Low energy availability, not stress of exercise, alters LH pulsatility in exercising women
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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The concept of the LEA threshold (30 kcal/kg FFM/day), below which health problems occurred, was based on short-term laboratory studies in a small sample of sedentary females.
“The concept of the LEA threshold (30 kcal/kg FFM/day), below which health problems occurred, was based on elegant but short-term laboratory studies that investigated stepwise changes in EA, perturbations of sex hormones 45 127 128 and changes in markers of bone turnover 125 in a small sample of sedentary females.”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [127]
Studies of LEA exposure have identified a somewhat more prominent effect of poor EI, rather than excessive EEE, in causing most of the physiological perturbations.
“Studies of LEA exposure have identified a somewhat more prominent effect of poor EI, rather than excessive EEE, in causing most of the physiological perturbations.127 160”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [127]
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“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).”
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Hoch, A., Papanek, P., Szabo, A., Widlansky, M. E., Schimke, J., & Gutterman, D. (2011) · Clinical Journal of Sports Medicine · doi:10.1097/jsm.0b013e3182042a9a · Cited by 105 · see citing works
“Energy availability is the amount of dietary energy remaining for other bodily functions after exercise energy expenditure(1,4) and has been demonstrated to be the key in terms of initiating the neuroendocrine cascade associated with the triad.(1,4) Energy intake was determined from a prospective 3-day food diary reco…”
BackgroundSouza, M. D. D., & Williams, N. (2005) · Current sports medicine reports · doi:10.1097/01.csmr.0000306070.67390.cb · Cited by 101 · see citing works
Benardot, D. (2005) · Human Kinetics eBooks · doi:10.5040/9781718220973 · Cited by 99 · see citing works
Dipla, K., Kraemer, R., Constantini, N., & Hackney, A. C. (2020) · HORMONES · doi:10.1007/s42000-020-00214-w · Cited by 98 · see citing works
“showed that the stress of exercise alone did not reduce LH pulse frequency nor did it increase LH pulse amplitude in exercising women [15].”
BackgroundInfluentialWithin-Day Energy Deficiency and Metabolic Perturbation in Male Endurance Athletes.
Torstveit, M. K., Fahrenholtz, I., Stenqvist, T. B., Sylta, O., & Melin, A. (2018) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2017-0337 · Cited by 97 · see citing works
Physiological factors associated with low bone mineral density in female endurance runners
Burrows, M. P., Nevill, A., Bird, S., & Simpson, D. (2003) · British Journal of Sports Medicine · doi:10.1136/bjsm.37.1.67 · Cited by 97
Negative Consequences of Low Energy Availability in Natural Male Bodybuilding: A Review.
Fagerberg, P. (2017) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2016-0332 · Cited by 96 · see citing works
“EEE easily gets confused with TEE during exercise and by subtracting NEEE from TEE during exercise, the error in EEE estimations can be minimized—as done in this review (Loucks, 2014; Loucks et al., 1998).”
BackgroundMethodResultInfluentialO'Leary, T., Wardle, S., & Greeves, J. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00142 · Cited by 95 · see citing works
“The suppressed pulsatile release of gonadotropin-releasing hormone from the hypothalamus, decreases LH pulse frequency from the pituitary, and results in low circulating oestradiol (15, 16).”
BackgroundPollock, N., Grogan, C., Perry, M., Pedlar, C., Cooke, K., Morrissey, D., & Dimitriou, L. (2010) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.20.5.418 · Cited by 95 · see citing works
“Unfortunately, we do not have data on the athletes’ energy intake or expenditure and are therefore unable to confirm the work of Loucks et al. (1998), who noted that the underpinning pathology is not the stress of training but the association with low energy availability.”
BackgroundThe Unexplored Crossroads of the Female Athlete Triad and Iron Deficiency: A Narrative Review
Petkus, D. L., Murray-Kolb, L. E., & De Souza, M. J. (2017) · Sports Medicine · doi:10.1007/s40279-017-0706-2 · Cited by 92 · see citing works
Arends, J., Cheung, M.-Y. C., Barrack, M., & Nattiv, A. (2012) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.22.2.98 · Cited by 91 · see citing works
“When counseling athletes with FHA and oligomenorrhea, it is important to emphasize that intentional caloric restriction is not necessary to lead to poor energy availability, and hunger is an insensitive measure of how many calories are needed (Loucks et al., 1998).”
BackgroundInfluentialCialdella-Kam, L., Guebels, C. P., Maddalozzo, G., & Manore, M. (2014) · Nutrients · doi:10.3390/nu6083018 · Cited by 90 · see citing works
Souza, M. D. D., Williams, N., Nattiv, A., Joy, E., Misra, M., Loucks, A., Matheson, G., Olmsted, M., Barrack, M., Mallinson, R. J., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2014-093958 · Cited by 90 · see citing works
Self-citationExercise-Related Leg Pain in Female Collegiate Athletes
Reinking, M. F. (2006) · American Journal of Sports Medicine · doi:10.1177/0363546506287298 · Cited by 90 · see citing works
“The stimulus for the development of menstrual abnormalities and subsequent bone demineralization is currently thought to be a negative energy balance state, in which the athlete is expending more calories than she is consuming.(29,49,63) Although no difference in FAST scores was found between athletes with and without…”
BackgroundPhysical activity and its effects on reproduction
Redman, L. M. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61183-2 · Cited by 103 · see citing works
“In comparison to eumenorrhoeic women, athletes with amenorrhoea produce low levels of both oestrogen and progesterone each day, indicating a complete absence of follicular development, ovulation and luteal function (Loucks et al., 1998).”
