The Female Athlete Triad

Aurelia Nattiv, M.D., FACSM; Anne B. Loucks, Ph.D., FACSM; Melinda M. Manore, Ph.D., R.D., FACSM; Charlotte F. Sanborn, Ph.D., FACSM; Jorunn Sundgot-Borgen, Ph.D.; Michelle P. Warren, M.D.

Disclosures

March 01, 2010

In This Article

Prevention and Treatment Recommendations

The discovery of suppressed bone formation and the failure of antiresorptive therapy to fully restore BMD in athletes with functional hypothalamic amenorrhea changed our understanding and recommendations for management of the Triad. Uncoupling of bone turnover with a reduction of bone formation and an increase in bone resorption can cause irreversible reductions in BMD.[35] Suppression of bone formation by moderate restrictions of energy availability also suggests that large numbers of only moderately energy-deficient adolescents without clinical hypoestrogenic menstrual disorders may fail to achieve their genetic potential for peak BMD.

Prevention and treatment of the Triad should employ a team approach including a physician or other health-care provider (physician's assistant or nurse practitioner), a registered dietitian, and for athletes with disordered eating or an eating disorder, a mental-health practitioner.[3,16,148,155,215] Health-care personnel with knowledge of disordered eating behavior and eating disorders in particular sports will be better able to understand the demands of those sports. Additional valuable team members may include a certified athletic trainer, an exercise physiologist, and the athlete's coach, parents and other family members. Barriers to the treatment of eating disorders in the U.S. should be recognized.[167]

Recommendation. Multidisciplinary treatment for the Triad disorders should include a physician (or other health-care professional), a registered dietitian, and, for athletes with disordered eating or an eating disorder, a mental health practitioner. Evidence category C-2.

Prevention

Athletic administrators and the entire health-care team should aim to prevent the Triad through education.[148,155,215] Emphasis should be placed on optimizing energy availability for prevention.[86,122,123] Special attention should also be given to maximizing bone mineral accrual in pediatric and adolescent athletes[103] and to maintaining bone health throughout life.[106] Children, adolescents, and young adults should be counseled on nutritional requirements for their age, including calcium and vitamin D,[88,196] and on the benefits of regular weight-bearing exercise for bone health.[106] Athletes with menstrual disorders and/or low energy availability with or without disordered eating or eating disorders should be educated about the risk of impaired bone mineral accrual, declining BMD, osteoporosis, and stress fractures.

Like other organizations,[4,89] ACSM recommends that national and international governing bodies of sports and athletic organizations put procedures and policies in place to eliminate potentially harmful weight loss practices of female athletes. Procedures and policies are not specified, because best practices may be sport-specific.

Treatment

Nonpharmacological Therapy. Increases in BMD of 5% per year have accompanied increases in body weight in cohort and case studies of amenorrheic athletes.[47,58,118,201,202,218] In anorexia nervosa, increases in BMD of 2-3% per year have been seen with weight gain in most[12,15,24,64,83,87,135] but not all[36,164] studies. Therefore, the first aim of therapy to restore menstrual cycling and increase BMD is to modify diet and exercise behavior to increase energy availability by increasing energy intake, reducing energy expenditure, or a combination[49,108] according to the athlete's compliance with recommendations. Menstrual cycles may be restored by increasing energy availability to more than 30 kcal·kg−1 FFM·d−1,[108] but the strong association between increases in BMD and increases in body weight[47,58,118,201,202,218] implies that increasing BMD may require more than 45 kcal·kg−1 FFM·d−1. This value corresponds to energy balance in healthy young women.[122,123,141] Athletes practicing restrictive eating behaviors should be counseled that increases in body weight may be necessary to increase BMD. More research is needed to determine whether this is true.

Affected athletes should be referred to a dietitian for nutrition counseling and to have their energy availability estimated. Exercise, diet, and low/fluctuating weight should all be discussed. Adequate amounts of bone-building nutrients such as calcium (1000-1300 mg·d−1), vitamin D (400-800 IU·d−1), and vitamin K (60-90 μg·d−1) are needed.[65,88,146,147,194] Supplements for calcium and vitamin D may be necessary. More research is needed to determine if higher intakes of calcium and vitamin D increase BMD and reduce fractures in female athletes with the Triad disorders. Protein needs for female athletes engaged in intense exercise training may also be higher (1.2-1.6 g·kg−1·d−1)[126,188] than those recommended for the population at large (0.8 g·kg−1·d−1).[193] Increased energy availability should continue until menses resume and be maintained while training and competing.

The treatment goal for athletes with disordered eating or eating disorders is to optimize overall nutritional status, normalize eating behavior, modify unhealthy thought processes that maintain the disorder, and treat possible emotional issues that for some athletes create a need for the disorder. Treatment success is based on a trusting relationship between the athlete and the care providers. The younger the athlete, the more the family's involvement is recommended. In addition to nutrition counseling and individual psychotherapy, treatment includes cognitive behavioral, group and family therapy.[6,7,16,19,62,110,167]

An athlete in treatment for disordered eating or eating disorders should meet minimal criteria to continue training and competition. The athlete must agree (i) to comply with all treatment strategies; (ii) to be closely monitored by health-care professionals; (iii) to place precedence on treatment over training and competition; and depending on her medical status (iv) to modify the type, duration, and intensity of training and competition.[16,185] A written contract may be used to specify these agreements. Close follow-up of progress and ongoing communication with the health-care team are essential. If the athlete does not accept treatment, breaks her contract, or her eating behavior and weight do not improve, she may need to be excluded from training and competition, but follow-up should continue.

Recommendations. The first aim of treatment is to increase energy availability by increasing energy intake and/or reducing energy expenditure. Athletes without disordered eating or eating disorders should be referred for nutritional counseling. Evidence category C-1. Athletes practicing restrictive eating behaviors should be counseled that increases in body weight may be necessary to increase BMD. Evidence category C-1. Treatment for disordered eating and eating disorders includes nutritional counseling and individual psychotherapy. Cognitive behavioral, group therapy, and/or family therapy may also be used. Evidence category B. Athletes with disordered eating and eating disorders who do not comply with treatment may need to be restricted from training and competition. Evidence category C-2.

Pharmacological Therapy. Antidepressants are often utilized for bulimia nervosa, anorexia nervosa following weight restoration, ED-NOS, and for concomitant depression and anxiety disorders,[2,7,62,110,167,214] but no pharmaceutical agent approved for use in this population has been shown to fully restore BMD in women with functional hypothalamic amenorrhea. When 93 women diagnosed with functional hypothalamic amenorrhea (without anorexia nervosa) chose between two pharmacological treatments or no treatment, 30% had still not recovered menstrual cycles after 8 yr.[54] There was no benefit from hormone replacement therapy (HRT) and the oral contraceptive pill (OCP) delayed and reduced the likelihood of restoring menstrual cycles. No woman recovered whose body mass index (BMI) declined, but all those whose BMI increased did recover (54).

Bone mineral density increased by less than 4% per year in two cohort studies of women with functional hypothalamic amenorrhea who were treated with HRT,[38,69] but not in a third.[202] In a cohort study of anorexia nervosa patients, adjustment for weight gain cancelled out apparent effects of HRT.[64] Evidence of the effectiveness of OCP for increasing BMD in athletes and other women with functional hypothalamic amenorrhea without eating disorders is also mixed,[119] with some randomized clinical trials and cohort studies finding partial recovery[32,40,69,71,76,163,205] and others not,[61,66] but concurrent changes in body weight were often not reported. One study reported that the increase in BMD was accompanied by an increase in weight[163] and another reported that the effect of weight gain exceeded the effect of OCP.[69] Neither HRT nor OCP has increased BMD in any prospective study of women with anorexia nervosa.[63,64,68,105,109,142,180]

It must be emphasized that pharmacological restoration of regular menstrual cycles with OCP will not normalize metabolic factors that impair bone formation, health and performance. Thus it is unlikely to fully reverse the low BMD in this population.[39,138,202] Bone mineral density should be monitored annually in women with persistent functional hypothalamic amenorrhea, disordered eating, and/or low BMD. If BMD declines in an athlete greater than 16 yr of age with persistent functional hypothalamic amenorrhea despite adequate nutritional intake and weight, then OCP may be considered with the hope of minimizing further bone loss. There are no established guidelines as to when or if to administer OCP to the adolescent athlete less than 16 yr of age with functional hypothalamic amenorrhea,[3] due to concern about premature closure of growth plates and lack of research to support this therapy in this age group.

Bisphosphonates approved for the treatment of postmenopausal osteoporosis should not be used in the young athlete with functional hypothalamic amenorrhea for two reasons. The first is because of their unproven efficacy in women of child-bearing age.[134] The second reason is that the bisphosphonates may reside in a woman's bone for many years, potentially causing harm to a developing fetus during pregnancy.[156]

If a further aim of therapy is to restore fertility in the athlete who wishes to become pregnant, induction of ovulation with agents such as clomiphene citrate and exogenous gonadotropins is indicated, although the athlete should be warned about the risks and hazards of having a low birth weight infant when an undernourished mother does not reform her dietary habits.[192]

Clearly, more research is needed to resolve whether any currently approved or new form of hormone therapy is effective for increasing BMD in athletes with functional hypothalamic amenorrhea. In this research, BMD and other factors should be monitored carefully to distinguish pharmacological and nonpharmacological effects. Research is also needed on other types of pharmacologic therapies. Pending further research, increased energy availability and restoration of gonadal function are the cornerstones of treatment for the Triad.

Evidence Statement. In functional hypothalamic amenorrhea, increases in BMD are more closely associated with increases in weight than with OCP/HRT administration. Evidence category C-1. OCP should be considered in an athlete with functional hypothalamic amenorrhea over age 16, if BMD is decreasing with nonpharmacological management, despite adequate nutrition and body weight. Evidence category C-2.

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