Categories:

Exercise Induced Menstrual Disorders

Also See:
Exercise Induced Stress
Exercise and Effect on Thyroid Hormone
Potential Adverse Cardiovascular Effects from Excessive Endurance Exercise
Ray Peat, PhD: Quotes Relating to Exercise
Ray Peat, PhD and Concentric Exercise

“Sometimes progesterone seems to be chronically deficienct (leading to slight-though possibly prolonged-menstruation, or amenorrhea), in women who exercise hard. Since progesterone can be converted into cortisone to handle stress, this would explain why well trained athletes (who need lots of cortisone) so often miss periods. It seems to be a simple over-consumption of progesterone, which is probably a reasonable biological adaptation, preventing pregnancy during times of stress.” -Ray Peat, PhD

Proc Biol Sci. 1998 October 7; 265(1408): 1847–1851.
Physical work causes suppression of ovarian function in women.
G Jasieńska and P T Ellison
The suppression of reproductive function is known to occur in women engaging in activities that require high energetic expenses, such as sport participation and subsistence work. It is still unclear, however, if reproductive suppression is a response to high levels of energy expenditure, or only to the resulting state of negative energy balance. To our knowledge, this study provides the first evidence that work-related energy expenditure alone, without associated negative energy balance, can lead to the suppression of reproductive function in women. We document suppression of ovarian function expressed as lowered salivary progesterone levels in women from an agricultural community who work hard, but remain in neutral energy balance. We propose two alternative evolutionary explanations (the ‘pre-emptive ovarian suppression’ hypothesis and the ‘constrained down-regulation’ hypothesis) for the observed results.

Croat Med J. 2001 Feb;42(1):79-82.
Influence of high intensity training on menstrual cycle disorders in athletes.
Dusek T.
AIM:
To estimate the influence of intensive training on menstrual cycles in female athletes.
METHOD:
The questionnaire was used to determine the time of menarche, and the prevalence of primary and secondary amenorrhea and dysmenorrhea in 72 active female athletes from Zagreb (10 volleyball players, 18 basketball players, 10 ballet dancers, and 34 runners) aged between 15 and 21. The control group comprised 96 girls of the same age not engaged in any sports activity.
RESULTS:
The prevalence of secondary amenorrhea was three times higher in athletes than in the control group (p=0.037). The prevalence of primary amenorrhea was substantially higher in athletes than in the control group (6/72 vs. 0/96, p=0.014), whereas the prevalence of dysmenorrhea was twofold lower in athletes than in the control group (p<0.001). The highest prevalence of secondary amenorrhea was recorded in runners (14/31), particularly long-distance runners (11/17), whereas there was only one case of secondary amenorrhea among basketball players. Menarche was significantly delayed in the athletes who started physical activities before the onset of menstruation (13.8+1.4 vs. 12.6+1.0 years, p<0.001).
CONCLUSION:
High-intensity training before menarche postpones its onset. Type of training may be related to a significantly higher prevalence of secondary amenorrhea in runners than in basketball players.

Br J Sports Med. 2005 Mar;39(3):141-7.
Participation in leanness sports but not training volume is associated with menstrual dysfunction: a national survey of 1276 elite athletes and controls.
Torstveit MK, Sundgot-Borgen J.
OBJECTIVE:
To examine the prevalence of menstrual dysfunction in the total population of Norwegian elite female athletes and national representative controls in the same age group.
METHODS:
A detailed questionnaire that included questions on training and/or physical activity patterns, menstrual, dietary, and weight history, oral contraceptive use, and eating disorder inventory subtests was administered to all elite female athletes representing the country at the junior or senior level (aged 13-39 years, n = 938) and national representative controls in the same age group (n = 900). After exclusion, a total of 669 athletes (88.3%) and 607 controls (70.2%) completed the questionnaire satisfactorily.
RESULTS:
Age at menarche was significantly (p<0.001) later in athletes (13.4 (1.4) years) than in controls (13.0 (1.3) years), and differed among sport groups. A higher percentage of athletes (7.3%) than controls (2.0%) reported a history of primary amenorrhoea (p<0.001). A similar percentage of athletes (16.5%) and controls (15.2%) reported present menstrual dysfunction, but a higher percentage of athletes competing in leanness sports reported present menstrual dysfunction (24.8%) than athletes competing in non-leanness sports (13.1%) (p<0.01) and controls (p<0.05).
CONCLUSIONS:
These novel data include virtually all eligible elite athletes, and thus substantially extend previous studies. Age at menarche occurred later and the prevalence of primary amenorrhoea was higher in elite athletes than in controls. A higher percentage of athletes competing in sports that emphasise thinness and/or a specific weight reported present menstrual dysfunction than athletes competing in sports focusing less on such factors and controls. On the basis of a comparison with a previous study, the prevalence of menstrual dysfunction was lower in 2003 than in 1993.

Hum Reprod. 2010 Feb;25(2):491-503. Epub 2009 Nov 26.
High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures.
De Souza MJ, Toombs RJ, Scheid JL, O’Donnell E, West SL, Williams NI.
BACKGROUND:
The identification of subtle menstrual cycle disturbances requires daily hormone assessments. In contrast, the identification of severe menstrual disturbances, such as amenorrhea and oligomenorrhea, can be established by clinical observation. The primary purpose of this study was to determine the frequency of subtle menstrual disturbances, defined as luteal phase defects (LPD) or anovulation, in exercising women, with menstrual cycles of 26-35 days, who engage in a variety of sports, both recreational and competitive. Secondly, the prevalence of oligomenorrhea and amenorrhea was also determined via measurement of daily urinary ovarian steroids rather than self report alone.
METHODS:
Menstrual status was documented by daily measurements of estrone and pregnanediol glucuronide and luteinizing hormone across two to three consecutive cycles and subsequently categorized as ovulatory (Ovul), LPD, anovulatory (Anov), oligomenorrheic (Oligo) and amenorrheic (Amen) in sedentary (Sed) and exercising (Ex) women.
RESULTS:
Sed (n = 20) and Ex women (n = 67) were of similar (P > 0.05) age (26.3 +/- 0.8 years), weight (59.3 +/- 1.8 kg), body mass index (22.0 +/- 0.6 kg/m2), age of menarche (12.8 +/- 0.3 years) and gynecological maturity (13.4 +/- 0.9 years). The Sed group exercised less (P < 0.001) (96.7 +/- 39.1 versus 457.1 +/- 30.5 min/week) and had a lower peak oxygen uptake (34.4 +/- 1.4 versus 44.3 +/- 0.6 ml/kg/min) than the Ex group. Among the menstrual cycles studied in the Sed group, the prevalence of subtle menstrual disturbances was only 4.2% (2/48); 95.8% (46/48) of the observed menstrual cycles were ovulatory. This finding stands in stark contrast to that observed in the Ex group where only 50% (60/120) of the observed menstrual cycles were ovulatory and as many as 50% (60/120) were abnormal. Of the abnormal cycles in the Ex group, 29.2% (35/120) were classified as LPD (short, inadequate or both) and 20.8% (25/120) were classified as Anov. Among the cycles of Ex women with severe menstrual disturbances, 3.5% (3/86) of the cycles were Oligo and 33.7% (29/86) were Amen. No cycles of Sed women (0/20) displayed either Oligo or Amen.
CONCLUSIONS:
This study suggests that approximately half of exercising women experience subtle menstrual disturbances, i.e. LPD and anovulation, and that one third of exercising women may be amenorrheic. Estimates of the prevalence of subtle menstrual disturbances in exercising women determined by the presence or absence of short or long cycles does not identify these disturbances. In light of known clinical consequences of menstrual disturbances, these findings underscore the lack of reliability of normal menstrual intervals and self report to infer menstrual status.