BackgroundAllaway, H. C. M., Southmayd, E. A., & De Souza, M. J. (2016) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2015-0053 · Cited by 89 · see citing works
Leptin concentrations experience a delayed reduction after resistance exercise in men
NINDL, B. C., KRAEMER, W. J., ARCIERO, P. J., SAMATALLEE, N., LEONE, C. D., MAYO, M. F., & HAFEMAN, D. L. (2002) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200204000-00008 · Cited by 87 · see citing works
Metabolic Fuel and Clinical Implications for Female Reproduction
Mircea, C. N., Lujan, M. E., & Pierson, R. A. (2007) · Journal of Obstetrics and Gynaecology Canada · doi:10.1016/s1701-2163(16)32661-5 · Cited by 86 · see citing works
Menstrual irregularity and musculoskeletal injury in female high school athletes.
Thein-Nissenbaum, J., Rauh, M., Carr, K., Loud, K., & McGuine, T. (2012) · Journal of athletic training · doi:10.4085/1062-6050-47.1.74 · Cited by 86 · see citing works
Low energy availability in female athletes: from the lab to the field
Heikura, I. A., Stellingwerff, T., & Areta, J. L. (2022) · European Journal of Sport Science · doi:10.1080/17461391.2021.1915391 · Cited by 84 · see citing works
“…main cause of functional hypothalamic amenorrhea and disrupts normal endocrine responses during the early follicular phase, such as reducing pulse frequency and increased pulse amplitude of luteinizing hormone (LH) (Loucks, 2006; Loucks & Thuma, 2003; Loucks & Verdun, 1998; Loucks et al., 1998).”
BackgroundResultInfluentialExercise, Training, and the Hypothalamic-Pituitary-Gonadal Axis in Men and Women
Sokoloff, N. C., Misra, M., & Ackerman, K. (2016) · Frontiers of Hormone Research · doi:10.1159/000445154 · Cited by 83 · see citing works
“Changes in LH pulse frequency and amplitude were noted in both energy-restricted states, but LH pulse frequency was less decreased when equivalent energy deficiency was achieved mostly from exercise [75].”
BackgroundO'Donnell, E., Harvey, P., Goodman, J., & Souza, M. D. D. (2007) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00547.2006 · Cited by 82 · see citing works
“Since endothelial dysfunction is considered to be an important permissive factor for the development of atherosclerosis, short or long-term impairment of endothelial function in women with EAA may translate into increased long-term cardiovascular risk.”
InfluentialVescovi, J. D., Jamal, S. A., & De Souza, M. J. (2008) · Osteoporosis International · doi:10.1007/s00198-007-0518-6 · Cited by 81 · see citing works
LH secretion and testosterone concentrations are blunted after resistance exercise in men.
Nindl, B., Kraemer, W., Deaver, D., Peters, J. L., Marx, J. O., Heckman, J., & Loomis, G. A. (2001) · Journal of applied physiology · doi:10.1152/jappl.2001.91.3.1251 · Cited by 81 · see citing works
“Our finding of a reduced LH secretion after exercise further extends the results from previous investigations in women (18, 33).”
BackgroundResultInfluentialMedical Concerns in the Female Athlete
Committee on Sports Medicine and Fitness (2000) · PEDIATRICS · doi:10.1542/peds.106.3.610 · Cited by 80 · see citing works
Physical Activity And Risk of Hot Flashes among Women in Midlife
Whitcomb, B., Whiteman, M., Langenberg, P., Flaws, J., & Romani, W. (2007) · Journal of Women's Health · doi:10.1089/jwh.2006.0046 · Cited by 77 · see citing works
Beals, K., & Meyer, N. (2007) · Clinics in Sports Medicine · doi:10.1016/j.csm.2006.11.002 · Cited by 77 · see citing works
Hooper, D. R., Kraemer, W. J., Saenz, C., Schill, K. E., Focht, B. C., Volek, J. S., & Maresh, C. M. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3623-z · Cited by 76 · see citing works
“, inadequate energy intake to support high levels of physical activity) demonstrate reduced LH pulsatility (Loucks et al. 1998), which leads to amenorrhea and can eventually lead to osteoporosis.”
Jagim, A., Fields, J., Magee, M., Kerksick, C., & Jones, M. T. (2022) · Nutrients · doi:10.3390/nu14050986 · Cited by 76 · see citing works
“[25,26] observed disruptions in luteinizing hormone pulsatility and low triiodothyronine-3 (T3) levels [27] at a threshold of energy availability, whereas Reed et al.”
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
- 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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