Rapid Maturation of the Reproductive Axis during Perimenarche Independent of Body Composition1
Abstract
The development of the reproductive axis is thought to be a gradual process, but our understanding of the complex endocrine changes that accompany the transition from premenarche to reproductive life in women has been hampered by the paucity of longitudinal studies. We studied 112 premenarchal Caucasian females at 6-month intervals over 4 yr and obtained a detailed reproductive and dietary history. We quantified reproductive hormones in 24-h urine collections as a measure of daily output and measured body composition biometrically and with the use of dual energy x-ray absortiometry scans. The percent body fat did not change appreciably in the study period (range, 21-24%) and was unrelated to menarche. Sex steroid and gonadotropin levels changed exponentially in the year approaching menarche. FSH levels peaked at menarche and then progressively declined thereafter. Estradiol output increased rapidly in the year approaching menarche and then plateaued thereafter. The frequency of menstrual bleeding increased rapidly and plateaued at 1 yr postmenarche. At 1 yr, 65% of these adolescent women had established a pattern of 10 or more menstrual episodes/yr, and by 3 yr postmenarche this figure exceeded 90%. There were no significant changes in dietary intake of protein, carbohydrate, or fat in the same period. Menarche occurs as a result of rapid maturation of the reproductive axis and heralds the reestablishment of a negative sex steroid feedback loop that parallels the adult threshold. These events appear to develop independent of changes in body composition and diet, but may reflect the improved nutrition and socioeconomic status of the late 20th century.
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Anovulatory cycles can persist until nearly 5 years after menarche.
“Both Metcalf et al. [62] and Apter [63] reported that anovulatory cycles can persist until nearly 5 years after menarche.”
From The Diagnosis of Polycystic Ovary Syndrome during Adolescence (2015) · cites this paper as [62]
Cites
Physical growth: National Center for Health Statistics percentiles
Hamill, P. V. V., Drizd, T. A., Johnson, C., Reed, R. B., Roche, A., & Moore, W. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.3.607 · Cited by 2,322 · see citing works
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., & Hasemeier, C. M. (1997) · PEDIATRICS · doi:10.1542/peds.99.4.505 · Cited by 1,709 · see citing works
Frisch, R. E., & McArthur, J. W. (1974) · Science · doi:10.1126/science.185.4155.949 · Cited by 1,412 · see citing works
(1989) · Medical Entomology and Zoology · Cited by 1,150 · see citing works
Height and weight at menarche and a hypothesis of critical body weights and adolescent events
Frisch, R. E., & Revelle, R. (1970) · Science · doi:10.1126/science.169.3943.397 · Cited by 721 · see citing works
Saltation and Stasis: a Model of Human Growth
Lampl, M., Veldhuis, J. D., & Johnson, M. L. (1992) · Science · doi:10.1126/science.1439787 · Cited by 387 · see citing works
Clinical Use of Bone Densitometry
Desforges, J. F., Johnston, C. C., Slemenda, C. W., & Melton, L. J. (1991) · New England Journal of Medicine · doi:10.1056/nejm199104183241606 · Cited by 375 · see citing works
McNATTY, K. P., MAKRIS, A., DEGRAZIA, C., RAPIN, O., & RYAN, K. J. (1979) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-49-5-687 · Cited by 367 · see citing works
Leptin Is Inversely Related to Age at Menarche in Human Females*
Matkovic, V., Ilich, J. Z., Skugor, M., Badenhop, N. E., Goel, P. K., Clairmont, A., Klisovic, D. D., Nahhas, R. W., & Landoll, J. D. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.10.4280 · Cited by 364 · see citing works
Gutin, B., Litaker, M. S., Islam, S., Manos, T. M., Smith, C., & Treiber, F. A. (1996) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.3.287 · Cited by 264 · see citing works
Secondary sex characteristics of girls 12 to 17 years of age: The U.S. Health examination survey
Daniel, W. A., Harlan, W. R., Harland, E. A., & Grillo, G. P. (1980) · The Journal of Pediatrics · doi:10.1016/s0022-3476(80)80647-0 · Cited by 203 · see citing works
Body-composition assessment by dual-energy x-ray absorptiometry in subjects aged 4-26 y
