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Follicular waves are associated with transient fluctuations in FSH but not oestradiol or inhibin-A concentrations in anoestrous ewes

Published online by Cambridge University Press:  18 August 2016

A.C.O. Evans
Affiliation:
Department of Animal Science and Production, University College Dublin, Dublin 4, Ireland
P. Duffy
Affiliation:
Lyons Research Farm, Conway Institute for Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland
K. M. Quinn
Affiliation:
Department of Animal Science and Production, University College Dublin, Dublin 4, Ireland
P. G. Knight
Affiliation:
School of Animal and Microbial Sciences, University of Reading, Whiteknights, Reading, UK
M. P. Boland
Affiliation:
Department of Animal Science and Production, University College Dublin, Dublin 4, Ireland
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Abstract

The aim was to examine statistically the changes among days in the numbers of follicles relative to the growth of large follicles to test the hypothesis that follicular development occurs in a wave-like fashion in anoestrous ewes. The relationships among the patterns of circulating concentrations of FSH, oestradiol and inhibin-A and the pattern of follicular growth as well as relationships among follicular fluid steroid and inhibin-A concentrations were also studied. The ovaries of 11 ewes were examined daily using transrectal ultrasonography for 14 days and blood samples were collected every 8 h for 9 days. Five ewes were ovariectomized on the last day of ultrasound scanning. One to three identified follicles (a cohort) emerged every 2 to 5 days (mean 2·9 (s.e. 0·2) days) in individual ewes. The numbers of 4 and 5 mm follicles were fewest (P < 0·05) before and greatest (P < 0·05) 1 day after cohort emergence. This change in the numbers of follicles indicates a wave-like pattern of follicular growth. FSH concentrations were greatest (P < 0·05) on the day before wave emergence and lowest (P < 0·05) on the day of wave emergence. Peripheral concentrations of oestradiol and inhibin-A did not fluctuate (P > 0·05) in association with the emergence of follicular waves. The follicles that were collected at ovariectomy originated from one of three different waves. Oestradiol and inhibin-A concentrations in follicular fluid and the oestradiol-to-progesterone ratio were not different among the largest follicles of successive waves, when follicles were collected at the same time, indicating that new waves of follicles developed before the demise of old waves.

In conclusion, waves of follicles emerged about every 3 days in anoestrous ewes (defined as significant changes in numbers of follicles) and were associated with fluctuations in FSH concentrations but not peripheral oestradiol or inhibin-A concentrations. New follicular waves also emerged in the presence of steroidogenically active (positive oestradiol-to-progesterone ratio), inhibin-A producing follicles from a previous wave suggesting that follicles do not exert functional dominance during the non-breeding season.

