Medical Problems of the Athlete:

In the past 30 years, women have made tremendous progress in the area of athletics. This has been largely the result of Title IX of the 1972 Education Assistance Act, which mandated that "any institution that accepts federal funding must provide equal opportunity for women and men to participate in all athletic programs."¹ Title IX has dramatically increased the number of women who are involved in sports at all levels.

As the world of sport has embraced the participation of women and girls, the incidence of health problems that pertain specifically to premenopausal female athletes has increased significantly. One of these is the female athlete triad, which consists of 3 interrelated medical conditions associated with athletic training:

• Disordered eating.
• Amenorrhea.
• Osteoporosis.

Because female athletes are pressured both by societal ideals of attractiveness and the weight standards set by certain sports, they often are preoccupied with body weight. The triad occurs in all sports, but especially those in which low body weight is emphasized for appearance and/or performance, such as running, swimming, diving, ballet, gymnastics, and figure skating.

This increasingly common disorder can have life-threatening consequences-yet too often it goes unrecognized, and the opportunity for early intervention is missed. In this article, we will discuss the warning signs and symptoms of the female athlete triad and also present the latest approaches to treatment and prevention.

UNDERSTANDING FEMALE ATHLETE TRIAD

The American College of Sports Medicine (ACSM) identified the female athlete triad in 1992.² In 1997, the ACSM published the first position paper on the triad, which defined the condition, outlined treatment options, and called for a more concentrated effort at prevention.² In 2000, to address growing concerns regarding female athletes-particularly adolescents-the American Academy of Pediatrics published a policy statement on the triad.³

Disordered eating. This is the central aspect of the triad. When the triad was initially described, the term "eating disorder" was reserved for the clinical diagnoses of anorexia nervosa and bulimia nervosa as defined by the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) criteria of the American Psychiatric Association (APA).⁴ Many athletes did not necessarily meet all the criteria for an eating disorder, yet still exhibited pathogenic weight control behavior. For example, their body weight might not have met the DSM-IV criterion for anorexia or bulimia nervosa (more than 15% below normal weight).⁴ Athletes' weight may seem to be adequate because of the in- creased muscle mass that training has produced.

Thus, the term "disordered eating" was adopted for the female athlete triad to avoid underdiagnosis. Since then, the APA has recognized that its criteria for eating disorders excluded many women with abnormal eat- ing patterns (not just athletes). They consequently added the diagnosis "eating disorder not otherwise specified."⁴Table 1 lists the criteria for this diagnosis.

The prevalence of anorexia nervosa in the general population is approximately 1%; that of bulimia nervosa, 1% to 3%.⁴ However, among female athletes, the frequency both of eating disorders that meet DSM-IV criteria and of pathogenic weight control is between 15% and 62%.^2,5-8 This wide range can be attributed to differences in the percentages associated with various sports and to different definitions of disordered eating.

Despite their increasing prevalence, eating disorders may remain clinically undetected in up to 50% of cases.⁹ The potential warning signs of disordered eating include:

• Ritualized eating.

• Food restriction.

• Obsessive training.

• Other compulsive behavior.

Amenorrhea. Female athletes are at significant risk for amenorrhea; these young women have a higher prevalence of delayed menarche, primary amenorrhea, and secondary amenorrhea. The prevalence of amenorrhea in the general population is 2% to 5%, but in athletes it ranges from 4% to 66%.^5-8,10,11 Again, the variability results from differences in the populations of women who have been studied. The highest frequency is seen in ballet dancers and runners.

Amenorrhea in female athletes results from hypothalamic dysfunction.¹² Until recently, the accepted physiologic explanation of the origin of this dysfunction was the "caloric deficit" or "energy drain" theory. According to this theory, disturbance in menses results when the caloric intake is insufficient to maintain the endocrine components of the female reproductive system. The most current explanation is the "energy availability" theory. This theory holds that when the CNS detects that dietary energy intake is not sufficient to support both exercise and other physiologic functions, it reduces energy expenditure by suppressing reproductive function.¹³ Luteinizing hormone pulsatility is lost, which results in low estrogen levels and a hypogonadal state.¹²

Osteoporosis. Premature bone loss or inadequate bone formation results in low bone mass, increased bone fragility, and increased risk of fracture. Osteoporosis can affect all skeletal sites.^14,15 Below is the classification of bone density according to World Health Organization criteria¹⁶:

• Normal: bone mineral density (BMD) less than 1 SD below the young adult mean.

