Continuing improvements in the performance of female endurance runners and increasing levels of participation have generated the need to know more about the physiology of this group. Specific research is needed in this area, as data referring to male endurance runners cannot legitimately be applied to the female endurance runner because of their markedly different physiological and hormonal profiles. Recent developments in our understanding of an athlete’s physiology (mainly in relation to the male endurance runner) have revealed new areas of interest that need to be assessed with specific reference to the female athlete.
Relatively little attention has been directed towards identifying the major physiological characteristics of the highly trained/elite female endurance runner in general, and that which has been published on such factors and the effects of the menstrual cycle have produced equivocal results. Moreover, the impact of such training upon the menstrual cycle and endurance running performance is a controversial area, especially when assessing its subsequent impact on health-related issues. Reports of the condition referred to as the ‘female athlete triad’ have increased in recent years, with a decrease in bone mineral density predisposing the female athlete to increased risks of stress fractures. The aetiology of this triad is multifactorial, with such risk factors including nutrition, menstrual status, training intensity and frequency, body size and composition and psychology/physical stress. However, research limitations and flaws have lead to controversy in the literature regarding the immediate and long term effects of the triad on the female athlete. Likewise, the effects of the oral contraceptive pill on health and endurance performance also remain elusive, with a dearth of research pertaining to how oral contraceptive agents can aid athletic performance and the long term health of the female athlete.
The purpose of this paper is to critically appraise the existing literature to provide a current review of the physiological scientific knowledge base in relation to the female athlete, health, training and performance, with suggestions for future areas of research. It is well known that certain menstrual and health-related performance factors of the female athlete, that is, physiological predictors of performance and body fat, have been extensively investigated over the last 30 years. However, a variety of methodological flaws and inconsistencies are present within the research and thus only the most prominent and well controlled studies within this area over the past 30 years will be referred to.
1. The Menstrual Cycle: Regulation, Alteration and Health-Related Issues
1.1 Regulation of the Menstrual Cycle
The normal menstrual cycle varies greatly in length from 22 to 36 days for women aged between 20 to 40 years. The cycle is typically divided into 3 phases. The first phase coinciding with menstrual bleeding is termed the menstrual phase, the second phase is dominated by estrogens and is termed the follicular phase, and the third phase is dominated by progesterone and is known as the luteal phase. These phases result from the highly regulated cyclic fluctuations of the anterior pituitary gonadotropins [specifically luteinising hormone (LH) and follicle-stimulating hormone (FSH)], growth hormone (GH) and prolactin that act upon the ovaries. FSH stimulates the growth and development of the primary follicles in the ovary, leading to ovulation, while LH is responsible for estrogen production and secretion forming the corpus luteum, which in turn releases progesterone for the maintenance of the endometrium (fig. 1).
This highly complex and intricate relationship is believed to be based on both positive and negative feedback mechanisms co-ordinated by the hypothalamic-pituitary-ovarian axis, and a disruption at any point in this sequence will result in menstrual disturbances (fig. 2).
In the context of exercise-related menstrual disturbances, the main focus of research and debate to date have been the steroid hormones of estrogen and progesterone. Our current understanding points towards exercise altering, in some as yet unknown manner, the pulsatile release of gonadotropin-releasing hormone (GnRH), which has a concomitant effect on LH release and consequently the levels of estrogen and progesterone. The physiological actions of estrogens and progesterone in the body are extremely complex, and are detailed elsewhere.[6,7] When relating to endurance performance, most research has focused upon the surge of endogenous progesterone around the middle of a ‘normal’ ovulatory cycle. However, the rise in endogenous progesterone does not imply ovulation has taken place, as increases in progesterone have been reported in anovulatory cycles. Although a strong correlation has been shown between progesterone levels and ovulation if values exceed 25 nmol/L, one can never be sure whether the actual peak values are being measured if daily samples are not taken, such as in blood sampling.[6,8] Indeed, other than pregnancy, the recovery of an ovum is the only possible evidence that ovulation has occurred. However, such procedures are impractical, inconvenient, uncomfortable and expensive. Therefore, progesterone levels analysed in saliva via radioimmunoassay/enzyme immunoassay have been reported to be a reliable substitute and are the standard method utilised to date in the identification of luteal phase onset and prediction of ovulation.[9,10]
1.2 Alterations to the Menstrual Cycle
An appreciation of the possible effects of vigorous exercise on the menstrual cycle has clear implications for health for the female athlete.[11,12] Whilst there is no published research supporting the myth that vigorous exercise during menstruation can have a direct, long term detrimental affect on the female reproductive system, research has suggested an association between vigorous training and a variety of menstrual cycle disorders which are prevalent in athletic women. Although the true incidence of menstrual cycle alterations associated with chronic exercise are not fully known because of the lack of good normative data, the causes are now thought to be multifactorial, including rapid bodyweight loss, sudden onset of strenuous training or exercise, inadequate nutrition to meet energy requirements,[13,14] and psychological and/or physical stress.[4,15]
As growing numbers of women participate in sports requiring sustained high energy demands, impairment of reproductive function is being reported with increasing frequency, suggesting that such alterations may constitute an integral component of the physiological adaptations to exercise as a stressor. There still remains uncertainty as to the effects of exercise on menstrual function (table I), and the effects of menstrual function on sports performance (table II), because many studies suffer from serious methodological flaws. However, athletic performance is affected by many physiological, psychological and environmental factors, all of which may have a larger effect on performance than the menstrual cycle itself. For the highly trained/elite female endurance runner, even small individual variations may make the menstrual cycle an important factor.
Sport and its association with menstrual abnormalities are well documented in the literature,[41–43] with the prevalence of menstrual cycle alterations in the athlete being considerably higher than in sedentary control individuals. Changes in reproductive endocrine function leading to irregular menses have been reported to range from 1 to 66% among athletes,[31,45] compared with 2 to 5% in the nonathletic population. Thus, because of the physiological stress placed upon the body through sport and the fact that athletes often have a low body mass combined with high training volumes and restricted diets, alterations of the menstrual cycle may prevail. However, there is substantial evidence indicating that the link between low body mass/fat mass and menstrual cycle disorders is weak (refer to section 1.2.1). The detrimental effects to skeletal and reproductive function caused by the suppression of the reproductive system is not fully known, but the characteristic lower body mass values found amongst amenorrhoeic women is widely documented[47–49] and cause for concern, along with the recently documented effects on bone mineral density (BMD) [see section 1.3].
The main alterations to the menstrual cycle have been classified as athletic amenorrhoea (0 to 3 periods/year), dysmenorrhoea (pelvic pain and/or cramps that occur at any time during the menstrual cycle), oligomenorrhoea (4 to 9 periods/year), anovulation and shortened luteal phases (duration of less than 14 days) and delayed menarche (no occurrence of menses before the age of 16 years). All these alterations are accompanied by low levels of the reproductive hormones estrogen and progesterone, along with a decrease in the regularity and/or establishment of an ovulatory cycle, which can greatly compromise BMD levels (refer to section 1.3).
1.2.1 Athletic Amenorrhoea and Delayed Menarche
Athletic amenorrhoea is the most widely reported menstrual dysfunction, with many studies attempting to determine the cause of athletic amenorrhoea from surveys based on historical recall and/or physical characteristics of the women.[50,51] However, such studies are limited by the factors they choose to measure, their use of retrospective data, and the subjective feelings of the participants. Thus, to increase the reliability and validity of these findings, a number of variables have been associated by means of correlation analysis with the incidence of athletic amenorrhoea, oligomenorrhoea and delayed menarche.[2,53] Numerous studies have associated the prevalence of menstrual cycle irregularity with the age of the athletes, low body fat percentage,[23,47] bodyweight changes, training intensity, age at menarche, intense training before menarche, prior menstrual cycle irregularities, prior training histories,[55,56] the endocrine conditioning model, the energy drain theory, pregnancy and endogenous opioids.[20,21,58]
The critical fat hypothesis received wide attention when it first suggested that menstrual cycle disturbances increased once the female athlete was below a certain body fat percentage threshold. However, recent research indicates that menstrual disturbances may not be caused by bodyweight loss or low body fat levels alone, but combined with the host of other factors already mentioned.[2,59] Indeed, Keizer and Rogol and Prior et al. stated that no one factor can be singled out as the primary cause of menstrual cycle dysfunction, with athletic amenorrhoea resulting from a manifestation of nutritional deprivation, physical illness, stress and excessive exercise. Bonen went further and stated that the progressive loading of metabolic stressors increases the extent of menstrual cycle changes culminating in the stimulation of the adrenal axis, in turn stimulating the hypothalamic neurotransmitter corticotropin-releasing hormone, down-regulating GnRH release and suppressing LH pulse frequency. Such disturbances can be seen on a continuum (fig. 3) causing the progression from eumenorrhoea to oligomenorrhoea and amenorrhoea at the extremes. Indeed, Bullen et al. suggested that moderate endurance training triggers the release of an array of hormones (several of which possess antireproductive properties), producing a dose-response curve having the effect of altering the athlete’s menstrual cycles in either direction along such a continuum.
