Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 83

The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.

Relative Energy Deficiency in Sport (REDs): Endocrine Manifestations, Pathophysiology and Treatments

Angelidi, Angeliki M, Stefanakis, Konstantinos, Chou, Sharon H, Valenzuela-Vallejo, Laura, Dipla, Konstantina, Boutari, Chrysoula, Ntoskas, Konstantinos, Tokmakidis, Panagiotis, Kokkinos, Alexander, Goulis, Dimitrios G, Papadaki, Helen A, Mantzoros, Christos S·2024·Endocrine Reviews
DOI 10.1210/endrev/bnae011
Open this paper in CoChat — free account

Abstract

Research on lean, energy-deficient athletic and military cohorts has broadened the concept of the Female Athlete Triad into the Relative Energy Deficiency in Sport (REDs) syndrome. REDs represents a spectrum of abnormalities induced by low energy availability (LEA), which serves as the underlying cause of all symptoms described within the REDs concept, affecting exercising populations of either biological sex. Both short- and long-term LEA, in conjunction with other moderating factors, may produce a multitude of maladaptive changes that impair various physiological systems and adversely affect health, well-being, and sport performance. Consequently, the comprehensive definition of REDs encompasses a broad spectrum of physiological sequelae and adverse clinical outcomes related to LEA, such as neuroendocrine, bone, immune, and hematological effects, ultimately resulting in compromised health and performance. In this review, we discuss the pathophysiology of REDs and associated disorders. We briefly examine current treatment recommendations for REDs, primarily focusing on nonpharmacological, behavioral, and lifestyle modifications that target its underlying cause-energy deficit. We also discuss treatment approaches aimed at managing symptoms, such as menstrual dysfunction and bone stress injuries, and explore potential novel treatments that target the underlying physiology, emphasizing the roles of leptin and the activin-follistatin-inhibin axis, the roles of which remain to be fully elucidated, in the pathophysiology and management of REDs. In the near future, novel therapies leveraging our emerging understanding of molecules and physiological axes underlying energy availability or lack thereof may restore LEA-related abnormalities, thus preventing and/or treating REDs-related health complications, such as stress fractures, and improving performance.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1210/endrev/bnae011

Cites

71 of 71 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 71 references

Research works printed but not linked: 323

  1. Areta, 2021, Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males, Eur J Appl Physiol, 121, 1, 10.1007/s00421-020-04516-0 · DOI · Paper page
  2. Burke, 2018, Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes, Int J Sport Nutr Exerc Metab, 28, 350, 10.1123/ijsnem.2018-0142 · DOI · Paper page
  3. Loucks, 2011, Energy availability in athletes, J Sports Sci, 29, S7, 10.1080/02640414.2011.588958 · DOI · Paper page
  4. Wade, 2004, Neuroendocrinology of nutritional infertility, Am J Physiol Regul Integr Comp Physiol, 287, R1277, 10.1152/ajpregu.00475.2004 · DOI · Paper page
  5. Burke, 2023, Mapping the complexities of Relative Energy Deficiency in Sport (REDs): development of a physiological model by a subgroup of the International Olympic Committee (IOC) Consensus on REDs, Br J Sports Med, 57, 1098, 10.1136/bjsports-2023-107335 · DOI · Paper page
  6. Nattiv, 2007, American College of Sports Medicine position stand. The female athlete triad, Med Sci Sports Exerc, 39, 1867
  7. Nattiv, 1994, The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis, Clin Sports Med, 13, 405, 10.1016/S0278-5919(20)30338-0 · DOI
  8. Otis, 1997, American College of Sports Medicine position stand. The female athlete triad, Med Sci Sports Exerc, 29, i, 10.1097/00005768-199705000-00037 · DOI · Paper page
  9. De Souza, 2014, 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, 48, 289, 10.1136/bjsports-2013-093218 · DOI · Paper page
  10. Hattori, 2022, Female athlete triad and male athlete triad syndrome induced by low energy availability: an animal model, Calcif Tissue Int, 111, 116, 10.1007/s00223-022-00983-z · DOI
  11. Hattori, 2014, Food restriction causes low bone strength and microarchitectural deterioration in exercised growing male rats, J Nutr Sci Vitaminol (Tokyo), 60, 35, 10.3177/jnsv.60.35 · DOI
  12. Stewart, 2000, Total and regional bone density in male runners, cyclists, and controls, Med Sci Sports Exerc, 32, 1373, 10.1097/00005768-200008000-00003 · DOI
  13. Kraus, 2019, Bone stress injuries in male distance runners: higher modified Female Athlete Triad Cumulative Risk Assessment scores predict increased rates of injury, Br J Sports Med, 53, 237, 10.1136/bjsports-2018-099861 · DOI
