Click on link below for write up in recent One Dance publication
Relative energy deficiency in sport (RED-S) is a clinical syndrome encompassing adverse health and performance (figure 1) consequences of low energy availability (LEA) in male and female exercisers of all ages and all levels from recreational to elite.
LEA is a situation where energy intake is insufficient to cover the combined energy demands of training and baseline physiological processes to maintain health. LEA can arise unintentionally or intentionally (figure 2). Unintentional LEA results from increased training load, which is not matched by an increased energy intake. Intentional LEA is more likely to arise in sports where low body weight confers a performance or aesthetic advantage, for example, gravitational sports including cycling, ski-jumping, climbing; weight-category sports including boxing and judged artistic sports including gymnastics, aquatic disciplines. RED-S is also a risk in dancers of all genres, but in particular ballet. Intentional LEA can be due to spectrum of disordered eating to eating disorders. The body responds to LEA by downregulating fundamental physiological processes. This ‘energy saving mode’ is of particular clinical significance in the endocrine network system (figure 3).
For women, LEA can manifest itself as menstrual disruption, in men this corresponds to low testosterone. The net effects of dysfunctional endocrine feedback loops are adverse effects on health and dampened response to training stimuli. For example, endocrine dysfunction manifests as suboptimal bone health with increased risk of bone stress injuries. Increased duration of LEA accrues cumulative effects on endocrine networks and hence health and performance (figure 2). Although the exerciser may initially improve athletic performance with short-term LEA, long-term LEA will lead to deterioration in health and performance.
Therefore, early identification of those at risk of LEA is essential in preventing the clinical consequences of RED-S. This is the purpose of the BASEM website Health4Performance to raise awareness of RED-S among athletes/dancers, coaches, parents, friends and healthcare professionals to encourage a multidisciplinary team approach to identifying and supporting those at risk of RED-S.
Dr Nicola Keay, Department of Sport and Exercise Sciences, Durham University, UK.
Dr Alan Rankin Department of Sports Medicine, Sport Ireland Institute, Dublin, Ireland
Br J Sports Med 2019;0:1–3. doi:10.1136/bjsports-2018-100354
1 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 Med 2014;48:491–7.
2 Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med 2018;52:687–97.
3 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 Exerc Med 2018;4:e000424.
4 Keay N. Raising Awareness of RED-S in Male and Female Athletes and Dancers. Br J Sport Med blog 2018. https://blogs.bmj.com/bjsm/2018/10/30/raisingawareness-of-red-s-in-male-and-female-athletes-anddancers/ (accessed 19 Jan 2019).
5 Health4Performance. Educational BASEM website raising awareness of RED-S Working group on RED-S. BMJ Open Sport Exerc Med 2018. http:// health4performance.co.uk (accessed 19 Jan 2019).
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
© Author(s) (or their employer(s)) 2019. No commercial re-use. See rights and permissions. Published by BMJ. To cite Keay N, Rankin A. Br J Sports Med Epub ahead of print: [please include Day Month Year]. doi:10.1136/ bjsports-2018-100354
Although improvements are being made in raising awareness and in effective medical management of relative energy deficiency in sport (RED-S)[1, 2] what about once an athlete/dancer is “medically cleared” to return to sport/dance? What advice/support is there for athletes/dancers and their coaches/teachers? After discussions with coaches, here are some suggestions on how to achieve return to sport/dance after RED-S.
To recap, RED-S is a situation of low energy availability (LEA), which can lead to adverse health and performance consequences[3,4]. LEA can be a result of intentional energy restriction, which covers a spectrum of issues with eating from disordered eating to full blown clinical eating disorder. Ironically the original intention of these eating issues may have been to improve athletic performance, yet sustained LEA will ultimately lead to stagnation and deterioration in performance as found in male athletes.
The desire to return to full fitness can be a powerful incentive to address LEA. Nevertheless return to sport/dance needs to be carefully structured in collaboration with coaches to prevent injury and avoiding regression to the LEA state.
Structured return to training and nutrition
- Initially focus should be on body weight strength and conditioning (S&C). Inevitably in RED-S adaptive responses to training stimuli will be dampened due to shut down of hormones networks into an energy saving mode. Once adequate EA has been established, hormone networks will be able to respond. Restoring muscle tone and working on proprioception forms a good basis to build from to mitigate injury risk. Impaired neuromuscular skills have been reported in female athletes in LEA, together with adverse effects of LEA on bone health increases injury risk.
