With this modification of the guidelines, the overall prevalence of triad components on their respective spectrums has increased, although the total prevalence of athletes with this condition is unknown. Table 1 compares the prevalence of the female athlete triad based on the 1992 and 2007 diagnostic guidelines. Prior to the updated 2007 definition, 1% to 4% of the patients presented with all three components of the triad according to self-reported questionnaires and dual-energy x-ray absorptiometry (DEXA) measurements of high school and elite athletes.11,14 Because all three interrelated components no longer have to be present concomitantly, the overall prevalence of the condition has increased. In a prospective study of high school athletes and sedentary students, Hoch et al15 found that the prevalence of sedentary students who had at least one component of the triad was 65%, whereas 78% of female athletes had one or more of the pathologic constituents. In a prospective study of women and girls who exercise, Barrack et al6 found that the risk of developing a bone stress injury among active females increased from 15% to 21% in the presence of one risk factor (eg, disordered eating, menstrual dysfunction, weight-controlling behavior) but increased to 21% to 30% with two risk factors and 29% to 50% with three risk factors.
When assessing the specific components of the triad, the prevalence of menstrual irregularities among high school female athletes ranged from 18.8% to 54% based on data collected from self-reported questionnaires.4,15 Martinsen and colleagues12,21 conducted two studies to observe the prevalence of disordered eating and eating disorders in elite female high school athletes. In one study,12 11% to 25% of female athletes had pathogenic eating behaviors or were considered at risk of having an eating disorder as characterized by criteria described in the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV). In a second study,21 a clinical interview was conducted after the athlete completed the questionnaire and was deemed to be at risk of developing an eating disorder. The results of the interviews demonstrated that 14% of the female athletes had a true eating disorder compared with 5% of the controls. The most common eating disorder encountered in both studies was eating disorder not otherwise specified (EDNOS).12,21 EDNOS is an eating disorder that does not meet the specific criteria of bulimia nervosa or anorexia nervosa.22 Persons with EDNOS may display some of the attributes required for diagnosis of a specific eating disorder, yet not enough for an official diagnosis (eg, a female who meets the criteria for anorexia nervosa but menstruates regularly).22 Given that disordered eating no longer has to be present for diagnosis of the triad and is now more broadly defined as energy availability, it is likely that the prevalence of the decreased energy availability component of the new triad definition is higher than what is reported here. However, current studies include only the old definition relating to energy availability, which specifically requires that disordered eating be present.
In 2012 and 2013, the Female Athlete Triad Coalition convened to develop a consensus statement for triad screening, treatment, and return to play.23 The document lists 11 risk factors that should be screened, including a history of menstrual irregularity, stress fracture, dieting, and overtraining as well as personality factors such as perfectionism and obsessiveness. In addition, the importance of early intervention was emphasized along with the need to revolutionize the currently unstandardized preparticipation examinations for female athletes. The coalition proposed the use of a point system to assess athletes with risk factors for the female athlete triad during the preparticipation examination and to determine when an athlete is able to return to play. Each risk factor is allocated a certain number of points based on history or current findings. For example, the risk factor of stress reaction/fracture ranges from 0 to 2 points based on the athletes’ history. Two points are added to the magnitude of risk score if the patient has had more than two stress injuries, more than one high risk factor, or injury involving trabecular bone sites. An athlete with no history of stress injury is considered low risk, and zero points would be added. Athletes with a cumulative risk score of six or more points should be restricted from sport participation.23
Present Definition of the Female Athlete Triad
Originally known as “disordered eating,” this triad component is now termed “energy availability.” The spectrum of energy availability ranges from optimal to low. An athlete does not have to be diagnosed with an eating disorder to have this component of the triad.5 Low energy availability can result from inadequate caloric intake caused by pathologic caloric restriction (as in the setting of anorexia nervosa or bulimia nervosa) or by expending more energy than the body is designed for at a given time. To determine a patient’s energy availability, the amount of energy that is expended is subtracted from the amount of caloric energy consumed from diet and is divided by lean body mass in kilograms. To begin the assessment of energy availability, body mass index (BMI) should be calculated. If the BMI is <17.5 kg/m2, it is likely that the athlete has low energy stores. In athletes with a normal BMI, it is more difficult to assess energy availability. To determine if energy availability is suboptimal, a detailed history, including diet and energy expenditure, must be elicited from the patient. Even with the most accurate history, determining availability of energy is not completely precise.23 Low energy availability is determined to be <45 kcal/kg of lean-body mass per day; however, energy availability ≤30 kcal/kg of lean-body mass is associated with most of the negative effects.5,15,23
Adequate nutrition education among athletes is necessary for the prevention and treatment of low energy availability.5 In underweight athletes (BMI <17.5 kg/m2), increasing BMI to 18.5kg/m2 may be enough to increase energy stores, but it is not typically that simple.23 The management of low energy availability requires a multidisciplinary approach, especially in patients with an eating disorder. A registered dietician, a primary care physician with expertise in treating athletes with the triad, and a mental health provider are important members of the treatment team. In athletes diagnosed with an eating disorder (as characterized by DSM-IV criteria) or low self-esteem, a psychiatrist or primary care physician may opt to prescribe antidepressants.5
Prior to sport participation, a thorough history should be obtained, including the patient’s dietary behaviors, menstrual pattern, training, and subjective weight (ie, how the athlete views her weight). A thorough physical examination is also important because certain findings should raise suspicion for low energy availability and a possible eating disorder. These findings include, but are not limited to, low body weight (BMI <17.5 kg/m2), bradycardia, lanugo, orthostatic hypotension, poor dentition, chipmunk cheeks (caused by swollen parotid glands from vomiting), and the Russell sign (ie, a callus on the back of a finger caused by self-induced vomiting).5,22-24 It should be noted that athletes who are overweight can also be energy deficient. The overall prevalence of energy imbalance and disordered eating among athletes varies based on the study evaluation criteria, as shown in Table 2.12,19,21,25,26 Thus, the actual prevalence is unknown. However, prevention of decreased energy availability aids the prevention of other health risks, including amenorrhea, low BMD, and fractures. Female athletes who suffer from disordered eating have been found to have a twofold to fourfold increased risk of developing a sports-related injury.4,27 Females who participate in a sport where being thin or lean is considered ideal are at increased risk of suboptimal energy availability or disordered eating, as defined by the original description of the female athlete triad.2,4,5,9,11 Athlete education about proper nutrition and energy status is crucial to prevent the negative consequences associated with the triad, particularly those involving bone and reproductive health.5
The spectrum of menstrual function ranges from eumenorrhea to amenorrhea.5 Eumenorrhea is defined as regular menstruation at approximately every 28 days. Amenorrhea is divided into primary and secondary subsets; primary amenorrhea is the absence of menarche after age 15, and secondary amenorrhea is the cessation of menses for three consecutive cycles after menarche. Oligomenorrhea, menstruation every 35 days or fewer than nine menstrual cycles in 1 year, is considered abnormal. Subclinical menstrual irregularities, such as a luteal phase defect and anovulation, also fall along the spectrum and are important to rule out during the triad screening process.5,23,28
Functional hypothalamic amenorrhea (FHA) associated with the female athlete triad results from an unpredictable release of gonadotropin-releasing hormone (GnRH). Prolonged exertion and weight loss have been shown to influence GnRH release, although the pathophysiology is not entirely clear. GnRH directly affects the release of luteinizing hormone and follicle-stimulating hormone from the pituitary gland. When this pathway is disrupted, it directly affects the release of estrogen from the ovaries, causing FHA.28,29 If an athlete has amenorrhea, regardless whether it is primary or secondary, it is prudent to exclude causes other than FHA, including thyroid abnormalities, structural anomalies, pregnancy, polycystic ovary syndrome, and pituitary tumor.28
Estrogen plays an important and complicated role in the physiology of BMD and bone formation. Estrogen inhibits bone remodeling and bone resorption, which then increases and enhances bone formation. In an estrogen-deficient state, BMD is decreased, thus leading to an increased risk of fragility fracture.30 In a cross-sectional study of the possible risk factors that contribute to stress fractures in female endurance athletes, menstrual dysfunction was prevalent.31 Nineteen athletes were diagnosed with a stress fracture; 15 had a history of amenorrhea and 13 reported current amenorrhea or oligomenorrhea at the time of the study. The high prevalence of menstrual dysfunction in athletes with a stress fracture is not surprising considering the direct effect of estrogen on BMD.
Treatment of FHA begins with increasing energy availability to an optimal state. In some athletes, this directly correlates to an increase in BMI by increasing caloric intake, reducing energy expenditure, or both. An increase in caloric intake has been shown to be directly related to weight gain and resumption of menses, as long as energy expenditure is controlled.23,24,32 The mainstay and cornerstone of treatment of FHA is to increase energy availability through nutrition/caloric intake to normalize the secretions of luteinizing hormone and follicle-stimulating hormone.23 Hormone replacement therapy and oral contraceptive pills (OCPs) have been used in the past as a first-line treatment for athletes with amenorrhea, but a significant benefit has not been demonstrated in this population. Oral contraceptive use was considered in the setting of a continued decrease in BMD in an athlete with persistent amenorrhea.5 To date, data on the effects of OCPs on BMD remain inconclusive.32 Recently, the use of OCPs in these athletes has fallen out of favor because data have suggested that OCP use causes further harm by reducing BMD if taken over a long period of time (ie, ≥2 years).33
A female athlete with menstrual dysfunction (eg, FHA, oligomenorrhea, subclinical amenorrhea) should be assessed for other components of the triad. In a prospective study of high school athletes, Rauh et al27 found that athletes who self-reported amenorrhea or oligomenorrhea had a nearly threefold greater risk of musculoskeletal injury (exact injury type was not recorded). However, the overall prevalence of menstrual dysfunction among the athletic population requires further study (Table 3). The importance of proper nutrition must be conveyed to athletes; proper nutrition leads to adequate energy availability and has a direct effect on reproductive health. With proper education at the beginning of an athlete’s sports participation, menstrual irregularities may be prevented.
Bone Mineral Density
The spectrum of BMD includes osteoporosis but also encompasses reduced BMD because of its role in increased risk of injury in female athletes with the female athlete triad.5 Younger female athletes must understand that, for most women, 90% of peak BMD is reached by age 18 years and that the greatest level of accrual is between the ages of 11 and 14 years.36 To obtain optimal BMD, adequate nutrition (ie, protein, calcium, and vitamin D consumption; moderate physical activity with weight-bearing exercise) is required.23,37 After the peak BMD has been reached, it may only be lost or maintained.37 It is crucial that athletes possess this knowledge so that they can build and maintain BMD during these years to optimize bone health. The overall prevalence of low BMD among athletes is unknown and varies by study depending on the method of evaluation4,14-18,27,31,34,35 (Table 4).
DEXA is the diagnostic modality of choice for evaluation of BMD. When interpreting BMD from a DEXA scan of a premenopausal female athlete aged ≥20 years, the Z-score of the hip and a PA radiographic view of the lumbar spine should be used. In adolescents and children, a PA radiographic view of the spine and total body less the head are the preferred methods for evaluating BMD.38 The Z-score is used to compare the subject with a control of the same sex and age. The T-score, which is also used to evaluate BMD, can be used to compare the patient’s BMD to that of an average adult at peak BMD and is used to evaluate BMD in postmenopausal women. BMD is considered low when the Z-score is <−2.0 standard deviations (compared with normal controls). In premenopausal female athletes, a score >−1.0 standard deviation is considered abnormal and requires further evaluation. If a female athlete has a history of stress fractures or stress reactions, further investigation of low BMD is required.5,15
Treatment of low BMD depends on the underlying cause. Exercise and adequate nutrition are important for treatment and prevention. Weight-bearing and dynamic exercises have a positive effect on bone formation and BMD, especially in premenopausal females.23 Calcium and vitamin D supplements may be desirable in some cases. The recommended amount of calcium and vitamin D intake for adults is 1,000 mg and 600 to 800 IU, respectively.39 It is also prudent to screen for other factors that may accelerate bone loss, including corticosteroid use, regular alcohol consumption, cigarette smoking, protein deficiency, and hyperthyroidism.40 In the female athlete, menstrual function should be evaluated and must be corrected if it is abnormal because estrogen plays a direct role in bone health and remodeling. Increasing energy availability is the mainstay of treatment for amenorrhea. OCPs should not be used as a first-line treatment to halt additional bone loss. Because an increase in weight has been shown to correlate with an increase in BMD, increasing weight should be the initial focus of treatment in these patients.5,28 Education of athletes with regard to proper nutrition, menstrual function, and low BMD is needed to help prevent the manifestation of this component of the triad in female athletes.
Summary and Future Research
As female participation in sports continues to increase and become more competitive, it is important to prevent, diagnose, and manage the components of the female athlete triad in athletes. Educating the athlete about proper nutrition is an important part of preventing this condition. In the past, diagnosis of the triad based on its original definition was an easier task because all three components (disordered eating, amenorrhea, osteoporosis) had to be present simultaneously. Pharmacologic treatment was used to restore menses and was believed to halt loss of BMD. However, the use of pharmacologic therapy has fallen out of favor, and the current mainstay of treatment is to increase energy availability, which leads to the resumption of menses and halts additional bone loss. Because the definition of the triad has been modified to that of a spectrum disorder, index of suspicion plays an important role in diagnosis during the assessment of a female athlete. Although the female athlete triad poses a great health risk, the benefits of participation in sports significantly outweigh the risks.15
Any athlete who falls under the so-called umbrella of the triad should be questioned and educated regarding all of the components and potential health risks of this condition. By preventing premature bone loss in young female athletes, we can prevent future fragility fractures. Education of athletes is crucial to prevention. If athletes can understand the importance of optimal energy availability and how it directly affects bone and reproductive health, the pathology associated with the components of the triad may be avoided.
Coaches, athletic trainers, and healthcare providers should also be educated about the female athlete triad to detect and recognize its components before athletes reach the pathologic end of the spectrum. A thorough history and physical examination by a healthcare provider is also prudent in discovering if a female athlete is at risk for developing any of the pathologic entities of the triad. Treating this cohort of athletes is a multidisciplinary effort. First, educating the athlete must be an integral component of the treatment plan. Healthcare providers such as orthopaedists or primary care physicians should be involved. A mental health provider is essential for treating athletes with disordered eating. A registered dietician also plays an integral role in treatment given that most of the negative effects associated with the triad originate with low energy availability.
Further research is needed to determine the true prevalence of the triad and identify which females are at risk. Awareness levels among athletes, coaches, and healthcare professionals should be assessed to determine where education is needed most. A patient may present with any of the components of the triad; therefore, an awareness of these components among all involved in the care of female athletes is prudent.
Evidence-based Medicine: Levels of evidence are described in the table of contents. In this article, references 4, 33, and 35 are level II studies. References 6, 11, 12, 15, 18, 19, 21, and 29 are level III studies. References 14, 16, 17, 20, 25-27, 31, 34, and 36 are level IV studies. References 3, 5, 23, 24, 28, 30, 32, 37, and 40 are level V expert opinion.
References printed in bold type are those published within the past 5 years.
2. Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J: American College of Sports Medicine position stand. The female athlete triad
. Med Sci Sports Exerc 1997;29(5):i–ix.
3. Thein-Nissenbaum JM, Carr KE: Female athlete triad
syndrome in the high school athlete. Phys Ther Sport 2011;12(3):108–116.
4. Thein-Nissenbaum JM, Rauh MJ, Carr KE, Loud KJ, McGuine TA: Associations between disordered eating, menstrual dysfunction, and musculoskeletal injury among high school athletes. J Orthop Sports Phys Ther 2011;41(2):60–69.
5. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine: American College of Sports Medicine position stand. The female athlete triad
. Med Sci Sports Exerc 2007;39(10):1867–1882.
6. Barrack MT, Gibbs JC, De Souza MJ, et al.: Higher incidence of bone stress injuries with increasing female athlete triad
-related risk factors: A prospective multisite study of exercising girls and women. Am J Sports Med 2014;42(4):949–958.
8. Vincent LM: The Dancer's Book of Health. Hightstown, NJ, Princeton Book Company Publishers, 1988.
9. Yeager KK, Agostini R, Nattiv A, Drinkwater B: The female athlete triad
: Disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 1993;25(7):775–777.
10. Troy K, Hoch AZ, Stavrakos JE: Awareness and comfort in treating the female athlete triad
: Are we failing our athletes? WMJ 2006;105(7):21–24.
11. Torstveit MK, Sundgot-Borgen J: The female athlete triad
exists in both elite athletes and controls. Med Sci Sports Exerc 2005;37(9):1449–1459.
12. Martinsen M, Sundgot-Borgen J: Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45(6):1188–1197.
13. Pantano KJ: Current knowledge, perceptions, and interventions used by collegiate coaches in the U.S. regarding the prevention and treatment of the female athlete triad
. N Am J Sports Phys Ther 2006;1(4):195–207.
14. Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS: Prevalence of the female athlete triad
syndrome among high school athletes. Arch Pediatr Adolesc Med 2006;160(2):137–142.
15. Hoch AZ, Pajewski NM, Moraski L, et al.: Prevalence of the female athlete triad
in high school athletes and sedentary students. Clin J Sport Med 2009;19(5):421–428.
16. Beals KA, Manore MM: Disorders of the female athlete triad
among collegiate athletes. Int J Sport Nutr Exerc Metab 2002;12(3):281–293.
17. Thompson SH: Characteristics of the female athlete triad
in collegiate cross-country runners. J Am Coll Health 2007;56(2):129–136.
18. Pollock N, Grogan C, Perry M, et al.: Bone-mineral density and other features of the female athlete triad
in elite endurance runners: A longitudinal and cross-sectional observational study. Int J Sport Nutr Exerc Metab 2010;20(5):418–426.
19. Doyle-Lucas AF, Akers JD, Davy BM: Energetic efficiency, menstrual irregularity, and bone mineral density in elite professional female ballet dancers. J Dance Med Sci 2010;14(4):146–154.
20. Schtscherbyna A, Soares EA, de Oliveira FP, Ribeiro BG: Female athlete triad
in elite swimmers of the city of Rio de Janeiro, Brazil. Nutrition 2009;25(6):634–639.
21. Martinsen M, Bratland-Sanda S, Eriksson AK, Sundgot-Borgen J: Dieting to win or to be thin? A study of dieting and disordered eating among adolescent elite athletes and non-athlete controls. Br J Sports Med 2010;44(1):70–76.
22. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders, ed 4. Washington, DC, American Psychiatric Association, 2000.
23. De Souza MJ, Nattiv A, Joy E, et al.; Expert Panel: 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. Br J Sports Med 2014;48(4):289.
24. Mallinson RJ, Williams NI, Olmsted MP, Scheid JL, Riddle ES, De Souza MJ: A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr 2013;10(34).
25. Torres-McGehee TM, Monsma EV, Gay JL, Minton DM, Mady-Foster AN: Prevalence of eating disorder
risk and body image distortion among National Collegiate Athletic Association Division I varsity equestrian athletes. J Athl Train 2011;46(4):431–437.
26. Beekley MD, Byrne R, Yavorek T, Kidd K, Wolff J, Johnson M: Incidence, prevalence, and risk of eating disorder
behaviors in military academy cadets. Mil Med 2009;174(6):637–641.
27. Rauh MJ, Nichols JF, Barrack MT: Relationships among injury and disordered eating, menstrual dysfunction, and low bone mineral density
in high school athletes: A prospective study. J Athl Train 2010;45(3):243–252.
28. Practice Committee of the American Society for Reproductive Medicine: Current evaluation of amenorrhea. Fertil Steril. 2004;82 Suppl 1S33–9.
29. Falsetti L, Gambera A, Barbetti L, Specchia C: Long-term follow-up of functional hypothalamic amenorrhea and prognostic factors. J Clin Endocrinol Metab 2002;87(2):500–505.
30. Syed F, Khosla S: Mechanisms of sex steroid effects on bone. Biochem Biophys Res Commun 2005;328(3):688–696.
31. Duckham RL, Peirce N, Meyer C, Summers GD, Cameron N, Brooke-Wavell K: Risk factors for stress fracture in female endurance athletes: A cross-sectional study. BMJ Open 2012;2(6).
32. Ducher G, Turner AI, Kukuljan S, et al.: Obstacles in the optimization of bone health outcomes in the female athlete triad
. Sports Med 2011;41(7):587–607.
33. Scholes D, Hubbard RA, Ichikawa LE, et al.: Oral contraceptive use and bone density change in adolescent and young adult women: A prospective study of age, hormone dose, and discontinuation. J Clin Endocrinol Metab 2011;96(9):E1380–E1387.
34. Thein-Nissenbaum JM, Rauh MJ, Carr KE, Loud KJ, McGuine TA: Menstrual irregularity and musculoskeletal injury in female high school athletes. J Athl Train 2012;47(1):74–82.
35. Nattiv A, Kennedy G, Barrack MT, et al.: Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: A 5-year prospective study in collegiate track and field athletes. Am J Sports Med 2013;41(8):1930–1941.
36. Matkovic V, Jelic T, Wardlaw GM, et al.: Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis: Inference from a cross-sectional model. J Clin Invest 1994;93(2):799–808.
37. Anderson JJ, Tylavsky FA, Halioua L, Metz JA: Determinants of peak bone mass in young adult women: A review. Osteoporos Int. 1993;(3 suppl):132–6.
40. Watts NB, Bilezikian JP, Camacho PM, et al.; AACE Osteoporosis Task Force: American Association of Clinical Endocrinologists Medical Guidelines for Clinical Practice for the diagnosis and treatment of postmenopausal osteoporosis. Endocr Pract 2010;16(suppl 3):1–37.
Keywords:© 2015 by American Academy of Orthopaedic Surgeons
female athlete triad; female athlete; eating disorder; low bone mineral density