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Amenorrhea Associated With the Female Athlete Triad: Etiology, Diagnosis, and Treatment

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Amenorrhea

Part of the book series: Contemporary Endocrinology ((COE))

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The Female Athlete Triad [1, 2] is a syndrome of interrelated conditions that involves disordered eating, low bone mass, and amenorrhea in physically active women and female athletes. This condition was first described by the American College of Sports Medicine in 1997 [1] and is associated with significant health risks. The condition is most common in women involved in sports that emphasize leanness, such as cross country running, gymnastics, and figure skating [2, 3]; however, this condition also impacts recreationally physically active women [4]. Inadequate nutrition precedes the clinical sequelae of amenorrhea and low bone mass. Nutritional deficits are typically associated with internal and external pressures on these women to maintain a low body weight, and most often present as disordered eating [5–7]. The etiology of amenorrhea in exercising women is secondary to inadequate caloric intake in the face of high exercise-related energy expenditure, resulting in a net energy deficit. The energy deficit, in turn, stimulates compensatory mechanisms such as weight loss and energy conservation that translate to hypothalamic suppression of ovarian function and amenorrhea [6, 8, 9].

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References

  1. Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J (1997) American College of Sports Medicine position stand. The Female Athlete Triad. Med Sci Sports Exerc 29:i–ix

    Article  PubMed  CAS  Google Scholar 

  2. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP (2007) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39:1867–1882

    Article  PubMed  Google Scholar 

  3. Beals KA, Manore MM (2002) Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab 12:281–293

    PubMed  Google Scholar 

  4. De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL (1998) 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 83:4220–4232

    Article  PubMed  Google Scholar 

  5. Beals KA, Manore MM (2000) Behavioral, psychological, and physical characteristics of female athletes with subclinical eating disorders. Int J Sport Nutr Exerc Metab 10:128–143

    PubMed  CAS  Google Scholar 

  6. De Souza MJ, Williams NI (2004) Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod Update 10:433–448

    Article  PubMed  Google Scholar 

  7. Sundgot-Borgen J (1994) Risk and trigger factors for the development of eating disorders in female elite athletes. Med Sci Sports Exerc 26:414–419

    PubMed  CAS  Google Scholar 

  8. Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama A, Cameron JL (2001) Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J Clin Endocrinol Metab 86:5184–5193

    Article  PubMed  CAS  Google Scholar 

  9. Williams NI, Caston-Balderrama AL, Helmreich DL, Parfitt DB, Nosbisch C, Cameron JL (2001) Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea. Endocrinology 142:2381–2389

    Article  PubMed  CAS  Google Scholar 

  10. AAP (2000) American Academy of Pediatrics. Committee on Sports Medicine and Fitness. Medical concerns in the female athlete. Pediatrics 106:610–613

    Article  Google Scholar 

  11. Loucks AB, Thuma JR (2003) Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 88:297–311

    Article  PubMed  CAS  Google Scholar 

  12. De Souza MJ, Hontscharuk R, Olmsted M, Kerr G, Williams NI (2007) Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite 48(3):359–367

    Article  PubMed  Google Scholar 

  13. De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI (2008) The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 43:140–148

    Article  PubMed  CAS  Google Scholar 

  14. De Souza MJ, Williams NI (2005) Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep 4:38–44

    PubMed  Google Scholar 

  15. Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19:1231–1240

    Article  PubMed  Google Scholar 

  16. Cobb KL, Bachrach LK, Greendale G, Marcus R, Neer RM, Nieves J, Sowers MF, Brown BW Jr, Gopalakrishnan G, Luetters C, Tanner HK, Ward B, Kelsey JL (2003) Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 35:711–719

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  18. Feicht CB, Johnson TS, Martin BJ, Sparkes KE, Wagner WW Jr (1978) Secondary amenorrhoea in athletes. Lancet 2:1145–1146

    Article  PubMed  CAS  Google Scholar 

  19. Glass AR, Deuster PA, Kyle SB, Yahiro JA, Vigersky RA, Schoomaker EB (1987) Amenorrhea in Olympic marathon runners. Fertil Steril 48:740–745

