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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Influential
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Dai, W., Liu, J., Qiu, Y., Teng, Z., Li, S., Huang, J., Xiang, H., Tang, H., Wang, B., Chen, J., et al. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110498 · Cited by 15
Characterizing the resting metabolic rate ratio in ovulatory exercising women over 12 months
Strock, N. C. A., Koltun, K. J., Mallinson, R. J., Williams, N. I., & Souza, M. J. D. (2020) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13688 · Cited by 17
Progesterone-Mediated Inhibition of the GnRH Pulse Generator: Differential Sensitivity as a Function of Sleep Status
Kim, S. H., Lundgren, J. A., Bhabhra, R., Collins, J. S. P., Patrie, J. T., Solorzano, C. M. B., Marshall, J. C., & McCartney, C. R. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02299 · Cited by 15
“preferentially reduced daytime LHpulse frequency (20, 21).”
Progesterone has rapid positive feedback actions on LH release but fails to reduce LH pulse frequency within 12 h in estradiol-pretreated women
Hutchens, E. G., Ramsey, K. A., Howard, L. C., Abshire, M. Y., Patrie, J. T., & McCartney, C. R. (2016) · Physiological Reports · doi:10.14814/phy2.12891 · Cited by 12
“2012) and other studies in late follicular phase women (Loucks and Heath 1994; Loucks et al. 1998).”
Result
The Female Athlete: Some Gynecologic Considerations
Pfeifer, S. M., & Patrizio, P. (2002) · Sports Medicine and Arthroscopy Review · doi:10.1097/00132585-200210010-00002 · Cited by 8
“Loucks et al.28 and Loucks and Heath7 studied the role of diet and exercise in supplying and reducing energy, respectively.”
BackgroundInfluential
Overtraining Syndrome in Athletes: A Comprehensive Review and Novel Perspectives
Cadegiani, F. (2020) · doi:10.1007/978-3-030-52628-3 · Cited by 13
Physiologic and Pathophysiologic Alterations of the Neuroendocrine Components of the Reproductive Axis
Nass, R. M., & Evans, W. S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00020-2 · Cited by 10
Exercise and the Hypothalamus. Ovulatory Adaptations
Petit, M., & Prior, J. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-314-5_8 · Cited by 13
Comparison of Bone Quality Among Winter Endurance Athletes with and Without Risk Factors for Relative Energy Deficiency in Sport (REDs): A Cross-Sectional Study
Wyatt, P. M., Drager, K., Groves, E. M., Stellingwerff, T., Billington, E., Boyd, S., & Burt, L. (2023) · Calcified Tissue International · doi:10.1007/s00223-023-01120-0 · Cited by 12
“, < 30 kcal/kg fat free mass/ day) [6], adverse bone health outcomes can occur.”
Background
Examination of Athlete Triad Symptoms Among Endurance-Trained Male Athletes: A Field Study
Moore, E. M., Drenowatz, C., Stodden, D. F., Pritchett, K., Brodrick, T. C., Williams, B. T., Goins, J. M., & Torres-McGehee, T. M. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.737777 · Cited by 11
“The regression equation for T and EA was not significant [F(1,23) = 3.”
Background
Multi-organ Transcriptome Atlas of a Mouse Model of Relative Energy Deficiency in Sport (REDs)
van Rosmalen, L., Zhu, J.-Y., Maier, G., Gacasan, E., Lin, T., Zhemchuzhnikova, E., Rothenberg, V., Razu, S. S., Deota, S., Ramasamy, R. K., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.08.001 · Cited by 11
Adolescence is characterized by more sedentary behaviour and less physical activity even among highly active forager-farmers
Caldwell, A. E., Cummings, D. K., Hooper, P. L., Trumble, B. C., Gurven, M., Stieglitz, J., Davis, H. E., & Kaplan, H. S. (2023) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2023.1764 · Cited by 12
Energy availability and RED-S risk assessment among Kho-Kho players in India
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“Energy deficits have been associated with compromised physiological functioning, with a four-day reduced LEA exhibiting reductions in reproductive hormones among female athletes [31].”
