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Publication Date: 2009-12-18
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Uribe Velásquez, L. F., Correa Orozco, A., & Osorio, J. H. (2009). Characteristics of ovarian follicle development during estrous cycle in sheep. Biosalud, 8, 117–131. Retrieved from https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/5534
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Abstract
In most domestic animals, the later stages of follicle development appear to have a wavelike pattern during the estrous cycle. A follicle wave is characterized by the synchronous growth of a cohort of follicles, one (or a speciesspecific number) which continues growing (dominant follicle), while the others regress due to development inhibition (subordinate follicles). Follicular function has been widely studied in sheep, although the description of the follicular development pattern has been controversial in early studies. Some authors described follicular growth as continuous and independent of the cycle stage. Other studies were supportive of a wave-like pattern. Currently, there is a general agreement that reconciles both viewpoints, which is based on the high variability in the number of cohorts developing in each wave (the cohort of follicles) and the high variability in the number of cohorts developing in each estrous cycle. In this way, follicles > 5 mm in diameter would exhibit a wave-like pattern, whilst follicles smaller than 4 mm would grow randomly. Most studies describe two to four follicle waves during the estrous cycle, with one study describing up to six waves per cycle. Follicular selection is the process that results in a decrease in the number of growing follicles in a wave according to the species-specific number of follicles that ovulate. During the estrous cycle, the dominant and largest subordinate follicles reach maximum diameters of 5-7 and 3-5 mm, respectively. In many cases the ovulatory follicles develop from a cohort of follicles from the last follicular wave. However, the ovulatory follicles can also derive from the second-to-last follicular wave. Understanding the pattern of follicle development in small ruminants is increasingly important for designing improved methods to manipulate reproduction and production.
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References
Driancourt MA, Gibson WR, Cahill LP. Follicular dynamics throught the oestrus cycle in sheep. A review. Reprod Nutr Develop 1985;25:1-15.
Cunningham NF, Symons AM, Saba N. Levels of progesterone, LH and FSH in the plasma of sheep during the oestrus cycle. J Reprod Fertil 1975;45:177-180.
Pant HC, Hopkinson CRN, Fitzpatrick RJ. Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrus cycle. J Endocrinol 1977;73:247-255.
Bindon BM, Blanc MR, Pelletier J, Terqui M, Thimonier J. Periovulatory gonadotrophin and ovarian steroid patterns in sheep of breeds with differing fecundity. J Reprod Fertil 1979;55:15-25.
Currie WD, Medhamurthy RJ, Cook SJ, Rawlings NC. Seasonal fluctuation in diurnal rhythms of luteinizing hormone secretion in ewes during the mid-luteal phase of the oestrus cycle. J Reprod Fertil 1993;97:71-74.
Schrick FN, Surface RA, Pritchard JY, Dailey RA, Townsend EC, Inskeep EK. Ovarian structures during the estrous cycle and early pregnancy in ewes. Biol Reprod 1993;49:1133-1140.
Ravindra JP, Rawlings NC, Evans ACO, Adams GP. Ultrasonographic study of ovarian follicular dynamics in ewes during the estrous cycle. J Reprod Fert 1994;101:501-509.
Leyva V, Buckrell BC, Walton JS. Regulation of follicular and ovulation in ewes by exogenous progestagen. Theriogenology 1998;50:395-416.
Contreras-Solis I, Diaz T, Lopez G, Caigua A, Lopez-Sebastian, A, Gonzalez-Bulnes A. Systemic and intraovarian effect of corpus luteum on folicular dynamics during estrous cycle in hair breed sheep. Anim Reprod Sci 2008;104:47-55.
González-Reyna A, Valencia MJ, Foote WC, Murphy BD. Hair sheep in México: reproduction in the Pelibuey sheep. Anim Breed Abstr 1991;59:509-524.
Evans ACO, Duffy P, Hynes N, Boland MP. Waves of follicle development during the estrous cycle in sheep. Theriogenology 2000;53:699-715.
Peter AT, Levine H, Drost M, Bergfelt DR. Compilation of classical and contemporary terminology used to describe morphological aspects of ovarian dynamics in cattle. Theriogenology 2009;71:1343-1357.
