The Female Athlete Triad (Triad) was first defined by a group of clinical and scientific experts in 1992 (28). Since then, two American College of Sports Medicine (ACSM) Position Stands have been published (1997, 2007) (21,22), and more recently, the Female Athlete Triad Coalition Consensus on Clearance and Return to Play (5). The Consensus Statement was the first to provide evidence-based guidance to sports medicine clinicians on clinical decision making for clearance and return to play for females affected by the Triad.
The Consensus Statement identifies six evidence-based risk factors for low bone mass and stress fracture/bone stress injury (BSI), which includes stress reactions that are often graded in severity by magnetic resonance imaging (9,20). The risk factors include low energy availability (EA) with or without disordered eating (DE)/eating disorder (ED), low body mass index (BMI), delayed menarche, oligomenorrhea/amenorrhea, low bone mineral density (BMD), and history of stress fracture/BSI. Each risk factor is assigned a point value of 0, low risk; 1, moderate risk; and 2, high risk. A cumulative risk score of 0 to 1 identifies a low-risk individual and full clearance. A score of 2 to 5 identifies someone at moderate risk, and either provisional or limited clearance, allowing for full participation with close follow-up, or limited participation respectively. A cumulative risk score of 6 or greater indicates higher risk for low bone mass and BSI and may result in either restriction from training and competition, or in some cases, disqualification from sport participation (5) (see Figs. 1 and 2).
Prevalence of the Triad varies by sport, with athletes participating in sports where leanness confers a competitive advantage or sports that require body conforming uniforms (i.e., long distance running, gymnastics, swimming, and diving). However, any female athlete is at risk for the Triad if the desire to optimize body composition for sport leads to low EA (5,21,25).
Low EA is the foundation of the Female Athlete Triad. Low EA can occur with or without DE or an ED. In the case of without DE/ED, a highly competitive athlete may be training for 6 h·d−1 and despite a dietary intake of 2500 calories would not be meeting her overall energy requirements. Over time, this can result in low EA. However, low EA often results when dietary intake is intentionally restricted (3,4,8). EA can be calculated using the following formula: (5,11,14,21).
Average daily dietary energy intake can be estimated using something as simple as the MyFitnessPal app (www.myfitnesspal.com/apps) on a smartphone or other application. Mean daily exercise energy expenditure can be calculated using the following formula:
MET value of a given activity can be found on the Physical Activity Compendium (1) or related web site: (https://sites.google.com/site/compendiumofphysicalactivities/Activity-Categories). Finally, fat-free mass (FFM) can be determined a number of ways such as bioelectrical impedance scales, BodPod measurement, and dual-energy absorptiometry (DXA) scan assessment of body composition. EA of at least 30 kcal·kg−1 FFM is considered sufficient to support normal reproductive function (15). EA less than 30 kcal·kg−1 of FFM is associated with disruption of normal menstrual cycles (15). However, an EA of 35 to 45 kcal·kg−1 FFM or likely greater than 45 kcal·kg−1 FFM is desired for resumption of menses in women with either oligomenorrhea or amenorrhea (5,12,16,21).
The clearance and return to play matrix can be completed during the preparticipation evaluation (PPE), or at a subsequent follow-up visit in athletes identified as at-risk for the Triad during PPE screening. Likewise, determination of EA is best performed at a follow-up office visit, with adequate time to counsel and determine next steps based on the results.
A consequence of low EA is low BMI. Low-risk BMI is defined as ≥ 18.5 kg·m2, or weight that is 90% or greater than what is expected for height and age. Moderate risk is defined as a BMI between 17.6 and 18.4 kg·m2, or weight between 85% and 90% of expected, or a 5% to 10% weight loss in a month. Finally, high risk is a BMI ≤ 17.5 kg·m2, weight < 85% of expected, or ≥ 10% weight loss per month (5). For older adolescents, it is helpful to have access to their childhood, early adolescent growth charts to see their historical baselines for height and weight. In essence, it can provide a “place to aim for” in restoration of a BMI that supports normal physiologic functioning.
Menarche is considered delayed if it happens after age 15 yr (2). The average age of menarche in the United States is 12.8 yr (4). Delayed menarche is an independent risk factor for low BMD (21,27). BMD declines as the number of missed menstrual cycles accumulates (6,26). Delayed menarche is also independently associated with a risk of stress fractures and BSI (8,13,24). The same is true for oligomenorrhea (menstrual cycles at intervals longer than 35 d) and secondary amenorrhea (defined as > 90 d between menstrual cycles) (3,7,20). In the case of a 17-yr-old female who has not yet menstruated, she would accumulate two points for delayed menarche, another two points for < 6 menses in the past 12 months, and be considered high risk in two categories — delayed menarche and oligomenorrhea and/or amenorrhea.
The Coalition Consensus Statement outlines when a DXA scan should be obtained (4). One or more high-risk Triad risk factors, two or more stress fractures/BSI or 1 higher risk stress fracture (e.g., pelvis or femoral neck); or two or moderate Triad risk factors should prompt evaluation of BMD. A prior DXA with Z-score < −2.0 should prompt reevaluation of BMD in 1 yr.
According to the International Society of Clinical Densitometry, DXA Z-scores (comparing to age matched controls) in contrast to DXA T-scores (comparing to peak BMD) should be used in children, adolescents and premenopausal women (10). For children and adolescents (less than age 20 yr), the DXA procedure is to scan whole body or total body less head, in addition to the lumbar spine BMD (10). The lowest DXA value is used to guide clinical interventions, which is typically the spine, as less subject to weight bearing force and more sensitive to nutritional and hormonal deficits.
A history of either stress reaction or fracture is a well-documented risk for future stress fracture/BSI (5,19,24). A history of two or more high-risk stress fractures should prompt modification in exercise volume and/or intensity, close attention to modifiable risk factors; and in some, discussion regarding the safety of future participation in at risk sports (5).
It is worth noting that some risk factors in the clearance and return to play matrix are modifiable (EA, BMI, menstrual function (oligomenorrhea and amenorrhea), and DXA Z-score. However, delayed menarche and stress fracture history are presently nonmodifiable. The same is true for moderate risk EA which includes “history of DE/ED.” Thus, it is possible for a female to be in the following situation (see Table).
A cumulative risk score of 6 is consistent with a recommendation to consider restriction from training and competition; however, in this example, 5 of 6 points are all due to nonmodifiable medical history. Given no evidence of current low EA, normal BMI, and regular menstruation, clinical judgment would likely result in provisional clearance and close interval follow-up to ensure maintenance of health.
A few known risk factors for low BMD are absent from the scoring system, but should be taken into consideration when evaluating an individual affected by the Triad. These include a family history of osteoporosis, low dietary calcium intake, vitamin D deficiency, and medical conditions associated with low BMD, such as celiac disease, other disorders involving malabsorption, and hyperthyroidism, among others.
Since the Coalition Consensus Statement was published, a recently published prospective cohort investigation has established its validity. Tenforde et al. (23) found that moderate- and high-risk college athletes were more likely to sustain a BSI, and that both prior stress fracture and current oligomenorrhea/amenorrhea were independent risk factors for subsequent BSI. The International Olympic Committee also has developed a clinical assessment tool for male and female athletes expected to have relative energy deficiency (18) to aid in return to play decisions (17), although to date, it has not been validated.
The Coalition Consensus Statement represents the first effort at quantifying and stratifying risk for women affected by the Triad (5). Early evidence suggests that the cumulative risk scoring system predicts BSI (23). Clinical judgment in the case of history, as well as for risk factors not accounted for in the risk scoring system, should be considered when addressing clearance and return to play decision-making. Given the independent nature of prior stress fracture/BSI and current oligomenorrhea/amenorrhea on incidence of subsequent BSI, future research should evaluate modification of the cumulative risk scoring system that weight those risk factors reflecting their greater influence on injury risk (i.e., a weighted risk assessment). Likewise, the addition of risk factors in the scoring system should be considered, such as family history of osteoporosis. Further outcome studies would then be recommended to validate a modified weighted version of the Coalition Consensus Statement Triad risk assessment that take into account risk factors that are most predictive of BSI and/or low BMD.
The authors declare no conflict of interest and do not have any financial disclosures.
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