Relative Energy Deficiency in Sport (RED-S)
Introduction[edit | edit source]
Relative Energy Deficiency in Sport (RED-S) (the updated model of the female athlete triad) was defined by the International Olympic Committee in 2014 as: ‘impaired physiological functioning caused by relative energy deficiency, and includes but is not limited to impairments on metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health’
This term has replaced the female athlete triad, which is the interrelationship between menstrual dysfunction, low energy availability and reduced bone mineral density . This is because it is now evident that this syndrome impacts both female and male individuals experiencing low energy availability, and that the effects of the low energy availability extend far further than menstrual function and bone health.
Glossary[edit | edit source]
- Amenorrhea - An abnormal absence of menstruation
- Dysmenorrhea - Painful menstruation, typically involving abdominal cramps
- The Female Athlete Triad – The interrelationship of menstrual cycle dysfunction, reduced energy availability and reduced bone mineral density
- Hypomenorrhea – Abnormally light menstrual bleeding
- Menarche – ‘The occurrence of the first menstrual period in the female adolescent’ 
- Menorrhagia – Heavy menstrual blood loss
- Menstrual cycle - The process of ovulation and menstruation
- Menstruation - The process of discharging blood and other material from the lining of the uterus at intervals of about one lunar month from puberty to the menopause, except during pregnancy
- Oligomenorrhea - Menstrual cycle length of greater than 45 days
- Osteopenia - A medical condition in which the protein and mineral content of bone is reduced, but less severely than in osteoporosis
- Relative Energy Deficiency in Sport (RED-S) - This is impaired physiological function including, but not limited to impairment of: metabolic rate; menstrual function; bone health; immunity; protein synthesis; and cardiovascular health, caused by energy deficiency
Low Energy Availability (LEA)[edit | edit source]
LEA underpins RED-S, and is the instance in which there is a chronic mismatch between nutritional intake and energy expenditure, thus leaving insufficient energy available for essential physiological functions . As a result, physiological functions are down-regulated in order to preserve energy for more essential functions and for movement, thus leading to detrimental health and performance implications for the athlete.
LEA may be intentional, with the athlete intentionally restricting their dietary intake, or unintentional, in which the athlete's nutrition simply does not meet the demand of their training load . Whether the LEA is intentional or unintentional, there remain the same significant implications to the health and performance of the athlete, but it is essential to recognise which form of LEA an athlete may be suffering, as management for each differs.
- Intentional LEA - the athlete is intentionally restricting their dietary intake to control body weight and/or body composition .This is more commonly seen in sports in which their is a weight category such as light-weight boxing and rowing due to the additional external pressure and emphasis on aesthetics or appearance .
- Management - management is complex because relationship with food and psychology must be addressed. This requires a multidisciplinary team approach with medical, dietary and mental health support
- Unintentional LEA - the athlete is not meeting the demands of their sport, commonly during periods with increased training volume or when engaging in sports with high energy expenditure 
- Management - this is easier to manage, and it may be sufficient to simply educate the patient on the nutritional demands of their training load
Epidemiology of RED-S[edit | edit source]
The prevalence of RED-S is not well documented due to the inherent methodological difficulties in diagnosing true low energy availability. A narrative review conducted in 2020 found prevalence varies between sports, and ranges in the literature between 22-58% in the female population. There is significant difficulty in estimating LEA due to the wide variety of methods used to estimate LEA, and therefore comparing data across studies proves challenging.
Additionally, the understanding of RED-S and its symptoms are poorly known by athletes and coaches, and therefore it is also not commonly recognised. A further review identified that fewer than 50% of physicians, coaches, physiotherapists and athletic trainers could identify the triad components (Low energy availability +/- disordered eating, menstrual dysfunction, low bone mineral density). As a result, fewer cases will be recognised, diagnosed, and therefore highlighted as suffering from RED-S.
Health and Performance Implications of RED-S[edit | edit source]
Health implications are multi-system, affecting the endocrine, metabolic, skeletal, cardiovascular and immune systems; and in women, the menstrual cycle is disrupted. Not infrequently are also significant ramifications on the psychological state of the individual, given the prevalence of disordered eating in this population.
- Endocrine health- LEA disrupts the hypothalamic-pituitary-gonodal axis, and has subsequent implications on thyroid function. These hormonal changes occur as a response to LEA, thus attempting to conserve energy for more important functions .
- Menstrual function - Stress and low energy availability cause suppression of the hypothalamic–pituitary–axis (HPA) and subsequent reduction in the volume of GnRH secreted from the hypothalamus. As a result, the menstrual cycle is disrupted, in a condition called hypothalamic amenorrhea.The degree to which the HPG axis is affected, directly dictates the severity of menstrual dysfunction. For example, oligomenorrhea may develop into amenorrhea with further disuprtion to the HPA axis and reductions to GnRH, LH and FSH levels.
- Prevalence of amenorrhea - the prevalence of amenorrhea has been estimated to be between 2.6% and 4.4% by Bachmann and Kemmann (1982), and Pettersson et al., (1973), respectively. Similarly, a third study found that in a population of pre- menopausal women, 4% had experienced secondary amenorrhea (Miller and Klibanski, 1999). More recently, in a systematic review, the prevalence of amenorrhea in a sporting population was reported to be 27.7% , and is therefore far higher than in the general female population.
- Bone Health - LEA causes a chronic state of hypoestrogenism, which in turn causes down-regulation of osteoclast activity . As a result of the suppression of osteoclasts, normal bone remodelling is not initiated, and therefore bone mineral density is reduced . With less robust bone health, there is an increased prevalence of stress injuries and stress responses in individuals suffering with LEA.
- Metabolic implications - Resting metabolic rate is reduced in order to conserve energy
- Cardiovascular implications - Individuals with LEA/RED-S are found to have lower heart rates and systolic blood pressure, and atherosclerosis has been found to be associated with hypoestrogenism
- Gastrointestinal impact - the influence of LEA on gastrointestinal function is important, as these symptoms resulting from LEA are commonly used in screening tools (as detailed below). Individuals suffering from LEA may experience: altered sphincter function and constipation
- Immunological - LEA is commonly associated with increased bouts of illness, most commonly upper respiratory symptoms, but also inclusive of symptoms relating to the gastrointestinal tract 
- Psychological - In the population of individuals with RED-S, there is an increased prevalence of eating disorders and disordered eating. This has significant implications for psychological well-being, by potentially exacerbating low self-esteem, anxiety and depression. The aforementioned drive for thinness seen in athletes competing in weight categories is associated with higher depressive traits and worsened ability to manage stress , and higher social insecurity.
Performance implications are significant and are the result of the negative influences on training adaptations, coordination, endurance performance, muscle strength, worsened concentration, irritability, impaired judgement, and the increased risk of injury.
- Muscular strength and endurance - Adaptations associated with LEA are known to negatively influence muscular adaptations in both endurance and strength and power athletes. Endurance athletes, because of a negative impact on mitochondrial protein synthesis and strength, and power athletes, because of a negative impact on muscle protein synthesis. 
- Neuromuscular performance and reaction times are reduced 
Red Flags for RED-S[edit | edit source]
- Cardiac abnormalities
- Recent weight loss
- Restrictive eating and body dysmorphia
- Stress fractures
- Overuse injuries
- Recurrent illnesses
Screening Tools[edit | edit source]
- RED-S CAT - Relative Energy Deficiency in Sport (RED-S) Clinical Assessment Tool (CAT) https://bjsm.bmj.com/content/bjsports/49/7/421.full.pdf 
- Can assess males and female athletes at risk of RED-S
- Is a more functional model using a traffic light system
- Assess both risk of RED-S and guides return to play decisions
- LEAF-Q - Low Energy Availability in Females Questionnaire http://www.diva-portal.org/smash/get/diva2:1303041/FULLTEXT02.pdf 
- For female athletes only
- High Sensitivity (78%) and specificity (90%)
- Covers injury history, gastrointestinal function and menstrual function
RED-S in Male Athletes[edit | edit source]
As mentioned, there has been a move away from the female athlete triad towards relative energy deficiency in sport, as it is known to affect both female and male athletes, although the physiological effects of the condition inevitably differ.
