The Female Athlete Triad (2024)

Abstract

Keywords: female athlete triad, disordered eating, amenorrhea, bone mineral density

The female athlete triad (the triad) refers to a constellation of 3 clinical entities: menstrual dysfunction, low energy availability (with or without an eating disorder), and decreased bone mineral density (BMD). This complex disorder was first coined by the American College of Sports Medicine in 1992 after many experts in the field had noticed a pattern among adolescent and young adult female athlete patients.^92,133 Even though this condition has been described for 2 decades, there is still much debate about how the components of the triad interrelate and how clinicians should manage patients with this complicated condition.

Epidemiology

The prevalence of menstrual irregularities, disordered eating, and low BMD varies widely in the general population and in the athletic community. In women who participate in sports that emphasize aesthetics or leanness, such as ballet or running, the prevalence of secondary amenorrhea can be as high as 69%, compared with 2% to 5% in the general population.^{1,8,37,98,113}

Disordered eating—including a range of irregular eating behaviors that do not necessarily meet criteria for severe disorders, such as anorexia nervosa (AN) and bulimia nervosa (BN)—is also fairly common in the athletic community. Up to 70% of elite athletes competing in weight class sports (male and female) are dieting and have some type of disordered eating pattern with the goal to reduce weight before competition.¹¹⁸ The prevalence of clinical eating disorders among female elite athletes ranges from 16% to 47%.^{25,118,119,123} The differences in prevalence rates among studies are likely related to variability in the sports studied (eg, weight class or aesthetic sports versus ball games), different screening methods (eg, questionnaires versus interviews), intensity and ages of athletes, and other methodological differences.¹¹⁸ However, the various prevalence rates of eating disorders in athletes are still in stark contrast to the 0.5% and 10% prevalence among nonathletic men and women in the general population.^25,119

The prevalence of low BMD in the female athlete has been studied as well. The prevalence of osteopenia ranges from 22% to 50% in female athletes, with osteoporosis spanning 0% to 13%.⁶⁷ This compares to the 12% and 2.3% prevalence reported in the average population, respectively.⁹³ However, these percentages are based on T-Scores, a diagnostic measure previously used in research and clinical settings that is no longer applicable to premenopausal women. More recently, when assessing bone density in the adolescent population or in any premenopausal woman, Z-Scores are utilized to determine low bone density for age and osteoporosis.^49,59 The reason for using Z-Scores (which compare DXA results among age-matched peers) instead of T-Scores (which compare DXA results of postmenopausal women to young adult women in their 20s) is that adolescent patients are still growing and not expected to have achieved the BMD of women outside their age group.⁴⁹ The International Society for Clinical Densitometry has defined a Z-Score of ≤ −2.0 SD as “below expected range for age” and a Z-Score > −2.0 SD as “within the expected range for age.”⁵⁹ Because athletes participating in weightbearing activities typically have higher BMD than nonathletes,¹²¹ the American College of Sports Medicine defines “low BMD” in an athlete as a Z-Score between −1 and −2 along with clinical risk factors for fracture (eg, decreased energy availability, amenorrhea, history of stress fractures). It considers “osteoporosis” in an athlete to be a BMD Z-Score ≤ −2.0 with clinical risk factors for fracture (Table 1).⁹³

It is difficult to assess the pervasiveness of the triad when considered separately. One study examining female athletes found that the prevalence of all 3 components of the triad was 4.3%, not far off from the 3.4% found among healthy controls.¹²⁴ However, the prevalence of 2 components of the triad ranged from 5.4% to 26.6%.¹²⁴

The findings in these studies indicate that while the number of athletes suffering from all 3 aspects of the triad simultaneously is fairly low, there are still many young women who are affected by some component of the spectrum of the disease. It is also important to realize that not all components of the triad need to be present concurrently for a female athlete to suffer negative health sequelae of the triad, as the 3 components may have different time sequences of presentation.

