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IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update

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Mountjoy, Margo, Sundgot-Borgen, Jorunn Kaiander, Burke, Louise M, Ackerman, Kathryn E, Blauwet, Cheri, Constantini, Naama, Lebrun, Constance, Lundy, Bronwen +6 more·2018·British Journal of Sports Medicine

Abstract

In 2014, the IOC published a consensus statement entitled ‘Beyond the Female Athlete Triad: Relative Energy Deficiency in Sport (RED-S)’. The syndrome of RED-S refers to ‘impaired physiological functioning caused by relative energy deficiency and includes, but is not limited to, impairments of metabolic rate, menstrual function, bone health, immunity, protein synthesis and cardiovascular health’. The aetiological factor of this syndrome is low energy availability (LEA).1 The publication of the RED-S consensus statement stimulated activity in the field of Female Athlete Triad science, including some initial controversy2 3 followed by numerous scientific publications addressing: 1. The health parameters identified in the RED-S conceptual model (figure 1).1 4 2. Relative energy deficiency in male athletes. 3. The measurement of LEA. 4. The performance parameters identified in the RED-S conceptual model (figure 2).1 4 The IOC RED-S consensus authors have reconvened to provide an update summary of the interim scientific progress in the field of relative energy deficiency with the ultimate goal of stimulating advances in RED-S awareness, clinical application and scientific research to address current gaps in knowledge. Figure 1 Health consequences of Relative Energy Deficiency in Sport (RED-S) showing an expanded concept of the Female Athlete Triad to acknowledge a wider range of outcomes and the application to male athletes (*Psychological consequences can either precede RED-S or be the result of RED-S).1 4 Figure 2 Potential Performance consequences of Relative Energy Deficiency in Sport (*Aerobic and anerobic performance).1 4 ### Low energy availability LEA, which underpins the concept of RED-S, is a mismatch between an athlete’s energy intake (diet) and the energy expended in exercise, leaving inadequate energy to support the functions required by the body to maintain optimal health and performance. Operationally, energy availability (EA) is defined as: ![Formula][1] where exercise energy expenditure (EEE) is calculated as the additional energy expended above that of … [1]: /embed/mml-math-1.gif

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  • REDs is a syndrome of impaired physiological and/or psychological functioning experienced by female and male athletes that is caused by exposure to problematic (prolonged and/or severe) low energy availability.

    “a syndrome of impaired physiological and/or psychological functioning experienced by female and male athletes that is caused by exposure to problematic (prolonged and/or severe) low energy availability.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [6]

    The Introduction defines RED-S as impaired physiological functioning caused by relative energy deficiency and identifies low energy availability as its cause. The Conclusions figure caption extends the concept to male athletes and says psychological consequences can be a result of RED-S. The copy does not define the causative exposure as specifically ‘problematic (prolonged and/or severe)’ low energy availability; the male-athlete section says the threshold and duration required to induce RED-S in men are unknown. Page numbers are unavailable in the indexed passages. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • There have been numerous scientific advances in the field of REDs since the publication of the 2018 IOC consensus update statement.

    “As evidenced by this consensus statement, there have been numerous scientific advances in the field of REDs since the publication of the 2018 IOC consensus update statement 6”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [6]

    The Introduction and Conclusions report numerous scientific advances since the original 2014 IOC consensus statement. The cited 2018 update does not establish that advances occurred after its own publication, which is the timeframe the citing sentence attributes to it. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Low energy availability is more common in female athletes compared to male athletes.

    “LEA is more common in female athletes compared to male athletes [8].”

    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 [8]

    The section ‘Low energy availability in male athletes’ says that LEA prevalence ‘has been suggested to be higher in females than in males,’ but adds that ‘precise differences are unknown.’ The citing sentence presents that suggested difference as an established fact. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • Although the 2014 and 2018 consensus statements alluded to the impact of LEA and REDs in male athletes, the available research on males at the time was scant.

    “Although the 2014 IOC REDs consensus statement 5 and the 2018 update paper 6 alluded to the impact of LEA and REDs in male athletes, the available research on males at the time was scant.”
  • There has been increased awareness of the risk factors for and consequences of REDs, where psychological factors contributing to LEA and mental health consequences have been highlighted, although less well understood.