- The other reason for gradual return to training is that a routine of fuelling around training (before, during, after) needs to be established. In particular recovery nutrition within 30 minutes window to enable hormonal responses to training. Note that having this recovery nutrition does not mean reducing intake at the next meal!
- Long endurance should be eased into after restoring muscle strength and control, in order to prevent injury. Additionally this type of training will necessitate a higher energy requirement. If adequate energy availability has only recently been restored, the balance is fragile and so too much training too soon can have negative effects. Especially if a fuelling strategy around training has not been established as described above.
- High intensity/interval training should be the last type of training to be resumed as this places the highest stress and requires the highest energy demand on the athlete/dancer.
- Injury, soft tissue and bone stress responses are more frequent in hormonal dysfunction of RED-S in both male and female athletes. If an injury has been sustained during this period of LEA then particular emphasis needs to be on initial S&C. In the case of previous bone stress responses, multi-direction loading is key to build bone strength before resuming formal run training in athletes who are runners. Even if a bone injury has not occurred, bone turnover is one of the first systems to be adversely impacted by RED-S, so including this type of multidirectional bone loading in the initial structured return for all athletes/dancers would be beneficial.
- Discuss with your coach a realistic, attainable goal if this will help. Maybe a low key race/event several months down the track
What to look out for
- Don’t ignore injury niggles, illness or fatigue. Discuss with your coach and back off if necessary. This is a process, not a sprint.
- Female athletes. You may well have experienced menstrual disruption during your time in LEA. This is a crucial training metric. Please use it! If your menstruation becomes irregular/stops this is your warning sign that your body is not ready to step up training. Male coaches please reinforce this and be aware of this point. Remember Gwen Jorgensen posting her periods on Training Peaks as a training metric?
- Flexibility in approach. Try not to put pressure on yourself to return to your previous PBs. It is important to have a plan, but you can be flexible. Everyone is different so this process of returning to sport/dance does not have a set, rigid timetable.
- Enjoyment! Don’t forget the original reason that you started your sport/dance was for enjoyment! This is an opportunity to rediscover that joy, whether you return to competition or not.
- “Recovery?” Does anyone fully “recover” from disordered eating/eating disorder? I don’t think so. To be a successful athlete, or indeed successful in life you need self-motivation, drive, determination. All admirable qualities, but sometimes these can get diverted to cause unhealthy eating/training patterns. So be aware that in times of stress it may be tempting to revert to old habits of under eating/over exercise to reassure yourself that you are in control.
- Be prepared for questions: why have you been off training? Why are you not doing fully training schedule? Maybe you want to tell your team mates/friends. Maybe you don’t. That is your call.
So good luck with your return to sport/dance after RED-S, if that is what you want to do. Always discuss with you coach how to approach this.
1 BASEM Educational website www.health4perforamnce.co.uk
2 BJSM blog: Update on RED-S N Keay 2018
3, 4 IOC consensus statements on RED-S BJSM 2014 and update 2018
5 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. N Keay, G Francis, K Hind. BMJ Open in Sport and Exercise Medicine 2018
5 Reduced Neuromuscular Performance in Amenorrheic Elite Endurance Athletes.
Tornberg Å Melin A Koivula F Johansson A Skouby S et. al.Medicine and science in sports and exercise 2017 vol: 49 (12) pp: 2478-2485
6 Low Energy Availability Is Difficult to Assess but Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes Heikura, Ida A. Uusitalo, Arja L.T. Stellingwerff, Trent et al International Journal of Sport Nutrition and Exercise Metabolism 2018, 28, 4, 403-411
7 What’s so good about Menstrual Cycles? N Keay BJSM blog 2019
Menstrual periods are a barometer of healthy hormones. The evolutionary purpose of ovulation is to reproduce. Furthermore the carefully biologically choreographed variation of hormones that occurs during an ovulatory menstrual cycle is crucial to health and athletic performance.
Why? Hormones are chemical messengers that have far reaching effects throughout the body and drive the beneficial adaptations to exercise. In the case of menstrual cycles, the fluctuations of oestrogen and progesterone are key to this process. The effects of these sex steroids go far beyond reproduction. These hormones play important roles in bone strength, cardiovascular health, optimal lipid profile and production of neurotransmitters to regulate mood. The effects of low levels of oestrogen and progesterone are well documented in menopausal women who experience loss in bone mass, risk of osteoporosis and fracture, together with an increase risk of cardiovascular disease.
