Summary
This article aims to clarify why, and by which mechanisms, exercise may influence the normal menstrual cycle. Therefore, the vast amount of literature on this subject is reviewed and a critical appraisal of the most widespread hypotheses is offered.
The strikingly low body mass which frequently accompanies exercise-related menstrual irregularities (ERMI) has led some authors to develop a hypothesis which postulates that a critical percentage of body fat is essential to trigger normal menstruation. The relevance of any reference to anorexia nervosa to support this view lacks consistency: female athletes differ in many ways from patients with anorexia nervosa, not least in their excellent physical status which is essential to deliver first-class performances.
ERMI is not identical to the so-called female athlete triad, a complicated pathology that involves ERMI, premature osteoporosis and disordered eating. ERMI itself does not seem to have any substantial pathological effects as long as attention is paid to preventing osteoporosis or stress fractures which may result from prolonged hypo-estrogenaemia. In the female athlete with ERMI who wishes to conceive, the accompanying subfertility may necessitate a response other than a prompt reduction in training intensity, as this is hardly a first choice for any top athlete.
During recent years, a number of prospective studies have greatly contributed to our understanding of the complexity of the mechanisms involved in ERMI. Older hypotheses, such as those considering hyperprolactinaemia as the cornerstone of ERMI, have now been firmly rejected. The present hypotheses emphasise the importance of caloric deficiency and limited energy availability, although they still fail to identify the actual mechanism that causes ERMI. There is, however, evidence that ERMI is produced by a disturbance of the hypothalamic gonadotrophin-releasing hormone oscillator. This disturbance is caused by either an insufficient estrogen or progesterone feedback or by an imbalance of local opioid peptide and catecholamine activities mediated by γ-aminobutyric acid (GABA), corticotrophin-releasing hormone and insulin-like growth factor-1.
More recent experiments have also linked ERMI with changes in steroid metabolism, in particular, an increasing activity of catecholestrogens possibly leading to enhanced intracerebral noradrenaline (norepinephrine) levels that may interfere with normal gonadotrophin release.
This article demonstrates that the outcome of the many studies on ERMI is characterised by much controversy and numerous methodological flaws. The importance and complexity of some recent findings necessitate a comprehensive study which links older and newer findings within a critical perspective.
Similar content being viewed by others
References
Keizer HA, Poortman J, Bunnik GSJ. Influence of physical exercise on sex-hormone metabolism. J Appl Physiol 1980; 48 (5): 765–9
Keizer HA, Van Schaik FW, De Beer EL. Exercise-induced changes in estradiol metabolism and their possible physiological meaning. Med Sport 1981; 14: 141–7
Keizer HA, Kuipers H, Verstappen FT. Limitations of concentration measurements for evaluation of endocrine status of exercising women. Can J Appl Sport Sci 1982; 7 (2): 79–84
Bonen A. Exercise-related disturbances in the menstrual cycle. In: Borer KT, Edington DW, White TR, editors. Frontiers of exercise biology. Champaign (IL): Human Kinetics Publishers, 1983: 214–37
Keizer HA. Exercise- and training-induced menstrual cycle irregularities (AMI). Int J Sports Med 1986; 7: 38–44
Baker ER. Menstrual dysfunction and hormonal status in athletic women: a review. Fertil Steril 1981; 36 (6): 691–6
Carlberg KA, Buckman MT, Peake GT. Body composition of oligo/amenorrheic athletes. Med Sci Sports Exerc 1983; 15 (3): 215–7
Frisch RE, Wyshak G, Vincent L. Delayed menarche and amenorrhea in ballet dancers. N Engl J Med 1980; 303: 17–9
Jurkowski JE, Jones NL, Walker WC. Ovarian hormonal responses to exercise. J Appl Physiol 1978; 44 (1): 109–14
Prior JC. Endocrine ‘conditioning’ with endurance training, a preliminary review. Can J Appl Sport Sci 1982; 7: 148–57
Prior JC, Cameron K, Yuen BH. Menstrual cycle changes with marathon training: anovulation and short-luteal phase. Can J Appl Sport Sci 1982; 7: 173–7
Shangold MM. Sports and menstrual function. Physician Sports Med 1980; 8 (8): 66–70
Harber VJ, Webber CE, Sutton JR. The effect of amenorrhea on bone calcaneal bone density and total bone turnover in runners. Int J Sports Med 1991; 12 (5): 505–8
Heinrich CH, Going SB, Pamentier RW. Bone mineral content of cyclically menstruating female resistance and endurance trained athletes. Med Sci Sports Exerc 1990; 22 (5): 558–63
Arena B, Maffuli N, Maffuli F. Reproductive hormone and menstrual changes with exercise in female athletes. Sports Med 1995; 19 (4): 278–87
Bonen A, Keizer HA. Athletic menstrual irregularity, endocrine responses to exercise and training. Physician Sports Med 1984; 12 (8): 78–90
Highet R. Athletic amenorrhea: an update on aetiology, complications and management. Sports Med 1989; 7 (2): 82–108
Keizer HA, Rogol AD. Physical exercise and menstrual cycle alterations: what are the mechanisms?. Sports Med 1990; 10 (4): 218–35
Kolka MA, Stephenson LA. The menstrual cycle and the female athlete. Phys Educ 1982; 39 (2): 136–41
Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc 1985; 17 (1): 56–72
Loucks AB, Cameron JB, De Souza MJ. Durability of the reproductive axis in eumenorrheic women during 1 yr of endurance training [letter]. J Appl Physiol 1993; 74 (4): 2045–6
Tremblay MS, Chu SY, Mureika R. Methodological and statistical considerations for exercise-related hormone evaluations. Sports Med 1995; 20 (2): 90–108
Vollmann RF. The menstrual cycle. Philadelphia (PA): W.B. Saunders, 1977
