The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.
Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women
Open accessAbstract
Because the effect of exercise on leptin was not established, we controlled energy intake (I) and exercise energy expenditure (E) to distinguish the independent effects of energy availability (A = I − E) and exercise stress (everything associated with exercise except its energy cost) on the diurnal leptin rhythm in healthy young women. In random order, we set A = 45 and 10 kcal ⋅ kg lean body mass−1(LBM) ⋅ day−1 for 4 days during the early follicular phase of separate menstrual cycles in sedentary (S, n = 7) and exercising (X, n = 9: E = 30 kcal ⋅ kg LBM−1 ⋅ day−1) women. Low energy availability suppressed the 24-h mean ( P < 10−6) and amplitude ( P < 10−5), whereas exercise stress did not (both P> 0.2). Suppressions of the 24-h mean (−72 ± 3 vs. −53 ± 3%, P < 0.001) and amplitude (−85 ± 3 vs. −58 ± 6%, P < 0.001) were more extreme in S vs. X than previously reported effects on luteinizing hormone pulsatility and carbohydrate availability. Thus the diurnal rhythm of leptin depends on energy, or carbohydrate, availability, not intake, and exercise has no suppressive effect on the diurnal rhythm of leptin beyond the impact of its energy cost on energy availability.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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 [160]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In this same study, leptin levels decreased by 50% in response to dietary restriction, and this difference is proportional to the reductions in CHO intake [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 [45]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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 [45]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“it has been demonstrated that skeletal muscle alters its fuel source in response to LEA conditions, oxidizing less CHO and more fat during exercise [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 [45]
The cited source says what the claim attributes to it.
In the citing paper
“In two conditions of identical LEA (with one achieved from dietary restriction and the other one achieved from exercise), CHO availability was 57% higher in women who reduced EA via exercise compared to reduced EA via dietary restriction [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 [45]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Human Leptin Levels Are Pulsatile and Inversely Related to Pituitary–Ardenal Function
Licinio, J., Mantzoros, C., Negrão, A. B., Cizza, G., Wong, M.-L., Bongiorno, P. B., Chrousos, G. P., Karp, B., Allen, C., Flier, J. S., et al. (1997) · Nature Medicine · doi:10.1038/nm0597-575 · Cited by 632
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, S. A. J. R. T. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.1.37 · Cited by 539 · cited 9×
“The experimental protocol has been described in detail previously (28).”
BackgroundMethodResultInfluentialSelf-citationLoucks, A. B. (1994) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.78.4.910 · Cited by 174
Self-citation
Research works printed but not linked: 40
- 10.1038/382250a0 · DOI · Paper page
- 10.1016/0196-9781(96)00025-3 · DOI
- Bergendahl M., 1999, J. Clin. Endocrinol. Metab., 84, 883
- Boden G., 1996, J. Clin. Endocrinol. Metab., 81, 3419
- Bourdon L., 1995, Aviat. Space Environ. Med., 66, 787
- 10.1159/000127262 · DOI
- 10.1056/NEJM199602013340503 · DOI · Paper page
- 10.1095/biolreprod60.2.216 · DOI
- 10.1016/S0026-0495(98)90055-5 · DOI
- 10.1210/endo.139.11.6297 · DOI
- 10.1093/ajcn/66.6.1352 · DOI
- 10.1152/ajpendo.1997.272.4.E562 · DOI
- 10.1007/s001250050686 · DOI
- 10.1038/38717 · DOI · Paper page
- 10.1152/jappl.1988.65.6.2601 · DOI
- Kohrt W. M., 1996, J. Clin. Endocrinol. Metab., 81, 3980
- 10.2337/diab.45.11.1511 · DOI
- Kolaczynski J. W., 1996, J. Clin. Endocrinol. Metab., 81, 4162
- 10.1210/jcem.83.5.4717 · DOI
- Laughlin G. A., 1998, J. Clin. Endocrinol. Metab., 83, 25
- 10.1210/jcem.82.1.3840 · DOI
- 10.1016/0006-8993(88)91035-9 · DOI
- Loucks A. B., 1994, J. Clin. Endocrinol. Metab., 78, 910
- 10.1210/jcem-68-2-402 · DOI
- 10.1038/nm1195-1155 · DOI · Paper page
- 10.2337/diab.47.2.294 · DOI
- 10.1210/endo.139.2.5716 · DOI
- 10.1159/000054335 · DOI
- Olson B. R., 1995, J. Clin. Endocrinol. Metab., 80, 1187
- 10.1152/ajpendo.1998.274.2.E280 · DOI
- 10.1152/jappl.1997.83.1.5 · DOI
- 10.1006/hbeh.1998.1453 · DOI
- 10.1172/JCI119717 · DOI
- 10.1210/jcem.83.6.4864 · DOI · Paper page
- 10.1172/JCI118551 · DOI
- 10.1046/j.1365-2265.1998.00434.x · DOI
- 10.1038/sj.ijo.0800784 · DOI
- 10.1152/ajpendo.1996.270.1.E1 · DOI
- 10.1038/31474 · DOI
- Weigle D. S., 1997, J. Clin. Endocrinol. Metab., 82, 561
Cited by
Sorted by citations
Mountjoy, M., Ackerman, K. E., Bailey, D. M., Burke, L. M., Constantini, N., Hackney, A. C., Heikura, I. A., Melin, A., Pensgaard, A. M., Stellingwerff, T., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-106994 · Cited by 724
Aubry, M., Cantu, R., Dvořák, J., Graf-Baumann, T., Johnston, K., Kelly, J., Lovell, M., McCrory, P., Meeuwisse, W., & Schamasch, P. (2002) · Physician and sportsmedicine · doi:10.1136/bjsm.36.1.6 · Cited by 722
De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M., Goolsby, M., Matheson, G., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093218 · Cited by 661
“9 23 – 25 A causal relationship for the induction of menstrual disorders associated with low EA was carefully documented in the literature.”
