Skip to main content
SpringerLink
Log in

Low Energy Availability in Exercising Women: Historical Perspectives and Future Directions

  • Review Article
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

Research on the health of female athletes has developed substantially over the past 50 years. This review aims to provide an overview of this research and identify directions for future work. While early cross-sectional studies focused primarily on menstruation, research has progressed to now encompass hormonal changes, bone health and lipid profiles. The seminal work of Loucks and colleagues distinguished that these health concerns were due to low energy availability (LEA) rather than exercise alone. LEA occurs when the body has insufficient energy available to meet the needs of training and normal physiological functioning. While there appears to be agreement that LEA is the underlying cause of this syndrome, controversy regarding terminology has emerged. Originally coined the female athlete triad (Triad), some researchers are now advocating the use of the term relative energy deficiency in sport (RED-S). This group argues that the term Triad excludes male athletes who also have the potential to experience LEA and its associated negative impact on health and performance. At present, implications of LEA among male athletes are poorly understood and should form the basis of future research. Other directions for future research include determination of the prevalence and long-term risks of LEA in junior and developmental athletes, and the development of standardised tools to diagnose LEA. These tools are required to aid comparisons between studies and to develop treatment strategies to attenuate the long-term health consequences of LEA. Continued advances in knowledge on LEA and its associated health consequences will aid development of more effective prevention, early detection and treatment strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Female fertility and the body fat connection [book review]. N Engl J Med. 2003;348:869–70. doi:10.1056/NEJM200302273480924.

  2. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29(1):7–15.

    Article  Google Scholar 

  3. New Zealand Government, Ministry of Health. Be active every day. 2010, 2013. http://www.health.govt.nz/our-work/eating-and-activity-guidelines. Accessed 7 Apr 2016.

  4. US Department of Health and Human Services. 2008 Physical activity guidelines for Americans. 2008. http://fitprogram.ucla.edu/workfiles/Documents/Fit%20for%20residents%20curriculum/Step_5/2008_Physical_Activity_Guidelines_for_Americans.pdf. Accessed 7 Apr 2016.

  5. World Health Organisation. Global recommendations on physical activity for health. 2010. http://www.who.int/dietphysicalactivity/publications/9789241599979/en/. Accessed 7 Apr 2016.

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. 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(3):1354–9.

    Article  CAS  PubMed  Google Scholar 

  9. Friday KE, Drinkwater BL, Bruemmer B, et al. Elevated plasma low-density lipoprotein and high-density lipoprotein cholesterol levels in amenorrheic athletes: effects of endogenous hormone status and nutrient intake. J Clin Endocrinol Metab. 1993;77(6):1605–9.

    CAS  PubMed  Google Scholar 

  10. Boyden TW, Pamenter RW, Stanforth P, et al. Evidence for mild thyroidal impairment in women undergoing endurance training. J Clin Endocrinol Metab. 1982;54(1):53–6.

    Article  CAS  PubMed  Google Scholar 

  11. De Souza M, Toombs R, Scheid J, 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.

    Article  PubMed  Google Scholar 

  12. 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.

    Article  PubMed  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. 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.

    Article  PubMed  Google Scholar 

  15. Selye H. The effect of adaptation to various damaging agents on the female sex organs in the rat. Endocrinology. 1939;25(4):615–24.

    Article  CAS  Google Scholar 

  16. Sadlier RMFS. The ecology of reproduction in wild and domestic mammals. London: Metheun; 1969.

    Book  Google Scholar 

  17. Vaughan MR, Keith LB. Demographic response of experimental snowshoe hare populations to overwinter food shortage. J Wildl Manag. 1981;45(2):354–80.

    Article  Google Scholar 

  18. Hansen L, Batzli GO. The influence of food availability on the white-footed mouse: populations in isolated woodlots. Can J Zool. 1978;56(12):2530–41.

    Article  Google Scholar 

  19. Fordham R. Field populations of deermice with supplemental food. Ecology. 1971;52:138–46.

    Article  Google Scholar 

  20. Boutin S. Effect of late winter food addition on numbers and movements of snowshoe hares. Oecologia. 1984;62:393–400.

    Article  Google Scholar 

  21. Merson M, Kirkpatrick R. Relative sensitivity of reproductive activity and body-fat level to food restriction in white-footed mice. Am Midl Nat. 1981;106(2):305–12.

    Article  Google Scholar 

  22. Merry B, Holehan AM. Onset of puberty and duration of fertility in rats fed a restricted diet. J Reprod Fertil. 1979;57(2):253–9.

    Article  CAS  PubMed  Google Scholar 

  23. Morin L. Environment and hamster reproduction: responses to phase-specific starvation during estrous cycle. Am J Physiol Regul Integr Comp. 1986;251(4):R663–9.

