Int J Sports Med 2023; 44(04): 236-246
DOI: 10.1055/a-1947-3174
Review

Relative Energy Deficiency in Sport (RED-S) in Adolescents – A Practical Review

1   Oxsport, Oxford University Hospitals NHS Foundation Trust, Oxford, United Kingdom of Great Britain and Northern Ireland
,
1   Oxsport, Oxford University Hospitals NHS Foundation Trust, Oxford, United Kingdom of Great Britain and Northern Ireland
,
Julia L Newton
1   Oxsport, Oxford University Hospitals NHS Foundation Trust, Oxford, United Kingdom of Great Britain and Northern Ireland
› Author Affiliations

Abstract

There are many immediate and longer-term physical, psychological and metabolic benefits of being active during adolescence. These benefits exist when exercise and physical activity are undertaken in a state of energy balance. When exercise occurs in an environment of low energy availability, this is currently termed relative energy deficiency in sport and there are potential significant negative effects on mental well-being, bone, endocrine and metabolic health. Therefore, relative energy deficiency in sport may present to many different specialists or allied health professionals depending upon the symptoms or reasons for seeking help, which include injury, such as bone stress or soft tissue problems, irregular or absent menstruation, stress, anxiety or low mood, or sporting underperformance as examples. The promotion of physical activity in adolescence is a critical part of public health strategy. In parallel with this positive public health message, there needs to be an increase in the awareness of, and education about, relative energy deficiency in sport for those working with and looking after adolescents.This review provides an up to date, practical evidenced based guide on the recognition, investigation and management of relative energy deficiency in sport in the adolescent, both male and female.



Publication History

Received: 15 November 2021

Accepted: 15 September 2022

Accepted Manuscript online:
19 September 2022

Article published online:
02 December 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Mountjoy M, Sundgot-Borgen J, Burke L. et al. The IOC consensus statement: Beyond the female athlete triad-relative energy deficiency in sport (RED-S). Br J Sports Med 2014; 48: 491-497
  • 2 Mountjoy M, Sundgot-Borgen JK, Burke LM. et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med 2018; 52: 687-697
  • 3 Nattiv A, De Souza MJ, Koltun KJ. et al. The Male Athlete Triad – A consensus statement from the female and male athlete triad coalition Part 1: Definition and Scientific Basis. Clin J Sport Med 2021; 31: 335-348
  • 4 Fredericson M, Kussman A, Misra M. et al. The Male Athlete Triad – A consensus statement from the female and male athlete triad coalition Part II: Diagnosis, Treatment, and Return-To-Play. Clin J Sport Med 2021; 31: 349-366
  • 5 Loucks AB. Energy balance and body composition in sports and exercise. J Sports Sci 2004; 22: 1-14
  • 6 Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003; 88: 297-311
  • 7 Holtzman B, Ackerman KE. Measurement, determinants, and implications of energy intake in athletes. Nutrients 2019; 11: 1-13
  • 8 Das JK, Salam RA, Thornburg KL. et al. Nutrition in adolescents: physiology, metabolism, and nutritional needs. Ann N Y Acad Sci 2017; 1393: 21-33
  • 9 World Health Organization. Adolescent Health https://www.who.int/health-topics/adolescent-health accessed 1 Sep 2021
  • 10 García-Hermoso A, Ramírez-Vélez R, Saavedra JM. Exercise, health outcomes, and pædiatric obesity: A systematic review of meta-analyses. J Sci Med Sport 2019; 22: 76-84
