Advertisement

Exercise and the Hypothalamus: Ovulatory Adaptations

  • Angela Y. Liu
  • Moira A. Petit
  • Jerilynn C. PriorEmail author
Chapter
  • 108 Downloads
Part of the Contemporary Endocrinology book series (COE)

Abstract

Physically active women with regular menstrual cycles (21–35 days long) who increase exercise training may experience adaptive changes of their reproductive system. Ovulatory disturbances, oligomenorrhea, and amenorrhea are no longer evidence of “disease,” but of protection from pregnancy while adapting to energetic and other training-related demands; this is known as relative energy deficiency in sport. The most common hypothalamic reproductive adaptation for women is the development of subclinical ovulatory disturbances (regular cycles without ovulation or with short luteal phases). If the woman in athletic training is an adolescent, <12 years from menarche, or took combined hormonal contraception before developing robustly ovulatory cycles, and is also experiencing psychosocial stressors, then she may further develop oligomenorrhea (cycles >35 but <90 days apart) or amenorrhea (cycles ≥90 days apart). The common path to hypothalamic adaptation in exercising men and women involves exercise-related relative energy insufficiency and other stressful experiences. Accounting for the life experience and current context of an exercising woman with hypothalamic adaptation, gradually increasing exercise intensity and duration, creating a positive and supportive social/emotional environment, and sharing knowledge that these changes are protective and reversible will decrease any negative effects of intense physical exercise.

Keywords

Amenorrhea Menstrual Cycles Women Athletes Progesterone Estrogen Reproduction 

References

  1. 1.
    Selye H. The effect of adaptation to various damaging agents on the female sex organs in the rat. Endocrinology. 1939;25:615–24.CrossRefGoogle Scholar
  2. 2.
    Shangold MM, Freeman R, Thysen B, Gatz M. The relationship between long-distance running, plasma progesterone, and luteal phase length. Fertil Steril. 1979;31:130–3.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Bonen A. Recreational exercise does not impair menstrual cycles: a prospective study. Int J Sports Med. 1992;13:110–20.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Prior JC, Vigna YM, Schechter MT, Burgess AE. Spinal bone loss and ovulatory disturbances. New Engl J Med. 1990;323:1221–7.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Rogol AD, Weltman A, Weltman JY, Serp RI, Snead DB, Levine S, et al. Durability of the reproductive axis in eumenorrheic women during 1 yr of endurance training. J Appl Physiol. 1992;72:1571.CrossRefGoogle Scholar
  6. 6.
    Prior JC. Endocrine “conditioning” with endurance training: a preliminary review. Can J Appl Sport Sci. 1982;7:149–57.Google Scholar
  7. 7.
    Drinkwater BL, Nilson K, Chesnut CH, Bremner WJ, Shainholtz S, Southworth MB. Bone mineral content of amenorrheic and eumenorrheic athletes. New Engl J Med. 1984;311:277–81.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Vollman RF. The menstrual cycle. In: Friedman EA, editor. Major problems in obstetrics and gynecology, Vol 7. 1. Toronto: W.B. Saunders Company; 1977. p. 11–193.Google Scholar
  9. 9.
    Prior JC, Naess M, Langhammer A, Forsmo S. Ovulation prevalence in women with spontaneous normal-length menstrual cycles – a population-based cohort from HUNT3, Norway. PLOS One. 2015;10(8):e0134473.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Abraham GE. The normal menstrual cycle. In: Givens JR, editor. Endocrine causes of menstrual disorders. 1. Chicago: Year Book Medical Publishers, Inc; 1978. p. 15–44.Google Scholar
  11. 11.
    Prior JC, Vigna YM, Schulzer M, Hall JE, Bonen A. Determination of luteal phase length by quantitative basal temperature methods: validation against the midcycle LH peak. Clin Invest Med. 1990;13:123–31.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Taaffe DR, Robinson TR, Snow CM, Marcus R. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res. 1997;12(2):255–60.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Nielsen HK, Brixen K, Bouillon R, Mosekilde L. Changes in biochemical markers of osteoblastic activity during the menstrual cycle. J Clin Endocrinol Metab. 1990;70:1431–7.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Prior JC. Perimenopause: the complex endocrinology of the menopausal transition. Endocr Rev. 1998;19:397–428.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Welt CK. The physiology and pathophysiology of inhibin, activin and follistatin in female reproduction. Curr Opin Obstet Gynecol. 2002;14(3):317–23.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Landgren BH, Unden AL, Diczfalusy E. Hormonal profile of the cycle in 68 normally menstruating women. Acta Endocr Copenhagen. 1980;94:89–98.Google Scholar
  17. 17.
    Fraser IS, Baird DT. Endometrial cystic glandular hyperplasia in adolescent girls. J Obstet Gynecol. 1972;79:1009–13.Google Scholar
  18. 18.
    Van Look PF, Lothian H, Hunter WM, Michie EA, Baird DT. Hypothalamic-pituitary-ovarian function in perimenopausal women. Clin Endocrinol. 1977;7:13–31.CrossRefGoogle Scholar
  19. 19.
    Cowan LD, Gordis L, Tonascia JA, Jones GS. Breast cancer incidence in women with a history of progesterone deficiency. Am J Epidemiol. 1981;114(2):209–17.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Sherman BM, Korenman SG. Hormonal characteristics of the human menstrual cycle throughout reproductive life. J Clin Investig. 1975;55:699–706.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Sowers M, Randolph JF, Crutchfield M, Jannausch ML, Shapiro B, Zhang B, et al. Urinary ovarian and gonadotropin hormone levels in premenopausal women with low bone mass. J Bone Miner Res. 1998;13(7):1191–202.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Aksel S, Wiebe RH, Tyson JE, Jones GS. Hormonal findings associated with aluteal cycles. Obstet Gynecol. 1996;48(5):598–602.Google Scholar
  23. 23.
    Soules MR, McLachlan RI, Marit EK, Dahl KD, Cohen NL, Bremner WJ. Luteal phase deficiency: characterization of reproductive hormones over the menstrual cycle. J Clin Endocrinol Metab. 1989;69:804–12.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Petsos P, Ratcliffe WA, Heath DF, Anderson DC. Comparison of blood spot, salivary and serum progesterone assays in the normal menstrual cycle. Clin Endocrinol. 1986;24:31–8.CrossRefGoogle Scholar
  25. 25.
