Current Concepts With The Female Triad And Sports Injuries

Women with the female athlete triad can experience lower extremity injuries as a result of low energy that may be associated with interrelated conditions such as eating disorders, menstrual dysfunction and low bone mineral density. Accordingly, this author shares pertinent insights in diagnosing and managing these issues to facilitate a return to athletic activity.

Since the implementation of Title IX in 1972, the number of women participating in sports has dramatically increased. In the 2014-2015 school year, there were 7.8 million high school athletes participating in sports and girls comprised about 42 percent of this population.^1,2  

In the 1980s and the 1990s, physicians started recognizing the female athlete triad, a syndrome of interrelated conditions frequently observed in physically active women.^3,4 The triad involves low energy availability with and without disordered eating, menstrual cycle disturbances, and low bone mineral density. The American College of Sports Medicine first described the triad in 1997, using the initial terms disordered eating, amenorrhea and osteoporosis to define the triad.⁵

The female triad is associated with significant health risks.³ The focus is now more on the underlying metabolic features of the syndrome, emphasizing the combination of low-energy availability with or without disordered eating, menstrual dysfunction and low bone mineral density.^1,9 Treatment and return to play guidelines for athletes with the triad and related medical problems were published by the Female Athlete Triad Coalition in 2014.^6,7 For women who experience the syndrome, most are those involved in sports that have high energy expenditure, have a lean physique and/or an aesthetic component, such as gymnastics, swimming, running (track and field) and figure skating.^3,6,7,8 The triad is not only isolated to diagnosed women athletes but can affect recreational physically active women as well.⁹

According to Matzkin and colleagues, in the 2007 guidelines, all three components of the triad do not need to be present for a patient to have a diagnosis of the female athlete triad.¹⁰ If the patient has one or two of the components, then one can diagnose the female athlete triad.  

Women affected by the triad often present with one or more of the three triad components (low energy availability with or without disordered eating, menstrual disturbances and low bone density), and the presence of only one component is sufficient to diagnose the triad.^3–7 A review of the female athlete triad literature reported that the prevalence of one component of the triad ranged from 16 to 60 percent, the prevalence of any two components ranged from 2.7 to 27 percent and the prevalence of all three conditions presenting simultaneously ranged from 0 to 16 percent.¹¹

One of the main components incorporated in the triad is energy deficiency (with or without disordered eating) in contrast to the old definition of disordered eating in isolation such as anorexia nervosa or bulimia nervosa, based on the criteria of the third edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM III) of the American Psychiatric Association.¹² Harmful behavior patterns range in severity from restricting food intake and using diet pills, diuretics or laxatives to periods of binge eating and purging; or having anorexia nervosa and bulimia nervosa at the extreme end of the spectrum.^5,13

A preoccupation with weight and dieting has become so common among young women that researchers note it has become a normal behavior pattern.^14,15 This should not imply that all women athletes develop diagnosable eating disorders.¹⁶ Researchers have suggested a number of risk factors for the development of eating disorders.^15,16 General predisposing risk factors for eating disorders are as follows: chronic dieting, low self-esteem, family dysfunction, physical or sexual abuse, biologic factors, perfectionism, and lack of nutritional knowledge. There are also a number of sport-specific trigger factors that may lead to eating disorders. These include emphasis on body weight for performance or appearance; pressure to lose weight from coaches and parents; exercising through injury; self-identity as an athlete (no identity outside of sports); being overtrained and undernourished; and traumatic event (injury).

What You Should Know About Low Energy Availability

Low energy availability is a relatively common complaint among women athletes. Energy availability is defined as energy obtained through oral nutrition minus energy expended during exercise. As a result, low energy may be due to increased energy expenditure, decreased oral nourishment (either intentional or unintentional), or a combination of the two. When the energy deficit in the woman athlete becomes a chronic problem, it can result in musculoskeletal and reproductive dysfunction.

Disordered eating is defined as an intentional energy deficit. Women athletes are five to 10 times more likely to suffer from an eating disorder than men.¹⁷ The prevalence of clinical eating disorders (such as anorexia nervosa or bulimia nervosa) among elite women athletes ranges from 16 to 47 percent.¹⁷ In high school athletes, disordered eating is reportedly as high as 20 percent in all sports.^18,19 In addition, authors have reported that 32 percent of women athletes regularly participate in pathogenic weight control behaviors, such as self-induced vomiting and laxative or diuretic abuse.^18,19 A high percentage of those women athletes who suffer from an eating disorder also suffer from a concomitant personality disorder, substance abuse disorder, obsessive compulsive disorder and higher suicide rates than healthy women of the same age.¹⁷ The prevalence of disordered eating in athletes is more than 5 percent and greatly exceeds that observed in non-athletes.²⁰ There seems to be a correlation of eating disorders among the amenorrheic, not the regularly menstruating athletes.  

