Within‐day energy deficiency and reproductive function in female endurance athletes
Open accessAbstract
We aimed to estimate and compare within‐day energy balance (WDEB) in athletes with eumenorrhea and menstrual dysfunction (MD) with similar 24‐hour energy availability/energy balance (EA/EB). Furthermore, to investigate whether within‐day energy deficiency is associated with resting metabolic rate (RMR), body composition, S‐cortisol, estradiol, T 3 , and fasting blood glucose. We reanalyzed 7‐day dietary intake and energy expenditure data in 25 elite endurance athletes with eumenorrhea (n = 10) and MD (n = 15) from a group of 45 subjects where those with disordered eating behaviors (n = 11), MD not related to low EA (n = 5), and low dietary record validity (n = 4) had been excluded. Besides gynecological examination and disordered eating evaluation, the protocol included RMR measurement; assessment of body composition by dual‐energy X‐ray absorptiometry, blood plasma analysis, and calculation of WDEB in 1‐hour intervals. Subjects with MD spent more hours in a catabolic state compared to eumenorrheic athletes; WDEB < 0 kcal: 23.0 hour (20.8‐23.4) vs 21.1 hour (4.7‐22.3), P = .048; WDEB < −300 kcal: 21.8 hour (17.8‐22.4) vs 17.6 hour (3.9‐20.9), P = .043, although similar 24‐hour EA: 35.6 (11.6) vs 41.3 (12.7) kcal/kg FFM/d, ( P = .269), and EB: −659 (551) vs −313 (596) kcal/d, ( P = .160). Hours with WDEB <0 kcal and <−300 kcal were inversely associated with RMR ratio ( r = −.487, P = .013, r = −.472, P = .018), and estradiol ( r = −.433, P = .034, r = −.516, P = .009), and positively associated with cortisol ( r = .442, P = .027, r = .463, P = .019). In conclusion, although similar 24‐hour EA/EB, the reanalysis revealed that MD athletes spent more time in a catabolic state compared to eumenorrheic athletes. Within‐day energy deficiency was associated with clinical markers of metabolic disturbances.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Sufficient energy is crucial for training consistency, particularly during intensified periods, as prolonged energy restriction can lead to impaired physiological function, maladaptation to prescribed training, and an increased risk of fatigue, illness, and injury.
“It is widely accepted that sufficient energy is crucial for training consistency, particularly during intensified periods, as prolonged energy restriction can lead to impaired physiological function, maladaptation to prescribed training, and an increased risk of fatigue, illness, and injury [61,64,114–116].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [61]
Cites
(2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318149f111 · Cited by 1,554 · see citing works
Self-citationBlack, A. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801376 · Cited by 1,490 · see citing works
Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., Meyer, N., Sherman, R., Steffen, K., Budgett, R., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2014-093502 · Cited by 1,469 · see citing works
Self-citationThomas, D. T., Erdman, K. A., & Burke, L. M. (2016) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2015.12.006 · Cited by 1,359 · see citing works
Eating Disorder Inventory-2 ; Pro-fessional Manual
Garner, D. (1991) · Medical Entomology and Zoology · Cited by 1,283 · see citing works
Loucks, A. B., & Thuma, J. R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020369 · Cited by 760 · see citing works
American College of Sports Medicine position stand, rhe female athlete triad
Nattiv, A. (2007) · Medicine & Science in Sports & Exercise · Cited by 551 · see citing works
Dietary protein for athletes: From requirements to optimum adaptation
Phillips, S. M., & Van Loon, L. J. C. (2011) · Journal of Sports Sciences · doi:10.1080/02640414.2011.619204 · Cited by 530 · see citing works
Energy availability in athletes
Loucks, A. B., Kiens, B., & Wright, H. H. (2011) · Journal of Sports Sciences · doi:10.1080/02640414.2011.588958 · Cited by 513 · see citing works
Melin, A., Tornberg, Å. B., Skouby, S., Faber, J., Ritz, C., Sjödin, A., & Sundgot-Borgen, J. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093240 · Cited by 435 · see citing works
Self-citationRedman, L. M., Heilbronn, L. K., Martin, C. K., de Jonge, L., Williamson, D. A., Delany, J. P., Ravussin, E., & for the Pennington CALERIE team (2009) · PLoS ONE · doi:10.1371/journal.pone.0004377 · Cited by 355 · see citing works
