The Triad’s new definition specifies low energy availability, menstrual irregularity, and low bone mineral density as predictors of future health risks, including lower extremity injuries. This broader definition means far more female athletes may be at risk than previously thought, particularly in the high school setting.
By Jill Thein-Nissenbaum, PT, DSc, SCS, ATC
Female sports participation at the high school level has significantly increased since the 1970s; in the 2010-2011 school year, 41% of participants in all high school sports were girls. Although physical activity has numerous positive benefits, a select population of female high school athletes may experience symptoms related to the female athlete triad (Triad), which refers to the interrelationships among energy availability, menstrual function, and bone mineral density (BMD). Clinical manifestations of the Triad are distributed along a spectrum between optimal health and disease, and all components may not be present simultaneously.
Current research has also demonstrated a relationship between various Triad components and lower extremity overuse injuries in female athletes. Girls and women with components of the Triad appear to have an increased risk for regional pain syndromes and slow healing from overuse injuries, and may also experience musculoskeletal injuries such as tendinitis and tendinosis at higher rates than their healthy counterparts.
Female athlete triad
In 1992, the American College of Sports Medicine (ACSM) identified an association of disordered eating, amenorrhea, and osteoporosis in athletes participating in sporting activities that emphasize a lean physique. This condition was recognized as the “female athlete triad,” and the ACSM published its first Position Stand on the condition in 1997.1 The ACSM revised the Position Stand in 2007 based on updated scientific evidence and discoveries made in the decade since the 1997 paper.2 Because the original Position Stand had strict criteria required for definitions of each component, clinicians and researchers hypothesized that large numbers of athletes with less severe conditions were not being recognized as having the Triad.
Thus, current terms used to describe components of the female athlete triad are broader and include energy availability, menstrual function, and BMD. With these new definitions, more athletes are now recognized as having components of the Triad.2
The updated Position Stand changed the term “disordered eating” to “energy availability.” Energy availability is defined as energy intake minus energy expenditure, or the amount of energy remaining after exercise for regulation of normal bodily functions.2-4 Energy availability occurs along a spectrum, ranging from optimal energy availability to low energy availability, in which low energy availability may occur with or without an eating disorder2 (Figure 1). In other words, some athletes may have low energy availability because they are intentionally restricting caloric intake while others may fall into a negative energy balance simply because they are unaware of the caloric intake needed for bodily function regulation plus exercise.5,6
Athletes who intentionally reduce energy availability do so through mechanisms such as restrictive eating, fasting, skipping meals, diet pills, laxatives, diuretics, enemas, or binge-eating followed by purging (vomiting); these behaviors are identified as disordered eating (DE).2-4,6,7 Prior research suggests that unhealthy eating behaviors in the general population are first formed during adolescence.8-12
Currently, research on the prevalence of DE or low energy availability among high school athletes is limited.13-17 Disordered eating is generally assessed through self-reporting methods with questionnaires such as the Eating Disorders Examination-Questionnaire (EDE-Q).15 16,18,19 Studies utilizing the EDE-Q reported that the prevalence of DE in female high school athletes ranges from 18.2% to 35.4%15,18,19 (Table 1). A possible reason for the difference in prevalence estimates between researchers may be the sports included in the respective studies. Studies that assessed aesthetic sports (e.g., diving, cheer, dance, gymnastics), such as the Thein-
Nissenbaum et al study,19 report a higher prevalence of DE.
Menstrual function refers to a spectrum ranging from eumenorrhea, or normal menses, to amenorrhea (absence of menses)2 (Figure 1). Menstrual dysfunction is often referred to as menstrual irregularity (MI), and includes primary amenorrhea, secondary amenorrhea, and oligomenorrhea.2 Primary amenorrhea refers to a lack of menses by in female individuals aged 15 years and older.2,20 Secondary amenorrhea is defined as a cessation of menstruation for three consecutive months in a previously menstruating adolescent. Oligomenorrhea is defined as menstrual cycles occurring more than 35 days apart.2 Although only a small amount of evidence exists, a higher prevalence of MI has been reported in high school athletes compared with the general high school population.2,14,21,22
The few studies that have examined the prevalence of MI in high school populations report the prevalence as ranging from 18.8% to 54%.14,15,18,19 The high prevalence estimates for menstrual irregularity suggest it may be a medical problem among high school athletes.14,15,18,19 However, the reported prevalence of MI in the adolescent population should be interpreted cautiously. Menstrual irregularity immediately postmenarche is common, though nearly 90% of young women have normal menstrual cycles within two years of menarche.23
In the studies discussed previously, the majority of participants were more than two years postmenarche, so the normal fluctuations commonly observed immediately postmenarche would not have been reported.14,15,18,19 Healthcare professionals should screen for MI in all female athletes at the high school level, regardless of sport type. Research findings related to high school MI are summarized in Table 1.
Bone mineral density
The 2007 Position Stand refers to BMD as ranging from optimal bone health to osteoporosis2 (Figure 1). Because of the challenges surrounding BMD assessment in adolescents, the International Society for Clinical Densitometry (ISCD) recommends against using the World Health Organization criteria for diagnosis of osteopenia and osteoporosis in postmenopausal women for diagnosis in premenopausal women and girls.24 Instead of T-scores, which are values obtained when a dual-energy X-ray absorptiometry scan is performed on postmenopausal women, the ISCD recommends expressing BMD in premenopausal women and children as Z-scores, as these scores compare individuals to age and sex-matched controls. Any Z-score lower than -2 is defined as “low bone density for chronological age” (not osteoporosis) in children.25 However, all male and female athletes who engage in weight-bearing sports typically have a BMD that is 12% to 15% higher than age-matched controls.26 Therefore, a Z-score lower than -2 in an athlete who plays one of those sports is somewhat alarming.
Assessing bone health in the adolescent female athlete is also challenging because an athlete’s BMD is a reflection of her energy availability, menstrual status, genetic composition, Tanner Stage (a sexual maturity rating), and environmental factors. Because of this, one must consider how the BMD of the adolescent female athlete changes over time—a “snapshot” of BMD in the adolescent female may not provide as much information as longitudinal data. For example, at onset of amenorrhea, immediate changes in bone density may not be seen, but with prolonged amenorrhea, skeletal demineralization will occur.27 Similarly, resuming regular menses does not immediately restore optimal bone health, but with prolonged eumenorrhea, mineral accumulation will occur and improve BMD.2,28 Thus, low BMD measurements in adolescent girls must be interpreted in the context of age, menstrual status, and nutrition history. In addition, strong consideration should be given to repeating BMD assessments over time as part of the treatment plan for the young athlete with low bone density.
Because of these challenges, studies related to BMD in the female adolescent population are very limited and must be interpreted cautiously.14,15,29 Nichols et al15 determined the prevalence of low bone mass in 170 female high school students was 21.8%. Hoch et al assessed BMD in 80 female high school athletes and reported that 13% (n = 11) had a Z-score between -1 and -1.9 and 3% (n = 2) had a Z-score of -2 or lower.14
The Triad and musculoskeletal injury
Recently, several studies have attempted to determine if a relationship exists between any Triad components and other conditions, such as musculoskeletal injuries. Although researchers have reported an association between MI and stress fractures in collegiate populations,30,31 very few studies have determined if there is a relationship between Triad components and musculoskeletal injuries other than stress fractures, which fall under the Triad umbrella, in the high school population.19,32,33
One study of 331 female high school athletes determined that those who met the criteria for DE were more than twice as likely to sustain a musculoskeletal injury during their current sports season than those who did not meet the criteria19 (Table 2). Using a slightly different definition for injury, Rauh et al33 also determined that female high school athletes reporting DE were more than twice as likely to incur a musculoskeletal injury than female high school athletes who reported normal eating behaviors (Table 2).
One theory that may support the relationship between DE and increased risk of musculoskeletal injury is the role DE plays in low energy availability, which researchers have suggested is crucial to the healing process.2,34 If energy availability is below the level required for normal homeostasis, alterations in cellular maintenance, growth, and thermoregulation can occur.2,34 Therefore, a female athlete with low energy availability—incurred either intentionally or unintentionally—may not have enough caloric support for growth and repair of injured tissues.
A few researchers have reported an association between menstrual irregularity and musculoskeletal injury.32,33 Rauh et al33 determined that high school athletes who reported MI were three times more likely to sustain a musculoskeletal injury than athletes with normal menses. A study of 62 female high school athletes participating in cross country running, an endurance sport, evaluated the association between abnormal menstrual function and exercise-related leg pain (ERLP).32 ERLP is a regional pain syndrome in athletes that presents as pain with exercise occurring below the knee and above the ankle. The authors determined that athletes with abnormal menstrual function were at four times greater risk of experiencing ERLP than those with normal menses.32 This is most likely because energy levels are inadequate to support healing of overused tissues; if the athlete has abnormal menstrual function due to negative energy balance, there will not be enough energy left to promote tissue healing.
In our experience, high school athletes usually do not recognize menstrual irregularity as problematic; in contrast, they often view oligomenorrhea and amenorrhea as convenient and desirable. These misconceptions may exacerbate the existing associations between menstrual dysfunction and musculoskeletal injury, resulting in an increased risk of potentially preventable sport-related injuries among young female athletes.
Compared with the original Position Stand, the updated document uses broader criteria to define the various Triad components. The new terms—energy availability, menstrual function, and bone mineral density—capture women and girls who were previously not identified as having Triad-related issues. Because of the broader terms, the prevalence of female athletes with Triad-related conditions has increased. As such, older studies that utilized the definitions from the original Position Stand would have excluded female athletes who might now be identified with components of the triad. When possible, clinicians should seek out studies based on the concepts in the current Position Stand and use those studies to guide best practice.
The established relationship between low energy availability and menstrual function has caused researchers to question whether low energy availability is linked to other conditions, including musculoskeletal injuries such as tendinitis and tendinosis.33 The future direction of Triad-related research will most likely attempt to identify associations between Triad components and other conditions, such as overuse injury, balance impairments, and aerobic and anaerobic fitness.
Most research to date on the female athlete triad has focused on collegiate and elite athletes. However, with the 2007 ACSM Position Stand’s broader framework for the Triad, it is clear that many more female athletes experience problems along the spectrum of energy balance, menstrual function, and bone mineral density. There is a growing body of literature about high school athletes and their experiences with Triad components. Research suggests that disordered eating behaviors may inadvertently cause low energy availability in female high school athletes and nonathletes alike. Menstrual irregularity exists in the high school population, even after accounting for the typical fluctuations seen with the onset of menses. Bone density abnormalities have also been observed in high school athletes.
Healthcare professionals should inquire about Triad components in young female athletes with musculoskeletal injuries, especially those with overuse or recurrent injuries. Ongoing research and education programs about the female athlete triad syndrome geared toward sports medicine professionals, coaches, and high school athletes and their parents are warranted.
Jill Thein-Nissenbaum, PT, DSc, SCS, ATC, is an assistant professor in the Doctor of Physical Therapy Program and a staff physical therapist in the Athletic Department at the University of Wisconsin-Madison.
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