Relative energy deficiency in sport (REDs) is a multifactorial syndrome associated with negative long-term health and performance consequences.1 REDs affects a high number of athletes, with those competing in endurance, aesthetic, and weight-classification sports particularly vulnerable.2 The underlying etiology of REDs is problematic low energy availability (LEA), defined as severe and/or prolonged inadequate energy intake (EI) relative to exercise energy expenditure (EEE). Problematic LEA causes hormonal perturbations leading to a multitude of impairments to important physiological and psychological body systems. This includes several negative effects on musculoskeletal (MSK) health and performance such as deteriorations in bone health and muscle atrophy, leading to reduced muscular strength, power, and reduced muscular work capacity.
For athletes diagnosed with REDs, a treatment plan should aim to prevent long-term health and performance sequelae1 and maximize the likelihood of a full and successful return to performance (RTP). Although guidelines exist to support clinicians and trainers with decision making during an athlete’s recovery from REDs,3,4 specific recommendations around exercise prescription, alongside nutritional intervention, are currently lacking. There is clear evidence that MSK training (ie, resistance training, ballistic power training, plyometric-based exercise) offers a multitude of benefits to MSK health,5 assuming energy needs are met. Furthermore, resistance training is a safe and effective exercise modality for individuals suffering from chronic diseases such as osteoarthritis6 and inflammatory-related conditions.7 Given the wide-reaching benefits of MSK training, it is therefore hypothesized that MSK-based exercises should be utilized as an integral component of the exercise intervention treatment of REDs. The aim of this brief commentary is to discuss the health and performance implications of problematic LEA on the MSK system and examine the potential role that MSK-based training modalities play during an RTP REDs treatment plan. The paper also aims to offer practical guidelines using the available evidence and combined clinical expertise around the safe and effective use of MSK training for athletes recovering from REDs.
Consequences of REDs on Musculoskeletal Health and Performance
Figure 1 provides a visual summary of the consequences of problematic LEA on the MSK system, and the potential performance and injury manifestations of these effects. LEA causes marked perturbations to an athlete’s hormone profile including the suppression of estrogen, testosterone, leptin, triiodothyronine (T3), and insulin-like growth factor-1, which are all involved in the regulation of bone (re)modeling.8 Consequently, athletes with REDs exhibit low bone mineral density (BMD), total and cross-sectional bone area, bone strength, and thinner cortices, each of which may contribute to the development of a bone stress injury when accumulated mechanical stress exceeds the load tolerance of a bone.9 Indeed, male and female athletes exhibiting several primary indicators for REDs, including low BMD, are more likely to suffer a bone stress injury.10,11 Adolescent athletes exhibiting REDs symptoms, including delayed menarche in females, are of particular concern in this regard, as peak bone mass occurs around 19 years of age.12
—Physiological consequences of problematic LEA on the musculoskeletal system, with potential performance and injury implications. EA represents EI minus EEE. EA is considered optimal when EI is sufficient to support biological processes after EEE is deducted. LEA can be caused by an increase in EEE, without an increase in EI or a reduced EI without a decrease in EEE. Problematic LEA results from severe and/or prolonged inadequate EI relative to EEE. EA indicates energy availability; EEE, exercise energy expenditure; EI, energy intake; LEA, low energy availability.