Background
Moderate Weight Loss is associated with Reductions in LH Pulse Frequency and Increases in 24-hour Cortisol with no change in Perceived Stress in Young Ovulatory Women.
Ruffing, K., Koltun, K. J., Souza, M. D. D., & Williams, N. (2022) · Physiology and Behavior · doi:10.1016/j.physbeh.2022.113885 · Cited by 11
Overtraining and the endocrine system—Part 2: Review of the scientific studies
Platen, P. (2002) · European Journal of Sport Science · doi:10.1080/17461390200072109 · Cited by 11
“They could already be demonstrated in female athletes in correlation with high training load and a simultaneous hypocaloric diet (25, 27).”
Background
Metabolic clues regarding the enhanced performance of elite endurance athletes from orchiectomy-induced hormonal changes
Atwood, C., & Bowen, R. L. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.08.037 · Cited by 12
“Recent studies have suggested that it is not so much the ‘stress’ of exercise, but low energy availability that lowers serum gonadotropins and sex steroids [87,96,97].”
Background
Low Energy Availability in Athletes
Kuikman, M. A., & Burke, L. M. (2023) · Nutrition Today · doi:10.1097/nt.0000000000000603 · Cited by 9
Health Considerations in Female Runners
Kim, B. Y., & Nattiv, A. (2015) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2015.08.011 · Cited by 12
“It is worth noting that, contrary to popular belief, the stress of exercise itself, independent of EA, does not alter LH pulsatility in women.(58)”
Persistence of Sleep-Associated Decrease in GnRH Pulse Frequency in the Absence of Gonadal Steroids
Shaw, N. D., Gill, S., Lavoie, H. B., Marsh, E. E., & Hall, J. E. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1188 · Cited by 12
Factors in the regulation of fertility in deprived populations
Rosetta, L., & Mascie-Taylor, C. G. (2009) · Annals of Human Biology · doi:10.1080/03014460903103921 · Cited by 10
Puberty and Athletic Sports in Female Adolescents
Klentrou, P. (2006) · Annales Nestlé (English ed ) · doi:10.1159/000093015 · Cited by 10
Methodological problems in studying the female athlete triad.
Loucks, A. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000218146.91864.b5 · Cited by 10
Self-citation
Female Athlete Triad
Lebrun, C. M., & Rumball, J. S. (2002) · Sports Medicine and Arthroscopy Review · doi:10.1097/00132585-200210010-00005 · Cited by 21
Overtraining the female athlete
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Physiology of Health and Performance: Enabling Success of Women in Combat Arms Roles.
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Does eating less or exercising more to reduce energy availability produce distinct metabolic responses?
Halsey, L. G., Areta, J. L., & Koehler, K. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0217 · Cited by 8
“The secretion of luteinizing hormone (LH), a key hormone responsible for the regulation of reproduction, by the anterior pituitary gland, was shown to be affected by low energy availability, and independently of the presence of exercise [58], with decreasing levels of energy availability showing more profound alterati…”
Background
Amenorrhea and oligomenorrhea risk related to exercise training volume and intensity: Findings from 3705 participants recruited via the STRAVA™ exercise application.
Baranauskas, M. N., Freemas, J. A., Carter, S. J., Blodgett, J. M., Pedlar, C., & Bruinvels, G. (2023) · Journal of Science and Medicine in Sport · doi:10.1016/j.jsams.2023.07.001 · Cited by 9
Bone parameters of elite athletes with oligomenorrhea and prevalence seeking medical attention: a cross-sectional study
Tsukahara, Y., Torii, S., Yamasawa, F., Iwamoto, J., Otsuka, T., Goto, H., Kusakabe, T., Matsumoto, H., & Akama, T. (2021) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-021-01234-1 · Cited by 9

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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