    “A parallel focus has been the increased awareness of the risk factors for and the consequences of REDs, where psychological factors contributing to LEA and mental health consequences have been highlighted, 5 although less well understood.6 35 66”

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  1. De Souza MJ, Williams NI, Nattiv A, et al. Misunderstanding the female athlete triad: refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2014;48:1461-5. · DOI
  2. Mountjoy M, Sundgot-Borgen J, Burke L, et al. Authors' 2015 additions to the IOC consensus statement: Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2015;49:417-20. · DOI
  3. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci 2011;29:S7-15. · DOI · Paper page
  4. Melin A, Lundy B. Measuring energy availability. In: Burke L, Deakin V, eds. Clinical Sports Nutrition. Sydney: McGraw-Hilll, 2015:146-57.
  5. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol Regul Integr Comp Physiol 1994;266:R817-R823. · DOI
  6. 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
  7. Burke LM, Deakin V. Clinical sports nutrition. 5th edn: McGraw-Hilll Education Australia, 2015.
  8. 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
  9. 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-E39. on July 25, 2023 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from Consensus statement · DOI
  10. Melin A, Tornberg AB, Skouby S, et al. The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. Br J Sports Med 2014;48:540-5. · DOI · Paper page
  11. Burke LM, Melin A, Lundy B. Pitfalls and problems with measuring energy availability. Int J Sport Nutr Exerc Metab 2018. In press.
  12. Cialdella-Kam L, Guebels CP, Maddalozzo GF, et al. Dietary intervention restored menses in female athletes with exercise-associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients 2014;6:3018-39. · DOI
  13. Aparicio-Ugarriza R, Mielgo-Ayuso J, Benito PJ, et al. Physical activity assessment in the general population; instrumental methods and new technologies. Nutr Hosp 2015;31(Suppl 3):219-26. · DOI
  14. Pinheiro Volp AC, Esteves de Oliveira FC, Duarte Moreira Alves R, et al. Energy expenditure: components and evaluation methods. Nutr Hosp 2011;26:430-40. · DOI
  15. Barron E, Cano Sokoloff N, Maffazioli GDN, et al. Diets high in fiber and vegetable protein are associated with low lumbar bone mineral density in young athletes with oligoamenorrhea. J Acad Nutr Diet 2016;116:481-9. · DOI
  16. Gaskins AJ, Mumford SL, Zhang C, et al. Effect of daily fiber intake on reproductive function: the BioCycle Study. Am J Clin Nutr 2009;90:1061-9. · DOI
  17. 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 2017:1-30. · DOI · Paper page
  18. Melin A, Tornberg ÅB, Skouby S, et al. Low-energy density and high fiber intake are dietary concerns in female endurance athletes. Scand J Med Sci Sports 2016;26:1060-71. · DOI · Paper page
  19. Reed JL, De Souza MJ, Kindler JM, et al. Nutritional practices associated with low energy availability in Division I female soccer players. J Sports Sci 2014;32:1499-509. · DOI
  20. 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. · DOI
  21. Berkovich BE, Eliakim A, Nemet D, et al. Rapid weight loss among adolescents participating in competitive judo. Int J Sport Nutr Exerc Metab 2016;26:276-84. · DOI
  22. Burke LM, Tenforde AS, Morton JP, et al. Relative energy deficiency in sport (RED-S) in male athletes. Int J Sport Nutr Exerc Metab 2018. In press.
  23. Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: a review. Int J Sport Nutr Exerc Metab 2017:1-31. · DOI
  24. Tenforde AS, Barrack MT, Nattiv A, et al. Parallels with the Female Athlete Triad in male athletes. Sports Med 2016;46:171-82. · DOI
  25. Viner RT, Harris M, Berning JR, et al. Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. Int J Sport Nutr Exerc Metab 2015;25:594-602. · DOI · Paper page
  26. Wilson G, Hawken MB, Poole I, et al. Rapid weight-loss impairs simulated riding performance and strength in jockeys: implications for making-weight. J Sports Sci 2014;32:383-91. · DOI
  27. Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med 2007;37:348-52. · DOI
  28. Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise: development of the "exercise-hypogonadal male condition". Acta Physiol Hung 2005;92:121-37. · DOI
  29. Hooper DR, Kraemer WJ, Saenz C, et al. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J Appl Physiol 2017;117:1349-57. · DOI · Paper page
  30. Blauwet CA, Brook EM, Tenforde AS, et al. Low energy availability, menstrual dysfunction, and low bone mineral density in individuals with a disability: implications for the para athlete population. Sports Med 2017;47:1697-708. · DOI
  31. Buchholz AC, Pencharz PB. Energy expenditure in chronic spinal cord injury. Curr Opin Clin Nutr Metab Care 2004;7:635-9. · DOI · Paper page
  32. Price M. Energy expenditure and metabolism during exercise in persons with a spinal cord injury. Sports Med 2010;40:681-96. · DOI
  33. Krempien JL, Barr SI. Risk of nutrient inadequacies in elite Canadian athletes with spinal cord injury. Int J Sport Nutr Exerc Metab 2011;21:417-25. · DOI
