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The Female Athlete Triad: Causes, Diagnosis, and Treatment

Angela D. Smith, MD

THE PHYSICIAN AND SPORTSMEDICINE - VOL 24 - NO. 7 - JULY 96


In Brief: The female athlete triad of disordered eating, amenorrhea, and osteoporosis affects women and girls in many sports, but the messages conveyed to those in "appearance" sports like gymnastics may play a role. Because the triad may result in irreversible bone loss and death, early detection is imperative. Friends, parents, coaches, and physicians can be alert to behaviors like eating alone, trips to the bathroom during or after meals, and the use of laxatives. Other signs and symptoms of the female athlete triad may include fatigue, anemia, depression, cold intolerance, lanugo, and eroded tooth enamel from frequent vomiting. Multidisciplinary treatment typically involves education, determining contributing factors, restoring adequate nutrition, and prescribing estrogen therapy when appropriate.

Physical fitness is associated with decreased mortality (1) and improved psychological outlook. Improved physical fitness may result from physical labor or leisure activity.

In the early 1800s, North American women could not reasonably avoid fitness-enhancing labor—they hauled water for cooking and drinking, cut and carried logs for firewood, and hefted small children. They used their upper extremities for kneading bread, milking cows, and churning butter. Their aerobic exercise included walking for miles to get supplies or visit a neighbor.

At the turn of the century, however, many women were told that physical activity and education decreased reproductive health. Strolls and gentle gardening were considered appropriate activities for ladies, but running and bicycling were viewed with disdain. Wasp-waist corsets kept them from taking a deep breath, so aerobic exercise would have been very difficult. Since the corsets also apparently caused disuse atrophy of abdominal muscles, women reportedly raced into their corsets first thing in the morning to avoid fainting (2).

The roaring '20s brought the backlash—suffragettes walked for their cause, and dance steps became very lively, with the Charleston and the cakewalk all the rage. In the '40s, the activity level of middle class women increased with the physical labors of wartime mill work and victory gardens.

In the 1950s, many North Americans found more leisure time, and women enjoyed the jitterbug, golf, and tennis. Since the 1960s, few limits have existed. Today's women run marathons, kayak in white water, and swim the English Channel. Many are highly competitive in their sports. Social sports also prosper, as do fitness activities that can have a cosmetic focus, such as aerobics, step classes, and workouts on fitness machines. Of course, physical labor continues to be the primary physical activity for many women.

Destructive Messages and the Triad

Despite the interest in healthy exercise, mixed messages abound. Female competitors are expected to be assertive or even aggressive, yet have the appearance of sweet little girls. They are expected to be tough competitors—and soft-spoken, elegant ladies. Today's "healthy" look is thin, according to society's current definition. Unfortunately, unhealthy behaviors are associated with this very slender appearance. The most touted body image is unattainable by most: slim, androgynous hips combined with voluptuous breasts. The supermodels with their personal trainers and, in some cases, enhanced breasts are the idols of today's teenagers.

It can be extremely difficult for any adolescent girl to try to resolve these messages into something she can reasonably attain. It is even more difficult for the young athlete—especially when under pressure from coaches, parents, siblings, and agents—to resolve the conflicting requirements for aggressiveness and sweetness, strength and daintiness, and optimal weight for performance and desired thinness for look. Unfortunately, some young athletes cannot resolve all these issues effectively and consequently develop disordered eating behaviors. The problem is generally compounded by the external pressures placed on the athlete, particularly when financial issues and others' egos intervene. Often the main issue is control, and the athlete's weight may be one of the few things she completely controls.

Most young women have normal concerns about body shape. This concern is typically strong at the time of puberty, when body shape changes rapidly. However, girls' concerns span a broad spectrum, from the normal interest in maintaining a healthy weight to excessive preoccupation with body shape to a markedly distorted body image.

Healthcare professionals should always emphasize that the benefits of sports far outweigh the risks. Proven benefits include improved health and fitness and increased longevity. However, the risks include injury and development of the female athlete triad of disordered eating, amenorrhea, and osteoporosis. Consequences of the female athlete triad may include psychological sequelae, irreversible bone loss, other disorders related to starvation and decreased serum estrogen levels, and death.