In male athletes, the mechanism is the same: low energy availability (intentional or unintentional) leads to a host of health and performance consequences . In male athletes it is predominantly characterised by low testosterone levels, thus impacting both the health and performance of the athlete.
RED-S in Specific Sports[edit | edit source]
The higher prevalence of RED-S has been documented in combat sports, in rowers and in jockeys all of which have weight categorisations, and therefore an increased emphasis on the weight of the athlete and drive for thinness pre-competition.
RED-S is prevalent in male cyclists, and the negative association between risk level and peak power has been identified . A sport-specific screening tool (SEAQ-1) has been created to help with the identification of those at risk and the diagnosis of individuals experiencing RED-S. This is particularly important in cyclists, given the lack of impact and weight-bearing activity their sport requires, thus increasing the risk of reduced BMD.
For further information on RED-S in Male Athletes, a second Physiopedia page has been created: The Male Athlete Triad
Management[edit | edit source]
Non-pharmacologic – When a patient is diagnosed with RED-S, the following management strategies should be implemented: education; optimising energy availability; modification of exercise and nutrition; supplementation of vitamin D and calcium; and CBT. An MDT approach should be adopted, including mental health support. Sport participation may be used as leverage. High-impact should be avoided due to the increased risk of developing a stress response, and therefore exercise should consist of resistance training and low-impact weight bearing exercise in order to optimise BMD
Pharmacologic – oral contraceptive is not recommended as it creates false menstruation or a ‘pseudo-period’ in female athletes. The use of recombinant parathyroid hormones and its role in improving bone mineral density is currently under review .
The role of physiotherapists in management of RED-S: As holistic practitioners, physiotherapists are well-placed to identify and treat the multimodal causes of physical impairment. They can assess, modify and monitor an individual's activity levels during recovery, prescribe an appropriate training schedule for the athlete, and work as part of the multidisciplinary team to develop treatment goals for the patient.
Conclusion[edit | edit source]
Regular screening for RED-S is essential for holistic, patient-centred care, as there are significant health implications (both physical and psychological) and performance implications resulting from this condition. It is important that clinicians consider RED-S not only in sporting populations, but in any individual at risk from a chronic mismatch between energy input and expenditure (both male and female).
Author and Affiliations[edit | edit source]
Physiotherapist at Isokinetic Medical Centre, Harley Street
References[edit | edit source]
- ↑ 1.0 1.1 1.2 1.3 1.4 1.5 1.6 Mountjoy, M., Sundgot-Borgen, J., Burke, L. M., Carter, S., Constantini, N., Lebrun, C., ... Ljungqvist, A. (2014). The IOC consensus statement: beyond the female athlete triad--relative energy deficiency in sport (red-s). British Journal of Sports Medicine, 48(7), 491–497. https://doi.org/10.1136/bjsports-2014-093502
- ↑ Nazem TG, Ackerman KE. The female athlete triad. Sports Health. 2012 Jul;4(4):302-11. doi: 10.1177/1941738112439685. PMID: 23016101; PMCID: PMC3435916.
- ↑ 3.0 3.1 3.2 3.3 3.4 Ferin, M., Jewelewicz, R., Warren, M. (1993) The Menstrual cycle. Oxford: Oxford University Press (pp. 186-187)
- ↑ 4.0 4.1 Nazem and Ackerman, 2012. The Female Athlete Triad. Sports Health. 4(4). [Online].