Ogle, G. D., Allen, J., HUMPHRIES, I. R. J., Lu, P., Briody, J., Morley, K., Howman-Giles, R. B., & Cowell, C. (1995) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/61.4.746 · Cited by 201 · see citing works
de Ridder, C. M., Thijssen, J. H. H., Bruning, P. F., den Brande, J. L. V., Zonderland, M. L., & Erich, W. B. M. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.2.1639945 · Cited by 193 · see citing works
Frisch, R. E., Revelle, R. R., & Cook, S. (1973) · PubMed · Cited by 183 · see citing works
SERUM STEROIDS AND PITUITARY HORMONES IN FEMALE PUBERTY: A PARTLY LONGITUDINAL STUDY
Apter, D. L. (1980) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1980.tb02125.x · Cited by 182 · see citing works
Incidence of ovulation in the years after the menarche
Metcalf, M. G., SKIDMORE, D. S., Lowry, G. F., & Mackenzie, J. A. (1983) · Journal of Endocrinology · doi:10.1677/joe.0.0970213 · Cited by 165 · see citing works
Lee, P. A., XENAKIS, T., WINER, J., & MATSENBAUGH, S. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-43-4-775 · Cited by 130 · see citing works
Anovulation after Precocious Pubarche: Early Markers and Time Course in Adolescence1
Ibáñez, L., de Zegher, F., & Potau, N. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5883 · Cited by 128 · see citing works
Lloyd, T., Rollings, N. J., Andon, M. B., Demers, L. M., Eggli, D. F., Kieselhorst, K., Kulin, H. E., Landis, J. R., Martel, J. K., & Orr, G. A. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.2.1639940 · Cited by 120 · see citing works
Self-citationDevelopmental processes in early adolescence
Nottelmann, E. D., Susman, E. J., Dorn, L. D., Inoff-Germain, G., Loriaux, D. L., Cutler, G. B., & Chrousos, G. P. (1987) · Journal of Adolescent Health Care · doi:10.1016/0197-0070(87)90428-1 · Cited by 110 · see citing works
WENNINK, J. M. B., de Waal, H. A. D., Schoemaker, R. C., SCHOEMAKER, H., & Schoemaker, J. (1989) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1989.tb01279.x · Cited by 103 · see citing works
Lloyd, T., Schaeffer, J., Walker, M., & Demers, L. (1991) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/54.6.1005 · Cited by 89 · see citing works
Self-citationChanges in dimeric inhibin A and B during normal early puberty in boys and girls
Crofton, P. M., Illingworth, P. J., Groome, N. P., Stirling, H. F., Swanston, I. A., Gow, S., Wu, F. C. W., McNeilly, A. S., & Kelnar, C. J. H. (1997) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1997.d01-1744.x · Cited by 85 · see citing works
The Weight and Fitness Status of United States Children
Schlicker, S. A., Borra, S. T., & Regan, C. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1994.tb01348.x · Cited by 80 · see citing works
Evaluation of a new set of calibration standards for the measurement of fat content via DPA and DXA
Goodsitt, M. M. (1992) · Medical Physics · doi:10.1118/1.596890 · Cited by 67 · see citing works
The Development of Cyclic Pituitary—Gonadal Function in Adolescent Females
Winter, J. S. D., & Faiman, C. (1973) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-37-5-714 · Cited by 62 · see citing works
The neuroendocrinology of human puberty. An ontogenetic perspective
Grumbach, M. M. (1990) · Medical Entomology and Zoology · Cited by 55 · see citing works
Santner, S. J., Santen, R. J., Kulin, H. E., & Demers, L. M. (1981) · Clinical Chemistry · doi:10.1093/clinchem/27.11.1892 · Cited by 53 · see citing works
Self-citationAge at menarche of European, Afro-Caribbean and Indo-Pakistani schoolgirls living in London
Ulijaszek, S. J., Evans, E., & Miller, D. S. (1991) · Annals of Human Biology · doi:10.1080/03014469100001502 · Cited by 50 · see citing works
Heinrichs, C., Munson, P. J., Counts, D., Cutler, G. B., & Baron, J. (1995) · Science · doi:10.1126/science.7716552 · Cited by 45 · see citing works
Age-related course of urinary gonadotropins in children
Demir, A., Dunkel, L., Stenman, U., & Voutilainen, R. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.4.7714124 · Cited by 37 · see citing works
Gonadotropin Excretion and Body Composition
Penny, R., Goldstein, I. P., & Frasier, S. D. (1978) · PEDIATRICS · doi:10.1542/peds.61.2.294 · Cited by 25 · see citing works
Fluctuations of Gonadotropin Levels in Children
Johanson, A. J., & VANN, E. (1974) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-39-1-154 · Cited by 24 · see citing works
Estimation of body fat from skinfolds and surface area.