    PubMed  CAS  Google Scholar 

  20. Sanborn CF, Martin BJ, Wagner WW Jr (1982) Is athletic amenorrhea specific to runners? Am J Obstet Gynecol 143:859–861

    PubMed  CAS  Google Scholar 

  21. Shangold MM, Levine HS (1982) The effect of marathon training upon menstrual function. Am J Obstet Gynecol 143:862–869

    PubMed  CAS  Google Scholar 

  22. Nichols JF, Rauh MJ, Barrack MT, Barkai HS, Pernick Y (2007) Disordered eating and menstrual irregularity in high school athletes in lean-build and nonlean-build sports. Int J Sport Nutr Exerc Metab 17:364–377

    PubMed  Google Scholar 

  23. Beals KA, Hill AK (2006) The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes. Int J Sport Nutr Exerc Metab 16:1–23

    PubMed  Google Scholar 

  24. Abraham SF, Beumont PJ, Fraser IS, Llewellyn-Jones D (1982) Body weight, exercise and menstrual status among ballet dancers in training. Br J Obstet Gynaecol 89:507–510

    Article  PubMed  CAS  Google Scholar 

  25. Pettersson F, Fries H, Nillius SJ (1973) Epidemiology of secondary amenorrhea. I. Incidence and prevalence rates. Am J Obstet Gynecol 117:80–86

    PubMed  CAS  Google Scholar 

  26. Singh KB (1981) Menstrual disorders in college students. Am J Obstet Gynecol 140:299–302

    PubMed  CAS  Google Scholar 

  27. Bachmann GA, Kemmann E (1982) Prevalence of oligomenorrhea and amenorrhea in a college population. Am J Obstet Gynecol 144:98–102

    PubMed  CAS  Google Scholar 

  28. Baker ER, Mathur RS, Kirk RF, Williamson HO (1981) Female runners and secondary amenorrhea: correlation with age, parity, mileage, and plasma hormonal and sex-hormone-binding globulin concentrations. Fertil Steril 36:183–187

    PubMed  CAS  Google Scholar 

  29. Frisch RE, Wyshak G, Vincent L (1980) Delayed menarche and amenorrhea in ballet dancers. N Engl J Med 303:17–19

    Article  PubMed  CAS  Google Scholar 

  30. Malina RM (1994) Physical growth and biological maturation of young athletes. Exerc Sport Sci Rev 22:389–433

    Article  PubMed  CAS  Google Scholar 

  31. Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG, Hamilton L (2003) Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: a longitudinal study. Fertil Steril 80:398–404

    Article  PubMed  Google Scholar 

  32. Malina RM, Ryan RC, Bonci CM (1994) Age at menarche in athletes and their mothers and sisters. Ann Hum Biol 21:417–422

    Article  PubMed  CAS  Google Scholar 

  33. ASRM (2006) Current evaluation of amenorrhea.The Practice Committee of the American Society of Reproductive Medicine. Fertil Steril 86:S148–S155

    Google Scholar 

  34. Awdishu S, Williams NI, Laredo S, De Souza MJ (2009) Oligomenorrhea in exercising women: a PCOS phenotype or distinct entity? Sports Med 39(12):1055–1069

    Article  PubMed  Google Scholar 

  35. Veldhuis JD, Evans WS, Demers LM, Thorner MO, Wakat D, Rogol AD (1985) Altered neuroendocrine regulation of gonadotropin secretion in women distance runners. J Clin Endocrinol Metab 61:557–563

    Article  PubMed  CAS  Google Scholar 

  36. De Souza MJ, Lee DK, VanHeest JL, Scheid JL, West SL, Williams NI (2007) Severity of energy-related menstrual disturbances increases in proportion to indices of energy conservation in exercising women. Fertil Steril 88:971–975

    Article  PubMed  Google Scholar 

  37. Vescovi JD, Scheid JL, Hontscharuk R, De Souza MJ (2008) Cognitive dietary restraint: impact on bone, menstrual and metabolic status in young women. Physiol Behav 95:48–55