N Engl J Med. 1985 May 23;312(21):1349-53.
Induction of menstrual disorders by strenuous exercise in untrained women.
Bullen BA, Skrinar GS, Beitins IZ, von Mering G, Turnbull BA, McArthur JW.
We performed a prospective study of 28 initially untrained college women with documented ovulation and luteal adequacy to determine whether strenuous exercise spanning two menstrual cycles would induce menstrual disorders. To ascertain the influence, if any, that weight loss might exert, we randomly assigned the subjects to weight-loss and weight-maintenance groups. Subjects were expected to run 4 miles (6.4 km) per day, progressing to 10 miles (16.1 km) per day by the fifth week, and to engage daily in 3 1/2 hours of moderate-intensity sports. The normalcy of the menstrual cycles during the period of exercise was judged independently according to clinical and hormonal criteria, the latter comprising serial measurements of gonadotropin and sex-steroid excretion. A higher percentage of abnormalities proved to be detectable by hormonal means (P less than 0.02). Only four subjects (three in the weight-maintenance group) had a normal menstrual cycle during training. In the weight-loss group, the number of women who had luteal abnormalities as compared with those who lost the surge in luteinizing hormone altered significantly over time, the latter occurring more frequently (P less than 0.01) as training progressed. Within six months of termination of the study, all subjects were again experiencing normal menstrual cycles. We conclude that vigorous exercise, particularly if compounded by weight loss, can reversibly disturb reproductive function in women.

J Clin Endocrinol Metab. 1991 Jun;72(6):1350-8.
Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone.
Beitins IZ, McArthur JW, Turnbull BA, Skrinar GS, Bullen BA.
We have previously reported that during 2 months of strenuous exercise, untrained young women with documented ovulatory menstrual cycles developed secondary oligoamenorrhea and luteal phase defects. In this study we tested the hypothesis that such abnormalities arise by altered neuroendocrine regulation of menstrual hormone secretion and that weight loss potentiates such effects. We supply a detailed analysis of the 20 cycles, of the total of 53, in which luteal phase abnormalities occurred. During the control month and 2 exercise months, all subjects collected daily overnight urine samples for the determination of LH, FSH, estriol (E3), and free progesterone (P) excretion by RIAs and creatinine by chemical assay. The characteristics of the abnormal luteal phase cycles were determined by comparing the excreted hormone levels and patterns during the control cycles with those of exercise cycles. The area under the curve (AUC) for each hormone was calculated for the follicular and luteal phases of each cycle. Six of the exercise cycles exhibited an inadequate luteal phase. This was characterized by a mean integrated P area of 202.4 (SEM, -61.8) nmol/day.nmol creatinine, compared with 331.7 (SEM, 64.7) during the corresponding control cycles, over a period of 9 or more days after the urinary LH peak to the onset of menses. Fourteen of the exercise cycles exhibited a short luteal phase. This was characterized by a mean integrated P area of 75.9 (30.9) nmol/day.nmol creatinine, compared to 267 (61.7) during the corresponding control cycles, over a span of 8 days or less from the urinary LH peak to the onset of menses. Additional abnormalities occurred only in the short luteal phase cycles. These included an increase in the length and AUC for E3 of the follicular phase and a decrease in the AUC of LH during the luteal phase. We conclude that the initiation of strenuous endurance training in previously ovulating untrained women frequently leads to corpus luteum dysfunction associated with insufficient P secretion and, in the case of short luteal phase cycles, decreased luteal phase length. That exercise may alter the neuroendocrine system is suggested by a delay in the ovulatory LH peak in spite of increased E3 excretion; moreover, less LH is excreted during the luteal phase. The lack of positive feedback to estrogens and decreased LH secretion during the luteal phase could compromise corpus luteum function. In contrast, decreased free P excretion was the sole abnormality noted in menstrual cycles with an inadequate luteal phase.

Annu Rev Med. 1988;39:443-51.
Exercise-induced menstrual dysfunction.
Henley K, Vaitukaitis JL.
Menstrual cycle changes associated with vigorous exercise can range widely. They may be only subtle abnormalities, ranging from delayed onset of spontaneous menses or anovulatory cycles to loss of spontaneous menses. They may be more serious, however. Significant adverse bone mineral changes, resulting in clinically significant osteoporosis and fractures, may occur concomitantly with exercise-induced menstrual dysfunction.

Sports Med. 1990 Oct;10(4):218-35.
Physical exercise and menstrual cycle alterations. What are the mechanisms?
Keizer HA, Rogol AD.
The prevalence of menstrual cycle alterations in athletes is considerably higher than in sedentary controls. There appears to be a multicausal aetiology, which makes it extremely difficult to dissociate the effects of physical exercise on the menstrual cycle from the other predisposing factors. From cross-sectional studies it appeared that physical training eventually might lead to shortening of the luteal phase and secondary amenorrhoea. Prospective studies in both trained and previously untrained women have shown that the amount and/or the intensity of exercise has to exceed a certain limit in order to elicit this phenomenon. We hypothesise, therefore, that apart from a certain predisposition, athletes with a training-induced altered menstrual cycle are overreached (short term overtraining, which is reversible in days to weeks after training reduction). Menstrual cycle alterations are most likely caused by subtle changes in the episodic secretion pattern of luteinising hormone (LH) as have been found in sedentary women with hypothalamic amenorrhoea as well as in athletes after very demanding training. The altered LH secretion then, might be caused by an increased corticotrophin-releasing hormone (CRH) secretion which inhibits the gonadotrophin-releasing hormone (GnRH) release. In addition, increased CRH tone will lead to increased beta-endorphin levels which will also inhibit the GnRH signaller. Finally, the continuous activation of the adrenals will result in a higher catecholamine production, which may be converted to catecholestrogens. These compounds are known to be potent inhibitors of GnRH secretion. In conclusion, menstrual cycle alterations are likely to occur after very demanding training, which causes an increase secretion of antireproductive hormones. These hormones can inhibit the normal pulsatile secretion pattern of the gonadotrophins.

Med Sci Sports Exerc. 2003 Sep;35(9):1553-63.
Menstrual disturbances in athletes: a focus on luteal phase defects.
De Souza MJ.
Subtle menstrual disturbances that affect the largest proportion of physically active women and athletes include luteal phase defects (LPD). Disorders of the luteal phase, characterized by poor endometrial maturation as a result of inadequate progesterone (P4) production and short luteal phases, are associated with infertility and habitual spontaneous abortions. In recreational athletes, the 3-month sample prevalence and incidence rate of LPD and anovulatory menstrual cycles is 48% and 79%, respectively. A high proportion of active women present with LPD cycles in an intermittent and inconsistent manner. These LPD cycles are characterized by reduced follicle-stimulating hormone (FSH) during the luteal-follicular transition, a somewhat blunted luteinizing hormone surge, decreased early follicular phase estradiol excretion, and decreased luteal phase P4 excretion both with and without a shortened luteal phase. LPD cycles in active women are associated with a metabolic hormone profile indicative of a hypometabolic state that is similar to that observed in amenorrheic athletes but not as comprehensive or severe. These metabolic alterations include decreased serum total triiodothyronine (T3), leptin, and insulin levels. Bone mineral density in these women is apparently not reduced, provided an adequate estradiol environment is maintained despite decreased P4. The high prevalence of LPD warrants further investigation to assess health risks and preventive strategies.