    Finn MM, Gosling JP, Tallon DF, Madden AT, Meehan FP, Fottrell PF. Normal salivary progesterone levels throughout the ovarian cycle as determined by a direct enzyme immunoassay. Fertil Steril. 1988;50:882–7.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Santoro N, Rosenberg J, Adel T, Skurnick JH. Characterization of reproductive hormonal dynamics in the perimenopause. J Clin Endocrinol Metab. 1996;81(4):1495–501.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Bullen BA, Skrinar GS, Beitins IZ, von Mering G, Turnbull BA, McArthur JW. Induction of menstrual disorders by strenuous exercise in untrained women. New Engl J Med. 1985;312:1349–53.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    McNeely MJ, Soules MR. The diagnosis of luteal phase deficiency: a critical review. Fertil Steril. 1988;50:1–15.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Hinney B, Henze C, Kuhn W, Wuttke W. The corpus luteum insufficiency: a multifactorial disease. J Clin Endocrinol Metab. 1996;81:565–70.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Prior JC, Vigna YM, Barr SI, Kennedy S, Schulzer M, Li DK. Ovulatory premenopausal women lose cancellous spinal bone: a five year prospective study. Bone. 1996;18:261–7.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Hitchcock CL, Bishop C, Prior JC, editors. Modelling ovulation and detecting subclinical ovulatory disturbances. Chicago: The 12th conference of the Society for Menstrual Cycle Research; 1997.Google Scholar
  32. 32.
    McCarthy JJ, Rockette HE. A comparison of methods to interpret the basal body temperature graph. Fertil Steril. 1983;39:640–6.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Royston JP, Abrams RM. An objective methods for detecting the shift in basal body temperature in women. Biometrics. 1980;36:217–24.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Prior JC, Vigna YM, Barr SI, Rexworthy C, Lentle BC. Cyclic medroxyprogesterone treatment increases bone density: a controlled trial in active women with menstrual cycle disturbances. Am J Med. 1994;96:521–30.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Bedford JL, Prior JC, Hitchcock CL, Barr SI. Detecting evidence of luteal activity by least-squares quantitative basal temperature analysis against urinary progesterone metabolites and the effect of wake-time variability. Eur J Obstet Gynecol Reprod Biol. 2009;146(1):76–80.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Prior JC. Physical exercise and the neuroendocrine control of reproduction. Baillieres Clin Endocrinol Metab. 1987;1:299–317.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Prior JC. Exercise-associated menstrual disturbances. In: Adashi EY, Rock JA, Rosenwaks Z, editors. Reproductive endocrinology, surgery and technology. New York: Raven Press; 1996. p. 1077–91.Google Scholar
  38. 38.
    Petraglia F, Sutton S, Vale W, Plotsky P. Corticotropin-releasing factor decreases plasma luteinizing hormone levels in female rats by inhibiting gonadotropin-releasing hormone release into hypophysial-portal circulation∗. Endocrinology. 1987;120:1083–8.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Hakimi O, Cameron LC. Effect of exercise on ovulation: a systematic review. Sports Med. 2017;47(8):1555–67.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Prior JC. Reproduction: exercise-related adaptations and the health of women and men. In: Bouchard C, Shephard RJ, Stephens T, Sutton JR, McPherson BD, editors. Exercise, fitness and health. 1. Champaign: Human Kineteic Books; 1990. p. 661–75.Google Scholar
  41. 41.
    Barr SI, Janelle KC, Prior JC. Energy intakes are higher during the luteal-phase of ovulatory menstrual cycles. Am J Clin Nutr. 1995;61(1):39–43.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Kaplan JR, Adams MR, Clarkson TB, Koritnik DR. Psychological influences on female ‘protection’ among cynomolgus macaques. Atherosclerosis. 1984;53:283–95.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Kowalski W, Chatterton RT Jr, Kazer RR, Wentz AC. The impact of subchronic hypercortisolemia on progesterone metabolism and the luteinizing hormone-progesterone axis in the Cynomolgus monkey. J Clin Endocrinol Metab. 1993;77(6):1597–603.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Chatterton RT, Kazer RR, Rebar RW. Depletion of luteal phase serum progesterone during constant infusion of cortisol phosphate in the cynomolgus monkey ∗†∗Supported by grant HD 21921 from the National Institutes of Health, Bethesda, Maryland. †Presented at the 71st Annual Meeting of the Endocrine Society, Seattle, Washington, June 21, 1989. Fertil Steril. 1991;56(3):547–54.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Warren MP, Siris ES, Petrovich C. The influence of severe illness on gonadotropin secretion in the postmenopausal female. J Clin Endocrinol Metab. 1977;45:99–104.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Nagata I, Kato K, Seki K, Furuya K. Ovulatory disturbances. Causative factors among Japanese student nurses in a dormitory. J Adolesc Health Care. 1986;7:1–5.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Schweiger U, Laessle RG, Schweiger M, Herman F, Riedel W, Pirke KM. Caloric intake, stress and menstrual function in athletes. Fertil Steril. 1988;49:447–50.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Warren MP. Effects of undernutrition on reproductive function in the human. Endocr Rev. 1983;4:363–77.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    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;83:76–80.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Barron JL, Noakes TD, Levy W, Smith C, Millar RP. Hypothalamic dysfunction in overtrained athletes. J Clin Endocrinol Metab. 1985;60:803–6.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Ding JH, Sheckter CB, Drinkwater BL, Soules MR, Bremner WJ. High serum cortisol levels in exercise-associated amenorrhea. Ann Intern Med. 1988;108:530–4.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Berga SL, Daniels TL, Giles DE. Women with functional hypothalamic amenorrhea but not other forms of anovulation display amplified cortisol concentrations. Fertil Steril. 1997;67(6):1024–30.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Loucks AB, Mortola JF, Girton L, Yen SSC. Alterations in the hypothalamic-pituitary-ovarian and the hypothalamic-pituitary-adrenal axes in athletic women. J Clin Endocrinol Metab. 1989;68:402–11.CrossRefGoogle Scholar