Citation: International Journal of Sports Physiology and Performance 19, 7; 10.1123/ijspp.2023-0532
Problematic LEA is characterized by a catabolic physiological state, which over time alters body composition, including reductions in lean body mass.13 In particular, when LEA is induced via caloric restriction, there is a resultant reduction in skeletal muscle protein synthesis14 and glycogen content,15 thereby decreasing lean body mass and hindering recovery processes. Several prospective studies of military recruits exposed to energy deficits have also noted significant reductions in power and force-producing capabilities, which correlate with losses in muscle mass.13,16,17 Furthermore, a decrease in muscle work capacity and reaction time has been observed in female athletes with menstrual dysfunction compared with eumenorrheic athletes.18 Lower neuromuscular performance in this study was associated with lower fat-free mass in the leg, and lower glucose, estrogen, and T3, providing a biologically plausible link between chronic LEA and neuromuscular deficiencies.18 It seems likely that problematic LEA could impair sport performance via these aforementioned mechanisms.19
Reductions in lean body mass, BMD, and strength-related capabilities associated with REDs may also leave an athlete vulnerable to injury upon their return to sport.1 Prospective studies have demonstrated that muscular weakness may predispose athletes to injury20,21 and stronger athletes have a greater tolerance to higher absolute workloads and spikes in workload compared with weaker athletes.21 Clearly addressing any MSK deficiencies relative to norms in the athlete’s sport, alongside appropriate nutritional intervention, should be a priority during recovery from REDs to maximize long-term performance and health outcomes.
Treatment of REDs and Return to Practice and Performance
The IOC REDs Clinical Assessment Tool-Version 2 (CAT2)3,22 provides a guide for medical professionals in the diagnosis and management of athletes presenting with REDs. Alongside addressing any psychological concerns related to an eating disorder or disordered eating behaviors, the primary objective of REDs treatment is nutritional intervention with the involvement of a sports dietitian.22 An accurate and ongoing measurement of an athlete’s EA is challenging; therefore, pragmatic REDs treatment strategies have also been recommended.4,23 The clinical management and RTP process for athletes with REDs should ideally occur with the input of an experienced multidisciplinary sports medicine team, including being overseen by a sports medicine doctor/physician, but also involving a sports dietitian, exercise physiologist, physical or athletic therapist/trainer, and a sports/clinical psychologist or psychiatrist.1
In athletes categorized in the “yellow light” zone (mild risk/severity) on the REDs CAT2,3 it is unnecessary to cease sports training and competition. However, the athlete should address energy deficits via increases in EI and be monitored regularly. Athletes classified on the REDs CAT2 in the “orange light” zone (moderate to high risk/severity) may require modification of their training and/or competition plan with close monitoring to assess clinical status.3 In athletes satisfying the clinical criteria for a “red light” zone diagnosis, significant modifications to training are necessary.3 Prioritizing restoration of EA by increasing EI and decreasing EEE will stimulate anabolic processes and reverse energy-conserving adaptations in the short term; however, recovery of menstrual status and hormonal profile is likely to take months.24 Athletes may gradually return to full sport and exercise training as part of an agreed treatment plan once they are no longer considered “high risk,” with frequent monitoring necessary.1,3
Specific recommendations and criteria for RTP following REDs are largely based on anecdotal practices.25 MSK training has been highlighted as an important nonpharmacological strategy in the early treatment of REDs23 and is advocated by clinicians.26 Similarly, for athletes recovering from an eating disorder, the Safe Exercise at Every Stage guidance endorses resistance training as an important first step in the return to training.27 Importantly, individualized exercise prescriptions during REDs treatment plans should be supported and endorsed by the responsible medical doctor/physician.
During recovery from REDs, an important goal for athletes is to minimize losses in fitness while balancing the potentially conflicting need to remain in a caloric surplus. There is a dearth of evidence-based information on exercise interventions as part of an RTP process in REDs.1 Cardiorespiratory exercise has clear physiological relevance for performance in many sports, yet is energetically expensive28 and fails to address deficiencies in MSK health caused by REDs. An alternative approach to prioritizing cardiorespiratory or “sport-specific” training during the initial stages of REDs rehabilitation, is to emphasize MSK-based exercise, which involves high-intensity short-duration bouts of physical activity, designed to stimulate adaptations in MSK structure and neuromuscular function.5 This type of exercise is relatively energy efficient28 and promotes underlying physiological qualities (eg, maximal strength, power, reactive strength) that are important for long-term performance and injury prevention.5 Development of MSK capacities during the early stages of an RTP process is therefore likely to support higher volumes of sport-specific preparation and mitigate against injury risk in the long term.21 Furthermore, the period of rehabilitation from REDs affords athletes the opportunity to target potential areas of weakness that can provide a refreshing change to their previous training routine.29
Musculoskeletal Training During REDs Treatment
MSK-based exercise is well-recognized as a training modality that is important for sport performance and health.5 Increases in muscular strength are associated with improvements in athletic tasks demanding explosive power (eg, jumping and sprinting)30 and endurance performance.31 Moreover, the protective effect of strength training32 and broader “neuromuscular training”33 programs on the incidence of sport injuries is well-established. In individuals with altered hormonal regulation, compared to age-matched sedentary people, resistance training also increases basal levels of anabolic hormones,34 which may be advantageous for MSK health outcomes in athletes recovering from REDs.
