If you are striving to reach your peak performance, then the PEAQ can help you reach your personal full potential. Click here to get started on the PEAQ
Matching your energy intake to your energy demands helps you reach your personal peak health and exercise performance. On the other hand, failing to meet your energy demands results in low energy availability. This increases your risk of developing relative energy deficiency (REDs) and its adverse health and performance consequences.
People of any age, whatever their level and type of exercise, can be at risk of developing REDs; from elite dancers and athletes to recreational exercisers.
The PEAQ is a mobile Application that will guide you through a series of questions about exercise, physical characteristics, nutrition, hormone function and well-being. It just takes a few minutes.
Your PEAQ report instantly generates a REDs Risk Score and provides valuable insights into your energy status and potential risks, along with guidance. The PEAQ is intended for those 16 years of age and over.
The PEAQ has been developed based on in several published research studies where the questionnaire responses and scores have been correlated with measurements of hormones and bone health in athletes in various sports [1-7] and dancers [8-12]. These questionnaires were cited in the updated International Olympic Committee (IOC) consensus statement on REDs 2013.
Assessment of Relative Energy Deficiency in Sport, Malnutrition Prevalence in Female Endurance Runners by Energy Availability Questionnaire, Bioelectrical Impedance Analysis and Relationship with Ovulation status. Clinical Nutrition Open Science 2025S.
Body composition, malnutrition, and ovulation status as RED-S risk assessors in female endurance athletes, Clinical Nutrition ESPEN 2023, 58 :720-721
Keay N, Craghill E, Francis G Female Football Specific Energy Availability Questionnaire and Menstrual Cycle Hormone Monitoring. Sports Injr Med 2022; 6: 177
Nicolas J, Grafenuer S. Investigating pre-professional dancer health status and preventative health knowledge Front. Nutr. Sec. Sport and Exercise Nutrition. 2023 (10)
Nicola Keay, Martin Lanfear, Gavin Francis. Clinical application of monitoring indicators of female dancer health, including application of artificial intelligence in female hormone networks. Internal Journal of Sports Medicine and Rehabilitation, 2022; 5:24.
Nicola Keay, Martin Lanfear, Gavin Francis. Clinical application of interactive monitoring of indicators of health in professional dancers J Forensic Biomech, 2022, 12 (5) No:1000380
Mountjoy M, Ackerman KE, Bailey DM et al 2023 International Olympic Committee’s (IOC) consensus statement on Relative Energy Deficiency in Sport (REDs) British Journal of Sports Medicine 2023;57:1073-1098
This article explores the current state of play regarding relative energy deficiency in sport (REDs), highlighting the recent updates from the International Olympic Committee (IOC) consensus statement September 2023. Psychological factors and mental health are recognised as having a reciprocal relationship in both the aetiology and outcome of chronic low energy availability leading to REDs. This has important implications in terms of prevention and management of individuals experiencing REDs. Unintentional or intentional unbalanced behaviours around exercise and nutrition leads to a situation of low energy availability. Low energy availability is not synonymous with REDs. Rather cumulative, sustained low energy availability, particularly low carbohydrate availability, leads to the clinical syndrome of REDs comprising a constellation of adverse consequences on all aspects of health and performance. This situation can potentially arise in both biological sexes, all ages and level of exerciser. This is of particular concern for the young aspiring athlete or dancer, where behaviours are being established and in terms of long-term consequences on mental and physical health. The mechanism of sustained low energy availability leading to these negative health outcomes is through the adaptive down regulation of the endocrine networks. Therefore, raising awareness of the risk of REDs and implementing effective prevention and identification strategies is a high priority.
Introduction
Relative energy deficiency in sport (REDs) was first described in the International Olympic Committee (IOC) consensus statement published in the British Journal of Sports and Exercise Medicine (BJSM) 2014(Mountjoy, 2014). Since then, there have been updates published in 2018 (Mountjoy, 2018) and most recently in September 2023 (Mountjoy, 2023).
Seminal studies of female collegiate runners in 1980s found that those athletes with higher weekly training load, but same food intake as those with lower training load, experienced menstrual disruption, including secondary amenorrhoea and poor bone health (Drinkwater, 1984). This led to the description of the female athlete triad, which comprises a clinical spectrum of eating patterns, menstrual function and bone health. This ranges from optimal fuelling, menstrual function and bone health; to eating disorders, amenorrhoea and osteoporosis.
