Current Osteoporosis Reports

, Volume 15, Issue 6, pp 577–587 | Cite as

Current Status of the Female Athlete Triad: Update and Future Directions

  • Mary Jane De Souza
  • Kristen J. Koltun
  • Clara V. Etter
  • Emily A. Southmayd
Nutrition, Exercise, and Lifestyle in Osteoporosis (S Shapses and J Lappe, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Nutrition, Exercise, and Lifestyle in Osteoporosis


Purpose of Review

This review provides an update on the primary clinical sequelae of the Female Athlete Triad.

Recent Findings

Scientific advancements have contributed to improve understanding of Triad-related conditions, including leptin’s role as a potential neuroendocrine link between energy status and reproductive function. Use of finite element analysis of HRpQCT imaging has provided a more accurate assessment of bone geometry and bone strength and may be clinically relevant. New perspectives aimed at developing and implementing a multi-disciplinary, personalized approach in the prevention and early treatment of triad-related symptoms are provided.


The Female Athlete Triad is a multi-dimensional condition that affects active women across the lifespan. Energy availability impacts reproductive function and bone with implications for health and performance. Understanding the contributions of each individual component as well as their interconnected effects is necessary for progression and expansion of the Triad literature.


Female athlete triad Energy availability Menstrual cycle Bone health 


Compliance with Ethical Standards

Conflict of Interest

Kristen Koltun, Clara Etter, Emily Southmayd, and Mary Jane De Souza declare no conflict of interest.

Human and Animal Rights and Informed Consent

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/nation/institutional guidelines).

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance.