BackgroundIntegrative physiology of human adipose tissue
Frayn, K. N., Karpe, F., Fielding, B. A., Macdonald, I. A., & Coppack, S. W. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802326 · Cited by 480
Physical Activity and Exercise in the Regulation of Human Adipose Tissue Physiology
Thompson, D., Karpe, F., Lafontan, M., & Frayn, K. N. (2012) · Physiological Reviews · doi:10.1152/physrev.00012.2011 · Cited by 425
Barrack, M. T., Gibbs, J. C., De Souza, M. J., Williams, N. I., Nichols, J. F., Rauh, M. J., & Nattiv, A. (2014) · The American Journal of Sports Medicine · doi:10.1177/0363546513520295 · Cited by 349
“An energy deficit, defined as an inadequate calorie intake relative to exercise energy expenditure, sustained over a period of weeks or months can lower leptin, estradiol, and insulin-like growth factor–1 and can increase cortisol.(19,21,29) These hormone disruptions can decrease osteoblast activity and increase bone…”
BackgroundEnergy balance and body composition in sports and exercise
Loucks, A. B. (2004) · Journal of Sports Sciences · doi:10.1080/0264041031000140518 · Cited by 344
“Since then, we have shown that the diurnal rhythm of leptin depends instead on the availability of energy and, more specifically, of carbohydrate (Hilton and Loucks, 2000).”
BackgroundInfluentialSelf-citationLogue, D. M., Madigan, S. M., Melin, A., Delahunt, E., Heinen, M., Donnell, S.-J. M., & Corish, C. A. (2020) · Nutrients · doi:10.3390/nu12030835 · Cited by 321
“Rigorously executed studies have identified low EA, not the stress of exercise, as the underlying mechanism causing disruption to the female hypothalamic-pituitary-gonadal axis [51,53].”
BackgroundLogue, D., Madigan, S. M., Delahunt, E., Heinen, M., Mc Donnell, S.-J., & Corish, C. A. (2018) · Sports Medicine · doi:10.1007/s40279-017-0790-3 · Cited by 274
“A study of healthy exercising females demonstrated that the pulsatility of leptin is dependent on EA and not exercise-induced stress; exercise had no suppressive effect on the diurnal rhythm of leptin when EI was adequate [50].”
BackgroundKraemer, R. R., Chu, H., & Castracane, V. D. (2002) · Experimental Biology and Medicine · doi:10.1177/153537020222700903 · Cited by 205
Joy, E. A., Souza, M. J. D., Nattiv, A., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M. P., Goolsby, M. A., Matheson, G. O., et al. (2014) · Current Sports Medicine Reports · doi:10.1249/jsr.0000000000000077 · Cited by 265
Self-citationEndocrine Effects of Relative Energy Deficiency in Sport
Elliott-Sale, K. J., Tenforde, A. S., Parziale, A. L., Holtzman, B., & Ackerman, K. E. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0127 · Cited by 229
Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes
Burke, L. M., Lundy, B., Fahrenholtz, I. L., & Melin, A. K. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0142 · Cited by 244
Areta, J. L., Taylor, H. L., & Koehler, K. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04516-0 · Cited by 214
“The vast majority of studies measuring leptin after LEA (Table 2) report a decrease with values of ≤ 30 kcal/kg LBM/day, regardless of whether LEA is achieved through dietary restriction alone or in combination with exercise (Hilton and Loucks 2000; Koehler et al.”