Resistance training and high-impact plyometric exercise are a potent stimulus for increasing BMD and bone geometry in healthy populations35; however, less is known about the response of bone to mechanical loading during and following problematic LEA. A prospective study in women recovering from an eating disorder reported that resumption of menstrual function and increases in lean body mass were necessary for increasing spine and hip BMD.36 Furthermore, a study in male endurance cyclists identified as being “at risk” of REDs found that 6 months of resistance training and jumping exercise (15–20 min per session; 3× per week) significantly improved lumbar spine BMD compared to a group that only cycled.37 Conversely, recent work has demonstrated that plyometric exercise is unlikely to offer an osteogenic stimulus for new bone formation38 and prevent bone stress injury39 if athletes remain in a state of LEA. Similarly, performing a bout of heavy-resistance exercise in short-term caloric restriction appears to attenuate bone resorption but not promote bone formation40; which is why restoration of optimal LEA remains the first target for treatment.
In the absence of sufficient mechanical loading to the MSK system, the majority of weight regained in individuals with problematic LEA due to an eating disorder is represented by fat mass, while muscle mass appears to lag or remain unchanged.41 Since the size of a muscle has a strong relationship with its maximal force-producing capability, it would be prudent for athletes aiming to increase their body mass to engage in resistance training alongside nutritional intervention, which promotes muscle hypertrophy.42 LEA is known to impair increases in muscle mass associated with resistance training,43 and nutritional guidance alongside resistance training appears important for obtaining long-term gains in lean body mass in elite athletes.44 Collectively, these findings suggest that MSK-based exercise that aims to increase muscle mass and bone strength can be an important underappreciated component of recovery from REDs, provided energy needs are met.
Practical Applications and Conclusions
Prescription of exercise, including MSK training, during the REDs RTP process should be individualized and account for the athlete’s unique situation, including training history.3 The overarching aims of MSK training in the context of REDs treatment along with evidence-based guidelines and examples of exercise prescription from clinical practice are shown in Table 1. For both plyometric and resistance training, it is strongly advised that exercises are performed under qualified supervision and initial sessions prioritize development of movement competency at lower intensity. This is particularly important for athletes with minimal MSK training experience. Athletes with prior experience of structured MSK training should initially aim to reestablish technical competence in exercises, but may be capable of progressing at a faster rate compared to those with less training experience, assuming energy needs are met.