- ↑ Yaffe, H., Ron, M., Polishuk, W. Amenorrhea, Hypomenorrhea, and Uterine Fibrosis. American Journal of Obstetrics and Grynaecology. 130(5): 599-601
- ↑ Lacroix, A., Gondal, H., Langaker, M., 2020. Physiology, Menarche. StatPearls Publishing. Treasure Island (FL)
- ↑ National Institute for Health and Care Excellence 2018. Menorrhagia: What is it? Clinical Knowledge Summaries
- ↑ Riaz Y, Parekh U. Oligomenorrhea. [Updated 2022 Aug 1]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK560575/
- ↑ 9.0 9.1 9.2 9.3 Wasserfurth, P., Palmowski, J., Hahn, A. et al. Reasons for and Consequences of Low Energy Availability in Female and Male Athletes: Social Environment, Adaptations, and Prevention. Sports Med - Open 6, 44 (2020). https://doi.org/10.1186/s40798-020-00275-6
- ↑ Burke L, Lundy B, Fahrenholtz L et al, & Melin. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. International Journal of Sport Nutrition and Exercise Metabolism2018; 28(4):350–363
- ↑ Gillbanks L, Mountjoy M, Filbay SR. Lightweight rowers' perspectives of living with Relative Energy Deficiency in Sport (RED-S). PLoS One. 2022 Mar 17;17(3):e0265268. doi: 10.1371/journal.pone.0265268. PMID: 35298499; PMCID: PMC8929546.
- ↑ De Souza, M. J., Williams, N. I., Nattiv, A., Joy, E., Misra, M., Loucks, A. B., ... Rauh, M. J. (2014). Misunderstanding the female athlete triad: refuting the IOC consensus state- ment on relative energy deficiency in sport (red-s). British Journal of Sports Medicine, 48(1461–1465), 1461–1465. https://doi.org/10.1136/bjsports-2014-093958
- ↑ 13.0 13.1 Logue DM, Madigan SM, Melin A, Delahunt E, Heinen M, Donnell SM, Corish CA. Low Energy Availability in Athletes 2020: An Updated Narrative Review of Prevalence, Risk, Within-Day Energy Balance, Knowledge, and Impact on Sports Performance. Nutrients. 2020 Mar 20;12(3):835. doi: 10.3390/nu12030835. PMID: 32245088; PMCID: PMC7146210.
- ↑ Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2018 Apr;57(3):847-859. doi: 10.1007/s00394-017-1498-8. Epub 2017 Jul 18. PMID: 28721562; PMCID: PMC5861178.
- ↑ Gordon, C., Ackerman, K., Berga, S., Kaplan, J., Misra, M., Murad, H., Santoro, N., Wareen, M. 2017. Functional Hypothalamic Amenorrhea: An Endocrine Society Clinical Practice Guideline. The Journal of Clinical Endocrinology and Metabolism. 102(5). Pp. 1413 – 1439.
- ↑ Koltun KJ, Williams NI, Scheid JL, De Souza MJ. Discriminating hypothalamic oligomenorrhea/amenorrhea from hyperandrogenic oligomenorrhea/amenorrhea in exercising women. Appl Physiol Nutr Metab. 2020 Jul;45(7):707-714. doi: 10.1139/apnm-2019-0640. Epub 2019 Dec 9. PMID: 31815525.
- ↑ Bachmann, G., Kemmann, E. 1982. Prevalence of Oligomenorrhea and Amenorrhea in a College Population. American Journal of Obstetrics and Gynaecology. 144(1). Pp. 98 – 102.
- ↑ Petterson, F., Fries, H., Nillius, S. 1973 Epidemiology of Secondary Amenorrhea: I. Incidence and Prevalence Rates. American Journal of Obstetrics and Gynaecology. 117 (1). Pp. 80 – 86.
- ↑ Miller, K., Klibanski, K., 1999. Amenorrheic Bone Loss, The Journal of Clinical Endocrinology & Metabolism. 84(6) pp 1775–1783
- ↑ Gibbs, J., Williams, N., De Souza, M. 2012. Prevalence of Individual and Combined Components of the Female Athlete Triad. Medicine and Science in Sports and Exercise.
- ↑ Sona C. Dave, Martin Fisher. Relative energy deficiency in sport (RED – S). Current Problems in Pediatric and Adolescent Health Care. Volume 52, Issue 8, 2022,
- ↑ Boyce BF, Yao Z, Xing L. Osteoclasts have multiple roles in bone in addition to bone resorption. Crit Rev Eukaryot Gene Expr. 2009;19(3):171-80. doi: 10.1615/critreveukargeneexpr.v19.i3.10. PMID: 19883363; PMCID: PMC2856465.
- ↑ Melin, A., & Lundy, B. (2015). Measuring energy availability. In L. Burke & V. Deakin (Eds.), Clinical Sports Nutrition (5th ed., pp. 146–157). Sydney: McGraw-Hilll.
- ↑ O’Donnell, E., Goodman, J. M., & Harvey, P. J. (2011). Cardio- vascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women. Journal of Clinical Endocrinology and Metabolism, 96(12), 3638–3648. https://doi.org/10.1210/jc.2011-1223
- ↑ Norris, M. L., Harrison, M. E., Isserlin, L., Robinson, A., Feder, S., & Sampson, M. (2016). Gastrointestinal complications associated with anorexia nervosa: a systematic review. International Journal of Eating Disorders, 49(3), 216–237. https://doi.org/10.1002/eat.22462
- ↑ Shimizu, K., Suzuki, N., Nakamura, M., Aizawa, K., Imai, T., Suzuki, S., Akama, T. (2012). Mucosal immune func- tion comparison between amenorrheic and eumenorrheic distance runners. Journal of Strength and Conditioning Research, 26(5), 1402–1406. https://doi.org/10.1519/ JSC.0b013e31822e7a6c
- ↑ Bomba, M., Corbetta, F., Bonini, L., Gambera, A., Tremolizzo, L., Neri, F., & Nacinovich, R. (2014). Psychopathological traits of adolescents with functional hypothalamic amen- orrhea: a comparison with anorexia nervosa. Eating and Weight Disorders, 19(1), 41–48. https://doi.org/10.1007/s40519-013-0056-5
- ↑ Tornberg, Å. B., Melin, A., Koivula, F. M., Johansson, A., Skouby, S., Faber, J., & Sjödin, A. (2017). Reduced neu- romuscular performance in amenorrheic elite endurance athletes. Medicine and Science in Sports and Exercise, 49(12), 2478–2485.
- ↑ Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A, Ackerman K. RED-S CAT. Relative Energy Deficiency in Sport (RED-S) Clinical Assessment Tool (CAT). Br J Sports Med. 2015 Apr;49(7):421-3. doi: 10.1136/bjsports-2015-094873. PMID: 25896450.
- ↑ Melin A, Tornberg ÅB, Skouby S, et al. The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. British Journal of Sports Medicine 2014;48:540-545.
- ↑ 31.0 31.1 Burke LM, Close GL, Lundy B, Mooses M, Morton JP, Tenforde AS. Relative Energy Deficiency in Sport in Male Athletes: A Commentary on Its Presentation Among Selected Groups of Male Athletes. Int J Sport Nutr Exerc Metab. 2018 Jul 1;28(4):364-374. doi: 10.1123/ijsnem.2018-0182. Epub 2018 Jul 24. PMID: 30040508.
- ↑ Sim, A., Burns, S.F. Review: questionnaires as measures for low energy availability (LEA) and relative energy deficiency in sport (RED-S) in athletes. J Eat Disord 9, 41 (2021). https://doi.org/10.1186/s40337-021-00396-7
- ↑ Martyn-St James M, Carroll S. Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. Journal of bone and mineral metabolism. 2010 May 1;28(3):251-67.