Disordered Eating and Its Effects

The spectrum of disordered eating behavior ranges from moderate restriction of food intake or occasional bingeing and purging to severe food restriction (as in anorexia nervosa) and regular bingeing and purging (as in bulimia nervosa). (See the Nutrition Adviser, "Food Fight: Calling a Truce With Disordered Eating".) Among female athletes, the prevalence of disordered eating behavior is between 15% and 62% (3,4), depending on the particular survey examined. Disordered eating is most common among those in appearance sports, such as gymnastics, ballet, figure skating, equestrian sports, and diving. However, disordered eating behavior can be seen in other sports in which appearance should not figure so strongly (since they are not judged), such as tennis, swimming, and running.

The symptoms of anorexia nervosa include morbid fear of fatness, distorted body image, refusal to maintain a weight at least 85% of that expected for height and age, and amenorrhea (defined in the fourth edition of the Diagnostic and Statistical Manual of Mental Disorders [DSM-IV] as the absence of at least three consecutive menstrual cycles in a postmenarcheal female). There are two forms of anorexia nervosa. Those with the restrictive type do not regularly engage in bingeing and purging. Those with the bingeing-purging type use this behavior regularly during an episode of anorexia nervosa, according to the DSM-IV.

The symptoms of bulimia nervosa include recurrent episodes of binge eating, with a sense of a lack of control over eating. Bulimic athletes may purge by vomiting or using laxatives or diuretics. Nonpurging activities that can substitute for purging include fasting and exercising excessively. To fit the definition of bulimia nervosa, the bingeing and purging must occur at least twice a week for at least 3 months. Bulimics are overly concerned with body shape and weight, but they do not have the markedly distorted body image of anorexic women. To fit the definition, the bulimia must not occur exclusively during episodes of anorexia nervosa. Bulimia nervosa has now been divided into two types also: purging and nonpurging.

Ratnasuriya et al (5) showed that 6 (15%) of 41 hospitalized nonathletes with anorexia nervosa died of the disorder. The morbidity of eating disorders is also high. Serious problems include disturbances of the cardiovascular, endocrine, and gastrointestinal systems, disruption of temperature regulation, psychological sequelae, and irreversible bone loss.

Amenorrhea and Its Effects

A girl is described as having primary amenorrhea if she has reached 16 without the onset of menses, or if she has gone 2 years following thelarche (development of secondary sex characteristics) without menarche. Secondary amenorrhea exists when a patient with previously normal menstrual cycles has fewer than six to nine periods annually (the definition varies according to different sources). The prevalence of amenorrhea is 2% to 5% among the general population, but 3% to 66% among athletes in different sports (6). Amenorrhea is often associated with decreased serum estrogen levels. Lack of protective estrogen leads to decreased bone mass and may raise cardiac risk (7).

Osteoporosis and Its Effects

Osteoporotic bone has decreased bone mineral content compared with normal bone (see "Guidelines for Diagnosing Osteoporosis" by Gail P. Dalsky, PhD). The bony trabeculae are thin and weak, and the cortex is thinned. The decreased bone mass may be from one of two causes. Bone may have been inadequately acquired during adolescence, which is the usual time for deposition of the "bank" of bone mineral that will take a young woman through adulthood—or a woman may have had normal bone mineral content but lost it prematurely.

The prevalence of osteoporosis among athletes in general is unknown. Osteoporosis has been found among female runners with amenorrhea or oligomenorrhea and among ballet dancers.

Drinkwater's group (8) first sounded the call about osteoporosis in amenorrheic runners when they found that such runners had much lower bone mineral density than normally menstruating runners. Fisher et al (9) also studied the bone mineral content of amenorrheic and eumenorrheic runners, finding a direct correlation in the amenorrheic runners between bone mineral content of the lower lumbar spine and estradiol level. However, others have not found such a correlation, which suggests a more complex interaction of multiple factors (10).

Recent data suggest that portions of the skeleton may be protected from osteoporosis in athletes (including amenorrheic athletes) who participate in sports that include high impact loading, such as figure skating and gymnastics. Robinson et al (11) compared competitive female gymnasts with competitive female runners, each group having the same incidence of menstrual irregularities. They found that the gymnasts had greater bone mass values for the hip and total body than did controls, and the runners' values were lower than the controls' values.

A study by Kirchner et al (12) of college gymnasts found that they had higher bone mineral density than control students matched by age, height, and weight, despite having a higher incidence of menstrual irregularities and inadequate calcium intake. This finding was true for all sites tested (lumbar spine, total proximal femur, femoral neck, Ward's triangle, and whole body). Finally, Slemenda and Johnston (13) measured the bone density of figure skaters and found they had higher bone mineral density in the lower extremity and pelvis than did controls. This was true even for amenorrheic skaters.

