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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Impact of a 4-Week Intensified Endurance Training Intervention on Markers of Relative Energy Deficiency in Sport (RED-S) and Performance Among Well-Trained Male Cyclists
Stenqvist, T. B., Torstveit, M. K., Faber, J., & Melin, A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.512365 · Cited by 43
“Clinical trials exposing eumenorrheic females to low energy availability (<30 kcal·kg−1 FFM·day−1) for only 5 days found reductions in levels of insulinlike growth factor-1 (IGF-1), leptin, insulin, triiodothyronine (T3), and luteinizing hormone (12, 14).”
Background
The path towards progress: a critical review to advance the science of the female and male athlete Triad and relative energy deficiency in sport
De Souza, M. J., Strock, N. C. A., Ricker, E. A., Koltun, K. J., Barrack, M., Joy, E., Nattiv, A., Hutchinson, M., Misra, M., & Williams, N. I. (2022) · Sports Medicine · doi:10.1007/s40279-021-01568-w · Cited by 39
Disordered eating and eating disorders in aquatic sports.
Melin, A., Torstveit, M. K., Burke, L., Marks, S., & Sundgot-Borgen, J. (2014) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2014-0029 · Cited by 39
“In healthy young adults, the average energy intake for weight stable women has been reported to be ~189 ± 25 kJ/kg of FFM/ day (45 ± 6 kcal/kg of FFM/day; Loucks et al., 1998, 2011; Loucks & Thuma, 2003).”
Background
The influence of dance training on growth and maturation of young females: A mixed longitudinal study
Matthews, B., Bennell, K., McKay, H., Khan, K., Baxter-Jones, A., Mirwald, R., & Wark, J. (2006) · Annals of Human Biology · doi:10.1080/03014460600635951 · Cited by 39
“However, restricted linear growth in height may also be attributable to energy deficiencies, which may in turn affect hormone secretion (Smith et al. 1995; Loucks et al. 1998; Hilton and Loucks 2000).”
Background
Effects of intensive training on menstrual function and certain serum hormones and peptides related to the female reproductive system
Cho, G. J., Han, S. W., Shin, J., & Kim, T. (2017) · Medicine · doi:10.1097/md.0000000000006876 · Cited by 51
“dietary intake for the energy cost of exercise can have a profound suppressive effect on the reproductive axis.([24,25]) Although exact volume and intensity of training could not be measured in this study, all participants completed all of physical training.”
Background
Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction,,
Mitchell, D. M., Tuck, P., Ackerman, K., Sokoloff, N. C., Woolley, R., Slattery, M., Lee, H., Bouxsein, M., & Misra, M. (2015) · Bone · doi:10.1016/j.bone.2015.06.021 · Cited by 38
“excessive physical activity can lead to energy imbalance and functional hypothalamic oligo-amenorrhea [3].”
Metabolic Influences on Reproduction: Adiponectin Attenuates GnRH Neuronal Activity in Female Mice
Klenke, U., Taylor‐Burds, C., & Wray, S. (2014) · Endocrinology · doi:10.1210/en.2013-1677 · Cited by 40
“function and ovarian cyclicity (1, 2) or reducing fertility”
Background
Energy availability and infertility
Loucks, A. B. (2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3282f1cb6a · Cited by 46
Self-citation
Practical use of the International Olympic Committee Medical Commission Position Stand on the Female Athlete Triad: a case example.
Sherman, R., & Thompson, R. A. (2006) · International Journal of Eating Disorders · doi:10.1002/eat.20232 · Cited by 38
Effects of short-term strenuous endurance exercise upon corpus luteum function.
Williams, N., Bullen, B., Mcarthur, J., Skrinar, G., & Turnbull, B. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199907000-00006 · Cited by 38
Athletes’ and Coaches’ Perceptions of Nutritional Advice: Eating More Food for Health and Performance
Logue, D., Mahony, L., Corish, C., Tobin, D., Doherty, R., O’Higgins, G., & Madigan, S. (2021) · Nutrients · doi:10.3390/nu13061925 · Cited by 37
“Adequate energy intake is essential for maintaining normal reproductive function and bone health [6,7].”
Background
Maternal physical and sedentary activities in relation to reproductive outcomes following IVF
Gaskins, A., Williams, P. L., Keller, M. G., Souter, I., Hauser, R., & Chavarro, J. (2016) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2016.07.002 · Cited by 35
Despite a high prevalence of menstrual disorders, bone health is improved at a weight-bearing bone site in world-class female rhythmic gymnasts.
Maïmoun, L., Coste, O., Georgopoulos, N., Roupas, N., Mahadea, K., Tsouka, A., Mura, T., Philibert, P., Gaspari, L., Mariano-Goulart, D., et al. (2013) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2013-2794 · Cited by 35
Influence of Ghrelin and Adipocytokines on Bone Mineral Density in Adolescent Female Athletes with Amenorrhea and Eumenorrheic Athletes
Russell, M., & Misra, M. (2010) · Medicine and sport science/Medicine and sport · doi:10.1159/000321975 · Cited by 32
“Decreased energy availability can result from increased energy expenditure, decreased energy intake or both (20), and is associated with low fat mass and a suppression of the H-PG axis.”
Background
The female athlete triad: What’s a doctor to do?
Lebrun, C. (2007) · Current sports medicine reports · doi:10.1097/01.csmr.0000305620.72745.81 · Cited by 35
A Review of Nonpharmacological Strategies in the Treatment of Relative Energy Deficiency in Sport.
