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Review
Primary, secondary and tertiary prevention of Relative Energy Deficiency in Sport (REDs): a narrative review by a subgroup of the IOC consensus on REDs
  1. Monica Klungland Torstveit1,
  2. Kathryn E Ackerman2,
  3. Naama Constantini3,
  4. Bryan Holtzman2,
  5. Karsten Koehler4,
  6. Margo L Mountjoy5,
  7. Jorunn Sundgot-Borgen6,
  8. Anna Melin7
  1. 1Department of Sport Science and Physical Education, University of Agder, Kristiansand, Norway
  2. 2Wu Tsai Female Athlete Program, Division of Sports Medicine, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts, USA
  3. 3Sport Medicine, Shaare Zedek Medical Center, The Hebrew University, Jerusalem, Israel
  4. 4Department of Sport and Health Sciences, Technical University of Munich, München, Germany
  5. 5Department of Family Medicine, McMaster University, Hamilton, Ontario, Canada
  6. 6Department of Sports Medicine, Norwegian School of Sport Sciences, Oslo, Norway
  7. 7Department of Sport Science, Linnaeus University, Vaxjo/Kalmar, Sweden
  1. Correspondence to Professor Monica Klungland Torstveit, Department of Sport Science and Physical Education, University of Agder, Kristiansand, Norway; monicakt{at}uia.no

Abstract

Relative Energy Deficiency in Sport (REDs) is common among female and male athletes representing various sports at different performance levels, and the underlying cause is problematic low energy availability (LEA). It is essential to prevent problematic LEA to decrease the risk of serious health and performance consequences. This narrative review addresses REDs primary, secondary and tertiary prevention strategies and recommends best practice prevention guidelines targeting the athlete health and performance team, athlete entourage (eg, coaches, parents, managers) and sport organisations. Primary prevention of REDs seeks to minimise exposure to and reduce behaviours associated with problematic LEA. Some of the important strategies are educational initiatives and de-emphasising body weight and leanness, particularly in young and subelite athletes. Secondary prevention encourages the early identification and management of REDs signs or symptoms to facilitate early treatment to prevent development of more serious REDs outcomes. Recommended strategies for identifying athletes at risk are self-reported screening instruments, individual health interviews and/or objective assessment of REDs markers. Tertiary prevention (clinical treatment) seeks to limit short-term and long-term severe health consequences of REDs. The cornerstone of tertiary prevention is identifying the source of and treating problematic LEA. Best practice guidelines to prevent REDs and related consequences include a multipronged approach targeting the athlete health and performance team, the athlete entourage and sport organisations, who all need to ensure a supportive and safe sporting environment, have sufficient REDs knowledge and remain observant for the early signs and symptoms of REDs.

  • energy
  • deficiency
  • sport
  • athletes
  • preventive medicine
http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bjsports-2023-106932

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    Introduction

    Relative Energy Deficiency in Sport (REDs) is a syndrome caused by exposure to problematic (prolonged and/or severe) low energy availability (LEA).1 Problematic LEA and REDs are common among both female and male athletes at different ages and performance levels and may result in serious health and performance consequences.1 Hence, there is a need for prevention strategies to mitigate REDs.

    Prevention of a health condition may be described in terms of primary, secondary and tertiary prevention where primary prevention aims to prevent a disease from ever occurring, secondary prevention emphasises early disease detection and tertiary prevention targets both the clinical and outcome stages of a disease, also commonly used synonymously with treatment.2 Transferring these definitions to the syndrome of REDs and considering that problematic LEA is the underlying etiological factor, primary prevention should prioritise modifying risk factors for problematic LEA exposure, secondary prevention should encourage early identification and management of REDs signs and symptoms and tertiary prevention should seek to limit the longer-term health and performance consequences of the syndrome (figure 1). To date, there are no publications detailing a broad and thorough understanding of the prevention of REDs.

    Figure 1
    Figure 1

    A primary, secondary and tertiary prevention model of Relative Energy Deficiency in Sport (REDs). Pictures from pixabay.com.

    The main aim of this narrative review is therefore to address REDs primary, secondary and tertiary prevention strategies. A secondary aim is to recommend best practice guidelines targeting the athlete health and performance team, the athlete entourage and sport organisations.