BackgroundInfluentialDifferential regulation of metabolic, neuroendocrine, and immune function by leptin in humans.
Chan, J. L., Matarese, G., Shetty, G. K., Raciti, P., Kelesidis, I., Aufiero, D., De Rosa, V., Perna, F., Fontana, S., & Mantzoros, C. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505429103 · Cited by 213
Energy Availability, Not Body Fatness, Regulates Reproductive Function in Women
Loucks, A. B. (2003) · Exercise and Sport Sciences Reviews · doi:10.1097/00003677-200307000-00008 · Cited by 206
“Since then, however, we have shown that the level and diurnal rhythm of leptin actually depend on energy availability (defined as dietary energy intake minus exercise energy expenditure) and that exercise itself has no suppressive effect on leptin beyond the impact of its energy cost on energy availability (4).”
BackgroundSelf-citationOvarian Suppression Impairs Sport Performance in Junior Elite Female Swimmers
VanHeest, J. L., Rodgers, C. D., Mahoney, C. E., & De Souza, M. J. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3182a32b72 · Cited by 203
Parallels with the Female Athlete Triad in Male Athletes
Tenforde, A. S., Barrack, M. T., Nattiv, A., & Fredericson, M. (2015) · Sports Medicine · doi:10.1007/s40279-015-0411-y · Cited by 236
“The reduction in leptin observed in men parallels findings in women consuming a diet yielding a low energy availability of 10 kcal/kgFFM/day [68].”
BackgroundINTERACTIONS OF CORTISOL, TESTOSTERONE, AND RESISTANCE TRAINING: INFLUENCE OF CIRCADIAN RHYTHMS
Hayes, L. D., Bickerstaff, G. F., & Baker, J. S. (2010) · Chronobiology International · doi:10.3109/07420521003778773 · Cited by 180
“The mechanisms of this increased C production were explained by Hilton and Loucks (2000), who concluded that low energy availability (availability = intake − expenditure), and not solely the stress of exercise, induced hypercortisolism.”
BackgroundWasserfurth, P., Palmowski, J., Hahn, A., & Krüger, K. (2020) · Sports Medicine - Open · doi:10.1186/s40798-020-00275-6 · Cited by 190
“Lower leptin levels depend solely on energy availability, as shown in male rowers [72] and exercising healthy females [16], but are also a response to chronic exercise training [73].”
BackgroundInfluentialThong, F. S. L., McLean, C., & Graham, T. (2000) · Journal of applied physiology · doi:10.1152/jappl.2000.88.6.2037 · Cited by 189
“However, increasing evidence suggests the dependence of LH pulsatility on energy availability is mediated by leptin (8, 14, 20).”
BackgroundExercise and Humoral Mediators of Peripheral Energy Balance: Ghrelin and Adiponectin
Kraemer, R., & Castracane, V. (2007) · Experimental biology and medicine · doi:10.3181/00379727-207-2320184 · Cited by 184
“Because ghrelin is one of the peptides that functions to regulate energy homeostasis, and because energy balance is known to affect reproductive function as well as the circadian rhythm of the satiety hormone, leptin (55, 56), a study was conducted to ascertain whether ghrelin concentrations in premenopausal women var…”
BackgroundEffects of exercise on energy-regulating hormones and appetite in men and women
Hagobian, T. A., Sharoff, C. G., Stephens, B. R., Wade, G. N., Silva, J. E., Chipkin, S. R., & Braun, B. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90671.2008 · Cited by 173
Koehler, K., Hoerner, N. R., Gibbs, J. C., Zinner, C., Braun, H., De Souza, M. J., & Schaenzer, W. (2016) · Journal of Sports Sciences · doi:10.1080/02640414.2016.1142109 · Cited by 164
“…Loucks’ experiments, which demonstrated that effects were more pronounced when energy availability was reduced to 10–20 kcal · kg−1 FFM · day−1 when compared to 30 kcal · kg−1 FFM · day−1 (Hilton & Loucks, 2000; Ihle & Loucks, 2004; Loucks & Heath, 1994; Loucks & Thuma, 2003; Loucks et al., 1998).”
BackgroundResultInfluentialOvarian Dysfunction, Stress, and Disease: A Primate Continuum
Kaplan, J. R., & Manuck, S. B. (2004) · ILAR Journal · doi:10.1093/ilar.45.2.89 · Cited by 139
“…deficits has also focused much interest on leptin, the hormone that promotes satiety but that also may act to suppress the HPA axis and potentiate activity of the GnRH neurons (Barash et al. 1996; Chrousos et al. 1998; Cunningham et al. 1999; Hilton and Loucks 2000; Miller et al. 1998).”
