Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T22:29:10.289Z Has data issue: false hasContentIssue false
  • English
  • Français

Antral follicular count and its relationship with ovarian volume, preantral follicle population and survival, oocyte meiotic progression and ultrastructure of in vitro matured bovine cumulus–oocyte complexes

Published online by Cambridge University Press:  19 August 2020

Gisvani Lopes de Vasconcelos ,
Renata Maculan ,
Ellen Vasconcelos da Cunha ,
Anderson Weiny Barbalho Silva ,
Ana Liza Souza Batista ,
Mariana Aragão Matos Donato ,
Christina Alves Peixoto ,
José Roberto Viana Silva Open the ORCID record for José Roberto Viana Silva [Opens in a new window]  and
José Camisão de Souza
Gisvani Lopes de Vasconcelos
Affiliation:
Animal Science Department, Federal University of Lavras, Lavras, MG, Brazil
Renata Maculan
Affiliation:
Federal Institute South of Minas Gerais, Machado, MG, Brazil
Ellen Vasconcelos da Cunha
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction – LABIREP, Federal University of Ceará, Sobral, CE, Brazil
Anderson Weiny Barbalho Silva
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction – LABIREP, Federal University of Ceará, Sobral, CE, Brazil
Ana Liza Souza Batista
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction – LABIREP, Federal University of Ceará, Sobral, CE, Brazil
Mariana Aragão Matos Donato
Affiliation:
Laboratory of Ultrastructure, CNPqAM/FIOCRUZ, Federal University of Pernambuco, Recife, PE, Brazil
Christina Alves Peixoto
Affiliation:
Laboratory of Ultrastructure, CNPqAM/FIOCRUZ, Federal University of Pernambuco, Recife, PE, Brazil
José Roberto Viana Silva
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction – LABIREP, Federal University of Ceará, Sobral, CE, Brazil
José Camisão de Souza*
Affiliation:
Animal Science Department, Federal University of Lavras, Lavras, MG, Brazil
*
Author for correspondence: JC Souza. Federal University of Lavras, Aquenta Sol, Caixa Postal 3037, CEP 37200-900, Lavras, MG, Brazil. Tel: +55 35 3829.1122/1502. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study aimed to evaluate the relationship between antral follicular count (AFC) and ovarian volume (OV), preantral follicular population and survival, meiotic progression and ultrastructure of cumulus–oocyte complexes (COCs) after in vitro maturation. In experiment 1, the relationship between AFC and preantral follicle population and survival was evaluated by classical histology. In experiment 2, the relationship among AFC, OV, ability of oocytes to resume meiosis and ultrastructure of in vitro matured bovine COCs was studied. A positive correlation (P < 0.05) between AFC and the numbers of healthy primordial, degenerate and total follicles was observed, as well as with healthy secondary follicles and total follicles. The numbers of grades I and II oocytes in ovaries of high AFC class were higher compared with those with intermediate or lower AFC. After in vitro maturation, COCs from ovaries of high AFC had a higher percentage of oocytes in metaphase II compared with those of intermediate and low AFC (P < 0.0001). Ovaries of intermediate AFC had a higher percentage of oocytes in metaphase II compared with ovaries with low AFC (P < 0.0001). The proportion of oocytes in metaphase I, telophase I and anaphase I in COCs from ovaries of intermediate AFC (26.04%) was higher (P < 0.05) compared with that seen in COCs of ovaries with high (8.55%) and low (14.15%) AFC. No differences in the ultrastructure of oocytes were seen. In conclusion, after in vitro maturation, cow ovaries with high AFC have higher numbers of oocytes that reach in metaphase II (MII), but they also have higher numbers of degenerated primordial and primary follicles.

