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The Path Towards Progress: A Critical Review to Advance the Science of the Female and Male Athlete Triad and Relative Energy Deficiency in Sport

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Abstract

Energy status plays a key role in the health of athletes and exercising individuals. Energy deficiency/low energy availability (EA), referring to a state in which insufficient energy intake and/or excessive exercise energy expenditure has resulted in compensatory metabolic adaptations to conserve fuel, can affect numerous physiological systems in women and men. The Female Athlete Triad, Male Athlete Triad, and Relative Energy Deficiency in Sport (RED-S) models conceptualize the effects of energy deficiency in athletes, and each model has strengths and limitations. For instance, the Female Athlete Triad model depicts relationships between low EA, reproductive, and bone health, underpinning decades of experimental evidence, but may be perceived as limited in scope, while the more recent RED-S model proposes a wider range of potential health effects of low EA, though many model components require more robust scientific justification. This critical review summarizes current evidence regarding the effects of energy deficiency on athlete health by addressing the quality of the underlying science, the strengths and limitations of each model, and highlighting areas where future research is needed to advance the field. With the health and wellness of athletes and exercising individuals as the overarching priority, we conclude with specific steps that will help focus future research on the Female and Male Athlete Triad and RED-S, and encourage all researchers, clinicians, and practitioners to collaborate to support the common goal of promoting the highest quality science and evidence-based medicine in pursuit of the advancement of athletes’ health, well-being, and performance.

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References

  1. Feicht CB, Johnson TS, Martin BJ, et al. Secondary amenorrhoea in athletes. Lancet. 1978;2(8100):1145–6.

    CAS  PubMed  Google Scholar 

  2. Dale E, Gerlach DH, Wilhite AL. Menstrual dysfunction in distance runners. Obstet Gynecol. 1979;54(1):47–53.

    CAS  PubMed  Google Scholar 

  3. Erdelyi G. Gynecologic survey of female athletes. J Sports Med Phys Fitness. 1962;2:174–9.

    Google Scholar 

  4. Erdelyi G. Effects of exercise on the menstrual cycle. Phys Sportsmed. 1976;4:79–81.

    Google Scholar 

  5. Drinkwater BL, Nilson K, Chesnut CH 3rd, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med. 1984;311(5):277–81.

    CAS  PubMed  Google Scholar 

  6. Drinkwater BL, Nilson K, Ott S, Chesnut CH 3rd. Bone mineral density after resumption of menses in amenorrheic athletes. JAMA. 1986;256(3):380–2.

    CAS  PubMed  Google Scholar 

  7. Drinkwater BL, Bruemner B, Chesnut CH 3rd. Menstrual history as a determinant of current bone density in young athletes. JAMA. 1990;263(4):545–8.

    CAS  PubMed  Google Scholar 

  8. Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc. 1990;22(3):275–80.

    CAS  PubMed  Google Scholar 

  9. Yeager KK, Agostini R, Nattiv A, et al. The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc. 1993;25(7):775–7.

    CAS  PubMed  Google Scholar 

  10. Nattiv A, Agostini R, Drinkwater B, et al. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. 1994;13(2):405–18.

    CAS  PubMed  Google Scholar 

  11. 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(5):i–ix.

    CAS  PubMed  Google Scholar 

  12. Lloyd T, Myers C, Buchanan JR, et al. Collegiate women athletes with irregular menses during adolescence have decreased bone density. Obstet Gynecol. 1988;72(4):639–42.

    CAS  PubMed  Google Scholar 

  13. Marcus R, Cann C, Madvig P, et al. Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med. 1985;102(2):158–63.

    CAS  PubMed  Google Scholar 

  14. Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–82.

    PubMed  Google Scholar 

  15. Loucks AB, Heath EM. 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(4):910–5.

    CAS  PubMed  Google Scholar 

  16. Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol. 1993;264(5 Pt 2):R924–30.

    CAS  PubMed  Google Scholar 

  17. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19(8):1231–40.

