Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Preantral follicle density in ovarian biopsy fragments and effects of mare age

K. A. Alves A B , B. G. Alves A , G. D. A. Gastal A , K. T. Haag A , M. O. Gastal A , J. R. Figueiredo C , M. L. Gambarini B and E. L. Gastal A D
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Food and Nutrition, Southern Illinois University, 1205 Lincoln Dr, Carbondale, IL 62901, USA.

B Center for Studies and Research in Animal Reproductive Biology, College of Veterinary and Animal Science, Federal University of Goiás, Campus Samambaia, 74690-900, Goiânia, GO, Brazil.

C Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), State University of Ceará, Campus do Itaperi, 60714-903, Fortaleza, CE, Brazil.

D Corresponding author. Email: egastal@siu.edu

Reproduction, Fertility and Development 29(5) 867-875 https://doi.org/10.1071/RD15402
Submitted: 21 June 2015  Accepted: 14 December 2015   Published: 5 February 2016

Abstract

The aims of the present study were to: (1) evaluate preantral follicle density in ovarian biopsy fragments within and among mares; (2) assess the effects of mare age on the density and quality of preantral follicles; and (3) determine the minimum number of ovarian fragments and histological sections needed to estimate equine follicle density using a mathematical model. The ovarian biopsy pick-up method was used in three groups of mares separated according to age (5–6, 7–10 and 11–16 years). Overall, 336 preantral follicles were recorded with a mean follicle density of 3.7 follicles per cm2. Follicle density differed (P < 0.05) among animals, ovarian fragments from the same animal, histological sections and age groups. More (P < 0.05) normal follicles were observed in the 5–6 years (97%) than the 11–16 years (84%) age group. Monte Carlo simulations showed a higher probability (90%; P < 0.05) of detecting follicle density using two experimental designs with 65 histological sections and three to four ovarian fragments. In summary, equine follicle density differed among animals and within ovarian fragments from the same animal, and follicle density and morphology were negatively affected by aging. Moreover, three to four ovarian fragments with 65 histological sections were required to accurately estimate follicle density in equine ovarian biopsy fragments.

Additional keywords: aging, female, fertility preservation, horse, ovary.


References

Aerts, J. M., Oste, M., and Bols, P. E. (2005). Development and practical applications of a method for repeated transvaginal, ultrasound-guided biopsy collection of the bovine ovary. Theriogenology 64, 947–957.
Development and practical applications of a method for repeated transvaginal, ultrasound-guided biopsy collection of the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 16054498PubMed |

Alves, K. A., Alves, B. G., Rocha, C. D., Visonna, M., Mohallem, R. F., Gastal, M. O., Jacomini, J. O., Beletti, M. E., Figueiredo, J. R., Gambarini, M. L., and Gastal, E. L. (2015). Number and density of equine preantral follicles in different ovarian histological section thicknesses. Theriogenology 83, 1048–1055.
Number and density of equine preantral follicles in different ovarian histological section thicknesses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MrgsVOlsg%3D%3D&md5=03e17e85aea7eed69cb3b601f4cb51c8CAS | 25628263PubMed |

Baerwald, A. R. (2009). Human antral folliculogenesis: what we have learned from the bovine and equine models. Anim. Reprod. 6, 20–29.

Baerwald, A. R., Walker, R. A., and Pierson, R. A. (2009). Growth rates of ovarian follicles during natural menstrual cycles, oral contraception cycles, and ovarian stimulation cycles. Fertil. Steril. 91, 440–449.
Growth rates of ovarian follicles during natural menstrual cycles, oral contraception cycles, and ovarian stimulation cycles.Crossref | GoogleScholarGoogle Scholar | 18249401PubMed |

Campos, J. R., and Rosa, E. S. A. C. (2011). Cryopreservation and fertility: current and prospective possibilities for female cancer patients. ISRN Obstet. Gynecol. 2011, 350813.
Cryopreservation and fertility: current and prospective possibilities for female cancer patients.Crossref | GoogleScholarGoogle Scholar | 22191044PubMed |

Campos-Chillon, F., Farmerie, T. A., Bouma, G. J., Clay, C. M., and Carnevale, E. M. (2015). Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reprod. Fertil. Dev. 27, 925–933.
Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFOlsbnI&md5=14495d00f2410e23e67219abfa7e2df7CAS |

Carnevale, E. M. (2008). The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 69, 23–30.
The mare model for follicular maturation and reproductive aging in the woman.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=3237254d19d2e44981af14219c542570CAS | 17976712PubMed |

Chambers, E. L., Gosden, R. G., Yap, C., and Picton, H. M. (2010). In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility. Hum. Reprod. 25, 2559–2568.
In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFyltLjM&md5=5a2e5b635f09f84cc6d9df49110a2a35CAS | 20699246PubMed |

Cortvrindt, R. G., and Smitz, J. E. (2001). Fluorescent probes allow rapid and precise recording of follicle density and staging in human ovarian cortical biopsy samples. Fertil. Steril. 75, 588–593.
Fluorescent probes allow rapid and precise recording of follicle density and staging in human ovarian cortical biopsy samples.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3gslSjsA%3D%3D&md5=c6f76661faf8dcca658a83ef474c5f4eCAS | 11239546PubMed |