J Clin Endocrinol Metab. 2003 Jan;88(1):337-46.
Luteal phase deficiency in recreational runners: evidence for a hypometabolic state.
De Souza MJ, Van Heest J, Demers LM, Lasley BL.
Exercising women with amenorrhea exhibit a hypometabolic state. The purpose of this study was to evaluate the relationship of luteal phase deficient (LPD) menstrual cycles to metabolic hormones, including thyroid, insulin, human GH (hGH), leptin, and IGF-I and its binding protein levels in recreational runners. Menstrual cycle status was determined for three consecutive cycles in sedentary and moderately active women. Menstrual status was defined as ovulatory or LPD. Subjects were either sedentary (n = 10) or moderately active (n = 20) and were matched for age (27.7 +/- 1.2 yr), body mass (60.2 +/- 3.3 kg), menstrual cycle length (28.4 +/- 0.9 d), and reproductive age (14.4 +/- 1.2 yr). Daily urine samples for the determination of estrone conjugates, pregnanediol 3-glucuronide, and urinary levels of LH were collected. Blood was collected on a single day during the follicular phase (d 2-6) of each menstrual cycle for analysis of TSH, insulin, total T3, total T4, free T4, leptin, hGH, IGF-I, and IGF binding protein (IGFBP)-1 and IGFBP-3. Among the 10 sedentary subjects, 28 of 31 menstrual cycles were categorized as ovulatory (SedOvul). Among the 20 exercising subjects, 24 menstrual cycles were included in the ovulatory category (ExOvul), and 21 menstrual cycles were included in the LPD category (ExLPD). TSH, total T4, and free T4 levels were not significantly different among the three categories of cycles. Total T3 was suppressed (P = 0.035) in the ExLPD (1.63 +/- 0.07 nmol/liter) and the ExOvul categories of cycles (1.75 +/- 0.8 nmol/liter) compared with the SedOvul category of cycles (2.15 +/- 0.1 nmol/liter). Leptin levels were lower (P < 0.001) in both the ExOvul (5.2 +/- 0.4 microg/liter) and the ExLPD categories of cycles (5.1 +/- 0.4 microg/liter) when compared with the SedOvul category of cycles (13.7 +/- 1.7 microg/liter). Insulin was lower (P = 0.009) only in the ExLPD category of cycles (31.9 +/- 2.8 pmol/liter) compared with the SedOvul (60.4 +/- 8.3 pmol/liter) and ExOvul (61.8 +/- 10.4 pmol/liter) categories of cycles. IGF-I, IGFBP-1, IGFBP-3, IGF-I/IGFBP-1, IGF-I/IGFBP-3, and hGH were comparable among the different categories of cycles. These data suggest that exercising women with LPD menstrual cycles exhibit hormonal alterations consistent with a hypometabolic state that is similar to that observed in amenorrheic athletes and other energy-deprived states, although not as comprehensive. These alterations may represent a metabolic adaptation to an intermittent short-term negative energy balance.

J Clin Endocrinol Metab. 1998 Dec;83(12):4220-32.
High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition.
De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL.
The purposes of this investigation were to evaluate the characteristics of three consecutive menstrual cycles and to determine the frequency of luteal phase deficiency (LPD) and anovulation in a sample of sedentary and moderately exercising, regularly menstruating women. For three consecutive menstrual cycles, subjects collected daily urine samples for analysis of FSH, estrone conjugates (E1C), pregnanediol-3-glucuronide (PdG), and creatinine (Cr). Sedentary (n=11) and exercising (n=24) groups were similar in age (27.0+/-1.3 yr), weight (60.3+/-3.1 kg), gynecological age (13.8+/-1.2 yr), and menstrual cycle length (28.3+/-0.8 days). Menstrual cycles were classified by endocrine data as ovulatory, LPD, or anovulatory. No sedentary women (0%) had inconsistent menstrual cycle classifications from cycle to cycle, but 46% of the exercising women were inconsistent. The sample prevalence of LPD in the exercising women was 48%, and the 3-month sample incidence was 79%. In the sedentary women, 90% of all menstrual cycles were ovulatory (SedOvul; n=28), whereas in the exercising women only 45% were ovulatory (ExOvul; n=30); 43% were LPD (ExLPD; n=28), and 12% were anovulatory (ExAnov; n=8). In ExLPD cycles, the follicular phase was significantly longer (17.9+/-0.7 days), and the luteal phase was significantly shorter (8.2+/-0.5 days) compared to ExOvul (14.8+/-0.9 and 12.9+/-0.3 days) and SedOvul (15.9+/-0.6 and 12.9+/-0.4 days) cycles. Luteal phase PdG excretion was lower (P < 0.001) in ExLPD (2.9+/-0.3 microg/mg Cr) and ExAnov (0.8+/-0.1 microg/mg Cr) cycles compared to SedOvul cycles (5.0+/-0.4 microg/mg Cr). ExOvul cycles also had less (P < 0.01) PdG excretion during the luteal phase (3.7+/-0.3 microg/mg Cr) than the SedOvul cycles. E1C excretion during follicular phase days 2-5 was lower (P=0.05) in ExOvul, ExLPD, and ExAnov cycles compared to SedOvul cycles and remained lower (P < 0.02) in the ExLPD and ExAnov cycles during days 6-12. The elevation in FSH during the luteal-follicular transition was lower (P < 0.007) in ExLPD (0.7+/-0.1 ng/mg Cr) cycles compared to SedOvul and ExOvul cycles (1.0+/-0.1 and 1.1+/-0.1 ng/mg Cr, respectively). Energy balance and energy availability were lower (P < 0.05) in ExAnov cycles than in other menstrual cycle categories. The blunted elevation in FSH during the luteal-follicular transition in exercising women with LPD may explain their lower follicular estradiol levels. These alterations in FSH may act in concert with disrupted LH pulsatility as a primary and proximate factor in the high frequency of luteal phase and ovulatory disturbances in regularly menstruating, exercising women.

