The DOI matches its Crossref record; 46 of the 47 references it cites were found in a registry or an index.
High Frequency of Luteal Phase Deficiency and Anovulation in Recreational Women Runners: Blunted Elevation in Follicle-Stimulating Hormone Observed during Luteal-Follicular Transition1
Abstract
The purposes of this investigation were to evaluate the characteristics of three consecutive menstrual cycles and to determine the frequency ofluteal phase deficiency (LPD) and anovulation in a sample of sedentary and moderately exercising, regularly menstruating women. For three consecutive menstrual cycles, subjects collected daily urine samples for analysis of FSH, estrone conjugates (E1C), pregnanediol-3-glucuronide (PdG), and creatinine (Cr). Sedentary (n=11) and exercising (n=24) groups were similar in age (27.0+/-1.3 yr), weight (60.3+/-3.1 kg), gynecological age (13.8+/-1.2 yr), and menstrual cycle length (28.3+/-0.8 days). Menstrual cycles were classified by endocrine data as ovulatory, LPD, or anovulatory. No sedentary women (0%) had inconsistent menstrual cycle classifications from cycle to cycle, but 46% of the exercising women were inconsistent. The sample prevalence of LPD in the exercising women was 48%, and the 3-month sample incidence was 79%. In the sedentary women, 90% of all menstrual cycles were ovulatory (SedOvul; n=28), whereas in the exercising women only 45% were ovulatory (ExOvul; n=30); 43% were LPD (ExLPD; n=28), and 12% were anovulatory (ExAnov; n=8). In ExLPD cycles, the follicular phase was significantly longer (17.9+/-0.7 days), and the luteal phase was significantly shorter (8.2+/-0.5 days) compared to ExOvul (14.8+/-0.9 and 12.9+/-0.3 days) and SedOvul (15.9+/-0.6 and 12.9+/-0.4 days) cycles. Luteal phase PdG excretion was lower (P < 0.001) in ExLPD (2.9+/-0.3 microg/mg Cr) and ExAnov (0.8+/-0.1 microg/mg Cr) cycles compared to SedOvul cycles (5.0+/-0.4 microg/mg Cr). ExOvul cycles also had less (P < 0.01) PdG excretion during the luteal phase (3.7+/-0.3 microg/mg Cr) than the SedOvul cycles. E1C excretion during follicular phase days 2-5 was lower (P=0.05) in ExOvul, ExLPD, and ExAnov cycles compared to SedOvul cycles and remained lower (P < 0.02) in the ExLPD and ExAnov cycles during days 6-12. The elevation in FSH during the luteal-follicular transition was lower (P < 0.007) in ExLPD (0.7+/-0.1 ng/mg Cr) cycles compared to SedOvul and ExOvul cycles (1.0+/-0.1 and 1.1+/-0.1 ng/mg Cr, respectively). Energy balance and energy availability were lower (P < 0.05) in ExAnov cycles than in other menstrual cycle categories. The blunted elevation in FSH during the luteal-follicular transition in exercising women with LPD may explain their lower follicular estradiol levels. These alterations in FSH may act in concert with disrupted LH pulsatility as a primary and proximate factor in the high frequency of luteal phase and ovulatory disturbances in regularly menstruating, exercising women.
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“In a follow-up study, an acute bout of moderate intensity aerobic exercise did not exert the same effects on ghrelin and insulin for women using a monophasic COC and the participants maintained an energy deficit after exercise”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [139]
Citations
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Low energy availability, not stress of exercise, alters LH pulsatility in exercising women
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“In this context, energy availability may be usefully defined as dietary energy intake minus exercise energy expenditure (30, 40).”
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(2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318149f111 · Cited by 1,554
Self-citationLoucks, A. B., & Thuma, J. R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020369 · Cited by 760
Self-citationMountjoy, M., Ackerman, K. E., Bailey, D. M., Burke, L. M., Constantini, N., Hackney, A. C., Heikura, I. A., Melin, A., Pensgaard, A. M., Stellingwerff, T., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-106994 · Cited by 724
De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M., Goolsby, M., Matheson, G., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093218 · Cited by 661
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 674
Metadata
- Authors
- De Souza, M. J., Miller, B. E., Loucks, A. B., Luciano, A. A., Pescatello, L. S., Campbell, C. G., & Lasley, B. L.
- Affiliations
- Center for Fertility and Reproductive Endocrinology (M.J.D.S., B.E.M., A.A.L.), New Britain General Hospital, New Britain, Connecticut 06050
- New Britain General Hospital (US)
- Ohio University (US)
- University of Hartford (US)
- University of California, Davis (US)
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1998-12-01
- Volume
- 83
- Issue
- 12
- Pages
- 4220-4232
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2135324780
- Cited by
- 315
- References
- 47
- Citations by year
- 2026: 1 · 2025: 11 · 2024: 8 · 2023: 12 · 2022: 10 · 2021: 13 · 2020: 12 · 2019: 12 · 2018: 6 · 2017: 11 · 2016: 18 · 2015: 9 · 2014: 22 · 2013: 16 · 2012: 16
- FWCI
- 3.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Environmental Health Sciences (ES 06198, P01ES006198)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Keywords
- luteal phase deficiency, anovulation, female runners, follicle-stimulating hormone, luteal phase, follicular phase, pregnanediol-3-glucuronide, estrone conjugates, ovulation, exercise-induced amenorrhea, urinary hormone excretion, sedentary women
- MeSH terms
- Adolescent, Adult, Anovulation, Energy Intake, Energy Metabolism, Estrogens, Female, Follicular Phase, Follicle Stimulating Hormone, Humans, Luteal Phase, Menstrual Cycle, Nutritional Physiological Phenomena, Physical Education and Training, Progesterone, Recreation, Running
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