• Osteopenia: BMD 1 to 2.5 SD below young adult mean.

• Osteoporosis: BMD greater than 2.5 SD below young adult mean.

Female athletes with amenorrhea have low bone density as a result of their hypoestrogenic state.^8,17,18 The prevalence of osteoporosis among female athletes is unknown, and not all athletes with a history of amenorrhea will experience osteoporosis. However, studies have shown that lumbar bone density in amenorrheic athletes is 14% less than that of eumenorrheic athletes and 27% less than that of sedentary women with normal cycles.¹⁸

Osteoporosis in a young athlete is alarming because it indicates that bone density is declining at a time when peak bone mass should be forming. Until recently, it was believed that peak bone mass was achieved around the age of 30 years. Recent studies suggest that peak bone mass is actually achieved between 18 and 25 years of age.^11,19 This may mean that younger female athletes with decreased bone density never reach optimal levels of peak bone mass-which puts them at risk for premature osteoporosis, stress fractures, and later fractures of the hip and vertebrae.

Isolated stress fractures are a common complication of the female athlete triad and may serve as a warning sign. Stress fractures are a common overuse injury. Epidemiologic data have shown that they occur more frequently in women than in men^20-22; however, they may be seen in healthy menstruating athletes as well as in patients with the triad. The actual incidence in women with female athlete triad is not known. Runners, gymnasts, dancers, swimmers, rowers, and lacrosse and basketball players may all be affected; the greatest reported incidence is in runners. Stress fractures account for 4.4% to 15.6% of all injuries to runners.²⁰

Studies have shown that BMD increases when the menses resume.²³ However, this increase lessens over time, and the BMD of previously amenorrheic athletes often remains below normal for their age.^17,23 This fact underscores the importance of early intervention when any aspect of the female athlete triad is suspected.

DIAGNOSIS

Screening. The screening history can identify any warning signs or risk factors for the triad (Table 2) and includes a complete menstrual, diet, exercise, and psychosocial history (Table 3). An excellent time to screen is during preparticipation sports physical examinations.²⁴ A history of amenorrhea is one of the most easily detected signs of early-stage female athlete triad.

Educate adolescents and their parents about the effects of exercise on menstruation. Note any abnormalities in the menstrual cycle; they should not be dismissed as the result of stress from exercise. One study reported that, during preparticipation sports examinations, a majority of women whose menstruation had stopped for longer than 3 months had been previously told by their primary care physician that amenorrhea was "normal" in athletes.²⁴

Once regular cycles have begun, the cessation of menses for 3 months or more is abnormal and warrants evaluation.^2,10,25 Persistent oligomenorrhea, with no regular cycles since the onset of menses, should also be considered abnormal and deserves evaluation.^2,24

Physical examination. Recordcurrent height and weight and compare these figures with previous measurements. The appropriateness of the patient's weight for her height and age can be determined by calculating body mass index (BMI) (weight in kilograms divided by the square of the height in meters). According to DSM-IV, a BMI of less than 17.5 satisfies one of the diagnostic criteria for anorexia nervosa, which may be used as a guideline.³ However, keep in mind that BMI is often not reliable in athletes because of increased lean tissue.

Review vital signs closely, including temperature, heart rate, and supine and standing blood pressure. The cardiac manifestations of poor nutrition may include bradycardia or dysrhythmias.

When examining the mouth, look for erosions of the tooth enamel or pharyngitis caused by vomiting. Swelling of the parotid and submandibular glands and abrasions on the dorsum of the hand are also associated with self-induced vomiting.⁹ Skin findings that point to the triad include lanugo, hypercarotenemia, and dyshydrosis. In sexually active patients, perform a full pelvic examination to exclude possible causes of amenorrhea, and do a Papanicolaou test.

