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
Charlène Rico A , Laurence Drouilhet A , Pascal Salvetti B , Rozenn Dalbiès-Tran A , Peggy Jarrier A , Jean-Luc Touzé A , Elodie Pillet B , Claire Ponsart B , Stéphane Fabre A and Danielle Monniaux A C
+ Author Affiliations
- Author Affiliations
A Physiologie de la Reproduction et des Comportements, UMR 085 INRA-UMR 7247 CNRS-Université de Tours-IFCE, Centre INRA de Tours, 37380 Nouzilly, France.
B UNCEIA, Department of Research and Development, 13 rue Jouet, 94704 Maisons-Alfort, France.
C Corresponding author. Email: dmonniaux@tours.inra.fr
Reproduction, Fertility and Development 24(7) 932-944 https://doi.org/10.1071/RD11290
Submitted: 19 November 2011 Accepted: 17 February 2012 Published: 20 March 2012
Abstract
High between-animal variability in the number of embryos produced by multiple ovulation and embryo transfer (MOET) and ovum pick-up and in vitro production (OPU–IVP) methods remains a major limit to the development of embryo biotechnologies in cattle. The measurement of anti-Müllerian hormone (AMH) endocrine concentrations in cows can help to predict their follicular and ovulatory responses to gonadotrophin treatment. The present study aimed to provide practical information for a simple prognostic method based on AMH measurement in Holstein cows. Accurate AMH concentrations could be measured with ELISA in blood or plasma. In cows undergoing repeated OPU protocols over 1 year, the AMH concentrations measured in plasma samples collected before each gonadotrophin treatment were found to be highly repeatable and were tightly correlated with follicular responses. From data obtained at both an experimental station and farm settings, it was possible to propose AMH cut-off values to identify low-responding cows. Gonadotrophin-stimulated cows producing fewer than 15 large follicles at oestrus and fewer than 10 embryos in MOET protocols could be discarded efficiently with plasma AMH concentrations below 87 and 74 pg mL–1, respectively. In conclusion, we propose a prognostic method based on a single AMH measurement to improve the results of embryo biotechnologies.
Additional keywords: assisted reproductive technology, bovine species, FSH, ovulation.
References
Almeida, J., Ball, B. A., Conley, A. J., Place, N. J., Liu, I. K., Scholtz, E. L., Mathewson, L., Stanley, S. D., and Moeller, B. C. (2011). Biological and clinical significance of anti-Müllerian hormone determination in blood serum of the mare. Theriogenology 76, 1393–1403.| Biological and clinical significance of anti-Müllerian hormone determination in blood serum of the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12isbvI&md5=5283a5f5caf8713ad1f4e74ffeba32d8CAS | 21798581PubMed |
Amer, S. A., Li, T. C., and Ledger, W. L. (2009). The value of measuring anti-Müllerian hormone in women with anovulatory polycystic ovary syndrome undergoing laparoscopic ovarian diathermy. Hum. Reprod. 24, 2760–2766.
| The value of measuring anti-Müllerian hormone in women with anovulatory polycystic ovary syndrome undergoing laparoscopic ovarian diathermy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSgsrbK&md5=1ac14d2cec9201aaf6b311c3b37d76d4CAS | 19640893PubMed |
Asada, Y., and Terawaki, Y. (2002). Heritability and repeatability of superovulatory responses in Holstein population in Hokkaido, Japan. Asian-Australas. J. Anim. Sci. 15, 944–948.
Benyei, B., Gaspardy, A., Komlosi, I., and Pecsi, A. (2004). Repeatability and heritability of ovulation number and embryos in dam–daughters pairs in superovulated Holstein–Friesian cows. Reprod. Domest. Anim. 39, 99–102.
| Repeatability and heritability of ovulation number and embryos in dam–daughters pairs in superovulated Holstein–Friesian cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7ntlClsA%3D%3D&md5=2cb9942b91245506ec7aded00d9950a3CAS | 15065991PubMed |
Boni, R., Roelofsen, M. W., Pieterse, M., Kogut, J., and Kruip, T. A. (1997). Follicular dynamics, repeatability and predictability of follicular recruitment in cows undergoing repeated follicular puncture. Theriogenology 48, 277–289.
| Follicular dynamics, repeatability and predictability of follicular recruitment in cows undergoing repeated follicular puncture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVykug%3D%3D&md5=156bf73ade0adcc14da9fd2eb7fe2338CAS | 16728127PubMed |
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=bef337b92bfae91db2ebe980b352b211CAS | 15744026PubMed |
Coyral-Castel, S., Rame, C., Monniaux, D., Freret, S., Fabre-Nys, C., Fritz, S., Monget, P., Dupont, F., and Dupont, J. (2011). Ovarian parameters and fertility of dairy cows selected for one QTL located on BTA3. Theriogenology 75, 1239–1250.
