Female Athlete Triad

Disease/Disorder

Definition

The Female Athlete Triad was classically defined as amenorrhea, disordered eating (DE) 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) introduced Relative Energy Deficiency in Sports (RED-S) in 2014 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 athlete 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

Etiology

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 (kcal) minus exercise energy expenditure (kcal) divided by fat free body (kg) mass, as shown in the equation below.

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 Subclinical low EA is the amount of energy that is sustainable in a controlled manner for a short time, and is defined as an EA between 30 kcal/kg and 45 kcal/kg.⁵

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.⁶ Sport-specific risk factors for the development of female athlete triad are summarized in Table 1.⁷ 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 Although the estimated prevalence of the triad is low (0-1.2%), the prevalence of any 2 or any 1 of the triad conditions ranges from 2.7-27.0% and 16.0-60.0%, respectively.² 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.⁸ The strongest risk factor for low BMD is prior anorectic behavior. Menstrual disorders in adolescence is also strongly associated with low BMD.⁹

Table 1: Specific Sports at Risk for Female Athlete Triad

Patho-anatomy/physiology

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 approximately 30 kcal/kg of fat free mass, there is a disruption in gonadotropin releasing hormone pulsatility at the hypothalamus, leading to altered release of luteinizing hormone and follicle stimulating hormone from the pituitary gland, as well as decreased estradiol and progesterone levels. This causes a form of functional hypothalamic amenorrhea.¹⁰  Alterations in pulsatility also results in an uncoupling of bone turnover.¹¹ Furthermore, evidence suggests the hypoestrogenic state can result in cardiovascular dysfunction due to impaired arterial vasodilation, as well as valve abnormalities, pericardial effusion, severe bradycardia, and arrhythmias in more severe cases of low EA.^10,12

Low energy availability may affect other systems with manifestations including depression, fatigue, gastrointestinal disorders, relative immunodeficiency, and negative impact on performance (Table 2).^2,3,12

Table 2: Additional organ systems involved in Female Athlete Triad.

Disease progression including natural history, disease phases or stages, disease trajectory (clinical features and presentation over time)

Females with subthreshold 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.¹³Those with menstrual dysfunction are at risk for infertility and cardiovascular dysfunction.^3,12 Athletes with low BMD are at risk for stress fractures, failure to reach peak BMD and irreversible loss of bone.¹³ Recent research has identified that a higher female athlete triad risk score is more strongly associated with stress-injuries in trabecular-rich bones than cortical-rich bones.¹⁴ In females with DE behaviors, “overexercising” is the variable most strongly associated with suicidal behaviors.¹⁵

Essentials of Assessment

History

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 (consider using the 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.¹⁶ 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 affected individuals from seeking medical attention and delays diagnosis, especially in athletes who value health and physical fitness.^1,17 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 athletes 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.¹⁸

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, et al.)

Pre-participation Physical Exam Female Athlete Triad Screening Questions

• Have you ever had a menstrual period?
• How old were you when you had your first menstrual period?
• When was your most recent menstrual period?
• How many periods have you had in the last 12 months?
• Are you presently taking any female hormones (estrogen, progesterone, and birth control pills)?
• Do you worry about your weight?
• Are you trying to or has anyone recommended that you gain or lose weight?
• Are you on a special diet or do you avoid certain types of food or food groups?
• Have you ever had an eating disorder?
• Have you ever had a stress fracture?
• Have you ever been told you have low bone density (osteopenia or osteoporosis)?

