What is one potential negative effect of chronic inadequate fat intake and energy restriction?

  1. Sundgot-Borgen J, Torstveit MK. Aspects of disordered eating continuum in elite high-intensity sports: disordered eating in elite athletes. Scand J Med Sci Sports. 2010;20:112–21. https://doi.org/10.1111/j.1600-0838.2010.01190.x.

    Article  PubMed  Google Scholar 

  2. Martinsen M, Bratland-Sanda S, Eriksson AK, Sundgot-Borgen J. 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. https://doi.org/10.1136/bjsm.2009.068668.

    Article  CAS  PubMed  Google Scholar 

  3. de Bruin AP (Karin), Oudejans RRD, Bakker FC. Dieting and body image in aesthetic sports: a comparison of Dutch female gymnasts and non-aesthetic sport participants. Psychol Sport Exerc 2007;8:507–520. doi.https://doi.org/10.1016/j.psychsport.2006.10.002.

  4. Hagmar M, Hirschberg AL, Berglund L, Berglund B. Special attention to the weight-control strategies employed by olympic athletes striving for leanness is required. Clin J Sport Med. 2008;18:5–9. https://doi.org/10.1097/JSM.0b013e31804c77bd.

    Article  PubMed  Google Scholar 

  5. Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med Off J Can Acad Sport Med. 2004;14:25–32. https://doi.org/10.1097/00042752-200401000-00005.

    Article  Google Scholar 

  6. Slater J, Brown R, McLay-Cooke R, Black K. Low energy availability in exercising women: historical perspectives and future directions. Sports Med Auckl NZ. 2017;47:207–20. https://doi.org/10.1007/s40279-016-0583-0.

    Article  Google Scholar 

  7. Mountjoy M, Sundgot-Borgen JK, Burke LM, Ackerman KE, Blauwet C, Constantini N, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018;52:687–97. https://doi.org/10.1136/bjsports-2018-099193.

    Article  PubMed  Google Scholar 

  8. Tenforde A, Beauchesne A, Borg-Stein J, Hollander K, McInnis K, Kotler D, et al. Awareness and comfort treating the female athlete triad and relative energy deficency in sport among healthcare p-roviders. Dtsch Z Für Sportmed. 2020;71:76–80. https://doi.org/10.5960/dzsm.2020.422.

    Article  Google Scholar 

  9. Brunet P, Ambresin A-E, Gojanovic B. What do you know of RED-S ? A field study on adolescent coaches’ knowledge. Rev Med Suisse. 2019;15:1334–8.

    PubMed  Google Scholar 

  10. Mountjoy M, Costa A, Budgett R, Dvorak J, Engebretsen L, Miller S, et al. Health promotion through sport: international sport federations’ priorities, actions and opportunities. Br J Sports Med. 2018;52:54–60. https://doi.org/10.1136/bjsports-2017-097900.

    Article  PubMed  Google Scholar 

  11. Mukherjee S, Chand V, Wong XX, Choong PP, Lau VS, Wang SC, et al. Perceptions, awareness and knowledge of the female athlete triad amongst coaches – are we meeting the expectations for athlete safety? Int J Sports Sci Coach. 2016;11:545–51. https://doi.org/10.1177/1747954116654781.

    Article  Google Scholar 

  12. 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. https://doi.org/10.1016/j.jpag.2013.11.014.

    Article  PubMed  Google Scholar 

  13. 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. https://doi.org/10.1016/j.jpag.2016.09.013.

    Article  PubMed  Google Scholar 

  14. Shetty P. Adaptation to low energy intakes: the responses and limits to low intakes in infants, children and adults. Eur J Clin Nutr. 1999;53:s14–33. https://doi.org/10.1038/sj.ejcn.1600741.

    Article  PubMed  Google Scholar 

  15. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the female athlete triad—relative energy deficiency in sport (RED-S). Br J Sports Med. 2014;48:491–7. https://doi.org/10.1136/bjsports-2014-093502.

    Article  PubMed  Google Scholar 

  16. Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol-Endocrinol Metab. 2000;278:E43–9. https://doi.org/10.1152/ajpendo.2000.278.1.E43.

    Article  CAS  PubMed  Google Scholar 

  17. Loucks AB, Verdun M, Heath EM, (With the Technical Assistance of T. Law, Sr. and J. R. Thuma). Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 1998;84:37–46. doi https://doi.org/10.1152/jappl.1998.84.1.37.

  18. Koehler K, Hoerner NR, Gibbs JC, Zinner C, Braun H, De Souza MJ, 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. https://doi.org/10.1080/02640414.2016.1142109.