    Methods

    We conducted a narrative review aimed to provide a general overview of the existing literature on the prevention strategies related to REDs, rather than to answer a focused research question or to conduct an exhaustive literature review, as appropriate for a systematic or scoping review. The coauthor subgroups working with primary, secondary and tertiary prevention were tasked to explore relevant databases for inclusion of scientific literature related to their specific prevention area.

    Equity, diversity and inclusion statement

    The author group included six women and two men representing a variety of disciplines to cover the holistic perspective of this review paper (eg, sports medicine, endocrinology, paediatrics, internal medicine, psychology, nutrition, exercise physiology). The authors represented the following nationalities: American, Canadian, German, Israeli, Norwegian and Swedish. Our review paper examined the topic of REDs prevention in a broad perspective in terms of gender, race, age, demographics, sport disciplines and socioeconomic status.

    Primary prevention

    Background

    Primary prevention aims to prevent a disease prior to its occurrence by minimising exposure to hazards and increasing resistance in case of exposure (figure 1).2 Target groups for primary prevention of REDs should include the athlete health and performance team (eg, physicians, physiotherapists, dietitians, psychologists and physiologists), athlete entourage (eg, coaches, parents and managers) and sport organisations. Specific at-risk groups, including athletes in weight-sensitive and leanness-demanding sports, and female and adolescent athletes, warrant particular focus.3 As problematic LEA is the underlying cause of REDs, the objectives of primary prevention are to minimise exposure to and reduce behaviours associated with LEA (table 1).

    View this table:
    Table 1

    Risk factors and approaches for primary prevention of Relative Energy Deficiency in Sport (REDs) in healthy athletes

    1. Exposure to LEA. LEA can result from intentional dietary restriction to reduce body weight or achieve leanness.4 5 LEA can also occur inadvertently from poor nutritional knowledge, lack of time, food insecurity, low energy density diets or exercise-related changes in appetite.4 6 7 Given that LEA is a mismatch between dietary energy intake and exercise energy expenditure, increases in training volume or intensity may also contribute to LEA.

    2. Behaviours associated with LEA. Restrictive eating is often associated with concerns around body weight and shape, which occur frequently in weight-sensitive and leanness-demanding sports.8 Weight and shape concerns can be exacerbated from within and outside the athletic community. Although assessment and management of body weight and composition are often considered important for optimising athletic performance,9 focus from coaches on athletes’ body composition and weight often causes concerns,10 11 especially for young athletes who are at increased risk of developing negative physical and mental health outcomes.1 5 Peers (teammates, competitors) can also be sources for unhealthy dieting behaviours,10 since influential athletes may intentionally or unintentionally put pressure on others.5 Social media exposes athletes to potential behaviours in a variety of ways, including issues related to body image, body shaming and bullying.12 13 Independent of the source, negative comments and weight pressure can reinforce body dissatisfaction and restrictive eating behaviour.8 11 12 Recent literature suggests that exercise addiction may present an additional risk factor for REDs.14 15

    3. Non-modifiable risk factors for LEA. Although any athlete can develop REDs, the risk is highest in weight-sensitive and leanness-demanding sports, including but not limited to weight class sports (eg, combat disciplines), aesthetically judged sports (eg, gymnastics), sports in which a low body weight might provide a performance advantage (eg, antigravity disciplines, such as high jump) and in sports with high exercise energy expenditure (eg, endurance disciplines).9 Due to the prominence of menstrual disturbances as a symptom of exposure to problematic LEA and the greater prevalence of risk behaviours associated with REDs (eg, disordered eating (DE) behaviour), female athletes have historically been, and still are, considered at high risk of problematic LEA and associated symptoms.1 16 While other non-modifiable risks such as genetic factors may exist, there is currently insufficient scientific evidence to support genetic factors contributing to REDs.17

    Primary prevention strategies

    The central roles of unhealthy dietary and/or exercise behaviours in the development of problematic LEA and REDs necessitate that primary prevention strategies focus on education about the importance of adequate energy availability to ensure optimal health and performance.1 3 18 Educational initiatives targeting all individuals in the athlete’s ecosystem (the athlete health and performance team and members of the entourage) should include strengthening of protective factors and reducing risk factors (table 1).1 3 9 19

    Studies on the prevention of eating disorders (EDs) among adolescent and collegiate athletes suggest that interactive workshops involving discussions or cognitive dissonance tasks can promote a positive body image, encourage self-care and reduce ED risk factors.19–21 Similar findings have been reported in female dancers22 and in female and male collegiate athletes.20 23 24 Considering these promising findings in light of the established links among body dissatisfaction, DE behaviour/EDs and LEA,25 a similar approach may be effective in preventing problematic LEA and REDs.

    Prevention strategies should be appropriate for age, gender, competition level and sport discipline and account for sociocultural aspects of the target audience.26 A critical period for primary prevention is the transitional time of puberty. Communication with this age group should focus on themes related to variations in body shape, natural biological and psychological changes, maturation and how these factors relate to athletic performance, positive behaviours, peer pressure resistance and building an environment that supports a positive body image.19 To minimise the risk of developing REDs, athletes and their health and performance team should aim to de-emphasise body weight and leanness, particularly in young and subelite athletes.9 Except for medical purposes (eg, growth progression), assessment of body weight and composition is not recommended for underage athletes.1 8 27 When weight loss or reduction in body fat is recommended for elite athletes, careful planning and realistic body weight/composition goals are essential, and necessary energy deficits should be kept in moderation to avoid problematic LEA (table 1). Ideally, the elite athletes and their health and performance team initiate an evidence-based management and rationale for weight or body fat reductions (table 1).1 5 Sport organisations should be aware of the implications of rules related to body weight (eg, weight-category sports) and sport uniforms (eg, female beach volleyball) and course designs that include more climbing and thereby favour lighter athletes (eg, cross country skiing, road cycling) that might create a culture of dieting and unhealthy eating practices (table 1).

    There is little evidence of REDs primary prevention programmes’ efficacy in healthy athletes. Although education interventions may improve knowledge,1 28 29 it remains unclear if they result in behaviour changes that reduce the risk of developing REDs.18

    Secondary prevention

    Secondary prevention encourages the early identification and management of REDs signs or symptoms to facilitate early treatment, thus preventing the development of more serious REDs outcomes (eg, osteoporosis, EDs) (figure 1). Self-reported screening instruments, individual health interviews and objective assessment of REDs markers may be useful strategies for secondary prevention.

    Subjective assessment of symptoms

    Screening of self-reported symptoms either by questionnaires or individual health interviews are convenient and simple methods for the early identification of REDs. Relevant physical symptoms include menstrual dysfunction in females,30–32 reduced erectile function in males,33 recurrent illnesses34 and injuries.31 35 Psychological symptoms may include mood changes, reduced well-being and depression.1 36 Symptoms can also be related to an athlete’s behaviour, such as excessive exercise, frequent non-performance-related measurements of body weight or composition, or DE behaviour/EDs.1 To date, no validated screening instrument includes all of these aspects. Hence, a combination of instruments should be used to increase the possibility of optimal secondary prevention of REDs.

    Validated or tested questionnaires used in athletic populations to assess LEA, REDs and DE behaviour are summarised in table 2. For a more complete list of questionnaires frequently used in athletic populations, also including non-validated/tested questionnaires,37–43 see online supplemental table 1.

    View this table:
    Table 2

    Questionnaires validated/tested in athletic populations to assess low energy availability (LEA), Relative Energy Deficiency in Sport (REDs) and disordered eating (DE) behaviour

    The Low Energy Availability in Females Questionnaire was originally validated against clinical signs of LEA (eg, functional hypothalamic amenorrhoea (FHA) assessed by gynaecological examination, low bone mineral density (BMD) assessed by dual energy X-ray absorptiometry (DXA) and blood biomarkers) in female endurance athletes31 and is also commonly used for assessing physiological symptoms of LEA in other female athletic groups.44 To date, only one questionnaire has been developed and tested for use in male athletes (the Low Energy Availability in Males Questionnaire (LEAM-Q)).45 Validation of the LEAM-Q was based on clinical verification of signs of LEA (eg, blood biomarkers and low BMD) in elite and subelite male athletes from multiple countries and ethnicities, including athletes from a variety of endurance and weight-sensitive sports. While several questionnaire variables had sufficient sensitivity, only low sex drive score was associated with perturbations in key clinical REDs signs (eg, low blood testosterone concentrations).45

    It is recommended that questionnaires identifying symptoms of EDs should be included in REDs screening.1 The Eating Disorder Examination Questionnaire46 is frequently used to assess behavioural and cognitive symptoms of EDs. Other DE/EDs screening instruments used in athletic populations are shown in table 2. Furthermore, exercise addiction has been shown to be related to REDs in both male and female athletes.14 15 47 Consequently, validated questionnaires about excessive training behaviour may prove useful in a REDs assessment, although none have been validated yet for this purpose (table 2). There is some evidence that other psychological symptoms, such as mood disturbances/fluctuations, cognitive dietary restraint, perfectionistic tendencies, sleep disturbances, depressive symptoms, anxiety and reduced well-being, are associated with REDs.1 36 Therefore, screening for psychological and behavioural symptoms should also be considered in future research and clinical practice.

    Most questionnaires have been developed and validated for an adult athletic population; adolescent athletes, however, are at high risk for REDs and stand to benefit substantially from secondary prevention. Of note, the Brief Eating Disorder in Athletes Questionnaire,48 the REDs Screening Tool49 and the Disordered Eating Screen for Athletes50 show promising results for screening adolescent athletes (table 2). To date, no validated screening questionnaire for REDs in para athletes has been published.

    While questionnaires are easy to use, response bias and under-reporting may occur. Thus, to allow a more in-depth athlete clinical assessment, questionnaires should be accompanied by other information-gathering tools, such as personal interviews.51 Observation from coaches, parents, health personnel or others may serve as an opportunity to identify symptoms, such as excessive exercise behaviour, expressed need for recurrent and non-performance-related measures of body weight and composition, or concerning eating or dieting related behaviours.

    Objective assessment of symptoms

    Objective assessment of REDs signs may be used for the early identification of REDs and verification of self-reported symptoms (table 3). For example, self-reported menstrual dysfunction is strongly associated with clinically verified FHA in female endurance athletes.31 Furthermore, FHA is associated with lower female sex hormones and lower BMD.52 In males, subclinically or clinically low testosterone levels are potential biomarkers of problematic LEA53 54 and are associated with low libido45 and bone stress injuries.55

    View this table:
    Table 3

    Recommended treatment of outcomes of Relative Energy Deficiency in Sport (REDs)

    Evaluation of multiple REDs signs is necessary to accurately diagnose and determine the severity of REDs (table 3).1 For example, although FHA is commonly reported among female athletes,56 polycystic ovary syndrome (PCOS) is one of the most frequent menstrual disturbances in the general population, and athletes with PCOS may concomitantly have problematic LEA with FHA,57 EDs or low BMD.31 Therefore, FHA is a diagnosis of exclusion (table 3). Studies in recreationally active women have reported a 12%–30% prevalence of asymptomatic anovulation.56 It is recommended to confirm ovulation over at least three consecutive menstrual cycles to verify eumenorrhea in female athletes.58

    It is important to note that many female athletes use contraceptives containing exogenous hormones59 and may or may not have a withdrawal bleed, which is not equivalent to a menstrual cycle. Hence, assessing normal reproductive function can only be performed in the absence of exogenous hormones.

    There are strong associations between signs of problematic LEA (eg, low oestrogen/testosterone levels) and adverse bone parameters.1 55 Bone health can be assessed by DXA in the setting of suspected problematic LEA or recurrent bone stress injuries. Because of the osteogenic stimulus of weight-bearing exercise, low BMD in athletes has been defined as a Z-score<−1.0, as opposed to <−2.0 in the general population,16 and warrants further clinical evaluation. However, it has recently been proposed that there is a need for sport discipline-specific Z-score ranges in order not to underestimate low BMD in athletes representing high impact sports.60

    Subclinically or clinically low serum concentration of total or free triiodothyronine (T3) is a valid LEA biomarker in both male and female athletes.31 53 55

    Many athletes with REDs have a body weight within the normal reference range and may be lean or have more body fat than expected,61 and athletes with EDs may have a body weight that is under, within or above the normal reference range.62 Thus, it is important to assess athletes for REDs independent of percent body fat, body weight and body mass index.

    Secondary prevention is embodied in step one and two of the International Olympic Committee’s REDs Clinical Assessment Tool 2 (REDs CAT2), which is a three-step approach framework to operationalise the secondary and tertiary prevention of REDs.1 When early signs or symptoms of REDs are identified, it is necessary to progress to tertiary prevention corresponding to step three of the REDs CAT2, with focus on clinical diagnosis and treatment to safeguard athletes’ health.

    Tertiary prevention

    General principles

    The objective of tertiary prevention (clinical treatment) is to promote rehabilitation to prevent or limit short-term and long-term severe health consequences of REDs (figure 1). Accurate diagnosis of REDs versus other causes of the clinical presentation is essential for determining correct treatment and subsequent commencement of an effective management programme. The cornerstone of treatment is to identify the source of and treat the underlying cause: problematic LEA. Reversing LEA can be achieved by increasing energy intake, decreasing exercise energy expenditure or a combination of both. A multidisciplinary clinical team is recommended for comprehensive treatment. This team can include clinicians specialising in sports medicine, sports nutrition, sports psychiatry, sports psychology, exercise physiology, endocrinology and gynaecology.3 The expected timeline for recovery from REDs is variable and depends on multiple factors, such as the specific REDs condition, the severity, the presence of other medical issues and the underlying cause of LEA.63–66 The following section outlines treatment principles for the possible clinical sequelae of REDs (table 3).

    Impaired reproductive function

    Correcting LEA is the mainstay of treatment for hypothalamic–pituitary–gonadal axis dysfunction in both sexes,1 52 but few intervention studies have been performed.64 65 67 There is limited evidence in females with FHA that cognitive–behavioural therapy lowers circulating cortisol levels and improves reproductive function.68

    Impaired bone health

    Both the timing and duration of LEA are particularly relevant when considering bone-related REDs outcomes (eg, bone stress injuries, low BMD). Adolescence is a critical time of peak bone mineral accrual for both females and males, with peak bone mass typically achieved around the end of the third decade and most bone accrual having occurred by age 20 years.69 The development of REDs in childhood or adolescence necessitates swift treatment to prevent long-term consequences. With nutritional and menstrual recovery in REDs, some ‘catch-up’ bone accrual may occur, but less so if problematic LEA continues into young adulthood and beyond with increased risk for bone stress injuries, premature osteoporosis and full fractures over time.70

    Recommendations regarding optimal calcium and vitamin D intake vary depending on national recommendations; correcting LEA and optimising these bone-building nutrients is important (table 3).

    In adolescent and young adult female athletes with FHA, 12 months of transdermal 17-β oestradiol with cyclic oral progesterone improved DXA-measured BMD and was superior to oral contraceptives and no hormonal treatment.71 Thus, in female adolescents and adults, this treatment may be an appropriate adjunct to nutritional intervention.52

    The negative bone consequences of LEA are less studied in male athletes than female athletes, though it has been shown that low BMD and bone stress injuries occur in LEA-exposed exercising men.55 72 As with female athletes, correcting LEA is the mainstay of treatment, but adjunctive treatment with exogenous male reproductive hormones in male athletes has not been studied and is not recommended. While oestrogen is an important hormone for bone development for males, exogenous oestrogen treatment would lead to potentially unwanted feminising effects.73

    Impaired gastrointestinal (GI) function

    Cross-sectional studies have demonstrated a higher prevalence of GI issues in female athletes with LEA compared with those with adequate energy availability,31 47 and in male athletes with DE behaviours compared with controls.47 The treatment of GI consequences of REDs is derived from studies of patients with EDs, where GI complications are thought to stem from (a) poorly managed medical conditions that have GI-predominant symptoms (eg, coeliac disease); (b) physiological and anatomical changes that result from EDs and malnutrition; and (c) functional GI diseases that frequently accompany malnutrition (eg, motility disturbances, visceral hypersensitivity, mucosal changes, altered gut microbiome).74

    As athletes attempt to increase energy availability, it is important to determine the cause of various GI complaints, such as clarifying if abdominal pain or diarrhoea are from an underlying condition (eg, coeliac disease, inflammatory bowel disease). Consultation with a physician and/or a registered dietitian can aid in narrowing the differential diagnosis or when GI-specific adjunctive treatment is needed. Medications can be used to improve specific symptoms (eg, constipation, diarrhoea, bloating) on an interim basis until symptoms improve with improvement in EA.

    Other endocrine system impairments

    Various endocrine systems are interconnected and disrupted with LEA.75 Most hormonal disruptions seen in REDs (eg, decreased T3 and insulin-like growth factor 1 (IGF-1), increased cortisol) are the result of problematic LEA exposure, and resolution of LEA typically improves the hormonal disruptions.1

    Iron deficiency

    LEA may increase the risk of iron deficiency due to a lower dietary iron intake and/or a lower iron bioavailability.76 Dietary factors (eg, vegan diet) may reduce iron absorption,76 as well as elevated hepatic hepcidin levels post training.77 LEA may increase the hepcidin concentration directly or indirectly via low carbohydrate availability, low oestrogen or testosterone levels, and/or interleukin 6-induced alterations in hepcidin levels post exercise, and thereby increase the risk of iron deficiency.77 Consequently, iron intake to ensure a ferritin level above 30 µg/L, in addition to general nutritional rehabilitation to improve LEA, is appropriate.78 Consuming a diet high in iron is often not enough to replete iron stores in an athlete with iron deficiency, and 100–200 mg of elementary iron intake every other day until ferritin normalises is recommended.76 Iron supplementation alone, however, is not a panacea for an athlete’s iron deficiency, and diagnosing and treating the underlying cause is paramount.77

    Growth and development

    In young athletes with stunted growth and delayed non-constitutional pubertal development due to REDs, the treatment is restoring energy availability and body weight.66 79 Growth hormone (GH) and IGF-1 therapy have been studied in non-athletes with anorexia nervosa, but currently are indicated only if there is a primary GH deficiency or other endocrinopathy.1 80

    Mental health

    The treatment of mental health symptoms related to REDs may occur in outpatient or inpatient settings, depending on the severity. Psychotherapy is an integral component to the treatment of DE behaviour/EDs and can occur simultaneously with or subsequent to nutritional rehabilitation; the order of treatment is determined on a case-by-case basis. Weight restoration with repletion of energy availability has been shown to improve cognitive function and mood in anorexia nervosa.81 Additionally, the treatment of other underlying psychologic illnesses (eg, depression, anxiety, sleep disorders) should be prioritised in the overall treatment scheme. Pharmacotherapy is typically recommended for treating comorbid psychiatric illnesses, not primary treatment of DE behaviour/EDs. Bupropion is contraindicated in anorexia nervosa and bulimia nervosa treatment because of an association with higher seizure incidence.82 Patients with anorexia nervosa have an increased risk of suicide.83 Therefore, REDs and sports-related presentations of DE behaviour/EDs must include a suicide risk assessment.

    Other potential mental health outcomes of REDs include depression, anxiety and sleep disturbances.36 As an adjunct to correcting the underlying LEA and psychotherapy, relevant pharmacotherapies should be implemented with consideration of the potential negative impacts on sport performance, safety risks and limitations imposed by the World Anti-Doping Agency Prohibited List. Sleep hygiene education and cognitive–behavioural therapy have been helpful in treating sleep disturbances in the athlete population.84

    Cardiovascular

    Cardiovascular complications of severe LEA have been well described in patients with anorexia nervosa.85 Bradycardia can be a normal training adaptation.86 However, bradycardia and orthostatic hypotension are seen in severe LEA states (eg, anorexia nervosa) and can be life-threatening.85 Thus, bradycardia and orthostatic hypotension should be considered in the context of suspected problematic LEA and may require a higher level of care and abrupt cessation of training.87

    Endothelial dysfunction and unfavourable lipid profiles (high total cholesterol and low-density lipoprotein cholesterol) have been reported in athletes with FHA.88 Improved energy availability with resumption of menses may reduce cholesterol levels and improve vascular endothelial function.89 Endothelial dysfunction, however, has not been demonstrated in males.

    Immune system

    Impaired immune function, primarily demonstrated as increased viral illness susceptibility (eg, upper respiratory tract infections), is a potential presentation of REDs.34 90 The link between LEA and immunity in athletes is complex, and many factors may mediate this relationship.90 Recent data suggest that low carbohydrate availability may play a significant role in negatively affecting the immune system.91 Therefore, the best treatment to offset the impaired immune function would be restoring energy and carbohydrate availability,91 92 and may also include supplementation of probiotics, vitamin C and vitamin D.92

    Urinary incontinence (UI) (female athletes)

    In a cross-sectional study of 1000 female athletes, those with indicators of LEA reported more UI than those without LEA indicators.93 It is important to confirm the aetiology of UI by ruling out causes other than problematic LEA (table 3). UI can be classified as stress, urge, overflow or mixed based on the underlying cause, with stress and urge incontinence more common in female athletes with EDs than those without.94–96 As with all REDs health outcomes, attention to reversing the LEA is paramount. The most recommended treatment for UI is pelvic floor muscle training (with or without biofeedback); other treatments include lifestyle interventions, electrical stimulation or surgery.97

    Recommended guidelines for REDs prevention

    The best approach to preserve health and improve performance is primary prevention of REDs. A multipronged approach is recommended, targeting the athlete health and performance team, athlete entourage and sport organisations, which together need to create a supportive and safe sport environment, have sufficient REDs knowledge and be observant for the early signs and symptoms of REDs (table 4).

    View this table:
    Table 4

    Suggested guidelines for the prevention of Relative Energy Deficiency in Sport (REDs), targeting the athlete health and performance team, athlete entourage and sport organisations

    Early identification of athletes at risk is critical to prevent the progression of REDs. Before screening for REDs, it is important to have a multidisciplinary athlete health and performance team available to identify and respond to signs and symptoms of REDs. Screening for REDs by a sports medicine physician should be included in the periodic health evaluation or by clinical indication (table 4). The treatment strategy recommended by the athlete health and performance team should be supported by the sports organisation and coaching staff to optimise athlete compliance and treatment outcomes (table 4).

    Conclusion

    The current review highlights that primary, secondary and tertiary prevention strategies of problematic LEA and REDs are necessary to promote and protect athlete health and performance. First, primary prevention is crucial to minimise exposure to and reduce behaviours associated with problematic LEA. A special focus on at-risk groups is recommended. Second, early identification of athletes with symptoms or signs of problematic LEA is important to prevent the progression of REDs. Recommended secondary prevention tools are questionnaires, health interviews and objective REDs markers. Finally, tertiary prevention strategies include clinical treatment to prevent or limit short-term and long-term severe health consequences of REDs. Reversing the underlying cause of REDs, namely problematic LEA, can be achieved by increasing energy intake, decreasing exercise energy expenditure, or a combination of both. A multidisciplinary approach that targets the athlete health and performance team, coaches and sport organisations, focussing on a supportive and safe sporting environment, is recommended for the prevention of REDs.

    Summary box

    What is already known?

    • Male and female athletes in various sports may be at risk for developing Relative Energy Deficiency in Sport (REDs).

    • Questionnaires are frequently used to identify athletes at risk of low energy availability (LEA) and/or REDs.

    • Reversal of problematic LEA is the cornerstone of treatment of REDs.

    What are the new findings?

    • Special consideration should be aimed towards young female athletes during the adolescent transition period that is considered high risk for problematic LEA/REDs.

    • Few questionnaires used to identify athletes at risk of LEA and/or REDs are validated.

    • Evaluation of multiple REDs signs and symptoms (physiological, psychological, and behavioural) is necessary for optimal identification and management of REDs.

    • The REDs Clinical Assessment Tool 2 provides a clinical framework to operationalise the secondary (early identification) and tertiary (treatment) prevention of REDs.

    Ethics statements

    Patient consent for publication

    Ethics approval

    Not applicable.

    Acknowledgments

    The authors would like to thank the International Olympic Committee for their prioritisation and support of athlete health.

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    Footnotes

    • X @MMonicakt, @drkateackerman, @BSHoltzman, @margo.mountjoy, @jorunn_SB, @AnnaMelin4

    • Contributors MKT and AM were responsible for leading and coordinating the manuscript. KK and JSB were responsible for drafting the section on primary prevention. AM and MKT were responsible for drafting the section on secondary prevention. MLM, KEA, BH and NC were responsible for drafting the section on tertiary prevention. All authors were involved in the final manuscript’s conception, revising and approval before submission.

    • 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 MLM is a deputy editor of the BJSM and a member of the BJSM IPHP editorial board. KEA is a deputy editor of the BJSM and an associate editor of the BJSM IPHP.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.