Cox, L., Vanderwall, D. K., Parkinson, K. C., Sweat, A., and Isom, C. (2015). Expression profiles of selected genes in cumulus–oocyte complexes from young and aged mares. Reprod. Fertil. Dev. 27, 914–924.
Expression profiles of selected genes in cumulus–oocyte complexes from young and aged mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFOlsbnF&md5=ee05dbe33193ba4ac94b549834ad7756CAS |

Fabbri, R., Vicenti, R., Macciocca, M., Pasquinelli, G., Lima, M., Parazza, I., Magnani, V., and Venturoli, S. (2012). Cryopreservation of ovarian tissue in pediatric patients. Obstet. Gynecol. Int. 2012, 910698.
Cryopreservation of ovarian tissue in pediatric patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rmsFCnuw%3D%3D&md5=a9858b6ef74383a0a5fdb5cabae0c64bCAS | 22518166PubMed |

Fransolet, M., Labied, S., Henry, L., Masereel, M. C., Rozet, E., Kirschvink, N., Nisolle, M., and Munaut, C. (2014). Strategies for using the sheep ovarian cortex as a model in reproductive medicine. PLoS One 9, e91073.
Strategies for using the sheep ovarian cortex as a model in reproductive medicine.Crossref | GoogleScholarGoogle Scholar | 24614306PubMed |

Gastal, E. L. (2009). Recent advances and new concepts on follicle and endocrine dynamics during the equine periovulatory period. Anim. Reprod. 6, 144–158.

Gastal, E. L. (2011). Ovulation: part 1. Follicle development and endocrinology during the periovulatory period. In ‘Equine Reproduction’. Edn 2, Vol. 2. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala, and D. D. Varner.) pp. 2020–2031. (Wiley-Blackwell: Ames, IA.)

Ginther, O. J. (2012). The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women. Theriogenology 77, 818–828.
The mare: a 1000-pound guinea pig for study of the ovulatory follicular wave in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOmtr0%3D&md5=c90413d073bac3eaf69388f815ca5809CAS | 22115815PubMed |

Ginther, O. J., Gastal, E. L., Gastal, M. O., Bergfelt, D. R., Baerwald, A. R., and Pierson, R. A. (2004). Comparative study of the dynamics of follicular waves in mares and women. Biol. Reprod. 71, 1195–1201.
Comparative study of the dynamics of follicular waves in mares and women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtLo%3D&md5=e8be729666630a2670cccf59396c38a0CAS | 15189824PubMed |

Ginther, O. J., Beg, M. A., Gastal, E. L., Gastal, M. O., Baerwald, A. R., and Pierson, R. A. (2005). Systemic concentrations of hormones during the development of follicular waves in mares and women: a comparative study. Reproduction 130, 379–388.
Systemic concentrations of hormones during the development of follicular waves in mares and women: a comparative study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFWisr3E&md5=a54ac54531261da6d229034d75ec35b8CAS | 16123245PubMed |

Gleicher, N., Weghofer, A., and Barad, D. H. (2011). Defining ovarian reserve to better understand ovarian aging. Reprod. Biol. Endocrinol. 9, 23.
Defining ovarian reserve to better understand ovarian aging.Crossref | GoogleScholarGoogle Scholar | 21299886PubMed |

Gosden, R., and Nagano, M. (2002). Preservation of fertility in nature and ART. Reproduction 123, 3–11.
Preservation of fertility in nature and ART.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtV2gsrc%3D&md5=7c8f148b260a6b9e11be13229b2413caCAS | 11869181PubMed |

Haag, K. T., Magalhaes-Padilha, D. M., Fonseca, G. R., Wischral, A., Gastal, M. O., King, S. S., Jones, K. L., Figueiredo, J. R., and Gastal, E. L. (2013a). Equine preantral follicles obtained via the biopsy pick-up method: histological evaluation and validation of a mechanical isolation technique. Theriogenology 79, 735–743.
Equine preantral follicles obtained via the biopsy pick-up method: histological evaluation and validation of a mechanical isolation technique.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3szislKktg%3D%3D&md5=3b25a1bfad4a2793de83a8a14eb7f70eCAS | 23352704PubMed |

Haag, K. T., Magalhaes-Padilha, D. M., Fonseca, G. R., Wischral, A., Gastal, M. O., King, S. S., Jones, K. L., Figueiredo, J. R., and Gastal, E. L. (2013b). Quantification, morphology, and viability of equine preantral follicles obtained via the biopsy pick-up method. Theriogenology 79, 599–609.
Quantification, morphology, and viability of equine preantral follicles obtained via the biopsy pick-up method.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s3ktVOlsQ%3D%3D&md5=75d9284cdb71acc9d9a79a603f6399f1CAS | 23260865PubMed |

Haag, K, T., Magalhaes-Padilha, D. M., Fonseca, G. R., Wischral, A., Gastal, M. O., King, S. S., Jones, K. L., Figueiredo, J. R., and Gastal, E. L. (2013c). In vitro culture of equine preantral follicles obtained via the biopsy pick-up method. Theriogenology 79, 911–917.
In vitro culture of equine preantral follicles obtained via the biopsy pick-up method.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3svgs1KjsQ%3D%3D&md5=46a11fd3add2ebd10d08230b6e2b070fCAS |