Menstrual Dysfunction

Menstrual dysfunction in the female athlete includes a wide spectrum of disorders. The most commonly discussed menstrual abnormality is amenorrhea, which is generally defined as the absence of menses 3 months or more, but can be subcategorized into primary and secondary types. Primary amenorrhea refers to a delay in the age of menarche (no menses by age 15 years in the presence of normal secondary sexual development or within 5 years after breast development if that occurs before the age of 10 years).⁵ Secondary amenorrhea is a loss of menses after menarche. Other types of menstrual irregularity include anovulation, luteal phase deficiency, and oligomenorrhea (Table 2).⁹⁶

Amenorrhea can be caused by a variety of diseases and genetic abnormalities, as well as energy deficiency and even stress.¹²⁶ The type of amenorrhea resulting from changes in energy availability is functional hypothalamic amenorrhea (FHA). FHA is characterized by the absence of menses due to suppression of the hypothalamic-pituitary-ovarian axis, without an identifiable anatomic or organic cause.^48,87 This type of amenorrhea, commonly associated with exercising and stress, is most relevant to the female athlete.⁸⁶ FHA is caused by an alteration in gonadotropin-releasing hormone pulsatility,⁴⁸ which in turn causes a disruption of luteinizing hormone pulses from the pituitary and gonadal steroid release from the ovaries.⁸⁶ It reflects a state of estrogen deficiency, which may be one of the causes of decreased BMD.⁸⁵ FHA may also be associated with several physiological changes, including overactivity of the hypothalamic-pituitary-adrenal axis (causing an increase in cortisol release) and disturbances of the hypothalamic-pituitary-thyroid axis (resulting in a “sick euthyroid” pattern).²¹ Leptin, a cytokine expressed by adipose tissue and strongly associated with fat mass, is lower in the amenorrheic athlete, most likely due to changes in body composition, particularly a decrease in fat mass.²⁸ Since leptin has a positive effect on gonadotropin-releasing hormone secretion and regulates the release of gonadotropins,²⁸ its deficiency contributes to the loss of menses. In amenorrheic athletes, luteinizing hormone pulsatility is disrupted while pituitary responsiveness to gonadotropin-releasing hormone is increased, causing amenorrhea of a hypothalamic origin.^80,125

Energy Availability

Energy availability is the amount of dietary energy for all physiologic functions after accounting for energy expenditure from exercise.⁹³ Low energy availability may be the result of an eating disorder but can also occur in the absence of a psychiatric diagnosis such as AN or BN. Athletes may have disordered eating simply by unknowingly failing to attain their energy requirements secondary to time constraints or lack of nutritional knowledge.³³ Some studies have also found that athletes often lack the appetite necessary to promote food intake as compensation for energy expenditure from intense exercise regimens.^22,78

Female athletes are at risk of developing eating disorders due to pressure to maintain a low body weight along with poor guidance about nutrition and weight loss from the athletic community.⁹⁵ Many have placed blame on the coach, who often fails to teach athletes about healthy dieting or cultivates an environment in which weight loss is encouraged regardless of the methods employed to attain it.^33,116 Disordered eating and amenorrhea are most common among sports that emphasize leanness, aesthetics, a weight class, or endurance,^33,78,95 including gymnastics, ballet, figure skating, lightweight rowing, and running.^{32,79,109,111}

There is a wide spectrum of disordered eating among athletes that ranges from simple dieting to clinically defined eating disorders such as AN, BN, and an eating disorder not otherwise specified (EDNOS) (Table 3). Anorexia athletica is a term used by some researchers to describe a disordered eating pattern seen in the female athlete who has an intense fear of gaining weight, even though she is underweight.¹¹⁹ Women with anorexia athletica reduce their energy intake and exercise excessively. They may display features of AN and BN without meeting strict criteria for these diagnoses.¹¹⁹

Among female athletes, there also exist several different forms of dieting that fall on a continuum. Healthy dieting is considered a modest lowering of daily calories, while harmful dieting or disordered eating includes restrictive behaviors, such as fasting, skipping meals, use of diet pills or laxatives, and binging and purging.^11,108 Some athletes practice what has been called dietary restraint, an intent to limit food intake, regardless of how successful it is in execution.¹¹

Bone Health

The greatest accretion of bone mass happens during puberty.^43,44 Maximal increases in bone mass accrual occur between 11 and 14 years of age in girls.⁸⁹ Menarche is a signal of bone mass growth, and 25% of bone mass accrual occurs in the 2 years that surround menarche.^115,122 Generally, young healthy women achieve 92% of their total body bone mineral content by 18 years of age and approximately 99% by age 26 years.⁵⁶ Bone loss usually occurs later with menopause and aging.⁹

