Cited by 59Eating Disorders and BehaviorsSports Performance and TrainingRegulation of Appetite and Obesity

Mapping the complexities of Relative Energy Deficiency in Sport (REDs): development of a physiological model by a subgroup of the International Olympic Committee (IOC) Consensus on REDs

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Burke, Louise M, Ackerman, Kathryn E, Heikura, Ida A, Hackney, Anthony C, Stellingwerff, Trent·2023·British Journal of Sports Medicine

Abstract

The 2023 International Olympic Committee (IOC) consensus statement on Relative Energy Deficiency in Sport (REDs) notes that exposure to low energy availability (LEA) exists on a continuum between adaptable and problematic LEA, with a range of potential effects on both health and performance. However, there is variability in the outcomes of LEA exposure between and among individuals as well as the specific manifestations of REDs. We outline a framework for a ‘systems biology’ examination of the effect of LEA on individual body systems, with the eventual goal of creating an integrated map of body system interactions. We provide a template that systematically identifies characteristics of LEA exposure (eg, magnitude, duration, origin) and a variety of moderating factors (eg, medical history, diet and training characteristics) that could exacerbate or attenuate the type and severity of impairments to health and performance faced by an individual athlete. The REDs Physiological Model may assist the diagnosis of underlying causes of problems associated with LEA, with a personalised and nuanced treatment plan promoting compliance and treatment efficacy. It could also be used in the strategic prevention of REDs by drawing attention to scenarios of LEA in which impairments of health and performance are most likely, based on knowledge of the characteristics of the LEA exposure or moderating factors that may increase the risk of harmful outcomes. We challenge researchers and practitioners to create a unifying and dynamic physiological model for each body system that can be continuously updated and mapped as knowledge is gained.

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  1. Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med 2018;52:687-97. · DOI · Paper page
  2. Otis CL, Drinkwater B, Johnson M, et al. American college of sports medicine position stand. The female athlete Triad. Med Sci Sports Exerc 1997;29:i-ix. · DOI · Paper page
  3. Nattiv A, De Souza MJ, Koltun KJ, et al. The male athlete Triad-A consensus statement from the female and male athlete Triad coalition part 1: definition and scientific basis. Clin J Sport Med 2021;31:345-53. · DOI
  4. Fredericson M, Kussman A, Misra M, et al. The male athlete Triad-A consensus statement from the female and male athlete Triad coalition part II: diagnosis, treatment, and return-to-play. Clin J Sport Med 2021;31:349-66. · DOI
  5. Stellingwerff T, Mountjoy ML, McClusky WTP, et al. A review of the scientific rationale, development, and validation of the IOC relative energy deficiency in sport clinical assessment tool -version 2 (IOC Reds Cat2): by a sub-group of the IOC consensus on. REDs British Journal of Sports Medicine 2023.
  6. Mathisen TFet al. Body composition practices as antecedents of Reds: minimizing risks and optimizing benefits of assessment -a narrative review by a sub-group of the IOC consensus on relative energy deficiency in sport (Reds). Br J Sports Med 2023.
  7. Torstveit MK, Ackerman KE, Constantini N, et al. Primary, secondary, and tertiary prevention of Reds -a narrative review by a sub-group of the IOC consensus on relative energy deficiency in sport (Reds). Br J Sports Med 2023.
  8. Holtzman B, Rogers M, Heikura IA, et al. Methods to study Reds -a narrative review by a sub-group of the IOC consensus on relative energy deficiency in sport (Reds). Br J Sports Med 2023.
  9. De Souza MJ, Strock NCA, Ricker EA, et al. The path towards progress: A critical review to advance the science of the female and male athlete Triad and relative energy deficiency in sport. Sports Med 2022;52:13-23. · DOI · Paper page
  10. Loucks AB. The response of luteinizing hormone Pulsatility to 5 days of low energy availability disappears by 14 years of gynecological age. J Clin Endocrinol Metab 2006;91:3158-64. · DOI
  11. Koehler K, Hoerner NR, Gibbs JC, et al. Low energy availability in exercising men is associated with reduced Leptin and insulin but not with changes in other metabolic hormones. J Sports Sci 2016;34:1921-9. · DOI · Paper page
  12. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol 1994;266(3 Pt 2):R817-23. · DOI
  13. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 2004;19:1231-40. · DOI · Paper page
  14. Logue D, Madigan SM, Delahunt E, et al. Low energy availability in athletes: A review of prevalence, dietary patterns, physiological health, and sports performance. Sports Med 2018;48:73-96. · DOI · Paper page
  15. Loucks AB, Thuma JR. Luteinizing hormone Pulsatility is disrupted at a threshold of energy availability in regularly Menstruating women. J Clin Endocrinol Metab 2003;88:297-311. · DOI · Paper page
  16. Williams NI, Young JC, McArthur JW, et al. Strenuous exercise with caloric restriction: effect on luteinizing hormone secretion. Med Sci Sports Exerc 1995;27:1390-8.