J Clin Endocrinol Metab. 1997 Sep;82(9):2867-76.
Bone health is not affected by luteal phase abnormalities and decreased ovarian progesterone production in female runners.
De Souza MJ, Miller BE, Sequenzia LC, Luciano AA, Ulreich S, Stier S, Prestwood K, Lasley BL.
The primary purpose of this study was to determine whether decreased ovarian progesterone production, associated with short and inadequate luteal phases in exercising women, was associated with decreased bone mineral density (BMD) and altered bone metabolism. Thirty-three eumenorrheic menstruating women participated in this study for 3 months. Subjects were required to collect daily urine samples for three consecutive menstrual cycles and have blood and urine collected weekly. Daily urine samples were analyzed for free LH, estrone conjugates (E1C), and pregnanediol 3-glucuronide (PdG), adjusted for creatinine, whereas weekly blood and urine samples were analyzed for bone markers, estradiol, progesterone, FSH, and LH. Based on the analyses of these samples, subjects were divided into three groups: sedentary ovulatory (SedOvul; n = 9), exercising ovulatory (ExOvul; n = 14), and exercising luteal phase defects (ExLPD; n = 10). The three groups were matched for age (27.6 +/- 1.0 yr), weight (60.6 +/- 1.9 cm), and reproductive maturity (14.5 +/- 1.0 yr), PdG production during the luteal phase was lower (P = 0.004) in the ExLPD women compared to that in the SedOvul group (2.4 +/- 0.4 vs. 5.1 +/- 0.6 ng/mL creatinine, respectively). The ExOvul group also had less (P < 0.01) PdG production during the luteal phase (3.5 +/- 0.3 ng/mL creatinine) compared to the SedOvul group. The total production of PdG, as assessed by area under the curve analysis, was also lower (P < 0.001) in the ExOvul and ExLPD groups compared to that in the SedOvul group. E1C production, however, was not different (P > 0.05) among the groups, except for E1C during the early follicular phase, which was lower (P = 0.043) in the ExLPD group than that in the SedOvul group. BMD and biochemical markers of bone metabolism were unaffected by and not associated with the compromised progesterone environment, but BMD values at the proximal femur (r = 0.354; P = 0.061) and total body (r = 0.359; P = 0.056) were associated with decreased early follicular E1C production. We conclude the following. 1) Luteal phase disturbances occur independent of training volume, and volume of training does not have to be severe to result in menstrual disturbances. 2) As a result of exercise, disturbance in progesterone production is not associated with decreased bone mass. 3) Long follicular phases are associated with reduced estrogen production during the early follicular phase, which are both associated with decreased bone mass. 4) Provided the estradiol status is adequately maintained, BMD is unaffected by decreased progesterone production associated with short and inadequte luteal phases in exercising women.

Clin Endocrinol (Oxf). 1990 Sep;33(3):345-53.
Luteinizing hormone and follicle stimulating hormone secretion patterns in female athletes with and without menstrual disturbances.
Pirke KM, Schweiger U, Broocks A, Tuschl RJ, Laessle RG.
Thirty-one young female athletes and 13 age-matched sedentary controls were studied throughout one menstrual cycle or over a 6 week period. Blood was sampled on 5 days per week. Episodic gonadotrophin secretion was measured in the early follicular phase and in the late luteal phase by blood sampling over a 12-h period at 15-min intervals. Eight athletes had anovulatory cycles, nine had impaired progesterone (P4) secretion during the luteal phase and 14 had normal cycles as judged from oestradiol (E2) and P4 plasma levels. Athletes with normal cycles had shorter cycles, lower E2 maxima at midcycle, and lower E2 and P4 concentrations during the luteal phase than had sedentary controls. Episodic luteinizing hormone (LH) secretion in the early follicular phase was significantly impaired in the anovulatory athletes: the average LH values over 12 h and the number of secretion episodes were significantly reduced. No significant changes were seen in follicle stimulating hormone secretion.

Br J Obstet Gynaecol. 1982 Jul;89(7):507-10.
Body weight, exercise and menstrual status among ballet dancers in training.
Abraham SF, Beumont PJ, Fraser IS, Llewellyn-Jones D.
A prospective study of the menstrual pattern and weight changes was made in the first year of training of 29 new female entrants to a professional ballet school. Seventy-nine per cent of the student girls had menstrual disturbances at entry: primary amenorrhoea, four; secondary amenorrhoea, 11; irregular menses, eight. The incidence of secondary amenorrhoea increase substantially by the end of the year (20), but was not associated with any significant change in body weight. Only three students menstruated regularly during the year. Menstrual regularity improved during periods of injury and long vacation and it appears that deterioration of the menstrual pattern during dancing periods was related to strenuous physical exercise rather than to any change in body weight.

Gynecol Endocrinol. 2006 Jan;22(1):31-5.
Influence of high-intensity training and of dietetic and anthropometric factors on menstrual cycle disorders in ballet dancers.
Castelo-Branco C, Reina F, Montivero AD, Colodrón M, Vanrell JA.
Background. Intensity of exercise and low energy consumption, specific type and amount of training, early age at initiation, previous menstrual dysfunctions, low body mass index (BMI) or percentage body fat, pathological feeding habits and psychological stress have been suggested as potential factors accountable for menstrual irregularities in female athletes.
Aim. To evaluate the influence of intensive training and of dietetic and anthropometric factors on menstrual cycles in female ballet dancers.
Method. A case-control study, in which a structured interview and physical examination were carried out in two groups of teenagers aged between 12 and 18 years. The study included a total of 115 adolescent girls distributed in two groups: dancers (group B, n = 38) and girls of the same age not engaged in any sports activity (group C, n = 77).
Results. Early starting high-intensity training delayed the onset of menarche ( p < 0.001). Dancers had a higher prevalence of oligomenorrhea and amenorrhea than control girls ( p = 0.004). Additionally, the dancers had lower scores in anthropometric variables: breast circumference 80 cm vs. 86.6 cm for controls ( p = 0.0001), low weight in 18% of dancers vs. 2.6% of controls ( p = 0.0001), and low height in 18% of dancers vs. 9% of controls ( p = 0.016). In addition, in dancers, low BMI was observed in 21% compared with 13% of controls ( p = 0.0001). Finally, 32% of the dancers were on a weight-control diet while this percentage decreased to 12% for the girls in control group (odds ratio = 3.49, 95% confidence interval = 1.31-9.25).
Conclusions. In ballet dancers, high-intensity training was associated with late onset of menarche, menstrual disorders, lower weight and height development, and abnormal feeding behaviors.

Clin Obstet Gynecol. 1983 Sep;26(3):728-35.
Exercise, sports, and menstrual dysfunction.
Hale RW.
With the increasing involvement of women in exercise programs, the physician is faced with more and more questions regarding the effect of exercise upon the reproductive system. Currently, it appears that premenarchal training may have the effect of delaying the onset of menses in some girls. There is no evidence that it delays the other stage of puberty or that it causes any harmful development by this delay. In the postmenarchal woman, strenuous exercise can definitely alter her bleeding pattern. The usual result is oligomenorrhea progressing toward amenorrhea as the exercise increases. This is not a universal phenomenon, however, and other factors such as percentage of body fat, stress, diet, and energy drain also play a role. The menses will usually resume its preexercise pattern after a period of rest.

Med Clin North Am. 1985 Jan;69(1):83-95.
Causes, evaluation, and management of athletic oligo-/amenorrhea.
Shangold MM.
Oligomenorrhea and amenorrhea are more common among athletes than among the general population. Although these conditions in athletes are often related to exercise and thinness, they may be caused by serious pathology too. All athletes with menstrual dysfunction deserve thorough evaluation and most need treatment.

Aust Fam Physician. 1984 Sep;13(9):659-63.
Oligomenorrhoea and amenorrhoea associated with exercise. A literature review.
Williams M.
Increasing numbers of women are embarking on more strenuous and constant exercise; their menstrual patterns are changing as a result. This review of the literature indicates that oligomenorrhoea and amenorrhoea in the physically active (particularly distance runners, gymnasts, ballet dancers and swimmers) are related to each woman’s physiological and psychological makeup.