    Article  PubMed  CAS  Google Scholar 

  38. Wade GN, Schneider JE, Li HY (1996) Control of fertility by metabolic cues. Am J Physiol 270:E1–E19

    PubMed  CAS  Google Scholar 

  39. Jasienska G, Ellison PT (1998) Physical work causes suppression of ovarian function in women. Proc Biol Sci 265:1847–1851

    Article  PubMed  CAS  Google Scholar 

  40. Ellison PT (1994) Advances in human reproductive ecology. Annu Rev Anthropol 23:255–275

    Article  PubMed  CAS  Google Scholar 

  41. Ellison PT (2003) Energetics and reproductive effort. Am J Hum Biol 15:342–351

    Article  PubMed  Google Scholar 

  42. Warren MP (1980) The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab 51:1150–1157

    Article  PubMed  CAS  Google Scholar 

  43. Danforth E Jr, Burger A (1984) The role of thyroid hormones in the control of energy expenditure. Clin Endocrinol Metab 13:581–595

    Article  PubMed  CAS  Google Scholar 

  44. Danforth E Jr, Burger AG (1989) The impact of nutrition on thyroid hormone physiology and action. Annu Rev Nutr 9:201–227

    Article  PubMed  CAS  Google Scholar 

  45. De Souza MJ, Leidy HJ, O’Donnell E, Lasley B, Williams NI (2004) Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones. J Clin Endocrinol Metab 89:3536–3542

    Article  PubMed  CAS  Google Scholar 

  46. Laughlin GA, Yen SS (1996) Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 81:4301–4309

    Article  PubMed  CAS  Google Scholar 

  47. Kaufman BA, Warren MP, Dominguez JE, Wang J, Heymsfield SB, Pierson RN (2002) Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels. J Clin Endocrinol Metab 87:2777–2783

    Article  PubMed  CAS  Google Scholar 

  48. Myerson M, Gutin B, Warren MP, May MT, Contento I, Lee M, Pi-Sunyer FX, Pierson RN Jr, Brooks-Gunn J (1991) Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc 23:15–22

    PubMed  CAS  Google Scholar 

  49. De Souza MJ, Van Heest J, Demers LM, Lasley BL (2003) Luteal phase deficiency in recreational runners: evidence for a hypometabolic state. J Clin Endocrinol Metab 88:337–346

    Article  PubMed  Google Scholar 

  50. Leibel RL, Rosenbaum M, Hirsch J (1995) Changes in energy expenditure resulting from altered body weight. N Engl J Med 332:621–628

    Article  PubMed  CAS  Google Scholar 

  51. Harris JA, Benedict FG (1919) A biometric study of the basal metabolism in man. Carnegie Institution of Washington, Washington, D.C., Pub No. 279

    Google Scholar 

  52. Marra M, Polito A, De Filippo E, Cuzzolaro M, Ciarapica D, Contaldo F, Scalfi L (2002) Are the general equations to predict BMR applicable to patients with anorexia nervosa? Eat Weight Disord 7:53–59

    PubMed  CAS  Google Scholar 

  53. Melchior JC, Rigaud D, Rozen R, Malon D, Apfelbaum M (1989) Energy expenditure economy induced by decrease in lean body mass in anorexia nervosa. Eur J Clin Nutr 43:793–799

    PubMed  CAS  Google Scholar 

  54. Polito A, Fabbri A, Ferro-Luzzi A, Cuzzolaro M, Censi L, Ciarapica D, Fabbrini E, Giannini D (2000) Basal metabolic rate in anorexia nervosa: relation to body composition and leptin concentrations. Am J Clin Nutr 71:1495–1502

    PubMed  CAS  Google Scholar 

  55. Loucks AB, Callister R (1993) Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol 264:R924–R930

    PubMed  CAS  Google Scholar 

  56. Loucks AB, Heath EM (1994) Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol 266:R817–R823

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  58. Sanborn CF, Horea M, Siemers BJ, Dieringer KI (2000) Disordered eating and the female athlete triad. Clin Sports Med 19:199–213