Katch, F. I., Behnke, A. R., & Katch, V. L. (1979) · PubMed · Cited by 19 · see citing works
Lloyd, T., Rollings, N. J., & Chinchilli, V. M. (1998) · Springer eBooks · doi:10.1007/978-1-4612-2228-6_2 · Cited by 14 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The Diagnosis of Polycystic Ovary Syndrome during Adolescence
Witchel, S. F., Oberfield, S., Rosenfield, R. L., Codner, E., Bonny, A., Ibáñez, L., Pena, A., Horikawa, R., Gomez-Lobo, V., Joel, D., et al. (2015) · Hormone Research in Paediatrics · doi:10.1159/000375530 · Cited by 3,113 · see citing works
Parent, A.-S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J.-P. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0019 · Cited by 1,762 · see citing works
Elliott-Sale, K. J., Minahan, C. L., de Jonge, X. A. K. J., Ackerman, K. E., Sipilä, S., Constantini, N. W., Lebrun, C. M., & Hackney, A. C. (2021) · Sports Medicine · doi:10.1007/s40279-021-01435-8 · Cited by 731 · see citing works
Witchel, S. F., Oberfield, S. E., & Peña, A. S. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2019-00078 · Cited by 653 · see citing works
Pubertal Development: Correspondence Between Hormonal and Physical Development
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009) · Child Development · doi:10.1111/j.1467-8624.2009.01263.x · Cited by 614 · see citing works
Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline
Gordon, C. M., Ackerman, K. E., Berga, S. L., Kaplan, J. R., Mastorakos, G. P., Misra, M., Murad, M. H., Santoro, N. F., & Warren, M. P. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00131 · Cited by 634 · see citing works
Adolescent polycystic ovary syndrome according to the international evidence-based guideline
Peña, A. S., Witchel, S. F., Hoeger, K. M., Oberfield, S. E., Vogiatzi, M. G., Misso, M. L., Garad, R. M., Dabadghao, P., & Teede, H. J. (2020) · BMC Medicine · doi:10.1186/s12916-020-01516-x · Cited by 331 · see citing works
Functional Hypothalamic Amenorrhea
Gordon, C. M. (2010) · New England Journal of Medicine · doi:10.1056/nejmcp0912024 · Cited by 253 · see citing works
Cannot exclude torsion—a 15-year review
Oltmann, S. C., Fischer, A. C., Barber, R. G., Huang, R., Hicks, B., & García, N. M. (2009) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2009.02.028 · Cited by 252 · see citing works
Somatotropic and Gonadotropic Axes Linkages in Infancy, Childhood, and the Puberty-Adult Transition
Veldhuis, J. D., Roemmich, J. N., Richmond, E. J., & Bowers, C. Y. (2006) · Endocrine Reviews · doi:10.1210/er.2005-0006 · Cited by 235 · see citing works
Endocrinology of the Menopause
Hall, J. E. (2015) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2015.05.010 · Cited by 223 · see citing works
Dimitri, P., Bishop, N. J., Walsh, J., & Eastell, R. (2011) · Bone · doi:10.1016/j.bone.2011.05.011 · Cited by 213 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
In utero exposure to organochlorines and age at menarche
Vasiliu, O. (2004) · Human Reproduction · doi:10.1093/humrep/deh292 · Cited by 177 · see citing works
Effects of obesity on growth and puberty
Dunger, D. B., Ahmed, M. L., & Ong, K. K. (2005) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2005.04.005 · Cited by 158 · see citing works
Serum DDT, age at menarche, and abnormal menstrual cycle length
Ouyang, F., Perry, M. J., Venners, S. A., Chen, C., Wang, B., Yang, F., Fang, Z., Zang, T., Wang, L., Xu, X., et al. (2005) · Occupational and Environmental Medicine · doi:10.1136/oem.2005.020248 · Cited by 157 · see citing works
Adolescent Anovulation: Maturational Mechanisms and Implications
Rosenfield, R. L. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1770 · Cited by 139 · see citing works
Female Athlete Triad and Its Components: Toward Improved Screening and Management
Javed, A., Tebben, P. J., Fischer, P. R., & Lteif, A. N. (2013) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2013.07.001 · Cited by 125 · see citing works
