Predictive value of antral follicle count and anti-Müllerian hormone for follicle and oocyte developmental competence during the early prepubertal period in a sheep model
Laura Torres-Rovira A , Antonio Gonzalez-Bulnes B , Sara Succu A , Antonio Spezzigu C , Maria E. Manca A , Giovanni G. Leoni A , Marina Sanna A , Salvatore Pirino A , Marilia Gallus D , Salvatore Naitana A and Fiammetta Berlinguer A EA Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Italy.
B Department of Animal Reproduction, INIA, Avda. Puerta de Hierro s/n, 28040 Madrid, Spain.
C Embryo Sardegna, Technology, Reproduction and Fertility, 07034 Perfugas, Località Suiles (SS), Italy.
D Department of Animal Production, AGRIS Sardegna, Loc. Bonassai S.S. 291 Sassari-Fertilia – Km. 18,600, 07100 Sassari, Italy.
E Corresponding author. Email: berling@uniss.it
Reproduction, Fertility and Development 26(8) 1094-1106 https://doi.org/10.1071/RD13190
Submitted: 18 June 2013 Accepted: 2 August 2013 Published: 6 September 2013
Abstract
Circulating anti-Müllerian hormone (AMH) and antral follicle count (AFC) are addressed as suitable markers of oocyte quantity and quality during adulthood. To investigate whether AFC and circulating AMH could predict follicle development and oocyte quality during the prepubertal period we used 40-day-old ewe lambs with high, intermediate and low AFC (≥30, 16–29 and ≤15 follicles respectively). The analysis of the response to the exogenous FSH ovarian reserve test showed a positive correlation between AFC, AMH plasma levels, total follicle number and the number of large follicles (≥3 mm) grown after exogenous FSH administration. The incorporation of abattoir-derived oocytes collected from ovaries with different AFC in an in vitro embryo production system showed that a high AFC can predict oocyte quality in prepubertal ovaries, reflecting an ovarian status suitable for follicular development. The histological quantification of the ovarian reserve evidenced that AFC was not predictive of differences in either the number of healthy follicles or the size of the primordial follicle pool in prepubertal ovaries. Further studies are needed to investigate the implication on the reproductive performance of the significant inter-individual differences found in the present study in AFC and circulating AMH in the early prepubertal period.
Additional keywords: embryo, ovary, preantral follicle, ultrasound.
References
Beck-Peccoz, P., Padmanabhan, V., Baggiani, A. M., Cortelazzi, D., Buscaglia, M., Medri, G., Marconi, A. M., Pardi, G., and Beitins, I. Z. (1991). Maturation of hypothalamic–pituitary–gonadal function in normal human fetuses: circulating levels of gonadotrophins, their common α-subunit and free testosterone, and discrepancy between immunological and biological activities of circulating follicle-stimulating hormone. J. Endocrinol. Invest. 14, 861–865.| 1802924PubMed |
Burns, D. S., Jimenez-Krassel, F., Ireland, J. L., Knight, P. G., and 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. Biol. Reprod. 73, 54–62.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1Srtrk%3D&md5=7acd1cb6f72a58e79b37e64ea03e6a31CAS | 15744026PubMed |
Campbell, B. K., Telfer, E. E., Webb, R., and Baird, D. T. (2004). Evidence of a role for follicle-stimulating hormone in controlling the rate of preantral follicle development in sheep. Endocrinology 145, 1870–1879.
| Evidence of a role for follicle-stimulating hormone in controlling the rate of preantral follicle development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1SisL8%3D&md5=2344c00a5e482e36389c5a2587aad082CAS | 14684605PubMed |
Campbell, B. K., Clinton, M., and Webb, R. (2012). The role of anti-Müllerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology 153, 4533–4543.
| The role of anti-Müllerian hormone (AMH) during follicle development in a monovulatory species (sheep).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtlagtb%2FJ&md5=7f9d9427e9be15a047f84daed8cb607dCAS | 22778215PubMed |
Cushman, R. A., Allan, M. F., Kuehn, L. A., Snelling, W. M., Cupp, A. S., and Freetly, H. C. (2009). Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: investigation of influence of stage of the oestrous cycle, age and birth weight. J. Anim. Sci. 87, 1971–1980.
| Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: investigation of influence of stage of the oestrous cycle, age and birth weight.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1eju7w%3D&md5=343ca94d61659176453a0a163134b50dCAS | 19286826PubMed |
Da Silva-Buttkus, P., Marcelli, G., Franks, S., Stark, J., and Hardy, K. (2009). Inferring biological mechanisms from spatial analysis: prediction of a local inhibitor in the ovary. Proc. Natl. Acad. Sci. USA 106, 456–461.
| Inferring biological mechanisms from spatial analysis: prediction of a local inhibitor in the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGksbc%3D&md5=3ba742fb8e4ebcc8f2615cf4467d2c7bCAS | 19122142PubMed |
de Vet, A., Laven, J. S., de Jong, F. H., Themmen, A. P., and Fauser, B. C. (2002). Anti-Müllerian hormone serum levels: a putative marker for ovarian aging. Fertil. Steril. 77, 357–362.
| Anti-Müllerian hormone serum levels: a putative marker for ovarian aging.Crossref | GoogleScholarGoogle Scholar | 11821097PubMed |
Durlinger, A. L., Kramer, P., Karels, B., de Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (1999). Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 140, 5789–5796.
| Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12htLc%3D&md5=e7e5c0a24a837ff5044cca7be0472e45CAS | 10579345PubMed |
Durlinger, A. L., Gruijters, M. J., Kramer, P., Karels, B., Kumar, T. R., Matzuk, M. M., Rose, U. M., de Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (2001). Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 142, 4891–4899.
| Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGqu78%3D&md5=3a48ac20a7ddde1eddf18dff8082b11fCAS | 11606457PubMed |
Durlinger, A. L., Gruijters, M. J., Kramer, P., Karels, B., Ingraham, H. A., Nachtigal, M. W., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (2002a). Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143, 1076–1084.
| Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVeisLs%3D&md5=0c44db4cdb34b343c604a18e80ce63c9CAS | 11861535PubMed |
Durlinger, A. L., Visser, J. A., and Themmen, A. P. (2002b). Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction 124, 601–609.
| Regulation of ovarian function: the role of anti-Müllerian hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Kltg%3D%3D&md5=4fd0399764cc47ab7b74be5fec3a5cf1CAS | 12416998PubMed |
Evans, A. C., Mossa, F., Fair, T., Lonergan, P., Butler, S. T., Zielak-Steciwko, A. E., Smith, G. W., Jimenez-Krassel, F., Folger, J. K., Ireland, J. L., and Ireland, J. J. (2010). Causes and consequences of the variation in the number of ovarian follicles in cattle. Soc. Reprod. Fertil. Suppl. 67, 421–429.
| 1:STN:280:DC%2BC3MnosFemug%3D%3D&md5=0c687004b0eb871a36e8c26653d81417CAS | 21755688PubMed |
Fleming, R., Kelsey, T. W., Anderson, R. A., Wallace, W. H., and Nelson, S. M. (2012). Interpreting human follicular recruitment and anti-Müllerian hormone concentrations throughout life. Fertil. Steril. 98, 1097–1102.
| Interpreting human follicular recruitment and anti-Müllerian hormone concentrations throughout life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1ektbzN&md5=ce5d431f2250291bcc2811ac4f3d8198CAS | 22921077PubMed |
Genro, V. K., Grynberg, M., Scheffer, J. B., Roux, I., Frydman, R., and Fanchin, R. (2011). Serum anti-Müllerian hormone levels are negatively related to Follicular Output RaTe (FORT) in normo-cycling women undergoing controlled ovarian hyperstimulation. Hum. Reprod. 26, 671–677.
| Serum anti-Müllerian hormone levels are negatively related to Follicular Output RaTe (FORT) in normo-cycling women undergoing controlled ovarian hyperstimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitVSntrs%3D&md5=ded4325fd6bf81e1690dab4df84f03e3CAS | 21177311PubMed |
Gonzalez-Bulnes, A., Santiago-Moreno, J., Garcia-Lopez, M., Gomez-Brunet, A., and Lopez-Sebastian, A. (1994). Observacion del ovario en la oveja y eficacia en la deteccion de foliculos y cuerpos luteos mediante ecografia transrectal. Investigación agraria: Producción y sanidad animales 9, 319–329.