  14. Viner, 2015, Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density, Int J Sport Nutr Exerc Metab, 25, 594, 10.1123/ijsnem.2015-0073 · DOI · Paper page
  15. Hackney, 2005, Testosterone and endurance exercise: development of the “exercise-hypogonadal male condition”, Acta Physiol Hung, 92, 121, 10.1556/APhysiol.92.2005.2.3 · DOI
  16. O'Leary, 2020, Energy deficiency in soldiers: the risk of the athlete triad and relative energy deficiency in sport syndromes in the military, Front Nutr, 7, 142, 10.3389/fnut.2020.00142 · DOI
  17. Nattiv, 2021, 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, 31, 345
  18. Fredericson, 2021, 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, 31, 349, 10.1097/JSM.0000000000000948 · DOI · Paper page
  19. MacDougall, 1992, Relationship among running mileage, bone density, and serum testosterone in male runners, J Appl Physiol (1985), 73, 1165, 10.1152/jappl.1992.73.3.1165 · DOI
  20. Hattori, 2020, Comparison of bone mineral density between male long distance runners and non-athletes, J Run Sci, 31, 9
  21. Dipla, 2021, Relative energy deficiency in sports (RED-S): elucidation of endocrine changes affecting the health of males and females, Hormones (Athens), 20, 35, 10.1007/s42000-020-00214-w · DOI
  22. Rogers, 2021, 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, 55, 38, 10.1136/bjsports-2019-101517 · DOI · Paper page
  23. Mountjoy, 2018, IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update, Br J Sports Med, 52, 687, 10.1136/bjsports-2018-099193 · DOI · Paper page
  24. Elliott-Sale, 2018, Endocrine effects of relative energy deficiency in sport, Int J Sport Nutr Exerc Metab, 28, 335, 10.1123/ijsnem.2018-0127 · DOI · Paper page
  25. Williams, 2019, Female athlete triad and relative energy deficiency in sport: a focus on scientific rigor, Exerc Sport Sci Rev, 47, 197, 10.1249/JES.0000000000000200 · DOI
  26. Torstveit, 2019, Exercise dependence, eating disorder symptoms and biomarkers of Relative Energy Deficiency in Sports (RED-S) among male endurance athletes, BMJ Open Sport Exerc Med, 5, e000439, 10.1136/bmjsem-2018-000439 · DOI
  27. Boutari, 2020, The effect of underweight on female and male reproduction, Metabolism, 107, 154229, 10.1016/j.metabol.2020.154229 · DOI
  28. Zhang, 2017, Leptin function and regulation, Compr Physiol, 8, 351, 10.1002/cphy.c160041 · DOI
  29. Dardeno, 2010, Leptin in human physiology and therapeutics, Front Neuroendocrinol, 31, 377, 10.1016/j.yfrne.2010.06.002 · DOI · Paper page
  30. Mantzoros, 1999, The role of leptin in human obesity and disease: a review of current evidence, Ann Intern Med, 130, 671, 10.7326/0003-4819-130-8-199904200-00014 · DOI · Paper page
  31. Mantzoros, 1998, Leptin: in search of role(s) in human physiology and pathophysiology, Clin Endocrinol (Oxf), 49, 551, 10.1046/j.1365-2265.1998.00571.x · DOI
  32. Chan, 2003, The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men, J Clin Invest, 111, 1409, 10.1172/JCI200317490 · DOI · Paper page
  33. Perakakis, 2018, Regulation of the activins-follistatins-inhibins axis by energy status: impact on reproductive function, Metabolism, 85, 240, 10.1016/j.metabol.2018.05.003 · DOI
  34. Chan, 2006, Differential regulation of metabolic, neuroendocrine, and immune function by leptin in humans, Proc Natl Acad Sci U S A, 103, 8481, 10.1073/pnas.0505429103 · DOI · Paper page
  35. Chou, 2011, Leptin is an effective treatment for hypothalamic amenorrhea, Proc Natl Acad Sci U S A, 108, 6585, 10.1073/pnas.1015674108 · DOI · Paper page
  36. Nakamura, 2020, Two adipocytokines, leptin and adiponectin, independently predict osteoporotic fracture risk at different bone sites in postmenopausal women, Bone, 137, 115404, 10.1016/j.bone.2020.115404 · DOI
  37. Upadhyay, 2015, The role of leptin in regulating bone metabolism, Metabolism, 64, 105, 10.1016/j.metabol.2014.10.021 · DOI · Paper page
  38. Schett, 2004, Serum leptin level and the risk of nontraumatic fracture, Am J Med, 117, 952, 10.1016/j.amjmed.2004.07.044 · DOI
  39. Papageorgiou, 2018, Reduced energy availability: implications for bone health in physically active populations, Eur J Nutr, 57, 847, 10.1007/s00394-017-1498-8 · DOI · Paper page
  40. Perakakis, 2019, Follistatins in glucose regulation in healthy and obese individuals, Diabetes Obes Metab, 21, 683, 10.1111/dom.13572 · DOI
  41. Logue, 2018, Low energy availability in athletes: a review of prevalence, dietary patterns, physiological health, and sports performance, Sports Med, 48, 73, 10.1007/s40279-017-0790-3 · DOI · Paper page
  42. Loucks, 2003, Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women, J Clin Endocrinol Metab, 88, 297, 10.1210/jc.2002-020369 · DOI · Paper page
  43. Loucks, 1994, Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability, Am J Physiol, 266, R817