    Article  PubMed  Google Scholar 

  19. Melin A, Tornberg ÅB, Skouby S, Møller SS, Sundgot-Borgen J, Faber J, et al. Energy availability and the female athlete triad in elite endurance athletes: energy availability in female athletes. Scand J Med Sci Sports. 2015;25:610–22. https://doi.org/10.1111/sms.12261.

    Article  CAS  PubMed  Google Scholar 

  20. 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. https://doi.org/10.1210/jc.2002-020369.

    Article  CAS  PubMed  Google Scholar 

  21. Melin AK, Heikura IA, Tenforde A, Mountjoy M. Energy availability in athletics: health, performance, and physique. Int J Sport Nutr Exerc Metab. 2019;29:152–64. https://doi.org/10.1123/ijsnem.2018-0201.

    Article  PubMed  Google Scholar 

  22. Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: a review. Int J Sport Nutr Exerc Metab. 2018;28:385–402. https://doi.org/10.1123/ijsnem.2016-0332.

    Article  CAS  PubMed  Google Scholar 

  23. De Souza MJ, Koltun KJ, Strock NC, Williams NI. Rethinking the concept of an energy availability threshold and its role in the female athlete triad. Curr Opin Physiol. 2019;10:35–42. https://doi.org/10.1016/j.cophys.2019.04.001.

    Article  Google Scholar 

  24. Hausenblas HA, Downs DS. Comparison of body image between athletes and nonathletes: a meta-analytic review. J Appl Sport Psychol. 2001;13:323–39. https://doi.org/10.1080/104132001753144437.

    Article  Google Scholar 

  25. Swami V, Steadman L, Tovée MJ. A comparison of body size ideals, body dissatisfaction, and media influence between female track athletes, martial artists, and non-athletes. Psychol Sport Exerc. 2009;10:609–14. https://doi.org/10.1016/j.psychsport.2009.03.003.

    Article  Google Scholar 

  26. Byrne S, McLean N. Elite athletes: effects of the pressure to be thin. J Sci Med Sport. 2002;5:80–94. https://doi.org/10.1016/S1440-2440(02)80029-9.

    Article  CAS  PubMed  Google Scholar 

  27. Varnes JR, Stellefson ML, Janelle CM, Dorman SM, Dodd V, Miller MD. A systematic review of studies comparing body image concerns among female college athletes and non-athletes, 1997-2012. Body Image. 2013;10:421–32. https://doi.org/10.1016/j.bodyim.2013.06.001.

    Article  PubMed  Google Scholar 

  28. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, 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;48:289. https://doi.org/10.1136/bjsports-2013-093218.

    Article  PubMed  Google Scholar 

  29. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39:1867–82. https://doi.org/10.1249/mss.0b013e318149f111.

    Article  PubMed  Google Scholar 

  30. Burke LM, Close GL, Lundy B, Mooses M, Morton JP, Tenforde AS. Relative energy deficiency in sport in male athletes: a commentary on its presentation among selected groups of male athletes. Int J Sport Nutr Exerc Metab. 2018;28:364–74. https://doi.org/10.1123/ijsnem.2018-0182.

    Article  PubMed  Google Scholar 

  31. Heaney S, O’Connor H, Naughton G, Gifford J. Towards an understanding of the barriers to good nutrition for elite athletes. Int J Sports Sci Coach. 2008;3:391–401. https://doi.org/10.1260/174795408786238542.

    Article  Google Scholar 

  32. Giel KE, Hermann-Werner A, Mayer J, Diehl K, Schneider S, Thiel A, et al. Eating disorder pathology in elite adolescent athletes. Int J Eat Disord. 2016;49:553–62. https://doi.org/10.1002/eat.22511.

    Article  PubMed  Google Scholar 

  33. Condon EM, Dube KA, Herbold NH. The influence of the low-carbohydrate trend on collegiate athletesʼ knowledge, attitudes, and dietary intake of carbohydrates. Top Clin Nutr. 2007;22:175–84. https://doi.org/10.1097/01.TIN.0000270136.22969.d7.

    Article  Google Scholar 

  34. Rosenbloom C. Popular diets and athletes: premises, promises, pros, and pitfalls of diets and what athletes should know about diets and sports performance. Nutr Today. 2014;49:244–8. https://doi.org/10.1097/NT.0000000000000043.

    Article  Google Scholar 

  35. Shriver LH, Betts NM, Wollenberg G. Dietary intakes and eating habits of college athletes: are female college athletes following the current sports nutrition standards? J Am Coll Heal. 2013;61:10–6. https://doi.org/10.1080/07448481.2012.747526.