    PubMed  Google Scholar 

  18. 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(1):297–311.

    CAS  PubMed  Google Scholar 

  19. Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol. 1998;84(1):37–46.

    CAS  PubMed  Google Scholar 

  20. De Souza MJ, Miller BE, Loucks AB, et al. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab. 1998;83(12):4220–32.

    PubMed  Google Scholar 

  21. Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes. A twelve-month prospective study. Am J Sports Med. 1996;24(6):810–8.

    CAS  PubMed  Google Scholar 

  22. De Souza MJ, Toombs RJ, Scheid JL, et al. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod. 2010;25(2):491–503.

    PubMed  Google Scholar 

  23. Southmayd EA, Mallinson RJ, Williams NI, et al. Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int. 2017;28(4):1365–76.

    CAS  PubMed  Google Scholar 

  24. Southmayd EA, Williams NI, Mallinson RJ, et al. Energy deficiency suppresses bone turnover in exercising women with menstrual disturbances. J Clin Endocrinol Metab. 2019;104(8):3131–45.

    PubMed  Google Scholar 

  25. Koltun KJ, De Souza MJ, Scheid JL, et al. Energy availability is associated with luteinizing hormone pulse frequency and induction of luteal phase defects. J Clin Endocrinol Metab. 2020;105:185–93.

    Google Scholar 

  26. Mallinson RJ, Williams NI, Hill BR, et al. Body composition and reproductive function exert unique influences on indices of bone health in exercising women. Bone. 2013;56(1):91–100.

    PubMed  Google Scholar 

  27. 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(1):E29-39.

    CAS  PubMed  Google Scholar 

  28. Williams NI, Mallinson RJ, De Souza MJ. Rationale and study design of an intervention of increased energy intake in women with exercise-associated menstrual disturbances to improve menstrual function and bone health: the REFUEL study. Contemp Clin Trials Commun. 2019;14: 100325.

    PubMed  PubMed Central  Google Scholar 

  29. Williams NI, Helmreich DL, Parfitt DB, et al. Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J Clin Endocrinol Metab. 2001;86(11):5184–93.

    CAS  PubMed  Google Scholar 

  30. Williams NI, Caston-Balderrama AL, Helmreich DL, et al. Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea. Endocrinology. 2001;142(6):2381–9.

    CAS  PubMed  Google Scholar 

  31. De Souza MJ, Nattiv A, Joy E, et al. 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(4):289.

    PubMed  Google Scholar 

  32. De Souza MJ, Nattiv A, Joy E, et al. 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, CA, May 2012, and 2nd International Conference held in Indianapolis, IN, May 2013. Clin J Sport Med. 2014;24(2):96–119.

    PubMed  Google Scholar 

  33. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(7):491–7.

    PubMed  Google Scholar 

  34. 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(11):687–97.

    PubMed  Google Scholar 

  35. 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(7):417–20.

    PubMed  Google Scholar 

  36. Gordon CM, Ackerman KE, Berga SL, et al. Functional hypothalamic amenorrhea: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2017;102(5):1413–39.

    PubMed  Google Scholar 

  37. Ozier AD, Henry BW, American DA. Position of the American Dietetic Association: nutrition intervention in the treatment of eating disorders. J Am Diet Assoc. 2011;111(8):1236–41.

    PubMed  Google Scholar 

  38. Osteoporosis prevention, diagnosis, and therapy. NIH Consensus Statement. 2000;17(1):1–45.

  39. Wheeler GD, Wall SR, Belcastro AN, et al. Reduced serum testosterone and prolactin levels in male distance runners. JAMA. 1984;252(4):514–6.

    CAS  PubMed  Google Scholar 

  40. MacConnie SE, Barkan A, Lampman RM, et al. Decreased hypothalamic gonadotropin-releasing hormone secretion in male marathon runners. N Engl J Med. 1986;315(7):411–7.

    CAS  PubMed  Google Scholar 

  41. Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-trained and untrained males. Med Sci Sports Exerc. 1988;20(1):60–5.

