Studies suggest that endurance athletes exhibit a higher risk of developing DE or EDs, menstrual dysfunction, and low bone mass compared with those participating in other sport types. While the loading nature of endurance sports can be characterized as less osteogenic than ball or other sports involving high- and odd-impact loads, endurance athletes are also at high risk of developing an energy deficit, which negatively impacts bone .

Previous studies document higher estimates of menstrual dysfunction among endurance runners spanning various ages and levels of competition. Reports indicate that up to 66 % of female competitive endurance runners exhibit menstrual disturbances [91–93], values that are approximately 3–5 times higher than the 5–15 % [94, 95] prevalence reported in normal, healthy young women and girls. Gibson et al. observed a 66 % prevalence of menstrual irregularity among 50 elite endurance runners, while Dusek et al., upon evaluation of 72 female athletes, found a 3 times higher prevalence of secondary amenorrhea among athletes compared with controls, with the highest prevalence of secondary amenorrhea (65 %) reported among female endurance runners [93, 96].

Additionally, it is established that adolescent, collegiate, and postcollegiate runners spanning a range of levels of competition exhibit lower bone mass than athletes in other sports. In studies among endurance runners, prevalence estimates of low bone mass are as high as 40 %, using a Z-score − 1.0 cutoff. This is significantly higher than the 5–10 % prevalence reported among non-endurance runner athletes, and the 16 % prevalence expected in a normal population distribution [91, 92]. Mudd et al., when comparing data from 99 collegiate athletes participating in 12 sport types, found that endurance runners had lower total body and lumbar spine BMD values when compared with gymnasts and softball players [97, 98]. Robinson et al. evaluated bone mass among a sample of collegiate gymnasts, runners, and nonathlete controls [98]. Runners exhibited significantly lower lumbar spine, femoral neck, and total body BMD compared with the other two groups [98].

Little research has evaluated eating attitudes and behaviors, menstrual function, and bone mass among female endurance cyclists. Unlike other endurance sports, more has been reported in male rather than female cyclists. Among these studies, male cyclists exhibit an increased pressure to lose weight, have elevated scores on the eating attitudes test (EAT), and have a higher use of diet pills, laxatives, and self-induced vomiting, particularly during competition [102]. Additionally, studies report lower levels of bone mass among endurance cyclists, particularly among male master cyclists with an average of 20 years of participation in the sport. According to Nichols et al., male master cyclists had significantly lower lumbar spine and total hip BMD compared with age-matched controls and young adult cyclists [103]. Additionally, 15 % of the male master cyclists exhibited BMD T-scores − 2.5, the cutoff used in the diagnosis of osteoporosis in older adults [103]. Further research is needed among female cyclists to better identify the prevalence of DE, menstrual dysfunction, and low bone mass.

The few studies evaluating swimmers also identified an elevated prevalence of DE. Da Costa and colleagues assessed eating attitudes and behaviors using three surveys among adolescent swimmers and reported a 44 % prevalence of DE [104] . Anderson and Petrie utilized the Eating Disorder Diagnosis questionnaire and found that approximately 28 % of collegiate swimmers met criteria for either subclinical DE or a clinical ED [105]. Additionally, among Norwegian elite athletes, swimmers exhibited lower BMD values than athletes in ball or power sports [106]. In a systematic review of 64 studies focused on swimmers’ bone mass, structure, and metabolism , most of the studies found similar BMD values in swimmers versus sedentary controls, but many showed lower BMD in swimmers versus other sport groups, including gymnasts, runners, volleyball players, soccer players, and basketball players [107]. This indicates that while swimming does not exert a weight-bearing, osteogenic effect on bone, it does not appear to be associated with a high prevalence of low BMD. There may be a lower rate of menstrual dysfunction and higher fat mass in swimmers versus athletes in leaner sports, which complicates conclusions regarding the additive effects of non-weight-bearing exercise in the setting of eumenorrhea. Future research is needed to investigate the prevalence of menstrual dysfunction among swimmers with better control for menstrual function and lean and fat mass.