Brisson GR, Dulac S, Peronnet F. The onset of menarche: a late event in pubertal progression to be affected by physical training. Can J Appl Sport Sci 1982; 7 (2): 61–7
Frisch RE, Gotz-Welbergen AV, MacArthur JW. Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA 1981; 246: 1559–63
Mesaki N, Sasaki J, Shoji M. Delayed menarche followed by early onset of athletic training [English abstract]. Acta Obstet Gynaec Jpn 1984; 36 (1): 49–56
Warren MP, Brooks-Gunn J, Hamilton LH. Scoliosis and fractures in young ballet dancers. Relation to delayed menarche and secondary amenorrhea. N Engl J Med 1986; 314 (21): 1348–53
Warren MP. The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab 1980; 51: 1150–7
Stager JM, Robertshaw D, Miescher E. Delayed menarche in swimming in relation to age and onset of training and athletic performance. Med Sci Sports Exerc 1984; 16: 550–5
Malina RM. Menarche in athletes: a synthesis and hypothesis. Ann Hum Biol 1983; 10 (1): 1–24
Bonen A, Belcastro AN, Ling WY. Profiles of selected hormones during menstrual cycles of teenage athletes. J Appl Physiol 1981; 50: 545–51
Prior JC, Ho Yuen B, Clement P. Reversible luteal phase changes and infertility associated with marathon training. Lancet 1982; II (8292): 269–70
Prior JC, Vigna YM, Schulzer M. Determination of luteal phase length by quantitative basal temperature methods: validation against the midcycle LH peak. Clin Invest Med 1990; 13: 123–31
Shangold MM. Menstrual irregularity in athletes: basic principles, evaluation, and treatment. Can J Appl Sport Sci 1982; 7 (2): 68–70
Bauman JE. Basal body temperature: unreliable method of ovulation detection. Fertil Steril 1981; 36 (6): 729–33
Wetzels LCG, Hoogland HJ, De Haan J. Basal body temperature as a method of ovulation detection: comparison with ultrasonographical findings. Gynaecol Obstet Invest 1982; 13: 239–40
De Crée C, Lewin R, Ostyn M. Failure to induce ovulation with clomiphene citrate and bromocriptine in luteal deficient women athletes. Int J Sports Med 1991; 12 (3): 269–75
Loucks A, Mortola JF, Girton L. Alterations in the hypothalamicpituitary- ovarian and the hypothalamic-pituitary-adrenal axes in athletic women. J Clin Endocrinol Metab 1989; 68 (2): 402–11
Harlow SD, Matanoski GM. The association between weight, physical activity, stress and variation in the length of the menstrual cycle. Am J Epidemiol 1991; 133 (1): 38–49
Prior JC. Exercise-related adaptive changes of the menstrual cycle. In: MacLeod D., Maughan O, Nimmo M, et al., editors. Exercise: benefits, limits and adaptations. London: E. & F.N. Spon, 1987: 239–54
Bonen A. Exercise-induced menstrual cycle changes: a functional temporary adaptation to metabolic stress. Sports Med 1994; 17 (6): 373–92
Feicht CB, Sanborn C, Martin BJ. Is athletic amenorrhea specific to runners?. Am J Obstet Gynecol 1982; 143: 859–61
Glass AR, Deuster PA, Kyle SB. Amenorrhea in Olympic marathon runners. Fertil Steril 1987; 48 (5): 740–5
Lutter JM, Cushman S. Menstrual patterns in female runners. Physician Sports Med 1982; 10 (9): 60–72
Mann GV. Menstrual effects of athletic training. Med Sport 1981; 14: 198–9
Schwartz B, Cumming DC, Riordan E. Exercise-induced amenorrhea: a distinct identity. Am J Obstet Gynecol 1981; 141 (6): 662–70
Speroff L, Redwine DB. Exercise and menstrual dysfunction. Physician Sports Med 1980; 8: 41–52
Wakat DK, Sweeney KA, Rogol AD. Reproductive system function in women cross-country runners. Med Sci Sports Exerc 1982; 14: 263–9
Yen SSC. Female hypogonadotropic hypogonadism: hypothalamic amenorrhea syndrome. Endocrin Metabol Clin North Am (Neuroendocrinology II) 1993; 22 (1): 29–58
Baker ER, Mathur RS, Kirk RF. 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
Abraham SF, Beumont PJV, Fraser IS. Body weight, exercise and menstrual status among ballet dancers in training. Br J Obstet Gynaecol 1982; 89 (7): 507–10
Calabrese LH, Kirkendall DT, Floyd M. Menstrual abnormalities, nutritional patterns and body composition in female classical ballet dancers. Physician Sports Med 1983; 11 (2): 86–98
Graves JE, Pollock ML, Sparling PB. Body composition of elite female distance runners. Int J Sports Med 1987; 8 Suppl. 2: 96–102
Plowman SA, Liu NY, Wells CL. Body composition and sexual maturation in premenarcheal athletes and nonathletes. Med Sci Sports Exerc 1991; 23 (1): 23–9
Henley K. Exercise-induced menstrual dysfunction. Ann Rev Med 1988; 39: 443–51
Myburgh KH, Watkin VA, Noakes TD. Are risk factors for menstrual dysfunction cumulative. Physician Sports Med 1992; 20 (4): 114–25
Loucks AB, Horvath SM, Freedom PS. Menstrual status and validation of body fat prediction in athletes. Hum Biol 1984; 56: 383–92
Frisch RE, Revelle R, Cook S. Components of weight at menarche and the initiation of the adolescent growth spurt in girls: estimated total water lean body weight and fat. Hum Biol 1973; 45: 449–83
Gray P, Dale E. Variables associated with secondary amenorrhea. J Sport Sci 1983; 1: 55–67
Cohen JL, Kim CS, May PB. Exercise, body weight and amenorrhea in professional ballet dancers. Physician Sports Med 1982; 10 (4): 92–101
Frisch RE, MacArthur JW. Menstrual cycles: fatness as a determinant of minimum weight for height necessary for the maintenance or onset of menstruation. Science 1974; 185: 949–51
Brooks SM, Sanborn CF, Albrecht BH. Diet in athletic amenorrhea. Lancet 1984; II: 559–60
Mansfield MJ, Emans SJ. Anorexia nervosa, athletics and amenorrhea. Pediatr Clin North Am 1989; 36: 533–49
Sanborn CF, Martin BJ, Wagner WW. Is athletic amenorrhoea specific to runners?. Am J Obstet Gynecol 1982; 143: 859–61
Beumont PJV, Abraham SF, Argall WJ. Plasma gonadotrophins and LHRH infusions in anorexia nervosa. Obstet Gynecol Surv 1980; 130: 609–10
Brooks-Gunn J, Warren MP, Hamilton LH. The relation of eating problems and amenorrhea in ballet dancers. Med Sci Sports Exerc 1987; 19 (1): 41–4