Fabre S, Pierre A, Mulsant P, Bodin L, Di Pasquale E, Persani L, et al. Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod Biol Endocrinol 2006;4:20.
Scaramuzzi RJ, Adams NR, Baird DT, Campbell BK, Downing JA, Findlay JK, et al. A model for follicle selection and the determination of ovulation rate in the ewe. Reprod Fertil Dev 1993;5:459-478.
Campbell BK, Scaramuzzi RJ, Webb R. Control of antral follicle development and selection in sheep and cattle. J Reprod Fertil 1995;49:335-350.
Mariana JC, Monniaux D, Driancourt MA, Mauléon P. Folliculogenesis. In: Cupps PT. Reproduction in domestic animals. 4 ed. San Diego: Academic Press; 1991. pp.119-171.
Brand A, De Jong WHR. Qualitative and quantitative micromorphological investigations of the tertiary follicle population during the oestrus cycle in sheep. J Reprod Fert 1973;33:431-439.
McNeilly AS, Picton HM, Campbell BK, Baird DT. Gonadotrofic control of follicle growth in the ewe. J Reprod Fert 1991;43:177-186.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008;40:83-88.
Cahill LP, Mauleón P. Influences of season, cycle and breed on follicular growth rates in sheep. J Reprod Fertil 1980;58:321-328.
Cahill LP, Mariana JC, Mauleon P. Total follicular populations in ewes of high and low ovulation rates. J Reprod Fertil 1979;55:27-36.
Picazo RA, López AS. Desarrollo folicular en el ovario de la especie ovina. Invest Agrar: Prod Sanid Anim 1995;10:77-93.
Bartlewski PM, Beard AP, Rawlings N.C. An ultrasound-aided study of temporal relationships between the pattern of LH/FSH secretion, development of ovulatory-sized antral follicles and formation of corpora lutea in ewes. Theriogenology 2000;54:229-245.
Noel B, Bister JL, Pierquin B, Paquay R. Effects of FGA and PMSG on follicular growth and LH secretion in Suffolk ewes. Theriogenology 1994;41:719-727.
Souza CJ, Campbell BK, Baird DT. 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. J Endocrinol 1998;156:563-572.
Barrett DMW, Bartlewski PM, Batista-Arteaga M, Symington A, Rawlings NC. Ultrasound and endocrine evaluation of the ovarian response to a single dose of 500 IU of eCG following a 12-day treatment with progestogen-releasing intravaginal sponges in the breeding and nonbreeding season in ewes. Theriogenology 2004;61:311-327.
Bister JL, Noel B, Perrad B, Mandiki SNM, Mbayahaga SNM, Paquay R. Control of ovarian follicles activity in the ewe. Dom Anim Endoc 1999;17:315-328.
Uribe-Velásquez LF, Oba E, Souza MIL, Vélez-Marín M. Ondas foliculares durante o ciclo estral em ovelhas Bergamácia sob luteólise natural e induzida. En: Mem. Resúmenes 46º Reunión Anual de la Sociedad Brasilera de Zootecnia. Maringá – Paraná (Brasil); 2009. p. 1-3.
Liu X, Dai Q, Hart EJ, Duggavathi R, Barret DMW, Rawlings NC, et al. Ovarian and endocrine responses to prostaglandin F2α (PGF2α) given at the expected time of the endogenous FSH peak at mid-cycle in ewes. Theriogenology 2006;66:811-821.
Ginther OJ, Kot K, Wiltbank MC. Associations between emergence of follicular waves and fluctuations in FSH concentrations during the estrous cycle in ewes. Anim Reprod Sci 1995;43:689-703.
Lucy MC, Savio JD, Badinga L, De La Sota RL, Thatcher WW. Factors that affect ovarian follicular dynamics in cattle. J Anim Sci 1992;70:3615-3626.
Cahill LP, Mauleón P. A study of the population of primordial and small follicles in the sheep. J Reprod Fertil 1981;62:201-206.
Ackland JF, Schwartz NB, Mayo NB, Dodson RE. Nonsteroidal signals originating in the gonads. Physiol Rev 1992;73:731-787.