In young female athletes with the triad, a compromise in bone strength, ranging from low BMD and stress fractures to osteoporosis, may occur at a much younger age.¹⁵ Several different components contribute to bone strength, including bone mineral content, BMD, bone microarchitecture, and bone remodeling.¹⁰⁵ Bone remodeling, or bone turnover, is a constant process of bone formation and matrix development by osteoblasts and bone breakdown by osteoclasts. When this process is interrupted, bone is weakened and more prone to injury.⁶³

Healthy athletes tend to have a higher BMD than their nonathletic counterparts as physical activity, particularly weightbearing exercise has a beneficial effect on bone accrual and architecture.⁸⁴ High-impact physical activity increases bone density in women.⁸⁴ Exercise can even cause a 4% to 5% gain in bone accrual in prepubertal children.⁴⁰ Despite similar weightbearing exercise, amenorrheic athletes have lower BMD than their eumenorrheic counterparts.^99,106 In fact, amenorrheic athletes have 10% to 20% less lumbar spine BMD than eumenorrheic athletes.^20,35 Oligomenorrhea and amenorrhea can be detrimental to bone because they are hypoestrogenic states.³⁴ Since estrogen normally inhibits osteoclast activity, a lack of this important hormone may cause disruption of bone remodeling and accelerated bone resorption.¹⁰² As a result, menstrual status in these young female athletes may override the beneficial effects of physical activity on bone.

Complications of the Triad

Several health consequences occur in athletes with the triad. Menstrual dysfunction may lead to infertility due to lack of ovarian follicular development, anovulation, or luteal-phase defects.⁹³ Alternatively, in some young women recovering from the triad, while menses are being restored, premature ovulation may occur and result in unexpected pregnancy in the absence of contraception.⁹³ There are also negative consequences associated with hypoestrogenism. Low levels of estrogen can cause endothelial dysfunction, resulting in cardiovascular disease.^72,97 Women with hypoestrogenism have elevated low-density lipoprotein cholesterol levels.¹⁰¹ Women with the triad also have decreased immune function^90,94 and impaired skeletal muscle oxidative metabolism.⁵⁵

Many athletes with low bone density and/or menstrual irregularity suffer from stress fractures.^{18,19,23,70,76,112} The most frequent site is the tibia, accounting for 25% to 63% of all stress fractures.^13,19,60,112 Menstrual irregularity increases this risk of injury.^60,76,91,112 Amenorrheic athletes have 2 to 4 times greater risk for stress fracture than their eumenorrheic counterparts.¹⁷

Low bone density also puts these women at risk for suboptimal peak bone mass acquisition. While the effects may not be immediate after diagnosis of the triad, a decrease in peak skeletal BMD, along with skeletal demineralization occurring slowly over time, can lead to these conditions.⁹³ Similarly, the resumption of menses does not resolve BMD issues immediately but starts the necessary rebuilding of bone to decrease the risk of future osteoporosis and fracture.⁹³ Depending on the age of the patient, the duration of the triad, and the time to recovery, BMD may stabilize and even improve but not necessarily “catch up” to normal, age-appropriate BMD.^12,34 In adulthood, a 10% decrease in BMD is associated with a two- to threefold increase in fracture risk.⁶⁸

Decreased energy availability may also have serious consequences. It may cause nutritional deficits; many of these athletes limit protein, carbohydrate, and fat intake and increase fiber intake.^82,129 A deficiency in macronutrients, particularly essential amino acids and fatty acids, can be detrimental to the body’s ability to build bone, maintain muscle mass, repair damaged tissue, and recover from injury.⁸³

Disordered eating associated with low energy availability also has serious psychological ramifications, including depression, low self-esteem, and various anxiety disorders.⁷³ It can be a slippery slope, leading to body image issues and severe eating disorders.¹¹⁶ A 2011 meta-analysis examined outcomes in patients with AN during 166 642 person years, BN during 32 798 person years, and EDNOS during 22 644 person years.⁶ There was an increased mortality rate among women with disordered eating, especially associated with AN. The standardized mortality ratios were 5.86 for AN, 1.93 for BN, and 1.92 for EDNOS; 20% of those with AN who died had committed suicide.⁶

Regardless of the severity of symptoms stemming from the components of the triad, it is important for health care professionals as well as coaches and nutritionists involved in these female athletes’ care to be cognizant of the risks and potential consequences of the syndrome.

Screening and Diagnosis

The greatest challenge in treating young female athletes with the triad may be making the initial diagnosis of the condition. Screening for elements of the triad should take place at preparticipation physical examinations or at annual health checkups. Clinicians may also have the opportunity to make a diagnosis when athletes present with related problems, such as amenorrhea or recurrent injury, particularly multiple stress fractures. It is important to screen any athlete who presents with 1 component of the triad for the others.⁹³

Screening for the triad should start with a detailed, guided history, including questions regarding physical activity, past injuries, diet and eating behaviors, and menstrual history.⁸³ Focused questions regarding eating habits and exercise energy expenditure can be helpful in determining energy balance in these young athletes. Patients should be asked about binging or purging behaviors and any recent psychosocial stressors.⁴⁸ Athletes with disordered eating may reveal a fear of weight gain or issues with body image and should be referred to a mental health care professional for further guidance and treatment in those cases.⁹³ Questions about family history and maternal age of menarche may be helpful when assessing menstrual status. When evaluating primary or secondary amenorrhea, etiologies such as thyroid disorders (hyper- or hypothyroidism), pituitary tumors (ie, a prolactinoma), polycystic ovarian syndrome, intrauterine devices, and medications (antipsychotic agents, combined oral contraceptive pills, or depot medroxyprogesterone acetate injections) should be considered.⁴⁸

On physical examination, signs associated with the triad include bradycardia, orthostatic hypotension, and hypothermia, which are common among young women of low weight but are also common in hypothyroidism.¹⁶ Many women with eating disorders show physical signs of persistent vomiting (Russell sign, callused knuckles), gingival abrasions, parotid enlargement, and loss of dental enamel.⁴⁸ Women with AN may also present with dry skin, hypercarotenemia, lanugo, and acrocyanosis.¹⁶ Because hypothalamic amenorrhea is a diagnosis of exclusion, other etiologies must be ruled out.⁴⁸ For example, hyperandrogenism (hirsutism and acne) may suggest polycystic ovarian syndrome or, more rarely, an androgen-secreting tumor or late-onset adrenal hyperplasia as the cause of amenorrhea. Physical signs of hyperthyroidism include enlarged thyroid, proptosis, tremor, or increased heart rate. The musculoskeletal examination should include palpation of the spine and shins. If pain is detected, a tuning fork assessment for vibratory pain and/or radiological imaging may be warranted to rule out stress fracture.

In a young female athlete who is suspected of having disordered eating, a complete blood count, electrolytes, urea nitrogen, creatinine, glucose, calcium, phosphorus, magnesium, and albumin should be checked.¹²⁷ In athletes presenting with amenorrhea, laboratory testing should include a complete blood count and chemistry panel to rule out chronic illnesses associated with amenorrhea, beta-human chorionic gonadotropin testing to rule out pregnancy, thyroid-stimulating hormone and free thyroxine to test for primary and central thyroid dysfunction, prolactin to assess for a pituitary mass, and follicle-stimulating hormone to rule out ovarian insufficiency.⁴⁸ If hyperandrogenism is in the differential diagnosis, luteinizing hormone (to check for a luteinizing hormone:follicle-stimulating hormone ratio greater than 2:1, suggesting polycystic ovarian syndrome),⁷¹ total testosterone and sex hormone binding globulin (to calculate the free androgen index),¹³² and steroids dehydroepiandrosterone sulfate and 17-hydroxyprogesterone should also be included.^7,77 Many patients with hypothalamic amenorrhea present with a decreased estradiol level, but this is not necessary for diagnosis.⁴⁸ A progesterone challenge test may be considered in patients as part of the initial workup or after mild weight gain to assess estrogen status. The progesterone challenge test is performed by giving oral medroxyprogesterone acetate (Provera), 10 mg daily for 5 to 10 days. Withdrawal bleeding 2 to 7 days later confirms that there is some estradiol present and there is not an outflow obstruction (see Table 4).⁵⁸

