The IOC consensus statement: beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S)

Protecting the health of the athlete is a goal of the International Olympic Committee (IOC). The IOC convened an expert panel to update the 2005 IOC Consensus Statement on the Female Athlete Triad. This Consensus Statement replaces the previous and provides guidelines to guide risk assessment, treatment and return-to-play decisions. The IOC expert working group introduces a broader, more comprehensive term for the condition previously known as ‘Female Athlete Triad’. The term ‘Relative Energy Deficiency in Sport’ (RED-S), points to the complexity involved and the fact that male athletes are also affected. The syndrome of RED-S refers to impaired physiological function including, but not limited to, metabolic rate, menstrual function, bone health, immunity, protein synthesis, cardiovascular health caused by relative energy deficiency. The cause of this syndrome is energy deficiency relative to the balance between dietary energy intake and energy expenditure required for health and activities of daily living, growth and sporting activities. Psychological consequences can either precede RED-S or be the result of RED-S. The clinical phenomenon is not a ‘triad’ of the three entities of energy availability, menstrual function and bone health, but rather a syndrome that affects many aspects of physiological function, health and athletic performance. This Consensus Statement also recommends practical clinical models for the management of affected athletes. The ‘Sport Risk Assessment and Return to Play Model’ categorises the syndrome into three groups and translates these classifications into clinical recommendations.

[1]  M. Pollock,et al.  Practical Assessment of Body Composition. , 1985, The Physician and sportsmedicine.

[2]  J. Skinner,et al.  Treatment of athletic amenorrhea with a diet and training intervention program. , 1996, International journal of sport nutrition.

[3]  C. Gordon,et al.  Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. , 2011, The Journal of clinical endocrinology and metabolism.

[4]  B. Sonntag,et al.  An integrated view on the luteal phase: diagnosis and treatment in subfertility , 2012, Clinical endocrinology.

[5]  D. Rhea Eating disorder behaviors of ethnically diverse urban female adolescent athletes and non-athletes. , 1999, Journal of adolescence.

[6]  J. Compston,et al.  The localization of androgen receptors in human bone. , 1997, The Journal of clinical endocrinology and metabolism.

[7]  J. Johnston,et al.  Does Physical Activity in Adolescence Have Site‐Specific and Sex‐Specific Benefits on Young Adult Bone Size, Content, and Estimated Strength? , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[8]  B. Poh,et al.  The female athlete triad among elite Malaysian athletes: prevalence and associated factors. , 2009, Asia Pacific journal of clinical nutrition.

[9]  F. Greenway,et al.  Endocrine and nutritional management of the post-bariatric surgery patient: an Endocrine Society Clinical Practice Guideline. , 2010, The Journal of clinical endocrinology and metabolism.

[10]  C. Christiansen,et al.  Low bone mass and high bone turnover in male long distance runners. , 1993, The Journal of clinical endocrinology and metabolism.

[11]  A. Volpe,et al.  Recombinant human leptin in women with hypothalamic amenorrhea. , 2004, The New England journal of medicine.

[12]  G. Matheson,et al.  2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad , 2014, Current sports medicine reports.

[13]  T. Wimmer,et al.  Progesterone and bone: a closer link than previously realized , 2012, Climacteric : the journal of the International Menopause Society.

[14]  G. Summers,et al.  Risk factors for stress fracture in female endurance athletes: a cross-sectional study , 2012, BMJ Open.

[15]  G. Vicente-Rodríguez How does Exercise Affect Bone Development during Growth? , 2006, Sports medicine.

[16]  B. Kitchin Nutrition counseling for patients with osteoporosis: a personal approach. , 2013, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[17]  C. Fairburn Cognitive Behavior Therapy and Eating Disorders , 2008 .

[18]  T. Kubo,et al.  A displaced stress fracture of the femoral neck in an adolescent female distance runner with female athlete triad: A case report , 2010, Sports medicine, arthroscopy, rehabilitation, therapy & technology : SMARTT.

[19]  M. Goldstein,et al.  Weight gain and restoration of menses as predictors of bone mineral density change in adolescent girls with anorexia nervosa-1. , 2008, The Journal of clinical endocrinology and metabolism.

[20]  Juli E Jones,et al.  Neuroendocrinology of nutritional infertility. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[21]  M. Bemben,et al.  Bone density comparisons in male competitive road cyclists and untrained controls. , 2009, Medicine and science in sports and exercise.

[22]  T. Lohman,et al.  How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the Ad Hoc Research Working Group on Body Composition, Health and Performance, under the auspices of the IOC Medical Commission , 2013, British Journal of Sports Medicine.

[23]  M. Fredericson,et al.  Normalization of bone density in a previously amenorrheic runner with osteoporosis. , 2005, Medicine and science in sports and exercise.

[24]  D. Bailey,et al.  Bone mineral accrual from 8 to 30 years of age: An estimation of peak bone mass , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[25]  S. Grinspoon,et al.  Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in women with hypothalamic amenorrhea and osteopenia: an open-label extension of a double-blind, placebo-controlled study. , 2005, Contraception.

[26]  A. Baum Eating Disorders in the Male Athlete , 2006, Sports medicine.

[27]  S. Cremers,et al.  Prolonged bisphosphonate release after treatment in children. , 2007, The New England journal of medicine.

[28]  K. Wurster [Menstrual disorders in athletes]. , 1998, Therapeutische Umschau. Revue therapeutique.

[29]  M. Rauh,et al.  Associations between disordered eating, menstrual dysfunction, and musculoskeletal injury among high school athletes. , 2011, The Journal of orthopaedic and sports physical therapy.

[30]  M. Fredericson,et al.  Influence of Sports Participation on Bone Health in the Young Athlete: A Review of the Literature , 2011, PM & R : the journal of injury, function, and rehabilitation.

[31]  K. Ackerman,et al.  Bone Health and the Female Athlete Triad in Adolescent Athletes , 2011, The Physician and sportsmedicine.

[32]  Anne B Loucks,et al.  Dose‐Response Relationships Between Energy Availability and Bone Turnover in Young Exercising Women , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[33]  J. Marini Do bisphosphonates make children's bones better or brittle? , 2003, The New England journal of medicine.

[34]  P. Ebeling,et al.  Treatment of osteoporosis in men with bisphosphonates: rationale and latest evidence , 2013, Therapeutic advances in musculoskeletal disease.

[35]  J. Rumball,et al.  Use of the Preparticipation Physical Examination Form to Screen for the Female Athlete Triad in Canadian Interuniversity Sport Universities , 2005, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[36]  E. Stice,et al.  Future Directions in Etiologic, Prevention, and Treatment Research for Eating Disorders , 2012, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[37]  V. Goosey-Tolfrey,et al.  Nutritional practices of competitive British wheelchair games players. , 2010, Adapted physical activity quarterly : APAQ.

[38]  Laurel M. Wentz,et al.  Dietary and training predictors of stress fractures in female runners. , 2012, International journal of sport nutrition and exercise metabolism.

[39]  G. Matheson,et al.  Return-to-Play Decisions: Are They the Team Physician's Responsibility? , 2011, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[40]  K Sudi,et al.  Underweight in ski jumping: The solution of the problem. , 2006, International journal of sports medicine.

[41]  Arthur D. Stewart,et al.  Current Status of Body Composition Assessment in Sport , 2012, Sports Medicine.

[42]  L. Gai,et al.  Effect of depot medroxyprogesterone acetate on bone mineral density in adolescent women , 2013, Chinese medical journal.

[43]  F. Facchinetti,et al.  Psychoneuroendocrine correlates of secondary amenorrhea , 2003, Archives of Women's Mental Health.

[44]  M. Manore,et al.  Active women before/after an intervention designed to restore menstrual function: resting metabolic rate and comparison of four methods to quantify energy expenditure and energy availability. , 2014, International journal of sport nutrition and exercise metabolism.

[45]  R. Recker,et al.  The Impact of Lifestyle Factors on Stress Fractures in Female Army Recruits , 2001, Osteoporosis International.

[46]  A. Loucks Energy balance and body composition in sports and exercise , 2004, Journal of sports sciences.

[47]  G. Lovell Vitamin D Status of Females in an Elite Gymnastics Program , 2008, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[48]  P. J. Adams Hillard Menstruation in adolescents: what's normal? , 2008, Medscape journal of medicine.

[49]  A. McGoldrick,et al.  An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys , 2012, Journal of Bone and Mineral Metabolism.

[50]  J. Skinner,et al.  Energy and nutrient status of amenorrheic athletes participating in a diet and exercise training intervention program. , 1999, International journal of sport nutrition.

[51]  M. Barrack,et al.  Restoration of menses with nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. , 2012, International journal of sport nutrition and exercise metabolism.

[52]  G. Chodick,et al.  High Prevalence of Vitamin D Insufficiency in Athletes and Dancers , 2010, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[53]  L. Dai,et al.  Mechanisms of osteoporosis in spinal cord injury , 2006, Clinical endocrinology.

[54]  L. Jones,et al.  Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone, or placebo over 12 months. , 1997, American journal of obstetrics and gynecology.

[55]  M. Bouxsein,et al.  Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. , 2012, Bone.

[56]  M. Manore,et al.  Disorders of the female athlete triad among collegiate athletes. , 2002, International journal of sport nutrition and exercise metabolism.

[57]  M. McClung,et al.  Bone density recovery after depot medroxyprogesterone acetate injectable contraception use. , 2008, Contraception.

[58]  K. Briot,et al.  Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry. , 2013, Metabolism: clinical and experimental.

[59]  R. Dalle Grave,et al.  Marked increases in bone mineral density and biochemical markers of bone turnover in patients with anorexia nervosa gaining weight. , 2007, Bone.

[60]  K. Schenck-Gustafsson,et al.  Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. , 2005, The Journal of clinical endocrinology and metabolism.

[61]  Aurelia Nattiv,et al.  A Displaced Femoral Neck Stress Fracture in an Amenorrheic Adolescent Female Runner , 2012, Sports health.

[62]  J. Sundgot-Borgen,et al.  Higher prevalence of eating disorders among adolescent elite athletes than controls. , 2013, Medicine and science in sports and exercise.

[63]  D. Felsenberg,et al.  Detrimental effect of oral contraceptives on parameters of bone mass and geometry in a cohort of 248 young women. , 2007, Bone.

[64]  A. Stewart,et al.  Total and regional bone density in male runners, cyclists, and controls. , 2000, Medicine and science in sports and exercise.

[65]  L. Sutton,et al.  Body composition in sport, exercise and health , 2012 .

[66]  M. Michalopoulou,et al.  Physical activity is associated with bone geometry of premenarcheal girls in a dose-dependent manner. , 2013, Metabolism: clinical and experimental.

[67]  S. Abraham,et al.  Body weight, exercise and menstrual status among ballet dancers in training , 1982, British journal of obstetrics and gynaecology.

[68]  Aurelia Nattiv,et al.  The Female Athlete Triad , 2007, Mental Health in the Athlete.

[69]  J. Scheid,et al.  Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. , 2011, Bone.

[70]  I. Lambrinoudaki,et al.  Pathophysiology of bone loss in the female athlete , 2010, Annals of the New York Academy of Sciences.

[71]  Jing Fang,et al.  Variations in hip fracture hospitalization rates among different race/ethnicity groups in New York City. , 2004, Ethnicity & disease.

[72]  M. Blythe,et al.  Contraception and Adolescents , 2000, Pediatrics.

[73]  Michael Fredericson,et al.  Update on stress fractures in female athletes: epidemiology, treatment, and prevention , 2013, Current Reviews in Musculoskeletal Medicine.

[74]  A. Klibanski,et al.  Effects of recombinant human IGF-I and oral contraceptive administration on bone density in anorexia nervosa. , 2002, The Journal of clinical endocrinology and metabolism.

[75]  Aurelia Nattiv,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 , 2014, British Journal of Sports Medicine.

[76]  B. Drinkwater,et al.  Irreversible bone loss in former amenorrheic athletes , 1997, Osteoporosis International.

[77]  J. Nichols,et al.  Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. , 2007, Bone.

[78]  A. Rogol,et al.  Neuroendocrine alterations in the exercising human: implications for energy homeostasis. , 2013, Metabolism: clinical and experimental.

[79]  P. Hinton,et al.  Participation in road cycling vs running is associated with lower bone mineral density in men. , 2008, Metabolism: clinical and experimental.

[80]  A. Loucks,et al.  Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. , 1998, Journal of applied physiology.

[81]  A. Loucks,et al.  Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. , 2003, The Journal of clinical endocrinology and metabolism.

[82]  G. Matheson,et al.  The International Olympic Committee (IOC) Consensus Statement on periodic health evaluation of elite athletes March 2009 , 2009, British Journal of Sports Medicine.

[83]  J. Vescovi,et al.  Strategies to reverse bone loss in women with functional hypothalamic amenorrhea: a systematic review of the literature , 2008, Osteoporosis International.

[84]  Aurelia Nattiv,et al.  American College of Sports Medicine position stand. The female athlete triad. , 2007, Medicine and science in sports and exercise.

[85]  Mary T. Brinkoetter,et al.  Leptin is an effective treatment for hypothalamic amenorrhea , 2011, Proceedings of the National Academy of Sciences.

[86]  D. Richardson,et al.  Current Concept Review: Vitamin D and Stress Fractures , 2012, Foot & ankle international.

[87]  J. Vanheest,et al.  Ovarian suppression impairs sport performance in junior elite female swimmers. , 2014, Medicine and science in sports and exercise.

[88]  M. Olmsted,et al.  A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration , 2013, Journal of the International Society of Sports Nutrition.

[89]  J. A. Evans,et al.  Low lumbar spine bone mineral density in both male and female endurance runners. , 2006, Bone.

[90]  A. Klibanski,et al.  Bone health in anorexia nervosa , 2011, Current opinion in endocrinology, diabetes, and obesity.

[91]  P. Braverman,et al.  Menstruation in Girls and Adolescents: Using the Menstrual Cycle as a Vital Sign , 2016, Pediatrics.

[92]  A. Jeukendrup,et al.  Multiple transportable carbohydrates enhance gastric emptying and fluid delivery , 2010, Scandinavian journal of medicine & science in sports.

[93]  S. Boonen,et al.  Androgens and bone. , 2004, Calcified tissue international.

[94]  Ian Shrier,et al.  Return-to-Play in Sport: A Decision-based Model , 2010, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[95]  D. König,et al.  Energy Intake and Energy Expenditure of Elite Cyclists During Preseason Training , 2005, International journal of sports medicine.

[96]  M. K. Torstveit,et al.  Aspects of disordered eating continuum in elite high‐intensity sports , 2010, Scandinavian journal of medicine & science in sports.

[97]  A. Hackney,et al.  Effects of endurance exercise on the reproductive system of men: The “exercise-hypogonadal male condition” , 2008, Journal of endocrinological investigation.

[98]  R. Marx,et al.  Stress Fracture Sites Related to Underlying Bone Health in Athletic Females , 2001, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[99]  W. Martinson Eating disorders in sport , 2011 .

[100]  Mary T. Brinkoetter,et al.  Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women. , 2011, Metabolism: clinical and experimental.

[101]  M. Goldstein,et al.  Effects of rhIGF-1 administration on surrogate markers of bone turnover in adolescents with anorexia nervosa. , 2009, Bone.

[102]  A. Nattiv Stress fractures and bone health in track and field athletes. , 2000, Journal of science and medicine in sport.

[103]  James E Mitchell,et al.  Biological therapies for eating disorders. , 2013, The International journal of eating disorders.

[104]  K. Fasting,et al.  International Olympic Committee , 2008, Permanent Missions to the United Nations No.301.

[105]  Jacques P. Brown,et al.  Standards and guidelines for performing central dual-energy x-ray absorptiometry in premenopausal women, men, and children. , 2004, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[106]  P. Fischer,et al.  Female athlete triad and its components: toward improved screening and management. , 2013, Mayo Clinic proceedings.

