The DOI matches its Crossref record; 77 of the 77 references it cites were found in a registry or an index.
Characterization of Ovarian Follicular Wave Dynamics in Women1
Abstract
A wave phenomenon of ovarian follicular development in women has recently been documented in our laboratory. The objective of the present study was to characterize follicular waves to determine whether women exhibit major and minor wave patterns of follicle development during the interovulatory interval (IOI). The ovaries of 50 women with clinically normal menstrual cycles were examined daily using transvaginal ultrasonography for one IOI. Profiles of the diameters of all follicles >or=4 mm and the numbers of follicles >or=5 mm were graphed during the IOI. Major waves were defined as those in which one follicle grew to >or=10 mm and exceeded all other follicles by >or=2 mm. Minor waves were defined as those in which follicles developed to a diameter of <10 mm and follicle dominance was not manifest. Blood samples were drawn to measure serum concentrations of estradiol-17beta, LH, and FSH. Women exhibited major and minor patterns of follicular wave dynamics during the IOI. Of the 50 women evaluated, 29/34 women with two follicle waves (85.3%) exhibited a minor-major wave pattern of follicle development and 5 women (14.7%) exhibited a major-major wave pattern. Ten of the 16 women with three follicle waves (62.5%) exhibited a minor-minor-major wave pattern, 3 women (18.8%) exhibited a minor-major-major wave pattern, and 3 women (18.8%) exhibited a major-major-major wave pattern. Documentation of major and minor follicular waves during the menstrual cycle challenges the traditional theory that a single cohort of antral follicles grows only during the follicular phase of the menstrual cycle.
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“The use of high-resolution transvaginal ultrasonography has underpinned the hypothesis that, similar to ruminants, follicular growth and development in human is characterized by waves (31, 32)”
From Mathematical Modeling and Simulation Provides Evidence for New Strategies of Ovarian Stimulation (2021) · cites this paper as [31]
Citations
Cites
Initial and cyclic recruitment of ovarian follicles
McGee, E. A., & Hsueh, A. J. W. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.2.0394 · Cited by 1,771
Regulation of ovarian follicular development in primates: facts and hypotheses
GOUGEON, A. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-2-121 · Cited by 1,497
Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause
Faddy, M. J., Gosden, R. G., Gougeon, A., Richardson, S. J., & Nelson, J. F. (1992) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137570 · Cited by 1,361
Dynamics of follicular growth in the human: a model from preliminary results
Gougeon, A. (1986) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136365 · Cited by 741
Sirois, J., & Fortune, J. E. (1988) · Biology of Reproduction · doi:10.1095/biolreprod39.2.308 · Cited by 731
Adams, G. P., Matteri, R. L., Kastelic, J. P., Ko, J. C., & Ginther, O. J. (1992) · Reproduction · doi:10.1530/jrf.0.0940177 · Cited by 677
Self-citationSelection of the Dominant Follicle in Cattle1
Ginther, O. J., Wiltbank, M. C., FRICKE, P. M., Gibbons, J. R., & Kot, K. (1996) · Biology of Reproduction · doi:10.1095/biolreprod55.6.1187 · Cited by 647
QUANTITATIVE MORPHOLOGICAL INVESTIGATIONS OF THE FOLLICULAR SYSTEM IN WOMEN
Block, E. (2008) · Acta Anatomica · doi:10.1159/000140595 · Cited by 518
