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Author: Laura M Gottschlich, DO, Assistant Professor of Family and Community Medicine, Medical College of Wisconsin; Consulting Staff, St. Joseph Family Medicine Residency Program

Laura M Gottschlich is a member of the following medical societies: American Academy of Family Physicians, American College of Sports Medicine, American Medical Association, American Medical Society for Sports Medicine, and American Osteopathic Association

Coauthor(s): Craig C Young, MD, Professor, Departments of Orthopedic Surgery and Community and Family Medicine, Medical Director of Sports Medicine, Sports Medicine Fellowship Director, Medical College of Wisconsin; Boone Barrow, MD, Consulting Staff, Department of Family Medicine, Scott and White Clinic

Editors: Leslie Milne, MD, Assistant Clinical Instructor, Department of Emergency Medicine, Harvard University School of Medicine; Francisco Talavera, PharmD, PhD, Senior Pharmacy Editor, eMedicine; Russell D White, MD, Professor of Medicine, Department of Community and Family Medicine, University of Missouri-Kansas City School of Medicine, Truman Medical Center Lakewood; Jon B Whitehurst, MD, Clinical Instructor of Surgery, University of Illinois College of Medicine; Partner and Executive Board Member, Rockford Orthopedic Associates; Orthopedic Chairman, Rockford Memorial Hospital; Craig C Young, MD, Professor, Departments of Orthopedic Surgery and Community and Family Medicine, Medical Director of Sports Medicine, Sports Medicine Fellowship Director, Medical College of Wisconsin

Author and Editor Disclosure

Synonyms and related keywords: FAT, sports amenorrhea, sports-related amenorrhea, amenorrhea, female athletes, disordered eating, anorexia, bulimiaosteoporosis, energy availability, low energy availability in the female athlete, menstrual dysfunction, menstruation disorders, bone health, functional hypothalamic amenorrhea

Background

History

Athletic activity by women and girls has dramatically increased in the last few decades. Much of this increase can be attributed to Title IX legislation, which mandated that equal money and opportunities be made available to females at publicly funded institutions, particularly public schools, ranging from elementary schools to the universities.1, 2 For the most part, this legislation has led to many health benefits, as generations of young women were given to chance to compete in a variety of sports.

Women's athletics has grown to the point that women's basketball has become a professional sport in the United States. The number of girls participating in youth baseball or tee-ball has risen from almost a rarity to rates that nearly match those of their male counterparts. Participation in high school sports rose from 3.7% in 1972 to 40% in 2002, and participation in college spots rose from 2% in 1972 to 43% in 2002.

With the increase in female participation in sports, the incidence of a triad of disorders particular to women has also increased. This triad, the female athlete triad, although more common in the athletic population, can also occur in the nonathletic population. However, despite first being described by the American College of Sports Medicine (ACSM) Meeting in 1993,3, 4 observations about bone mineral densities (BMDs), stress fractures, eating disorders, and female athletics had been described for decades before the syndrome was named.

Often difficult to recognize, the female athlete triad can have a significant impact on morbidity and even mortality in a relatively young segment of the population. Indeed, the full impact of this syndrome may not be realized until these women reach menopause, when bone loss is accelerated.

For excellent patient education resources, visit eMedicine's Osteoporosis and Bone Health Center, Exercise, Nutrition, and Weight Management Center, and Women's Health Center. Also, see eMedicine's patient education articles Anorexia Nervosa, Bulimia, and Amenorrhea.

Related eMedicine topics:
Amenorrhea
Eating Disorder: Anorexia
Eating Disorder: Bulimia
Stress Fractures

Related Medscape topics:
Resource Center Adolescent Medicine
Resource Center Exercise and Sports Medicine
Resource Center Nutrition
CME Bone Density Evaluation in Teens Prevents Future Osteoporosis
The Female Athlete Triad: Do Female Athletes Need to Take Special Care to Avoid Low Energy Availability

Components of the Female Athlete Triad

The components of the triad put forth by the 1997 ACSM positional stand consisted of disordered eating, amenorrhea, and osteoporosis.5 Not all patients have all 3 components of the triad, and new data are beginning to emerge that even having only 1 or 2 elements of the triad greatly increases these females' long-term morbidity. In addition, a study by Burrows et al has suggested that the current triad components do not identify all at-risk women; rather, the authors suggest that criteria such as exercise-related menstrual alterations, disordered eating, and osteopenia may be more appropriate.6

Research on the female athlete triad for the past decade or so has culminated in an updated definition published by ACSM. The 2007 ACSM positional stand looks at each disorder as it exists on a continuous spectrum instead of a severe pathologic endpoint.7 Disordered eating has been replaced by a spectrum from “optimal energy availability” to “low energy availability with or without an eating disorder.” Amenorrhea has been replaced by a spectrum from “eumenorrhea” to “functional hypothalamic amenorrhea.” Finally, osteoporosis has been replaced by a spectrum from “optimal bone health” to “osteoporosis.”

The 2007 ACSM positional stand also emphasizes that energy availability is the cornerstone that the rest of the triad stems from.7 Without correction of this key component, full recovery from the female athlete triad is not possible.

Energy Availability7, 8

This component of the female athlete triad is defined as “dietary energy intake minus exercise energy expenditure” and is aimed toward capturing the athletes who may have eating and weight concerns, but who do not have “significant psychopathology” and who do not meet the criteria for disordered eating.
 
The term disordered eating was coined to include pathologic eating behaviors that do not meet the strict Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) requirements for anorexia or bulimia and therefore includes anorexia nervosa and bulimia nervosa but is not limited to these diagnoses. Indeed, disordered eating includes a spectrum of behaviors from as simple as the athlete not taking in enough food to offset the energy that is expended to preoccupation with eating and a fear of becoming fat by instituting measures such as food restrictions and/or the use of diet pills, laxatives, and/or diuretics.