    CAS  Google Scholar 

  24. Manning JM, Bronson F. Suppression of puberty in rats by exercise: effects on hormone levels and reversal with GnRH infusion. Am J Physiol Regul Integr Comp. 1991;260(4):R717–23.

    CAS  Google Scholar 

  25. Manning JM, Bronson FH. Effects of prolonged exercise on puberty and luteinizing hormone secretion in female rats. Am J Physiol. 1990;258:R1395–401.

    Google Scholar 

  26. Carlberg KA, Fregly MJ. Disruption of estrous cycles in exercise-trained rats. Proc Soc Exp Biol Med. 1985;179(1):21–4.

    Article  CAS  PubMed  Google Scholar 

  27. Schneider JE, Wade GN. Availability of metabolic fuels controls estrous cyclicity of Syrian hamsters. Science. 1989;244(4910):1326–8.

    Article  CAS  PubMed  Google Scholar 

  28. Bronson F, Heideman PD. Short-term hormonal responses to food intake in peripubertal female rats. Am J Physiol Regul Integr Comp Physiol. 1990;259(1):R25–31.

    CAS  Google Scholar 

  29. 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 

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. DiMarco NM, Dart L, Sanborn CB. Modified activity-stress paradigm in an animal model of the female athlete triad. J App Physiol. 2007;103(5):1469–78.

    Article  CAS  Google Scholar 

  32. International Olympic Committee. Factsheet: women in the Olympic movement. 2014. http://www.olympic.org/Documents/Reference_documents_Factsheets/Women_in_Olympic_Movement.pdf. Accessed 4 June 2015.

  33. Erdelyi GJ. Gynecological survey of female athletes. J Sports Med Phys Fitness. 1962;2:174–9.

    Google Scholar 

  34. Malina RM, Spirduso WW. Age at menarche and selected menstrual characteristics in athletes at different competitive levels and in different sports. Med Sci Sport. 1977;10(3):218–22.

    Google Scholar 

  35. The United States Department of Justice. Overview of Title IX of the Education Amendments of 1972, 20 U.S.C. A§ 1681 Et. Seq. Updated 2015 Aug 7. http://www.justice.gov/crt/overview-title-ix-education-amendments-1972-20-usc-1681-et-seq. Accessed 19 Sep 2015.

  36. Warren MP, Brooks-Gunn J, Hamilton LH. Scoliosis and fractures in young ballet dancers. Relation to delayed menarche and secondary amenorrhea. N Engl J Med. 1986;314(21):1348–53.

    Article  CAS  PubMed  Google Scholar 

  37. Howat PM, Carbo ML, Mills GQ, et al. The influence of diet, body fat, menstrual cycling, and activity upon the bone density of females. J Am Diet Assoc. 1989;89(9):1305–7.

    CAS  PubMed  Google Scholar 

  38. Marcus R, Cann C, Madvig P, et al. Menstrual function and bone mass in elite women distance runners. Ann Intern Med. 1985;102:158–63.

    Article  CAS  PubMed  Google Scholar 

  39. 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.

    Article  CAS  PubMed  Google Scholar 

  40. 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.

    Article  CAS  PubMed  Google Scholar 

  41. Cann CE, Martin MC, Genant HK, et al. Decreased spinal mineral content in amenorrheic women. JAMA. 1984;251:626–9.

    Article  CAS  PubMed  Google Scholar 

  42. Davis C. Cowles MA comparison of weight and diet concerns and personality factors among female athletes and non-athletes. J Psychosom Res. 1989;33(5):527–36.

    Article  CAS  PubMed  Google Scholar 

  43. Pasman LT, Thompson JK. Body image and eating disturbance in obligatory runners, obligatory weightlifters, and sedentary individuals. Int J Eat Disord. 1988;7(6):759–69.

    Article  Google Scholar 

  44. Rosen LW, Hough DO. Pathogenic weight-control behaviors of female college gymnasts. Phys Sportsmed. 1988;16(9):140.

    Article  CAS  PubMed  Google Scholar 

  45. Sundgot-Borgen J. Prevalence of eating disorders in elite female athletes. Int J Sport Nutr. 1993;3(1):29–40.

    Article  CAS  PubMed  Google Scholar 

  46. Benson J, Allemann Y, Theintz G, et al. Eating problems and calorie intake levels in Swiss adolescent athletes. Int J Sports Med. 1990;11(4):249–52.

    Article  CAS  PubMed  Google Scholar 

  47. Sundgot-Borgen J, Larsen S. Pathogenic weight-control methods and self-reported eating disorders in female elite athletes and controls. Scand J Med Sci Sports. 1993;3:150–5.

    Article  Google Scholar 

  48. Warren BJ, Stanton AL, Blessing DL. Disordered eating patterns in competitive female athletes. Int J Eat Disord. 1990;9(5):565–9.

