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Histological Characteristics and Steroid Concentration of Ovarian Follicles at Different Stages of Development in Pregnant and Non-pregnant Dairy Cows

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Abstract

The aim of the study was to investigate the histological characteristics and steroid concentrations in follicular fluid of different populations of follicles at different stages of development, during pregnancy and the oestrous cycle in cows. Follicles from ovaries collected at a slaughterhouse were allocated into three size categories (small, 2–5.9 mm; medium, 6–13.9 mm; and large, 14–20 mm) in pregnant and non-pregnant cows. Slices were stained with HE and PAS for histological analysis. Follicular fluid was pooled according to size and pregnancy status and estradiol, testosterone and progesterone concentrations in follicular fluid were determined by RIA. Characteristics of healthy follicles did not differ, regardless of follicle size or pregnancy status. Total histological atresia was significantly higher in pregnant cows than in non-pregnant cows (p < 0.05). Estradiol increased and testosterone decreased significantly, while follicles increased in size, in both non-pregnant and pregnant cows (p < 0.05). Nonpregnant cows had the highest estradiol values in follicles of all sizes. Medium and large follicles from pregnant cows showed the lowest testosterone concentration (p < 0.05). Progesterone levels increased with follicle size only in non-pregnant animals. In large follicles, progesterone concentration was significantly higher in non-pregnant cows than in pregnant cows (p < 0.05). Considering steroid concentration and histological findings, most large follicles might be atretic during pregnancy in cattle.

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Abbreviations

CL:

corpus luteum

E2 :

estradiol

FF:

follicular fluid

HE:

haematoxylin–eosin

P4 :

progesterone

RIA:

radioimmunoassay

T:

testosterone

References

  • Ayoub, M.A. and Hunter, A.G., 1993. Inhibitory effect of bovine follicular fluid on in vitro maturation of bovine oocytes. Journal of Dairy Science, 76, 95–100

    PubMed  CAS  Google Scholar 

  • Beg, M.A., Bergfelt, D.R., Kot., K. and Ginther, O.J., 2002. Follicle selection in cattle: Dynamics of follicular fluid factors during development of follicle dominance. Biology of Reproduction, 66, 120–126

    Article  PubMed  CAS  Google Scholar 

  • Bergfelt, D.R., Kastelic, J.P. and Ginther, O.J., 1991. Continued periodic emergence of follicular waves in nonbred progesterone-treated heifers. Animal Reproduction Science, 24, 193–204

    Google Scholar 

  • Bigelow, K.L. and Fortune, J.E., 1998. Characteristics of prolonged dominant versus control follicles: follicles cell numbers, steroidogenic capabilities, and messenger ribonucleic acid for steroidogenic enzymes. Biology of Reproduction, 58, 1241–1249

    Article  PubMed  CAS  Google Scholar 

  • Braw-Tal, R. and Yossefi, S., 1997. Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. Journal of Reproduction and Fertility, 109, 165–171

    PubMed  CAS  Google Scholar 

  • Calder, M.D., Salfen, B.E., Bao, B., Youmgquist, R.S. and Garverick, H.A., 1999. Administration of progesterone to cows with ovarian follicular cysts results in a reduction in mean LH and LH pulse frequency and initiates ovulatory follicular growth. Journal of Animal Science, 77, 3037–3042

    PubMed  CAS  Google Scholar 

  • Campbell, B.K., Scaramuzzi, R.J. and Webb, R., 1995. Control of antral follicle development and selection in sheep and cattle. Journal of Reproduction and Fertility, 49, 335–350

    PubMed  CAS  Google Scholar 

  • Dieleman, S.J., Kruip, T.A., Fortijne, P., de Jong, W.H. and van der Weyden, G.C., 1983. Changes in oestradiol, progesterone and testosterone concentrations in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone. Journal of Endocrinology, 97, 31–42

    Article  PubMed  CAS  Google Scholar 

  • Dominguez, M.M., 1995. Effects of body condition, reproductive status and breed on follicular population and oocyte quality in cows. Theriogenology, 43, 1405–1418

    Google Scholar 

  • Driancourt, M.A. and Thuel, B., 1998. Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. A review. Reproduction, Nutrition, Development, 38, 345–362

    CAS  Google Scholar 

  • Einspanier, R., Schusterh, Y. and Schams, D., 1993. A comparison of hormone levels in follicle-lutein-cysts and in normal bovine ovarian follicles. Theriogenology, 40, 181–188