  17. Ruffing KM, Koltun KJ, De Souza MJ, et al. Moderate weight loss is associated with reductions in LH pulse frequency and increases in 24-hour Cortisol with no change in perceived stress in young Ovulatory women. Physiology & Behavior 2022;254:113885. · DOI
  18. Baer JT. Endocrine parameters in Amenorrheic and Eumenorrheic adolescent female runners. Int J Sports Med 1993;14:191-5. · DOI
  19. Gibbs JC, Williams NI, Scheid JL, et al. The Association of a high drive for thinness with energy deficiency and severe Menstrual disturbances: confirmation in a large population of exercising women. Int J Sport Nutr Exerc Metab 2011;21:280-90. · DOI
  20. Gibbs JC, Williams NI, Mallinson RJ, et al. Effect of high dietary restraint on energy availability and Menstrual status. Med Sci Sports Exerc 2013;45:1790-7. · DOI
  21. De Souza MJ, Koltun KJ, Strock NC, et al. Rethinking the concept of an energy availability threshold and its role in the female athlete Triad. Current Opinion in Physiology 2019;10:35-42. · DOI
  22. Gadgil M, Bossert WH. Life historical consequences of natural selection. The American Naturalist 1970;104:1-24. · DOI · Paper page
  23. Stearns SC. The evolution of life histories Oxford. New York: Oxford University Press, 1992.
  24. Lieberman JL, DE Souza MJ, Wagstaff DA, et al. Menstrual disruption with exercise is not linked to an energy availability threshold. Med Sci Sports Exerc 2018;50:551-61. · DOI · Paper page
  25. Williams NI, Leidy HJ, Hill BR, et al. Magnitude of daily energy deficit predicts frequency but not severity of Menstrual disturbances associated with exercise and caloric restriction. Am J Physiol Endocrinol Metab 2015;308:E29-39. · DOI
  26. Lundy B, Torstveit MK, Stenqvist TB, et al. Screening for low energy availability in male athletes: attempted validation of LEAM-Q. Nutrients 2022;14:1873. · DOI · Paper page
  27. Torstveit MK, Fahrenholtz I, Stenqvist TB, et al. Within-day energy deficiency and metabolic perturbation in male endurance athletes. Int J Sport Nutr Exerc Metab 2018;28:419-27. · DOI
  28. Elliott-Sale KJ, Minahan CL, de Jonge XAKJ, et al. Methodological considerations for studies in sport and exercise science with women as participants: A working guide for standards of practice for research on women. Sports Med 2021;51:843-61. · DOI · Paper page
  29. Loucks AB. No evidence of absence of an energy availability threshold for Menstrual disturbances. Med Sci Sports Exerc 2019;51:1790. · DOI
  30. Areta JL, Taylor HL, Koehler K. Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males. Eur J Appl Physiol 2021;121:1-21. on April 3, 2024 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2023-107335 on 26 September 2023. Downloaded from Review 41 · DOI · Paper page
  31. Burke LM, Lundy B, Fahrenholtz IL, et al. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. Int J Sport Nutr Exerc Metab 2018;28:350-63. · DOI · Paper page
  32. Tenforde AS, Fredericson M, Sayres LC, et al. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med 2015;43:1494-504. · DOI
  33. Jurov I, Keay N, Rauter S. Reducing energy availability in male endurance athletes: a randomized trial with a three-step energy reduction. J Int Soc Sports Nutr 2022;19:179-95. · DOI
  34. Burke LM, Whitfield J, Ross MLR, et al. Short severe energy restriction with refueling reduces body mass without altering training-associated performance improvement. Med Sci Sports Exerc 2023;55:1487-98. · DOI
  35. Fensham NC, Heikura IA, McKay AKA, et al. Short-term carbohydrate restriction impairs bone formation at rest and during prolonged exercise to a greater degree than low energy availability. J Bone Miner Res 2022;37:1915-25. · DOI · Paper page
  36. McKay AKA, Peeling P, Pyne DB, et al. Six days of low carbohydrate, not energy availability, alters the iron and immune response to exercise in elite athletes. Med Sci Sports Exerc 2022;54:377-87. · DOI · Paper page
