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 condition referred to as the “Female Athlete Triad” (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. Research supports that exercise has no suppressive effect on reproductive function in women beyond the impact of its energy cost on energy availability, and the suppression was found to occur abruptly below a threshold of 30 kcal/kg 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. The chapter also discusses in more detail the means for controlling energy availability in the experiments, as well as the magnitude of errors that can occur in estimates of energy availability from estimates of body fatness, energy expenditure, and energy intake.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover 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

Abbreviations

ACSM:

American College of Sports Medicine

BMI:

Body mass index

BW:

Body weight

EA:

Energy availability

EI:

Energy intake

FFM:

Fat-free mass

GH:

Growth hormone

GnRH:

Gonadotropin-releasing hormone

HPG:

Hypothalamic-pituitary-gonadal

IGFBP:

IGF-binding protein

IGF-I:

Insulin-like growth factor-I

kcal:

Kilocalories

LBM:

Lean body mass

LH:

Luteinizing hormone

NEB:

Negative energy balance

NEEE:

Non-exercise energy expenditure

PYY:

Peptide YY

RM:

Resting metabolism

T3:

Tri-iodothyronine

TEEE:

Total energy expended during exercise

WEE:

Waking energy expenditure

References

  1. Nattiv A, Loucks AB, Manore MM, 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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    Article  PubMed  Google Scholar 

  4. Joy E, De Souza MJ, Nattiv A, 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. Curr Sports Med Rep. 2014;13(4):219–32.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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  CAS  PubMed  Google Scholar 

  7. Frisch RE, Revelle R. Height and weight at menarche and a hypothesis of menarche. Arch Dis Child. 1971;46(249):695–701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Schneider JE, Wade GN. Control of fertility by metabolic cues – reply. Am J Physiol Endocrinol Metab. 1997;273(1):E231–E2.

    Article  CAS  Google Scholar 

  9. 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(3):200–4.

    Article  CAS  PubMed  Google Scholar 

  10. Bronson FH, Manning JM. The energetic regulation of ovulation: a realistic role for body fat. Biol Reprod. 1991;44(6):945–50.

    Article  CAS  PubMed  Google Scholar 

  11. Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc. 1985;17(1):56–72.

    Article  CAS  PubMed  Google Scholar 

  12. Scott EC, Johnston FE. Critical fat, menarche, and the maintenance of menstrual cycles: a critical review. J Adolesc Health Care. 1982;2(4):249–60.

    Article  CAS  PubMed  Google Scholar 

  13. Sinning WE, Little KD. Body composition and menstrual function in athletes. Sports Med. 1987;4(1):34–45.

    Article  CAS  PubMed  Google Scholar 

  14. Loucks AB, Horvath SM, Freedson PS. Menstrual status and validation of body fat prediction in athletes. Hum Biol. 1984;56(2):383–92.

    CAS  PubMed  Google Scholar 

  15. 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(6):2483–7.

    Article  CAS  PubMed  Google Scholar 

  16. Di Carlo C, Palomba S, De Fazio M, Gianturco M, Armallino M, Nappi C. Hypogonadotropic hypogonadotropism in obese women after biliopancreatic diversion. Fertil Steril. 1999;72(5):905–9.

    Article  PubMed  Google Scholar 

  17. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372(6505):425–32.

    Article  CAS  PubMed  Google Scholar 

  18. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292–5.

    Article  CAS  PubMed  Google Scholar 

  19. Tena-Sempere M. Roles of ghrelin and leptin in the control of reproductive function. Neuroendocrinology. 2007;86(3):229–41.

    Article  CAS  PubMed  Google Scholar 

  20. Castellano JM, Bentsen AH, Mikkelsen JD, Tena-Sempere M. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res. 2010;1364:129–38.

    Article  CAS  PubMed  Google Scholar 

  21. Chou SH, Chamberland JP, Liu X, Matarese G, Gao C, Stefanakis R, et al. Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci U S A. 2011;108(16):6585–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ma Z, Gingerich RL, Santiago JV, Klein S, Smith CH, Landt M. Radioimmunoassay of leptin in human plasma. Clin Chem. 1996;42(6 Pt 1):942–6.

