Women's participation in sports has greatly expanded over the past 25 years. With this has come an increased awareness of new conditions and pathologies unique to this population. Women who are active as girls have greater self-confidence and pride in their abilities. 1 In the United States, both Title IX and the Amateur Sports Act served as driving forces to promote equalization of the number of women in competitive sport, and it appears that these laws have produced a high level of participation of women at the high school and college levels. 2
Although until recently, medical practitioners believed that intense athletic training would stress a woman's reproductive system, the differences between men's and women's injuries are more attributable to sport specificity than to gender. In addition, special attention has been focused on both young 3 and older female athletes.
In 1992, the term female athlete triad was coined to describe three distinct, but frequently interrelated, disorders found in the female athletic population: disordered eating, amenorrhea, and osteoporosis. Individually, each of these entities can cause significant morbidity. Together, they are synergistically detrimental.
The triad can begin with disordered eating patterns, intentional or unintentional, which can then progress to menstrual disorders, and finally to decreased bone density and osteoporosis. It is also thought that menstrual dysfunction can occur with an increase in training, in combination with physical or psychological stress. The female athlete triad should be of concern to all female athletes, 4 whether they are highly-trained athletes, health club and running “addicts,” or simply physically active girls and women.
The first component of the triad is typically initiated by an athlete's desire to lose weight by dieting. To some extent, all athletes are concerned with diet and body image, but in susceptible individuals, this preoccupation can become pathologic. Disordered eating patterns cover a wide spectrum, from simple food restriction to the frank eating disorders of anorexia and bulimia nervosa. All can have significant implications for an athlete's health.
One main worry that female athletes encounter, leading to these destructive patterns, is body image. Body image is multi-faceted, and includes perceptual, attitudinal, and behavioral aspects. 5 An athlete's inner mental view of herself, combined with her associated attitudes and behaviors, can often lead to a distorted body image. In addition, there is constant pressure for these women to preserve slender athletic bodies that are still “feminine.” Body composition can also affect selection of athletes for their sport. For example, dancers must attempt to “achieve a weight that is uniform with other dancers, that can be lifted, and that fits costumes and the vision of the choreographer.”6 Many other sports have a similar athletic component and stereotype.
There appears to be a higher tendency toward dieting in white adolescent girls from higher-income families. 7 It is a matter of concern that not only has dieting become routine in normal-weight adolescents, but that more girls and women aged 15 to 24 are dieting. 8 One explanation for the higher preponderance of eating disorders in girls than in boys may stem from societal values. Girls tend to diet to lose weight; boys usually attempt to gain weight (especially muscle mass) by eating. The effect of the media on occurrence of eating disorders is still unknown. 9,10
Regardless, studies have continued to suggest that athletes, as a subgroup, have an even higher incidence of disordered eating than the general population. 11 Compared to non-élite athletes, élite athletes seem to be at increased risk for eating disorders, 12 especially in sports emphasizing leanness 7 and in weight-class sports. 13 In a study of young élite swimmers, it was found that 60.5% of average-weight girls and 17.9% of underweight girls were trying to lose weight. 14 Johnson et al. 15 found the incidence of eating disorders among NCAA student athletes in 1999 to be more conservative than in similar previous studies, yet female athletes continue to report more disordered eating patterns than males.
Various factors have been postulated to be involved in the development of eating disorders. Powers et al. 5 describe the psychosomatic model, which comprises predisposing, precipitating, and sustaining factors. Predisposing factors include cultures idealizing thinness, families with poor conflict resolution, and obsessive-compulsive personality disorders. Precipitating factors include dieting, being teased about size or shape, death of a family member, and the onset of a developmental stage for which the athlete is unprepared. Sustaining factors are development of physiologic consequences of the disordered eating patterns or emergence of other psychiatric disorders.
Athletes are at as much risk of encountering these factors as the general population. However, athletes face additional stressors. These include pressure to perform or to meet unrealistic weight or body fat goals from demanding coaches, peers, and family. The very personality traits that aid an athlete to reach the top of his or her sport—perfectionism, compulsiveness, and high achievement expectations–are also personality risk factors for development of eating disorders. 3 Beals and Manore 16 found that there were specific characteristics commonly found in female athletes with subclinical eating disorders. These included “preoccupation with food, energy intake, and body weight; distorted body image and body weight dissatisfaction; undue influence of body weight on self-evaluation; intense fear of gaining weight even though at or slightly below (approximately 5%) normal weight; attempts to lose weight using one or more pathogenic weight control methods; food intake governed by self-hatred upon breaking a rule; absence of medical disorder to explain energy restriction, weight loss, or maintenance of low body weight, and menstrual dysfunction.”16 Certain sports seem to be at a higher risk for development of any component of the triad, especially those in which leanness is perceived to optimize performance. 3 In addition, sports with specific weight categories, such as rowing or martial arts, are also predisposed to potentiate such behavior.
Anorexia nervosa (AN) is characterized by weight loss from self-starvation. 17,18 Several characteristics can accompany this disorder, namely a distorted body image (the hallmark), a strong denial pattern, and perfectionism. 4,19 Clinical signs include amenorrhea, 4 minimal subcutaneous fat, muscle loss, dry hair and skin, bradycardia and orthostatic hypotension, and lanugo hair. 19,20 These reflect the body's response to starvation. Numerous psychological characteristics are also associated with these symptoms. All of the criteria in Table 1 must be satisfied in order to make the diagnosis.