Dufour J, Cahill LP, Mauleón P. Short- and long-term effects of hypophysectomy and unilateral ovariectomy on ovarian follicular populations in sheep. J Reprod Fertil 1979;57:301-309.
Fortune, J.E. Ovarian follicular growth and development in mammals. Biol Reprod 1994;50:225-232.
Lussier JG, Matton P, Dufour JJ. Growth rates of follicles in the ovary of the cow. J Reprod Fertil 1987;81:301-307.
Quirk SM, Fortune JE. Plasma concentrations of gonadotrophins, preovulatory follicular development and luteal function associated with bovine follicular fluid-induced delay of oestrus in heifers. J Reprod Fertil 1986;76:609-621.
Hyttel P, Callesen H, Greve T, Schmidt M. Oocyte maturation and sperm transport in superovulated cattle. Theriogenology 1991;35:91-108.
Dufour J, Whitmore HL, Ginther OJ, Casida LE. Identification of the ovulatory follicle by its size on different days of the estrous cycle in heifers. J Anim Sci 1972;34:85-87.
Matton P, Adelakoun V, Couture Y, Dufour JJ. Growth and replacement of the bovine ovarian follicles during the estrous cycle. J Anim Sci 1981;52:813-819.
Lahlou-Kassi A, Mariana JC. Ovarian follicular growth during the oestrus cycle in two breeds of ewes of different ovulation rate, the D’Man and the Timahdite. J Reprod Fertil 1984;72:301-310.
Pierson RA, Ginther JO. Follicular populations during the estrous cycle in heifers. I - influence of day. Anim Reprod Sci 1987;14:165-176.
Ginther OJ, Knopf L, Kastelic JP. Temporal associations among events in cattle during oestrus cycle with two or three follicular waves. J Reprod Fertil 1989;87:223-230.
Haresign W, Cooper AC, Khalid M, Hanrahan JP. Patterns of gonadotropin secretion in cyclic Finn ewes selected for low and again high ovulation rate. Anim Sci 1995;61:251-257.
Sirois J, Fortune JE. Lengthening of the bovine estrous cycle with low levels of exogenous progesterone: a model for studying ovarian follicular dominance. Endocrinology 1990;127:916-925.
Fortune JE. Follicular dynamics during the bovine estrous cycle: A limiting factor in improvement of fertility? Anim Reprod Sci 1993;33:111-125.
Badinga L, Thatcher WW, Wilcox CJ, Morris G, Entwistle K, Wolfenson D. Effect of season on follicular dynamics and plasma concentrations of estradiol-17β, progesterone and luteinizing hormone in lactating Holstein cows. Theriogenology 1994;42:1263-1274.
Viñoles C, Banchero G, Rubianes E. Follicular wave pattern and progesterone concentrations in cycling ewes with high and low body condition score. En: Mem. Resúmenes de la Conferencia Annual de la Sociedad Internacional de Transferencia de Embriones. Québec City – Québec (Canadá); 1999. p. 437.
Pierson RA, Ginther JO. Follicular populations during the estrous cycle in heifers. II - Influence of right and left sides and intraovarian effect of the corpus luteum. Anim Reprod Sci 1987;14:177-186.
Scaramuzzi RJ, Downing, JA. The distribution of ovulations from the ovaries of Merino and Border Leicester x Merino ewes and its effect on the survival of their embryos. Anim Reprod Sci 1997;47:327-336.
Dufour J, Ginther OJ, Casida LE. Intraovarian relationship betwen corpora lutea and ovarian follicles in ewes. Am J Vet Res 1972;33:1445-1446.
Dailey RA, Fogwell RL, Thayne WV. Distribution of visible follicles on the ovarian surface in ewes. J Anim Sci 1982;54:1196-1204.
Hutchinson JSM, Robertson HA. The growth of the follicle and corpus luteum in the ovary of the sheep. Res Vet Sci 1966;7:17-24.
Noel B, Bister JL, Paquay R. Ovarian follicular dynamics in Suffolk ewes at differents periods of the year. J Reprod Fert 1993;99:695-700.
Driancourt MA. Follicular dynamics in sheep and cattle. Theriogenology 1991;35:55-68.