Petit, M. A., Beck, T., Lin, H.-M., Bentley, C. M., Legro, R. S., & Lloyd, T. (2004) · Bone · doi:10.1016/j.bone.2004.05.008 · Cited by 124 · see citing works
Self-citationFifty-year trends in serial body mass index during adolescence in girls: the Fels Longitudinal Study
Demerath, E. W., Lǐ, J., Sun, S. S., Chumlea, W. C., Remsberg, K. E., Czerwinski, S. A., Towne, B., & Siervogel, R. M. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.2.441 · Cited by 120 · see citing works
Pubertal Development and Menarche
DiVall, S. A., & Radovick, S. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1429.026 · Cited by 110 · see citing works
Boyne, M. S., Thame, M. M., Osmond, C., Fraser, R. A., Gabay, L., Reid, M. E., & Forrester, T. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0080 · Cited by 108 · see citing works
Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress
Ruttle, P. L., Shirtcliff, E. A., Armstrong, J. M., Klein, M. H., & Essex, M. J. (2013) · Developmental Psychobiology · doi:10.1002/dev.21138 · Cited by 107 · see citing works
Ibáñez, L., Ong, K., Ferrer, A., Amin, R., Dunger, D., & de Zegher, F. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-022002 · Cited by 100 · see citing works
Menarche and Time to Cycle Regularity Among Individuals Born Between 1950 and 2005 in the US
Wang, Z., Asokan, G., Onnela, J.-P. “., Baird, D. D., Jukic, A. M. Z., Wilcox, A. J., Curry, C. L., Fischer‐Colbrie, T., Williams, M. A., Hauser, R. B., et al. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.12854 · Cited by 97 · see citing works
Milk Intake and Total Dairy Consumption: Associations with Early Menarche in NHANES 1999-2004
Wiley, A. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014685 · Cited by 94 · see citing works
Boukaidi, S. A., Delotte, J., Steyaert, H., Valla, J. S., Sattonnet, C., Bouaziz, J., & Bongain, A. (2011) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2011.01.033 · Cited by 92 · see citing works
Alonso, L. C., & Rosenfield, R. L. (2002) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1053/beem.2002.0177 · Cited by 89 · see citing works
Kent, S. C., Gnatuk, C. L., Kunselman, A. R., Demers, L. M., Lee, P. A., & Legro, R. S. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1958 · Cited by 88 · see citing works
Self-citationDevelopment of Ovulatory Menstrual Cycles in Adolescent Girls
Carlson, L. J., & Shaw, N. D. (2019) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/j.jpag.2019.02.119 · Cited by 90 · see citing works
Onset of Ovulation after Menarche in Girls: A Longitudinal Study
Zhang, K., Pollack, S., Ghods, A., Dicken, C., Isaac, B., Adel, G., Zeitlian, G., & Santoro, N. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1846 · Cited by 84 · see citing works
Stevens–Simon, C., Beach, R. K., & McGregor, J. (2002) · Journal of Perinatology · doi:10.1038/sj.jp.7210694 · Cited by 79 · see citing works
Mueller, N. T., Jacobs, D. R., MacLehose, R. F., Demerath, E. W., Kelly, S. P., Dreyfus, J., & Pereira, M. A. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.100958 · Cited by 77 · see citing works
International evidence-based recommendations for polycystic ovary syndrome in adolescents
Peña, A. S., Witchel, S. F., Boivin, J., Burgert, T. S., Ee, C., Hoeger, K. M., Lujan, M. E., Mousa, A., Oberfield, S. E., Tay, C. T., et al. (2025) · BMC Medicine · doi:10.1186/s12916-025-03901-w · Cited by 89 · see citing works
Association of Concussion With Abnormal Menstrual Patterns in Adolescent and Young Women
Snook, M. L., Henry, L. C., Sanfilippo, J. S., Zeleznik, A. J., & Kontos, A. P. (2017) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2017.1140 · Cited by 75 · see citing works
Relationship Between Body Mass Index and Early Menarche of Adolescent Girls in Seoul
Oh, C., Oh, I., Choi, K.-S., Choe, B., Yoon, T., & Choi, J. (2012) · Journal of Preventive Medicine and Public Health · doi:10.3961/jpmph.2012.45.4.227 · Cited by 73 · see citing works
Endocrinology of female puberty
DiVall, S. A., & Radovick, S. (2009) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283207937 · Cited by 71 · see citing works
