The Female Athlete Triad/Relative Energy Deficiency in Sports


The female athlete triad (triad) is a medical condition often observed in physically active girls and women. The three interrelated components of the triad are energy availability (EA), menstrual status, and bone health. These components each present along a physiologic spectrum: EA ranges from optimal to low EA to eating disorder (ED), menstrual function ranges from eumenorrhea to oligomenorrhea to amenorrhea, and bone health ranges from normal to low bone mineral density (BMD) to osteoporosis. ,

Optimum health in the female athlete is indicated by optimal EA, eumenorrhea, and optimal bone health, whereas at the other end of the spectrum, the most severe presentation of the triad is characterized by low EA with or without disordered eating/eating disorder (DE/ED), functional hypothalamic amenorrhea (FHA), and osteoporosis. An athlete's condition moves along each spectrum at different rates depending on her diet and exercise behaviors. The relationships among these three components are illustrated in Fig. 25.1 .

Fig. 25.1, Female athlete triad. The spectrums of energy availability, menstrual function, and bone mineral density (BMD) along which female athletes are distributed ( narrow arrows ). An athlete's condition moves along each spectrum at a different rate, in one direction or the other, according to her diet and exercise habits. Energy availability, defined as dietary energy intake minus exercise energy expenditure, affects BMD both directly via metabolic hormones and indirectly via effects on menstrual function and thereby estrogen levels ( thick arrows ).

Relative energy deficiency in sports (RED-S) is a broader, more comprehensive term used more recently in the literature defining a syndrome that occurs in both female and male athletes ( Fig. 25.2 ). Low EA may lead to altered reproductive hormones (including menstrual dysfunction in the female) and/or low BMD, as well as abnormalities in other systems (e.g., metabolic, cardiovascular, gastrointestinal, immunologic), that may have both health and performance consequences. , For the purposes of this chapter, we will focus on the specific causes and consequences of the triad on the female athlete.

Fig. 25.2, (A) Health consequences of relative energy deficiency in sports (RED-S) showing an expanded concept of the female athlete triad. (B) Potential performance (aerobic and anaerobic) consequences of RED-S.

In the 2017 Consensus Statement, Female Athlete Issues for the Team Physician, it was noted that it is essential for the team physician to recognize that the components of the triad are interrelated and emphasized the comprehensiveness of evaluating female athletes who may fall into this category. Team physicians should coordinate a multidisciplinary healthcare team to address the medical, nutritional, psychologic, and sports-participation-related issues and develop a return-to-play protocol.

Low Energy Availability in the Female Athlete

What is Low Energy Availability?

EA has been defined as the dietary energy intake (measured in kilocalories) minus the energy cost of exercise (measured in kilocalories) relative to fat-free mass (FFM, measured in kilograms). For an athlete, this value is the amount of energy remaining for physiologic processes and activities of daily living after accounting for exercise training. Failure to balance energy intake and exercise energy expenditure will result in a negative energy balance.

This energy deficiency, known as low EA, occurs when an athlete has insufficient energy to support normal physiologic functions. Low EA is defined as <30 kcal/kg FFM per day and negative implications begin to arise below this value. Low EA predisposes athletes to possible physical injury, systemic pathology, psychologic stress, and poor athletic performance. Optimal EA is >45 kcal/kg FFM per day. , , Low EA occurs with a reduction in energy intake and/or an increased exercise load. Consequences of various levels of EA are delineated in Table 25.1 .

Table 25.1
Loucks' Proposed Energy Availability Ranges for Different Athletic Functions.
Adapted from Loucks .
Energy Availability Range Effect on Body Mass/Composition
>45 kcal/kg FFM/day
(>188 kJ/kg FFM/day)
Gain of body mass, muscle hypertrophy, carbohydrate loading
∼45 kcal/kg FFM/day
(188 kJ/kg FFM/day)
Maintenance of body size and mass; focus on skill development
30–45 kcal/kg FFM/day
(125–188 kJ/kg FFM/day)
Loss of body mass or fat
FFM , fat-free mass.