Kuikman, M., Mountjoy, M., Stellingwerff, T., & Burr, J. (2021) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2020-0211 · Cited by 34
“However, while LEA induced from low EI, as opposed to the direct stress of EEE per se, has been shown to alter LH pulsatility in normal weight sedentary females (Loucks et al., 1998), this may not be representative of the effect of chronic and extreme EEE on the hypothalamic–pituitary–gonadal (HPG) axis in well-traine…”
Background
Effects of Estrogen Replacement on Bone Geometry and Microarchitecture in Adolescent and Young Adult Oligoamenorrheic Athletes: A Randomized Trial
Ackerman, K., Singhal, V., Slattery, M., Eddy, K., Bouxsein, M., Lee, H., Klibanski, A., & Misra, M. (2019) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3887 · Cited by 34
Physiological Implications, Performance Assessment and Risk Mitigation Strategies of Women in Combat-Centric Occupations
Greeves, J. (2015) · Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000001116 · Cited by 34
“Low energy availability impairs bone health through 2 separate pathways: impaired reproductive function by neuroendrocine mechanisms (39), which suppresses estrogen production and up-regulates bone resorption (16); and, hepatic suppression of insulin-like growth factor 1 (IGF-1), which decreases bone formation (26).”
Background
Leptin and Endocrine Parameters in Marathon Runners
Bobbert, T., Mai, K., Brechtel, L., Schulte, H., Weger, B., Pfeiffer, A., Spranger, J., & Diederich, S. (2012) · International Journal of Sports Medicine · doi:10.1055/s-0031-1291251 · Cited by 34
Patterns of energy availability of free-living athletes display day-to-day variability that is not reflected in laboratory-based protocols: Insights from elite male road cyclists
Taylor, H. L., Garabello, G., Pugh, J. N., Morton, J. P., Langan‐Evans, C., Louis, J. B., Borgersen, R., & Areta, J. L. (2022) · Journal of Sports Sciences · doi:10.1080/02640414.2022.2115676 · Cited by 34
“Energy availability (EA) was calculated using the most recent definition of EA, [EA = (Energy Intake – Net Exercise Energy Expenditure)/Fat Free Mass] (Areta et al., 2021; Loucks et al., 1998).”
Method
A Displaced Femoral Neck Stress Fracture in an Amenorrheic Adolescent Female Runner
Goolsby, M. A., Barrack, M. T., & Nattiv, A. (2011) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738111429929 · Cited by 35
“gonadotropin-releasing hormone pulsatility and a subsequent decrease in luteinizing hormone, follicle-stimulating hormone, and estradiol—leads to the reversible suppression of menstrual function known as functional hypothalamic amenorrhea.(16,23,24) Therefore, the target of treatment for her menstrual dysfunction was…”
Background
Exercise and fertility: an update
Olive, D. (2010) · Current Opinion in Obstetrics and Gynecology · doi:10.1097/gco.0b013e32833c7227 · Cited by 32
Maturation of Sleep–Wake Gonadotrophin‐Releasing Hormone Secretion Across Puberty in Girls: Potential Mechanisms and Relevance to the Pathogenesis of Polycystic Ovary Syndrome
McCartney, C. R. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02029.x · Cited by 44
Knowledge, attitude, and skill of high school coaches with regard to the female athlete Triad
Pantano, K. J. (2017) · Journal of Pediatric and Adolescent Gynecology · doi:10.1016/j.jpag.2016.09.013 · Cited by 32
Physiological Mechanisms Integrating Metabolism and Reproduction
Krasnow, S. M., & Steiner, R. D. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50052-x · Cited by 33
Irisin: circulating levels in serum and its relation to gonadal axis
Luo, Y., Qiao, X., Xu, L., & Huang, G. (2022) · Endocrine · doi:10.1007/s12020-022-02981-5 · Cited by 30
“is generally accepted; this hypothesis holds that the imbalance between energy intake and energy expenditure is an important cause of menstrual disorders and that the inhibition of reproductive function is an adaptive response to reduced energy expenditure [88].”
Background
Prospective associations between physical activity and BMI with irregular periods and heavy menstrual bleeding in a large cohort of Australian women
Mena, G. P., Mielke, G. I., & Brown, W. J. (2021) · Human Reproduction · doi:10.1093/humrep/deab055 · Cited by 31
Bone Accrual in Oligo-Amenorrheic Athletes, Eumenorrheic Athletes and Non-Athletes
Singhal, V., Reyes, K., Pfister, B., Ackerman, K., Slattery, M., Cooper, K., Toth, A. T., Gupta, N., Goldstein, M., Eddy, K., et al. (2018) · Bone · doi:10.1016/j.bone.2018.05.010 · Cited by 30
“When energy intake is insufficient to meet the caloric needs of vigorous exercise, luteinizing hormone (LH) pulsatility is impacted resulting in a decline in estrogen production, a hormone known to inhibit bone resorption (16).”
Background
Polycystic ovary-like syndrome in adolescent competitive swimmers.
Coste, O., Paris, F., Galtier, F., Letois, F., Maïmoun, L., & Sultan, C. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.07.006 · Cited by 30
The female athlete triad and cardiovascular dysfunction.
Hoch, A., Lal, S., Jurva, J., & Gutterman, D. (2007) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2007.05.001 · Cited by 30
Influence of sports participation and menarche on bone mineral density of female high school athletes.
Barkai, H., Nichols, J., Rauh, M., Barrack, M., Lawson, M. J., & Levy, S. (2007) · Journal of Science and Medicine in Sport · doi:10.1016/j.jsams.2006.05.018 · Cited by 30
Energy availability is associated with luteinizing hormone pulse frequency and induction of luteal phase defects.
Koltun, K. J., Souza, M. D. D., Scheid, J., & Williams, N. (2019) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/clinem/dgz030 · Cited by 30

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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