    Article  CAS  PubMed  Google Scholar 

  23. Laughlin GA, Yen SSC. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab. 1997;82(1):318–21.

    Article  CAS  PubMed  Google Scholar 

  24. Mantzoros C, Flier JS, Lesem MD, Brewerton TD, Jimerson DC. Cerebrospinal fluid leptin in anorexia nervosa: correlation with nutritional status and potential role in resistance to weight gain. J Clin Endocrinol Metab. 1997;82(6):1845–51.

    CAS  PubMed  Google Scholar 

  25. Miller KK, Parulekar MS, Schoenfeld E, Anderson E, Hubbard J, Klibanski A, 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(7):2309–12.

    CAS  PubMed  Google Scholar 

  26. Jimerson DC, Mantzoros C, Wolfe BE, Metzger ED. Decreased serum leptin in bulimia nervosa. J Clin Endocrinol Metab. 2000;85(12):4511–4.

    CAS  PubMed  Google Scholar 

  27. 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.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

  30. Berga SL, Marcus MD, Loucks TL, Hlastala S, Ringham R, Krohn MA. Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril. 2003;80(4):976–81.

    Article  PubMed  Google Scholar 

  31. Kolaczynski JW, Considine RV, Ohannesian J, Marco C, Opentanova I, Nyce MR, et al. Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves. Diabetes. 1996;45(11):1511–5.

    Article  CAS  PubMed  Google Scholar 

  32. Kolaczynski JW, Ohannesian JP, Considine RV, Marco CC, Caro JF. Response of leptin to short-term and prolonged overfeeding in humans. J Clin Endocrinol Metab. 1996;81:4162–5.

    CAS  PubMed  Google Scholar 

  33. Weigle DS, Duell PB, Connor WE, Steiner RA, Soules MR, Kuijper JL. Effect of fasting, refeeding, and dietary fat restriction on plasma leptin levels. J Clin Endocrinol Metab. 1997;82:561–5.

    CAS  PubMed  Google Scholar 

  34. Jenkins AB, Markovic TP, Fleury A, Campbell LV. Carbohydrate intake and short-term regulation of leptin in humans. Diabetologia. 1997;40(3):348–51.

    Article  CAS  PubMed  Google Scholar 

  35. Wang J, Liu R, Hawkins M, Barzilai N, Rossetti L. A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature. 1998;393(6686):684–8.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16(2):235–72.

    Article  CAS  PubMed  Google Scholar 

  39. Bronson FH, Heideman PD. Seasonal regulation of reproduction in mammals. In: Knobil E, Neill J, editors. The physiology of reproduction, vol. 2. New York: Raven Press; 1994. p. 541–83.

    Google Scholar 

  40. 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-Verlag; 1989. p. 42–9.

    Chapter  Google Scholar 

  41. Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Phys. 1996;270(1 Pt 1):E1–19.

    CAS  Google Scholar 

  42. Furman M, Wade GN. Animal models in the study of nutritional infertility. Curr Opin Endocrinol. 2007;14(6):475–81.

    Article  Google Scholar 

  43. Laughlin GA, Yen SSC. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab. 1996;81(12):4301–9.

    CAS  PubMed  Google Scholar 

  44. Christo K, Cord J, Mendes N, Miller KK, Goldstein MA, Klibanski A, et al. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study. Clin Endocrinol. 2008;69(4):628–33.

    Article  CAS  Google Scholar 

  45. Scheid JL, Williams NI, West SL, VanHeest SL, De Souza MJ. Elevated PYY is associated with energy deficiency and indices of subclinical disordered eating in exercising women with hypothalamic amenorrhea. Appetite. 2009;52(1):184–92.

    Article  CAS  PubMed  Google Scholar 

  46. 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;23:15–22.

    Article  CAS  PubMed  Google Scholar 

  47. Loucks AB, Laughlin GA, Mortola JF, Girton L, Nelson JC, Yen SSC. Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. J Clin Endocrinol Metab. 1992;75(2):514–8.

    CAS  PubMed  Google Scholar 

  48. Loucks AB, Mortola JF, Girton L, Yen SS. 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 

  49. 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.

    Article  CAS  PubMed  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. Marcus R, Cann C, Madvig P, Minkoff J, Goddard M, Bayer M, et al. Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med. 1985;102(2):158–63.

    Article  CAS  PubMed  Google Scholar 

  52. Nelson ME, Fisher EC, Catsos PD, Meredith CN, Turksoy RN, Evans WJ. Diet and bone status in amenorrheic runners. Am J Clin Nutr. 1986;43(6):910–6.