  44. Ihle, 2004, Dose-response relationships between energy availability and bone turnover in young exercising women, J Bone Miner Res, 19, 1231, 10.1359/JBMR.040410 · DOI · Paper page
  45. Lane, 2019, Prevalence of low energy availability in competitively trained male endurance athletes, Medicina (Kaunas), 55, 665, 10.3390/medicina55100665 · DOI · Paper page
  46. Lieberman, 2018, Menstrual disruption with exercise is not linked to an energy availability threshold, Med Sci Sports Exerc, 50, 551, 10.1249/MSS.0000000000001451 · DOI · Paper page
  47. Williams, 2015, Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction, Am J Physiol Endocrinol Metab, 308, E29, 10.1152/ajpendo.00386.2013 · DOI
  48. Kelesidis, 2010, Narrative review: the role of leptin in human physiology: emerging clinical applications, Ann Intern Med, 152, 93, 10.7326/0003-4819-152-2-201001190-00008 · DOI · Paper page
  49. Hilton, 2000, Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women, Am J Physiol Endocrinol Metab, 278, E43, 10.1152/ajpendo.2000.278.1.E43 · DOI · Paper page
  50. Shimizu, 2012, Mucosal immune function comparison between amenorrheic and eumenorrheic distance runners, J Strength Cond Res, 26, 1402, 10.1519/JSC.0b013e31822e7a6c · DOI
  51. Lieberman, 2013, Luteal phase defects induced by exercise and diet are associated with low energy availability, Med Sci Sports Exerc, 521
  52. Barrack, 2013, Update on the female athlete triad, Curr Rev Musculoskelet Med, 6, 195, 10.1007/s12178-013-9168-9 · DOI
  53. Woods, 2017, New approaches to determine fatigue in elite athletes during intensified training: resting metabolic rate and pacing profile, PLoS One, 12, e0173807, 10.1371/journal.pone.0173807 · DOI
  54. Nazem, 2012, The female athlete triad, Sports Health, 4, 302, 10.1177/1941738112439685 · DOI
  55. Papageorgiou, 2017, Effects of reduced energy availability on bone metabolism in women and men, Bone, 105, 191, 10.1016/j.bone.2017.08.019 · DOI · Paper page
  56. Burke, 2018, 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, 28, 364, 10.1123/ijsnem.2018-0182 · DOI · Paper page
  57. Hackney, 2017, Endurance exercise training and male sexual libido, Med Sci Sports Exerc, 49, 1383, 10.1249/MSS.0000000000001235 · DOI · Paper page
  58. McKay, 2022, Six days of low carbohydrate, not energy availability, alters the iron and immune response to exercise in elite athletes, Med Sci Sports Exerc, 54, 377, 10.1249/MSS.0000000000002819 · DOI · Paper page
  59. De Souza, 2010, High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures, Hum Reprod, 25, 491, 10.1093/humrep/dep411 · DOI · Paper page
  60. Melin, 2015, Energy availability and the female athlete triad in elite endurance athletes, Scand J Med Sci Sports, 25, 610, 10.1111/sms.12261 · DOI · Paper page
  61. Gordon, 2017, Functional hypothalamic amenorrhea: an endocrine society clinical practice guideline, J Clin Endocrinol Metab, 102, 1413, 10.1210/jc.2017-00131 · DOI · Paper page
  62. Gimunová, 2022, The prevalence of menstrual cycle disorders in female athletes from different sports disciplines: a rapid review, Int J Environ Res Public Health, 19, 14243, 10.3390/ijerph192114243 · DOI
  63. Loucks, 1998, Low energy availability, not stress of exercise, alters LH pulsatility in exercising women, J Appl Physiol (1985), 84, 37, 10.1152/jappl.1998.84.1.37 · DOI · Paper page
  64. Wheeler, 1984, Reduced serum testosterone and prolactin levels in male distance runners, JAMA, 252, 514, 10.1001/jama.1984.03350040044020 · DOI · Paper page
  65. Jin, 2014, Molecular regulation of hypothalamus-pituitary-gonads axis in males, Gene, 551, 15, 10.1016/j.gene.2014.08.048 · DOI
  66. Ruffing, 2022, Moderate weight loss is associated with reductions in LH pulse frequency and increases in 24-hour cortisol with no change in perceived stress in young ovulatory women, Physiol Behav, 254, 113885, 10.1016/j.physbeh.2022.113885 · DOI
  67. Roberts, 1993, Overtraining affects male reproductive status, Fertil Steril, 60, 686, 10.1016/S0015-0282(16)56223-2 · DOI · Paper page
  68. Aakvaag, 1978, Testosterone and Testosterone Binding Globulin (TeBG) in young men during prolonged stress, Int J Androl, 1, 22, 10.1111/j.1365-2605.1978.tb00573.x · DOI
  69. Aakvaag, 1978, Hormonal changes in serum in young men during prolonged physical strain, Eur J Appl Physiol Occup Physiol, 39, 283, 10.1007/BF00421452 · DOI
  70. Opstad, 1984, The thyroid function in young men during prolonged exercise and the effect of energy and sleep deprivation, Clin Endocrinol (Oxf), 20, 657, 10.1111/j.1365-2265.1984.tb00116.x · DOI
  71. Opstad, 1981, The effect of a high calory diet on hormonal changes in young men during prolonged physical strain and sleep deprivation, Eur J Appl Physiol Occup Physiol, 46, 31, 10.1007/BF00422172 · DOI
