Skip to main content

Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function

  • Chapter
  • First Online:
Endocrinology of Physical Activity and Sport

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

Abstract

This chapter begins with a brief description of our current understanding of the female athlete triad. It explains what had been the three most widely held hypotheses about the cause of the triad, and then summarizes the prospective clinical experiments that identified low energy availability as the specific cause. Exercise was found to have no suppressive effect on reproductive function beyond the impact of its energy cost on energy availability, and the suppression was found to occur abruptly below a threshold of 30 kcal per kilogram of fat-free mass per day. The chapter closes by identifying four distinct origins of low energy availability among female athletes, and stresses the importance of identifying the particular origin in each case of the triad before attempting to modify that athlete’s diet and exercise behavior.

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

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  2. 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:i–ix.

    Article  PubMed  CAS  Google Scholar 

  3. Frisch RE, McArthur JW. Menstrual cycles: fatness as determinant of minimum weight for height necessary for their maintenance or onset. Science. 1974;185:949–51.

    Article  PubMed  CAS  Google Scholar 

  4. Frisch RE, Revelle R. Height and weight at menarche and a hypothesis of menarche. Arch Dis Child. 1971;46:695–701.

    Article  PubMed  CAS  Google Scholar 

  5. Schneider JE, Wade GN. Control of fertility by metabolic cues—reply. Am J Physiol Endocrinol Metab. 1997;273:E231–2.

    CAS  Google Scholar 

  6. Crist DM, Hill JM. Diet and insulin like growth factor I in relation to body composition in women with exercise-induced hypothalamic amenorrhea. J Am Coll Nutr. 1990;9:200–4.

    PubMed  CAS  Google Scholar 

  7. Bronson FH, Manning JM. The energetic regulation of ovulation: a realistic role for body fat. Biol Reprod. 1991;44:945–50.

    Article  PubMed  CAS  Google Scholar 

  8. Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc. 1985;17:56–72.

    PubMed  CAS  Google Scholar 

  9. Scott EC, Johnston FE. Critical fat, menarche, and the maintenance of menstrual cycles: a critical review. J Adolesc Health Care. 1982;2:249–60.

    Article  PubMed  CAS  Google Scholar 

  10. Sinning WE, Little KD. Body composition and menstrual function in athletes. Sports Med. 1987;4:34–45.

    Article  PubMed  CAS  Google Scholar 

  11. Loucks AB, Horvath SM, Freedson PS. Menstrual status and validation of body fat prediction in athletes. Hum Biol. 1984;56:383–92.

    PubMed  CAS  Google Scholar 

  12. Bronson FH. Food-restricted, prepubertal, female rats: rapid recovery of luteinizing hormone pulsing with excess food, and full recovery of pubertal development with gonadotropin-releasing hormone. Endocrinology. 1986;118:2483–7.

    Article  PubMed  CAS  Google Scholar 

  13. Di Carlo C, Palomba S, De Fazio M, et al. Hypogonadotropic hypogonadotropism in obese women after biliopancreatic diversion. Fertil Steril. 1999;72:905–9.

    Article  PubMed  Google Scholar 

  14. Zhang Y, Proenca R, Maffei M, et al. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372:425–32.

    Article  PubMed  CAS  Google Scholar 

  15. Considine RV, Sinha MK, Heiman ML, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334:292–5.

    Article  PubMed  CAS  Google Scholar 

  16. Tena-Sempere M. Roles of ghrelin and leptin in the control of reproductive function. Neuroendocrinology. 2007;86:229–41.

    Article  PubMed  CAS  Google Scholar 

  17. Castellano JM, Bentsen AH, Mikkelsen JD, et al. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res. 2010;1364:129–38.

    Article  PubMed  CAS  Google Scholar 

  18. Chou SH, Chamberland JP, Liu X, et al. Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci U S A. 2011;108:6585–90.

    Article  PubMed  CAS  Google Scholar 

  19. Ma Z, Gingerich RL, Santiago JV, et al. Radioimmunoassay of leptin in human plasma. Clin Chem. 1996;42:942–6.

    PubMed  CAS  Google Scholar 

  20. Laughlin GA, Yen SSC. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab. 1997;82:318–21.

    Article  PubMed  CAS  Google Scholar 

  21. Mantzoros C, Flier JS, Lesem MD, et al. Cerebrospinal fluid leptin in anorexia nervosa: correlation with nutritional status and potential role in resistance to weight gain. J Clin Endocrinol Metab. 1997;82:1845–51.