    CAS  PubMed  Google Scholar 

  42. 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(7):383–91.

    PubMed  Google Scholar 

  43. Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long distance runners. Med Sci Sports Exerc. 1989;21(1):66–70.

    CAS  PubMed  Google Scholar 

  44. 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;31:335–48.

    PubMed  Google Scholar 

  45. 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. https://doi.org/10.1097/JSM.0000000000000948.

    Article  PubMed  Google Scholar 

  46. DiPietro L, Stachenfeld NS. The female athlete triad myth. Med Sci Sports Exerc. 2006;38(4):795 (author reply 6).

    PubMed  Google Scholar 

  47. Di Pietro L, Stachenfeld N. Refutation of the myth of the female athlete triad. Br J Sport Med. 2007;41(1):57–8.

    Google Scholar 

  48. Loucks AB, Stachenfeld NS, DiPietro L. The female athlete triad: do female athletes need to take special care to avoid low energy availability? Med Sci Sports Exerc. 2006;38(10):1694–700.

    PubMed  Google Scholar 

  49. Loucks AB, Verdun M. Slow restoration of LH pulsatility by refeeding in energetically disrupted women. Am J Physiol. 1998;275(4 Pt 2):R1218–26.

    CAS  PubMed  Google Scholar 

  50. Strock NCA, De Souza MJ, Williams NI. Eating behaviours related to psychological stress are associated with functional hypothalamic amenorrhoea in exercising women. J Sports Sci. 2020;38(21):2396–406.

    PubMed  Google Scholar 

  51. Strock NCA, Koltun KJ, Mallinson RJ, et al. Characterizing the resting metabolic rate ratio in ovulatory exercising women over 12 months. Scand J Med Sci Sports. 2020;30(8):1337–47.

    PubMed  Google Scholar 

  52. Strock NCA, Koltun KJ, Southmayd EA, et al. Indices of resting metabolic rate accurately reflect energy deficiency in exercising women. Int J Sport Nutr Exerc Metab. 2020;29:1–11.

    Google Scholar 

  53. Williams NI, Bullen BA, McArthur JW, et al. Effects of short-term strenuous endurance exercise upon corpus luteum function. Med Sci Sports Exerc. 1999;31(7):949–58.

    CAS  PubMed  Google Scholar 

  54. Bullen BA, Skrinar GS, Beitins IZ, von Mering G, Turnbull BA, McArthur JW. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med. 1985;312(21):1349–53.

    CAS  PubMed  Google Scholar 

  55. De Souza MJ, Mallinson RJ, Strock NCA, et al. Randomized controlled trial of the effects of increased energy intake on menstrual recovery in exercising women with menstrual disturbances: the “REFUEL” Study. Hum Reprod. 2021;36:2285–97.

    PubMed  PubMed Central  Google Scholar 

  56. De Souza MJ, Ricker EA, Mallinson RJ, et al. Randomized controlled trial assessing the effects of increased energy intake on BMD changes in exercising women with menstrual disturbances: the “REFUEL” Study. Am J Clin Nutr. 2021 (in review).

  57. Ackerman KE, Singhal V, Baskaran C, et al. Oestrogen replacement improves bone mineral density in oligo-amenorrhoeic athletes: a randomised clinical trial. Br J Sports Med. 2019;53(4):229–36.

    PubMed  Google Scholar 

  58. Ackerman KE, Singhal V, Slattery M, et al. Effects of estrogen replacement on bone geometry and microarchitecture in adolescent and young adult oligoamenorrheic athletes: a randomized trial. J Bone Miner Res. 2020;35(2):248–60.

    CAS  PubMed  Google Scholar 

  59. Allaway HCM, Misra M, Southmayd EA, et al. Are the effects of oral and vaginal contraceptives on bone formation in young women mediated via the growth hormone-IGF-I axis? Front Endocrinol (Lausanne). 2020;11:334.

