Cited by 539Hypothalamic control of reproductive hormonesOvarian function and disordersRegulation of Appetite and Obesity

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Low energy availability, not stress of exercise, alters LH pulsatility in exercising women

Loucks, A. B., Verdun, M., Heath, E. M., (With the Technical Assistance of T. Law, Sr. and J. R. Thuma)·1998·Journal of Applied Physiology

DOI 10.1152/jappl.1998.84.1.37

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Abstract

We tested two hypotheses about the disruption of luteinizing hormone (LH) pulsatility in exercising women by assaying LH in blood samples drawn at 10-min intervals over 24 h from nine young, habitually sedentary, regularly menstruating women on days 8, 9, or 10 of two menstrual cycles after 4 days of intense exercise [E = 30 kcal.kg lean body mass (LBM)-1.day-1 at 70% of aerobic capacity]. To test the hypothesis that LH pulsatility is disrupted by low energy availability, we controlled the subjects' dietary energy intakes (I) to set their energy availabilities (A = I - E) at 45 and 10 kcal.kg LBM-1.day-1 during the two trials. To test the hypothesis that LH pulsatility is disrupted by the stress of exercise, we compared the resulting LH pulsatilities to those previously reported in women with similar controlled energy availability who had not exercised. In the exercising women, low energy availability reduced LH pulse frequency by 10% (P 0.4). During exercise, the proportion of energy derived from carbohydrate oxidation was reduced from 73% while A = 45 kcal.kg LBM-1.day-1 to 49% while A = 10 kcal.kg LBM-1.day-1 (P < 0.0001). These results contradict the hypothesis that LH pulsatility is disrupted by exercise stress and suggest that LH pulsatility in women depends on energy availability.

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Metabolic fuels and reproduction in female mammals
Wade, G. N., & Schneider, J. E. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80183-6 · Cited by 686
Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women
Loucks, A. B. (1994) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.78.4.910 · Cited by 174
Self-citation
Effect of low blood glucose on plasma CRF, ACTH, and cortisol during prolonged physical exercise
Tabata, I., Ogita, F., Miyachi, M., & Shibayama, H. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.71.5.1807 · Cited by 83 · cited 1×
“It is particularly noteworthy, therefore, that carbohydrate administration during prolonged exercise prevents the usual exerciseinduced rise in cortisol levels in both rats (26) and men (27).”
Background

Show all 0 references

Research works printed but not linked: 27

10.1210/jcem-68-2-301 · DOI · Paper page
10.1095/biolreprod44.6.945 · DOI
10.1152/jappl.1995.79.1.194 · DOI
10.1001/jama.1992.03480090092034 · DOI · Paper page
Counts D. R., 1992, J. Clin. Endocrinol. Metab., 75, 762
Judd S. J., 1995, J. Clin. Endocrinol. Metab., 80, 818
10.1210/jcem-42-6-1031 · DOI
10.1210/endo.132.5.8477640 · DOI
10.1210/jcem-64-4-755 · DOI
Laughlin G. A., 1996, J. Clin. Endocrinol. Metab., 81, 4301
Loucks A. B., 1993, Am. J. Physiol., 264, R924
Loucks A. B., 1994, Am. J. Physiol., 266, R817
Loucks A. B., 1994, J. Clin. Endocrinol. Metab., 78, 910
10.1249/00005768-198502000-00010 · DOI
Loucks A. B., 1992, J. Clin. Endocrinol. Metab., 75, 514
10.1210/jcem-68-2-402 · DOI
10.1097/00000441-199303000-00001 · DOI
Olson B. R., 1995, J. Clin. Endocrinol. Metab., 80, 1187
10.1095/biolreprod45.4.523 · DOI · Paper page
10.1016/0026-0495(91)90231-K · DOI
10.1210/endo-25-4-615 · DOI
10.2165/00007256-198704010-00004 · DOI
10.1152/jappl.1990.69.3.989 · DOI
10.1111/j.1365-2265.1977.tb03347.x · DOI
10.1152/jappl.1972.32.5.712 · DOI
Wade G. N., 1996, Am. J. Physiol., 270, E1
10.1249/00005768-199510000-00007 · DOI