    Article  PubMed  CAS  Google Scholar 

  22. Miller KK, Parulekar MS, Schoenfeld E, et al. Decreased leptin levels in normal weight women with hypothalamic amenorrhea: the effects of body composition and nutritional intake. J Clin Endocrinol Metab. 1998;83:2309–12.

    Article  PubMed  CAS  Google Scholar 

  23. Jimerson DC, Mantzoros C, Wolfe BE, et al. Decreased serum leptin in bulimia nervosa. J Clin Endocrinol Metab. 2000;85:4511–4.

    Article  PubMed  CAS  Google Scholar 

  24. 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.

    PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  CAS  Google Scholar 

  26. Loucks AB. The response of luteinizing hormone pulsatility to five days of low energy availability disappears by 14 years of gynecological age. J Clin Endocrinol Metab. 2006;91:3158–64.

    Article  PubMed  CAS  Google Scholar 

  27. Berga SL, Marcus MD, Loucks TL, et al. Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril. 2003;80:976–81.

    Article  PubMed  Google Scholar 

  28. Kolaczynski JW, Considine RV, Ohannesian J, et al. Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves. Diabetes. 1996;45:1511–5.

    Article  PubMed  CAS  Google Scholar 

  29. Kolaczynski JW, Ohannesian JP, Considine RV, et al. Response of leptin to short-term and prolonged overfeeding in humans. J Clin Endocrinol Metab. 1996;81:4162–5.

    Article  PubMed  CAS  Google Scholar 

  30. Weigle DS, Duell PB, Connor WE, et al. Effect of fasting, refeeding, and dietary fat restriction on plasma leptin levels. J Clin Endocrinol Metab. 1997;82:561–5.

    Article  PubMed  CAS  Google Scholar 

  31. Jenkins AB, Markovic TP, Fleury A, et al. Carbohydrate intake and short-term regulation of leptin in humans. Diabetologia. 1997;40:348–51.

    Article  PubMed  CAS  Google Scholar 

  32. Wang J, Liu R, Hawkins M, et al. A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature. 1998;393:684–8.

    Article  PubMed  CAS  Google Scholar 

  33. Warren MP. The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab. 1980;51:1150–7.

    Article  PubMed  CAS  Google Scholar 

  34. Winterer J, Cutler Jr GB, Loriaux DL. Caloric balance, brain to body ratio, and the timing of menarche. Med Hypotheses. 1984;15:87–91.

    Article  PubMed  CAS  Google Scholar 

  35. Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16:235–72.

    Article  PubMed  CAS  Google Scholar 

  36. Bronson FH, Heideman PD. Seasonal regulation of reproduction in mammals. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven; 1994. p. 541–83.

    Google Scholar 

  37. Bronson FH, Manning J. Food consumption, prolonged exercise, and LH secretion in the peripubertal female rat. In: Pirke KM, Wuttle W, Schweiger U, editors. The menstrual cycle and its disorders. Berlin: Springer; 1989. p. 42–9.

    Chapter  Google Scholar 

  38. Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol. 1996;270:E1–19.

    PubMed  CAS  Google Scholar 

  39. Furman M, Wade GN. Animal models in the study of nutritional infertility. Curr Opin Endocrinol Diabetes Obes. 2007;14:475–81.

    Article  PubMed  Google Scholar 

  40. Laughlin GA, Yen SSC. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab. 1996;81:4301–9.

    Article  PubMed  CAS  Google Scholar 

  41. Myerson M, Gutin B, Warren MP, et al. Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc. 1991;23:15–22.

    PubMed  CAS  Google Scholar 

  42. Loucks AB, Laughlin GA, Mortola JF, et al. Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. J Clin Endocrinol Metab. 1992;75:514–8.

