Consumption of Two Eggs Daily Increases Serum Leptin in Amenorrheic Runners with Low Energy Availability without Changes in Lipid Profile — Oak Academic Publishing
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Consumption of Two Eggs Daily Increases Serum Leptin in Amenorrheic Runners with Low Energy Availability without Changes in Lipid Profile
Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
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Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
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Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
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Department of Biomedical and Nutritional Sciences, University of Massachusetts Lowell, Lowell, MA, USA
1 Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
2 Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
3 Biomedical Engineering and Biotechnology Program, University of Massachusetts Lowell, Lowell, MA, USA
4 Department of Biomedical and Nutritional Sciences, University of Massachusetts Lowell, Lowell, MA, USA
Background/Objective: Low energy availability (EA) occurs in athletes due to inadequate dietary intake to meet the energy expenditure during exercise. A detrimental consequences of low EA in female athletes is suppression of menstrual function leading to chronic hypoestrogenism, which may reduce bone mass while elevating the risk of injury. The primary aim of this study was to investigate the effects of increased dietary cholesterol intake through the consumption of eggs on ovarian sex hormone and leptin levels in amenorrheic female endurance athletes. Methods: Division I female distance runners classified as amenorrheic (AMEN, n = 5) or eumenorrheic (EUMEN, n = 5) via self-report questionnaire participated in this study. Participants consumed two eggs per day for 12 weeks over the course of the outdoor track and field season. EA was calculated at baseline and post-intervention using 3-day dietary records, triaxial accelerometers, and heart rate (HR) monitors. Maximal oxygen uptake (VO 2 max) was measured to calculate exercise energy expenditure with training HR data. Serum hormones, body composition, and blood lipids were measured at baseline and post-intervention. Results: There were no significant differences exhibited between the AMEN and EUMEN groups in body composition, EA, or sex hormones at baseline and after the dietary intervention. However, when examining differences within groups between baseline and post-intervention, serum leptin levels increased in the AMEN group by 70% (p = 0.02) compared to baseline following egg consumption, while no change in serum leptin was observed in the EUMEN group. Also, at baseline, EA was calculated to be below 30 kcal·kg − 1 ·FFM·d − 1 threshold for only the AMEN group, while the EUMEN group was right at the threshold, whereas post-intervention, EA was calculated to be below the threshold in both groups, but not significantly when compared to baseline. Importantly, no changes in serum lipids and lipoprotein cholesterol levels were observed in either treatment group post-intervention with the consumption of eggs compared to baseline. Conclusions: Twelve-week consumption of two eggs per day increased serum leptin in amenorrheic athletes with low EA, with no changes in ovarian sex hormones. The serum lipid profile was not adversely affected by increased dietary cholesterol in the form of eggs.
Loucks, A.B., Kiens, B. and Wright, H.H. (2011) Energy Availability in Athletes. Journal of Sports Sciences , 29, S7-S15. https://doi.org/10.1080/02640414.2011.588958
Fahrenholtz, I.L., Melin, A.K., Wasserfurth, P., Stenling, A., Logue, D., Garthe, I., et al . (2022) Risk of Low Energy Availability, Disordered Eating, Exercise Addiction, and Food Intolerances in Female Endurance Athletes. Frontiers in Sports and Active Living , 4, Article ID: 869594. https://doi.org/10.3389/fspor.2022.869594