  1. 1.
    Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–82. Scholar
  2. 2.
    Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J. American College of Sports Medicine position stand. The Female Athlete Triad. Med Sci Sports Exerc. 1997;29(5):i–ix.CrossRefPubMedGoogle Scholar
  3. 3.
    •• 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(4):289. This consensus statement, composed by an international, multidisciplinary team of scientists and clinicians comprising the Female Athlete Triad Coalition, is the only resource published to date that relies on current evidence-based knowledge to offer specific recommendations for the screening, diagnosis, and treatment, as well as detailed return to play guidelines for the Female Athlete Triad. CrossRefPubMedGoogle Scholar
  4. 4.
    •• 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, CA, May 2012, and 2nd International Conference held in Indianapolis, IN, May 2013. Clin J Sport Med. 2014;24(2):96–119. This consensus statement, composed by an international, multidisciplinary team of scientists and clinicians comprising the Female Athlete Triad Coalition, is the only resource published to date that relies on current evidence-based knowledge to offer specific recommendations for the screening, diagnosis, and treatment, as well as detailed return to play guidelines for the Female Athlete Triad. PubMedGoogle Scholar
  5. 5.
    Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab. 2002;12(3):281–93.CrossRefPubMedGoogle Scholar
  6. 6.
    De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, 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. Scholar
  7. 7.
    De Souza MJ, Toombs RJ, Scheid JL, O’Donnell E, West SL, Williams NI. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod. 2010;25(2):491–503. Scholar
  8. 8.
    Southmayd EA, Hellmers AC, De Souza MJ. Food versus Pharmacy: assessment of nutritional and pharmacological strategies to improve bone health in energy-deficient exercising women. Curr Osteoporos Rep. 2017;
  9. 9.
    Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc. 2013;45(5):985–96. Scholar
  10. 10.
    Baker ER, Mathur RS, Kirk RF, Williamson HO. Female runners and secondary amenorrhea: correlation with age, parity, mileage, and plasma hormonal and sex-hormone-binding globulin concentrations. Fertil Steril. 1981;36(2):183–7.CrossRefPubMedGoogle Scholar
  11. 11.
    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(7):491–7. Scholar
  12. 12.
    Rosano GM, Spoletini I, Vitale C. Cardiovascular disease in women, is it different to men? The role of sex hormones. Climacteric. 2017;20(2):125–8. Scholar
  13. 13.
    De Souza MJ, Williams NI, Nattiv A, Joy E, Misra M, Loucks AB, 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. Scholar
  14. 14.
    Loucks AB. Energy availability, not body fatness, regulates reproductive function in women. [Review] [15 refs]. Exerc Sport Sci Rev. 2003;31(3):144.CrossRefPubMedGoogle Scholar
  15. 15.
    Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37(4–5):348–52. 37NaN19 CrossRefPubMedGoogle Scholar
  16. 16.
    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. Scholar
  17. 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. Scholar
  18. 18.
    Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16(2):235–72.CrossRefPubMedGoogle Scholar
  19. 19.
    Danforth E Jr, Burger AG. The impact of nutrition on thyroid hormone physiology and action. Annu Rev Nutr. 1989;9:201–27.CrossRefPubMedGoogle Scholar
  20. 20.
    De Souza MJ, Leidy HJ, O’Donnell E, Lasley B, Williams NI. Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones. J Clin Endocrinol Metab. 2004;89(7):3536–42. Scholar
  21. 21.
    Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab. 1996;81(12):4301–9.PubMedGoogle Scholar
  22. 22.
    Scheid JL, Toombs RJ, Ducher G, Gibbs JC, Williams NI, De Souza MJ. Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. Bone. 2011;49(2):194–201. Scholar
  23. 23.
    De Souza MJ, Lee DK, VanHeest JL, Scheid JL, West SL, Williams NI. Severity of energy-related menstrual disturbances increases in proportion to indices of energy conservation in exercising women. Fertil Steril. 2007;88(4):971–5. Scholar
  24. 24.
    Dominguez CE, Laughlin GA, Nelson JC, Yen SS. Altered binding of serum thyroid hormone to thyroxine-binding globulin in women with functional hypothalamic amenorrhea. Fertil Steril. 1997;68(6):992–6.CrossRefPubMedGoogle Scholar
  25. 25.
    Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Phys. 1993;264(5 Pt 2):R924–30.Google Scholar
  26. 26.
    Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Phys. 1994;266(3 Pt 2):R817–23.Google Scholar
  27. 27.