Amenorrhoea=lack of menstrual cycles
Menarche= start of menstrual cycles
According to the Royal College of Obstetrics and Gynaecology
Primary Amenorrhoea: no onset of menstrual cycles by age 16 years.
Secondary amenorrhoea: cessation of menstrual cycles in a previously regularly menstruating woman for > 6months
Oligomenorrhoea: < 9 menstrual cycles per calendar year
Any form of amenorrhoea requires medical investigation to exclude an underlying medical condition. The most common medical causes of amenorrhoea are polycystic ovary syndrome (PCOS), prolactinoma, thyroid conditions and other endocrine conditions. Functional hypothalamic amenorrhoea (FHA) is a diagnosis of exclusion. In other words before arriving at a diagnosis of FHA , medical conditions that could potentially cause amenorrhoea have to be ruled out.
Relative energy deficiency in sport (RED-S) is a situation of low energy availability (LEA) that can be unintentional or intentional as a result of a mismatch between energy intake and energy requirement. The two sources of energy demand arise from exercise training load and maintenance of fundamental physiological function across multiple body systems . In female athletes/dancers with RED-S the most obvious clinical sign is amenorrhoea as a result of FHA. In all cases of RED-S the management strategy is directed to address the underlying issue of LEA .
In female athletes/dancer with FHA due to RED-S, there is the possibility of pharmacological intervention based on the RED-S Clinical Assessment Tool . In other words evidence from DXA of Z-score of lumbar spine < -1 and/or stress fracture. What are the most effect hormonal interventions in such cases?
What’s in a name? It is every woman’s right to choose the form of contraception she wishes to use. Hormonal contraception provides a convenient method. The combined oral contraceptive pill (OCP) contains oestrogen and progesterone to prevent ovulation. The OCP produces regular withdrawal bleeds in response to these external hormones. Progesterone-only contraception can be taken orally, via implant or delivered by an intrauterine coil and typically does not produce withdrawal bleeds. As with any medication there are potential side effects, which have to be weighed up against the benefits. Regarding the effect of hormonal contraception on bone in young menstruating women, there is evidence that such medication can impair bone health .
The OCP produces regular withdrawal bleeds. These are NOT menstrual periods; ovulation is prevented. Rather the OCP causes withdrawal bleeds driven by external non-physiological hormones, as opposed to internally physiologically produced hormones. This is a reason why the OCP is not recommended in FHA, as this medication will mask what is happening with internal hormones . In other words the barometer of healthy hormones has been removed when taking the OCP.
Furthermore, studies show that the OCP can impact other hormone systems that play a role in bone health. The OCP is taken orally thereby producing first pass effects in the liver. These effects include induction of liver enzymes and increased production of binding proteins for hormones. Binding proteins reduce the freely available active form of hormones such insulin like growth factor 1 (IGF-1). This effect is particularly marked in those OCP with non-physiological ethinyl oestradiol. In the case of RED-S there is already a low level of active IFG-1, due to the general suppression of the hypothalamic-pituitary axis.
Therefore in addition to masking FHA, the OCP can also further decrease IGF-1 and thus compound the negative effect on bone. This has been shown to be the case in the clinical setting where the OCP was found to have no bone protective effect on bone mineral density (BMD) in women with FHA. Rather hormone replacement therapy (HRT) consisting of transdermal physiological oestrogen with cyclic micro-ionised progesterone was found to have a positive effect on BMD [7 , 8]
Therefore, if hormonal treatment is to be used in RED-S, HRT (transdermal oestradiol and cyclic micro-ionised progesterone) is best clinical practice. This decision requires careful discussion with the athlete/dancer clarifying that HRT should only be a short-term measure to protect bone health whilst the underlying issue of LEA is being resolved. Behavioural measures relating to training load, nutrition and recovery are essential to restore global hormonal function.