However, with further evidence emerging it became apparent that the impact of under fuelling is not confined to menstrual and bone health. Rather that the consequences of under fuelling are multisystem and can include male athletes. This led to the initial description of REDs in 2014 as a syndrome comprised of the potential adverse effects on many systems in the body with both physical and mental health implications. Crucially, unlike the female athlete trad, REDs also included the potential negative sequalae on athletic performance. Ultimately the goal for all athletes is to perform to their best, so REDs is not something of interest just in academic or clinical circles. REDs is highly relevant to both biological sexes and all levels and ages of exerciser.
What is Energy Availability?
The underlying aetiology of REDs is low energy availability. The life history theory describes how biological processes compete for energy resources (Shirley, 2022). Energy requirement for movement is prioritised from an evolutionary point of view in order to take evasion action from predators. The residual energy from food intake is described as energy availability. This is roughly equivalent to resting metabolic rate for the individual. Simply lying in bed all day, staying alive, is high energy demand for humans as homeotherms. The numerical value of energy availability is expressed in Kcals/Kg of fat free mass. The energy availability requirement for health will vary between individuals depending on sex, age and body composition. Although energy availability is a very useful concept, in practice is it not actually measured outside of the research setting. Rather objective surrogates indicating energy availability can be measured such as triiodothyronine (T3) which is used as a primary indicator of low energy availability as outlined in the update REDs clinical assessment tool described in further detail below (Stellingwerff, 2023 ).
An important highlight from the updated consensus statement on REDs is that it is specifically low carbohydrate availability that is most detrimental, especially for reproductive hormone networks. Comparing isocaloric intake, where there is a low proportion of energy from carbohydrate, this has the most marked negative consequence on both hormone health and performance. The mechanism of sustained low carbohydrate availability appears to involve the hormone leptin, an adipokine, secreted by adipose tissue. Low levels of leptin cause suppression of the reproductive axis via the hypothalamus-pituitary axis (Keay, 2022).
Aetiology of Low Energy Availability
Low energy availability is a situation where, once energy demand from movement has been met, the residual energy available is insufficient to support the functioning of other biological life process.
Low energy availability could arise unintentionally or intentionally (Keay, 2019). Unintentional low energy availability is where an exerciser does not appreciate the energy demands of exercise and other activities with an energy demand. For example, many athletes will not consider the energy required to “commute” to a training session on foot or bike. Unintentional low energy availability could be due to practical issues: for example, a long cycle ride over several hours will require the cyclist to take nutritional sources in the pockets of clothing and/or plan ahead suitable stops where it is possible to obtain nutrition. Similarly, going on a training camp, especially at altitude, will greatly increase energy demand from exercise and needs to factored in. Finances could also be a limiting factor.
On the other hand, intentional low energy availability is where an exerciser intentionally restricts nutrition intake in the belief that this might confer a performance advantage in terms of body weight, composition or shape. This is particularly associated with any exercise against gravity such as running, road cycling, climbing; weight category sports like martial arts and aesthetic forms of sport (diving, gymnastics) and dance.
For individuals with intentional low energy availability, psychology and mental health can have a reciprocal interaction (Pensgaard, 2023). Those exercisers with personality characteristics such as self-motivation, perfectionism can be very laudable traits in terms of dedication to exercise training to achieve success. However, when these characterises impact and support rigid behaviours around training and nutrition, this can become problematic. This is shown in Figure 1 “Psychological factors in REDs”. Those who are able to adapt to external pressures and have a flexible approach to training and nutrition are more likely to experience positive outcomes. Whereas those who have a more rigid approach, which might include disordered eating and or an eating disorder and/or exercise dependence are more likely to experience negative outcomes. This reinforces self-doubt and culminates in a vicious circle of perpetuating rigid behaviours and negative outcomes in terms of both physical and mental health.
Evidence for this interaction between psychological factors and risk of REDs was found in our study of dancers, referenced in the updated IOC consensus statement. A significant relationship was found between psychological factors such as anxiety around body shape/weight and missing training. These psychological factors in turn had significant associations between physical manifestations of low energy availability (low body weight) and physiological outcomes (menstrual irregularity) (Keay, 2020). Similarly, in more of our published research papers referenced in the IOC consensus statement focusing on male athletes, an significant association was found between cognitive nutritional restraint and negative physiological and performance outcomes (Jorov, 2021).