De Souza, M. J., Miller, B. E., Loucks, A. B., Luciano, A. A., Pescatello, L. S., Campbell, C. G., & Lasley, B. L. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.12.5334 · Cited by 315 · see citing works
Neuroendocrinology of nutritional infertility
Wade, G. N., & Jones, J. E. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00475.2004 · Cited by 296 · see citing works
Energy availability and the female athlete triad in elite endurance athletes
Melin, A., Tornberg, Å., Skouby, S., Møller, S., Sundgot-Borgen, J., Faber, J., Sidelmann, J., Aziz, M., & Sjödin, A. (2015) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.12261 · Cited by 289 · see citing works
Self-citationMeasuring the thermic effect of food
Reed, G., & Hill, J. (1996) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.2.164 · Cited by 253 · see citing works
Ovarian 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 · see citing works
Loucks, A. B. (1994) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.78.4.910 · Cited by 174 · see citing works
Goldsmith, R., Joanisse, D. R., Gallagher, D., Pavlovich, K., Shamoon, E., Leibel, R. L., & Rosenbaum, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00053.2009 · Cited by 171 · see citing works
Relationship between energy deficits and body composition in elite female gymnasts and runners
DEUTZ, R. C., Benardot, D., Martin, D. E., & Cody, M. M. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200003000-00017 · Cited by 169 · see citing works
Self-citationDietary Recommendations and Athletic Menstrual Dysfunction
Manore, M. M. (2002) · Sports Medicine · doi:10.2165/00007256-200232140-00002 · Cited by 135 · see citing works
Phelain, J. F., Reinke, E., Harris, M. A., & Melby, C. L. (1997) · Journal of the American College of Nutrition · doi:10.1080/07315724.1997.10718664 · Cited by 119 · see citing works
Burke, L. M. (2001) · Canadian Journal of Applied Physiology · doi:10.1139/h2001-055 · Cited by 112 · see citing works
Gibbs, J. C., Williams, N. I., Scheid, J. L., Toombs, R. J., & Souza, M. J. D. (2011) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.21.4.280 · Cited by 106 · see citing works
Effect of meal frequency and timing on physical performance
Hawley, J. A., & Burke, L. M. (1997) · British Journal of Nutrition · doi:10.1079/bjn19970107 · Cited by 99 · see citing works
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
Self-citationScheid, J. L., Williams, N. I., West, S., VanHeest, J. L., & Souza, M. J. D. (2008) · Appetite · doi:10.1016/j.appet.2008.09.016 · Cited by 78 · see citing works
Menstrual Disorders in Athletes
Redman, L., & Loucks, A. (2005) · Sports Medicine · doi:10.2165/00007256-200535090-00002 · Cited by 75 · see citing works
Guebels, C. P., Kam, L., Maddalozzo, G., & Manore, M. (2014) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2012-0165 · Cited by 73 · see citing works
Intra-individual variation in resting metabolic rate during the menstrual cycle
Henry, C. J., Lightowler, H. J., & Marchini, J. (2003) · British Journal Of Nutrition · doi:10.1079/bjn2003839 · Cited by 64 · see citing works
Olson, B. R., Cartledge, T. P., Sebring, N. G., Defensor, R., & Nieman, L. K. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.4.7714088 · Cited by 58 · see citing works
Reduced catecholamine response to exercise in amenorrheic athletes.
Schaal, K., Loan, M. V., & Casazza, G. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181e91ece · Cited by 45 · see citing works
Effects of meal frequency on body composition during weight control in boxers
Iwao, S., Mori, K., & Sato, Y. (1996) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.1996.tb00469.x · Cited by 44 · see citing works
O’Donnell, E., Harvey, P., & Souza, M. J. D. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03332.x · Cited by 39 · see citing works
Benardot, D. (2013) · Pensar en Movimiento Revista de Ciencias del Ejercicio y la Salud · doi:10.15517/pensarmov.v11i2.10841 · Cited by 26 · see citing works
Self-citationTIMING OF ENERGY AND FLUID INTAKE
Benardot, D. (2007) · ACSMʼs Health & Fitness Journal · doi:10.1249/01.fit.0000281226.23643.de · Cited by 22 · see citing works
Self-citationEnergy balance and reproductive function in active women.