Keywords

CattleIn vitro maturationMorphologyOocyte qualityOvarian follicular reserve
Type
Research Article
Information
Zygote , Volume 28 , Issue 6 , December 2020 , pp. 495 - 503
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amsterdam, A, Hanoch, T, Dantes, A, Tajima, K, Strauss, JF and Seger, R (2002). Mechanisms of gonadotrophin desensitization. Mol Cell Endocrinol 187, 69–74.CrossRefGoogle ScholarPubMed
Bakri, NM, Ibrahim, S F, Osman, NA, Hasan, N, Jaffar, FHF, Rahman, ZA and Osman, K (2016). Embryo apoptosis identification: oocyte grade or cleavage stage? Saudi J Biol Sci 23, S50–5.CrossRefGoogle ScholarPubMed
Bezerra, FTG, Silva, AWB, Rissi, VB, Rosa, PA, Cesaro, MP, Costa, JJN, Gonçalves, PBD and Silva, JRV (2016). Cilostamide and follicular hemisections inhibit oocyte meiosis resumption and regulate gene expression and cAMP levels in bovine cumulus–oocyte complexes. Livest Sci 184, 112–8.CrossRefGoogle Scholar
Burns, DS, Jimenez-Krassel, FJ, Ireland, JLH, Knight, PG and 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, 54–62.CrossRefGoogle Scholar
Chacur, MGM, Valentim, NC, Martinez, AIS, Tostes, RA and Kronka, SN (2006). Morphometry of ovaries of female zebu Bos taurus indicus collected in slaughterhouse. Acta Sci Vet 34, 65–70.CrossRefGoogle Scholar
Chaves, RN, Martins, FS, Saraiva, MV, Celestino, JJH, Lopes, CA, Correia, JC, Verde, IB, Matos, MH, Báo, SN, Name, KP, Campello, CC, Silva, JR and Figueiredo, JR (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod Fertil Dev 20, 640–7.CrossRefGoogle ScholarPubMed
Cushman, RA, de Souza, JC, Hedgpeth, VS and Britt, JH (1999). Superovulatory response of one ovary is related to the micro and macroscopic population of follicles in the contralateral ovary of the cow. Biol Reprod 60, 349–54.CrossRefGoogle ScholarPubMed
Favoreto, MG, Loureiro, B, Ereno, RL, Pupulim, AG, Queiroz, V, Silva, NAS and Barros, CM (2019). Follicle populations and gene expression profiles of Nelore and Angus heifers with low and high ovarian follicle counts. Mol Reprod Dev 86, 197–208.CrossRefGoogle ScholarPubMed
Ireland, JLH, Scheetz, D, Jimenez-Krassel, F, Themmen, APN, Ward, F, Lonergan, P, Smith, GW, Perez, GI, Evans, ACO and Ireland, JJ (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod 79, 1219–25.CrossRefGoogle ScholarPubMed
Ireland, JJ, Smith, GW, Scheetz, D, Jimenez-Krassel, F, Folger, JK, Ireland, JLH, Mossa, F, Lonergan, P and 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.CrossRefGoogle ScholarPubMed
Ireland, JJ, Ward, F, Jimenez-Krassel, F, Ireland, JLH, Smith, GW, Lonergan, P and 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, 1687–95.CrossRefGoogle ScholarPubMed
Ireland, JJ, Zielak-Steciwko, AE, Jimenez-Krassel, F, Folger, J, Bettegowda, A, Scheetz, D, Walsh, S, Mossa, F, Knight, PG, Smith, GW, Lonergan, P and Evans, AC (2009). Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol Reprod 80, 954–64.CrossRefGoogle ScholarPubMed
Jimenez-Krassel, F, Folger, J, Ireland, JLH, Smith, GW, Hou, X, Davis, JS, Lonergan, P, Evans, ACO and 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 reproductive cycles of single-ovulating species. Biol Reprod 80, 1272–81.CrossRefGoogle Scholar
Kwee, J, Elting, ME, Schats, R, McDonnell, J and Lambalk, CB (2007). Ovarian volume and antral follicle count for the prediction of low and hyper responders with In vitro fertilization. Reprod Biol Endoc 15, 5–9.Google Scholar
Lonegro, N, Napoli, N, Pesce, R and Chacón, C (2016). Antral follicle count as a predictor of ovarian response. Rev Argent Radiol 80, 252–7.CrossRefGoogle Scholar
Lowman, BGN, Scott, NA and Somerville, SH (1976). Condition scoring of cattle. Edinburgh: The Edinburgh School of Agriculture, 5 pp. East of Scotland College of Agriculture. Bulletin 6.Google Scholar
Meng, L, Jan, SZ, Hamer, G, van Pelt, AM, van der Stelt, I, Keijer, J and Teerds, KJ (2018). Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostly through apoptosis. Biol Reprod 99, 853–863.Google ScholarPubMed
Mercé, LT, Bau, S, Barco, MJ, Troyano, J, Gay, R, Sotos, F and Villa, A (2006). Assessment of the ovarian volume. Number and volume of follicles and ovarian vascularity by three-dimensional ultrasonography and power Doppler angiography on the HCG day to predict the outcome in IVF/ICSI cycles. Hum Reprod 21, 1218–26.CrossRefGoogle ScholarPubMed
Modina, SC, Tessaro, I, Lodde, V, Franciosi, F, Corbani, D and Luciano, AM (2013). Reductions in the number of mid-sized antral follicles are associated with markers of premature ovarian senescence in dairy cows. Reprod Fertil Dev 2, 235–44.Google Scholar