  34. Krempien JL, Barr SI. Eating attitudes and behaviours in elite Canadian athletes with a spinal cord injury. Eat Behav 2012;13:36-41. · DOI
  35. Colantonio A, Mar W, Escobar M, et al. Women's health outcomes after traumatic brain injury. J Womens Health 2010;19:1109-16. · DOI · Paper page
  36. Ranganathan P, Kumar RG, Davis K, et al. Longitudinal sex and stress hormone profiles among reproductive age and post-menopausal women after severe TBI: a case series analysis. Brain Inj 2016;30:452-61. · DOI · Paper page
  37. Ripley DL, Harrison-Felix C, Sendroy-Terrill M, et al. The impact of female reproductive function on outcomes after traumatic brain injury. Arch Phys Med Rehabil 2008;89:1090-6. · DOI · Paper page
  38. Gonzalez EG, Corcoran PJ, Reyes RL. Energy expenditure in below-knee amputees: correlation with stump length. Arch Phys Med Rehabil 1974;55:111-9.
  39. Goktepe AS, Yilmaz B, Alaca R, et al. Bone density loss after spinal cord injury: elite paraplegic basketball players vs. paraplegic sedentary persons. Am J Phys Med Rehabil 2004;83:279-83.
  40. Pernick Y, Nichols JF, Rauh MJ, et al. Disordered eating among a multi-racial/ethnic sample of female high-school athletes. J Adolesc Health 2006;38:689-95. · DOI
  41. Rhea DJ. Eating disorder behaviors of ethnically diverse urban female adolescent athletes and non-athletes. J Adolesc 1999;22:379-88. · DOI
  42. Lappe JM, Stegman MR, Recker RR. The impact of lifestyle factors on stress fractures in female Army recruits. Osteoporos Int 2001;12:35-42. · DOI
  43. Tam N, Santos-Concejero J, Tucker R, et al. Bone health in elite Kenyan runners. J Sports Sci 2018;36:456-61. · DOI
  44. Mukeshi M, Thairu K. Nutrition and body build: a Kenyan review. World Rev Nutr Diet 1993;72:218-26.
  45. Beis LY, Willkomm L, Ross R, et al. Food and macronutrient intake of elite Ethiopian distance runners. J Int Soc Sports Nutr 2011;8:7-19. · DOI · Paper page
  46. Muia EN, Wright HH, Onywera VO, et al. Adolescent elite Kenyan runners are at risk for energy deficiency, menstrual dysfunction and disordered eating. J Sports Sci 2016;34:598-606. · DOI
  47. Manore MM, Patton-Lopez MM, Meng Y, et al. Sport nutrition knowledge, behaviors and beliefs of high school soccer players. Nutrients 2017;9:350. · DOI
  48. Iwamoto J, Sato Y, Takeda T, et al. Analysis of stress fractures in athletes based on our clinical experience. World J Orthop 2011;2:7-12. · DOI
  49. Quah YV, Poh BK, Ng LO, et al. The female athlete triad among elite Malaysian athletes: prevalence and associated factors. Asia Pac J Clin Nutr 2009;18:200-8.
  50. Allaway HCM, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Horm Mol Biol Clin Investig 2016;25:91-119. · DOI · Paper page
  51. 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
  52. 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
  53. Misra M. Neuroendocrine mechanisms in athletes. Handb Clin Neurol 2014;124:373-86. · DOI
  54. Jasienska G. Energy metabolism and the evolution of reproductive suppression in the human female. Acta Biotheor 2003;51:1-18. · DOI
  55. Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 2004;287:R1277-96. · DOI
  56. 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
  57. McColl EM, Wheeler GD, Gomes P, et al. The effects of acute exercise on pulsatile LH release in high-mileage male runners. Clin Endocrinol 1989;31:617-22. · DOI · Paper page
  58. 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
  59. Papageorgiou M, Dolan E, Elliott-Sale KJ, et al. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr 2018;57:1. · DOI
  60. 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
  61. Gordon CM, Ackerman KE, Berga SL, et al. Functional hypothalamic amenorrhea: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 2017;102:1413-39. · DOI
  62. Curry EJ, Logan C, Ackerman K, et al. Female athlete triad awareness among multispecialty physicians. Sports Med Open 2015;1:38. · DOI · Paper page
  63. Ackerman KE, Nazem T, Chapko D, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 2011;96:3123-33. · DOI
  64. Ackerman KE, Putman M, Guereca G, et al. Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non- athletes. Bone 2012;51:680-7. · DOI
  65. 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
  66. Andreoli A, Monteleone M, Van Loan M, et al. Effects of different sports on bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc 2001;33:507-11. · 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. on July 25, 2023 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from · DOI
  68. Fredericson M, Chew K, Ngo J, et al. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med 2007;41:664-8. · DOI
  69. Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone 2006;39:880-5. · DOI
  70. Morel J, Combe B, Francisco J, et al. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int 2001;12:152-7. · DOI
  71. Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res 2011;25:727-34. · DOI
  72. Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc 2000;32:1373-7. · DOI
  73. 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