Loucks, A.B. and Thuma, J.R. (2003) Luteinizing Hormone Pulsatility Is Disrupted at a Threshold of Energy Availability in Regularly Menstruating Women. The Journal of Clinical Endocrinology & Metabolism , 88, 297-311. https://doi.org/10.1210/jc.2002-020369
Wade, G.N. and Schneider, J.E. (1992) Metabolic Fuels and Reproduction in Female Mammals. Neuroscience & Biobehavioral Reviews , 16, 235-272. https://doi.org/10.1016/s0149-7634(05)80183-6
Wade, G.N., Schneider, J.E. and Li, H.Y. (1996) Control of Fertility by Metabolic Cues. American Journal of Physiology - Endocrinology and Metabolism , 270, E1-E19. https://doi.org/10.1152/ajpendo.1996.270.1.e1
Williams, N.I., Helmreich, D.L., Parfitt, D.B., Caston-Balderrama, A. and Cameron, J.L. (2001) Evidence for a Causal Role of Low Energy Availability in the Induction of Menstrual Cycle Disturbances during Strenuous Exercise Training. The Journal of Clinical Endocrinology & Metabolism , 86, 5184-5193. https://doi.org/10.1210/jcem.86.11.8024
Gallant, T.L., Ong, L.F., Wong, L., Sparks, M., Wilson, E., Puglisi, J.L., et al . (2025) Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-Analysis. Sports Medicine , 55, 325-339. https://doi.org/10.1007/s40279-024-02130-0
De Souza, M.J., Toombs, R.J., Scheid, J.L., O’Donnell, E., West, S.L. and Williams, N.I. (2010) High Prevalence of Subtle and Severe Menstrual Disturbances in Exercising Women: Confirmation Using Daily Hormone Measures. Human Reproduction , 25, 491-503. https://doi.org/10.1093/humrep/dep411
Berga, S.L., Mortola, J.F., Girton, L., Suh, B., Laughlin, G., Pham, P., et al . (1989) Neuroendocrine Aberrations in Women with Functional Hypothalamic Amenorrhea. The Journal of Clinical Endocrinology & Metabolism , 68, 301-308. https://doi.org/10.1210/jcem-68-2-301
Meczekalski, B., Podfigurna-Stopa, A., Warenik-Szymankiewicz, A. and Genazzani, A.R. (2008) Functional Hypothalamic Amenorrhea: Current View on Neuroendocrine Aberrations. Gynecological Endocrinology , 24, 4-11. https://doi.org/10.1080/09513590701807381
Ihle, R. and Loucks, A.B. (2004) Dose-Response Relationships between Energy Availability and Bone Turnover in Young Exercising Women. Journal of Bone and Mineral Research , 19, 1231-1240. https://doi.org/10.1359/jbmr.040410
De Souza, M.J. and Williams, N.I. (2005) Beyond Hypoestrogenism in Amenorrheic Athletes: Energy Deficiency as a Contributing Factor for Bone Loss. Current Sports Medicine Reports , 4, 38-44. https://doi.org/10.1097/01.csmr.0000306070.67390.cb
De Souza, M.J., West, S.L., Jamal, S.A., Hawker, G.A., Gundberg, C.M. and Williams, N.I. (2008) The Presence of Both an Energy Deficiency and Estrogen Deficiency Exacerbate Alterations of Bone Metabolism in Exercising Women. Bone , 43, 140-148. https://doi.org/10.1016/j.bone.2008.03.013
Mallinson, R.J., Williams, N.I., Hill, B.R. and De Souza, M.J. (2013) Body Composition and Reproductive Function Exert Unique Influences on Indices of Bone Health in Exercising Women. Bone , 56, 91-100. https://doi.org/10.1016/j.bone.2013.05.008
Kelsey, J.L., Bachrach, L.K., Procter-Gray, E., Nieves, J., Greendale, G.A., Sowers, M., et al . (2007) Risk Factors for Stress Fracture among Young Female Cross-Country Runners. Medicine & Science in Sports & Exercise , 39, 1457-1463. https://doi.org/10.1249/mss.0b013e318074e54b
Barrack, M.T., Gibbs, J.C., De Souza, M.J., Williams, N.I., Nichols, J.F., Rauh, M.J., et al . (2014) Higher Incidence of Bone Stress Injuries with Increasing Female Athlete Triad-Related Risk Factors. The American Journal of Sports Medicine , 42, 949-958. https://doi.org/10.1177/0363546513520295
Nattiv, A., Kennedy, G., Barrack, M.T., Abdelkerim, A., Goolsby, M.A., Arends, J.C., et al . (2013) Correlation of MRI Grading of Bone Stress Injuries with Clinical Risk Factors and Return to Play: A 5-Year Prospective Study in Collegiate Track and Field Athletes. The American Journal of Sports Medicine , 41, 1930-1941. https://doi.org/10.1177/0363546513490645
Nattiv, A., Loucks, A.B., Manore, M.M., Sanborn, C.F., Sundgot-Borgen, J. and Warren, M.P. (2007) American College of Sports Medicine Position Stand. The Female Athlete Triad. Medicine & Science in Sports & Exercise , 39, 1867-1882.
