The Female Athlete Triad was classically defined as amenorrhea, disordered eating and low bone mineral density. The components of the female athlete triad are unique but interrelated conditions, each of which can occur on a spectrum of severity.1-3 The syndrome is now characterized by any one or combination of: 1) low energy availability (EA) with or without disordered eating, 2) menstrual dysfunction and 3) low bone mineral density (BMD).2 Since this clinical entity is caused by energy deficiency affecting multiple systems, the International Olympic Committee (IOC) recently introduced Relative Energy Deficiency in Sports (RED-S) as a more comprehensive and broad term for the overall syndrome.2 According to the new definition, athletes do not have to have characteristics of all three diagnoses. Subclinical disorders associated with female athletic triad include low energy availability (EA) with inadvertent disordered eating, oligomenorrhea, and BMD below expected for chronologic age. Early intervention is necessary to prevent or slow the progression of the disorder to clinical eating disorders, amenorrhea (no menstruation for >3 months) and osteoporosis.1,2
Impaired reproductive and skeletal health is linked to the concept of low EA, which can be caused by insufficient dietary caloric intake, excessive caloric expenditure, or a combination of both.4 Daily EA is defined as energy intake minus energy expenditure divided by fat free body mass. Energy balance in a normal individual is estimated as an EA of 45 kcal/kg of fat free mass per day. Detrimental physiological changes in reproductive function, metabolism, and bone density may occur when daily EA falls below 30 kcal/kg of fat free body mass.3
Epidemiology including risk factors and primary prevention
Reduced EA has been reported in up to 62% of athletes compared to the 1-5% of normal population. 5 Sport-specific risk factors for the development of female athlete triad are summarized in Table 1.6 Much of the research on female athlete triad has been done on Caucasian women. African American women have an overall lower risk of eating disorders and higher BMD compared with Caucasian women. While the focus of this summary is the female athlete triad, relative energy deficiency syndrome (RED-S) is also reported in males.2
Regarding the specific components of the triad, the prevalence of menstrual disorders varies greatly among studies, from 6% to 69% depending on age, type of sport, intensity and volume of the training.3 Based on the World Health Organization criteria for low BMD, the prevalence of osteopenia and osteoporosis in female athletes is estimated to be 22-50% and 0-13% respectively.3 However, the International Society of Clinical Densitometry recommends utilizing the Z-score rather than the T-score in reporting BMD in premenopausal women as this allows comparison to sex and age matched controls. Z-scores below -2.0 are classified as low bone density for chronological age.7 The strongest risk factor for low BMD in women is amenorrhea or oligomenorrhea.
Table 1: Specific Sports at Risk for Female Athlete Triad
|Sports with subjective scores||Figure skating|
|Endurance sports||Distance running|
|Sports with body contouring clothes||Volleyball|
|Sports with weight categories||Wrestling|
|Sports favoring prepubertal body habitus||Gymnastics|
The underlying physiological issue that predisposes athletes to female athlete triad is low EA. In a normal, healthy individual, there will be enough EA for physiological homeostasis, thereby meeting the daily metabolic demands outside that used for exercise. If EA decreases, normal bodily functions can become disordered. Once daily EA falls below 30 kcal/kg of fat free mass, there is a disruption in luteinizing hormone pulsatility needed for ovulation and an uncoupling of bone turnover. New evidence suggests the hypoestrogen state can result in cardiovascular dysfunction due to impaired arterial vasodilation.8 Low energy availability may affect other systems with manifestations including depression, fatigue, gastrointestinal disorders, relative immunodeficiency, and negative impact on performance (Table 2).2,3,8
Table 2: Additional organ systems involved in Female Athlete Triad.
|System/Organ||Symptoms, Disorders, and Associations|
|Endocrine||Vitamin D deficiency, thyroid dysfunction|
|Cardiovascular||Poor lipid profile, impaired arterial vasodilation|
|Hematologic||Anemia due to nutritional deficiencies|
|Gastrointestinal||Esophagitis, poor nutritional status|
|Psychological||Depression, anxiety, low self esteem, body dysmorphic disorder|
Disease progression including natural history, disease phases or stages, disease trajectory (clinical features and presentation over time)
Females with sub-threshold symptoms or manifestations of any of the components of the triad may go undiagnosed. They are then at increased risk for progression to prolonged amenorrhea, repetitive strain injuries, stress fractures, fatigue, and chronic pain.