Practical Guidelines for the Use of Musculoskeletal-Based Exercise Training (Plyometric and Resistance Training) During Return to Performance Following Relative Energy Deficiency in Sport
| Plyometric training | Resistance training | |
|---|---|---|
| Primary aims related to treatment for relative energy deficiency in sport | • Improve explosive and reactive strength • Improve bone health • Injury risk reduction on return to performance • Psychological well-being | • Increase lean body mass • Improve maximal strength • Improve bone health • Injury risk reduction on return to performance • Psychological well-being |
| Key characteristics | • High-impact jumping/hopping • Multidirectional elements • Minimal equipment | • Multijoint functional movement patterns • External load (free weights) required as the athlete progresses |
| Prescription guidelines | • Initial focus on technique under supervision • Perform on most days • Short ground-contact time • Maximize rebound height/distance • 50 foot contacts per session (60–100 as strength improves) | • Initial focus on technique (body weight) under supervision • 2–3 days per week • 8–12 repetitions per set (less as strength improves) • 2–3 sets per exercise (more as strength improves) • 2–3 min between sets • Inclusion of axial loading exercises |
| Session example (familiarization/early recovery from relative energy deficiency in sport | 2–3 sets of 10 repetitions (∼1 min interset recovery): • Pogo jumps • Lateral step and stick | 2–3 sets of 12 repetitions (2 min interset recovery): • Body-weight squat • Gluteal bridge • Split squat • Modified press-up • Band-resisted row |
| Session example (experienced athlete): | 3–4 sets of 6-10 repetitions (∼1 min interset recovery): • 30-cm-hurdle rebound jumps • Broad jumps • Zig-zag bounding | 3–4 sets of 5 repetitions (3 min interset recovery): • Back squat • Deadlift • Overhead press • Barbell step-up • Single-arm dumbbell row |
In athletes with a prolonged history of severe REDs and/or an eating disorder, little is known about the risks and contraindications associated with exercise during early treatment. Concerns have been raised around the safety of high-impact plyometric exercise in individuals with osteoporosis, who are prone to bone stress injuries.45 However, recent expert consensus indicates there is little evidence that those with low BMD are at greater risk of harm, including fractures, when performing low-volume plyometric- or resistance-based exercise under qualified supervision.35 Furthermore, several cardiovascular impacts of prolonged problematic LEA have been identified, such as orthostatic hypotension and tachycardia.46 Athletes displaying cardiovascular complications must be medically investigated before exercise reengagement and modifications to the initial prescription (eg, supine versions of exercises) may be required with monitoring.
To promote adaptations related to bone health and explosive strength, it is recommended that moderate- to high-impact plyometric exercise is included on most days, provided athletes remain energy replete. Sessions should aim to include around 50 foot contacts split across several exercises and multiple sets, each interspersed with 1 to 2 min passive recovery.35 Resistance training also provides an osteogenic stimulus and is recommended for increasing skeletal muscle mass and maximal strength. Furthermore, resistance training may be particularly important for promoting changes in hip BMD compared with plyometric-based training.47 Multijoint exercises targeting all muscle groups should be utilized on 2 to 3 days per week with several sets performed per exercise to nonrepetition failure, but with a “high level of effort.”42 If these guidelines are met, loads appear to be less important for stimulating a hypertrophy response (and maximal strength in lesser strength-trained athletes); however, intensity is an important factor for promoting adaptations to bone, therefore loads that can be lifted for a maximum of 8 to 12 repetitions are recommended.35 A progressive overload stimulus is essential to promote further improvements, with current evidence indicating maximal strength training should involve a load between 80% and 100% of an athlete’s 1 repetition maximum, lifted for 1 to 6 repetitions per set, 3 to 5 sets per exercise, with a 3-min interset recovery.48
In conclusion, REDs has serious long-term implications for an athlete’s performance and health. Periods of problematic LEA cause disruptions to an athlete’s hormone profile resulting in negative physiological and psychological effects, including many that impact MSK health and performance. Restoring optimal EA via nutritional intervention represents the cornerstone of treatment for REDs. Athletes presenting with high-risk/severity scores, as defined by the REDs CAT2, are advised to reduce or cease training and competition, based on professional clinical diagnosis. An athlete’s individualized treatment plan should be implemented by a multidisciplinary support team and include a carefully structured RTP, with regular monitoring to inform decision making. MSK-based training (ie, resistance training and plyometrics), which improves MSK health and neuromuscular capabilities, should be an important component of an athlete’s RTP program during REDs treatment to maximize long-term health and performance outcomes. The practical guidelines and session examples presented in this paper are informed by scientific evidence and clinical practice; however, research training studies using these methods in athletes recovering from REDs are needed to establish efficacy and to explore the feasibility, acceptability, and potential wider psychological benefits of MSK training in this population.
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