The findings are equivocal with regard to dysmenorrhoea in the highly trained/elite female endurance runner. Dysmenorrhoea is characterised by a range of symptoms, foremost of which are lower abdominal pain that may radiate to the lower back or legs, headache, nausea and vomiting. Although exercise is generally thought to alleviate the discomfort associated with dysmenorrhoea, the scientific literature on this phenomenon displays mixed results. Studies have shown decreases in the severity of dysmenorrhoea with aerobic training, intensive training decreasing symptoms compared with occasional training, and no relation whatsoever.[64,65] Exercise has also been suggested to decrease dysmenorrhoea because of the endorphins associated with intense, long duration exercise decreasing depression, anxiety and anger. However, one very consistent factor in the research to date is that dysmenorrhoea occurs after ovulation when progesterone levels are high (fig. 2). Thus, it has been suggested that high levels of progesterone are the primary cause of dysmenorrhoea. However, in studies comparing athletes and nonathletes, the investigators did not know whether the women avoided activity because of their menstrual complaints or if the activity actually decreased the dysmenorrhoea, so no causation between inactivity and dysmenorrhoea can be claimed. Further varying definitions of dysmenorrhoea have been utilised, with many studies failing to control for disposition and mood, which have been shown to have a marked effect on dysmenorrhoea.
1.2.3 Anovulation and Shortened Luteal Phase
Anovulation and shortened luteal phases are a cause of infertility and, although they may not represent a problem in the young adolescent athlete, they certainly pose a problem in adults who wish to conceive. The occurrence and causes of shortened luteal phases and anovulatory cycles is equivocal, with a dearth of research in this area. Studies conducted by Boyden et al. and Bonen found that regular physical activity alters the menstrual cycle in female swimmers by heightening the prevalence of shortened luteal phases and anovulatory cycles. However, in this study the participant cohort was small (4 individuals) with the age of the cohort between 15 and 19 years, an age when the hypothalamic-pituitary-ovarian axis is immature and thus could be responsible for the altered cycles and not the physical activity per se. Despite these confounding variables, the high degree of consistency found within the results is astounding.
1.3 Health-Related Issues
Women athletes are under increasing pressure not only to be strong competitors but also to have the perfect body type and bodyweight for their chosen sport. High training loads coupled with the restricted energy intake often seen in female athletes (in an attempt to retain low body masses), has resulted in increases in the syndrome termed the ‘female athlete triad’. The female athlete triad is composed of 3 conditions prevalent in female athletes: amenorrhoea, disordered eating and osteoporosis. Any female athlete is at risk from this triad, but women who participate in sports where a low body fat percentage is advantageous, such as endurance running, are at the highest risk for extreme bodyweight-control behaviours.
1.3.1 Amenorrhoea and Osteoporosis
Amenorrhoea is a much more complex phenomenon than once thought, with bodyweight loss, the presence/absence of body fat, and emotional and physical stress all playing an integral role. The endocrine status of an amenorrhoeic female athlete shows a long term estrogen-deficient state similar to that of postmenopausal women. Because estradiol is extremely important in facilitating calcium uptake into the bone, amenorrhoea and the associated hypoestrogenic state may predispose female athletes to premature osteoporosis. The long term health consequences of amenorrhoea have received little attention in the past, despite the now realised effects on estrogen and progesterone production, affecting bone formation and remodelling.[66–68] The withdrawal of estrogens at any age is associated with bone loss that could lead to osteoporosis if prolonged, and is more critical than low progesterone levels for the onset of bone decalcification.[22,67] Indeed, a female athlete whose menstrual cycle is not regular runs the risk of decreasing BMD to such an extent that stress fractures occur under minimal impact loading of the bone.[46,67–69] Osteoporosis (decreased bone quality and quantity), which was once considered a disease of elders, is prevalent in female athletes of any age whose bone mass has fallen below the ‘critical threshold’.
Active and athletic women who lose their periods as a result of exercise patterns are strong candidates for premature bone loss, with 2 to 6% of bone lost per year in amenorrhoea, and a total loss of as much as 25% of total bone mass possible. Montagnani et al. and Myburgh et al. found that the total number of years of regular menses predicted lumbar spine BMD more accurately than any other menstrual/training factor. Indeed, over the past 15 years a number of studies have reported that women with menstrual cycle irregularities have bone mass values that are significantly lower than other women athletes and nonathletes. Consequently, the present concern is that many women athletes whose rigorous training schedules and restricted dietary practices have led to extended periods of amenorrhoea may have suffered irreversible bone loss.[68,72–74]
There are no long term follow-up studies of former amenorrhoeic athletes that enable determination of whether normal BMD can be attained following several years of normal menses or use of oral contraceptives. Indeed, the early studies suggesting that small gains in vertebral BMD could be attained following 14 months resumption of menses in formerly amenorrhoeic runners are now questioned. Martin and Houston and Micklesfield et al. stated that the bone mass of the lumbar spine of women with a history of oligomenorrhoea/amenorrhoea may never reach that of women who have had regular menstrual cycles, because of the bone loss and/or bone accretion. A recent study conducted by Keen and Drinkwater reported that after 6 to 10 years of amenorrhoea, oligomenorrhoea or oral contraceptive use, even previously amenorrhoeic athletes did not show significant improvements in vertebral BMD values when compared with eumenorrhoeic athletes over the same period. Thus, these findings suggest that oligomenorrhoea is as detrimental to lumbar spine BMD as amenorrhoea. Moreover, the long term effects of amenorrhoea on fertility are still unclear, although there are data suggesting that the reproductive deficiencies associated with amenorrhoea are reversible when the problem is treated.
BMD loss is a silent process and the athlete is usually unaware that a problem exists until a related injury, such as stress fracture, occurs or osteopenia is diagnosed. Osteopenia (a decreased calcification or density of bone) and osteoporosis have been associated with an increased risk of stress fractures and nontraumatic fractures in athletes that could put the athlete at risk of premature osteoporotic fractures in the future. Peak bone mass is reached during the first 3 decades of life, with 95% of maximum density reached by the age of 18 years and all women experiencing similar age-related bone loss after this time. Consequently, maximising peak bone mass during these first 3 decades is of utmost importance, as it is a time when athletes should be storing bone for the inevitable loss in later years. Indeed, as the 2 or 3 years that constitute the pubertal growth spurt are accompanied by deposition of 60% of the final bone mass, any dietary inadequacy and high exercise intensities at this time may more severely alter bone formation than at any other time in life.
Despite considerable research attention, the specific role of physical activity in the maintenance or enhancement of bone mass or architecture remains elusive, with results inconsistent and inconclusive because of numerous methodological variations and limitations. Physical activity has been shown to increase BMD in animals and human females by 0.9% per year. However, it is still controversial whether exercise compensates for the adverse affects of amenorrhoea on spinal trabecular bone density. Okano et al. reported BMD values within the average range for sedentary individuals in amenorrhoeic runners, suggesting that the physical activity can offset bone loss caused by exercise-induced amenorrhoea. However, today’s elite and subelite female athletes participate at a very high intensity, duration and frequency of training, beyond that considered in the previous research. This, coupled with poor eating habits and irregular menstrual cycles, may increase the risk of osteoporosis in this population. Therefore, whilst moderate exercise loads may be beneficial, extreme loads may be detrimental to bone health.
Several studies have demonstrated that extremely high running training loads may have a detrimental effect on bone via hormonal mechanisms,[70,71,80–82] whilst other studies have failed to demonstrate a relationship between training patterns and osteoporosis. Current opinions and research are beginning to suggest a running threshold, above which increases in running mileage alter the hormonal responses, over-riding the load-induced stimulus for bone formation and predisposing the athlete to fractures. However, the current consensus of a running threshold is equivocal because of a paucity of research. Most studies have looked at the amount of exercise per day or week, including duration and frequency. Chilibeck et al. suggested a running threshold of approximately 20 to 30 km/week, with a frequency of 2 to 3 days/week for 20 to 60 min/day, to increase BMD. Frost suggested that a minimum effective strain stimulus of mechanical loading is required to evoke an increase in the level of BMD, suggesting that strain rates should be high and distributed in unusual patterns, short in duration and frequent, to result in strengthening of the bone, although no quantitative numbers can be assigned to the specific overload variables. Moreover, Fehling et al. stated that such magnitudes of mechanical loading might decrease the negative effects of an estrogen-deficient hormonal environment.
It has been suggested that even though the estrogen levels are not high enough to support menstruation in athletic amenorrhoea, they might be of sufficient levels to provide a protective effect on BMD. Micklesfield et al. and Snow-Harter support the possibility that the total months of endogenous estrogen sufficiency is the critical determinant of spinal density. However, these findings conflict with those of Zanker, who stated that undernutrition may over-ride the effects of an estrogen deficiency on bone turnover via its metabolic consequences, precipitating a bone remodelling imbalance, reducing bone formation and leading to bone loss in young women with exercise-associated amenorrhoea. An alternative hypothesis is that of the ‘sport-specific’ response to increased bone density, stating that the human skeleton will respond with enhanced BMD at specific locations, with the magnitude and rate of the loading regimen playing an integral part in influencing BMD. Heinonen et al. supported this specificity stimulus to bone formation. They found that weight training provides a more effective osteogenic stimulus than endurance running. However, a normal ovulatory cycle is necessary for the response to positively affect bone formation.
To date, the efficacy of one regimen over another for enhancing/maintaining BMD has not been demonstrated. The exercise advantage gained is only temporary, for the bone remodelling of these athletes has been altered and the resulting bone formation is less than expected.[75–77,84,87] The primary goal of an exercise programme to decrease bone loss should be to elevate circulating estrogen levels. This could be achieved by decreasing training intensity and/or volume, restoring menses, or increasing the nutritional calcium intake (up to 1200 to 1500 mg/day) and colecalciferol (vitamin D) to stabilise reproductive endocrine status. Calcium and colecalciferol supplementation regimens have been recommended for osteoporosis in premenopausal and postmenopausal women.[70,79] Likewise, hormone replacement therapy and oral contraceptive use have been considered to prevent the rapid bone loss accompanying an estrogen deficiency such as those during menopause, with positive associations observed in a few studies.[79,88] However, Fehily et al. found no association between the use of oral contraceptive agents and BMD, which is consistent with the findings of most other studies.[75,87,89]
1.3.2 Anorexia and Disordered Eating
The ‘disordered eating’ concept is extremely common among female endurance athletes, with reports that 15 to 62% of athletes participate in pathogenic bodyweight-control behaviours. Any of the disordered eating behaviours (anorexia/bulimia nervosa) can be unhealthy and expose the female athlete to serious health problems, performance impairment and injury. As the body initially adapts to these nutritional deficiencies, a decrease in performance may not be seen for some time and athletes may falsely believe disordered eating practices are harmless. However, food restriction and purging can result not only in menstrual dysfunction and potentially irreversible bone loss, but psychological and medical complications as well, including depression, fluid/electrolyte imbalances and changes in endocrine/thermoregulatory systems. A variety of factors may contribute to the development of disordered eating patterns in the female athlete, such as environment, mood, performance pressures and so on.
Disagreements exist regarding the influence of diet in athletes with menstrual irregularities who demonstrate decreased BMD. Some authors have shown that amenorrhoeic athletes consume significantly fewer calories compared with eumenorrheic athletes, while others have reported similar energy intakes between the 2 groups. In addition, specific nutrients, such as fibre, protein, calcium, colecalciferol and vitamin K, have been implicated in menstrual irregularity and decreased BMD, again with conflicting results.[14,49,74,89,90] However, athletes with eating disorders have been shown to have decreased vertebral BMD compared with normal values, but higher than nonathletic people with disordered eating. Thus, training may lessen the amount of bone loss but exercise will not completely protect the athlete from losing BMD. There is currently little evidence to support dietary deficiencies, in particular calcium intake, as a risk factor for osteoporosis in otherwise healthy recreational and elite athletes, although abnormal and restrictive eating behaviours do seem to be related to a greater likelihood of fractures.
1.3.3 Suggestions for Management of the Female Athlete Triad
It is not uncommon for female athletes to train at very high intensities, consume inadequate diets and experience a great deal of stress. Why athletes continue with such practices without regard to the possible health consequences is possibly because of a lack of education or compulsive exercise habits within such groups. If symptoms associated with the female athlete triad, such as fractures and injuries, do not manifest themselves, then a change in behaviour is unlikely. However, there is very little known about the long term physical and psychological effects of the female athlete triad. If menstrual cycle irregularities are suspected or confirmed, it is vital that the female athlete should be educated in the possible health consequences to fertility and osteoporosis, especially if symptoms have persisted over the long term. Assessment of bone density via a bone scan may also be relevant for a diagnosis of osteopenia and/or osteoporosis, and may be enough for the athlete to initiate a change in behaviour.
Because of the multifactorial nature of the female athlete triad, the coach and support staff should be in touch with various outside information sources such as clinicians and health therapists and refer when appropriate. If menstrual cycle irregularities are noted, it is possible that other parts of the triad are also manifesting themselves. If dietary changes or training modifications are not acceptable to the athlete, then estradiol replacement should be considered upon the advice from the general practitioner.
The menstrual cycle is controlled via a highly complex and intricate hormonal relationship that can be influenced by a multitude of factors, including excessive training levels and diet. The female athlete triad and menstrual cycle irregularities can seriously affect BMD, with the resulting decrease in BMD predisposing an athlete to increased risks of stress fractures along with other health complications. Although weight-bearing activity is associated with increased bone density, excess exercise may be associated with a higher incidence of menstrual cycle irregularities and hence reduced BMD. It is possible that each individual has her own ‘sensitivity threshold’ regarding each variable associated with the triad. In addition, the hypothalamus may react differently to certain stresses from one athlete to the other. These possibilities could explain why firm conclusions regarding specific causal factors have not been reached. Thus, a sensible training load and adequate calorific intake (especially calcium and colecalciferol), which is sufficient to retain normal menstrual functioning, will enable the young female athlete to optimise her peak bone mass. Failing this, hormonal therapies may help to avoid the negative effects of the female athlete triad of disordered eating, amenorrhoea and osteoporosis, after adolescence.
2. The Menstrual Cycle and Endurance Running Performance
The physiological and psychological attributes of elite athletes are well documented and specific to the demands of the sport.[52,91–96] In activities such as endurance running, research has established that many factors influence endurance performance, for example running economy (RE),[97,98] maximal oxygen uptake (V̇O2max),[99,100] oxygen uptake (V dotO2), ventilatory and lactate thresholds (LT),[102,103] recovery from last bout of exercise,[104,105] metabolic and substrate factors,[34,106,107] and diet and ergogenic aids. However, most research in such areas relates mainly to male athletes because of the added confounding variable of the menstrual cycle when studying females.
