Sports Medicine & Arthroscopy Review:
The Female Athlete
Endocrinologic Changes in Exercising Women
Arena, Bruno M.D.*; Maffulli, Nicola M.D., M.S., Ph.D., FRCS(Orth)
Section Editor(s): Maffulli, Nicola M.D.
*From Servizio Materno Infantile, Azienda Sanitaria Locale, Corso Vittorio Emanuele 163a, 29100 Piacenza, Italy.
†From the Department of Trauma and Orthopedic Surgery, Keele University School of Medicine, North Staffordshire Hospital, Thornburrow Drive, Hartshill, Stoke on Trent, Staffordshire, ST4 7QB, England.
Address correspondence and reprint requests to: Nicola Maffulli, M.D., Department of Trauma and Orthopedic Surgery, Keele University School of Medicine, North Staffordshire Hospital, Thornburrow Drive, Hartshill, Stoke on Trent, Staffordshire, ST4 7QB, England. E-mail: firstname.lastname@example.org
Exercise produces hormonal changes. The more intensive and prolonged the exercise is, the more pronounced the changes are. In postpubertal female athletes, these changes are generally transient (for example, anovulation and menstrual cycle irregularity), with no long-term effects. In younger athletes, however, the hormonal changes produced by prolonged and strenuous exercise, particularly when competition is involved, require careful monitoring for their potential effects on the time of onset of puberty and the delay in menarche. Stress, anxiety, recurrent increase in body core temperature produced by strenuous physical activity, and an inadequate diet are among the most important factors that can enhance these hormonal alterations. We review the recent literature on hormonal changes in exercising women, focusing on the effects of exercise on gonadotrophins, sex steroid hormones, cortisol, prolactin, melatonin, growth hormone, endorphins, and parathyroid hormone.
Endocrine responses to exercise tend to produce anabolic effects: hypertrophy of the muscles, increase in bone size and calcification, and reduction in the percentage of body fat. A body core temperature of at least 38°C seems to be necessary before exercise can produce significant hormonal changes, particularly of growth hormone (GH), prolactin (PRL), epinephrine (E), and norepinephrine (NE). 1 The increase in core temperature may interfere with the binding of hormones to plasma proteins, with a consequent increase of the circulating, metabolically active hormonal fraction. 2 Nutrition can influence the metabolic and hormonal responses to exercise: a protein-carbohydrate supplement before and after heavy-resistance exercise reduces lactate, GH, PRL, and testosterone (T) responses to exercise. 3 Exercise may also affect the immune system by stimulating chemotaxis of peritoneal macrophages. 4
Maximal aerobic power increases significantly with exercise, whereas plasminogen activator inhibitor type 1 and tissue plasminogen activator decrease. Fasting plasma insulin and glucose are also lower in exercising women, and lipid and lipoprotein profiles tend to improve toward a less atherogenic pattern. 5
Acidosis that develops with prolonged, strenuous exercise is considered an important cofactor in the onset of hormonal changes. Administration of NaHCO3 before and during a bout of anaerobic exercise can blunt the increase of beta-endorphin, reduce GH release, and enhance the PRL increase commonly seen with exercise. 6 Regular exercise affects the homeostasis of blood glucose; this should be taken into account in the management of diabetic patients who practice sport, because the neuroendocrine and metabolic counterregulatory responses to hypoglycemia can be blunted and insulin sensitivity can be enhanced. 7
Regular exercise can reduce depression and anxiety. In animal models, the effects on brain biochemistry vary with the type of exercise performed. Chronic wheel running increases NE levels in the pons medulla at rest and protects against NE depletion in the cell bodies of the locus ceruleus after administration of a footshock. A decrease of γ-aminobutyric acid (GABA) receptors in the corpus striatum has also been noticed. In contrast, treadmill exercise training increases the metabolism of NE in ascending terminal areas of the brain for NE, and has no effect on GABA receptor density. 8 In humans, there is a rise in catecholamine (C) and T levels prior to competition, significantly higher for C in winners than in losers. 9