    Article  Google Scholar 

  36. Cockburn E, Fortune A, Briggs M, Rumbold P. Nutritional knowledge of UK coaches. Nutrients. 2014;6:1442–53. https://doi.org/10.3390/nu6041442.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Torres-McGehee TM, Pritchett KL, Zippel D, Minton DM, Cellamare A, Sibilia M. Sports nutrition knowledge among collegiate athletes, coaches, athletic trainers, and strength and conditioning specialists. J Athl Train. 2012;47:205–11. https://doi.org/10.4085/1062-6050-47.2.205.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Condo D, Lohman R, Kelly M, Carr A. Nutritional intake, sports nutrition knowledge and energy availability in female Australian rules football players. Nutrients. 2019;11:971. https://doi.org/10.3390/nu11050971.

    Article  CAS  PubMed Central  Google Scholar 

  39. Baranauskas M, Stukas R, Tubelis L, Žagminas K, Šurkienė G, Švedas E, et al. Nutritional habits among high-performance endurance athletes. Medicina (Mex). 2015;51:351–62. https://doi.org/10.1016/j.medici.2015.11.004.

    Article  Google Scholar 

  40. Sundgot-Borgen J, Garthe I. Elite athletes in aesthetic and Olympic weight-class sports and the challenge of body weight and body compositions. J Sports Sci. 2011;29:S101–14. https://doi.org/10.1080/02640414.2011.565783.

    Article  PubMed  Google Scholar 

  41. Torstveit MK, Rosenvinge JH, Sundgot-Borgen J. Prevalence of eating disorders and the predictive power of risk models in female elite athletes: a controlled study: eating disorders in athletes and controls. Scand J Med Sci Sports. 2007;18:108–18. https://doi.org/10.1111/j.1600-0838.2007.00657.x.

    Article  PubMed  Google Scholar 

  42. Goltz FR, Stenzel LM, Schneider CD. Disordered eating behaviors and body image in male athletes. Rev Bras Psiquiatr. 2013;35:237–42. https://doi.org/10.1590/1516-4446-2012-0840.

    Article  PubMed  Google Scholar 

  43. Helms ER, Prnjak K, Linardon J. Towards a sustainable nutrition paradigm in physique sport: a narrative review. Sports. 2019;7:172. https://doi.org/10.3390/sports7070172.

    Article  PubMed Central  Google Scholar 

  44. Henriksen K, Schinke R, Moesch K, McCann S, Parham WD, Larsen CH, et al. Consensus statement on improving the mental health of high performance athletes. Int J Sport Exerc Psychol. 2019:1–8. https://doi.org/10.1080/1612197X.2019.1570473.

  45. Appleton PR, Duda JL. Examining the interactive effects of coach-created empowering and disempowering climate dimensions on athletes’ health and functioning. Psychol Sport Exerc. 2016;26:61–70. https://doi.org/10.1016/j.psychsport.2016.06.007.

    Article  Google Scholar 

  46. Beckner BN, Record RA. Navigating the thin-ideal in an athletic world: influence of coach communication on female athletes’ body image and health choices. Health Commun. 2016;31:364–73. https://doi.org/10.1080/10410236.2014.957998.

    Article  PubMed  Google Scholar 

  47. Stirling AE, Kerr GA. The perceived effects of elite athletes’ experiences of emotional abuse in the coach–athlete relationship. Int J Sport Exerc Psychol. 2013;11:87–100. https://doi.org/10.1080/1612197X.2013.752173.

    Article  Google Scholar 

  48. Trakman G, Forsyth A, Devlin B, Belski R. A systematic review of athletes’ and coaches’ nutrition knowledge and reflections on the quality of current nutrition knowledge measures. Nutrients. 2016;8:570. https://doi.org/10.3390/nu8090570.

    Article  PubMed Central  Google Scholar 

  49. Heffner JL, Ogles BM, Gold E, Marsden K, Johnson M. Nutrition and eating in female college athletes: a survey of coaches. Eat Disord. 2003;11:209–20. https://doi.org/10.1080/10640260390218666.

    Article  PubMed  Google Scholar 

  50. I Was the Fastest Girl in America, Until I Joined Nike 2019. https://www.nytimes.com/2019/11/07/opinion/nike-running-mary-cain.html.

  51. Ackerman KE, Stellingwerff T, Elliott-Sale KJ, Baltzell A, Cain M, Goucher K, et al. #REDS (Relative Energy Deficiency in Sport): time for a revolution in sports culture and systems to improve athlete health and performance. Br J Sports Med. 2020;54:369–70. https://doi.org/10.1136/bjsports-2019-101926.

    Article  PubMed  Google Scholar 

  52. Kong P, Harris LM. The sporting body: body image and eating disorder symptomatology among female athletes from leanness focused and nonleanness focused sports. Aust J Psychol. 2015;149:141–60. https://doi.org/10.1080/00223980.2013.846291.