    Article  PubMed  CAS  Google Scholar 

  59. Smolak L, Murnen SK, Ruble AE (2000) Female athletes and eating problems: a meta-­analysis. Int J Eat Disord 27:371–380

    Article  PubMed  CAS  Google Scholar 

  60. Garner D (1991) Eating disorder inventory-2 professional manual. Pshychological Assessment Resources, Odessa, FL

    Google Scholar 

  61. Sands R (2000) Reconceptualization of body image and drive for thinness. Int J Eat Disord 28:397–407

    Article  PubMed  CAS  Google Scholar 

  62. Herman CP, Polivy J (1980) Restrained eating. In: Stunkard AJ (ed) Obesity. WB Saunders, Philadelphia, PA, pp 208–225

    Google Scholar 

  63. Van Loan MD, Keim NL (2000) Influence of cognitive eating restraint on total-body measurements of bone mineral density and bone mineral content in premenopausal women aged 18-45 y: a cross-sectional study. Am J Clin Nutr 72:837–843

    PubMed  Google Scholar 

  64. Barr SI, Prior JC, Vigna YM (1994) Restrained eating and ovulatory disturbances: possible implications for bone health. Am J Clin Nutr 59:92–97

    PubMed  CAS  Google Scholar 

  65. Drinkwater BL, Nilson K, Chesnut CH III, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311:277–281

    Article  PubMed  CAS  Google Scholar 

  66. Marcus R, Cann C, Madvig P, Minkoff J, Goddard M, Bayer M, Martin M, Gaudiani L, Haskell W, Genant H (1985) Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med 102:158–163

    PubMed  CAS  Google Scholar 

  67. Nelson ME, Fisher EC, Catsos PD, Meredith CN, Turksoy RN, Evans WJ (1986) Diet and bone status in amenorrheic runners. Am J Clin Nutr 43:910–916

    PubMed  CAS  Google Scholar 

  68. Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, Gupta N, Herzog DB, Klibanski A, Misra M (2008) Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics 121:1127–1136

    Article  PubMed  Google Scholar 

  69. ISCD (2004) Diagnosis of osteoporosis in men, premenopausal women, and children. International Society for Clinical Densitometry Position Development Conference. J Clin Densitom 7:17–26

    Article  Google Scholar 

  70. Gremion G, Rizzoli R, Slosman D, Theintz G, Bonjour JP (2001) Oligo-amenorrheic long-distance runners may lose more bone in spine than in femur. Med Sci Sports Exerc 33:15–21

    PubMed  CAS  Google Scholar 

  71. Tomten SE, Falch JA, Birkeland KI, Hemmersbach P, Hostmark AT (1998) Bone mineral density and menstrual irregularities. A comparative study on cortical and trabecular bone structures in runners with alleged normal eating behavior. Int J Sports Med 19:92–97

    Article  PubMed  CAS  Google Scholar 

  72. Khan KM, Liu-Ambrose T, Sran MM, Ashe MC, Donaldson MG, Wark JD (2002) New ­criteria for female athlete triad syndrome? As osteoporosis is rare, should osteopenia be among the criteria for defining the female athlete triad syndrome? Br J Sports Med 36:10–13

    Article  PubMed  CAS  Google Scholar 

  73. Nattiv A (2000) Stress fractures and bone health in track and field athletes. J Sci Med Sport 3:268–279

    Article  PubMed  CAS  Google Scholar 

  74. Ducher G, Eser P, Hill B, Bass S (2009) History of amenorrhoea compromises some of the exercise-induced benefits in cortical and trabecular bone in the peripheral and axial skeleton: a study in retired elite gymnasts. Bone 45:760–767

    Article  PubMed  CAS  Google Scholar 

  75. Misra M, Prabhakaran R, Miller KK, Goldstein MA, Mickley D, Clauss L, Lockhart P, Cord J, Herzog DB, Katzman DK, Klibanski A (2008) Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-1. J Clin Endocrinol Metab 93:1231–1237