One important concern of athletes participating in leanness activities is the focus on body appearance in their sports. For example, a high lean to fat mass ratio is important in sports such as figure skating, gymnastics, and sports dance for aesthetic reasons [80]. Aesthetic sports are associated with a negative self-perception during puberty because of body maturation, physiological, and behavioral changes [108]. Moreover, certain characteristics of some athletes such as competitiveness, concern with performance and body shape, and perfectionism, have also been associated with eating problems [109]. Therefore, all of these factors can influence athletes to start irregular eating behaviors, in order to improve performance and meet a specific body shape. Van Durme et al. showed that eating pathology is prevalent in aesthetic sports, especially in female athletes, and that eating concerns and sport-related factors such as competition anxiety could contribute to the dieting behavior of these athletes [110]. In general, studies of female skaters, dancers, and gymnasts have revealed a tendency toward energy-restricted diets, and high rates of clinical and subclinical EDs [79, 110–112]. One meta-analysis concluded that elite athletes in lean sports, especially dance, were at higher risk of developing EDs [109]. A large study of elite athletes showed that the prevalence of EDs in female athletes was as high as 42 % in aesthetic sports compared with 24 % in endurance , 17 % in technical, and 16 % in ball games sports [78]. Additionally, it is common to start aesthetic activities in early childhood. In a study of 5 and 7-year-old girls, those participating in aesthetic sports reported higher weight concerns than girls in nonaesthetic sports or no sports [113]. Over time, those who had reported high weight concerns or body dissatisfaction across ages 5 to 7 reported higher dietary restraint, poorer eating attitudes, and increased likelihood of dieting at age 9, regardless of their weight status [114]. A study in elite female synchronized skaters observed significant differences between perceived ideal and current body shape and reported a low mean energy intake of just 26 kcal/kg body weight [115], well below what would be required to fuel exercise expenditure and basic metabolic and reproductive functioning.

Menstrual dysfunction is more common in sports emphasizing thinness with a prevalence ranging between 1.4 and 27.7 % [86]. However, some studies have reported particularly higher prevalence of menstrual disorders in aesthetic athletes. A study including 311 female athletes, reported menstrual irregularities in 38.1 % of aesthetic athletes (including dance, sports, diving, and gymnastics) compared with 19 % in endurance athletes and team/anaerobic sports [116]. A meta-analysis showed that 36.5–70 % professional ballet dancers had a lifetime history of menstrual disturbances and also reported a 4-year incidence of secondary amenorrhea as high as 85 % [117]. Similarly, studies in gymnasts have shown high prevalence of menstrual irregularities (71.4–78 %) and delayed puberty [87, 118]. Delayed puberty has also been reported in figure skaters, especially in elite and more specialized pair skaters [119].

Aesthetic sports have been variably associated with bone impairment. Some studies have suggested that despite the high prevalence of menstrual irregularities and EDs, female gymnasts and figure skaters have improved BMD in weight-bearing bone sites [120, 121]. Stress fractures in figure skaters have been linked more to the excessive forces placed on the skeleton rather than lower BMD [122]. Moreover, gymnasts have shown improved BMD compared with runners, despite menstrual status [98, 123, 124]. A possible explanation is that the mechanical loading of this sport, may counterbalance the negative effect of menstrual disorders and hypoestrogenism. Conversely, other studies of gymnasts and dancers found lower BMD than other athletes and controls, and concluded that the protective effects of exercise on bone is lost in the presence of menstrual irregularities [125, 126]. A study in retired gymnasts showed greater spinal BMC and BMD, trabecular volumetric density, and strength in gymnasts without a history of amenorrhea , but not in those with a history of primary or secondary amenorrhea [126] . It is possible that weight-bearing exercise improves BMD when athletes do not have accompanying metabolic, menstrual or eating irregularities, and that bone impairment is more pronounced later in life, when the protective effect of exercise is lost.

Other athletes at higher risk of developing the Triad are those competing in sports with weight categories such as wrestling, judo, karate, and rowing. In these sports, athletes wish to gain a competitive advantage by obtaining the lowest possible body weight or weight category while maximizing strength [80]. It is known that athletes competing in combat sports periodically practice short-term weight fluctuations prior to a competition season. One study reported that almost 90 % of judoists participating in international tournaments had a rapid weight loss of 5–10 % of their body weight over a 7-day period [127]. Although weight reduction in these athletes is motivated mainly by optimization of performance, meeting sport-specific demands, and is often seasonal [128, 129], a high proportion of weight-class athletes are using extreme weight-control methods [130]. The rules of some sports may be associated with the risk of continuous dieting , energy deficit, and/or use of extreme weight loss methods that can be detrimental to health and performance [130]. Even though high-impact-loading sports have a protective effect on bone [131, 132] and wrestlers have increased BMD at the lumbar spine [133], chronic states of low energy availability and cyclic weight lost can have negative effects on health parameters such as nutritional status, hormonal status, and immune functions [128].

For instance, one study of adolescent female athletes showed that the exercise-induced osteogenic benefits were less when rowing training was associated with low estrogen and progesterone metabolite excretion [134]. Also a small study in lightweight female rowers showed that 76 % athletes had a history of menstrual irregularities and it was associated with lower lumbar BMD [135]. There is a lack of literature regarding the specific prevalence of Triad among female athletes competing in weight-class sports. However, there are several studies in which these sports are included and categorized as “leanness sports,” with the prevalence of all components of the Triad and stress fractures being higher than other sports [86, 87, 136]. Finally, small studies in male wrestlers have demonstrated hormonal alterations such as lower testosterone and estradiol levels, and found that estrogen was a more important predictor of BMD than testosterone in this population [137, 138]. This evidence suggests that female and male athletes competing in these sports could be at risk of hormonal, bone, and nutritional impairment.

There are other sports in which body composition and weight play an important role because of mechanical and gravitational factors. This is the case with ski jumping and high jump, which require vertical movements of the body, with fat mass being considered a disadvantage [80]. A lower body weight may result in improved speed in sports that require the body to be lifted against the earth’s gravitational field [139]. For this reason, most ski jumpers are underweight and can present with EDs. For instance, the mean BMI in ski jumpers has decreased from 23.6 kg/m² in 1970 to 19.4 kg/m² in 2002, with values as low as 16.4 kg/m² in World Cup athletes that year[139]. In an effort to prevent the myriad negative health effects on such athletes, there have been recent changes in the regulations of this sport in order to make it less attractive and even disadvantageous to be severely underweight. For instance, athletes with lower weight must have shorter skis, which represent an aerodynamic disadvantage that may compensate for the lower weight.

Weight concerns are also quite relevant in horseracing. Jockeys are required to have very low weight and strict weight control during the competitive seasons. Unfortunately, weight control measures in these athletes include saunas, smoking, excessive exercise, skipping meals, and restricting food intake in the 24 h prior to racing that certainly are detrimental to health [140, 141]. In one study of jockeys, energy intake was well below the recommendation for such athletes [142]. Furthermore, other studies have shown low BMD and disrupted hormonal activity in jockeys [143–145]. Thus, it is important to maintain a high level of suspicion to identify athletes at risk of the Triad, especially in sports with emphasis on lean appearance.

Several investigators have evaluated the prevalence of the Triad among adolescent athletes. Based on the original definition of the Triad (from the 1993 ACSM Position Statement) [150], including DE/EDs, amenorrhea, and osteoporosis , among 170 high school athletes participating in a range of interscholastic sports, there was an 18 % prevalence of DE/EDs based on the EDE-Q, 24 % prevalence of menstrual irregularity (amenorrhea or oligomenorrhea), and a 22 % prevalence of low bone mass (Z-score ≤ − 1) [90]. In another study, by Hoch et al., using the updated definition of the Triad (the 2007 ACSM Position Statement) [10], which includes low energy availability as the first component, there was a 36 % prevalence of low energy availability (defined as < 45 kcal/kg/lean body mass), a 54 % prevalence of menstrual abnormalities and a 16 % prevalence of low bone mass (Z-score ≤ − 2.0) [151]. In this latter study, the athletes exhibited a higher prevalence of menstrual abnormalities, but a lower prevalence of low bone mass compared with sedentary controls [151].

Barrack et al. identified female adolescent endurance runners as an athlete population with an elevated prevalence of low BMD and reported a 40 versus 10 % prevalence of BMD Z-scores < − 10.0, among runners compared with adolescent non-runner athletes [152]. In a subsequent investigation, risk factors associated with low bone mass among the adolescent runners included elevated dietary restraint, amenorrhea, and participating in five or more seasons of an endurance running sport [92]. In a 3-year follow-up among the high school runner sample (mean age of 16 years at baseline and age 19 years at follow-up) the authors found that despite an average approximate 10-pound weight gain during the 3 years, about 90 % of runners with low BMD at baseline continued to exhibit low bone mass at the follow-up assessment [153]. These findings underscore the importance of accruing sufficient bone mass during the adolescent years, since it may be difficult to significantly increase bone mass during and after the third decade of life [44].

Current literature indicates that males participating in certain weight-class sports are at risk of developing DE behaviors to cut weight. Wrestling stands as one of the highest profile sports associated with DE, as it is not uncommon for wrestlers to attempt competition in a weight class below their natural weight, as mentioned previously [102]. Behaviors reported among wrestlers to lose weight include self-induced vomiting, sauna use, excessive exercise, use of laxatives, diuretics, and wearing heavy clothing [102]. Misuse of these weight-cutting techniques has been associated with the death of at least three collegiate wrestlers [154]. As a result, new regulations have been implemented to promote the health and safety of the athletes, which included banning pathogenic behaviors and changing the timing of weigh-ins [102].

Other male athlete groups at risk of developing DE, altered hormone levels, and reduced bone mass include endurance runners and cyclists. As mentioned previously, male young adult endurance cyclists report increased pressure to lose weight, use of pathogenic behaviors, and DE, while male master cyclists exhibit reduced bone mass [102]. Several studies report significantly lower testosterone levels among male endurance runners compared with nonathlete controls [155–159], while other investigators identified lower lumbar spine BMD levels in male endurance runners compared with non-runner athletes [160] or nonathlete controls ([161]).

Interestingly, investigators report negative associations between running training volume and bone mass or sex hormones among male endurance runners [162, 163]. In these instances, running training volume may serve as a proxy for exercise energy expenditure, which may suggest that the insults to bone and reductions in the sex hormone levels may be due to an energy deficit, much like the effect of an energy drain on sex hormone levels and bone in the Female Athlete Triad. This is a notable finding since short-bout, explosive exercise movements are associated with increased testosterone levels [164]. These studies suggest that male, like female, endurance runners may be subject to similar hormone disruptions and bone-related risks.

While traditionally testosterone was thought to be the critical hormone in males for bone health , more recent research suggests that it is the conversion of androgens to estradiol that makes it beneficial to bone. In fact, in a study by Ackerman et al., estradiol levels, BMI, and resistance training were found to be more important determinants of BMD in male collegiate athletes (wrestlers, runners, and golfers) than testosterone [137]. Other male athlete sport groups with preliminary data potentially implicating them as an at-risk sport associated with behaviors and outcomes consistent with the Triad include ski jumping, sport climbing, sprint football, bodybuilding, weight lifting, rowing, and horseracing [102]. Future research is needed to more comprehensively outline male athlete’s risk profile and potential negative short- and long-term effects.

A multidisciplinary approach is required to treat and prevent further complications of Triad. Involvement of a primary-care physician and/or sport physician, dietician, psychiatrist or therapist, team coaches, and family members is necessary during recovery of athletes. There are non-pharmacology and pharmacology therapies for treating the Triad; however, there is still some controversy about which is the best approach.

In general, the primary goal of treatment is to normalize body weight and energy balance with lifestyle and dietary modifications. Diet and exercise regimen modifications should be the main focus to increase daily energy availability . When addressing these issues with athletes , a restrained and stepwise manner is advisable. For instance, modest exercise reduction (10–20 %) and an increase of energy availability to at least 30–45 kcal/kg of fat-free mass per day are reasonable goals [10]. Caloric intake should be increased slowly to avoid raising the patient’s fear of becoming fat and to avoid the negative sequelae of “refeeding syndrome.” Referral to a sports nutritionist/dietitian will also promote a gradual increase in energy intake and optimize overall nutrient intake. Restoration of menstrual cycles and increases in BMD have been seen with weight gain in several studies [10, 165]. Though getting BMD to an optimal range is sometimes not possible, an improvement in BMD may be seen depending on the timing, severity, and duration of energy restriction [166]. Athletes should be advised to achieve a BMI of > 18.5 kg/m² or > 90 % of ideal body weight [13]. However, these weight goals may be difficult to attain and are not always sustained over time. It is also important to remember that some athletes may need to achieve even higher weight goals to restore normal menstrual function , because they may have a higher amount of lean muscle mass and a relatively lower amount of adipose tissue.

Another challenge for the physician is that many athletes are reluctant to follow activity and dietary recommendations. Therefore, pharmacological therapy may need to be considered in conjunction with behavior modifications. Oral contraceptive pills (OCPs) containing estrogen and progestin are commonly used in athletes suffering amenorrhea, although evidence regarding the effects on bone density is inconclusive [13, 167, 168]. Recently, research has focused on alternative ways of delivering hormonal therapy. Transdermal estrogen may have a better impact on bone than OCPs because of minimal effects on IGF-1, which is a bone trophic hormone essential for bone formation and remodeling [169]. Studies on postmenopausal women have shown that transdermal estrogens (alone or plus progesterone) are more effective than OCPs in increasing BMD and decreasing fracture risks [170, 171]. Spine and hip BMD improvement was also seen with transdermal estrogen and oral progesterone therapy in adolescent anorexia patients [172]. However, further studies proving the efficacy of transdermal estrogen in treating Triad are needed. Some small studies have also tested the subcutaneous analog leptin therapy for recovering menstrual cycles and improving BMD in those with FHA, but with its side effect of weight loss, adjusting dosing and confirmation of an overall benefit of leptin therapy through larger studies is absolutely required [173, 174].

Additionally, calcium, vitamin D, and sometimes potassium supplementation is recommended in athletes , especially those with restrictive eating behaviors. The daily doses suggested are 1300 mg/day of elemental calcium in divided doses in adolescents (1000 mg in women ≥ 19 years old), 400–800 IU of vitamin D, and 60–90 mg of potassium [169, 175]. In general, bisphosphonates are not recommended for BMD treatment in premenopausal populations, except in extreme circumstances and under the guidance of a bone metabolism specialist, such as an endocrinologist [13]. Antidepressant medications, specifically selective serotonin reuptake inhibitors (SSRIs), may be useful in certain cases. Several studies have shown SSRIs to be effective in the treatment of bulimia nervosa, significantly reducing the frequency of binge eating and purging; however, the evidence is less clear in the case of anorexia nervosa [176, 177]. Another advantage of using antidepressants is the treatment of comorbid conditions such as anxiety, depression, and obsessive compulsive disorder [13]. The main drawback of SSRIs is that they have been linked with weight loss in some individuals with negative effects on BMD [13, 178, 179].

The Triad is a challenging diagnosis and the management has several difficulties. Therefore, education and prevention are fundamental in reducing morbidity and mortality. Prevention and early detection are more effective strategies to reduce symptoms and decrease the risk of serious long-term complications.

Awareness of the Triad is the first step. When 180 Australian female exercisers (ages 18–40 years) were surveyed about the Triad, only 10 % could name all three components and 45 % did not think amenorrhea could affect bone health . A total of 22 % of those in lean-build sports answered that they would do nothing if they were amenorrheic [180]. Of 103 American female high school track athletes, more than 90 % provided incorrect answers about the consequences of bone loss and the link to menstrual irregularity [181]. In a survey of 240 health-care professionals and coaches, fewer than half the physicians could identify the three Triad components and only 8 % of the coaches answered correctly [182]. Thus, more information needs to be disseminated to health professionals, coaches, and athletes, alike.

The preparticipation evaluation (PPE) is an excellent time to screen athletes for the Triad. The majority of the US National Collegiate Athletic Association (NCAA) Division 1 universities require a PPE, including a history and physical, prior to sports participation. However, only about a third require an annual update [183]. The Female Athlete Triad Coalition developed 12 questions for inclusion in the PPE [184]. However, only 9 % of the NCAA Division 1 schools had ≥ 9 of the 12 recommended Triad-related questions as part of their PPEs, with 44 % of the universities including ≤ 4 items [183, 184]. The most recent edition of the PPE history and physical examination form endorsed by the American Academy of Family Physicians, American Academy of Pediatrics, ACSM, and others, is the most commonly recommended tool for use with PPEs for middle school through college-aged athletes. It includes 7 of the 12 items recommended by the Female Athlete Triad Coalition, omitting some of DE-related questions [185].

Recently, athlete-focused DE prevention programs have been evaluated. In an 8-week program known called Athletes Targeting Healthy Exercise and Nutrition Alternatives (ATHENA), coaches and peers led sessions with high school athletes. Topics in the sessions included depression, self-esteem, healthy norms, societal pressures to be thin, and steroid use. Student athletes who participated in the ATHENA program reported less diet pill use and positive improvements in diet habits and exercise self-efficacy versus those who only received informational pamphlets on the topics. When followed for up to 3 years, athletes in ATHENA showed decreases in marijuana and alcohol use, but unfortunately not in eating pathology [186] .

In cognitive dissonance-based prevention (DBP), participants confront the thin-ideal standard of female beauty through various activities and discussions in order to create cognitive dissonance. In a healthy weight intervention (HWI), participants learn to make small lifestyle changes to their dietary and exercise habits in order to maintain a healthy weight. Becker et al. compared an athlete-modified DBP (AM-DBP) and an athlete-modified HWI (AM-HWI) approach in a study of 157 female collegiate athletes [187]. Both interventions reduced thin-ideal internalization, dietary restraint, bulimic pathology, shape and weight concern, and negative affect at the 6-week follow-up, with sustained reductions in bulimic pathology , shape concern, and negative affect at 1 year. In addition, there was an increase in students spontaneously seeking medical consultation for the Triad [187].

In a small study of college athletes who had achieved recovery from EDs, participants were asked what advice they would give to coaches, parents, and other athletes at risk for EDs [188]. Coaches were advised to (1) become educated on EDs to increase awareness, (2) emphasize proper athlete nutrition, (3) focus on sport skill rather than body weight to achieve performance goals, (4) refrain from singling out athletes for their body weight or shape, (5) confront an athlete with an ED if even suspected, (6) provide emotional support, (7) refer the athlete to professional care (e.g., physician, psychologist, and/or nutritionist), (8) prohibit sports participation if health risks are evident, (9) try to pair the athlete up with another athlete who has recovered from an ED, and (10) notify the athlete’s family. Advice to parents also involved providing emotional support, encouraging professional treatment, and becoming educated about EDs. Suggestions for other athletes with EDs included (1) keeping optimistic about recovery, (2) determining the underlying cause of and triggers for the ED, (3) getting professional treatment, (4) seeking out emotional support from others, (5) focusing on the benefits of recovery, (6) putting the ED in perspective in terms of how it is skewing life values, and (7) focusing on what has been learned from the ED experiences [188]. Certainly enhancing awareness and taking the advice of those who have experienced aspects of the Triad are future directions in which we need to head.

The Triad and its individual components can occur in female athletes at any age and in any sport. Early awareness and education can help prevent struggles ranging from unsatisfying sports performances to lifelong emotional and physical health problems. Because we know there are certain sport populations at increased risk for the Triad, increased efforts need to be made to improve detection and care in these groups. Following suggestions provided by the IOC, the Female Athlete Triad Coalition, ACSM and other groups of professionals with expertise on this topic is important. In the past decade, researchers have gained a better understanding of the complexity of the Triad and the interrelationship of its components. This understanding needs to be more widely disseminated and further research needs to be conducted to enhance the care of those afflicted by the Triad.