Manipulation of Human Ovarian Function: Physiological Concepts and Clinical Consequences*
Fauser, B. C. J. M., & van Heusden, A. M. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.1.0290 · Cited by 509
Reproductive endocrinology, surgery, and technology
Adashi, E. Y., Rock, J. A., & Rosenwaks, Z. (1996) · Medical Entomology and Zoology · Cited by 504
Gougeon, A., Écochard, R., & Thalabard, J. (1994) · Biology of Reproduction · doi:10.1095/biolreprod50.3.653 · Cited by 456
Hillier, S. G. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138480 · Cited by 456
A new model for ovarian follicular development during the human menstrual cycle
Baerwald, A. R., Adams, G. P., & Pierson, R. A. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00544-2 · Cited by 327
Self-citationCorrelation of ultrasonic and endocrinologic assessment of human follicular development
Hackelöer, B.-J., Fleming, R., Robinson, H. P., Adam, A. H., & Coutts, J. R. T. (1979) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(79)80029-0 · Cited by 325
Adams, G. P., Matteri, R. L., & Ginther, O. J. (1992) · Reproduction · doi:10.1530/jrf.0.0960627 · Cited by 321
Self-citationMorphometric studies of small follicles in ovaries of women at different ages
Gougeon, A., & Chainy, G. B. N. (1987) · Reproduction · doi:10.1530/jrf.0.0810433 · Cited by 305
Knopf, L., Kastelic, J. P., Schallenberger, E., & Ginther, O. J. (1989) · Domestic Animal Endocrinology · doi:10.1016/0739-7240(89)90040-4 · Cited by 299
Wallach, E. E., & Hodgen, G. D. (1982) · Fertility and Sterility · doi:10.1016/s0015-0282(16)46509-x · Cited by 276
Ultrasound Scanning of Ovaries to Detect Ovulation in Women
Queenan, J. T., O'Brien, G. D., Bains, L. M., Simpson, J., Collins, W. P., & Campbell, S. C. (1980) · Fertility and Sterility · doi:10.1016/s0015-0282(16)44889-2 · Cited by 248
Growth patterns of nondominant ovarian follicles during the normal menstrual cycle
Pache, T. D., Wladimiroff, J. W., de Jong, F. H., Hop, W. C. J., & Fauser, B. C. J. M. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53821-7 · Cited by 247
Comparative patterns of follicle development and selection in ruminants
Adams, G. P. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.4.002 · Cited by 245
Self-citationA model for follicular selection and ovulation: Lessons from superovulation
Baird, D. T. (1987) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(87)90289-5 · Cited by 197
Intragonadal Regulation of Follicular Maturation
Tonetta, S. A., & diZerega, G. S. (1989) · Endocrine Reviews · doi:10.1210/edrv-10-2-205 · Cited by 191
van Santbrink, E. J. P., Hop, W. C. J., van Dessel, T. J. H. M., de Jong, F. H., & Fauser, B. C. J. M. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57652-3 · Cited by 189
The Ovarian Triad of the Primate Menstrual Cycle
GOODMAN, A. L., & HODGEN, G. D. (1983) · Proceedings of the 1982 Laurentian Hormone Conference · doi:10.1016/b978-0-12-571139-5.50005-7 · Cited by 178
Follicular Development during the Luteal Phase of the Human Menstrual Cycle
McNatty, K. P., Hillier, S. G., BOOGAARD, A. M. J. V. D., Trimbos-Kemper, T. C. M., REICHERT, L. E., & van Hall, E. V. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-5-1022 · Cited by 165
Follicular populations during the estrous cycle in heifers. I. Influence of day
Pierson, R. A., & Ginther, O. J. (1987) · Animal Reproduction Science · doi:10.1016/0378-4320(87)90080-7 · Cited by 162
Self-citationFollicle Selection in Cattle: Role of Luteinizing Hormone1
Ginther, O. J., Bergfelt, D. R., Beg, M. A., & Kot, K. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.1.197 · Cited by 159
