Continuing Education Activity

Female athletes often complain of low energy availability, which is defined as energy from oral nutrition less energy used for exercise. As such, low energy may result (whether intentionally or unintentionally) from more energy expenditure, less oral nourishment, or both. A chronic energy deficit can occur in the female athlete with musculoskeletal and reproductive dysfunction. Low energy (with or without an eating disorder) in combination with a menstrual disorder and altered mineral bone density is known as the female athlete triad. This activity reviews the pathophysiology and presentation of the female athlete triad and highlights the role of the interprofessional team in its management.

Objectives:

• Describe the pathophysiology of female athlete triad.
• Review the work up of a female athlete triad.
• Summarize the treatment of a female athlete triad.
• Outline the importance of improving care coordination among interprofessional team members to improve outcomes for patients affected by female athlete triad.

Introduction

Female athletes often complain of low energy availability, which is defined as energy from oral nutrition less energy used for exercise. As such, low energy may result (whether intentionally or unintentionally) from more energy expenditure, less oral nourishment, or both. A chronic energy deficit can occur in the female athlete with musculoskeletal and reproductive dysfunction. Low energy (with or without an eating disorder) in combination with a menstrual disorder and altered mineral bone density is known as the female athlete triad. Early identification of low energy in the female athlete and thorough understanding of the syndrome and its progression is important to prevent short- and long-term consequences.[1][2][3][4]

Etiology

The limiting factor for performance during training and competition in high-intensity sports of long duration is energy intake. A substantial percentage of energy intake is provided through carbohydrates, and to a lesser extent, proteins and fats. To maintain optimal energy availability, increased energy expenditure should ideally justify increased nutritional intake. However, this is not always the case.  Many female athletes, either deliberately or inadvertently, fail to maintain adequate energy intake. There exists a direct correlation between carbohydrate availability and reproductive and skeletal health.[5][6][7]

Epidemiology

Female athletes in any sport, regardless of competition level, can potentially develop the triad. However, females participating in endurance sports such as track and field, swimming, and rowing or those requiring subjective judging like gymnastics and figure skating are most at risk.[8][9]

When females intentionally create this energy deficit, it is described as an eating disorder. Females athletes are 5 to 10 times more likely than male athletes to have an eating disorder. The prevalence of clinical eating disorders, such as anorexia nervosa or bulimia nervosa, among female elite athletes ranges from 16% to 47%. A substantial percentage of females with eating disorders also have a concomitant personality disorder, substance abuse disorder, or obsessive-compulsive disorder, and the rates of suicide are greater for these women than for healthy females of the same age.

Pathophysiology

Low Energy Availability

Energy availability the energy acquired through oral nutrition less the energy expended during exercise and baseline daily metabolic requirements. Energy availability, whether through increased expenditure or decreased oral intake, is the main factor in the triad. Disordered eating may be intentional or unintentional. Eating disorders such as anorexia nervosa or bulimia nervosa are intentional causes.  However, many female athletes without the diagnosis of an eating disorder may exhibit disordered eating habits. Most of the time, this will occur unknowingly, and the athlete will not take in enough energy. The extensive continuum of disordered eating ranges from healthy dieting to fasting, skipping meals, using diet pills or laxatives, and binging and purging A direct correlation exists between carbohydrate availability and reproductive and skeletal health. Low energy availability secondary to disordered eating results in menstrual dysfunction and low mineral density.

Altered Bone Mineral Density

Bone tissue is dynamic and constantly being remodeled by osteoclasts (which resorb old bone) and osteoblasts (which form new bone). This is done under the control of polypeptides, steroid hormones, thyroid hormones, cytokines, and growth factors. Secondary to hypothalamic dysfunction, female athletes function at a low estrogen state.  Estrogen's principal role in bone is to directly act on osteoblasts, and it has an indirect effect on osteoclasts to prevent bone resorption Athletes should have a 5% to 15% higher bone mineral density than age-matched nonathlete. Altered bone mineral density will increase bone fragility and increase the risk of fractures. The incidence of stress fractures is greater in amenorrheic athletes, and bone density has been shown to negatively correlate with the number of missed menstrual cycles since menarche.

Menstrual Dysfunction (amenorrhea or oligomenorrhea)

Menstrual abnormalities result from altered hypothalamic function. Menstrual dysfunction in the female athlete directly correlates to decreased estrogen. It may be primary or secondary amenorrhea. Primary amenorrhea is defined as no menstruation by 14 years of age without the development of secondary sexual characteristics or by 16 years, even if the female has undergone other normal changes that occur during puberty. The persistent absence of menstrual cycles beginning sometime after menarche is called secondary amenorrhea. 

History and Physical

All female athletes need a thorough history in addition to the routine history, with a focus on the components of the athlete's nutritional, musculoskeletal, menstrual, endocrine/metabolic, psychosocial, performance, and medication history.

• Nutritional history - Nutritional intake and eating patterns, quantity of protein, carbohydrate, vitamins, and minerals consumed.
• Menstrual history - The age at menarche, average length of menses, average time between menstrual periods, menstrual changes with increased training, and number of cycles annually. Pregnancy should be excluded in the case of amenorrhea.
• Endocrine/metabolic history - Any personal and family history of thyroid disorders, pituitary disorders, and diabetes should be sought. Obtain signs and symptoms of polycystic ovarian syndrome,
• Psychosocial history - Discuss eating patterns. The Eating Disorder Inventory (EDI) may be used. Document any alcohol, tobacco, or drug use.  Ask about social support, depression, anxiety, and any history of physical, emotional, or sexual abuse.
• Performance history - Ask about changes in strength or performance.
• Medication history - Review all medications, dietary supplements, and herbal agents. Obtain information about oral contraceptives separately as patients often do not consider this a medication. Ask about any anabolic steroid use. Determine if the patient uses emetics, diet pills, stool softeners, or laxatives.  

The physical examination should screen for pathologies that could cause metabolic and hormonal abnormalities. Thyroid should be palpated for evidence of enlargement or irregularity. Pay particular attention to the teeth, noting tooth decay from repeated vomiting and subsequent hard brushing, and parotid glands for evidence of hypertrophy, as with bulimia nervosa. Perform visual field testing to assess for pituitary macroadenoma; if large enough, it may press on the optic chiasm and cause bitemporal non-homonomous hemianopsia. A thorough skin exam should also be performed.  

A pelvic examination should be performed when appropriate, particularly when a patient presents with delayed or disordered menarche.

Evaluation

Laboratory testing

A trainer or team physician should conduct a baseline urinary acetoacetate measurement. Normally menstruating athletes can self-measure or have a trainer perform monthly measurements of urinary acetoacetate in times of increased training. The goal is to completely remove urinary ketones before and after a meal as well as before and after training.

• B-HCG can be performed in the presence of amenorrhea to rule out pregnancy
• A complete metabolic panel to assess electrolyte levels, renal function, and hepatic function and a complete blood cell (CBC) count to evaluate for anemia
• A thyroid panel to assess for thyroid dysfunction
• Secondary lab tests involve testosterone (free and bound), luteinizing hormone, follicle  stimulating hormone, estradiol, and prolactin levels

Imaging

Pelvic Ultrasound can be useful for determining the etiology of primary amenorrhea (eg, the presence of ovaries, uterus). If an abnormal pituitary function is suspected, thin-section magnetic resonance imaging (MRI) of the head through the sella turcica should be performed. Electrocardiography may show bradycardia, which is common in athletes, and a resting heart rate of fewer than 50 beats per minute should be explored with a baseline ECG.

If evidence from the patient's history or physical examination suggests the presence of a stress fracture, plain radiography should be the initial test of choice. A 3-phase bone scan should be performed if the radiographs are negative. Dual radiograph absorptiometry can be used in athletes with multiple stress fractures.

A dual-energy x-ray absorptiometry scan can also be used to assess for osteopenia or osteoporosis.

Treatment / Management

Initial treatment involves correction of the underlying cause. Most of the time this is a low energy state whether through an increased caloric intake, decreased physical activity, or both. Consulting a nutritionist or sports dietician is important.[10][11][12][13]

For menstrual dysfunction, the female athlete should be referred to an OB/GYN who can evaluate and treat the patient. Treatments for menstrual dysfunction in the female athlete are initially limited to hormone replacement therapy with cyclic estrogen and progesterone.

Female athletes with osteopenia or osteoporosis may be treated with oral vitamin D and calcium or bisphosphonates depending on the severity of the bone mineral density loss and risk factors for fractures.  

Those females diagnosed with a mental health disorder such as depression, anxiety, or an eating disorder should be referred to a psychiatrist and/or psychologist for evaluation and treatment.  

Differential Diagnosis

• Androgen excess

• Drug interactions

• Depression

• Hypogonadotropic hypoestrogenism

• Hypothalamic disorders

• Hyperthyroidism

• Hypothyroidism

• Luteal phase inadequacy

• Nutritional deficiencies

• Ovarian defect

• Ovarian insufficiency

• Pituitary disorders

Enhancing Healthcare Team Outcomes

A 2014 consensus statement published in the British Journal of Sports Medicine stated that successful treatment of athletes and exercising women is contingent on an interprofessional approach for recovery from the triad, including a primary care and/or sports medicine physician, a sports dietitian, and a mental health nurse/practitioner. These patients have multiple organ dysfunction and yet at the same time remain noncompliant with therapy. The treatment is often prolonged and these patients need long term monitoring including bone density. The outcomes of these patients is guarded; despite mental health counseling, relapses are common. [2][14][15] (Level V)