This reciprocal interaction between internal and external factors is a systems biology approach, highlighted in the recent updated IOC consensus statement. From a physiological point of view the brain is a high energy demand organ, requiring a good supply of glucose. So low carbohydrate availability will restrict this cerebral supply, which can impair cognitive function and ultimately good decision making. It is interesting to reflect that the neuroendocrine gatekeeper, the hypothalamus keeps a watching brief on internal and external factors, not distinguishing between the source of stressors when putting in motion an adaptive response (Keay, 2022).
Consequences of Low Energy Availabiity
Low energy availability is not synonymous with REDs. Indeed, short term low energy availability might initially bring some good performances. Low energy availability becomes problematic depending on the time scale, which in turn determines the degree of adaptive response, described in the clinical physiological model of REDs (Burke, 2023). The first system to adapt to low energy availability is bone: bone turnover moves in favour of resorption over formation. This is why bone stress responses, specifically bone stress fractures, can be an early warning sign of REDs and designated a primary indicator in the updated IOC consensus statement. There will follow sequential down regulation of metabolic rate mediated via the thyroid axis, followed by the reproductive axis. In women primary amenorrhoea or sustained functional hypothalamic amenorrhoea (FHA) of 6 months or more duration is a severe primary indicator of REDs. In men, low rage testosterone is a severe primary indicator. Ultimately body composition will be adversely affected, with the only endocrine system to be up regulated being that of the hypothalamic-pituitary-adrenal axis (Keay, 2019).
Health
Cumulative low energy availability causes the syndrome of REDs, which produces progressive adverse effects on all aspects of health: physical, mental and social, described in the REDs conceptual model. Poor sleep will compound these negative health effects (Keay, 2022).
Performance
Although there may be some initial good performances, chronic low energy availability will result in adverse performance consequences of REDs, described in the REDs performance conceptual model. In our referenced papers in the consensus statement, we found that in male athletes, short term low energy availability impacted performance (Jurov, 2022). In another of our referenced studies we showed that male cyclists in sustained low energy availability over 6 months, not only experienced bone loss commensurate to astronauts in space, but these cyclists also underperformed compared to their energy replete fellow cyclists (Keay, 2019). On a positive note, explaining to athletes and dancers that improving energy availability will improve their performance, can help in overcoming problematic behaviours.
Identification of those at risk
In view of the potential adverse health and performance effects of REDs, it is a priority to raise awareness of this risk to affect prevention. To this end the British Association of Sports and Exercise Medicine (BASEM) has a website health4performance.co.uk dedicated to providing reliable information on REDs for athletes, parents, coaches and health care professionals together with BASEM endorsed online courses. Targeting and identifying those at increased risk is very important. Young athletes and dancers can be most severely affected as down regulation of hormone function due to low energy availability can cause delay in growth and development. In particular, delayed puberty and menarche dampens the accrual of peak bone mass, with implications for bone health (Keay, 2000). Furthermore, there is evidence that these adverse effects on bone health might not be fully reversible (Keay, 1997)
From a psychological point of view, the young aspiring athlete and dancer is also at heightened risk. Explored and viewed by many dancers in “The Dark Side of Ballet Schools” Panorama (season 33, episode 28). Selection for specialised training will inevitably favour those who are self-motivated and dedicated. In a group of individuals sharing similar psychological traits this could act as a “breeding ground” for reinforcing these characteristics in ways that could lead to behaviours which are not conducive to positive outcomes. Rather reinforcing the negative interpretation of external and internal factors, leading to a vicious circle of reinforcing attitudes and behaviours leading to REDs, as described in Figure 1
Risk stratification
Early identification of those at risk of developing REDs is an important preventative strategy. Especially for young aspiring athletes and dancers where behaviours around eating and exercise are being developed and established. A step-by-step approach is provided in the updated version 2 of the Relative Energy Deficiency in sport Clinical Assessment Tool (REDsCat v2) to identify and risk stratify individuals (Stellingwerff, 2023 ). Initial, low cost, screening questionnaires can be helpful, particularly if tailored to a specific sport/activity or dance. For example: sports specific energy availability questionnaire (SEAQ) (Keay, 2018) and dance energy availability energy questionnaire (DEAQ) (Keay, 2020). This can be helpful in identifying those individuals where further investigation is clinically indicated. As REDs is a diagnosis of exclusion, targeted blood testing excludes medical conditions per se and provide objective quantification in the stratification of risk. Severe primary indicators of REDs are issues in the reproductive axis: long duration of amenorrhoea in females and low range testosterone in males.
