The Harms of Undereating for Athletes: Low Energy Availability & RED-S

Background Context

Athletes tend to have increased energy requirements due to the nature and amount of their training and competition. However, for a variety of reasons, athletes commonly under-consume calories. Over time, more and more has been understood about the potentially harmful effects (acutely and chronically) on both performance and health.

Athlete’s are in a physiological state of “low energy availability” (LEA) when their energy intake is insufficient to support health, function, and daily living, once the energy expended during their training (and other exercise) sessions and competition is accounted for.

In this Sigma Statement, we discuss the evidence on the implications of low energy availability for athletes’ health, the diagnosis of relative energy deficiency in sport (RED-S), and identifying athletes at risk of, or experiencing, RED-S.

Low Energy Availability (LEA)

Energy availability (EA) can be thought of the amount of energy that is ‘available’ to sustain all physiological functions, after accounting for the energy expended through exercise.

EA can be represented via an equation (that has changed over time, as shown by Areta et al. (2021) in the table below). Most recently it has been defined as the difference between energy intake (EI) and exercise energy expenditure (EEE), expressed relative to an individual’s lean body mass (LBM).

EA = (EI – EEE)/LBM

EI = energy intake; EEE = exercise energy expenditure; LBM = lean body mass

Low energy availability (LEA) occurs when an individual has insufficient energy to support normal physiological function after the cost of energy expended during exercise has been removed.

LEA is commonly referenced as an EA below 30 kcal/kg LBM/day. However, there exists significant debate in academia about the existence of specific cut-off thresholds for LEA.

The sports medicine literature has documented that LEA has the potential to impair physiological function beyond menstrual function and bone health. And, importantly, that LEA can occur even when an athlete is in a state of energy balance. For example, an athlete deficient in energy may still maintain their normal body weight due to physiological training adaptations, such as decreased resting metabolic rate (RMR).

Therefore, these impairments in function have been refererred to as a syndome known as Relative Energy Deficiency in Sports (RED-S).

What is Relative Energy Deficiency in Sports?

Relative Energy Deficiency in Sports (RED-S), formerly known as the ‘Female Athlete Triad’ (TRIAD), is a syndrome caused by an energy deficiency relative to the balance between dietary energy intake and the energy expenditure required to support health, activities of daily living, growth, and sport. An IOC consensus group defines RED-S as the “impaired physiological function including, but not limited to, metabolic rate, menstrual function, bone health, immunity, protein synthesis, cardiovascular health caused by RED.”

RED-S is a complex syndrome with multifactorial health and performance consequences that may present in athletes/physically active for many reasons. As research focuses predominantly on elite athletes, we refer to ‘athletes’ as the affected population throughout this statement. However, RED-S can present in other physically active individuals that may not consider themselves to be ‘athletes,’ for example, dancers or amateur competitors.

Its etiology may result from unintentional behaviors (e.g., a lack of dietary understanding) or more conscious behaviors that mirror clinical eating disorders. In addition, a combination of other external factors may influence the development of RED-S, such as the type of sport and periodization of training. The prevalence rates are highest in those engaged in endurance, aesthetic, and weight-class sports.

RED-S Classification

The IOC’s original definition of the TRIAD was described as follows:

 “the combination of disordered eating and irregular menstrual cycles eventually leading to a decrease in endogenous estrogen and other hormones, resulting in low bone mineral density.”

The objective of the original guidance was to support the female athletes’ wider team (coaches and health professionals) for early identification, risk assessment, treatment, and return-to-play decisions.

In 2007, the American College of Sports Medicine (ACSM) updated the definition, specifically the clinical importance of optimal ‘energy availability’ (instead of the presence of an eating disorder that was in the original TRIAD classification).

As amenorrhea or irregular menses were significant consequences, the TRIAD concept was widely seen as a sex-specific disorder, impacting female athletes only. However, the understanding that energy deficiency’s health and performance consequences were not unique to female athletes continued to evolve. Therefore, the IOC updated their guideline to address these limitations. The IOC also commented that the terminology used to describe the TRIAD excluded those who did not see themselves as “athletes” but did engage in regularly physically active, such as professional performers (e.g., ballet dancers). Also, it no longer met the definition of a TRIAD but rather a syndrome resulting from relative energy deficiency that affects many functions beyond menstrual and bone health.

In 2018, the IOC consensus group reconvened to provide an update on scientific progress with the ultimate goal of generating awareness of the clinical application of RED-S and addressing gaps in current knowledge. The new guideline reflects the complexity of the syndrome. Due to limited research findings in diverse study populations, most evidence for RED-S still lacks an understanding of ethnic populations and para-athletes.