BackgroundFarr, O. M., Tsoukas, M. A., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.07.004 · Cited by 153
“Two well-controlled studies have shown that long-term exercise produces a sufficient energy imbalance (intake versus expenditure) to suppresses 24-hmean and amplitude of the diurnal rhythm of leptin in women [212,213].”
BackgroundPlasma leptin in moderately obese men: independent effects of weight loss and aerobic exercise
Thong, F. S. L., Hudson, R., Ross, R., Janssen, I., & Graham, T. E. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.2.e307 · Cited by 121
“However, exercise has been shown to have no acute effects on leptin secretion (16, 22) or its diurnal rhythm (12).”
BackgroundFedewa, M. V., Hathaway, E. D., Ward-Ritacco, C. L., Williams, T. D., & Dobbs, W. C. (2018) · Sports Medicine · doi:10.1007/s40279-018-0897-1 · Cited by 135
Methods to Standardize Dietary Intake Before Performance Testing
JEACOCKE, N. A., & Burke, L. M. (2010) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.20.2.87 · Cited by 127
Thivel, D., Isacco, L., Montaurier, C., Boirie, Y., Duché, P., & Morio, B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029840 · Cited by 120
“In contrast, when energy is replaced, mixed results are obtained depending on exercise characteristics such as duration and intensity [21,22,23,24,25].”
BackgroundLuteal phase deficiency in recreational runners: evidence for a hypometabolic state.
Souza, M. D. D., Heest, J. L. V., Demers, L., & Lasley, B. (2003) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2002-020958 · Cited by 119
“Loucks et al. (9) have also demonstrated that an acute exposure to a combined regime of exercise training and caloric restriction significantly reduces circulating insulin levels.”
BackgroundInfluentialJürimäe, J., Mäestu, J., Jürimäe, T., Mangus, B. C., & von DUVILLARD, S. P. (2010) · Metabolism · doi:10.1016/j.metabol.2010.02.009 · Cited by 106
“The independent effect of negative energy balance on leptin concentration was also demonstrated by Hilton and Loucks [55] who found that the pulsatility of leptin depends on energy availability and that exercise has no suppressive effect on the diurnal rhythm of leptin beyond the impact of its energy cost on energy av…”
BackgroundBurke, L. M. (2001) · Canadian Journal of Applied Physiology · doi:10.1139/h2001-055 · Cited by 112
Leptin and Metabolic Control of Reproduction
Schneider, J. E., Zhou, D., & Blum, R. M. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1590 · Cited by 101
Doucet, É., Imbeault, P., St-Pierre, S., Alméras, N., Mauriège, P., Despres, J., Bouchard, C., & Tremblay, A. (2003) · Clinical science · doi:10.1042/cs20020252 · Cited by 101
Benardot, D. (2005) · Human Kinetics eBooks · doi:10.5040/9781718220973 · Cited by 99
Δίπλα, Κ., Kraemer, R. R., Constantini, N., & Hackney, A. C. (2020) · HORMONES · doi:10.1007/s42000-020-00214-w · Cited by 182
“To distinguish between the independent effects of energy availability and exercise stress on diurnal leptin rhythm, Hilton and Loucks [61] examined different levels of energy availability in healthy young women.”
BackgroundSerum leptin responses after acute resistance exercise protocols
Zafeiridis, A., Smilios, I., Considine, R. V., & Tokmakidis, S. P. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00330.2002 · Cited by 90
“Furthermore, recent findings suggest that leptin responds to low carbohydrate and energy availability, constituting a link between energy intake and storage (12).”
BackgroundAcute exercise effect on postabsorptive serum leptin
Fisher, J. S., Pelt, R. E. V., Zinder, O., Landt, M., & Kohrt, W. M. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.2.680 · Cited by 55
“Hilton and Loucks (11) examined sedentary and exercising women for whom daily energy expenditure was matched with daily energy intake (;1,400 kcal/ day expended by walking was replaced by an equivalent dietary intake in the exercising women), and they concluded that exercise stress without decreased energy availabilit…”
BackgroundInfluentialLeptin responses to short term exercise in college level male rowers
Jürimäe, J., & Jürimäe, T. (2004) · British Journal of Sports Medicine · doi:10.1136/bjsm.2003.008516 · Cited by 88
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
“The findings from our study support the prevailing consensus that leptin suppression is not due to exercise per se but rather the energy deficit induced by the EPOC after acute, heavy-resistance exercise (3,8).”
