Female Athletic Triad

Summary

Key Points

• The female athlete triad is a metabolic injury. It includes an imbalance between input and output, which can be intentional or inadvertent
• The goal is to restore the balance between energy intake and energy expenditure by increasing energy in and/or decreasing exercise energy expenditure
• Prevention and early recognition of the triad are key

Basic Information

Background Information

• The female athlete triad (triad) is an intertwined relationship between EA (energy availability), bone health, and menstrual dysfunction that can be observed in physically active girls and women
• The ACSM (American College of Sports Medicine) initially defined the triad in 1992, and in 1997 the first position statement was published by the ACSM¹. In 2007, an updated position statement was released, and in 2014, the Female Athlete Triad Coalition released a consensus statement on treatment and return to play²³⁴
• The triad is a severe injury that has both short-term and long-term impacts on individual health
• Prevention and early recognition should be the cornerstones of management
• Although awareness of the triad has increased since the first position statement in 1997, no standardized clearance or return to play guidelines exist

Epidemiology

• Although the triad is typically believed to affect competitive athletes, it can have an impact on athletes at all experience levels, from recreational to the elite
• The triad is a spectrum of diseases, therefore making determining exact prevalence difficult.⁵⁶⁷ Gibbs et al⁶ performed a systemic review of 65 studies in exercising women to identify prevalence estimates of the triad
  • There is a paucity of literature regarding all 3 of the components of the triad and, in this systemic review, only 9 studies reported the prevalence of all 3 components, with a range of 0% to 15.9%
  • The majority of the existing research looks at each individual component of the triad (menstrual dysfunction, disordered eating, and low bone mineral density [BMD])
  • The study found the prevalence of any 1 component of the triad 1 to be 6% to 60% and any 2 components 2.7% to 27%⁷
  • Gibbs et al⁶ also examined the prevalence of all 3 triad components in lean sport versus nonlean sport athletes. As expected, the prevalence of all 3 components as well as each individual component was higher in lean sport athletes compared with nonlean sport athletes

Etiology and Risk Factors

Risk Factors

• Any girl or woman involved in exercise, organized or not, is at increased risk for the triad
• Sports and activities that emphasize leanness, aesthetics, and/or endurance place girls and women at greatest increased risk²⁶
  • Commonly implicated activities include swimming, diving, running, dancing, gymnastics, cheerleading, rowing, and wrestling
• Risk factors for low EA include restriction of dietary energy intake, prolonged periods of exercise, vegetarians, and those who limit the types of food they consume
• Risk factors for stress fractures include low BMD, menstrual dysfunction, dietary deficiencies, training errors, biomechanical abnormalities, and genetic predisposition²⁸

Risk Models and Risk Scores

• The 2014 Triad consensus statement recommends a risk stratification approach that optimizes the athlete’s health while minimizing the risk of injury and illness
  • They developed a risk stratification protocol for care of the triad athlete, including a worksheet to aid physicians and the entire care team in the risk assessment³
• Once the risk score is calculated, clearance recommendations ranging from full clearance to restriction from all activities can be determined
• Athletes in moderate-risk and high-risk categories should be placed under a written contract with goals and parameters that must be met prior to return to activity³

Diagnosis

Approach to Diagnosis

• The work-up and evaluation of an athlete who has signs and symptoms of the triad include laboratory testing, cardiac work-up, and imaging
• Female athletes presenting with menstrual dysfunction, disordered eating, eating disorders, or other risk factors for the triad should undergo laboratory testing to evaluate for an underlying etiology, such as thyroid disease, or complications, such as electrolyte disturbances. A more extensive laboratory evaluation may be indicated depending on the clinical features of each case
• An electrocardiogram is recommended in athletes with suspected triad because metabolic dysregulation can increase an athlete’s risk for cardiac arrhythmias

Diagnostic Criteria

• The definition of the triad has evolved over time. The classic terminology included disordered eating, amenorrhea, and osteoporosis. It is now described as a metabolic injury that can be observed in physically active girls and women. The most recent definition contains the following parameters²³⁴:
  • Low EA with or without disordered eating
  • Menstrual dysfunction
  • Low BMD (bone mineral density)
• The components of the triad exist on a continuum. It is not uncommon for an individual initially to have only 1 or 2 of the components, at which time she may be referred to as having pretriad, and it is critical to intervene to prevent progression
• In 2014, the International Olympic Committee introduced a new phrase to describe the concept of energy imbalance, which is called relative energy deficiency of sports, which refers to a syndrome of impaired physiologic function instead of a triad
  • The relative energy deficiency results in impaired functions within the realms of metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health
  • It broadens the definition to include both boys and men and girls and women⁹
• Low EA (energy availability)
  • Some athletes decrease EA by restricting intake whereas others expend more energy
  • This imbalance is not always intentional. Athletes progressing to a higher level of demand can inadvertently get into a negative energy balance due to increased energy expenditure without realizing the need for additional intake²³⁴
  • Low EA is obvious when there is a BMI (body mass index) less than 17.5 kg/m² or less than 85% of expected body weight in adolescents
  • When overt signs of low EA are absent, determining the EA is more complex but can be calculated as energy intake (kcal) minus exercise energy expenditure (kcal) divided by fat-free mass (kg)
  • Estimates of exercise energy expenditure are subject to bias because they are largely a self-reported measure. Recruiting the help of an experienced dietician can be useful in calculating these assessments
  • Low EA is defined as less than 30 kcal/kg of fat-free mass per day and below this value is where negative implications, such as menstrual dysfunction and bone health issues, begin to arise
  • Optimal EA is greater than 45 kcal/kg of fat-free mass per day^2341011
• Menstrual dysfunction
  • Menstrual irregularities exist on a spectrum from eumenorrhea to functional hypothalamic amenorrhea
  • Girls and women presenting with amenorrhea, either primary or secondary, warrant investigation for an underlying etiology because functional hypothalamic amenorrhea is a diagnosis of exclusion²³⁴
  • Menstrual irregularities often can be one of the first clues that a female athlete is in an energy crisis
  • Return of normal menses can take more than 1 year after improvement of the EA¹¹
• Low BMD
  • The ACSM (American College of Sports Medicine) as well as the International Society of Clinical Densitometry have published definitions for low BMD and osteoporosis in children, adolescents, and premenopausal women. The z score is used in the interpretation, not the T score that is traditionally used in postmenopausal women
  • The ACSM defines low BMD as a z score that is less than -1.0 in female athletes in weight-bearing sports instead of less than or equal to -2.0 as defined by the International Society of Clinical Densitometry because they expect bone mass should be higher in these athletes. Therefore, a BMD z score between -1.0 and -2.0 warrants further evaluation and attention^2561213

Workup

Physical Examination

• Physical examination of many athletes with the triad is often normal or may only demonstrate low BMI (body mass index) or bradycardia
  • Relying on the vital signs of an athlete as a means of risk stratification can be difficult because many athletes have a lower resting heart rate and bradycardia is common
  • In extreme cases, however, the examination may demonstrate abnormalities

Laboratory Tests

• Not all studies have recommended testing leptin in the initial evaluation; however, it is suggested by several centers that treat athletes with severe eating disorders, including the McCallum Place, St. Louis, Missouri
  • Leptin is an adipocyte-secreted hormone that plays a key part in energy homoeostasis
    • Advances in leptin physiology have established that the key role of this hormone is to signal EA (energy availability) in energy-deficient states
    • Studies in animals and humans have shown that low concentrations of leptin are partly if not fully responsible for starvation-induced changes in neuroendocrine axes, including low reproductive, thyroid, and insulin-like growth factor hormones
    • Disease states, such as exercise-induced hypothalamic amenorrhea and anorexia nervosa, are also associated with low concentrations of leptin and a similar spectrum of neuroendocrine abnormalities¹⁵
  • Having a baseline level of leptin at the initiation of treatment can be helpful to determine the extent of malnutrition. Following this level longitudinally can be useful for the athlete as well as the care team to demonstrate overall improvement and response to treatment

Imaging Studies

• DXA (dual-energy x-ray absorptiometry) is the gold standard to measure BMD (bone mineral density). The 2014 Female Athlete Triad Coalition consensus statement divides those that should get DXA scans into 3 categories, namely:
  • Those considered at high risk
  • Those considered at moderate risk
  • Those with a history of previous fracture³
• Although DXA, a 2-D assessment of a 3-D structure, is the gold standard for evaluation of BMD, newer technology that provides a 3-D evaluation is available, however not as readily accessible
• Axial quantitative CT scan and peripheral quantitative CT scan can measure bone geometry, bone mass, and volumetric BMD specific to trabecular and cortical bone. Early studies are promising that this imaging provides a more accurate reflection of the bone health in triad and pretriad individuals

Treatment

Approach to Treatment

• Treatment of the triad requires a multidisciplinary approach
• Key components of treatment include modification of diet as well as exercise behaviors to increase EA (energy availability) and restore a positive energy balance⁷
• No medication (or pharmacologic therapy) has been shown consistently effective in treatment of the triad
• The Triad Consensus Panel recommends pharmacologic options be considered if there is lack of response to nonpharmacologic treatments for at least 1 year or if new fractures develop during nonpharmacologic management

Nondrug and Supportive Care

• Restoring energy balance is critical and can be done by increasing intake or decreasing output. Translating that into clinical practice can be challenging
• A dietician with training and interest in sports nutrition is crucial to helping the athlete overcome the negative energy balance
  • Nutritional education, counseling, and monitoring are sometimes all that is required to reverse the energy deficiency, especially when the energy imbalance was inadvertent¹⁰
• A study published in the Clinical Journal of Sports Medicine in 2014 found that dancers with disordered eating displayed lower levels of nutritional knowledge, and this was believed to have an impact on BMI (body mass index)¹⁷. This finding emphasized the necessity of educating athletes on the importance of adequate nutrition
• Replacing cardiovascular training with weight and resistive training is recommended by the American Physical Therapy Association to reduce energy expenditure and increase BMD (bone mineral density)
  • Introducing a new form of exercise results in skeletal adaptations due to new loading patterns that ultimately are beneficial for bone strength¹¹
  • Plyometrics also can be beneficial, however should be avoided when recovering from a stress fracture

Drug Therapy

• In the past, oral contraceptive pills were frequently prescribed to restore normal menses
  • Research regarding oral contraceptive pills has had contradictory outcomes, with some studies showing a benefit to bone health, others showing a decrease in BMD, and some no change⁷¹¹
  • This approach also does not address the multitude of other hormonal factors that likely contribute to the underlying physiologic dysregulation/disturbance⁷
  • Initiating oral contraceptive pills also results in the loss of the natural marker for when a girl or woman regains optimal energy balance
• Bisphosphonate therapy in young women with the triad should be executed only by or in consultation with a board-certified endocrinologist or specialist in metabolic bone diseases, and this is done on a case-by-case basis if all nonpharmacologic treatments have failed
  • Bisphosphonates are commonly used in postmenopausal women for the treatment of osteoporosis because they reduce bone turnover
  • Limited evidence regarding use of bisphosphonates in premenopausal women exists and the studies that have been done are conflicting
  • Another barrier to use of bisphosphonates in this age group is that long-term effects of bisphosphonates are unknown and, due to their long half-life, they have potential teratogenic effects on a developing fetus¹¹
• It must be emphasized that the aforementioned pharmacologic therapies are not currently approved by the Food and Drug Administration for increasing BMD or for fracture reduction in young or adult athletes³
• Calcium-rich foods and vitamin D intake should be encouraged and optimized. There is no consensus as to the optimal calcium dosage; however, the ACSM (American College of Sports Medicine (ACSM) recommends between 1000 mg/d and 1300 mg/d of calcium and at least 600 IU/d of vitamin D³¹¹¹⁸
  • Recombinant leptin as well as insulin-like growth factor I are potential treatments for individuals with amenorrhea and anorexia nervosa as well as functional hypothalamic amenorrhea A limiting factor in the use of leptin is a potential side effect of weight loss⁷¹¹

Follow-up

Referral

• Cases of disordered eating or eating disorders require professional mental health evaluation and management by health care providers with an expertise in eating disorders
  • These providers need to have an appreciation for the mental as well as physical demands of an individual’s sport¹⁰
  • Athletes suffering from acute anorexia nervosa often have associated depression, rigidity, weight phobia, and a preoccupation with thoughts related to food and eating¹⁹
    • These associated thoughts make treatment difficult, and placing the athlete on a written contract is often necessary to ensure that they follow the treatment guidelines determined by the care team
    • The written contract provides accountability for the athlete to attend therapy sessions, office visits, and weigh-ins
    • The contract is often specific to the particular athlete and can vary based on the severity of the case
• Cognitive behavioral therapy is also an effective psychotherapy for eating disorders

Screening and Prevention

Screening

• Few data exist regarding the effectiveness of screening; however, early detection of athletes at risk for the triad is critical²⁰. It is currently recommended to screen female athletes during the preparticipation or annual health examination
• Furthermore, when girls and women present for evaluation of related issues, such as fatigue, declining performance, recurrent injury, or illnesses, triad components should be inquired about
• Screening can be done with a triad-specific questionnaire, such as the Triad Consensus Panel Screening Questionnaire, published in British Journal of Sports Medicine and Current Sports Medicine Report in 2014, as follows²³⁴¹⁶:
  • Have you ever had a menstrual period?
  • How old were you when you had your first period?
  • When was your most recent menstrual period?
  • How many periods have you had in the past 12 months?
  • Are you presently taking any female hormones (estrogen, progesterone, or birth control pills)?
  • Do you worry about your weight?
  • Are you trying to or has anyone recommended that you gain or lose weight?
  • Are you on a special diet or do you avoid certain types of foods or food groups?
  • Have you ever had an eating disorder?
  • Have you ever had a stress fracture?
  • Have you ever been told you have low bone density (osteopenia or osteoporosis)?
• Screening should occur at both the high school and collegiate levels. Identification of any 1 of the components of the triad should prompt further investigation for the other components²³⁴¹⁶

Prevention

• Prevention of the triad is key and this starts with increased awareness. The entire health care team, athletic administrators, coaches, and parents as well as athletes should have education regarding identification of risk factors for the triad as well as the 3 components of the triad
• Knowing and understanding the components of the triad are critical to being able to recognize it early as well as implanting measures to prevent its occurrence
• When a risk factor and/or component of the triad is identified, providers are obligated to initiate further evaluation to limit progression and future metabolic insult

References

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