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Self-citation
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Background
Nutrition, santé et performance du sportif d’endurance
Rousseau, A. (2022) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2021.11.004 · Cited by 2
A new action of peptide hormones for survival in a low-nutrient environment.
Sato, T., Nemoto, T., Hasegawa, K., Ida, T., & Kojima, M. (2019) · Endocrine journal · doi:10.1507/endocrj.ej19-0274 · Cited by 2
“For example, limiting energy intake in non-athlete women who regularly menstruate has resul‐ ted in increases in GH with decreases in IGF-1 [44, 45].”
Background
Acute hypothalamic suppression significantly affects trabecular bone but not cortical bone following recovery and ovariectomy surgery in a rat model
Yingling, V., Mitchell, K., & Lunny, M. (2016) · PeerJ · doi:10.7717/peerj.1575 · Cited by 2
“Conclusion: These data suggest that following a transient delay in pubertal onset, trabecular bone volume was significantly lower and no restoration of bone volume occurred following recovery or post-OVX surgery.”
Background
The relationship between postural stability sway, balance, and injury in adolescent female soccer players in the eThekwini district of KwaZulu-Natal
Koenig, J. (2014) · doi:10.51415/10321/1108 · Cited by 2
Clinical review: Cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women.
O'Donnell, E., Goodman, J., & Harvey, P. (2011) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2011-1223 · Cited by 2
The Relationship Between Within-Day Energy Balance and Menstruation in Active Females: 743
Friel, A. J., & Benardot, D. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000402875.10880.50 · Cited by 2
“It is not definitively known why athletes under-consume energy, but it is possible that athletes find it difficult to take in food in such large amounts or do so in a purposeful attempt to modify body composition (Loucks et al., 1998).”
Background
Frau und Sport
Wolf, A. (2010) · Gynäkologische Endokrinologie · doi:10.1007/s10304-010-0370-1 · Cited by 2
Oral Contraceptives and Bone Health in Female Runners
Kelsey, J. (2006) · doi:10.21236/ada400469 · Cited by 2
“Botii oligo/amenorrhea and disordered eating have been associated with low serum estrogen concentrations (25,49,50), which would be expected to have an adverse effect on BMD.”
Background
Influence of moderate physical activity, including physical activity during menstruation, on the course of menstrual cycle among nullipara — an attempt to evaluate
Szpak, A. (2021) · Health Promotion & Physical Activity · doi:10.5604/01.3001.0015.2814 · Cited by 2
“It is often associated with patterns of dietary decisions or mental health [8-10].”
Background
Exercise and the Hypothalamus: Ovulatory Adaptations
Liu, A. Y., Petit, M. A., & Prior, J. C. (2020) · Contemporary Endocrinology · doi:10.1007/978-3-030-33376-8_8 · Cited by 9
Sport and Menses
Hirschberg, A. (2019) · Encyclopedia of Endocrine Diseases · doi:10.1016/b978-0-12-801238-3.64954-1 · Cited by 2
Hormonal and Reproductive Changes Associated with Physical Activity and Exercise
Gibbs, J. C., Mallinson, R. J., & Souza, M. J. D. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3402-7_12 · Cited by 2
Impact of Physical Activity and Exercise on Female Reproductive Potential
Mallinson, R. J., Gibbs, J., & Souza, M. D. D. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3402-7_11 · Cited by 2
Nutrients, Health and Chronic Disease in Masters Athletes
Caterson, I., Gifford, J., O'Connor, H., & Honey, A. (2015) · doi:10.1201/b17541-13 · Cited by 2
Hormonal Regulations of the Effects of Exercise on Bone: Positive and Negative Effects
Chilibeck, P. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-314-5_14 · Cited by 2
Reproductive Changes and the Endurance Athlete
Loucks, A. B. (2000) · Wiley eBooks · doi:10.1002/9780470694930.ch49 · Cited by 2
Self-citation
From Routine Blood Tests to Metabolomics: A Contextual Framework for Interpreting Biomarkers of Training Load, Recovery, and Metabolic Stress in Athletes
Muñoz-López, M., Quesada-Fernández, G., Sancho-Haro, E. S., Viúdez, X. R. D. L. P., Baz-Valle, E., López‐Gil, J. F., & Tornero-Aguilera, J. F. (2026) · Metabolites · doi:10.3390/metabo16070483
Androgen levels of premenopausal females are not observably associated with body composition and physical performance, but may interact with hormonal contraceptive use
Salmi, V. M., Karppinen, J. E., Piltonen, T., Kyröläinen, H., Hulmi, J., Ihalainen, J., & Mikkonen, R. (2025) · European Journal of Applied Physiology · doi:10.1007/s00421-025-05993-x · Cited by 1
“Potential confounders, such as physical activity and diet, which may affect hormone concentrations (Ennour-Idrissi et al. 2015; Hulmi et al. 2017; Loucks et al. 1998; Loucks and Thuma 2003), body composition (Dupuit et al. 2020; Gao et al. 2016; Hays et al. 2025; Mouad et al. 2025; Nolte et al.…”
The Women’s Tennis Association (WTA) Multidisciplinary Education and Treatment Protocol for the Female Athlete Triad (1996–2022)
Ricker, E. A., Koltun, K. J., Otis, C., Peavler, A. S., & Souza, M. D. D. (2025) · Sports · doi:10.3390/sports13070205 · Cited by 1
“Causal evidence obtained through human [5–7] and animal studies [8,9] has demonstrated that ED/LEA is the underlying cause of menstrual disturbances and poor bone health in women with the Triad [1,2].”
Male Endurance Athletes: Examination of Energy and Carbohydrate Availability and Hormone Responses
Moore, E. M., Drenowatz, C. J., Williams, B. T., Brodrick, T. C., Stodden, D. F., & Torres-McGehee, T. M. (2024) · Nutrients · doi:10.3390/nu16213729 · Cited by 2
“Based on previous literature by Loucks et al. [41] and Koehler et al. [15], an effect size between 1.0 and 3.0 was indicated, requiring a sample size of 2–16 subjects.”
MethodInfluential
Modified activity-based anorexia paradigm dampens chronic food restriction-induced hyperadiponectinemia in adolescent female mice
Kuriyama, T., Murata, Y., Ohtani, R., Yahara, R., Nakashima, S., Mori, M., Ohe, K., Mine, K., & Enjoji, M. (2023) · PLoS ONE · doi:10.1371/journal.pone.0289020 · Cited by 1
Adolescence is characterized by more sedentary behavior and less physical activity even 4 among highly active forager-farmersPreprint
Caldwell, A., Cummings, D. K., Hooper, P. L., Trumble, B., Gurven, M., Stiegltz, J., Davis, H. E., & Kaplan, H. (2023) · medRxiv · doi:10.1101/2023.03.15.23287308 · Cited by 1
The Impact of Hyperthecosis on Sporting Performance of Female Players
Zara, S., Sattar, S., Tabassum, Y., Akhtar, S., & Shafqat, M. (2021) · Journal of Pharmaceutical Research International · doi:10.9734/jpri/2021/v33i58b34176 · Cited by 1
“These findings suggest that higher T levels can enhance sporting performance in females, to levels more comparable to male physiology, and raises questions on how to ensure fairness of competition in female athletes [35].”
Background
Commentary in Response to “A Review of Nonpharmacological Strategies in the Treatment of Relative Energy Deficiency in Sport”
Strock, N. C. A., Koltun, K. J., & Ricker, E. A. (2021) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2021-0084 · Cited by 1
“1 International Journal of Sport Nutrition and Exercise Metabolism, (Ahead of Print) https://doi.org/10.1123/ijsnem.2021-0084 © 2021 Human Kinetics, Inc. LETTER TO THE EDITOR Unauthenticated | Downloaded 06/01/21 03:33 AM UTC (Areta et al., 2021; Burke et al., 2018), it is equally important to discuss how the EA thres…”
BackgroundInfluential
The Clinical Aspects of Energy Balance Disorders in Physical Excercise
Brel, Y. (2019) · Health and Ecology Issues · doi:10.51523/2708-6011.2019-16-1-1 · Cited by 1
Low Energy Availability in a Sleep-Low Training Study.
Mettler, S., Müller, B., & Haudum, J. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001360 · Cited by 1
“mass per day that results in a disruption of sex hormones (1).”
Background
The Effectiveness of the Female Athlete Triad in Identifying Athletes’ Potential Risk of Long Term Health Consequences
Volberding, J., Tapps, T., Hawkey, M. J., & Tapps, C. (2017) · doi:10.17265/2332-7839/2017.03.001 · Cited by 1
“Even minor diminished bone health causes the female athlete to be prone to increase in injuries, susceptible to stress fractures and osteoporotic fractures later in life [28, 39].”
Background
Hypothalamic Amenorrhea: Causes, Complications, & Controversies
Collins, T., & Rompolski, K. L. (2017) · Journal of Student Research · doi:10.47611/jsr.v6i1.288 · Cited by 1
Når kroppsfokus blir patologisk
Mathisen, T. F., & Olsen, T. (2016) · Norsk tidsskrift for ernæring · doi:10.18261/ntfe.14.3.2 · Cited by 1
Female athletes and health
Malara, M., & Lutosławska, G. (2016) · Biomedical Human Kinetics · doi:10.1515/bhk-2016-0012 · Cited by 2
“However, a close association was shown between a disturbed sex hormonal profile and low energy availability (energy intake reduced by energy expenditure) in women who engaged in strenuous physical activity [31, 34, 63].”
Background