Specific secondary or associated conditions and complications
With prolonged female athlete triad, there is involvement of multiple organ systems (Table 2). Those with subclinical eating disorders are at much higher risk to develop a life-threatening eating disorder. There is an increased risk of anxiety, depression, obsessive-compulsive disorder, drug abuse and suicide in affected females.9 Those with menstrual dysfunction are at risk for infertility and cardiovascular dysfunction.3,8 Athletes with low BMD are at risk for stress fractures, failure to reach peak BMD and irreversible loss of bone.9
2. ESSENTIALS OF ASSESSMENT
Screening for female athletic triad is recommended during pre-participation exam or annual physician visit as well as for the cases where there is clinical suspicion.3 Structured history taking is the most important aspect of making an accurate diagnosis. The practitioner should inquire about symptoms covering a wide variety of organ systems, especially focusing on eating habits (considering to use eating disorder inventory), menstrual history (delayed menarche, irregular cycles, oligomenorrhea, amenorrhea), use of oral contraceptive and supplements, and injuries including a history of stress fractures.10 Review of systems should include cardiovascular (arrhythmias, palpitations), endocrine (heat or cold intolerance) and integumentary (dry skin and/or nails) systems.
Clinicians must recognize the psychosocial implications of being diagnosed with an eating disorder, which potentially deters people from seeking medical attention and delays diagnosis, especially in athletes who value health and physical fitness.1,11 Practitioners must ask sensitive questions in a way that the athlete will feel comfortable providing truthful answers. Those at risk for an eating disorder tend to have an underlying personality trait of perfectionism and a strong will. Typical features for athlete with a high drive for thinness score (a validated self-reported measure about body image) include preoccupation with body weight and shape, fear of weight gain, and association of thinness with self-worth. Studies show 66% of athletes with high drive for thinness scores are clinically energy-deficient.12
The Female Athlete Triad Coalition produced a consensus statement after their International Consensus Conferences including recommendations for screening questions during pre-participation physical examination, adapted in Table 3.1
Table 3: Triad consensus panel screening questions. (from Joy E, De Souza MJ, Nattiv A, et al. 2014 female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad. Current sports medicine reports 2014;13:219-32.)
|Pre-participation Physical Exam Female Athlete Triad Screening Questions|
- Vital Signs
- Body mass index and percent body fat
- General appearance
- Oropharyngeal erythema and/or ulceration
- Parotid gland palpation for hypertrophy
- Bradycardia or tachycardia
- Orthostatic hypotension
- Abdominal exam
- Consider pelvic exam if menstrual dysfunction is suspected
- Skin, hair, nails
- Skeletal exam
- Assess for point tenderness on the bone consistent with stress fracture
- Hand exam for callous formation (seen in those who induce vomiting)
- Thyroid exam
- Cold extremities
Supplemental assessment tools and psychological testing
Use of the Minnesota Multiphasic Personality Inventory (MMPI), Beck depression scores (21 questions with scores of 0-3 each with high scores indicating more severe depression) or other psychological testing is appropriate as psychological pathology increases the risk for development of female athlete triad and is associated with poor outcomes.