BMD should be assessed in all young women with a history of hypoestrogenism (ie, amenorrhea), disordered eating, and/or a history of stress fractures or a fracture from minimal trauma.⁶⁶ There are several imaging modalities available for analysis of bone structure. Dual-energy x-ray absorptiometry (DXA) is most commonly used to assess BMD because of its speed, precision, safety, low cost, and widespread availability.^9,10,49 DXA is one of the few imaging techniques with reference to pediatric data.¹⁰ It can measure bone mass and areal BMD for the whole body as well as specific regions such as the lumbar spine, hip, and distal radius.¹⁰ Measurement of spine and hip are standard for young adult women.^54,65 Measurement of the spine and whole body is preferred in adolescents because of the lack of precision in the hip region in identifying anatomic landmarks.⁹ If symptoms of the triad persist, low DXA BMD results should be reevaluated every 12 months, ideally with the same machine to ensure comparison with accuracy and precision.

Bone microarchitecture is an important factor to consider when assessing bone strength and fragility. Amenorrheic athletes have impaired bone microarchitecture compared with their eumenorrheic and nonathletic counterparts, which may increase fracture risk.² Unfortunately, DXA is unable to directly measure bone geometry and microstructure. High-resolution peripheral quantitative computed tomography is employed in research settings to determine these parameters. It assesses bone structure and distinguishes between cortical and trabecular bone elements, which further details the effects of menstrual status and exercise on bone health.²⁴

Treatment

There is still much debate on the best method of treatment for young female athletes with the triad. A multidisciplinary approach is usually necessary for recovery. Support from a primary care and/or sports physician, as well as a nutritionist or dietitian, psychiatrist or therapist, the team coach, and family members, is extremely important throughout the rehabilitation process.

The primary goal of treatment is restoration of regular menstrual cycling and enhancement of BMD. The first step in attaining these goals is modification of the diet and exercise regimens to increase overall energy availability (ie, reduce energy expenditure and maximize energy intake). Athletes may need to increase energy availability to at least 30 kcal/kg of fat-free mass per day to resume menses.⁸¹ LH levels were measured in 29 regularly menstruating sedentary women (18-30 years old) with controlled levels of energy expenditure and intake. Luteinizing hormone pulsatility was disrupted when caloric intake was restricted to < 30 kcal/kg fat-free mass per day in most women.⁸¹ These exact numbers might not be applicable to all women; each patient has a different response to changes in energy balance. There may also be differences in acute versus chronic energy restriction.

The concurrent increase in body weight that occurs with alteration of diet and exercise and resumption of menses improves BMD in previously amenorrheic athletes.^36,41,74 However, this change is not immediate and does not always fully undo the negative effects of amenorrhea on bone health. In fact, increases in BMD are small and short-lived if not achieved at a young enough age and sustained.⁶⁴

Many athletes are resistant to reductions in training or alterations in their diet. Therefore, other methods of treatment may need to be explored while concurrently emphasizing the need to improve the energy balance. Drug intervention is often considered for these women to help restore menstruation or provide adequate hormonal supplementation. The oral contraceptive pill (OCP) contains estrogen and progestin and has few side effects.³ It also has the added benefit of being an effective form of contraception for young women. It has been widely used in adolescents suffering from amenorrhea and low bone density, even though data are unresolved regarding its benefits in this patient population. Some studies have found hormonal replacement therapy with an OCP to improve BMD,^{26,31,52,53,57,100} but other research has shown no significant effect.^42,69,110 An OCP can also have a masking effect in the amenorrheic athlete with the triad. OCPs can cause a resumption of menstrual bleeding, giving young women a false sense of improvement without any change in energy availability. It may be helpful to allow athletes time to alter their workout and dietary habits before starting an OCP to ensure a natural return of their menstrual cycles and improvement in BMD.

Because of inconclusive data regarding OCPs, research has recently shifted toward finding other ways of delivering estrogen replacement that may be more effective in improving bone density. Transdermal estrogen may have a better impact on bone than an OCP because of its minimal effect on insulin-like growth factor 1, a bone trophic hormone essential for bone formation and remodeling. Oral estrogen is known to decrease systemic insulin-like growth factor 1, while transdermal formulations maintain or increase concentrations of this growth factor.^61,130 Transdermal estrogen replacement may be more effective than OCPs in maintaining or increasing BMD and preventing future fracture risk, as has been demonstrated in postmenopausal women.^38,107,128 Because research on transdermal estrogen has been performed mainly in postmenopausal women and not in young amenorrheic athletes, further research is needed to determine its utility as a treatment option in the triad.