González-Bulnes, A., García-García, R. M., Castellanos, V., Santiago-Moreno, J., Ariznavarreta, C., Domínguez, V., López-Sebastián, A., Tresguerres, J. A., and Cocero, M. J. (2003). Influence of maternal environment on the number of transferable embryos obtained in response to superovulatory FSH treatments in ewes. Reprod. Nutr. Dev. 43, 17–28.
| Influence of maternal environment on the number of transferable embryos obtained in response to superovulatory FSH treatments in ewes.Crossref | GoogleScholarGoogle Scholar | 12785447PubMed |
Gonzalez-Bulnes, A., Garcia-Garcia, R. M., Carrizosa, J. A., Urrutia, B., Souza, C. J., Cocero, M. J., Lopez-Sebastian, A., and McNeilly, A. S. (2004). Plasma inhibin A determination at start superovulatory FSH treatments is predictive for embryo outcome in goats. Domest. Anim. Endocrinol. 26, 259–266.
| 1:CAS:528:DC%2BD2cXhsVKgtrs%3D&md5=f3ddbeb9da8f28db57ca728cdddfc6c1CAS | 15036379PubMed |
Gougeon, A. (1996). Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 17, 121–155.
| 1:CAS:528:DyaK28XislGisbc%3D&md5=d6971992e06b1257c7ed78c58e17acdcCAS | 8706629PubMed |
Hage, A. J., Groen-Klevant, A. C., and Welschen, R. (1978). Follicle growth in the immature rat ovary. Acta Endocrinol. (Copenh.) 88, 375–382.
| 1:STN:280:DyaE1c3gslChtA%3D%3D&md5=2d8c62dca1add22cec68e0bdd17d4054CAS | 580836PubMed |
Hagen, C. P., Aksglaede, L., Sørensen, K., Main, K. M., Boas, M., Cleemann, L., Holm, K., Gravholt, C. H., Andersson, A. M., Pedersen, A. T., Petersen, J. H., Linneberg, A., Kjaergaard, S., and Juul, A. (2010). Serum levels of anti-Müllerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J. Clin. Endocrinol. Metab. 95, 5003–5010.
| Serum levels of anti-Müllerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2nsbjL&md5=4f267799f953c36d2ed6a6ea184660cfCAS | 20719830PubMed |
Hansen, K. R., Hodnett, G. M., Knowlton, N., and Craig, L. B. (2011). Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil. Steril. 95, 170–175.
| Correlation of ovarian reserve tests with histologically determined primordial follicle number.Crossref | GoogleScholarGoogle Scholar | 20522327PubMed |
Holte, J., Brodin, T., Berglund, L., Hadziosmanovic, N., Olovsson, M., and Bergh, T. (2011). Antral follicle counts are strongly associated with live-birth rates after assisted reproduction, with superior treatment outcome in women with polycystic ovaries. Fertil. Steril. 96, 594–599.
| Antral follicle counts are strongly associated with live-birth rates after assisted reproduction, with superior treatment outcome in women with polycystic ovaries.Crossref | GoogleScholarGoogle Scholar | 21880276PubMed |
Ireland, J. L., Scheetz, D., Jimenez-Krassel, F., Themmen, A. P., Ward, F., Lonergan, P., Smith, G. W., Perez, G. I., Evans, A. C., and Ireland, J. J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 79, 1219–1225.
| Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCltL3M&md5=60d206909bf0010a7640c68c04a83ab1CAS | 18768912PubMed |
Ireland, J. J., Zielak-Steciwko, A. E., Jimenez-Krassel, F., Folger, J., Bettegowda, A., Scheetz, D., Walsh, S., Mossa, F., Knight, P. G., Smith, G. W., Lonergan, P., and Evans, A. C. (2009). Variation in the ovarian reserve is linked to alterations in intrafollicular oestradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol. Reprod. 80, 954–964.
| Variation in the ovarian reserve is linked to alterations in intrafollicular oestradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVajsr4%3D&md5=90eec3699aa7003c27c07b999f994ba3CAS | 19164170PubMed |
Ireland, J. J., Smith, G. W., Scheetz, D., Jimenez-Krassel, F., Folger, J. K., Ireland, J. L., Mossa, F., Lonergan, P., and Evans, A. C. (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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3ktFajtw%3D%3D&md5=e2aea670a34b3ade46497e0e036c4a08CAS | 21366975PubMed |
Jayaprakasan, K., Deb, S., Batcha, M., Hopkisson, J., Johnson, I., and Campbell, B. (2010). The cohort of antral follicles measuring 2–6 mm reflects the quantitative status of ovarian reserve as assessed by serum levels of anti-Müllerian hormone and response to controlled ovarian stimulation. Fertil. Steril. 94, 1775–1781.
| The cohort of antral follicles measuring 2–6 mm reflects the quantitative status of ovarian reserve as assessed by serum levels of anti-Müllerian hormone and response to controlled ovarian stimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1SrtL%2FP&md5=457c4e00f04b23b4bae5f32f01b72505CAS | 19931077PubMed |
Jimenez-Krassel, F., Folger, J. K., Ireland, J. L., Smith, G. W., Hou, X., Davis, J. S., Lonergan, P., Evans, A. C., and 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 oestrous cycles in cattle. Biol. Reprod. 80, 1272–1281.
| Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during oestrous cycles in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGmsb4%3D&md5=d02f7d6f909ef4a58d9ac4a5426d637aCAS | 19211804PubMed |
Kelsey, T. W., Wright, P., Nelson, S. M., Anderson, R. A., and Wallace, W. H. (2011). A validated model of serum anti-Müllerian hormone from conception to menopause. PLoS ONE 6, e22024.
| A validated model of serum anti-Müllerian hormone from conception to menopause.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWqs7%2FN&md5=b0b905c8304e668fa918a8391874fecfCAS | 21789206PubMed |
Kuiri-Hänninen, T., Seuri, R., Tyrväinen, E., Turpeinen, U., Hämäläinen, E., Stenman, U. H., Dunkel, L., and Sankilampi, U. (2011). Increased activity of the hypothalamic–pituitary–testicular axis in infancy results in increased androgen action in premature boys. J. Clin. Endocrinol. Metab. 96, 98–105.
| Increased activity of the hypothalamic–pituitary–testicular axis in infancy results in increased androgen action in premature boys.Crossref | GoogleScholarGoogle Scholar | 20881260PubMed |
Kupesic, S., Kurjak, A., Bjelos, D., and Vujisic, S. (2003). Three-dimensional ultrasonographic ovarian measurements and in vitro fertilization outcome are related to age. Fertil. Steril. 79, 190–197.
| Three-dimensional ultrasonographic ovarian measurements and in vitro fertilization outcome are related to age.Crossref | GoogleScholarGoogle Scholar | 12524087PubMed |
Kwee, J., Schats, R., McDonnell, J., Schoemaker, J., and Lambalk, C. B. (2006). The clomiphene citrate challenge test versus the exogenous follicle-stimulating hormone ovarian reserve test as a single test for identification of low responders and hyper-responders to in vitro fertilization. Fertil. Steril. 85, 1714–1722.
| The clomiphene citrate challenge test versus the exogenous follicle-stimulating hormone ovarian reserve test as a single test for identification of low responders and hyper-responders to in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 16650416PubMed |
Lahoz, B., Alabart, J. L., Monniaux, D., Mermillod, P., and Folch, J. (2012). Anti-Müllerian hormone plasma concentration in prepubertal ewe lambs as a predictor of their fertility at a young age. BMC Vet. Res. 8, 118.