    Article  PubMed  CAS  Google Scholar 

  76. Misra M, Prabhakaran R, Miller KK, Goldstein MA, Mickley D, Clauss L, Lockhart P, Cord J, Herzog DB, Katzman DK, Klibanski A (2008) Prognostic indicators of changes in bone density measures in adolescent girls with anorexia nervosa-II. J Clin Endocrinol Metab 93:1292–1297

    Article  PubMed  CAS  Google Scholar 

  77. Hergenroeder AC, Smith EO, Shypailo R, Jones LA, Klish WJ, Ellis K (1997) Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone, or placebo over 12 months. Am J Obstet Gynecol 176:1017–1025

    Article  PubMed  CAS  Google Scholar 

  78. Zipfel S, Seibel MJ, Lowe B, Beumont PJ, Kasperk C, Herzog W (2001) Osteoporosis in eating disorders: a follow-up study of patients with anorexia and bulimia nervosa. J Clin Endocrinol Metab 86:5227–5233

    Article  PubMed  CAS  Google Scholar 

  79. Welt CK, Chan JL, Bullen J, Murphy R, Smith P, DePaoli AM, Karalis A, Mantzoros CS (2004) Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med 351:987–997

    Article  PubMed  CAS  Google Scholar 

  80. Miller KK, Grinspoon S, Gleysteen S, Grieco KA, Ciampa J, Breu J, Herzog DB, Klibanski A (2004) Preservation of neuroendocrine control of reproductive function despite severe undernutrition. J Clin Endocrinol Metab 89:4434–4438

    Article  PubMed  CAS  Google Scholar 

  81. Thong FS, McLean C, Graham TE (2000) Plasma leptin in female athletes: relationship with body fat, reproductive, nutritional, and endocrine factors. J Appl Physiol 88:2037–2044

    PubMed  CAS  Google Scholar 

  82. Laughlin GA, Yen SS (1997) Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab 82:318–321

    Article  PubMed  CAS  Google Scholar 

  83. Lee NJ, Wong IP, Baldock PA, Herzog H (2008) Leptin as an endocrine signal in bone. Curr Osteoporos Rep 6:62–66

    Article  PubMed  Google Scholar 

  84. Yadav VK, Oury F, Suda N, Liu Z, Gao X, Confavreux C, Klemenhagen KC, Tanaka KF, Gingrich JA, Guo XE, Tecott LH, Mann JJ, Hen R, Horvath TL, Karsenty G (2009) A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 138:976–989

    Google Scholar 

  85. Loucks AB, Laughlin GA, Mortola JF, Girton L, Nelson JC, Yen SS (1992) Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. J Clin Endocrinol Metab 75:514–518

    Article  PubMed  CAS  Google Scholar 

  86. ASRM (2004) Current evaluation of amenorrhea. The Practice Committee of the American Society of Reproductive Medicine. Fertil Steril 82(suppl 1):S33–S39

    Google Scholar 

  87. Vescovi JD, Jamal SA, De Souza MJ (2008) Strategies to reverse bone loss in women with functional hypothalamic amenorrhea: a systematic review of the literature. Osteoporos Int 19:465–478

    Article  PubMed  CAS  Google Scholar 

  88. Warren MP, Chua AT (2008) Exercise-induced amenorrhea and bone health in the adolescent athlete. Ann N Y Acad Sci 1135:244–252

    Article  PubMed  Google Scholar 

  89. Kopp-Woodroffe SA, Manore MM, Dueck CA, Skinner JS, Matt KS (1999) Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr 9:70–88

    PubMed  CAS  Google Scholar 

  90. Dueck CA, Manore MM, Matt KS (1996) Role of energy balance in athletic menstrual ­dysfunction. Int J Sport Nutr 6:165–190

    PubMed  CAS  Google Scholar 

  91. Dueck CA, Matt KS, Manore MM, Skinner JS (1996) Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr 6:24–40

    PubMed  CAS  Google Scholar 

  92. Scheid JL WN, West SL, Awdishu S, De Souza MJ (2008) Increased caloric intake in energy deficient exercising women with functional hypothalamic amenorrhea is associated with decreased ghrelin and increased bone formation: preliminary data from an RCT to reverse exercise-associated menstrual disturbances. J Bone Miner Res 23(S1):S286