    Article  PubMed  CAS  Google Scholar 

  43. 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;68:402–11.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  45. Kaiserauer S, Snyder AC, Sleeper M, et al. Nutritional, physiological, and menstrual status of distance runners. Med Sci Sports Exerc. 1989;21:120–5.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  47. Nelson ME, Fisher EC, Catsos PD, et al. Diet and bone status in amenorrheic runners. Am J Clin Nutr. 1986;43:910–6.

    PubMed  CAS  Google Scholar 

  48. Edwards JE, Lindeman AK, Mikesky AE, et al. Energy balance in highly trained female endurance runners. Med Sci Sports Exerc. 1993;25:1398–404.

    PubMed  CAS  Google Scholar 

  49. Wilmore JH, Wambsgans KC, Brenner M, et al. Is there energy conservation in amenorrheic compared with eumenorrheic distance runners? J Appl Physiol. 1992;72:15–22.

    PubMed  CAS  Google Scholar 

  50. Mertz W, Tsui JC, Judd JT, et al. What are people really eating? The relation between energy intake derived from estimated diet records and intake determined to maintain body weight. Am J Clin Nutr. 1991;54:291–5.

    PubMed  CAS  Google Scholar 

  51. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332:621–8.

    Article  PubMed  CAS  Google Scholar 

  52. Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod. 1991;45:523–32.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  54. Asahina K, Kitahara F, Yamanaka M, et al. Influence of excessive exercise on the structure and function of rat organs. Jpn J Physiol. 1959;9:322–6.

    Article  PubMed  CAS  Google Scholar 

  55. Axelson JF. Forced swimming alters vaginal estrous cycles, body composition, and steroid levels without disrupting lordosis behavior or fertility in rats. Physiol Behav. 1987;41:471–9.

    Article  PubMed  CAS  Google Scholar 

  56. Chatterton Jr RT, Hartman AL, Lynn DE, et al. Exercise-induced ovarian dysfunction in the rat. Proc Soc Exp Biol Med. 1990;193:220–4.

    PubMed  CAS  Google Scholar 

  57. Manning JM, Bronson FH. Effects of prolonged exercise on puberty and luteinizing hormone secretion in female rats. Am J Physiol. 1989;257:R1359–64.

    PubMed  CAS  Google Scholar 

  58. Manning JM, Bronson FH. Suppression of puberty in rats by exercise: effects on hormone levels and reversal with GnRH infusion. Am J Physiol. 1991;260:R717–23.

    PubMed  CAS  Google Scholar 

  59. De Souza MJ, Maguire MS, Maresh CM, et al. Adrenal activation and the prolactin response to exercise in eumenorrheic and amenorrheic runners. J Appl Physiol. 1991;70:2378–87.

    PubMed  Google Scholar 

  60. De Souza MJ, Luciano AA, Arce JC, et al. Clinical tests explain blunted cortisol responsiveness but not mild hypercortisolism in amenorrheic runners. J Appl Physiol. 1994;76:1302–9.

    PubMed  Google Scholar 

  61. Ding J-H, Scheckter CB, Drinkwater BL, et al. High serum cortisol levels in exercise-associated amenorrhea. Ann Intern Med. 1988;108:530–4.

    PubMed  CAS  Google Scholar 

  62. Suh BY, Liu JH, Berga SL, et al. Hypercortisolism in patients with functional hypothalamic-­amenorrhea. J Clin Endocrinol Metab. 1988;66:733–9.

    Article  PubMed  CAS  Google Scholar 

  63. Gold PW, Gwirtsman H, Averinos PC, et al. Abnormal hypothalamic-pituitary-adrenal function in anorexia nervosa: pathophysiologic mechanisms in underweight and weight-corrected patients. N Engl J Med. 1986;314:1335–42.

    Article  PubMed  CAS  Google Scholar 

  64. Slentz CA, Davis JM, Settles DL, et al. Glucose feedings and exercise in rats: glycogen use, hormone responses, and performance. J Appl Physiol. 1990;69:989–94.

    PubMed  CAS  Google Scholar 

  65. Tabata I, Ogita F, Miyachi M, et al. Effect of low blood glucose on plasm CRF, ACTH, and cortisol during prolonged physical exercise. J Appl Physiol. 1991;71:1807–12.

