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Female athletes that consume to little energy compared to what the body needs are at risk of developing menstrual dysfunction, low bone mineral density and poor health.

Female Athlete Triad

The Female Athlete Triad is a medical condition often seen in physically active girls and women. When the female athlete does not consume enough calories to cover physiological needs and energy spent during exercise, it may lead to menstrual disturbances and loss of bone mass. The Female Athlete Triad involves three components:

 

  1. Low energy availability (with or without disordered eating)

  2. Menstrual dysfunction

  3. Low bone mineral density

​

Not normal to lose menses

 

It is not normal for active girls and women to have irregular menses or to experience complete loss of menstrual function. We know that exercise has no suppressive effect on reproductive function apart from its energy cost (1).

 

The notion that it is normal for female athletes to have irregular menses still exists, but is explicitly refuted by both the International Olympic Committee (IOC) (1) and the American College of Sports Medicine (ACSM) (2,3). The ACSM stated as early as 1997 that «it is a symptom of an underlying problem that requires medical evaluation within the first 3 months of occurrence» (3).

 

If an athlete shows signs of one or more of the triad components, it is important to intervene at an early stage to prevent it from progressing to the serious endpoints of the triad, including eating disorder, loss of menstrual function (amenorrhea), and osteoporosis.

 

It is a problem that many female athletes and coaches still think that amenorrhea indicates that the athlete has reached an adequate training intensity, rather than realizing that it is a serious symptom that requires medical attention.

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Energy availability

 

Low energy availability is at center of the Female Athlete Triad. When the body gets to little calories to what it needs, it starts shutting down bodily functions that it considers to be of less importance, including reproductive function, in order to save energy.

 

The amount of energy (calories) that the body has available to spend to maintain bodily functions (metabolic needs) is what is known as energy availability. It is therefore defined as dietary intake minus exercise energy expenditure (2).

 

Energy availability ranges from optimal to low. The optimal energy availability in female athletes is 45 kilocalories (kcal) per kilo of fat free mass (FFM) (4,5). This assures enough calories for the body to spend on its everyday needs.

 

Low energy availability, however, is when the athlete has less than 30 kcal per kg of FFM left after subtracting the calories spent during exercise. This is when most of the negative effects occur, including significant changes in reproductive and metabolic hormone concentrations and markers of bone formation and resorption in the blood (6,7).

​

Let us take an example:

​

If a 17-year-old female athlete weighs 60 kg and has only 15 % body fat, she would have a fat free mass of 51 kg. If she eats 2000 kcal and spends 600 kcal during exercise, her energy availability would be:

 

(2000 kcal - 600 kcal) / 51 kg FFM

= 27.5 kcal per kg FFM

​

In this example, we see that 2000 kcal is way too little for this athlete, and that she eats too little to cover her energy demands. If this athlete were to follow the recommendations, she should consume:

​

(45 kcal × 51 kg FFM) + 600 kcal

= 2895 kcal

 

If the female athlete in the example above continues to consumes 2000 kcal per day (which is the recommended intake for sedentary adults and moderately active adolescents by the U.S. Department of Health and Human Services (HHS) (8), and the recommended average daily intake for women by the National Health Service in the UK (9)), the athlete would, in fact, be energy deficient.

 

Through this example, we can see how it is possible for an athlete to have low energy availability without disordered eating. It is crucial that athletes take into account their energy expenditure and that they increase their caloric intake accordingly. This is especially important in endurance athletes, because of their high energy expenditure during training.

  1. Drinkwater, B. L., Loucks, A., Sherman, R. T., Sundgot-Borgen, J., & Thompson, R. A. (2005). Position Stand on the female athlete triad.

  2. Nattiv, A., Loucks, A. B., Manore, M. M., Sanborn, C. F., Sundgot-Borgen, J., & Warren, a. M. P. (2007). The female athlete triad. Med. Sci. Sports Exerc, 39(10), 1867-1882.

  3. Otis, C. L., Drinkwater, B., Johnson, M., Loucks, A., & Wilmore, J. (1997). ACSM position stand: The female athlete triad. Medicine & Science in Sports & Exercise, 29(5), i-ix.

  4. Nose‐Ogura, S., Harada, M., Hiraike, O., Osuga, Y., & Fujii, T. (2018). Management of the female athlete triad. Journal of Obstetrics and Gynaecology Research, 44(6), 1007-1014.

  5. Statuta, S. M. (2020). The Female Athlete Triad, Relative Energy Deficiency in Sport, and the Male Athlete Triad: The Exploration of Low-Energy Syndromes in Athletes. Current sports medicine reports, 19(2), 43-44.