Bovine model for study of ovarian follicular dynamics in humans
Adams, G. P., & Pierson, R. A. (1995) · Theriogenology · doi:10.1016/0093-691x(94)00015-m · Cited by 145
Self-citationKerin, J. F., EDMONDS, D. K., Warnes, G. M., Cox, L. W., Seamark, R. F., Matthews, C. D., Young, G. B., & Baird, D. T. (1981) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1981.tb00947.x · Cited by 139
Ginther, O. J., Bergfelt, D. R., Kulick, L. J., & Kot, K. (2000) · Biology of Reproduction · doi:10.1095/biolreprod62.4.920 · Cited by 135
Transvaginal three-dimensional ultrasound: accuracy of follicular volume measurements
Kyei-Mensah, A., Zaidi, J., Pittrof, R., Shaker, A. G., Campbell, S. C., & Tan, S. L. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58102-3 · Cited by 130
Gougeon, A., & Lefèvre, B. (1983) · Reproduction · doi:10.1530/jrf.0.0690497 · Cited by 117
Ultrasonographical and hormonal description of the normal ovulatory menstrual cycle
Bakos, O., Lundkvist, Ö., Wide, L., & Bergh, T. (1994) · Acta Obstetricia et Gynecologica Scandinavica · doi:10.3109/00016349409072507 · Cited by 113
Collins, W., Jurkovic, D., Bourne, T., Kurjak, A., & Campbell, S. C. (1991) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137332 · Cited by 111
Baird, D. T., Baker, T. G., McNatty, K. P., & Neal, P. (1975) · Reproduction · doi:10.1530/jrf.0.0450611 · Cited by 107
Hormonal Correlates of Follicular Development in the Human Ovary
McNatty, K. P. (1981) · Australian Journal of Biological Sciences · doi:10.1071/bi9810249 · Cited by 106
Preovulatory Changes of Blood Flow in Different Regions of the Human Follicle
Brännström, M., Zackrisson, U., Hagström, H.-G., Josefsson, B., Hellberg, P., Granberg, S., Collins, W. P., & Bourne, T. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00544-x · Cited by 106
Follicle Selection in Primates: “Many Are Called but Few Are Chosen”1
Zeleznik, A. J. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.3.655 · Cited by 105
Mean versus individual hormonal profiles in the menstrual cycle
Alliende, M. E. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03167-9 · Cited by 101
Major and Minor Follicular waves During the Equine Estrous Cycle
Ginther, O. J. (1993) · Journal of Equine Veterinary Science · doi:10.1016/s0737-0806(07)80012-8 · Cited by 100
Concentration of oestrone and oestradiol in follicular fluid and ovarian venous blood of women
BAIRD, D. T., & FRASER, I. S. (1975) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1975.tb01533.x · Cited by 99
Echographic Study of Follicular Maturation and Ovulation During the Normal Menstrual Cycle
Renaud, R. L., Macler, J., Dervain, I., Ehret, M.-C., Aron, C., Plas-Roser, S., Spira, A., & Pollack, H. J. (1980) · Fertility and Sterility · doi:10.1016/s0015-0282(16)44592-9 · Cited by 96
Chikazawa, K., Araki, S., & Tamada, T. (1986) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-62-2-305 · Cited by 95
Follicle Deviation and Intrafollicular and Systemic Estradiol Concentrations in Mares1
Gastal, E. L., Gastal, M. O., Wiltbank, M. C., & Ginther, O. J. (1999) · Biology of Reproduction · doi:10.1095/biolreprod61.1.31 · Cited by 94
Gastal, E. L., Bergfelt, D. R., Nogueira, G. D. P., Gastal, M. O., & Ginther, O. J. (1999) · Biology of Reproduction · doi:10.1095/biolreprod61.6.1492 · Cited by 89
Ultrastructure of the Resting Ovarian Follicle Pool in Healthy Young Women1
de Bruin, J. P., Dorland, M., Spek, E. R., Posthuma, G., van Haaften, M., Looman, C. W. N., & Velde, E. R. T. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.4.1151 · Cited by 87