Gonadotrophins and Sex Steroid Hormones
Exercising women achieve higher strength when the training sessions are held mainly during the follicular phase of the cycle, when estradiol levels are higher, rather than spread over the whole of the cycle. 10 Acute exercise determines an increase in 4-hydroxyestrogens (4-OHE), also known as catecholestrogens, which have a strong estrogenic potency and an affinity for the enzyme catechol-O-methyltransferase (COMT), the enzyme that deactivates catecholamines. This increase may contribute to the onset of the menstrual irregularities associated with exercise. When insufficiently methylated, 4-OHE may raise mutagenic superoxide free radicals and produce cellular DNA damage, a potential cancerigenic effect. 11
Menstrual disturbances and anovulation in runners do not appear to be linked to an increase in opioid tone, and the hypothalamic-gonadotropic axis shows a normal response to administration of estrogen and progesterone. 12 Prolonged and strenuous exercise can affect the pulsatile release of luteinizing hormone (LH), causing its reduction or even disappearance, particularly when the stress of competition is high. 13,14 Follicle-stimulating hormone (FSH) has a longer half-life than LH, and FSH levels in the blood may rise after an endurance exercise. Blood levels of LH, sex hormone binding globulin (SHBG), and estradiol are lower after exercise in athletic women compared with eumenorrheic controls. 15 Low gonadotrophin levels can produce anovulation and temporary infertility. 16
Decreased plasma levels of estrogens and progesterone can produce oligomenorrhea or amenorrhea and, in the long term, the changes in bone mineral density usually found in postmenopausal women. 17,18 Low estrogen levels are probably more significant than low progesterone levels in determining bone remodeling and decalcification, 19 whereas the reduction in SHBG produced by exercise has a protective effect against bone resorption in postmenopausal women. 20
Women who have regular periods while practicing sport differ in their hormonal response to exercise from women who develop oligomenorrhea or amenorrhea. Eumenorrheic runners show a reduced gonadotrophin response after administration of GnRH compared with their amenorrheic counterparts. 21,22
Estrogen and progesterone can affect the metabolic response to exercise by determining a preferential oxidation of lipids rather than carbohydrates. 23 Intensive competition season training loads and body weight reduction in female lightweight rowers is associated with a significant reduction in excretion of progesterone metabolites and a lesser decrease in excretion of estrone metabolites. 24
The hormonal response to exercise may vary according to the individual level of training. In trained, healthy women, an increase in plasma estradiol during an acute bicycle ergometer bout and a decrease in plasma estradiol metabolic clearance are more pronounced than in untrained controls. The phase of the menstrual cycle during exercise can also affect the hormonal response: estradiol tends to vary less following moderate exercise in the follicular phase than in the mid-luteal phase. 15,25,26
Blood levels of dehydroepiandrosterone sulphate (DHEA-S), androstenedione (A), and testosterone (T) can all increase following exercise, but only DHEA-S remains elevated for more than 2 hours. This is thought to depend on a prolonged adrenocorticotropin stimulation or on a reduced hepatic clearance. 27,28 The increased androgen levels may further enhance the muscular hypertrophy produced by exercise, while DHEA-S can increase high-density lipoprotein cholesterol (HDL-C), which has a cardioprotective effect. 29
ACTH and Cortisol
Sustained physical activity at an altitude of 3700 m activates the adrenocortical function in healthy individuals, producing an increase in the level of cortisol. In 30% of individuals, administration of 1 mg of dexamethasone does not suppress this increase.