Obstacles in the Optimization of Bone Health Outcomes in the Female Athlete Triad
Ducher, G., Turner, A. I., Kukuljan, S., Pantano, K. J., Carlson, J. L., Williams, N. I., & Souza, M. J. D. (2011) · Sports Medicine · doi:10.2165/11588770-000000000-00000 · Cited by 69 · see citing works
Efficient Fat Storage in Premenopausal Women and in Early Pregnancy: A Role for Estrogen
O’Sullivan, A., Martin, A. M., & Brown, M. A. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.10.7941 · Cited by 68 · see citing works
Puberty and its disorders in the female
Rosenfield, R. L., Cooke, D. W., & Radovick, S. (2014) · Elsevier eBooks · doi:10.1016/b978-1-4557-4858-7.00024-x · Cited by 67 · see citing works
Oral contraceptive use by teenage women does not affect peak bone mass: a longitudinal study
Lloyd, T., Taylor, D. S., Lin, H. M., Matthews, A. E., Eggli, D. F., & Legro, R. S. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00719-6 · Cited by 66 · see citing works
Self-citationSleep EEG Evidence of Sex Differences in Adolescent Brain Maturation
Campbell, I. G., Darchia, N., Khaw, W. Y., Higgins, L. M., & Feinberg, I. (2005) · SLEEP · doi:10.1093/sleep/28.5.637 · Cited by 64 · see citing works
Petit, M. A., Beck, T., Hughes, J. M., Lin, H.-M., Bentley, C. M., & Lloyd, T. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.071018 · Cited by 62 · see citing works
Self-citationMenstrual patterns in the first gynecological year: a systematic review
Gunn, H. M., Tsai, M.-C., McRae, A., & Steinbeck, K. S. (2018) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/j.jpag.2018.07.009 · Cited by 60 · see citing works
Polycystic Ovary Syndrome in Adolescents: Challenges in Diagnosis and Treatment
Tehrani, F. R., & Amiri, M. (2019) · Intern J Endocrinol Metab · doi:10.5812/ijem.91554 · Cited by 65 · see citing works
Coming of age in R oman B ritain: Osteological evidence for pubertal timing
Arthur, N. A., Gowland, R. L., & Redfern, R. C. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22929 · Cited by 56 · see citing works
The incidence and surgical management of paratubal cysts in a pediatric and adolescent population
Muolokwu, E., Sánchez, J., Bercaw, J. L., Sangi‐Haghpeykar, H., Banszek, T., Brandt, M. L., & Dietrich, J. E. (2011) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2011.04.054 · Cited by 57 · see citing works
Healthy post-menarchal adolescent girls demonstrate multi-level reproductive axis immaturity
Sun, B. Z., Kangarloo, T., Adams, J. M., Sluss, P. M., Welt, C. K., Chandler, D. W., Zava, D. T., McGrath, J. A., Umbach, D. M., Hall, J. E., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00595 · Cited by 55 · see citing works
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Change in leptin, body composition and other hormones around menarche – a visual representation
Bandini, L. G., Must, A., Naumova, E. N., Anderson, S., Caprio, S., Spadano-Gasbarro, J. L., & Dietz, W. H. (2008) · Acta Paediatrica · doi:10.1111/j.1651-2227.2008.00948.x · Cited by 48 · see citing works
Peña, A. S., Doherty, D. A., Atkinson, H. C., Hickey, M., Norman, R. J., & Hart, R. (2018) · Archives of Disease in Childhood · doi:10.1136/archdischild-2017-312968 · Cited by 47 · see citing works
Diagnosis and treatment of polycystic ovarian syndrome in adolescents
Nicandri, K. F., & Hoeger, K. M. (2012) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e32835a1a03 · Cited by 47 · see citing works
Perimenarchal air pollution exposure and menstrual disorders
Mahalingaiah, S., Missmer, S., Cheng, J. J., Chavarro, J. E., Laden, F., & Hart, J. E. (2018) · Human Reproduction · doi:10.1093/humrep/dey005 · Cited by 46 · see citing works
Urinary Free Cortisol Increases in Adolescent Caucasian Females during Perimenarche
Legro, R. S., Lin, H. M., Demers, L. M., & Lloyd, T. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020256 · Cited by 44 · see citing works
Self-citationPuberty and Its Disorders in the Female