    Article  CAS  PubMed  Google Scholar 

  • Eppig, J., 2001. Oocyte control of ovarian follicular development and function in mammals. Reproduction, 122, 829–838

    Article  PubMed  CAS  Google Scholar 

  • Fortune, J.E., 1994. Ovarian follicular growth and development in mammals. Biology of Reproduction, 50, 225–232

    Article  PubMed  CAS  Google Scholar 

  • Fortune, J.E. and Hansel, W., 1985. Concentration of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation. Biology of Reproduction, 32, 1069–1079

    Article  PubMed  CAS  Google Scholar 

  • Fortune, J.E., Sirois, J., Turzillo, A.M. and Lavoir, M., 1991. Follicle selection in domestic animals. Journal of Reproduction and Fertility, 43, 187–198

    PubMed  CAS  Google Scholar 

  • Fortune, J.E., Rivera, G.M., Evans A.C. and Turzillo, A.M., 2001. Differentiation of dominant versus subordinate follicles in cattle. Biology of Reproduction, 65, 648–654

    Article  PubMed  CAS  Google Scholar 

  • Fortune, J.E., Rivera, G.M. and Yang, M.Y., 2004. Follicular development: the rol of the follicular microenvironment in selection of the dominant follicle. Animal Reproduction Science, 82–83, 109–126

    PubMed  Google Scholar 

  • Gibbons, J.R., Wiltbank, M.C. and Ginther, O.J., 1999. Relationship between follicular development and the decline in the follicle-stimulating hormone surge in heifers. Biology of Reproduction, 60, 72–77

    Article  PubMed  CAS  Google Scholar 

  • Ginther, O.J., Wiltbank, M.C. Fricke, P.M., Gibbons, J.R. and Kot, K., 1996a. Selection of the dominant follicle in cattle. Biology of Reproduction, 55, 1187–1194

    Article  CAS  Google Scholar 

  • Ginther, O.J., Kot, K., Kulick, L.J., Martin, S.Y. and Wiltbank, M.C., 1996b. Relationships between FSH and ovarian follicular waves during the last six months of pregnancy in cattle. Journal of Reproduction and Fertility, 108, 271–279

    CAS  Google Scholar 

  • Ginther, O.J., Beg, M.A., Bergfelt, D.R., Donadeu, F.X. and Kot, K., 2001. Follicle selection in monovular species. Biology of Reproduction, 65, 638–647

    PubMed  CAS  Google Scholar 

  • Grimes, R.W., Matton. P. and Ireland, J.J., 1987. A comparison of histological and non-histological indexes of atresia and follicular function. Biology of Reproduction, 37, 82–86

    Article  PubMed  CAS  Google Scholar 

  • Guilbault, L.A., Dufour, J.J., Thatcher, W.W., Drost, M. and Haibel, G.K., 1986. Ovarian follicular development during early pregnancy in cattle. Journal of Reproduction and Fertility, 78, 127–135

    PubMed  CAS  Google Scholar 

  • Hazeleger, N.L., Hill, D.J., Stubbings, R.B. and Walton, J.S., 1995. Relationship of morphology and follicular fluid environment of bovine oocytes to their developmental potential in vitro. Theriogenology, 43, 509–522

    PubMed  CAS  Google Scholar 

  • Hendriksen, P.J.M., Vos, P.L.A.M., Steenweg, W.N.M., Bevers, M.M. and Dieleman, S.J., 2000. Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology, 53, 11–20

    Article  PubMed  CAS  Google Scholar 

  • Hirshfield, A.N., 1991. Development of follicles in the mammalian ovary. International Review Cytology, 124, 43–101

    CAS  Google Scholar 

  • Ireland, J.J. and Roche, J.F. 1982. Development of antral follicles in cattle after prostaglandin-induced luteolysis: changes in serum hormones, steroid in follicular fluid, and gonadotropin receptors. Endocrinology, 34, 39–54

    Google Scholar 

  • Jolly, P.D., Tisdall, D.J., Heath, D.A., Lun, S. and McNatty, K.P., 1994. Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3',5'-monophosphate response to follicle stimulating-hormone and luteinizing hormone, and follicular atresia. Biology of Reproduction, 51, 934–944