| Ovarian parameters and fertility of dairy cows selected for one QTL located on BTA3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12jtrc%3D&md5=148bacfb51f1034b50bcf679b10fb3baCAS | 21196034PubMed |
De Roover, R., Bols, P. E., Genicot, G., and Hanzen, C. (2005). Characterisation of low, medium and high responders following FSH stimulation prior to ultrasound-guided transvaginal oocyte retrieval in cows. Theriogenology 63, 1902–1913.
| Characterisation of low, medium and high responders following FSH stimulation prior to ultrasound-guided transvaginal oocyte retrieval in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1KjtLc%3D&md5=e0976017ab0eec2e191327cfb4dd039dCAS | 15823347PubMed |
di Clemente, N., Jamin, S. P., Lugovskoy, A., Carmillo, P., Ehrenfels, C., Picard, J.-Y., Whitty, A., Josso, N., Pepinsky, R. B., and Cate, R. L. (2010). Processing of anti-Müllerian hormone regulates receptor activation by a mechanism distinct from TGF-β. Mol. Endocrinol. 24, 2193–2206.
| Processing of anti-Müllerian hormone regulates receptor activation by a mechanism distinct from TGF-β.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFSns7rP&md5=2429c1ef7240c89c064f4c53436fcce8CAS | 20861221PubMed |
Driancourt, M. A. (2001). Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction. Theriogenology 55, 1211–1239.
| Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisr8%3D&md5=a53fbd14759ece292371455f79c64d30CAS | 11327681PubMed |
Eriksson, S., Häggström, M., and Stalhammar, H. (2007). Genetic parameters for superovulatory response in Swedish Red Cattle and Swedish Holstein heifers. In ‘58th Annual Meeting of the European Association for Animal Production, Dublin’. pp. 1–6. (Wageningen Academic Publishers: Wageningen, The Netherlands.)
Fadini, R., Comi, R., Mignini Renzini, M., Coticchio, G., Crippa, M., De Ponti, E., and Dal Canto, M. (2011). Anti-Müllerian hormone as a predictive marker for the selection of women for oocyte in vitro maturation treatment. J. Assist. Reprod. Genet. 28, 501–508.
| Anti-Müllerian hormone as a predictive marker for the selection of women for oocyte in vitro maturation treatment.Crossref | GoogleScholarGoogle Scholar | 21671163PubMed |
Greiner, M., Pfeiffer, D., and Smith, R. D. (2000). Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev. Vet. Med. 45, 23–41.
| Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3msVajsQ%3D%3D&md5=1cef366972d703be9a4ea25561555a5dCAS | 10802332PubMed |
Haddeland, U., Bennick, A., and Brosstad, F. (1994). Fibrinogen present in EDTA–anticoagulated plasma stimulates the tissue-type plasminogen activator-catalysed conversion of plasminogen to plasmin. Blood Coagul. Fibrinolysis 5, 767–772.
| Fibrinogen present in EDTA–anticoagulated plasma stimulates the tissue-type plasminogen activator-catalysed conversion of plasminogen to plasmin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjs1SjsrY%3D&md5=b23ea8c50a3974cd839f2fe6f256beccCAS | 7865683PubMed |
Haddeland, U., Bennick, A., and Brosstad, F. (1995). Stimulating effect on tissue-type plasminogen activator – a new and sensitive indicator of denatured fibrinogen. Thromb. Res. 77, 329–336.
| Stimulating effect on tissue-type plasminogen activator – a new and sensitive indicator of denatured fibrinogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsl2ntb0%3D&md5=fc4144e32fa6571bacfb596d8f53fbfeCAS | 7740524PubMed |
Humblot, P., Le Bourhis, D., Fritz, S., Colleau, J. J., Gonzalez, C., Guyader Joly, C., Malafosse, A., Heyman, Y., Amigues, Y., Tissier, M., and Ponsart, C. (2010). Reproductive technologies and genomic selection in cattle. Vet. Med. Int. 2010, Article ID 192787.
| Reproductive technologies and genomic selection in cattle.Crossref | GoogleScholarGoogle Scholar |
Ireland, J. J., Ward, F., Jimenez-Krassel, F., Ireland, J. L., Smith, G. W., Lonergan, P., and Evans, A. C. (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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1ejtLo%3D&md5=bb7499416ac30736cd50a88684f99b35CAS | 17468258PubMed |
Ireland, J. L. H., Scheetz, D., Jimenez-Krassel, F., Themmen, A. P., Ward, F., Lonergan, P., Smith, G. W., Perez, G. I., Evans, A. C. O., 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=6a1fc32f02dfc46af213239f3cbfdb1bCAS |
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=3b366c459c75bd495398062154f03b90CAS | 21366975PubMed |
Kevenaar, M. E., Meerasahib, M. F., Kramer, P., van de Lang-Born, B. M., de Jong, F. H., Groome, N. P., Themmen, A. P., and Visser, J. A. (2006). Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology 147, 3228–3234.
| Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlOrsr8%3D&md5=f006bb540f23b14f1e2bf7d9820bd6f4CAS | 16556768PubMed |
Lee, R. K., Wu, F. S., Lin, M. H., Lin, S. Y., and Hwu, Y. M. (2011). The predictability of serum anti-Müllerian level in IVF/ICSI outcomes for patients of advanced reproductive age. Reprod. Biol. Endocrinol. 9, 115.
| The predictability of serum anti-Müllerian level in IVF/ICSI outcomes for patients of advanced reproductive age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGktrzO&md5=d265504ce38dc79060229aaa978dfd81CAS | 21843363PubMed |
Li, L., Chen, X., Mo, Y., Chen, Y., Wenig, M., and Yang, D. (2010). Elevated serum anti-Müllerian hormone in adolescent and young adult Chinese patients with polycystic ovary syndrome. Wien. Klin. Wochenschr. 122, 519–524.
| Elevated serum anti-Müllerian hormone in adolescent and young adult Chinese patients with polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WhtL3N&md5=14cb6aff9ddd5a3e19c3265649ea4f19CAS | 20809108PubMed |
Machado, S. A., Reichenbach, H. D., Weppert, M., Wolf, E., and Goncalves, P. B. (2006). The variability of ovum pick-up response and in vitro embryo production from monozygotic twin cows. Theriogenology 65, 573–583.
| The variability of ovum pick-up response and in vitro embryo production from monozygotic twin cows.Crossref | GoogleScholarGoogle Scholar | 16045974PubMed |
Mapletoft, R. J., Steward, K. B., and Adams, G. P. (2002). Recent advances in the superovulation in cattle. Reprod. Nutr. Dev. 42, 601–611.
| Recent advances in the superovulation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1ymtr8%3D&md5=18b09d4c6bb19af7006a027e83de8573CAS | 12625424PubMed |
Merton, J. S., de Roos, A. P., Mullaart, E., de Ruigh, L., Kaal, L., Vos, P. L., and Dieleman, S. J. (2003). Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology 59, 651–674.
| Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38jjslKrtA%3D%3D&md5=fe439915d796f29f45df110700ee3aa1CAS | 12499010PubMed |
Merton, J. S., Ask, B., Onkundi, D. C., Mullaart, E., Colenbrander, B., and Nielen, M. (2009). Genetic parameters for oocyte number and embryo production within a bovine ovum pick-up–in vitro production embryo-production program. Theriogenology 72, 885–893.
| Genetic parameters for oocyte number and embryo production within a bovine ovum pick-up–in vitro production embryo-production program.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnjsVarsg%3D%3D&md5=9174e803ca5ceedc1bc2b3c6d2beb52fCAS | 19716168PubMed |
Monniaux, D., di Clemente, N., Touzé, J. L., Belville, C., Rico, C., Bontoux, M., Picard, J. Y., and Fabre, S. (2008). Intrafollicular steroids and anti-Müllerian hormone during normal and cystic ovarian follicular development in the cow. Biol. Reprod. 79, 387–396.
| Intrafollicular steroids and anti-Müllerian hormone during normal and cystic ovarian follicular development in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWmsb0%3D&md5=0edd0214eff7f93a9313f7718ee99d10CAS | 18448844PubMed |
Monniaux, D., Barbey, S., Rico, C., Fabre, S., Gallard, Y., and Larroque, H. (2010). Anti-Müllerian hormone: a predictive marker of embryo production in cattle? Reprod. Fertil. Dev. 22, 1083–1091.
| Anti-Müllerian hormone: a predictive marker of embryo production in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOgu7vE&md5=9eef3fb4fb5762e27c89c43decf1ddb2CAS | 20797346PubMed |
Monniaux, D., Baril, G., Laine, A. L., Jarrier, P., Poulin, N., Cognie, 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=1a4c44add802715dfa6f37e8c5dfe821CAS | 21930684PubMed |
Nachtigal, M. W., and Ingraham, H. A. (1996). Bioactivation of Müllerian inhibiting substance during gonadal development by a kex2/subtilisin-like endoprotease. Proc. Natl. Acad. Sci. USA 93, 7711–7716.