  37. Martin D, Papageorgiou M, Colgan H, et al. The effects of short-term low energy availability, achieved through diet or exercise, on cognitive function in oral contraceptive users and Eumenorrheic women. Appl Physiol Nutr Metab 2021;46:781-9. · DOI
  38. Papageorgiou M, Elliott-Sale KJ, Parsons A, et al. Effects of reduced energy availability on bone metabolism in women and men. Bone 2017;105:191-9. · DOI · Paper page
  39. Papageorgiou M, Martin D, Colgan H, et al. Bone metabolic responses to low energy availability achieved by diet or exercise in active Eumenorrheic women. Bone 2018;114:181-8. · DOI
  40. Jurov I, Keay N, Spudić D, et al. Inducing low energy availability in trained endurance male athletes results in poorer explosive power. Eur J Appl Physiol 2022;122:503-13. · DOI · Paper page
  41. Kojima C, Ishibashi A, Ebi K, et al. Exogenous glucose oxidation during endurance exercise under low energy availability. PLoS One 2022;17:e0276002. · DOI
  42. Ishibashi A, Kojima C, Tanabe Y, et al. Effect of low energy availability during three consecutive days of endurance training on iron metabolism in male long distance runners. Physiol Rep 2020;8:e14494. · DOI
  43. Woods AL, Garvican-Lewis LA, Lundy B, et al. New approaches to determine fatigue in elite athletes during intensified training: resting metabolic rate and pacing profile. PLoS One 2017;12:e0173807. · DOI
  44. Kettunen O, Ihalainen JK, Ohtonen O, et al. Energy availability during training camp is associated with signs of Overreaching and changes in performance in young female cross-country skiers. Biomed Hum Kinet 2021;13:246-54. · DOI
  45. Heydenreich J, Kayser B, Schutz Y, et al. Total energy expenditure, energy intake, and body composition in endurance athletes across the training season: A systematic review. Sports Med -Open 2017;3. · DOI · Paper page
  46. Burke LM, Slater GJ, Matthews JJ, et al. ACSM expert consensus statement on weight loss in weight-category sports. Curr Sports Med Rep 2021;20:199-217. · DOI
  47. Longman DP, Dolan E, Wells JCK, et al. Patterns of energy allocation during energetic scarcity; evolutionary insights from ultra-endurance events. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 2023;281:111422. · DOI
  48. Lombardi G, Lanteri P, Graziani R, et al. Bone and energy metabolism parameters in professional cyclists during the Giro D'Italia 3-weeks stage race. PLoS ONE 2012;7:e42077. · DOI
  49. Heikura IA, Quod M, Strobel N, et al. n.d. Alternate-day low energy availability during spring classics in professional cyclists. Int J Sports Physiol Perform;14:1233-43. · DOI
  50. Koltun KJ, De Souza MJ, Scheid JL, et al. Energy availability is associated with luteinizing hormone pulse frequency and induction of Luteal phase defects. The Journal of Clinical Endocrinology & Metabolism 2020;105:185-93. · DOI
  51. Loucks AB, Heath EM, Law T. Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young Menstruating women. J Clin Endocrinol Metab 1994;78:910-5. · DOI · Paper page
  52. Mujika I, Halson S, Burke LM, et al. An integrated, Multifactorial approach to Periodization for optimal performance in individual and team sports. Int J Sports Physiol Perform 2018;13:538-61. · DOI · Paper page
  53. Stellingwerff T, Maughan RJ, Burke LM. Nutrition for power sports: middle-distance running, track Cycling, rowing, canoeing/Kayaking, and swimming. Journal of Sports Sciences 2011;29:S79-89. · DOI
  54. Deutz RC, Benardot D, Martin DE, et al. Relationship between energy deficits and body composition in elite female gymnasts and runners. Medicine & Science in Sports & Exercise 2000;32:659-68. · DOI
  55. Lundstrom EA, De Souza MJ, Canil HN, et al. Sex differences and indications of metabolic compensation in within-day energy balance in elite division 1 swimmers. Appl Physiol Nutr Metab 2023;48:74-87. · DOI
  56. Fahrenholtz IL, Sjödin A, Benardot D, et al. Within-day energy deficiency and reproductive function in female endurance athletes. Scand J Med Sci Sports 2018;28:1139-46. 10.1111/sms.13030 Available: http://doi.wiley.com/10.1111/ sms.2018.28.issue-3 72 · DOI
  57. Wells KR, Jeacocke NA, Appaneal R, et al. The Australian Institute of sport (AIS) and national eating disorders collaboration (NEDC) position statement on disordered eating in high performance sport [British journal of sports medicine 2020:bjsports- 2019-1]. Br J Sports Med 2020;54:1247-58. · DOI · Paper page
  58. Burke L, Fahrenholtz I, Garthe I, et al. Low energy availability: challenges and approaches to measurement and treatment. In: Burke L, Deakin V, Minehan M, eds. Clinical Sports Nutrition. 6th ed. Sydney: McGraw-Hill 2021:110-43, 74
  59. Melin AK, Areta JL, Heikura IA, et al. Direct and indirect impact of low energy availability on sports performance. Scandinavian Med Sci Sports 2023. · DOI
  60. Sabaratnam R, Wojtaszewski JFP, Højlund K. Factors mediating Exercise-Induced organ Crosstalk. Acta Physiol (Oxf) 2022;234:e13766. · DOI
  61. Petkus DL, Murray-Kolb LE, Scott SP, et al. Iron status at opposite ends of the Menstrual function spectrum. J Trace Elem Med Biol 2019;51:169-75. · DOI
  62. Dolan E, McGoldrick A, Davenport C, et al. An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing Jockeys. J Bone Miner Metab 2012;30:534-42. · DOI
  63. Heikura IA, Uusitalo ALT, Stellingwerff T, et al. Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. Int J Sport Nutr Exerc Metab 2018;28:403-11. · DOI · Paper page
  64. De Souza MJ, West SL, Jamal SA, et al. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 2008;43:140-8. · DOI
  65. Gibbs JC, Nattiv A, Barrack MT, et al. Low bone density risk is higher in exercising women with multiple Triad risk factors. Med Sci Sports Exerc 2014;46:167-76. · DOI
  66. Mitchell DM, Tuck P, Ackerman KE, et al. Altered trabecular bone morphology in adolescent and young adult athletes with Menstrual dysfunction. Bone 2015;81:24-30. · DOI
  67. Barrack MT, Rauh MJ, Nichols JF. Prevalence of and traits associated with low BMD among female adolescent runners. Med Sci Sports Exerc 2008;40:2015-21. · DOI
  68. Ackerman KE, Cano Sokoloff N, DE Nardo Maffazioli G, et al. Fractures in relation to Menstrual status and bone parameters in young athletes. Med Sci Sports Exerc 2015;47:1577-86. · DOI
  69. De Souza MJ, Arce JC, Pescatello LS, et al. Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training. Int J Sports Med 1994;15:383-91. · DOI
  70. Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J Clin Endocrinol Metab 1993;77:770-5. · DOI
  71. Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance- trained and untrained males. Med Sci Sports Exerc 1988;20:60-5. · DOI · Paper page
  72. Hackney AC, Dolny DG, Ness RJ. Comparison of resting reproductive hormonal profiles in select athletic groups. Biol Sport 1988;4:200-8.
  73. Dale E, Gerlach DH, Wilhite AL. Menstrual dysfunction in distance runners. Obstet Gynecol 1979;54:47-53. · DOI
  74. Hetland ML, Haarbo J, Christiansen C, et al. Running induces Menstrual disturbances but bone mass is unaffected, except in Amenorrheic women. Am J Med 1993;95:53-60. · DOI
  75. Shirley MK, Longman DP, Elliott-Sale KJ, et al. A life history perspective on athletes with low energy availability. Sports Med 2022;52:1223-34. · DOI · Paper page
  76. Oliveira-Junior G, Pinto RS, Shirley MK, et al. The Skeletal muscle response to energy deficiency: A life history perspective. Adaptive Human Behavior and Physiology 2022;8:114-29. · DOI
  77. Dolan E, Koehler K, Areta J, et al. Energy constraint and compensation: insights from endurance athletes. COMP Biochem Physiol A Mol Integr Physiol. 2023;285:111500.
  78. Dobzhansky T. Nothing in biology makes sense except in the light of evolution. The American Biology Teacher 1973;35:125-9. · DOI · Paper page
  79. Areta JL. Physical performance during energy deficiency in humans: an evolutionary perspective. Comp Biochem Physiol A Mol Integr Physiol 2023;284:111473. · DOI
  80. Thurber C, Dugas LR, Ocobock C, et al. Extreme events reveal an Alimentary limit on sustained maximal human energy expenditure. Sci Adv 2019;5:eaaw0341. · DOI · Paper page
  81. Pontzer H, Durazo-Arvizu R, Dugas LR, et al. Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr Biol 2016;26:410-7. 100 · DOI · Paper page
  82. Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev 2015;43:110-6. 101 · DOI
  83. Gonzalez JT, Batterham AM, Atkinson G, et al. Perspective: is the response of human energy expenditure to increased physical activity additive or constrained? Adv Nutr 2023;14:406-19. 102 · DOI
  84. Fothergill E, Guo J, Howard L, et al. "Persistent metabolic adaptation 6 years after "the biggest loser" competition". Obesity (Silver Spring) 2016;24:1612-9. 103 · DOI · Paper page
  85. Hall KD. "Energy compensation and metabolic adaptation: "the biggest loser" study reinterpreted". Obesity 2022;30:11-3. 104 · DOI
  86. Aronne LJ, Hall KD, M. Jakicic J, et al. Describing the weight-reduced state: physiology, behavior, and interventions. Obesity 2021;29:S9-24. 10.1002/ oby.23086 Available: https://onlinelibrary.wiley.com/toc/1930739x/29/S1 106 · DOI · Paper page
  87. Ravussin E, Smith SR, Ferrante AW Jr. Physiology of energy expenditure in the weight-reduced state. Obesity 2021;29:S31-8. 10.1002/oby.23095 Available: https://onlinelibrary.wiley.com/toc/1930739x/29/S1 107 · DOI
  88. Loucks AB. Commentary 2. female athlete Triad and energy availability. In: Burke L, Deakin V, eds. Clinical Sports Nutrition. 5th ed. Sydney: McGraw Hill 2015:140-45, 110
  89. Sipilä S, Törmäkangas T, Sillanpää E, et al. Muscle and bone mass in middle-aged women: role of menopausal status and physical activity. J Cachexia Sarcopenia Muscle 2020;11:698-709. 111 · DOI
  90. Hadjidakis D, Kokkinakis E, Sfakianakis M, et al. The type and time of Menopause as decisive factors for bone mass changes. Eur J Clin Invest 1999;29:877-85. 112 · DOI
  91. Phillips BE, Williams JP, Greenhaff PL, et al. Physiological adaptations to resistance exercise as a function of age. JCI Insight 2017;2:e95581. 113 · DOI
  92. Fontana L, Garzia E, Marfia G, et al. Epigenetics of functional hypothalamic Amenorrhea. Front Endocrinol (Lausanne) 2022;13:953431. 114 · DOI
  93. Curtis EM, Fuggle NR, Cooper C, et al. Epigenetic regulation of bone mass. Best Pract Res Clin Endocrinol Metab 2022;36:101612. 115 · DOI
  94. Ralston SH, Uitterlinden AG. Genetics of osteoporosis. Endocr Rev 2010;31:629-62. 116 · DOI
  95. Bilen O, Pokharel Y, Ballantyne CM. Genetic testing in hyperlipidemia. Cardiol Clin 2015;33:267-75. 117 · DOI
  96. Korpelainen R, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001;29:304-10. 118 · DOI
  97. Lungaro L, Manza F, Costanzini A, et al. Osteoporosis and celiac disease: updates and hidden pitfalls. Nutrients 2023;15:1089. 119 · DOI
  98. Rothman MS, Arciniegas DB, Filley CM, et al. The Neuroendocrine effects of traumatic brain injury. J Neuropsychiatry Clin Neurosci 2007;19:363-72. 122 · DOI
  99. Jonvik KL, Vardardottir B, Broad E. How do we assess energy availability and RED-S risk factors in para athletes Nutrients 2022;14:1068. 123 · DOI · Paper page
  100. Klubo-Gwiezdzinska J, Wartofsky L. Hashimoto thyroiditis: an evidence-based guide to etiology, diagnosis and treatment. Pol Arch Intern Med 2022;132:16222. 124 · DOI
  101. Tai FWD, McAlindon ME. Non-Steroidal anti-inflammatory drugs and the gastrointestinal tract. Clin Med (Lond) 2021;21:131-4. 125 · DOI
  102. Van Staa TP, Leufkens HG, Abenhaim L, et al. Use of oral corticosteroids and risk of fractures. J Bone Miner Res 2000;15:993-1000. 126 · DOI · Paper page
  103. Kelsey JL, Bachrach LK, Procter-Gray E, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sports Exerc 2007;39:1457-63. 127 · DOI
  104. Tenforde AS, Sayres LC, McCurdy ML, et al. Identifying sex-specific risk factors for stress fractures in adolescent runners. Med Sci Sports Exerc 2013;45:1843-51. 128 · DOI
  105. Herzog W, Minne H, Deter C, et al. Outcome of bone mineral density in anorexia Nervosa patients 11.7 years after first admission. J Bone Miner Res 1993;8:597-605. 129 · DOI
  106. Hartman D, Crisp A, Rooney B, et al. Bone density of women who have recovered from anorexia Nervosa. Int J Eat Disord 2000;28:107-12. 130 · DOI
  107. Javed A, Kashyap R, Lteif AN. Hyperandrogenism in female athletes with functional hypothalamic Amenorrhea: a distinct phenotype. Int J Womens Health 2015;7:103-11. 131 · DOI
  108. Bellver M, Del Rio L, Jovell E, et al. Bone mineral density and bone mineral content among female elite athletes. Bone 2019;127:393-400. 132 · DOI
  109. Scofield KL, Hecht S. Bone health in endurance athletes: runners, cyclists, and swimmers. Curr Sports Med Rep 2012;11:328-34. 133 · DOI
  110. Sherk VD, Barry DW, Villalon KL, et al. Bone loss over 1 year of training and competition in female cyclists. Clin J Sport Med 2014;24:331-6. 134 · DOI
  111. Stojanović E, Radovanović D, Dalbo VJ, et al. Basketball players possess a higher bone mineral density than matched non-athletes, swimming, soccer, and volleyball athletes: a systematic review and meta-analysis. Arch Osteoporos 2020;15:123. 135 · DOI
  112. Miller BJ, Pate RR, Burgess W. Foot impact force and Intravascular hemolysis during distance running. Int J Sports Med 1988;9:56-60. 136 · DOI
  113. Telford RD, Sly GJ, Hahn AG, et al. Footstrike is the major cause of hemolysis during running. Journal of Applied Physiology 2003;94:38-42. 137 · DOI
  114. Warden SJ, Edwards WB, Willy RW. Preventing bone stress injuries in runners with optimal workload. Curr Osteoporos Rep 2021;19:298-307. 138 · DOI
  115. Tenforde AS, DeLuca S, Wu AC, et al. Prevalence and factors associated with bone stress injury in middle school runners. PM R 2022;14:1056-67. 139 · DOI
  116. Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes. A study of 320 cases. Am J Sports Med 1987;15:46-58. 140 · DOI
  117. Murphy C, Koehler K. Energy deficiency impairs resistance training gains in lean mass but not strength: A meta-analysis and meta-regression. Scand J Med Sci Sports 2022;32:125-37. 10.1111/sms.14075 Available: https://onlinelibrary.wiley.com/toc/ 16000838/32/1 142 · DOI
  118. Heikura IA, Burke LM, Hawley JA, et al. A short-term Ketogenic diet impairs markers of bone health in response to exercise. Front Endocrinol (Lausanne) 2019;10:880. 143 · DOI · Paper page
  119. Spaulding SW, Chopra IJ, Sherwin RS, et al. Effect of caloric restriction and dietary composition of serum T3 and reverse T3 in man. J Clin Endocrinol Metab 1976;42:197-200. 144 · DOI
  120. Lane AR, Duke JW, Hackney AC. Influence of dietary carbohydrate intake on the free testosterone: Cortisol ratio responses to short-term intensive exercise training. Eur J Appl Physiol 2010;108:1125-31. 145 · DOI
  121. Shimasaki Y, Nagao M, Miyamori T, et al. Evaluating the risk of a fifth Metatarsal stress fracture by measuring the serum 25-Hydroxyvitamin D levels. Foot Ankle Int 2016;37:307-11. 146 · DOI
  122. Millward D, Root AD, Dubois J, et al. Association of serum vitamin D levels and stress fractures in collegiate athletes. Orthopaedic Journal of Sports Medicine 2020;8:232596712096696. 147 · DOI