    Article  PubMed  CAS  Google Scholar 

  • Jolly, P.D., Tisdall, D.J., Detath, G., Heath, D.A., Lun, S., Hudson, N.L. and McNatty, K.P., 1997. Granulosa cell apoptosis, aromatase activity, cyclic adenosine 3',5'-monophospate response to gonadotrophins, and follicular fluid steroid levels during spontaneous and induced follicular atresia in ewes. Biology of Reproduction, 56, 830–836

    PubMed  CAS  Google Scholar 

  • Kruip, T.A. and Dieleman, S.J., 1985. Steroid hormone concentrations in the fluid of bovine follicles relative to size, quality and stage of the oestrus cycle. Theriogenology, 24, 395–401

    Article  CAS  PubMed  Google Scholar 

  • Manikkam, M. and Rajamahendran, R., 1997. Progesterone-induced atresia of the proestrus dominant follicle in the bovine ovary: changes in diameter, the insulin-like growth factors system, aromatase activity, steroid hormones and apoptotic index. Biology of Reproduction, 57, 580–587

    Article  PubMed  CAS  Google Scholar 

  • Manikkam, M., Calder, M.D., Salfen, B.E., Youngquist, R.S., Keisler D.H.A. and Garverick, H., 2001. Concentrations of steroids and expression of messenger RNA for steroidogenic enzymes and gonadotropin receptors in bovine ovarian follicles of first and second waves and changes in second wave follicles after pulsatile LH infusion. Animal Reproduction Science, 67, 189–203

    PubMed  CAS  Google Scholar 

  • McNatty, K.P., Heath, D.A., Henderson, S., Lun, S., Hurst, P.R., Ellis, L.M., Montgomery, G.W., Morrison, L. and Thurley, D.C., 1984. Some aspects of thecal and granulosa cells function during follicular development in the bovine ovary. Journal of Reproduction and Fertility, 72, 39–53

    PubMed  CAS  Google Scholar 

  • Meidan, R., Wolfenson, D., Thatcher, W.W., Gilad, E., Aflalo, L., Greber, Y., Shoshani, E. and Girsh, E., 1993. Oxytocin and estradiol concentrations in follicular fluid as a means for the classification of large bovine follicles. Theriogenology, 39, 421–432

    Article  PubMed  CAS  Google Scholar 

  • Melvin, E.J., Lindsey, B.R., Quintal-Franco, J., Zanella, E., Fike, K.E., Van Tassell, C.P. and Kimder, J.E., 1999. Circulating concentrations of estradiol, luteinizing hormone and follicle-stimulating hormone during waves of ovarian follicular development in prepuberal cattle. Biology of Reproduction, 60, 405– 412

    Article  PubMed  CAS  Google Scholar 

  • Naton, D.P., Burke, C.R., Rhodes, F.M. and McMillan, K.L., 1999. The interovarian distribution of dominant follicles is influenced by the location of the corpus luteum of pregnancy. Animal Reproduction Science, 56, 169–176

    Google Scholar 

  • Pierson, R.A. and Ginther, O.J., 1986. Ovarian follicular populations during early pregnancy in heifers. Theriogenology, 26, 649–659

    Article  PubMed  CAS  Google Scholar 

  • Price, C.A., Carriere, P.D., Bhatia, B. and Groome, N.P., 1995. Comparison of hormonal and histological changes during follicular growth, as measured by ultrasonography, in cattle. Journal of Reproduction and Fertility, 103, 63–68

    PubMed  CAS  Google Scholar 

  • Rajakoski, E., 1960. The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical and left-right variations. Acta Endocrinologica Supplementum, 52, 7–68.

    Google Scholar 

  • Rexroad, C.E. and Casida, L.E., 1975. Ovarian follicular development in cows, sows and ewes in different stages of pregnancy as affected by number of corpora lutea in the same ovary. Journal of Animal Science, 41, 1090–1097

    PubMed  Google Scholar 

  • Roberts, A.J. and Skinner, M.K., 1990a. Hormonal regulation of thecal cell function during antral follicle development in bovine ovaries. Endocrinology, 127, 2907–2917

    CAS  Google Scholar 

  • Roberts, A.J. and Skinner, M.K., 1990b. Estrogen regulation of thecal cell steroidogenesis and differentiation: thecal cell–granulosa interactions. Endocrinology, 127, 2918–2929

