Dynamic Chiropractic Canada – June 1, 2014, Vol. 07, Issue 06

A Lesson in The Female Athlete Triad

By Michelle Laframboise, BKin (Hons), DC, FRCCSS(C)

Canadian female athletes in the early 1900s were excluded from sport participation because people thought that sport would cause excessive stress on the female body, most importantly, the reproductive organs. Fortunately, the landscape of Canadian female athletics has changed drastically in the past three decades and so has the thought processes of both the medical community as well as the general population in Canada.

This change in the belief system for the female athlete is largely due to the induction of Title IX in the United States of America in 1972. Title IX mandated equal access for sport participation in schools for males and females alike.1,2,3 Since the induction of Title IX in 1972 there has been a 1,000 percent increase in the number of female athletes participating in organized sport.

Sport participation has the ability to increase self-esteem and self-confidence and reduce risky behaviors such as drug abuse and teen pregnancy in female athletes. However, people face a unique set of psychological pressures from society and female seem to be highly affected. Western society has placed a strong emphasis on ultra-thinness as the ideal body shape and size for females and some female athletes. This cultural ideal places females at an increased risk of developing disordered eating patterns in an effort to conform to the ultra-thin ideal of Western society.1 The female athlete is not immune to societal pressures of ultra-thinness. Female athletes that have a desire to improve performance, a win at all cost mentality, combined with an overly controlling parent or coach, may have an increased risk for developing the female athlete triad.

female athlete - Copyright – Stock Photo / Register Mark The three spectrums include energy availability, menstrual function, and bone mineral density.4,7,8 These three spectrums occur on a sliding scale ranging from optimal energy availability, eumenorrhea, and optimal bone mineral density to low energy availability with or without an eating disorder, functional hypothalamic amenorrhea, and osteoporosis respectively.4 The three distinct clinical entities may occur alone or in combination with the other disorders. All three clinical entities may also occur at a sub-clinical level. The athletes' condition may move along each spectrum at a different rate, in one direction or the other, according to her diet and exercise habits.4,7,8

The American College of Sports Medicine (ACSM) position stand states that females that are at risk for developing the female athlete triad are the following:4,5,6

  1. Those that are required to have frequent weigh-ins
  2. Those with consequences for weight gain in sport
  3. The pressure to win at all costs
  4. Societal pressures to look a particular way

The female athlete triad most commonly presents in sports that with the following qualities:4,5,6

  1. Have subjective scoring of the female's performance
  2. Endurance sports
  3. Sports that emphasize low body weight
  4. Sports that have multiple weight categories
  5. Pre-pubertal athletic participation
  6. Sports that require the athlete to wear revealing or tight clothing

Energy Availability

Energy availability is defined as the amount of energy that remains in the body to be used during training and sport participation and performance. Female athletes experience energy deficiency with high-energy expenditure due to training without adequate compensation in energy intake via calories. Energy availability occurs along a spectrum ranging from optimal energy to low energy with or without an eating disorder or disordered eating.9 The prevalence of inadvertent low energy in female athletes is unknown. However, the prevalence of disordered eating among athletes is 28-62%.9

Clinical eating disorders including anorexia nervosa, bulimia nervosa, and eating disorders not otherwise specified are common in female athletes. According to the DSM IV, the prevalence of eating disorders in female athletes is 25-31%. Some female athletes may have no energy available for training and sport participation because they intentionally restrict daily caloric intake while others may fall into a negative energy balance because they are unaware of the calories needed for their specific sport.4,8,9,10,11,12

Menstrual Function

Menstrual function ranges from normal menstruation, also known as eumenorrhea to amenorrhea which means no menstruation > 3 months. In young adolescent female athletes under the age of eighteen the prevalence of menstrual dysfunction is 45-50% , adult female athletes over eighteen years of age the prevalence is estimated to be higher at 12-79%.9 Comparatively, the prevalence of menstrual dysfunction in adult non-athletes is approximately two to five percent.9 The prevalence of oligomenorrhea is extremely difficult to determine in adolescent females since menstrual cycle intervals of >35 days are encountered in approximately 65% of females during their first 12 months following menarche.9,13 Also, ovulatory status and menstrual cycle lengths are highly variable for the first five years post-menarche in females making taking menstrual cycles and diagnosing menstrual dysfunction very difficult.9,13