Am Fam Physician. 1984 May;29(5):233-7.
The female athlete.
Wilkerson LA.
Anatomic considerations are the female athlete’s wider pelvis, shorter extremities and lower center of gravity. There is little qualitative difference in the muscle tissue of men and women; differences in strength stem from the amount of muscle mass. Amenorrhea/oligomenorrhea is common in runners, ballet dancers, cyclists, gymnasts, body builders, figure skaters and, to a lesser extent, swimmers. Pregnancy limits activity, but current evidence indicates that exercise during pregnancy is not harmful to either the mother or the fetus.

Int J Neurosci. 2006 Dec;116(12):1549-63.
Effects of menstrual cycle on sports performance.
Kishali NF, Imamoglu O, Katkat D, Atan T, Akyol P.
The aim of this study was to examine the effects of menstrual cycle on female athletes’ performance. Forty-eight teak-wondo athletes, 76 judoka, 81 volleyball, and 36 basketball players (total 241) elite athletes participated in the study. A questionnaire constituted from 21 questions about menstrual cycle applied. A one-way analysis of variance and scheffe tests were performed to assess differences between sport branches about physical and physiological characteristics. Chi square was used to evaluate the regularity of menstrual cycle, performance, and drug taking. The mean age of teak-wondo athletes, judokas, volleyball and basketball players were 20.71 +/- 0.41, 16.91 +/- 0.27, 21.22 +/- 0.26, and 21.03 +/- 0.63 years, respectively. The menarche ages of the athletes were 13.92, 13.22, 13.75, 13.86 years, respectively. 27.8% participated in regional competitions, 46.1% participated in just the national competitions, and 26.1% participated in the international competitions. Whereas the menstrual disorder was seen in 14.5% of the athletes in normal time, during the intensive exercise this ratio was increased to 20.7%. It was determined that during the competition 11.6% of the athletes used drug, 36.9% had a painful menstruation, 17.4% did not have a painful menstruation, 45.6% sometimes had a painful menstruation, and 63.1% of the athletes said that their pain decreased during the competition. First 14 days after the menstruation began, 71% of the athletes said that they felt themselves well. 71% of the athletes felt worst just before the menstruation period, 62.2% of the athletes said that their performance was same during the menstruation, and 21.2% said that their performance got worse. Both in general and during the training the menstruation period of the athletes was found to be regular (p < .01). Most of the athletes said that they have a painful menstruation period, and during the competition their pain decreased. As a result of the questionnaire, during the training and competition the number of athletes that did not use drugs were higher than the athletes that used drug (p < .01). The number of athletes that felt good before and during the menstruation were significantly higher (p < .05, p < .01). Between the menstruation periods the athletes said that they felt better in the first 14 days than the second 14 days (p < .01). When the non-menses period and menses period were compared the athletes said that their performance did not change (p < .01). It has been concluded that the menarche age was high in the athletes. It has found that the physical performance was not affected by the menstrual period and the pain decreased during the training and competition.

Am Fam Physician. 1989 Feb;39(2):213-21.
Exercise-induced amenorrhea.
Olson BR.
Strenuous exercise may cause menstrual abnormalities, including amenorrhea. The hypoestrogenemia that accompanies amenorrhea has been associated with a low bone mineral content and an increased incidence of stress fractures. With the resumption of menses, which usually occurs soon after female athletes decrease the intensity of their training or increase their body weight, bone mineral content increases and the incidence of stress fractures decreases.

Med Sci Sports Exerc. 1990 Jun;22(3):275-80.
Effects of exercise training on the menstrual cycle: existence and mechanisms.
Loucks AB.
This review evaluates the status of the evidence that exercise training affects the menstrual cycle beginning with evidence for the existence of delayed menarche, amenorrhea, and luteal suppression in athletes. A later age of menarche and a higher prevalence of amenorrhea and luteal suppression have been observed in athletes, but there is no experimental evidence that athletic training delays menarche, and alternative sociological and statistical explanations for delayed menarche have been offered. Cross-sectional studies of amenorrheic athletes have revealed abnormal reproductive hormone patterns, suggesting that the GnRH pulse generator in the hypothalamus is failing to initiate normal hypothalamic-pituitary-ovarian function. Longitudinal data show that the abrupt initiation of a high volume of aerobic training can disrupt the menstrual cycle in at least some women, but these women may be more susceptible to reproductive disruption than others, and some aspect of athletic training other than exercise (such as caloric deficiency) may be responsible for the observed disruption. Luteal suppression may be an intermediate condition between menstrual regularity and amenorrhea in athletes, or it may be the endpoint of a successful acclimation to exercise training. A potential endocrine mechanism of menstrual disruption in athletes involving the hypothalamic-pituitary-adrenal axis is discussed. Finally, promising future directions for research on this topic are described.

Appetite. 2010 Dec;55(3):379-87. Epub 2010 Aug 13.
Are female athletes at increased risk for disordered eating and its complications?
Coelho GM, Soares Ede A, Ribeiro BG.
The purpose of the study was to make a systematic review and describe and confront recent studies that compare the presence of disordered eating and its complications in young female athletes and controls subjects – PubMed, Scielo, Medline, ScienceDirect, WILEY InterScience, Lilacs and Cochrane were the databases used for this review. Out of 169 studies 22 were selected and 11,000 women from 68 sports were studied. The short version of the EAT was the most common instrument used to track disordered eating. Results showed that 55% found no significant difference in the percentage of disordered eating between athletes and controls. Also a higher percentage of studies reported higher frequency of menstrual dysfunction in athletes than controls and finally 50% of the studies found incidence of low bone mass in controls. Not all the studies that investigated all the conditions in the triad, but the authors concluded that it seemed that athletes were in more severe stage of this disorder. Due to the heterogeneity of the studies, a definitive conclusion about the groups and at highest risk for disordered eating and its complications remains to be elucidated.

Bone. 2009 Oct;45(4):760-7. Epub 2009 Jun 30.
History of amenorrhoea compromises some of the exercise-induced benefits in cortical and trabecular bone in the peripheral and axial skeleton: a study in retired elite gymnasts.
Ducher G, Eser P, Hill B, Bass S.
BACKGROUND:
Female gymnasts frequently present with overt signs of hypoestrogenism, such as late menarche or menstrual dysfunction. The objective was to investigate the impact of history of amenorrhoea on the exercise-induced skeletal benefits in bone geometry and volumetric density in retired elite gymnasts.
SUBJECTS AND METHODS:
24 retired artistic gymnasts, aged 17-36 years, who had been training for at least 15 h/week at the peak of their career and had been retired for 3-18 years were recruited. They had not been engaged in more than 2 h/week of regular physical activity since retirement. Former gymnasts who reported history of amenorrhoea (‘AME’, n=12: either primary or secondary amenorrhoea) were compared with former gymnasts (‘NO-AME’, n=12) and controls (‘C’, n=26) who did not report history of amenorrhoea. Bone mineral content (BMC), total bone area (ToA) and total volumetric density (ToD) were measured by pQCT at the radius and tibia (4% and 66%). Trabecular volumetric density (TrD) and bone strength index (BSI) were measured at the 4% sites. Cortical area (CoA), cortical thickness (CoTh), medullary area (MedA), cortical volumetric density (CoD), stress-strain index (SSI) and muscle and fat area were measured at the 66% sites. Spinal BMC, areal BMD and bone mineral apparent density (BMAD) were measured by DXA.
RESULTS:
Menarcheal age was delayed in AME when compared to NO-AME (16.4+/-0.5 years vs. 13.3+/-0.4 years, p<0.001). No differences were detected between AME and C for height-adjusted spinal BMC, aBMD and BMAD, TrD and BSI at the distal radius and tibia, CoA at the proximal radius, whereas these parameters were greater in NO-AME than C (p<0.05-0.005). AME had lower TrD and BSI at the distal radius, and lower spinal BMAD than NO-AME (p<0.05) but they had greater ToA at the distal radius (p<0.05).
CONCLUSION:
Greater spinal BMC, aBMD and BMAD as well as trabecular volumetric density and bone strength in the peripheral skeleton were found in former gymnasts without a history of menstrual dysfunction but not in those who reported either primary or secondary amenorrhoea. History of amenorrhoea may have compromised some of the skeletal benefits associated with high-impact gymnastics training.