Type
Reproduction
Copyright
Copyright © British Society of Animal Science 2001

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References

Baird, D. T. and McNeilly, A. S. 1981. Gonadotrophic control of follicular development and function during the oestrous cycle of the ewe. Journal of Reproduction and Fertility, Supplement 30: 119133.Google ScholarPubMed
Baird, D. T. and Scaramuzzi, R. J. 1976. The source of ovarian oestradiol and androstenedione in the sheep during the luteal phase. Acta Endocrinologica 83: 402409.Google ScholarPubMed
Bartlewski, P. M., Beard, A. P., Cook, S. J., Chandolia, R. K., Honaramooz, A. and Rawlings, N. C. 1999a. Ovarian antral follicular dynamics and their relationships with endocrine variables throughout the oestrous cycle in breeds of sheep differing in prolificacy. Journal of Reproduction and Fertility 115: 111124.CrossRefGoogle ScholarPubMed
Bartlewski, P. M., Beard, A. P., Cook, S. J. and Rawlings, N. C. 1998. Ovarian follicular dynamics during anoestrus in ewes. Journal of Reproduction and Fertility 113: 275285.CrossRefGoogle ScholarPubMed
Bartlewski, P. M., Beard, A. P. and Rawlings, N. C. 1999b. Ovarian function in ewes during the transition from breeding season to anoestrus. Animal Reproduction Science 57: 5166.CrossRefGoogle ScholarPubMed
Bartlewski, P. M., Vanderpol, J., Beard, A. P., Cook, S. J. and Rawlings, N. C. 2000. Ovarian antral follicular dynamics and their associations with peripheral concentrations of gonadotropins and ovarian steroids in anoestrous Finnish Landrace ewes. Animal Reproduction Science 58: 273291.CrossRefGoogle ScholarPubMed
Bister, J. L. and Paquay, R. 1983. Fluctuations in the plasma levels of the follicle-stimulating hormone during oestrous cycle, anoestrus, gestation and lactation in the ewe: evidence for an endogenous rhythm of FSH release. Theriogenology 19: 565582.CrossRefGoogle Scholar
Bleach, E. C. L., Glencross, R. G., Feist, S. A., Groome, N. P. and Knight, P. G. 2001. Plasma inhibin A in heifers: relationship with gonadotropins, steriods and follicle dynamics during the estrous cycle and after treatment with bovine follicular fluid. Biology of Reproduction 64: 743752 CrossRefGoogle Scholar
Brand, A. and Jong, W. H. de. 1973. Qualitative and quantitative micromorphological investigations of the tertiary follicle population during the oestrous cycle in sheep. Journal of Reproduction and Fertility 33: 431439.CrossRefGoogle ScholarPubMed
Cahill, L. P. and Mauleon, P. 1980. Influences of season, cycle and breed on follicular growth rates in sheep. Journal of Reproduction and Fertility 58: 321328.CrossRefGoogle ScholarPubMed
Campbell, B. K., Mann, G. E., McNeilly, A. S. and Baird, D. T. 1990. The pattern of ovarian inhibin, estradiol, and androstenedione secretion during the estrous cycle of the ewe. Endocrinology 127: 227235.CrossRefGoogle ScholarPubMed
Campbell, B. K., McNeilly, A. S., Mann, G. E. and Baird, D. T. 1991. The effect of stage of estrous cycle and follicular maturation on ovarian inhibin production in sheep. Biology of Reproduction 44: 483490.CrossRefGoogle ScholarPubMed
Crowe, M. A., Padmanabhan, V., Hynes, N., Sunderland, S. J., Enright, W. J., Beitins, I. Z. and Roche, J. F. 1997. Validation of a sensitive radioimmunoassay to measure serum follicle-stimulating hormone in cattle: correlation with biological activity. Animal Reproduction Science 48: 123136.CrossRefGoogle ScholarPubMed
Evans, A. C. O., Duffy, P., Hynes, N. and Boland, M. P. 2000. Waves of follicle development during the estrous cycle in sheep. Theriogenology 53: 699715.CrossRefGoogle ScholarPubMed
Evans, A. C. O., Komar, C. M., Wandji, S.-A. and Fortune, J. E. 1997. Changes in androgen secretion and luteinizing hormone pulse amplitude are associated with the recruitment and growth of ovarian follicles during the luteal phase of the bovine estrous cycle. Biology of Reproduction 57: 394401.CrossRefGoogle ScholarPubMed
Fortune, J. E. 1994. Ovarian follicular growth and development in mammals. Biology of Reproduction 50: 225232.CrossRefGoogle ScholarPubMed