Eumenorrhea, "normal" menstrual cycle, is described as menstrual cycles lasting 28+7 days in duration.5,14 To maintain a physical state of eumenorrhea females need to consume approximately 45kcal/kg free fat mass (FFM) per day.5,14 FFM is described as the weight of the athlete minus the weight of their fat and water mass. Oligomenorrhea is defined as menstrual cycles lasting >35 days in duration and can occur in females consuming <30kcal/kg FFM per day. Lastly, the most severe form of menstrual dysfunction is amenorrhea which is described as menstrual cycles lasting >90 days in duration.4,5,9,14

There are two specific types of amenorrhea, primary and secondary. Firstly, primary amenorrhea occurs in females that are 15 years of age or older with the absence of menstruation but with the presence of other secondary sex characteristics. Furthermore, primary amenorrhea can also be described as females that are 14 years of age with no secondary sex characteristics present. Secondly, secondary amenorrhea occurs in females with a cessation of menstruation for >90 days that had once previously menstruated.4,5,9,14 The latter is common in female athletes and can be termed functional hypothalamic amenorrhea (FHA). A physician will be able to determine the type of amenorrhea that the female athlete is experiencing.

FHA occurs in female athletes due to low energy availability due to intentional or unintentional caloric restriction, this occurs when the athlete has disordered eating patterns or do not know the amount of energy that is required for their sport repectively.13,15 FHA is associated with increased physical activity leading to an increase in calories used and weight loss resulting in hypoestrogenism, ultimately resulting in a failure to obtain peak bone loss.13

Low energy availability in the female athlete results in changes in physiological and neuroendocrine response including a decrease in leptin, T3, insulin, IGF-, and plasma glucose, and a resultant increase in grelin, cortisol, and growth hormone. Physiological and neuroendocrine changes within the body will signal to the hypothalamus to stop producing gonado-tropin-releasing hormone (GnRH). A decrease in GnRH halts the releases of Luteinizing hormone (LH) and follicle stimulating hormone (FSH) from the pituitary gland. Further, an overall decrease in LH and FSH suppresses the ovaries from producing estrogen and progesterone leading to abnormal menses in the female athlete.13,15,16,17,18,19,20

Bone Mineral Density

Osteoporosis is a skeletal disorder that is characterized by compromised bone strength and can predispose a person to an increased risk of fracture throughout life. Osteoporosis can develop through a decline in bone mineral density during adulthood but can also develop through the failure to accumulate sufficient bone mass during adolescent years.5,13,21,22 Osteopenia is defined as a T-score between -1 and -2.5 and osteoporosis is < -2.5, this definition is only for females that are postmenopausal. However, the terms osteopenia and osteoporosis in pre-menopausal females are not used in the same manner.13 Z-scores are defined as the number of standard deviations above or below the mean for the patient's age, sex and ethnicity on a bone mineral density scan (DXA). T-scores are defined as the number of standard deviations above or below the mean for a healthy 30-year-old adult of the same sex and ethnicity as the patient.22

The International Society for Clinical Densitometry (ISCD) states that z-scores on DXA scans should be used in adolescent pre-menopausal females for comparison not t-scores.23 Osteoporosis in young females is diagnosed with a z-score below -2 together with the presence of a stress fracture, a clinically significant fracture history, disordered eating patterns, or hypogonadism.5,9,13,24 Currently the epidemiological data relating to bone mineral density and fractures in premenopausal females is lacking and there is no agreement on standards for adjusting bone mineral density for bone size, pubertal stage, skeletal maturity, or body composition. Thus, fracture risk for premenopausal females cannot be predicted similarly to postmenopausal females.9,13

According to the ACSM, recommending DXA scans for premenopausal females that are suspected to have the female athlete triad should follow the following guidelines; oligomenorrhea/amenorrhea > six months in duration, disordered eating/eating disorders for equal to or more than six months in duration, and the presence of a stress fracture or a fracture from minimal trauma.4 Therefore, the diagnosis of osteoporosis in young females is not made on densitometric criteria alone.9 Clinically significant fracture history is defined as a long bone fracture of the lower extremity, a compression fracture of the spine, or two or more long bone fractures of the upper extremities. DXA scans should be performed on the lumbar spine and forearm in female athletes. Females that participate in sports have an increase in weight bearing trabecular bone growth in the hip and lumbar spine, thus using the forearm is a unbiased region of the body. However, female athletes have increased bone mineral density of full body.4,9,25,26,27,28

Shockingly, the female athlete triad may not be a triad after all, emerging research shows evidence that the female athlete triad may be a tetrad of interconnected conditions.29,30,31 The new emerging component is endothelial dysfunction leading to heart disease. Endothelial dysfunction is proposed to be caused by a decrease in estrogen throughout the body ultimately from low energy availability.1,29,30,31

This a concerning condition because the sentinel event in cardiovascular disease pathogenesis is impaired endothelial function. Vessels contain estrogen receptors so they play a regulatory role in vascular function. Estrogen stimulates the production of endothelial nitric oxide synthase, leading to increased production of endothelial-derived nitric oxide ultimately leading to vasodilation.1,29 The problem is amenorrhea is similar to menopause due to low estrogen levels. Whether in a pre or post-menopause, low estrogen will theoretically cause impaired endothelial cell function and resultant impaired arterial dilation leading to cardiovascular disease.1,29,30,31

When there is a decrease in estrogen present in the vessels there will be an reduced in the flow mediated dilation within the vessels leading to a decrease in vasodilation. This decrease in vasodilation can have detrimental affects for athletes. Firstly, a loss of flow mediated dilation in conduit arteries may lead to a restriction in exercise-induced dilation of the vessels and limit maximum blood profusion to the tissues being supplied.1,31 This has the ability to lead to a reduction in exercise capacity and performance in athletes by restricting the amount of blood flow to critical muscles involved in exercise. Further, chronic endothelial dysfunction can lead to premature vascular changes by accelerating the development of atherosclerosis which in turn will lead to an increased risk of cardiovascular events.1,31


The management of the female athlete triad/tetrad is controversial in the literature. A team approach to care is the best way to surround the athlete and make the largest difference. Currently there is little knowledge about the clinical management of the female athlete triad, specifically, how to manage low bone mineral density and fracture risks in young females.9 Some physicians are prescribing estrogen therapy in the form of oral contraceptives (birth control pills) to improve bone health, but this is also very controversial and does not have efficacy in the current body of literature. Bisphosphonates have been shown in the literature to increase bone mineral density compared to the traditional use of calcium and vitamin D but this management strategy has not approved by the FDA as of late. Thus, the only management strategy that has been proven to increase bone mineral decrease, restore hormonal levels, and provide more energy for sport is increasing caloric intake.