    Article  CAS  PubMed  Google Scholar 

  53. Edwards JE, Lindeman AK, Mikesky AE, Stager JM. Energy balance in highly trained female endurance runners. Med Sci Sports Exerc. 1993;25(12):1398-404.

    Article  PubMed  Google Scholar 

  54. Wilmore JH, Wambsgans KC, Brenner M, Broeder CE, Paijmans I, Volpe JA, et al. Is there energy conservation in amenorrheic compared with eumenorrheic distance runners? J Appl Physiol. 1992;72(1):15–22.

    Article  CAS  PubMed  Google Scholar 

  55. Mertz W, Tsui JC, Judd JT, Reiser S, Hallfrisch J, Morris ER, 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(2):291–5.

    Article  CAS  PubMed  Google Scholar 

  56. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332(10):621–8.

    Article  CAS  PubMed  Google Scholar 

  57. 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  CAS  PubMed  Google Scholar 

  58. 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 

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

    Article  CAS  PubMed  Google Scholar 

  60. 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(5):471–9.

    Article  CAS  PubMed  Google Scholar 

  61. Chatterton RT Jr, Hartman AL, Lynn DE, Hickson RC. Exercise-induced ovarian dysfunction in the rat. Proc Soc Exp Biol Med. 1990;193(3):220–4.

    Article  CAS  PubMed  Google Scholar 

  62. Manning JM, Bronson FH. Effects of prolonged exercise on puberty and luteinizing hormone secretion in female rats. Am J Phys. 1989;257(6 Pt 2):R1359–64.

    CAS  Google Scholar 

  63. Manning JM, Bronson FH. Suppression of puberty in rats by exercise: effects on hormone levels and reversal with GnRH infusion. Am J Phys. 1991;260(4 Pt 2):R717–23.

    CAS  Google Scholar 

  64. De Souza MJ, Maguire MS, Maresh CM, Kraemer WJ, Rubin KR, Loucks AB. Adrenal activation and the prolactin response to exercise in eumenorrheic and amenorrheic runners. J Appl Physiol. 1991;70(6):2378–87.

    Article  PubMed  Google Scholar 

  65. De Souza MJ, Luciano AA, Arce JC, Demers LM, Loucks AB. Clinical tests explain blunted cortisol responsiveness but not mild hypercortisolism in amenorrheic runners. J Appl Physiol. 1994;76(3):1302–9.

    Article  PubMed  Google Scholar 

  66. Ding J-H, Scheckter CB, Drinkwater BL, Soules MR, Bremner WJ. High serum cortisol levels in exercise-associated amenorrhea. Ann Intern Med. 1988;108:530–4.

    Article  CAS  PubMed  Google Scholar 

  67. Suh BY, Liu JH, Berga SL, Quigley ME, Laughlin GA, Yen SS. Hypercortisolism in patients with functional hypothalamic-amenorrhea. J Clin Endocrinol Metab. 1988;66(4):733–9.

    Article  CAS  PubMed  Google Scholar 

  68. Gold PW, Gwirtsman H, Averinos PC, Nieman LK, Gallucci WT, Kaye W, et al. Abnormal hypothalamic-pituitary-adrenal function in anorexia nervosa: pathophysiologic mechanisms in underweight and weight-corrected patients. N Engl J Med. 1986;314(21):1335–42.

    Article  CAS  PubMed  Google Scholar 

  69. Kuo T, Harris CA, Wang JC. Metabolic functions of glucocorticoid receptor in skeletal muscle. Mol Cell Endocrinol. 2013;380(1–2):79–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  72. Bonen A. Recreational exercise does not impair menstrual cycles: a prospective study. Int J Sports Med. 1992;13(2):110–20.

    Article  CAS  PubMed  Google Scholar 

  73. Boyden TW, Pamenter RW, Stanforth P, Rotkis T, Wilmore JH. Sex steroids and endurance running in women. Fertil Steril. 1983;39(5):629–32.

    Article  CAS  PubMed  Google Scholar 

  74. Bullen BA, Skrinar GS, Beitins IZ, Carr DB, Reppert SM, Dotson CO, et al. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J Appl Physiol. 1984;56(6):1453–63.

    Article  CAS  PubMed  Google Scholar 

  75. Rogol AD, Weltman JY, Evans WS, Veldhuis JD, Weltman AL. Long-term endurance training alters the hypothalamic-pituitary axes for gonadotropins and growth hormone. Endocrinol Metab Clin North Am. 1992;21(4):817–32.

    Article  CAS  PubMed  Google Scholar 

  76. Loucks AB, Cameron JL, De Souza MJ. Subject assignment may have biased exercise results [letter; comment]. J Appl Physiol. 1993;74(4):2045–7.

    Article  CAS  PubMed  Google Scholar 

  77. Bullen BA, Skrinar GS, Beitins IZ, von Mering G, Turnbull BA, McArthur JW. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med. 1985;312(21):1349–53.

    Article  CAS  PubMed  Google Scholar 

  78. Williams NI, Young JC, McArthur JW, Bullen B, Skrinar GS, Turnbull B. Strenuous exercise with caloric restriction: effect on luteinizing hormone secretion. Med Sci Sports Exerc. 1995;27(10):1390–8.

    Article  CAS  PubMed  Google Scholar 

  79. Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Phys. 1993;264(5 Pt 2):R924–30.

    CAS  Google Scholar 

  80. 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.

    CAS  Google Scholar 

  81. 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(4):910–5.

    CAS  PubMed  Google Scholar 

  82. Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol. 1998;84(1):37–46.

    Article  CAS  PubMed  Google Scholar 

  83. Loucks AB, Verdun M. Slow restoration of LH pulsatility by refeeding in energetically disrupted women. Am J Phys. 1998;275(4 Pt 2):R1218–26.

    CAS  Google Scholar 

  84. Loucks A. Is stress measured in joules? Mil Psychol. 2009;21(S1):S101–S7.

    Article  Google Scholar 

  85. Treloar AE, Boynton RE, Behn BG, Brown BW. Variation of the human menstrual cycle through reproductive life. Int J Fertil. 1967;12(1 Pt 2):77–126.

    CAS  PubMed  Google Scholar 

  86. Olson BR, Cartledge T, Sebring N, Defensor R, Nieman L. Short-term fasting affects luteinizing hormone secretory dynamics but not reproductive function in normal-weight sedentary women. J Clin Endocrinol Metab. 1995;80(4):1187–93.

    CAS  PubMed  Google Scholar 

  87. Alvero R, Kimzey L, Sebring N, Reynolds J, Loughran M, Nieman L, et al. Effects of fasting on neuroendocrine function and follicle development in lean women. J Clin Endocrinol Metab. 1998;83(1):76–80.

    CAS  PubMed  Google Scholar 

  88. 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.

    Article  CAS  PubMed  Google Scholar 

  89. Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama AL, 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.

    Article  CAS  PubMed  Google Scholar 

  90. 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  CAS  PubMed  Google Scholar 

  91. Bursztein S, Elwyn DH, Askanazi J, Kinney JM. Fuel utilization in normal, starving, and pathological states. Energy metabolism, indirect calorimetry, and nutrition. Baltimore: Williams & Wilkins; 1989. p. 146.

    Google Scholar 

  92. Bronson FH, Heideman PD. Short-term hormonal responses to food intake in peripubertal female rats. Am J Phys. 1990;259(1 Pt 2):R25–31.

    CAS  Google Scholar 

  93. Foster DL, Ebling FJ, Micka AF, Vannerson LA, Bucholtz DC, Wood RI, 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(1):342–50.

    Article  CAS  PubMed  Google Scholar 

  94. McCann JP, Hansel W. Relationships between insulin and glucose metabolism and pituitary-ovarian functions in fasted heifers. Biol Reprod. 1986;34(4):630–41.

    Article  CAS  PubMed  Google Scholar 

  95. 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(2):749–56.

    Article  CAS  PubMed  Google Scholar 

  96. 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(9):3770–6.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  98. Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37(4–5):348–52.

    Article  PubMed  Google Scholar 

  99. Kopp-Woodroffe SA, Manore MM, Dueck CA, Skinner JS, Matt KS. 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 

  100. 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.

    PubMed  Google Scholar 

  101. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Mineral Res. 2004;19(8):1231–40.

    Article  Google Scholar 

  102. Compston JE. Sex steroids and bone. Physiol Rev. 2001;81(1):419–47.

    Article  CAS  PubMed  Google Scholar 

  103. 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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  105. Weaver CM, Martin BR, Plawecki KL, Peacock M, Wood OB, Smith DL, et al. Differences in calcium metabolism between adolescent and adult females. Am J Clin Nutr. 1995;61(3):577–81.