Sirinathsinghj DJ, Mills IH. Concentration of plasma dehydroepiandrosterone, 5-androstenediol and their sulphates, testosterone, and cortisol in normal healthy women and in women with anorexia nervosa. Acta Endocrinol 1985; 108 (2): 255–60
Loucks AB, Horvath SM. Exercise-induced stress responses of amenorrheic and eumenorrheic runners. J Clin Endocrinol Metab 1984; 59 (6): 1109–20
Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol 1993; 264 (33): R924–30
Loucks AB, Vaitukaitis J, Cameron JL. The reproductive system and exercise in women. Med Sci Sports Exerc 1992; 24 (6 Suppl.): S288–93
Loucks AB, Verdun M, Heath EM. Low energy availability, not the stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 1998; 84 (1): 37–46
Wilmore JH, Wambsgans KC, Brenner M. Is there energy conservation in amenorrheic compared with eumenorrheic distance runners?. J Appl Physiol 1982; 72 (1): 15–22
Dominguez C. Altered binding of serum thyroid hormone to thyroxine-binding globulin in women with functional hypothalamic amenorrhea. Fertil Steril 1997; 68 (6): 992–6
Carlberg KA, Buckman MT, Peake GT. Body composition of oligo-amenorrheic athletes. Med Sci Sports Exerc 1983; 15 (3): 215–7
Katch FI, Katch VL, Behnke AR. The underweight female. Physician Sports Med 1980; 8: 55–60
McArthur JW, Bullen BA, Beitins IZ. Hypothalamic amenorrhea in runners of normal body composition. Endocr Res Comm 1980; 7: 13–25
Bullen BA, Skrinar GS, Beitins IZ. Induction of menstrual cycle disorders by strenuous exercise in untrained women. N Engl J Med 1985; 312: 1349–53
Trussel J. Statistical flaws in evidence for the Frisch hypothesis that fatness triggers menarche. Hum Biol 1980; 52 (2): 711–20
De Souza MJ, Maresh CM, Abraham A. Body compositions of eumenorrheic, oligomenorrheic and amenorrheic runners. J Appl Sport Sci Res 1987; 2: 13–5
Sanborn CF, Albrecht BH, Wagner Jr WW. Athletic amenorrhea: lack of association with body fat. Med Sci Sports Exerc 1987; 19 (3): 207–12
Wells RF. Body composition and the menstrual cycle. Excel 1988; 4 (3): 18–9
Bronson FH, Manning JM. The energetic regulation of ovulation: A realistic role for body fat. Biol Reprod 1991; 44 (6): 945–50
Sinning WE, Little KD. Body composition and menstrual function in athletes. Sports Med 1987; 4: 35–45
Vigersky RA, Andersen AE, Thompson RH. Hypothalamic dysfunction in secondary amenorrhea, associated with simple weight loss. N Engl J Med 1977; 297: 1141
Warren MP, Vande Wiele RL. Clinical and metabolic features of anorexia nervosa. Am J Obstet Gynecol 1973; 117: 435
Deuster PA, Kyle SB, Moser PB. Nutritional survey of highly trained women runners. Fertil Steril 1986; 46: 636–43
Keys A, Brozek J. The biology of human starvation. Minneapolis (MN): University of Minnesota Press, 1950
Dale E, Goldberg DL. Implications of nutrition in athletes’ menstrual cycle irregularities. Can J Appl Sport Sci 1982; 7 (2): 74–8
Smith NJ. Excessive weight loss and food aversion in athletes simulating anorexia nervosa. Pediatrics 1980; 66 (1): 139–42
Yates A, Leekey K, Shisslak CM. Running An analogue of anorexia?. N Engl J Med 1983; 308: 251–5
Loosli AR, Gillien DM, Benson J. Inadequate nutrition and chronic caloric restriction among ballet dancers. Med Sci Sports Exerc 1985; 77 (2): 201
Kaiserauer SA, Snyder AC, Sleeper M. Nutritional, physiological, and menstrual status of the distance runner. Med Sci Sports Exerc 1989; 21: 120–5
Myerson M, Gutin B, Warren MP. Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc 1991; 23: 15–22
Nelson ME, Fisher EC, Catsos PO. Diet and bone status in amenorrheic runners. J Clin Nutr 1986; 43: 910–6
Mulligan K, Butterfield GE. Discrepancies between energy intake and expenditure in physically active women. Br J Nutr 1990; 64: 23–36
Dueck CA, Manore MM, Matt KS. Role of energy balance in athletic menstrual dysfunction. Int J Sport Nutr 1996; 6: 165–90
Edwards JE, Lindeman A, Stanger J. Energy balance in highly trained female endurance runners. Med Sci Sports Exerc 1993; 25: 1398–404
De Crée C, Lewin A, Barros A. Hypoestrogenemia rhabdomyelysis in the female judoist: a new worrying phenomenon?. J Clin Endocrinol Metab 1995; 80 (12): 3639–46
Borgen JS, Corbin Ch B. Eating disorders among female athletes. Physician Sports Med 1987; 15 (2): 88–95
Walberg JL, Johnston CS. Menstrual function and eating behavior in female recreational weight lifters and competitive body builders. Med Sci Sports Exerc 1991; 23 (1): 30–6
Johnson MD. Disordered eating in active and athletic women. Clin Sports Med 1994; 13: 355–69
Weight LM, Noakes TD. Is running an analog of anorexia?. A survey of the incidence of eating disorders in female distance runners. Med Sci Sports Exerc 1987; 19 (3): 213–7
Schoeller DA, Bandini LG, Dietz WH. Inaccuracies in selfreported intake identified by comparison with the doubly labelled water method. Can J Physiol Pharmacol 1990; 68: 941–9
Pirke KM, Schweiger U, Strowitzki T. Dieting causes menstrual irregularities in normal weight young women through impairment of episodic luteinizing hormone secretion. Fertil Steril 1989; 51: 2263–8
De Souza MJ, Metzger DA. Reproductive dysfunction in amenorrheic athletes and anorexic patients: a review. Med Sci Sports Exerc 1991; 23 (9): 995–1007
Frisch RE. Amenorrhea, vegetarianism, and/or low fat. Lancet 1986; I: 1024
Hill PL, Garbaczewski L. Haley N. Diet and follicular development. Am J Clin Nutr 1984; 39: 771–7
Morimoto Y, Dishi T, Hanasaki N. Interrelations among amenorrhea, serum gonadotropins and body weight in anorexia nervosa. Endocr Jpn 1980; 27: 191–4
Steiner RA. Nutritional and metabolic factors in the regulation of reproductive hormone secretion in the primate. Proc Nutr Soc 1987; 46: 159–75
Schweiger U, Laessle R, Pfister H. Diet-induced menstrual irregularities: effects of age and weight loss. Fertil Steril 1987; 48 (5): 746–51
Mesaki N, Sasaki J, Shoji M. Menstrual characteristics in college athletes [English abstract]. Acta Obst Gynaec Jpn 1984; 36 (2): 247–54
Morin LP. Environment and hamster reproduction: responses to phase-specific starvation during estrous cycle. Am J Physiol 1986; 251: R663–669
Gray JM, Greenwood MRC. Time course of effects of ovarian hormones on food intake and metabolism. Am J Physiol 1982; 243: E407–12
Enoch MA, Kaye WH, Rotondo A. 5-HT2A promoter polymorphism - 1438G/A, anorexia nervosa, and obsessive-compulsive disorder. Lancet 1998; 351 (9118): 1785
Moisan J, Meyer F, Gingra S. Leisure physical activity and age at menarche. Med Sci Sports Exerc 1991; 23 (10): 1170–5
Yaginuma T. Progress and therapy of stress amenorrhea. Fertil Steril 1979; 32: 36–9
Shangold MM, Levine HS. The effect of marathon training upon menstrual function. Am J Obstet Gynecol 1982; 143 (8): 862–9
Webb JL, Millan DL, Stolz CJ. Gynecological survey of American female athletes competing at the Montreal Olympic Games. J Sport Med Phys Fitness 1979; 12: 405–12
Tomten SE, Høstmark AT, Strømme SB. Exercise intensity: an important factor in the etiology of menstrual dysfunction?. Scan J Med Sci Sports 1996; 6: 329–36
Keizer HA, Platen P, Menheere PP. The hypothalamic/pituitary axis under exercise stress: the effects of aerobic and anaerobic training. In: Rogol A, Laron Z, editors. Hormones and sport. Serono Symposium Publications (vol. 55). New York: Raven Press, 1989: 101–15
Zaharieva E. Survey of sports women at the Tokyo Olympics. J Sports Med Phys Fitness 1965; 5: 215–9
Warren MP, Jeweewicz R, Dyren Furth I. The significance of weightloss in the evaluation of pituitary response to LH-RH in women with secondary amenorrhea. J Clin Endocrinol Metab 1975; 40: 601
Dixon G, Eurman P, Stern B. Hypothalamic function in amenorrheic runners. Fertil Steril 1984; 42: 377–83
Mougin C, Baulay A, Henriet MT. Assessment of plasma opioid peptides, b-endorphin and met-enkephalin, at the end of an international nordic ski race. Eur J Appl Physiol 1987; 56 (3): 281–6
Qian P. Menstrual dysfunction in Norwegian top athletes. Acta Obstet Gynecol Scand 1984; 63: 693–7
Güler F, Hasçelik Z. Menstrual dysfunction rate and delayed menarche in top athletes of team games. Sports Med Training Rehab 1993; 4 (2): 99–106
Mesaki N, Sasaki J, Nabeshima Y. Decrease of pulsatile gonadotropin secretion in female athletes. Jpn J Phys Fitness Sports Med 1991; 40 (4): 365–71
Ronkainen H, Pakarinen A, Kauppila A. Pubertal and menstrual disorders of female runners, skiers and volleyball players. Gynecol Obstet Invest 1984; 18: 183–9
Kuipers H, Keizer HA. Overtraining in elite athletes: a review and directions for the future. Sports Med 1988; 6: 79–92
Keller N, Richardson UI, Yates FE. Protein binding and the biological activity of corticosteroids: the in vivo induction of hepatic and pancreatic alanine amnio-transferases by corticosteroids in normal and estrogen-treated rats. Endocrinology 1969; 84: 49
Pardridge W. Transport of protein-bound hormones into tissues in vivo. Endocr Rev 1981; 2 (1): 103–23
Berg A, Keul J. Physiological and metabolic responses of female athletes during laboratory and field exercise. In: Women and sport: series on medicine and sport 14. Basel: Karger, 1981: 125–40
Speroff L, Glass RH, Kase NG. Clinical gynaecological endocrinology and infertility. 3rd ed. Baltimore: Williams & Wilkins, 1983
Vervoorn C, Quist AM, Erich WR. Trainingsbegeleiding met hulp van hormoongegevens (Coaching and use of hormonal data) [English abstract]. Geneeskd Sport 1990; 23 (2): 65–73
Vervoorn C, Vermulst L, Boelens-Quist AM. Toepassing van hormoononderzoek bij trainingsbegeleiding van Nederlandse toproeisters (Application of hormonal investigation in the coaching of Dutch top-oarswomen) [English abstract]. Geneeskd Sport 1990; 23 (3): 87–96
Scott G, Tuttle WW. The periodic fluctuation in physical efficiency during the menstrual cycle. Res Q 1932; 3: 137–44
Bemben DA, Salm PC, Salm AJ. Ventilatory and blood lactate responses to maximal treadmill exercise during the menstrual cycle. J Sports Med Phys Fitness 1995; 35 (4): 257–62
De Bruyn-Prévost P, Masset C, Sturbois X. Physiological response from 18-25 years women to aerobic and anaerobic physical fitness tests at different periods during the menstrual cycle. J Sports Med Phys Fitness 1984; 24: 144–8
De Souza MJ, Maguire MS, Rubin KR. Effects of menstrual phase and amenorrhea on exercise performance in runners. Med Sci Sports Exerc 1990; 22 (5): 575–80
Higgs SZ, Robertson LA. Cyclic variations in perceived exertion and physical work capacity in females. Can J Appl Sport Sci 1981; 6 (4): 191–6
Jurkowski JE Hall, Jones NL, Toews CJ. Effects of menstrual cycle on blood lactate, O2 delivery, and performance during exercise. J Appl Physiol 1981; 51 (6): 1493–9
Stephenson LA, Kolka MA, Wilkerson JE. Perceived exertion and anaerobic threshold during the menstrual cycle. Med Sci Sports Exerc 1982; 14: 218–22
Frye AJ, Kamon E. Responses to dry heat of men and women with similar aerobic capacities. J Appl Physiol 1981; 50: 65–70
Kawahata A. Sex differences in sweating. In: Yoshimura EH, Ogata K, Itoh S, editors. Essential problems in climactic physiology. Kyoto: Nakado, 1960: 169–84
Schoene RB, Robertson HT, Pierson DJ. Respiratory drives and exercises in menstrual cycles of athletic and non-athletic women. J Appl Physiol 1981; 50 (6): 1300–5
Lebrun CM, McKenzie DC, Prior JC. Effects of menstrual cycle phase on athletic performance. Med Sci Sports Exerc 1995; 27 (3): 437–44
Lebrun CM. The effect of the phase of the menstrual cycle and the birth control pill in athletic performance. Clin Sports Med 1994; 13: 419–41
Schoene RB, Pierson DJ, Lakshminaragavan S. Effect of medroxyprogesteroneacetate on respiratory drives and occlusion pressure. Bull Eur Physiopath Resp 1980; 16: 645–53
Keizer HA, Kuipers H, de Haan J. Multiple hormonal responses to physical exercise in eumenorrheic trained and untrained women. Int J Sports Med 1987; 8 Suppl. 3: 139–50
Lavoie J.-M, Dionne N, Helie R. Menstrual cycle phase dissociation of blood glucose homeostasis during exercise. J Appl Physiol 1987; 62 (3): 1084–9
Nicklas BJ, Hackney AC, Sharp RL. The menstrual cycle and exercise: performance, muscle glycogen and substrate responses. Int J Sports Med 1989; 10: 264–9
Achmed-Soraur H, Bailey CJ. Role of ovarian hormones in the long-term control of glucose homeostasis, glycogen formation and gluconeogenesis. Ann Nutr Metab 1981; 25: 208–12
Kendrick ZV, Ellis GS. Effect of estradiol on tissue glycogen metabolism and lipid availability in exercising male rats. J Appl Physiol 1991; 71 (5): 1694–9
Bonen A, Haynes FJ, Watson-Wright W. Effects of the menstrual cycle on metabolic responses to exercise. J Appl Physiol 1983; 55: 1506–13
Eston RG, Burke EJ. Effects of the menstrual cycle on selected responses to short constant-load exercise. J Sport Sciences 1984; 2 (2): 145–53
Lamont LS. Lack of influence of the menstrual cycle on blood lactate. Physician Sports Med 1986; 14: 159–63
Quadagno DL, Faquin L, Lim G-N. The menstrual cycle: does it affect athletic performance?. Physician Sports Med 1991; 19: 121–4
Casper RF, Wilkinson D, Cotteral MA. The effect of increased cardiac output on luteal phase gonadal steroids: a hypothesis for runners’ amenorrhea. Fertil Steril 1984; 41: 264–368
Khodiguian N, Farrar PA, Nguyen M. Effect of menstrual cycle on ligamentous knee joint laxity [abstract 965]. Med Sci Sports Exerc 1994; 26 (5 Suppl.): S172
Chen H, Tang Y. Effects of menstrual cycle on respiratory muscle function. Am Rev Resp Dis 1989; 140: 1359–62
Sarwar R, Beltran Niclos B, Rutherford OM. Changes in muscle strength, relaxation rate and fatiguability during human menstrual cycle. J Physiol 1996; 493 (1): 267–72
Davies BN, Elford JC, Jamieson KF. Variations in performance of simple muscle tests at different phases of the menstrual cycle. J Sports Med Phys Fitness 1991; 31 (4): 532–7
Greeves JP, Cable NT, Luckas MJ. Effects of acute changes in oestrogen on muscle function of the first dorsal interosseus muscle in humans. J Physiol 1997; 500 (1): 265–70
Rice PL. Relationship of estrogen to strength, percent body fat and oxygen uptake in women. J Sports Med Phys Fitness 1988; 281: 45–50
Phillips SK, Rutherford OM, Birch K. Hormonal influences on muscle force: evidence for an inotropic effect of oestrogen. Sports Exerc Injury 1995; 1: 58–63
Dibrezzo RO, Fort IL, Brown B. Dynamic strength and work variations during three stages of the menstrual cycle. J Orthopaedic Sports Phys Ther 1988; 10: 113–6
Dibrezzo R, Fort IL, Brown B. Relationships among strength, endurance, weight and body fat during three phases of the menstrual cycle. J Sports Med Phys Fitness 1991; 31: 89–94
Gaebelein CJ, Senay Jr LC. Vascular volume dynamics during ergometer exercise at different menstrual phases. Eur J Appl Physiol 1982; 50 (1): 1–11
Nielsen B, Sjøgaard G, Bonde-Petersen F. Cardiovascular, hormonal and body fluid changes during prolonged exercise. Eur J Appl Physiol 1984; 53: 63–70
Dombovy ML, Bonekat HW, Williams TJ. Exercise performance and ventilatory response in the menstrual cycle. Med Sci Sports Exerc 1987; 19: 111–7
Haymes EM. Physiological responses of female athletes to heat stress: a review. Med Sci Sports Exerc 1984; 12 (3): 45–59
Doskin VA, Kozeeva TV, Lisitskaya TS. Changes in working capacity of female athletes in different phases of the menstrual cycle. Hum Physiol 1980; 5: 144–9
Puretz SL. Menses and exercise: attitudes and actions. J Sports Med Phys Fitness 1986; 26: 140–5
Robertson LA, Higgs SL. Menstrual cycle variations in physical work capacity, post exercise blood lactate and perceived exertion [abstract]. Can J Appl Sport Sci 1983; 8: 220
Friedmann B, Kindermann W. Energy metabolism and regulatory hormones in women and men during endurance exercise. Eur J Appl Physiol 1989; 59 (1-2): 1–9
Eston RG. The regular menstrual cycle and athletic performance. Sports Med 1984; 1 (6): 431–45
Bolch OH, Warren JC. Induction of premature menstruation with anabolic steroids. Am J Obstet Gynecol 1973; 117 (1): 121–5
Donike M, Ueki M, Kuroda Y. Detection of dihydrotestosterone (DHT) doping: alterations in steroid profile and reference ranges for DHT and its 5a-metabolites. J Sports Med Phys Fitness 1995; 35 (4): 235–50
Sutton JR, Coleman MJ, Casey JH. Androgen responses during physical exercise. BMJ 1973; 1 (352): 520–2
Keizer HA, Beckers E, de Haan J. Exercise-induced changes in the percentage of free testosterone and estradiol in trained and untrained women. Int J Sports Med 1987; 8 Suppl. 3: 151–3
Brown WJ. Oestradiol response to exercise ‘through the ages’. Aust J Sci Med Sport 1992; 24 (1): 18–24
Bunt JC. Metabolic actions of estradiol: significance for acute and chronic response. Med Sci Sports Exerc 1990; 22: 286–90
Bunt JC, Bahr JM, Bemben DA. Comparison of estradiol and testosterone levels during and immediately following prolonged exercise in moderately active and trained males and females. Endocr Res 1987; 13 (2): 157–72
Mesaki N, Sasaki J, Shoji M. Hormonal changes during incremental exercise in athletic women [English abstract]. Acta Obst Gynaec Jpn 1986; 38 (1): 45–52
Mesaki N, Sasaki J, Shoji M. Hormonal changes during continuous exercise in athletic women [English abstract]. Acta Obst Gynaec Jpn 1987; 39 (1): 63–9
Bullen BA, Skrinar GS Beitins IZ. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J Appl Physiol 1984; 56 (6): 1453–63
Cumming DC, Rebar RW, Stern B. The effects of acute exercise on endocrine homeostasis. In. Rogol A, Laron Z, editors. Hormones and sport. Serono Symposium Publications (vol. 55). New York: Raven Press, 1989: 73–87
Galbo H. Hormonal and metabolic adaptation to exercise. Stuttgart: Georg Thieme Verlag, 1983
Baker ER, Mathur RS, Kirk RF. Plasma gonadotropins, prolactin and steroid hormone concentration in female runners immediately after a long distance run. Fertil Steril 1982; 38: 38–41
Brisson GR, Volle MA, De Caruifel D. Exercise dissociation of the blood prolactin response in young women according to sports habits. Horm Metab Res 1980; 12: 201–5
Chang FE, Dodds WG, Sullivan M. The acute effects of exercise on prolactin and growth hormone secretion: comparison between sedentary women and women runners with normal and abnormal menstrual cycles. J Clin Endocrinol Metab 1986; 62 (3): 551–6
Keizer HA, van Soest OP, Beckers E. Exercise-induced changes in estradiol metabolism and their possible physiological meaning. Med Sport 1981; 14: 141–7
Mesaki N, Motobu M, Sasaki J. Hypothalamic-pituitary function in female athletes [English abstract]. Jpn J Fertil Steril 1988; 33 (2): 291–6
Mesaki N, Sasaki J, Nabeshima Y. Exercise decreases the pulsatile secretion of luteinizing hormone. Jpn J Fertil Steril 1992; 37 (1): 16–21
Zichella L, Agatone S, Carilli I. Sport and reproduction in women. Med Sports 1981; 14: 209–15
Carr DB, Bullen BA, Skrinar GS. Physical conditioning facilitates the exercise-induced secretions of beta-endorphin and beta-lipotropin in women. N Engl J Med 1981; 305 (10): 560–3
Heitkamp H.-C, Huber W, Scheib K. b-Endorphin and adrenocorticotrophin after incremental exercise and marathon running: female responses. Eur J Appl Physiol 1996; 72 (5-6): 417–24
McMurray RG, Forsythe WA, Mar MH. Exercise intensityrelated responses of b-endorphin and catecholamines. Med Sci Sports Exerc 1987; 19 (6): 570–4
Rakhila P, Hakala E, Salminen K. Responses of plasma endorphins to running exercises in male and female endurance athletes. Med Sci Sports Exerc 1987; 19 (5): 451–5
Rauramo I, Salminen K, Laatikainen T. Release of b-endorphin in response to physical exercise in non-pregnant and pregnant women. Acta Obstet Gynecol Scand 1986; 65 (6): 609–12
Troullos ES, Hargreaves KM, Goldstein DS. Epinephrine suppresses stress-induced increases in plasma immunoreactive b-endorphin in humans. J Clin Endocrinol Metab 1989; 69 (3): 546–51
Viswanathan M, Van Dijk JP, Graham TE. Exercise- and coldinduced changes in plasma b-endorphin and b-lipotropin in men and women. J Appl Physiol 1987; 62 (2): 622–7
Goldfarb AH, Jamurtas AZ. b-Endorphin response to exercise: an update. Sports Med 1997; 24 (1): 8–16
Mesaki N, Sasaki J, Motobu M. Effect of naloxone on hormonal changes during exercise. Acta Obst Gynaec Jpn 1989; 41 (12): 1991–8
Métivier G. Pituitary and gonadal secretory variations and control mechanisms during physical exercise. J Sports Med 1985; 25: 18–26
Yahiro J, Glass AR, Ferns WB. Exaggerated gonadotropin response to luteinizing hormone-releasing hormone in amenorrheic runners. Am J Obstet Gynecol 1987; 156 (3): 586–91
Sforzo GA. Opioids and exercise: an update. Sports Med 1989; 7 (2): 82–108
Platen P, Schenkmann A, Velde C. Effects of high voluminous training and hypocaloric diets on the hypothalamo-pituitarythyroidal axis in female athletes [abstract]. Med Sci Sports Exerc 1996; 28 (5 Suppl.): S25
Weltman JY, Veldhuis JD, Weltman AL. Reliability of estimates of pulsatile characteristics of luteinizing hormone (LH) and growth hormone (GH) release in women. J Clin Endocrinol Metab 1990; 71: 1646–52
Hornum M, Cooper DM, Brasel JA. Exercise-induced changes in circulating growth factors with cyclic variation in plasma estradiol in women. J Appl Physiol 1997; 82 (6): 1946–51
Shangold MM, Gatz ML, Thysen B. Acute effects of exercise on plasma concentrations of prolactin and testosterone in recreational women runners. Fertil Steril 1981; 35 (6): 699–702
De Crée C. The possible role of endogenous opioid peptides and catecholestrogens in provoking menstrual irregularities in women athletes. Int J Sports Med 1990; 11 (5): 329–48
De Crée C, Ball P, Seidlitz B, et al. Plasma 2-hydroxycatecholestrogen responses to acute submaximal and maximal exercise in untrained women. J Appl Physiol 1997; 82 (1): 364–70
De Crée C, Ball P, Seidlitz B, et al. Responses of catecholestrogen metabolism to acute graded exercise in normal menstruating women before and after training training. J Clin Endocrinol Metab 1997; 82 (10): 3342–8
De Crée C, Van Kranenburg G, Geurten P, et al. 4-Hydroxycatecholestrogen metabolism responses to exercise and training: possible implications for menstrual cycle irregularities and breast cancer. Fertil Steril 1997; 67 (3): 505–16
Bonen A, Keizer HA. Pituitary, ovary and adrenal hormone responses to marathon running. Int J Sports Med 1987; 8 Suppl. 3: 161–7
Bortz WW. II, Angwin P, Meford IN. Catecholamines, dopamine, and endorphin levels during extreme exercise. N Engl J Med 1981; 305: 466–7
Cumming DC, Vickovic MM, Wall SR. The effect of acute exercise on pulsatile release of luteinizing hormone in women runners. Am J Obstet Gynec 1985; 153 (5): 482–5
Demers LM, Harrison TS, Halbert DR. Effect of prolonged exercise on plasma prostaglandin levels. Prostaglandins Med 1981; 6: 413–8
Hale RW, Kosasa T, Krieger J. A marathon: the immediate effect on female runners’ luteinizing hormone, follicle stimulating hormone, prolactin, testosterone, and cortisone levels. Am J Obstet Gynecol 1984; 146 (5): 550–6
McArthur JW. Endorphins and exercise in females: possible connection with reproductive dysfunction. Med Sci Sports Exerc 1985; 17 (1): 82–8
Strassman RJ, Appenzeller O, Lewy AJ. Increase in plasma melatonin, b-endorphin, and cortisol after a 28.5 mile mountain race: relationship to performance and lack of effect of Naltrexone. J Clin Endocrinol Metab 1989; 69 (3): 540–5
Montagnani CF, Arena B, Maffuli N. Estradiol and progesterone during exercise in healthy untrained women. Med Sci Sports Exerc 1992; 24 (7): 764–8