    PubMed  CAS  Google Scholar 

  66. Bonen A. Recreational exercise does not impair menstrual cycles: a prospective study. Int J Sports Med. 1992;13:110–20.

    Article  PubMed  CAS  Google Scholar 

  67. Boyden TW, Pamenter RW, Stanforth P, et al. Sex steroids and endurance running in women. Fertil Steril. 1983;39:629–32.

    PubMed  CAS  Google Scholar 

  68. Bullen BA, Skrinar GS, Beitins IZ, et al. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J Appl Physiol. 1984;56:1453–63.

    PubMed  CAS  Google Scholar 

  69. Rogol AD, Weltman JY, Evans WS, et al. Long-term endurance training alters the hypothalamic-­pituitary axes for gonadotropins and growth hormone. Endocrinol Metab Clin North Am. 1992;21:817–32.

    PubMed  CAS  Google Scholar 

  70. Loucks AB, Cameron JL, De Souza MJ. Subject assignment may have biased exercise results. J Appl Physiol. 1993;74:2045–7.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  72. Williams NI, Young JC, McArthur JW, et al. Strenuous exercise with caloric restriction: effect on luteinizing hormone secretion. Med Sci Sports Exerc. 1995;27:1390–8.

    PubMed  CAS  Google Scholar 

  73. Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol. 1993;264:R924–30.

    PubMed  CAS  Google Scholar 

  74. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol. 1994;266:R817–23.

    PubMed  CAS  Google Scholar 

  75. Loucks AB, Heath EM. Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J Clin Endocrinol Metab. 1994;78:910–5.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  77. Loucks AB, Verdun M. Slow restoration of LH pulsatility by refeeding in energetically disrupted women. Am J Physiol. 1998;275:R1218–26.

    PubMed  CAS  Google Scholar 

  78. Loucks A. Is stress measured in joules? Military Psychol. 2009;21:S101–7.

    Article  Google Scholar 

  79. Treloar AE, Boynton RE, Behn BG, et al. Variation of the human menstrual cycle through reproductive life. Int J Fertil. 1967;12:77–126.

    PubMed  CAS  Google Scholar 

  80. Olson BR, Cartledge T, Sebring N, et al. Short-term fasting affects luteinizing hormone secretory dynamics but not reproductive function in normal-weight sedentary women. J Clin Endocrinol Metab. 1995;80:1187–93.

    Article  PubMed  CAS  Google Scholar 

  81. Alvero R, Kimzey L, Sebring N, et al. Effects of fasting on neuroendocrine function and follicle development in lean women. J Clin Endocrinol Metab. 1998;83:76–80.

    Article  PubMed  CAS  Google Scholar 

  82. 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;142:2381–9.

    Article  PubMed  CAS  Google Scholar 

  83. 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;86:5184–93.

    Article  PubMed  CAS  Google Scholar 

  84. DiMarco NM, Dart L, Sanborn C. Modified activity-stress paradigm in an animal model of the female athlete triad. J Appl Physiol. 2007;103:1469–78.

    Article  PubMed  CAS  Google Scholar 

  85. Bursztein S, Elwyn DH, Askanazi J, et al. Fuel utilization in normal, starving, and pathological states energy metabolism, indirect calorimetry, and nutrition. Baltimore, MD: Williams & Wilkins; 1989. p. 146.

    Google Scholar 

  86. Bronson FH, Heideman PD. Short-term hormonal responses to food intake in peripubertal female rats. Am J Physiol. 1990;259:R25–31.

    PubMed  CAS  Google Scholar 

  87. Foster DL, Ebling FJ, Micka AF, et al. Metabolic interfaces between growth and reproduction. I. Nutritional modulation of gonadotropin, prolactin, and growth hormone secretion in the growth-­limited female lamb. Endocrinology. 1989;125:342–50.

    Article  PubMed  CAS  Google Scholar 

  88. McCann JP, Hansel W. Relationships between insulin and glucose metabolism and pituitary-ovarian functions in fasted heifers. Biol Reprod. 1986;34:630–41.

    Article  PubMed  CAS  Google Scholar 

  89. Parfitt DB, Church KR, Cameron JL. Restoration of pulsatile luteinizing hormone secretion after fasting in rhesus monkeys (Macaca mulatta): dependence on size of the refeed meal. Endocrinology. 1991;129:749–56.

