Ovarian follicular waves during the menstrual cycle: physiologic insights into novel approaches for ovarian stimulation

Elucidation of multiple waves of antral ovarian follicular development during the menstrual cycle has challenged traditional concepts of female reproductive physiology and foundations of assisted reproductive therapies. Approximately two-thirds of women develop two follicle waves throughout an interovulatory interval and the remainder exhibit three waves of follicle development. Major and minor waves of follicle development have been observed. Major waves are those in which a dominant follicle develops; dominant follicles either regress or ovulate. In minor waves, physiologic selection of a dominant follicle is not manifest. Knowledge of waves of antral follicular development has led to the global adoption of novel ovarian stimulation strategies in which stimulation can be initiated at various times throughout the cycle. Random-start and luteal-phase ovarian stimulation regimens have had important clinical applications for women requiring urgent oocyte or embryo cryopreservation for fertility preservation prior to chemotherapy. Ovarian stimulation twice in the same cycle, referred to as double stimulation, may be used to optimize clinical outcomes in women with a poor ovarian response to stimulation as well as in those requiring fertility preservation before chemotherapy. Elucidation of multiple waves of antral ovarian follicular development during the menstrual cycle has challenged traditional concepts of female reproductive physiology and foundations of assisted reproductive therapies. Approximately two-thirds of women develop two follicle waves throughout an interovulatory interval and the remainder exhibit three waves of follicle development. Major and minor waves of follicle development have been observed. Major waves are those in which a dominant follicle develops; dominant follicles either regress or ovulate. In minor waves, physiologic selection of a dominant follicle is not manifest. Knowledge of waves of antral follicular development has led to the global adoption of novel ovarian stimulation strategies in which stimulation can be initiated at various times throughout the cycle. Random-start and luteal-phase ovarian stimulation regimens have had important clinical applications for women requiring urgent oocyte or embryo cryopreservation for fertility preservation prior to chemotherapy. Ovarian stimulation twice in the same cycle, referred to as double stimulation, may be used to optimize clinical outcomes in women with a poor ovarian response to stimulation as well as in those requiring fertility preservation before chemotherapy. Discuss: You can discuss this article with its authors and other readers at https://www.fertstertdialog.com/posts/30540 Discuss: You can discuss this article with its authors and other readers at https://www.fertstertdialog.com/posts/30540 The human ovary is a dynamic endocrine organ that undergoes profound changes in both structure and function throughout the menstrual cycle. The growth and regression of follicles and resultant development of luteal glands within the ovary are responsible for cyclic hormonal changes. Early studies in the 1950s-1970s to characterize antral follicular development during the menstrual cycle were based on histologic characterizations of ovarian structure (postmortem or after oophorectomy) or endocrinologic markers of ovarian function over time (1Baird D. Fraser I. Blood production and ovarian secretion rates of estradiol and estrone in women throughout the menstrual cycle.J Clin Endocrinol Metab. 1974; 38: 1009-1017Crossref PubMed Google Scholar, 2Baird D. Fraser I.S. Concentration of oestrone and oestradiol in follicular fluid and ovarian venous blood of women.Clin Endocrinol. 1975; 4: 259-266Crossref PubMed Google Scholar, 3Bjersing L. On the morphology and endocrine function of granulosa cells of ovarian follicles and corpora lutea.Acta Endocrinol. 1967; 125: 5Crossref Google Scholar, 4Block E. Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle.Acta Endocrinol. 