Low energy availability in female athletes: from the lab to the field
Abstract
Decades of laboratory research have shown impairments to several body systems after only 4–5 days of strictly controlled consistent low energy availability (LEA); where energy availability (EA) = Energy Intake (EI) − Exercise Energy Expenditure (EEE)/Fat‐Free Mass. Meanwhile, cross‐sectional reports exist on the interrelatedness of LEA, menstrual dysfunction and impaired bone health in females (the Female Athlete Triad). These findings have demonstrated that LEA is the key underpinning factor behind a broader set of health and performance outcomes, recently termed as Relative Energy Deficiency in Sport (RED‐S). There is utmost importance of early screening and diagnosis of RED‐S to avoid the development of severe negative health and performance outcomes. However, a significant gap exists between short‐term laboratory studies and cross‐sectional reports, or clinically field‐based situations, of long‐term/chronic LEA and no definitive, validated diagnostic tests for RED‐S exist. This review aims to highlight methodological challenges related to the assessment of the components of EA equation in the field (e.g. challenges with EI and EEE measures). Due to the uncertainty of these parameters, we propose the use of more chronic “objective” markers of LEA (i.e. blood markers). However, we note that direct extrapolations of laboratory‐based outcomes into the field are likely to be problematic due to potentially poor ecological validity and the extreme variability in most athlete's daily EI and EEE. Therefore, we provide a critical appraisal of the scientific literature, highlighting research gaps, and a potential set of leading objective RED‐S markers while working in the field. Highlights: Direct application of short‐term laboratory‐based findings in the field is problematic. Calculation of energy availability (EA) in the field is methodologically challenging and prone to errors. The use of several biomarkers may allow the detection of early exposure to low EA in the female athlete.
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In the real world, athletes experience exposure to LEA (purposefully or inadvertently) in various manners along the continuum from adaptable to problematic.
“In the real world, athletes experience exposure to LEA (purposefully or inadvertently) in various manners along the continuum from adaptable to problematic.”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [40]
The Figure 2 legend describes several ways athletes may experience LEA in real-world settings, and the Introduction describes a continuum from health to disease. Our copy does not say whether exposure is purposeful or inadvertent, or specifically describe an adaptable-to-problematic continuum. (LLM, conf=0.84)
Experimental — accuracy not yet measuredEmerging definitions highlight short-term LEA as a few days to weeks, medium-term as weeks to months and long-term as months to years.
“Emerging definitions highlight short-term LEA as a few days to weeks, mediumterm as weeks to months and long-term as months to years.37 40”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [40]
The Introduction defines medium-term LEA as weeks to under three months and long-term LEA as more than three months to years, matching the claim broadly. It defines short-term LEA as less than seven days, however, so the claim's 'few days to weeks' extends that category beyond the paper's definition. (LLM, conf=0.87)
Experimental — accuracy not yet measuredEndocrine changes due to low energy availability include triiodothyronine alterations and decreases in leptin, which affect the metabolism and systemic availability of carbohydrate.
“Endocrine changes due to LEA include triiodothyronine (T3) alterations and decreases in leptin, which affect the metabolism and systemic availability of CHO [44].”
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 [44]
Section 3.1 reports that low energy availability reduces leptin and downregulates T3. Section 4.2 says reduced carbohydrate availability can affect leptin and T3, which in turn affect resting metabolic rate. It does not say these hormonal changes affect the systemic availability of carbohydrate; the carbohydrate relationship it describes runs in the other direction. (LLM, conf=0.87)
Experimental — accuracy not yet measuredProtocols to undertake EA assessments or EA-based diet prescription will continue to be challenged by the errors associated with accurately measuring EI, EEE and other contributing components (eg, FFM, resting metabolic rate (RMR)).
“Also, protocols to undertake EA assessments or EA-based diet prescription will continue to be challenged by the errors associated with accurately measuring EI, EEE and other contributing components (eg, FFM, resting metabolic rate (RMR)), 40 49 129”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [40]
Low energy availability, mediated by reduced carbohydrate availability, affects leptin and triiodothyronine concentrations, which can suppress resting metabolic rate.
“LEA, mediated by reduced CHO availability, affects leptin and triiodothyronine (T3) concentrations, which, in turn, can suppress the resting metabolic rate (RMR) [44].”