Häkkinen K, Pakarinen A, Kyröläinen H. Neuromuscular adaptations and serum hormones in females during prolonged power training. Int J Sports Med 1990; 11 (2): 91–8
Kraemer WJ, Fleck SJ, Dziados JE. Changes in hormonal concentrations after different heavy-resistance exercise protocols in women. J Appl Physiol 1993; 75 (2): 594–604
Kraemer WJ, Gordon SE, Fleck SJ. Endogenous anabolic hormonal and growth factor responses to heavy resistance exercise in male and females. Int J Sports Med 1991; 12 (2): 228–35
Walberg-Rankin J, Franke WD, Gwazdaukas FC. Response of beta-endorphin and estradiol to resistance exercise in females during energy balance and energy restriction. Int J Sports Med 1992; 13 (7): 542–7
Weiss LW, Cureton KJ, Thompson FN. Comparison of serum testosterone and androstenedione responses to weight lifting in men and women. Eur J Appl Physiol 1983; 50 (3): 413–20
Cumming DC, Wall SR, Galbraith MA. Reproductive hormone responses to resistance exercise. Med Sci Sports Exerc 1987; 19 (3): 234–8
Kraemer R, Heleniak R, Tryniecki J. Follicular and luteal phase hormonal responses to low-volume resistive exercise. Med Sci Sports Exerc 1995; 27 (6): 809–17
Peltenburg AL, Erich WB, Thijssen JH. Sex hormone profiles of premenarcheal athletes. Eur J Appl Physiol 1984; 52 (4): 385–92
Carli G, Martinelli A, Balid L. The effect of swimming training on hormone levels in girls. J Sports Med 1983; 23: 45–50
Keizer HA. Hormonal responses in women as a function of physical exercise and training. Int J Sports Med 1987; 8 Suppl. 3: 137–74
Keizer HA, Kuipers H, de Haan J. Effect of a 3-month endurance training program on metabolic and multiple hormonal responses to exercise. Int J Sports Med 1987; 8 Suppl. 3: 154–60
Keizer HA, van Soest OP. Exercise-induced androgen responses in trained and untrained women. Exerc Physiol 1986; 2: 35–48
Tegelman R, Johansson C, Hemmingson P. Endogenous anabolic and catabolic steroid hormones in male and female athletes during off season. Int J Sports Med 1989; 10 (2): 103–6
Broocks A, Pirke KM, Sschweiger U. Cyclic ovarian function in recreational athletes. J Appl Physiol 1990; 68 (5): 2083–6
Boyden TW, Pamenter RW, Stanforth P. Sex steroids and endurance running in women. Fertil Steril 1983; 39: 629–32
Russel JB, Mitchell D, Musey PI. The relationship of exercise to anovulatory cycles in female athletes: hormonal and physical characteristics. Obstet Gynecol 1984; 63 (4): 452–6
De Crée C, Ball P, Seidlitz B, et al. Effects of a training program on resting plasma 2-hydroxycatecholestrogen levels in eumenorrheic women. J Appl Physiol 1997; 83 (5): 1551–6
Snow R, Barbieri RL, Frisch R. Estrogen 2-hydroxylase oxidation and menstrual function among elite oarswomen. J Clin Endocrinol Metab 1989; 69 (2): 369–76
De Crée C, Van Kranenburg G, Geurten P, et al. Exerciseinduced changes in enzymatic O-methylation of catcholestrogens by erythrocytes of normal menstruating females. Med Sci Sports Exerc 1997; 29 (12): 1580–7
Sanfilippo JS, Nealon NA. Relationship between beta endorphin and prolactin in female runners. Infertility 1985; 8 (1): 59–67
Westerlind KC, Byrnes WC, Freedson PS. Exercise and serum androgens in women. Physician Sports Med 1987; 15 (5): 87–94
Jenkins PJ, Ibanez-Santos X, Holly J. IGFBP-1: A metabolic signal associated with exercise-induced amenorrhea. Neuroendocrinology 1993; 57 (4): 600–4
Chandra AM, Patra PB, Chatterjee P. Adrenocortical activity in female rats following long-term exposure to treadmill running. Endokrinologie 1978; 72: 239–42
Chandra AM, Patra PB, Chatterjee P. Effect of longterm treadmill running on gonadal activity in female rats. Endokrinologie 1978; 72: 299–303
Casanueva FF, Borras CG, Burguera B. Steroids and neuroendocrine function in anorexia nervosa. J Steroid Biochem 1987; 27: 1–3
De Souza MJ, Maguire MS, Maresh CM. Adrenal activation and the prolactin response to exercise in eumenorrheic and amenorrheic runners. J Appl Physiol 1991; 70 (6): 2378–87
Ding JH, Sheckter CB, Drinkwater BL. High serum cortisol levels in exercise-associated amenorrhea. Ann Int Med 1988; 108: 530–4
Harber VJ, Sutton JR, Duncan MacDougal J. Plasma concentrations of b-endorphin in trained eumenorrheic and amenorrheic women. Fertil Steril 1997; 67 (4): 648–53
Hohtari H, Salminen-Lappalainen K, Laatikainen T. Response of plasma endorphins, corticotropin, cortisol, and luteinizing hormone in the corticotropin-releasing stimulation test in eumenorrheic and amoenorrheic athletes. Fertil Steril 1991; 55: 276–80
Hohtari H, Elovaino R, Salminen K. Plasma corticotropinreleasing hormone, corticotropin, and endorphin at rest and during exercise in eumenorrheic and amenorrheic athletes. Fertil Steril 1988; 50 (2): 233–8
Boyden TW, Pamenter RW, Grosso D. Prolactin responses, menstrual cycles and body composition of women runners. J Clin Endocrinol Metab 1982; 54 (4): 711–4
Rogol AD, Weltman A, Weltman JY. Durability of the reproductive axis in eumenorrheic women during 1 yr of endurance training. J Appl Physiol 1992; 72 (4): 1571–80
Boyden TW, Pamenter RW, Stanforth PR. Impaired gonadotropin responses to gonadotropin-releasing hormone stimulation in endurance-trained women. Fertil Steril 1984; 41: 359–63
Rogol AD, Weltman JY, Evans WS. Long-term endurance training alters the hypothalamic pituitary axes for gonadotropins and growth-hormone. Endocrinol Metab Clin North Am (Neuroendocrinology I) 1992; 21 (4): 817–32
Bonen A. Recreational exercise does not impair menstrual cycles: a prospective study. Int J Sports Med 1992; 13 (2): 110–20
Beitins IZ, McArthur JW, Turnbull BA. Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone. J Clin Endocrinol Metab 1991; 72: 1350–8
Mesaki N, Sasaki J, Sohda S. Suppression by L-dopa of prolactin secretion during exercise in female athletes. Jpn J Fertil Steril 1991; 36 (4): 739–44
O’Herlihy C. Jogging and suppression of ovulation [letter]. N Engl J Med 1982; 306 (1): 50–1
