Female Athlete Triad: Future Directions for Energy Availability and Eating Disorder Research and Practice

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Key points

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    The impact of low energy availability (EA) on reproductive function can be modified by gynecologic age, psychological factors, and genetics. As such, a more individualized approach to diagnosing and treating low EA is warranted.

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    In practice, the accurate measurement of EA (in combination with the difficulties of diagnosing and treating the increasing number of athletes with disordered eating) represent key challenges in Triad research going forward.

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    Recently published guidelines for determining

Low energy availability: gaps and clarifications

EA has been a focus of Triad research since the 2007 American College of Sports Medicine Position Stand2 on the Female Athlete Triad emphasized the critical role of EA (with or without DE) in the etiology of the Triad. Current knowledge on the underlying mechanism of exercise-related menstrual disorders has been informed by prospective studies in nonhuman primates25 and previously untrained women.3, 26 These have shown that aerobic exercise, in combination with caloric restriction, can induce

Etiology of low energy availability

Appropriate treatment of low EA as it relates to the induction of menstrual and bone sequelae requires an understanding of how and why EA is low. What is the pathway to low EA? As described in the Female Athlete Triad Coalition Consensus Statement,43 there are 4 distinct pathways to low EA:

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    DE

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    Clinical eating disorder (ED)

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    Intentional weight loss without DE

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    Inadvertent undereating

As such, screening and treatment strategies need to target these individual pathways. If the etiology of low EA involves

Gynecologic age

The importance of low EA as a causal factor in Triad conditions has been established. Yet, the individual variation in the susceptibility to low EA may be attributable to factors that modify the relation among EA, ovarian disruption, and/or bone metabolism. A critical factor that has not been addressed in Triad literature is gynecologic age; that is, the difference between one’s chronologic age and the age of menarche. The natural prevalence of menstrual disturbances decreases with advancing

Genetics

An individual’s genetics may contribute to one’s susceptibility to functional hypothalamic amenorrhea (FHA). Caronia and colleagues60 reported that in a sample of 55 women with FHA, 7 had heterozygous mutations associated with hypothalamic hypogonadism, in which mutations to the following genes were found: fibroblast growth factor receptor-1, the Kallmann syndrome 1 sequence, prokineticin receptor 2, and the GnRH receptor. No such mutations were found in 422 control subjects with normal

Psychological factors

Although much of the Triad condition relates to states of low EA, it is well documented that psychological and social stress can impact reproductive function in humans and animals.65, 66, 67, 68, 69, 70, 71, 72, 73 Despite this fact, specific Triad literature lacks the recognition that exercise-associated menstrual disturbances are a subtype of this stress-induced reproductive disruption paralleling anorexia, DE, bulimia, and other psychosocial stressors. It is likely that these

Female Athlete Triad and relative energy deficiency in sport

As Triad research evolves, it is important to keep in focus that the primary physiologic and clinical presentations of the Triad continue to be low EA with or without DE, menstrual disturbances, and low bone mass. These are the medical conditions that clinicians and practitioners have deemed clinically important enough to warrant treatment and prevention strategies. Secondary physiologic and clinical consequences of the Triad have also been documented in exercising women, including alterations

Male athlete triad

Interest in whether a parallel to the Female Athlete Triad occurs in male athletes has increased recently.100 Clinically, this is a challenge to ascertain, as outward reproductive manifestations are difficult to identify and may require sperm and fertility testing as well as tracking of hormone levels. Testosterone levels are affected by physical activity with levels shifting in response to time/duration of exercise, endurance versus resistance-trained sport, and age.101 Testosterone production

Eating disorders and disordered eating

Most cases of the Female Athlete Triad involve low EA that results from the conscious restriction of food intake that occurs along a continuum of severity. As Joy and colleagues49 noted in a recent extensive review, the concern surrounding eating behaviors in athletes is pressing, as the rates of EDs in the general population are on the rise for individuals in their late teenage years105 and are high among elite adolescent athletes.106 Added attention to certain research gaps would assist with

Applying triad science and clinical judgment to inform clearance and return to play decisions

Although the scientific underpinnings and epidemiology of the Female Athlete Triad have been well explored in the literature and updated position stands are available, a gap in practice-based applications of Triad science still exists. This is arguably the most difficult step in addressing public health issues, and as such, represents a gap in the area of the Female Athlete Triad. The recent Female Athlete Triad Coalition Consensus Statement43 provided the first comprehensive effort to provide

Summary

Research on the Female Athlete Triad has spanned several decades. Despite this, there still exist many gaps in the research. Low EA is the key factor in the etiology of the Triad, but the impact of low EA on reproductive function can be modified by gynecologic age, psychological factors, genetics, and likely many other factors. As such, a more individualized approach to diagnosing and treating low EA is warranted, and more research is necessary to improve the measurement of EA and how these

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      Relative energy deficiency in sports (RED-S), introduced in 2007 as a new entity that replaced the term, “female athlete triad,” that consisted of disordered eating, amenorrhea, and osteoporosis.26 RED-S is a more inclusive entity referring to impaired menstrual function, metabolic rate, and bone and cardiovascular health resulting from relative energy deficiency.27 It is often difficult to exclude a coexisting ED in athletes with RED-S.

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    Disclosure Statements: N.I. Williams has nothing to disclose.

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