Health Consequences

The cause of RED-S is complex due to its multifactorial nature, but the core component is relative energy deficiency. Much of the evidence to date relates to the TRIAD, but irrespective of the terminology, both share the same causative factor: low energy availability (LEA). The health consequences of LEA may be subtle, developing slowly over time and with or without the expected symptoms.

During periods where weight loss is a priority (e.g., pre-race for cyclists), restoring energy availability (EA) following intense training may seem counterintuitive. Furthermore, the time demand of high volumes of endurance training can make it challenging for athletes to meet their energy requirements, resulting in unintentional LEA. This can make identification and diagnosis challenging. The potential health consequences of RED-S, as conceptualized by the IOC, are depicted in the image below.

The conceptual model highlights the limitations of the original TRIAD classification while acknowledging its continued relevance in the syndrome but with the extension to other bodily functions and systems. Importantly, it recognizes that psychological consequences may occur in two directions, as a consequence of RED and as a driving factor in the development of RED-S (such as a pre-existing or vulnerability to eating disorders or disordered eating).

In the following subsections, we briefly present the current evidence for RED-S and the most widely explored health system, the variability in a presentation based on individual characteristics, and the influence of sport and the periodization of training.

Menstrual Dysfunction

A regular menstrual cycle is an essential sign of reproductive health and hormonal imbalance. Functional hypothalamic amenorrhea (FHA) is a common form of secondary amenorrhea resulting in estrogen deficiency in young premenopausal women. The cause of this disorder is related to psychological stress, excessive exercise, disordered eating, or a combination of these factors resulting in suppression of the hypothalamic–pituitary–ovarian axis. An increasingly high incidence of secondary amenorrhea and other menstrual cycle disorders has been recorded among female athletes. In sports emphasizing aesthetics or leanness, such as ballet or running, the prevalence of secondary amenorrhea can be as high as 69%, compared with 2% to 5% in the general population.

A combination of factors can contribute to menstrual irregulatries, including:

• High intensity training
• specific type and amount of training
• reduced body weight
• lower body fat percentage
• psychological stress

In addition, recent evidence in elite Norwegian athletes demonstrated that age at menarche (the first occurrence of menstruation) occurred later in elite athletes than in non-athletes.

FHA occurs at a time when female athletes are in their peak reproductive years, which may result in infertility. For some athletes, this may be emotionally distressing; however, it has been widely observed that many female athletes see the absence of menses as positive. Many generally feel well and avoid the common symptoms of menses disturbing their training cycles. However, the long-term fertility repercussion (i.e., infertility or increased risk miscarriage) should be communicated to female athletes by the athletes’ health teams during health risk assessment. The involvement of all health team members is vital, as a variation in athletes’ comfort levels when discussing menstrual cycles with male coaches has been reported.

While menstrual function is unique to female athletes, reproductive repercussions may also impact male athletes. Evidence suggests the consequences are related to physical characteristics of the sport, such as mechanical trauma to the testis in elite male cyclists or the illicit use of prohibited drugs resulting in hypogonadism and infertility. More research is required to reach the level of evidence that currently exists for female athletes.

Bone Health

LEA can harm bone health, independent of whether estrogen levels are low. Evidence has shown that LEA can increase bone resorption markers and decrease bone formation markers. In addition, various investigations have demonstrated a dose-response relationship between EA and low BMD when EA falls below 30 kcal/kg FFM/day.

Athletes, elite or otherwise, presenting with long-term LEA are at greater risk of low BMD, altered bone metabolism, and increased risk for stress fracture injuries. In a recent study published by Lane et al., 2021, the investigators categorized competitive athletes (non-elite) as ‘high-risk’ for RED-S if their LEA was under 30 kcal/kg FFM. These high-risk athletes were more likely to have reduced total body BMD (r= -0.360, P=0.005), even when hormonal and bone biomarkers were in normal clinical ranges. This highlights the importance of comprehensive assessment in determining athletes’ risk profiles and presentation of RED-S.

Additionally, the criteria for LEA (< 30 kcal/kg FFM) was initially determined for female athletes, limiting its use in male studies, particularly given sex-dependent differences in body composition. LEA is also associated with an increased risk of stress fractures in elite and non-elite athletes, ultimately impacting sporting performance. The incidence of stress fractures increases with age, highlighting the delayed consequences and, thus, the importance of early identification and treatment of LEA. Again, given the focus on the TRIAD, most findings are in female athletes with menstrual dysfunction; however, most recent evidence indicates distinct sex differences for stress fracture risk. The pathophysiology and treatment strategies need more exploration in males and ethnically diverse athletes.

Endocrine System Dysfunction

Hormones play a significant role in athletes’ health and performance, as outlined by Dr. Nicky Keay. Beyond hormonal dysfunctions resulting from FHA in women, reduced testosterone in males, and adverse effects on bone health in both sexes, LEA alters multiple hormonal pathways, as illustrated in the image below. The hypothalamus, responsible for regulating the release of numerous hormones (e.g., cortisol, estrogen, and testosterone), can be detrimentally impacted by continuous LEA. The alterations result in a variety of physiological consequences, such as:

• thyroid hormone signalling pathways
• leptin levels, carbohydrate metabolism
• the growth hormone/insulin-like growth factor-1 axis

Traditionally, energy status is assessed over 24 hours. Within-day energy deficiency research may offer new learnings regarding real-time endocrine responses due to fluctuations across 24 hours of EA. One study of male endurance athletes explored the relationship between within-day energy balance and RMR:

• Study of 46 male cyclists, triathletes, and long-distance runners
• 65% had a suppressed RMR
• Despite similar EA and 24-hr energy balance, athletes with a supressed RMR spent more time in a severe energy deficit ( classified as a deficit greater than 400 kcal).
• The RMR-supressed athletes also had larger single-hour energy deficit, which were associated with higher cortisol levels and lower testosterone.

Metabolic Dysfunction

Suppressed RMR has been explored as a proxy for LEA. Chronic energy deficiency results in numerous metabolic adaptations that conserve energy for vital processes such as cellular maintenance, thermoregulation, and movement. As a result of these energy-conserving adaptations and a reduction of lean body mass, resting metabolic rate (RMR) is suppressed in chronically energy-deficient individuals.

It is more pronounced in females due to a lower metabolic rate (up to 10% lower) than men, even when they are of the same body weight and height. This lower RMR is due to differences in hormone status, skeletal muscle metabolism, and sympathetic nervous system activity. Additionally, variations by ethnicity have also been documented, where African American females are more likely to have a lower RMR than white females. As a lower RMR means less energy is required to maintain normal body weight, it can often conceal the presence of RED-S.

In both sedentary and athletic females, LEA has also been associated with significant changes in:

• metabolic hormones
• leptin, insulin
• ghrelin
• testosterone
• IGF-1

However, in male athletes reductions were only observed in leptin and insulin.

Psychological Dysfunction

While substantial evidence has been generated to support some attributes, especially those associated with the TRIAD, more evidence is required to advance knowledge of other proposed effects, including interactions with psychological health.

The potential adverse psychological effects of combining high levels of physical activity with inadequate nutrition and competition are wide-ranging and include (here and here):

• anxiety
• depression
• substance misuse
• compulsive and excessive training
• extreme performance orientations
• poor self-esteem
• disordered eating
• eating disorders

Endurance and aesthetic-dependent athletes (e.g., figure skating or gymnastics) are considered particularly vulnerable to developing RED-S as they face psycho-socio cultural pressures of a sporting body “ideal.” The evidence to date supports the bidirectional relationship in the RED-S health model; i.e., psychological factors can precede RED-S and be caused by RED-S. These athletes may experience prolonged LEA or energy deficits due to the duration of training or engaging in disordered eating behaviors to maintain a competition weight or body composition. While both will increase the risk of developing RED-S, the psychology of the recovery process is generally different, with the former resulting from unintentional under-fuelling and the latter more closely aligned with the socio-psychological practices of disordered eating.

The prevalence of disordered eating can range from 0-19% in male athletes. These prevalence rates are lower than female athletes (6-45%) but are still significant and shouldn’t be overlooked. Recent evidence describes how compulsive exercise behavior is associated with disordered eating characteristics, such as perfectionism and weight concerns in male cyclists. These pressures can promote restrictive eating habits, which can develop into disordered eating or more severe clinical eating disorders. Therefore, the evolution of the restrictive behavior will strongly guide the treatment strategies and the athlete’s road to recovery.

Other Health Consequences

Many other health consequences have been suggested, including impacts on cardiovascular dysfunction, specifically endothelial dysfunction and lipid metabolism. In addition, immune function is believed to be impaired in RED-S; however, there is a lack of evidence in determining if LEA independently contributes to these health consequences and their involvement in RED-S syndrome. Nutrient deficiencies leading to conditions such as anemia with chronic fatigue and immunological effects have been observed in athletes with LEA, predisposing them to an increased risk of infections. Other dietary factors such as diet quality and differing attitudes towards food groups would be an exciting area of further investigation when assessing for risk of LEA and RED-S. 

Performance Consequences

As illustrated below, the performance impacts are linked to the core component, RED-S. It has been widely reported that athletes are more motivated to engage with treatment strategies when there are detrimental impacts on performance, compared to negative health consequences.

LEA influences many body systems, for example, reproductive health and menstrual cycle disruption, as a means to protect energy. However, it is important to consider the other hormonal pathways that are altered. Numerous interrelated endocrine consequences have been observed, including increased cortisol levels and reduced triiodothyronine, luteinizing hormone pulsatility, and hypoestrogenism. In addition, LEA-associated menstrual dysfunction is associated with bone stress injury risk, which can impair training and competition participation. Reduced neuromuscular performance was observed in elite endurance athletes with menstrual dysfunction compared to those with normal menstrual cycles. While these findings cannot provide complete evidence for a causal link between these biomarkers and performance, it is biologically plausible.

One study by Van Heest et al. in 2014 demonstrated that adolescent female swimmers with ovarian suppression (determined to have LEA) showed poorer swimming performance (400-m swim velocity) than those with normal functioning ovaries. All athletes completed a time trial before and after a 12-week training cycle. The results showed that those with normal functioning ovaries and energy availability were 8.2% faster. Alarmingly, those in the ovarian-suppressed group were 10% slower than their original time following the training period.

Besides physical athleticism, being driven and determined are essential characteristics of success. If performance advantages can be obtained by other modifiable factors, such as body weight, this can become a competitive goal. Having said that, the long-term consequences of LEA produce adverse effects on body composition, such as increased fat: lean tissue ratio and reduction in BMD. The opposite effects of what an energy-restricted athlete is trying to achieve.

Ackerman et al. reported that LEA (assessed by self-report questionnaires in a large population of female athletes) was associated with aspects of declining performance, such as:

• decreased training response/endurance performance
• impaired judgment
• decreased coordination and concentration
• irritability
• depression

How can health and sports teams identify an athlete with RED-S?

We will examine this issue on three levels:

1. Clinical Assessment
2. Risk Assessments
3. RED-S Decision-based Return-to-play model

Clinical Assessment

Determining energy availability is not an appropriate clinical assessment for diagnosing RED-S. Quantifying energy availability has practical issues regarding reliability and accuracy due to recall biases and recording. However, specific biomarkers may offer an objective assessment, with several endocrine and metabolic hormones linked to performance consequences such as stress fractures in male and female athletes.

In the case of female athletes, it is generally believed that the absence of a menstrual cycle is the most apparent indicator; however, amenorrhea doesn’t present in all cases. In addition, female athletes taking hormonal contraceptives will still experience regular withdrawal bleeding, mimicking menses, and suppressing natural hormones. The lack of obvious or yet determined clinical consequences in males may go undiagnosed. There is no validated threshold of LEA resulting in amenorrhoea or low testosterone in males. Therefore the IOC recommends that individual clinical evaluation take the form of an overall health, lifestyle, and behaviors assessment.

Risk Assessments

The RED-S Clinical Assessment Tool (RED-S CAT) is based on the Sports Concussion Assessment Tool (SCAT5). The assessment aims to support the screening of athletes and determine return-to-play guidance. It is based on the traffic light system as a model for risk stratification.

• ‘Red Light’: This category flags athletes with an active energy deficiency, severe physical or psychological conditions related to their LEA, or engaging in dangerous weight loss practices. This category will identify athletes at extreme risk if they return to training or competitive practice.
• ‘Yellow Light’: This category lists the syndrome’s characteristics if the athlete has any health implications. It is recommended that the practitioner reflects on how they can overcome these factors (e.g., weight loss, bone health, prolonged LEA, stress fractures) to allow the athlete to address these issues and continue training.
• ‘Green Light’: This category represents healthy eating habits with sufficient EA, normal endocrine and metabolic function, and normal bone mineral density.

Athletes in the ‘Red Light’ category are denied participation in sports. The RED-S CAT supports coaches and practitioners to make decisions based on informed risk stratification, which gives them leverage when withdrawing the athlete from training until treatment interventions are accepted, adhered to, and demonstrable improvements are observed.

Most athletes affected by RED-S who move to the ‘Yellow Light’ category can resume training with a supervised medical treatment plan. Competition can resume once cleared under supervision and is re-evaluated every 1-3 months.

There are limitations to the RED-S CAT. For example, identifying an athlete/dancer with RED-S is more complicated. In sports where being lightweight results in performance or aesthetic advantage, the coaching team will have difficulty distinguishing between “naturally” lean athletes and those who have reached low body fat levels via disordered eating.

In addition, RED-S CAT relies heavily on athletes’ open and honest engagement. And some athletes may not want to share their experiences about sensitive topics openly, particularly if they are in stages of denial or not yet willing to consider behavioral changes.

RED-S Decision-based Return-to-Play Model

The RED-S Return-to-Play model is modified from the Creighton et al. model published in 2010 to provide a quantitative decision-based model for clinical use by sports medicine practitioners. The RED-S Return to Play Model outlines the sports activity recommended for each risk assessment category, as illustrated in the image below.

Interventions and Treatment

RED-S presents as a multi-system dysfunction caused by a disrupted periodization of nutrition, training, and recovery. Once medical conditions receive treatment as required, the athlete’s motivation to address these imbalances in nutrition and exercise will largely determine outcomes. This requires intensive and continued education, plus psychological support from multidisciplinary teams, including sports psychologists, dietitians, coaches, and medical staff. In addition, the type of sport will largely influence treatment. However, tailored treatment plans are limited to specific sports and still require validation.

The oral contraceptive pill will lead to withdrawal bleeds, which can “mask” amenorrhoea. Therefore, experts recommend athletes against using pharmacological interventions as first-line management. 

Gaps in Current Knowledge

The RED-S conceptual model and consensus statements have highlighted the limitation of the previous TRIAD model. However, there still needs to be more evidence in understanding newly determined consequences, their relationship to the previous TRIAD model, and avenues for clinical treatment as a syndrome. Future research should focus on developing the male athlete TRIAD, specifically determining long-term health effects. It has been argued that the current evidence base on RED-S does not support the current conceptual model. Future research on RED-S should establish its clinical relevance and clearly define the components of RED-S, their interconnections, and the causal effects of RED-S and the health and performance outcomes proposed. As mentioned throughout the statement, evidence in males is still limited compared to females. There is also an apparent need for more data on particular groups, such as para-athletes and athletes of various ethnicities. The majority of evidence is in elite, white athletes.

Summary & Conclusions

• Low energy availability (LEA) occurs when an individual has insufficient energy to support normal physiological function after the cost of energy expended during exercise has been removed.
  
• LEA can lead to impaired physiological function, beyond menstrual function and bone health. In addition, LEA may occur in an energy balanced state. Therefore, these impairments in function have been refererred to as a syndome known as Relative Energy Deficiency in Sports (RED-S).
  
• RED-S is a syndrome which results in “impaired physiological function including, but not limited to, metabolic rate, menstrual function, bone health, immunity, protein synthesis, cardiovascular health caused by RED”.
  
• RED-S is a complex syndrome with multifactorial health and performance consequence that may present in athletes/physically active for many reasons.
  
• The prevalence rates are highest in those engaged in endurance, aesthetic and weight-class sports.
  
• An increasingly high incidence of secondary amenorrhea and other menstrual cycle disorders have been recorded among female athletes.
  
• LEA can have a negative impact on bone health, independent of whether estrogen levels are low.
  
• Low LEA results in a variety of physiological consequences, such as thyroid hormone signalling pathways, leptin levels, carbohydrate metabolism, and the growth hormone/insulin-like growth factor-1 axis.
  
• Endurance and aesthetic-dependent athletes (e.g., figure skating or gymnastics) are considered particularly vulnerable to developing RED-S as they face psycho-socio cultural pressures of a sporting body “ideal”.
  
• In the long-term, a chronic state of LEA may produce adverse effects on body composition, such as increased fat:lean tissue ratio and reduction in BMD. Thus, the actual opposite effects of what an energy-restricted athlete is trying to achieve.
  
• The RED-S Return-to-Play model is a quantitative decision-based model for clinical use by sports medicine practitioners. The RED-S Return-to-Play Model outlines the sport activity recommended for different risk categories.

About this Statement

• Lead on Research & Writing: Niamh Aspell, PhD
• Editing & Additional Commentary: Danny Lennon
• Primary Reviewer: Alan Flanagan, PhD

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