If an eating disorder is suspected, the following tests should be obtained:
- Chemistry profile
- Complete blood count
- Erythrocyte sedimentation rate
- Thyroid function test
If a menstrual dysfunction is suspected, a full work-up for secondary amenorrhea should be obtained. (Normal values are presented in parentheses; the levels of these hormone may vary depending on the time of the day or stage of ovulatory cycle):
- Pregnancy test
- FSH (1-25 IU/L)
- LH (0.5 to 76.3 IU/L)
- Prolactin (< 14 ng/mL)
- TSH (0.5-5 mIU/L)
- Cortisol (3-20 ug/dl).
- Serum estradiol (2-16 ng/dL)
- Progesterone challenge (optional).
If an athlete has amenorrhea, disordered eating for more than six months, or has had stress or low impact fracture, a DEXA scan should be obtained for a Z-score which compares BMD to the mean based on the chronological age.5 Other imaging (x-ray, MRI) is generally not needed unless the athlete has a symptomatic injury. If an athlete is suspected to have a stress fracture, plain radiography is warranted. However, if this is negative, further work-up with magnetic resonance imaging (MRI) with fat suppression or triple-phase bone scan should be performed if clinical suspicion remains high.
3. REHABILITATION MANAGEMENT AND TREATMENTS
Available or current treatment guidelines
The position stand from the American College of Sport Medicine (ACSM) in 2007 emphasizes prevention, early detection, and multidisciplinary treatment of female athlete triad.3 This statement also highlight policy changes among sport governing bodies discouraging unhealthy weight loss practices of athletes. Screening for female athlete triad is recommended during the pre-participation exam and athletes with one component of the female athlete triad should be assessed for the others. More recent consensus statement from the International Consensus Conference on the female athlete triad is available as a supplement to the ACSM’s position stand.2
Coordination of care
A team approach is essential in treating the athletes with components of female athlete triad. The treatment team should include physician, dietician, and mental health provider if eating disorder is identified and may involve athletic trainer, exercise physiologist, coach, parents and other family members. All the members of the treatment team must understand the factors that lead to the development of female athlete triad and coordinate the treatment. One study found that less than half of primary care providers (internists, family physicians and pediatricians) were aware of female athlete triad. Increasing awareness of the triad among practitioners will likely lead to earlier diagnosis and more efficient intervention.13
Restoring normal energy status by increasing dietary intake and modifying the exercise training is the main goal of treatment. Normalization of body weight is the best strategy to correct the abnormalities, including normal menstruation and improved BMD. The time required to resume normal menstruation is typically months however, it varies depending on the severity and duration of the energy deficiency. Weight bearing exercise is encouraged to improve BMD. Recovery of BMD may not be observed until years after recovery of energy status and menstrual status.2 If pathologic eating disorders is identified, referral to mental health practitioner is recommended. Oral contraceptives should be considered in an athlete with functional hypothalamic amenorrhea over age 16 if BMD is decreasing with nonpharmacological treatment despite adequate nutrition and body weight.3
Patient & family education
A diagnosis such as this may come with a negative connotation to the female athlete.
The athlete may also feel that her identity as one who emphasizes health and wellness is being questioned. Healthcare providers should ensure confidentiality while providing an environment conducive to honest communication. Providers may discuss the condition as a lack of energy availability due to a training error that is correctable with caloric and activity modifications likely resulting in improved athletic performance. Removing “blame” from the athlete may improve the likelihood of compliance with treatment recommendations. There are many misconceptions about female athletes; parents and athletes may also believe that it is normal for an athlete to be amenorrheic or have a below normal BMI. Proper education is important for both primary and secondary prevention.
Social role and social support system
Athletes with components of female athlete triad will require a large social support system, including the physician, family, coach, athletic trainer, dietitian and mental health practitioner.
Early predictors of outcomes
Psychological comorbidities, especially including anxiety, depression, body dysmorphism and high drive for thinness are predictors of poor outcomes.