BackgroundLow 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
“Without exception, laboratory studies focusing on LEA implement very brief (3-5 days) protocols (Hilton & Loucks, 2000; Ihle & Loucks, 2004; Koehler, 2016; Loucks & Callister, 1993; Loucks & Heath, 1994a, 1994b; Loucks & Thuma, 2003; Loucks et al., 1998; Papageorgiou, 2018).”
BackgroundInfluentialResting leptin responses to acute and chronic resistance training in type 2 diabetic men and women
Kanaley, J., Fenicchia, L., Miller, C., Ploutz-Synder, L., Weinstock, R., Carhart, R., & Azevedo, J. (2001) · International Journal of Obesity · doi:10.1038/sj.ijo.0801797 · Cited by 81
Christ, E., Zehnder, M., Boesch, C., Trepp, R., Mullis, P., Diem, P., & Décombaz, J. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02106 · Cited by 78
Souza, M. J. D., Nattiv, A., Joy, E. A., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M. P., Goolsby, M. A., & Matheson, G. O. (2014) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0000000000000085 · Cited by 191
Influence of weeks of circadian misalignment on leptin levels
Wright (2009) · Nature and Science of Sleep · doi:10.2147/nss.s7624 · Cited by 74
Hukshorn, C. J., & Saris, W. H. M. (2004) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200411000-00007 · Cited by 65
Puberty as a life history transition
Ellison, P. T., Reiches, M. W., Shattuck-Faegre, H., Breakey, A., Konecna, M., Urlacher, S., & Wobber, V. (2012) · Annals of Human Biology · doi:10.3109/03014460.2012.693199 · Cited by 73
Koehler, K., Achtzehn, S., Braun, H., Mester, J., & Schaenzer, W. (2013) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2012-0373 · Cited by 87
Resting thyroid and leptin hormone changes in women following intense, prolonged exercise training
Baylor, L. M., & Hackney, A. C. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0737-7 · Cited by 66
“Hilton and Loucks (2000) reported that low energy availability (i.e. an energy deficiency) can suppress 24 h mean leptin concentrations.”
BackgroundBlack, S. E., Mitchell, E. A., Freedson, P. S., Chipkin, S. R., & Braun, B. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00291.2005 · Cited by 63
“These results are concordant with other human studies, which generally show that leptin levels change with exercise only when there is a concurrent change in energy balance (36, 49, 51) or energy availability (16).”
ResultHagobian, T., Sharoff, C., & Braun, B. (2008) · Metabolism: Clinical and Experimental · doi:10.1016/j.metabol.2007.10.016 · Cited by 71
“In the rare cases when exercise energy expenditure has been replaced by adding calories to the diet, the effects of exercise on leptin, insulin, and/or ghrelin have been inconsistent and likely depend upon timing of measurement(s), intensity and/ or duration of exercise, subject training status, etc [1,14-21].”
InfluentialMaïmoun, L., Georgopoulos, N., & Sultan, C. (2014) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2013-3030 · Cited by 69
“Moreover, the absence of a leptin diurnal rhythm along with hypoinsulinemia and hypercortisolemia suggests the preponderant role of metabolic adaptations to chronic energy deficits (26, 41), whereas exercise stress alone has no effect on leptin production (41).”
BackgroundHammond, K. M., Sale, C., Fraser, W., Tang, J., Shepherd, S. O., Strauss, J. A., Close, G. L., Cocks, M., Louis, J., Pugh, J., et al. (2019) · The Journal of Physiology · doi:10.1113/jp278209 · Cited by 68
Nutritional and exercise-related determinants of bone density in elite female runners
Gibson, J. H., Mitchell, A., Harries, M., & Reeve, J. (2004) · Osteoporosis International · doi:10.1007/s00198-004-1589-2 · Cited by 67
“Plasma leptin is reportedly low [39] in athletes with inappropriately low energy intakes.”
BackgroundHulver, M. W., & Houmard, J. A. (2003) · Sports Medicine · doi:10.2165/00007256-200333070-00001 · Cited by 94
Hypothalamic-pituitary-adrenal axis in the night eating syndrome
Birketvedt, G. S., Sundsfjord, J., & Florholmen, J. R. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00251.2001 · Cited by 64
“In two reports, stress did not influence the diurnal secretion of leptin (9, 19), whereas in two other reports, stress indeed inhibited the leptin secretion and abolished the diurnal secretion (5, 12).”
Cognitive dietary restraint: impact on bone, menstrual and metabolic status in young women.