Menstrual Dysfunction7

This component is now used to describe the spectrum from eumenorrhea to amenorrhea and enables clinicians to capture a large portion of athletes who may have low estrogen levels but who may still experience menstruation. This condition includes luteal suppression, anovulation, oligomenorrhea, and primary and secondary amenorrhea. Luteal suppression is marked by a shortened luteal phase and a prolonged follicular phase in which there is a decrease in estradiol levels. The cycle length usually does not change, the athlete will continue to ovulate—although it may be later in the cycle—and the athlete usually has regular menstruation.

Anovulation is marked by low levels of estradiol and progesterone that deter follicular development, as well as an absence of ovulation. Although the circulating hormones are decreased, female athletes will often menstruate, some experiencing shortened or prolonged cycles due to their uterine lining being stimulated by the low levels of estradiol. Oligomenorrhea is defined as “greater than 35 days between cycles.”

Amenorrhea usually refers to secondary amenorrhea, although delayed menarche (primary amenorrhea) can occur in young athletes. By consensus, secondary amenorrhea is the “absence of menstrual cycles lasting more than 3 months after menarche has occurred.” Physicians are cautioned that a full workup be completed to rule out any other causes of menstrual dysfunction before attribution to low estradiol levels stemming from low energy availability.9

Bone Health7, 10

The final component of the female athlete triad exists on a continuum from optimal bone health to osteoporosis and focuses on bone strength, which consists of BMD and/or content and bone quality. Bone quality refers to bone turnover rates—resorption versus formation, microarchitecture or trabeculae, time for maturation of the new bone matrix, bone geometry and size, etc. The inability to measure bone quality at this time leaves one half of the equation for bone health empty and offers an explanation for why some athletes with the same poor bone density as their colleagues, may suffer more fractures. Therefore, dual energy x-ray absorptiometry (DXA) scans are used as a quantitative measure of bone health.

When reporting BMD, T-scores are used for the diagnosis of osteopenia and osteoporosis. However, the T-score measures the standard deviations (SDs) below the mean to predict fracture risks for postmenopausal woman. Concern over mislabeling of our premenopausal athletes, adolescents and children, led to a positional stand to be issued by the International Society for Clinical Densitometry (ISCD).10 The recommendation is to determine BMD by comparing chronologic age and sex using a Z-score distribution. The ISCD further recommends that the term osteopenia not be used in describing bone density and that the term osteoporosis be reserved for “low BMDs” with secondary clinical risk factors such as “chronic malnutrition, eating disorders, hypogonadism, glucocorticoid exposure, and previous fractures.”10

Athletes that have a Z-score that is 2 SDs below the mean are to be termed “low bone density below the expected range for age” for premenopausal women and “low bone density for chronologic age” for children. The ACSM, in their 2007 positional stand, further defined “low BMD” as “a history of nutritional deficiencies, hypoestrogenism, stress fractures, and/or other secondary clinical risk factors for fracture together with a BMD Z-score between –1.0 and –2.0,” and osteoporosis as “secondary clinical risk factors for fracture with a Z-score ≤ –2.0.”7
 
Because most athletes already have a higher BMD than nonathletes, the ACSM also cautions physicians to perform further workup for any athlete with a BMD Z-score < –1.0, even in the absence of fracture.7

Related eMedicine topics:
Low Energy Availability in the Female Athlete
Menstruation Disorders
Utility of Bone Markers in Osteoporosis

Related Medscape topics:
Resource Center Eating Disorders
Specialty Site Women's Health

Frequency

United States

Although all female athletes are at risk for the female athlete triad or any of its components, sports that have an aesthetic component (eg, ballet, figure skating, gymnastics) or sports tied to a weight class (eg, tae kwon do, judo, wrestling) have a higher prevalence of affected female athletes.7, 11, 12, 13, 14 Obtaining exact epidemiologic data is difficult because of the lack of reporting and/or gathering of data from athletes. Similar to individuals with anorexia or bulimia, many athletes with the triad try to hide their symptoms or behavior from friends, family, trainers, or coaches. This is the primary reason why diagnosis is so difficult. In fact, the vast majority of cases are diagnosed only after advanced symptoms become apparent. Milder cases may be extremely difficult to diagnose if the physician does not already have a high degree of suspicion.7, 15, 16, 17, 18

The prevalence of how many athletes suffer from low energy availability is difficult to assess. Multiple factors (eg, gathering accurate caloric intake data from athletes, measuring energy expenditure, which sports to include, which eating attitude survey to use, definitions of “eating disorder”) compound the issue. However, it is known that an athlete is at increased risk to suffer from the spectrum of reduced to low energy availability with or without an eating disorder if the athlete has a comorbid psychologic disorder, such as anxiety, depression, and/or obsessive compulsive disorder (OCD). In some studies, disordered eating in the female athletic population has been estimated to be as high as 62%, with the incidence of anorexia nervosa and bulimia (as defined in the DSM-IV) estimated at 4-39%.

The prevalence of menstrual dysfunction is also difficult to assess. Many studies have reported a range from as low as 6% to as high as 79%, depending on the sport studied, the patient's age, the definition and assessment of menstrual dysfunction, the use of oral contraceptives, the training volume, and the presence of subclinical menstrual disorders, such as luteal suppression and anovulation. Studies continue to be performed, and hopefully, more data will be available soon.

The prevalence of bone health, reported in the form of BMD, is likewise difficult to assess due to the cost prohibitiveness of DXA scans. Osteopenia has been reported as high as 50% and as low as 22% for athletes relative to 12% in the nonathlete population. Osteoporosis has been also reported from 0-13% for athletes and 2.3% for nonathletes. With the ISCD recommendations of using Z-scores instead of T-scores, more research will need to be done to obtain accurate data for athletes.