Driancourt MA, Webb R, Fry RC. Does follicular dominance occur in ewes? J Reprod Fert 1991;93:63-70.
Kruip, A.M., Brand, A. Follicular growth during the normal cycle and after treatment with progestagens in the ewe. Ann Biol Anim Biochem Biophys 1975;15:191-204.
González-Bulnes A, Moreno JS, García LM, Gomez BA, Lopez SA. Observación del ovario en la oveja y eficacia en la detección de folículos y cuerpos lúteos mediante ecografía transrectal. Invest Agr Prod Sanid Anim 1994;9:319-329.
Rubianes E, Castro T, Carbajal B. Effect of high progesterone levels during the growing phase of the dominant follicle of wave 1 in ultrasonically monitored ewes. Can J Anim Sci 1996b;76:1-13.
Souza CJH, Campbell BK, Baird DT. Follicular dynamics and ovarian steroid in sheep during anoestrus. J Reprod Fertil 1996;108:101-106.
Uribe-Velásquez LF, Oba E, Lara-Herrera LC, Souza MIL, Villa-Velásquez H, Trinca LA, et al. Respostas endócrinas e ovarianas associadas com o folículo dominante da primeira onda folicular em ovelhas sincronizadas com CIDR ou PGF2α. Rev Bras Zootec 2002;31(2):944-953.
Bartlewski PM, Beard AP, Rawlings NC. The relationship between ovarian follicular wave development and transient increases in serum FSH and oestradiol concentration throught the ovine oestrus cycle. En: Annual Conference for the Study of Fertility. Glasgow: Society for the Study of Fertility; 1998. pp. 12-13.
Evans ACO. Characteristics of ovarian follicle development in domestic animals. Reprod Dom Anim 2003; 38:240-246.
Hirshfield AN. Relationship between the supply of primordial follicles and the onset of follicular growth in rats. Biol Reprod 1994;50:421-428.
Adams GP, Matteri RL, Kastelic JP, Ko JCH, Ginther OJ. Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers. J Reprod Fertil 1992;94:77-88.
Cahill LP, Driancourt MA, Chamley WA, Findlay JK. Role of intrafollicular regulators and FSH in growth and development of large antral follicles in sheep. J Reprod Fertil 1985;75:599-607.
Driancourt MA, Gougeon A, Royère D, Thibault C. Ovarian function. In: Thibault C, Levasseur MC, Hunter RHF. Reproduction in mammals and man. Paris: Ellipses; 1993. pp. 283-305.
Gong JG, Campbell BK, Bramley TA, Webb R. Treatment with recombinant bovine somatotrophin enhances ovarian follicle development and increases the secretion of insulin-like growth factor-I by ovarian follicles in ewes. Anim Reprod Sci 1996;41:13-26.
Findlay JK. Peripheral and local regulators of folliculogenese. Reprod Fertil Dev 1996;6:127-139.
Rubianes E, Castro T, Ungerfeld R. Ondas de desarrollo folicular y respuesta ovárica en la oveja. En: Simposio Internacional de Reproducción Animal. Córdoba: Instituto de Reproducción Animal Córdoba (IRAC); 1996. pp. 87-97.
Roche JF, Boland MP. Turnover of dominant follicles in cattle of differents reproductive states. Theriogenology 1991;35:81-90.
Cunningham NF, Symons AM, Saba N. Levels of progesterone, LH and FSH in the plasma of sheep during the oestrus cycle. J Reprod Fertil 1975;45:177-180.
Pant HC, Hopkinson CRN, Fitzpatrick RJ. Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrus cycle. J Endocrinol 1977;73:247-255.
Bindon BM, Blanc MR, Pelletier J, Terqui M, Thimonier J. Periovulatory gonadotrophin and ovarian steroid patterns in sheep of breeds with differing fecundity. J Reprod Fertil 1979;55:15-25.
Currie WD, Medhamurthy RJ, Cook SJ, Rawlings NC. Seasonal fluctuation in diurnal rhythms of luteinizing hormone secretion in ewes during the mid-luteal phase of the oestrus cycle. J Reprod Fertil 1993;97:71-74.