    Koehler K, Williams NI, Mallinson RJ, Southmayd EA, Allaway HC, De Souza MJ. Low resting metabolic rate in exercise-associated amenorrhea is not due to a reduced proportion of highly active metabolic tissue compartments. Am J Physiol Endocrinol Metab. 2016;311(2):E480–7. Scholar
  28. 28.
    De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone. 2008;43(1):140–8. Scholar
  29. 29.
    De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep. 2005;4(1):38–44.CrossRefPubMedGoogle Scholar
  30. 30.
    Mallinson RJ, Williams NI, Hill BR, De Souza MJ. Body composition and reproductive function exert unique influences on indices of bone health in exercising women. Bone. 2013;56(1):91–100. Scholar
  31. 31.
    De Souza MJ, Toombs RJ. Amenorrhea associated with the female athlete triad: etiology, diagnosis, and treatment. In: Santoro N, editor. Amenorrhea: A case-Based, Clinical Guide. Springer Science+Business Media, LLC. Humana Press, New York; 2010.Google Scholar
  32. 32.
    Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332(10):621–8.CrossRefPubMedGoogle Scholar
  33. 33.
    Deuster PA, Kyle SB, Moser PB, Vigersky RA, Singh A, Schoomaker EB. Nutritional intakes and status of highly trained amenorrheic and eumenorrheic women runners. Fertil Steril. 1986;46(4):636–43.CrossRefPubMedGoogle Scholar
  34. 34.
    Kaiserauer S, Snyder AC, Sleeper M, Zierath J. Nutritional, physiological, and menstrual status of distance runners. Med Sci Sports Exerc. 1989;21(2):120–5.CrossRefPubMedGoogle Scholar
  35. 35.
    Myerson M, Gutin B, Warren MP, May MT, Contento I, Lee M, et al. Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc. 1991;23(1):15–22.CrossRefPubMedGoogle Scholar
  36. 36.
    Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985). 1998;84(1):37–46.Google Scholar
  37. 37.
    Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders in female elite athletes. Med Sci Sports Exerc. 1994;26(4):414–9.CrossRefPubMedGoogle Scholar
  38. 38.
    • 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(3):154–62. The paper provides an update on the epidemiology, diagnostics, and treatment of eating disorders among athletes, elucidating the necessity for multidisciplinary approaches among sports medicine professionals when evaluating athletes suffering from eating disorders. CrossRefPubMedGoogle Scholar
  39. 39.
    Shriver LH, Wollenberg G, Gates GE. Prevalence of disordered eating and its association with emotion regulation in female college athletes. Int J Sport Nutr Exerc Metab. 2016;26(3):240–8. Scholar
  40. 40.
    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(1):25–32.CrossRefPubMedGoogle Scholar
  41. 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. Scand J Med Sci Sports. 2008;18(1):108–18. Scholar
  42. 42.
    Reinking MF, Alexander LE. Prevalence of disordered-eating behaviors in undergraduate female collegiate athletes and non athletes. J Athl Train. 2005;40(1):47–51.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Nichols JF, Rauh MJ, Barrack MT, Barkai H-S, Pernick Y. Disordered eating and menstrual irregularity in high school athletes in lean-build and nonlean-build sports. Int J Sport Nutr Exerc Metab. 2007;17(4):364–77.CrossRefPubMedGoogle Scholar
  44. 44.
    Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS. Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med. 2006;160(2):137–42. Scholar
  45. 45.
    Bonci CM, Bonci LJ, Granger LR, Johnson CL, Malina RM, Milne LW, et al. National Athletic Trainers’ Association position statement: preventing, detecting, and managing disordered eating in athletes. J Athl Train. 2008;43(1):80–108.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Rosen LW, McKeag DB, Hough DO, Curley V. Pathogenic weight-control behavior in female athletes. Phys Sportsmed. 1986;14(1):79–86. Scholar
  47. 47.
    Bardone-Cone AM, Wonderlich SA, Frost RO, Bulik CM, Mitchell JE, Uppala S, et al. Perfectionism and eating disorders: current status and future directions. Clin Psychol Rev. 2007;27(3):384–405. Scholar
  48. 48.
    Beals KA, Manore MM. Behavioral, psychological, and physical characteristics of female athletes with subclinical eating disorders. Int J Sport Nutr Exerc Metab. 2000;10(2):128–43.CrossRefPubMedGoogle Scholar
  49. 49.
    Torstveit MK, Sundgot-Borgen J. Participation in leanness sports but not training volume is associated with menstrual dysfunction: a national survey of 1276 elite athletes and controls. Br J Sports Med. 2005;39(3):141–7. Scholar
  50. 50.
    Gibbs JC, Williams NI, Mallinson RJ, Reed JL, Rickard AD, De Souza MJ. Effect of high dietary restraint on energy availability and menstrual status. Med Sci Sports Exerc. 2013;45(9):1790–7. Scholar
  51. 51.