Authors: Loucks, A. B., Verdun, M., Heath, E. M., & (With the Technical Assistance of T. Law, S. A. J. R. T.
Affiliations: Ohio University (US)
Venue: Journal of Applied Physiology
Publisher: American Physiological Society
Published: 1998-01-01
Volume: 84
Issue: 1
Pages: 37-46
ISSN: 0161-7567 (ISSN-L)
8750-7587
1522-1601
DOI: 10.1152/jappl.1998.84.1.37
OpenAlex: W2136430560
Cited by: 539
References: 0
Citations by year: 2026: 18 · 2025: 19 · 2024: 20 · 2023: 29 · 2022: 18 · 2021: 32 · 2020: 31 · 2019: 21 · 2018: 17 · 2017: 22 · 2016: 32 · 2015: 6 · 2014: 28 · 2013: 20 · 2012: 10
FWCI: 12.66
Type: journal article
Language: en
Open access: closed
Locations: Journal of Applied Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (1r55hd029547-01)
National Center for Research Resources (M01-RR-00034, M01RR000034)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (1R55-HD-29547-01)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: luteinizing hormone, LH pulsatility, energy availability, exercise stress, high-intensity exercise, menstrual cycle, LH pulse frequency, LH pulse amplitude, carbohydrate oxidation, caloric restriction, women
MeSH terms: Adolescent, Adult, Blood Glucose, Energy Metabolism, Follicle Stimulating Hormone, Humans, Luteinizing Hormone, Male, Growth Hormone, Stress, Physiological, Exercise

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Low energy availability, not stress of exercise, alters LH pulsatility in exercising women

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