Many of us have heard the harrowing stories of athletes suffering the consequences of the female athlete triad (triad) or Relative Energy Deficiency in Sport (RED-S). Accounts of injuries, disrupted training and long term health consequences that arise from inappropriate energy intake for training and life requirements. The words of warning resonate a little too close to home for some. But in the world of high performance sport where there is a fine line between peak performance and injury/illness how do we know what is ok and what is not? When and what action is needed? The Female Athlete Triad Coalition (1), International Olympic Committee (2, 3) and Endocrine Society (4) have all published guidelines to help athletes, coaches and clinicians make informed decisions to promote health and performance.
The female athlete triad has evolved from its initial definition of eating disorders, amenorrhea (absence of menstrual periods) and osteoporosis to now refer to an interrelationship of energy availability (with or without disordered eating), menstrual function and bone health which exists along a spectrum from optimal to ill-health. The International Olympic Committee (IOC) expanded the consequences of low energy availability to 20 health and performance effects which can occur in males and females, athletes and active individuals, in their 2014 RED-S consensus (2). This was met with some debate but energy availability, menstrual function and bone health are common to both paradigms and are central to the current screening tools.
The female athlete triad coalition (Coalition) and IOC both recommend periodic screening of athletes which can include questionnaire, physical health and laboratory tests (1, 3). The Coalition published a cumulative risk assessment tool (figure 1) which applies a score to six risk factors. Cumulative scores result in low (0-2 points), moderate (3-5 points) or high (6+ points) risk for bone stress injuries (BSI). This can guide decisions on sports participation and return to play (figure 2). This assessment has been shown to predict bone stress injuries in female and male (modified tool) runners. However, elevated risk on any variable warrants further investigation irrespective of cumulative score in order to minimise damage e.g. dietary restriction or menstrual irregularity without any other risk factors may result in a low risk score, but left without investigation may evolve to a greater risk.
A similar tool (RED-S clinical assessment tool (REDSCAT)) was published by the IOC (5). This is designed to guide clinicians’ decisions based on a traffic light system. The Low Energy Availability in Females Questionnaire (6) applies a scoring system to classify athletes at risk of low EA based on a wider range of factors. A similar questionnaire has been developed for males.
Where questionnaire results identify an athlete at risk for triad/ RED-S, The Coalition, IOC and Endocrine Society recommend further clinical screening. Depending on severity, this can include blood biomarkers, bone density and cardiac screening and psychological screens for eating disorders and other mental health conditions.
As poor bone health is a well-established consequence of both triad and RED-S, current guidelines (4) recommend bone mineral density assessment (BMD) in cases of 6+ months of amenorrhea (absence of menses for 90+ days or not reaching menarche by 15 years) or prolonged (2 years) oligomenorrhea (irregular cycles >35 days in length). The American College of Sports Medicine (ACSM) recommend a modified BMD z-score classification for athletes in weight bearing sports (figure 3) (7). However, BMD is slow to change (6+ months for measurable change). Low BMD is associated with increased fracture risk but normal BMD does not indicate no risk. Irrespective of BMD, low EA or menstrual dysfunction should be a red flag. We are currently using bone remodelling markers found in blood and urine to assess normal values in athletes with the intention of providing more sensitive markers in future.
IOC, Coalition and Endocrine Society recommendations all highlight the need to address underlying low EA. The source of low EA informs treatment. Where inadvertent undereating or lack of time/ finance is the cause, education may resolve the energy deficit. Where disordered eating/ eating disorders are suspected this must be evaluated and multidisciplinary care which provides psychological support is necessary (8). EA may be restored within days or weeks through modified diet and/or exercise but where disordered eating exists this may take longer.
Functional hypothalamic amenorrhea (FHA) is a diagnosis of exclusion meaning that all other causes of menstrual dysfunction are ruled out prior to diagnosis. This is important to ensure appropriate treatment. Nutrition intervention is the recommended treatment. However, in cases of prolonged amenorrhea and failure to respond to nutritional changes transdermal estrogen may be prescribed. The oral contraceptive pill is not recommended for the sole purpose of addressing FHA as it does not restore normal estrogen levels which controls bone resorption (break-down) and may reduce bone formation (building).
Due to lack of studies in premenopausal women pharmaceutical interventions are not generally recommended to treat bone health in triad/RED-S (4). Restoration and maintenance of optimal EA and menstrual function is recommended but addressing poor bone health takes a considerable period of time (Figure 4) (1).
The published guidelines can inform detection and appropriate treatment of triad/ RED-S related conditions but the consequences cannot be completely reversed. Of particular concern is the presence of triad/RED-S during adolescence, a time of rapid growth where lifetime bone health is heavily influenced. An ounce of prevention is worth a pound of cure. As outlined by the IOC in the 2018 update of the RED-S consensus (3), educational programmes that increase awareness and multimodal programmes addressing the multiple components of the triad and RED-S need to be developed and implemented.
For more information:
- De Souza et al (2014) ‘ 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad’ Current Sports Medicine Reports, 13(4):219-3, https://www.ncbi.nlm.nih.gov/pubmed/25014387
- Mountjoy et al (2014) ‘The IOC consensus statement: beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S)’, British Journal of Sports Medicine, 48(7): 491-497, https://www.ncbi.nlm.nih.gov/pubmed/24620037
- Mountjoy et al (2018) ‘IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update’, British Journal of Sports Medicine, 52(11): 687-697 https://www.ncbi.nlm.nih.gov/pubmed/29771168
- Gordon et al (2017) ‘Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline’, The Journal of Clinical Endocrinology and Metabolism, 102(5): 1413-1439, https://www.ncbi.nlm.nih.gov/pubmed/28368518
- Mountjoy et al (2015) ‘RED-S CAT Relative Energy Deficiency in Sport (RED-S) Clinical Assessment Tool (CAT), 49(7): 421-3 https://www.ncbi.nlm.nih.gov/pubmed/25896450
- Melin et al (2014) ‘The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad’, British Journal of Sports Medicine, 48(7):540-5 https://www.ncbi.nlm.nih.gov/pubmed/24563388
- Nattiv et al (2007) ‘The female athlete triad’, Medicine and Science in Sports and Exercise, 39(10): 1867-1882 https://www.ncbi.nlm.nih.gov/pubmed/29135634
- Joy et al (2016) ‘2016 update on eating disorders in athletes: A comprehensive narrative review with a focus on clinical assessment and management’, British Journal of Sports Medicine, 50(3): 154-62, https://www.ncbi.nlm.nih.gov/pubmed/26782763
Jennifer Higgins is a PhD researcher in the Department of Physical Education and Sport Sciences at the University of Limerick. Her current research interests include the role of nutrition and physical activity on bone health in female endurance athletes. You can contact Jennifer via email at Jennifer.Higgins@ul.ie.