Energy availability, whether it is through increased expenditure (kcals) or decreased oral intake (kcals), is the main factor in the triad.¹⁷ Disordered eating by the woman athlete may be intentional or unintentional. Eating disorders such as anorexia nervosa or bulimia nervosa are intentional causes. Often, many women athletes may exhibit altered eating habits, even without the formal diagnosis of an eating disorder. This may occur where the athlete fails to obtain the appropriate energy intake without being aware of this alteration.

How Menstrual Dysfunction Affects Athletes

Athletes have a higher incidence of delayed menarche and primary and secondary amenorrhea than non-athletes.^21,22 The prevalence in the general population is 2 to 5 percent but the percentage in athletes ranges from 3.4 to 66 percent.²³ The highest frequency of amenorrhea is in ballet dancers and runners.²³

Studies have shown that the average recommended energy allowance for light to moderately active women age 15 to 24 is 2,200 kcal per day.²⁴ However, the mean total consumption for women athletes is reportedly as low as 1,272 kcal per day to as high as 2,400 kcal per day.^25,26 This has caused a discussion as to whether the athlete is expending more calories than she is consuming, resulting in a negative balance of calories and too little energy to maintain the endocrine reproductive system. There is agreement that in order to maintain optimal menstrual function, there has to be availability of metabolic fuel and the reliance of reproductive function on food availability and energy balance.²⁷ There also seems to be a correlation of eating disorders among those with amenorrhea but not among athletes who menstruate regularly.

For patients in whom the energy availability is a result of intentional restrictive caloric intake and/or excessive caloric expenditure, treatment requires a multidisciplinary approach. In the case of intentional low energy availability, reversal will not be successful without the input of a mental health professional.^28,29 The physician, registered dietitian, sports nutritionist, psychologist or other mental health professional each has a role. The goals for this athlete center around normalizing her eating behaviors and altering negative beliefs related to food and body image.³⁰

For cases in which the energy availability is unintentional, the sport physician may allow the athlete to practice and compete with certain restrictions. In this case, the key professional will be either the trainer or the physical therapist, who will be responsible for designing the athlete’s training program. The trainer or physical therapist must work closely with the sports nutritionist or registered dietitian to design a program for the athlete that provides and maintains a positive energy balance.¹⁴

The sports physician should obtain a complete menstrual history. This includes the age at menarche, average length of menses, average time between menstrual periods, variations during times of increased training and number of cycles per year.

Understanding The Impact Of Low Bone Mineral Density And Osteoporosis

For the female athlete triad, the term osteoporosis refers to premature bone loss or inadequate bone formation, or a combination of the two, resulting in low bone mass, microarchitectural deterioration, increased skeletal fragility, and an increased risk of fracture.¹⁴ Amenorrheic athletes are at greater risk of low bone mass (premature osteoporosis) and stress fractures. Amenorrheic athletes have a low bone mass.^25,31,32 This patient population is at much higher risk for development of femoral stress fractures.³³

Poor bone health is the third interrelated condition of the female athlete triad. Bone health issues incurred by female athletes and exercising women with the triad are the failure to achieve peak bone mass, low bone mineral density, low volumetric bone mineral density, compromised bone geometry, decreased bone strength, increased stress reactions, and increased stress fractures.^31,35,36 Stress fractures are two to four times more common in amenorrheic athletes than in menstruating athletes.³⁶ Amenorrheic female athletes, especially oligomenorrheic female runners, have a lower bone mineral density. This patient population is at much higher risk for development of femoral stress fractures.³³    

Although runners, both men and women, have a high risk for development of stress fractures, female sex is an independent risk factor for lower-extremity stress fracture development.³⁷ The authors of a multicenter study reported an analysis of the impact of the female athlete triad factors on the incidence of bone stress injuries.³⁸ The study showed that of 259 women athletes (mean age of 18), 28 athletes sustained a bone injury (11 percent) and the risk of injury increased from 15 to 20 percent with the presence of a single triad factor to 30 to 50 percent in athletes with two or more triad risk factors.

In the case of the female athlete triad, osteoporosis refers to the premature loss of bone or inadequate bone formation in younger women, which also results in a greater risk of fracture.³⁷ The World Health Organization has defined osteoporosis as a bone mass measurement more than 2.5 standard deviations below the young adult mean.³⁹ This amounts to a loss of 25 to 30 percent from normal peak bone mass. Osteopenia refers to a lesser degree of bone loss, in which the measured density is between 1.0 and 2.5 standard deviations below normal peak bone mass. This amounts to a loss of 10 percent to 25 percent.

Peak bone density (or peak bone mass) is the highest amount of bone mass attained during a lifetime. Peak bone mass reportedly occurs in the 20s or 30s. Women acquire 85 to 90 percent of adult peak bone mass by age 18 in comparison to age 20 in men. Some research studies have shown that peak bone mass may occur as early as 18 years of age in women.⁴⁰

The two most important factors in the development of osteoporosis are the amount of peak bone mass attained and the rate of bone loss.⁴¹ In order to prevent osteoporosis, a young athlete needs to maximize peak bone density while maintaining that bone density through weightbearing activities, resistance training, calcium intake (via diet or supplementation) and vitamin D₃ intake. Calcium intake has been associated with growth and maintenance, while a lower intake is associated with a loss of bone mineral density.⁴² Some studies have shown that certain high-impact loading activities may counteract, to a certain extent, the bone loss often associated with amenorrhea.⁴³

Studies have demonstrated that amenorrheic athletes will have continued declines in their bone mineral density as long as amenorrhea is present.⁴⁴ If amenorrhea goes untreated, women will continue to lose bone mass at a rate of 2 to 3 percent per year.^45-47 The impact of amenorrhea can be dramatic for the young athlete. A lack of menstruation for as little as six months during adolescence, which is a critical time for development of bone density, can result in bone loss of 1 to 2 percent.^46,47 Female athletes who experience osteopenia or osteoporosis may use oral calcium and vitamin D supplements, or bisphosphonates depending on the severity of the bone mineral density loss and risk factors for fractures. Evidence-based studies have shown that vitamin D and calcium supplementation can prevent stress fractures in the athletic population.⁴⁸

Quantitative computed tomography (QCT) is the only testing that provides an actual measurement of volumetric bone density. Other testing includes single and dual energy X-ray absorptiometry (SXA, DXA). The most commonly employed densitometry technique is the bone densitometry scan. One would measure bone mineral density in the spine, hip (femoral neck) and wrist. They are the most commonly affected sites for fracture in patients with osteoporosis.

There are two interpretations from the bone densitometry scan. The first is the T-score, which is the number of standard deviations above or below the adult mean. It is approximately what the peak bone density should have been for patients at approximately 20 years of age. For every standard deviation below normal, the fracture risk doubles. The other interpretation is the Z-score. When the prevalence of low bone mineral density in exercising women is reportedly between 0 and 15 percent, this is defined as a Z-score of -2.0 or less. When it is between 0 to 40 percent, this results in a Z-score between -1.0 and -2.0.

There are number of factors that increase a women’s risk for osteoporotic fracture. They include anorexia nervosa, low estrogen levels, insulin-dependent diabetes, HIV infection, hyperparathyroidism, hyperthyroidism, inflammatory bowel disease, multiple sclerosis and renal failure. Other environmental factors include below normal weight, loss of menstrual function, low calcium and vitamin D3 intake, inactivity/sedentary lifestyle, prolonged corticosteroid/anticonvulsant use, cigarette smoking, excessive alcohol intake, and caffeine intake.

In Conclusion

The components of the female athlete triad are low energy availability (with and without an eating disorder), menstrual dysfunction, and low bone mineral density. These conditions can occur singularly or in combination. Signs and symptoms can include restrictive eating or fasting, rapid weight loss, use of diet pills, cessation of menstruation in an amenorrheic woman, and overuse injuries and stress fractures that are slow to heal.

Bone mineral testing should include laboratory testing and assessment of bone mineral density. A bone densitometry scan would be beneficial as a baseline and one to compare against during the woman athlete’s career and later into life. A multidisciplinary team working together with the team physician is a benefit to the woman athlete. Nutritional, biomechanical, psychological, gynecological and endocrinological are pieces of the total athletic care puzzle. Conservative non-pharmacological treatment is best when treating one or all of triad components. The various team specialists can help the woman athlete resume her athletic activities with full participation and return to a healthy lifestyle.

Dr. Ross is an Associate Professor in the Division of Vascular Surgery and Endovascular Therapy in the Michael E. DeBakey Department of Surgery at the Baylor College of Medicine in Houston. He is a Fellow of the American College of Foot and Ankle Surgeons, and a Diplomate of the American Board of Podiatric Surgery. Dr. Ross is a Past President of the American Academy of Podiatric Sports Medicine and a Fellow of the American College of Sports Medicine.   

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