Parr RB, Bachman LA, Moss RA. Iron deficiency in female athletes. Physician Sports Med 1984; 12 (4): 81–6
Burrow GN, Wortzman G, Rewcastle NB. Micro adenomas of the pituitary and abnormal sellar tomograms in an unselected autopsy series. N Engl J Med 1981; 304 (3): 156–8
Strauzenberg SE, Kassner R, Bohm R. Iron deficiency in female athletes. Med Sport 1981; 14: 200–8
Veldhuis JD, Evans WS, Demers LM. Altered neuroendocrine regulation of gonadotropin secretion in women distance runners. J Clin Endocrinol Metab 1985; 61 (3): 557–63
Soules MR, Clifton DK, Cohen NL. Luteal phase deficiency: abnormal gonadotropin and progesterone secretion patterns. J Clin Endocrinol Metab 1989; 69: 813–9
Soules MR, McLachlan RI, Ek ML. Luteal phase deficiency: characterization of reproductive hormones over the menstrual cycle. J Clin Endocrinol Metab 1989; 69: 804–12
Cumming DC, Vickovic MM, Wall SR. Defects in pulsatile LH release in normally menstruating runners. J Clin Endocrinol Metab 1985; 60 (4): 810–2
Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc 1990; 22: 275–80
Warren MP. Amenorrhea in endurance runners. J Clin Endocrinol Metab 1992; 75 (6): 1393–7
Loucks AB, Heath EM, Law Sr T. 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
Loucks AB, Laughlin GA, Mortola JF. Hypothalamic-pituitarythyroidal function in eumenorrheic and amenorrheic athletes. J Clin Endocrinol Metab 1992; 75 (2): 514–8
Frisch RE, Canick JA, Tulchinsky D. Human fatty marrow aromatizes androgen to estrogen. J Clin Endocrinol Metab 1980; 51: 394–6
De Crée C. Endogenous opioid peptides in the control of the normal menstrual cycle and their possible role in athletic menstrual irregularities. Obstet Gynecol Surv 1989; 44 (10): 720–32
Ellingboe J, Veldhuis JD, Mendelson JH. Effect of endogenous opioid blockade on the amplitude and frequency of pulsatile luteinizing hormone secretion in man. J Clin Endocrinol Metab 1982; 54: 854–7
Ruffin MT, Hunter RE, Arendt EA. Exercise and secondary amenorrhoea linked through endogenous opioids. Sports Med 1990; 10: 65–71
Russel JB, DeCherney AH, Collins DC. The effect of naloxone and metoclopramide on the hypothalamic pituitary axis in oligomenorrheic and eumenorrheic swimmers. Fertil Steril 1989; 52 (4): 583–8
Sheps DS, Koch G, Bradgon EE. The reproducibility of resting and post-exercise plasma b-endorphins. Life Sci 1981; 43 (9): 787–91
Grossman A, Moult PJ, McIntyre H. Opiate mediation of amenorrhea in hyperpolactinaemia and in weight-loss related amenorrhea. Clin Endocrinol 1982; 17: 379–88
Behrman HR, Hall AK, Preston SL. Antagonistic interactions of adenosine and prostaglandin F2a modulate acute responses of luteal cells to luteinizing hormone. Endocrinol 1982; 110 (1): 38–46
Gambacciani M, Yen SSC, Rasmussen DD. GnRH release from the mediobasal hypothalamus: in vitro inhibition by corticotropin-releasing factor. Neuroendocrinology 1986; 43 (4): 533–6
Genazzani AD, Petraglia F, Gastaldi M. Growth hormone (GH)- releasing hormone-induced GH response in hypothalamic amenorrhea: evidence of altered central neuromodulation. Fertil Steril 1996; 65 (5): 935–8
Laughlin GA, Yen SSC. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 1996; 81 (12): 4301–9
Laughlin GA, Dominguez CE, Yen SS. Nutritional and endocrinemetabolic aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrinol Metab 1998; 83 (1): 25–32
Hiney JK, Ojeda SR, Dees WL. Insulin-like growth factor I: a possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology 1991; 54: 420–3
Laughlin GA, Yen SS. Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol Metab 1997; 82 (1): 318–21
Monahan T. Treating athletic amenorrhea: a matter of instinct. Physician Sports Med 1987; 15 (7): 184–9
De Crée C, Vermeulen A, Ostyn M. Are high-performance young women athletes doomed to become low-performance old wives?. Reconsidering the increased risk for osteoporosis in female athletes. J Sports Med Phys Fitness 1991; 31 (1): 108–14
Loucks AB. Skeletal demineralization in the amenorrheic athlete. In. MacLeod D, Maughan R, Nimmo M, et al., editors. Exercise: benefits, limits and adaptations. London: E. & F. N. Spon, 1987: 255–69
Prior JC. Ovulation disturbances and exercise training. Clin Obstet Gynecol 1991; 34: 180–90
Genazzani AD, Petraglia F, Gastaldi M. Naltrexone treatment restores menstrual cycles in patients with weight loss-related amenorrhea. Fertil Steril 1995; 64 (5): 951–6
Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988; 16 (3): 209–16
Dugowson CE. Nontraumatic femur fracture in an oligomenorrheic athlete. Med Sci Sports Exerc 1991; 23 (12): 1323–5
Lloyd T, Triantafyllou SJ, Baker ER. Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med Sci Sports Exerc 1986; 18 (4): 374–9
Snead DB, Stubbs C, Weltman JY. Dietary patterns, eating behavior, and bone mineral density in women runners. Am J Clin Nutr 1992; 56: 705–11
Sutton JR, Nilson KL. Repeated stress fractures in an amenorrheic marathoner. Physician Sports Med 1989; 17 (4): 65–71
American College of Sports Medicine. Position stand: the female athletic triad. Med Sci Sports Exerc 1997; 29 (5): i-ix
Chilibeck PD, Sale DG, Webber CE. Exercise and bone mineral density. Sports Med 1995; 19 (2): 103–22
Prior JC, Vigna YM, McKay DW. Reproduction for the athletic woman: new understandings of physiology and management. Sports Med 1992; 14 (3): 190–9
De Crée C, Lewin R, Ostyn M. The suitability of cyproterone acetate in the treatment of osteoporosis associated with athletic amenorrhea. Int J Sports Med 1988; 9 (3): 187–92
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
De Crée, C. Sex Steroid Metabolism and Menstrual Irregularities in the Exercising Female. Sports Med 25, 369–406 (1998). https://doi.org/10.2165/00007256-199825060-00003
Published:
Issue Date:
DOI: https://doi.org/10.2165/00007256-199825060-00003