Rosenfield, R. L., Cooke, D. W., & Radovick, S. (2008) · Elsevier eBooks · doi:10.1016/b978-141604090-3.50019-3 · Cited by 44 · see citing works
Polycystic Ovary Syndrome and Hyperandrogenic States
Chang, R. J., & Dumesic, D. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00021-4 · Cited by 41 · see citing works
Selmeczy, D., Fandakova, Y., Grimm, K. J., Bunge, S. A., & Ghetti, S. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.10.003 · Cited by 41 · see citing works
Puberty onset in Northern Italy: A random sample of 3597 Italian children
Castellino, N., Bellone, S., Rapa, A., Vercellotti, A., Binotti, M., Petri, A., & Bona, G. (2005) · Journal of Endocrinological Investigation · doi:10.1007/bf03347256 · Cited by 38 · see citing works
Samara-Boustani, D., Colmenares, A., Elie, C., Dabbas, M., Beltrand, J., Caron, V., Ricour, C., Jacquin, P., Tubiana-Rufi, N., Levy-Marchal, C., et al. (2012) · European Journal of Endocrinology · doi:10.1530/eje-11-0670 · Cited by 37 · see citing works
Polycystic ovary syndrome in adolescents
Dabadghao, P. (2019) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2019.04.006 · Cited by 36 · see citing works
Witchel, S. F., & Topaloglu, A. K. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00017-2 · Cited by 40 · see citing works
Changes and Tracking of Fat Mass in Pubertal Girls
Vink, E. E., van Coeverden, S. C. C. M., van Mil, E., Felius, B. A., van Leerdam, F. J. M., & de Waal, H. A. D. (2009) · Obesity · doi:10.1038/oby.2009.366 · Cited by 32 · see citing works
Eriksson, A., Suuriniemi, M., Mahonen, A., Cheng, S., & Ohlsson, C. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000163383.49747.b5 · Cited by 30 · see citing works
Kelsey, M. M., Braffett, B. H., Geffner, M. E., Levitsky, L. L., Caprio, S., McKay, S. V., Shah, R. D., Sprague, J., Arslanian, S. A., & TODAY Study Group (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00132 · Cited by 29 · see citing works
Functional hypothalamic amenorrhea: Impact on bone and neuropsychiatric outcomes
Pedreira, C. C., Maya, J., & Misra, M. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.953180 · Cited by 28 · see citing works
Optimal management of polycystic ovary syndrome in adolescence
Baldauff, N. H., & Arslanian, S. A. (2015) · Archives of Disease in Childhood · doi:10.1136/archdischild-2014-306471 · Cited by 27 · see citing works
Beal, S. J., Dorn, L. D., Sucharew, H. J., Sontag-Padilla, L. M., Pabst, S. R., & Hillman, J. B. (2014) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000099 · Cited by 26 · see citing works
Peripubertal estrogen levels and physical activity affect femur geometry in young adult women
Devlin, M. J., Stetter, C., Lin, H. ‐., Beck, T. J., Legro, R. S., Petit, M. A., Lieberman, D. E., & Lloyd, T. (2009) · Osteoporosis International · doi:10.1007/s00198-009-0999-6 · Cited by 24 · see citing works
Self-citationNeurobiology of puberty and its disorders
Witchel, S. F., & Plant, T. M. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820683-6.00033-6 · Cited by 23 · see citing works
Salivary Progesterone Levels Before Menarche: A Prospective Study of Adolescent Girls
Gray, S. H., Ebe, L. K., Feldman, H. A., Emans, S. J., Osganian, S. K., Gordon, C. M., & Laufer, M. R. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0125 · Cited by 24 · see citing works
Irregular Cycles, Ovulatory Disorders, and Cardiometabolic Conditions in a US-Based Digital Cohort
Wang, Z., Jukic, A. M. Z., Baird, D. D., Wilcox, A. J., Li, H., Curry, C. L., Fischer‐Colbrie, T., Onnela, J.-P. “., Williams, M. A., Hauser, R. B., et al. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.9657 · Cited by 23 · see citing works
Paratubal cysts, obesity, and hyperandrogenism
Muolokwu, E., Sánchez, J., Bercaw, J. L., Sangi‐Haghpeykar, H., Banszek, T., Brandt, M. L., & Dietrich, J. E. (2011) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2011.07.011 · Cited by 23 · see citing works
What is adolescent polycystic ovary syndrome?