    Google Scholar 

  60. Baskaran C, Cunningham B, Plessow F, et al. Estrogen replacement improves verbal memory and executive control in oligomenorrheic/amenorrheic athletes in a randomized controlled trial. J Clin Psychiatry. 2017;78(5):e490–7.

    PubMed  PubMed Central  Google Scholar 

  61. Plessow F, Singhal V, Toth AT, et al. Estrogen administration improves the trajectory of eating disorder pathology in oligo-amenorrheic athletes: a randomized controlled trial. Psychoneuroendocrinology. 2019;102:273–80.

    CAS  PubMed  Google Scholar 

  62. 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(20):1461–5.

    PubMed  Google Scholar 

  63. Williams NI, Koltun KJ, Strock NCA, et al. Female athlete triad and relative energy deficiency in sport: a focus on scientific rigor. Exerc Sport Sci Rev. 2019;47(4):197–205.

    PubMed  Google Scholar 

  64. 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(9):1721–37.

    PubMed  Google Scholar 

  65. Ackerman KE, Holtzman B, Cooper KM, et al. Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport. Br J Sports Med. 2019;53:628–33.

    PubMed  Google Scholar 

  66. Hooper DR, Mallard J, Wight JT, et al. Performance and health decrements associated with relative energy deficiency in sport for division i women athletes during a collegiate cross-country season: a case series. Front Endocrinol. 2021;12:12.

    Google Scholar 

  67. Rogers MA, Appaneal RN, Hughes D, et al. Prevalence of impaired physiological function consistent with Relative Energy Deficiency in Sport (RED-S): an Australian elite and pre-elite cohort. Br J Sports Med. 2021;55(1):38–45.

    PubMed  Google Scholar 

  68. Mathisen TF, Heia J, Raustol M, et al. Physical health and symptoms of relative energy deficiency in female fitness athletes. Scand J Med Sci Sports. 2020;30(1):135–47.

    PubMed  Google Scholar 

  69. 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(7):540–5.

    PubMed  Google Scholar 

  70. Enck P, Aziz Q, Barbara G, et al. Irritable bowel syndrome. Nat Rev Dis Primers. 2016;24(2):16014.

    Google Scholar 

  71. Camilleri M, Camilleri MJA. Diarrhea and constipation. In: Jameson J, Fauci AS, Kasper DL, Hauser SL, Longo DL, Jameson J, editors. Harrison’s principles of internal medicine. 20th ed. New York: McGraw-Hill; 2014.

    Google Scholar 

  72. Waterman JJ, Kapur R. Upper gastrointestinal issues in athletes. Curr Sports Med Rep. 2012;11(2):99–104.

    PubMed  Google Scholar 

  73. Qamar MI, Read AE. Effects of exercise on mesenteric blood flow in man. Gut. 1987;28(5):583–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. ter Steege RW, Geelkerken RH, Huisman AB, et al. Abdominal symptoms during physical exercise and the role of gastrointestinal ischaemia: a study in 12 symptomatic athletes. Br J Sports Med. 2012;46(13):931–5.

    PubMed  Google Scholar 

  75. Gutekunst K, Kruger K, August C, et al. Acute exercises induce disorders of the gastrointestinal integrity in a murine model. Eur J Appl Physiol. 2014;114(3):609–17.

    PubMed  Google Scholar 

  76. Holland AM, Hyatt HW, Smuder AJ, et al. Influence of endurance exercise training on antioxidant enzymes, tight junction proteins, and inflammatory markers in the rat ileum. BMC Res Notes. 2015;30(8):514.

    Google Scholar 

  77. Koon G, Atay O, Lapsia S. Gastrointestinal considerations related to youth sports and the young athlete. Transl Pediatr. 2017;6(3):129–36.

    PubMed  PubMed Central  Google Scholar 

  78. Walsh NP. Nutrition and athlete immune health: new perspectives on an old paradigm. Sports Med. 2019;49(Suppl 2):153–68.