Friday, K.E., Drinkwater, B.L., Bruemmer, B., Chesnut, C. and Chait, A. (1993) Elevated Plasma Low-Density Lipoprotein and High-Density Lipoprotein Cholesterol Levels in Amenorrheic Athletes: Effects of Endogenous Hormone Status and Nutrient Intake. The Journal of Clinical Endocrinology & Metabolism , 77, 1605-1609. https://doi.org/10.1210/jcem.77.6.8263148
Rickenlund, A., Eriksson, M.J., Schenck-Gustafsson, K. and Hirschberg, A.L. (2005) Amenorrhea in Female Athletes Is Associated with Endothelial Dysfunction and Unfavorable Lipid Profile. The Journal of Clinical Endocrinology & Metabolism , 90, 1354-1359. https://doi.org/10.1210/jc.2004-1286
Schaal, K., van Loan, M.D. and Casazza, G.A. (2011) Reduced Catecholamine Response to Exercise in Amenorrheic Athletes. Medicine & Science in Sports & Exercise , 43, 34-43. https://doi.org/10.1249/mss.0b013e3181e91ece
Lieberman, M. and Marks, A.D. (2012) Cholesterol Synthesis. In: Peet, A, Ed., Marks ’ Basic Medical Biochemistry , 4th Edition, Wolters Kluwer, 630-632.
Li, L., Xiao, N., Yang, X., Gao, J., Ding, J., Wang, T., et al . (2012) A High Cholesterol Diet Ameliorates Hippocampus-Related Cognitive and Pathological Deficits in Ovariectomized Mice. Behavioural Brain Research , 230, 251-258. https://doi.org/10.1016/j.bbr.2012.02.024
Peyghan, R., Gooraninejad, S., Shahriari, A. and Jamshidi, Z. (2012) Feeding Effect of Cholesterol in the Diet on Sex Hormones Concentrations and the Gonads’ Growth of Yearling Common Carp. Iranian Journal of Veterinary Medicine , 6, 23-28.
Clark, L.R., Dellogono, M.J., Mangano, K.M. and Wilson, T.A. (2018) Clinical Menstrual Dysfunction Is Associated with Low Energy Availability but Not Dyslipidemia in Division I Female Endurance Runners. Journal of Exercise Physiology Online , 21, 265-276.
Londraville, R.L., Macotela, Y., Duff, R.J., Easterling, M.R., Liu, Q. and Crespi, E.J. (2014) Comparative Endocrinology of Leptin: Assessing Function in a Phylogenetic Context. General and Comparative Endocrinology , 203, 146-157. https://doi.org/10.1016/j.ygcen.2014.02.002
Kyriakidis, M., Caetano, L., Anastasiadou, N., Karasu, T. and Lashen, H. (2016) Functional Hypothalamic Amenorrhoea: Leptin Treatment, Dietary Intervention and Counselling as Alternatives to Traditional Practice—Systematic Review. European Journal of Obstetrics & Gynecology and Reproductive Biology , 198, 131-137. https://doi.org/10.1016/j.ejogrb.2016.01.018
Hill, J.W., Elmquist, J.K. and Elias, C.F. (2008) Hypothalamic Pathways Linking Energy Balance and Reproduction. American Journal of Physiology - Endocrinology and Metabolism , 294, E827-E832. https://doi.org/10.1152/ajpendo.00670.2007
Dardeno, T.A., Chou, S.H., Moon, H., Chamberland, J.P., Fiorenza, C.G. and Mantzoros, C.S. (2010) Leptin in Human Physiology and Therapeutics. Frontiers in Neuroendocrinology , 31, 377-393. https://doi.org/10.1016/j.yfrne.2010.06.002
Laughlin, G.A. and Yen, S.S.C. (1997) Hypoleptinemia in Women Athletes: Absence of a Diurnal Rhythm with Amenorrhea. The Journal of Clinical Endocrinology & Metabolism , 82, 318-321. https://doi.org/10.1210/jcem.82.1.3840