Anorexia nervosa is the most common cause of weight loss in adolescent girls in the United States. 5 Most patients who are diagnosed with this condition are not overweight in the beginning. One study found that 20% of anorexia nervosa patients were underweight, 50% were normal weight, and only 30% were overweight before onset of the disorder. 21
Athletes may have a distinct psychological makeup that is different from nonathletic patients with anorexia. Sundgot-Borgen 21 has proposed a new and slightly different classification system for the athlete:anorexia athletica. For positive diagnosis of this disorder, patients must meet five criteria:
- Excessive fear of becoming obese
- Restriction of caloric intake
- Weight loss
- No medical disorder
- Gastrointestinal symptoms
In addition to these, they must also exhibit one or more of the following:
- Disturbance in body image
- Compulsive exercising
- Binge eating
- Use of purging methods
- Delayed puberty
- Menstrual dysfunction
To date, there are no studies documenting the true incidence of anorexia athletica, or comparing it with anorexia nervosa as defined by the DSM-IV criteria.
Bulimia nervosa (BN) is similar to AN in terms of a distorted body image and a drive for thinness, yet the patient's body weight throughout the illness is typically at or above normal. 4,23 Often, the person is reaching out for help, and is aware of her disordered eating behavior. Bulimia is characterized by binge eating, followed by some type of purging behavior (Table 2). Factors leading to binge eating may include inappropriate food restriction, overt hunger, and stress. 5
There are no precise estimates of incidence of BN, due to the secretiveness of patients, diverse study designs, and short diagnostic history. 7 Yet the numbers seem to be on the increase. Clinical signs include fluctuations in weight, facial edema, erosion of tooth enamel from recurrent vomiting, esophagitis, calluses on the dorsum of the hand, and enlargement of the parotid glands and cervical lymph nodes. 4 Other warning signs include not eating with the team, visits to the washroom after meals, and excessive preoccupation with quantities of food or calories.
There are two subgroups of bulimia nervosa: purging and non-purging types. Purging involves regular self-induced vomiting or the misuse of laxatives, diuretics, or enemas, whereas non-purging types use other methods to compensate, such as fasting or excessive exercise. 17 The latter type is frequently the abnormal behavior demonstrated by athletes.
Eating Disorders Not Otherwise Specified (EDNOS)
Because not all disordered eating behaviors fit the exact description of the frank eating disorders above, there is an additional classification of Eating Disorders Not Otherwise Specified (EDNOS). 17 Some characteristics of anorexia or bulimia may be evident, while others may not present at all (Table 3).
Although it is important to understand the etiology of the eating disorders, it is also necessary to know that in most situations, the athlete has developed a disordered eating behavior that simply does not provide an adequate amount of calories for the amount of energy expended during exercise. Fagan 24 refers to a pattern of eating in which the athlete does not sit down to a full meal, but snacks or skips the meal entirely, continuing to train as usual. In the long run, this may lead to an energy deficit.
There are multiple complications which can arise from the subclinical eating disorders, as well as the more severe forms of AN and BN. In the athlete, disordered eating patterns are thought to impair athletic performance and increase risk of musculoskeletal injury. 3 Consequences may include depression, fluid and electrolyte imbalance, and changes in the cardiovascular, endocrine, gastrointestinal, and thermoregulatory systems. 25,26 The human body can initially adapt to these changes, and therefore, athletes falsely believe these practices are harmless. Long-term health problems include possible infertility, cardiac abnormalities, and the third component of the female athlete triad, osteoporosis. 27 Complications from severe eating disorders can potentially be fatal. 3
Body composition is a highly debated topic, and the various methods of measurement and the perceived importance in successful athletics cannot be ignored. Sports such as gymnastics, ballet dancing, and figure skating all involve lifting or movement of body mass, which highlights a desire for a high lean to fat mass ratio. 28 However, continued weight loss does not equal athletic success or continual improvements in performance. In fact, it can lead to decrements in performance and health. Muscle strength, anaerobic power, and endurance can all be adversely affected. 29 There is little or no evidence that a reduction in weight will improve performance in athletes who are already lean. 28
Normal Menstrual Cycle
Normal menstrual function is dependent on intact hormonal signals between the hypothalamus, pituitary, ovaries, and uterus. 4 Both luteinizing hormone (LH) and follicle-stimulating hormone (FSH), arising from the anterior pituitary, are released in response to gonadotropin releasing hormone (GnRH) from the hypothalamus. Depending on the phase of the cycle (follicular or luteal), differing amounts of each hormone regulate the growth and development of the follicle. Any alteration in hormone secretion beyond normal pulsatile function will affect menstrual function. A normal menstrual cycle usually lasts 23 to 35 days and will occur 10 to 13 times per year. This is referred to as eumenorrhea 4 (Fig. 1).
Oligomenorrhea, Amenorrhea, Luteal Phase Deficiency
There are three types of menstrual dysfunction: amenorrhea (primary and secondary), oligomenorrhea, and luteal phase deficiency. 29–31 A diagnosis of primary amenorrhea is made when the athlete has not begun menarche after the age of 16, despite having secondary sex characteristics. Although many different definitions exist for secondary amenorrhea, it is usually defined as the absence of at least 3 to 6 consecutive menstrual cycles after the establishment of menses. The American College of Sports Medicine position stand on the female athlete triad uses this definition. 18 The International Olympic Committee, however, defines amenorrhea as one or fewer menstrual periods per year. 32 Athletes with oligomenorrhea have menstrual periods that occur at intervals longer than every 35 days. 30–32 In the adolescent female, irregular periods or amenorrhea may last for three to six months in the first several years after menarche. A diagnosis of secondary amenorrhea or oligomenorrhea is therefore only made when menses stop for longer than 3 months after regular cycles have been established. 33
The profile of menstrual dysfunction varies considerably. With luteal phase deficiency, considered the least severe form, 34 total cycle length may be normal, yet progesterone levels decrease and there is a shortening of the luteal phase. 4 The main problem associated with luteal phase deficiency is decreased fertility during those particular cycles in which it occurs. The situation becomes more severe when follicles start to develop, but the process ceases before ovulation. This can create an environment of unopposed estrogen, which potentially increases the risk for endometrial cancer. 34 In these anovulatory cycles, irregular bleeding may still occur, so the athlete may think that there is no problem. Amenorrhea is the end stage, with no follicular development, no ovulation, no menstrual bleeding, and a permanent hypoestrogenic state. Unfortunately, many athletes view amenorrhea as simply “one less hassle while training.”24
The incidence of amenorrhea among female athletes varies widely, largely because of a bias in group selection, inconsistency in the definition, and lack of reporting. 23 However, the prevalence is much higher in athletes, compared with the general population: the range within athletes is from 3.4% to 66%, compared with 2% to 5% in the general population. 4
So-called athletic amenorrhea is a subset of hypothalamic amenorrhea, but this is a diagnosis of exclusion. 24,25 All other medical causes must have been ruled out by a thorough history and physical examination, as well as appropriate investigations. Because weight, body composition, fat distribution, eating behavior, and exercise all influence menstrual function, 34 these factors must also be considered. Other causes of amenorrhea are outlined in Table 4.
In swimmers, amenorrhea may be caused by a different entity. In most female athletes, amenorrhea is due to hypoestrogenism. Constantini and Warren 36 found that reproductive dysfunction in swimmers may actually be caused by mild hyperandrogenism. Warren and Perlroth 37 extended these findings to athletes involved in sports emphasizing strength over leanness.
Body Fat Percentage
Although body fat percentage has an important role in the development of amenorrhea, it is not the sole factor. It was previously thought that there was a critical level of body fat necessary to maintain normal menstrual function, although this has since been disproved. Athletes with percentages as low as 4% can have regular menses. 38 There is still a possibility that there is an individual threshold of body fat for normal menses, but it would require careful monitoring of each athlete to determine whether this is actually true. 28 It is not uncommon for athletes to stop having regular menstrual cycles during their competitive season and resume them in the off-season, when their training is less intense.
Diet and Energy Availability
After a period of dieting, low caloric intakes result in what is known as an energy deficit or drain. This may be unintentional, resulting from the high-energy demands of intense training with inadequate nutritional replenishment; or intentional, to supposedly improve appearance or performance. 3 Luteinizing hormone (LH) pulsatility depends on energy availability, which, in turn, affects menstrual regulation. Various metabolic functions are altered as well, including “hypoglycemia, hypoinsulinemia, hypothyroidism, hypercortisolism, and the suppression of the 24-hour mean and amplitude of the diurnal rhythm of leptin.”39–43 Amenorrhea, in this situation, could be the body's adaptation to conserve energy. 34
Beyond caloric deficit, there exists some evidence that diet, in particular vegetarianism, plays a role in determination of menstrual function. 44 High dietary fiber intake may interfere with estrogen reabsorption, and the activity and binding ability of estradiol may be hindered because of the weak estrogenic activity of plant lignins and isoflavones. 45
Estrogen Fuel Hypothesis
Estrogen absorption may also be affected by its metabolites. Snow et al. 46 found that athletes with a greater fraction of estrogen metabolites that are lacking peripheral estrogen activity had menstrual irregularities. They suggested that the ensuing increase in catecholamines and decrease in estriol resulted in a hypoestrogenic state. A decrease in body fat because of the high-intensity work further restricted peripherally active estrogen.
Exercise Changes in Circulating Growth Factors and Leptins
Members of the Insulin-like Growth Factor (IGF) family and their binding proteins are found in brain, pituitary, and ovarian tissue, and thus play a role in the regulation of the reproductive hormones GnRH, FSH, and LH. Because their concentrations also change in response to high-intensity exercise and stress, these factors may be partially responsible for changes in hormone levels. With an increase in exercise, there is an increase in the concentration of leptins, which act on the hypothalamus to increase basal metabolism and decrease appetite. 47
Certain athletes who increase training intensity may continue to have regular menstrual cycles. However, when psychological stress is added, this may affect menstrual function. 34 This stress may be present in the form of precompetition anxiety, or something unrelated to sports, such as family conflict or academic deadlines.
Although each theory on its own presents valid evidence for causing menstrual irregularities, amenorrhea itself may be exacerbated by a combination of these factors. The effects of two or more of these factors together would likely be synergistic and increase morbidity.
Amenorrhea has been associated with reproductive dysfunction, decreased bone density, and an altered cholesterol profile. 48–50 Because of its resulting hypoestrogenic state, amenorrhea can affect many different functions, including athletic performance.