  6. De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., . . . 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, May 2013. Br J Sports Med, 48(4), 289-289.

  7. Matzkin, E., Curry, E. J., & Whitlock, K. (2015). Female athlete triad: past, present, and future. JAAOS-Journal of the American Academy of Orthopaedic Surgeons, 23(7), 424-432.

  8. U.S. Department of Health and Human Services, H. Appendix 2. Estimated Calorie Needs per Day, by Age, Sex, and Physical Activity Level. Retrieved from https://health.gov/our-work/food-nutrition/2015-2020-dietary-guidelines/guidelines/appendix-2/

  9. National Health Service, N. (2019). What should my daily intake of calories be? Retrieved from https://www.nhs.uk/common-health-questions/food-and-diet/what-should-my-daily-intake-of-calories-be/

  10. Joy, E., Kussman, A., & Nattiv, A. (2016). 2016 update on eating disorders in athletes: A comprehensive narrative review with a focus on clinical assessment and management. Br J Sports Med, 50(3), 154-162.

  11. Sundgot-Borgen, J. (1993). Prevalence of eating disorders in elite female athletes. International Journal of Sport Nutrition and Exercise Metabolism, 3(1), 29-40.

  12. Sundgot-Borgen, J., & Torstveit, M. K. (2004). Prevalence of eating disorders in elite athletes is higher than in the general population. Clinical journal of sport medicine, 14(1), 25-32.

  13. Martinsen, M., & Sundgot-Borgen, J. (2013). Higher prevalence of eating disorders among adolescent elite athletes than controls. Medicine & Science in Sports & Exercise, 45(6), 1188-1197.

  14. Thiemann, P., Legenbauer, T., Vocks, S., Platen, P., Auyeung, B., & Herpertz, S. (2015). Eating disorders and their putative risk factors among female German professional athletes. European Eating Disorders Review, 23(4), 269-276.

  15. Bruserud, I. S., Roelants, M., Oehme, N. H. B., Madsen, A., Eide, G. E., Bjerknes, R., . . . Juliusson, P. B. (2020). References for Ultrasound Staging of Breast Maturation, Tanner Breast Staging, Pubic Hair, and Menarche in Norwegian Girls. The Journal of Clinical Endocrinology & Metabolism, 105(5), dgaa107.

  16. Gynecologists, A. C. o. O. a. (2015). Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Committee Opinion No. 651. Obstret Gynecol, 126, 126:e143-126.

  17. Norsk barnelegeforening. (2017). 2.6 Manglende eller forsinket pubertet. Retrieved from https://www.helsebiblioteket.no/pediatriveiledere?menuitemkeylev1=5962&menuitemkeylev2=5964&key=144409

  18. Medicine, P. C. o. t. A. S. f. R. (2004). Current evaluation of amenorrhea. Fertility and sterility, 82, 33-39.

  19. Calthorpe, L., Brage, S., & Ong, K. K. (2019). Systematic review and meta‐analysis of the association between childhood physical activity and age at menarche. Acta Paediatrica, 108(6), 1008-1015.

  20. Beals, K. A., & Manore, M. M. (2002). Disorders of the female athlete triad among collegiate athletes. International Journal of Sport Nutrition and Exercise Metabolism, 12(3), 281-293.

  21. Schneider, J. E. (2004). Energy balance and reproduction. Physiology & behavior, 81(2), 289-317.

  22. Drinkwater, B. L., Loucks, A., Sherman, R. T., Sundgot-Borgen, J., & Thompson, R. A. (2005). Position Stand on the Female Athlete Triad.

  23. Nattiv, A., Loucks, A. B., Manore, M. M., Sanborn, C. F., Sundgot-Borgen, J., & Warren, a. M. P. (2007). The Female Athlete Triad. Med. Sci. Sports Exerc, 39(10), 1867-1882.

  24. Otis, C. L., Drinkwater, B., Johnson, M., Loucks, A., & Wilmore, J. (1997). ACSM position stand: The Female Athlete Triad. Medicine & Science in Sports & Exercise, 29(5), i-ix.

  25. Nose‐Ogura, S., Harada, M., Hiraike, O., Osuga, Y., & Fujii, T. (2018). Management of the Female Athlete Triad. Journal of Obstetrics and Gynaecology Research, 44(6), 1007-1014.

  26. Statuta, S. M. (2020). The Female Athlete Triad, Relative Energy Deficiency in Sport, and the Male Athlete Triad: The Exploration of Low-Energy Syndromes in Athletes. Current sports medicine reports, 19(2), 43-44.

  27. De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., . . . 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, May 2013. Br J Sports Med, 48(4), 289-289.

  28. Matzkin, E., Curry, E. J., & Whitlock, K. (2015). Female Athlete Triad: past, present, and future. JAAOS-Journal of the American Academy of Orthopaedic Surgeons, 23(7), 424-432.

  29. U.S. Department of Health and Human Services, H. Appendix 2. Estimated Calorie Needs per Day, by Age, Sex, and Physical Activity Level. Retrieved from https://health.gov/our-work/food-nutrition/2015-2020-dietary-guidelines/guidelines/appendix-2/

  30. National Health Service, N. (2019). What should my daily intake of calories be? Retrieved from https://www.nhs.uk/common-health-questions/food-and-diet/what-should-my-daily-intake-of-calories-be/

  31. Joy, E., Kussman, A., & Nattiv, A. (2016). 2016 update on eating disorders in athletes: A comprehensive narrative review with a focus on clinical assessment and management. Br J Sports Med, 50(3), 154-162.

  32. Sundgot-Borgen, J. (1993). Prevalence of eating disorders in elite female athletes. International Journal of Sport Nutrition and Exercise Metabolism, 3(1), 29-40.

  33. Sundgot-Borgen, J., & Torstveit, M. K. (2004). Prevalence of eating disorders in elite athletes is higher than in the general population. Clinical journal of sport medicine, 14(1), 25-32.

  34. Martinsen, M., & Sundgot-Borgen, J. (2013). Higher prevalence of eating disorders among adolescent elite athletes than controls. Medicine & Science in Sports & Exercise, 45(6), 1188-1197.

  35. Thiemann, P., Legenbauer, T., Vocks, S., Platen, P., Auyeung, B., & Herpertz, S. (2015). Eating disorders and their putative risk factors among female German professional athletes. European Eating Disorders Review, 23(4), 269-276.

  36. Gynecologists, A. C. o. O. a. (2015). Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Committee Opinion No. 651. Obstret Gynecol, 126, 126:e143-126.

  37. Medicine, P. C. o. t. A. S. f. R. (2004). Current evaluation of amenorrhea. Fertility and sterility, 82, 33-39.

  38. Calthorpe, L., Brage, S., & Ong, K. K. (2019). Systematic review and meta‐analysis of the association between childhood physical activity and age at menarche. Acta Paediatrica, 108(6), 1008-1015.

  39. Beals, K. A., & Manore, M. M. (2002). Disorders of the Female Athlete Triad among collegiate athletes. International Journal of Sport Nutrition and Exercise Metabolism, 12(3), 281-293.

  40. Schneider, J. E. (2004). Energy balance and reproduction. Physiology & behavior, 81(2), 289-317.

Not getting your period might be convenient, but it is not normal.

Stable weight and low energy availability can coexist

 

Energy deficient athletes often has low body weight, which makes it difficult to use this as evidence that the athlete consumes enough calories. For most of us, this would seem as a paradox, since we know that the only way to lose weight is to eat less calories than we consume.

 

The reason for this is that when energy availability is low, the body depresses physiological functions to save energy. This reduces the energy needs so that less calories are needed to maintain energy balance. This means that an athlete can be in a state of low energy availability and energy balance at the same time.

 

Because of this, stable weight cannot be used as proof that the athlete consumes enough calories. However, underweight athletes with a BMI of <17.5 likely has low energy stores (7).

 

Eating disorders in female athletes

 

Eating disorders are more common among female athletes than in the general population (10). Several studies on Norwegian adolescents shows that eating disorders are far more prevalent among sports colleges (15-20 %) t % with an eating disorder there are far more that has an eating disorder among college athletes than other colleges (11-13).

 

We also see that rates of eating disorders are higher in aesthetic sports, in sports where lower weight is seen as advantageous, and in weight-class sports (11,12,14).

 

The incidence of eating disorders among amenorrhoeic women are particularly high. In one study, 62 % of amenorrhoeic patients were diagnosed with an eating disorder, compared with 11 % in the normal menstruation group (4).

 

The most common eating disorder is a group called EDNOS (eating disorder not otherwise specified). EDNOS is an eating disorder that does not meet the criteria for anorexia nervosa, bulimia nervosa or binge eating disorder. It often consist of cycles of restricting food, then bingeing.

Menstrual dysfunction

 

The most recognizable component of the Female Athlete Triad is the absence of menstruation (amenorrhea). We divide absence of menstruation into two groups:

 

  • Primary amenorrhea: Absence of first menstrual cycle by age 15

  • Secondary amenorrhea: Cessation of previously regular menses for 3 months or more, or irregular menses for more than 6 months

​

Primary amenorrhea

 

The average age of the first menstrual cycle (menarche) lies between 12-13 years in most developed countries, and 98 % of girls will have had their first menstrual cycle by age (15). Primary amenorrhea is because of this defined as the absence of menarche by age 15 (5).