J Clin Endocrinol Metab. 1980 Nov;51(5):1150-7.
The effects of exercise on pubertal progression and reproductive function in girls.
Warren MP.
To determine whether a significant energy drain during adolescence had a significant effect on puberty and normal reproductive function, 15 ballet dancers, aged 13–15 yr, who maintained a high level of physical activity from early adolescence were followed for 4.0 yr. Menarche was remarkably delayed in this group, occurring at a mean of 15.4 yr, significantly different (P < 0.01) from normal controls (12.5 yr) and normal music students (12.6 yr). In 2 dancers aged 18 yr, primary amenorrhea has persisted. While premenarchial, all of the dancers had varying breast development (Tanner stages 2–4) and low to low normal gonadotropin levels, normal PRL and T4 levels, and normal skull x-rays. The dancers’ mean body weight and calculated body fat were significantly less than in controls (P < 0.05). The progression of sexual development and the onset of menarche correlated in 10 or 15 subjects with a decrease in exercise and/or injury causing forced rest of at least 2-month duration. During this interval, weight gain was minimal or absent, with no significant change in body composition. A significant dichotomy in the order of pubertal development was also noted; while breast development and menarche were delayed, pubic hair development was not affected. Reversion to the amenorrheic state occurred in 11 of 13 patients with a return to exercise without a change in weight. In conclusion, energy drain may have an important modulatory effect on the hypothalamic pituitary set point at puberty and, in combination with low body weight, may prolong the prepubertal state and induce amenorrhea.

Clin Obstet Gynecol. 1985 Sep;28(3):573-9.
Body weight and the initiation of puberty.
Baker ER.
The onset and progression through the various stages of puberty are influenced by a number of factors (Fig. 2). In both animals and humans, the age of puberty appears to be related more to body weight than to chronologic age. Undernutrition and low body fat, or an altered ratio of lean mass to body fat, seem to delay the adolescent spurt and to retard the onset of menarche. According to Frisch, a minimum level of fatness (17% of body weight) is associated with menarche; however, a heavier minimum weight for height, representing an increased amount of body fat (22%), appears necessary for the onset and maintenance of regular menstrual cycles in girls over 16 years of age. This critical amount of body fat implies that a particular body composition, in addition to other environmental and psychosocial factors, is important in triggering and maintaining the pubertal process.
PIP:
Biological factors which influence the progression through female puberty stages are delineated, and an increase in the proportion of the body’s fat content is identified as a critical prerequisite for the onset and maintenance of regular ovulatory cycles. Excessive exercise or malnutrition may interfere with the normal increase in the proportion of body fat and retard the onset of menarche. Pubic hair growth and breast development begins in most American females between the ages of 8-13. Menarche follows 4.2 years later for 50% of the females, but of others, the time period ranges from 18 months to 6 mor years. Both males and females experience hormonal changes before the 1st physical signs of puberty are manifested. As sex hormones increase, changes in the body’s proportion of lean, fat, and skeletal mass occur. For females an increase in body fat begins at 7 years and continues through ages 16-18 years. Studies indicate that the body’s fat content must account for 17% of the body’s weight before menarche can occur and that, at age 18 years, the fat content must be at least 22% for the maintenance of regular menstrual cycles. Apparently, hypothalamic sensitivity to estrogens is decreased when the critical ratio of lean mass to body fat is reached, and changes in the hypothalamic and pituitary hormones promote pubertal progression and the establishment of reproductive functions. Poor nutrition alters the ratio of lean mass to body fat and delays the onset of menarche. In the US, the age at menarche decreased by 3 years since 1840 due to improvements in the population’s nutritional status. Underweight females generally experience menarche at later ages than normal weight females. In contrast overweight females often experience menarche earlier than the average weight female. Athletic females and ballet dancers frequently experience late menarche, and these delays may be due to the disruption in fat accumulation which results from excessive exercise. Physically, inactive adolescents, on the other hand, tend to experience menarche at an earlier age than normally active females. In conclusion, the body’s fat content along with a variety of environmental and psychosocial factors are responsible for the development and maintenance of female reproductive functions.

J Sports Med Phys Fitness. 1996 Mar;36(1):49-53.
Gymnasts, distance runners, anorexics body composition and menstrual status.
Bale P, Doust J, Dawson D.
Ten top class female distance runners, ten female anorexics and twenty female gymnasts of a similar age were compared for height, mass, %fat, fat mass, lean body mass, age of menarche and incidence of amenorrhoea. The mean age of the distance runners, anorexics, and gymnasts was 13.6 years, 14.7 years, and 13.3 years respectively. In comparison to normal data on females of a similar age they were shorter, lighter, had lower fat masses, and %fat, and the gymnasts and anorexics had lower lean body masses. However, the gymnasts and runners had higher lean body masses compared with the anorexic group. There were no significant differences in body composition by hydrostatic weighing but of these three groups the anorexics tended to have the highest total skinfold, %fat and fat masses. Only 20% of the gymnasts, 40% of the runners and 70% of the anorexics had started menstruating compared with 95% of girls of a similar age. Of the girls in our study who had started menstruating one gymnast, (25% of sub-group) two runners (50% of sub-group) and seven anorexics (100% of sub-group) had developed secondary amenorrhoea. The low body masses, low fat masses, delayed menarche and secondary amenorrhoea in athletes are discussed in relation to low caloric intake, stress, hormone levels, high training loads and genetic factors. Our data demonstrating no significant differences in body composition variables between the three groups of young girls, support the main contention that this type of physique may arise through different mechanisms leading to a common outcome, but without a proven causal link between anorexia and athletic performance.