    Vescovi JD, Scheid JL, Hontscharuk R, De Souza MJ. Cognitive dietary restraint: impact on bone, menstrual and metabolic status in young women. Physiol Behav. 2008;95(1–2):48–55. Scholar
  52. 52.
    Stunkard AJ, Messick S. The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res. 1985;29(1):71–83.CrossRefPubMedGoogle Scholar
  53. 53.
    De Souza MJ, Hontscharuk R, Olmsted M, Kerr G, Williams NI. Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite. 2007;48(3):359–67. Scholar
  54. 54.
    Veldhuis JD, Evans WS, Demers LM, Thorner MO, Wakat D, Rogol AD. Altered neuroendocrine regulation of gonadotropin secretion in women distance runners. J Clin Endocrinol Metab. 1985;61(3):557–63.CrossRefPubMedGoogle Scholar
  55. 55.
    Gordon CM, Ackerman KE, Berga SL, Kaplan JR, Mastorakos G, Misra M, et al. Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2017;
  56. 56.
    Current evaluation of amenorrhea. Fertil Steril. 2008;90(5 Suppl):S219–25.
  57. 57.
    De Souza MJ. Menstrual disturbances in athletes: a focus on luteal phase defects. Med Sci Sports Exerc. 2003;35(9):1553–63. Scholar
  58. 58.
    McNeely MJ, Soules MR. The diagnosis of luteal phase deficiency: a critical review. Fertil Steril. 1988;50(1):1–15.CrossRefPubMedGoogle Scholar
  59. 59.
    Soules MR, McLachlan RI, Ek M, Dahl KD, Cohen NL, Bremner WJ. Luteal phase deficiency: characterization of reproductive hormones over the menstrual cycle. J Clin Endocrinol Metab. 1989;69(4):804–12. Scholar
  60. 60.
    Ellison PT. Advances in human reproductive ecology. Annu Rev Anthropol. 1994;23:255–75. Scholar
  61. 61.
    Ellison PT. Energetics and reproductive effort. Am J Hum Biol. 2003;15(3):342–51. Scholar
  62. 62.
    Panter-Brick C, Lotstein DS, Ellison PT. Seasonality of reproductive function and weight loss in rural Nepali women. Hum Reprod. 1993;8(5):684–90.CrossRefPubMedGoogle Scholar
  63. 63.
    Jasienska G, Ellison PT. Energetic factors and seasonal changes in ovarian function in women from rural Poland. Am J Hum Biol. 2004;16(5):563–80. Scholar
  64. 64.
    Ellison PT, Peacock NR, Lager C. Salivary progesterone and luteal function in two low-fertility populations of Northeast Zaire. Hum Biol. 1986;58(4):473–83.PubMedGoogle Scholar
  65. 65.
    Williams NI, Caston-Balderrama AL, Helmreich DL, Parfitt DB, Nosbisch C, Cameron JL. 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.CrossRefPubMedGoogle Scholar
  66. 66.
    Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama A, Cameron JL. 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. Scholar
  67. 67.
    • Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, De Souza MJ. 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. This is the first study to describe a dose-response relationship between the magnitude of energy deficiency, induced by the abrupt onset of exercise and caloric restriction, and the frequency of exercise-related menstrual disturbances during a three-month randomized control trial in young, sedentary women. CrossRefPubMedGoogle Scholar
  68. 68.
    Mantzoros CS, Magkos F, Brinkoetter M, Sienkiewicz E, Dardeno TA, Kim SY, et al. Leptin in human physiology and pathophysiology. Am J Physiol Endocrinol Metab. 2011;301(4):E567–84. Scholar
  69. 69.
    Laughlin GA, Yen SS. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab. 1997;82(1):318–21.CrossRefPubMedGoogle Scholar
  70. 70.
    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(1):E43–9.PubMedGoogle Scholar
  71. 71.
    Welt CK, Chan JL, Bullen J, Murphy R, Smith P, DePaoli AM, et al. Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med. 2004;351(10):987–97. Scholar
  72. 72.
    Drinkwater BL, Nilson K, Chesnut CH 3rd, Bremner WJ, Shainholtz S, Southworth MB. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med. 1984;311(5):277–81. Scholar
  73. 73.
    Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, et al. Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone. 2012;51(4):680–7. Scholar
  74. 74.
    Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab. 2011;96(10):3123–33. Scholar
  75. 75.
    • 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; This investigation uniquely described the effect of a single Triad risk factor and combinations of 2 and 3 Triad risk factors on the incidence of bone stress injuries in exercising adolescent girls and women, thereby informing evidence-based clinical assessment of injury risk in this population.
  76. 76.
    • Mallinson RJ, Williams NI, Gibbs JC, Koehler K, Allaway HC, Southmayd E, et al. Current and past menstrual status is an important determinant of femoral neck geometry in exercising women. Bone. 2016;88:101–12. Building upon the classic work of Dr. Drinkwater, this study described the cumulative effect of current and past menstrual irregularity on femoral neck geometry, highlighting the persistent and significant detriment of estrogen deficiency on bone strength estimates. CrossRefPubMedGoogle Scholar