  54. 54.
    Constantini NW, Warren MP. Menstrual dysfunction in swimmers: a distinct entity. J Clin Endocrinol Metab. 1995;80(9):2740–4.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Prior JC. Ovulatory disturbances: they do matter. Can J Diagn. 1997;14:64–82.Google Scholar
  56. 56.
    Graham TE, Viswanathan M, Van Dijk JP, Bonen A, George JC. Thermal and metabolic responses to cold by men and by eumenorrheic and amenorrheic women. J Appl Physiol. 1989;67(1):282–90.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Kaye WH, Gwirtsman HE, George DT, Ebert MH, Jimerson DC, Tomai TP, et al. Elevated cerebrospinal fluid levels of immunoreactive corticotropin-releasing hormone in anorexia nervosa: relation to state of nutrition, adrenal function, and intensity of depression. J Clin Endocrinol Metab. 1987;64(2):203–8.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Pirke KM, Schweiger U, Strowitzki T, Tuschl RJ, Laessle RG, Broocks A, et al. Dieting causes menstrual irregularities in normal weight women through impairment of luteinizing hormone. Fertil Steril. 1989;51:263–8.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Suh BY, Liu JH, Berga SL, Quigley ME, Laughlin GA, Yen SSC. Hypercortisolism in patients with functional hypothalamic amenorrhea. J Clin Endocrinol Metab. 1988;66:733–9.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Constantini NW. Medical concerns of the dancer. Book of Abstracts, XXVII FIMS World Congress of Sports Medicine, Budapest, Hungary, 2002;151.Google Scholar
  63. 63.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Reed JL, De Souza MJ, Mallinson RJ, Scheid JL, Williams NI. Energy availability discriminates clinical menstrual status in exercising women. J Int Soc Sports Nutr. 2015;12:11.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Stunkard AJ, Messick S. The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res. 1985;29:71–83.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Laessle RG, Tuschl RJ, Kotthaus BC, Pirke KM. Behavioral and biological correlates of dietary restraint in normal life. Appetite. 1989;12:83–94.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Tuschl RJ, Platte P, Laessle RG, Stichler W, Pirke KM. Energy expenditure and everyday eating behavior in healthy young women. Am J Clin Nutr. 1990;52(1):81–6.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Schweiger U, Tuschl RJ, Platte P, Broocks A, Laessle RG, Pirke KM. Everyday eating behavior and menstrual function in young women. Fertil Steril. 1992;57:771–5.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Barr SI, Prior JC, Vigna YM. Restrained eating and ovulatory disturbances: possible implications for bone health. Am J Clin Nutr. 1994;59:92–7.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Barr SI, Janelle KC, Prior JC. Vegetarian versus nonvegetarian diets, dietary restraint, and subclinical ovulatory disturbances: prospective six month study. Am J Clin Nutr. 1994;60:887–94.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Bedford JL, Prior JC, Barr SI. A prospective exploration of cognitive dietary restraint, subclinical ovulatory disturbances, cortisol and change in bone density over two years in healthy young women. J Clin Endocrinol Metab. 2010;95(7):3291–9.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Allaway HC, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Horm Mol Biol Clin Invest. 2016;25(2):91–119.Google Scholar
  73. 73.
    Sathi P, Kalyan S, Hitchcock CL, Pudek M, Prior JC. Progesterone Therapy increases Free Thyroxine Levels- data from a randomized placebo-controlled 12-week hot flush trial. Clin Endocrinol (Oxf). 2013;79:282–7.CrossRefGoogle Scholar
  74. 74.
    Bonen A, Belcastro AN, Simpson AA. Profiles of menstrual cycle hormones in teenage athletes. J Appl Physiol. 1981;50:545–51.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Ronkainen HR. Depressed follicle stimulating hormone, luteinizing hormone releasing hormone, thyrotopin releasing hormone, and metoclopramide. Fertil Steril. 1985;40:755–9.CrossRefGoogle Scholar
  76. 76.
    Malina RM. Menarche in athletes: a synthesis and hypothesis. Ann Hum Biol. 1983;10:1–24.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Rees M. Menarche when and why? Lancet. 1993;342(8884):1375–6.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Warren MP. The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab. 1980;51(5):1150–7.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Treloar SA, Martin NG. Age at menarche as a fitness trait: nonadditive genetic variance detected in a large twin sample. Am J Hum Genet. 1990;47(1):137–48.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Frisch RE, Gotz-Welbergen AV, McArthur JW, Albright TE, Witschi J, Bullen BA, et al. Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. J Am Med Assoc. 1981;246:1559–63.CrossRefGoogle Scholar
  81. 81.