  123. Ruohola J-P, Laaksi I, Ylikomi T, et al. Association between serum 25(OH)D concentrations and bone stress fractures in Finnish young men. J Bone Miner Res 2006;21:1483-8. 148 · DOI
  124. Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM R 2010;2:740-50; 149 · DOI
  125. Burgi AA, Gorham ED, Garland CF, et al. High serum 25-Hydroxyvitamin D is associated with a low incidence of stress fractures. J Bone Miner Res 2011;26:2371-7. 150 · DOI
  126. Snyder AC, Dvorak LL, Roepke JB. Influence of dietary iron source on measures of iron status among female runners. Medicine & Science in Sports & Exercise 1989;21:7-10. 151 · DOI
  127. Gibson-Smith E, Storey R, Ranchordas M. Dietary intake, body composition and iron status in experienced and elite climbers. Front Nutr 2020;7:122. 152 · DOI
  128. Barrack MT, Fredericson M, Tenforde AS, et al. Evidence of a cumulative effect for risk factors predicting low bone mass among male adolescent athletes. Br J Sports Med 2017;51:200-5. 153 · DOI
  129. Lundy B, McKay AKA, Fensham NC, et al. The impact of acute calcium intake on bone turnover markers during a training day in elite male rowers. Med Sci Sports Exerc 2023;55:55-65. 155 · DOI
  130. Berga SL, Marcus MD, Loucks TL, et al. Recovery of ovarian activity in women with functional hypothalamic Amenorrhea who were treated with cognitive behavior therapy. Fertil Steril 2003;80:976-81. 158 · DOI
  131. Fioroni L, Fava M, Genazzani AD, et al. Life events impact in patients with secondary Amenorrhoea. J Psychosom Res 1994;38:617-22. 159 · DOI
  132. Woods AL, Sharma AP, Garvican-Lewis LA, et al. Four weeks of classical altitude training increases resting metabolic rate in highly trained middle-distance runners. Int J Sport Nutr Exerc Metab 2017;27:83-90. 160 · DOI
  133. McLean BD, Buttifant D, Gore CJ, et al. Year-to-year variability in Haemoglobin mass response to two altitude training camps. Br J Sports Med 2013;47 Suppl 1(Suppl 1):i51-8. 161 · DOI
  134. Govus AD, Garvican-Lewis LA, Abbiss CR, et al. Pre-altitude serum Ferritin levels and daily oral iron supplement dose mediate iron parameter and hemoglobin mass responses to altitude exposure. PLoS One 2015;10:e0135120. 162 · DOI · Paper page
  135. Okazaki K, Stray-Gundersen J, Chapman RF, et al. Iron insufficiency diminishes the erythropoietic response to moderate altitude exposure. J Appl Physiol (1985) 2019;127:1569-78. on April 3, 2024 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2023-107335 on 26 September 2023. Downloaded from · DOI

Cited by

Sorted by citations

Authors
Burke, L. M., Ackerman, K. E., Heikura, I. A., Hackney, A. C., & Stellingwerff, T.
Affiliations
  • Australian Catholic University (AU)
  • Boston Children's Hospital (US)
  • University of Victoria (CA)
  • University of North Carolina at Chapel Hill (US)
Corresponding author
Burke, Louise M
Venue
British Journal of Sports Medicine
Publisher
BMJ
Published
2023-09
Volume
57
Issue
17
Pages
1098-1110
ISSN
  • 0306-3674 (ISSN-L)
  • 1473-0480
OpenAlex
W4387036475
Cited by
59
References
21
Citations by year
2026: 23 · 2025: 18 · 2024: 14 · 2023: 4
FWCI
2.99
Type
journal article
Language
en
Open access
Locations
  • British Journal of Sports Medicine (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • HighWire Press Open Archive (submittedVersion)
Topics
  • Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords
relative energy deficiency in sport, low energy availability, systems biology, athlete health, athletic performance, moderators, interindividual variability
MeSH terms
Relative Energy Deficiency in Sport, Consensus Statements as Topic, Humans, Sports, Athletes

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