Monniaux, D, Clément, F, Dalbiès-Tran, R, Estienne, A, Fabre, S, Mansanet, C and Monget, P (2014). The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: What is the link? Biol Reprod 90, 1–11.CrossRefGoogle ScholarPubMed
Morotti, F, Moretti, R, dos Santos, GMG, Silva-Santos, KC, Ramos Cerqueira, PH and Seneda, MM (2018). Ovarian follicular dynamics and conception rate in Bos indicus cows with different antral follicle counts subjected to timed artificial insemination. Ani Reprod Sci 188, 170–7.CrossRefGoogle ScholarPubMed
Mossa, F, Duffy, P, Naitana, S, Lonergan, P and Evans, ACO (2007). Association between numbers of ovarian follicles in the first follicle wave and superovulatory response in ewes. Anim Reprod Sci 100, 391–6.CrossRefGoogle ScholarPubMed
Mossa, F, Walsh, SW, Butler, ST, Berry, DP, Carter, F, Lonergan, P and Evans, AC (2012). Low numbers of ovarian follicles ≥3 mm in diameter are associated with low fertility in dairy cows. J Dairy Sci 95, 2355–61.CrossRefGoogle ScholarPubMed
Nagai, K, Yanagawa, Y, Katagiri, S and Nagano, M (2015). Fertilizability of oocytes derived from Holstein cows having different antral follicle counts in ovaries. Anim Reprod Sci 163, 172–8.CrossRefGoogle ScholarPubMed
Nagai, K, Yanagawa, Y, Katagiri, S and 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. Biomed Res 37, 63–71.CrossRefGoogle Scholar
Penitente-Filho, JM, Jimenez, CR, Zolini, AM, Carrascal, E, Azevedo, JL, Silveira, CO, Oliveira, FA and Torres, CAA (2015). Influence of corpus luteum and ovarian volume on the number and quality of bovine oocytes. Anim Sci J 86, 148–52.CrossRefGoogle ScholarPubMed
Rico, C, Fabre, S, Médigue, C, di Clemente, N, Clément, F, Bontoux, M, Touzé, J, Dupont, M, Briant, E, Rémy, B, Beckers, J and Monniaux, D (2009). Anti-Müllerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod 80, 50–9.CrossRefGoogle ScholarPubMed
Rodrigues, AS, Oliveira, SN, Loiola, MVG, Ferraz, PA, Chalhoub, M, Bittencourt, RF, Araujo, EAB, Santos, TCB, Bittencourt, C and Filho, ALR (2015) Antral follicle count in Nelore females subjected to fixed-time artificial insemination. Cienc Rural 45, 711–7.CrossRefGoogle Scholar
Santos, GMGD, Silva-Santos, KC, Barreiros, TRR, Morotti, F, Sanches, BV, de Moraes, FLZ, Blaschi, W and 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.CrossRefGoogle Scholar
Scheffer, GJ, Broekmans, FJ, Looman, CW, Blankenstein, M, Fauser, B.C, de Jong FH and te Velde ER (2003). The number of antral follicles in normal women with proven fertility is the best reflection of reproductive age. Human Reprod 18, 700–6.CrossRefGoogle ScholarPubMed
Silva-Santos, KC, Santos, GM, Koetz Júnior, C, Morotti, F, Siloto, LS, Marcantonio, TN, Urbano, MR, Oliveira, RL, Lima, DC and Seneda, MM (2014) 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, 228–32.CrossRefGoogle ScholarPubMed
Singh, J, Domínguez, M, Jaiswal, R and Adams, GP (2004). A simple ultrasound test to predict the superstimulatory response in cattle. Theriogenology 62, 227–43.CrossRefGoogle ScholarPubMed
Silva-Santos, KC, Marinho, LSR, Santos, GMG, Machado, FZ, Gonzalez, SM, Lisboa, LA and Seneda, MM (2013). Ovarian follicle reserve: emerging concepts and applications. Anim Reprod 10, 180–6.Google Scholar
Silva, JRV, Ferreira, MAL, Costa, SHF, Santos, RR, Carvalho, FCA, Rodrigues, APR, Lucci, CM, Báo, SN and Figueiredo, JR (2002). Degeneration rate of preantral follicles in the ovaries of goats. Small Rum Res 43, 203–9.CrossRefGoogle Scholar
Silva, JRV, van Den Hurk, R, Costa, SH, Andrade, ER, Nunes, AP, Lobo, RNB and Figueiredo, JR (2004). Survival and growth of goat primordial follicles after in vitro culture of ovarian cortical slices in media containing coconut water. Anim Reprod Sci 81, 273–86.CrossRefGoogle ScholarPubMed
Stringfellow, DA and Givens, MD (2010). Manual of the International Embryo Transfer Society. 4th edn. International Embryo Transfer Society. Champaign. IL.Google Scholar
Swanson, M, Sauerbrei, EE and Cooperberg, PL (1981). Medical implications of ultrasonically detected polycystic ovaries. J Clin Ultrasound 9, 219–22.CrossRefGoogle ScholarPubMed
Tamassia, M, Heyman, Y, Lavergne, Y, Richard, C, Gelin, V, Renard, J and Chastant-Maillard, S (2003). Evidence of oocyte donor cow effect over oocyte production and embryo development in vitro. Reproduction 126, 629–37.CrossRefGoogle ScholarPubMed