OCP V HRT
• What? Both provide oestrogen and progesterone, but in different forms: non-physiological v physiological
• Why? Purpose of the OCP is to suppress production of endogenous female hormones and prevent ovulation. Purpose of HRT is to replace the physiological amount and form of oestrogen and progesterone
• How? The OCP decreases levels of active, unbound IGF-1. Not bone protective in FHA of RED-S. HRT shown to improve BMD in FHA of RED-S
What to do? Hormonal contraception is a choice for women. In some medical conditions where there is adequate/excess oestrogen such as endometriosis or PCOS, hormonal contraception is effective in clinical management. However in the case of FHA, in particular when occurring as a consequence of LEA in RED-S there is evidence that the OCP is not bone protective and masks the clinical sign of menstruation.
The priority in managing RED-S is to address LEA. If bone protection is required, whilst addressing LEA, HRT (transdermal oestrogen and cyclic progesterone) is best clinical practice.
 Joy, E., De Souza, M. J., Nattiv, A., Misra, M., Williams, N. I., Mallinson, R. J., … Borgen, J. S. (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), 219–232. https://doi.org/10.1249/JSR.0000000000000077
 Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., … Ljungqvist, A. (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://doi.org/10.1136/bjsports-2014-093502
 Mountjoy, M., Sundgot-Borgen, J. K., Burke, L. M., Ackerman, K. E., Blauwet, C., Constantini, N., … Budgett, R. (2018). IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. British Journal of Sports Medicine, 52(11), 687–697. https://doi.org/10.1136/bjsports-2018-099193
 Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., … Ackerman, K. (2015, April 1). Relative energy deficiency in sport (RED-S) clinical assessment tool (CAT). British Journal of Sports Medicine. BMJ Publishing Group. https://doi.org/10.1136/bjsports-2015-094873
 Beksinska M, Smit J, Hormonal contraception and bone mineral density. Expert Review of Obstetrics & Gynecology, 2011 vol: 6 (3) pp: 305-319
 Gordon, C. M., Ackerman, K. E., Berga, S. L., Kaplan, J. R., Mastorakos, G., Misra, M., … Warren, M. P. (2017). Functional hypothalamic amenorrhea: An endocrine society clinical practice guideline. Journal of Clinical Endocrinology and Metabolism, 102(5), 1413–1439. https://doi.org/10.1210/jc.2017-00131
 Ackerman, K. E., Singhal, V., Baskaran, C., Slattery, M., Campoverde Reyes, K. J., Toth, A., … Misra, M. (2018). Oestrogen replacement improves bone mineral density in oligo-amenorrhoeic athletes: A randomised clinical trial. British Journal of Sports Medicine. BMJ Publishing Group. https://doi.org/10.1136/bjsports-2018-099723
 Singhal, V., Ackerman, K. E., Bose, A., Torre Flores, L. P., Lee, H., & Misra, M. (2018). Impact of Route of Estrogen Administration on Bone Turnover Markers in Oligoamenorrheic Athletes and its Mediators. The Journal of Clinical Endocrinology & Metabolism. https://doi.org/10.1210/jc.2018-02143
There is growing evidence that for athletes, being replete in vitamin D is important for many key areas of health and performance. For bone health, muscle strength and to support immune function.
At the recent International Association of Dance Medicine conference, in addition to presenting on Dance Endocrinology I also took part in a “duel” on vitamin D to argue the case for vitamin D supplementation, in dance/athletic populations. In fact Vitamin D is a type of steroid hormone. An article in BJSM discussed the synergistic action of steroid hormones, in particular vitamin D and the sex steroids. In dancers who train in studios inside, away from the sun then there is evidence that levels of vitamin D can become low, particularly during winter months. Supplementing with vitamin D in these elite female dancers reduced injuries and significantly improved muscle strength and jump height.
What about athletes that train outside? What about male athletes? You might think that competitive road cyclists would benefit from plenty of time spent outside and that vitamin D levels would be close to athlete recommended level of 90 nmol/L. However, in our recent study of 50 competitive male road cyclists, the majority had low athlete levels of vitamin D. Even some cyclists who reported taking supplementation for this vitamin were found to have low levels, reflecting variations and uncertainties in what dose to take. Conversely some riders taking supplementation had levels that were well above recommended athlete levels. More is not necessarily better in this situation and very high levels can lead to toxicity.