  77. 77.
    Nattiv A. Stress fractures and bone health in track and field athletes. J Sci Med Sport. 2000;3(3):268–79.CrossRefPubMedGoogle Scholar
  78. 78.
    Radetti G, Rigon F, Tonini G, Tato L, Bernasconi S, Bona G, et al. Geometry and bone density. Panminerva Med. 2006;48(3):181–6.PubMedGoogle Scholar
  79. 79.
    Barrack MT, Rauh MJ, Nichols JF. Prevalence of and traits associated with low BMD among female adolescent runners. Med Sci Sports Exerc. 2008;40(12):2015–21. Scholar
  80. 80.
    Goolsby MA, Barrack MT, Nattiv A. A displaced femoral neck stress fracture in an amenorrheic adolescent female runner. Sports Health. 2012;4(4):352–6. Scholar
  81. 81.
    Okamoto S, Arai Y, Hara K, Tsuzihara T, Kubo T. A displaced stress fracture of the femoral neck in an adolescent female distance runner with female athlete triad: a case report. Sports Med Arthrosc Rehabil Ther Technol. 2010;2:6. Scholar
  82. 82.
    • Gibbs JC, Nattiv A, Barrack MT, Williams NI, Rauh MJ, Nichols JF, et al. Low bone density risk is higher in exercising women with multiple triad risk factors. Med Sci Sports Exerc. 2014;46(1):167–76. This investigation uniquely described the effect of a single Triad risk factor and a combination of 2 and 3 Triad risk factors on bone health, identifying specific energetic and menstrual factors that are associated with low bone mineral density in exercising adolescent girls and women. CrossRefPubMedGoogle Scholar
  83. 83.
    Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest. 2006;116(5):1186–94. Scholar
  84. 84.
    • Southmayd EA, Mallinson RJ, Williams NI, Mallinson DJ, De Souza MJ, et al. Osteoporos Int. 2016; This is the first study to isolate the contribution of energy status versus estrogen status on volumetric bone mineral density, bone geometry, and estimated bone strength in exercising women with and without menstrual disturbances.
  85. 85.
    Guntur AR, Rosen CJ. IGF-1 regulation of key signaling pathways in bone. Bonekey Rep. 2013;2:437. Scholar
  86. 86.
    Cornish J, Callon KE, Bava U, Lin C, Naot D, Hill BL, et al. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol. 2002;175(2):405–15.CrossRefPubMedGoogle Scholar
  87. 87.
    Combs CE, Nicholls JJ, Duncan Bassett JH, Williams GR. Thyroid hormones and bone development. Minerva Endocrinol. 2011;36(1):71–85.PubMedGoogle Scholar
  88. 88.
    Vescovi JD, VanHeest JL. Case study: impact of inter- and intra-day energy parameters on bone health, menstrual function, and hormones in an elite junior female triathlete. Int J Sport Nutr Exe. 2016;26(4):363–9. Scholar
  89. 89.
    Deutz RC, Benardot D, Martin DE, Cody MM. Relationship between energy deficits and body composition in elite female gymnasts and runners. Med Sci Sports Exerc. 2000;32(3):659–68. Scholar
  90. 90.
    Benardet D. Timing of energy and fluid intake: new concepts for weight control and hydration. ACSMs Health Fit J. 2007;11(4):13–9. Scholar
  91. 91.
    Vanheest JL, Rodgers CD, Mahoney CE, De Souza MJ. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46(1):156–66. Scholar
  92. 92.
    Muia EN, Wright HH, Onywera VO, Kuria EN. Adolescent elite Kenyan runners are at risk for energy deficiency, menstrual dysfunction and disordered eating. J Sports Sci. 2016;34(7):598–606. Scholar
  93. 93.
    Quah YV, Poh BK, Ng LO, Noor MI. The female athlete triad among elite Malaysian athletes: prevalence and associated factors. Asia Pac J Clin Nutr. 2009;18(2):200–8.PubMedGoogle Scholar
  94. 94.
    Movaseghi S, Dadgostar H, Dahaghin S, Chimeh N, Alenabi T, Dadgostar E, et al. Clinical manifestations of the female athlete triad among some Iranian athletes. Med Sci Sports Exerc. 2012;44(5):958–65. Scholar
  95. 95.
    Schtscherbyna A, Soares EA, de Oliveira FP, Ribeiro BG. Female athlete triad in elite swimmers of the city of Rio de Janeiro, Brazil. Nutrition. 2009;25(6):634–9. Scholar
  96. 96.
    Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sports Med. 2016;46(2):171–82. Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Mary Jane De Souza
    • 1
  • Kristen J. Koltun
    • 2
  • Clara V. Etter
    • 2
  • Emily A. Southmayd
    • 2
  1. 1.Department of Kinesiology and Physiology Women’s Health and Exercise Lab, 104 Noll Laboratory, College of Health and Human DevelopmentThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Kinesiology Women’s Health and Exercise Lab, College of Health and Human DevelopmentThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations