Low Energy Availability: Identification, Management and Treatment

Jessica Piasecki

Highlights

• • When runners fail to consume enough calories in their diet to support their training, daily living tasks, and normal physical functioning, a state of low energy availability can arise,
• • The Female Athlete Triad describes a medical condition containing three inter-related conditions: low energy availability, menstrual cycle dysfunction and low bone mineral density.
• • The relative energy' deficiency in sport (RED-S) syndrome was developed to reflect the broad range of potentially serious health and performance consequences that can result from prolonged periods of low energy availability in both male and female athletes.
• • Several tools are available to identify athletes who may be at risk of developing the Triad and RED-S.
• • Governing bodies and coaches have a duty of care towards their athletes; therefore, an understanding of RED-S is of paramount importance.

Introduction

Energy is a necessity for all bodily functions. In the case of runners, energy' availability is the energy' that is left over for daily functioning of the body after the energy expended during exercise is taken away from the energy consumed in food. Low energy availability occurs when there is insufficient energy' left to fuel other life processes such as those needed to maintain health and daily activity. This may arise if the runner is unaware of the amount of energy expended throughout their training, or if they fail to match energy intake when increasing physical training. Alternatively, runners may purposefully restrict dietary' intakes, due to the perception that being ‘lighter’ is beneficial for their performance. If a state of low energy' availability persists over a prolonged period of time, a sy'ndrome known as ‘relative energy' deficiency in sport’ (RED-S) can arise, which results in impaired physiological function affecting a range of systems within the body', including metabolism, bone health, tissue repair, cardiovascular health, immunity and reproductive function (Mountjoy et al., 2014).

This chapter aims to describe how low energy availability develops and can be assessed in an applied setting. Sections also cover relevant and current research that may help readers gain a better understanding of the importance of the RED-S syndrome to allow informed decisions to be made with regards to themselves or the athletes they support.

Key Definitions of Energy Balance

Energy balance is defined by the First Law of Thermodynamics (Kondepudi, 2008), as the amount of dietary energy added to or lost from the body’s own energy stores following the completion all physiological processes within a day (Loucks et al., 2011; Loucks, 2004). Energy' balance can be calculated as energy' intake minus total energy expenditure. The concept of energy balance can be difficult to manage within an athlete’s diet and training programme due to the issues with collecting accurate information on energy' intake and expenditure (Loucks, 2004; Loucks et al., 2011). Energy deficiency is a negative discrepancy in energy balance whereby energy intake is less than total energy expenditure. This deficit creates a loss in stored energy' and causes compensatory mechanisms to maintain homeostasis in vital physiological systems but reduce the functioning of others, e.g. reproductive function causing menstrual cycle irregularity' (Otis et al., 1997). Adjustments are also common within endocrine, metabolic and functional systems, although more research is needed to assess other systemic changes following a prolonged energy' deficit (Mountjoy' et al., 2014).

Energy' availability is the remaining energy' for the body’s metabolic systems following the deduction of energy costs required to carry out normal physiological systems. For a runner, this is the remaining energy' available for maintaining normal bodily function following the energy' cost of exercise. Energy availability is equal to energy' intake minus energy' expended from exercise (Wade and Jones, 2004). Low energy' availability occurs when an individual’s energy' intake is inadequate for maintaining the energy costs required for normal physiological functions as well as for sporting performance (Mountjoy et al., 2014). Healthy energy' availability has been categorised in adult populations as a value of ~45 kcal.kg fat free mass (FFM)''.day^H, and low energy availability has been categorised as below ~ 30 kcal.kg FFM '. day^-1 (Nattiv et al., 1994).

Assessing Energy Expenditure

Assessing the components of an athlete’s energy' balance is difficult due to the complexity of its two components (Loucks et al., 2011). Total energy' expenditure is comprised of various factors including physical activity, basal metabolic rate (BMR) and the thermic effect of food. Collectively, these three components encompass all energy outputs of one individual system, illustrating the difficulties in obtaining an of accurate value (Hills et al., 2014; Schoeller et al., 1995). To add to the complications, BMR can be altered by a range of environmental factors such as food consumption, drug intake, genetics and physical activity'. Given this complexity, it can be very hard to accurately research and monitor precise energy intake within athlete populations.

Self-report diaries are often utilised in research and applied settings to monitor and measure energy' intake. This method tends to involve questionnaires and food diaries that are kept by athletes, allowing large populations to be monitored effectively (Stone et al., 1999). However, this method can also be unreliable, due to athletes not accurately defining their food and/or amounts, as well as being time-consuming for the athlete to complete. Additionally', self-reporting energy intake can exude some level of bias as athletes may be attempting to ‘eat better’ for the time period they are under observation to avoid judgement. There are similar issues with the measurement of total energy expenditure; therefore, without constant observations and direct calorimetry (to measure resting metabolic rate), the validity of data is questionable. Self-report is frequently used in scientific research as it requires fewer financial resources than other, more valid, methods (Stone et al., 1999).

Self-reporting food intake can be considered the best field method for collecting a large amount of data for analysis and is the most easily integrated within runners. Dual methods using equipment in conjunction with self-reporting can be considered more appropriate in defining total energy' expenditure. Most athletes now employ the use of global positioning systems (GPS) and heart rate devices, which makes the monitoring of training more accurate than previously (Melin et al., 2014) and improves the validity of screening for athletes at risk of RED-S. The Low Energy' Availability in Females Questionnaire (LEAF-Q) is also a validated tool that can identify female athletes at risk of RED-S.

The Female Athlete Triad

The Female Athlete Triad (Triad) was first coined in 1992 by the American College of Sports Medicine encompassing the interrelated phenomena of disordered eating, amenorrhea and osteoporosis (Otis et al., 1997). This triad identifies how low energy availability' can have an impact on the menstrual cycle of females (tending to become absent or irregular). Menstrual cycle dysfunction is caused by low levels of oestrogen, which is a key regulator of bone formation. Consequently, low oestrogen results in a decline in bone health, and in most severe cases osteoporosis (the third dimension of the Triad). The Female Athlete Coalition (De Souza et al., 2014b) subsequently published a consensus statement on the Triad, in response to the high volume of emerging research on poor bone health in female athletes, particularly in endurance events and sports requiring a lean body physique. The consensus statement offers expert guidance on identifying and treating this condition and provides help for coaches and practitioners with return-to-play decisions. Several revisions of the Triad have developed the concept into a three-dimensional triangular model (Figure 18.1) displaying each of the three components on a continuum, with optimal energy' availability, regular menstruation and optimal bone health lying on one side of the spectrum, and low energy' availability', amenorrhoea and osteoporosis ly'ing at the opposite end (De Souza et al., 2014b; Nattiv et al., 1994).

Critics of the Triad highlight that this excludes male athletes and does not identify reasons for an energy' deficit (Manore et al., 2007). It is important to recognise that eating disorders cannot be defined as the aetiology oflow energy availability. This was demonstrated in a study on 40 female athletes, which showed that while 63% of the sample were identified as having low energy availability', only 25% were categorised as positive for having an eating disorder (Melin et al., 2014). Eating disorders or disordered eating is therefore not the only reason that low energy' availability may arise.

Development of Relative Energy Deficiency in Sport

RED-S is a new term, originally put forward by the International Olympic Committee (IOC), to encompass the numerous physiological implications that may arise as a result of prolonged low energy availability (Figure 18.2. Mountjoy et al., 2014). The intention of using

FIGURE 18.1 Tlie Female Athlete Triad showing the spectrums of energy availability, menstrual function and bone mineral density (BMD). An athlete’s condition may move along each spectrum at a different rate, in either direction, depending on their diet and training habits. Energy' availability may affect bone mineral density both directly via metabolic hormones and indirectly via menstrual dysfunctions, leading to changes in oestrogen

Sourer. Taken from Nattiv et al. (2007).

RED-S was to extend beyond the Triad to include a greater number of physiological and health-related implications that are associated with low energy availability. Ultimately, as with the Triad, low energy availability may be either intentional or unintentional, and if sustained over a long period of time, an athlete’s health and performance will be negatively affected.

If a runner is exposed to long periods of low energy' availability in which they, intentionally or unintentionally, do not meet the energy' demands of their training and day-to-day life, then they are at a heightened risk of developing RED-S. Specifically, RED-S increases the likelihood of illness and infection, alters circulating hormonal levels, increases susceptibility for injury and lengthens the time taken to grow and repair damaged muscles (Ackerman et al., 2018; Barrack et al., 2013; Shimizu et al., 2012; Petkus et al., 2017; Loucks et al., 1992; Elliott-Sale et al., 2018). If the athlete has one, many or all of these alterations due to low energy' availability, then their performance will also be affected as a consequence of decreased glycogen stores, endurance performance, concentration, coordination, adaptability and impaired judgement (Melin et al., 2019).

The term RED-S not only broadens the potential impact of low energy availability compared to the Triad, but it also allows the sy'ndrome to be applied to male athletes who may also experience a number of the same physiological consequences. It has been suggested that males experience similar monthly fluctuations in hormones to that of females, but this is widely

FIGURE 18.2 The left image denotes the health consequences of relative energy deficiency in sport (RED-S), and the right image shows the performance consequences of RED-S. * Psychological consequences can either precede RED-S or be the results of RED-S

Somrr. Taken from Mountjoy et al. (2014).

under-researched due to inadequacy and consistency of methods (Tenforde et al., 2016). A recent update on the RED-S paradigm suggested that future research should be directed towards the inclusion of male athletes (Mountjoy et al., 2018a) as well as increasing awareness and education to athletes, coaches, parents and other practitioners.

Research on RED-S

Most research that is available on RED-S has been drawn from studies with small sample sizes and a limited number of variables. In 2016 only a handful of publications were available on RED-S; however, in recent years there have been a plethora of publications, with over 20 original research studies published in 2019 and 2020 investigating the implications of low energy availability. Using validated questionnaires (Brief Eating Disorder in Athletes Questionnaire, Eating Disorder Screen for Primary Care and self-reported history of eating disorders or disordered eating), Ackerman et al. (2018) assessed energy availability, and the health and performance consequences of RED-S in a group of around 1000 female athletes. Data revealed that approximately half of the athletes surveyed had experienced low energy' availability, which was clearly associated with health and performance consequences. These data reaffirm the high prevalence of female athletes that experience both these health and performance consequences as a result of low energy' availability.

One of the main reasons for the development of the RED-S framework is to ensure that research in males at risk or with low energy availability is increased. The inclusion of males in RED-S related research is currently limited, and only since the definition of RED-S have males begun to be included, or deemed at risk for low energy' availability, alongside females. Studies have demonstrated a high prevalence of males at risk of RED-S within endurance sports. Of 108 non-elite competitive endurance athletes ~80% were deemed to be at risk for low energy' availability; in particular, cyclists had a very low energy intake at around 29 kcal/ kg FFM/day compared to runners at 34 kcal/kg FFM/day (Lane et al., 2019).

A six-point assessment has been validated to determine the risk of developing the Triad and suffering a bone stress-related injury (see Table 18.1). The factors identified in the model for being at risk of developing the Triad are: a low energy' availability (with or without disordered eating/eating disorder), low body mass index (BMI), delayed age of menarche (onset of periods), oligomenorrhea (longer menstrual cycles) and/or amenorrhea, and low bone mineral density and/or stress reaction/fracture (De Souza et al., 2020; Joy et al., 2014). An adapted version of the risk assessment system has been developed for male athletes, including low energy' availability, low BMI, low bone mineral density and prior bone stress injuries (Kraus et al., 2019). These factors are strongly predictive with the prospective injuries sustained by male athletes, suggesting that males are at a similar risk as females for bone stress injuries in low energy' availability environments (Kraus et al., 2019; Tenforde et al., 2016).

In male athletes, compared to females, there is no obvious indication that may suggest an athlete is at risk of RED-S that may warrant further investigation. In contrast, in female athletes who are non-hormonal contraceptive users, regularity of the menstrual cycle can be used as a barometer to indicate when RED-S may be developing. Specific menstrual cycle dysfunctions such as anovulatory cycle (seemingly normal menstrual pattern but absence of ovulation) or luteal phase defect (low progesterone levels and/or a short luteal phase) require more detailed testing. However, female runners are strongly encouraged to track their own cycle, behaviours, and symptoms to enable them to recognise and respond to changes quickly'.

TABLE 18.1 Female Athlete Triad cumulative risk assessment

Source: Kraus et al. (2019); De Souza ct al. (2020, 2014a)

Note: This assessment provides an objective method of determining an athlete’s risk using risk stratification and evidence-based risk factors for the Female Athlete Triad. BMD, bone mineral density; BMI, body mass index; DE, disordered eating; DSM-V, Diagnostic and Statistical Manual of Mental Disorders, 5th edition; EA, energy availability; E1), eating disorder; EW, expected weight.

$ Some dietary restriction as evidenced by self-report or low/inadequate energy intake on diet logs.

• * History/current history.
• ** >90% EW; absolute BMI cut-offs should not be used for adolescents.
• *** Weight-bearing sport. fHigh-risk skeletal sites associated with low BMD and delay in return to play in athletes with one or more components of the Triad include stress reaction/fracture of trabecular sites (femoral neck, sacrum, pelvis).

For males a similar score as detailed previously is now available without the necessity to include the delayed menarche and oligomenorrhea/amenorrhea risk.

Changes to the male reproductive system as a result of low energy availability require more intricate assessment, some of which may necessitate sperm and fertility analysis. However, a few studies have been performed to evidence changes in metabolism and reproduction in males with low energy availability (McColl et al., 1989; Hackney et al., 1988) but more studies are required to evaluate dietary and endocrine function over a longer time period.

In studies that have included male athletes, it can be concluded that testosterone is affected by low energy availability; in a similar manner to the alterations of the hypothalamic-pituitary- axis that influences oestrogen levels in females. Testosterone is an important anabolic hormone that regulates sex drive, contributes to production of red blood cells and is responsible for re-building damaged tissues (e.g. bone and muscle) following exercise bouts. A small number of studies have demonstrated 10-30% lower levels of testosterone amongst male endurance runners training at a high volume (over 100 km per week). Moreover, even male athletes on a lower volume of endurance training have still demonstrated lower levels of testosterone in comparison to sedentary or less active males (Tenforde et al., 2016). Some studies have shown that as mileage of endurance runners increases, testosterone levels decrease at a similar rate (Wheeler et al., 1986); however, these studies do reiterate that the lower levels of testosterone that tend to be observed are still considered to be within a ‘normal’ range. However, the longterm implications of low testosterone in male athletes is currently unknown.

REDS 'at Risk' Assessment Tool

A proposed clinical assessment tool is available for medical practitioners that enables athletes to be screened for RED-S and categorised at different levels of risk (Mountjoy et al., 2015a; Mountjoy et al., 2015b). The tool provides a traffic light system, which uses specific behaviours and symptoms associated with RED-S to categorise athletes (see Table 18.2). The assessment tool also details specific guidance for return to training and performance. Diagnosing RED-S can be difficult due to the subtle and sometimes unrecognisable symptoms. Therefore, it is necessary to focus on those athletes most at risk for developing RED-S, which includes athletes in endurance sports such as distance running. If early detection is possible, then improvements in performances are still achievable, as is the prevention of long-term health consequences. It is recommended that screening is undertaken as part of a periodic health exam/routine check-up when an athlete presents with one of some of the following symptoms; disordered eating/ eating disorders, weight loss, lack of normal growth and development, endocrine dysfunction, recurrent injuries and illnesses, decreased performance/performance variability or mood changes. Any athletes who are in the red and yellow risk categories should receive medical treatment, preferably undertaken by a team of health professionals, which would include a sports medical doctor, a sports dietician, an exercise physiologist, coaches and sports psychologists, as and when appropriate. Treatment should focus on correcting the energy deficit through increasing energy' intake and/or decreasing the energy' expended. Prior to the athlete returning to sport a full assessment of the athletes heath and nutritional requirements are necessary (detailed in the steps that follow).

Step 1: Evaluations of health status; this should be conducted by a medical practitioner taking into account the demographics, medical symptoms history and seriousness of their current status.

Step 2: Evaluation of participation risk; taking into account the type of sport played and completion level.

Step 3: Decision modification; return to training may be adjusted according to time of the season, pressure from the athlete and external pressures and any fears of litigation.

Preventing RED-S

The cornerstone of RED-S prevention is education, with runners themselves, plus parents, coaches, teachers and practitioners that provide support to athletes. It is currently concerning that less than half of practitioners working with athletes and runners can accurately identify the Triad components (see: Mountjoy et al., 2018a). More worryingly, many female runners have been informed by their coaches or medical professionals that an absence of menstrual

TABLE 18.2 Risk assessment model for RED-S

Source: Taken from Mountjoy cl at. (2015a).

Note: EA, energy availability; BMD, bone mineral density

High risk - Red Light; this is a very serious situation for the athlete and any sport participation would pose serious risk to the athletes health (male or female).

Moderate risk - Yellow Light; supervised sports participation is suitable with an adequate treatment plan in place. Evaluation of the athlete’s progression and risk should be carried out at regular intervals to detect changes in clinical status.

Low risk - Green Light; full sport participation is appropriate.

cycles is ‘normal’ for exercising females, despite clear scientific evidence that menstrual dysfunction is a risk factor for bone stress injury.

The following recommendations are largely for coaches, but should be used by runners

themselves and sports medicine professionals working with athletes:

• • Coaches and practitioners are responsible for enhancing their knowledge of this concept.
• • Coaches should aim to build strong relationships with their athletes and families to enable open conversations and discussions around the issue of eating disorders and RED-S.
• • Coaches should reduce emphasis on body weight being an important determinant of performance in distance running. Instead, focus should be placed upon nutrition and health as the most important means of enhancing performance.
• • Coaches should never be critical of an athlete’s body shape or weight.
• • Coaches should be aware (and educate their athletes) that exceptional performances by an athlete does not necessarily mean the athlete is healthy.
• • If weight loss is part of a distance runner’s objectives, goals should be long-term, realistic and health-promoting.
• • Coaches can relay the importance of a healthy balanced diet and emphasise that any increases in training volume should be met with increases in energy intake.
• • When presented with an athlete whose performance has deteriorated despite a period of uninterrupted training, coaches should consider that it may be related to low energy availability⁷. If coaches suspect that this is the case, they should consult with a qualified nutritionist or dietician to investigate further.

• • For younger runners who may be competing in other school and extracurricular sports, monitoring the volume of physical exercise and adjusting for the needs of the individual athlete is crucial.
• • Wherever possible, athletes should undergo an annual health examination to screen for eating disorders, weight loss, growth (in the case of young athletes), menstrual dysfunction, injury history, illnesses and performance changes. Governing bodies should include adequate education within coaching qualifications and ensure that athletes at elite through to beginner level have the relevant knowledge of RED-S to support their training needs,

Summary and Reflections

Energy deficiency occurs when the balance between energy intake from the diet is exceeded by the energy' required for physical training, daily living activities and normal physiological functions. Chronic periods of low energy' availability are common in distance runners, either because they unintentionally do not consume enough calories to support the energy they expend in training, or intentionally as they believe that weight loss will provide them with a performance advantage. The Female Athlete Triad provides a medical framework that describes three inter-related conditions (low energy availability with or without disordered eating or an eating disorder, menstrual dysfunction and low bone mineral density') that each exist on a continuum from normal/optimal to serious endpoints. More recently, the term RED-S was developed by the IOC to describe a syndrome caused by low energy' availability that negatively impacts a broader range of physiological systems in both males and females. These physiological consequences can manifest in poor health, injury and deteriorations in running performance. Despite there being a lack of research around RED-S, the concept has most certainly raised awareness in the running and coaching community of the health and performance consequences of low energy' availability'. Several assessment tools are available for those at risk of the Triad and RED-S, including the Female Athlete Triad cumulative risk assessment, LEAF- Q, and risk assessment model for RED-S. Coaches should endeavour to educate themselves and their runners about RED-S, be vigilant for signs of disordered eating, and downplay the importance of weight loss as a performance enhancement strategy. Further research is required to better understand the mechanisms of RED-S and its prevalence amongst sub-populations of athletes, including male runners, para-athletes and different ethnicities.

As many well-established names in the endurance running world have now begun to share their own experiences of RED-S, there seems to be an increasing awareness of the serious health-related issues than can arise as a result of chronic low energy' availability. Raising awareness in this manner gives the younger generation of athletes a relatable ‘role model’ and a better sense of these issues, re-iterating the importance of adequate energy intake. For older athletes, this information and insight was not readily available when they were at their peak, even at the elite level. For the current generation there is now an opportunity to reduce the number of negative consequences that young athletes have suffered in the past. It should be noted that RED-S does not exclusively occur in elite populations, those at the ‘sub-elite level’, compete and train to a high level but often without additional support. As such, these groups should also be made aware of the consequences of RED-S and how to avoid the syndrome. Governing bodies and those involved with the design of coach education curricula across all sports have a duty of care to protect their current and prospective athletes of the future. The more athletes that can make it through their careers with adequate energy' intake, the higher calibre of athlete populations we are likely to have in years to come.

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