| Anti-Müllerian hormone plasma concentration in prepubertal ewe lambs as a predictor of their fertility at a young age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2jsb3L&md5=3775e63a93f656bbe460222e579a79b7CAS | 22824005PubMed |
La Marca, A., Giulini, S., Tirelli, A., Bertucci, E., Marsella, T., Xella, S., and Volpe, A. (2007). Anti-Müllerian hormone measurement on any day of the menstrual cycle strongly predicts ovarian response in assisted reproductive technology. Hum. Reprod. 22, 766–771.
| Anti-Müllerian hormone measurement on any day of the menstrual cycle strongly predicts ovarian response in assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVCqtr8%3D&md5=0f85d3080c07ec7711ca8e70151ea914CAS | 17071823PubMed |
Laven, J. S., Mulders, A. G., Visser, J. A., Themmen, A. P., De Jong, F. H., and Fauser, B. C. (2004). Anti-Müllerian hormone serum concentrations in normo-ovulatory and anovulatory women of reproductive age. J. Clin. Endocrinol. Metab. 89, 318–323.
| Anti-Müllerian hormone serum concentrations in normo-ovulatory and anovulatory women of reproductive age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCitw%3D%3D&md5=62c9ca33803fe5cdc0e46aa845241124CAS | 14715867PubMed |
Leoni, G., Bogliolo, L., Berlinguer, F., Rosati, I., Pintus, P. P., Ledda, S., and Naitana, S. (2002). Defined media for vitrification, warming and rehydration: effects on post-thaw protein synthesis and viability of in vitro-derived ovine embryos. Cryobiology 45, 204–212.
| Defined media for vitrification, warming and rehydration: effects on post-thaw protein synthesis and viability of in vitro-derived ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVWlsL0%3D&md5=07d43bb790a433fc416b56e33613b851CAS | 12510005PubMed |
Leoni, G. G., Succu, S., Berlinguer, F., Rosati, I., Bebbere, D., Bogliolo, L., Ledda, S., and Naitana, S. (2006). Delay on the in vitro kinetic development of prepubertal ovine embryos. Anim. Reprod. Sci. 92, 373–383.
| Delay on the in vitro kinetic development of prepubertal ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287ot1entQ%3D%3D&md5=84bef3834e698b9809b62b936bbe6acdCAS | 16054784PubMed |
Leoni, G. G., Berlinguer, F., Succu, S., Bebbere, D., Mossa, F., Madeddu, M., Ledda, S., Bogliolo, L., and Naitana, S. (2008). A new selection criterion to assess good-quality ovine blastocysts after vitrification and to predict their transfer into recipients. Mol. Reprod. Dev. 75, 373–382.
| A new selection criterion to assess good-quality ovine blastocysts after vitrification and to predict their transfer into recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCqug%3D%3D&md5=a50260524d8292fc823d46a5e8e3da07CAS | 17440971PubMed |
Loh, J. S., and Maheshwari, A. (2011). Anti-Müllerian hormone: is it a crystal ball for predicting ovarian ageing? Hum. Reprod. 26, 2925–2932.
| Anti-Müllerian hormone: is it a crystal ball for predicting ovarian ageing?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGktb3K&md5=e6bdda218733b05dc90aba7a2eefb458CAS | 21849297PubMed |
Menchaca, A., Vilariño, M., Crispo, M., de Castro, T., and Rubianes, E. (2010). New approaches to superovulation and embryo transfer in small ruminants. Reprod. Fertil. Dev. 22, 113–118.
| New approaches to superovulation and embryo transfer in small ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlagu7w%3D&md5=6f90991494d4050f2956773d9b4104fbCAS | 20003852PubMed |
Monniaux, D., Baril, G., Laine, A. L., Jarrier, P., Poulin, N., Cognié, J., and Fabre, S. (2011). Anti-Müllerian hormone as a predictive endocrine marker for embryo production in the goat. Reproduction 142, 845–854.