  74. Wilson G, Hill J, Sale C, et al. Elite male Flat jockeys display lower bone density and lower resting metabolic rate than their female counterparts: implications for athlete welfare. Appl Physiol Nutr Metab 2015;40:1318-20. · DOI
  75. Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long distance runners. Med Sci Sports Exerc 1989;21:66-70. · DOI
  76. De Souza MJ, Nattiv A, Joy E, et al. Expert Panel. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med 2014;48:289. · DOI · Paper page
  77. Thralls KJ, Nichols JF, Barrack MT, et al. Body mass-related predictors of the female athlete triad among adolescent athletes. Int J Sport Nutr Exerc Metab 2016;26:17-25. · DOI
  78. 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
  79. Barrack MT, Gibbs JC, De Souza MJ, et al. Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med 2014;42:949-58. · DOI · Paper page
  80. Tenforde AS, Carlson JL, Chang A, et al. Association of the female athlete triad risk assessment stratification to the development of bone stress injuries in collegiate athletes. Am J Sports Med 2017;45:302-10. · DOI
  81. Melin A, Tornberg ÅB, Skouby S, et al. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports 2015;25:610-22. · DOI
  82. 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:e0173807-17. · DOI
  83. Koehler K, De Souza MJ, Williams NI. Less-than-expected weight loss in normal- weight women undergoing caloric restriction and exercise is accompanied by preservation of fat-free mass and metabolic adaptations. Eur J Clin Nutr 2017;71:365-71. · DOI
  84. Petkus DL, Murray-Kolb LE, De Souza MJ. The unexplored crossroads of the female athlete triad and iron deficiency: a narrative review. Sports Med 2017;47:1721-37. · DOI · Paper page
  85. Ackerman KE, Holtzman B, Cooper KM, et al. Low energy availability surrogates correlate with health and performance consequences of relative energy deficiency in sport (RED-S). Br J Sports Med 2018. In press.
  86. Lantzouni E, Frank GR, Golden NH, et al. Reversibility of growth stunting in early onset anorexia nervosa: a prospective study. J Adolesc Health 2002;31:162-5. · DOI
  87. Modan-Moses D, Yaroslavsky A, Kochavi B, et al. Linear growth and final height characteristics in adolescent females with anorexia nervosa. PLoS One 2012;7:e45504-8. · DOI
  88. Modan-Moses D, Yaroslavsky A, Novikov I, et al. Stunting of growth as a major feature of anorexia nervosa in male adolescents. Pediatrics 2003;111:270-6. · DOI
  89. Fazeli PK, Klibanski A. Determinants of GH resistance in malnutrition. J Endocrinol 2014;220:R57-R65. · DOI
  90. Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 1996;81:4301-9. 100 · DOI
  91. Waters DL, Qualls CR, Dorin R, et al. Increased pulsatility, process irregularity, and nocturnal trough concentrations of growth hormone in amenorrheic compared to eumenorrheic athletes. J Clin Endocrinol Metab 2001;86:1013-9. 101 · DOI
  92. O'Donnell E, Goodman JM, Harvey PJ. Clinical review: cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women. J Clin Endocrinol Metab 2011;96:3638-48. 102 · DOI
  93. Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, et al. Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. J Clin Endocrinol Metab 2005;90:1354-9. 103 · DOI
  94. Hoch AZ, Jurva JW, Staton MA, et al. Athletic amenorrhea and endothelial dysfunction. WMJ 2007;106:301-6. 104
  95. O'Donnell E, Goodman JM, Mak S, et al. Discordant orthostatic reflex renin- angiotensin and sympathoneural responses in premenopausal exercising- hypoestrogenic women. Hypertension 2015;65:1089-95. 105 · DOI
  96. Spaulding-Barclay MA, Stern J, Mehler PS. Cardiac changes in anorexia nervosa. Cardiol Young 2016;26:623-8. 106 · DOI
  97. Norris ML, Harrison ME, Isserlin L, et al. Gastrointestinal complications associated with anorexia nervosa: A systematic review. Int J Eat Disord 2016;49:216-37. 107 · DOI
  98. Shimizu K, Suzuki N, Nakamura M, et al. Mucosal immune function comparison between amenorrheic and eumenorrheic distance runners. J Strength Cond Res 2012;26:1402-6. 108 · DOI
  99. Drew M, Vlahovich N, Hughes D, et al. Prevalence of illness, poor mental health and sleep quality and low energy availability prior to the 2016 Summer Olympic Games. Br J Sports Med 2018;52:47-53. 109 · DOI
  100. Drew MK, Vlahovich N, Hughes D, et al. A multifactorial evaluation of illness risk factors in athletes preparing for the Summer Olympic Games. J Sci Med Sport 2017;20:745-50. 110 · DOI
  101. De Souza MJ, Hontscharuk R, Olmsted M, et al. Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite 2007;48:359-67. 111 · DOI
  102. Bomba M, Gambera A, Bonini L, et al. Endocrine profiles and neuropsychologic correlates of functional hypothalamic amenorrhea in adolescents. Fertil Steril 2007;87:876-85. 112 · DOI
  103. Marcus MD, Loucks TL, Berga SL. Psychological correlates of functional hypothalamic amenorrhea. Fertil Steril 2001;76:310-6. 113 · DOI
  104. Bomba M, Corbetta F, Bonini L, et al. Psychopathological traits of adolescents with functional hypothalamic amenorrhea: a comparison with anorexia nervosa. Eat Weight Disord 2014;19:41-8. 114 · DOI
  105. Petrie T, Galli N, Greenleaf C, et al. Psychosocial correlates of bulimic symptomatology among male athletes. Psychol Sport Exerc 2014;15:680-7. 115 · DOI