Additional screening tools for female athlete triad/RED-S have been introduced since the 2014 female athlete triad coalition consensus statement. These include the Low Energy Availability in Females Questionnaire (LEAF-Q) and the International Olympic Committee Relative Energy Deficiency in Sport Clinical Assessment Tool Version 2 (IOC REDs CAT2). The LEAF-Q was developed as a screening tool to identify those at risk of female athlete triad.¹⁹ The IOC REDs CAT2, on the other hand, is a clinical assessment tool aimed at aiding in the assessment of male and female athletes suspected to be at risk for low EA, risk stratification, and guiding return-to-sport decision making. The IOC REDs CAT2 implements a three-step process of initial screening; risk stratification based on clinical signs and symptoms; and a physician-led diagnosis and treatment plan with the athlete, coach, and treatment team.²⁰

Physical examination

General:

•  Vital Signs
•  Body mass index and percent body fat
•  General appearance

HEENT

•  Oropharyngeal erythema and/or ulceration
•  Parotid gland palpation for hypertrophy

Cardiac:

•  Bradycardia or tachycardia
•  Orthostatic hypotension
•  Arrhythmias

Gastrointestinal:

• Abdominal exam

Gynecologic:

• Consider pelvic exam if menstrual dysfunction is suspected

Integumentary:

• Skin, hair, nails
• Dry skin, hypercarotenemia, lanugo, and acrocyanosis may be seen in DE ²¹

Musculoskeletal:

•  Skeletal exam
•  Assess for point tenderness on the bone consistent with stress fracture
•  Hand exam for callous formation (seen in those who induce vomiting)

Endocrine:

•  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.

Laboratory studies

If an eating disorder is suspected, the following tests should be obtained:

• Electrocardiogram
• Chemistry profile
• Complete blood count
• Erythrocyte sedimentation rate
• Thyroid function test
• Urinalysis

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).

Imaging

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.⁶ 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.

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 highlights 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. A 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.²²

Treatment guidelines

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 are identified, referral to a mental health practitioner is recommended.  A transdermal 17β-estradiol patch should be considered as an adjunct treatment in adolescents and young adults with oligomenorrhea or amenorrhea, as it has been shown to be superior to combined oral contraceptive pills in improving bone mineral density.²³

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 (P-PE) 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.

Cutting Edge/Emerging and Unique 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.²⁴ Relative energy deficiency has been shown to occur in males just as it does in females. Recent data suggests that reproductive and skeletal health of the male athlete may require a more severe energy deficiency than the female athlete.²⁵ A study by Papageorgiou et al, demonstrated that reduced energy availability in women resulted in decreased bone formation and increased bone resorption, but the same level of reduced energy availability in men did not affect their bone turnover markers.²⁶ However, further research is needed to fully elucidate this association.  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.”²⁷ Further validation of an age appropriate screening tool for female athlete triad and relative energy deficiency risk that can be used by young athletes, coaches, trainers for early intervention is needed.²⁸

Gaps in The Evidence-Based Knowledge

More studies are needed to estimate the accurate prevalence of subclinical and clinical female athlete triad and implement systematic methods to treat these patients of different severity with outcome monitoring. Furthermore, it should be noted that despite the importance of determining whether an athlete has adequate EA, an accurate measurement of EA is not yet feasible. Challenges to direct measurement of EA include no standardized protocol for assessing EA, variance in athletes’ baseline activities/lifestyle, need for specialized equipment, compliance of the athlete, and the time and expertise needed to complete the assessment as well as analyze the information.¹⁰ Therefore, additional research is needed to develop a validated protocol to identify athletes at risk for female athlete triad/RED-S.

As previously mentioned, most of the research conducted on the female athlete triad has been done on able-bodied Caucasian women. Published research on female athlete triad/RED-S in non-Caucasian populations is lacking, thus there is a need to include more diverse populations of athletes in research to better recognize risk and implement prevention and treatment strategies. Additionally, as participation in para-sport from recreation to elite levels is increasing, it becomes imperative to investigate the prevalence and impact of low EA in the para-athlete population based on underlying disability.

References

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Original Version of the Topic

Kathryn T. Gollotto, DO. Female athlete triad. 7/20/2012.

Previous Revision(s) of the Topic

Mooyeon Oh-Park, MD, Dena Abdelshahed, MD. Female Athlete Triad. 8/23/2016.

Mooyeon Oh-Park, MD, Ruben Rivera, MD. Female Athlete Triad. 2/23/2021

Author Disclosure

Mooyeon Oh-Park, MD
Nothing to Disclose

Deanna Brinks, MD
Nothing to Disclose

Lauren Bartels, DO
Nothing to Disclose