Am Fam Physician. 1996 Mar;53(4):1185-94.
Evaluation of amenorrhea.
Kiningham RB, Apgar BS, Schwenk TL.
Pregnancy is the most common cause of amenorrhea and must be ruled out before proceeding with diagnostic evaluation. A careful history and physical examination may reveal evidence of androgen excess, estrogen deficiency or other endocrinopathies. Serum prolactin and thyroid-stimulating hormone (TSH) levels should be checked in all women who are not pregnant. Galactorrhea by history or on examination and/or an elevated prolactin level should be investigated with an imaging study to rule out a pituitary adenoma. If serum prolactin and TSH levels are normal, a progesterone challenge test should be performed to determine outflow tract patency and estrogen status. In women with hypoestrogenic amenorrhea, indicated by a negative challenge test and a competent outflow tract, serum gonadotropin, follicle-stimulating hormone and luteinizing hormone levels may be measured to determine whether amenorrhea represents ovarian failure or pituitary or hypothalamic dysfunction. Hypothalamic amenorrhea is common in women with a history of weight loss, stress or vigorous exercise. Amenorrheic women with adequate estrogen levels should receive cyclic progesterone. Hormonal therapy and calcium supplementation in hypoestrogenic amenorrhea.

Obstet Gynecol. 1979 Jul;54(1):47-53.
Menstrual dysfunction in distance runners.
Dale E, Gerlach DH, Wilhite AL.
The problem of menstrual dysfunction in women who engage in endurance training for participation in distance running events has been studied. Through survey, selected aspects of the personal, training, menstrual, and contraceptive histories of 168 women who were defined as runners, joggers, or controls were evaluated. In addition, defined subsets of the study subjects were evaluated for serum levels of pituitary and ovarian hormones and determination of percentage body fat. The data show significant differences among the 3 groups. It is concluded that menstrual dysfunction in distance runners is a real phenomenon. Presumably this is related to decreased percentage of body fat and/or minimal ovarian function secondary to diminished hypothalamic or pituitary hormone secretion.

Ugeskr Laeger. 1994 Nov 28;156(48):7219-23.
[Bone metabolism in female runners. Menstruation disorders are frequent among long-distance runners, but the bone mass is not influenced, with the exception of runners with amenorrhea].
[Article in Danish]
Hetland ML, Haarbo J, Christiansen C, Larsen T.
The purpose of the study was to investigate the prevalence of exercise-related menstrual and sex hormonal disturbances and the effect of exercise on bone mass and metabolism in female runners at various training levels. Two hundred and five premenopausal women (running 0-140 km a week) were recruited from a large population of female runners, who had responded to a questionnaire regarding exercise habits. Maximum oxygen uptake was determined by treadmill testing. Gynaecological status was assessed on entries in a menstrual calendar and by transvaginal ultrasonography; and sex hormonal status was measured three times with 10-day intervals. Bone mass was measured in the lumbar spine, proximal femurs and total body by dual energy x-ray absorptiometry, and in the forearm by single photon absorptiometry. Bone turnover was assessed by plasma osteocalcin, serum alkaline phosphatase, and urinary calcium and hydroxyproline. The results showed that sex hormonal disturbances were significantly related to training intensity. Compared with the normally active women, the baseline levels and fluctuations of oestradiol and progesterone in the elite runners were reduced by up to 25-44%, (0.01 < p < 0.05). The prevalence of amenorrhoea increased from 1% in the normally active to 11% in the elite runners. No statistically significant relation was found between running activity and bone mass or bone turnover. However, the group of amenorrhoeic runners had a 10% reduction in lumbar bone mass as compared to the normally menstruating runners (p < 0.05), but the bone turnover was similar.(ABSTRACT TRUNCATED AT 250 WORDS)

Am J Med. 1993 Jul;95(1):53-60.
Running induces menstrual disturbances but bone mass is unaffected, except in amenorrheic women.
Hetland ML, Haarbo J, Christiansen C, Larsen T.
PURPOSE:
To investigate the prevalence of exercise-related menstrual and sex hormonal disturbances and the effect of exercise on bone mass and metabolism in female runners at various training levels.
SUBJECTS AND METHODS:
Two hundred five premenopausal women (running 0 to 140 km a week) were recruited from a large population of female runners who had responded to a questionnaire regarding exercise habits. Maximum oxygen uptake was determined by treadmill testing. Gynecologic status was assessed on entries in a menstrual calendar and by transvaginal ultrasonography; sex hormonal status was measured three times with 10-day intervals. Bone mass was measured in the lumbar spine, proximal femurs, and total body by dual-energy x-ray absorptiometry, and in the forearm by single-photon absorptiometry. Bone turnover was assessed by measurement of plasma osteocalcin, serum alkaline phosphatase, and urinary calcium and hydroxyproline.
RESULTS:
Sex hormonal disturbances were significantly related to training intensity. Compared with the normally active women, the baseline levels and fluctuations of estradiol and progesterone in the elite runners were reduced by up to 25% to 44% (0.01 < p < 0.05). The prevalence of amenorrhea increased from 1% in the normally active subjects to 11% in the elite runners. No statistically significant relation was found between running activity and bone mineral measurements or bone turnover. However, the group of amenorrheic runners had a 10% reduction in lumbar bone density as compared with the normally menstruating runners (p < 0.05), but the bone turnover was similar. CONCLUSION: In the large majority of the female runners, no skeletal affection was found despite significant sex hormonal and menstrual disturbances. Only the runners with amenorrhea might be at increased risk of osteoporosis.

Fertil Steril. 1981 Dec;36(6):691-6.
Menstrual dysfunction and hormonal status in athletic women: a review.
Baker ER.
Since women have become more involved in physical fitness and competitive endurance sports, the incidence of menstrual dysfunction has increased. Long-distance running and other sports may lead to alterations in gonadotropins, androgens, estrogens, progesterone, or prolactin, which in some women may directly or indirectly result in amenorrhea or infertility. The effects of running and strenuous exercise on the menstrual cycle and reproductive hormones remain controversial. Reported incidences of menstrual dysfunction vary widely, and many factors have been implicated in the onset of this problem. Exercise associated menstrual dysfunction seems to occur more frequently in nulliparous athletes, in athletes with delayed menarche, and in athletes with low body fat. It is important to realize that disruption of the menstrual cycle, ranging from mild changes in flow to amenorrhea, is a relatively common problem for the female athlete engaged in strenuous endurance sports. Yet no evidence exists at present to indicate conclusively that this menstrual dysfunction is harmful to the female athlete’s reproductive system.

South Med J. 1983 May;76(5):619-24.
Athletic activity and menstruation.
Diddle AW.
Menstrual dysfunction characterized by delayed menarche, irregular menses, or secondary amenorrhea often affects women who compete in athletics over a prolonged time. Loss of body fat and emotional stress are important predisposing factors. Under these circumstances, hypoestrogenism, an altered ratio of follicle-stimulating hormone to luteinizing hormone, and elevation of serum testosterone, prolactin, catecholamines, and opioids are fairly common. There is controversy over whether the working capacity and performance of the average woman varies appreciably during various phases of the menstrual cycle. Apparently, those who suffer from premenstrual tension do have a diminution in working capacity. Generally, the causes of menstrual dysfunction are the same for athletes and nonathletes, and there are currently no data to forbid athletes’ training at any time during the menses. A gynecologic examination should be done before menstrual dysfunction is considered to be due to physical exercise. If this assumption is substantiated, and if amenorrhea persists for one year or more, a periodic estrogen-progesterone regimen should be offered to minimize vascular problems, osteoporosis, and stress fractures, and to protect the endometrium and ovarian function.