Laboratory evaluation. Order urinalysis, complete blood cell count, serum chemistry panel, and thyroid function tests. Always consider a urine pregnancy test to rule out pregnancy as a cause of amenorrhea. Urinalysis may reveal ketones or abnormal pH, which often indicate inadequate nutrition. Anemia, leukopenia, and thrombocytopenia are often associated with nutritional deficiencies. Hypokalemia, hyponatremia, and hypoglycemia are common in underweight patients and in those who vomit or use diuretics or laxatives. Thyroid function tests often reflect euthyroid sick syndrome, with decreased levels of triiodothyronine and levothyroxine but normal or slightly decreased levels of thyroid-stimulating hormone.²⁶

Diagnostic studies. If abnormal electrolyte levels or bradycardia are found, an ECG is recommended.

There are no current data on the cost-effectiveness of dual energy x-ray absorptiometry (DXA) scanning or other methods of evaluating bone density in amenorrheic athletes. Consequently, the ACSM, the American Academy of Pediatrics, the American College of Obstetrics and Gynecology, and the American Academy of Family Physicians have made no formal recommendations. However, consider ordering a DXA scan for athletes who have been amenorrheic for more than 6 months or who have had recurrent stress fractures.^9,27,28

Further workup. Bear in mind that physical examination findings and laboratory values may be normal in a patient with female athlete triad. Thus, these normal results do not rule out the triad, and further investigation is warranted, with a focus on identifying any signs of abnormal exercise or eating habits.

TREATMENT

If disordered eating is suspected in a female athlete, the best approach involves a multidisciplinary team that consists of a physician, coach, athletic trainer, nutritionist, and mental health professional. The primary care physician plays an integral role in coordinating this care. For most patients with disordered eating, successful treatment that prevents relapse is a lifelong process and requires active participation by the athlete, parents, physician, and possibly other healthcare professionals.

Education is the most important aspect of treatment. Focus on teaching the patient about diet, lifestyle issues, exercise modification, and the potential long-term adverse effects the condition can have on her health.

Nutrition. Educate the patient about nutrition and dietary choices. Dispel myths regarding body composition and athletic performance, and emphasize the body's need for energy in order to perform. Calculate her caloric needs on the basis of weight, height, and energy expenditure. If caloric intake needs to be increased, it is recommended that this be done slowly, by 100 kcal per week, with close monitoring.^6,29

Set a realistic goal weight early on, based on the patient's body build and height. A weight gain of 0.5 to 1.0 pound per week is recommended until this goal is achieved.¹⁶ Even after goal weight is reached, continue to monitor the patient's weight closely for at least 2 to 3 months.

Promote meal sharing with teammates and friends-environments in which the patient feels encouraged to eat and can also be observed.

Exercise. The patient's health status will determine whether she is able to continue training. Recent research may support continuation of the athlete's exercise regimen, provided her diet is sufficiently modified; however, more definitive studies are needed.¹³ It is often helpful to have a written contract with conditions under which the patient may train or compete, such as weight gain, resumption of menses, and regular counseling sessions.²⁹

Psychotherapy. This is an essential component of treatment of the female athlete triad. In the initial phase of therapy, involvement of the family is crucial, both to help the therapist explore the patient's social setting and to educate family members about the triad. Therapy examines how the patient's eating behaviors are related to emotional challenges in her life and provides coping mechanisms and stress management techniques. Together, the therapist and the patient create a relapse plan, and the patient is taught to recognize situations that may increase her risk of relapse. Most importantly, psychotherapy provides the patient an opportunity to focus on her emotional state and the ways in which it is connected with her exercise and eating.

Pharmacotherapy. Medication also has a role in the treatment of female athlete triad and its complications.