Vescovi, J., Scheid, J., Hontscharuk, R., & Souza, M. D. D. (2008) · Physiology and Behavior · doi:10.1016/j.physbeh.2008.04.003 · Cited by 63
“Women who diet or restrict their food intake demonstrate metabolic adaptations consistent with an energy deficiency, to include suppressed REE [45], free and total T3 [45,46], and leptin levels [47,48] as well as elevated ghrelin concentrations [49].”
The effects of weight loss strategies on gastric emptying and appetite control
Horner, K. M., Byrne, N. M., Cleghorn, G. J., Näslund, E. B., & King, N. A. (2011) · Obesity Reviews · doi:10.1111/j.1467-789x.2011.00901.x · Cited by 64
Burke, L. M., Ackerman, K. E., Heikura, I. A., Hackney, A. C., & Stellingwerff, T. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-107335 · Cited by 59
Muscle Glycogen Content during Endurance Training under Low Energy Availability
KOJIMA, C., ISHIBASHI, A., TANABE, Y., IWAYAMA, K., KAMEI, A., TAKAHASHI, H., & GOTO, K. (2020) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002098 · Cited by 55
“Previous studies determined the influence of low EA onmetabolic hormones (leptin, insulin-like growth factor 1 [IGF-1], triiodothyronine, insulin) and reproductive hormones in both women (12,13) and men (14) in a controlled laboratory setting.”
BackgroundKeller, P., Keller, C., Steensberg, A., Robinson, L. E., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00592.2004 · Cited by 46
“was counteracted by CHO ingestion, which indicates sensitivity to energy availability or to hormones affected by the presence of CHO, as previously shown in rodents (35) and in humans (1, 15).”
BackgroundMars, M., de Graaf, C., de Groot, L. C. P. G. M., & Kok, F. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.3.570 · Cited by 54
“Several studies have shown that, during energy restriction, not only fasting leptin concentrations, but also the diurnal variation of these concentrations, is decreased (26, 27).”
BackgroundPoppitt, S. D., Leahy, F. E., Keogh, G. F., Wang, Y., Mulvey, T. B., Stojkovic, M., Chan, Y., Choong, Y. S., McArdle, B. H., & Cooper, G. J. S. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602270 · Cited by 53
“Fasting (Boden et al., 1996; Kolaczynski et al., 1996a; Weigle et al., 1997) and exercise (Hilton, 2000) cause an acute drop, and overfeeding a rise (Kolaczynski et al., 1996a) in leptin.”
BackgroundRelative Energy Deficiency in Sport (RED-S) in Adolescents – A Practical Review
Gould, R. J., Ridout, A. J., & Newton, J. L. (2022) · International Journal of Sports Medicine · doi:10.1055/a-1947-3174 · Cited by 65
“There is suppression of the normal diurnal rhythm of the anorexigenic hormone leptin, which is independent of exer - cise stress [62], adiponectin is raised in dancers with LEA [63], the orexigenic hormone ghrelin is raised in low energy states [64], and the appetite suppressant Peptide YY is…”
BackgroundWilliams, N. I., Statuta, S. M., & Austin, A. (2017) · Clinics in Sports Medicine · doi:10.1016/j.csm.2017.05.003 · Cited by 69
Ghrelin but Not Peptide YY Is Related to Change in Body Weight and Energy Availability
Scheid, J. L., Souza, M. J. D., Leidy, H. J., & Williams, N. I. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31821e52ab · Cited by 42
“(6) have shown that energy availability has been slTongly related fo changes in metabolic hormones such as triiodofhyronine (33), leptin (23), and ghrelin (6) in exercising women.”
BackgroundInfluentialEffects of exercise combined with caloric restriction on inflammatory cytokines
Reed, J. L., Souza, M. J. D., & Williams, N. I. (2010) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h10-046 · Cited by 42
“More research is required to elucidate the mechanism underlying these changes (Hilton and Loucks 2000; Howell et al. 2009).”
BackgroundCurrent Status of the Female Athlete Triad: Update and Future Directions
Souza, M. D. D., Koltun, K. J., Etter, C. V., & Southmayd, E. A. (2017) · Current Osteoporosis Reports · doi:10.1007/s11914-017-0412-x · Cited by 47
Sports medicine in the Netherlands
Durstine, J. L., Thompson, R. W., Drowatzky, K., & Bartoli, W. (2001) · British Journal of Sports Medicine · doi:10.1136/bjsm.35.1.5 · Cited by 47
Hickey, M., & Calsbeek, D. (2001) · Sports Medicine · doi:10.2165/00007256-200131080-00003 · Cited by 45
“As Hilton and Loucks[20] suggest, this would imply that there is a threshold reduction in energy availability that must be reached to alter the”
BackgroundInfluentialModified activity-stress paradigm in an animal model of the female athlete triad
DiMarco, N. M., Dart, L., & Sanborn, C. (. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01137.2005 · Cited by 47
“The anabolic effects of voluntary wheel running in ad libitum-fed rats have been shown to have a positive and significant impact on multiple axial and appendicular skeletal sites (9, 35, 40, 66, 90, 96).”