[107]  J. Kelsey,et al.  The effect of oral contraceptives on bone mass and stress fractures in female runners. , 2007, Medicine and science in sports and exercise.

[108]  B. Kiens,et al.  Energy availability in athletes , 2011, Journal of sports sciences.

[109]  R. Ferber,et al.  Bone quality and muscle strength in female athletes with lower limb stress fractures. , 2011, Medicine and science in sports and exercise.

[110]  L. Bachrach,et al.  Clinical Report — Bone Densitometry in Children and Adolescents , 2010 .

[111]  I. Holme,et al.  The development of the brief eating disorder in athletes questionnaire. , 2014, Medicine and science in sports and exercise.

[112]  Kristin L. Sainani,et al.  Identifying sex-specific risk factors for stress fractures in adolescent runners. , 2013, Medicine and science in sports and exercise.

[113]  Hangyuan Guo Retraction: Guo H. Complication of central venous catheterization. N Engl J Med 2007; 356: e2. , 2007, The New England journal of medicine.

[114]  T. Stellingwerff,et al.  Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis , 2013, The Journal of physiology.

[115]  S. West,et al.  High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. , 2010, Human reproduction.

[116]  B L Drinkwater,et al.  Bone mineral density after resumption of menses in amenorrheic athletes. , 1986, JAMA.

[117]  A. Hirschberg,et al.  Special Attention to the Weight-Control Strategies Employed by Olympic Athletes Striving for Leanness Is Required , 2008, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[118]  E. Seeman,et al.  Osteoporosis in Men , 1999, Osteoporosis International.

[119]  D. Chappard,et al.  Evaluation of the bone status in high-level cyclists. , 2012, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[120]  C. Ohlsson,et al.  Sex steroid metabolism in the regulation of bone health in men , 2010, The Journal of Steroid Biochemistry and Molecular Biology.

[121]  C. Ferrand,et al.  Perfectionism and Risk for Disordered Eating among Young French Male Cyclists of High Performance , 2004, Perceptual and motor skills.

[122]  J. Nichols,et al.  Low bone mineral density in highly trained male master cyclists , 2003, Osteoporosis International.

[123]  E. Eriksen,et al.  New developments in the treatment of osteoporosis , 2013, Acta obstetricia et gynecologica Scandinavica.

[124]  T Dusek,et al.  Influence of high intensity training on menstrual cycle disorders in athletes. , 2001, Croatian medical journal.

[125]  A. Hoch,et al.  Female Athlete Triad Screening in National Collegiate Athletic Association Division I Athletes: Is the Preparticipation Evaluation Form Effective? , 2012, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[126]  P T Ellison,et al.  Moderate recreational running is associated with lowered salivary progesterone profiles in women. , 1986, American journal of obstetrics and gynecology.

[127]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[128]  S. Kaptoge,et al.  Changes in bone mineral density, body composition and biochemical markers of bone turnover during weight gain in adolescents with severe anorexia nervosa: a 1-year prospective study , 2005, Osteoporosis International.

[129]  E. Canalis Update in new anabolic therapies for osteoporosis. , 2010, The Journal of clinical endocrinology and metabolism.

[130]  American Academy of Pediatrics Committee on Adolescence: Contraception and adolescents. , 1990, Pediatrics.

[131]  I. Reid,et al.  Effects of vitamin D supplements on bone mineral density: a systematic review and meta-analysis , 2014, The Lancet.

[132]  A. Loucks,et al.  Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. , 1994, The American journal of physiology.

[133]  K. Koehler,et al.  Comparison of self-reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. , 2013, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

[134]  S. Barr,et al.  Negative spinal bone mineral density changes and subclinical ovulatory disturbances--prospective data in healthy premenopausal women with regular menstrual cycles. , 2014, Epidemiologic reviews.

[135]  J. Reed,et al.  Changes in energy availability across the season in Division I female soccer players , 2013, Journal of sports sciences.

[136]  J. Nichols,et al.  Disordered eating among a multi-racial/ethnic sample of female high-school athletes. , 2006, Journal of Adolescent Health.