Schrick FN, Surface RA, Pritchard JY, Dailey RA, Townsend EC, Inskeep EK. Ovarian structures during the estrous cycle and early pregnancy in ewes. Biol Reprod 1993;49:1133-1140.
Ravindra JP, Rawlings NC, Evans ACO, Adams GP. Ultrasonographic study of ovarian follicular dynamics in ewes during the estrous cycle. J Reprod Fert 1994;101:501-509.
Leyva V, Buckrell BC, Walton JS. Regulation of follicular and ovulation in ewes by exogenous progestagen. Theriogenology 1998;50:395-416.
Contreras-Solis I, Diaz T, Lopez G, Caigua A, Lopez-Sebastian, A, Gonzalez-Bulnes A. Systemic and intraovarian effect of corpus luteum on folicular dynamics during estrous cycle in hair breed sheep. Anim Reprod Sci 2008;104:47-55.
González-Reyna A, Valencia MJ, Foote WC, Murphy BD. Hair sheep in México: reproduction in the Pelibuey sheep. Anim Breed Abstr 1991;59:509-524.
Evans ACO, Duffy P, Hynes N, Boland MP. Waves of follicle development during the estrous cycle in sheep. Theriogenology 2000;53:699-715.
Peter AT, Levine H, Drost M, Bergfelt DR. Compilation of classical and contemporary terminology used to describe morphological aspects of ovarian dynamics in cattle. Theriogenology 2009;71:1343-1357.
Fabre S, Pierre A, Mulsant P, Bodin L, Di Pasquale E, Persani L, et al. Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod Biol Endocrinol 2006;4:20.
Scaramuzzi RJ, Adams NR, Baird DT, Campbell BK, Downing JA, Findlay JK, et al. A model for follicle selection and the determination of ovulation rate in the ewe. Reprod Fertil Dev 1993;5:459-478.
Campbell BK, Scaramuzzi RJ, Webb R. Control of antral follicle development and selection in sheep and cattle. J Reprod Fertil 1995;49:335-350.
Mariana JC, Monniaux D, Driancourt MA, Mauléon P. Folliculogenesis. In: Cupps PT. Reproduction in domestic animals. 4 ed. San Diego: Academic Press; 1991. pp.119-171.
Brand A, De Jong WHR. Qualitative and quantitative micromorphological investigations of the tertiary follicle population during the oestrus cycle in sheep. J Reprod Fert 1973;33:431-439.
McNeilly AS, Picton HM, Campbell BK, Baird DT. Gonadotrofic control of follicle growth in the ewe. J Reprod Fert 1991;43:177-186.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008;40:83-88.
Cahill LP, Mauleón P. Influences of season, cycle and breed on follicular growth rates in sheep. J Reprod Fertil 1980;58:321-328.
Cahill LP, Mariana JC, Mauleon P. Total follicular populations in ewes of high and low ovulation rates. J Reprod Fertil 1979;55:27-36.
Picazo RA, López AS. Desarrollo folicular en el ovario de la especie ovina. Invest Agrar: Prod Sanid Anim 1995;10:77-93.
Bartlewski PM, Beard AP, Rawlings N.C. An ultrasound-aided study of temporal relationships between the pattern of LH/FSH secretion, development of ovulatory-sized antral follicles and formation of corpora lutea in ewes. Theriogenology 2000;54:229-245.
Noel B, Bister JL, Pierquin B, Paquay R. Effects of FGA and PMSG on follicular growth and LH secretion in Suffolk ewes. Theriogenology 1994;41:719-727.
Souza CJ, Campbell BK, Baird DT. 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. J Endocrinol 1998;156:563-572.
Barrett DMW, Bartlewski PM, Batista-Arteaga M, Symington A, Rawlings NC. Ultrasound and endocrine evaluation of the ovarian response to a single dose of 500 IU of eCG following a 12-day treatment with progestogen-releasing intravaginal sponges in the breeding and nonbreeding season in ewes. Theriogenology 2004;61:311-327.
Bister JL, Noel B, Perrad B, Mandiki SNM, Mbayahaga SNM, Paquay R. Control of ovarian follicles activity in the ewe. Dom Anim Endoc 1999;17:315-328.