    CAS  Google Scholar 

  • Roche, J.F., Crowe, M.A. and Boland, M.P., 1992 Postpartum anoestrus in dairy and beef cows. Animal Reproduction Science, 28, 371–378

    Article  CAS  Google Scholar 

  • Roche, J.F., 1996. Control and regulation of folliculogenesis: a symposium in perspective. Reviews of Reproduction, 1, 19–27

    Google Scholar 

  • Sartori, R., Fricke, P.M., Joao, C.P., Ginther, O.J. and Wiltbank, M.C., 2001. Follicular deviation and acquisition of ovulatory capacity in bovine follicles. Biology of Reproduction, 65, 1403–1409

    Article  PubMed  CAS  Google Scholar 

  • Silván, G., Illera, J.C., Illera, M.J. and Lorenzo, P., 1993. Percentage of atretic and non atretic follicles in different follicular size of heifers and cows. Theriogenology, 39, 311 (Abstract)

    Google Scholar 

  • Sirois, S. and Fortune, J.E., 1988. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biology of Reproduction, 39, 308–317

    Article  PubMed  CAS  Google Scholar 

  • Soboleva, T.K., Peterson, A.J., Pleasants, A.B., McNatty, K.P. and Rhodes, F.M., 2000. A model of follicular development and ovulation in sheep and cattle. Animal Reproduction Science, 58, 45–57

    Article  PubMed  CAS  Google Scholar 

  • Sokal, R. and Rohlf, I., 1981. Biometry. The Principle and Practice of Statistics in Biological, (Freemand, San Francisco)

    Google Scholar 

  • Spicer, L.J., Matton, P., Echternkamp, S.E., Convey, E.M. and Tucker, H.A., 1987. Relationships between histological signs of atresia, steroids in follicular fluid and gonadotropin binding in individual bovine antral follicles during postpartum anovulation. Biology of Reproduction, 36, 890–898

    Article  PubMed  CAS  Google Scholar 

  • Sunderland, S.J., Crowe, M.A., Boland, M.P., Roche, J.F. and Ireland, J.J., 1994. Selection, dominance and atresia of follicles during the oestrus cycle of heifers. Journal Reproduction and Fertility, 101, 547–555

    CAS  Google Scholar 

  • Takagi, M., Tsukihara, T., Nishikata, Y. and Suzuki, T., 1993. Relationship between progesterone and estradiol contents of follicular fluid and the morphological appearance of granulosa cells of follicles coexisting with corpora lutea in bovine ovaries. Theriogenology, 40, 135–147

    Article  CAS  PubMed  Google Scholar 

  • Thatcher, W.W., Driancourt, M.A., Terqui, M. and Badinga, L., 1991. Dynamics of ovarian follicular development in cattle following hysterectomy and during early pregnancy. Domestic Animal Endocrinology, 8, 223–234

    Article  PubMed  CAS  Google Scholar 

  • Thatcher, W.W., De la Sota, R.L., Schmitt, E.J., Díaz, T.C., Badigna, L., Simmen, F.A., Staples, C.R. and Drost, M., 1996. Control and management of ovarian follicles in cattle to optimize fertility. Reproduction, Fertility, Development, 8, 203–207

    CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Animal Reproduction, Faculty of Veterinary Sciences, University of Chile, Casilla 2 Correo 15, Santiago, Chile

    M. De Los Reyes, M. L Villagrán & M. Duchens

  2. Laboratory of Histology, Faculty of Veterinary Sciences, University of Chile, Casilla 2 Correo 15, Santiago, Chile

    R. Cepeda

  3. Laboratory of Endocrinology, Faculty of Veterinary Sciences, University of Chile, Casilla 2 Correo 15, Santiago, Chile

    V. Parraguez & B. Urquieta

Authors
  1. M. De Los Reyes
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  2. M. L Villagrán
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  3. R. Cepeda
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  4. M. Duchens
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  5. V. Parraguez
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  6. B. Urquieta
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Correspondence to M. De Los Reyes.

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Reyes, M.D.L., Villagrán, M.L., Cepeda, R. et al. Histological Characteristics and Steroid Concentration of Ovarian Follicles at Different Stages of Development in Pregnant and Non-pregnant Dairy Cows. Vet Res Commun 30, 161–173 (2006). https://doi.org/10.1007/s11259-006-3100-3

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