    Article  PubMed  CAS  Google Scholar 

  90. Schreihofer DA, Renda F, Cameron JL. Feeding-induced stimulation of luteinizing hormone secretion in male rhesus monkeys is not dependent on a rise in blood glucose concentration. Endocrinology. 1996;137:3770–6.

    Article  PubMed  CAS  Google Scholar 

  91. Flatt JP. Energetics of intermediary metabolism. In: Kinney JM, editor. Assessment of energy metabolism in health and disease. Columbus, OH: Ross Laboratories; 1980. p. 77–87.

    Google Scholar 

  92. Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37:348–52.

    Article  PubMed  Google Scholar 

  93. Kopp-Woodroffe SA, Manore MM, Dueck CA, et al. Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr. 1999;9:70–88.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  96. Compston JE. Sex steroids and bone. Physiol Rev. 2001;81:419–47.

    PubMed  CAS  Google Scholar 

  97. Baker ER, Mathur RS, Kirk RF, et al. Female runners and secondary amenorrhea: correlation with age, parity, mileage, and plasma hormonal and sex-hormone-binding globulin concentrations. Fertil Steril. 1981;36:183–7.

    PubMed  CAS  Google Scholar 

  98. Ellison PT. Advances in human reproductive ecology. Annu Rev Anthropol. 1994;23:255–75.

    Article  PubMed  CAS  Google Scholar 

  99. Weaver CM, Martin BR, Plawecki KL, et al. Differences in calcium metabolism between adolescent and adult females. Am J Clin Nutr. 1995;61:577–81.

    PubMed  CAS  Google Scholar 

  100. 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;25:2328–39.

    Article  PubMed  CAS  Google Scholar 

  101. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29 Suppl 1:S7–15.

    Article  PubMed  Google Scholar 

  102. Braun DL, Sunday SR, Halmi KA. Psychiatric comorbidity in patients with eating disorders. Psychol Med. 1994;24:859–67.

    Article  PubMed  CAS  Google Scholar 

  103. Kaye WH, Bulik CM, Thornton L, et al. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry. 2004;161:2215–21.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  105. Rodriguez NR, DiMarco NM, Langley S. Position of the American dietetic association, dietitians of Canada, and the American college of sports medicine: nutrition and athletic performance. J Am Diet Assoc. 2009;109:509–27.

    Article  PubMed  Google Scholar 

  106. Hubert P, King NA, Blundell JE. Uncoupling the effects of energy expenditure and energy intake: appetite response to short-term energy deficit induced by meal omission and physical activity. Appetite. 1998;31:9–19.

    Article  PubMed  CAS  Google Scholar 

  107. Blundell JE, King NA. Physical activity and regulation of food intake: current evidence. Med Sci Sports Exerc. 1999;31:S573–83.

    Article  PubMed  CAS  Google Scholar 

  108. 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 Physiol. 2004;286:R350–8.

    Article  PubMed  CAS  Google Scholar 

  109. Horvath PJ, Eagen CK, Ryer-Calvin SD, et al. The effects of varying dietary fat on the nutrient intake in male and female runners. J Am Coll Nutr. 2000;19:42–51.

    PubMed  CAS  Google Scholar 

  110. Horvath PJ, Eagen CK, Fisher NM, et al. The effects of varying dietary fat on performance and metabolism in trained male and female runners. J Am Coll Nutr. 2000;19:52–60.

    PubMed  CAS  Google Scholar 

  111. Wardle J, Haase AM, Steptoe A. Body image and weight control in young adults: international comparisons in university students from 22 countries. Int J Obes (Lond). 2006;30:644–51.

    Article  CAS  Google Scholar 

  112. Martinsen M, Bratland-Sanda S, Eriksson AK, et al. 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne B. Loucks PHD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Loucks, A.B. (2013). Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function. In: Constantini, N., Hackney, A. (eds) Endocrinology of Physical Activity and Sport. Contemporary Endocrinology. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-314-5_11

Download citation

  • DOI: https://doi.org/10.1007/978-1-62703-314-5_11

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-62703-313-8

  • Online ISBN: 978-1-62703-314-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics