Jane S. Chung, MD

A female high school rower, aged 17 years, presents to your clinic for upper back pain. She is preparing for her senior year and would like to row competitively in college. Her back pain has been present for 2 months. Initially pain was only with rowing, but it has been progressively worsening and now she has pain at rest. Reviewing her medical record, you notice that she has lost 33 pounds since her last visit about 9 months ago. Her body mass index (BMI) was 24.3 kg/m

 (75.6% percentile) 9 months ago and today it is 18.6 kg/m

 (11.7%). On review of systems, you learn that she has not had a menstrual period in the last 6 months. Menarche occurred when she was aged 12 years. She endorses feelings of depression, but no suicidal ideation. Academically, she is a straight-A student.

A male cross-country runner with right lower leg pain for 2.5 weeks, aged 15 years, presents to your clinic. He was previously running about 30 miles per week but recently increased his mileage to 60 miles per week. He has a history of shin splints but his current pain feels like it is “in the bone of [his] lower leg.” The pain is focal to his midtibia. Pain is present with weight-bearing and he has a limp with walking due to pain. He stopped running a week prior, but he likes to be physically active and has been cross-training with core and upper-body resistance training. He has a history of a right tibial stress fracture from the past year. On review of systems, you learn that the patient’s BMI has decreased from 19.3 kg/m

 (3%) over the past 2 years. He is a vegetarian. X-ray today demonstrates a stress fracture (Figure 1).

The female athlete triad was first described in 1997 as the interrelationship among amenorrhea, osteoporosis, and disordered eating. In 2007, the triad was revised to better identify athletes at risk, recognizing that presentation can be on a spectrum, ranging from optimal health to subclinical and clinical disease (Figure 2). The 3 components are now called menstrual function, bone mineral density (BMD), and EA,1 with low EA being the root cause of the triad. Acknowledging the existence of a spectrum of disease allows athletes to be identified earlier and to receive earlier intervention. If an athlete has any of the 3 components, a more thorough investigation should be performed to evaluate for the other components, which may have subclinical presentations.

 Due to the spectrum of disease, it can be difficult to accurately estimate the prevalence of the female athlete triad. An athlete may have 1, 2, or all 3 components. It is estimated that all 3 components are present in 1.0% to 1.2% of high school athletes, 2 components in 4% to 18%, and 1 component in up to 54%.

 Any athlete can develop aspects of the triad, but athletes in sports that emphasize endurance, appearance, or weight class are most at risk. Sport specialization at an early age can also increase risk (Table 1). The Female Athlete Triad Coalition Consensus Panel recommends screening during the pre-participation physical exam or if there are concerns that an athlete may have the triad (Table 2).

EA is the amount of dietary energy (calories) remaining for physiologic function after exercise. Low EA is the root cause of the triad as it may affect bone health and lead to hormonal disturbances in the athlete.

Many athletes’ low EA is not intentional and they do not display pathologic eating or weight control behaviors. When this is the case, simply increasing caloric intake will treat the patient. However, restriction of caloric intake can be intentional in athletes who are trying to maintain a weight class or achieve a certain appearance. Disordered eating is estimated to occur in 6% to 45% of female athletes.

 Athletes who have specialized diets (vegan, vegetarian, pescatarian, etc) may also be at increased risk. In cases where the athlete has intentional disordered eating, psychological intervention and treatment may be required.

According to a study of 1000 female athletes by Ackerman et al, those with low EA were more likely to have negative performance effects, including decreases in coordination, concentration, endurance, and training response. In the clinic setting, it may be helpful to discuss with the athlete how decreased EA can negatively affect performance.

A low BMI is a strong predictor of low bone mineral density and stress fractures. An adolescent should be screened carefully if they have a BMI that is less than 17.5 kg/m

. An athlete’s goal weight should be >90% of expected body weight.

 However, it is important to keep in mind that even athletes with a normal BMI may still have low EA.

If you are able to work with a dietitian, you can calculate fat free mass (FFM) for your athlete patient. In order to have normal menstrual function, 30 kcal/kg of FFM/day are needed, but 45 kcal of FFM/day is ideal.

 Because this calculation can be difficult, it is helpful to have the athlete see a sports dietitian and exercise physiologist, if possible.

Even in the absence of amenorrhea, disordered eating can be associated with lower BMD in athletes.

Adolescence is the most crucial time for bone mass accumulation, so the presence of the athlete triad can be particularly harmful during this time. Maximum rate of bone formation usually occurs between the ages of 10 and 14 years, and 90% of peak bone mass is attained by 18 years.

 Diet, weight-bearing activities, and genetic makeup all contribute to an individual’s bone mass accrual. Achieving sufficient bone mass is important to decrease the risk of fracture and to prevent osteoporosis in adulthood. Lower estrogen and lower EA increase bone resorption and suppress bone formation and remodeling.

Stress fractures are often the initial presenting symptom in patients with the triad. Stress fractures usually occur due to chronic, repetitive micro-trauma that cause tiny cracks in the bone. Athletes with menstrual irregularities are more likely to have bone stress injuries. As with the other aspects of the triad, a spectrum of stress injury exists, ranging from stress reaction (intermediate injury; bone marrow edema) to fracture (when enough trauma has occurred to cause a break in the cortex).

A dual-energy radiograph absorptiometry (DXA) can be used to assess bone density and should be considered in athletes with a history of stress fractures, and/or menstrual dysfunction, and/or low EA for at least 6 months. Notably, DXAs are usually ordered on postmenopausal women, and separate standards exist for performing DXAs on children or adolescents. Therefore, DXA should ideally be done at a facility whose staff is familiar with interpreting results based on the patient’s age and gender. In adults, BMD is interpreted using the T-score, which compares the patient’s BMD with the maximum expected BMD achieved aged between 25 and 30 years. Pediatric bone density, however, is assessed using the Z-score, which compares the patient’s BMD with those of others of similar age and race. Further details are available in the guidelines provided by DeSouza et al.

 It may be helpful to discuss these with the performing radiologist.

Athletes who participate in high-impact and resistance activities would be expected to have a BMD that is 10% to 15% higher than those of athletes participating in nonimpact sports. This should be taken into consideration when interpreting DXA scans. Z-scores of less than –1.0 may be abnormal in an athlete, alerting concern for low BMD, but that score may be normal in a nonathlete. An athlete who has a Z-score of less than –1 should undergo further evaluation.

It is not normal for female athletes to have menstrual dysfunction; they should not lose their period during their sport season (a phenomenon most classically seen in cross-country runners). Functional hypothalamic amenorrhea (ie, amenorrhea with the female athlete triad) is a diagnosis of exclusion, so if an athlete is experiencing amenorrhea or oligomenorrhea, it is crucial to rule out other causes (Table 2).

 Primary amenorrhea is absence of menarche by age 15 years. Secondary amenorrhea is defined as absence of menses for 3 months or longer, while oligomenorrhea is defined as cycles lasting longer than 35 days.

 Maintaining normal menstrual function is important for the athlete’s bone health.

 As such, exogenous hormones (ie, birth control pills) may be perceived as beneficial. However, many studies have shown that oral contraception is not an effective way to restore bone health. An athlete with menstrual dysfunction may use oral birth control pills to prevent pregnancy, but it is important to let her know that having a period on birth control does not mean her bone health is improving.

Menstrual dysfunction can also negatively affect cardiovascular health in athletes. The results of some studies in ballet dancers and endurance athletes have shown that athletes with oligomenorrhea and amenorrhea had increased risk for high cholesterol and other vascular findings that correlate with the development of atherosclerotic disease.

It may take up to 1 year or longer to resume menses after EA restoration. Decreased bone density, the result of female athlete triad, may be irreversible, although it can improve with increasing EA. Early intervention is key, so it is crucial to screen for those at risk.

Relative energy deficiency in sport (RED-S)

The term RED-S was introduced in 2014 by the International Olympic Committee to encompass males and to acknowledge that energy deficiency can affect other aspects of an athlete’s health. These may include issues involving the endocrine, metabolic, hematologic, cardiovascular, gastrointestinal, and immunologic systems as well as growth and development. Research done by Ackerman et al demonstrated that athletes with low EA were more likely to have many of the ill effects of RED-S than those with appropriate EA.

The male athlete triad is a term used in males to describe the interrelationship of low EA, impaired bone health, and reproductive suppression. Low EA has been associated with decreased testosterone in male athletes due to a suppressed hypothalamic–pituitary–gonadal axis. True prevalence of low testosterone from hypogonadotropic hypogonadism is unknown.

 Low testosterone can have numerous effects on the male athlete, including decreased physical performance, sleep disturbances, fatigue, decreased motivation, sexual dysfunction, loss of muscle mass, sperm abnormalities, lower BMD, and depression.

Male athletes with recurrent bone stress injuries or with initial injury in a trabecular region (pelvis, sacrum, femoral neck) should be evaluated for nutrition and hormone function, especially if the athlete has other risk factors such as low BMI. Tenforde et al recommend screening for low BMD with DXA, nutritional evaluation (including a 25-hydroxy vitamin D test), and endocrine work-up (including free and total testosterone) in athletes with high-risk stress fracture in areas such as the pelvis or femoral neck, although more evidence-based guidelines are needed.

Restoring EA is the mainstay of treatment of both male and female athlete triad. This can be accomplished if the athlete increases caloric intake and decreases physical activity/energy expenditure. Working with a sports dietitian to increase EA to >45 kcal/kg FFM per day is ideal, but increasing calories by 300 to 600 per day and decreasing exercise by 1 day per week can be a productive starting point. This should be done on an individual basis depending on the athlete’s training regimen and expenditure. The goal is to increase BMI to >18.5 kg/m

 and to restore normal menstrual function. Working with a multidisciplinary team that includes a PCP, dietitian, psychologist, athletic trainer, and sports medicine specialist is helpful.

In the past, oral contraceptive pills were commonly used to restore menses; however, as mentioned above, this may offer a false sense of security and should be avoided unless they are necessary for other indications. Bisphosphonates are also generally not recommended in the pediatric/adolescent population. No evidence exists for their effectiveness and they may be teratogenic if an athlete were to become pregnant.

Calcium and vitamin D are important for bone health. The recommended daily amount of calcium is 1300 mg; if this is not achieved with diet alone, it should be supplemented. The recommendation for vitamin D for patients aged between 1 and 18 years is 600 IU, although higher doses may be considered depending on climate and deficiency. A recent systematic review of military submariners determined that the combination of vitamin D and calcium has a synergistic effect, and that vitamin D levels were most effectively increased with supplementation levels of 2000 IU/day.

 Weight-bearing exercise is also important for enhancing the accrual of bone mass.

Because the consequences of the athlete triad can be irreversible, affecting long-term bone, reproductive, and possibly cardiovascular health, a PCP must have a high index of suspicion for the triad in an athlete presenting with any of the above components. The annual well-child exam or sports physical is an opportunity for the PCP to screen patients for the athlete triad.

ACKNOWLEDGMENTS: We would like to thank Amanda Weiss Kelly, MD, for her mentorship and expertise on this topic.

1. De Souza MJ, Nattiv A, Joy E, et al. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. 

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2. Weiss Kelly AK, Hecht S; Council On Sports Medicine and Fitness. The female athlete triad. 

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3. Bratland-Sanda S, Sundgot-Borgen J. Eating disorders in athletes: overview of prevalence, risk factors and recommendations for prevention and treatment. 

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4. Ackerman KE, Holtzman B, Cooper KM, et al. Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport. 

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5. Hoch AZ, Papanek P, Szabo A, Widlansky ME, Schimke JE, Gutterman DD. Association between the female athlete triad and endothelial dysfunction in dancers. 

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6. Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, Lindén Hirschberg A. Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. 

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7. Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. 

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8. Sivakumar G, Koziarz A, Farrokhyar F. Vitamin D supplementation in military personnel: a systematic review of randomized controlled trials. 

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