  106. Kong P, Harris LM. The sporting body: body image and eating disorder symptomatology among female athletes from leanness focused and nonleanness focused sports. J Psychol 2015;149:141-60. 116 · DOI
  107. Sundgot-Borgen J. Prevalence of eating disorders in elite female athletes. Int J Sport Nutr 1993;3:29-40. 117 · DOI
  108. Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med 2004;14:25-32. 118 · DOI
  109. Sykora C, Grilo CM, Wilfley DE, et al. Eating, weight, and dieting disturbances in male and female lightweight and heavyweight rowers. Int J Eat Disord 1993;14:203-11. 119 · DOI
  110. Thiemann P, Legenbauer T, Vocks S, et al. Eating disorders and their putative risk factors among female German professional athletes. Eur Eat Disord Rev 2015;23:269-76. 120 · DOI
  111. Martinsen M, Bratland-Sanda S, Eriksson AK, et al. Dieting to win or to be thin? A study of dieting and disordered eating among adolescent elite athletes and non- athlete controls. Br J Sports Med 2010;44:70-6. 121 · DOI
  112. Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:1188-97. 122 · DOI
  113. Vo M, Accurso EC, Goldschmidt AB, et al. The impact of DSM-5 on eating disorder diagnoses. Int J Eat Disord 2017;50:578-81. 125 · DOI
  114. Stice E, South K, Shaw H. Future directions in etiologic, prevention, and treatment research for eating disorders. J Clin Child Adolesc Psychol 2012;41:845-55. 126 · DOI
  115. Arthur-Cameselle J, Sossin K, Quatromoni P. A qualitative analysis of factors related to eating disorder onset in female collegiate athletes and non-athletes. Eat Disord 2017;25:199-215. 127 · DOI
  116. Krentz EM, Warschburger P. A longitudinal investigation of sports-related risk factors for disordered eating in aesthetic sports. Scand J Med Sci Sports 2013;23:303-10. 128 · DOI
  117. Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders in female elite athletes. Med Sci Sports Exerc 1994;26:414-9. 129 · DOI
  118. Shanmugam V, Jowett S, Meyer C. Interpersonal difficulties as a risk factor for athletes' eating psychopathology. Scand J Med Sci Sports 2014;24:469-76. 130 · DOI
  119. Stirling A, Kerr G. Perceived vulnerabilities of female athletes to the development of disordered eating behaviours. Eur J Sport Sci 2012;12:262-73. 131 · DOI
  120. Baskaran C, Plessow F, Ackerman KE, et al. A cross-sectional analysis of verbal memory and executive control across athletes with varying menstrual status and non-athletes. Psychiatry Res 2017;258:605-6. 132 · DOI
  121. Burden RJ, Morton K, Richards T, et al. Is iron treatment beneficial in, iron-deficient but non-anaemic (IDNA) endurance athletes? A systematic review and meta- analysis. Br J Sports Med 2015;49:1389-97. 133 · DOI · Paper page
  122. Geesmann B, Gibbs JC, Mester J, et al. Association between energy balance and metabolic hormone suppression during ultraendurance exercise. Int J Sports Physiol Perform 2017;12:984-9. 134 · DOI
  123. Hagmar M, Berglund B, Brismar K, et al. Body composition and endocrine profile of male Olympic athletes striving for leanness. Clin J Sport Med 2013;23:197-201. 135 · DOI
  124. Harber VJ, Petersen SR, Chilibeck PD. Thyroid hormone concentrations and muscle metabolism in amenorrheic and eumenorrheic athletes. Can J Appl Physiol 1998;23:293-306. 136 · DOI
  125. Rauh MJ, Nichols JF, Barrack MT. Relationships among injury and disordered eating, menstrual dysfunction, and low bone mineral density in high school athletes: a prospective study. J Athl Train 2010;45:243-52. on July 25, 2023 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from Consensus statement 137 · DOI
  126. Thein-Nissenbaum JM, Carr KE, Hetzel S, et al. Disordered eating, menstrual irregularity, and musculoskeletal injury in high school athletes: a comparison of oral contraceptive pill users and nonusers. Sports Health 2014;6:313-20. 138 · DOI
  127. El Ghoch M, Soave F, Calugi S, et al. Eating disorders, physical fitness and sport performance: a systematic review. Nutrients 2013;5:5140-60. 139 · DOI
  128. Fogelholm M. Effects of bodyweight reduction on sports performance. Sports Med 1994;18:249-67. 140 · DOI · Paper page
  129. Tarnopolsky MA, Zawada C, Richmond LB, et al. Gender differences in carbohydrate loading are related to energy intake. J Appl Physiol 2001;91:225-30. 141 · DOI · Paper page
  130. Silva MR, Paiva T. Poor precompetitive sleep habits, nutrients' deficiencies, inappropriate body composition and athletic performance in elite gymnasts. Eur J Sport Sci 2016;16:726-35. 143 · DOI · Paper page
  131. Tornberg ÅB, Melin A, Koivula FM, et al. Reduced neuromuscular performance in amenorrheic elite endurance athletes. Med Sci Sports Exerc 2017;49:2478-85. 144 · DOI
  132. Mooses M, Hackney AC. Anthropometrics and body composition in East African runners: potential impact on performance. Int J Sports Physiol Perform 2017;12:422-30. 145 · DOI
  133. Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc 2013;45:985-96. 146 · DOI
  134. Brown KN, Wengreen HJ, Beals KA. Knowledge of the female athlete triad, and prevalence of triad risk factors among female high school athletes and their coaches. J Pediatr Adolesc Gynecol 2014;27:278-82. 147 · DOI · Paper page