  72. De Souza, 1994, Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training, Int J Sports Med, 15, 383, 10.1055/s-2007-1021075 · DOI
  73. Gebreegziabher, 2004, Sperm characteristics of endurance trained cyclists, Int J Sports Med, 25, 247, 10.1055/s-2004-819933 · DOI
  74. Loucks, 1993, Induction and prevention of low-T3 syndrome in exercising women, Am J Physiol, 264, R924
  75. Tornberg, 2017, Reduced neuromuscular performance in amenorrheic elite endurance athletes, Med Sci Sports Exerc, 49, 2478, 10.1249/MSS.0000000000001383 · DOI
  76. Loucks, 1992, Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes, J Clin Endocrinol Metab, 75, 514
  77. Harber, 1998, Thyroid hormone concentrations and muscle metabolism in amenorrheic and eumenorrheic athletes, Can J Appl Physiol, 23, 293, 10.1139/h98-017 · DOI
  78. Hartman, 1992, Augmented growth hormone (GH) secretory burst frequency and amplitude mediate enhanced GH secretion during a two-day fast in normal men, J Clin Endocrinol Metab, 74, 757, 10.1210/jcem.74.4.1548337 · DOI · Paper page
  79. Misra, 2003, Alterations in growth hormone secretory dynamics in adolescent girls with anorexia nervosa and effects on bone metabolism, J Clin Endocrinol Metab, 88, 5615, 10.1210/jc.2003-030532 · DOI
  80. Laughlin, 1998, Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea, J Clin Endocrinol Metab, 83, 25
  81. Ipsa, 2019, Growth hormone and insulin-like growth factor action in reproductive tissues, Front Endocrinol (Lausanne), 10, 777, 10.3389/fendo.2019.00777 · DOI
  82. Thissen, 1994, Nutritional regulation of the insulin-like growth factors, Endocr Rev, 15, 80
  83. Murphy, 2020, Caloric restriction induces anabolic resistance to resistance exercise, Eur J Appl Physiol, 120, 1155, 10.1007/s00421-020-04354-0 · DOI · Paper page
  84. Brundu, 2006, Increased cortisol in the cerebrospinal fluid of women with functional hypothalamic amenorrhea, J Clin Endocrinol Metab, 91, 1561, 10.1210/jc.2005-2422 · DOI
  85. De Souza, 1991, Adrenal activation and the prolactin response to exercise in eumenorrheic and amenorrheic runners, J Appl Physiol (1985), 70, 2378, 10.1152/jappl.1991.70.6.2378 · DOI
  86. Laughlin, 1997, Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea, J Clin Endocrinol Metab, 82, 318, 10.1210/jcem.82.1.3840 · DOI · Paper page
  87. Berga, 1997, Women with functional hypothalamic amenorrhea but not other forms of anovulation display amplified cortisol concentrations, Fertil Steril, 67, 1024, 10.1016/S0015-0282(97)81434-3 · DOI
  88. Ackerman, 2013, Cortisol secretory parameters in young exercisers in relation to LH secretion and bone parameters, Clin Endocrinol (Oxf), 78, 114, 10.1111/j.1365-2265.2012.04458.x · DOI
  89. Vamvini, 2011, Energy deprivation alters in a leptin- and cortisol-independent manner circulating levels of activin A and follistatin but not myostatin in healthy males, J Clin Endocrinol Metab, 96, 3416, 10.1210/jc.2011-1665 · DOI
  90. Christo, 2008, Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study, Clin Endocrinol (Oxf), 69, 628, 10.1111/j.1365-2265.2008.03237.x · DOI
  91. Sienkiewicz, 2011, Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women, Metabolism, 60, 1211, 10.1016/j.metabol.2011.05.016 · DOI · Paper page
  92. Donoso, 2010, Increased circulating adiponectin levels and decreased leptin/soluble leptin receptor ratio throughout puberty in female ballet dancers: association with body composition and the delay in puberty, Eur J Endocrinol, 162, 905, 10.1530/EJE-09-0874 · DOI
  93. Zaccaria, 2013, Plasma leptin and energy expenditure during prolonged, moderate intensity, treadmill exercise, J Endocrinol Invest, 36, 396
  94. De Souza, 2022, Bone mineral density in response to increased energy intake in exercising women with oligomenorrhea/amenorrhea: the REFUEL randomized controlled trial, Am J Clin Nutr, 115, 1457, 10.1093/ajcn/nqac044 · DOI · Paper page
  95. Popp, 2022, Impact of low energy availability on skeletal health in physically active adults, Calcif Tissue Int, 110, 605, 10.1007/s00223-022-00957-1 · DOI
  96. Evans, 2008, Effects of a 4-month recruit training program on markers of bone metabolism, Med Sci Sports Exerc, 40, S660, 10.1249/MSS.0b013e318189422b · DOI
  97. Abbott, 2023, Part II: risk factors for stress fractures in female military recruits, Mil Med, 188, 93, 10.1093/milmed/usac033 · DOI
  98. Tenforde, 2022, Female athlete triad risk factors are more strongly associated with trabecular-rich versus cortical-rich bone stress injuries in collegiate athletes, Orthop J Sports Med, 10, 10.1177/23259671221123588 · DOI
  99. Waterman, 2016, Epidemiology of lower extremity stress fractures in the United States military, Mil Med, 181, 1308, 10.7205/MILMED-D-15-00571 · DOI
  100. Bulathsinhala, 2017, Risk of stress fracture varies by race/ethnic origin in a cohort study of 1.3 million US army soldiers, J Bone Miner Res, 32, 1546, 10.1002/jbmr.3131 · DOI