 

Less than 2 % of all girls develops primary amenorrhea (15). Most cases of primary amenorrhea are the results of genetic or anatomical abnormalities, and only 3 % of cases can be attributed to low energy availability (16). Failure to menstruate by age 15 therefore requires medical investigation (16).

 

We see that the average age of the first menstrual cycle is higher in athletes than in non-athletes, especially in aesthetic sports like cheerleading, diving, gymnastics, rhythmic gymnastics, and ballet (2,4,17). In a study from 2002, 7.4 % of female college athletes did not get their first period before age 16 (primary amenorrhea was defined as "by 16 years" until 2004), and among athletes in aesthetic sports an astounding 22.2 % had not had their first period before age 16 (18).

 

It is believed that the difference in the prevalence of primary amenorrhea in athletes and non-athletes, for the most part, are related to low energy availability (2). Studies on animals clearly demonstrates that low energy availability before puberty suppresses growth and delays sexual development (19). In addition, it is also possible that delayed menarche and sexual development give advantages for young athletes in certain sports, which make them more likely to excel at certain sports, which might explain some of the difference in the prevalence of primary amenorrhea.

​

Cessation of menses (secondary amenorrhea)

​

The absence of previously regular menses for 3 months or irregular menses for more than 6 months is known as secondary amenorrhea (5). The most common cause of cessation of menses in female athletes are what is known as functional hypothalamic amenorrhea (FHA). In short, low energy availability disturbs the release of certain hormones from the brain which leads to lower estrogen levels in the body.

Low energy availability affects the release of gonadotrophic-releasing hormone (GnRH) from the hypothalamus. This affects the release of luteinizing hormone (LH) and follicle stimulating hormone from the pituitary gland, which in turn directly affects the release of estrogen from the ovaries(7).

 

It has previously been believed that exercise stress might affect menstrual function in female athletes, but this has been clearly refuted in scientific studies (1).  Some still use the term exercise induced amenorrhea instead of FHA, but this term gives the impression that secondary amenorrhea may be caused by the exercise itself and should therefore be used carefully.

 

The prevalence of secondary amenorrhea in college-aged women range from 2-5 %. The prevalence among female athletes is much higher, and studies have shown that as many as 44 % of dancers and 65 % of long-distance runners developed secondary amenorrhea (1). As with primary amenorrhea, the highest prevalences of secondary amenorrhea are found in endurance sports, aesthetic sports, and weigh class sports (1).

 

It is important to note that even though loss of menses is the most recognizable component of the Female Athlete Triad, it is only the endpoint of a spectrum with various degrees of dysfunction. The negative effects of the Female Athlete Triad, including bone loss, still occur in female athletes with subclinical menstrual disorders (disorders that are unnoticeable) (6).

 

Low bone mineral density

 

Low energy availability has both direct and indirect effects on bone mineral density (BMD). BMD in women is affected directly through changes metabolic hormones like insulin, cortisol, growth hormone, IGF-I, triiodothyronine, and leptin, which all play a part in increasing bone mass (2). These changes are not dependent on the presence of amenorrhea, which is why we also find mild-to-moderate reductions in BMD in females with subclinical menstrual disturbances (6).

 

BMD is also indirectly affected by low energy availability by causing FHA and reducing estrogen levels. Estrogen is a hormone that normally restrains bone resorption, so when levels are reduced bone resorption increases (2,7).

 

Bone loss in female athletes with FHA is often attributed to estrogen deficiency, and hormone replacement therapy and oral contraceptive pills have therefore been used in the past as a first-line treatment for athletes with amenorrhea. However, such therapies have failed to show a significant effect in preventing or treating bone loss in athletes with FHA (6,7). Studies have even shown that such therapies may cause further reductions in BMD in athletes (7).

 

This makes sense when we know that low energy availability also affects the release of other hormones that are important for bone mass. Artificially normalizing estrogen levels and thereby resuming menses does nothing to improve the underlying energy deficit, and it may provide a false sense of security so that the athlete continues to exercise with low energy availability. Hormone replacement therapy and oral contraceptive pills are therefore no longer recommended as a first-line treatment for treating FHA (4,6,7). The only way to effectively treat this condition is to increase energy availability.

The Female Athlete Triad is a spectrum disorder with various degrees of dysfunction in each of the three triad components. Based on (2). Illustration by Ken Fredin.

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Last updated: 12.05.2020
Ken Fredin
Physical therapist, Oslo, Norway
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