BackgroundSaeidi, A., Haghighi, M. M., Kolahdouzi, S., Daraei, A., Abderrahman, A. B., Essop, M. F., Laher, I., Hackney, A. C., & Zouhal, H. (2020) · Obesity Reviews · doi:10.1111/obr.13090 · Cited by 50
“and this depends on energy defects during excess post-exercise oxygen consumption.(216,217) However, extended exercise periods decrease leptin concentrations more immediately,(218) and this is likely due to lower leptin mRNA expression levels.”
BackgroundWhipple, T., Sharkey, N. A., Demers, L. M., & Williams, N. I. (2002) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2002.01630.x · Cited by 40
Circulating leptin concentrations do not distinguish menstrual status in exercising women
Corr, M., Souza, M. J. D., Toombs, R. J., & Williams, N. I. (2011) · Human Reproduction · doi:10.1093/humrep/deq375 · Cited by 38
Olympic Textbook of Medicine in Sport
Schwellnus, M. P., Komitee, I. O., & International Federation of Sportive Medicine (2008) · Wiley eBooks · doi:10.1002/9781444300635 · Cited by 42
“Subsequent investigations have reinforced this finding in both human and nonhuman primates (Hilton & Loucks 2000; Williams et al. 2001a,b).”
BackgroundMatthews, 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
Energy availability and infertility
Loucks, A. B. (2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3282f1cb6a · Cited by 46
Self-citationLeptin responses to glucose infusions in obesity-prone rats
Levy, J. R., Lesko, J. M., Krieg, R. J., Adler, R. A., & Stevens, W. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.5.e1088 · Cited by 33
“A diurnal variation of plasma leptin has been observed in humans (55), and the diurnal rhythm of plasma leptin has been shown to be entrained to meal timing (52) and to be dependent on energy availability (24).”
BackgroundA 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
“LEA suppresses leptin levels in both females (Hilton & Loucks, 2000) and males (Dubuc et al., 1998; Koehler, Hoerner, et al., 2016).”
BackgroundImpact of Body Mass Index on female fertility and ART outcomes
Imterat, M., Agarwal, A. K., Esteves, S. C., Meyer, J., & Harlev, A. (2019) · Panminerva Medica · doi:10.23736/s0031-0808.18.03490-0 · Cited by 42
Marathon Running: Physiology, Psychology, Nutrition and Training Aspects
Zinner, C., & Sperlich, B. (2016) · Cambridge International Law Journal · doi:10.1007/978-3-319-29728-6 · Cited by 34
“Gender and hormonal factors contribute to a higher risk of bone stress injury in women than men, particularly female athletes participating in leanness and endurance-focused sports (i.e. long-distance running) (Ihle and Loucks 2004; Hilton and Loucks 2000; Lawson et al. 2009).”
BackgroundLodge, M. T., Ward-Ritacco, C. L., & Melanson, K. J. (2023) · Nutrients · doi:10.3390/nu15204457 · Cited by 33
“In this same study, leptin levels decreased by 50% in response to dietary restriction, and this difference is proportional to the reductions in CHO intake [45].”
BackgroundInfluentialAppetite regulation in response to sitting and energy imbalance
Granados, K. E., Stephens, B. R., Malin, S. K., Zderic, T. W., Hamilton, M. T., & Braun, B. (2012) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h2012-002 · Cited by 39
de Assis, G. G., & Murawska‐Ciałowicz, E. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12134490 · Cited by 38
“The study by Hilton & Loucks [31] examined the effects of energy availability and exercise on diurnal leptin rhythms in non-overweight, young women by controlling energy”
BackgroundInfluentialKing, J. A., Garnham, J. O., Jackson, A. P., Kelly, B. M., Xenophontos, S., & Nimmo, M. A. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.12.050 · Cited by 35
“Existing work has shown that circulating levels of leptin are highly responsive to alterations in energy balance/availability [44,45].”
