The Female Athlete Triad - An investigation, diagnose and treatment
The female Athlete Triad (FAT) is a medical condition usually observed in female athletes, an includes three interrelated components: 1) low energy availability (LEA) with or without disordered eating, 2) menstrual dysfunction and 3) low bone mineral density (BMD) [(De Souza et al., 2014)]. Originally, an increase in stress fracture rates, decreases in BMD, and menstrual dysfunction has lead the American College of Sports Medicine (ACSM) to officially recognize the FAT in 1997 (Otis et al., 1997). LEA with or without eating disorders appears to have a causal role on FAT, resulting in de-regulation of the menstrual cycle and reductions of estrogen leading to low BMD (Márquez and Molinero, 2013). At the healthy side of the FAT spectrum, all energetic need are met and there are no irregularities with the reproductive system and BMD (Figure 1). Conversely, the unhealthy side is associated with LEA, amenorrhea and osteoporosis (De Souza et al., 2014). If any of the FAT components are present, an early intervention is crucial to prevent a more serious condition as the consequences of the exacerbation on these factors are associated with endothelial, endocrine, gastrointestinal, renal dysfunctions, increasing in cardiovascular risk, neuro-psychiatric disturbances, stress fractures and ultimately death (Barrack, Ackerman and Gibbs, 2013; De Souza et al., 2014).
Figure 1 - The female athlete triad continuum. Adapted from (De Souza et al., 2014).
LEA with or without disordered eating - According to Márquez and Molinero (2013), the amount of dietary energy for physiological body functions plus exercise in known as energy availability (EA) whereas nutritional intake is insufficient to provide energy is refered as LEA. LEA occurs when EA is < 30 kcal/kg of fat free mass per day (Mountjoy et al., 2014). Typically, LEA occurs in endurance sports where energy expenditure does not met dietary intake or in sports where leanness are emphasized (Torstveit and Sundgot-Borgen, 2005). When there is deficit of EA, physiological impairments occur to reduce the amount of energy used for cellular maintenance, growth, reproduction and temperature regulation (Nattiv et al., 2007). Moreover, not all cases of LEA are the same, disorder eating (DE) in classified when the athlete does not meet the necessary dietary requirement (Zach, Machin and Hoch, 2011), while eating disorders (ED) relates to potentially medical conditions such as anorexia and bulimia Nervosa (Márquez and Molinero, 2013).
Menstrual dysfunction - On the healthy side of the FAT, normal menstrual cycle is likely to occur (emenorrhea), conversely amenorrhea is present when there is a delay of menstrual cycle lasting more than 90 days (Mountjoy et al., 2014). Other types of menstrual irregularity include anovulation, luteal phase deficiency, oligomenorrhea and the subcategorisation of amenorrhea including primary (delay the first menarche) or secondary type (loss of menses after menarche) [(Nattiv et al., 2007)]. Functional hypothalamic amenorrhea (FHA) is triggered by LEA, combined with exercise and stress, and is characterized by lack of menses due to inhibition of the hypothalamic-pituitary-ovarian axis. FHA is caused by an alteration in gonadotropin-releasing hormone pulsatility which is likely to interfere with luteinizing hormone pulses from the pituitary and gonadal steroid release from the ovaries, thus affecting state of estrogen (Márquez and Molinero, 2013). Additionally, changes in body composition appears to attenuate leptin levels in amenorrheic athletes and this deficit is likely to decrease gonadotropin-releasing hormone secretion (Malinson and De Souza, 2014).
Low bone mineral density - Higher spine BMD has been reported in eumenorrheic high/odd impact athletes when compared to oligo/amenorrheic repetitive/nonimpact athletes (Nichols et al., 2007). Bone metabolism is directly affected in athletes with FAT, as with only 5 days of LEA below 30kcal/kg daily appears to promote reductions is bone formation and increase in bone resorption (Ihle and Loucks, 2004). According to De Souza et al. (2008), regardless of the estrogen status on female athletes, when EA is adequate there are no perturbations in bone formation or resorption and in athletes with LEA, estrogen deficiency is present, which is associated with is bone loss, suppressed bone formation and accelerated resorption. Since estrogen typically represses osteoclast activity, an absence of this hormone may cause disturbance of bone redesigning (Weitzmann and Pacifici, 2006). Therefore, LEA and estrogen deficiency in female athletes may override bone formation regardless of the type of sports those athletes are involved (Malinson and De Souza, 2014).
Early detection of FAT is critical to prevent exacerbation of the triad and a screening suggested by De Souza et al. (2014) should be applied as part of the Pre-Participation Physical Evaluation (appendix – Table 1). Diagnosis of LEA can be assessed in adults using BMI (Body weight kg/height m2) and a BMI < 17.5 Kg/m2 indicates low energy stores (De Souza et al., 2014). In adolescents, BMI percentiles values of 50th match the expected body weight and deviations from this range may be adjust body weight (appendix – figure 2 -3). A recent weight loss should be reported to avoid adaptation to chronic energy deficiency or otherwise energy intake (kcal) minus exercise energy expenditure divided by fat free mass (De Souza et al., 2014). Commonly, the cause of amenorrhea are identified ensuing a thorough medical history, physical examination, pregnancy andendocrinophathies tests, evaluation of thyroid stimulating hormone, follicle stimulating hormone and prolactin, primary ovarian insufficiency and hyperprolactinaemia (De Souza et al., 2014). Recommendations for clinical evaluation of primary or secondary amenorrhea can be found on appendix – figure 4. De Souza et al. (2014) suggested a questionnaire to evaluate if the athlete is at moderate or high risk of low BMD, which is used to determine in an athlete needs further diagnose by dual-energy X-ray absorptiometry (DXA). (Please see appendix figure 2 for the criteria and sites of DXA).
Energy availability - The primary goal of the management of the FAT is to restore EA to restore body weight modifying diet and nutritional status with help of a physiologist to determine energy expenditure and a sports dietitian. In case of LEA and DE, referral should to a physician and sports dietitian. If LEA is without DE, referral to a dietician. If the cause for low EA involves clinical ED, referral to a physician, sports dietitian and psychological treatment. Attention should be made for regaining body weight associated with normal menses, or achieve a BMI of ≥18.5 kg/m2 or ≥90% of predicted weight. Finally, EA intake should be set at >2000 kcal/day with consideration for exercise energy expenditure. BMD – The primary care to increase BMD in an increase EA and the intake of calcium and vitamin D (De Souza et al., 2014). Secondarily, exercise that promote should be addressed in particular weight-bearing with a combination of high-impact and resistance training .
Barrack, M. T., Ackerman, K. E. and Gibbs, J. C. (2013) “Update on the female athlete triad.,” Current Reviews in Musculoskeletal Medicine, 6(2), pp. 195–204. doi: 10.1007/s12178-013-9168-9.
Ihle, R. and Loucks, A. B. (2004) “Dose-response relationships between energy availability and bone turnover in young exercising women.,” Journal of Bone and Mineral Research: The Official Journal of The American Society for Bone and Mineral Research, 19(8), pp. 1231–40.
Malinson, R. and De Souza, M. (2014) “Current perspectives on the etiology and manifestation of the ‘ silent ’ component of the Female Athlete Triad,” International Journal of Women’s Health, (6), pp. 451–467.
Márquez, S. and Molinero, O. (2013) “Energy availability, menstrual dysfunction and bone health in sports; an overview of the female athlete triad.,” Nutrición Hospitalaria, 28(4), pp. 1010–7.
Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., Meyer, N., Sherman, R., Steffen, K., Budgett, R. and Ljungqvist, A. (2014) “The IOC consensus statement: beyond the Female Athlete Triad--Relative Energy Deficiency in Sport (RED-S).,” British Journal of Sports Medicine, 48(7), pp. 491–7.
Nattiv, A., Loucks, A. B., Manore, M. M., Sanborn, C. F., Sundgot-Borgen, J. and Warren, M. P. (2007) “American College of Sports Medicine position stand. The female athlete triad.” Medicine and Science in Sports and Exercise, 39(10), pp. 1867–82.
Nichols, J. F., Rauh, M. J., Barrack, M. T. and Barkai, H.-S. (2007) “Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading.,” Bone, 41(3), pp. 371–7.
Otis, C. L., Drinkwater, B., Johnson, M., Loucks, A. and Wilmore, J. (1997) “American College of Sports Medicine position stand. The Female Athlete Triad.,” Medicine and Science in Sports and Exercise, 29(5), pp. i–ix.
De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M., Goolsby, M. and Matheson, G. (2014) “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, M.,” British Journal of Sports Medicine, 48(4), p. 289.
De Souza, M. J., West, S. L., Jamal, S. A., Hawker, G. A., Gundberg, C. M. and Williams, N. I. (2008) “The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women.,” Bone, 43(1), pp. 140–8.
Torstveit, M. K. and Sundgot-Borgen, J. (2005) “The Female Athlete Triad: Are Elite Athletes at Increased Risk?,” Medicine & Science in Sports & Exercise, 37(2), pp. 184–193.
Weitzmann, M. N. and Pacifici, R. (2006) “Estrogen deficiency and bone loss: an inflammatory tale.,” The Journal of clinical investigation, 116(5), pp. 1186–94.
Zach, K. N., Machin, A. L. and Hoch, A. Z. (2011) “Advances in management of the female athlete triad and eating disorders.,” Clinics in sports medicine, 30(3), pp. 551–73. doi: 10.1016/j.csm.2011.03.005.