Energy Availability: Concept, Control and Consequences in relative energy deficiency in sport (RED-S)

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].

Slide1

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].

Slide1

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 and Royal National Orthopaedic Hospital, London

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

How to Identify Male Cyclists at Risk of RED-S?

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.

Sam

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.

References 

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

IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update BJSM 2018

The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad BJSM 2013

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

Male Athletes: the Bare Bones of Cyclists

Cyclists: How to Support Bone Health?

Synergistic interactions of steroid hormones Keay BJSM 2018

Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis Sports Medicine 2018

 

Relative Energy Deficiency in Sport (RED-S) 2018 update

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.

REDs
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.

References

IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update BJSM 2018

Male Cyclists: bones, body composition, nutrition, performance BJSM 2018

Male Athletes: the Bare Bones of Cyclists

Addiction to Exercise – what distinguishes a healthy level of commitment from exercise addiction? BJSM 2017

Sports Endocrinology – what does it have to do with performance? BJSM 2017

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

Cumulative Endocrine Dysfunction in Relative Energy Deficiency in Sport (RED-S) BJSM 2018

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

Part 2: Health, Hormones and Human Performance take centre stage BJSM 2018

Cyclists: How to Support Bone Health?

Healthy Hormones BASEM 2018