Chan, J.L., Heist, K., DePaoli, A.M., Veldhuis, J.D. and Mantzoros, C.S. (2003) The Role of Falling Leptin Levels in the Neuroendocrine and Metabolic Adaptation to Short-Term Starvation in Healthy Men. Journal of Clinical Investigation , 111, 1409-1421. https://doi.org/10.1172/jci200317490
Welt, C.K., Chan, J.L., Bullen, J., Murphy, R., Smith, P., DePaoli, A.M., et al . (2004) Recombinant Human Leptin in Women with Hypothalamic Amenorrhea. New England Journal of Medicine , 351, 987-997. https://doi.org/10.1056/nejmoa040388
Chou, S.H., Chamberland, J.P., Liu, X., Matarese, G., Gao, C., Stefanakis, R., et al . (2011) Leptin Is an Effective Treatment for Hypothalamic Amenorrhea. Proceedings of the National Academy of Sciences , 108, 6585-6590. https://doi.org/10.1073/pnas.1015674108
Zhao, S. and Wu, Z. (2005) Atorvastatin Reduces Serum Leptin Concentration in Hypercholesterolemic Rabbits. Clinica Chimica Acta , 360, 133-140. https://doi.org/10.1016/j.cccn.2005.04.021
Huang, Q., He, B., Yang, F., Zeng, H. and Zhao, Q. (2012) Effect of High-Cholesterol Diet on Serum Leptin and Blood Lipid in Rabbits. Journal of Animal and Veterinary Advances , 11, 1719-1721. https://doi.org/10.3923/javaa.2012.1719.1721
Day, D.S., Gozansky, W.S., Van Pelt, R.E., Schwartz, R.S. and Kohrt, W.M. (2005) Sex Hormone Suppression Reduces Resting Energy Expenditure and β -Adrenergic Support of Resting Energy Expenditure. The Journal of Clinical Endocrinology & Metabolism , 90, 3312-3317. https://doi.org/10.1210/jc.2004-1344
Montville, J.B., Ahuja, J.K.C., Martin, C.L., Heendeniya, K.Y., Omolewa-Tomobi, G., Steinfeldt, L.C., et al . (2013) USDA Food and Nutrient Database for Dietary Studies (FNDDS), 5.0. Procedia Food Science , 2, 99-112. https://doi.org/10.1016/j.profoo.2013.04.016
Schaafsma, G. (2000) The Protein Digestibility-Corrected Amino Acid Score. The Journal of Nutrition , 130, 1865S-1867S. https://doi.org/10.1093/jn/130.7.1865s
Wolfe, R.R. (2006) The Underappreciated Role of Muscle in Health and Disease. The American Journal of Clinical Nutrition , 84, 475-482. https://doi.org/10.1093/ajcn/84.3.475
Norton, L.E. and Layman, D.K. (2006) Leucine Regulates Translation Initiation of Protein Synthesis in Skeletal Muscle after Exercise. The Journal of Nutrition , 136, 533S-537S. https://doi.org/10.1093/jn/136.2.533s
Rodriguez, N.R., Vislocky, L.M. and Gaine, P.C. (2007) Dietary Protein, Endurance Exercise, and Human Skeletal-Muscle Protein Turnover. Current Opinion in Clinical Nutrition and Metabolic Care , 10, 40-45. https://doi.org/10.1097/mco.0b013e3280115e3b
Layman, D.K. and Rodriguez, N.R. (2009) Egg Protein as a Source of Power, Strength, and Energy. Nutrition Today , 44, 43-48. https://doi.org/10.1097/nt.0b013e3181959cb2
Layman, D.K. and Baum, J.I. (2004) Dietary Protein Impact on Glycemic Control during Weight Loss. The Journal of Nutrition , 134, 968S-973S. https://doi.org/10.1093/jn/134.4.968s