| Anti-Müllerian hormone as a predictive endocrine marker for embryo production in the goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1GqtLbO&md5=63814f114961e5a61571b05a02f7e248CAS | 21930684PubMed |
Monniaux, D., Drouilhet, L., Rico, C., Estienne, A., Jarrier, P., Touzé, J. L., Sapa, J., Phocas, F., Dupont, J., Dalbiès-Tran, R., and Fabre, S. (2013). Regulation of anti-Müllerian hormone production in domestic animals. Reprod. Fertil. Dev. 25, 1–16.
| Regulation of anti-Müllerian hormone production in domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVertLjF&md5=dfb3d2a34e2387df28763467b6d97871CAS |
Mossa, F., Leoni, G. G., Berlinguer, F., Succu, S., Madeddu, M., Bebbere, D., and Naitana, S. (2008). Recovery of COCs from ovaries with high follicle numbers enhances in vitro embryo yield in sheep. Anim. Reprod. Sci. 109, 134–145.
| Recovery of COCs from ovaries with high follicle numbers enhances in vitro embryo yield in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnpt1Cgsw%3D%3D&md5=f0a6d718a98dd6fe0694672c89cf0738CAS | 18162333PubMed |
Nelson, S. M., Messow, M. C., Wallace, A. M., Fleming, R., and McConnachie, A. (2011a). Nomogram for the decline in serum anti-Müllerian hormone: a population study of 9,601 infertility patients. Fertil. Steril. 95, 736–741.
| Nomogram for the decline in serum anti-Müllerian hormone: a population study of 9,601 infertility patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsl2juw%3D%3D&md5=d09cf3fc3a775423688bf354412f8f55CAS | 20869051PubMed |
Nelson, S. M., Messow, M. C., McConnachie, A., Wallace, H., Kelsey, T., Fleming, R., Anderson, R. A., and Leader, B. (2011b). External validation of nomogram for the decline in serum anti-Müllerian hormone in women: a population study of 15,834 infertility patients. Reprod. Biomed. Online 23, 204–206.
| External validation of nomogram for the decline in serum anti-Müllerian hormone in women: a population study of 15,834 infertility patients.Crossref | GoogleScholarGoogle Scholar | 21683652PubMed |
Pigny, P., Jonard, S., Robert, Y., and Dewailly, D. (2006). Serum anti-Müllerian hormone as a surrogate for antral follicle count for definition of the polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 91, 941–945.
| Serum anti-Müllerian hormone as a surrogate for antral follicle count for definition of the polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1CmtL0%3D&md5=da343c319cf162813c612c34e21d3250CAS | 16368745PubMed |
Rico, C., Drouilhet, L., Salvetti, P., Dalbiès-Tran, R., Jarrier, P., Touzé, J. L., Pillet, E., Ponsart, C., Fabre, S., and 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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Grs7vI&md5=72ed95e12517db9dc6b05ebadad7d79aCAS | 22935154PubMed |
Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., De la Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression. Biol. Reprod. 68, 236–243.
| Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=22a7b828b8425d4db390bd216ba6da79CAS | 12493719PubMed |
Romeu, A., Molina, I., Tresguerres, J. A., Pla, M., and Peinado, J. A. (1995). Effect of recombinant human luteinising hormone versus human chorionic gonadotrophin: effects on ovulation, embryo quality and transport, steroid balance and implantation in rabbits. Hum. Reprod. 10, 1290–1296.
| 1:CAS:528:DyaK2MXnt1Omsb0%3D&md5=172b2c59c412b16c9542b441f394e6d2CAS | 7657782PubMed |
Scheffer, G. J., Broekmans, F. J., Dorland, M., Habbema, J. D., Looman, C. W., and te Velde, E. R. (1999). Antral follicle counts by transvaginal ultrasonography are related to age in women with proven natural fertility. Fertil. Steril. 72, 845–851.
