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

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 | 16054498PubMed | open url image1

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 | 1:STN:280:DC%2BC2MrgsVOlsg%3D%3D&md5=03e17e85aea7eed69cb3b601f4cb51c8CAS | 25628263PubMed | open url image1

Baerwald, A. R. (2009). Human antral folliculogenesis: what we have learned from the bovine and equine models. Anim. Reprod. 6, 20–29. open url image1

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 | 18249401PubMed | open url image1

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 | 22191044PubMed | open url image1

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 | 1:CAS:528:DC%2BC2MXhtFOlsbnI&md5=14495d00f2410e23e67219abfa7e2df7CAS | open url image1

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 | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=3237254d19d2e44981af14219c542570CAS | 17976712PubMed | open url image1

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 | 1:CAS:528:DC%2BC3cXhtFyltLjM&md5=5a2e5b635f09f84cc6d9df49110a2a35CAS | 20699246PubMed | open url image1

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 | 1:STN:280:DC%2BD3M3gslSjsA%3D%3D&md5=c6f76661faf8dcca658a83ef474c5f4eCAS | 11239546PubMed | open url image1

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 | 1:CAS:528:DC%2BC2MXhtFOlsbnF&md5=ee05dbe33193ba4ac94b549834ad7756CAS | open url image1

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 | 1:STN:280:DC%2BC38rmsFCnuw%3D%3D&md5=a9858b6ef74383a0a5fdb5cabae0c64bCAS | 22518166PubMed | open url image1

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 | 24614306PubMed | open url image1

Gastal, E. L. (2009). Recent advances and new concepts on follicle and endocrine dynamics during the equine periovulatory period. Anim. Reprod. 6, 144–158. open url image1

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 | 1:CAS:528:DC%2BC38XivFOmtr0%3D&md5=c90413d073bac3eaf69388f815ca5809CAS | 22115815PubMed | open url image1

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 | 1:CAS:528:DC%2BD2cXnvVGqtLo%3D&md5=e8be729666630a2670cccf59396c38a0CAS | 15189824PubMed | open url image1

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 | 1:CAS:528:DC%2BD2MXhtFWisr3E&md5=a54ac54531261da6d229034d75ec35b8CAS | 16123245PubMed | open url image1

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 | 21299886PubMed | open url image1

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 | 1:CAS:528:DC%2BD38XhtV2gsrc%3D&md5=7c8f148b260a6b9e11be13229b2413caCAS | 11869181PubMed | open url image1

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 | 1:STN:280:DC%2BC3szislKktg%3D%3D&md5=3b25a1bfad4a2793de83a8a14eb7f70eCAS | 23352704PubMed | open url image1

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 | 1:STN:280:DC%2BC3s3ktVOlsQ%3D%3D&md5=75d9284cdb71acc9d9a79a603f6399f1CAS | 23260865PubMed | open url image1

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 | 1:STN:280:DC%2BC3svgs1KjsQ%3D%3D&md5=46a11fd3add2ebd10d08230b6e2b070fCAS | open url image1

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 | 18192670PubMed | open url image1

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 | 1:CAS:528:DC%2BC3sXjtVWjtr8%3D&md5=d974e825e3a01653a5a216badc712857CAS | 23409002PubMed | open url image1

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 | 1:CAS:528:DC%2BD1MXislKisbc%3D&md5=ba815c0bd1aadedee1d68e532af5c6a8CAS | 18954382PubMed | open url image1

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 | 1:CAS:528:DC%2BD2cXhtVSisb7E&md5=0f45651812d667ca1114e2f78dc0414bCAS | 15531477PubMed | open url image1

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 | 1:CAS:528:DC%2BD2MXls1Srtrg%3D&md5=7d311f6d84f808f4ef2730a3b144e327CAS | 15744017PubMed | open url image1

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 | 18638104PubMed | open url image1

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 | 1:CAS:528:DC%2BD2cXkvFOqu78%3D&md5=4d558d79990170bcf8931596982bad38CAS | 15129012PubMed | open url image1

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 | 1:STN:280:DC%2BD2cnisFOitw%3D%3D&md5=332ec6015838cba4336b315311c482fbCAS | 15498779PubMed | open url image1

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 | 1:STN:280:DC%2BD3c7it1ektA%3D%3D&md5=a61ba1081b71e36caca6330a049d9ff2CAS | 10655299PubMed | open url image1

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 | 1:STN:280:DC%2BD28vlt1Sisw%3D%3D&md5=5279d156aaf848727b4d7d186cfb0026CAS | open url image1

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 | 1:STN:280:DC%2BD3s3kvFyrtA%3D%3D&md5=d8a47e99047eb2dfdd7b96a332e78508CAS | 12773440PubMed | open url image1

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 | open url image1

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 | 23635350PubMed | open url image1

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 | 1:CAS:528:DC%2BD2MXitF2js70%3D&md5=e37fa8a32975f95964aa057a9e8ab2c9CAS | 15763114PubMed | open url image1

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 | 15205396PubMed | open url image1



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