Vitamins and minerals. For all patients in whom the triad is suspected, prescribe a regimen of calcium, 1500 mg/d, supplemented by vitamin D, 400 to 800 IU/d, to increase absorption.³⁰

Antidepressants and sedatives. Selective serotonin reuptake inhibitors (SSRIs) may be helpful-although no specific studies have been performed in athletes. SSRIs also have a tolerable side-effect profile. Fluoxetine has been useful in the treatment of bulimia nervosa and is currently the only FDA-approved medication for the condition.⁹ One study has suggested use of benzodiazepines for severe mealtime anxiety.²⁹

Hormonal therapy. Hormone replacement to treat female athlete triad is based on the theory that hypoestrogenism is the primary reason for loss of bone mass. Few studies of hormone replacement therapy (HRT) have been performed in athletes. Most evidence comes from studies of postmenopausal women. The majority of these studies used a standard dosage of 0.625 mg/d of estrogen, which produced a subsequent decrease in risk of fracture.³¹ The same estrogen dosages in amenorrheic premenopausal women have produced inconsistent results.

Retrospective studies have shown that athletes with a history of oral contraceptive use have a decreased risk of stress fractures.^32,33 This has led some physicians to regularly prescribe oral contraceptives for female athletes.

There are few data on specific indications or effects of HRT in athletes with amenorrhea and bone mineral changes. However, in one retrospective study of amenorrheic runners, the effects of HRT were compared with those of placebo over 24 to 30 months.³⁴ The hormonal therapy consisted of conjugated estrogen, 0.625 mg/d; or estradiol transdermal patch, 50 µg/d, plus medroxyprogesterone. The women who received hormonal therapy had significant increases in vertebral and femoral neck BMD (approximately 8% and 4.1%, respectively), while the control group had a nonsignificant decrease in BMD of less than 2.5%.

The only published randomized, controlled trial compared oral contraceptives with medroxyprogesterone and placebo in young women with hypothalamic amenorrhea (defined as no menses for the previous 6 months).³⁵ BMD was measured at baseline, 6 months, and 12 months. Oral contraceptives increased lumbar spine and total body BMD, but no differences in hip BMD were found among the 3 groups. Note that the women randomized to oral contraceptives received 35 µg/d of ethinyl estradiol, approximately 3.5 times the estrogen dosage used in postmenopausal studies. Thus, these results suggest that amenorrheic young women may require higher doses of estrogen to improve bone density. More studies are needed to determine the long-term effects of hormonal therapy in this population.

Little evidence exists regarding the optimal time to initiate hormonal therapy. Irreversible bone loss can occur after 3 years of amenorrhea.¹¹ Therefore, current recommendations are:

Consider hormonal therapy if amenorrhea has lasted longer than 6 months.

Strongly encourage hormonal therapy if imaging studies show any evidence of loss of BMD, either osteopenia or osteoporosis.

The various options for hormonal therapy, including oral contraceptives and cyclic estrogen/progesterone (similar to postmenopausal HRT), are listed in Table 4. More studies are needed to determine the optimal regimen.

References:

REFERENCES:

1.

Education Amendments of 1972: P.L. 92-318, Title IX: Prohibition of Sex Discrimination.

July 1, 1972 (codified at 20 USC 1681 [a]).

2.

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:i-ix.

3.

American Academy of Pediatrics, Committee on Sports Medicine and Fitness. Medical concerns in the female athlete.

Pediatrics

. 2000;106:610-613.

4.

American Psychiatric Association.

Diagnostic and Statistical Manual of Mental Disorders

. 4th ed. Washington, DC: American Psychiatric Association; 1994: 539-550.

5.

Rosen LW, Hough DO. Pathogenic weight-control behavior of female college gymnasts.

Physician Sportsmed.

1988;16:141-146.

6.

Sanborn CF, Horea M, Siemers BJ, Dieringer KI. Disordered eating and the female athlete triad.

Clin Sports Med.

2000;19:199-213.

7.

Rosen LW, McKeag DB, Hough DO, Curley V. Pathogenic weight-control behavior in female athletes.

Physician Sportsmed.

1986;14:79-86.

8.

Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad: the inter-relatedness of disordered eating, amenorrhea, and osteoporosis.

Clin Sports Med.

1994;13:405-418.

9.

Becker AE, Grinspoon SK, Klibanski A, Herzog DB. Eating disorders.