  101. Knapik, 2012, Stress fracture risk factors in basic combat training, Int J Sports Med, 33, 940, 10.1055/s-0032-1311583 · DOI
  102. MacGregor, 2022, Sex differences in the incidence and risk of ankle–foot complex stress fractures among U.S. military personnel, J Women's Health, 31, 586, 10.1089/jwh.2021.0292 · DOI
  103. Armstrong, 2004, Stress fracture injury in young military men and women, Bone, 35, 806, 10.1016/j.bone.2004.05.014 · DOI
  104. Millward, 2020, Association of serum vitamin D levels and stress fractures in collegiate athletes, Orthop J Sports Med, 8, 10.1177/2325967120966967 · DOI
  105. Jones, 2002, Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review, Epidemiol Rev, 24, 228, 10.1093/epirev/mxf011 · DOI · Paper page
  106. Milner, 2023, Biomechanics associated with tibial stress fracture in runners: a systematic review and meta-analysis, J Sport Health Sci, 12, 333, 10.1016/j.jshs.2022.12.002 · DOI
  107. Wright, 2015, Risk factors associated with lower extremity stress fractures in runners: a systematic review with meta-analysis, Br J Sports Med, 49, 1517, 10.1136/bjsports-2015-094828 · DOI
  108. Saxena, 2006, Navicular stress fractures: a prospective study on athletes, Foot Ankle Int, 27, 917, 10.1177/107110070602701109 · DOI
  109. Bennell, 1996, Risk factors for stress fractures in track and field athletes. A twelve-month prospective study, Am J Sports Med, 24, 810, 10.1177/036354659602400617 · DOI · Paper page
  110. Bennell, 1996, The incidence and distribution of stress fractures in competitive track and field athletes. A twelve-month prospective study, Am J Sports Med, 24, 211, 10.1177/036354659602400217 · DOI · Paper page
  111. Takkar, 2019, Stress fractures in military recruits: a prospective study for evaluation of incidence, patterns of injury and invalidments out of service, Med J Armed Forces India, 75, 330, 10.1016/j.mjafi.2018.09.006 · DOI
  112. Cosman, 2013, Determinants of stress fracture risk in United States Military Academy cadets, Bone, 55, 359, 10.1016/j.bone.2013.04.011 · DOI
  113. Wentz, 2011, Females have a greater incidence of stress fractures than males in both military and athletic populations: a systemic review, Mil Med, 176, 420, 10.7205/MILMED-D-10-00322 · DOI · Paper page
  114. Sarin, 2019, Molecular pathways mediating immunosuppression in response to prolonged intensive physical training, low-energy availability, and intensive weight loss, Front Immunol, 10, 907, 10.3389/fimmu.2019.00907 · DOI
  115. Murakami, 2010, Suppression of exercise-induced neutrophilia and lymphopenia in athletes by cystine/theanine intake: a randomized, double-blind, placebo-controlled trial, J Int Soc Sports Nutr, 7, 23, 10.1186/1550-2783-7-23 · DOI · Paper page
  116. Li, 2013, Combat-training increases intestinal permeability, immune activation and gastrointestinal symptoms in soldiers, Aliment Pharmacol Ther, 37, 799, 10.1111/apt.12269 · DOI
  117. McClung, 2013, Effects of a 7-day military training exercise on inflammatory biomarkers, serum hepcidin, and iron status, Nutr J, 12, 141, 10.1186/1475-2891-12-141 · DOI
  118. Pasiakos, 2016, Effects of exercise mode, energy, and macronutrient interventions on inflammation during military training, Physiol Rep, 4, e12820, 10.14814/phy2.12820 · DOI
  119. Shimizu, 2011, Influences of weight loss on monocytes and T-cell subpopulations in male judo athletes, J Strength Cond Res, 25, 1943, 10.1519/JSC.0b013e3181e4f9c6 · DOI
  120. Imai, 2002, Effect of weight loss on T-cell receptor-mediated T-cell function in elite athletes, Med Sci Sports Exerc, 34, 245, 10.1097/00005768-200202000-00011 · DOI
  121. Suzuki, 2003, Effects of weight reduction on neutrophil phagocytic activity and oxidative burst activity in female judoists, Luminescence, 18, 214, 10.1002/bio.727 · DOI
  122. Yaegaki, 2007, Change in the capability of reactive oxygen species production by neutrophils following weight reduction in female judoists, Br J Sports Med, 41, 322, 10.1136/bjsm.2006.032029 · DOI
  123. Tsai, 2011, Changes of mucosal immunity and antioxidation activity in elite male Taiwanese taekwondo athletes associated with intensive training and rapid weight loss, Br J Sports Med, 45, 729, 10.1136/bjsm.2009.062497 · DOI
  124. Drew, 2018, Prevalence of illness, poor mental health and sleep quality and low energy availability prior to the 2016 summer Olympic games, Br J Sports Med, 52, 47, 10.1136/bjsports-2017-098208 · DOI
  125. Drew, 2017, A multifactorial evaluation of illness risk factors in athletes preparing for the Summer Olympic Games, J Sci Med Sport, 20, 745, 10.1016/j.jsams.2017.02.010 · DOI
  126. Tsai, 2011, Impact of intense training and rapid weight changes on salivary parameters in elite female taekwondo athletes, Scand J Med Sci Sports, 21, 758, 10.1111/j.1600-0838.2010.01099.x · DOI