Br J Sports Med. 2005 Mar;39(3):141-7.
Participation in leanness sports but not training volume is associated with menstrual dysfunction: a national survey of 1276 elite athletes and controls.
Torstveit MK, Sundgot-Borgen J.
OBJECTIVE:
To examine the prevalence of menstrual dysfunction in the total population of Norwegian elite female athletes and national representative controls in the same age group.
METHODS:
A detailed questionnaire that included questions on training and/or physical activity patterns, menstrual, dietary, and weight history, oral contraceptive use, and eating disorder inventory subtests was administered to all elite female athletes representing the country at the junior or senior level (aged 13-39 years, n = 938) and national representative controls in the same age group (n = 900). After exclusion, a total of 669 athletes (88.3%) and 607 controls (70.2%) completed the questionnaire satisfactorily.
RESULTS:
Age at menarche was significantly (p<0.001) later in athletes (13.4 (1.4) years) than in controls (13.0 (1.3) years), and differed among sport groups. A higher percentage of athletes (7.3%) than controls (2.0%) reported a history of primary amenorrhoea (p<0.001). A similar percentage of athletes (16.5%) and controls (15.2%) reported present menstrual dysfunction, but a higher percentage of athletes competing in leanness sports reported present menstrual dysfunction (24.8%) than athletes competing in non-leanness sports (13.1%) (p<0.01) and controls (p<0.05).
CONCLUSIONS:
These novel data include virtually all eligible elite athletes, and thus substantially extend previous studies. Age at menarche occurred later and the prevalence of primary amenorrhoea was higher in elite athletes than in controls. A higher percentage of athletes competing in sports that emphasise thinness and/or a specific weight reported present menstrual dysfunction than athletes competing in sports focusing less on such factors and controls. On the basis of a comparison with a previous study, the prevalence of menstrual dysfunction was lower in 2003 than in 1993.

Gynecol Obstet Invest. 2000;49(1):41-6.
Women endurance runners with menstrual dysfunction have prolonged interruption of training due to injury.
Beckvid Henriksson G, Schnell C, Lindén Hirschberg A.
Strenuous exercise by women is associated with menstrual dysfunction, eating disorders and osteoporosis. Intensive training may also increase the susceptibility to infections. In this study, we investigated whether menstrual dysfunction was related to musculoskeletal injuries and/or upper respiratory tract infections in women middle/long-distance runners. A questionnaire was mailed to 127 Swedish female runners of whom 75% answered. This retrospective study showed a higher frequency of menstrual disorders (25%) in runners than in the general population. Furthermore, almost half of the athletes (46%) were classified as at risk of developing eating disorders. Women athletes with menstrual dysfunction were found to have had a longer interruption of training due to musculoskeletal injuries than those with regular cycles (34.1 +/- 3.0 vs. 9.0 +/- 9. 4 days, p < 0.05). However, no relation was found between susceptibility to infections and menstrual status.

Am J Obstet Gynecol. 1982 Aug 15;143(8):862-9.
The effect of marathon training upon menstrual function.
Shangold MM, Levine HS.
Detailed questionnaires were distributed to the 1,841 women who entered the 1979 New York City Marathon; the questions pertained to obstetric, gynecologic, and athletic histories, as well as height and weight. The incidence of oligomenorrhea/amenorrhea among the 394 respondents was 24% during training and 19% prior to training. The incidence of infertility among respondents was 10%. Of those women who had had regular menses prior to training, 93% continued to have regular menses during training. Amenorrheic women were significantly lighter (P less than 0.005) than regularly menstruating women and had significantly lower weight/height ratios (P less than. 0.0005). The best predictor of a women’s menstrual pattern during training was her pretraining menstrual pattern. Thinness was associated with amenorrhea, regardless of training.

Am J Physiol. 1994 Mar;266(3 Pt 2):R817-23.
Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability.
Loucks AB, Heath EM.
To investigate the relationship between energy availability (dietary energy intake minus energy expended during exercise) and thyroid metabolism, we studied 27 untrained, regularly menstruating women who performed approximately 30 kcal.kg lean body mass (LBM)-1.day-1 of supervised ergometer exercise at 70% of aerobic capacity for 4 days in the early follicular phase. A clinical dietary product was used to set energy availability in four groups (10.8, 19.0, 25.0, 40.4 kcal.kg LBM-1.day-1). For 9 days beginning 3 days before treatments, blood was sampled once daily at 8 A.M. Initially, thyroxine (T4) and free T4 (fT4), 3,5,3′-triiodothyronine (T3) and free T3 (fT3), and reverse T3 (rT3) were in the normal range for all subjects. Repeated-measures one-way analysis of variance followed by one-sided, two-sample post hoc Fischer’s least significant difference tests of changes by treatment day 4 revealed that reductions in T3 (16%, P < 0.00001) and fT3 (9%, P < 0.01) occurred abruptly between 19.0 and 25.0 kcal.kg LBM-1.day-1 and that increases in fT4 (11%, P < 0.05) and rT3 (22%, P < 0.01) occurred abruptly between 10.8 and 19.0 kcal.kg LBM-1.day-1. Changes in T4 could not be distinguished. If energy deficiency suppresses reproductive as well as thyroid function, athletic amenorrhea might be prevented or reversed by increasing energy availability through dietary reform to 25 kcal.kg LBM-1.day-1, without moderating the exercise regimen.

Am J Physiol. 1993 May;264(5 Pt 2):R924-30.
Induction and prevention of low-T3 syndrome in exercising women.
Loucks AB, Callister R.
To investigate the influence of exercise on thyroid metabolism, 46 healthy young regularly menstruating sedentary women were randomly assigned to a 3 x 2 experimental design of aerobic exercise and energy availability treatments. Energy availability was defined as dietary energy intake minus energy expenditure during exercise. After 4 days of treatments, low energy availability (8 vs. 30 kcal.kg body wt-1.day-1) had reduced 3,5,3′-triiodothyronine (T3) by 15% and free T3 (fT3) by 18% and had increased thyroxine (T4) by 7% and reverse T3 (rT3) by 24% (all P < 0.01), whereas free T4 (fT4) was unchanged (P = 0.08). Exercise quantity (0 vs. 1,300 kcal/day) and intensity (40 vs. 70% of aerobic capacity) did not affect any thyroid hormone (all P > 0.10). That is, low-T3 syndrome was induced by the energy cost of exercise and was prevented in exercising women by increasing dietary energy intake. Selective observation of low-T3 syndrome in amenorrheic and not in regularly menstruating athletes suggests that exercise may compromise the availability of energy for reproductive function in humans. If so, athletic amenorrhea might be prevented or reversed through dietary reform without reducing exercise quantity or intensity.

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Effect of luteal deficiency.

Acta Obstet Gynecol Scand. 1971;50(1):61-2.
Luteal insufficiency and pelvic adhesions.
Johansson ED, Persson BH, Gemzell C.
A young woman with a history of a septic abortion and left oophorectomy for a dermoid cyst was investigated before and after laparotomy with regard to the function of the corpus luteum. At laparotomy the remaining right ovary was surrounded and fixed by thick adhesions around the ovary. The adhesions were removed. During two regular menstrual cycles before operation, low plasma levels of progesterone were found during the luteal phase. After the removal of the adhesions normal plasma levels of progesterone were found. The urinary excretion of oestrogens also improved. Severe pelvic adhesions might be one cause of insufficient luteal function.

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