  • 11 Ravi S, Kujala UM, Tammelin TH. et al. Adolescent sport participation and age at menarche in relation to midlife body composition, bone mineral density, fitness, and physical activity. J Clin Med 2020; 9: 3797
  • 12 Kalabiska I, Zsakai A, Malina RM. et al. Bone mineral reference values for athletes 11 to 20 years of age. Int J Environ Res Public Health 2020; 17: 4930
  • 13 Pasqualini L, Leli C, Ministrini S. et al. Relationships between global physical activity and bone mineral density in a group of male and female students. J Sports Med Phys Fitness 2017; 57: 238-243
  • 14 Rodriguez-Ayllon M, Cadenas-Sánchez C, Estévez-López F. et al. Role of physical activity and sedentary behavior in the mental health of preschoolers, children and adolescents: A systematic review and meta-analysis. Sports Med 2019; 49: 1383-1410
  • 15 Meng K, Qiu J, Benardot D. et al. The risk of low energy availability in Chinese elite and recreational female aesthetic sports athletes. J Int Soc Sports Nutr 2020; 17: 13
  • 16 Sawai A, Mathis BJ, Natsui H. et al. Risk of female athlete triad development in Japanese collegiate athletes is related to sport type and competitive level. Int J Womens Health 2018; 10: 671-687
  • 17 Rogers MA, Appaneal RN, Hughes D. et al. Prevalence of impaired physiological function consistent with Relative Energy Deficiency in Sport (RED-S): An Australian elite and pre-elite cohort. Br J Sports Med 2021; 55: 38-45
  • 18 Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc 2013; 45: 985-996
  • 19 Burke LM, Close GL, Lundy B. et al. 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; 28: 364-374
  • 20 Berkovich BE, Eliakim A, Nemet D. et al. Rapid weight loss among adolescents participating in competitive judo. Int J Sport Nutr Exerc Metab 2016; 26: 276-284
  • 21 Koehler K, Achtzehn S, Braun H. et al. Comparison of self-reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. Appl Physiol Nutr Metab 2013; 38: 725-733
  • 22 Lee S, Kuniko M, Han S. et al. Association of low energy availability and suppressed metabolic status in Korean male collegiate soccer players: A pilot study. Am J Mens Health 2020; 14 DOI: 10.1177/1557988320982186.
  • 23 Brown KN, Wengreen HJ, Beals KA. Knowledge of the female athlete triad, and prevalence of triad risk factors among female high school athletes and their coaches. J Pediatr Adolesc Gynecol 2014; 27: 278-282
  • 24 Tosi M, Maslyanskaya S, Dodson NA. et al. The Female Athlete Triad: A comparison of knowledge and risk in adolescent and young adult figure skaters, dancers, and runners. J Pediatr Adolesc Gynecol 2019; 32: 165-169
  • 25 Feldmann JM, Belsha JP, Eissa MA. et al. Female adolescent athletes’ awareness of the connection between menstrual status and bone health. J Pediatr Adolesc Gynecol 2011; 24: 311-314
  • 26 Armento A, VanBaak K, Seehusen CN. et al. Presence and perceptions of menstrual dysfunction and associated quality of life measures among high school female athletes. J Athl Train 2021; 56: 1094-1099
  • 27 Carson TL, Tournat T, Sonneville K. et al. Cultural and environmental associations with body image, diet and well-being in NCAA DI female distance runners: a qualitative analysis. Br J Sports Med 2021; 55: 433-437
  • 28 Pantano KJ. Knowledge, attitude, and skill of high school coaches with regard to the female athlete triad. J Pediatr Adolesc Gynecol 2017; 30: 540-545
  • 29 Mukherjee S, Chand V, Wong XX. et al. Perceptions, awareness and knowledge of the Female Athlete Triad amongst coaches – Are we meeting the expectations for athlete safety?. Int J Sports Sci Coach 2016; 11: 545-551
  • 30 Kroshus E, Sherman RT, Thompson RA. et al. Gender differences in high school coaches’ knowledge, attitudes, and communication about the female athlete triad. Eat Disord 2014; 22: 193-208
  • 31 Troy K, Hoch AZ, Stavrakos JE. Awareness and comfort in treating the Female Athlete Triad: Are we failing our athletes?. Wis Med J 2006; 105: 21-24
  • 32 Kroshus E, DeFreese JD, Kerr ZY. Collegiate athletic trainers’ knowledge of the female athlete triad and relative energy deficiency in sport. J Athl Train 2018; 53: 51-59
  • 33 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 2020; 6: 44
  • 34 Hamer J, Desbrow B, Irwin C. Are coaches of female athletes informed of relative energy deficiency in sport? A scoping review. Women Sport Phys Act J 2021; 29: 38-46
  • 35 Mountjoy M, Costa A, Budgett R. et al. Health promotion through sport: International sport federations’ priorities, actions and opportunities. Br J Sports Med 2018; 52: 54-60
  • 36 Curry EJ, Logan C, Ackerman K. et al. Female athlete triad awareness among multispecialty physicians. Sports Med Open 2015; 1: 38
  • 37 Tenforde AS, Beauchesne AR, Borg-Stein J. et al. Awareness and comfort treating the female athlete triad and relative energy deficency in sport among healthcare providers. Dtsch Z Sportmed 2020; 71: 76-80
  • 38 Kroshus E, Fischer AN, Nichols JF. Assessing the awareness and behaviors of U.S. high school nurses with respect to the female athlete triad. J Sch Nurs 2015; 31: 272-279
  • 39 American College of Obstetricians and Gynecologists.. Menstruation in girls and adolescents: Using the menstrual cycle as a vital sign. Obstet Gynecol 2015; 126: e143-6
  • 40 National Institute for Health and Care Excellence. Amenorrhoea (2022). https://cks.nice.org.uk/topics/amenorrhoea/; (accessed 1 Mar 2022)
  • 41 Solnik M. BMJ Best Practice: Assessment of primary amenorrhoea. 2018 https://bestpractice.bmj.com/topics/en-gb/1101; accessed 1 Sep 2021
  • 42 Solnik M. BMJ Best Practice: Assessment of secondary amenorrhoea. 2018 https://bestpractice.bmj.com/topics/en-gb/1102 accessed 1 Sep 2021
  • 43 Gibson MES, Fleming N, Zuijdwijk C. et al. Where have the periods gone? The evaluation and management of functional hypothalamic amenorrhea. J Clin Res Pediatr Endocrinol 2020; 12: 18-27
  • 44 Golden NH, Carlson JL. The pathophysiology of amenorrhea in the adolescent. Ann N Y Acad Sci 2008; 1135: 163-178
  • 45 Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985) 1998; 84: 37-46
  • 46 Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003; 88: 297-311
  • 47 Lieberman J, De Souze M, Wagstaff D. et al. Menstrual disruption with exercise is not linked to an energy availability threshold. Med Sci Sports Exerc 2018; 50: 551-561
  • 48 Odén A, McCloskey EV, Kanis JA. et al. Burden of high fracture probability worldwide: secular increases 2010–2040. Osteoporos Int 2015; 26: 2243-2248
  • 49 Whiting SJ, Vatanparast H, Baxter-Jones A. et al. Factors that affect bone mineral accrual in the adolescent growth spurt. J Nutr 2004; 134: 696-700
  • 50 Goolsby MA, Boniquit N. Bone health in athletes: The role of exercise, nutrition, and hormones. Sports Health 2017; 9: 108-117
  • 51 Wiksten-Almströmer M, Hirschberg AL, Hagenfeldt K. Reduced bone mineral density in adult women diagnosed with menstrual disorders during adolescence. Acta Obstet Gynecol Scand 2009; 88: 543-549
  • 52 Berz K, McCambridge T. Amenorrhea in the female athlete: What to do and when to worry. Pediatr Ann 2016; 45: e97-e102
  • 53 Nieves JW, Ruffing JA, Zion M. et al. Eating disorders, menstrual dysfunction, weight change and DMPA use predict bone density change in college-aged women. Bone 2016; 84: 113-119
  • 54 Nose-Ogura S, Yoshino O, Dohi M. et al. Low bone mineral density in elite female athletes with a history of secondary amenorrhea in their teens. Clin J Sport Med 2020; 30: 245-250
  • 55 Patel H, Sammut L, Denison H. et al. The relationship between non-elite sporting activity and calcaneal bone density in adolescents and young adults: A narrative systematic review. Front Physiol 2020; 11: 167
  • 56 Kopiczko A, Adamczyk JG, Łopuszańska-Dawid M. Bone mineral density in adolescent boys: Cross-sectional observational study. Int J Environ Res Public Health 2020; 18: 245
  • 57 Sagayama H, Kondo E, Tanabe Y. et al. Bone mineral density in male weight-classified athletes is higher than that in male endurance-athletes and non-athletes. Clin Nutr ESPEN 2020; 36: 106-110
  • 58 Ikedo A, Ishibashi A, Matsumiya S. et al. Comparison of site-specific bone mineral densities between endurance runners and sprinters in adolescent women. Nutrients 2016; 8: 781
  • 59 Rauh MJ, Tenforde AS, Barrack MT. et al. Sport specialization and low bone mineral density in female high school distance runners. J Athl Train 2020; 55: 1239-1246
  • 60 Barrack MT, Fredericson M, Tenforde AS. et al. Evidence of a cumulative effect for risk factors predicting low bone mass among male adolescent athletes. Br J Sports Med 2017; 51: 200-205
  • 61 Jackson KA, Sanchez-Santos MT, MacKinnon AL. et al. Bone density and body composition in newly licenced professional jockeys. Osteoporos Int 2017; 28: 2675-2682
  • 62 Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab 2000; 278: E43-E49
  • 63 Elliott-Sale KJ, Tenforde AS, Parziale AL. et al. Endocrine effects of relative energy deficiency in sport. Int J Sports Nutr Exerc Metab 2018; 28: 335-349
  • 64 Kluge M, Schüssler P, Schmidt D. et al. Ghrelin suppresses secretion of Luteinizing Hormone (LH) and Follicle-Stimulating Hormone (FSH) in women. J Clin Endocrinol Metab 2012; 97: 448-451
  • 65 Ackerman KE, Slusarz K, Guereca G. et al. Higher ghrelin and lower leptin secretion are associated with lower LH secretion in young amenorrheic athletes compared with eumenorrheic athletes and controls. Am J Physiol Endocrinol Metab 2012; 302: E800-E806
  • 66 Christo K, Cord J, Mendes N. et al. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study. Clin Endocrinol 2008; 69: 628-633
  • 67 Dipla K, Kraemer RR, Constantini NW. et al. Relative energy deficiency in sports (RED-S): elucidation of endocrine changes affecting the health of males and females. Hormones 2021; 20: 35-47
  • 68 McGuire A, Warrington G, Doyle L. Low energy availability in male athletes: A systematic review of incidence, associations, and effects. Transl Sports Med 2020; 3: 173-187
  • 69 Narla A, Kaiser K, Tannock LR. Extremely low testosterone due to relative energy deficiency in sport: A case report. AACE Clin Case Rep 2018; 5: e129-e131
  • 70 Mancine R, Kennedy S, Stephan P. et al. Disordered eating and eating disorders in adolescent athletes. Spartan Med Res J 2020; 4: 11595
  • 71 Bomba M, Corbetta F, Bonini L. et al. Psychopathological traits of adolescents with functional hypothalamic amenorrhea: A comparison with anorexia nervosa. Eat Weight Disord 2014; 19: 41-48
  • 72 Ackerman KE, Holtzman B, Cooper KM. et al. Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport. Br J Sports Med 2019; 53: 628-633
  • 73 Silva MRG, Paiva T. Poor precompetitive sleep habits, nutrients’ deficiencies, inappropriate body composition and athletic performance in elite gymnasts. Eur J Sport Sci 2016; 16: 726-735
  • 74 Tornberg ÅB, Melin A, Koivula FM. et al. Reduced neuromuscular performance in amenorrheic elite endurance athletes. Med Sci Sports Exerc 2017; 49: 2478-2485
  • 75 Vanheest JL, Rodgers CD, Mahoney CE. et al. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc 2014; 46: 156-166
  • 76 Patel DR, Yamasaki A, Brown K. Epidemiology of sports-related musculoskeletal injuries in young athletes in United States. Transl Pediatr 2017; 6: 160-166
  • 77 Prieto-González P, Martínez-Castillo JL, Fernández-Galván LM. et al. Epidemiology of sports-related injuries and associated risk factors in adolescent athletes: An injury surveillance. Int J Environ Res Public Health 2021; 18: 4857
  • 78 Gram MCD, Clarsen B, Bø K. Injuries and illnesses among competitive Norwegian rhythmic gymnasts during preseason: a prospective cohort study of prevalence, incidence and risk factors. Br J Sports Med 2021; 55: 231-236
  • 79 Scheid JL, Stefanik ME. Drive for thinness predicts musculoskeletal injuries in division II NCAA female athletes. J Funct Morphol Kinesiol 2019; 4: 52
  • 80 Thein-Nissenbaum JM, Rauh MJ, Carr KE. et al. Associations between disordered eating, menstrual dysfunction, and musculoskeletal injury among high school athletes. J Orthop Sports Phys Ther 2011; 41: 60-69
  • 81 Fedewa MV, Bentley JL, Higgins S. et al. Celiac disease and bone health in children and adolescents: A systematic review and meta-analysis. J Clin Densitom 2020; 23: 200-211
  • 82 Smith R, Baldock J, FitzPatrick M. et al. Incidence of undiagnosed celiac disease presenting as bone stress injuries to a sport and exercise medicine clinic. Clin J Sport Med 2021; 31: e306-e312
  • 83 Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013; 45: 1188-1197
  • 84 National Institute for Health and Care Excellence (NICE 2020). Eating disorders: recognition and treatment [NG69]. https://www.nice.org.uk/guidance/NG69; (accessed 1 Sep 2021)
  • 85 Sim A, Burns SF. Review: questionnaires as measures for low energy availability (LEA) and relative energy deficiency in sport (RED-S) in athletes. J Eat Disord 2021; 9: 41
  • 86 Gibbs JC, Williams NI, Scheid JL. et al. The association of a high drive for thinness with energy deficiency and severe menstrual disturbances: Confirmation in a large population of exercising women. Int J Sport Nutr Exerc Metab 2011; 21: 280-290
  • 87 Smith KE, Mason TB, Murray SB. et al. Male clinical norms and sex differences on the Eating Disorder Inventory (EDI) and Eating Disorder Examination Questionnaire (EDE-Q). Int J Eat Disord 2017; 50: 769-775
  • 88 De Souza MJ, Nattiv A, Joy E. et al. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med 2014; 48: 289
  • 89 Ackerman KE, Stellingwerff T, Elliott-Sale KJ. et al. #REDS (Relative Energy Deficiency in Sport): Time for a revolution in sports culture and systems to improve athlete health and performance. Br J Sports Med 2020; 54: 2019-2021
  • 90 Gordon CM, Ackerman KE, Berga SL. et al. Functional hypothalamic amenorrhea: An endocrine society clinical practice guideline. J Clin Endocrinol Metab 2017; 102: 1413-1439
  • 91 Desbrow B, Cox G, Desbrow B. et al. Sports Dietitians Australia Position Statement : Sports nutrition for the adolescent athlete. Int J Sport Nutr Exerc Metab 2014; 24: 570-584
  • 92 Brown KN, Wengreen HJ, Beals KA. et al. Effects of peer-education on knowledge of the female athlete triad among high school track and field athletes: A pilot study. Women Sports Phys Act J 2016; 24: 1-6