Bone health in road cyclists can be compromised due to 2 factors. In the first instance, being a non weight bearing sport means lack of mechanical osteogenic (bone stimulating) skeletal loading. In addition, road cycling is a gravitational sport where being light weight confers a performance advantage in terms of power to weight ratio. This can lead to restrictive nutrition practices and low energy availability (LEA) in athletes/dancers. LEA is a situation where dietary energy intake is insufficient to support both training demands and the energy requirement to keep healthy. So LEA has adverse effects on both health and athletic performance described in the clinical model RED-S (relative energy availability in sport). This includes a negative impact on bone health. DXA is regarded as “gold standard” quantification of impact of LEA and RED-S on bone health. In our study a specially designed SEAQ-I (sports specific questionnaire and clinical interview) was found to be the most effective indicator of poor bone health found with DXA. 28% of the cyclists were identified as having LEA with correspondingly low bone mineral density for their age.
What about the effect of vitamin D levels on bone health? In those cyclists assessed as having adequate EA from SEAQ-I, then vitamin D was an important factor in bone health. However, in those 28% cyclists assessed as having LEA, vitamin D did not feature as as such an important factor. Essentially having adequate EA is the top priority for health and performance. The other observation is that many of those cyclists in LEA, although not consuming adequate calories, nevertheless were taking plenty of supplements in the belief that this would reduce any negative effects of restrictive nutrition. This strategy does not work. The reason being that LEA causes dysfunction not just of one hormone in isolation, rather interactive hormone networks become disrupted. Hormones are crucial for supporting bone health, particularly IGF-1, testosterone and vitamin D in males. Furthermore there is evidence to show that there is a synergistic interaction between testosterone and vitamin D in men. In out study those riders with chronic LEA were found to have significantly lower testosterone than the other cyclists. So even if male athletes with LEA have adequate levels of vitamin D, then low levels of other hormones, such as testosterone, will have net negative effect on bone health.
So male cyclists are at risk of poor bone health for the following reasons:
- Cycling is a non-weight bearing sport,
- Vitamin D can be below athlete recommended levels, even if EA adequate
- Long term LEA causes clinical consequences of RED-S including disruption of hormones necessary for maintaining bone health
Does this matter? An early warning sign in runners of LEA is stress fracture. In cyclists the first evidence of an issue with bone health could be vertebral fracture from a bike crash, as this is area of skeleton most adversely effected by LEA and most serious in terms of fracture site requiring longest time off bike. Moreover our study found that in some cyclists with chronic, long term LEA cycling performance in terms of 60 minute functional threshold power (FTP) was below that anticipated from training load.
To perform at your full athletic potential you need adequate EA and vitamin D.
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 and Exercise Medicine. Keay, Francis, Hind 2018
How do you identify male cyclist at risk of RED-S? BJSM, Dr N Keay 2018
Fuelling for Cycling Performance Science4Performance 2018
Synergistic interactions of steroid hormones BJSM, Dr N Keay 2018
Raising Awareness of RED-S in Male and Female Athletes and Dancers BJSM, Dr N Keay 2018
2018 UPDATE: Relative Energy Deficiency in Sport (RED-S) BJSM, Dr N Keay 2018
The influence of winter vitamin D supplementation on muscle function and injury occurrence in elite ballet dancers: A controlled study Journal of Science and Medicine in Sport 2014
Listen into a great discussion I had with Dr Nigel Callender an ex competitive climber and climbing coach about the “elephant in the room” in competitive climbing.
As a gravitational sport, being a light-weight climber confers a performance advantage. However, being alert to low energy availability and the clinical consequences of RED-S on health and performance is important for climbers. With climbing being included the next Olympics, then hopefully this will raise awareness of being alert to athletes at risk of low energy availability and RED-S.
Insights from Dr Nigel Callender, sports scientist turned medical doctor (anaesthetics/critical care trainee) an active researcher, largely into the exercise physiology aspects of climbing and ex-competitor, having represented Ireland at international level and been British bouldering champion before shoulder injuries ended that. Sport climbing is included in the 2020 Tokyo summer games in its three competitive disciplines; bouldering, lead climbing and speed climbing. Each sub-discipline has a slightly different athlete profile and physiological demands, but all are obviously under the heading of gravity dependent sports. Current participation figures put yearly indoor climbing participation at around the one million mark in the UK and it is said to be one of the fastest growing sports worldwide. The sport is being recognised as a great way to improve overall health and fitness, with recent papers citing it as a useful rehab activity for many physical and mental health conditions and also as a health promotion tool.