2.1 Maximal Oxygen Uptake
Studies that have investigated the effect of the menstrual cycle on oxygen utilisation suggest that the increase in resting metabolic rate and core body temperature during the luteal phase increases the circulatory and aerobic-metabolic strain on the female athlete at this time.[107,109] Other investigators report that performance is not significantly affected by such thermal changes, suggesting a dissociation of the metabolic and thermoregulatory responses to exercise. In studies that have utilised serum progesterone to confirm the luteal phase, trained individuals showed no changes in V̇O2max during a regular ovulatory menstrual cycle,[12,33,38,96,111] and only a few investigators have shown significant changes in V̇O2max in untrained individuals across the menstrual phases.[29,112]
2.2 Submaximal Oxygen Uptake
One factor that differentiates the performance of runners who are homogenous with respect to V̇O2max is RE. Intra- and interindividual differences in RE have been attributed to a host of physiological and biochemical factors such as core temperature, age, gender, training, fatigue, air and wind resistance, stride length manipulation, external mass loading,[115,116] elasticity of the musculature, mechanical power, altitude, heart rate, ventilation and muscle fibre type. However, there is a dearth of published literature pertaining to RE and the menstrual cycle. It is well established that progesterone levels can increase 10-fold from the follicular to the luteal phase of a eumenorrhoeic menstrual cycle. This increase in progesterone is associated with an increase in ventilation, which suggests increases in oxygen demand and hence reduced RE during the luteal phase of the menstrual cycle. While most data support the view that maximal exercise does not appear to be affected across the menstrual cycle, the literature concerning submaximal exercise responses contains conflicting results. The findings of studies that have investigated RE over the menstrual cycle phases range from no significant variations in RE to improvements of up to 5.3% in V̇O2 during the luteal phase. Hessemer and Bruck, and Williams and Krahenbuhl found no change in RE across the menstrual cycle at 50% V̇O2max, but decreases in V̇O2 during the luteal phase at 80% V̇O2max. These differences could be caused by the factors mentioned previously (i.e. training status) being uncontrolled across various studies. Moreover, the review by Daniels on RE states there may be a certain threshold of training or a particular type of training necessary for inducing significant changes in RE, with trained females experiencing no changes in RE whilst untrained females are more susceptible to changes over the menstrual cycle.
Ventilation has attracted a large amount of research concerning performance and the menstrual cycle. The increase in carbon dioxide production, an associated fall in blood bicarbonate levels and a fall in arterial pH are now believed to be prime stimulators of ventilation (V̇E). Ventilatory control is accomplished via the central nervous system through neurogenic and hormonal stimuli allowing sensitive control of the ventilatory response. It is this hormonal stimulus that is thought to have the major impact on endurance performance. During the luteal phase, progesterone levels increase with concomitant effects on the respiratory system such as a partially compensated respiratory alkalosis, and an increase in both resting hypercapnic and hypoxic ventilatory responses, which could be detrimental to endurance performance. Schoene et al. stated that there is a high correlation between low ventilatory drive and outstanding athletic performance. Bonekat et al. conducted a study to investigate the effects of progesterone on the ventilatory response and exercise performance. They found that during the luteal phase when endogenous progesterone was high, lower respiratory exchange ratio (RER) and lactate values were noted, decreasing ventilation and indicating increased fat utilisation and glycogen sparing at this time, potentially improving endurance performance. This was supported by Jurkowski et al., Jurkowski and Bonen and Keizer.
However, the female athletes in the study by Bonekat et al. did not experience any improvements in performance during the luteal phase, so it is possible that any increase in sensitivity of the respiratory centre is compensated for by a lower hydrogen ion concentration, thus accounting for a lack of difference in exercise during the luteal phase. Indeed, Doolittle and Engebretsen reported no significant differences across the 3 menstrual phases at rest, during submaximal walking, maximal running or recovery in an untrained group of individuals with regards to metabolic and cardiorespiratory responses. This was supported by Eston, who stated that while resting V̇E may be affected by the menstrual cycle, it does not follow that ventilation during exercise should be affected by such hormonal fluctuations.
2.4 Lactate Threshold
In well trained individuals, the LT is a more sensitive indicator of training improvements and for predicting optimal times in marathon races and similar events than V̇O2max. However, there is considerable controversy regarding the mechanism behind the LT.[121,125–129] Wasserman et al. stated that the development of lactic acidosis is essential in the performance of work rates above the LT for the hydrogen ion concentration raises capillary oxygen partial pressure (PO2) and facilitates oxygen diffusion into the mitochondria. Thus, any effect of the menstrual cycle on LT would also affect performance. A study on the metabolic actions of estradiol by Bunt found that there is a lower lactate accumulation during the luteal phase of the menstrual cycle and suggested a glycogen sparing effect by the ovarian steroids present in high quantities at this time, thus supporting a performance enhancing effect at 35 to 70% V̇O2max. This is in agreement with Jurkowski, Jurkowski et al., Bullen et al., Nicklas et al., and Lebrun who all reported an increased fat oxidation during the luteal phase, which could possibly aid endurance performance of the faster endurance events, such as 1500m, because of decreased blood lactate accumulation.
Indeed, isolated animal experiments and studies administering pharmacological dosages of exogenous estrogens in humans have led to the suggestion of a substantial involvement of estrogens in fuel metabolism during exercise, facilitating lipid metabolism. The mechanisms underlying the increased fat oxidation have been attributed to the increased estradiol levels at this time, causing a considerable proportion of the sex steroids to dissociate from its protein, increasing the free fraction and biological activity of estradiol during the luteal phase, sparing glycogen and lowering lactate and RER values.[35,36] However, other studies have shown that the pattern of substrate use and the RER are identical for the follicular phase and luteal phase of the menstrual cycle, suggesting no increase in performance potential.[28,29,36,133] Indeed, Stephenson et al. indicated no apparent change in the balance of metabolic fuels consumed at a given metabolic rate as a function of the menstrual cycle, as well as the physiological systems that support metabolism and hence performance. This is further supported by Lamont who reported no significant differences in blood lactate levels between early follicular phase and mid luteal phase of the menstrual cycle during moderate exercise.
The cyclical core body temperature changes across the menstrual cycle have been reported more extensively than any other single factor, establishing the characteristic patterns of a premenstrual rise in temperature and a postmenstrual fall, followed by a return to baseline. Studies to date have produced equivocal results with differences in body temperature and thermoregulatory responses over the phases of the menstrual cycle reported to be minor,[26,110] or nonsignificant.[109,134] Hessemer and Bruck reported differences in all thermoregulatory responses at rest, between the luteal and follicular phases as a result of higher body temperatures increasing the threshold for dissipation of heat and hence increasing core body temperature. This agrees with the findings of Carpenter and Nunneley; however, the tests were conducted between 3 and 4.30am when the deep body temperature difference between menstrual phases is at maximum, and thus has little consequence in the sporting world.
Other investigators,[136,137] have hypothesised that estrogen and progesterone are responsible for the lower sweat rates and higher core body temperatures often reported for females during exercise in hot ambient conditions. However, it has now been recognised that many of the early studies reporting male and female differences in heat tolerance were conducted before the influence of relative and absolute workloads on the thermoregulatory systems was widely recognised, whilst involving high ambient temperatures that necessitated low intensity or short duration exercise sessions. Furthermore, in such studies, hormonal analysis was not utilised to confirm menstrual phases.[26,30,138]
Sanborn and Jankoswki reported that thermoregulation could be compromised during prolonged exercise or heat exposure in the luteal phase because of the stimulation of the renin and angiotensin system by the addition of progesterone. The latter increases the excretion of water and sodium from the kidney which in turn increases aldosterone secretion while promoting an increase in antidiuretic hormone. This mechanism is thought to contribute to the postovulatory fluid retention and concomitant increase in body mass that may affect performance because of the extra stress on the thermoregulatory systems during this phase. The increase in temperature could contribute to the increased heart rate observed in some studies during the luteal phase of the menstrual cycle that could also be detrimental to exercise performance.[109,139] However, the majority of research suggests that heart rate is not substantially affected by the phases of the menstrual cycle during progressive or steady-state exercise.[28,29,34,37] Indeed, any observed menstrual cycle effects on cardiac output are probably mediated primarily through changes in plasma volume that occur in response to the various hormones.
Females have been found to have lower iron stores from losses during menses, which could have a detrimental effect on haemoglobin levels and an associated decrease in aerobic capacity. Indeed, maximal physical performance can be decreased by iron deficiency in females who experience an increased risk of athletic anaemia because of the blood loss during menstruation as well as the endurance exercise destroying the red blood cells from the repeated forces applied to the lower limbs whilst running. However, the Jurkowski et al. study upon the effects of the menstrual cycle on blood lactate, oxygen delivery and performance, found that haemoglobin levels increased from the follicular to the luteal phase, which agrees with the findings of Garlick and Bernauer.
Fluctuations present in female performance have on many occasions been attributed to the menstrual cycle. Although controversy still remains as to whether the characteristic hormonal fluctuations of the menstrual cycle alter athletic performance via physiological and/or psychological parameters,[52,140] a large bulk of the research and those studies conducted under rigorous identification of menstrual cycle phases, have suggested no significant effect of the menstrual cycle phases upon the physiological determinants of endurance running performance. However, a lack of published literature on the physiology of the female endurance performer has led to the conflict surrounding female athlete’s training, performance and the effects of the menstrual cycle. Indeed the physiological variable that best describes the capacities of the cardiovascular and respiratory systems is velocity at maximum speed during an incremental test to exhaustion (Vmax), and no studies have concentrated specifically on this variable and the menstrual cycle.