In the near future, epidemiologic data regarding the female athlete triad may become available. Many preparticipation physical questionnaires now include questions about whether the athlete is satisfied with her current weight and about how much weight she would like to gain or lose. These simple inquiries may reveal the first warning signs of the female athlete triad.

Functional Anatomy

Bones of the lower extremities, pelvis, and vertebrae are the most common to be affected by poor bone health when an athlete is suffering from the female athlete triad, manifesting as stress and frank fractures of these areas. Peak bone mass is obtained between the ages of 20 and 30 years, with peak bone mineral content being accrued between ages 9 and 20 years.

Menstruating athletes gain approximately 2-4% of bone mass per year, whereas amenorrheic athletes tend to loose 2% of BMD per year. Therefore, it is easy to see why athletes who are involved in high-impact sports can still be more susceptible to fractures than their nonathletic and menstruating athletic counterparts. Often these fractures are due to the increased stress sustained by these bones in the course of physical activity. In this respect, athletes with the female athlete triad are not unlike their healthy counterparts. However, those who have the triad or portions of it are more susceptible to multiple fractures, and they are also more likely to sustain fractures in larger, less commonly affected bones (eg, femoral neck, pelvis, vertebra).

Related eMedicine topics:
Femoral Neck Stress Fracture
Lumbosacral Spine Acute Bony Injuries
Pelvic Fractures

Related Medscape topics:
Resource Center Exercise and Sports Medicine
Resource Center Osteoporosis
Resource Center Trauma



History

When an athlete is identified as being at risk for the female athlete triad, a detailed screening history should be obtained. The purpose of the screening process is to gather information about the patient's medical history and dietary and exercise behaviors and to evaluate the athlete for existing psychopathology and medical complications.

The team physician should not undertake every aspect of the evaluation and care of a woman with female athlete triad; rather, a multidisciplinary approach should be used. If available and deemed necessary, consultation with a psychiatrist or clinical psychologist with experience in disordered eating, an orthopedic surgeon, a gynecologist, a cardiologist, a sports nutritionist, and the athlete's athletic trainer should be added to the treatment team to augment the physicians personal knowledge of the athlete and team.

Past medical history

Particular attention should be given to any other endocrine disorders, such as thyroid abnormalities, panhypopituitarism, and diabetes. A careful and thorough history of past stress fractures and complete fractures should be elicited, and the history should be verified with trainers, coaches, or parents, if possible.

Menstrual history

Menstrual history should include the age of menarche, length of menses, and menstrual cycle, as well as any missed menses and the menstrual pattern during the season or that time period when the athlete is exercising the most. Athletes in some sports in which strength is important may be using anabolic steroids, which are a potential cause of secondary amenorrhea. However, because the most common cause of secondary amenorrhea in young females is pregnancy, this possibility should be discussed and ruled out.

Psychosocial history

At the first visit, routine questions should be asked, such as those pertaining to tobacco or alcohol use. As trust is built up over the next few visits, further details about the patient's background should be elicited, such as illegal drug use, sexual or physical abuse, depression, anxiety, previous eating disorders, suicidal behavior, recent trauma or illness, change in coaches, failure at school or work, or other significant personal events.

The lack of a family or social support system is a risk factor for the female athlete triad. Women just entering college are often in a new environment that is physically distant from their friends and family. This move can be made more traumatic if the pressure to perform as a collegiate athlete is added to the athlete's psyche. Sometimes, these women fall back on athletics—one of the few things that may have remained constant since high school—to gain acceptance from coaches and fellow athletes.

Exercise history

The number of hours per day that the athlete spends in practice and exercise should be determined. The examiner should make a point of asking how much time is spent in formal practice with the team or coach and how much additional time apart from scheduled workouts is spent, for example, conditioning, running, and lifting. The athlete should also be asked if this workout pattern changes during the off-season or if it continues year round.

Nutritional assessment

Just because the athlete is consuming what would otherwise be considered a normal number of calories per day does not mean that she is consuming enough calories for her lifestyle. Women who exercise for hours per day are likely to need more than the 1600-2000 kcal that their body weight would indicate.

The Eating Disorder Inventory (EDI), for example, is a questionnaire designed to help identify those with disordered eating. Although the EDI is not a precise instrument to aid in identifying eating disorders, it can be used to identify people at risk for anorexia or bulimia.

Some athletes with the triad adopt restrictive diets, and they may sometimes use personal convictions or religious beliefs to justify their behavior. Many times, the athlete may develop a recognizable pattern of disordered eating in which they progressively establish and exceed dietary boundaries. For example, a diet of no red meat may progress to vegetarianism, then to veganism over the course of months.

The athlete's convictions may be subconscious excuses reflecting what is socially acceptable to her peers and authority figures. Of course, not every athlete with a diet that restricts certain foods has the female athlete triad, and not every athlete is consciously participating in disordered eating. For many athletes, the low energy availability is due to lack of education about caloric needs for their exercise and/or training. This is yet another reason why the diagnosis is difficult to establish.

Current medications

The patient's history should include the use of any prescription medications, including contraceptive medications, over-the-counter (OTC) medications, as well as herbal medicines and dietary supplements. Many people do not consider OTC medicines to be "real" medicines, and athletes with the triad commonly use or abuse dietary supplements or ergogenic aids. Athletes may take the common stimulant ephedrine, to lose weight or to burn fat; however, this stimulant is known to cause mild tachycardia and has been at least temporally associated with several deaths in the athletic population. This tachycardia could potentially mask the bradycardia found in athletes with advanced eating disorders. Attention should also be directed toward any present or past use of hormones because they can also cause menstrual irregularities.