The concomitant state of relative hypoxia is thought also to be important for this effect. 30 Exercise-induced increases in cortisol and prostaglandins could depress the cellular-mediated immune function and consequently impair the cancer surveillance capacity of the body. The significance of this effect is nevertheless still uncertain, 31 since serum cortisol levels do not always increase following exercise, as has been found during the first 4 weeks of training in female endurance athletes. 32
The level of training of the individual athlete can influence the hormonal responses to high-intensity exercise. In trained subjects, the maximum concentrations of adrenocorticotrophic hormone (ACTH) and β-endorphin tend to be significantly lower during the recovery period than in untrained subjects, 33 and postexercise elevations of serum cortisol and prolactin can be closely linked to the amount of workload. 34 Cortisol levels increase during exercise in amenorrheic subjects more than in eumenorrheic controls. 35 This increase can suppress the pulsatile release of LH by causing an imbalance between facilitating and inhibiting neurotransmitters, 36 and breast feeding can reduce ACTH and cortisol responses to exercise. 37 Subjects with atopic eczema and a poor ACTH and cortisol response to the administration of human corticotropin-releasing hormone have a significant ACTH and cortisol rise after an incremental graded bicycle exercise; this could be due to neuropeptides released during exercise, affecting the hypothalamic-pituitary-adrenal axis. 38
Serum prolactin (PRL) levels can show a variable response to exercise, as they may decrease after moderate endurance training and increase after heavy training. 39 The increase is more pronounced in eumenorrheic than in amenorrheic runners. 40
The increased release of PRL after exercise can be affected, as already mentioned, by the increase in body temperature produced by the exercise 41 and by the changes in peripheral tryptophan and branched chain amino acids concentration, which may influence prolactin response via modifications in the serotoninergic system. 42 In addition, opioid production during exercise can stimulate the release of PRL, 43 which can induce adrenal release of androgens 44 and interfere with the ovarian aromatization of androgens, precursors to estrogens.
Melatonin, an indole derivative of serotonin produced with a circadian rhythm, modulates the sleep–wakefulness cycle. Melatonin production decreases during light and increases during darkness. It is produced in the pineal gland, located in the roof of the third ventricle in the brain. The pineal gland in humans is under alpha- (inhibitory) and beta-adrenergic (stimulatory) influence. 45 In animals, melatonin protects liver, muscles, and brain against the oxidative damage and lipid peroxidation associated with exercise by acting as a free radicals scavenger, via electron donation. 46
Exercise may have a significant effect on melatonin secretion: it may delay the onset of nocturnal secretion by up to 24 hours and, if carried out in the late evening, when melatonin levels are increasing, may blunt this increase. Conversely, exercise carried out during the night, when melatonin levels are already elevated, may produce a further increase in melatonin levels by up to 50%. There appears to be no significant effect on melatonin secretion when the exercise is carried out during daytime. 47 When administered to rats run to exhaustion on a rodent treadmill, melatonin can preserve glycogen stores through changes in carbohydrate and lipid utilization. It reduces plasma lactate and increases lactate concentration in the liver, blood glucose levels, and muscle and liver glycogen content. 48 Melatonin is also likely to modulate pituitary secretion of GH, as suggested by the significant increase in exercise-induced GH secretion after a single dose of oral melatonin (5 mg) to healthy male subjects undergoing a bicycle exercise at a workload corresponding to 70% of maximum oxygen consumption (Vo2max). 49 Administration of melatonin prior to a bicycle ergometer exercise, with a 3-minute interval gradual increase of the workload to exhaustion, blunts the increase of plasma arginin vasopressin (AVP) (2.3 times levels instead of 3.6), while there is no significant effect on angiotensin II secretion. 50
Growth hormone secretion is stimulated by exercise via a hypothalamic pathway facilitated by melatonin. 49 Growth hormone response to exercise is more pronounced in women who use oral contraceptives than in non-users, 51 and training also reduces blood levels of GH binding protein (GHBP). As a consequence, the unbound, metabolically active fraction of GH increases. 52 Muscle hypertrophy produced by exercise is mostly induced by mechanical strain, but GH has an important role in reparative muscle growth. 53