3. The Oral Contraceptive Pill (OCP): Performance and Health-Related Issues
The old contraceptive pill (pre-1970s) received a bad press because of its high estrogen concentration (150µg) and consequently there was a lower usage because of the reported water retention, nausea, fatigue, headaches, thrombosis, hypertension and altered blood glucose/lipid metabolism that was experienced by oral contraceptive users. However, today’s advanced (post-1980s) oral contraceptives (lower estrogen [30µg] and progesterone dosages) could be utilised in the control of premenstrual symptoms, manipulation of the regularity of the cycle, and maintenance of BMD levels. Recent studies have shown that athletic women use oral contraceptive agents at least as often as sedentary women and thus it is imperative to increase the knowledge of these contraceptives and their effects on physiological functions and performance.[40,141]
3.1 The OCP and Endurance Running Performance
There is controversy regarding the OCP and its effects on various physiological determinants of performance and to what extent they may affect endurance running performance. As with other research, studies of the OCP have discrepancies related to methodological differences such as sample size, lack of randomisation, different pill dosages and formulations, training status of individuals, menstrual status of individuals, and the physiological variables measured.
The feeling of bloatedness and water retention commonly reported with the use of the old-type oral contraceptives has not been substantiated in studies with the new-type OCP with studies indicating no overall effect on bodyweight while taking oral contraceptives.[142,143] However, individual responses may result in either fluid retention or possibly appetite stimulation, caused by the hormonal levels.
Numerous investigators have looked into the effects of the OCP upon oxygen uptake because of its association with endurance running performance.[99,100] Some researchers have reported that the reductions in V dotO2max associated with the OCP appear to be reversible following cessation of its use,[11,144,145] whilst others failed to confirm a negative effect of the OCP on performance in laboratory-based tests.[101,103] Indeed, Bale and Davies conducted a study on menstruation and oral contraceptive effects on the performance of physical education students and reported that performance effects seem to be more psychological than physiological, suggesting that oral contraceptives had no effect upon performance. However, the study utilised questionnaires and retrospective data that have been reported as unreliable. Moreover, whether these findings translate to any effect on exercise performance is not clear, especially as endurance running is influenced by a myriad of other factors which could mask any effect of oral contraceptive use. However, the OCP has been found to decrease blood loss and thus could have positive influences on performance, as well as increasing oxygen delivery to the tissues via enhancing stroke volume and cardiac output.
Other physiological variables that have received attention in connection with the OCP are those of metabolism and lactate levels. The chronic use of the OCP has been suggested to alter carbohydrate and lipid metabolism,[33,147] with even the low dose OCP lowering fasting blood glucose levels and increasing serum triglycerides with an associated decrease in high intensity performance. Bonen et al. reported that moderately trained women had lower resting blood glucose values and higher free fatty acids with exercise than endurance trained individuals. Indeed, Bemben et al. found lower blood glucose levels and a lower total amount of carbohydrate use during prolonged submaximal exercise in 8 low dose OCP users compared with 8 controls, suggesting a greater carbohydrate sparing ability during prolonged exercise and thus delaying time to fatigue. However, other studies have reported no affect of oral contraceptive use on haemoglobin, ventilation, postexercise muscle glycogen or lactate, maximal heart rate or maximal RER, suggesting that a cellular mechanism could be involved.
The duration an individual is on the OCP could also affect variables associated with endurance running performance, for Lynch and Nimmo found peak blood lactate levels to be higher one week after ingesting the OCP (low dose, monophasic pill) compared with one week later, which could affect the hormonal milieu of the body impinging on endurance performance. However, they found no effect of the OCP on performance ranging from 75% to 100% V̇O2max which agrees with the findings of Bryner et al. The impact of these changes on substrate metabolism is not well understood and further research is required to gain a better understanding of the effect of these changes on performance in the field.
3.2 The OCP and Skeletal Health
As the estradiol and progesterone prevalent in the OCP have been shown to influence bone metabolism, it is reasonable to hypothesise that the use of the OCP could influence the skeletal health of athletes. Most studies conducted in oral contraceptive use and bone density have produced equivocal results for they have not controlled for confounding variables such as smoking, alcohol intake, endocrine status, body composition, dietary intake, and physical activity levels.
Whilst OCPs are primarily prescribed as a treatment for menstrual disturbances there is some support for a possible skeletal benefit. The OCP provides athletes who have menstrual disturbances with an exogenous source of estradiol to reduce the rate of remodelling and increase bone density and/or quality.[66,67,149,150] However, in contrast there have also been studies that have reported detrimental effects of oral contraceptive use on bone mass,[151–154] and future fracture risk, as well as those suggesting no effect of the OCP on bone density. However, these negative findings need further rigorous scientific studies before their clinical implications are supported because of a number of methodological issues. Indeed, evidence from many studies suggests that the OCP should be considered as a possible treatment for improving bone density. However, it is not at all clear if the induced improvement in bone density can persist through the postmenopausal acceleration of bone loss and thus provide a protective effect against osteoporotic fractures in later life.
Although it has been postulated that the OCP can enhance and decrease endurance running performance via various mechanisms, it does appear that apart from subtle changes in some variables there are no significant effects of the OCP on performance for most female endurance runners. However, researchers should exercise caution when utilising an oral contraceptive group in any study since the metabolic response to exercise may vary throughout one OCP cycle. Indeed, further research is required to elucidate such mechanisms underlying these responses in oral contraceptive users over time.
Oral contraceptives could allow athletes to reduce the risks associated with the female athlete triad syndrome,[156,157] by regulating the menstrual cycle and providing a protective effect on BMD and the occurrence of osteoporosis. Thus, the advantages of the OCP for sportswomen who are at risk would appear to outweigh any potential disadvantages, especially with the low dose pills currently available.
4. Conclusion and Implications
It is not uncommon for female athletes to train at very high intensities, consume inadequate diets and experience a great deal of stress, all of which may contribute to menstrual irregularities. Fluctuations present in female endurance running performance have on many occasions been attributed to the menstrual cycle. Although there is considerable evidence to validate physiological variations during the menstrual cycle at rest, the idea that these variations affect exercise performance is equivocal. The review of current literature suggests that the physiological determinants of endurance running performance in highly trained/elite female endurance runners is generally not affected by menstrual status, menstrual phase, or oral contraceptive use. The lack of any significant changes in all measured parameters as a result of exercise suggests several possibilities in that (i) either the variations observed at rest are of such a low magnitude that they are offset by exercise; or (ii) exercise serves as an antagonist to the fundamental compensatory reactions of the menstrual cycle.
The greatest worry for the female endurance runner is the alterations in menstrual cycle regularity often reported in those with high training volumes and/or intensities (>20 to 30 km/week) and the concomitant effects on health. Indeed, if menstrual cycle irregularities are observed in athletes then the possibility that other components of the female athlete triad may also be present need to be considered. For this reason it is important to screen for menstrual irregularities and investigate the causes. If there are prolonged disturbances a bone scan may be prudent to screen for possible osteopenia. Although it is not clearly established whether taking the OCP can protect bone density and reduce the risk of osteopenia, it may be an option for females with low endogenous estradiol levels. Furthermore, encouraging a healthy eating routine with adequate calcium, colecalciferol and vitamin K intake is sensible. Additional studies are needed to accurately determine a threshold of training above which menstrual cycle irregularity is increased with concomitant increases in the risks for osteopenia and osteoporosis in the trained and elite female endurance runner.
It has recently been suggested that once BMD loss has occurred the athlete cannot regain full BMD, thus the major aim should be to maximise peak BMD during the ages of puberty up to late twenties, which is typically the age when the athlete is most competitive and at the greatest risk of the female athlete triad.
Research to elucidate safe training volumes and intensities, menstrual cycle regularity and dietary influences on BMD for the female athlete is needed to prevent unnecessary decreases in performance as well as minimising long term health problems with its resulting cost to the public health services. Moreover, further studies assessing the long term health consequences of athletic amenorrhoea are essential.
Vollman N, editor. The menstrual cycle: major problems in obstetrics and gynaecology. Vol. 7. Philadelphia (PA): WB Saunders, 1977
Wells CL. Women, sport and performance: a physiological perspective. 2nd ed. Champaign (IL): Human Kinetics, 1991
Bonen A, Belcastro AN, Ling WY, et al. Profiles of selected hormones during menstrual cycles of teenage athletes. J Appl Physiol 1981; 50: 545–51
Arendt EA. Osteoporosis in the athletic female: amenorrhoea and amenorrhea osteoporosis. In: Pearl A J, editor. The athletic female. Champaign (IL): Human Kinetics, 1993: 41–59
Bonen A, Keizer HA. Athletic menstrual cycle irregularity: endocrine responses to exercise and training. Physician Sports Med 1984; 12: 78–90
Abdulla U, Diver MJ, Hipkin L, et al. Plasma progesterone levels as an index of ovulation. Br J Obstet Gynaecol 1983; 90: 543–8
Mishell DR, Davajan V, Lobo RA, editors. Infertility, contraception, and reproductive endocrinology. 3rd ed. Boston (MA): Blackwell Scientific Publications, 1991
Israel R, Mishell DR, Stone SC, et al. Single luteal phase serum progesterone assay as an indicator of ovulation. Am J Obstet Gynecol 1972 Apr 15; 112 (8): 1043–6
Webley GE, Edwards R. Direct assay for progesterone in saliva: comparison with a direct serum assay. Ann Clin Biochem 1985; 22: 579–85
O’Rorke A, Kane MM, Gosling JP, et al. Development and validation of a monoclonal antibody enzyme immunoassay for measuring progesterone in saliva. Clin Chem 1994; 40: 454–8
Daggett A, Davies B, Boobis L. Physiological and biomechanical responses to exercise following oral contraceptive use [abstract]. Med Sci Sports Exerc 1983; 15: 174
De Bruyn-Prevost P, Masset C, Sturbois X. Physiological response from 18–25 year old women to aerobic and anaerobic physical fitness tests at different periods during the menstrual cycle. J Sports Med Phys Fitness 1984; 24: 144–8
Lloyd T, Buchanan JR, Bitzer S, et al. Inter-relationships of diet, athletic activity, menstrual status, and bone density in collegiate females. Am J Clin Nutr 1987; 46: 681–4
Laughlin GA, Dominguez CE, Yen SS. Nutritional and endocrine-metabolic aberrations in women with functional hypothalamicn amenorrhea. J Clin Endocrinol Metab 1998; 83: 25–32
Sanborn CF, Jankowski CM. Physiologic considerations for women in sport. Clin Sports Med 1994; 13: 315–27
Arena B, Maffulli N. Endocrinological changes in exercising women. Sports Exerc Inj 1998; 4: 194–8
Jurkowski JE. Hormonal and physical responses to exercise in relation to the menstrual cycle. Can J Appl Sports Sci 1982; 7: 85–9
Boyden TW, Pamenter RW, Stanforth P, et al. Sex steroids and endurance running in women. Fertil Steril 1983; 39: 629–32
Bullen BA, Skrinar GS, Beitins IZ, et al. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J Appl Physiol 1984; 56: 1453–63
Ronkainen H. Depressed follicle-stimulating hormone, luteinizing hormone, and prolactin responses to the luteinizing hormone-releasing hormone, thyrotropin-releasing hormone, and metoclopramide test in endurance runners in the hard-training season. Fertil Steril 1985; 44: 755–9
Keizer HA, Kuipers HJ, Beckers E, et al. Multiple hormonal responses to physical exercise in eumenorrhoeic trained and untrained women. Int J Sports Med 1987; 8: 139–50
Baker E, Demers L. Menstrual status in female athletes: correlation with reproductive hormones and bone density. Obstet Gynecol 1988; 72: 683–7
Broocks A, Pirke KM, Schweiger V. Cyclic ovarian function in recreational athletes. J Appl Physiol 1990; 68: 2083–6
Montagnani GF, Arena B, Maffulli N. Oestradiol and progesterone during exercise in healthy untrained women. Med Sci Sports Exerc 1992; 24: 764–8
Okano H, Mizunuma H, Soda MY, et al. Effects of exercise and amenorrhoea on bone mineral density in teenage runners. Endocr J 1995; 42: 271–6
Wells CL, Horvath SM. Heat stress responses related to the menstrual cycle. J Appl Physiol 1974; 35: 1–5
Allsen PE, Parsons P, Bryce GR. Effects of the menstrual cycle on maximal oxygen uptake. Physician Sports Med 1977; 5: 53–5
Jurkowski JE, Jones NL, Toews CJ, et al. Effects of menstrual cycle on blood lactate, oxygen delivery, and performance during exercise. J Appl Physiol 1981; 51: 1493–9
Schoene RB, Robertson HT, Pierson DJ, et al. Respiratory drives and exercise in menstrual cycles of athletic and non-athletic women. J Appl Physiol 1981; 50: 1300–5
Stephenson LA, Kolka MA, Wilkerson JE. Metabolic and thermoregulatory responses to exercise during the human menstrual cycle. Med Sci Sports Exerc 1982; 14: 270–5
Bonen A, Haynes FJ, Watson-Wright W, et al. Effects of menstrual cycle on metabolic responses to exercise. J Appl Physiol 1983; 55: 1506–13
Lamont LS. Lack of influence of the menstrual cycle on blood lactate. Physician Sports Med 1986; 14: 159–63
Dombovy ML, Bonekat HW, Williams TJ, et al. Exercise performance and ventilatory response in the menstrual cycle. Med Sci Sports Exerc 1987; 19: 111–7
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
De-Souza MJ, Maguire MS, Rubin KR, et al. Effects of menstrual phase and amenorrhoea on exercise performance in runners. Med Sci Sports Exerc 1990; 22: 575–80
Kanaley JA, Boileau RA, Bahr JA, et al. Substrate oxidation and GH responses to exercise are independent of menstrual phase and status. Med Sci Sports Exerc 1992; 24: 873–80
Pivarnik JM, Marichal CJ, Spillman T, et al. Menstrual cycle phase affects temperature regulation during endurance exercise. J Appl Physiol 1992; 72: 543–8
Lebrun CM, McKenzie DC, Prior JC, et al. Effects of menstrual cycle phase on athletic performance. Med Sci Sports Exerc 1995; 27: 437–44
Williams TJ, Krahenbuhl GS. Menstrual cycle phase and running economy. Med Sci Sports Exerc 1997; 29: 1609–18
Lynch NJ, Nimmo MA. Effects of menstrual cycle phase and oral contraceptive use on intermittent exercise. Eur J Physiol 1999; 78: 565–72
Prior JC. Endocrine ‘conditioning’ with endurance training: a preliminary review. Can J Appl Sports Sci 1982 Sep; 7 (3): 148–57
Shangold M, Levine HS. The effect of marathon training upon menstrual function. Am J Obstet Gynecol 1982; 143: 862–9
Sanborn CF, Wagner WW. The female athlete and menstrual irregularity. In: Puhl JL, Brown CH, Voy RO, editors. Sport science perspectives for women. Champaign (IL): Human Kinetics, 1988: 111–30
Keizer HA, Rogol AD. Physical exercise and menstrual cycle alterations: what are the mechanisms? Sports Med 1990 Oct; 10 (4): 218–35
Loucks AB, Horvath SM. Athletic amenorrhoea: a review. Med Sci Sports Exerc 1985; 17: 56–72
Snow-Harter CM. Bone health and prevention of osteoporosis in active and athletic women. Clin Sports Med 1994; 13: 389–404
Frisch RE, McArthur JW. Menstrual cycle changes: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 1974; 185: 949–51
Frisch RE, Albright T, Gotz-Welbergen AV, et al. Delayed menarche and amenorrhoea of college athletes in relation to age of onset of training. JAMA 1981; 246 (14): 1559–63
Schwartz B, Selye H, Cumming D, et al. Exercise associated amenorrhoea. Am J Obstet Gynecol 1981; 141: 662–70
Erdelyi GJ. Gynaecological survey of female athletes. The American Medical Association Second National Conference on the Medical Aspects of Sports; 1960 Nov 27; Washington DC, 174–9
Zaharieva E. Survey of sportswomen at the Tokyo Olympics. J Sports Med Phys Fitness 1965; 5: 215–9
Eston RG. The regular menstrual cycle and athletic performance. Sports Med 1984; 1: 431–45