  135. Feldmann JM, Belsha JP, Eissa MA, et al. Female adolescent athletes' awareness of the connection between menstrual status and bone health. J Pediatr Adolesc Gynecol 2011;24:311-4. 148 · DOI
  136. Kroshus E, Sherman RT, Thompson RA, et al. Gender differences in high school coaches' knowledge, attitudes, and communication about the female athlete triad. Eat Disord 2014;22:193-208. 149 · DOI
  137. Mukherjee S, Chand V, Wong XX, et al. Perceptions, awareness and knowledge of the female athlete triad amongst coaches -are we meeting the expectations for athlete safety? Int J Sport Sci Coach 2016;11:545-51. 150
  138. Pantano KJ. Current knowledge, perceptions, and interventions used by collegiate coaches in the U.S. regarding the prevention and treatment of the female athlete triad. N Am J Sports Phys Ther 2006;1:195-207. 151
  139. Pantano KJ. Knowledge, attitude, and skill of high school coaches with regard to the female athlete triad. J Pediatr Adolesc Gynecol 2017;30:540-5. 152 · DOI · Paper page
  140. Troy K, Hoch AZ, Stavrakos JE. Awareness and comfort in treating the female athlete triad: are we failing our athletes? WMJ 2006;105:21. 153
  141. Kroshus E, Fischer AN, Nichols JF. Assessing the awareness and behaviors of U.S. high school nurses with respect to the female athlete triad. J Sch Nurs 2015;31:272-9. 154 · DOI
  142. Miller SM, Kukuljan S, Turner AI, et al. Energy deficiency, menstrual disturbances, and low bone mass: what do exercising Australian women know about the female athlete triad? Int J Sport Nutr Exerc Metab 2012;22:131-8. 155 · DOI
  143. Torres-McGehee TM, Pritchett KL, Zippel D, et al. Sports nutrition knowledge among collegiate athletes, coaches, athletic trainers, and strength and conditioning specialists. J Athl Train 2012;47:205-11. 156 · DOI
  144. Mountjoy M, Costa A, Budgett R, et al. Health promotion through sport: international sport federations' priorities, actions and opportunities. Br J Sports Med 2018;52:54-60. 157 · DOI
  145. Brown KN, Wengreen HJ, Beals KA, et al. Effects of peer-education on knowledge of the female athlete triad among high school track and field athletes: a pilot study. Women Sport Phys Activity J 2016;24:1-6. 158 · DOI
  146. Kilpela LS, Blomquist K, Verzijl C, et al. The body project 4 all: a pilot randomized controlled trial of a mixed-gender dissonance-based body image program. Int J Eat Disord 2016;49:591-602. 159 · DOI
  147. Temme KE, Hoch AZ, Jonardi M, et al. Prevalence of the female athlete triad and effect of a peer-based mentoring program on triad knowledge in high school girls. Clin J Sport Med 2013;23:134-5. 160
  148. Valliant MW, Emplaincourt HP, Wenzel RK, et al. Nutrition education by a registered dietitian improves dietary intake and nutrition knowledge of a NCAA female volleyball team. Nutrients 2012;4:506-16. 161 · DOI
  149. Bar RJ, Cassin SE, Dionne MM, et al. Eating disorder prevention initiatives for athletes: a review. Eur J Sport Sci 2016;16:325-35. 162 · DOI
  150. Martinsen M, Bahr R, Børresen R, et al. Preventing eating disorders among young elite athletes: a randomized controlled trial. Med Sci Sports Exerc 2014;46:435-47. 164 · DOI · Paper page
  151. Martinsen M, Sherman RT, Thompson RA, et al. Coaches' knowledge and management of eating disorders: a randomized controlled trial. Med Sci Sports Exerc 2015;47:1070-8. 165 · DOI
  152. de Bruin APK. Athletes with eating disorder symptomatology, a specific population with specific needs. Curr Opin Psychol 2017;16:148-53. 166 · DOI
  153. Fairburn CG, Beglin SJ. Assessment of eating disorders: interview or self-report questionnaire? Int J Eat Disord 1994;16:363-70. 167
  154. Garner DM, Garfinkel PE. The eating attitudes test: an index of the symptoms of anorexia nervosa. Psychol Med 1979;9:273-9. 168 · DOI
  155. Garner DM, Olmstead MP, Polivy J. Development and validation of a multidimensional eating disorder inventory for anorexia nervosa and bulimia. Int J Eat Disord 1983;2:15-34. 169 · DOI
  156. Hill LS, Reid F, Morgan JF, et al. SCOFF, the development of an eating disorder screening questionnaire. Int J Eat Disord 2010;43:344-51. 170 · DOI
  157. Hinton PS, Kubas KL. Psychosocial correlates of disordered eating in female collegiate athletes: validation of the ATHLETE questionnaire. J Am Coll Health 2005;54:149-56. 171 · DOI
  158. McNulty KY, Adams CH, Anderson JM, et al. Development and validation of a screening tool to identify eating disorders in female athletes. J Am Diet Assoc 2001;101:886-92. 172 · DOI
  159. Steiner H, Pyle RP, Brassington GS, et al. The College Health Related Information Survey (C.h.R.I.s.-73): a screen for college student athletes. Child Psychiatry Hum Dev 2003;34:97-109. 173 · DOI
  160. 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. 174 · DOI
  161. Plateau CR, Mcdermott HJ, Arcelus J, et al. Identifying and preventing disordered eating among athletes. What can we learn from coaches? Appetite 2013;71:483. 175 · DOI
  162. Plateau CR, Arcelus J, Leung N, et al. Female athlete experiences of seeking and receiving treatment for an eating disorder. Eat Disord 2017;25:273-7. 176 · DOI