Pierson, R. A., & Ginther, O. J. (1988) · Animal Reproduction Science · doi:10.1016/0378-4320(88)90029-2 · Cited by 80
Self-citationvan Dessel, H. J. H. M., Schipper, I., Pache, T. D., van Geldorp, H. J., de Jong, F. H., & Fauser, B. C. J. M. (1996) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1996.662483.x · Cited by 71
Side of ovulation and cycle characteristics in normally fertile women
Écochard, R. (2000) · Human Reproduction · doi:10.1093/humrep/15.4.752 · Cited by 69
Germinal vesicle breakdown in oocytes of human atretic follicles during the menstrual cycle
Gougeon, A., & Testart, J. (1986) · Reproduction · doi:10.1530/jrf.0.0780389 · Cited by 69
Sonographic Morphology of the Normal Menstrual Cycle
Hall, D. A., Hann, L. E., Ferrucci, J. T., Black, E. B., Braitman, B. S., Crowley, W. F., Nikrui, N., & Kelley, J. A. (1979) · Radiology · doi:10.1148/133.1.185 · Cited by 58
Experimental Assumption of Dominance by a Smaller Follicle and Associated Hormonal Changes in Mares1
Gastal, E. L., Gastal, M. O., & Ginther, O. J. (1999) · Biology of Reproduction · doi:10.1095/biolreprod61.3.724 · Cited by 55
Lenz, S. (1985) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348509154681 · Cited by 50
Characteristics of follicular evacuation during human ovulation
Hanna, M. D., Chizen, D. R., & Pierson, R. A. (1994) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.1994.04060488.x · Cited by 48
Self-citationMany Are Called, But Few Are Chosen.
Mattfield, J. A. (1972) · Cited by 47
The regulation of follicle growth: some clinical implications in reproductive endocrinology
Wallach, E. E., & Taymor, M. L. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58077-7 · Cited by 46
Sonographic evaluation of normal and induced ovulation.
Ritchie, W. G. M. (1986) · Radiology · doi:10.1148/radiology.161.1.3532176 · Cited by 46
Baird, D. T., Bäckström, T., McNeilly, A. S., Smith, S. K., & Wathen, C. G. (1984) · Reproduction · doi:10.1530/jrf.0.0700615 · Cited by 44
CURRENT STATUS OF ESTROGEN ASSAY IN GYNECOLOGY AND OBSTETRICS
Brown, J. B., & Beischer, N. A. (1972) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-197204000-00001 · Cited by 42
Ipsilateral Versus Contralateral Ovary Selection of Dominant Follicle in Succeeding Cycle
CHECK, J. H., Dietterich, C., & HOUCK, M. A. (1991) · Obstetrics and Gynecology · doi:10.1097/00006250-199102000-00016 · Cited by 40
Ovary and ovulation: Prediction of ovarian cycle outcome by follicular characteristics, stage 1
Gore, M. A., Nayudu, P. L., Vlaisavljević, V., & Thomas, N. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136292 · Cited by 38
Gougeon, A. (1979) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19790907 · Cited by 37
Ovarian follicular dynamics: from basic science to clinical practice
Pellicer, A., Gaitán, P., Neuspiller, F., Ardiles, G., Albert, C., Remohi, J. A., & Simón, C. (1998) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(98)00012-6 · Cited by 33
Ultrasonographic morphology of the human preovulatory follicle wall prior to ovulation
Martinuk, S. D., Chizen, D. R., & Pierson, R. A. (1992) · Clinical Anatomy · doi:10.1002/ca.980050502 · Cited by 32
Self-citationSelection of the Dominant Ovarian Follicle and Hormonal Enhancement of the Natural Cycle
Hodgen, G. D., KENIGSBURG, D., Collins, R. L., & Schenken, R. S. (1985) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1985.tb37502.x · Cited by 32
Does corpus luteum locally affect follicular growth negatively?