Female athletes are particularly susceptible to inadequate EA due to lack of nutritional education, higher prevalence of DE/ED, and prioritizing leanness more often in women's sports, even those with male equivalents (gymnastics, figure skating, ballet, beach volleyball). Genetics and age may alter an individual's initial condition and sensitivity to low EA, and therefore a high index of suspicion is necessary when evaluating female athletes. Importantly, it has been demonstrated that low EA, not the stress of exercise, will have negative implications on many hormonal, metabolic, and functional mechanisms. , ,

Low EA is prevalent across a variety of sports, not only those that encourage leanness. A study of female high-school varsity athletes participating in a range of sports found that 36% presented with low EA, with 6% at <30 kcal/kg lean body mass (LBM). A study of female Division 1 soccer players over the course of a season revealed mean EA was lowest midseason, with 33.3% of athletes demonstrating low EA at <30 kcal/kg LBM. Young female athletes, especially those participating in aesthetic or weight-restrictive sports, are often at risk.

Low Energy Availability and Disordered Eating

There are three main mechanisms by which athletes commonly reduce EA. First, by intentionally modifying body size and composition for performance. These methods, which include skipping meals, fasting, using diet pills, using laxatives, or self-induced vomiting, may be used for sport-specific short-term weight loss or may illustrate a long-term pattern of behavior. The tactics may be short-term diets or long-term patterns of behavior. Although these restrictive eating behaviors are considered DE, they do not involve any psychopathologic underpinnings.

In contrast, compulsively acting in a psychopathologic pattern of DE may indicate a clinical ED. EDs are classified by the Diagnostic and Statistical Manual of Mental Disorders (Fifth Edition) ( DSM-5 ) as psychiatric disorders often including a distortion of body image and often resulting in significant nutritional and medical complications. These include anorexia nervosa, bulimia nervosa, binge ED, or other specified EDs. Anorexia athletica refers to a DE pattern often observed in the female athlete who has an intense fear of gaining weight, despite being underweight. She reduces energy intake and body mass despite high physical performance. , Anorexia athletica has some, but not all, of the criteria of EDs, so it is considered a DE or a subclinical ED.

Third and finally, low EA may occur inadvertently, due to lack of knowledge about appropriate nutrition and the lack of biological drive to match energy intake to activity-induced energy expenditure. While DE very commonly underpins cases of low EA, , an athlete may in fact unknowingly fail to attain her energy requirements after a sudden increase in exercise commitment, because of time restraint, or due to lack of nutritional knowledge. , The athlete may lack the appetite necessary to ensure proper dietary energy intake to compensate for the energy expenditure of intense exercise.

Athletes participating in sports involving aesthetics, endurance, and weight classifications (i.e., gymnastics, ballet, figure skating, lightweight rowing, running) are at a particularly high risk for DE/ED and therefore low EA ( Table 25.2 ). In these high-risk sports, a greater percentage of female athletes demonstrated clinical EDs compared with athletes in other sports and nonathletic controls. The prevalence of EDs is also higher in female athletes of all sports as compared with their male counterparts. The risk factors associated with DE behavior that may put any individual, athlete or not, at risk include psychologic factors such as low self-esteem, perfectionism, and body image dissatisfaction and sociocultural factors such as peer pressure, media influence, family influence, or bullying. History of physical or sexual abuse may also be a contributing factor. Additionally, athlete- or sport-specific risk factors for DE may include frequent weight regulation, external pressure, lack of nutritional knowledge and energy requirements, traveling, lack of time, overtraining, injuries, and coaching behavior.

Table 25.2
High-Risk Stress Fractures: Characteristics and Initial Treatment.
Site Stress Fractures (%) Common Sports Initial Treatment
Femoral neck <5% Running, endurance athletes Compression-side: NWB × 4–6 week
Tension-side: surgical referral
Displaced: urgent surgical referral
Patella <1% Running, basketball, gymnastics Low grade a : activity restriction, WB as tolerated
High grade a : NWB, knee extension brace immobilization × 4–6 week
Displaced: surgical referral
Anterior tibia 0.8%–7% Basketball, gymnastics NWB × 6–8 week b
Surgical referral if poor healing at 3–6 months
Medial malleolus 0.6%–4.1% Running, track and field, basketball, gymnastics NWB and cast immobilization × 4–8 week b
Displaced: Surgical referral
Talus Running, pole vaulting, basketball, gymnastics NWB × 6 week with or without cast immobilization
Navicular 14%–25% Track and field, football, basketball Type 1: NWB and cast immobilization ≥6 week b
Type 2 or 3: surgical referral
Proximal fifth metatarsal <1% Soccer, basketball, football Low grade a : NWB and immobilization × 6 week
High grade (types 1–3) a : surgical referral
Sesamoid Dance, gymnastics, racquet sports, basketball, soccer, volleyball, running, sprinting NWB and immobilization × 6 week; orthotics
Surgical referral if poor healing at 3–6 months
NWB , non-weight-bearing; WB , weight-bearing.

a Low grade, stress reaction; high grade, fracture line.

b Early surgical intervention considered; may allow quicker return to play but further research is needed.

DE, clinical EDs, anorexia athletica, and inadvertent low energy intake will all affect the EA of an athlete. Understanding the cause of an individual athlete's low EA will allow the sports medicine team to generate a more effective treatment plan.

Physiologic Consequences of Low Energy Availability

Nearly every system of the human body may be affected by low EA. The nutritional deficiencies and electrolyte imbalances have implications on reproductive function, bone health, immune function, gastrointestinal problems (e.g., dental, gingival, bleeding, ulceration, bloating, constipation), cardiovascular abnormalities (e.g., arrhythmias, heart block, endothelial dysfunction), renal dysfunction (e.g., urinary incontinence), and psychiatric concerns (e.g., depression, anxiety, suicide). Comorbid EDs pose even greater health risks: EDs have one of the highest mortality rates of any mental health condition , most often caused by suicide or cardiac arrhythmia. ,

Athletic performance may suffer before the severe consequences of low EA are manifested. The loss of fat and LBM, electrolyte imbalances, and dehydration contribute to poor sport performance and increased risk of musculoskeletal injury. , The effects of low EA on the menstrual cycle and BMD are a specific concern in the female athlete.

Treatment of Low Energy Availability

The primary goal of treatment for any component of the triad is to increase EA. This may be accomplished by modifying the athlete's diet and exercise regimen to reduce energy expenditure and/or maximize energy intake. In order to remain at or above an EA level of 30 kcal/kg FFM per day, nutritional intake must be optimized. This is best accomplished by an interdisciplinary team including a sports medicine physician, dietitian, or nutritionist and possibly a mental health professional. Additionally, it is imperative to ensure the athlete has social support throughout the process, including coaches, athletic trainers, and family members.

Recovery of energy status may result in restimulation of anabolic hormones and bone formation, as well as reversal of energy conservation adaptations. This may be achieved in days or weeks. Fig. 25.3 depicts the various short-term and long-term consequences that may result from low EA. For many athletes with DE behavior, providing healthy nutritional information and monitoring behavior is sufficient. With cases of clinical EDs, however, psychotherapy may be necessary.

Fig. 25.3, Treatment of the triad. The recovery of the three components of the triad occurs at different rates with appropriate treatment. Recovery of energy status is observed typically after days or weeks of increased energy intake and/or decreased energy expenditure. Recovery of menstrual status is observed typically after months of increased energy intake and/or decreased energy expenditure, which improves energy status. Recovery of bone mineral density may not be observed until years after recovery of energy status and until menstrual status has been achieved. IGF-1 , insulinlike growth factor 1.

Primary prevention and early identification should be the highest priority of sports medicine teams. Screening for risk factors of DE behaviors may be performed at preparticipation physical examinations. Several nutritional assessments have been developed and validated for screening of EDs specifically for female athletes. Additionally, the Female Athlete Triad Consensus Panel Cumulative Risk Assessment tool provides an objective method of determining an athlete's risk using risk stratification and evidence-based risk factors. Beyond early screening, promoting healthy body image, providing nutritional information, dispelling misconceptions about body weight and composition relating to athletic performance, and discussing healthy weight control are important primary interventions that we can use with our athletes.

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