In lieu of reliable data, treatment options other than estrogen and progestin have been explored. Mantzoros and colleagues examined leptin analog administration in women with functional hypothalamic amenorrhea. The majority of participants receiving daily subcutaneous leptin injections resumed menses.²⁷ However, thus far, intervention studies have been small and of short duration and therefore inconclusive regarding long-term effects on BMD.^27,131

It is generally accepted that optimizing vitamin D and calcium intake in young women is important for bone health, especially since vitamin D levels are often found to be low in this age group.^30,50,51 There is still debate regarding the optimal daily intake of vitamin D, but based on the 2011 report on dietary requirements for calcium and vitamin D from the Institute of Medicine, it is suggested that adolescents should ingest 1300 mg of calcium and 600 IU of vitamin D daily.¹⁰³ For premenopausal women, the recommended daily doses are 1000 mg of calcium and 600 IU of vitamin D.¹⁰³

Bisphosphonates (antiresorptive bone medications) are not recommended for bone density treatment in adolescents or young women. While bisphosphonates do improve bone density in the postmenopausal population³⁹ and adult women with AN,^46,88 they are not generally accepted as an option for reproductive age women, as they remain active in bones for many years and have a potential teratogenic effect in pregnancy. In addition, the low BMD in postmenopausal women is most often from increased bone loss, while the low BMD in the triad is usually from a lack of bone mass accretion during maturation. The efficacy of bisphosphonates in a younger population may not be as robust, and evidence of their use in the triad is lacking. However, bisphosphonates may have a role in a very select, high-risk population and may be used in conjunction with a physician specializing in osteoporosis management in young athletes. Bisphosphonate use should be closely monitored and accompanied by intense nutritional and exercise guidance.²⁹

There has also been a recent movement toward the use of mechanical stimulation to treat bone loss because it mimics impact physical activity. Pulsed electromagnetic fields increase BMD in ovariectomized rats,⁷⁵ as well as in postmenopausal women.¹²⁰ Vibratory platforms can reduce and possibly prevent bone mass loss after only 20 minutes of quiet standing^104,114 and were correlated with BMD increases in 1 study of adolescent girls.⁴⁵ Therefore, these methods of bone stimulation may be a treatment option for low BMD in athletes with the triad who must decrease their physical activity. These techniques may allow women to experience some of the benefits of impact loading without hours of exercise that may be detrimental to their bone health. Research is needed to determine the proper dose and effectiveness of this therapy in young athletes.

One of the greatest barriers to the treatment of young women with the triad is overcoming the psychological component of their condition. Athletes are often determined, competitive people, with perfectionist personalities. Changing their mentality and altering their regimen of diet and exercise can be quite difficult. For athletes who present with classic symptoms of a clinical eating disorder, it is paramount to involve appropriate mental healthcare professionals in their care and management (eg, consideration of a psychiatric medication prescription with follow-up and/or cognitive behavioral therapy). Having athletes with disordered eating agree to a “contract” that outlines their responsibilities as well as the goals of treatment may be helpful.^14,117 Such a document can include consequences, such as exclusion from training and competition, if certain parameters of the contract are not followed.

Currently, the best approach to the triad is early detection and prevention. Preparticipation physical examinations are a particularly good time to screen for signs and symptoms. An athlete presenting with 1 component of the triad should always be evaluated for the other 2. Clinicians should screen for the cardinal signs of the triad: recent decline in performance, changes in mood, dramatic weight loss, and frequent injury, particularly fractures. Health care professionals as well as coaches and athletic administrators should aim to educate athletes on how to optimize their energy availability and bone health to prevent injury. Open lines of communication can also be helpful in recognizing a problem early so that an intervention can occur before the consequences are too difficult to reverse.

Conclusion

The female athlete triad is a potentially serious condition affecting many young women. Low bone density is a dangerous consequence of the triad, and the degree of low BMD in young patients is greatly dependent on age of onset and duration of amenorrhea.⁴⁷ Low energy availability plays a crucial role in menstrual function and bone health. There are several different theories about the best approach to treating this complicated condition. However, it is universally accepted that triad prevention, early recognition, and a multidisciplinary treatment plan with a focus on proper nutrition and resumption of menses are extremely important and should be priorities among health care professionals, coaches, and other adults involved in the lives of female athletes.

References