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 .
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.
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 .
|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|
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.
|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
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.
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.
Menstrual Dysfunction in the Female Athlete
The Menstrual Cycle
The menstrual cycle is a complex, coordinated sequence of events that involves the hypothalamus, anterior pituitary, ovary, and endometrium. The menstrual cycle can be easily disrupted by a variety of environmental factors including stress, extreme exercise, EDs, and obesity. It is important to understand the hormones underlying the normal menstrual cycle before studying menstrual dysfunction.
The hypothalamus secretes the gonadotropin-releasing hormone (GnRH), which stimulates the anterior pituitary to secrete follicle-stimulating hormone (FSH) and luteinizing hormone (LH). The levels and timing of secretion of each gonadotropin is correlated by GnRH, feedback from sex steroid hormones, and other autocrine and paracrine factors. The relationship among these hormones is depicted in Fig. 25.4 .
The gonadotropins FSH and LH stimulate the ovary to produce the steroid hormones, estrogen and progesterone. These ovarian steroid hormones stimulate endometrial proliferation and affect many other end organs. The feedback of estrogen and progesterone occurs primarily at the level of the anterior pituitary, through the release of GnRH. Folliculogenesis, ovulation, luteinization, and endometrium growth and shedding during the menstrual cycle depend on the factors produced from this hypothalamus-anterior pituitary-ovarian axis.
The menstrual cycle is most commonly broken up into the follicular and luteal phases as characterized by changes within the ovary. The endometrium cycles through the proliferative and secretory phases that correspond to the follicular and luteal phases in the ovary, respectively. The first day of the menstrual cycle is defined as the first day of menstrual bleeding. During this menstrual phase, the endometrium is sloughed because of low levels of estrogen. The proliferative phase is described as the time between menses and ovulation and is characterized by rising levels of estrogen, while progesterone levels remain low. As estrogen levels rise, the endometrial lining thickens with proliferation of stroma, glands, and elongation of the spiral arteries. The secretory phase is the time between ovulation and the next menses. After ovulation, progesterone levels rise, leading to the secretion of glycogen and mucus and the endometrium becomes receptive to a fertilized embryo. In the late secretory phase, in the absence of pregnancy and with the fall in both estrogen and progesterone levels, the spiral arteries vasoconstrict and the endometrium involutes, resulting in menses.
The average length of a menstrual cycle is approximately 28 days, with substantially large 95% confidence intervals (CIs) ranging from 23 to 32 days. Along with interwoman cycle variability, there is also intrawoman cycle variability. Cycle-to-cycle variability has been found to be >7 and <14 days in 42%–46% of females aged 18–44 years. , Creinin et al. found that 1 in 5 females had cycle-to-cycle variability of 14 days or more. Owing to the large inter- and intrawoman variability in cycle length, it cannot be assumed that all females have 28-day cycles or that any one female will always have consistent cycle lengths. Of note, most changes in cycle length occur in the 1–3 years leading up to menopause, and this is unlikely to begin before the age of 44 years.
In addition to total cycle length variability, there has been found to be follicular and luteal length variability. Most menstrual cycle disturbances have been presumed to be reflective of changes in the follicular phase length; however, luteal phase length variability must also be considered. It is therefore important to have a greater understanding of the cycle phase dynamics when evaluating athletes with deviations from the 28-day cycle. In a study of 165 premenopausal females, electronic fertility monitors characterized 1060 menstrual cycles and demonstrated the average follicular and luteal phase lengths to be 16.5 ± 3.4 days and 12.4 ± 2.0 days, respectively; however, the 95%CI for each phase was 9–23 days and 8–17 days, respectively. Another study used daily urine samples to determine cycle phase characteristics based on the timing of LH peak and reported mean follicular and luteal phase lengths of 14.7 ± 2.4 days and 13.2 ± 2.0 days, and 95%CI for each phase of 10–20 days and 9–17 days, respectively. In addition, when daily urine samples were collected from one female for eight consecutive menstrual cycles, total cycle length varied from 25 to 29 days and follicular and luteal lengths ranged from 10 to 17 days and 11–17 days, respectively. Interestingly, four of the eight cycles had a total length of 27 days, yet the follicular and luteal lengths ranged from 10 to 15 days and 12–17 days, respectively, indicating that even when multiple cycles from the same individual are equal in total length, both follicular and luteal phase lengths can vary.
Types of Menstrual Dysfunction
Menstrual dysfunction is the physiologic consequence of hypoestrogenism, which ranges from amenorrhea to subclinical conditions such as luteal phase defects and anovulation. These conditions lie on a spectrum based on estrogen levels, as shown in Fig. 25.5 , with amenorrhea resulting from the most extreme deficiency in estrogen and subclinical conditions resulting from less severe deficits in estrogen.