Layman, D.K. and Walker, D.A. (2006) Potential Importance of Leucine in Treatment of Obesity and the Metabolic Syndrome. The Journal of Nutrition , 136, 319S-323S. https://doi.org/10.1093/jn/136.1.319s
Bouzoni, E., Perakakis, N. and Mantzoros, C.S. (2020) Circulating Profile of Activin-Follistatin-Inhibin Axis in Women with Hypothalamic Amenorrhea in Response to Leptin Treatment. Metabolism , 113, Article 154392. https://doi.org/10.1016/j.metabol.2020.154392
Hall, J.E. (2019) Neuroendocrine Control of the Menstrual Cycle. In: Strauss, III, J.F. and Barbieri, R.L., Eds., Yen and Jaffe ’ s Reproductive Endocrinology , Elsevier, 149-166.e5. https://doi.org/10.1016/b978-0-323-47912-7.00007-x
Lee, A. and Griffin, B. (2006) Dietary Cholesterol, Eggs and Coronary Heart Disease Risk in Perspective. Nutrition Bulletin , 31, 21-27. https://doi.org/10.1111/j.1467-3010.2006.00543.x
US Department of Health and Human Services and US Department of Agriculture (2015) 2015-2020 Dietary Guidelines for Americans (8th Edition).
Kritchevsky, S.B. (2004) A Review of Scientific Research and Recommendations Regarding Eggs. Journal of the American College of Nutrition , 23, 596S-600S. https://doi.org/10.1080/07315724.2004.10719429
Qureshi, A.I., Suri, F.K., Ahmed, S., Nasar, A., Divani, A.A. and Kirmani, J.F. (2007) Regular Egg Consumption Does Not Increase the Risk of Stroke and Cardiovascular Diseases. Medical Science Monitor , 13, CR1-8.
DiMarco, D.M., Missimer, A., Murillo, A.G., Lemos, B.S., Malysheva, O.V., Caudill, M.A., et al . (2017) Intake of up to 3 Eggs/Day Increases HDL Cholesterol and Plasma Choline While Plasma Trimethylamine‐ N ‐Oxide Is Unchanged in a Healthy Population. Lipids , 52, 255-263. https://doi.org/10.1007/s11745-017-4230-9
Mutungi, G., Ratliff, J., Puglisi, M., Torres-Gonzalez, M., Vaishnav, U., Leite, J.O., et al . (2008) Dietary Cholesterol from Eggs Increases Plasma HDL Cholesterol in Overweight Men Consuming a Carbohydrate-Restricted Diet. The Journal of Nutrition , 138, 272-276. https://doi.org/10.1093/jn/138.2.272
Grundy, S.M. (1983) Absorption and Metabolism of Dietary Cholesterol. Annual Review of Nutrition , 3, 71-96. https://doi.org/10.1146/annurev.nu.03.070183.000443
McNamara, D. (2000) Dietary Cholesterol and Atherosclerosis. Biochimica et Biophysica Acta ( BBA ) -Molecular and Cell Biology of Lipids , 1529, 310-320. https://doi.org/10.1016/s1388-1981(00)00156-6
Herron, K.L., Vega-Lopez, S., Conde, K., Ramjiganesh, T., Roy, S., Shachter, N.S., et al . (2002) Pre-Menopausal Women, Classified as Hypo-or Hyper-Responders, Do Not Alter Their LDL/HDL Ratio Following a High Dietary Cholesterol Challenge. Journal of the American College of Nutrition , 21, 250-258. https://doi.org/10.1080/07315724.2002.10719218
Herron, K.L., Vega-Lopez, S., Ramjiganesh, T., Fernandez, M.L., Conde, K. and Shachter, N.S. (2003) Men Classified as Hypo-or Hyperresponders to Dietary Cholesterol Feeding Exhibit Differences in Lipoprotein Metabolism. The Journal of Nutrition , 133, 1036-1042. https://doi.org/10.1093/jn/133.4.1036