Female Athlete Triad
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Syndrome of three interrelated clinical entities: low energy availability (EA) (with or without disordered eating [DE]), menstrual dysfunction (MD), and low bone mineral density (BMD) (1). There is also emerging research to suggest an expanded syndrome referred to as Relative Energy Deficiency in Sport (RED-S), which acknowledges that male athletes maybe at risk (2).
- Female athlete triad was first described in 1992: Patients may meet criteria for only one or two parts of the triad.
- 2014 Female Athlete Triad Coalition consensus statement and the 2007 American College of Sports Medicine (ACSM) position stand suggest (1):
- Each component of the triad represents a spectrum ranging from health to dysfunction.
- EA is fundamental to the propagation of the triad.
- Full recovery is not possible without correction of low EA.
- The International Olympic Committee’s updated position statement from 2014 now considers RED-S to be a more accurate representation of the psychological and physiologic stresses placed on the athlete’s body.
- Metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular and psychological health are all effected (2).
- Prevention and early intervention are essential to prevent progression to serious clinical end points of eating disorders, amenorrhea, and osteoporosis.
- RED-S also takes into account the effects of relative energy deficiency on male athletes, who are often affected in weight-sensitive sports (gymnastics, wrestling, cycling, etc.) (2).
- The changes in physiology should be viewed as a spectrum, with normal EA, BMD, and regular menses at one extreme and clinical eating disorders, osteoporosis, and amenorrhea at the other (2).
- Dietary energy intake minus exercise energy expenditure; the core element of the triad
- Represents the amount of dietary energy remaining for bodily functions after correcting for exercise training
- EA (kcal/kg FFM/day) = [EI (kcal/day) − EEE (kcal/day)] where EEE is effective energy expenditure and FFM is fat free mass
- Low EA results in reduced capacity for cellular maintenance, thermoregulation, and growth.
- Low EA serves a causal role in the induction of exercise-associated menstrual disturbances.
- Low EA occurs either intentionally or inadvertently. Examples include increasing training disproportionately to energy intake; DE; and reducing energy intake by restricting, fasting, binging, and purging or use of diet pills, laxatives, diuretics, or enemas. Not all athletes meet diagnostic criteria from Diagnostic and Statistical Manual of Mental Disorders, 5th edition (DSM-5) for eating disorders.
- Low EA alters the hypothalamic-pituitary axis, resulting in functional hypothalamic amenorrhea.
- MD ranges from eumenorrhea to amenorrhea.
- MD includes athletes who have low estrogen levels but still experience menstruation.
- Energy deficit results in MD at ~30 kcal/kg lean body mass per day.
- MD includes luteal suppression (shortened luteal phase, prolonged follicular phase, and decreased estradiol level), anovulation, oligomenorrhea (menstrual cycle >35 days), and primary and secondary hypothalamic amenorrhea.
- Primary amenorrhea (no menarche by age 15 years), although less common, can occur in young athletes. Secondary amenorrhea is defined as the absence of menstrual cycles for >3 months after menarche has been established.
- Although hypothalamic suppression is the most common cause of secondary amenorrhea in these athletes, other causes must be ruled out.
- Ranges from optimal bone health to osteoporosis
- Peak BMD occurs at 19 years in females and 20.5 years in males.
- Bone health encompasses bone strength as well as bone quality. The current practice standard (dual energy x-ray absorptiometry [DEXA]) measures bone density, not bone quality. This research may help providers better understand why two athletes with the same BMD may have very different bone fracture histories (3).
- ACSM position stand recommends using the International Society for Clinical Densitometry (ISCD) guidelines for BMD Z-scores <−2.0 with a history of clinically significant fracture for diagnosis of osteoporosis.
- Because most athletes have a higher BMD than nonathletes, ACSM recommends further workup for any athlete with a Z-score <−1, even in the absence of fracture.
- Endothelial dysfunction
- Emerging evidence suggests that the female athlete triad is associated with endothelial dysfunction. Reduced levels of estrogen alter vasodilation. Athletic amenorrhea is associated with reduced brachial artery flow-mediated dilation, which has a 95% positive predictive value for coronary endothelial dysfunction. Consequences include decreased blood flow to muscles during exercise and accelerated atherosclerosis. In the future, this clinical syndrome may be considered a tetrad (4).
- Overall prevalence: 0–16% of female athletes (5). Prevalence of two criteria varies: MD + BMD 0–8% (n = 460), MD + LE 18% (n = 80), and BMD + LE 4% (n = 80) (3).
- DE higher than general population (3)
- MD: Prevalence of secondary amenorrhea is as high as 60% in female athletes compared to 2–5% in the general population (3).
- Bone health: Using the World Health Organization (WHO) criteria for low BMD, prevalence of osteopenia (T-score between −1 and −2) ranges from 0% to 40% in female athletes, as compared to ~12% in the general population (3).
Etiology and Pathophysiology
- In functional hypothalamic amenorrhea, low EA disrupts the hypothalamic-pituitary-ovarian axis, decreasing pulsatile gonadotropin-releasing hormone (GnRH) release (5).
- Low GnRH levels decrease luteinizing hormone (LH) and follicle-stimulating hormone (FSH) levels, decreasing estrogen production with resultant MD.
- Estrogen deficiency negatively affects bone density. A chronic state of malnutrition reduces the rate of bone formation and increases the rate of bone resorption. Changes in bone metabolism occur within 5 days of reductions in EA.
- History of menstrual irregularities and amenorrhea; history of stress fractures and recurrent or nonhealing injuries; history of critical comments about eating or weight from parent or coach; history of depression; history of dieting; personality factors, including perfectionism and/or obsessiveness, overtraining, and inappropriate coaching behaviors (1)
- Lean physique, sports with an aesthetic component (ballet, figure skating, gymnastics, distance running, diving, and swimming), or sports with weight classifications (martial arts and wrestling). Frequent weigh-ins, consequences for weight gain, and win-at-all-cost attitude all increase risk (2).
- A lack of family or social support; intense training hours; social isolation, or entering a new environment (boarding school or college); an athlete with comorbid psychological conditions (anxiety, depression, and/or obsessive-compulsive disorder)
- Education of athletes (middle school through college), coaches, trainers, parents, and physicians. Young athletes are extremely impressionable and may turn negative comments and unhealthy advice into maladaptive eating and exercising habits.
- General screening during preparticipation exam (PPE) and annual physicals are endorsed by AAP, AAFP, ACSM, AOSSM, and AMSSM (6).
- Female Athlete Triad Coalition has 11-question screening to use during PPE (1).
- Screen athletes presenting with “red flag” conditions such as fractures, weight changes, fatigue, amenorrhea, bradycardia, orthostatic hypotension, syncope, arrhythmias, electrolyte abnormalities, or depression.
Commonly Associated Conditions
- Anorexia nervosa, bulimia nervosa, avoidant or restrictive food intake disorder, and other psychological disorders, including low self-esteem, depression, and anxiety (5)
- Low BMD predisposes athletes to stress fractures and may not be fully reversible. This may lead to a higher rate of fractures after menopause.