N Engl J Med.

1999;340: 1092-1098.

10.

Otis CL. Exercise-associated amenorrhea.

Clin Sports Med

. 1992;11:351-362.

11.

Lu PW, Briody JN, Ogle GD, et al. Bone mineral density of total body, spine, and femoral neck in children and young adults: a cross-sectional and longitudinal study.

J

Bone Miner Res.

1994;9: 1451-1458.

12.

Warren MP. Health issues for women athletes: exercise induced amenorrhea.

J Clin Endocrinol Metab.

1999;84:1892-1898.

13.

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.

14.

Rencken ML, Chestnut CH, Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes.

JAMA.

1996;276:238-240.

15.

Myburgh KH, Bachrach LK, Lewis BT, et al. Low bone mineral density at axial and appendicular sites in amenorrheic athletes.

Med Sci Sports Exerc.

1993;25:1197-1202.

16.

World Health Organization. Assessment of fracture risks and its application to screening for post-menopausal osteoporosis.

WHO Technical Report Se

ries

. Geneva: WHO; 1994.

17.

Drinkwater BL, Bruemner B, Chestnut CH III. Menstrual history as a determinant of current bone density in young athletes.

JAMA.

1990;263:545-548.

18.

Drinkwater BL, Nilson K, Chestnut CH III, et al. Bone mineral content of amenorrheic and eumenorrheic athletes.

N Engl J Med.

1984;311:277-281.

19.

Matkovic V, Jelic T, Wardlaw GM, et al. Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis: inference from a cross-sectional model.

J Clin Invest.

1994;93: 799-808.

20.

Burr DB. Bone, exercise, and stress fractures.

Exerc Sport Sci Rev.

1997;25:171.

21.

Protzman RR, Griffis CC. Comparative stress fractures incidence in males and females in an equal training environment.

Athletic Training

. 1977;12: 126-130.

22.

Greaney RB, Gerber FH, Laughlin RL, et al. Distribution and natural history of stress fractures in US Marine recruits.

Radiology

. 1983;146:339-346.

23.

Drinkwater B, Nilson K, Ott S, et al. Bone mineral density after resumption of menses in amenorrheic athletes.

JAMA.

1986;256:380.

24.

Skolnick AA. 'Female athlete triad' risk for women.

JAMA.

1993;270:921-923.

25.

Shangold M, Rebar RW, Wentz AC, Schiff I. Evaluation and management of menstrual dysfunction in athletes.

JAMA

. 1990;263:1665-1669.

26.

Moshang T Jr, Parks JS, Baker L, et al. Low serum triiodothyronine in patients with anorexia nervosa.

J Clin Endocrinol Metab.

1975;40:470-473.

27.

Hobart JA, Smucker DR. The female athlete triad.

Am Fam Physician.

2000;61:3357-3364.

28.

Nichols DL, Bonnick SL, Sanborn CF. Bone health and osteoporosis.

Clin Sports

Med.

2000;19: 233-249.

29.

Joy E, Clark N, Ireland ML, et al. Team management of the female athlete triad, II: optimal treatment and prevention tactics.

Physician Sportsmed.

1997;25: 55-69.

30.

NIH Consensus conference. Optimal calcium intake. NIH Consensus Development Panel on Optimal Calcium Intake.

JAMA.

1994;272:1942-1948.

31.

Ettinger B, Genant HK, Cann CE. Long-term estrogen replacement therapy prevents bone loss and fractures.

Ann Intern Med.

1985;102:319-324.

32.

Nattiv A, Armsey TD Jr. Stress injury to bone in female athletes.

Clin Sports Med.

1997;16:197.

33.

Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in female track-and-field athletes: a retrospective analysis.

Clin

J Sport Med.

1995;5:229-235.

34.

Cumming DC. Exercise-associated amenorrhea, low bone density, and estrogen replacement therapy.

Arch Intern Med.

1996;156:2193-2195.

35.

Hergenroeder AC, Smith EO, Shypailo R, et al. Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone, or placebo over 12 months.

Am J Obstet Gynecol.

1997;176:1017-1025.