From a combination of all these results the individual can be placed in an appropriate risk category. The updated REDs CAT v2 includes a finer grained approach with four categories from green, yellow, amber to red.
This assessment also provides the background on which to base the appropriate level of support. For all, management will be directed at restoring energy availability and include modification of training and nutritional intake. However, the details will vary according to the severity of REDs. Individuals with intentional REDs, especially when formally diagnosed with an eating disorder, will need most intensive input than a person with transient unintentional low energy availability.
Management
A nuanced approach is required for individual athletes, depending on their risk stratification and biopsychosocial factors. In all cases some degree of psychological support will be helpful. Involvement of the extended multidisciplinary team is ideal: medical doctor, dietician, coach and parent (where appropriate) with the athlete/dancer at the centre.
In order to restore energy availability this will require careful discussion around nutrition in terms of consistency of eating patterns and composition of food groups consumed. This starts with regular meals containing good portions of complex carbohydrate and protein. Studies show that inconsistent intake of carbohydrate (eg “backloading” eating to the evening) produces an unfavourable hormone profile. Fuelling around training is also a high priority for hormone health and driving positive adaptations to exercise. Pre training consumption of carbohydrate together with post training refuelling with both complex carbohydrate and protein within 20 minutes of stopping are important behaviours for favourable hormone response to exercise (Keay, 2022).
In terms of pharmacological intervention, NICE guidelines have been updated 2022 in recommending body identical hormone replacement therapy (HRT) over the combined oral contraceptive pill (COCP) for bone protection in those with evidence of bone poor health due to functional hypothalamic amenorrhoea (FHA) as a consequence of REDs (BASEM, 2023). Poor bone health is defined as age matched Z score < -1 of the lumbar spine (trabecular bone particularly sensitive to low oestradiol) and/or 2 or more stress fractures at a site of concern (trabecular rich bone). For male athletes/dancers external testosterone is not appropriate as this supresses internal hormone production. Furthermore, testosterone is on the world anti-doping authority (WADA) banned list and it is not possible to obtain a therapeutic use exemption (TUE) as REDs is a functional condition, not a medical condition.
Prevention
Prevention is always the ultimate goal. In order to achieve this aim, a cultural shift in sport and dance is required. Emphasis on the fact that health is a prerequisite for performance. Pursuing a lighter body weight or leaner body composition will not automatically lead to improved performance. Each individual will have a personal tipping point. As we are all different, there is no such thing as a generic “ideal” weight/shape/body composition.
In practical terms, prevention can be considered as primary, secondary and tertiary (Torstveit, 2023). Primary prevention consists of providing and disseminating reliable educational resources. Secondary prevention includes early identification of those at risk of developing REDs, together with prompt and correct diagnosis. For example, regardless of whether an athlete or dancer, amenorrhoea in a woman of reproductive age (apart from physiological amenorrhoea of pregnancy) is never “normal”; whether blood tests are in range, or not. The tertiary level of prevention encompasses evidence-based treatments. As mentioned above, NICE guidelines are now in line with Endocrine Society and IOC in advising temporising HRT for bone protection in FHA. Not the COCP which masks underlying hormone dysfunction and is not bone protective. Similarly, thyroxine is not advised where there is downregulation of this axis as a consequence of REDs. This is not the same as the medical condition of a primary underactive thyroid indicated by raised thyroid stimulating hormone (TSH) (Keay, 2022).
Conclusion
Ultimately, we all have a role to play in supporting exercisers, athletes and dancers in avoiding “the REDs card” (Mountjoy, 2023). This involves the extended multidisciplinary team, starting with the individual exerciser, family, friends and coaches. Then bringing in health care professionals from medicine, dietetics and physiotherapy.
Imbalances in behaviours around exercise and nutrition can have potential negative consequences on all aspects of health and performance. On a positive note, exercise, supported with appropriate nutrition, is an excellent way to achieve and maintain optimal physical, mental and social health and support performance. This is applicable for all ages and levels of exercisers from the recreational to the amateur and elite athlete.
References
Burke LM, Ackerman KE, Heikura IAet al. Mapping the complexities of Relative Energy Deficiency in Sport (REDs): development of a physiological model by a subgroup of the International Olympic Committee (IOC) Consensus on REDs British Journal of Sports Medicine 2023;57:1098-1108.
Drinkwater B, Nilson K, Chesnut C. Bone Mineral Content of Amenorrheic and Eumenorrheic Athletes N Engl J Med 1984; 311:277-281 DOI: 10.1056/NEJM198408023110501
Jurov I, Keay N, Hadžić V et al. Relationship between energy availability, energy conservation and cognitive restraint with performance measures in male endurance athletes. J Int Soc Sports Nutr 2021;18:24. doi:10.1186/s12970-021-00419-3
Jurov I, Keay N, Spudić D et al. Inducing low energy availability in trained endurance male athletes results in poorer explosive power. Eur J Appl Physiol 2022;122:503–13. doi:10.1007/s00421-021-04857-4
Keay N, Overseas A, Francis G. Indicators and correlates of low energy availability in male and female dancers BMJ Open Sport & Exercise Medicine 2020;6:e000906. doi: 10.1136/bmjsem-2020-000906
Keay N, Francis G. Infographic. Energy availability: concept, control and consequences in relative energy deficiency in sport (RED-S) British Journal of Sports Medicine 2019;53:1310-1311.
Keay N, Rankin A. Infographic. Relative energy deficiency in sport: an infographic guide
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Keay N, Francis G, Hind K. Low energy availability assessed by a sport-specific questionnaire and clinical interview indicative of bone health, endocrine profile and cycling performance in competitive male cyclists BMJ Open Sport & Exercise Medicine 2018;4:e000424. doi: 10.1136/bmjsem-2018-000424
Keay N, Francis G, Entwistleet al. Clinical evaluation of education relating to nutrition and skeletal loading in competitive male road cyclists at risk of relative energy deficiency in sports (RED-S): 6-month randomised controlled trial BMJ Open Sport & Exercise Medicine 2019;5:e000523. doi: 10.1136/bmjsem-2019-000523
Keay N. The modifiable factors affecting bone mineral accumulation in girls: the paradoxical effect of exercise on bone. Nutrition Bulletin 2000, 25: 219-222. https://doi.org/10.1046/j.1467-3010.2000.00051.x
Keay N, Fogelman I, Blake G. Bone mineral density in professional female dancers.
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Mountjoy M, Ackerman KE, Bailey Det al. Avoiding the ‘REDs Card’. We all have a role in the mitigation of REDs in athletes British Journal of Sports Medicine 2023;57:1063-1064.
Pensgaard AM, Sundgot-Borgen J, Edwards Cet al. Intersection of mental health issues and Relative Energy Deficiency in Sport (REDs): a narrative review by a subgroup of the IOC consensus on REDs British Journal of Sports Medicine 2023;57:1127-1135.
Stellingwerff T, Mountjoy M, McCluskey Wet al. Review of the scientific rationale, development and validation of the International Olympic Committee Relative Energy Deficiency in Sport Clinical Assessment Tool: V.2 (IOC REDs CAT2)—by a subgroup of the IOC consensus on REDs British Journal of Sports Medicine 2023;57:1109-1118.
International Olympic Committee relative energy deficiency in sport clinical assessment tool 2 (IOC REDs CAT2) British Journal of Sports Medicine 2023;57:1068-1072.
Shirley M, Longman D, Elliott-Sale K et al. A Life History Perspective on Athletes with Low Energy Availability. Sports Med 2022 52, 1223–1234. https://doi.org/10.1007/s40279-022-01643-w
Todd E, Elliot N, Keay N. Relative energy deficiency in sport (RED-S) British Journal of General Practice 2022; 72 (719): 295-297. DOI: https://doi.org/10.3399/bjgp22X719777
Torstveit M, Ackerman K, Constantini N et al. Primary, secondary and tertiary prevention of Relative Energy Deficiency in Sport (REDs): a narrative review by a subgroup of the IOC consensus on REDs Br J Sports Med 2023;57:1119–1126.
Relative energy deficiency in sport (RED-S) is an issue of increasing concern in sports and exercise medicine. RED-S impact exercisers of all levels and ages, particularly where low body weight confers a performance or aesthetic advantage. Key to mitigating adverse health and performance consequences of RED-S is supporting athletes and dancers to change behaviours. These infographics aim to assist clinicians in communicating the concepts to exercisers and in implementing effective management of athletes in their care[1].