| Antral follicle counts by transvaginal ultrasonography are related to age in women with proven natural fertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FitlKntg%3D%3D&md5=f4efd0e89bc1cac1f82b708fb12c451fCAS | 10560988PubMed |
Scheffer, G. J., Broekmans, F. J., Looman, C. W., Blankenstein, M., Fauser, B. C., teJong, F. H., and teVelde, E. R. (2003). The number of antral follicles in normal women with proven fertility is the best reflection of reproductive age. Hum. Reprod. 18, 700–706.
| The number of antral follicles in normal women with proven fertility is the best reflection of reproductive age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtlansLo%3D&md5=30652bd396131f1fff5fd02b50bafb3eCAS | 12660259PubMed |
Schmidt, K. L., Kryger-Baggesen, N., Byskov, A. G., and Andersen, C. Y. (2005). Anti-Müllerian hormone initiates growth of human primordial follicles in vitro. Mol. Cell. Endocrinol. 234, 87–93.
| Anti-Müllerian hormone initiates growth of human primordial follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1SqtLc%3D&md5=7ddd67f8c52d2f154ac53e8fa4b4e231CAS | 15836957PubMed |
Veiga-Lopez, A., Gonzalez-Bulnes, A., Garcia-Garcia, R. M., Dominguez, V., and Cocero, M. J. (2005). The effects of previous ovarian status on ovulation rate and early embryo development in response to superovulatory FSH treatments in sheep. Theriogenology 63, 1973–1983.
| The effects of previous ovarian status on ovulation rate and early embryo development in response to superovulatory FSH treatments in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Kjtb0%3D&md5=554862808eb37b0c087f3ef0999abdbbCAS | 15823353PubMed |
Visser, J. A., and Themmen, A. P. (2005). Anti-Müllerian hormone and folliculogenesis. Mol. Cell. Endocrinol. 234, 81–86.
| Anti-Müllerian hormone and folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1SqtLY%3D&md5=c74caa49c363d5f8ac2a9592373ca007CAS | 15836956PubMed |
Visser, J. A., Durlinger, A. L., Peters, I. J., van den Heuvel, E. R., Rose, U. M., Kramer, P., de Jong, F. H., and Themmen, A. P. (2007). Increased oocyte degeneration and follicular atresia during the oestrous cycle in anti-Müllerian hormone-null mice. Endocrinology 148, 2301–2308.
| Increased oocyte degeneration and follicular atresia during the oestrous cycle in anti-Müllerian hormone-null mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFCgsLs%3D&md5=b40619e3bc814e243e3e408a1449d165CAS | 17255205PubMed |
Walker, S. K., Hill, J. L., Kleemann, D. O., and Nancarrow, C. D. (1996). Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol. Reprod. 55, 703–708.
| Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlKgurw%3D&md5=ac0fcd5858ee19251aff780df5ff1443CAS | 8862790PubMed |
Wallace, W. H., and Kelsey, T. W. (2004). Ovarian reserve and reproductive age may be determined from measurement of ovarian volume by transvaginal sonography. Hum. Reprod. 19, 1612–1617.
| Ovarian reserve and reproductive age may be determined from measurement of ovarian volume by transvaginal sonography.Crossref | GoogleScholarGoogle Scholar | 15205396PubMed |
Wallace, W. H., and Kelsey, T. W. (2010). Human ovarian reserve from conception to the menopause. PLoS ONE 5, e8772.
| Human ovarian reserve from conception to the menopause.Crossref | GoogleScholarGoogle Scholar | 20111701PubMed |
Webb, R., Campbell, B. K., Garverick, H. A., Gong, J. G., Gutierrez, C. G., and Armstrong, D. G. (1999). Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. Suppl. 54, 33–48.
| 1:CAS:528:DyaK1MXnslSisbg%3D&md5=4273160d641f2934cbb6f3d824908c3fCAS | 10692843PubMed |
Weenen, C., Laven, J. S., Von Bergh, A. R., Cranfield, M., Groome, N. P., Visser, J. A., Kramer, P., Fauser, B. C., and Themmen, A. P. (2004). Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 10, 77–83.
| Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1amtw%3D%3D&md5=aafaea150dd3d2afcc4ac8e3116f2708CAS | 14742691PubMed |