Forrester A, Korkia P. Vive la difference. Coaching News 1997; 4: 9–15
Bonen A. Alterations in menstrual cycles: effects of exercise. Mod Med Can 1986; 41: 331–42
Bonen A, Keizer HA. Pituitary, ovary, and adrenal hormone responses to marathon running. Int J Sports Med 1987; 8: 161–7
Dale E, Gerlach DHG, Martin DE, et al. Physical fitness profiles and reproductive physiology of the female distance runner. Physician Sports Med 1979 Jan; 7: 83–95
Warren P. Effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab 1980 Nov; 51 (5): 1150–7
Bale P. Body composition and menstrual irregularities of female athletes. Sports Med 1994; 17: 347–52
Howlett TA. Hormonal responses to exercise and training: a short review. Clin Endocrinol 1987; 26: 723–42
Prior JC, Vigna YM, Schulzer M, et al. Determination of luteal phase length by quantitative basal temperature methods: validation against the mid-cycle LH peak. Clin Invest Med 1990; 13: 123–31
Bonen A. Exercise-induced menstrual cycle changes: a functional, temporary adaptation to metabolic stress. Sports Med 1994; 17: 373–92
Israel RG, Sutton M, O’Brien K. Effects of aerobic training on primary dysmenorrhoea symptomology in college females. J Am Coll Health 1985; 33: 241–4
Izzo A, Labriola D. Dysmenorrhoea and sports activities in adolescence. Clin Exp Obstet Gynecol 1991; 18: 109–16
Jarrett M, Henkemper MM, Shaver JF, et al. Symptoms and self-care strategies in women with and without dysmenorrhoea. Health Care Women Int 1995; 16: 167–78
Harlow P. Physical activity is not associated with any pain parameter. Br J Obstet Gynaecol 1996; 103: 1134–42
Cann CE, Cavanaugh DJ, Schnurpfiel K, et al. Menstrual history is the primary determinants of trabecular bone density in women runners [abstract]. Med Sci Sports Exerc 1988; 20: 59
Cumming D. Exercise-associated amenorrhoea, low bone density and oestradiol replacement therapy. Arch Intern Med 1996; 156: 2193–5
Hergenroeder AC, Smith EOB, Shypailo R, et al. Bone mineral changes in young women with hypothalamic amenorrhoea treated with oral contraceptives, medroyxprogesterone, or placebo over 12 months. Am J Obstet Gynecol 1997; 176: 1017–25
Myburgh KH, Bachrach LK, Lewis B, et al. Low bone mineral density at axial and appendicular sites in amenorrhea athletes. Med Sci Sports Exerc 1993; 25: 1197–202
Fehily AM, Coles RJ, Evans WD, et al. Factors affecting bone density in young adults. Am J Clin Nutr 1992; 56: 579–86
Grimston SK, Willows ND, Hanley DA. Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc 1993 Nov; 25 (11): 1203–10
Marcus R, Cann C, Madvig P. Menstrual function and bone mass in elite women distance runners: endocrine and metabolic factors. Ann Intern Med 1985; 102: 158–63
Cook SD, Harding AF, Thomas KA, et al. Trabecular bone density and menstrual function in women runners. Am J Sports Med 1987; 15: 503–7
Wolman RL, Clark P, McNally E, et al. Menstrual state and exercise as determinants of spinal trabecular bone density in female athletes. BMJ 1990; 301: 516–8
Martin AD, Houston CS. Osteoporosis, calcium and physical activity. Can Med Assoc J 1987; 136: 587–93
Micklesfield LK, Lambert EV, Fataar AB, et al. Bone mineral density in mature, pre-menopausal ultra-marathon runners. Med Sci Sports Exerc 1995; 27: 688–96
Keen AD, Drinkwater BL. Irreversible bone loss in former amenorrhea athletes. Osteoporos Int 1997; 7: 311–5
Mishell DR. Non-contraceptive benefits of oral contraceptives. J Reprod Med 1993; 38: 1021–9
Wolff I, Croonenborg JJ, Kemper CG, et al. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int 1999; 9: 1–12
Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 1985; 37: 411–7
Chilibeck PD, Sale DG, Webber CE. Exercise and bone mineral density. Sports Med 1995; 19: 103–22
Heinonen A, Oja P, Kannus P, et al. Bone mineral density in female athletes representing sports with different loading characteristics of the skeleton. Bone 1995; 17: 197–203
Frost HM. Proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 1986; 42: 145–56
Fehling PC, Alekel L, Clasey J, et al. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 1995; 17: 205–10
Zanker CL. Bone metabolism in exercise-associated amenorrhoea: the importance of nutrition. Br J Sports Med 1999; 33: 228–9
Petit MA, Prior JC, Barr SI. Running and ovulation positively change cancellous bone in premenopausal women. Med Sci Sports Exerc 1999; 31: 780–7
Mazess RB, Varden HS. Bone density in pre-menopausal women: effects of age, dietary intake, physical activity, smoking, and birth control pills. Am J Clin Nutr 1991; 53: 132–42
Lindsay R, Tohme J, Kanders B. The effect of oral contraceptive use on vertebral bone mass in pre and postmenopausal women. Contraception 1986; 34: 333–40
Lloyd T, Buchanan JR, Ursino GR, et al. Long term oral contraceptive use does not affect trabecular bone density. Am J Obstet Gynecol 1991; 160: 402–4
Bennell K, Matheson G, Heevwisse W, et al. Risk factors for stress fractures. Sports Med 1999; 28: 91–122
Bunt JC. Hormonal alterations due to exercise. Sports Med 1986; 3: 331–45
Borch KW, Ingjer F, Larsen S, et al. Rate of accumulation of blood lactate during graded exercise as a predictor of anaerobic threshold. J Sport Sci 1993; 11: 49–55
Singer RN, Murphey M, Tennant LK. Handbook of research on sport psychology. New York (NY): Macmillan, 1993
Terry P. The efficacy of mood state profiling with elite performers: a review and synthesis. Sport Psychol 1995; 9: 309–24
Billat LV, Koralsztein JP. Significance of the velocity at V̇O2max and time to exhaustion at this velocity. Sports Med 1996; 22: 90–108
Boulay MR, Simoneau JA, Lortie G, et al. Monitoring high-intensity endurance exercise with heart rate and thresholds. Med Sci Sports Exerc 1997; 29: 125–32
Fay L, Londeree BR, Lafontaine TP, et al. Physiological parameters related to distance running performance in female athletes. Med Sci Sports Exerc 1989; 21: 319–24
Davies MJ, Mahar MT, Cunningham LN. Running economy: comparison of body mass adjustment methods. Res Q Exerc Sci 1997; 68: 177–81
Marti B, Howald H. Long term effects of physical training on aerobic capacity: controlled study of former elite athletes. J Appl Physiol 1990; 69: 1451–9
Muoio DM, Leddy JJ, Horvath PJ, et al. Effect of dietary fat on metabolic adjustments to maximal V̇O2 and endurance in runners. Med Sci Sports Exerc 1994 Jan; 26 (1): 81–8
Kravitz L, Robergs RA, Heyward VH, et al. Exercise mode and gender comparisons of energy expenditure at self-selected intensities. Med Sci Sports Exerc 1997; 29: 1028–35
Yoshida T, Udo M, Iwai K, et al. Physiological characteristics related to endurance running performance in female distance runners. J Sports Sci 1993; 11: 57–62
Usaji A, Starc V. Blood pH and lactate kinetics in the assessment of running endurance. Int J Sports Med 1996; 17: 34–40
Smith J, McNaughton L. The effects of intensity of exercise on excess postexercise oxygen consumption and energy expenditure in moderately trained men and women. Eur J Appl Physiol 1993 Nov; 67 (5): 420–5
Quinn TJ, Vroman NB, Kertzer R. Post exercise oxygen consumption in trained females: effect of exercise duration. Med Sci Sports Exerc 1994 Jul; 26 (7): 908–13
Schaeffer SA, Darby LA, Browder KD, et al. Percieved exertion and metabolic responses of women during aerobic dance exercise. Percep Motor skills 1995 Oct; 81 (2): 691–700