Figure 1 illustrates the concept of energy availability (EA) in RED-S. Preferentially energy derived from dietary intake covers the demands of training and the remaining energy, EA, is, quantified in Kcal/Kg of fat free mass[2]. In Figure 1, the central bar illustrates adequate EA in an athlete where energy intake is sufficient to cover the demands of training and fundamental life processes to maintain health. Conversely, low energy availability (LEA) is a situation of insufficient EA to cover basic physiological demands. LEA leads to the adverse consequences of RED-S[3]. LEA can arise unintentionally or intentionally, due to a mismatch between energy intake and energy requirement. In Figure 1 the bar on the left shows LEA resulting from reduced energy intake with maintained training load. On the right, LEA is a consequence of increased training load with maintained energy intake.
Figure 2 illustrates that EA is under the control of an athlete[4]. The three behaviours relating to training, nutrition and recovery determine EA. Integrated periodisation of these behaviours results in optimal health and performance. Conversely, an imbalance in these behaviours results in suboptimal functionally. LEA in the case of high training loads relative to nutritional intake. Thus, this figure reinforces the important point in the IOC statements on RED-S that psychological factors which determine these behaviours are key in both the development, continuation and management of RED-S[2,3].
Figure 2 also shows the temporal, synergistic effect of these behaviours to ensure a fully functioning endocrine system. Hormones are key for health and to drive positive adaptations to exercise, to improve athletic performance. Thus hormones can be informative in tracking the response of an individual to these three input variables. Furthermore, endocrine markers relate to the RED-S clinical outcome of stress fracture in athletes, being more reliable as objective, quantifiable indicators of EA than numerical calculation of EA from direct assessment[5].
Authors
Nicola Keay1, Gavin Francis2
1 Department of Sport and Exercise Sciences, Durham University
2 Science4Perforamnce, London
Br J Sports Med 2019;0:1–2. doi:10.1136/bjsports-2019-100611
References
1 http://health4performance.co.uk (accessed 21/01/2019) Health4Performance Educational BASEM website raising awareness of RED-S Working group on RED-S British Association of Sport and Exercise Medicine 2018
2 Mountjoy M, Sundgot-Borgen J, Burke L et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update Br J Sports Med2018;52(11):687-697
3 Mountjoy M, Sundgot-Borgen J, Burke L et al. The IOC consensus statement: beyond the Female Athlete Triad–Relative Energy Deficiency in Sport (RED-S). Br J Sports Med2014;48(7):491-7
4 Burke L, Lundy B, Fahrenholtz L et al, & Melin. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. International Journal of Sport Nutrition and Exercise Metabolism2018; 28(4):350–363. https://doi.org/10.1123/ijsnem.2018-0142
5 2Heikura I, Uusitalo A, Stellingwerff T et al. Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. International Journal of Sport Nutrition and Exercise Metabolism2018; 28(4):403–411. https://doi.org/10.1123/ijsnem.2017-0313
Relative energy deficiency in sport (RED-S) is a clinical model that describes the potential adverse health and performance consequences of low energy availability (LEA) in male and female athletes. Identification of athletes at risk of LEA can potentially prevent these adverse clinical outcomes.
Athletes at risk of RED-S are those involved in sports where low body weight confers a performance or aesthetic advantage. In the case of competitive road cycling, being light weight results in favourable power to weight ratio to overcome gravity when cycling uphill. How can male cyclists at risk of LEA be effectively identified in a practical manner?
Energy availability (EA) is defined as the residual energy available from dietary intake, once energy expenditure from exercise training has been subtracted. This available energy is expressed as KCal/Kg fat free mass (FFM). A value of 45 KCal/Kg FFM is roughly equivalent to basal metabolic rate, in other words the energy required to sustain health. In order to quantify EA, accurate measurements of energy intake and expenditure, and FFM assessed from dual X ray absorptiometry (DXA), need to be undertaken. However this is not practical or feasible to undertake all these measurements outside the research setting. Furthermore, methodology for assessing energy intake and expenditure is laborious and fraught with inaccuracies and subjectivity in the case of diet diaries for “free living athletes“. Even if a value is calculated for EA, this is only valid for the time of measurement and does not give any insights into the temporal aspect of EA. Furthermore, an absolute EA threshold has not been established, below which clinical symptoms or performance effects of RED-S occur.