Translation into practice: practice “pearls”/performance improvement in practice (PIPs)/changes in clinical practice behaviors and skills
Often, cursory pre-participation examination (PPE) without adequate screening tools for female athlete triad is unlikely to identify subclinical or clinical female athlete triad. All clinical sports medicine practices must maintain a high level of vigilance. Physiatrists and other sports medicine clinicians should also present the issues surrounding female athlete triad to the athlete and family in a “nonblaming” manner, focusing on lack of EA as a training error rather than a pathological disorder, which helps gain trust and opens communication.
4. CUTTING EDGE/EMERGING AND UNIQUE CONCEPTS AND PRACTICE
Cutting edge concepts and practice
The definition of female athlete triad is evolving and it is now recognized as a multiorgan disorder rather than a classic triad. Early detection and intervention is highly emphasized including educating practitioners, athletes, and families. Recent research reveals that males may experience similar effects that mirror the female athlete triad, including hypogonadism, abnormal bone mineral density, and low energy availability.14 Relative energy deficiency has been shown to occur in males just as it does in females. Furthermore, the term “Relative Energy Deficiency Syndrome” further captures those who participate in sport and exercise recreationally and may not necessarily consider themselves an “athlete.”15
5. GAPS IN THE EVIDENCE-BASED KNOWLEDGE
Gaps in the evidence-based knowledge
More studies are needed to estimate the accurate prevalence of subclinical and clinical female athlete triad and implementing systematic methods to treat these patients of different severity with outcome monitoring.
- Joy E, De Souza MJ, Nattiv A, et al. 2014 female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad. Current sports medicine reports 2014;13:219-32.
- Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the Female Athlete Triad–Relative Energy Deficiency in Sport (RED-S). British journal of sports medicine 2014;48:491-7.
- Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine position stand. The female athlete triad. Medicine and science in sports and exercise 2007;39:1867-82.
- Loucks AB, Stachenfeld NS, DiPietro L. The female athlete triad: do female athletes need to take special care to avoid low energy availability? Medicine and science in sports and exercise 2006;38:1694-700.
- Beals KA, Meyer NL. Female athlete triad update. Clinics in sports medicine 2007;26:69-89.
- West RV. The female athlete. The triad of disordered eating, amenorrhoea and osteoporosis. Sports medicine (Auckland, NZ) 1998;26:63-71.
- Leib ES, Lewiecki EM, Binkley N, Hamdy RC. Official positions of the International Society for Clinical Densitometry. Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry 2004;7:1-6.
- Hoch AZ, Lal S, Jurva JW, Gutterman DD. The female athlete triad and cardiovascular dysfunction. Physical medicine and rehabilitation clinics of North America 2007;18:385-400, vii-viii.
- Scully D, Kramer J, Meade MM, Graham R, Dudgeon K. Physical Exercise and Psyhological Well Being: a Critical Review. Br J Sports Med 1998:32:111-120.
- VanBaak K, Olson D. The Female Athlete Triad. Current sports medicine reports 2016;15:7-8.
- Lebrun CM. The female athlete triad: what’s a doctor to do? Current sports medicine reports 2007;6:397-404.
- Desouza M. Drive for thinnes score is a proxy indictor of energy deficiency in exercising women. Appitite 2007;48:359-67.
- Curry EJ, Logan C, Ackerman K, McInnis KC, Matzkin EG. Female Athlete Triad Awareness Among Multispecialty Physicians. Sports medicine – open 2015;1:38.
- Tenforde AS, Barrack MT, Nattiv A, Fredericson M. http://www.ncbi.nlm.nih.gov/pubmed/26497148 Sports Med. 2016 Feb;46(2):171-82.
- Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A. http://www.ncbi.nlm.nih.gov/pubmed/25950026 Br J Sports Med. 2015 Apr;49(7):417-20.
Original Version of the Topic:
Kathryn T. Gollotto, DO. Female athlete triad. Publication Date:2012/07/20
Mooyeon Oh-Park, MD
Nothing to Disclose
Dena Abdelshahed, MD
Nothing to Disclose