Uribe-Velásquez LF, Oba E, Souza MIL, Vélez-Marín M. Ondas foliculares durante o ciclo estral em ovelhas Bergamácia sob luteólise natural e induzida. En: Mem. Resúmenes 46º Reunión Anual de la Sociedad Brasilera de Zootecnia. Maringá – Paraná (Brasil); 2009. p. 1-3.
Liu X, Dai Q, Hart EJ, Duggavathi R, Barret DMW, Rawlings NC, et al. Ovarian and endocrine responses to prostaglandin F2α (PGF2α) given at the expected time of the endogenous FSH peak at mid-cycle in ewes. Theriogenology 2006;66:811-821.
Ginther OJ, Kot K, Wiltbank MC. Associations between emergence of follicular waves and fluctuations in FSH concentrations during the estrous cycle in ewes. Anim Reprod Sci 1995;43:689-703.
Lucy MC, Savio JD, Badinga L, De La Sota RL, Thatcher WW. Factors that affect ovarian follicular dynamics in cattle. J Anim Sci 1992;70:3615-3626.
Cahill LP, Mauleón P. A study of the population of primordial and small follicles in the sheep. J Reprod Fertil 1981;62:201-206.
Ackland JF, Schwartz NB, Mayo NB, Dodson RE. Nonsteroidal signals originating in the gonads. Physiol Rev 1992;73:731-787.
Dufour J, Cahill LP, Mauleón P. Short- and long-term effects of hypophysectomy and unilateral ovariectomy on ovarian follicular populations in sheep. J Reprod Fertil 1979;57:301-309.
Fortune, J.E. Ovarian follicular growth and development in mammals. Biol Reprod 1994;50:225-232.
Lussier JG, Matton P, Dufour JJ. Growth rates of follicles in the ovary of the cow. J Reprod Fertil 1987;81:301-307.
Quirk SM, Fortune JE. Plasma concentrations of gonadotrophins, preovulatory follicular development and luteal function associated with bovine follicular fluid-induced delay of oestrus in heifers. J Reprod Fertil 1986;76:609-621.
Hyttel P, Callesen H, Greve T, Schmidt M. Oocyte maturation and sperm transport in superovulated cattle. Theriogenology 1991;35:91-108.
Dufour J, Whitmore HL, Ginther OJ, Casida LE. Identification of the ovulatory follicle by its size on different days of the estrous cycle in heifers. J Anim Sci 1972;34:85-87.
Matton P, Adelakoun V, Couture Y, Dufour JJ. Growth and replacement of the bovine ovarian follicles during the estrous cycle. J Anim Sci 1981;52:813-819.
Lahlou-Kassi A, Mariana JC. Ovarian follicular growth during the oestrus cycle in two breeds of ewes of different ovulation rate, the D’Man and the Timahdite. J Reprod Fertil 1984;72:301-310.
Pierson RA, Ginther JO. Follicular populations during the estrous cycle in heifers. I - influence of day. Anim Reprod Sci 1987;14:165-176.
Ginther OJ, Knopf L, Kastelic JP. Temporal associations among events in cattle during oestrus cycle with two or three follicular waves. J Reprod Fertil 1989;87:223-230.
Haresign W, Cooper AC, Khalid M, Hanrahan JP. Patterns of gonadotropin secretion in cyclic Finn ewes selected for low and again high ovulation rate. Anim Sci 1995;61:251-257.
Sirois J, Fortune JE. Lengthening of the bovine estrous cycle with low levels of exogenous progesterone: a model for studying ovarian follicular dominance. Endocrinology 1990;127:916-925.
Fortune JE. Follicular dynamics during the bovine estrous cycle: A limiting factor in improvement of fertility? Anim Reprod Sci 1993;33:111-125.
Badinga L, Thatcher WW, Wilcox CJ, Morris G, Entwistle K, Wolfenson D. Effect of season on follicular dynamics and plasma concentrations of estradiol-17β, progesterone and luteinizing hormone in lactating Holstein cows. Theriogenology 1994;42:1263-1274.
Viñoles C, Banchero G, Rubianes E. Follicular wave pattern and progesterone concentrations in cycling ewes with high and low body condition score. En: Mem. Resúmenes de la Conferencia Annual de la Sociedad Internacional de Transferencia de Embriones. Québec City – Québec (Canadá); 1999. p. 437.