    PubMed  PubMed Central  Google Scholar 

  79. Meydani SN, Das SK, Pieper CF, et al. Long-term moderate calorie restriction inhibits inflammation without impairing cell-mediated immunity: a randomized controlled trial in non-obese humans. Aging. 2016;8(7):1416–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Shimizu K, Aizawa K, Suzuki N, et al. Influences of weight loss on monocytes and T-cell subpopulations in male judo athletes. J Strength Cond Res. 2011;25(7):1943–50.

    PubMed  Google Scholar 

  81. Tsai ML, Chou KM, Chang CK, et al. Changes of mucosal immunity and antioxidation activity in elite male Taiwanese taekwondo athletes associated with intensive training and rapid weight loss. Br J Sports Med. 2011;45(9):729–34.

    PubMed  Google Scholar 

  82. Abedelmalek S, Chtourou H, Souissi N, et al. Caloric restriction effect on proinflammatory cytokines, growth hormone, and steroid hormone concentrations during exercise in judokas. Oxid Med Cell Longev. 2015;2015: 809492.

    PubMed  PubMed Central  Google Scholar 

  83. Imai T, Seki S, Dobashi H, et al. Effect of weight loss on T-cell receptor-mediated T-cell function in elite athletes. Med Sci Sports Exerc. 2002;34(2):245–50.

    CAS  PubMed  Google Scholar 

  84. Tsai ML, Ko MH, Chang CK, et al. Impact of intense training and rapid weight changes on salivary parameters in elite female Taekwondo athletes. Scand J Med Sci Sports. 2011;21(6):758–64.

    PubMed  Google Scholar 

  85. Moriyama M, Hugentobler WJ, Iwasaki A. Seasonality of respiratory viral infections. Annu Rev Virol. 2020;7(1):83–101.

    CAS  PubMed  Google Scholar 

  86. Simancas-Racines D, Franco JV, Guerra CV, et al. Vaccines for the common cold. Cochrane Database Syst Rev. 2017;5: CD002190.

    PubMed  Google Scholar 

  87. Heikkinen T, Jarvinen A. The common cold. Lancet. 2003;361(9351):51–9.

    PubMed  PubMed Central  Google Scholar 

  88. Lei H, Li Y, **ao S, Lin CH, et al. Routes of transmission of influenza A H1N1, SARS CoV, and norovirus in air cabin: comparative analyses. Indoor Air. 2018;28(3):394–403.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Lei H, Tang JW, Li Y. Transmission routes of influenza A(H1N1)pdm09: analyses of inflight outbreaks. Epidemiol Infect. 2018;146(13):1731–9.

    CAS  PubMed  Google Scholar 

  90. 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(2):162–5.

    PubMed  Google Scholar 

  91. 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(9): e45504.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 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(2):270–6.

    PubMed  Google Scholar 

  93. Fazeli PK, Klibanski A. Determinants of GH resistance in malnutrition. J Endocrinol. 2014;220(3):R57-65.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab. 1996;81(12):4301–9.

    CAS  PubMed  Google Scholar 

  95. 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(3):1013–9.

    CAS  PubMed  Google Scholar 

  96. Slater J, McLay-Cooke R, Brown R, et al. Female recreational exercisers at risk for low energy availability. Int J Sport Nutr Exerc Metab. 2016;26(5):421–7.

    PubMed  Google Scholar 

  97. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924–6.

    PubMed  PubMed Central  Google Scholar 

  98. 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(20):1921–9.

    PubMed  Google Scholar 

  99. 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.

    CAS  PubMed  Google Scholar 

  100. 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.

    PubMed  Google Scholar 

  101. 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.

    CAS  PubMed  Google Scholar 

  102. Murphy MK, Black NA, Lam** DL, et al. Consensus development methods, and their use in clinical guideline development. Health Technol Assess. 1998;2(3):i–iv, 1–88.

  103. Dalkey NC, Helmer O. An experimental application of the Delphi method to the use of experts. Manag Sci. 1963;9:458–67.