    Google Scholar 

  93. Keen AD, Drinkwater BL (1997) Irreversible bone loss in former amenorrheic athletes. Osteoporos Int 7:311–315

    Article  PubMed  CAS  Google Scholar 

  94. Drinkwater BL, Nilson K, Ott S, Chesnut CH III (1986) Bone mineral density after resumption of menses in amenorrheic athletes. JAMA 256:380–382

    Article  PubMed  CAS  Google Scholar 

  95. Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG (2002) Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J Clin Endocrinol Metab 87:3162–3168

    Article  PubMed  CAS  Google Scholar 

  96. Berga SL, Marcus MD, Loucks TL, Hlastala S, Ringham R, Krohn MA (2003) Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril 80:976–981

    Article  PubMed  Google Scholar 

  97. Zanker CL, Cooke CB, Truscott JG, Oldroyd B, Jacobs HS (2004) Annual changes of bone density over 12 years in an amenorrheic athlete. Med Sci Sports Exerc 36:137–142

    Article  PubMed  Google Scholar 

  98. Fredericson M, Kent K (2005) Normalization of bone density in a previously amenorrheic runner with osteoporosis. Med Sci Sports Exerc 37:1481–1486

    Article  PubMed  Google Scholar 

  99. Castelo-Branco C, Vicente JJ, Pons F, Martinez de Osaba MJ, Casals E, Vanrell JA (2001) Bone mineral density in young, hypothalamic oligoamenorrheic women treated with oral contraceptives. J Reprod Med 46:875–879

    PubMed  CAS  Google Scholar 

  100. Cumming DC (1996) Exercise-associated amenorrhea, low bone density, and estrogen replacement therapy. Arch Intern Med 156:2193–2195

    Article  PubMed  CAS  Google Scholar 

  101. De Crée C, Lewin R, Ostyn M (1988) Suitability of cyproterone acetate in the treatment of osteoporosis associated with athletic amenorrhea. Int J Sports Med 9:187–192

    Article  PubMed  Google Scholar 

  102. Miller KK, Lee EE, Lawson EA, Misra M, Minihan J, Grinspoon SK, Gleysteen S, Mickley D, Herzog D, Klibanski A (2006) Determinants of skeletal loss and recovery in anorexia nervosa. J Clin Endocrinol Metab 91:2931–2937

    Article  PubMed  CAS  Google Scholar 

  103. Heer M, Mika C, Grzella I, Heussen N, Herpertz-Dahlmann B (2004) Bone turnover during inpatient nutritional therapy and outpatient follow-up in patients with anorexia nervosa compared with that in healthy control subjects. Am J Clin Nutr 80:774–781

    PubMed  CAS  Google Scholar 

  104. Hotta M, Shibasaki T, Sato K, Demura H (1998) The importance of body weight history in the occurrence and recovery of osteoporosis in patients with anorexia nervosa: evaluation by dual X-ray absorptiometry and bone metabolic markers. Eur J Endocrinol 139:276–283

    Article  PubMed  CAS  Google Scholar 

  105. Compston JE, McConachie C, Stott C, Hannon RA, Kaptoge S, Debiram I, Love S, Jaffa A (2006) Changes in bone mineral density, body composition and biochemical markers of bone turnover during weight gain in adolescents with severe anorexia nervosa: a 1-year prospective study. Osteoporos Int 17:77–84

    Article  PubMed  CAS  Google Scholar 

  106. Bolton JG, Patel S, Lacey JH, White S (2005) A prospective study of changes in bone turnover and bone density associated with regaining weight in women with anorexia nervosa. Osteoporos Int 16:1955–1962

    Article  PubMed  Google Scholar 

  107. Compston JE (2001) Sex steroids and bone. Physiol Rev 81:419–447

    PubMed  CAS  Google Scholar 

  108. Gibson JH, Mitchell A, Reeve J, Harries MG (1999) Treatment of reduced bone mineral density in athletic amenorrhea: a pilot study. Osteoporos Int 10:284–289