    McEwen BS. Protective and damaging effects of stress mediators. Seminars in Medicine of the Beth Israel Deaconess Medical Center. New Engl J Med. 1998;338(3):171–9.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Prior JC, Vigna YM, Watson D. Spironolactone with physiological female gonadal steroids in the presurgical therapy of male to female transexuals: a new observation. Arch Sex Behav. 1989;18:49–57.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Barr SI, Petit MA, Vigna YM, Prior JC. Eating attitudes and habitual calcium intake in peripubertal girls are associated with initial bone mineral content and its change over 2 years. J Bone Miner Res. 2001;16:940–7.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Rivier C, Rivier JE, Vale W. Stress-induced inhibition of reproductive functions: role of endogenous corticotropin-releasing factor. Science. 1986;231:607–9.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Berga SL, Loucks-Daniels TL, Adler LJ, Chrousos GP, Cameron JL, Matthews KA, et al. Cerebrospinal fluid levels of corticotropin-releasing hormone in women with functional hypothalamic amenorrhea. Am J Obstet Gynecol. 2000;182(4):776–81.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Williams NI, Berga SL, Cameron JL. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab. 2007;293(1):E270–E6.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Bonen A, Keizer HA. Athletic menstrual cycle irregularity: endocrine response to exercise and training. Phys Sportsmed. 1984;12:78–94.CrossRefGoogle Scholar
  88. 88.
    Prior JC, Cameron K, Ho Yeun B, Thomas J. Menstrual cycle changes with marathon training: anovulation and short luteal phase. Can J Appl Sport Sci. 1982;7:173–7.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Boyden TW, Pamenter RW, Stanforth PR, Rotkis TC, Wilmore JH. Sex steroids and endurance running in women. Fertil Steril. 1983;39:629–32.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Beitins IZ, McArthur JW, Turnbull BA, Skrinar GS, Bullen BA. Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone. J Clin Endocrinol Metab. 1991;72:1350–8.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Prior JC, Ho Yeun B, Clement P, Bowie L, Thomas J. Reversible luteal phase changes and infertility associated with marathon training. Lancet. 1982;1:269–70.CrossRefGoogle Scholar
  92. 92.
    Prior JC, Vigna YM, Alojado N, Sciarretta D, Schulzer M. Conditioning exercise decreases premenstrual symptoms: a prospective controlled six month trial. Fertil Steril. 1987;47:402–8.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Prior JC. Premenstrual symptoms and signs. In: Rabel RE, Bope ET, editors. Conn’s current therapy 2002. New York: W.B. Saunders Company; 2002. p. 1078–80.Google Scholar
  94. 94.
    Prior JC, Konishi C, Hitchcock CL, Kingwell E, Janssen P, Cheung AP, et al. Does molimina indicate ovulation? Prospective data in a hormonally documented single-cycle in spontaneously menstruating women. Int J Environ Res Pub Health. 2018;15(5):1016.CrossRefGoogle Scholar
  95. 95.
    Prior JC. Luteal phase defects and anovulation: adaptive alterations occurring with conditioning exercise. Semin Reprod Endocrinol. 1985;3:27–33.CrossRefGoogle Scholar
  96. 96.
    Bonen A. Exercise-induced menstrual cycle changes a functional, temporary adaptation to metabolic stress. Sports Med. 1994;17(6):373–92.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Cohen G, Prior JC, Vigna YM, Pride SM. Intense training during the first two trimesters of unapparent pregnancy. Phys Sportsmed. 1989;17:11–7.CrossRefGoogle Scholar
  98. 98.
    Li D, Hitchcock CL, Barr SI, Yu T, Prior JC. Negative spinal bone mineral density changes and subclinical ovulatory disturbances--prospective data in healthy premenopausal women with regular menstrual cycles. Epidemiol Rev. 2014;36(137):147.Google Scholar
  99. 99.
    Prior JC. Ovulatory disturbances and amenorrhea: a physiologic approach to diagnosis and therapy. In: Rosenberg JA, editor. Women’s health in primary care. Baltimore: Williams & Wilkins; 1997. p. 437–52.Google Scholar
  100. 100.
    Prior JC. Progesterone for the prevention and treatment of osteoporosis in women. Climacteric. 2018;21:366–74.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Goshtasebi A, Subotic Brajic T, Scholes D, Beres Lederer Goldberg T, Berenson A, Prior JC. Adolescent use of combined hormonal contraception and peak bone mineral density accrual: a meta-analysis of international prospective controlled studies. Clin Endocrinol. 2019;90(4):517–24.CrossRefGoogle Scholar
  102. 102.
    Prior JC. Adolescents’ use of combined hormonal contraceptives for menstrual cycle-related problem treatment and contraception: evidence of potential lifelong negative reproductive and bone effects. Women’s Reprod Health. 2016;3(2):73–92.CrossRefGoogle Scholar
  103. 103.
    Falsetti L, Gambera A, Barbetti L, Specchia C. Long-term follow-up of functional hypothalamic amenorrhea and prognostic factors. J Clin Endocrinol Metab. 2002;87(2):500–5.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Powell KE, Thompson PD, Caspersen CJ, Kendrick JS. Physical activity and the incidence of coronary heart disease. Ann Rev Public Health. 1987;8:253–87.CrossRefGoogle Scholar
  105. 105.
    Petit MA, Prior JC, Barr SI. Running and ovulation positively change cancellous bone in premenopausal women. Med Sci Sports Exerc. 1999;31(6):780–7.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    McCann L, Holmes DS. Influence of aerobic exercise on depression. J Pers Soc Psychol. 1984;46:1142–7.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Angela Y. Liu
    • 1
  • Moira A. Petit
    • 2
  • Jerilynn C. Prior
    • 3
    Email author
  1. 1.University of British Columbia, Medicine, Division of EndocrinologyVancouverCanada
  2. 2.Activ8, LLCSt. PaulUSA
  3. 3.University of British Columbia, Medicine, Division of Endocrinology and MetabolismVancouverCanada

Personalised recommendations