    Article  Google Scholar 

  49. Leichner P. Anorexia nervosa, bulimia and exercise. Coach Rev. 1986;66–8.

  50. Wilkins JA, Boland FJ. A comparison of male and female university athletes and nonathletes on eating disorder indices. J Sport Behav. 1991;14(2):129–43.

    Google Scholar 

  51. Johnson C, Powers PS, Dick R. Athletes and eating disorders: the National Collegiate Athletic Association study. Int J Eat Disord. 1999;26(2):179–88.

    Article  CAS  PubMed  Google Scholar 

  52. Klock SC, DeSouza MJ. Eating disorder characteristics and psychiatric symptomatology of eumenorrheic and amenorrheic runners. Int J Eat Disord. 1995;17(2):161–6.

    Article  CAS  PubMed  Google Scholar 

  53. Rosenvinge JH, Vig C. Eating disorders and associated symptoms among adolescent swimmers. Scand J Med Sci Sports. 1993;3:164–9.

    Article  Google Scholar 

  54. Abraham S. Eating and weight controlling behaviours of young ballet dancers. Psychopathology. 1996;29(4):218–22.

    Article  CAS  PubMed  Google Scholar 

  55. Loucks AB. Energy balance and body composition in sports and exercise. J Sports Sci. 2004;22(1):1–14.

    Article  PubMed  Google Scholar 

  56. Stubbs RJ, Hughes DA, Johnstone AM, et al. Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp. 2004;286:R350–8.

    Article  CAS  Google Scholar 

  57. Gardner DF, Kaplan MM, Stanley CS, et al. The effect of triiodothyronine replacement on the metabolic and pituitary responses to starvation. N Engl J Med. 1979;300:579–84.

    Article  CAS  PubMed  Google Scholar 

  58. Loucks AB, Mortola JF, Girton L, et al. Alterations in the hypothalamic–pituitary–ovarian and the hypothalamic–pituitary–adrenal axes in athletic women. J Clin Endocrinol Metab. 1989;68(2):402–11.

    Article  CAS  PubMed  Google Scholar 

  59. De Souza MJ, Miller B, Loucks A, 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 

  60. Prior JC, Vigna YM, Schechter MT, et al. Spinal bone loss and ovulatory disturbances. N Engl J Med. 1990;323(18):1221–7.

    Article  CAS  PubMed  Google Scholar 

  61. Micklesfield LK, Lambert EV, Fataar AB, et al. Bone mineral density in mature, premenopausal ultramarathon runners. Med Sci Sports Exerc. 1995;27:688–96.

    Article  CAS  PubMed  Google Scholar 

  62. Carmichael KA, Carmichael DH. Bone metabolism and osteopenia in eating disorders. Medicine. 1995;74:254–67.

    Article  CAS  PubMed  Google Scholar 

  63. Lauder TD, Williams MV, Campbell CS, et al. The female athlete triad: prevalence in military women. Mil Med. 1999;164:630–5.

    CAS  PubMed  Google Scholar 

  64. Frusztajer NT, Dhuper S, Warren MP, et al. Nutrition and the incidence of stress fractures in ballet dancers. Am J Clin Nutr. 1990;51(5):779–83.

    CAS  PubMed  Google Scholar 

  65. Rencken ML, Chesnut CH, Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes. JAMA. 1996;276(3):238–40.

    Article  CAS  PubMed  Google Scholar 

  66. Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab. 2002;12:281–93.

    Article  PubMed  Google Scholar 

  67. Bloomberg R. Coach says running affects menstruation. Phys Sportsmed. 1977;5(15):15.

    Article  CAS  PubMed  Google Scholar 

  68. Bullen BA, Skrinar GS, Beitins IZ, et al. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med. 1985;312(21):1349–53.

    Article  CAS  PubMed  Google Scholar 

  69. Loucks A, Heath E. 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 

  70. Loucks A, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol Regul Integr Comp Physiol. 1993;264(5):R924–30.

    CAS  Google Scholar 

  71. Loucks A, Verdun M, Heath E. 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 

  72. Kopp-Woodroffe S, Manore M, Dueck C, et al. Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr. 1999;9(1):70–88.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  74. Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J Clin Endocrinol Metab. 1993;77(3):770–5.

    CAS  PubMed  Google Scholar 

  75. MacDougall J, Webber C, Martin J, et al. Relationship among running mileage, bone density, and serum testosterone in male runners. J Appl Physiol. 1992;73(3):1165–70.