    Google Scholar 

  104. Vanheest JL, Rodgers CD, Mahoney CE, et al. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46(1):156–66.

    PubMed  Google Scholar 

  105. Stenqvist TB, Melin AK, Garthe I, Slater G, Paulsen G, Iraki J, et al. Prevalence of surrogate markers of relative energy deficiency in male Norwegian Olympic-level athletes. Int J Sport Nutr Exerc Metab. 2021. https://doi.org/10.1123/ijsnem.2020-0368Abstract.

    Article  PubMed  Google Scholar 

  106. Lane AR, Hackney AC, Smith-Ryan AE, Kucera K, Register-Mihalik JK, Ondrak K. Energy availability and RED-S risk factors in competitive, non-elite male endurance athletes. Transl Med Exerc Prescr. 2021;1(1):25–32.

    PubMed  PubMed Central  Google Scholar 

  107. Sharps FRJ, Wilson LJ, Graham CA, Curtis C. Prevalence of disordered eating, eating disorders and risk of low energy availability in professional, competitive and recreational female athletes based in the United Kingdom. Eur J Sports Sci. 2021. https://doi.org/10.1080/17461391.2021.1943712.

    Article  Google Scholar 

  108. Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM. 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(4):403–11.

    CAS  PubMed  Google Scholar 

  109. Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, Faber J, et al. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports. 2015;25(5):610–22.

    CAS  PubMed  Google Scholar 

  110. Brook EM, Tenforde AS, Broad EM, Matzkin EG, Yang HY, Collins JE, et al. Low energy availability, menstrual dysfunction, and impaired bone health: a survey of elite para athletes. Scand J Med Sci Sports. 2019;29(5):678–85.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Kinesiology and Physiology, Pennsylvania State University, University Park, PA, USA

    Mary Jane De Souza

  2. Department of Kinesiology, Pennsylvania State University, University Park, PA, 16802, USA

    Nicole C. A. Strock & Nancy I. Williams

  3. Consortium for Health and Military Performance, Department of Military and Emergency Medicine, F. Edward Hébert School of Medicine, Uniformed Services University, Bethesda, USA

    Emily A. Ricker

  4. Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, USA

    Emily A. Ricker

  5. Department of Sports Medicine and Nutrition, University of Pittsburgh, Pittsburgh, PA, USA

    Kristen J. Koltun

  6. Department of Family and Consumer Sciences, California State University Long Beach, Long Beach, CA, USA

    Michelle Barrack

  7. Intermountain Healthcare, Salt Lake City, USA

    Elizabeth Joy

  8. Department of Sports Medicine, University of California Los Angeles, Los Angeles, CA, USA

    Aurelia Nattiv

  9. Department of Orthopedics and Sports Medicine, University of Illinois Chicago, Chicago, IL, USA

    Mark Hutchinson

  10. Division of Pediatric Endocrinology, Massachusetts General Hospital, Boston, MA, USA

    Madhusmita Misra

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  1. Mary Jane De Souza
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  7. Aurelia Nattiv
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Corresponding author

Correspondence to Nancy I. Williams.

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Conflict of interest

Mary Jane De Souza, Nicole C. Strock, Emily A. Ricker, Kristen J. Koltun, Michelle Barrack, Elizabeth Joy, Aurelia Nattiv, Mark Hutchinson, Madhusmita Misra, and Nancy I. Williams declare that they have no conflicts of interest relevant to the content of this article.

The opinions and assertions expressed herein are those of the author(s) and do not necessarily reflect the official policy or position of the Uniformed Services University or the Department of Defense.

The contents of this publication are the sole responsibility of the author(s) and do not necessarily reflect the views, opinions or policies of The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. Government.

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No sources of funding were used to assist in the preparation of this article.

Authorship contributions

MJD, NCAS, EAR, KJK, NIW wrote the first draft of the manuscript. MB, EJ, AN, MH, MM revised the original manuscript. All authors read and approved the final manuscript.

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De Souza, M.J., Strock, N.C.A., Ricker, E.A. 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 52, 13–23 (2022). https://doi.org/10.1007/s40279-021-01568-w

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