  127. Martinez-Lopez, 1993, A longitudinal study of infections and injuries of Ranger students, Mil Med, 158, 433, 10.1093/milmed/158.7.433 · DOI
  128. Andreoli, 2001, Effects of different sports on bone density and muscle mass in highly trained athletes, Med Sci Sports Exerc, 33, 507, 10.1097/00005768-200104000-00001 · DOI · Paper page
  129. Rauh, 2010, Relationships among injury and disordered eating, menstrual dysfunction, and low bone mineral density in high school athletes: a prospective study, J Athl Train, 45, 243, 10.4085/1062-6050-45.3.243 · DOI
  130. Miralles-Amorós, 2023, Study the effect of relative energy deficiency on physiological and physical variables in professional women athletes: a randomized controlled trial, Metabolites, 13, 168, 10.3390/metabo13020168 · DOI
  131. Chow, 2022, Exerkines in health, resilience and disease, Nat Rev Endocrinol, 18, 273, 10.1038/s41574-022-00641-2 · DOI · Paper page
  132. Bouzoni, 2020, Circulating profile of activin-follistatin-inhibin axis in women with hypothalamic amenorrhea in response to leptin treatment, Metab Clin Exp, 113, 154392, 10.1016/j.metabol.2020.154392 · DOI
  133. Polyzos, 2020, Targeted analysis of three hormonal systems identifies molecules associated with the presence and severity of NAFLD, J Clin Endocrinol Metab, 105, e390, 10.1210/clinem/dgz172 · DOI
  134. Melin, 2024, Direct and indirect impact of low energy availability on sports performance, Scand J Med Sci Sports, 34, e14327, 10.1111/sms.14327 · DOI · Paper page
  135. Eliakim, 2002, Screening blood tests in members of the Israeli National Olympic team, J Sports Med Phys Fitness, 42, 250
  136. Malczewska, 2001, The assessment of frequency of iron deficiency in athletes from the transferrin receptor-ferritin index, Int J Sport Nutr Exerc Metab, 11, 42, 10.1123/ijsnem.11.1.42 · DOI
  137. Ziemann, 2013, Do high blood hepcidin concentrations contribute to low ferritin levels in young tennis players at the end of tournament season?, J Sports Sci Med, 12, 249
  138. Badenhorst, 2019, Hepcidin as a prospective individualized biomarker for individuals at risk of low energy availability, Int J Sport Nutr Exerc Metab, 29, 671, 10.1123/ijsnem.2019-0006 · DOI
  139. Sim, 2014, A seven day running training period increases basal urinary hepcidin levels as compared to cycling, J Int Soc Sports Nutr, 11, 14, 10.1186/1550-2783-11-14 · DOI
  140. Rickenlund, 2005, Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile, J Clin Endocrinol Metab, 90, 1354, 10.1210/jc.2004-1286 · DOI
  141. Costa, 2017, Systematic review: exercise-induced gastrointestinal syndrome-implications for health and intestinal disease, Aliment Pharmacol Ther, 46, 246, 10.1111/apt.14157 · DOI · Paper page
  142. Norris, 2016, Gastrointestinal complications associated with anorexia nervosa: a systematic review, Int J Eat Disord, 49, 216, 10.1002/eat.22462 · DOI
  143. Chantler, 2021, The effects of exercise on indirect markers of gut damage and permeability: a systematic review and meta-analysis, Sports Med, 51, 113, 10.1007/s40279-020-01348-y · DOI
  144. O'Connor, 2016, Altered appetite-mediating hormone concentrations precede compensatory overeating after severe, short-term energy deprivation in healthy adults, J Nutr, 146, 209, 10.3945/jn.115.217976 · DOI
  145. Karl, 2016, Altered metabolic homeostasis is associated with appetite regulation during and following 48-h of severe energy deprivation in adults, Metabolism, 65, 416, 10.1016/j.metabol.2015.11.001 · DOI
  146. Cahill, 1970, Starvation in man, N Engl J Med, 282, 668, 10.1056/NEJM197003192821209 · DOI · Paper page
  147. Boyle, 1989, Insulin, glucagon, and catecholamines in prevention of hypoglycemia during fasting, Am J Physiol, 256, E651
  148. Steinhauser, 2018, The circulating metabolome of human starvation, JCI Insight, 3, e121434, 10.1172/jci.insight.121434 · DOI
  149. Cahill, 2006, Fuel metabolism in starvation, Annu Rev Nutr, 26, 1, 10.1146/annurev.nutr.26.061505.111258 · DOI · Paper page
  150. Nykänen, 2022, Changes in body composition, energy metabolites and electrolytes during winter survival training in male soldiers, Front Physiol, 13, 797268, 10.3389/fphys.2022.797268 · DOI
  151. Gavrila, 2003, Serum adiponectin levels are inversely associated with overall and central fat distribution but are not directly regulated by acute fasting or leptin administration in humans: cross-sectional and interventional studies, J Clin Endocrinol Metab, 88, 4823, 10.1210/jc.2003-030214 · DOI · Paper page
  152. Pasiakos, 2011, Appetite and endocrine regulators of energy balance after 2 days of energy restriction: insulin, leptin, ghrelin, and DHEA-S, Obesity (Silver Spring), 19, 1124, 10.1038/oby.2010.316 · DOI
  153. De Souza, 2004, Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones, J Clin Endocrinol Metab, 89, 3536, 10.1210/jc.2003-032007 · DOI
  154. Sygo, 2018, Prevalence of indicators of low energy availability in elite female sprinters, Int J Sport Nutr Exerc Metab, 28, 490, 10.1123/ijsnem.2017-0397 · DOI · Paper page
  155. Hackney, 2020, Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment?, Front Endocrinol (Lausanne), 11, 11, 10.3389/fendo.2020.00011 · DOI
  156. Hamarsland, 2018, Depressed physical performance outlasts hormonal disturbances after military training, Med Sci Sports Exerc, 50, 2076, 10.1249/MSS.0000000000001681 · DOI
  157. Nindl, 2007, Utility of circulating IGF-I as a biomarker for assessing body composition changes in men during periods of high physical activity superimposed upon energy and sleep restriction, J Appl Physiol (1985), 103, 340, 10.1152/japplphysiol.01321.2006 · DOI · Paper page
  158. Kyröläinen, 2008, Hormonal responses during a prolonged military field exercise with variable exercise intensity, Eur J Appl Physiol, 102, 539, 10.1007/s00421-007-0619-0 · DOI
  159. Salonen, 2019, Neuromuscular performance and hormonal profile during military training and subsequent recovery period, Mil Med, 184, e113, 10.1093/milmed/usy176 · DOI
  160. Fazeli, 2014, Determinants of GH resistance in malnutrition, J Endocrinol, 220, R57, 10.1530/JOE-13-0477 · DOI
  161. Davey, 2001, STAT5b is required for GH-induced liver IGF-I gene expression, Endocrinology, 142, 3836, 10.1210/endo.142.9.8400 · DOI
  162. Nindl, 2003, Differential responses of IGF-I molecular complexes to military operational field training, J Appl Physiol (1985), 95, 1083, 10.1152/japplphysiol.01148.2002 · DOI
  163. Gomez-Merino, 2004, Influence of energy deficiency on the insulin-like growth factor I axis in a military training program, Horm Metab Res, 36, 506, 10.1055/s-2004-825730 · DOI
  164. Misra, 2014, Endocrine consequences of anorexia nervosa, Lancet Diabetes Endocrinol, 2, 581, 10.1016/S2213-8587(13)70180-3 · DOI · Paper page
  165. Fazeli, 2010, Effects of recombinant human growth hormone in anorexia nervosa: a randomized, placebo-controlled study, J Clin Endocrinol Metab, 95, 4889, 10.1210/jc.2010-0493 · DOI
  166. Georgopoulos, 2011, Abolished circadian rhythm of salivary cortisol in elite artistic gymnasts, Steroids, 76, 353, 10.1016/j.steroids.2010.10.013 · DOI
  167. Cho, 2017, Effects of intensive training on menstrual function and certain serum hormones and peptides related to the female reproductive system, Medicine (Baltimore), 96, e6876, 10.1097/MD.0000000000006876 · DOI
  168. Gifford, 2019, Positive adaptation of HPA axis function in women during 44 weeks of infantry-based military training, Psychoneuroendocrinology, 110, 104432, 10.1016/j.psyneuen.2019.104432 · DOI
  169. Vikmoen, 2020, Sex differences in the physiological response to a demanding military field exercise, Scand J Med Sci Sports, 30, 1348, 10.1111/sms.13689 · DOI
  170. Koski, 1999, Energy deficits suppress both systemic and gut immunity during infection, Biochem Biophys Res Commun, 264, 796, 10.1006/bbrc.1999.1596 · DOI
  171. Torstveit, 2023, Primary, secondary and tertiary prevention of Relative Energy Deficiency in Sport (REDs): a narrative review by a subgroup of the IOC consensus on REDs, Br J Sports Med, 57, 1119, 10.1136/bjsports-2023-106932 · DOI · Paper page
  172. Shimizu, 2012, Mucosal immune function comparison between amenorrheic and eumenorrheic distance runners, J Strength Condition Res, 26, 1402, 10.1519/JSC.0b013e31822e7a6c · DOI
  173. Abedelmalek, 2015, Caloric restriction effect on proinflammatory cytokines, growth hormone, and steroid hormone concentrations during exercise in judokas, Oxid Med Cell Longev, 2015, 809492, 10.1155/2015/809492 · DOI
  174. Horn, 2010, Lower white blood cell counts in elite athletes training for highly aerobic sports, Eur J Appl Physiol, 110, 925, 10.1007/s00421-010-1573-9 · DOI
  175. Kramer, 1997, Effects of food restriction in military training on T-lymphocyte responses, Int J Sports Med, 18, S84, 10.1055/s-2007-972704 · DOI
  176. Dubnov, 2004, Prevalence of iron depletion and anemia in top-level basketball players, Int J Sport Nutr Exerc Metab, 14, 30, 10.1123/ijsnem.14.1.30 · DOI · Paper page
  177. Ackerman, 2019, Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport, Br J Sports Med, 53, 628, 10.1136/bjsports-2017-098958 · DOI · Paper page
  178. Dubnov, 2006, High prevalence of iron deficiency and anemia in female military recruits, Mil Med, 171, 866, 10.7205/MILMED.171.9.866 · DOI
  179. Epstein, 2018, Prevalence of iron deficiency and iron deficiency anemia in strenuously training male army recruits, Acta Haematol, 139, 141, 10.1159/000485736 · DOI
  180. Yanovich, 2011, Anemia, iron deficiency, and stress fractures in female combatants during 16 months, J Strength Condition Res, 25, 3412, 10.1519/JSC.0b013e318215f779 · DOI