Self reported questionnaires have been shown to be surrogates of low EA in female athletes. However there are no such sport specific questionnaires, or any questionnaires for male athletes. Endocrine and metabolic markers have been proposed as quantitative surrogate measures of EA and shown to be linked to the RED-S clinical outcome of stress fractures in runners. In female athletes the clinical sign of regular menstruation demonstrates a functioning H-P ovarian axis, not suppressed by LEA. What about male athletes? Although hypothalamic suppression of the reproductive axis due to LEA can result in low testosterone, high training loads, in presence of adequate EA, can lead to the same negative effect on testosterone concentration.
Male cyclists present a further level of complexity in assessing EA status. In contrast to runners, stress fracture will not be an early clinical warning sign of impaired bone health resulting from low EA. Furthermore cyclists are already at risk of poor bone health due to the non weight bearing nature of the sport. Nevertheless, traumatic fracture from bike falls is the main type of injury in cycling, with vertebral fracture requiring the longest time off the bike. Chris Boardman, a serial Olympic medal winner in cycling, retired in his early 30s with osteoporosis. In other words, in road cycling, the combined effect of the lack of osteogenic stimulus and LEA can produce clinically significant adverse effects on bone health.
Using a decision tree approach, the factor most indicative of impaired age matched (Z score) lumbar spine BMD was sport specific clinical assessment of EA. This assessment took the form of a newly developed sports specific energy availability questionnaire and interview (SEAQ-I). Reinforcing the concept that the most important skill in clinical medical practice is taking a detailed history. Questionnaire alone can lead to athletes giving “correct” answers on nutrition and training load. Clinical interview gave details on the temporal aspects of EA in the context of cycle training schedule: whether riders where experiencing acute intermittent LEA, as with multiple weekly fasted rides, or chronic sustained LEA with prolonged periods of suppressed body weight. Additionally the SEAQ-I provided insights on attitudes to training and nutrition practices.
Cyclists identified as having LEA from SEAQ-I, had significantly lower lumbar spine BMD than those riders assessed as having adequate EA. Furthermore, the lowest lumbar spine BMD was found amongst LEA cyclists who had not practised any load bearing sport prior to focusing on cycling. This finding is of particular concern, as if cycling from adolescence is not integrated with weight bearing exercise and adequate nutrition when peak bone mass (PBM) is being accumulated, then this risks impaired bone health moving into adulthood.
Further extension of the decision tree analysis demonstrated that in those cyclists with adequate EA assessed from SEAQ-I, vitamin D concentration was the factor indicative of lumbar spine BMD. Vitamin D is emerging as an important consideration for athletes, for bone health, muscle strength and immune function. Furthermore synergistic interactions with other steroid hormones, such as testosterone could be significant.
What about the effects of EA on cycling performance? For athletes, athletic performance is the top priority. In competitive road cycling the “gold standard” performance measure is functional threshold power (FTP) Watts/Kg, produced over 60 minutes. In the current study, 60 minute FTP Watts/Kg had a significant relationship to training load. However cyclists in chronic LEA were under performing, in other words not able to produce the power anticipated for a given training load. These chronic LEA cyclists also had significantly lower testosterone concentration. Periodised carbohydrate intake for low intensity sessions is a strategy for increasing training stimulus. However if this acute intermittent LEA is superimposed on a background of chronic LEA, then this can be counter productive in producing beneficial training adaptations. Increasing training load improves performance, but this training is only effective if fuelling is tailored accordingly.
Male athletes can be at risk of developing the health and performance consequences of LEA as described in the RED-S clinical model. The recent study of competitive male road cyclists shows that a sport specific questionnaire, combined with clinical interview (SEAQ-I) is an effective and practical method of identifying athletes at risk of LEA. The temporal dimension of LEA was correlated to quantifiable health and performance consequences of RED-S.
What updates are presented in the IOC consensus statement on RED-S 2018?
Prevention
Awareness is the key to prevention. Yet RED-S continues to go unrecognised. Less than 50% of clinicians, physiotherapists and coaches are reported as able to identify the components of the female athlete triad. In a survey of female exercisers in Australia, half were unaware that menstrual dysfunction impacts bone health. Note that these concerning statistics relate to the female athlete triad. Lack of awareness of RED-S in male athletes is even more marked. RED-S as a condition impacting males, as well as females, was described in the initial IOC consensus statement published in 2014. However there is evidence of the occurrence of RED-S in male athletes pre-dating this.
Identification
Identifying an athlete/dancer with RED-S is not always straight forward. In dance or sports where being light weight confers a performance or aesthetic advantage, how can a coach/teacher distinguish between athletes who have this type of physique “naturally” and those who have disordered eating and are at risk of RED-S? Equally, low energy availability could be a result either of intentional nutrition restriction to control body weight and composition, or an unintentional consequence of not matching an increase in energy expenditure (due to increased training load), with a corresponding increase in energy intake.
Performance effects
Performance is paramount to any athlete or dancer. Apart from physical ability, being driven and determined are important characteristics to achieve success. If weight loss is perceived as achieving a performance advantage, then this can become a competitive goal in its own right: in terms of the individual and amongst teammates. This underlies the interactive effect of psychological factors in the development and progression in the severity of RED-S.
There is both theoretical and practical evidence that short term low energy availability impairs athletic performance as the body is less able to undertake high quality sessions and benefit from the physiological adaptations to exercise. Within day energy deficits have been shown to have adverse effects in both male and female athletes in terms of impact on oestradiol/testosterone and cortisol concentrations. Failure to refuel with carbohydrate and protein promptly after a training session in male runners has been shown to have an adverse effect on bone turnover markers.
To underline the adverse performance effect of low energy availability, a recent study demonstrated that in female athletes, those with functional hypothalamic amenorrhea displayed decreased neuromuscular performance compared to their eumenorrhoeic counterparts. This adverse effect on performance is of particular concern where such skills are crucial in precisely those sports/dance where RED-S is most prevalent. Clearly this situation puts such athletes at increased injury risk, especially if associated with adverse bone mineral density (BMD) due to low energy availability.
Ironically the long term consequences of low energy availability produce adverse effects on body composition: increased fat/lean and reduction in BMD. In other words, the precise opposite effects of what an energy restricted athlete is trying to achieve. In terms of bone health, the lumbar spine is most sensitive to nutrition/endocrine factors (apart from rowers where mechanical loading can attenuate BMD loss at this site in RED-S). Suboptimal BMD is associated with an increased risk of bone injury and therefore impaired performance.
Keay BJSM 2017
Medical Assessment
Low energy availability is the fundamental issue driving the multi-system dysfunction in the endocrine, metabolic, haematological, cardiovascular, gastrointestinal, immunological and psychological systems in RED-S. However, there are practical issues with directly quantifying energy availability as this is subject to the inaccuracies of reliably measuring energy intake and output. Endocrine and metabolic markers have been shown to more objective indicators of low energy availability, which in turn are correlated to performance outcomes such as bone stress injury in male and female athletes. In the case of female athletes there is an obvious clinical indicator of sufficient energy availability: menstrual cycles. As there is no such obvious clinical sign in male athletes is this why RED-S is less frequently recognised? In both female and male athletes there is some degree of clinical variation: there is no absolute threshold cut off with a set temporal component of low energy availability resulting in amenorrhoea or low testosterone in males. Therefore the IOC recommends that individual clinical evaluation include discussion of nutrition attitudes and practices, combined with menstrual history for females and endocrine markers for male and female athletes will give a very clear indication if an athlete is at risk of/has RED-S.
Management
RED-S is a diagnosis of exclusion. Once medical conditions per se have been excluded, RED-S presents a multi-system dysfunction caused by a disrupted periodisation of nutrition/training/recovery. For an athlete the motivation to address these imbalances is to be in a position reach their full athletic potential. This attainment is compromised in RED-S.
Pharmacological interventions are not recommended as first line management in amenorrhoeic athletes. Oral contraception (OCP) masks amenorrhoea with withdrawal bleeds. OCP does not support bone health and indeed may exacerbate bone loss by suppressing further IGF-1. Although transdermal oestrogen, combined with cyclic progesterone does not down regulate IGF-1, nevertheless any hormonal intervention cannot be a long term solution, as bone loss will continue if energy availability is not addressed as a priority.
What next?
The IOC statement suggests further research should include studies with allocation of athletes to intervention groups, with assessment of effects over a substantial time period. Currently a study of competitive male road cyclists over a training/competition season is being undertaken to evaluate the effects of nutrition advice and off bike skeletal loading exercise. Crucially outcome measures will not only be based on bone health and endocrine markers, but measures of performance in terms of power production and race results.
To raise awareness and build support pathways as recommended in the IOC statement, this is an on going process which requires communication between athlete/dancers, coaches/teachers, parents and healthcare professionals both medical and non medical working with male and female athletes.
Dr Nicky Keay 