| Bioactivation of Müllerian inhibiting substance during gonadal development by a kex2/subtilisin-like endoprotease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFSrsbg%3D&md5=c8b66f6b569922bb9dd413e551bb5346CAS | 8755541PubMed |
Pepinsky, R. B., Sinclair, L. K., Chow, E. P., Mattaliano, R. J., Manganaro, T. F., Donahoe, P. K., and Cate, R. L. (1988). Proteolytic processing of Müllerian inhibiting substance produces a transforming growth factor-beta-like fragment. J. Biol. Chem. 263, 18 961–18 964.
| 1:CAS:528:DyaL1MXjsVektQ%3D%3D&md5=7d5b925fe2422aa67007e978339dadbcCAS |
Place, N. J., Hansen, B. S., Cheraskin, J. L., Cudney, S. E., Flanders, J. A., Newmark, A. D., Barry, B., and Scarlett, J. M. (2011). Measurement of serum anti-Müllerian hormone concentration in female dogs and cats before and after ovariohysterectomy. J. Vet. Diagn. Invest. 23, 524–527.
| Measurement of serum anti-Müllerian hormone concentration in female dogs and cats before and after ovariohysterectomy.Crossref | GoogleScholarGoogle Scholar | 21908283PubMed |
Pontes, J. H., Melo Sterza, F. A., Basso, A. C., Ferreira, C. R., Sanches, B. V., Rubin, K. C., and Seneda, M. M. (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.
| Ovum pick-up, in vitro embryo production and pregnancy rates from a large-scale commercial program using Nelore cattle (Bos indicus) donors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MvptVWjuw%3D%3D&md5=7711fa961c6a801c92d3c4b3f09d4721CAS | 21334055PubMed |
Rico, C., Fabre, S., Médigue, C., di Clemente, N., Clément, F., Bontoux, M., Touzé, J.-L., Dupont, M., Briant, E., Rémy, B., Beckers, J.-F., and Monniaux, D. (2009). Anti-Müllerian hormone is an endocrine marker of ovarian gonadotrophin-responsive follicles and can help to predict superovulatory responses in the cow. Biol. Reprod. 80, 50–59.
| Anti-Müllerian hormone is an endocrine marker of ovarian gonadotrophin-responsive follicles and can help to predict superovulatory responses in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFKq&md5=f87fc07dce24a0f92b44bf9d4c1a121aCAS | 18784351PubMed |
Rico, C., Medigue, C., Fabre, S., Jarrier, P., Bontoux, M., Clement, F., and Monniaux, D. (2011). Regulation of anti-Müllerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular and granulosa cell levels. Biol. Reprod. 84, 560–571.
| Regulation of anti-Müllerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular and granulosa cell levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1Omt7c%3D&md5=c7357848b4d257ede866a3375fd3cf36CAS | 21076084PubMed |
Skaar, K. S., Nobrega, R. H., Magaraki, A., Olsen, L. C., Schulz, R. W., and Male, R. (2011). Proteolytically activated, recombinant anti-Müllerian hormone inhibits androgen secretion, proliferation and differentiation of spermatogonia in adult zebrafish testis organ cultures. Endocrinology 152, 3527–3540.
| Proteolytically activated, recombinant anti-Müllerian hormone inhibits androgen secretion, proliferation and differentiation of spermatogonia in adult zebrafish testis organ cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFOht7fM&md5=6593394a161656dd5da762cede3b2186CAS | 21750047PubMed |
Swets, J. A. (1988). Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.
| Measuring the accuracy of diagnostic systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3jsF2jtQ%3D%3D&md5=493d21c2bd2b17320993bcbcdad5647dCAS | 3287615PubMed |
Wilson, C. A., di Clemente, N., Ehrenfels, C., Pepinsky, R. B., Josso, N., Vigier, B., and Cate, R. L. (1993). Müllerian inhibiting substance requires its n-terminal domain for maintenance of biological activity, a novel finding within the transforming growth factor-beta superfamily. Mol. Endocrinol. 7, 247–257.
| Müllerian inhibiting substance requires its n-terminal domain for maintenance of biological activity, a novel finding within the transforming growth factor-beta superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvVelurs%3D&md5=c2670ab420a64d46b9fef5cd95a8e773CAS | 8469238PubMed |
Yeh, J., Kim, B., Peresie, J., Liang, Y. J., and Arroyo, A. (2007). Serum and ovarian Müllerian inhibiting substance, and their decline in reproductive aging. Fertil. Steril. 87, 1227–1230.
| Serum and ovarian Müllerian inhibiting substance, and their decline in reproductive aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslKgtbk%3D&md5=14b3edaed0fd920947ea52913dedb11aCAS | 17222835PubMed |