Peña, A. S., & Metz, M. P. (2017) · Journal of Paediatrics and Child Health · doi:10.1111/jpc.13821 · Cited by 23 · see citing works
Ptak, A., Ludewig, G., Robertson, L. W., Lehmler, H., & Gregoraszczuk, E. Ł. (2006) · Toxicology Letters · doi:10.1016/j.toxlet.2005.12.001 · Cited by 23 · see citing works
Factors Affecting Menstrual Cycle Developmental Trajectory in Adolescents: A Narrative Review
Naz, M. S. G., Farahmand, M., Dashti, S., & Tehrani, F. R. (2022) · Intern J Endocrinol Metab · doi:10.5812/ijem.120438 · Cited by 21 · see citing works
Female Puberty: Clinical Implications for the Use of Prolactin-Modulating Psychotropics
Becker, A. L., & Epperson, C. N. (2006) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2005.08.006 · Cited by 21 · see citing works
Genetic and environmental influences on testosterone in adolescents: Evidence for sex differences
Harden, K. P., Kretsch, N., Tackett, J. L., & Tucker–Drob, E. M. (2014) · Developmental Psychobiology · doi:10.1002/dev.21207 · Cited by 20 · see citing works
Hyperandrogenism in female athletes with functional hypothalamic amenorrhea: a distinct phenotype
Lteif, A. N., Kashyap, R., & Javed, A. (2015) · International Journal of Women s Health · doi:10.2147/ijwh.s73011 · Cited by 20 · see citing works
Puberty in the Female and Its Disorders
Rosenfield, R. L., Cooke, D. W., & Radovick, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-62520-3.00016-6 · Cited by 22 · see citing works
Adrenarche and Polycystic Ovary Syndrome: A Tale of Two Hypotheses
Nader, S. (2007) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/j.jpag.2007.05.001 · Cited by 19 · see citing works
Development of a novel risk prediction and risk stratification score for polycystic ovary syndrome
Deshmukh, H., Papageorgiou, M., Kilpatrick, E. S., Atkin, S. L., & Sathyapalan, T. (2018) · Clinical Endocrinology · doi:10.1111/cen.13879 · Cited by 18 · see citing works
Gregoraszczuk, E. Ł., Zemla, M., Ptak, A., & Grabic, R. (2005) · PubMed · Cited by 16 · see citing works
Hyperandrogenism during puberty in the development of polycystic ovary syndrome
Nader, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.03.013 · Cited by 15 · see citing works
Tzur, T., Smorgick, N., Sharon, N. Z., Pekar‐Zlotin, M., Maymon, R., & Melcer, Y. (2020) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2020.05.023 · Cited by 14 · see citing works
Paratubal Cyst Size Correlates With Obesity and Dysregulation of the Wnt Signaling Pathway
Dietrich, J. E., Adeyemi, O. A., Hakim, J. C.-E., Santos, X. M., Bercaw‐Pratt, J. L., Bournat, J. C., Chen, C. H., & Jorgez, C. J. (2017) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/j.jpag.2017.04.002 · Cited by 13 · see citing works
KISS1 expression in osteosarcoma: high in chinese clinical cases, but lower in cell lines.