Ginther, O. J., Kot, K. and Wiltbank, M. C. 1995. Associations between emergence of follicular waves and fluctuations in FSH concentrations during the estrous cycle in ewes. Theriogenology 43: 689703.CrossRefGoogle ScholarPubMed
Ginther, O. J., Wiltbank, M. C., Fricke, P. M., Gibbons, J. R. and Kot, K. 1996. Selection of the dominant follicle in cattle. Biology of Reproduction 55: 11871194.CrossRefGoogle ScholarPubMed
Goodman, A. L. and Hodgen, G. D. 1983. The ovarian triad of the primate menstrual cycle. Recent Progress in Hormone Research 39: 167.Google ScholarPubMed
Karsch, F. J., Dahl, G. E., Evans, N. P., Manning, J. M., Mayfield, K. P., Moenter, S. M. and Foster, D. L. 1993. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biology of Reproduction 49: 13771383.CrossRefGoogle Scholar
Knight, P. G., Feist, S. A., Tannetta, D. S., Bleach, E. C., Fowler, P. A., O’Brien, M. and Groome, N. P. 1998. Measurement of inhibin-A (a bA dimer) during the oestrous cycle, after manipulation of ovarian activity and during pregnancy in ewes. Journal of Reproduction and Fertility 113: 159166.CrossRefGoogle Scholar
Legan, S. J., Karsch, F. J. and Foster, D. L. 1977. The endocrine control of seasonal reproductive function in the ewe: a marked change in response to the negative feedback action of estradiol on luteinizing hormone secretion. Endocrinology 101: 818824.CrossRefGoogle Scholar
Mann, G. E., McNeilly, A. S. and Baird, D. T. 1989. Source of ovarian inhibin secretion during the oestrous cycle of the sheep. Journal of Endocrinology 123: 181188.CrossRefGoogle ScholarPubMed
Martin, G. B., Price, C. A., Thiery, J. C. and Webb, R. 1988. Interactions between inhibin, oestradiol and progesterone in the control of gonadotrophin secretion in the ewe. Journal of Reproduction and Fertility 82: 319328.CrossRefGoogle ScholarPubMed
Noel, B., Bister, J. L. and Paquay, R. 1993. Ovarian follicular dynamics in Suffolk ewes at different periods of the year. Journal of Reproduction and Fertility 99: 695700.CrossRefGoogle ScholarPubMed
Prendiville, D. J., Enright, W. J., Crowe, M. A., Finnerty, M., Hynes, N. and Roche, J. F. 1995. Immunization of heifers against gonadotropin-releasing hormone: antibody titers, ovarian function, body growth, and carcass characteristics. Journal of Animal Science 73: 23822389.CrossRefGoogle ScholarPubMed
Rajakoski, E. 1960. The ovarian follicular system in sexually mature heifers with special reference to seasonally, cyclical, and left-right variations. Acta Endocrinologica 52: (suppl. ) 168.Google Scholar
Roche, J. F., Mihm, M., Diskin, M. G. and Ireland, J. J. 1998. A review of regulation of follicle growth in cattle. Journal of Animal Science 76: (suppl. 3) 1629.CrossRefGoogle Scholar
Scaramuzzi, R. J. and Baird, D. T. 1977. Pulsatile release of luteinizing hormone and the secretion of ovarian steroids in sheep during anestrus. Endocrinology 101: 18011806.CrossRefGoogle ScholarPubMed
Souza, C. J., Campbell, B. K. and Baird, D. T. 1996. Follicular dynamics and ovarian steroid secretion in sheep during anoestrus. Journal of Reproduction and Fertility 108: 101106.CrossRefGoogle ScholarPubMed
Souza, C. J., Campbell, B. K. and Baird, D. T. 1998. Follicular waves and concentrations of steroids and inhibin A in ovarian venous blood during the luteal phase of the oestrous cycle in ewes with an ovarian autotransplant. Journal of Endocrinology 156: 563572.CrossRefGoogle ScholarPubMed
Souza, C. J., Campbell, B. K., Webb, R. and Baird, D. T. 1997. Secretion of inhibin A and follicular dynamics throughout the estrous cycle in the sheep with and without the Booroola gene (Fecb). Endocrinology 138: 53335340.CrossRefGoogle ScholarPubMed
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 oestrous cycle of heifers. Journal of Reproduction and Fertility 101: 547555.CrossRefGoogle ScholarPubMed
Wrathall, J. H., McLeod, B. J., Glencross, R. G., Beard, A. J. and Knight, P. G. 1990. Inhibin immunoneutralization by antibodies raised against synthetic peptide sequences of inhibin a subunit: effects on gonadotrophin concentrations and ovulation rate in sheep. Journal of Endocrinology 124: 167176.CrossRefGoogle Scholar