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 [44]
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Cites
Compendium of physical activities: an update of activity codes and MET intensities
AINSWORTH, B. E., HASKELL, W. L., WHITT, M. C., IRWIN, M. L., SWARTZ, A. M., STRATH, S. J., O???BRIEN, W. L., BASSETT, D. R., SCHMITZ, K. H., EMPLAINCOURT, P. O., et al. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200009001-00009 · Cited by 8,497 · see citing works
(2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318149f111 · Cited by 1,554 · 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 · cited 1× · see citing works
“health, immunity, protein synthesis, cardiovascular health caused by relative energy deficiency”(Mountjoy, 2014).”
BackgroundBone mineral content of amenorrheic and eumenorrheic athletes
Drinkwater, B. L., Nilson, K., Chesnut, C. H., Bremner, W. J., Shainholtz, S., & Southworth, M. B. (1984) · New England Journal of Medicine · doi:10.1056/nejm198408023110501 · Cited by 956 · see citing works
IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update
Mountjoy, M., Sundgot-Borgen, J. K., Burke, L. M., Ackerman, K. E., Blauwet, C., Constantini, N., Lebrun, C., Lundy, B., Melin, A. K., Meyer, N. L., et al. (2018) · British Journal of Sports Medicine · doi:10.1136/bjsports-2018-099193 · Cited by 883 · 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
Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline
Gordon, C. M., Ackerman, K. E., Berga, S. L., Kaplan, J. R., Mastorakos, G. P., Misra, M., Murad, M. H., Santoro, N. F., & Warren, M. P. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00131 · Cited by 634 · see citing works
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 11× · 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).”
BackgroundResultInfluentialDose-Response Relationships Between Energy Availability and Bone Turnover in Young Exercising Women
Ihle, R., & Loucks, A. B. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040410 · Cited by 523 · 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
The female athlete triad: disordered eating, amenorrhea, osteoporosis
YEAGER, K. K., AGOSTINI, R., NATTIV, A., & DRINKWATER, B. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199307000-00003 · Cited by 436 · see citing works
Heikura, I. A., Uusitalo, A. L. T., Stellingwerff, T., Bergland, D., Mero, A. A., & Burke, L. M. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2017-0313 · Cited by 318 · see citing works
Self-citationSouza, M. J. D., Toombs, R. J., Scheid, J. L., O’Donnell, E., West, S., & Williams, N. I. (2009) · Human Reproduction · doi:10.1093/humrep/dep411 · Cited by 306 · see citing works
Martin, D., Sale, C., Cooper, S. B., & Elliott-Sale, K. J. (2017) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2017-0330 · Cited by 292 · 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
EFFECT OF CALORIC RESTRICTION AND DIETARY COMPOSITION ON SERUM T3AND REVERSE T3IN MAN
Spaulding, S. W., CHOPRA, I. J., Sherwin, R. S., & Lyall, S. S. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-42-1-197 · Cited by 278 · see citing works
Exercise and bone health across the lifespan
Santos, L., Elliott-Sale, K. J., & Sale, C. (2017) · Biogerontology · doi:10.1007/s10522-017-9732-6 · Cited by 256 · see citing works
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 · see citing works
Joy, E., Souza, M. D. D., Nattiv, A., Misra, M., Williams, N., Mallinson, R. J., Gibbs, J., Olmsted, M., Goolsby, M. A., Matheson, G., et al. (2014) · Current sports medicine reports · doi:10.1249/jsr.0000000000000077 · Cited by 242 · see citing works
Thyroid hormone signaling in energy homeostasis and energy metabolism
McAninch, E. A., & Bianco, A. C. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12374 · Cited by 241 · see citing works
Validity of Dietary Assessment in Athletes: A Systematic Review
Capling, L., Beck, K. L., Gifford, J. A., Slater, G., Flood, V. M., & O'Connor, H. T. (2017) · Nutrients · doi:10.3390/nu9121313 · Cited by 239 · see citing works
Endocrine 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 · see citing works
Areta, J. L., Burke, L. M., Camera, D. M., West, D. W. D., Crawshay, S., Moore, D. R., Stellingwerff, T., Phillips, S. M., Hawley, J. A., & Coffey, V. G. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00590.2013 · Cited by 227 · see citing works
Self-citationRole of IGF-I in skeletal muscle mass maintenance
Clemmons, D. R. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.04.002 · Cited by 218 · see citing works
Areta, J. L., Taylor, H. L., & Koehler, K. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04516-0 · Cited by 214 · see citing works
Self-citationHilton, L. K., & Loucks, A. B. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.1.e43 · Cited by 214 · cited 4× · see citing works
“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).”
BackgroundInfluentialGarthe, I., Raastad, T., Refsnes, P. E., Koivisto, A., & Sundgot-Borgen, J. (2011) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.21.2.97 · Cited by 209 · see citing works
Leptin in humans: lessons from translational research
Blüher, S., & Mantzoros, C. S. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26788e · Cited by 203 · see citing works
Parallels with the Female Athlete Triad in Male Athletes
Tenforde, A., Barrack, M., Nattiv, A., & Fredericson, M. (2016) · Sports Medicine · doi:10.1007/s40279-015-0411-y · Cited by 199 · see citing works
Growth Hormone Release During Acute and Chronic Aerobic and Resistance Exercise
Wideman, L., Weltman, J. Y., Hartman, M. L., Veldhuis, J. D., & WELTMAN, A. L. (2002) · Sports Medicine · doi:10.2165/00007256-200232150-00003 · Cited by 192 · see citing works
O’Driscoll, R., Turicchi, J., Beaulieu, K., Scott, S., Matu, J., Deighton, K., Finlayson, G., & Stubbs, R. J. (2018) · British Journal of Sports Medicine · doi:10.1136/bjsports-2018-099643 · Cited by 189 · see citing works
Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability
Loucks, A. B., & Heath, E. M. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.3.r817 · Cited by 187 · see citing works
Fractures in Relation to Menstrual Status and Bone Parameters in Young Athletes
Ackerman, K. E., Sokoloff, N. C., Maffazioli, G. D. N., Clarke, H., Lee, H., & Misra, M. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000574 · Cited by 179 · see citing works
Metabolic adaptation to weight loss: implications for the athlete
Trexler, E. T., Smith‐Ryan, A. E., & Norton, L. E. (2014) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-11-7 · Cited by 178 · 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
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
Effects of reduced energy availability on bone metabolism in women and men
Papageorgiou, M., Elliott-Sale, K. J., Parsons, A., Tang, J. C. Y., Greeves, J. P., Fraser, W. D., & Sale, C. (2017) · Bone · doi:10.1016/j.bone.2017.08.019 · Cited by 159 · see citing works
Determinants of GH resistance in malnutrition
Fazeli, P. K., & Klibanski, A. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0477 · Cited by 158 · see citing works
Williams, N. I., Leidy, H. J., Hill, B. R., Lieberman, J. L., Legro, R. S., & Souza, M. J. D. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00386.2013 · Cited by 156 · see citing works
Induction and prevention of low-T3 syndrome in exercising women
Loucks, A. B., & Callister, R. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.264.5.r924 · Cited by 143 · see citing works
Souza, M. J. D., Lee, D. K., VanHeest, J. L., Scheid, J. L., West, S., & Williams, N. I. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.171 · Cited by 142 · see citing works
Hector, A. J., & Phillips, S. M. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2017-0273 · Cited by 137 · see citing works
Menstrual disruption with exercise is not linked to an energy availability threshold
LIEBERMAN, J. L., DE SOUZA, M. J., WAGSTAFF, D. A., & WILLIAMS, N. I. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001451 · Cited by 127 · see citing works
Luteal 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 · see citing works
Loucks, A. B. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0570 · Cited by 118 · see citing works
Carbohydrate intake and short-term regulation of leptin in humans
Jenkins, A. B., Markovic, T., Fleury, A. C., & Campbell, L. V. (1997) · Diabetologia · doi:10.1007/s001250050686 · Cited by 116 · see citing works
Drive for thinness score is a proxy indicator of energy deficiency in exercising women
Souza, M. J. D., Hontscharuk, R., Olmsted, M. P., Kerr, G. A., & Williams, N. I. (2006) · Appetite · doi:10.1016/j.appet.2006.10.009 · Cited by 106 · see citing works
Within‐day energy deficiency and reproductive function in female endurance athletes
Fahrenholtz, I. L., Sjödin, A., Benardot, D., Tornberg, Å. B., Skouby, S., Faber, J., Sundgot‐Borgen, J. K., & Melin, A. K. (2018) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.13030 · Cited by 106 · see citing works
The Bone Metabolic Response to Exercise and Nutrition
Dolan, E., Varley, I., Ackerman, K. E., Pereira, R. M. R., Elliott-Sale, K. J., & Sale, C. (2019) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000215 · Cited by 94 · see citing works
Reduced Neuromuscular Performance in Amenorrheic Elite Endurance Athletes
Tornberg, Å. B., Melin, A., Koivula, F. N. M., JOHANSSON, A., Skouby, S. O., Faber, J., & Sjödin, A. M. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001383 · Cited by 92 · see citing works
Cialdella-Kam, L., Guebels, C. P., Maddalozzo, G., & Manore, M. (2014) · Nutrients · doi:10.3390/nu6083018 · Cited by 90 · 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
Papageorgiou, M., Martin, D., Colgan, H., Cooper, S. B., Greeves, J. P., TANG, J. C. Y., Fraser, W. D., Elliott-Sale, K. J., & Sale, C. (2018) · Bone · doi:10.1016/j.bone.2018.06.016 · Cited by 75 · see citing works
Hulmi, J. J., Isola, V., Suonpää, M., Järvinen, N. J., Kokkonen, M., Wennerström, A., Nyman, K., Perola, M., Ahtiainen, J. P., & Häkkinen, K. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2016.00689 · Cited by 74 · see citing works
Koehler, K., Achtzehn, S., Braun, H., Mester, J., & Schaenzer, W. (2013) · Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme · doi:10.1139/apnm-2012-0373 · Cited by 73 · see citing works
Slow restoration of LH pulsatility by refeeding in energetically disrupted women
Loucks, A. B., Verdun, M., & Thuma), (. T. T. A. O. R. B. A. J. R. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1218 · Cited by 66 · see citing works
Al‐Khelaifi, F., Diboun, I., Donati, F., Botrè, F., Abraham, D., Hingorani, A. D., Albagha, O., Georgakopoulos, C. G., Suhre, K., Yousri, N. A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-56496-7 · Cited by 61 · see citing works
Koehler, K., Williams, N. I., Mallinson, R. J., Ricker, E. A., Allaway, H. C. M., & Souza, M. J. D. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00110.2016 · Cited by 52 · see citing works
Physical health and symptoms of relative energy deficiency in female fitness athletes
Mathisen, T. F., Heia, J., Raustøl, M., Sandeggen, M., Fjellestad, I., & Sundgot-Borgen, J. K. (2019) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13568 · Cited by 47 · see citing works
Alternate-Day Low Energy Availability During Spring Classics in Professional Cyclists
Heikura, I. A., Quod, M. J., Strobel, N., Palfreeman, R., Civil, R., & Burke, L. M. (2019) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2018-0842 · Cited by 32 · see citing works
Self-citationThe use of urine LH detection kits to time intrauterine insemination with donor sperm
Khattab, A. F., Mustafa, F., & Taylor, P. J. (2005) · Human Reproduction · doi:10.1093/humrep/dei098 · Cited by 27 · see citing works
Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function
Loucks, A. (2020) · Endocrinology of Physical Activity and Sport · doi:10.1007/978-1-62703-314-5_11 · Cited by 24 · see citing works
Westerterp, K. R. (2019) · European Journal of Clinical Nutrition · doi:10.1038/s41430-019-0408-y · Cited by 21 · see citing works
Areta, J. (2020) · International Journal of Sport Nutrition & Exercise Metabolism · doi:10.1123/ijsnem.2019-0284 · Cited by 18 · see citing works
Self-citationJohansen, J.-M., Eriksen, S., Sunde, A., Slettemeås, Ø. B., Helgerud, J., & Støren, Ø. (2020) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2019-0689 · Cited by 14 · see citing works
Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function
Loucks, A. B. (2020) · Contemporary Endocrinology · doi:10.1007/978-3-030-33376-8_11 · Cited by 13 · see citing works
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Self-citationMCKAY, A. K. A., PEELING, P., PYNE, D. B., TEE, N., WHITFIELD, J., SHARMA, A. P., HEIKURA, I. A., & BURKE, L. M. (2022) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002819 · Cited by 80 · see citing works
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Jagim, A. R., Fields, J. B., Magee, M. K., Kerksick, C. M., & Jones, M. T. (2022) · Nutrients · doi:10.3390/nu14050986 · Cited by 89 · see citing works
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Self-citationAckerman, K. E., Rogers, M. A., Heikura, I. A., Burke, L. M., Stellingwerff, T., Hackney, A. C., Verhagen, E., Schley, S., Saville, G. H., Mountjoy, M., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-107359 · Cited by 43 · see citing works
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Grabia, M., Perkowski, J., Socha, K., & Markiewicz‐Żukowska, R. (2024) · Nutrients · doi:10.3390/nu16030359 · Cited by 59 · see citing works
Hilkens, L., van Schijndel, N., Weijer, V., Boerboom, M., BURG, E. V. D., Peters, V., Kempers, R., Bons, J. A. P., van Loon, L. J. C., & van Dijk, J. (2023) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003113 · Cited by 34 · see citing works
Lodge, M. T., Ward-Ritacco, C. L., & Melanson, K. J. (2023) · Nutrients · doi:10.3390/nu15204457 · Cited by 33 · see citing works
Nutritional Considerations for Female Athletes in Weight Category Sports
Langan‐Evans, C., Reale, R., Sullivan, J., & Martin, D. (2021) · European Journal of Sport Science · doi:10.1080/17461391.2021.1936655 · Cited by 30 · see citing works
Nutritional optimization for female elite football players—topical review
de Sousa, M. V., Lundsgaard, A., Christensen, P. M., Christensen, L. H., Randers, M. B., Mohr, M., Nybo, L., Kiens, B., & Fritzen, A. M. (2021) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14102 · Cited by 34 · see citing works
Nutrition for female athletes: What we know, what we don't know, and why
Areta, J. L., & Elliott-Sale, K. J. (2022) · European Journal of Sport Science · doi:10.1080/17461391.2022.2046176 · Cited by 24 · see citing works
Self-citationJeppesen, J. S., Hellsten, Y., Melin, A., & Hansen, M. (2025) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.70089 · Cited by 21 · see citing works
Langan‐Evans, C., Hearris, M. A., McQuilliam, S. J., Burke, L. M., Stellingwerff, T., Elliott-Sale, K. J., & Morton, J. P. (2023) · International Journal of Sports Science & Coaching · doi:10.1177/17479541231163088 · Cited by 21 · see citing works
Self-citationDasa, M. S., Friborg, O., Kristoffersen, M., Pettersen, G., Sagen, J. V., Sundgot-Borgen, J. K., & Rosenvinge, J. H. (2023) · Sports Medicine - Open · doi:10.1186/s40798-023-00605-4 · Cited by 21 · see citing works
Dasa, M. S., Friborg, O., Kristoffersen, M., Pettersen, G., Sundgot-Borgen, J. K., & Rosenvinge, J. H. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19084770 · Cited by 18 · see citing works
Physical performance during energy deficiency in humans: An evolutionary perspective.
Areta, J. (2023) · Comparative biochemistry and physiology. Part A, Molecular & integrative physiology · doi:10.1016/j.cbpa.2023.111473 · Cited by 15 · see citing works
Self-citationDasa, 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
Stenqvist, T. B., Melin, A., & Torstveit, M. K. (2023) · Nutrients · doi:10.3390/nu15245086 · Cited by 14 · see citing works
Oxfeldt, M., Marsi, D., Christensen, P. M., Andersen, O. E., Johansen, F. T., Bangshaab, M., Risikesan, J., Jeppesen, J. S., Hellsten, Y., Phillips, S. M., et al. (2023) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003370 · Cited by 14 · see citing works
Coates, A. M., Thompson, K. M. A., Grigore, M. M., Baker, R. E., Pignanelli, C., Robertson, A. A., Frangos, S. M., Cheung, C. P., & Burr, J. (2023) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.14551 · Cited by 14 · see citing works
Nutritional perspectives in female soccer: a scoping review
Martinho, D. V., Field, A., Naughton, R. J., Ribeiro, A. S., Rebelo, A., Gouveia, É. R., & Sarmento, H. (2024) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2024.2366427 · Cited by 14 · see citing works
Marzuki, M. I. H., Jamil, N. A., Mohamad, M. I., Chai, W. J., Fauzi, N. F. M., Safii, N. S., & Jasme, J. K. (2024) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2024-002193 · Cited by 11 · see citing works
Edwards, V. C., Myers, S., Wardle, S. L., Siddall, A. G., Powell, S. D., Needham‐Beck, S. C., Kefyalew, S. S., Singh, P., Orford, E. R., Venables, M., et al. (2022) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2021-0190 · Cited by 11 · see citing works
Taguchi, M., & Manore, M. M. (2022) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2022.885631 · Cited by 11 · see citing works
Bonilla, D. A., Duque-Zuluaga, L. T., Muñoz-Urrego, L. P., Hoyos, K. F., Agudelo-Martínez, A., Kammerer-López, M., Petro, J. L., & Kreider, R. B. (2022) · Nutrients · doi:10.3390/nu14194059 · Cited by 8 · see citing works
Dambacher, L., Pritchett, K. L., PRITCHETT, R. C., & Larson, A. M. (2023) · Journal of Athletic Training · doi:10.4085/1062-6050-0454.23 · Cited by 7 · see citing works
Frazer, R., Bowler, A.-L. M., Condo, D., Cox, G. R., Pelly, F. E., & Slater, G. (2024) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2024-0002 · Cited by 7 · see citing works
Mursu, J., Ristimäki, M., Malinen, I., Petäjä, P., Isola, V., Ahtiainen, J. P., & Hulmi, J. J. (2023) · Nutrients · doi:10.3390/nu15020382 · Cited by 9 · see citing works
The Physiological Requirements of and Nutritional Recommendations for Equestrian Riders
Best, R., Williams, J. M., & Pearce, J. (2023) · Nutrients · doi:10.3390/nu15234977 · Cited by 7 · see citing works
Smith, E., Drager, K., Groves, E. M., Gabel, L., Boyd, S. K., & Burt, L. A. (2025) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2024-002320 · Cited by 5 · see citing works
Castellanos-Mendoza, M. C., Galloway, S. D. R., & Witard, O. C. (2023) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2023.1279534 · Cited by 5 · see citing works
Sim, A., Tan, H. Q., Ali, Y., & Burns, S. F. (2024) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2024-0037 · Cited by 6 · see citing works
Garay, J., Sebe, J. G., Strickland, J., Graves, L., & Voss, M. A. (2025) · Current Developments in Nutrition · doi:10.1016/j.cdnut.2025.106007 · Cited by 5 · see citing works
Study on the correlation between energy availability and subclinical menstrual disorders
Bingzheng, Z., Zhuo, J., Qihao, W., & Bai, L. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1479254 · Cited by 4 · see citing works
Rethinking Energy Availability from Conceptual Models to Applied Practice: A Narrative Review
Espinar, S., Sánchez-Fernández, M. A., Martín-Olmedo, J. J., Rueda-Córdoba, M., & Jurado‐Fasoli, L. (2026) · Nutrients · doi:10.3390/nu18030379 · Cited by 4 · see citing works
Risk of Low Energy Availability in New Zealand National Team and U20 Female Football Representatives
Coombes, I., & Badenhorst, C. E. (2024) · Women in Sport and Physical Activity Journal · doi:10.1123/wspaj.2023-0041 · Cited by 4 · see citing works
Wilson, P. B. (2025) · Sports Medicine · doi:10.1007/s40279-025-02372-6 · Cited by 4 · see citing works
Kettunen, O., Taipale, R. S., Mursu, J., Linnamo, V., & Ihalainen, J. K. (2023) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2023.1196659 · Cited by 4 · see citing works
Impact of Equation Choice on Resting Metabolic Rate Ratio in High-Level Men and Women Athletes
Alcántara, J. M. A., Hausen, M., Itaborahy, A. D. S., & Freire, R. (2024) · Journal of the American Nutrition Association · doi:10.1080/27697061.2023.2301405 · Cited by 3 · see citing works
Nutritional Considerations for Female Rock Climbers
Leslie-Wujastyk, M., & Gibson-Smith, E. (2024) · Journal of Science in Sport and Exercise · doi:10.1007/s42978-023-00267-4 · Cited by 3 · see citing works
Hiromatsu, C., & Goto, K. (2024) · Nutrients · doi:10.3390/nu16132048 · Cited by 3 · see citing works
Гаврилова, Е. А., Анатольевич, Ч. О., Pavlova, O. Y., Владимировна, Б. Е., Rasskazova, A. V., Gorkin, M. V., Sarkisov, A. K., Didora, A. B., & Shitova, V. I. (2024) · Human Physiology · doi:10.1134/s036211972470110x · Cited by 3 · see citing works
The Future of Sport and Exercise Science Research in the Female Athlete
Kelly, R. K., & Ackerman, K. E. (2023) · Springer eBooks · doi:10.1007/978-3-031-21881-1_23 · Cited by 3 · see citing works
Ferraris, C., Neri, L. D. C. L., Amoroso, A. P., Bosio, F., Fiorini, S., Guglielmetti, M., Nappi, R. E., & Tagliabue, A. (2025) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2025.2550317 · Cited by 2 · see citing works
Lis, D. M., & Strobel, N. (2026) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2025-0198 · Cited by 2 · see citing works
Ultra-endurance performance: Are women closing the gap? A systematic review and meta-analysis
Sitko, S., López‐Laval, I., Cirer-Sastre, R., & Valenzuela, P. L. (2025) · International Journal of Sports Science & Coaching · doi:10.1177/17479541251354909 · Cited by 2 · see citing works
Mikkonen, R., Hackney, A. C., Hulmi, J., Isola, V., Ahtiainen, J., & Ihalainen, J. (2025) · European Journal of Sport Science · doi:10.1002/ejsc.70076 · Cited by 2 · see citing works
Energy Availability in Female Collegiate Beach Volleyball Athletes
Willingham, B. D., Daou, M., VanArsdale, J., Thomas, M., & Saracino, P. G. (2024) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000004884 · Cited by 4 · see citing works
Toews, B. R., & Doyle–Baker, P. K. (2023) · International Journal of Kinesiology and Sports Science · doi:10.7575/aiac.ijkss.v.11n.3p.46 · Cited by 1 · see citing works
Ashby, J., Mullen, T. P., Smith, P., Rogers, J. P., & Dobbin, N. (2024) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2024-002250 · Cited by 1 · see citing works
Гаврилова, Е. А., Анатольевич, Ч. О., Pavlova, O. Y., Владимировна, Б. Е., Rasskazova, A. V., Gorkin, M. V., Sarkisov, A. K., Didora, A. B., & Shitova, V. I. (2024) · Human Physiology · doi:10.31857/s0131164624060095 · Cited by 1 · see citing works
Lundberg, H. E., Larsen, S. E., Sundgot‐Borgen, J., & Mathisen, T. F. (2026) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2026.2634184 · Cited by 2 · see citing works
Energy Availability and Health
Volpe, S. L. (2023) · ACSMʼs Health & Fitness Journal · doi:10.1249/fit.0000000000000872 · Cited by 1 · see citing works
Figueroa, Y. L., & PERRY, A. C. (2023) · International Journal of Strength and Conditioning · doi:10.47206/ijsc.v3i1.144
Epilogue: “How We Arrived at This Point in Time”
Lebrun, C. M. (2023) · Springer eBooks · doi:10.1007/978-3-031-21881-1_24
Dietary supplements in youth sport
Maughan, R. J., & Shirreffs, S. M. (2023) · doi:10.1093/med/9780192843968.003.0052
COMPARISON OF ACTUAL AND PREDICTED RESTING ENERGY EXPENDITURE IN SKILLED ENDURANCE ATHLETES
Loshkarova, I. O., & Pastukhova, V. A. (2024) · Bulletin of Problems Biology and Medicine · doi:10.29254/2077-4214-2024-1-172-462-469
Resting metabolic rate for energy availability assessment in high-performance sports
Loshkarova, I. O., & Pastukhova, V. A. (2024) · Reports of Vinnytsia National Medical University · doi:10.31393/reports-vnmedical-2024-28(1)-24
Sindrom relativnega energijskega pomanjkanja pri športu med mladostnik
Kozjek, A. K., Kozjek, N. R., & Tonin, G. (2024) · doi:10.18690/um.mf.4.2024.10
Pope, L., Roche, D. M., Marshall, Z. A., Alwan, N., & Webb, R. J. (2025) · Women in Sport and Physical Activity Journal · doi:10.1123/wspaj.2024-0115
Knowledge Gaps, Sleep Disturbances, and Energy Imbalance Among Female Field Hockey Players
Puchalt-Urbano, X., García, A. C., Huertas, J. R., Sánchez-Oliver, A. J., Torre, C. L.-D. L., Aguilar-Aguilar, E., López‐Soto, P. J., Luque, R. M., & Ordóñez, F. M. (2025) · Nutrients · doi:10.3390/nu17243934 · Cited by 1 · see citing works
Evaluating team sport performance: a review of inertial sensor technologies and their applications
Sang, S. (2025) · Sensor Review · doi:10.1108/sr-07-2025-0477
Shabbir, F., Ahmed, F., Ali, A., Azam, M., & Shabbir, B. (2025) · Physical Education of Students · doi:10.15561/20755279.2025.0606
Slater, P., Etxebarria, N., Minehan, M., & Fearon, A. (2026) · Women in Sport and Physical Activity Journal · doi:10.1123/wspaj.2025-0029
Reviewing a Physiologically Specific Tactical Training Program for Military Women
Carroll, R. M., & Ellis, C. E. (2025) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000950
Sozaeva, Z. Y., Атаева, М. В., Rozhkova, Y. V., Khubezhov, I. Y., Bagaeva, K. R., Bdaitsieva, E. S., Khozieva, A. I., Dzigoeva, A. O., Yashurkaeva, R. M., & Umarova, E. R. (2026) · Journal Of Biochemical Technology · doi:10.51847/in6tocscuc
Kanrar, S., Sinha, S., Chandra, S., & Adhikari, S. (2025) · International Journal of Kinanthropometry · doi:10.34256/ijk2533
Rueda-Córdoba, M., Martín-Olmedo, J. J., Espinar, S., Ruiz, J. R., & Jurado‐Fasoli, L. (2026) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2025-0469
Relationship between Energy Availability and Phenotype in Free-Living Athletes
Rueda-Córdoba, M., Martín-Olmedo, J. J., Espinar, S., Ruiz, J. R., & Jurado-Fasoli, L. (2025) · International Journal of Sports Medicine · doi:10.1055/a-2884-0122
Hsu, S.-C., Wu, C.-K., Yang, T., Chan, K., Chen, C.-H., & Lin, Y. (2026) · Research Square · doi:10.21203/rs.3.rs-10038707/v1
Lackner, S., Kärkkäinen, O. K., Mörkl, S., Müller, W., Fürhapter-Rieger, A., Hanhineva, K., & Holasek, S. J. (2026) · Experimental Physiology · doi:10.1113/ep092957
Relative Energy Deficiency in Sport (REDs) and Body Composition
Godley, M., Fink, D., Saupe, T., Edelmers, E., Pļaviņa, L., & Pilmane, M. (2026) · Sports · doi:10.3390/sports14080314
Parnell, S., Kaylor, M. G., Johnson, M. F., Addison, A., Braun-Trocchio, R., & Graybeal, A. J. (2026) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000005535
Methods of Calculating Energy Availability in Current Research: A Standardised Audit
Walker, A. E., McKay, A. K. A., Rogers, M. A., Kuikman, M. A., Ackerman, K. E., Stellingwerff, T., & Burke, L. M. (2026) · Sports Medicine · doi:10.1007/s40279-026-02526-0
Self-citationGuo, Q. (2026) · World Journal of Public Health · doi:10.11648/j.wjph.20261103.20
The Value of Mixed-Method Approaches to Menstrual Health in Sport: A Case of Elite Track Cycling
Schofield, K. (2026) · Springer eBooks · doi:10.1007/978-981-95-8357-7_13
Frazer, R., Askew, C. D., Bowler, A.-L. M., Burke, L. M., Condo, D., Cox, G. R., Feka, K., Halson, S. L., Montoye, A. H. K., Pelly, F. E., et al. (2026) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2026-0088
Forchino, F., Brade, C. J., Kerr, D. A., & Chapman, D. (2026) · Sports · doi:10.3390/sports14100446
Fusi, J., Scarfò, G., & Franzoni, F. (2026) · IntechOpen eBooks · doi:10.5772/intechopen.1018516
- Authors
- Heikura, I. A., Stellingwerff, T., & Areta, J. L.
- Affiliations
- University of Victoria (CA)
- Research Institute for Sport and Exercise Sciences Liverpool John Moores University Liverpool UK
- Corresponding author
- Heikura, Ida A.
- Venue
- European Journal of Sport Science
- Publisher
- Wiley
- Published
- 2021-05-03
- Volume
- 22
- Issue
- 5
- Pages
- 709-719
- ISSN
- 1536-7290 (ISSN-L)
- 1746-1391
- OpenAlex
- W3150555068
- Cited by
- 84
- References
- 66
- Citations by year
- 2026: 17 · 2025: 13 · 2024: 20 · 2023: 22 · 2022: 8 · 2021: 4
- FWCI
- 9.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Sport Science (publishedVersion)
- PubMed (publishedVersion)
- Liverpool John Moores University (acceptedVersion)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
- Physical Sciences › Engineering › Biomedical Engineering › Lower Extremity Biomechanics and Pathologies
- Keywords
- low energy availability, relative energy deficiency in sport, female athletes, energy intake, exercise energy expenditure, menstrual disorders, bone health, female athlete triad, biomarkers, ecological validity
- MeSH terms
- Relative Energy Deficiency in Sport, Energy Intake, Cross-Sectional Studies, Energy Metabolism, Female, Humans, Female Athlete Triad Syndrome, Athletes
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