Harber, V. (2004) · Canadian Journal of Applied Physiology · doi:10.1139/h04-005 · Cited by 19 · see citing works
Benardot, D. (2013) · Dialnet (Universidad de la Rioja) · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
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 · see citing works
Self-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 · see citing works
Self-citationEnergy Availability in Athletics: Health, Performance, and Physique
Melin, A. K., Heikura, I. A., Tenforde, A., & Mountjoy, M. (2019) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0201 · Cited by 258 · see citing works
Self-citationWasserfurth, P., Palmowski, J., Hahn, A., & Krüger, K. (2020) · Sports Medicine - Open · doi:10.1186/s40798-020-00275-6 · Cited by 190 · see citing works
Stellingwerff, T., Heikura, I. A., Meeusen, R., Bermon, S., Seiler, S., Mountjoy, M. L., & Burke, L. M. (2021) · Sports Medicine · doi:10.1007/s40279-021-01491-0 · Cited by 171 · see citing works
International society of sports nutrition position stand: nutritional concerns of the female athlete
Sims, S. T., Kerksick, C. M., Smith-Ryan, A. E., Janse de Jonge, X. A. K., Hirsch, K. R., Arent, S. M., Hewlings, S. J., Kleiner, S. M., Bustillo, E., Tartar, J. L., et al. (2023) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2023.2204066 · Cited by 91 · see citing works
“elevations in cortisol and decreases in RMR and estradiol the longer they delay nutrition intake, post-exercise [62].”
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 · see citing works
Civil, R., Lamb, A., Loosmore, D., Ross, L., Livingstone, K., Strachan, F., Dick, J. R., Stevenson, E. J., Brown, M. A., & Witard, O. C. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2018.00136 · Cited by 63 · see citing works
Self-reported periodization of nutrition in elite female and male runners and race walkers
Heikura, I. A., Stellingwerff, T., & Burke, L. M. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01732 · Cited by 40 · see citing works
Low Energy Availability and Relative Energy Deficiency in Sport: What Coaches Should Know
Charlton, B. T., Forsyth, S., & Clarke, D. C. (2022) · International Journal of Sports Science & Coaching · doi:10.1177/17479541211054458 · Cited by 36 · see citing works
Nutritional Needs of the Female Athlete: Risk and Prevention of Low Energy Availability
Black, K. E., Baker, D. F., & Sims, S. T. (2020) · Strength & Conditioning Journal · doi:10.1519/ssc.0000000000000464 · Cited by 15 · see citing works
Dasa, M. S., Friborg, O., Kristoffersen, M., Pettersen, G., Sagen, J. V., Torstveit, M. K., Sundgot‐Borgen, J., & Rosenvinge, J. H. (2024) · European Journal of Sport Science · doi:10.1002/ejsc.12129 · Cited by 15 · see citing works
Self-citationÞegar orkuna skortir–áhrif hlutfallslegs orkuskorts í íþróttum (RED-s) á heilsu og árangur
Faculty of Health promotion, S. A. L. S., Varðardóttir, B., Guðmundsdóttir, S. L., Faculty of Health promotion, S. A. L. S., Ólafsdóttir, A. S., & Faculty of Health promotion, S. A. L. S. (2020) · Læknablaðið · doi:10.17992/lbl.2020.09.596 · Cited by 10 · see citing works
- Authors
- Fahrenholtz, I. L., Sjödin, A., Benardot, D., Tornberg, Å. B., Skouby, S., Faber, J., Sundgot‐Borgen, J. K., & Melin, A. K.
- Affiliations
- University of Copenhagen (DK)
- Georgia State University (US)
- Lund University (SE)
- Norwegian School of Sport Sciences (NO)
- Corresponding author
- Melin, A. K.
- Venue
- Scandinavian Journal of Medicine & Science in Sports
- Publisher
- Wiley
- Published
- 2018-02-05
- Volume
- 28
- Issue
- 3
- Pages
- 1139-1146
- ISSN
- 0905-7188 (ISSN-L)
- 1600-0838
- OpenAlex
- W2775617072
- Cited by
- 106
- References
- 37
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 12 · 2023: 13 · 2022: 12 · 2021: 11 · 2020: 26 · 2019: 11 · 2018: 5
- FWCI
- 13.34
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Scandinavian Journal of Medicine and Science in Sports (publishedVersion)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Københavns Universitet
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Menstrual Health and Disorders
- Keywords
- energy deficiency, menstrual disorders, female endurance athletes, eumenorrhea, resting metabolic rate, estradiol, cortisol, body composition, energy availability, catabolic state, energy expenditure, thyroid hormones, fasting blood glucose, disordered eating, female athlete triad
- MeSH terms
- Adult, Basal Metabolism, Blood Glucose, Body Composition, Energy Metabolism, Estradiol, Feeding Behavior, Female, Humans, Hydrocortisone, Menstruation, Menstruation Disturbances, Physical Endurance, Saliva, Thyrotropin, Triiodothyronine, Diet Records, Young Adult, Athletes
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