1951; 8: 33-54Crossref PubMed Google Scholar, 5Block E. Quantitative morphological investigations of the follicular system in women: variations at different ages.Acta Anat. 1952; 14: 108-123Crossref PubMed Google Scholar, 6Gougeon A. 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The production of progesterone, androgens, and estrogens by granulosa cells, thecal tissue, and stromal tissue from human ovaries in vitro.J Clin Endocrinol Metab. 1979; 49: 687-699Crossref PubMed Google Scholar, 11McNatty K.P. Smith D.M. Makris A. Osathanondh R. Ryan K.J. The microenvironment of the human antral follicle: interrelationships among the steroid levels in antral fluid, the population of granulosa cells, and the status of the oocyte in vivo and in vitro.J Clin Endocrinol Metab. 1979; 49: 851-860Crossref PubMed Google Scholar, 12Mikhail G. Hormone secretion by the human ovaries.Gynecologic investigation. 1970; 1: 5-20Crossref PubMed Google Scholar, 13Ross G.T. Gonadtropins and preantral follicular matruation in women.Fertil Steril. 1974; 25: 522-543Abstract Full Text PDF PubMed Google Scholar, 14Ross G.T. Cargille C.M. Lipsett M.B. Rayford P.L. Marshall J.R. Strott C.A. et al.Pituitary and gonadal hormones in women during spontaneous and induced ovulatory cycles.Recent Progr Hormone Res. 1970; 26: 1-62PubMed Google Scholar, 15Sherman B.M. Korenman S.G. Hormonal characteristics of the human menstrual cycle throughout reproductive life.J Clin Invest. 1975; 55: 699-706Crossref PubMed Google Scholar). From those initial studies, it became generally accepted that antral follicles grow within the first 2 weeks of the average 28 day menstrual cycle, termed the “follicular phase,” while the corpus luteum grows in the absence of follicles during the last 2 weeks of the cycle, the “luteal phase” (16Taylor H. Pal L. Sell E. Regulation of the menstrual cycle.in: Taylor H. Pal L. Sell E. Speroff’s Clinical Gynecologic Endocrinology and Infertility. 9th ed. Lippincott Williams & Wilkins, 2020Google Scholar). Ovulation of a physiologically selected dominant follicle marked the transition between the follicular and luteal phases. In the absence of conception, menses followed the luteal phase and marked the transition to a new follicular phase (16Taylor H. Pal L. Sell E. Regulation of the menstrual cycle.in: Taylor H. Pal L. Sell E. Speroff’s Clinical Gynecologic Endocrinology and Infertility. 9th ed. Lippincott Williams & Wilkins, 2020Google Scholar). Early histologic and endocrinologic studies characterizing the menstrual cycle have been fundamental for understanding female reproductive physiology. However, histology does not allow multiple investigations over time and serial endocrine assays provide only indirect measures of ovarian function. The advent of transvaginal ultrasonography in the late 1980s provided a new tool for evaluating antral follicle development in both humans and animal species (17Pierson R.A. Ginther O.J. Follicular populations during the estrous cycle in heifers I. Influence of day.Anim Reprod Sci. 1987; 14: 165-176Crossref Scopus (0) Google Scholar, 18Queenan J.T. O’Brien G.D. Bains L.M. Simposn J. Collins W.P. Campbell S. Ultrasound scanning of ovaries to detect ovulation in women.Fertil Steril. 1980; 34: 99-105Abstract Full Text PDF PubMed Google Scholar). A model depicting multiple waves of antral follicular development during the human menstrual cycle has emerged with the use of both ultrasonographic and endocrinologic methods. Coincidentally, the most recent documentations of follicular waves in women (19Baerwald A.R. Adams G.P. Pierson R.A. A new model for ovarian follicular development during the human menstrual cycle.Fertil Steril. 2003; 80: 116-122Abstract Full Text Full Text PDF PubMed Scopus (191) Google Scholar, 20Baerwald A.R. Adams G.P. Pierson R.A. Characterization of ovarian follicular wave dynamics in women.Biol Reprod. 2003; 69: 1023-1031Crossref PubMed Scopus (226) Google Scholar) supported early histologic and ultrasonographic studies (4Block E. Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle.Acta Endocrinol. 