  181. Yanovich, 2015, Effects of basic combat training on iron status in male and female soldiers: a comparative study, US Army Med Dep J, Apr-Jun, 67
  182. McClung, 2006, Prevalence of iron deficiency and iron deficiency anemia among three populations of female military personnel in the US army, J Am Coll Nutr, 25, 64, 10.1080/07315724.2006.10719516 · DOI
  183. Dave, 2022, Relative energy deficiency in sport (RED - S), Curr Probl Pediatr Adolesc Health Care, 52, 101242
  184. Berthou, 2022, Iron, neuro-bioavailability and depression, eJHaem, 3, 263, 10.1002/jha2.321 · DOI
  185. Barbarich, 2003, Neurotransmitter and imaging studies in anorexia nervosa: new targets for treatment, Curr Drug Targets CNS Neurol Disord, 2, 61, 10.2174/1568007033338779 · DOI
  186. Kaye, 2008, Neurobiology of anorexia and bulimia nervosa, Physiol Behav, 94, 121, 10.1016/j.physbeh.2007.11.037 · DOI · Paper page
  187. Peuranpää, 2014, Effects of anemia and iron deficiency on quality of life in women with heavy menstrual bleeding, Acta Obstet Gynecol Scand, 93, 654, 10.1111/aogs.12394 · DOI
  188. Wang, 2018, Bone marrow fat and hematopoiesis, Front Endocrinol (Lausanne), 9, 694, 10.3389/fendo.2018.00694 · DOI
  189. Zhong, 2020, Single cell transcriptomics identifies a unique adipose lineage cell population that regulates bone marrow environment, Elife, 9, e54695, 10.7554/eLife.54695 · DOI · Paper page
  190. Deb, 2019, How stem cells turn into bone and fat, N Engl J Med, 380, 2268, 10.1056/NEJMcibr1905165 · DOI
  191. Devlin, 2011, Why does starvation make bones fat?, Am J Hum Biol, 23, 577, 10.1002/ajhb.21202 · DOI
  192. Devlin, 2010, Caloric restriction leads to high marrow adiposity and low bone mass in growing mice, J Bone Miner Res, 25, 2078, 10.1002/jbmr.82 · DOI · Paper page
  193. Tavassoli, 1974, Differential response of bone marrow and extramedullary adipose cells to starvation, Experientia, 30, 424, 10.1007/BF01921701 · DOI
  194. O’Donnell, 2015, Discordant orthostatic reflex renin-angiotensin and sympathoneural responses in premenopausal exercising-hypoestrogenic women, Hypertension, 65, 1089, 10.1161/HYPERTENSIONAHA.114.04976 · DOI
  195. Tomes, 2020, Relationships between heart rate variability, occupational performance, and fitness for tactical personnel: a systematic review, Front Public Health, 8, 583336, 10.3389/fpubh.2020.583336 · DOI
  196. Schmitt, 2013, Fatigue shifts and scatters heart rate variability in elite endurance athletes, PLoS One, 8, e71588, 10.1371/journal.pone.0071588 · DOI
  197. Costa, 2017, Systematic review: exercise-induced gastrointestinal syndrome—implications for health and intestinal disease, Aliment Pharmacol Ther, 46, 246, 10.1111/apt.14157 · DOI · Paper page
  198. Pugh, 2022, More than a gut feeling: what is the role of the gastrointestinal tract in female athlete health?, Eur J Sport Sci, 22, 755, 10.1080/17461391.2021.1921853 · DOI
  199. Zhang, 2019, Intestinal hyperpermeability in gulf war veterans with chronic gastrointestinal symptoms, J Clin Gastroenterol, 53, e298, 10.1097/MCG.0000000000001135 · DOI
  200. Putnam, 2006, Self-reported description of diarrhea among military populations in operations Iraqi freedom and enduring freedom, J Travel Med, 13, 92, 10.1111/j.1708-8305.2006.00020.x · DOI

200 of 323 shown

Cited by

Metadata

Authors
Angelidi, A. M., Stefanakis, K., Chou, S. H., Valenzuela-Vallejo, L., Dipla, K., Boutari, C., Ntoskas, K., Tokmakidis, P., Kokkinos, A., Goulis, D. G., Papadaki, H. A., & Mantzoros, C. S.
Affiliations
  • Department of Medicine, Boston VA Healthcare System, Boston, MA 02115 , USA
  • Division of Endocrinology, Diabetes and Hypertension, Brigham and Women's Hospital (BWH), Harvard Medical School , Boston, MA 02115 , USA
  • Exercise Physiology and Biochemistry Laboratory, Department of Sports Science at Serres, Aristotle University of Thessaloniki , Serres 62100 , Greece
  • Second Propaedeutic Department of Internal Medicine, Hippokration Hospital, School of Medicine, Aristotle University of Thessaloniki , Thessaloniki 54642 , Greece
  • Department of Internal Medicine, 251 Air Force General Hospital , Athens 11525 , Greece
  • First Propaedeutic Department of Internal Medicine, Laiko General Hospital, Medical School, National and Kapodistrian University of Athens , Athens 11527 , Greece
  • Unit of Reproductive Endocrinology, First Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki , Thessaloniki 54124 , Greece
  • Department of Hematology, University Hospital of Heraklion, School of Medicine, University of Crete , Heraklion 71500 , Greece
ORCID
Venue
Endocrine Reviews
Publisher
The Endocrine Society
Published
2024-03-15
Volume
45
Issue
5
Pages
676-708
ISSN
  • 0163-769X
  • 1945-7189
DOI
10.1210/endrev/bnae011
Cited by
83
References
71
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.