Antral follicle count in cattle: advantages, challenges, and controversy
Fábio Morotti, Amanda Fonseca Zangirolamo, Nathalia Covre da Silva, Camila Bizarro da Silva, Camila Oliveira Rosa, Marcelo Marcondes Seneda
Abstract
The antral follicle count (AFC) represents the number of follicles visualized by ultrasonography in the ovaries. Antral follicle count tends to be variable among cows but with high repeatability within the same individual. In the last decade, AFC has been considered a biological marker of fertility with many positive aspects of reproductive efficiency for those animals with high AFC. For instance, a larger number and better-quality embryos, better pregnancy rates, increased concentrations of circulating progesterone, in addition to other characteristics linked to fertility, are all responses observed in individuals with high compared with those with low AFC in Bos taurus cattle. However, the positive association between AFC and fertility did not follow the same pattern for Bos indicus. Recent articles showed no connection between fertility and number of antral follicles or better reproductive efficiency for high AFC group in Zebu cows. Thus, the aim of this review is to discuss the various data concerning AFC between indicus and taurus cattle. Additionally, we consider AFC to be a possible tool to improve cattle performance in reproductive biotechnology.
Keywords
References
Batista EOS, Macedo GG, Sala RV, Ortolan MDDV, Sá Filho MF, Del Valle TA, Jesus EF, Lopes RNVR, Renn 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 Domest Anim, 49:448-452.
Baruselli PS, Batista EOS, Ferreira RM. 2016. Plasma anti-müllerian hormone allows reproductive selection of donors with greater potential of embryo production. Spermova, 6:1-13.
Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. 2010. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod, 16:135-152.
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.
Burns DS, Jimenez-Krassel F, Ireland JLH, Knight PG, Ireland JJ. 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. Biol Reprod, 73:53-62.
Cate RL, Mattaliano RJ, Hession C, Tizard R, Farber NM, Cheung A, Ninfa EG, Frey AZ, Gash DJ, Chow EP, Fisher RA, Bertonis JM, Torres G, Wallner BP, Ramachandran KL, Ragin RC, Manganaro TF, MacLaughlin DT, Donahoe PK.1986. Isolation of the bovine and human genes for mullerian inhibiting substance and expression of the human gene in animal cells. Cell, 45:685-698.
Diskin MG, Morris DG. 2008. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim, 43:260-267.
Erickson BH. 1966. Development and senescence of the postnatal bovine ovary. J Anim Sci, 25:800-805.
Evans ACO, Mossa F, Walsh SW, Scheetz D, Jimenez-Krassel F, Ireland JLH, Smith GW, Ireland JJ. 2012. Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod Domest Anim, 47:31-37.
Guerreiro BM, Batista EOS, Vieira LM, Sá Filho MF, Rodrigues CA, Castro Netto A, Silveira CRA, Bayeux BM, Dias EAR, Monteiro FM, Accorsi,M, Lopes RNVR, Baruselli PS. 2014. Plasma antimullerian hormone: an endocrine marker for in vitro embryo production from Bos taurus and Bos indicus donors. Domest Anim Endocrinol, 49:96-104.
Hansen P. 2014. Current and future assisted reproductive technologies for mammalian farm animals. Adv Exp Med Biol, 752:1-22.
Hunter J. 1787. An experiment to determine the effect of extirpating one ovarium upon the number of young produced. Philos Trans R Soc Lond, 77:233-239.
Inskeep EK. 2004. Preovulatory, postovulatory, and postmaternal recognition effects of concentrations of progesterone on embryonic survival in the cow. J Anim. Sci, 82:24-39.
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 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-müllerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev, 23:1-14.
Ireland JLH, Scheetz D, Jimenez-Krasse 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.
Jimenez-Krassel F, Folger JK, Ireland JLH, Smith GW, Hou X, Davis JS, Lonergan P, Evans ACO, Ireland JJ. 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. Biol Reprod, 80:1272-1281.
Jimenez-Krassel F, Scheetz DM, Neuder LM, Ireland JLH, Pursley JR, Smith GW, Tempelman RJ, Ferris T, Roudebush WE, Mossa F, Lonergan P, Evans, ACO, Ireland JJ. 2015. Concentration of antiMüllerian hormone in dairy heifers is positively associated with productive herd life. J Dairy Sci, 98:3036-3045.
Jimenez-Krassel F, Scheetz DM, Neuder LM, Pursley JR, Ireland JJ. 2017. A single ultrasound determination of ≥25 follicles ≥3 mm in diameter in dairy heifers is predictive of a reduced productive herd life. J Dairy Sci, 100:5019-5027.
Mapletoft RJ, Hasler JF. 2005. Assisted reproductive technologies in cattle: a review. Rev Sci Tech, 24:393- 403.
Martinez MF, Sanderson N, Quirke LD, Lawrence SB, Juengel JL. 2016. Association between antral follicle count and reproductive measures in New Zealand lactating dairy cows maintained in a pasturebased production system. Theriogenology, 85:466-475.
McNeel AK, Cushman RA. 2015. Influence of puberty and antral follicle count on calving day in crossbred beef heifers. Theriogenology, 84:1061-1066.
Mendonça HGR, Santos GMG, Silva-Santos KC, Barreiros TRR, Blaschi W, Morotti F, Moraes FLZ, Seneda MM. 2013. Pregnancy rates following FTAI of Nelore heifers (Bos indicus) with high, intermediate and low numbers of antral follicles. Anim Reprod, 10:452. Abstract.
Monteiro FM, Batista EOS, Vieira LM, Bayeux BM, Accorsi M, Campanholi SP, Dias EAR, Souza AH, Baruselli PS. 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, 90:54-58.
Morotti F, Santos GMG, Silva-Santos KC, Moritz Y, Marcantonio TN, Seneda MM. 2014. Follicular dynamics in Nelore females (Bos indicus) with high or low numbers of antral follicles. Anim Reprod, 11:352. Abstract.
Morotti F, Barreiros TRR, Machado FZ, González SM, Marinho LSR, Seneda MM. 2015. Is the number of antral follicles an interesting selection criterium for fertility in cattle? Anim Reprod, 12:479-486.
Morotti F, Santos GMG, Koetz Júnior C, SilvaSantos KC, Roso VM, Seneda MM. 2017. Correlation between phenotype, genotype and antral follicle population in beef heifers. Theriogenology, 91:21-26.
Mossa F, Duffy P, Naitana S, Lonergan P, Evans AC. 2007. Association between numbers of ovarian follicles in the first follicle wave and superovulatory response in ewes. Anim Reprod Sci, 100:391-396.
Mossa F, Jimenez-Krassel F, Folger JK, Ireland JL, Smith GW, Lonergan P, Evans AC, Ireland JJ. 2010. Evidence that high variation in antral follicle count during follicular waves is linked to alterations in ovarian androgen production in cattle. Reproduction, 140:713- 720.
Mossa F, Walsh SW, Butler ST, Berry DP, Carter F, Lonergan P, Smith GW, Ireland JJ, Evans ACO. 2012. Low numbers of ovarian follicles ≥ 3 mm in diameter are associated with low fertility in dairy cows. J Dairy Sci, 95:2355-2361.
Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JLH, Hildebrandt TB, Lonergan P, Ireland JJ, Evans ACO. 2013. Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol Reprod, 88:92. doi: 10.1095/biolreprod.112.107235.
Pfeifer LFM, Leal SdCBdS, Schneider A, Schmitt E, Corrêa MN. 2012. Effect of the ovulatory follicle diameter and progesterone concentration on the pregnancy rate of fixed-time inseminated lactating beef cows. Rev Bras Zootec, 41:1004-1008.
Pohler KG, Geary TW, Atkins JA, Perry GA, Jinks EM, Smith MF. 2012. Follicular determinants of pregnancy establishment and maintenance. Cell Tissue Res, 349:649-664.
Pontes JHF, Melo-Sterza FA, Basso AC, Ferreira CR, Sanches BV, Rubin KCP, Seneda MM. 2011. Ovum pick up, in vitro embryo production, and pregnancy rates from a large-scale commercial program using Nelore cattle (Bos indicus) donors. Theriogenology, 75:1640-1646.
Rico C, Fabre S, Médigue C, Di Clemente N, Clément F, Bontoux M, Touzé JL, Dupont M, Briant E, Rémy B, Beckers JF, Monniaux D. 2009. Antimullerian 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.
Rico C, Drouilhet L, Salvetti P, Dalbiès-Tran R, Jarrier P, Touzé J-L, Pillet E, Ponsart C, Fabre S, Monniaux D. 2012. Determination of anti-müllerian 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.
Rosa CO, Marinho LSR, Lunardelli PA, Machado FZ, Gonzalez SM, Rosa PRA, Cesaro MP, Bueno JVR, Bordignon V, Seneda MM. 2015. In vitro embryo development and gene expression in granulosa and cumulus cells from Bos indicus cows with different numbers of antral follicles. Anim Reprod, 12:762. Abstract.
Sá Filho MF, Crespilho AM, Santos JE, Perry GA, Baruselli PS. 2010. Ovarian follicle diameter at timed insemination and estrous response influence likelihood of ovulation and pregnancy after estrous synchronization with progesterone or progestin-based protocols in suckled Bos indicus cows. Anim Reprod Sci, 120:23-30.
Santos GMG, Silva-Santos KC, Siloto LS, Morotti F, Marcantonio TN, Marinho LSR, Thasmo RLO, Koetz JRC, Cintra DML, Seneda MM. 2012.
Dinâmica folicular em fêmeas bovinas de alta, média e baixa contagem de folículos antrais: resultados preliminares. Acta Sci Vet, 40:422. Abstract.
Santos GMG, Silva-Santos KC, Barreiros TRR, Blaschi W, Morotti F, Silva CB, Moraes FLZ, Giudicissi DPL, Seneda MM. 2013. Conception rates following FTAI of Nelore cows (Bos indicus) with high, intermediate and low numbers of antral follicles. Anim Reprod, 10:451. Abstract.
Santos GMG, Silva-Santos KC, Barreiros TRR, Morotti F, Sanches, BV, Moraes FLZ, Blaschi W, Seneda MM. 2014. High numbers of antral follicles influence the in vitro embryo production, but not the conception rate of fixed-time artificial insemination in nelore cattle. Reprod Fertil Dev, 27:206.
Santos GMG, Silva-Santos KC, Barreiros TRR, Morotti F, Sanches BV, de Moraes FLZ, Blaschi W, Seneda MM. 2016. High numbers of antral follicles are positively associated with in vitro embryo production but not the conception rate for FTAI in Nelore cattle. Anim Reprod Sci, 165:17-21.
Silva-Santos KC, Santos GMG, Siloto LS, Hertel MF, Andrade ER, Rubinb MIB, Sturionc L, MeloSterza FA, Seneda MM. 2011. Estimate of the population of preantral follicles in the ovaries of Bos taurus indicus and Bos taurus taurus cattle. Theriogenology, 76:1051-1057.
Silva-Santos KC, Santos GMG, Koetz Júnior C, Morotti F, Siloto LS, Marcantonio TN, Urbano MR, Oliveira RL, Lima DCM, Seneda MM. 2014a. Antral follicle populations and embryo production - in vitro and in vivo - of Bos indicus-taurus donors from weaning to yearling ages. Reprod Domest Anim, 49:228-232.
Silva-Santos KC, Siloto LS, Santos GMC, Morotti F, Marcantonio TN, Seneda MM. 2014b. Comparison of antral and pre-antral ovarian follicle populations between Bos indicus and Bos indicus-taurus cows with high or low antral follicles counts. Reprod Domest Anim, 49:48-51.
Singh J, Dominguez M, Jaiswal R, Adams GP. 2004. A simple ultrasound test to predict the superstimulatory response in cattle. Theriogenology, 62:227-243.
Taneja M, Bols PE, Van De Velde A, Ju JC, Schreiber D, Tripp MW, Levine H, Echelard Y, Riesen J, Yang X. 2000. Developmental competence of juvenile calf oocytes in vitro and in vivo: influence of donor animal variation and repeated gonadotrophin stimulation. Biol Reprod, 62:206-213.
Walsh SW, Mossa F, Butler ST, Berry DP, Scheetz D, Jimenez-Krassel F, Tempelman RJ, Carter F, Lonergan P, Evans ACO, Ireland JJ. 2014. Heritability and impact of environmental effects during pregnancy on antral follicle count in cattle. J Dairy Sci, 97:4503-4511.
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email