    Article  PubMed  CAS  Google Scholar 

  109. Rickenlund A, Carlstrom K, Ekblom B, Brismar TB, Von Schoultz B, Hirschberg AL (2004) Effects of oral contraceptives on body composition and physical performance in female athletes. J Clin Endocrinol Metab 89:4364–4370

    Article  PubMed  CAS  Google Scholar 

  110. Warren MP, Miller KK, Olson WH, Grinspoon SK, Friedman AJ (2005) Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in women with hypothalamic amenorrhea and osteopenia: an open-label extension of a double-blind, placebo-controlled study. Contraception 72:206–211

    Article  PubMed  CAS  Google Scholar 

  111. Khosla S (2002) Leptin-central or peripheral to the regulation of bone metabolism? Endocrinology 143:4161–4164

    Article  PubMed  CAS  Google Scholar 

  112. Jenkins PJ, Ibanez-Santos X, Holly J, Cotterill A, Perry L, Wolman R, Harries M, Grossman A (1993) IGFBP-1: a metabolic signal associated with exercise-induced amenorrhea. Neuroendocrinology 57:600–604

    Article  PubMed  CAS  Google Scholar 

  113. Laughlin GA, Dominguez CE, Yen SS (1998) Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrinol Metab 83:25–32

    Article  PubMed  CAS  Google Scholar 

  114. Grinspoon S, Miller KK, Herzog DB, Grieco KA, Klibanski A (2004) Effects of estrogen and recombinant human insulin-like growth factor-I on ghrelin secretion in severe undernutrition. J Clin Endocrinol Metab 89:3988–3993

    Article  PubMed  CAS  Google Scholar 

  115. Grinspoon S, Miller K, Herzog D, Clemmons D, Klibanski A (2003) Effects of recombinant human insulin-like growth factor (IGF)-I and estrogen administration on IGF-I, IGF binding protein (IGFBP)-2, and IGFBP-3 in anorexia nervosa: a randomized-controlled study. J Clin Endocrinol Metab 88:1142–1149

    Article  PubMed  CAS  Google Scholar 

  116. Grinspoon S, Miller K, Coyle C, Krempin J, Armstrong C, Pitts S, Herzog D, Klibanski A (1999) Severity of osteopenia in estrogen-deficient women with anorexia nervosa and ­hypothalamic amenorrhea. J Clin Endocrinol Metab 84:2049–2055

    Article  PubMed  CAS  Google Scholar 

  117. Haberland CA, Seddick D, Marcus R, Bachrach LK (1995) A physician survey of therapy for exercise-associated amenorrhea: a brief report. Clin J Sport Med 5:246–250

    Article  PubMed  CAS  Google Scholar 

  118. Carlson JL, Curtis M, Halpern-Felsher B (2007) Clinician practices for the management of amenorrhea in the adolescent and young adult athlete. J Adolesc Health 40:362–365

    Article  PubMed  Google Scholar 

  119. Pantano KJ (2009) Strategies used by physical therapists in the U.S. for treatment and ­prevention of the female athlete triad. Phys Ther Sport 10:3–11

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Women’s Health and Exercise Laboratory, Noll Laboratory, Department of Kinesiology, Penn State University, University Park, PA, 16802, USA

    M. J. De Souza

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  1. M. J. De Souza
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  2. R. J. Toombs
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Correspondence to M. J. De Souza .

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  1. , Department of Obstetrics and Gynecology, University of Colorado Denver School of, Academic Office Building 1, Room 4010, Aurora, 80045, Colorado, USA

    Nanette F. Santoro

  2. , Department of Obstetrics and Gynecology, Albert Einstein College of Medicine, 1300 Morris Park Ave, Ullman 1211, Bronx, 10461, New York, USA

    Genevieve Neal-Perry

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De Souza, M.J., Toombs, R.J. (2010). Amenorrhea Associated With the Female Athlete Triad: Etiology, Diagnosis, and Treatment. In: Santoro, N., Neal-Perry, G. (eds) Amenorrhea. Contemporary Endocrinology. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60327-864-5_7

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  • DOI: https://doi.org/10.1007/978-1-60327-864-5_7

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