Hansen, K. R., Knowlton, N. S., Thyer, A. C., Charleston, J. S., Soules, M. R., and Klein, N. A. (2008). A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum. Reprod. 23, 699–708.
A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause.Crossref | GoogleScholarGoogle Scholar | 18192670PubMed |

Hummitzsch, K., Irving-Rodgers, H. F., Hatzirodos, N., Bonner, W., Sabatier, L., Reinhardt, D. P., Sado, Y., Ninomiya, Y., Wilhelm, D., and Rodgers, R. J. (2013). A new model of development of the mammalian ovary and follicles. PLoS One 8, e55578.
A new model of development of the mammalian ovary and follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtVWjtr8%3D&md5=d974e825e3a01653a5a216badc712857CAS | 23409002PubMed |

Jacob, J. C., Gastal, E. L., Gastal, M. O., Carvalho, G. R., Beg, M. A., and Ginther, O. J. (2009). Temporal relationships and repeatability of follicle diameters and hormone concentrations within individuals in mares. Reprod. Domest. Anim. 44, 92–99.
Temporal relationships and repeatability of follicle diameters and hormone concentrations within individuals in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislKisbc%3D&md5=ba815c0bd1aadedee1d68e532af5c6a8CAS | 18954382PubMed |

Maciel, G. A., Baracat, E. C., Benda, J. A., Markham, S. M., Hensinger, K., Chang, R. J., and Erickson, G. F. (2004). Stockpiling of transitional and classic primary follicles in ovaries of women with polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 89, 5321–5327.
Stockpiling of transitional and classic primary follicles in ovaries of women with polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSisb7E&md5=0f45651812d667ca1114e2f78dc0414bCAS | 15531477PubMed |

Malhi, P. S., Adams, G. P., and Singh, J. (2005). Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol. Reprod. 73, 45–53.
Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1Srtrg%3D&md5=7d311f6d84f808f4ef2730a3b144e327CAS | 15744017PubMed |

Mihm, M., and Evans, A. C. O. (2008). Mechanisms for dominant follicle selection in monovulatory species: a comparison of morphological, endocrine and intraovarian events in cows, mares and women. Reprod. Domest. Anim. 43, 48–56.
Mechanisms for dominant follicle selection in monovulatory species: a comparison of morphological, endocrine and intraovarian events in cows, mares and women.Crossref | GoogleScholarGoogle Scholar | 18638104PubMed |

Myers, M., Britt, K. L., Wreford, N. G., Ebling, F. J., and Kerr, J. B. (2004). Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127, 569–580.
Methods for quantifying follicular numbers within the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFOqu78%3D&md5=4d558d79990170bcf8931596982bad38CAS | 15129012PubMed |

Nichols, S. M., Bavister, B. D., Brenner, C. A., Didier, P. J., Harrison, R. M., and Kubisch, H. M. (2005). Ovarian senescence in the rhesus monkey (Macaca mulatta). Hum. Reprod. 20, 79–83.
Ovarian senescence in the rhesus monkey (Macaca mulatta).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cnisFOitw%3D%3D&md5=332ec6015838cba4336b315311c482fbCAS | 15498779PubMed |

Qu, J., Godin, P. A., Nisolle, M., and Donnez, J. (2000). Distribution and epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Hum. Reprod. 15, 302–310.
Distribution and epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1ektA%3D%3D&md5=a61ba1081b71e36caca6330a049d9ff2CAS | 10655299PubMed |

Santos, S. S. D., Biondi, F. C., Cordeiro, M. S., Miranda, M. S., Dantas, J. K., Figueiredo, J. R., and Ohashi, O. M. (2006). Isolation, follicular density, and culture of preantral follicles of buffalo fetuses of different ages. Anim. Reprod. Sci. 95, 1–15.
Isolation, follicular density, and culture of preantral follicles of buffalo fetuses of different ages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vlt1Sisw%3D%3D&md5=5279d156aaf848727b4d7d186cfb0026CAS |

Schmidt, K. L., Byskov, A. G., Andersen, N. A., Muller, J., and Andersen, Y. C. (2003). Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Hum. Reprod. 18, 1158–1164.
Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3kvFyrtA%3D%3D&md5=d8a47e99047eb2dfdd7b96a332e78508CAS | 12773440PubMed |

Soleimani, R., Heytens, E., Darzynkiewicz, Z., and Oktay, K. (2011). Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging (Albany NY) 3, 782–793.
| 21869459PubMed |

Telfer, E. E., and Zelinski, M. B. (2013). Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil. Steril. 99, 1523–1533.
Ovarian follicle culture: advances and challenges for human and nonhuman primates.Crossref | GoogleScholarGoogle Scholar | 23635350PubMed |

van den Hurk, R., and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–1751.
Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2js70%3D&md5=e37fa8a32975f95964aa057a9e8ab2c9CAS | 15763114PubMed |

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 |