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
“Previous research studies indicate that, in addition to menstrual dysfunction, chronic energy deficiency leads to hypothalamic and pituitary hormonal disturbances that negatively affect bone metabolism.(8,15,16) In a study of regularly menstruating young women, dietary intake and exercise expenditure were controlled f…”
BackgroundPlasma Leptin, Plasma Zinc, and Plasma Copper Are Associated in Elite Female and Male Judo Athletes
Casimiro-Lopes, G., de Oliveira-Junior, A. V., Portella, E. S., Lisboa, P., Donangelo, C., de Moura, E. D., & Koury, J. (2009) · Biological Trace Element Research · doi:10.1007/s12011-008-8236-2 · Cited by 32
“Many authors suggest that the hexosamine pathway could be related with leptin regulation in exercised individuals when the drop in leptinemia is not proportional to fat mass reduction [29, 33–35].”
BackgroundRahmani-Nia, F., Rahnama, N., Hojjati, Z., & Soltani, B. (2008) · Sport Sciences for Health · doi:10.1007/s11332-008-0050-x · Cited by 32
“There is clear evidence for the importance of exact control of energy balance in leptin and exercise studies [9].”
BackgroundInfluentialLegakis, I., Mantzouridis, T., Saramantis, A., & Lakka-Papadodima, E. (2004) · Journal of Endocrinological Investigation · doi:10.1007/bf03346255 · Cited by 29
Leptin signaling in skeletal muscle after bed rest in healthy humans
Guerra, B., Ponce‐González, J. G., Morales‐Álamo, D., Guadalupe‐Grau, A., Kiilerich, K., Fuentes, T., Ringholm, S., Biensø, R. S., Santana, A., Lundby, C., et al. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2779-4 · Cited by 25
Changes in serum leptin levels in strenuous exercise and its relation to zinc deficiency in rats
Gökbel, H., Baltacı, A., Uçok, K., Okudan, N., & Mogulkoc, R. (2005) · Biological Trace Element Research · doi:10.1385/bter:106:3:247 · Cited by 28
“The diurnal rhythm of leptin depends on energy availability, not intake (4).”
BackgroundEndocrine rhythms and sport: it is time to take time into account
Bellastella, G., Bellis, A. D., Maiorino, M. I., Paglionico, V. A., Esposito, K., & Bellastella, A. (2019) · Journal of Endocrinological Investigation · doi:10.1007/s40618-019-01038-1 · Cited by 27
Plasma leptin and energy expenditure during prolonged, moderate intensity, treadmill exercise
Zaccaria, M., Ermolao, A., Brugin, E., & Bergamin, M. (2012) · Journal of Endocrinological Investigation · doi:10.3275/8656 · Cited by 27
Braun, B., & Brooks, G. (2008) · Exercise and sport sciences reviews · doi:10.1097/jes.0b013e31815e42c2 · Cited by 27
“To address the question in a systematic way, Loucks and colleagues performed definitive studies in which they tested the hypothesis that energy deficit, not exercise itself, explained the disrupted menstrual function.”
BackgroundInfluentialLeptina: aspectos sobre o balanço energético, exercício físico e amenorréia do esforço
Ribeiro, S. M. L., dos Santos, Z. A., da Silva, R. J., Eliana, L. R., Donato, J., & Tirapegui, J. (2007) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302007000100005 · Cited by 18
Physical health of the female athlete: observations, effects, and causes of reproductive disorders.
Loucks, A. (2001) · Canadian Journal of Applied Physiology · doi:10.1139/h2001-052 · Cited by 27
Self-citationRecovery of menses after functional hypothalamic amenorrhoea: if, when and why
Pape, J., Herbison, A. E., & Leeners, B. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa032 · Cited by 31
Comparison of plasma leptin and zinc levels in elite athletes and sedentary people
Arıkan, Ş., Akkuş, H., Halifeoğlu, I., & Baltacı, A. (2008) · Cell Biochemistry and Function · doi:10.1002/cbf.1480 · Cited by 26
Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function
Loucks, A. B. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-314-5_11 · Cited by 10
Self-citation
Metadata
- Authors
- Hilton, L. K., & Loucks, A. B.
- Affiliations
- Ohio University (US)
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2000-01-01
- Volume
- 278
- Issue
- 1
- Pages
- E43-E49
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W2152128405
- Cited by
- 214
- References
- 0
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 5 · 2023: 11 · 2022: 8 · 2021: 11 · 2020: 12 · 2019: 8 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 7 · 2014: 11 · 2013: 19 · 2012: 8
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- National Institutes of Health (1r55hd029547-01)
- Directorate for Biological Sciences
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- leptin, diurnal cycle, energy availability, exercise stress, energy expenditure, energy intake, carbohydrate availability, luteinizing hormone pulsatility, menstrual cycle, follicular phase, young women
- MeSH terms
- Adult, Energy Intake, Circadian Rhythm, Energy Metabolism, Female, Humans, Reference Values, Exercise, Leptin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