  1. Lanser EM, Zach KN, Hoch AZ. The female athlete triad and endothelial dysfunction. PM & R?: the journal of injury, function, and rehabilitation. 2011;3(5):458-65.
  2. Lynch SL, Hoch AZ. The female runner: Gender Specifics. Clin Sports Med. 2010; 29:477-498.
  3. Mencias T, Noon M, Hoch AZ. Female athlete triad screening in National Collegiate Athletic Association Division I athletes: is the preparticipation evaluation form effective? Clinical journal of sport medicine?: official journal of the Canadian Academy of Sport Medicine. 2012;22(2):122-5.
  4. Otis CL, Drinkwater B, Johnson M, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc.1997;29:1669–1671.
  5. Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand. The female athlete triad. Medicine and science in sports and exercise. 2007;39(10):1867-82.
  6. Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. 1994 Apr; 13(2):405-18.
  7. Loucks AB. Energy availability, not body fatness, regulates reproductive function in women. Exerc. Sport Sci. Rev. 2003; 31(3):144-148.
  8. Thein-Nissenbaum JM, Carr KE. Female athlete triad syndrome in the high school athlete. Physical therapy in sport?: official journal of the Association of Chartered Physiotherapists in Sports Medicine. 2011;12(3):108-16.
  9. Ducher G, Turner AI, Kukuljan S, Pantano KJ, Carlson JI, Williams NI, De Souza MJ. Obstacles in the optimization of bone health outcomes in the female athlete triad. Sports Medicine. 2011;41(7): 587-607.
  10. Pantano KJ. Strategies used byPhysical therapy in sport?: official journal of the Association of Chartered Physiotherapists in Sports Medicine. 2009;10(1):3-11.
  11. Raymond-Baker P, Petroczi A, Quested E. Assessment of nutritional knowledge in female athletes susceptible to the female athlete triad syndrome. Journal of Occupational Medicine and Toxicology. 2007; 2(10): 1-11.
  12. Brunet M. Female athlete triad. Clinics in sports medicine. 2005;24(3):623-36
  13. Manore MM, Kam LC, Loucks AB. The female athlete triad: components, nutrition issues, and health consequences. Journal of sports sciences. 2007;25 Suppl 1(January 2012):S61-71.
  14. Loucks AB, Nattiv A. Essay: The female athlete triad. The Lancet 2005;366:S49-S50.
  15. Vescovi JD, Jamal SA, De Souza MJ. Strategies to reverse bone loss in women with functional hypothalamic amenorrhea: a systematic review of the literature. Osteoporosis International. 2008:19:465-478.
  16. Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 2004; 287:R1277-96.
  17. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003; 88(1):297-311.
  18. Laughlin GA, Yen SS (1996) Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 81:4301–4309
  19. Thong FS, McLean C, Graham TE. Plasma leptin in female athletes: Relationship with body fat, reproductive, nutritional, and endocrine factors. Journal of Applied Physiology. 200;88:2037 – 2044.
  20. Ackerman KE, Skrinar GS, Medvedova E, Misra M, Miller KK. Estradiol levels predict bone mineral density in male collegiate athletes: a pilot study. Clinical Endocrinology 2012; 76(3):339-345.
  21. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis and Therapy. Osteoporosis prevention, diagnosis, and therapy. Journal of the American Medical Association. 2001;285:785 – 795.
  22. Burr DB. The contribution of the organic matrix to bone's material properties. Bone. 2002;31:8 – 11.
  23. International Society for Clinical Densitometry Position Development Conference. The diagnosis of osteoporosis in men, premenopausal women and children. J Clin Densitom 2004; 7:17-26.
  24. Khan KM, Liu-Ambrose T, Sran MM, et al. New criteria for female athlete triad syndrome? Br J Sports Med 2002; 36:10-3.
  25. Hind K. Recovery of bone mineral density and fertility in a former amenorrheic athlete. J Sports Sci Med 2008; 7:415-8.
  26. Gremion G, Rizzoli R, Slosman D et al. Olio-amenorrheic long-distance runners may lose more bone in spine than in femur. Med Sci Sports Exerc 2001 Jan; 33 (1); 15-21.
  27. Braam LA, Knapen MH, Geusens P, Brouns F, Vermeer C. Factors affecting bone loss in female endurance athletes: A two year follow-up study. American Journal of Sports Medicine. 2003;31(6):889–895.
  28. Gordon CM, Lawrence NM. Amenorrhea and bone health in adolescent and young women. Obstetrics & Gynecology. 2003; 15(5): 377-384.
  29. Hoch AZ, Papanek P, Szabo A, et al. Association between the female athlete triad and endothelial dysfunction in dancers. Clinical journal of sport medicine?: official journal of the Canadian Academy of Sport Medicine. 2011;21(2):119-25.
  30. Hoch AZ, Lal S, Jurva JW, Gutterman DD. The female athlete trid and cardiovascular dysfunction. Physical Medicine and Rehabilitation Clinics of North America. 2007; 18(3): 385-400.
  31. Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, Hirschberg AL. Oral contraceptives improve endothelial function in amenorrheic athletes. The Journal of clinical endocrinology and metabolism. 2005;90(6):3162-7.

Dr. Michelle Laframboise is a sports fellow with the Royal College of Chiropractic Sports Sciences and is currently serving as chair of the public health committee. In addition to treating professional, Olympic and recreational athletes in practice at Back to Function in Orillia, Ontario, she has served as medical staff for provincial and national soccer clubs, figure-skating competitions, mountain bike competitions, wrestling and Taekwondo competitions. She has served as medical manager for the Ontario winter and summer games, as well as currently serving as team doctor for a junior 'A' hockey team.

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