Fukuda, M., Fukuda, K., Andersen, C. Y., & Byskov, A. G. (1997) · Human Reproduction · doi:10.1093/humrep/12.5.1024 · Cited by 30
Variability of ovarian follicular growth in natural menstrual cycles
Rossavik, I. K., & Gibbons, W. E. (1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48735-2 · Cited by 29
Scheele, F., & Schoernaker, J. (1996) · Gynecological Endocrinology · doi:10.3109/09513599609041271 · Cited by 24
Attaining dominance in vivo: distinguishing dominant from challenger follicles in humans
Gore, M. A., Nayudu, P. L., & Vlaisavljević, V. (1997) · Human Reproduction · doi:10.1093/humrep/12.12.2741 · Cited by 24
FSH and the control of follicular growth
Glasier, A. F., Baird, D. T., & Hillier, S. G. (1989) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(89)90159-3 · Cited by 23
Some aspects of the dynamics of ovarian follicular growth in the human.
Gougeon, A. (1989) · PubMed · Cited by 20
The ovarian follicle and fertility
McNeilly, A. S. (1991) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90164-z · Cited by 15
Endovaginal and transabdominal sonography of ovarian follicles.
Andreotti, R. F., Thompson, G. H., Janowitz, W. R., Shapiro, A. G., & Zusmer, N. R. (1989) · Journal of Ultrasound in Medicine · doi:10.7863/jum.1989.8.10.555 · Cited by 14
TSUJI, K., Sowa, M., & Nakano, R. (1983) · Endocrinologia Japonica · doi:10.1507/endocrj1954.30.251 · Cited by 9
Ultrasound of the Human Corpus Luteum
Parsons, A. K. (1994) · Ultrasound Quarterly · doi:10.1097/00013644-199412030-00001 · Cited by 8
Ultrasound monitoring of ovarian follicular growth during spontaneous cycles in Nigerian women.
Ojengbede, O. A., Abidogun, K. A., & Fatukasi, U. I. (1992) · PubMed · Cited by 4
Research works printed but not linked: 8
- 1993, Dynamics of human follicular growth: a morphologic perspective., 21
- 1980, Etude Echographique De La Croissance Du Follicle Ovarian Normal Et Detection De L’ovulation., Strasbourg
- 1995, Ovarian follicle dynamics in vivo: dominant follicle position and the subdominant follicle population dynamics., Biol Reprod, 52, 81
- 2000, Pulsed Doppler ultrasonography to assess follicular growth and the pattern of emergence of the dominant follicle and to determine ovarian follicular and stromal blood flow parameters in relation to follicular size., J Reprod Fertil, 45
- 1999, Comparative patterns of follicle development and selection in ruminants., J Reprod Fertil Suppl, 54, 17
- 1990, Effect of day of estrous cycle on pattern of luteinizing hormone (LH) secretion in the bovine female., J Anim Sci, 1990, 442
- 1990, Ultrasonographic visualization of human ovulation., 73
- 1996, The menstrual cycle: an integrative view., 104
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Metadata
- Authors
- Baerwald, A. R., Adams, G. P., & Pierson, R. A.
- Affiliations
- University of Saskatchewan (CA)
- ORCID
- Pierson, Roger A.
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-09-01
- Volume
- 69
- Issue
- 3
- Pages
- 1023-1031
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- OpenAlex
- W2050867024
- Cited by
- 359
- References
- 77
- Citations by year
- 2026: 10 · 2025: 15 · 2024: 9 · 2023: 22 · 2022: 17 · 2021: 14 · 2020: 20 · 2019: 14 · 2018: 17 · 2017: 21 · 2016: 19 · 2015: 16 · 2014: 13 · 2013: 25 · 2012: 15
- FWCI
- 10.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biology of Reproduction (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Reproductive Physiology in Livestock
- Keywords
- folliculogenesis, interovulatory interval, follicle dominance, antral follicles, estradiol, luteinizing hormone, follicle-stimulating hormone, menstrual cycle, transvaginal ultrasound
- MeSH terms
- Adult, Estradiol, Female, Follicle Stimulating Hormone, Ovarian Follicle, Humans, Luteinizing Hormone, Longitudinal Studies, Menstrual Cycle, Ovulation, Reference Values, Ultrasonography
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