    CAS  PubMed  Google Scholar 

  76. Loucks A, Thurma 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.

    Article  CAS  PubMed  Google Scholar 

  77. Sangenis P, Drinkwater BL, Loucks A, et al.; International Olympic Committee (IOC). Position Stand on the Female Athlete Triad. IOC Medical Commission Working Group Women in Sport. 2005. http://www.olympic.org/Documents/Reports/EN/en_report_917.pdf. Accessed 8 Apr 2016.

  78. De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod. 2004;10(5):433–48.

    Article  Google Scholar 

  79. Otis CL, Drinkwater B, Johnson M, et al. Response: the Female Athlete Triad [letter]. Med Sci Sports Exerc. 1997;29(12):1671.

    Article  Google Scholar 

  80. DiPietro L, Stachenfeld NS. The myth of the female athlete triad. Br J Sports Med. 2006;40(6):490–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Vertinsky P. “Run, Jane, Run”: central tensions in the current debate about enhancing women’s health through exercise. Women Health. 1998;27(4):81–111.

    Article  CAS  PubMed  Google Scholar 

  82. Williams NI, De Souza MJ. Female athlete triad errors and misunderstandings. Med Sci Sports Exerc. 2006;38(5):1021.

    Article  PubMed  Google Scholar 

  83. Loucks AB. Refutation of “the myth of the female athlete triad”. Br J Sports Med. 2007;41:55–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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.

    Article  PubMed  Google Scholar 

  85. 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.

    Article  PubMed  Google Scholar 

  86. Rector RS, Rogers R, Ruebel M, et al. Participation in road cycling vs running is associated with lower bone mineral density in men. Metabolism. 2008;57(2):226–32.

    Article  CAS  PubMed  Google Scholar 

  87. Smathers AM, Bemben MG, Bemben DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009;41(2):290–6.

    Article  PubMed  Google Scholar 

  88. MacKelvie K, Taunton J, McKay H, et al. Bone mineral density and serum testosterone in chronically trained, high mileage 40–55 year old male runners. Br J Sports Med. 2000;34(4):273–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Śliwicka E, Nowak A, Zep W, et al. Bone mass and bone metabolic indices in male master rowers. J Bone Miner Metab. 2015;33(5):540–6.

    Article  PubMed  Google Scholar 

  90. Beatty T, Webner D, Collina SJ. Bone density in competitive cyclists. Curr Sports Med Rep. 2010;9(6):352–5.

    Article  PubMed  Google Scholar 

  91. Beals KA, Manore MM. Nutritional status of female athletes with subclinical eating disorders. J Am Diet Assoc. 1998;98(4):419–25.

    Article  CAS  PubMed  Google Scholar 

  92. Williams NI, Reed JL, Leidy HJ, et al. Estrogen and progesterone exposure is reduced in response to energy deficiency in women aged 25–40 years. Hum Reprod. 2010;25(9):2328–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Sundgot-Borgen J, Larsen S. Nutrient intake of female elite athletes suffering from eating disorders. Int J Sport Nutr. 1993;3:431–42.

    Article  CAS  PubMed  Google Scholar 

  94. Marcos A. The immune system in eating disorders: an overview. Nutrition. 1997;13(10):853–62.

    Article  CAS  PubMed  Google Scholar 

  95. Nieman DC. Exercise and resistance to infection. Can J Physiol Pharmacol. 1998;76(5):573–80.

    Article  CAS  PubMed  Google Scholar 

  96. Hagmar M, Hirschberg AL, Berglund L, et al. Special attention to the weight-control strategies employed by Olympic athletes striving for leanness is required. Clin J Sports Med. 2008;18(1):5–9.

    Article  Google Scholar 

  97. Vogt S, Heinrich L, Schumacher YO, et al. Energy intake and energy expenditure of elite cyclists during preseason training. Int J Sports Med. 2005;26(8):701–6.

    Article  CAS  PubMed  Google Scholar 

  98. 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.

    Article  PubMed  Google Scholar 

  99. Martinsen M, Holme I, Pensgaard AM, et al. The development of the brief eating disorder in athletes questionnaire. Med Sci Sports Exerc. 2014;46(8):1666–75.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Human Nutrition, University of Otago, PO Box 56, Dunedin, New Zealand

    Joanne Slater, Rachel Brown, Rebecca McLay-Cooke & Katherine Black

Authors
  1. Joanne Slater
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachel Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebecca McLay-Cooke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Katherine Black
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katherine Black.

Ethics declarations

Funding

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

Conflict of interest

Joanne Slater, Rachel Brown, Rebecca McLay-Cooke and Katherine Black declare that they have no conflicts of interest relevant to the content of this review.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Slater, J., Brown, R., McLay-Cooke, R. et al. Low Energy Availability in Exercising Women: Historical Perspectives and Future Directions. Sports Med 47, 207–220 (2017). https://doi.org/10.1007/s40279-016-0583-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40279-016-0583-0

Keywords

Search

Navigation