Eumenorrheic and amenorrheic athletes show higher β-endorphin blood levels compared with sedentary controls, and the pattern of secretion of β-endorphins appears to be independent of the phase of the menstrual cycle during exercise. 54 Elevated levels of endorphins, such as those found in exercising women, can increase blood levels of GH and PRL, 43 but conversely interfere with the GnRH production and, consequently, the LH pulsatile secretion. 55 Naloxone appears to counteract this effect in eumenorrheic but not in amenorrheic athletes. 56
Moderate exercise can inhibit the secretion of PTH, whereas strenuous exercise can stimulate PTH secretion. This raises concerns for the possible effects on bone. In female athletes with healthy bone mineral density, PTH secretion can be suppressed temporarily soon after maximal anaerobic exercise. Secretion of PTH increases during recovery. 57
Endurance runners, compared to sex-matched, population-based controls, show a higher mineral density in the bones of the legs, but not in the lumbar spine or in the forearm. They also show lower levels of PTH and biochemical markers of bone metabolism. This confirms previous findings of a protective effect of specific types of exercise on different bone segments. Ovarian hormone levels of the individual athlete, as measured by estrogen and progesterone metabolites excretion, must also be considered to explain this effect. 58,59 After 60 minutes of bicycling, PTH increases by 50% of baseline values, despite an increase in serum levels of calcium, phosphorus, and magnesium. Pretreatment with 0.5 mg of dexamethasone affects serum levels of cortisol and ACTH, but has no apparent effect on PTH or calcium levels. 60
In elderly subjects, 6 weeks of endurance training increase exercise-related release of PTH and reduce the levels of osteocalcin, a marker of positive bone remodeling. Before training, a maximal exercise test produces an increase of serum levels of PTH, as well as of osteocalcin. These findings have to be considered when regular exercise is evaluated as a preventive measure of osteopenia in elderly subjects. 61 At the opposite end of the age scale, in preterm infants with very low birth weights, a physical activity program consisting of a range of motion with passive resistance to all extremities for 5 to 10 minutes daily enhances the effects of adequate nutrition on weight gain and bone mass. 62 Prolonged endurance exercise in healthy young male subjects produces a relative increase in osteocalcin levels, together with a pronounced decrease in carboxyterminal cross-linked telopeptide of type I collagen (ICTP), an index of a positive effect on bone mass. 63 Resting levels of PTH, as well as exercise-induced increases, are higher in heart transplant recipients than in healthy controls, and a short endurance training program does not alter this pattern. 64 A single bout of moderate endurance exercise (outdoor jogging for 45 minutes at an intensity of 50% of Vo2max) in young female subjects produces biochemical signs of increased bone collagen turnover, decrease in serum calcium levels, and an increase in PTH levels. 65 In a similar fashion, in well-trained men and women, one single bout of long-term, exhaustive running exercise can induce a temporary inhibition of bone formation and stimulate bone resorption, as evidenced by a decrease of carboxyterminal propeptide of type I procollagen (PICP), a decrease of osteocalcin, and an increase of the carboxyterminal cross-linked telopeptide of type I collagen (ICTP). 66
Serotonin (5-HT) is a neurotransmitter able to modulate both physiological and psychological aspects of fatigue. Exercise appears to induce a down-regulation of central serotoninergic receptors, which could play a significant role in producing the anxiolytic and antidepressive effects of exercise. 67 Acute endurance exercise can determine an increase in the peripheral concentration of tryptophan, the precursor of 5-HT, and a reduction of 5-HT receptors on the platelets. It is not clear whether this goes in parallel with an increased availability of 5-HT in the brain. 68
Although some sports (e.g., running) tend to produce hormonal changes and oligo-amenorrhea more often than others (e.g., swimming), particularly in women with predisposing factors (lower than normal body fat or a history of menstrual disturbances prior to the beginning of physical activity), physical exercise has definite positive effects on general health and fitness and can therefore be recommended without reservations. Younger, peri-pubertal athletes undergoing intensive physical training, particularly when competition is involved, will need closer supervision by experienced personnel than their older counterparts.
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Nicola Maffulli, M.D., Guest Editor
Women; Exercise; Hormonal imbalance
© 2002 Lippincott Williams & Wilkins, Inc.
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