The cardioprotective effect of estrogen on lipids and vessel walls may be lost with amenorrhea. 45 Amenorrheic athletes may be at higher risk for cardiovascular disease, because of an increased potential for lipid peroxidation after exercise. 34 In addition, the prolonged hypoestrogenic states may lead to long-term decrements in cardiovascular performance and health. 51 However, there is conflicting research in this area. One study found that athletes who were amenorrheic actually performed better than their eumenorrheic counterparts. 52
The research on recovery of reproductive function after amenorrhea is inconclusive. There is no evidence for long-term harmful effects on reproductive status, 52 but more studies should be conducted with longer-term amenorrhea. As amenorrheic athletes exhibit a decrease in the number of ovulatory cycles experienced throughout their lifetimes, they might have an increased incidence of breast, ovarian, and endometrial cancers. 45
To et al. 53 found a lower BMI and higher incidence of musculoskeletal injuries and chronic orthopedic problems in oligomenorrheic and amenorrheic students than in eumenorrheic students. They suggest that hypoestrogenism could be related to non-bony musculoskeletal injuries. 54
The main concern with prolonged amenorrhea, however, is the premature loss of bone density. This can lead to stress fractures and ultimately to early (and potentially irreversible) osteoporosis. The length of time for which amenorrhea is present is important, 18 and even after resumption of normal menses, amenorrheic athletes show only partial recovery of initial bone density. 34
These consequences highlight the need for education, not only for athletes, but also for parents, coaches, and health care professionals. Before engaging in high-intensity endeavors or a relatively rapid increase in training volume or intensity, female athletes should be made aware of the potential for menstrual irregularities. 34 Early identification of amenorrhea is crucial, because maximum bone loss occurs in the early stages of amenorrhea, 55 and it may lead to premature osteoporosis. 51
Athletes with amenorrhea or disordered eating patterns have yet another major concern: osteoporosis. A decrease in the levels of estrogen can affect bone density as well as reproductive function. Most bone mass is gained during the adolescent years. It is particularly important to increase bone density through exercise during this time. 56–58 By 18 years of age, most women have reached 95% of their peak bone mass. Once this peak is attained, women lose approximately 1% per year until the onset of menopause, 18 at which point there is a 10-fold increase in rate of bone loss. 19
When a young athlete presents with amenorrhea, she may have lost bone mass that had already accumulated, or may have failed to lay down the normal amount of bone that is gained during these critical years. 20 A 20-year-old woman with frank anorexia can present with bone structure profile similar to that of a 50- to 60-year-old woman. 59 The extent to which athletic amenorrhea affects bone mineral density (BMD) depends on factors such as age of menarche, timing and duration of amenorrhea, total energy intake, and type of exercise. 60 Other variables include BMI or body composition, free cortisol levels, exercise, or relative estrogen exposure. 61 The bottom line is that the degree of weight loss and duration of amenorrhea or eating disorder is directly related to BMD determination. 61
The World Health Organization defines osteoporosis as bone mineral density greater than 2.5 standard deviations (SDs) below the mean of a normal young female, and severe osteoporosis as also having one or more fragility fractures. 18 Osteopenia, the least severe form, is defined as bone density 1.0 SD below the mean. It is believed to affect 25 million people in the United States alone, and is the cause of 1.5 million fractures per year. 19
Numerous studies 62–64 have shown the positive effect of impact-loading on bone mineral density. However, even weight-bearing exercise may not be enough to offset deleterious effects of high-intensity training, poor nutritional behaviors, or genetic predisposition toward lower-than-average bone density. Although estrogen status is thought to be a major factor in the development of stress fractures and osteoporosis, this cannot be the only factor. This is evidenced by the fact that patients with frank anorexia nervosa have lower BMD than those with hypothalamic amenorrhea, such as athletes. 65 Bone density can also be affected by type of sport. Speed skaters, runners, gymnasts, and figure skaters may have increased BMD at specific sites, 51 due to the osteogenic effect of weight-bearing exercise. In addition, rowers may have increased BMD in the spine, due to increased load in this area. 66 These athletes may have higher BMD than others, despite the occurrence of menstrual disorders, but is it is not known whether these protective effects will continue with prolonged amenorrhea. 67 Additionally, most athletes do not reach this training intensity level. All amenorrheic athletes, regardless of sport type or level, should therefore have their BMD monitored on a regular basis.
The consequences of decreased BMD are not favorable. Even if the athlete re-establishes normal menses, she will still retain an increased risk of fracture after the competitive years are over. 68 For every SD that BMD falls below normal in young adults, fracture risk is approximately doubled. 61 If the athlete continues in her sport, not only is she at risk for a higher incidence of stress fractures during her competitive years, she is also at risk for development of premature osteoporosis. 69 Premature loss of bone may have already occurred if the athlete has missed more than six consecutive periods. Loss of trabecular bone reaches approximately 4% in the first hypoestrogenic year. Amenorrheic athletes experience a significantly lower BMD at multiple sites, 70,71 not limited exclusively to the axial skeleton, as it was previously thought.
Osteoporosis itself is responsible for over 1,300,000 fractures per year in the United States, and, for many, signifies the move from independence to total dependence. 4 As many as 20% of those suffering from a hip fracture die within the first year. 72
When an athlete has sufficient estrogen, mechanical loading on the skeleton has a positive effect on bone. 69 Exercise becomes a concern when the type, volume, frequency, or intensity of the sport places demands that are too high for the athlete to counteract. When treating an athlete, it may be difficult to convince her that being amenorrheic may cause her to sustain a serious fracture in the future. It may carry more weight to inform the athlete that a resultant stress fracture may well prohibit participation in her current activity. 24 Bone mineral density is important both in the long and short term of an athlete's lifespan.
Prevention is by far the first priority when dealing with the triad. Early detection is also crucial when dealing with athletes who already exhibit the signs and symptoms (Fig. 2). The preparticipation physical examination (PPE) 68 may be the best tool for prevention and detection of these disorders. Usually accompanied with a medical history form that can present red flags, the PPE can be used for follow-up for athletes considered to be at risk. Both the form and the examination itself can offer an excellent opportunity to screen for the triad disorders, 51,66 to establish rapport with the athlete, 73 and build the amount of historical information about the patient. 68
Many researchers have proposed that a section on the medical history form be directed specifically to the female athlete (Fig. 3). This section should consist of a gynecologic component and a nutritional component. 51 The gynecologic component should include questions on menstrual history, 5,51,55,66 age of menarche, 51,55,59,66,74 length and frequency of periods, 18,51,55 date of last period, 35,51,55,59,74 and use of medication or hormonal therapy. 51,55,59 The nutritional component should consist of questions relating to the person's desire to lose weight, current weight, admittance of disordered eating behavior, 51 and diet and weight history. 5 A detailed weight history, in particular, can aid in detection of the onset of disordered eating behavior. 5 Additional questions may include history of any stress fractures 51,66,74 or any increase in quantity and intensity of exercise. 35
If any red flags appear on the form after careful analysis, the examiner must follow them up. This can be accomplished by conducting a full PPE or by simply examining the specific question in further detail (e.g., by an interview with the athlete) to determine whether intervention is necessary. Routine lab tests are discouraged from being a part of the PPE, unless there is suspicion that the athlete in question has an eating disorder or other component of the triad. 73 Psychological screening tests, such as the Eating Disorders Inventory test, may be helpful if disordered eating patterns are suspected. However, these surveys have been developed in a nonathletic population, so they may not specifically pick up athletes at risk. There may also be emphatic denial on the part of the athlete.
Although prevention of these disorders is by far the best form of treatment, education is also key, and all personnel involved in athletics should be made aware of the significance of the triad. An excellent review article by Seidenfeld 75 provides a backdrop for treatment of early (or mild stage) to established (or moderate stage) eating disorders. Intervention must be implemented when patients exhibit dysfunctional eating or weight control patterns, even if relatively minor. The emphasis must be placed on maintenance of health, and an assessment of weight loss or control is advisable. The patient should be followed up within 1 to 2 months. If the patient shows signs of progression to the moderate stage, the implementation of additional specialist consultation is recommended. At this point, adequate caloric intake and limited expenditure should be ensured. Hospitalization is indicated only if the patient shows physiologic decompensation (temperature < 36°C, pulse < 45 bpm, altered mental status, etc.), rapid or excessive weight loss, or inability to break the cycle.
A secondary prevention program may be an excellent tool. When Sundgot-Borgen 76 implemented this in various sports, her group of investigators found a decrease in clinical eating disorders. Conversely, the occurrence was unchanged in those sports in which no program was used.
Because amenorrhea can occur prior to weight loss in up to one-fourth of patients with anorexia nervosa, 77 early detection of amenorrhea may help prevent worsening of this eating disorder. It is best to detect anorexic behaviors as quickly as possible, because body image disturbance may worsen with loss of weight. 5
Amenorrhea, specifically exercise-induced, is completely reversible. 52 The aim of a treatment program is to attempt to re-establish the athlete's regular menstrual cycle, while also preventing further bone loss. This may be accomplished simply by decreasing the amount of training. 20,52,77 Although studies have been conducted to determine specific levels of exercise that would allow return of normal menstrual function, 79,80 confounding factors, such as body composition changes and mental stress, make these levels difficult to determine. 24 Benson et al. 44 make the following suggestions: decrease the training by 10% to 20%, increase the caloric intake, gain 2% to 3% of body weight, add resistance training, supplement with calcium but not fiber, and monitor using bone density scans. Estrogen replacement therapy has also been proposed. One study found that amenorrheic athletes may have poor nutritional status because of poor food selection and decreased energy intake. The authors suggest a sport nutrition supplement to help alleviate these problems. 81
Ovulation often occurs prior to the restoration of normal menses. Therefore, these athletes should ensure that they use birth control if they wish to avoid pregnancy. 24
Although the most effective treatment for osteoporosis is still unknown, many therapies have been attempted, with varied success. Potential treatments include estrogen in the form of hormone replacement therapy or oral contraceptive pills, calcium, and insulin-like growth factors (IGF). 81 Bisphosphonates and calcitonin are mostly used in postmenopausal women, and are not widely researched for use in young athletes. Depot medroxyprogesterone acetate (“Depo-Provera”) may actually exert a negative effect on BMD, and is therefore not advised. 83 Sound nutritional practices are essential, but often difficult to implement. With athletes recovering from anorexia nervosa, bone mineral density may not be fully restored, even after the re-establishment of normal weight. 84–86
Oral contraceptive (OCP) use in athletes, particularly premenopausal, has raised several concerns. Although OCP usage can help diminish detrimental premenstrual symptoms and allow manipulation of the cycle for training purposes, 87 its effects on overall skeletal health are yet to be determined. Monophasic OCPs seem to reduce bone resorption, 88 but athletes may not benefit from this effect, because they may exhibit normal to low bone turnover without intervention. 87 While certain studies show improved bone mass in current or past users of OCPs, 89 particularly in the lumbar spine, 90 others have failed to show an association 91 or have even reported detrimental effects. 87,92 There is also conflicting research concerning the effects of OCP use on stress fractures, 87 even though, in practice, these medications are frequently used. 93 Most deleterious effects, however, are reversible after discontinuation of the OCP. 94
Hormone replacement therapy (HRT) is also controversial. It is thought to be of limited benefit for athletes with persistently low body weight. 75 Hormone replacement therapy is generally considered appropriate therapy after an overall treatment program has been adopted.
Although there are several treatment options to choose from, osteoporosis due to amenorrhea is potentially irreversible. 73,96 Return to normal menstrual function results in a significant increase in vertebral BMD. However, this may only take place during the first two years after resumption of menses. 73 Drinkwater et al. 96 found an initial 6% increase in the first year of menses return. Nevertheless, this increase in BMD soon reached a plateau. 97
When considering treatment, there is evidence for the effectiveness of the multidisciplinary team approach. 73 This team would ideally include the athletic trainer, physician, exercise physiologist, counselor or psychiatrist, and nutritionist. 73 There is controversy regarding the role of the coach as part of the team, because he or she may be perceived as a threat to the athlete (Table 5).
A call to action has been advanced to address prevention and treatment strategies for the female athlete triad. 18,66 This includes:
- Prevention: to educate, promote positive body images, and include screening
- Research: to facilitate and support research in this area
- Health consequences: to develop teams to evaluate and treat triad disorders, and define parameters for healthy percentages of lean body mass, strength, etc.
- Medical care: to increase awareness, to remove at risk athletes from sport or competition, and develop guidelines for assessment and treatment
- Education: to facilitate development of educational materials
- Agency/Administration: to better describe the administration's role in prevention
The female athlete triad can potentially occur in any female athlete. Education of the athlete, her coach, parents (in the cases of younger athletes), and teammates is paramount to successful prevention and intervention. A multidisciplinary team approach is key to effective treatment. All personnel involved with athletes—health care providers, trainers, coaches, and administration—should work together to promote a healthy and realistic body image and help increase awareness of the female athlete triad. Further research is warranted in areas such as appropriate treatment for osteoporosis in young athletes, effects of disordered eating practices in boys and men, changing or abolishing weight categories in sports, and effective ways to promote healthy body image in athletes. The benefits of exercise for girls and women far outweigh the risks. Therefore, participation in sport should continue to be encouraged for all ages.
1. Miller Lite Report on Women in Sports. East Meadow, NY, Women's Sport Foundation, 1985.
2. Lopiano DA. Modern history of women in sports: twenty-five years of Title IX. Clin Sports Med
3. American Academy of Pediatrics. Medical concerns in the female athlete. Pediatrics
4. Putukian M. The Female Athlete Triad. Clin Sports Med 1998; 17:675–696.
5. Powers PS. Eating disorders
: initial assessment and early treatment options for anorexia nervosa and bulimia nervosa. Psych Clin North Am 1996; 19:639–655.
6. Williams S, Speroff L. Dance and menstrual function. In: Ryan AJ, Stevens RE, eds. Dance medicine: a comprehensive guide. Chicago, IL: Pluribus Press, 1987:82–89.
7. Nielsen S. Epidemiology and mortality of eating disorders
. Psych Clin North Am 2001; 24:201–214.
8. Lucas AR, Crowson CS, O'Fallon M, et al. The ups and downs of anorexia nervosa. Int J Eat Disord 1999; 26:397–405.
9. Garner DM, Garfinkel PE. Socio-cultural factors in the development of anorexia nervosa. Psychol Med 1980; 10:647–656.
10. Van Hoeken D, Lucas AR, Hoek HW. Epidemiology. In: Hoek HW, Treasure JL, Katzman MA, eds. Neurobiology in the treatment of eating disorders
. Chichester, England: Wiley; 1998:97–126.
11. Smolak L, Murnen SK, Ruble AE. Female athletes and eating problems: a meta-analysis. Int J Eat Disord 2000; 27:371–380.
12. Sundgot-Borgen J. Eating disorders
among male and female elite athletes. Br J Sports Med 1999; 33:434.
13. Folgenholm M, Hiilloskorpi H. Weight and diet concerns in Finnish female and male athletes. Med Sci Sports Exerc 1999; 31:229–235.
14. Dummer GM, Rosen LW, Heusner WW, Roberts PJ, Councilman J. Pathogenic weight–control behaviors of young competitive swimmers. Phys Sports Med 1987; 5:22–27.
15. Johnson C, Powers PS, Dick R. Athletes and eating disorders
: the National Collegiate Athletic Association Study. Int J Eat Disord 1999; 26:179–188.
16. Beals KA, Manore M. Behavioral, psychological, and physical characteristics of female athletes with subclinical eating disorders
. Int J Sport Nutr Exerc Metab
17. American Psychiatric Association. In: Diagnostic and Statistical Manual of Mental Disorders: DSM-IV, ed. 4. Washington, DC: American Psychiatric Association, 1994.
18. Otis CL, Drinkwater B, Johnson M, et al. American College of Sports Medicine Position Stand: the Female Athlete Triad. Med Sci Sports Exerc 1997; 29 (5):i–ix.
19. Wiggins DL, Wiggins ME. The female athlete. Clin Sports Med 1997; 16:593–612.
20. Lebrun CM. The Female Athlete Triad: Disordered Eating, Amenorrhea, and Osteoporosis. Orthop Int Ed 1994; 2:519–526.
21. Powers PS, Powers HP. Inpatient treatment of anorexia nervosa. Psychosomatics 7:512, 1984.
Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders
in female elite athletes. Med Sci Sports Exerc 1994; 26:414–419.
23. Dueck CA, Manore MM, Matt KS. Role of energy balance in athletic menstrual dysfunction. Int J Sport Nutr 1996; 6:90–116.
24. Fagan KM. Pharmacologic management of athletic amenorrhea. Clin Sports Med 1998; 17:327–341.
25. Palla B, Litt IF. Medical complications of eating disorders
in adolescents. Pediatrics 1988; 81:613–623.
26. Ratnasuriya RH, Eisler I, Szmuckler GI, et al. Anorexia nervosa: outcome and prognostic factors after 20 years. Br J Psychiatry 1991; I58:495–502.
27. Garfinkel PE. Eating attitudes as part of a screening tool. Paper presented at: Anorexia Nervosa and Bulimia Nervosa: Can screening reduce the risk for young Americans?; February 22, 1995; Washington, DC.
28. Kohrt WM. Body composition. In: Drinkwater B, ed. Women In Sport: Volume VIII of the Encyclopedia of Sports Medicine. Oxford: Blackwell Science, 2000:353–363.
29. Shangold M, Rebar RW, Wentz AC, Schiff I. Evaluation and management of menstrual dysfunction in athletes. JAMA 1990; 263:1665–1669.
30. Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc 1990; 22:275–280.
31. Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc 1985; 17:56–72.
32. Marshall LA. Clinical evaluation of amenorrhea in active and athletic women. Clin Sports Med 1994; 13:371–387.
33. Emans SJ, Goldstein DP. Pediatric and Adolescent Gynecology.
ed. Boston, MA: Little, Brown, and Co., 1990.
34. Rose MZ, Lee TC, Maffulli N, et al. Special gynecological problems of the young female athlete. In: Maffulli N et al., eds. Sports Medicine for Specific Ages and Abilities. London: Churchill Livingstone, 2001:139–147.
35. Furia, J. The female athlete triad. Medscape Orthop Sports Med
36. Constantini NW, Warren MP. Menstrual dysfunction in swimmers: a distinct entity. J Clin Endocrinol Metab 1995; 80:2740–2744.
37. Warren MP, Perlroth NE. The effects of intense exercise on the female reproductive system. J Endocrinol 2000: 170:3–11.
38. Marcus R, Cann C, Madvig P, et al. Menstrual function and bone mass in elite women distance runners: endocrine and metabolic features. Ann Intern Med 1985; 102:158–163.
39. Loucks AB, Heath EM. Induction of low-T3
syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol 1994; 266:R817–R823.
40. Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise alters LH pulsatility in exercising women. J Appl Physiol 1998; 84:37–46.
41. Loucks AB, Callister R. Induction and prevention of low-T3
syndrome in exercising women. Am J Physiol 1993; 264:R924–R930.
42. Loucks AB, Heath EM. Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J Clin Endocrinol Metab 1994; 78:910–915.
43. Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metabol 1996; 81:4301–4309.
44. Benson JE. Nutritional aspects of amenorrhea in the female athlete triad. Int J Sport Nutr 1996; 6:134–145.
45. Lebrun, C.M. Female Athlete Triad. In: Maffulli N et al., eds. Sports Medicine for Specific Ages and Abilities. London: Churchill Livingstone, 2001:177–185.
46. Snow RC, Barbieri RL, Frisch RE. Estrogen 2-hydroxylase oxidation and menstrual function among elite oarswomen. J Clin Endocrinol Metab 1989; 69:369–376.
47. Kalra SP. Appetite and body weight regulation: is it all in the brain? Neuron 1997; 19:227–230.
48. Drinkwater, BL, Nilson K, Chestnut III, CH et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 1984; 311:277–278.
49. Lamon-Fava S, Fisher EC, Nelson ME. Effects of exercise and menstrual cycle on plasma lipids, low density lipoprotein particle size and apolipoproteins. J Clin Endocrinol Metab 1989; 68:17–21.
50. Schwartz B, Cumming DC, Riordan E, et al. Exercise-associated amenorrhea: a distinct entity? Am J Obstet Gynecol 1981; 141:662–667.
51. Van de Loo, DA, Johnson MD. The young female athlete. Clin Sports Med 1995; 14:687–707.
52. DeCree, C. Sex steroid metabolism and menstrual irregularities in the exercising female: a review. Sports Med 1998; 25:369–406.
53. To WWK, Wong MWN, Chan KM. The effect of dance training on menstrual function in collegiate dancing students. Aus NZ J Obstet Gyn 1995; 35:304–309.
54. Wong MWN, To WWK. Dance medicine. In: Maffulli, N et al., eds. Sports Medicine for Specific Ages and Abilities. London: Churchill Livingstone, 2001:161–168.
55. West, RV. The female athlete: the triad of disordered eating, amenorrhea, and osteoporosis. Sports Med 1998; 26:63–71.
56. Bass S, Pearce G, Bradney M, et al. Exercise and puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res 1998; 13:500–507.
57. Kemper HC, Twisk JW, van Mechelen W, et al. A fifteen-year longitudinal study in young adults on the relation of physical activity and fitness with the development of the bone mass: the Amsterdam Growth and Health Longitudinal Study. Bone 2000; 27:847–848.
58. Daly RM, Rich PA, Klein R, et al. Effects of high-impact exercise on ultrasonic and biochemical indices of skeletal status: a prospective study in young male gymnasts. J Bone Miner Res 1999; 14:1222–1230.
59. Skolnick, AA. `Female Athlete Triad' risk for women. JAMA 1993; 270:921–923.
60. Manore, MM. Nutritional needs of the female athlete. Clin Sports Med 1999; 18:549–563.
61. Treasure J, Serpell L. Osteoporosis in young people. Psych Clin North Am 2001; 24:359–370.
62. Taafe DR, Robinson TL, Snow CM, et al. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res 1997; 12:255–260.
63. Gibson JH, Harries M, Mitchell A, et al. Determinants of bone density and prevalence of osteopenia among female runners in their second to seventh decades of age. Bone 2000; 26:591–598.
64. Lehtonen-Veromaa M, Mottonen T, Svedstrom E, et al. Physical activity and bone mineral acquisition in peripubertal girls. Scand J Med Sci Sports 2000; 10 (4):236–243.
65. Grinspoon S, Miller K, Coyle C, et al. Severity of osteopenia in estrogen-deficient women with anorexia nervosa and hypothalamic amenorrhea. J Clin Endocrinol Metab 1999; 84:2049–2055.
66. Nattiv, A, Agostini R, Drinkwater, B, et al. The Female Athlete Triad: the interrelatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med 1994; 13:405–18.
67. Nichols DL, Bonnick SL, Sanborn CF. Bone health and osteoporosis. Clin Sports Med 2000; 19:233–249.
68. Glover, DW, Maron BJ, Matheson GO. The Preparticipation Physical Examination: steps toward consensus and uniformity. Phys Sports Med 1999; 27:29–34.
69. Drinkwater, BL. Exercise and bones: lessons learned from female athletes. Am J Sports Med 1996; 24:33–35.
70. Myburgh KH, Bachrach LK, Lewis B, et al. Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sports Exerc 1993; 25:1197–1202.
71. Rencken ML, Chestnut III, CH Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes. JAMA 1996; 276:238–240.
72. Gilchrist NL. Bone density estimation. NZ Med J 1988; 101:260.
73. Sanborn, C. et al. Disordered eating and the female athlete triad. Clin Sports Med 2000; 19:199–213.
74. Smith, DM. Preparticipation Physical Examination: development of uniform guidelines. Sports Med 1994; 18:293–300.
75. Seidenfeld ME. Impact of anorexia, bulimia and obesity on the gynecologic health of adolescents. Am Fam Physician 2001: 64:445–450.
76. Sundgot-Borgen J. Eating disorders
among male and female elite athletes. Br J Sports Med 1999; 33:434.
77. Katz J, Weiner J. The aberrant reproductive endocrinology of anorexia nervosa. In: Weiner H, Stunkard AJ. Brain, Behaviour, and Bodily Disease. New York, NY: Raven Press, 1981:165.
Williams MH. Nutrition for Health, Fitness & Sport (5th
ed.). Dubuque: McGraw-Hill, 1999:336.
79. Bullen BA, Skrinar GS, Beitins IZ, et al. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J Appl Physiol 1984; 56:1453–1463.
80. Bullen BA, Skrinar GS, Beitins IZ, et al. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl Med 1985; 312:1349–1353.
81. Kopp-Woodroffe SA, Manore MM, Dueck CA, et al. Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. Int J Sport Nutr 1999; 9:70–88.
Grinspoon S, Herzog D, Klibanski A. Mechanisms and treatment options for bone loss in anorexia nervosa. Psychopharmacol Bull 1997; 33:399–404.
83. Cromer BA. Effects of hormonal contraceptives on bone mineral density. Drug Saf 1999; 20:213–222.
84. Davies K, Pearson P, Huseman C, et al. Reduced bone mineral in patients with eating disorders
. Bone 1990; 11:143–147.
85. Hartman D, Crisp A, Rooney B, et al. Bone density of women who have recovered from anorexia nervosa. Int J Eat Disord 2000; 28:107–112.
86. Ward A, Brown N, Treasure J. Persistent osteopenia after recovery from anorexia nervosa. Int J Eat Disord 1997; 22:71–75.
87. Bennell K, White S, Crossley K. The oral contraceptive pill: a revolution for sportswomen? Br J Sports Med 1999; 33:231–238.
88. Paoletti AM, Orru M, Floris S, et al. Evidence that treatment with monophasic oral contraceptive formulations containing ethinylestradiol plus Gestodene reduces bone resorption in young women. Contraception 2000; 61:259–263.
89. Kuohung W, Borgotta L, Stubblefield P. Low-dose oral contraceptives and bone mineral density: an evidence-based analysis. Contraception 2000; 61:77–82.
90. Pasco JA, Kotowicz MA, Henry MJ, et al. Oral contraceptives and bone mineral density: a population-based study. Am J Obstet Gyn 2000; 182:265–269.
91. Lloyd T, Taylor DS, Lin HM. Oral contraceptive use by teenage women does not affect peak bone mass: a longitudinal study. Fertil Steril 2000; 74:734–738.
92. Weaver CM, Teegarden D, Lyle RM, et al. Impact of exercise on bone health and contraindication of oral contraceptive use in young women. Med Sci Sports Exerc 2001; 33:873–880.
93. Haberland CA, Seddick D, Marcus R, et al. A physician survey of therapy for exercise-associated amenorrhea: a brief report. Clin J Sport Med 1995; 5:1–5.
94. Petitti DB, Piaggio G, Mehta S, et al. Steroid hormone contraception and bone mineral density: a cross-sectional study in an international population. The WHO study of hormonal contraception and bone health. Obstet Gynecol 2000; 95:736–744.
Micklesfield LK, Reyneke L, Fataar A, et al. Long-term restoration of deficits in bone mineral density is inadequate in premenopausal women with prior menstrual irregularity. Clin J Sport Med 1998; 8:155–163.
96. Drinkwater BL, et al. Bone mineral density after resumption of menses in amenorrheic athletes. JAMA 1986; 25:380–382.
97. Keen AD, Drinkwater BL. Irreversible bone loss in former amenorrheic athletes. Osteoporos Int 1997; 7:311–315.
98. Lebrun CM. Effects of the menstrual cycle and oral contraceptive on sports performance. In: Drinkwater B, ed. Women in Sport: Volume VIII of the Encyclopedia of Sports Medicine. Oxford: Blackwell Science Ltd., 2000:37–61.
Nicola Maffulli, M.D., Guest Editor