Physical

In general, a complete screening physical examination should be preformed. As with the history taking, postponing some parts of the physical examination until a relationship has developed between the athlete and physician may be appropriate. For example, a gynecologic and breast examination may be better suited for a second or third visit. The exception to this rule is if the amenorrhea is primary, that is, if the athlete has never had normal menses. In this case, pelvic examination to verify the presence of a uterus should be performed at the first visit. Pelvic ultrasonography can aid in this determination. The diagnosis is largely clinical, and no test enables definitive diagnosis of the female athlete triad.

Many times, the physician diagnoses a stress fracture first; then the menstrual dysfunction; and, lastly, the low energy availability, with or without an eating disorder. However, this sequence is the reverse of the order in which the female athlete triad develops.

Of note, female athletes who come to a summertime preparticipation physical examination wearing many baggy clothes or sweatpants and sweatshirts should raise concern. Athletes with the triad may try to hide their body weight loss. In addition, some athletes may present for the examination and then refuse to let the physician or anyone else examine them. This is often the case in 14- to 16-year-old athletes who participate in high school sports.

  • Anthropometric data and vital signs should be obtained without comment about weight or weight-to-height ratios.
    • Body mass index (BMI) charts are calibrated for the general population and may not be suitable for the athletic subpopulation.
    • If possible, the patient's percentage of body fat composition can be determined.
    • Pediatric growth charts are often helpful in teenagers or college students.
  • The remainder of the physical examination is directed toward other causes of amenorrhea or osteoporosis and secondary signs of the triad.
    • The thyroid should be palpated for possible goiter.
    • The parotid glands should be palpated for evidence of hypertrophy. This is sometimes found after chronic purging.
    • Bulimia can cause bloodshot eyes and petechiae of the sclera or cheeks. Dental examination can show dental caries or pitting from the regurgitation of stomach acid through the oropharynx. If a finger is used to induce vomiting, the knuckles may be scarred from the patient biting down on them during regurgitation. The Russell sign is typical callous formation on the distal extensor surface of the long finger that is used to induce vomiting.
    • Anorexia may cause cachexia, bradycardia, and hypotension later in the course of the disease. Although many well-conditioned athletes may have a resting heart rate below that of the general population, an electrocardiogram (ECG) should be obtained if the athlete's resting heart rate less than 50 beats per minute (bpm).

      Sinus bradycardia is an early cardiac sign in eating disorders, but conduction abnormalities (eg, atrioventricular conduction blocks, ventricular tachycardia) may become evident in more advanced cases. A baseline ECG may also be obtained for future comparison.

    • Dermatologic examination sometimes reveals lanugo or the dry or yellow skin that is sometimes found in those with anorexia.
  • Athletes with the female athlete triad usually report signs or symptoms related to osteoporosis (eg, fracture, stress fracture) before they report menstrual abnormalities.

Causes

The theory behind the female athlete triad is that this syndrome is caused by an energy drain/caloric deficit (ie, the athlete's energy expenditure exceeds her dietary energy intake).7, 8 This low energy availability, whether subconscious or conscious, causes disruption of the hypothalamic-pituitary-ovarian axis, which results in decreased gonadotropin-releasing hormone (GnRH) pulsatility and low luteinizing hormone (LH) and follicle-stimulating hormone (FSH) levels.19 This, in turn, leads to decreased estrogen production, causing menstrual dysfunction, and the decreased estrogen levels in turn affect calcium resorption and bone accretion, causing decreased bone health.
 
Some studies have shown that 30 kcal/kg of lean body mass is a crucial threshold for maintaining menstrual function7; they have also demonstrated that increasing exercise drastically, but covering the energy expenditure with increased caloric intake did not result in disruption of LH pulsatility. Conversely, decreasing an athlete’s caloric intake to less than 30 kcal/kg within 5 days resulted in decreased LH pulsatility. All of which support the energy drain theory.

The hormone leptin has also garnered increased interest. Secreted by adipocytes, leptin appears to influence the metabolic rate, and levels are proportional to a person's BMI. This hormone may be a significant mediator of reproductive function, and many studies have demonstrated that low levels of leptin correlate positively with amenorrhea and infertility. Furthermore, leptin receptors have been found on hypothalamic neurons involved in the control of GnRH pulsatility and in bone, which may also affect osteoblastic function.

As discussed previously, athletes in some sports that are linked to an aesthetic component or a weight class are more likely to develop the triad. These athletes often attempt to reach unrealistic weight and body fat goals dictated by their sport, to the detriment of their health.11, 12, 20, 21 Emotional stressors can also often be identified as inciting factors in athletes with the triad. Death of a coach or family member, growth spurts, illness that prevents training, and other events that an athlete cannot control often lead to disordered eating and excessive training—a portion of their life that they can control.

For many, moving to a university setting initiates the triad cascade. Some young women may move long distances away from their family and friends, and they have the added increase in responsibility of a sports scholarship and academic workload. Collegiate athletes have the additional pressure of performing up to the more difficult standards of collegiate competition, with a new coach and trainer, as well as alongside athletes who may have had the benefit of 2-3 years of additional experience. Not surprisingly, the prevalence of the triad suddenly increases in college freshman.



Other Problems to Be Considered

Androgen excess (endogenous or exogenous)
Depression
Drug interactions
Generalized anxiety disorder
Hypogonadotropic hypoestrogenism
Hypothalamic disorders
Hypothyroidism or hyperthyroidism
Luteal-phase inadequacy
Nutritional deficiencies
Ovarian defect (eg, Turner syndrome, gonadal dysgenesis)
Pituitary disorders
Polycystic ovary disease
Premature ovarian failure



Lab Studies

Obtain the following laboratory studies in a female suspected of having the female athlete triad:

  • Urine or plasma pregnancy test to rule out pregnancy
  • Urinalysis with specific gravity to establish volume status
  • Complete blood cell (CBC) count to rule out anemia
  • Erythrocyte sedimentation rate (ESR) to check for inflammation or infection: A C-reactive protein (CRP) test may be ordered for verification, although this is usually not necessary because such a clinical problem is likely to have been present for months or years.
  • Complete metabolic panel to evaluate liver function, electrolyte levels, and kidney function
  • Thyroid panel to rule out hyperthyroidism and hypothyroidism: A thyrotropin (ie, TSH) test is standard to rule out these diseases, and a free thyroxine (T4) test can be performed to confirm the results. The standard thyroid panel used in most laboratories is now outdated, and the thyrotropin and T4 tests are the standard.
  • FSH and LH tests to evaluate pituitary function and possible premature ovarian failure
  • Prolactin test to evaluate pituitary function
  • Testosterone and dehydroepiandrosterone sulfate (DHEAS) tests to evaluate androgen excess and possible adrenal or ovarian tumors: Some forms of these tumors may be nonvirilizing and therefore difficult to diagnose without a laboratory test.
  • Direct estradiol measurements

Related Medscape topic:
Specialty Site Pathology & Lab Medicine

Imaging Studies

  • If the athlete presents with bone pain, as with a stress fracture, appropriate plain radiographs should be obtained.
  • Baseline dual-emission x-ray absorptiometric (DEXA) scans can be obtained in all athletes with the triad to identify undiagnosed osteoporosis or subclinical stress fractures, as well as to provide a reference for future monitoring. The ACSM and the American Academy of Pediatrics recommend that an athlete's BMD be evaluated if she has been amenorrheic for longer than 1 year, has a BMI less than 18, or a history of a stress fracture. The recommendation is a posteroanterior view of the spine and/or hip, if the athlete is >20 years old and a posteroanterior view of the spine and whole body, if the athlete is <20 years old, with the diagnosis made by a Z-score.
  • If the results of laboratory studies indicate abnormal pituitary function, thin-section magnetic resonance imaging of the head should be performed through the sella turcica.
  • In athletes with primary amenorrhea who lack a uterus (as determined at physical examination), pelvic ultrasonography can be used to verify the finding and to evaluate the presence and morphology of the ovaries. Hand images should also be obtained in these patients to establish their bone age.
  • When a 3-phase bone scan depicts a stress fracture, further imaging evaluation is usually not indicated. The presence of multiple stress fractures in an at-risk athlete is a warning sign for the female athlete triad.

Other Tests

  • The diagnosis is largely clinical, and no test enables definitive diagnosis of the female athlete triad.
  • As mentioned earlier, a resting ECG should be obtained in any athlete with a resting heart rate of less than 50 bpm. Many physicians believe that a baseline ECG should be performed in all athletes at risk for the triad. As with so many aspects of this disease, exact epidemiologic data are not yet available. Drawing on experience with anorexia and bulimia, for which a baseline ECG is usually recommended, proceeding with this noninvasive test may be a safe choice.
  • A progesterone challenge test can be used to determine if the uterine endometrium has been primed with estrogen and thus be ready to be shed, as in normal menstruation. A 10-day course of 5 or 10 mg of oral progesterone (Provera; Pfizer Inc, New York, NY) can be used to induce menstrual bleeding. Lack of menses indicates that the uterine endometrium has not been adequately exposed to estrogen since the last menses. A positive test result is confirmed when menstrual flow occurs; this finding provides indirect confirmation of the presence of adequate amounts of estrogen to sustain endometrial growth.

Procedures

  • During the workup for amenorrhea, an evaluation of the endometrium may be necessary.
  • The team physician can perform an endometrial biopsy, or a consultation with the primary care physician or gynecologist should be requested.
    • Endometrial sampling is performed by using a thin tube, usually a disposable pipette, inserted through the cervical os into the uterine cavity.
    • Suction is then applied to the tube, and endometrial tissue is drawn into it.
    • This sample can then be histologically examined to help determine the stage of growth of the endometrial tissue and, thus, the effects or presence of estrogen and progesterone.



Acute Phase

Rehabilitation Program

Physical Therapy

If a fracture or stress fracture is present, physical therapy may be appropriate, depending on the type of injury.

Medical Issues/Complications

In the acute phase, treatment is aimed at addressing the secondary complications of the female athlete triad. This treatment may involve immobilizing any stress fractures or prescribing a period of rest from athletic activities to allow the body to heal as much as possible.

Many initial laboratory and radiologic studies can be ordered at this time to aid in clinical decision making. For some tests, the patient may need to be referred to regional facilities or larger laboratories, and this time should be used to begin forming a relationship with the athlete. A restrained, understated manner often works to the advantage of the physician. For many people with disordered eating, their behavior represents a way of controlling at least one aspect of their lives. In the case of collegiate or professional athletes, many of their daily decisions are being made for them; they have control of only their eating habits and how they feel about their self-image.

The goal is to help the athlete to make the best decisions, especially in the initial visits. The athlete should not feel as though the medical staff is trying to take away her control. If a heavy-handed approach is used, many athletes may ignore or reject the advice given.

Although the physician may be able to restrict the patient's participation in organized practice and competition, most athletes also work out on their own, and they may continue to do so against medical advice. In early discussions with the athlete, the physician should persuade her to adhere to modest exercise reductions (eg, 10-20% reduction per week until acceptable goals are reached). More serious cases involving weight loss of more than 20% below the ideal body weight may require more aggressive activity cessation or even inpatient therapy, but fortunately, these cases are not as common as less severe cases.

The focus should be on lifestyle modifications. The athlete’s weight should not be used as the absolute indication of treatment success because body weight may be overemphasized already. Weight measurements should be taken as few times as possible, and once the patient has stopped losing weight, routine measurements should be stopped.

Dietary changes can also be made at this time, or a nutritionist may be consulted to address these issues. Again, modest changes should be attempted until a trusting relationship has been established. Sometimes the coach/trainer/physician must agree that the athlete will not return to the team or to competition until the weight reaches a minimum value (ie, the weight increases through lifestyle changes).
 