Webb P. 24-hour energy expenditure and the menstrual cycle. Am J Clin Nutr 1986; 44: 614–9
Maughan RJ, Greenhaff PL, Leiper JB, et al. Diet composition and the performance of high-intensity exercise. J Sports Sci 1997; 15: 265–75
Hessemer V, Bruck K. Influence of menstrual cycle on thermoregulatory, metabolic, and heart rate responses to exercise at night. J Appl Physiol 1985; 59: 1911–7
Lebrun CM. The effect of the phase of the menstrual cycle and the birth control pill on athletic performance. Clin Sports Med 1994; 13: 419–41
Loucks AB, Horvath SM. Exercise-induced stress responses of amenorrhea and eumenorrhoeic runners. J Clin Endocrinol Metab 1984; 59 (6): 1109–20
Horvath SM, Drinkwater BL. Thermoregulation and the menstrual cycle. Aviat Space Environ Med 1982; 53: 790–4
Jones AM. A five-year physiological case study into an Olympic runner. Br J Sports Med 1998; 32: 39–43
Morgan DW, Craib M. Physiological aspects of running economy. Med Sci Sports Exerc 1992; 24: 456–61
Krahenbuhl GS, Williams TJ. Running economy: changes with age during childhood and adolescence. Med Sci Sports Exerc 1992; 24: 462–6
Pate RR, Macera CA, Bailey SP, et al. Physiological, anthropometric, and training correlates of running economy. Med Sci Sports Exerc 1992; 24: 1128–33
Svedenhag J. Maximal and submaximal oxygen uptake during running: how should body mass be accounted for? Scand J Med Sci Sports 1995; 5: 175–80
Pate RR, Slentz CA, Katz DP. Relationships between skinfold thickness and performance of health related fitness test items. Res Q Exerc Sport 1989 Jun; 60 (2): 183–9
Williams KR, Cavanagh PR, Ziff JL. Biochemical studies of elite female distance runners. Int J Sports Med 1987 Nov; 8 Suppl. 2: 107–18
Hackney AC, Sinning WE, Bruot BC. Hypothalamic-pituitary-testicular axis function in endurance trained males. Int J Sports Med 1990 Aug; 11 (4): 298–303
Daniels JT. A physiologist’s view of running economy. Med Sci Sports Exerc 1985; 17: 332–8
Anderson GS, Rhodes EC. A review of blood lactate and ventilatory methods of detecting transition thresholds. Sports Med 1989; 8: 43–55
Bonekat HW, Dombovy ML, Staats BA. Progesterone-induced changes in exercise performance and ventilatory response. Med Sci Sports Exerc 1987; 19: 118–23
Doolittle TL, Engebretsen J. Performance variations during the menstrual cycle. J Sports Med 1972; 12: 54–8
Wasserman K, Beaver WL, Whipp BJ. Mechanisms and patterns of blood lactate increase during exercise in man. Med Sci Sports Exerc 1986; 18: 344–52
Garlick MA, Bernauer EM. Exercise during the menstrual cycle: variations in physiological baselines. Res Q Sport Exerc Sci 1968; 39: 533–42
Brooks GA. The lactate shuttle during exercise and recovery. Med Sci Sports Exerc 1985; 18: 360–8
Stainsby WN. Biochemical and physiological bases for lactate production. Med Sci Sports Exerc 1986; 18: 341–3
Katz A, Sahlin K. Role of oxygen in regulation of glycolysis and lactate production in human skeletal muscle. Exerc Sports Sci Rev 1997 Mar: 1–27
Wasserman K, Hansen JE, Sue DY. Facilitation of oxygen consumption by lactic acidosis during exercise. News Physiol Sci 1991; 6: 29–34
Bunt JC. Metabolic actions of oestradiol: significance for acute and chronic exercise responses. Med Sci Sports Exerc 1990; 22: 286–90
Kendrick ZV, Ellis GS. Effect of estradiol in tissue gylcogen metabolism and lipid availability in exercising male rats. J Appl Physiol 1991; 71: 1694–9
Eston RG, Burke EJ. Effects of the menstrual cycle on selected responses to short constant load exercise. J Sports Sci 1984; 2: 145–53
Scarperi M, Bleichert A. Non-thermal influences on thermoregulatory behaviour. J Thermoreg Biol 1983; 8: 179–81
Carpenter AJ, Nunneley SA. Endogenous hormones subtly alter women’s responses to heat stress. J Appl Physiol 1988; 65: 2313–7
Haslag WM, Hertzman AR. Temperature regulation in young women. J Appl Physiol 1965; 20: 1283–8
Sargent F, Weinman KP. Eccrine sweat gland activity during the menstrual cycle. J Appl Physiol 1966; 21: 1685–7
Avellini BA, Kamon E, Krajewski JT. Physiological responses of physically fit men and women to acclimation to humid heat. J Appl Physiol 1980; 49: 254–61
Albohm M. Does menstruation affect performance in sports? Physician Sports Med 1976; 4: 76–8
Choi PYL, Salmon P. Symptom changes across the menstrual cycle in competitive sportswomen, exercisers and sedentary women. Br J Clin Psychol 1995; 34: 447–60
Bale P, Davies J. Effects of menstruation and contraceptive pill on the performance of physical education students. Br J Sports Med 1983; 17: 46–50
Dusterberg B, Ellman H, Mulller H et al. A three-year clinical investigation into efficacy, cycle control, and tolerability of a new low-dose monophasic oral contraceptive containing gestodene. Gynecol Endocrinol 1996; 10 (1): 33–9
Rosenberg M. Weight changes with oral contraceptive use during the menstrual cycle: results of daily measurements. Contraception 1998; 58: 345–9
Notelovitz M, Zauner C, McKenzie L, et al. The effect of low-dose oral contraceptive on cardio respiratory function, coagulation, and lipids in exercise in young women: a prelimary report. Am J Obstet Gynecol 1987; 156: 591–8
Lebrun CM. Effect of the different phases of the menstrual cycle and oral contraceptive use on athletic performance. Sports Med 1993; 16: 400–30
Littler WA, Bojorges-Bueno R, Banks J. Cardiovascular dynamics in women during the menstrual cycle and oral contraceptive therapy. Thorax 1974; 29: 567–70
Bonen A, Haynes FW, Graham TE. Substrate and hormonal responses to exercise in women using oral contraceptives. J Appl Physiol 1991; 70: 1917–27
Bryner RW, Toffle RC, Ullrich IH, et al. Effect of low dose oral contraceptives on exercise performance. Br J Sports Med 1996 Mar; 30 (1): 36–40
Bemben DA, Boileau RA, Bahr JM, et al. Effects of oral contraceptives on hormonal and metabolic responses during exercise. Med Sci Sports Exerc 1992; 24: 434–41
Recker RR, Davies M, Hinders SM, et al. Bone gains in young adult women. JAMA 1992; 268: 2403–8
Sowers MF, Wallace RB, Lemke JH. Correlates of forearm bone mass among women during maximal bone mineralisation. Prev Med 1985; 14: 585–96
Polatti F, Perotti F, Filippa N, et al. Bone mass and long-term monophasic oral contraceptive treatment in young women. Contraception 1995; 51: 221–4
Hartard M, Bottermann P, Bartenstein P, et al. Effects on bone mineral density of low-dosed oral contraceptives compared to and combined with physical activity. Contraception 1997; 55: 87–90
Register TC, Jayo MJ, Jerome CP. Oral contraceptive treatment inhibits the normal acquisition of bone mineral in skeletally immature young adult female monkeys. Osteoporos Int 1997; 7: 348–52
Prior JC, Kreiger JN, Tenehouse A, et al. No positive effect of oral contraceptives on bone density: a population-based cross-sectional study in women aged 25–45 from the Canadian multicentre osteoporosis study [abstract]. Bone 1998; 23 Suppl.: 5304
Cooper C, Hannaford P, Croft P, et al. Oral contraceptive use and fractures in women: a prospective study. Bone 1993; 14: 41–5
Schelkun PH. Exercise and the pill. Physician Sports Med 1991; 19: 143–52
About this article
Cite this article
Burrows, M., Bird, S. The Physiology of the Highly Trained Female Endurance Runner. Sports Med 30, 281–300 (2000). https://doi.org/10.2165/00007256-200030040-00004
- Bone Mineral Density
- Menstrual Cycle
- Luteal Phase
- Female Athlete
- Oral Contraceptive Pill