    Article  Google Scholar 

  53. Jones RL, Glintmeyer N, McKenzie A. Slim bodies, eating disorders and the coach-athlete relationship: a tale of identity creation and disruption. Int Rev Sociol Sport. 2005;40:377–91. https://doi.org/10.1177/1012690205060231.

    Article  Google Scholar 

  54. Jowett S, Shanmugan V. Relational coaching in sport: its psychological underpinnings and practical effectiveness. Routledge Int. Handb. Sport Psychol. Abingdon, Oxon: Routledge; 2016. p. 471–84.

    Google Scholar 

  55. Arthur-Cameselle JN, Quatromoni PA. Factors related to the onset of eating disorders reported by female collegiate athletes. Sport Psychol. 2011;25:1–17. https://doi.org/10.1123/tsp.25.1.1.

    Article  Google Scholar 

  56. Engel SG, Johnson C, Powers PS, Crosby RD, Wonderlich SA, Wittrock DA, et al. Predictors of disordered eating in a sample of elite Division I college athletes. Eat Behav. 2003;4:333–43. https://doi.org/10.1016/S1471-0153(03)00031-X.

    Article  PubMed  Google Scholar 

  57. Reel JJ, Petrie TA, SooHoo S, Anderson CM. Weight pressures in sport: examining the factor structure and incremental validity of the weight pressures in sport — Females. Eat Behav. 2013;14:137–44. https://doi.org/10.1016/j.eatbeh.2013.01.003.

    Article  PubMed  Google Scholar 

  58. Barlett CP, Vowels CL, Saucier DA. Meta-analyses of the effects of media images on men’s body-image concerns. J Soc Clin Psychol. 2008;27:279–310. https://doi.org/10.1521/jscp.2008.27.3.279.

    Article  Google Scholar 

  59. Grabe S, Ward LM, Hyde JS. The role of the media in body image concerns among women: a meta-analysis of experimental and correlational studies. Psychol Bull. 2008;134:460–76. https://doi.org/10.1037/0033-2909.134.3.460.

    Article  PubMed  Google Scholar 

  60. Geurin-Eagleman AN, Burch LM. Communicating via photographs: a gendered analysis of Olympic athletes’ visual self-presentation on Instagram. Sport Manag Rev. 2016;19:133–45. https://doi.org/10.1016/j.smr.2015.03.002.

    Article  Google Scholar 

  61. Smith LR, Sanderson J. I’m going to Instagram it! An analysis of athlete self-presentation on Instagram. J Broadcast Electron Media. 2015;59:342–58. https://doi.org/10.1080/08838151.2015.1029125.

    Article  Google Scholar 

  62. Vogel EA, Rose JP, Roberts LR, Eckles K. Social comparison, social media, and self-esteem. Psychol Pop Media Cult. 2014;3:206–22. https://doi.org/10.1037/ppm0000047.

    Article  Google Scholar 

  63. Villalon C, Weiller-Abels K. NBC’s televised media portrayal of female athletes in the 2016 Rio Summer Olympic Games: a critical feminist view. Sport Soc. 2018;21:1137–57. https://doi.org/10.1080/17430437.2018.1442206.

    Article  Google Scholar 

  64. Avena KA. Gender equality in the Olympic movement: not a simple question, not a simple answer. J Philos Sport. 2017;44:329–41. https://doi.org/10.1080/00948705.2017.1359616.

    Article  Google Scholar 

  65. Bailey SD, Ricciardelli LA. Social comparisons, appearance related comments, contingent self-esteem and their relationships with body dissatisfaction and eating disturbance among women. Eat Behav. 2010;11:107–12. https://doi.org/10.1016/j.eatbeh.2009.12.001.

    Article  PubMed  Google Scholar 

  66. Nowell C, Ricciardelli LA. Appearance-based comments, body dissatisfaction and drive for muscularity in males. Body Image. 2008;5:337–45. https://doi.org/10.1016/j.bodyim.2008.06.002.

    Article  PubMed  Google Scholar 

  67. O’Malley K. The rhetoric surrounding Mary Cain. Pepperdine J Comm Res:35–42.

  68. Trexler ET, Smith-Ryan AE, Norton LE. Metabolic adaptation to weight loss: implications for the athlete. J Int Soc Sports Nutr. 2014;11:7. https://doi.org/10.1186/1550-2783-11-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Laughlin GA, Yen SSC. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab. 1997;82:318–21. https://doi.org/10.1210/jcem.82.1.3840.

    Article  CAS  PubMed  Google Scholar 

  70. MacLean PS, Bergouignan A, Cornier M-A, Jackman MR. Biology’s response to dieting: the impetus for weight regain. Am J Physiol-Regul Integr Comp Physiol. 2011;301:R581–600. https://doi.org/10.1152/ajpregu.00755.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Thompson J, Manore MM, Skinner JS. Resting metabolic rate and thermic effect of a meal in low- and adequate-energy intake male endurance athletes. Int J Sport Nutr. 1993;3:194–206. https://doi.org/10.1123/ijsn.3.2.194.

    Article  CAS  PubMed  Google Scholar 

  72. Desgorces F, Chennaoui M, Gomez-Merino D, Drogou C, Guezennec C. Leptin response to acute prolonged exercise after training in rowers. Eur J Appl Physiol. 2004;91. https://doi.org/10.1007/s00421-003-1030-0.

  73. Fedewa MV, Hathaway ED, Ward-Ritacco CL, Williams TD, Dobbs WC. The effect of chronic exercise training on leptin: a systematic review and meta-analysis of randomized controlled trials. Sports Med. 2018;48:1437–50. https://doi.org/10.1007/s40279-018-0897-1.

    Article  PubMed  Google Scholar 

  74. Ahima RS, Saper CB, Flier JS, Elmquist JK. Leptin regulation of neuroendocrine systems. Front Neuroendocrinol. 2000;21:263–307. https://doi.org/10.1006/frne.2000.0197.

    Article  CAS  PubMed  Google Scholar 

  75. Bi X, Loo YT, Henry CJ. Does circulating leptin play a role in energy expenditure? Nutrition. 2019;60:6–10. https://doi.org/10.1016/j.nut.2018.08.015.

    Article  CAS  PubMed  Google Scholar 

  76. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Phys. 1994;266:R817–23. https://doi.org/10.1152/ajpregu.1994.266.3.R817.

    Article  CAS  Google Scholar 

  77. Müller MJ, Enderle J, Pourhassan M, Braun W, Eggeling B, Lagerpusch M, et al. Metabolic adaptation to caloric restriction and subsequent refeeding: the Minnesota Starvation Experiment revisited. Am J Clin Nutr. 2015;102:807–19. https://doi.org/10.3945/ajcn.115.109173.

    Article  CAS  PubMed  Google Scholar 

  78. Alén M, Pakarinen A, Häkkinen K. Effects of prolonged training on serum thyrotropin and thyroid hormones in elite strength athletes. J Sports Sci. 1993;11:493–7. https://doi.org/10.1080/02640419308730018.

    Article  PubMed  Google Scholar 

  79. Hohtari H, Pakarinen A, Kauppila A. Serum concentrations of thyrotropin, thyroxine, triiodothyronine and thyroxine binding globulin in female endurance runners and joggers. Acta Endocrinol. 1987;114:41–6. https://doi.org/10.1530/acta.0.1140041.

    Article  CAS  Google Scholar 

  80. Logue D, Madigan SM, Delahunt E, Heinen M, Mc Donnell S-J, Corish CA. Low energy availability in athletes: a review of prevalence, dietary patterns, physiological health, and sports performance. Sports Med. 2018;48:73–96. https://doi.org/10.1007/s40279-017-0790-3.

    Article  PubMed  Google Scholar 

  81. Stellingwerff T, Maughan RJ, Burke LM. Nutrition for power sports: middle-distance running, track cycling, rowing, canoeing/kayaking, and swimming. J Sports Sci. 2011;29:S79–89. https://doi.org/10.1080/02640414.2011.589469.

    Article  PubMed  Google Scholar 

  82. Silva M-RG, Paiva T. Low energy availability and low body fat of female gymnasts before an international competition. Eur J Sport Sci. 2015;15:591–9. https://doi.org/10.1080/17461391.2014.969323.

    Article  CAS  PubMed  Google Scholar 

  83. Sundgot-Borgen J, Meyer NL, Lohman TG, Ackland TR, Maughan RJ, Stewart AD, et al. How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the Ad Hoc Research Working Group on Body Composition, Health and Performance, under the auspices of the IOC Medical Commission. Br J Sports Med. 2013;47:1012–22. https://doi.org/10.1136/bjsports-2013-092966.

    Article  PubMed  Google Scholar 

  84. Kojima C, Ishibashi A, Tanabe Y, Iwayama K, Kamei A, Takahashi H, et al. Muscle glycogen content during endurance training under low energy availability. Med Sci Sports Exerc. 2020;52:187–95. https://doi.org/10.1249/MSS.0000000000002098.

    Article  CAS  PubMed  Google Scholar 

  85. Walsh JME, Wheat ME, Freund K. Detection, evaluation, and treatment of eating disorders: the role of the primary care physician. J Gen Intern Med. 2000;15:577–90. https://doi.org/10.1046/j.1525-1497.2000.02439.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. De Souza MJ, Koltun KJ, Etter CV, Southmayd EA. Current status of the female athlete triad: update and future directions. Curr Osteoporos Rep. 2017;15:577–87. https://doi.org/10.1007/s11914-017-0412-x.

    Article  PubMed  Google Scholar 

  87. Reed JL, De Souza M, Mallinson RJ, Scheid JL, Williams NI. Energy availability discriminates clinical menstrual status in exercising women. J Int Soc Sports Nutr. 2015;12:11. https://doi.org/10.1186/s12970-015-0072-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Tornberg ÅB, Melin A, Koivula FM, Johansson A, Skouby S, Faber J, et al. Reduced neuromuscular performance in amenorrheic elite endurance athletes. Med Sci Sports Exerc. 2017;49:2478–85. https://doi.org/10.1249/MSS.0000000000001383.

    Article  PubMed  Google Scholar 

  89. 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;28:403–11. https://doi.org/10.1123/ijsnem.2017-0313.

    Article  CAS  PubMed  Google Scholar 

  90. Sale C, Elliott-Sale KJ. Nutrition and athlete bone health. Sports Med. 2019;49:139–51. https://doi.org/10.1007/s40279-019-01161-2.

  91. Fahrenholtz IL, Sjödin A, Benardot D, Tornberg ÅB, Skouby S, Faber J, et al. Within-day energy deficiency and reproductive function in female endurance athletes. Scand J Med Sci Sports. 2018;28:1139–46. https://doi.org/10.1111/sms.13030.

    Article  CAS  PubMed  Google Scholar 

  92. Southmayd EA, De Souza MJ. A summary of the influence of exogenous estrogen administration across the lifespan on the GH/IGF-1 axis and implications for bone health. Growth Hormon IGF Res. 2017;32:2–13. https://doi.org/10.1016/j.ghir.2016.09.001.

    Article  CAS  Google Scholar 

  93. Ackerman KE, Singhal V, Baskaran C, Slattery M, Campoverde Reyes KJ, Toth A, et al. Oestrogen replacement improves bone mineral density in oligo-amenorrhoeic athletes: a randomised clinical trial. Br J Sports Med. 2019;53:229–36. https://doi.org/10.1136/bjsports-2018-099723.

    Article  PubMed  Google Scholar 

  94. Nose-Ogura S, Yoshino O, Kanatani M, Dohi M, Tabei K, Harada M, et al. Effect of transdermal estradiol therapy on bone mineral density of amenorrheic female athletes. Scand J Med Sci Sports. 2020;sms.13679. https://doi.org/10.1111/sms.13679.

  95. Papageorgiou M, Elliott-Sale KJ, Parsons A, Tang JCY, Greeves JP, Fraser WD, et al. Effects of reduced energy availability on bone metabolism in women and men. Bone. 2017;105:191–9. https://doi.org/10.1016/j.bone.2017.08.019.

    Article  CAS  PubMed  Google Scholar 

  96. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res Off J Am Soc Bone Miner Res. 2004;19:1231–40. https://doi.org/10.1359/JBMR.040410.

    Article  Google Scholar 

  97. Papageorgiou M, Martin D, Colgan H, Cooper S, Greeves JP, Tang JCY, et al. Bone metabolic responses to low energy availability achieved by diet or exercise in active eumenorrheic women. Bone. 2018;114:181–8. https://doi.org/10.1016/j.bone.2018.06.016.

    Article  PubMed  Google Scholar 

  98. Hooper DR, Tenforde AS, Hackney AC. Treating exercise-associated low testosterone and its related symptoms. Phys Sportsmed. 2018;46:427–34. https://doi.org/10.1080/00913847.2018.1507234.

    Article  PubMed  Google Scholar 

  99. Mäestu J, Eliakim A, Jürimäe J, Valter I, Jürimäe T. Anabolic and catabolic hormones and energy balance of the male bodybuilders during the preparation for the competition. J Strength Cond Res. 2010;24:1074–81. https://doi.org/10.1519/JSC.0b013e3181cb6fd3.

    Article  PubMed  Google Scholar 

  100. Henning PC, Margolis LM, McClung JP, Young AJ, Pasiakos SM. High protein diets do not attenuate decrements in testosterone and IGF-I during energy deficit. Metabolism. 2014;63:628–32. https://doi.org/10.1016/j.metabol.2014.02.007.

    Article  CAS  PubMed  Google Scholar 

  101. Wong HK, Hoermann R, Grossmann M. Reversible male hypogonadotropic hypogonadism due to energy deficit. Clin Endocrinol. 2019:cen.13973. https://doi.org/10.1111/cen.13973.

  102. Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sports Med. 2016;46:171–82. https://doi.org/10.1007/s40279-015-0411-y.

    Article  PubMed  Google Scholar 

  103. Tenforde AS, Sayres LC, Sainani KL, Fredericson M. Evaluating the relationship of calcium and vitamin D in the prevention of stress fracture injuries in the young athlete: a review of the literature. PM R. 2010;2:945–9. https://doi.org/10.1016/j.pmrj.2010.05.006.

    Article  PubMed  Google Scholar 

  104. Elloumi M, El Elj N, Zaouali M, Maso F, Filaire E, Tabka Z, et al. IGFBP-3, a sensitive marker of physical training and overtraining. Br J Sports Med. 2005;39:604–10. https://doi.org/10.1136/bjsm.2004.014183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Nemet D, Connolly PH, Pontello-Pescatello AM, Rose-Gottron C, Larson JK, Galassetti P, et al. Negative energy balance plays a major role in the IGF-I response to exercise training. J Appl Physiol. 2004;96:276–82. https://doi.org/10.1152/japplphysiol.00654.2003.

    Article  CAS  PubMed  Google Scholar 

  106. Deyssig R, Frisch H, Blum WF, Waldhör T. Effect of growth hormone treatment on hormonal parameters, body composition and strength in athletes. Acta Endocrinol. 1993;128:313–8. https://doi.org/10.1530/acta.0.1280313.

    Article  CAS  Google Scholar 

  107. Calder PC. Feeding the immune system. Proc Nutr Soc. 2013;72:299–309. https://doi.org/10.1017/S0029665113001286.

    Article  PubMed  Google Scholar 

  108. Walsh NP. Nutrition and athlete immune health: new perspectives on an old paradigm. Sports Med. 2019;49:153–68. https://doi.org/10.1007/s40279-019-01160-3.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Keaney LC, Kilding AE, Merien F, Dulson DK. The impact of sport related stressors on immunity and illness risk in team-sport athletes. J Sci Med Sport. 2018;21:1192–9. https://doi.org/10.1016/j.jsams.2018.05.014.

    Article  PubMed  Google Scholar 

  110. Drew M, Vlahovich N, Hughes D, Appaneal R, Burke LM, Lundy B, 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. https://doi.org/10.1136/bjsports-2017-098208.

    Article  PubMed  Google Scholar 

  111. Sarin HV, Gudelj I, Honkanen J, Ihalainen JK, Vuorela A, Lee JH, et al. Molecular pathways mediating immunosuppression in response to prolonged intensive physical training, low-energy availability, and intensive weight loss. Front Immunol. 2019;10:907. https://doi.org/10.3389/fimmu.2019.00907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Hennigar SR, McClung JP, Pasiakos SM. Nutritional interventions and the IL-6 response to exercise. FASEB J Off Publ Fed Am Soc Exp Biol. 2017;31:3719–28. https://doi.org/10.1096/fj.201700080R.

    Article  CAS  Google Scholar 

  113. Pasiakos SM, Margolis LM, Murphy NE, McClung HL, Martini S, Gundersen Y, et al. Effects of exercise mode, energy, and macronutrient interventions on inflammation during military training. Phys Rep. 2016;4. https://doi.org/10.14814/phy2.12820.

  114. Badenhorst CE, Black KE, O’Brien WJ. Hepcidin as a prospective individualized biomarker for individuals at risk of low energy availability. Int J Sport Nutr Exerc Metab. 2019;29:671–81. https://doi.org/10.1123/ijsnem.2019-0006.

    Article  CAS  PubMed  Google Scholar 

  115. Ackerman KE, Holtzman B, Cooper KM, Flynn EF, Bruinvels G, Tenforde AS, 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. https://doi.org/10.1136/bjsports-2017-098958.

    Article  PubMed  Google Scholar 

  116. Torstveit MK, Fahrenholtz IL, Lichtenstein MB, Stenqvist TB, Melin AK. Exercise dependence, eating disorder symptoms and biomarkers of relative energy deficiency in sports (RED-S) among male endurance athletes. BMJ Open Sport Exerc Med. 2019;5:e000439. https://doi.org/10.1136/bmjsem-2018-000439.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Leonard BE. HPA and immune axes in stress: involvement of the serotonergic system. Neuroimmunomodulation. 2006;13:268–76. https://doi.org/10.1159/000104854.

    Article  CAS  PubMed  Google Scholar 

  118. Nakamura Y, Walker BR, Ikuta T. Systematic review and meta-analysis reveals acutely elevated plasma cortisol following fasting but not less severe calorie restriction. Stress Amst Neth. 2016;19:151–7. https://doi.org/10.3109/10253890.2015.1121984.

    Article  CAS  Google Scholar 

  119. Bellastella G, De Bellis A, Maiorino MI, Paglionico VA, Esposito K, Bellastella A. Endocrine rhythms and sport: it is time to take time into account. J Endocrinol Investig. 2019;42:1137–47. https://doi.org/10.1007/s40618-019-01038-1.

    Article  CAS  Google Scholar 

  120. Keay N, Francis G, Hind K. Low energy availability assessed by a sport-specific questionnaire and clinical interview indicative of bone health, endocrine profile and cycling performance in competitive male cyclists. BMJ Open Sport Exerc Med. 2018;4:e000424. https://doi.org/10.1136/bmjsem-2018-000424.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Saris WH. The concept of energy homeostasis for optimal health during training. Can J Appl Physiol Rev Can Physiol Appl. 2001;26(Suppl):S167–75. https://doi.org/10.1139/h2001-051.

    Article  Google Scholar 

  122. Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17:162–84. https://doi.org/10.1016/j.cmet.2012.12.012.

    Article  CAS  PubMed  Google Scholar 

  123. Steinacker JM, Brkic M, Simsch C, Nething K, Kresz A, Prokopchuk O, et al. Thyroid hormones, cytokines, physical training and metabolic control. Horm Metab Res. 2005;37:538–44. https://doi.org/10.1055/s-2005-870419.

    Article  CAS  PubMed  Google Scholar 

  124. Hildebrandt T, Lai JK, Langenbucher JW, Schneider M, Yehuda R, Pfaff DW. The diagnostic dilemma of pathological appearance and performance enhancing drug use. Drug Alcohol Depend. 2011;114:1–11. https://doi.org/10.1016/j.drugalcdep.2010.09.018.

    Article  PubMed  Google Scholar 

  125. Sheffield-Moore M, Urban RJ. An overview of the endocrinology of skeletal muscle. Trends Endocrinol Metab. 2004;15:110–5. https://doi.org/10.1016/j.tem.2004.02.009.

    Article  CAS  PubMed  Google Scholar 

  126. Degoutte F, Jouanel P, Bègue RJ, Colombier M, Lac G, Pequignot JM, et al. Food restriction, performance, biochemical, psychological, and endocrine changes in Judo athletes. Int J Sports Med. 2006;27:9–18. https://doi.org/10.1055/s-2005-837505.

    Article  CAS  PubMed  Google Scholar 

  127. Mårtensson S, Nordebo K, Malm C. High training volumes are associated with a low number of self-reported sick days in elite endurance athletes. J Sports Sci Med. 2014;13:929–33.

    PubMed  PubMed Central  Google Scholar 

  128. Logue DM, Madigan SM, Heinen M, McDonnell S-J, Delahunt E, Corish CA. Screening for risk of low energy availability in athletic and recreationally active females in Ireland. Eur J Sport Sci. 2019;19:112–22. https://doi.org/10.1080/17461391.2018.1526973.

    Article  PubMed  Google Scholar 

  129. Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2018;57:847–59. https://doi.org/10.1007/s00394-017-1498-8.

    Article  PubMed  Google Scholar 

  130. Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh 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. https://doi.org/10.1177/0363546513520295.

    Article  PubMed  Google Scholar 

  131. Bojsen-Møller J, Magnusson SP, Rasmussen LR, Kjaer M, Aagaard P. Muscle performance during maximal isometric and dynamic contractions is influenced by the stiffness of the tendinous structures. J Appl Physiol. 2005;99:986–94. https://doi.org/10.1152/japplphysiol.01305.2004.

    Article  PubMed  Google Scholar 

  132. Chidi-Ogbolu N, Baar K. Effect of estrogen on musculoskeletal performance and injury risk. Front Physiol. 2018;9:1834. https://doi.org/10.3389/fphys.2018.01834.

    Article  PubMed  Google Scholar 


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Components of total daily energy expenditure and adaptions to low energy availability are shown. a Total daily energy expenditure (TDEE) consists of the resting energy expenditure (REE) and the non-resting energy expenditure (NREE). NREE can be further subdivided into the thermic effect of food (TEF), non-exercise activity thermogenesis (NEAT), and exercise activity thermogenesis (EAT). Of those components, NEAT and EAT describe energy expended through physical activity (PA). b When energy availability is low, either by restricted dietary energy intake or increased energy exercise expenditure (EEE), metabolic adaptions to conserve energy occur. Those encompass a decline in basal metabolic rate (BMR), NEAT, and, if caloric intake is restricted, also in TEF. Generally, EAT will decrease as well but may be elevated in individuals increasing their training volume. Therefore, adaptations in this component are variable. Figure modified according to MacLean et al. [70]