A team member or fellow athlete may also help with treatment. Most athletes with the female athlete triad are either loners or have only one friend on the team.

Hospitalization may be required at any time during the treatment process if it is determined that the athlete is continuing to harm herself or if she shows signs of multi-organ dysfunction due to extreme weight loss. The decision is highly individualized and should be made in consultation with a trained psychiatrist who is willing to treat such patients. Hospitalization for affected patients is often a long-term process, and months-long hospital stays are not uncommon. A good prognosis is far from ensured, even with optimal treatment.

Related Medscape topics:
Resource Center Eating Disorders
Resource Centers Patient-Provider Relations in Psychiatry & Mental Health
Specialty Site Psychiatry & Mental Health
Specialty Site Women's Health

Surgical Intervention

Unless a fracture or stress fracture requires surgical intervention, surgery is usually not indicated.

Consultations

A multidisciplinary approach should be used in the treatment of the female athlete triad. A team approach to care of the athlete with the team physician or primary care physician coordinating care is vital, not only to ensure that all details are covered but also to provide the athlete with an individual to whom she can always go to with questions.7

A psychologist or psychiatrist familiar with eating disorders should be contacted for assistance with psychosocial issues. The consultant should be aware that most athletes do not meet the strict DSM-IV criteria for bulimia or anorexia and that these individuals are most likely to have disordered eating. Psychotherapy for behavior modification is often useful in adjusting habits that may be detrimental to the athlete’s health. Antidepressants or antipsychotic medications are rarely indicated for these patients. Some physicians do recommend selective serotonin reuptake inhibitors (SSRIs) in individual cases. The advantage is treatment of the comorbid depression, anxiety, and or OCD that may exist; however, a disadvantage is that some individuals lose weight. Therefore, the use of SSRIs is a judgment call.

A nutritionist, especially one with experience in sports nutrition, is of great help. Many larger universities and professional organizations employ a nutritionist to care for its athletes. Even if the athlete being treated is not a member of one of these organizations, the training or medical staff of these institutions may be able to provide the physician with a contact for assistance. The nutritionist should be able to help the medical staff in assessing the patient's caloric intake and output and to advise them about how to help the patient make modifications that will have a maximal impact on the disease while causing the least amount of trepidation by the athlete.

A cardiologist may need to be consulted if cardiac arrhythmias are present. Cardiac arrhythmia is the leading cause of death in patients with anorexia and often starts as simple sinus bradycardia. Prompt referral should be made at the earliest sign of a cardiac abnormality. Few patients with anorexia complain of the classical chest pain or shortness of breath until late in the course of the disease.

If the athlete develops a fracture or stress fracture that requires surgical intervention, referral to an orthopedist is needed. Many such injuries can be managed conservatively; however, femoral neck stress fractures or compression vertebral fractures may require consultation with a specialist. If casts or braces are needed, they may need to be used for a longer period than usual because of the patient's altered nutritional status.

If the team physician is not comfortable with performing pelvic examinations, he or she should refer the athlete to her primary care provider or gynecologist. Endometrial biopsy is sometimes necessary as part of the workup for the triad, and this should be preformed by a physician experienced with these procedures.

Close contact with the coach and medical staff should be maintained to monitor the athlete's attitude, affect, practice regimen, eating patterns. Especially with athletes who travel for competition or who are part of an organized athletic squad, the athletic trainer may be able to report any unusual behavior. Skipped meals, meals taken by herself when the rest of the team is eating together, and exercising in addition to scheduled practices are all behaviors that should reported to the medical staff.

Related Medscape topics:
Resource Center Adolescent Medicine
Resource Center Exercise and Sports Medicine
Resource Center Nutrition

Other Treatment

Other treatments can be directed at secondary musculoskeletal problems that may arise, but the focus should remain on the underlying problem of the triad.

Recovery Phase

Rehabilitation Program

Physical Therapy

Physical therapy can be continued, if needed.

Medical Issues/Complications

Treatment should quickly move into the recovery phase to minimize further damage. This phase can involve the use of multiple medications and supplements directed at various systems in the athlete’s body.

Nutritional modifications can continue at this point, with the assistance of a sports nutritionist. Caloric intake should be increased slowly to avoiding compound the patient’s fear of becoming fat. A food diary and 24-hour recall can be used to monitor intake. If the athlete is part of a large college or university, its nutritional staff can prepare special diets and monitor the patient's intake. The athlete should be encouraged to eat with friends and during accepted eating times. Eating alone makes it easier for the patient to leave larger portions of the diet uneaten. A "food buddy" can make sure the athlete attends all meals and does not simply load her plate with lettuce and carrots and later define this as an adequate diet.

Activity modifications can help reduce the energy drain that may be contributing to the triad. Again, modest reductions in activity levels help prevent the athlete from ignoring the physician's recommendations. If the restrictions are too severe, the athlete may completely ignore them, with the justification that they are unreasonable. If necessary, a contract may be used to set the guidelines for exercise.

If the patient ignores the recommendations of the physician or one of the consultants, the athlete's temporary removal from the team or sport may be imposed. This approach is obviously more difficult to enforce in athletes who have acquired the triad as part of an individual sport or outside organized sports. Moreover, this approach may change the athlete’s attitude toward the medical staff to a more adversarial tone, which can lead to noncompliance or therapy failure.

Calcium, vitamin D, and potassium dietary supplementation may help to minimize the osteoporosis that can occur with the female athlete triad, especially in athletes who have strict or unusual dietary restrictions. A dose of 1200-1500 mg of elemental calcium, 400-800 IU of vitamin D, and 60-90 mg of potassium is suggested for young adults with menstrual dysfunction. Although only a few studies have been conducted to investigate the effects of calcium supplementation in women with the female athlete triad, the low cost and benign nature of this mineral makes it a safe suggestion.

Per the 2007 ACSM positional stand, hormone replacement therapy and oral contraceptive pills are not commonly used in athletes suffering from the triad.7 Rather, restoration of menstrual function should focus on correcting the low energy availability by meeting the athlete’s caloric needs. This will restore GnRH and LH pulsatility and menstruation. Furthermore, restoring regular menstruation has not shown to increase BMD and only at best has been shown to halt further bone mineral loss while the athlete works to correct other components of the triad. Bisphosphonates have been shown to not have a role in significantly increasing BMD and should never be used in premenopausal woman due to the uncertainty of their half life and their teratogenic effects on an unborn fetus.  

Again, a reduction and not cessation of activity should be emphasized early in the course of treatment. As previously suggested, a 10-20% activity reduction per week may be appropriate until acceptable goals are reached.

Consultations

Continued close contact with consultants should be maintained.



Medical treatment is of secondary importance after changing the eating and exercise habits of the athletes affected with the female athlete triad. Some medicines can be used in conjunction with behavior modifications. The medications mainly consist of those used for hormone replacement and dietary supplementation.
 
Some physicians recommend SSRIs in individual cases. The advantage in using such agents is treatment of OCD, depression, and anxiety; however, a disadvantage is that some individuals lose weight. Therefore, the use of SSRIs is a judgment call.

Drug Category: Contraceptive, Oral

Oral contraceptive agents can be used in athletes >16 years old whose BMD continues to decline during treatment for the female athlete triad despite a normalized caloric intake and weight.

Drug NameMedroxyprogesterone acetate (Cycrin, Amen)
DescriptionFor hormonal cycling and reestablishment of the hypothalamic-pituitary axis. Administer cyclically 12 d/mo to prevent the endometrial hyperplasia that unopposed estrogen may cause.

In young women, regular withdrawal bleeding is preferable, because even young women with premature ovarian failure have a 5-10% chance of spontaneous pregnancy (unlike postmenopausal women).
Adult DoseUse as directed; 10 mg PO qd for first 12 d of menstrual cycle is suggested
Pediatric DoseNot recommended
ContraindicationsDocumented hypersensitivity; known or suspected pregnancy; breast cancer; endometrial cancer; hepatic cancer; undiagnosed abnormal vaginal bleeding; active thrombophlebitis or thromboembolic disorders; history of thrombophlebitis, thrombosis, or thromboembolic disorders associated with previous estrogen use (check the PDR for additional contraindications)
InteractionsMay reduce the hypoprothrombinemic effect of anticoagulants; coadministration of barbiturates, rifampin, and other agents that induce hepatic microsomal enzymes may reduce estrogen levels; pharmacologic and toxicologic effects of corticosteroids may occur as a result of estrogen-induced inactivation of the hepatic P450 enzyme; check the PDR for additional interactions
PregnancyX - Contraindicated; benefit does not outweigh risk
PrecautionsCertain patients may experience headache, breast edema and tenderness, weight gain, thromboembolism, MI, thrombophlebitis, retinal and cerebral thrombosis; check the PDR for additional precautions.



Return to Play

In mild to moderate cases of the female athlete triad, many athletes continue to participate in their activity even while in treatment. Activity modifications should be in place, however, and the time that the patient spends exercising should be closely monitored. When inquiring about exercise times, the physician should ask about formal practice sessions as well as exercise away from the structured environment. Often, the extra activity burns much of the athlete's caloric intake.

When the physician discusses exercise restrictions, the athlete often finds it easier to accept a restriction of her private workouts rather than her practice time with a team or coach. As with anorexia and bulimia, the triad is a secretive disorder. Just as the athlete may want to hide evidence of the disease, she may also try to hide evidence of the treatment. By allowing her to continue activity with her peers or coaches, she may not resist treatment.

Unless necessary, withdrawal from activity should not be used as a form of punishment for noncompliance or lack of objective improvement. This can often result in loss of the trust that has been built up between the clinician and athlete and can lead to the athlete's resumption of self-directed exercise. Instead, the physician should work with the athlete to try to make her understand the necessity of the restrictions that are being set. This should minimize the likelihood of the athlete stopping therapy or being lost to follow-up.

If the athlete has been restricted from athletics because of poor compliance with the proscribed regimen or due to physical limitation (eg, stress fracture), a slow resumption of exercise should be attempted. In advanced or difficult cases, resumption of activity should not be allowed until the athlete is within 10-15% of the suggested body weight. Even in cases in which the athlete meets the weight goal, only slow resumption should be attempted. If a physical limitation is required (eg, to let a stress fracture heal), the limitation may be needed for longer than usual to permit complete healing in the osteoporotic bone.

Complications

Continued bone loss leading to irreversible osteoporosis is the most worrisome complication of the triad. Some evidence exists to suggest that BMD can be regained to a small degree, but it is doubtful that a significant loss can be completely corrected, even with years of therapy.

Multiple stress fractures or complete fractures can, of course, lead to increased incidence of osteoarthritis, depending on the site of the fractures. Other fractures may heal without any long-term sequelae. Careful monitoring of these fractures should be provided, as they may take longer to heal than one would expect. The negative nutritional balance often leads to slowed or delayed healing of fractures.

End-stage eating disorders can result in more serious complications, such as prolonged hospitalization, cardiac arrhythmias, or even death. Anorexia nervosa has an estimated mortality rate of 15% once the diagnosis is made. Compared with other individuals, athletes are less likely to meet the criteria for anorexia or bulimia, but significant morbidity and mortality can occur.

Prevention

Because of the difficulty in diagnosing the female athlete triad and in treating patients with the condition, prevention is fundamental in reducing morbidity and mortality rates. Early detection reduces symptoms and decreases the likelihood of serious long-term consequences.

There is substantial debate between physicians and the coaching community regarding the role of weigh-ins for sports. Some coaches or instructors have strict guidelines based on height or body type, and they set maximal weights for eligibility for competition. This regimented approach often places increased stress on the athlete and sends the wrong message about the importance of weight. It also does not account for how well the athlete has been performing in her sport (eg, a situation in which the best athlete on the team is also 5 lb over the weight limit).

The situation can be made worse when overweight athletes are "punished" with running or performing push-ups or when they are forced to weigh in in front of the team. As a beginning step, the team physician should discourage such public weigh-ins and punishment and emphasize specific athletic achievement instead of weight.

The preparticipation physical examination presents an ideal opportunity to screen all female athletes for signs or symptoms of the triad. A high index of suspicion should be maintained for all female athletes because of the difficulty in diagnosing this disease. Many preparticipation questionnaires now include questions concerning the athlete's menstrual history and contentment with her current body weight. These questions often bring otherwise asymptomatic individuals to the attention of the medical and training staff. If these questions are not a part of the questionnaire, the physician should consider making them part of his or her routine examination. Most women will not volunteer this information unless asked; therefore, a proactive approach should be used in routine history taking.

Better education of team physicians, other healthcare providers, trainers, coaches, parents, and the athletes themselves should reduce the yearly incidence of the female athlete triad. Many young women consider oligomenorrhea or amenorrhea during the season or at times of peak activity a sign of hard work and dedication. Not long ago, the medical community considered athletic amenorrhea a benign condition and treated it as such. If both the athlete and physician are aware of the potential damage that can occur as a result of menstrual dysfunction, they may be able to prevent this insidious disease.

Prognosis

For many athletes, the long-term prognosis is good. Few athletes with the female athlete triad are admitted to the hospital for inpatient treatment, and few die from their disease. However, significant long-term morbidity may affect these women later in life.

The diagnosis of the female athlete triad was established in the early 1990s, and this constellation of symptoms had been noted for years before a name was given to it.3, 20, 22, 23 However, no long-term data about future problems are available. The first generation of athletes in whom this condition was diagnosed is still years away from menopause. Therefore, whether osteoporosis that occurs at a younger age affects mortality or leads to more advanced osteoporosis later in life or an increased risk of significant fractures (eg, hip fractures) is unknown.

For mild to moderate cases of the female athlete triad, some improvement in bone health is thought to occur. The lost BMD is unlikely to be replaced in its entirety, and the bone mass that should have been accumulated during this important time in bone development may or may not be regained. However, many case reports show that bone density does not increase, and the losses may be permanent. Unfortunately, no long-term, double-blinded, controlled studies are available (and cannot be performed).

As more information about the female athlete triad and its complications is gathered, everyone involved may better understand the significant morbidity that can occur years or decades after the disease is diagnosed and treated.

Education

Educating athletes may lead to earlier detection of the female athlete triad. If women know that amenorrhea is not a positive sign of hard work but a harbinger of disease, they may seek treatment sooner. Of course, the triad has a secretive nature, and once an athlete is showing signs of disordered eating, education may not be enough to help these women seek help. If the general athletic population is aware of the signs and symptoms of this disease, the female athlete triad might be caught in its early stages.

Physicians need to do better in educating trainers, coaches, and parents (as well as the athletes themselves). These are the people who will have daily contact with the athlete, and they may be the persons who first raise concerns about a particular individual. Taking the time to talk to the athletic staff about the warning signs may help in preventing the disease or catching it in its early stages.

Related eMedicine topics:
Amenorrhea
Eating Disorder: Anorexia
Eating Disorder: Bulimia
Menstruation Disorders
Stress Fractures

Related Medscape topics:
Resource Center Eating Disorders
Resource Center Exercise and Sports Medicine
Resource Center Nutrition
CME Bone Density Evaluation in Teens Prevents Future Osteoporosis
The Female Athlete Triad: Do Female Athletes Need to Take Special Care to Avoid Low Energy Availability



Medical/Legal Pitfalls

  • The main medicolegal complication is most likely the failure to diagnose the female athlete triad in a timely manner.
  • Because the diagnosis was formalized in the past decade or so, the direction the legal community has decided to take regarding the triad is still being established.
  • Medical malpractice suits are likely to follow patterns established in the diagnosis of anorexia and bulimia.
  • Although the diagnosis of the female athlete triad is relatively new, legal-civil penalties could be harsh because of the severity of the disease and the population it affects.
  • As with most diseases, timely diagnosis and initiation of treatment is paramount in avoiding lawsuits. Diagnosis of the female athlete triad can be delayed because the stress fracture is diagnosed first, followed by the amenorrhea and, lastly, the eating disorder.
  • What may make civil litigation difficult are the secretive nature of the disease and the significant rate of patient noncompliance with treatment.
  • Even with rapid diagnosis and treatment, bad outcomes are possible.

Related Medscape topic:
Resource Center Medical Malpractice and Legal Issues

Special Concerns

  • The female athlete triad affects a specific subpopulation, and as such, this disease poses a few special concerns to consider.
  • Pregnancy is usually not an issue because of the amenorrhea involved with the triad. If the athlete is lacking this portion of the triad, pregnancy is still unlikely because of the physical and nutritional stresses she is experiencing. If the athlete does become pregnant while exhibiting other signs of the triad, a more aggressive treatment approach must be pursued in decreasing her activity levels and in addressing her nutritional changes.
  • The female athlete triad rarely affects women older than 40-50 years. By far, most women are affected in their early teens to late 20s. This disease is simply not one that affects the geriatric population. It can, however, affect girls who have not yet experienced menarche. In these patients, differentiating primary amenorrhea from congenital abnormalities or hormonal imbalances during the initial workup becomes significantly more important.

Related Medscape topics:
Resource Center Adolescent Medicine
Specialty Site Women's Health



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Female Athlete Triad excerpt

Article Last Updated: May 30, 2008