Although climbing has been a formal competitive sport in some sense since the late 80’s, it still lacks much in the way of formal training and medical guidelines. Being a gravity dependent sport, strength to weight ratio is important, however Dr Callender and his colleagues are seeing a high incidence of restrictive eating patterns at all levels of the sport and a lack of awareness around the performance impairments and health risks associated with a significant or prolonged negative energy balance in some athletes.
The Outdoor Athlete Podcast is a bit of a winter project that came about to establish a gold-standard resource, driven by credible experts in their relevant fields, as an attempt to provide high-quality and evidence-based information amongst the confusing advice that is now the internet. It’s free and always will be and it was inspired by the BJSM Podcasts though broadly aiming at ‘Outdoor Athletes’ e.g. Climbers, Fell/Trail runners, Mountain bikers and anyone happy to listen.
For more information on climbing in the UK, including competition climbing see http://www.thebmc.co.uk
Health4Performance is a recently developed BASEM open access educational resource
This is a world premier: a resource developed for and by athletes/dancers, coaches/teachers, parents/friends and healthcare professionals to raise awareness of Relative Energy Deficiency in Sport (RED-S)
Optimal health is required to attain full athletic potential. Low energy availability (LEA) can compromise health and therefore impair athletic performance as described in the RED-S clinical model.
Dietary energy intake needs to be sufficient to cover the energy demands of both exercise training and fundamental physiological function required to maintain health. Once the energy demands for training have been covered, the energy left for baseline “housekeeping” physiological function is referred to as energy availability (EA). EA is expressed relative to fat free mass (FFM) in KCal/Kg FFM. The exact value of EA to maintain health will vary between genders and individuals, roughly equivalent to resting metabolic rate of the individual athlete/dancer. LEA for an athlete or dancer will result in the body going into “energy saving mode” which has knock on effects for many interrelated body systems, including readjustment to lower the resting metabolic rate in the longer term. So although loss in body weight may be an initial sign, body weight can be steady in chronic LEA due to physiological energy conservation adaptations. Homeostasis through internal biological feedback loops in action.
The most obvious clinical sign of this state of LEA in women is cessation of menstruation (amenorrhea). LEA as a cause of amenorrhoea is an example of functional hypothalamic amenorrhoea (FHA). In other words, amenorrhoea arising as a result of an imbalance in training load and nutrition, rather than an underlying medical condition per se, which should be excluded before arriving at a diagnosis of FHA. All women of reproductive age, however much exercise is being undertaken, should have regular menstrual cycles, which is indicative of healthy hormones. This explains why LEA was first described as the underlying aetiology of the female athlete triad, as women in LEA display an obvious clinical sign of menstrual disruption. The female athlete triad is a clinical spectrum describing varying degrees of menstrual dysfunction, disordered nutrition and bone mineral density. However it became apparent that the clinical outcomes of LEA are not limited to females, nor female reproductive function and bone health in female exercisers. Hence the evolution of the clinical model of RED-S to describe the consequences of LEA on a broader range of body systems and including male athletes.
A situation of LEA in athletes and dancers can arise unintentionally or intentionally. In the diagram below the central column shows that an athlete where energy intake is sufficient to cover the demands from training and to cover basic physiological function. However in the column on the left, although training load has remained constant, nutritional intake has been reduced. This reduction of energy intake could be an intentional strategy to reduce body weight or change body composition in weight sensitive sports and dance. On the other hand in the column on the right, training load and hence energy demand to cover this has increased, but has not been matched by an increase in dietary intake. In both these situations, whether unintentional or intentional, the net results is LEA, insufficient to maintain health. This situation of LEA will also ultimately impact on athletic performance as optimal health is necessary to realise full athletic potential.
Although LEA is the underlying aetiology of RED-S, there are many methodological and financial issues measuring LEA accurately in “free living athletes“. In any case, the physiological response varies between individuals and depends on the magnitude, duration and timing of LEA. Therefore it is more informative to measure the functional responses of an individual to LEA, rather than the value calculated for EA. As such, Endocrine markers provide objective and quantifiable measures of physiological responses to EA. These markers also reflect the temporal dimension of LEA; whether acute or chronic. In short, as hormones exert network effects, Endocrine markers reflect the response of multiple systems in an individual to LEA. So by measuring these key markers, alongside taking a sport specific medical history, provides the information to build a detailed picture of EA for the individual, with dimensions of time and magnitude of LEA. This information empowers the athlete/dancer to modify the 3 key factors under their control of training load, nutrition and recovery to optimise their health and athletic performance.
Who is at risk of developing RED-S? Any athlete involved in sports or dance where being light weight confers a performance or aesthetic advantage. This is not restricted to elite athletes and dancers. Indeed the aspiring amateur or exerciser could be more at risk, without the benefit of a support team present at professional level. Young athletes are at particular risk during an already high energy demand state of growth and development. Therefore early identification of athletes and dancers at risk of LEA is key to prevention of development of the health and performance consequences outlined in the RED-S clinical model. Although there is a questionnaire available for screening for female athletes at risk of LEA, more research is emerging for effective and practical methods which are sport specific and include male athletes.
Early medical input is important as RED-S is diagnosis of exclusion. In other words medical conditions per se need to be ruled out before arriving at a diagnosis of RED-S. Prompt medical review is often dependent on other healthcare professionals, fellow athletes/dancers, coaches/teachers and parents/friends all being aware and therefore alert to RED-S. With this in mind, the Health4Performance website has areas for all of those potentially involved, with tailored comments on What to look out for? What to do? Ultimately a team approach and collaboration between all these groups is important. Not only in identification of those at risk of LEA, but in an integrated support network for the athlete/dancer to return to optimal health and performance.
Heath4Performance BASEM Educational Resource
Video introduction to Health4Performance website
What is Dance Medicine? BJSM 2018
Identification and management of RED-S Podcast 2018
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 Keay, Francis, Hind. BJM Open Sport and Exercise Medicine 2018
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.
What practical clinical tools are most effective at identifying competitive male cyclists at risk of the health and performance consequences of LEA outlined in the RED-S model? This was the question our recent study addressed. The lumbar spine is a skeletal site known to be most impacted by nutrition and endocrine factors and DXA is recognised as the “gold standard” of quantifying age matched Z score for bone mineral density (BMD) in the risk stratification of RED-S. What is the clinical measure indicative of this established and clinically significant sign of RED-S on lumbar spine BMD? Would it be testosterone concentration, as suggested in the study of runners? Another blood marker? Cycle training load? Off bike exercise, as suggested in some previous studies? Clinical assessment by interview?
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.
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 Keay, Francis, Hind, BMJ Open in Sport and Exercise Medicine 2018
2018 UPDATE: Relative Energy Deficiency in Sport (RED-S) Keay, BJSM 2018
Fuelling for Cycling Performance Science4Performance
Pitfalls of Conducting and Interpreting Estimates of Energy Availability in Free-Living Athletes International Journal of Sport Nutrition and Exercise Metabolism 2018
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 Metabolism 2018
Treating exercise-associated low testosterone and its related symptoms The Physician and Sports Medicine 2018
Male Cyclists: bones, body composition, nutrition, performance Keay, BJSM 2018
Cyclists: Make No Bones About It Keay, BJSM 2018
Synergistic interactions of steroid hormones Keay BJSM 2018
Traditionally dance medicine has been somewhat the poor relation of sports medicine. Why is this the case? There is no doubt that dancers, of whatever genre, require the physical and psychological attributes of athletes. However, dance involves an additional artistic component where ultimately performance on stage is judged not according to a score card as in aesthetic sports, rather on the ability of the dancers to forge an emotional connection with the audience.
As with athletes, injuries are always an important topic for dancers: how to recognise the aetiology of injuries and thus develop prevention strategies. Dance UK have published two reports on national enquiries into the health of dancers. Dance UK has now evolved into the organisation One Dance which includes the National Institute of Dance Medicine and Science (NIDMS). One Dance provides delivery of the Healthier Dancer Programme (HDP) whose talks regularly engage 1500+ dancers and dance professionals per year and which will be a part of the One Dance UK conference at the end of November, an overarching event for the entire dance sector. One Dance holds a list of healthcare professionals with experience and expertise in dance. One Dance is an especially an important resource for independent dancers who will not have access to the provision for those working in larger dance companies.
However, beyond injury management, there are important aspects of the health of dancers which need to be considered, highlighted in an information booklet “Your body, Your risk” from Dance UK. The female athlete triad is well established as a clinical spectrum comprising of disordered eating, menstrual dysfunction and impaired bone health. Indeed impaired bone mineral density many persist even after retirement in female dancers. The recent evolution of the female athlete triad into relative energy deficiency in sports (RED-S) provides an important clinical model. RED-S includes male athletes/dancers, involves multiple body systems and crucially, evidence of detrimental effects on athletic performance is being researched and described. In other words RED-S is not restricted to female dancers/athletes with bone stress injuries.