1951; 8: 33-54Crossref PubMed Google Scholar, 5Block E. Quantitative morphological investigations of the follicular system in women: variations at different ages.Acta Anat. 1952; 14: 108-123Crossref PubMed Google Scholar, 18Queenan J.T. O’Brien G.D. Bains L.M. Simposn J. Collins W.P. Campbell S. Ultrasound scanning of ovaries to detect ovulation in women.Fertil Steril. 1980; 34: 99-105Abstract Full Text PDF PubMed Google Scholar, 21Dervain I. Étude échographique de la croissance du follice ovarian normal et détection de l’ovulation. Université Louis Pasteur, Strasbourg1980Google Scholar, 22Hackeloer B.J. Fleming R. Robinson H.P. Adam A.H. Coutts J.R.T. Correlation of ultrasonic and endocrinologic assessment of human follicular development.Amer J Obstet Gynecol. 1979; 135: 122-128PubMed Google Scholar). Collectively, there is now evidence to validate the idea that multiple waves of antral folliculogenesis occur throughout the human menstrual cycle, similarly to those previously reported in several other mammalian species (23Adams G.P. Singh J. Baerwald A.R. Large animal models for the study of ovarian follicular dynamics in women.Therio. 2012; 78: 1733-1748Crossref PubMed Scopus (0) Google Scholar, 24Ginther O.J. Gastal E.L. Gastal M.O. Bergfelt D.R. Baerwald A.R. Pierson R.A. Comparative study of the dynamics of follicular waves in mares and women.Biol Reprod. 2004; 71: 1195-1201Crossref PubMed Scopus (103) Google Scholar). The concept of follicular waves has challenged traditional models of ovarian physiology and led to the optimization of ovarian stimulation protocols for women undergoing assisted reproduction (25Sighinolfi G. Sunkara S.K. la Marca A. New strategies of ovarian stimulation based on the concept of ovarian follicular waves: from conventional to random and double stimulation.Reprod Biomed Online. 2018; 37: 489-497Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar, 26Srikanthan A. Amir E. Bedard P. Giuliani M. Hodgson D. Laframboise S. et al.Fertility preservation in post-pubescent female cancer patients: a practical guideline for clinicians.Mol Clin Oncol. 2018; 8: 153-158PubMed Google Scholar, 27Vaiarelli A. Venturella R. Vizziello D. Bulletti F. Ubaldi F.M. Dual ovarian stimulation and random start in assisted reproductive technologies: from ovarian biology to clinical application.Curr Opinion Obstet Gynecol. 2017; 29: 153-159Crossref PubMed Scopus (0) Google Scholar). The objective of the present minireview is to summarize the different theories of human antral folliculogenesis, novel ovarian stimulation approaches that have recently been developed, clinical applications for these novel protocols, and directions for future research. A literature search was conducted in the United States National Library of Medicine’s PubMed database. The following search terms were used from article title fields: random start stimulation, luteal phase stimulation, duostim, double stimulation, luteal, ovarian stimulation, follicle waves, waves, ovarian, and emergency IVF. Only English-language articles were chosen for review. Original and review articles were included. Collectively, studies over the past 70 years have resulted in the development of three theories of antral follicular development (Fig. 1). Research conducted in animals (rats, sheep) and women led investigators to conclude that antral follicles ≤4–6 mm in size were “recruited” for growth continuously throughout the estrous and menstrual cycle, independently from FSH and LH (8McNatty K.P. Hormonal correlates of follicular development in the human ovary.Australian J Biol Sci. 1981; 34: 249-468Crossref PubMed Scopus (71) Google Scholar, 28Baird D. A model for follicular selection and ovulation: lessons from superovulation.J Steroid Biochem. 1987; 27: 15-23Crossref PubMed Scopus (0) Google Scholar, 29Wiele R.L.V. Bogumil J. Dyrenfurth I. Ferin M. Jewelewicz R. Warren M. et al.Mechanisms regulating the menstrual cycle in women.Recent Prog Horm Res. 1970; 26: 63-103PubMed Google Scholar, 30Baird D.T. Factors regulating the growth of the preovualtory follicle in the sheep and human.J Reprod Fertil. 1983; 69: 343-352Crossref PubMed Google Scholar, 31Green S.H. Zuckerman S. The number of oocytes in the mature rhesus monkey (Macaca mulatta).J Endocrinol. 1951; 7: 194-202Crossref PubMed Google Scholar, 32Mandle A. Zuckerman S. Numbers of normal and atretic oocytes in ulilaterally spayed rats.J Endocrinol. 1950; 7: 194-202Google Scholar, 33Turnbull K.E. Braden A.W. Mattner P.E. The pattern of follicular growth and atresia in the ovine ovary.Aust J Biol Sci. 1977; 30: 229-241Crossref PubMed Scopus (101) Google Scholar, 34Westergaard L. Christensen I.J. McNatty K.P. Steroid levels in ovarian follicular fluid related to follicle size and health status during the normal menstrual cycle in women.Hum Reprod. 1986; 1: 227-232Crossref PubMed Scopus (62) Google Scholar). From the continuous pool of recruited antral follicles, a single dominant follicle developed in the early follicular phase, resulting in ovulation at mid-cycle. The dominant follicle was thought to be selected because it was at an optimal stage of maturity to be able to respond to rising FSH following luteal regression. In contrast to the concept of continuous recruitment of follicles ≤4–6 mm in size, recruitment has been described as a cyclical increase in the number of antral follicles 2–5 mm in size from a continuous supply of smaller follicles, occurring once, in the late luteal phase or early follicular phase of the cycle (35Chikazawa K. Araki S. Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle.J Clin Endocrinol Metab. 1986; 62: 305-313Crossref PubMed Google Scholar, 36Gougeon A. Qualitative changes in medium and large antral follicles in the human ovary during the menstrual cycle.Ann Biol Anim Biochim Biophys. 1979; 19: 1464-1468Crossref Google Scholar, 37O’Herlihy C. Monitoring ovarian follicular development with real-time ultrasound.Br J Obstet Gynaecol. 1980; 87: 613-618Crossref PubMed Google Scholar). Rising FSH, following luteal regression, was thought to be responsible for the recruitment of a cohort of follicles 2–5 mm in size that left the resting pool of primordial follicles around the same time several months previously (38Fauser B. Van Heusden A. Manipulation of human ovarian function: physiological concepts and clinical consequences.Endo Rev. 1997; 18: 71-106Crossref PubMed Scopus (0) Google Scholar). Therefore, antral follicle recruitment was referred to as secondary recruitment, as distinguished from the primary recruitment of preantral follicles from the primordial pool (39McGee E. Hsueh A. Initial and cyclic recruitment of ovarian follicles.Endocr Rev. 2000; 21: 200-214Crossref PubMed Scopus (972) Google Scholar). Secondary recruitment of the antral follicular cohort was thought to result from either stimulation (38Fauser B. 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Follicular development during the luteal phase of the human menstrual cycle.J Clin Endocrinol Metab. 1983; 56: 1022-1031Crossref PubMed Google Scholar, 45Pache T. Wladimiroff J. DeJong F. Hop W. Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle.Fertil Steril. 1990; 54: 638-642Abstract Full Text PDF PubMed Google Scholar, 46van Santbrink E. Hop W. Dessel Tv Jong Fd Fauser B. Decremental follicle-stimulating hormone and dominant follicle development during the normal menstrual cycle.Fertil Steril. 1995; 64: 37-43Abstract Full Text PDF PubMed Google Scholar) by FSH. In women and nonhuman primates, estradiol and inhibin A from the corpus luteum (CL) were thought to suppress FSH and resultant growth of antral follicles >4 mm in size throughout the luteal phase (8McNatty K.P. Hormonal correlates of follicular development in the human ovary.Australian J Biol Sci. 1981; 34: 249-468Crossref PubMed Scopus (71) Google Scholar, 12Mikhail G. Hormone secretion by the human ovaries.Gynecologic investigation. 1970; 1: 5-20Crossref PubMed Google Scholar, 35Chikazawa K. Araki S. Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle.J Clin Endocrinol Metab. 1986; 62: 305-313Crossref PubMed Google Scholar, 44McNatty K.P. Hillier S.G. Boogaard A.M.V.D. Trimbos-Kemper T.C. Reichert L.K. Hall E.V.V. Follicular development during the luteal phase of the human menstrual cycle.J Clin Endocrinol Metab. 1983; 56: 1022-1031Crossref PubMed Google Scholar, 47Baird D.T. Backstrom T. McNeilly A.S. Smith S.K. Wathen A.G. Effect of enucleation of the corpus luteum at different stages of the luteal phase of the human menstrual cycle on subsequent follicular development.J Reprod Fertil. 1984; 70: 615-624Crossref PubMed Google Scholar, 48Basseti S.G. Winters S.J. Keeping H.S. Zeleznik A.J. 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From the single recruited cohort of follicles 2–5 mm in size, a dominant follicle was shown to be selected for preferential growth in the early to middle follicular phase, resulting in ovulation (4Block E. Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle.Acta Endocrinol. 1951; 8: 33-54Crossref PubMed Google Scholar, 35Chikazawa K. Araki S. Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle.J Clin Endocrinol Metab. 1986; 62: 305-313Crossref PubMed Google Scholar, 42Hodgen G. The dominant ovarian follicle.Fertil Steril. 1982; 38: 281-300Abstract Full Text PDF PubMed Google Scholar, 45Pache T. Wladimiroff J. DeJong F. Hop W. Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle.Fertil Steril. 1990; 54: 638-642Abstract Full Text PDF PubMed Google Scholar, 46van Santbrink E. Hop W. Dessel Tv Jong Fd Fauser B. Decremental follicle-stimulating hormone and dominant follicle development during the normal menstrual cycle.Fertil Steril. 1995; 64: 37-43Abstract Full Text PDF PubMed Google Scholar, 58Baird D. The selection of the follicle of the month.in: Evers J. Heineman M. From ovulation to implantation. Proceedings of the VII Reinier de Graaf Symposium. Maastricht. Excerpta Medica, The Netherlands1990Google Scholar, 59Zeleznik A.J. Follicle selection in primates: “many are called but few are chosen”.Biol Reprod. 2001; 65: 655-659Crossref PubMed Google Scholar, 60Zeleznik A.J. The physiology of follicle selection.Reprod Biol Endocrinol. 2004; 2: 31Crossref PubMed Scopus (75) Google Scholar, 61Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results.Hum Reprod. 1986; 1: 81-87Crossref PubMed Scopus (464) Google Scholar). On day 6–9 of the follicular phase, at a mean diameter of 10 mm, the dominant follicle continued to grow while the underlying (i.e., subordinate) follicles regressed (4Block E. Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle.Acta Endocrinol. 1951; 8: 33-54Crossref PubMed Google Scholar, 35Chikazawa K. Araki S. Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle.J Clin Endocrinol Metab. 1986; 62: 305-313Crossref PubMed Google Scholar, 42Hodgen G. The dominant ovarian follicle.Fertil Steril. 1982; 38: 281-300Abstract Full Text PDF PubMed Google Scholar, 45Pache T. Wladimiroff J. DeJong F. Hop W. Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle.Fertil Steril. 1990; 54: 638-642Abstract Full Text PDF PubMed Google Scholar, 46van Santbrink E. Hop W. Dessel Tv Jong Fd Fauser B. Decremental follicle-stimulating hormone and dominant follicle development during the normal menstrual cycle.Fertil Steril. 1995; 64: 37-43Abstract Full Text PDF PubMed Google Scholar, 61Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results.Hum Reprod. 1986; 1: 81-87Crossref PubMed Scopus (464) Google Scholar). From the FSH threshold/window/gate hypothesis, it was proposed that the duration of the rise in FSH above a critical level determines the number of dominant follicles selected from the recruited cohort (28Baird D. A model for follicular selection and ovulation: lessons from superovulation.J Steroid Biochem. 1987; 27: 15-23Crossref PubMed Scopus (0) Google Scholar, 40Brown J.B. Pituitary control of ovarian function: concepts derived from gonadotrophin therapy.Aust N Z J Obstet Gynaecol. 1978; 18: 47-54Crossref Google Scholar, 62Gibbons J.R. Wiltbank M.C. Ginther O.J. Functional interrelationships between follicles greater than 4 mm and the follicle-stimulating hormone surge in heifers.Biol Reprod. 1997; 57: 1066-1073Crossref PubMed Scopus (76) Google Scholar, 63Schipper I. Jong F.H.d. Fuser B.C. Lack of correlation between maximum early follicular phase serum follicle stimulating hormone concentrations and menstrual cycle characteristics in women under the age of 35 years.Hum Reprod. 