Wang, F.-S., Chen, H., Wu, Z., & Lin, J. (2011) · PubMed · Cited by 13 · see citing works
Pediatric and adolescent gynecology
Bieber, E. J., Sanfilippo, J. S., Horowitz, I., & Shafi, M. I. (2015) · Cambridge University Press eBooks · doi:10.1017/cbo9781139628938.035 · Cited by 12 · see citing works
Amoruso, I., Fonzo, M., Barro, A., Scardina, C., Titton, F., Bertoncello, C., & Baldovin, T. (2024) · Psychology of sport and exercise · doi:10.1016/j.psychsport.2024.102653 · Cited by 11 · see citing works
Normal Pubertal Physiology in Females
Boswell, H. B. (2014) · Springer eBooks · doi:10.1007/978-1-4939-0912-4_2 · Cited by 11 · see citing works
Estradiol variability is associated with brain structure in early adolescent females
Zwaan, I. S., Felmingham, K. L., Vijayakumar, N., Patton, G. C., Mundy, L. K., Byrne, M. L., Simmons, J. G., & Whittle, S. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105943 · Cited by 10 · see citing works
Styne, D. M., & Grumbach, M. M. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-499-5_3 · Cited by 10 · see citing works
França, T. F. A., Segura, I. A., Dias, N. M., Miranda, M. C., & Pompéia, S. (2025) · Developmental Psychobiology · doi:10.1002/dev.70069 · Cited by 9 · see citing works
Rovner, P., Keltz, J., Allshouse, A. A., Isaac, B., Hickmon, C., Lesh, J., Chosich, J., & Santoro, N. F. (2017) · Reproductive Sciences · doi:10.1177/1933719117741377 · Cited by 8 · see citing works
Sopher, A. B., Oberfield, S. E., & Witchel, S. F. (2021) · Seminars in Reproductive Medicine · doi:10.1055/s-0041-1735892 · Cited by 8 · see citing works
A Preliminary Analysis of the Age of Full Expression of Sexually Dimorphic Cranial Traits
Stock, M. K. (2018) · Journal of Forensic Sciences · doi:10.1111/1556-4029.13780 · Cited by 7 · see citing works
Afkhamzadeh, A., Rahmani, K., Habibi, A., & Faraji, O. (2018) · Shiraz E-Medical Journal · doi:10.5812/semj.69802 · Cited by 7 · see citing works
Fisiología reproductiva y cambios evolutivos con la edad de la mujer
Vantman, B. D., & Vega, B. M. (2010) · Revista Médica Clínica Las Condes · doi:10.1016/s0716-8640(10)70545-9 · Cited by 7 · see citing works
Age at Menarche, Growth Velocity, and Adiposity Indices in Italian Girls Aged 10 to 14
Gualdi‐Russo, E., Rinaldo, N., Mazzoni, G., Mandini, S., Masotti, S., Toselli, S., & Zaccagni, L. (2022) · Children · doi:10.3390/children9121928 · Cited by 6 · see citing works
Menarche at Amarna: Timing and the further implications
Dabbs, G. R. (2023) · American Journal of Biological Anthropology · doi:10.1002/ajpa.24856 · Cited by 6 · see citing works
Javed, A., Kumar, S., Simmons, P. S., & Lteif, A. N. (2015) · Hormone Research in Paediatrics · doi:10.1159/000435883 · Cited by 6 · see citing works
- Authors
- Legro, R. S., Lin, H. M., Demers, L. M., & Lloyd, T.
- Affiliations
- Pennsylvania State University (US)
- Corresponding author
- Legro, Richard S.
- ORCID
- Legro, Richard S.
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2000-03
- Volume
- 85
- Issue
- 3
- Pages
- 1021-1025
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2006967917
- Cited by
- 154
- References
- 35
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 9 · 2023: 3 · 2022: 5 · 2021: 6 · 2020: 2 · 2019: 8 · 2018: 11 · 2017: 11 · 2016: 5 · 2015: 11 · 2014: 6 · 2013: 12 · 2012: 2
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (MO1 RR10732, M01RR010732)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K08 HD0118, R01 HD 25973, R01HD025973)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Keywords
- menarche, body composition, sex steroid feedback, follicle-stimulating hormone, estradiol, gonadotropins, menstrual frequency, dietary intake
- MeSH terms
- Adipose Tissue, Adolescent, Body Composition, Breast, Diet, Estradiol, Female, Follicle Stimulating Hormone, Humans, Luteinizing Hormone, Menarche, Menstruation, Reference Values, Reproduction, Sexual Maturation, Testosterone, Body Mass Index
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