), 228-232. doi: 10.1111/rda.12 255
Spicer, L. J., Alpizar, E., & Echternkamp, S. E. (1993). Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and(or) insulin-like growth factor I production in vitro1. Journal of Animal Science, 71(5), 1232-1241. doi: 10.2527/1993.7151232x
Takuma, T., Sakai, S., Ichimaru, H., Jinnouchi, T., Kaedei, Y., Nagai, T., & Otoi, T. (2010). Effects of season and reproductive phase on the quality, quantity and developmental competence of oocytes aspirated from japanese black cows. Journal of Reproduction and Development, 56(1), 55-59. doi: 10. 1262/jrd.09-071h
Webb, R., Garnsworthy, P. C., Gong, J.-G., & Armstrong, D. G. (2004). Control of follicular growth: local interactions and nutritional influences. Journal of Animal Science, 82(E-Suppl.), E63-74. doi: 10.2527/ 2004.8213_supplE63x
Williams, G. L., & Stanko, R. L. (2000). Dietary fats as reproductive nutraceuticals in beef cattle. Journal of Animal Science, 77(E-Suppl.), 1. doi: 10.2527/jas2000.77E-Suppl1n
Wright, J. (1998). Photomicrographic illustration of embryo codes. In S. M. Stringfellow, & D. A. Seidel (Eds.), Manual of the international embryo transfer society (3nd ed., pp. 167-170). Savory, IL, USA, International Embryo Transfer Society.
Zeng, Z., Liu, F., & Li, S. (2017). Metabolic adaptations in pregnancy: a review. Annals of Nutrition and Metabolism, 70(1), 59-65. doi: 10.1159/000459633
Zhang, Y., Xu, Y., Xue, Q., Shang, J., Yang, X., Shan, X.,… Zeng, C. (2019). Discordance between antral follicle counts and anti-Müllerian hormone levels in women undergoing in vitro fertilization. Reproductive Biology and Endocrinology, 17(1), 51-51. doi: 10.1186/s12958-019-0497-4
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2021-07-02
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Droher, R. G., Cavalieri, F. L. B., Morotti, F., Zangirolamo, A. F., Andreazzi, M. A., & Seneda, M. M. (2021). Increased antral follicle population and in vitro embryo production in pregnant Holstein. Semina: Ciências Agrárias, 42(5), 2851–2866. https://doi.org/10.5433/1679-0359.2021v42n5p2851
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