    Article  CAS  PubMed  Google Scholar 

  106. Williams NI, Reed JL, Leidy HJ, Legro RS, De Souza MJ. 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 

  107. Lieberman JL, DS MJ, Wagstaff DA, Williams NI. Menstrual disruption with exercise is not linked to an energy availability threshold. Med Sci Sports Exerc. 2018;50(3):551–61.

    Article  PubMed  PubMed Central  Google Scholar 

  108. 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.

    Article  CAS  PubMed  Google Scholar 

  109. Redman LM, Loucks AB. Menstrual disorders in athletes. Sports Med. 2005;35(9):747–55.

    Article  PubMed  Google Scholar 

  110. Vollman RF. The menstrual cycle. Major Probl Obstet Gynecol. 1977;7:1–193.

    Google Scholar 

  111. Cialdella-Kam L, Guebels CP, Maddalozzo GF, Manore MM. Dietary intervention restored menses in female athletes with exercise-associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients. 2014;6(8):3018–39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Guebels CP, Kam LC, Maddalozzo GF, Manore MM. Active women before/after an intervention designed to restore menstrual function: resting metabolic rate and comparison of four methods to quantify energy expenditure and energy availability. Int J Sport Nutr Exerc Metab. 2014;24(1):37–46.

    Article  PubMed  Google Scholar 

  113. Dueck CA, Matt KS, Manore MM, Skinner JS. Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr. 1996;6(1):24–40.

    Article  CAS  PubMed  Google Scholar 

  114. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sport Sci. 2011;S1:S7–S15.

    Article  Google Scholar 

  115. Braun DL, Sunday SR, Halmi KA. Psychiatric comorbidity in patients with eating disorders. Psychol Med. 1994;24(4):859–67.

    Article  CAS  PubMed  Google Scholar 

  116. Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiat. 2004;161(12):2215–21.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  118. Thomas DT, Erdman KA, Burke LM. American College of Sports Medicine joint position statement. Nutrition and athletic performance. Med Sci Sports Exerc. 2016;48(3):543–68.

    Article  CAS  PubMed  Google Scholar 

  119. 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(1):9–19.

    Article  CAS  PubMed  Google Scholar 

  120. Blundell JE, King NA. Physical activity and regulation of food intake: current evidence. Med Sci Sports Exerc. 1999;31(11 Suppl):S573–83.

    Article  CAS  PubMed  Google Scholar 

  121. Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N, 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 Phys. 2004;286(2):R350–8.

    CAS  Google Scholar 

  122. Horvath PJ, Eagen CK, Ryer-Calvin SD, Pendergast DR. The effects of varying dietary fat on the nutrient intake in male and female runners. J Am Coll Nutr. 2000;19(1):42–51.

    Article  CAS  PubMed  Google Scholar 

  123. Horvath PJ, Eagen CK, Fisher NM, Leddy JJ, Pendergast DR. The effects of varying dietary fat on performance and metabolism in trained male and female runners. J Am Coll Nutr. 2000;19(1):52–60.

    Article  CAS  PubMed  Google Scholar 

  124. Wardle J, Haase AM, Steptoe A. Body image and weight control in young adults: international comparisons in university students from 22 countries. Int J Obesity. 2006;30(4):644–51.

    Article  CAS  Google Scholar 

  125. Martinsen M, Bratland-Sanda S, Eriksson AK, Sundgot-Borgen J. Dieting to win or to be thin? A study of dieting and disordered eating among adolescent elite athletes and non-athlete controls. Br J Sport Med. 2010;44(1):70–6.

    Article  CAS  Google Scholar 

  126. Loucks AB. The Female Athlete Triad: a metabolic phenomenon. Pensar En Movimiento. 2014;12(1):1–23.

    Article  Google Scholar 

Download references

Conflict of Interest

Anne Loucks is a founder and shareholder of AEIOU Scientific, LLC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne B. Loucks .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Loucks, A.B. (2020). Exercise Training in the Normal Female: Effects of Low Energy Availability on Reproductive Function. In: Hackney, A., Constantini, N. (eds) Endocrinology of Physical Activity and Sport. Contemporary Endocrinology. Humana, Cham. https://doi.org/10.1007/978-3-030-33376-8_11

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-33376-8_11

  • Published:

  • Publisher Name: Humana, Cham

  • Print ISBN: 978-3-030-33375-1

  • Online ISBN: 978-3-030-33376-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics