Luteinizing Hormone Pulsatility Is Disrupted at a Threshold of Energy Availability in Regularly Menstruating Women
Abstract
To investigate the dependence of LH pulsatility on energy availability (dietary energy intake minus exercise energy expenditure), we measured LH pulsatility after manipulating the energy availability of 29 regularly menstruating, habitually sedentary, young women of normal body composition for 5 d in the early follicular phase. Subjects expended 15 kcal/kg of lean body mass (LBM) per day in supervised exercise at 70% of aerobic capacity while consuming a clinical dietary product to set energy availability at 45 and either 10, 20, or 30 kcal/kg LBM.d in two randomized trials separated by at least 2 months. Blood was sampled daily during treatments and at 10-min intervals for the next 24 h. Samples were assayed for LH, FSH, estradiol (E2), glucose, beta-hydroxybutyrate, insulin, cortisol, GH, IGF-I, IGF-I binding protein (IGFBP)-1, IGFBP-3, leptin, and T3. LH pulsatility was unaffected by an energy availability of 30 kcal/kg LBM.d (P > 0.3), but below this threshold LH pulse frequency decreased, whereas LH pulse amplitude increased (all P < 0.04). This disruption was more extreme in women with short luteal phases (P < 0.01). These incremental effects most closely resembled the effects of energy availability on plasma glucose, beta-hydroxybutyrate, GH, and cortisol and contrasted with the dependencies displayed by the other metabolic hormones (simultaneously P < 0.05). These results demonstrate that LH pulsatility is disrupted only below a threshold of energy availability deep into negative energy balance and suggest priorities for future investigations into the mechanism that mediates the nonlinear dependence of LH pulsatility on energy availability.
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Low energy availability occurs when energy intake is less than energy expenditure through exercise, leaving insufficient energy to sustain physiological functions outside of exercise.
“Low energy availability (LEA) is the underlying etiology of relative energy deficiency in sport (RED-S) [114] and occurs when energy intake is less than energy expenditure through exercise. As a result, the body does not have enough energy left to appropriately sustain physiological functions outside of exercise [63,64].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [63]
Specific guidelines for an optimal energy availability for competitive female athletes have not been established.
“Specific guidelines for an optimal EA for competitive female athletes have not been established”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [63]
Conceptual models of energy availability thresholds have been proposed from well-controlled laboratory studies.
“conceptual models of energy availability thresholds have been proposed from well-controlled laboratory studies [63–65].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [63]
Most LEA intervention studies are accompanied by a substantial reduction (25%-60%) in carbohydrate ingestion, resulting in concurrent LCA.
“Most LEA intervention studies are also accompanied by a substantial reduction (25%-60%, depending on magnitude of LEA) in carbohydrate (CHO) ingestion, resulting in concurrent LCA.”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [45]
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 [45]
Seminal research around EA in habitually sedentary females identified a continuum of zones ranging from low to high risk of harm (eg, high EA for mass gain and growth ≥45 kcal/kg FFM/day; adequate EA for weight maintenance and support of body function = ~45 kcal/kg FFM/day; reduced EA for body...).
“Seminal research 45 125 around EA in habitually sedentary females identified a continuum of zones ranging from low to high risk of harm (eg, high EA for mass gain and growth ≥45 kcal/kg FFM/day; adequate EA for weight maintenance and support of body function = ~45 kcal/kg FFM/day; reduced EA for body”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [45]
Most intervention studies assessing low energy availability in athletes are also accompanied by a considerable reduction in carbohydrate intake, approximately 25-60% depending on the magnitude of low energy availability.
“Most intervention studies assessing LEA in athletes are also accompanied by a considerable reduction in CHO intake (approximately 25–60% reduction in CHO, depending on the magnitude of LEA) [16,23,24,25].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [23]
There is a dose-dependent effect of low energy availability on carbohydrate availability, and dietary restriction is detrimental to the use of carbohydrate during activity.
“These data demonstrate that there is a dose-dependent effect of LEA on CHO availability and that dietary restriction is detrimental to the use of CHO during activity [23].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [23]
Few studies have attempted to define carbohydrate availability; one study calculated carbohydrate availability as the difference between dietary carbohydrate intake and the amount of carbohydrate oxidized during exercise beyond the requirements of normal activity.
“Few studies have attempted to define CHO availability; however, one study calculated CHO availability as the difference between dietary CHO intake and the amount of CHO oxidized during exercise beyond the requirements of normal activity [23].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [23]
Restricted energy availability conditions due to reduced energy intake of 10, 20, and 30 kcal/kg lean body mass/day reduced carbohydrate availability by approximately 80%, 60%, and 40%, respectively.
“Restricted EA conditions, due to reduced energy intake, of 10 kcal/kg LBM/day, 20 kcal/kg LBM/day, 30 kcal/kg LBM/day, reduced CHO availability by approximately 80%, 60%, and 40%, respectively [23].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [23]
LH pulsatility may depend on CHO as opposed to EA, as evidenced by disruption to LH pulsatility at a level of CHO availability between 90-130 g/d of glucose.
“Furthermore, luteinizing hormone (LH) pulse frequency suggests that LH pulsatility may depend on CHO as opposed to EA, as evidenced by disruption to LH pulsatility at a level of CHO availability between 90–130 g/d of glucose [23,45].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [23]
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International society of sports nutrition position stand: nutritional concerns of the female athlete
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“tility is observed after as little as 5 days in healthy females [64,65,129,140,141].”
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Low‐energy density and high fiber intake are dietary concerns in female endurance athletes
Melin, A., Tornberg, Å. B., Skouby, S., Møller, S. S., Faber, J., Sundgot‐Borgen, J., & Sjödin, A. (2016) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.12516 · Cited by 89 · see citing works
Energy availability discriminates clinical menstrual status in exercising women
Reed, J. L., De Souza, M. J., Mallinson, R. J., Scheid, J. L., & Williams, N. I. (2015) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-015-0072-0 · Cited by 86 · see citing works
Low energy availability in female athletes: from the lab to the field
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Low Energy Availability in Exercising Women: Historical Perspectives and Future Directions
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Low Energy Availability, Plasma Lipids, and Hormonal Profiles of Recreational Athletes
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Low Energy Availability and Relative Energy Deficiency in Sport: What Coaches Should Know
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Is RED-S in athletes just another face of malnutrition?
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- Authors
- Loucks, A. B., & Thuma, J. R.
- Affiliations
- Ohio University (US)
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2003-01
- Volume
- 88
- Issue
- 1
- Pages
- 297-311
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2057490855
- Cited by
- 760
- References
- 53
- Citations by year
- 2026: 52 · 2025: 45 · 2024: 57 · 2023: 50 · 2022: 54 · 2021: 58 · 2020: 54 · 2019: 35 · 2018: 34 · 2017: 27 · 2016: 27 · 2015: 17 · 2014: 35 · 2013: 29 · 2012: 22
- FWCI
- 17.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (MO1 RR 00034, M01RR000034)
- 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 pulsatility, energy availability, negative energy balance, LH pulse frequency, LH pulse amplitude, short luteal phase, follicular phase, exercise energy expenditure, energy intake, young women, reproductive endocrinology, leptin, insulin-like growth factor I, cortisol, beta-hydroxybutyrate
- MeSH terms
- Adult, Body Weight, Circadian Rhythm, Energy Metabolism, Estradiol, Female, Follicle Stimulating Hormone, Hormones, Humans, Luteinizing Hormone, Menstrual Cycle, Pulsatile Flow, Sleep, Wakefulness, Carbohydrate Metabolism
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