  • 93 Krick RL, Brown AF, Brown KN. Increased female athlete triad knowledge following a brief video educational intervention. J Nutr Educ Behav 2019; 51: 1126-1129
  • 94 Subasinghe AK, Garland SM, Gorelik A. et al. Using mobile technology to improve bone-related lifestyle risk factors in young women with low bone mineral density: feasibility randomized controlled trial. JMIR Form Res 2019; 3: e9435
  • 95 Stewart TM, Pollard T, Hildebrandt T. et al. The Female Athlete Body project study: 18-month outcomes in eating disorder symptoms and risk factors. Int J Eat Disord 2019; 52: 1291-1300
  • 96 Keay N, Francis G, Entwistle I. et al. Clinical evaluation of education relating to nutrition and skeletal loading in competitive male road cyclists at risk of relative energy deficiency in sports (RED-S): 6-month randomised controlled trial. BMJ Open Sport Exerc Med 2019; 5: e000523
  • 97 Cialdella-Kam L, Guebels CP, Maddalozzo GF. et al. Dietary intervention restored menses in female athletes with exercise-associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients 2014; 6: 3018-3039
  • 98 Mallinson RJ, Williams NI, Olmsted MP. et al. A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr 2013; 10: 34
  • 99 Kuikman M, Mountjoy M, Stellingwerff T. et al. A review of nonpharmacological strategies in the treatment of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab 2021; 31: 268-275
  • 100 Hammond KM, Sale C, Fraser W. et al. Post-exercise carbohydrate and energy availability induce independent effects on skeletal muscle cell signalling and bone turnover: implications for training adaptation. J Physiol 2019; 597: 4779-4796
  • 101 Upadhyay J, Farr OM, Mantzoros CS. The role of leptin in regulating bone metabolism. Metabolism 2015; 64: 105-113
  • 102 Wells KR, Jeacocke NA, Appaneal R. et al. The Australian Institute of Sport (AIS) and National Eating Disorders Collaboration (NEDC) position statement on disordered eating in high performance sport. Br J Sports Med 2020; 54: 1247-1258
  • 103 Smith TJ, Tripkovic L, Lanham-New SA. et al. Vitamin D in adolescence: Evidence-based dietary requirements and implications for public health policy. Proc Nutr Soc 2018; 77: 292-301
  • 104 Taylor SN. Vitamin D in toddlers, preschool children, and adolescents. Ann Nutr Metab 2020; 76: 30-41
  • 105 Amrein K, Scherkl M, Hoffmann M. et al. Vitamin D deficiency 2.0: an update on the current status worldwide. Eur J Clin Nutr 2020; 74: 1498-1513
  • 106 Ackerman KE, Singhal V, Baskaran C. et al. Oestrogen replacement improves bone mineral density in oligo-amenorrhoeic athletes: A randomised clinical trial. Br J Sports Med 2019; 53: 229-236
  • 107 Nose-Ogura S, Yoshino O, Kanatani M. et al. Effect of transdermal estradiol therapy on bone mineral density of amenorrheic female athletes. Scand J Med Sci Sports 2020; 30: 1379-1386
  • 108 Petkus DL, Murray-Kolb LE, De Souza MJ. The unexplored crossroads of the female athlete triad and iron deficiency: A narrative review. Sports Med 2017; 47: 1721-1737
  • 109 Perez-Lopez FR, Perez-Roncero G, Lopez-Baena MT. Vitamin D and adolescent health. Adolesc Health Med Ther 2010; 1: 1-8
  • 110 Shuhart CR, Yeap SS, Anderson PA. et al. Executive summary of the 2019 ISCD position development conference on monitoring treatment, DXA cross-calibration and least significant change, spinal cord injury, peri-prosthetic and orthopedic bone health, transgender medicine, and pediatrics. J Clin Densitom 2019; 22: 453-471