  163. Ljungqvist A, Jenoure P, Engebretsen L, et al. The International Olympic Committee (IOC) consensus statement on periodic health evaluation of elite athletes March 2009. Br J Sports Med 2009;43:631-43. 177 American Academy of Family Physicians, American Academy of Pediatrics, American College of Sports Medicine. Preparticipation physical evaluation. 4th edn. Washington, DC: American Academy of Family Physicians, 2010. 178 · DOI
  164. Mountjoy M, Sundgot-Borgen J, Burke L, et al. RED-S CAT. Relative energy deficiency in sport (RED-S) clinical assessment tool (CAT). Br J Sports Med 2015;49:421-3. 179 · DOI · Paper page
  165. a DC, Matt KS, Manore MM, et al. Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr 1996;6:24-40. 180
  166. Kopp-Woodroffe SA, Manore MM, Dueck CA, et al. Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr 1999;9:70-88. 181 · DOI
  167. Mallinson RJ, Williams NI, Olmsted MP, et al. A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr 2013;10:34. 182 · DOI
  168. Moreira CA, Bilezikian JP. Stress Fractures: concepts and therapeutics. J Clin Endocrinol Metab 2017;102:525-34. 184 · DOI
  169. Ruohola JP, 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. 185 · DOI
  170. U.S. Department of Agriculture. USDA national nutrient database for standard reference. 2011 http://www. ars. usda. gov/ ba/ bhnrc/ ndl. 186 Golden NH, Carey DE. Vitamin D in health and disease in adolescents: when to screen, whom to treat, and how to treat. Adolesc Med State Art Rev 2016;27:125-39. 187
  171. Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. Endocrine Society. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2011;96:1911-30. 188 · DOI
  172. Sacheck JM, Van Rompay MI, Chomitz VR, et al. Impact of three doses of Vitamin D3 on serum 25(OH)D deficiency and insufficiency in at-risk schoolchildren. J Clin Endocrinol Metab 2017;102:4496-505. 189 · DOI
  173. Myburgh KH, Hutchins J, Fataar AB, et al. Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med 1990;113:754-9. 191 · DOI
  174. 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. 192 US Department of Health and Human Services. 2015-2020 Dietary guidelines for Americans. Washington DC: USDA, 2015. 193 · DOI
  175. Berga SL, Loucks TL. Use of cognitive behavior therapy for functional hypothalamic amenorrhea. Ann N Y Acad Sci. , 2006:1092, 114-29. 194 · DOI
  176. Michopoulos V, Mancini F, Loucks TL, et al. Neuroendocrine recovery initiated by cognitive behavioral therapy in women with functional hypothalamic amenorrhea: a randomized, controlled trial. Fertil Steril 2013;99:2084-91. 195 · DOI
  177. Arends JC, Cheung MY, Barrack MT, et al. Restoration of menses with nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. Int J Sport Nutr Exerc Metab 2012;22:98-108. on July 25, 2023 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from 196 · DOI
  178. Joy E, Kussman A, Nattiv A. 2016 update on eating disorders in athletes: a comprehensive narrative review with a focus on clinical assessment and management. Br J Sports Med 2016;50:154-62. 197 · DOI
  179. Cobb KL, Bachrach LK, Sowers M, et al. The effect of oral contraceptives on bone mass and stress fractures in female runners. Med Sci Sports Exerc 2007;39:1464-73. 198 · DOI
  180. Ducher G, Turner AI, Kukuljan S, et al. Obstacles in the optimization of bone health outcomes in the female athlete triad. Sports Med 2011;41:587-607. 199 · DOI
  181. Lopez LM, Chen M, Mullins Long S, et al. Steroidal contraceptives and bone fractures in women: evidence from observational studies. Cochrane Database Syst Rev 2015;7:CD009849. 200 · DOI
  182. Lopez LM, Grimes DA, Schulz KF, et al. Steroidal contraceptives: effect on bone fractures in women. Cochrane Database Syst Rev 2014:CD006033. 201 · DOI
  183. Misra M, Katzman D, Miller KK, et al. Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. Journal of Bone and Mineral Research 2011;26:2430-8. 202 · DOI
  184. Fazeli PK, Wang IS, Miller KK, et al. Teriparatide increases bone formation and bone mineral density in adult women with anorexia nervosa. The Journal of Clinical Endocrinology & Metabolism 2014;99:1322-9. 204 · DOI
  185. Temme KE, Hoch AZ. Recognition and rehabilitation of the female athlete triad/ tetrad: a multidisciplinary approach. Curr Sports Med Rep 2013;12:190-9. 205 · DOI
  186. Thompson RA, Sherman RT. Eating disorders in sport. Abingdon, UK: Routledge, 2011. 206
  187. Clausen L, Lübeck M, Jones A. Motivation to change in the eating disorders: a systematic review. Int J Eat Disord 2013;46:755-63. 207 · DOI
  188. Arthur-Cameselle JN, Quatromoni PA. Eating disorders in collegiate female athletes: factors that assist recovery. Eat Disord 2014;22:50-61. 208 · DOI
  189. Giel KE, Hermann-Werner A, Mayer J, et al. GOAL study group. Eating disorder pathology in elite adolescent athletes. Int J Eat Disord 2016;49:553-62. 209 · DOI
  190. Sansone RA, Sansone LA. Eating disorders and psychiatric co-morbidity: prevalence and treatment modifications. In: Yager J, Power PS, eds. Clinical manual of eating disorders. Washington DC: American Psychiatric Publishing Inc, 2007:79-112. on July 25, 2023 by guest. Protected by copyright. http://bjsm.bmj.com/ Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded

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Authors
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., Sherman, R. T., Tenforde, A. S., Klungland Torstveit, M., & Budgett, R.
Affiliations
  • McMaster University (CA)
  • Norwegian School of Sport Sciences (NO)
  • Boston Children's Hospital (US)
  • Brigham and Women's Hospital (US)
  • Hebrew University of Jerusalem (IL)
  • University of Alberta (CA)
  • University of Copenhagen (DK)
  • University of Colorado Colorado Springs (US)
  • Harvard University (US)
  • International Olympic Committee (CH)
Corresponding author
Mountjoy, Margo
Venue
British Journal of Sports Medicine
Publisher
BMJ
Published
2018-05-17
Volume
52
Issue
11
Pages
687-697
ISSN
  • 0306-3674 (ISSN-L)
  • 1473-0480
OpenAlex
W2803329575
Cited by
883
References
11
Citations by year
2026: 125 · 2025: 77 · 2024: 119 · 2023: 131 · 2022: 126 · 2021: 136 · 2020: 94 · 2019: 56 · 2018: 15 · 2017: 1 · 2016: 1
FWCI
88.43
Type
journal article
Language
en
Open access
Locations
  • British Journal of Sports Medicine (publishedVersion)
  • PubMed (publishedVersion)
  • Research Bank (Australian Catholic University) (submittedVersion)
  • HighWire Press Open Archive (submittedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
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
relative energy deficiency in sport, low energy availability, female athlete triad, energy balance, exercise energy expenditure, menstrual function, bone health, immune function, protein synthesis, cardiovascular health, athletic performance, male athletes, energy intake
MeSH terms
Energy Intake, Energy Metabolism, Ethnicity, Female, Persons with Disabilities, Disabled Persons, Humans, Male, Consensus, Malnutrition, Female Athlete Triad Syndrome, Sports Nutritional Physiological Phenomena

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