Pierson RA, Ginther JO. Follicular populations during the estrous cycle in heifers. II - Influence of right and left sides and intraovarian effect of the corpus luteum. Anim Reprod Sci 1987;14:177-186.
Scaramuzzi RJ, Downing, JA. The distribution of ovulations from the ovaries of Merino and Border Leicester x Merino ewes and its effect on the survival of their embryos. Anim Reprod Sci 1997;47:327-336.
Dufour J, Ginther OJ, Casida LE. Intraovarian relationship betwen corpora lutea and ovarian follicles in ewes. Am J Vet Res 1972;33:1445-1446.
Dailey RA, Fogwell RL, Thayne WV. Distribution of visible follicles on the ovarian surface in ewes. J Anim Sci 1982;54:1196-1204.
Hutchinson JSM, Robertson HA. The growth of the follicle and corpus luteum in the ovary of the sheep. Res Vet Sci 1966;7:17-24.
Noel B, Bister JL, Paquay R. Ovarian follicular dynamics in Suffolk ewes at differents periods of the year. J Reprod Fert 1993;99:695-700.
Driancourt MA. Follicular dynamics in sheep and cattle. Theriogenology 1991;35:55-68.
Driancourt MA, Webb R, Fry RC. Does follicular dominance occur in ewes? J Reprod Fert 1991;93:63-70.
Kruip, A.M., Brand, A. Follicular growth during the normal cycle and after treatment with progestagens in the ewe. Ann Biol Anim Biochem Biophys 1975;15:191-204.
González-Bulnes A, Moreno JS, García LM, Gomez BA, Lopez SA. Observación del ovario en la oveja y eficacia en la detección de folículos y cuerpos lúteos mediante ecografía transrectal. Invest Agr Prod Sanid Anim 1994;9:319-329.
Rubianes E, Castro T, Carbajal B. Effect of high progesterone levels during the growing phase of the dominant follicle of wave 1 in ultrasonically monitored ewes. Can J Anim Sci 1996b;76:1-13.
Souza CJH, Campbell BK, Baird DT. Follicular dynamics and ovarian steroid in sheep during anoestrus. J Reprod Fertil 1996;108:101-106.
Uribe-Velásquez LF, Oba E, Lara-Herrera LC, Souza MIL, Villa-Velásquez H, Trinca LA, et al. Respostas endócrinas e ovarianas associadas com o folículo dominante da primeira onda folicular em ovelhas sincronizadas com CIDR ou PGF2α. Rev Bras Zootec 2002;31(2):944-953.
Bartlewski PM, Beard AP, Rawlings NC. The relationship between ovarian follicular wave development and transient increases in serum FSH and oestradiol concentration throught the ovine oestrus cycle. En: Annual Conference for the Study of Fertility. Glasgow: Society for the Study of Fertility; 1998. pp. 12-13.
Evans ACO. Characteristics of ovarian follicle development in domestic animals. Reprod Dom Anim 2003; 38:240-246.
Hirshfield AN. Relationship between the supply of primordial follicles and the onset of follicular growth in rats. Biol Reprod 1994;50:421-428.
Adams GP, Matteri RL, Kastelic JP, Ko JCH, Ginther OJ. Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers. J Reprod Fertil 1992;94:77-88.
Cahill LP, Driancourt MA, Chamley WA, Findlay JK. Role of intrafollicular regulators and FSH in growth and development of large antral follicles in sheep. J Reprod Fertil 1985;75:599-607.
Driancourt MA, Gougeon A, Royère D, Thibault C. Ovarian function. In: Thibault C, Levasseur MC, Hunter RHF. Reproduction in mammals and man. Paris: Ellipses; 1993. pp. 283-305.
Gong JG, Campbell BK, Bramley TA, Webb R. Treatment with recombinant bovine somatotrophin enhances ovarian follicle development and increases the secretion of insulin-like growth factor-I by ovarian follicles in ewes. Anim Reprod Sci 1996;41:13-26.
Findlay JK. Peripheral and local regulators of folliculogenese. Reprod Fertil Dev 1996;6:127-139.
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