1998; 13: 1442-1448Crossref PubMed Scopus (92) Google Scholar). Increasing the duration of the rise in FSH above the threshold, as seen with exogenous gonadotropin use during ovarian stimulation, thereby allows multiple follicles to be selected simultaneously (64Schoemaker J. van Weissenbruch M.M. Scheele F. van der Meer M. The FSH threshold concept in clinical ovulation induction.Baillieres Clin Obstet Gynaecol. 1993; 7: 297-308Abstract Full Text PDF PubMed Google Scholar). The introduction of transabdominal ultrasonography in the late 1970s resulted in the ability to monitor follicle growth over time, albeit at suboptimal resolution. No, or nonsignificant, increases in the numbers of antral follicles 2–5 and 2–10 mm throughout the cycle were initially reported (45Pache T. Wladimiroff J. DeJong F. Hop W. Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle.Fertil Steril. 1990; 54: 638-642Abstract Full Text PDF PubMed Google Scholar, 65van Disseldorp J. Lambalk C.B. Kwee J. Looman C.W. Eijkemans M.J. Fauser B.C. et al.Comparison of inter- and intra-cycle variability of anti-müllerian hormone and antral follicle counts.Hum Reprod. 2010; 25: 221-227Crossref PubMed Scopus (231) Google Scholar). The nonsignificant rises in antral follicle count in the early luteal phase were thought to reflect interindividual differences and to be of limited biologic importance (45Pache T. Wladimiroff J. DeJong F. Hop W. Fauser B. Growth patterns of nondominant ovarian follicles during the normal menstrual cycle.Fertil Steril. 1990; 54: 638-642Abstract Full Text PDF PubMed Google Scholar). In contrast to notions of continuous recruitment, or a single episode of cyclic recruitment, cohorts of antral follicles, referred to as waves, have been shown to emerge multiple times during the menstrual cycle. The earliest reports of follicular waves in women were based on histologic evaluation of ovaries (4Block E. Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle.Acta Endocrinol. 1951; 8: 33-54Crossref PubMed Google Scholar). Subsequent studies used transabdominal (18Queenan J.T. O’Brien G.D. Bains L.M. Simposn J. Collins W.P. Campbell S. Ultrasound scanning of ovaries to detect ovulation in women.Fertil Steril. 1980; 34: 99-105Abstract Full Text PDF PubMed Google Scholar, 21Dervain I. Étude échographique de la croissance du follice ovarian normal et détection de l’ovulation. Université Louis Pasteur, Strasbourg1980Google Scholar, 22Hackeloer B.J. Fleming R. Robinson H.P. Adam A.H. Coutts J.R.T. Correlation of ultrasonic and endocrinologic assessment of human follicular development.Amer J Obstet Gynecol. 1979; 135: 122-128PubMed Google Scholar) and transvaginal ultrasonography (19Baerwald A.R. Adams G.P. Pierson R.A. A new model for ovarian follicular development during the human menstrual cycle.Fertil Steril. 2003; 80: 116-122Abstract Full Text Full Text PDF PubMed Scopus (191) Google Scholar, 20Baerwald A.R. Adams G.P. Pierson R.A. Characterization of ovarian follicular wave dynamics in women.Biol Reprod. 2003; 69: 1023-1031Crossref PubMed Scopus (226) Google Scholar) to further support the notion that multiple waves of antral follicles developed throughout the menstrual cycle in healthy women. A follicular wave is defined as the synchronous growth of a group of antral follicles 2–5 mm in size that occurs at regular intervals during the menstrual/estrous cycle; follicles in each wave are similar, but not identical, in diameter (17Pierson R.A. Ginther O.J. Follicular populations during the estrous cycle in heifers I. Influence of day.Anim Reprod Sci. 1987; 14: 165-176Crossref Scopus (0) Google Scholar, 19Baerwald A.R. Adams G.P. Pierson R.A. A new model for ovarian follicular development during the human menstrual cycle.Fertil Steril. 2003; 80: 116-122Abstract Full Text Full Text PDF PubMed Scopus (191) Google Scholar, 24Ginther O.J. Gastal E.L. Gastal M.O. Bergfelt D.R. Baerwald A.R. Pierson R.A. Comparative study of the dynamics of follicular waves in mares and women.Biol Reprod. 2004; 71: 1195-1201Crossref PubMed Scopus (1