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Adolescent Gyn Series

The Female Athlete Triad

Erica J. Gibson, MD; Susan M. Coupey, MD

Although there are myriad physical and emotional benefits of exercise for female adolescents, it is important to remember that competitive pressures can also lead to medical problems.

The female athlete triad is a syndrome of amenorrhea, disordered eating, and osteoporosis in athletic women and girls. This syndrome has become more prevalent over the past few decades as young women have begun to participate more actively in athletics. Since girls gained equal access to school-sponsored sports in 1972, the number of young female athletes in the United States has increased from one in 27 high-school girls to one in three in 1998.1 But with the benefits of an active, competitive lifestyle have also come the physical and psychological effects of overtraining. Female athletes now engage in high-level competition from a very young age, increasing the risk of the triad, particularly in sports where leanness or a slender appearance factor into performance (eg, long-distance running, figure skating). Psychosocial issues such as social isolation, a highly structured life, lack of a support system, and a family history of eating disorders (anorexia nervosa, bulimia nervosa) have also been associated with the female athlete triad.2

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THE FEMALE ATHLETE TRIAD

In adolescents, the female athlete triad can be conceptualized as a disruption in normal pubertal growth and development secondary to inadequate nutrition and overexercising. These two mechanisms interact to suppress the hypothalamic-pituitary-ovarian axis, which in turn leads to a decrease in estrogen levels, amenorrhea, and decreased bone mineralization. Research has confirmed that the hypothalamic suppression is most likely secondary to an imbalance between caloric intake and energy expenditure—ie, “energy drain”—that causes a decrease in pulsatility of luteinizing hormone (LH).3 It is also important to consider why a young athlete has become caught in this dangerous “loop” of such significant energy imbalance; pressure to perform at a high level from the athlete herself, coaches, and family often results in excessive stress and inappropriate training regimens that contribute to the triad. The triad can present as primary or secondary amenorrhea, disordered eating patterns, or as stress fractures due to osteoporosis.


Amenorrhea

The incidence of secondary amenorrhea in the general population is approximately 5%, compared with 10% to 20% in female athletes and 30% to 50% in elite athletes.4 In an adolescent, secondary amenorrhea is defined as the absence of menses for 6 months in a girl who has had at least one menstrual period. However, many young athletes present with primary amenorrhea—ie, the absence of menses by age 13 years without secondary sex characteristics, or the absence of menses by age 15 years with secondary sex characteristics. Primary amenorrhea and persistent hypo-estrogenemia is of particular concern for bone mineralization; without intervention, adequate peak bone mass may never be achieved in these girls.


Disordered Eating

Disordered eating in the female athlete triad is manifested as a caloric intake that is lower than caloric expenditure. Most girls with the triad do not fulfill the criteria for anorexia nervosa outlined in the American Psychiatric Association’s Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV),5 but because of the vastly increased caloric intake required for exercise, they underestimate how much they should eat. Nonetheless, some girls with the triad also have comorbid anorexia nervosa, and require intensified intervention to prevent further deterioration. Many athletes with the triad fulfill the DSM-IV criteria for eating disorder, not otherwise specified (Table 1).5

Table not available online

Table 1. Diagnostic Criteria for Eating Disorder—Not Otherwise Specified5


Osteoporosis

Under the influence of pubertal hormones, girls accumulate approximately 40% of their peak bone mass between ages 11 and 18 years. Peak bone mass is usually attained by age 25 years, but the rate of bone mineralization slows dramatically after age 17 years.6,7 While weight-bearing activity in young women enhances bone mineralization, such activity in the context of disordered eating, low body weight, and low estrogen levels may result in osteopenia or even osteoporosis. These conditions put athletes at risk of stress fractures in the legs, feet, and spine (Figure).1

Figure not available online

Figure . Radiograph showing left tibia stress fracture. A 14-year-old female long-distance runner presented with left anterior shin pain.

Courtesy of Eric Small, MD, Family Sports Medicine and Nutrition, Mount Kisco, NY.


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EVALUATION

Adolescents with the female athlete triad may present with a spectrum of signs and symptoms manifested in physical appearance, vital signs, injuries, and delays in growth or development. Thorough menstrual, diet, and exercise histories should be elicited together with a review of the patient’s psychosocial situation. Numerous general and sports-specific factors have been associated with eating disorders, and physicians should inquire explicitly about these issues (Table 2).8 The clinician should ask if there is a family history of anorexia nervosa or bulimia nervosa in the patient’s mother or close female relatives, as such disorders have familial associations. Screening questionnaires such as the Eating Disorder Inventory, the Eating Attitudes Test, and the Eating Disorder Examination can be useful.9 It is important to plot weight, height, and blood pressure on a growth chart that indicates the fifth and 95th percentiles for age.

Table not available online

Table 2 . Risk Factors for the Development of Eating Disorders in the Female Athlete8

Signs of undernutrition may include loss of subcutaneous fat, dry hair, dry skin, cold extremities, and bradycardia. Initial laboratory evaluation should include a complete blood cell count, basic metabolic panel, and thyroid function tests, as well as levels of prolactin, estradiol, free testosterone, LH, and follicle-stimulating hormone. A β-human chorionic gonadotropin test should be done to rule out pregnancy. Testing the erythrocyte sedimentation rate can help screen for chronic illness. Many of these laboratory tests will also rule out other conditions that can lead to irregular menses.9 A progesterone challenge test may be helpful to evaluate estrogen status.

Bone density may be assessed with a dual-energy X-ray absorptiometry scan to evaluate for osteopenia. Although the results may not affect management, they may help to convince the athlete of her vulnerability to fractures.10 It is important to interpret adolescent bone-density measurements appropriately with pediatric/adolescent-specific computer software that calculates Z-scores rather than T-scores. The Z-score compares the patient’s bone density with a reference population of the same age and sex, whereas T-scores use a reference group of 30-year-old women. Therefore, T-scores are not appropriate for adolescents who have not yet achieved peak bone mass (Table 3).11

Table not available online

Table 3 . Pitfalls of Dual-energy X-ray Absorptiometry in Pediatrics11

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MANAGEMENT

Ideal management of any multifactorial syndrome is multidisciplinary in nature. Girls with the female athlete triad require the support of family, coaches, trainers, nutritionists, physicians, and counselors. Referral to a physician specializing in sports medicine who has experience with high-level athletes, athletic training regimens, and competition schedules is often very helpful. Athletes must first be encouraged to decrease their energy expenditure. Specific recommendations may include decreasing overall weekly aerobic activity by 10% to 20%, or replacing aerobic activity with strength training 1 or 2 days per week. If the athlete is given specific recommendations and a plan is developed with the physician, coach, trainer, and athlete, there is a higher likelihood of compliance.

Improved nutrition must appropriately support the energy expended on exercise. Supplemental calcium and vitamin D are recommended. Referral to a nutritionist and psychologist or social worker should be considered to address disordered eating; this is mandatory if anorexia nervosa is diagnosed. Close medical follow-up should be continued as long as the patient has abnormal findings on physical examination or there is concern for medical complications.

While numerous studies have shown that combination oral contraceptives (OCs) have a positive effect on bone mineral density (BMD) in adult women who have already acquired peak bone mass, the benefits of estrogen therapy for BMD in adolescents remain to be established.12,13 Although no large-scale studies have been conducted on adolescents, small studies have produced variable results. Some girls have shown improvement in BMD, while others have shown no change or loss of BMD.14-18 However, there is evidence that combined (estrogen/progestin) hormonal contraception may suppress bone metabolic turnover in adolescents, which—while slowing bone resorption—may have an adverse effect on bone development.19,20 While the American Academy of Pediatrics formerly recommended hormonal therapy in the form of OCs in amenorrheic athletes who were at least 3 years post menarche and at least age 16 years, they now recommend OCs only for “mature” amenorrheic athletes.21 Optimal regimens have not been determined. Treatment with hormones results in “artificial” menstruation and has no effect on the underlying cause of the disorder. Bisphosphonates, while commonly used to treat osteopenia in postmenopausal women, are not approved for use in menstruating women, and may have unknown adverse effects on adolescents and their future offspring.

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CONCLUSION

Ideally, the goal is to prevent the female athlete triad by educating young athletes, parents, trainers, and coaches about the risks it presents. All young female athletes should be routinely monitored for undue stress, overexercising, insufficient nutrition, inappropriate weight loss, amenorrhea, and osteopenia.

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Erica J. Gibson, MD, is postdoctoral fellow, Division of Adolescent Medicine, The Children’s Hospital at Montefiore, Bronx, NY. Susan M. Coupey, MD, is professor of pediatrics; and chief, Division of Adolescent Medicine, The Children’s Hospital at Montefiore and Albert Einstein College of Medicine, Bronx, NY.


References

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  3. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003;88(1):297-311.
  4. Kazis K, Iglesias E. The female athlete triad. Adolesc Med. 2003;14(1):87-95.
  5. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 1994:550.
  6. Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG. Changes in vertebral bone density in black girls and white girls during childhood and puberty. New Engl J Med. 1991;325(23):1597-1600.
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  15. Emans SJ, Grace E, Hoffer FA, Gundberg C, Ravnikar V, Woods ER. Estrogen deficiency in adolescents and young adults: impact on bone mineral content and effects of estrogen replacement therapy. Obstet Gynecol. 1990;76(4):585-592.
  16. Bachrach LK, Katzman DK, Litt IF, Guido D, Marcus R. Recovery from osteopenia in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab. 1991;72(3):602-606.
  17. Hergenroeder AC, Smith EO, Shypailo R, Jones LA, Klish WJ, Ellis K. 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(5):1017-1025.
  18. Almstedt Shoepe H, Snow CM. Oral contraceptive use in young women is associated with lower bone mineral density than that of controls. Osteoporos Int. 2005; 16(12):1538-1544.
  19. Rome E, Ziegler J, Secic M, et al. Bone biochemical markers in adolescent girls using either depot medroxyprogesterone acetate or an oral contraceptive. J Pediatr Adolesc Gynecol. 2004;17(6):373-377.
  20. Wreje U, Brynhildsen J, Aberg H, Bystrom B, Hammar M, von Schoultz B. Collagen metabolism markers as a reflection of bone and soft tissue turnover during the menstrual cycle and oral contraceptive use. Contraception. 2000;61(4):265-270.
  21. Committee on Sports Medicine and Fitness. American Academy of Pediatrics: Medical Concerns in the Female Athlete. Pediatrics. 2000;106(3);610-613.

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