Recognizing the Triad

Recognition of the female athlete triad is important but may be difficult. Athletes with disordered eating may be very secretive about their behavior, although teammates or roommates may be aware of an athlete's behavior that suggests disordered eating (table 1) (14). However, only friends, coaches, or parents who have been alerted to these behaviors as possible signs of disordered eating are likely to notice them. Such behaviors—some of which may be elicited during history taking—include frequent eating alone, trips to the bathroom immediately after (or during) meals, feet pointing toward the toilet in a bathroom stall (bulimics may learn to vomit so quietly that it sounds like urination), and the use of laxatives. Of course, a thorough menstrual history is also essential.

Table 1. Behavioral Signs Suggestive of Disordered Eating

Preoccupation with food and weight
Repeatedly expressed concerns about being fat
Increasing criticism of one's body
Frequent eating alone
Use of laxatives
Trips to the bathroom during or following meals
Feet pointing toward the toilet in a bathroom stall
Continuous drinking of diet soda or water
Compulsive, excessive exercise
Complaining of always being cold

Those who provide medical care for athletes should be alert to stress fractures as possible signs of the triad, particularly noting unusual fractures that occur from minimal trauma, such as fractures of the femur, ribs, or pelvis. Physical signs and symptoms may include fatigue, anemia, and depression (table 2). Other occasional findings include erosion of tooth enamel from frequent vomiting and enlarged parotid glands.

Table 2. Signs and Symptoms of the Female Athlete Triad

Fatigue
Anemia
Depression
Stress fracture
Decreased ability to concentrate
Cold intolerance
Hypothermia
Cold and discolored hands and feet
Enlargement of the parotid glands
Sore throat
Callused knuckles from pressure against the teeth during induced vomiting
Erosion of dental enamel from frequent vomiting
Abdominal pain and bloating
Constipation
Dry skin
Face and extremity edema
Lightheadedness
Bradycardia
Changes in orthostatic blood pressure
Chest pain
Lanugo
Carotenemia

Obstacles to Overcome

Some myths that athletes believe may be difficult to combat. One is the idea that loss of menstrual periods means the athlete is training at an appropriate intensity, rather than indicating an unhealthy state (or pregnancy).

Another myth is that very low body fat is the key to excellent athletic performance. If the athlete does not draw this conclusion herself from watching successful athletes in her sport, it may be impressed upon her continually by her coaches, parents, or (less often) peers. It can be helpful to point out individual athletes who have had their best successes at higher percentages of body fat, or with a body shape that is something other than very slender. Athletes do not always understand that the optimal weight for appearance is not necessarily the optimal weight for performance, and that neither of these may be the optimal weight for good health.

An additional problem that needs to be understood concerns the methods of determining body fat. Although underwater weighing is considered the gold standard, the body fat value will be falsely high with underwater weighing when bone density is decreased. This occurs because the standard equations do not take into account the increased porosity of osteoporotic bone.

Breaking the Triad

When an athlete is found to have triad symptoms, a multidisciplinary approach is required. This involves the primary care physician, a dietitian, and a psychiatrist or psychologist. They work with the athlete to identify issues that may have contributed to disordered eating and to address these issues, as well as to assist her in restoring adequate food intake. Hormone replacement may be required* (see "Hormone Therapy and the Female Athlete Triad"). Parents of minors and sometimes coaches need to be closely involved. Often an orthopedist, certified athletic trainer, and/or physical therapist can provide important interaction and services.

With regard to diet, it is useful to emphasize increasing lean-body mass—and sustaining the lean body mass by eating a well-rounded, high-carbohydrate diet. The patient should understand that she needs sufficient calories to meet both her routine daily needs and her sport needs. Calcium is recommended at a level of 1,500 mg/day, to provide some protective effect to the bones. The patient also needs sufficient vitamin D from the sun and/or her diet.

The national governing bodies of several sports either have in place or are developing programs aimed at preventing elements of the triad, educating athletes, and treating symptoms. A group of leaders from sports in which the female athlete triad seems to occur most frequently met in Atlanta last September to discuss the problems and potential answers. Because of this group's recommendation, the International Olympic Committee Medical Commission appointed a task force to address the triad issues.

Keeping Watch for Warning Signs

It is unlikely that the extrinsic and intrinsic pressures on female athletes to be thin will abate any time soon. Therefore, we must be alert to signs and symptoms that suggest the presence of the potentially very serious disorders of the female athlete triad. Early, multidisciplinary intervention may decrease morbidity and save lives. By making every effort to minimize the risks to which athletes are exposed, we can help ensure that women have opportunities to experience the marvelous benefits of sports and exercise.

Hormone Therapy and the Female Athlete Triad

(Back up to article)

Who needs hormone replacement therapy?
Hormone replacement therapy (HRT) should be prescribed for every woman who has the female athlete triad, since all such patients are estrogen deficient.* Provided that other pathologic conditions have been ruled out by a thorough hormonal evaluation, some form of estrogen therapy should be prescribed. Progestational therapy should be included in the prescription for every woman who has a uterus.

How should hormone therapy be prescribed?
Hormone therapy can be prescribed as HRT (separate estrogen and progestogen) or as combination oral contraceptive pills. If prescribed as HRT, estrogen may be administered in oral form daily or in a transdermal patch that is changed once or twice weekly. Oral estrogen may be prescribed as conjugated estrogens (0.625 to 0.9 mg) or as micronized estradiol (1 to 2 mg), as well as in other, less commonly prescribed preparations. Progestational therapy for endometrial protection is most commonly prescribed as oral medroxyprogesterone acetate (2.5 to 5 mg daily on the first 12 days of every calendar month or on the last 14 days of a 28-day cycle).

HRT in the levels described here contains enough estrogen to provide bone protection and to induce periods but insufficient estrogen and progestogen to ensure contraception. Thus, oral contraceptives, rather than HRT, may be chosen by women who are sexually active or who prefer the convenience or psychological aspects of this form of treatment (they can help patients feel more "normal").

Oral contraceptive therapy is a perfectly acceptable option for hypoestrogenic amenorrheic women, regardless of whether they are sexually active. It usually induces regular periods, and it provides bone protection and contraceptive efficacy.

Mona M. Shangold, MD

References

  1. Blair SN, Kohl HW III, Paffenbarger RS Jr, et al: Physical fitness and all-cause mortality: a prospective study of healthy men and women. JAMA 120219;262 (17):2395-2401
  2. Kreuter GVL: And Jill came tumbling after: a history of women's participation in sports and games, read before the American College of Sports Medicine Annual Meeting, Dallas, May 1992
  3. Dummer GM, Rosen LW, Heusner WW, et al: Pathogenic weight-control behaviors of young competitive swimmers. Phys Sportsmed 120217;15(5):75-86
  4. Rosen LW, Hough DO: Pathogenic weight-control behaviors of female college gymnasts. Phys Sportsmed 120218;16(9):141-146
  5. Ratnasuriya RH, Eisler I, Szmukler GI, et al: Anorexia nervosa: outcome and prognostic factors after 20 years. Br J Psychiatry 1991;158:495-502
  6. Yeager KK, Agostini R, Nattiv A, et al: The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 1993;25(7):775-777
  7. The Writing Group for the PEPI Trial: Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women: the Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA 1995;273(3):199-208
  8. Drinkwater BL, Nilson K, Chesnut CH III, et al: Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 120214;311(5):277-281
  9. Fisher EC, Nelson ME, Frontera WR, et al: Bone mineral content and levels of gonadotropins and estrogens in amenorrheic running women. J Clin Endocrin Metab 120216;62(6):1232-1236
  10. Snead DB, Weltman A, Weltman JY, et al: Reproductive hormones and bone mineral density in women runners. J Appl Physiol 1992;72(6):2149-2156
  11. Robinson TL, Snow-Harter C, Taaffe DR, et al: Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 1995;10(1):26-35
  12. Kirchner EM, Lewis RD, O'Connor PJ: Bone mineral density and dietary intake of female college gymnasts. Med Sci Sport Exerc 1995;27(4):543-549
  13. Slemenda CW, Johnston CC: High intensity activities in young women: site specific bone mass effects among female figure skaters. Bone Miner 1993;20 (2):125-132
  14. Johnson MD: Disordered eating in active and athletic women. Clin Sports Med 1994;13(2):355-369

*Editor's Note: The Physician and Sportsmedicine is aware that there is controversy about HRT prescription for the female athlete triad. Please send your comments to Forum Editor, The Physician and Sportsmedicine, 4530 W 77th St, Minneapolis, MN 55435 (e-mail to [email protected]).

Dr Smith is an assistant professor of orthopedics at Case Western Reserve University School of Medicine in Cleveland and codirector of Rainbow Sports Medicine at the University Hospitals of Cleveland. She is the team physician for the US Figure Skating World Team, a fellow of the American College of Sports Medicine, and an editorial board member of The Physician and Sportsmedicine. Address correspondence to Angela Smith, MD, University Hospitals of Cleveland, 1074 Abington Rd, Cleveland, OH 44106.


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