The fundamental cause of RED-S is low energy availability where nutritional intake is insufficient to cover energy requirements for training and resting metabolic rate. In this situation the body goes into energy saving mode, which includes shut down of many hypothalamic-pituitary axes and hence endocrine network dysfunction. As hormones are crucial to backing up adaptations to exercise training, dysfunction will therefore have an effect not just on health, but on athletic performance. In dance, neuromuscular skills and proprioception are key for performance. Hence, of concern is that these skills are adversely impacted in functional hypothalamic amenorrhoea, which together with impaired bone health from RED-S, greatly increases injury risk.
Low energy availability can arise in dance and sport where low body weight confers an aesthetic and/or performance advantage. There is no doubt that being light body weight facilitates pointe work in female dancers and ease of elevation in male dancers. Thus, low energy availability can occur intentionally in an effort to achieve and maintain low body weight. Low energy availability can also be unintentional as a result of increased expenditure from training, rehearsal and performance demands and the practicality of fuelling. This situation is of particular concern for young dancers in training, as this represents a high energy demand state, not just for full time training, additionally in terms of energy demands for growth and development, including attainment of peak bone mass.
Despite the significance of RED-S in terms of negative consequences on health and performance, as outlined by the IOC in the recent consensus update, further work is required in terms of raising awareness, identification and prevention. Fortunately these issues are being addressed with the development of an online educational resource on RED-S for athletes/dancers, their coaches/teachers/parents and healthcare professionals which is backed by British Association of Sport and Exercise Medicine (BASEM) and with input from One Dance and NIDMS. In terms of research to facilitate the proliferation of evidence base in dance medicine, One Dance lists calls for research, whilst NHS NIDMS clinics provide access to clinical dance medicine. The importance of the application of this growing field of dance medicine and science for the health and performance of dancers was recently outlined in an article “Raising the barre: how science is saving ballet dancers“.
On the international stage, the International Association for Dance Medicine & Science (IADMS) strives to promote an international network of communication between dance and medicine. To this end, IADMS will hold its 28th Annual Conference in Helsinki, Finland from October 25-28, 2018. In addition to extensive discussion of dance injuries, there will be presentations on “Sleep and Performance” and “Dance Endocrinology”.
So maybe Dance Medicine and Science is not so much the poor relation of Sports Medicine, rather showing the way in terms of integrating input between dancers, teachers and healthcare professionals to optimise the health of dancers and so enable dancers to perform their full potential.
Fit to Dance? Report of National inquiry into dancers’ health.
Fit to Dance 2 Dance UK
Your body your risk. Dance UK
Fit but fragile. National Osteoporosis Society
Bone mineral density in professional female dancers N. Keay, BJSM
2018 UPDATE: Relative Energy Deficiency in Sport (RED-S) Dr N Keay BJSM 2018
Reduced Neuromuscular Performance in Amenorrheic Elite Endurance Athletes Medicine and Science in Sports & Exercise 2017
Dancing through Adolescence Dr N Keay BJSM
Healthy Hormones Dr N Keay BASEM 2018
Dancers, Periods and Osteoporosis, Keay N, Dancers, Periods and Osteoporosis, Dancing Times, September 1995, 1187-1189
A study of Dancers, Periods and Osteoporosis, Keay N, Dance Gazette, Issue 3, 1996, 47
Raising the barre: how science is saving ballet dancers The Guardian 2018
International Association for Dance Medicine and Science Medicine & Science in Sports and Exercise
What updates are presented in the IOC consensus statement on RED-S 2018?
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.
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 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.
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.
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.
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.
Within‐day energy deficiency and reproductive function in female endurance athletes Scandinavian Journal of Science and medicine in Sports 2017
The Effect of Postexercise Carbohydrate and Protein Ingestion on Bone Metabolism Translational Journal of the American College of Sports Medicine 2017
Reduced Neuromuscular Performance in Amenorrheic Elite Endurance Athletes Medicine & Science in Sports & Exercise. 49(12):2478–2485, DEC 2017
Cyclists: Make No Bones About It BJSM 2018
Low Energy Availability is Difficult to Assess But Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes Sports Nutrition and Exercise Metabolism 2017
Healthy Hormones BASEM 2018