Cited by 70Eating Disorders and BehaviorsNutrition, Health and Food BehaviorHypothalamic control of reproductive hormones

Screening for low energy availability in male athletes: attempted validation of LEAM-Q

Open access
Lundy, Bronwen, Torstveit, Monica K., Stenqvist, Thomas B., Burke, Louise M., Garthe, Ina, Slater, Gary J., Ritz, Christian, Melin, Anna K.·2022·Nutrients

Abstract

A questionnaire-based screening tool for male athletes at risk of low energy availability (LEA) could facilitate both research and clinical practice. The present options rely on proxies for LEA such screening tools for disordered eating, exercise dependence, or those validated in female athlete populations. in which the female-specific sections are excluded. To overcome these limitations and support progress in understanding LEA in males, centres in Australia, Norway, Denmark, and Sweden collaborated to develop a screening tool (LEAM-Q) based on clinical investigations of elite and sub-elite male athletes from multiple countries and ethnicities, and a variety of endurance and weight-sensitive sports. A bank of questions was developed from previously validated questionnaires and expert opinion on various clinical markers of LEA in athletic or eating disorder populations, dizziness, thermoregulation, gastrointestinal symptoms, injury, illness, wellbeing, recovery, sleep and sex drive. The validation process covered reliability, content validity, a multivariate analysis of associations between variable responses and clinical markers, and Receiver Operating Characteristics (ROC) curve analysis of variables, with the inclusion threshold being set at 60% sensitivity. Comparison of the scores of the retained questionnaire variables between subjects classified as cases or controls based on clinical markers of LEA revealed an internal consistency and reliability of 0.71. Scores for sleep and thermoregulation were not associated with any clinical marker and were excluded from any further analysis. Of the remaining variables, dizziness, illness, fatigue, and sex drive had sufficient sensitivity to be retained in the questionnaire, but only low sex drive was able to distinguish between LEA cases and controls and was associated with perturbations in key clinical markers and questionnaire responses. In summary, in this large and international cohort, low sex drive was the most effective self-reported symptom in identifying male athletes requiring further clinical assessment for LEA.

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 · 10.3390/nu14091873

Cites

14 of 14 references verified0 citation errors · 0 not checkable

Statistics

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?

  • Two emerging potential indicators of REDs in males are the presence of low libido and decreased morning erections, which have been identified as physiological consequences of LEA.

    “Two emerging potential indicators of REDs in males are the presence of low libido and decreased morning erections, which have been identified as physiological consequences of LEA.[108][109][110][111]”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [108]

    The Results (section 3.3) report that low sex-drive scores distinguished LEA cases from controls, and the Methods (section 2.3) show that the score included questions about morning erections. The paper does not establish decreased morning erections as an independent indicator or demonstrate that either symptom is a physiological consequence caused by LEA. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

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

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

Cites

Flagged first, then by citations

Research works printed but not linked: 98

  1. [2]Loucks A.B. Thuma J.R. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women J. Clin. Endocrinol. Metab. 2003 88 297 311 10.1210/jc.2002-020369 12519869 · DOI · Paper page
  2. [3]De Souza M.J. Koltun K.J. Williams N.I. The role of energy availability in reproductive function in the female athlete triad and extension of its effects to men: An initial working model of a similar syndrome in male athletes Sports Med. 2019 49 125 137 10.1007/s40279-019-01217-3 31696452 PMC6901401 · DOI
  3. [5]Fredericson M. Kussman A. Misra M. Barrack M.T. De Souza M.J. Kraus E. Koltun K.J. Williams N.I. Joy E. Nattiv A. 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 10.1097/JSM.0000000000000948 34091538 · DOI
  4. [7]Mountjoy M. Sundgot-Borgen J. Burke L. Ackerman K.E. Blauwet C. Constantini N. Lebrun C. Lundy B. Melin A. Meyer N. International Olympic Committee (IOC) Consensus Statement on Relative Energy Deficiency in Sport (RED-S): 2018 update Int. J. Sport Nutr. Exerc. Metab. 2018 28 316 331 10.1123/ijsnem.2018-0136 29771168 · DOI · Paper page
  5. [8]Nattiv A. De Souza M.J. Koltun K.J. Misra M. Kussman A. Williams N.I. Barrack M.T. Kraus E. Joy E. Fredericson M. 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 10.1097/JSM.0000000000000946 34091537 · DOI
  6. [9]Heikura I.A. Burke L.M. Bergland D. Uusitalo A.L.T. Mero A.A. Stellingwerff T. Impact of Energy Availability, Health, and Sex on Hemoglobin-Mass Responses Following Live-High-Train-High Altitude Training in Elite Female and Male Distance Athletes Int. J. Sports Physiol. Perform. 2018 13 1090 1096 10.1123/ijspp.2017-0547 29431548 · DOI · Paper page
  7. [10]Keay N. Francis G. Hind K. Low energy availability assessed by a sport-specific questionnaire and clinical interview indicative of bone health, endocrine profile and cycling performance in competitive male cyclists BMJ Open Sport Exerc. Med. 2018 4 e000424 10.1136/bmjsem-2018-000424 PMC6196965 30364549 · DOI
  8. [11]Dolan E. O’Connor H. McGoldrick A. O’Loughlin G. Lyons D. Warrington G. Nutritional, lifestyle, and weight control practices of professional jockeys J. Sports Sci. 2011 29 791 799 10.1080/02640414.2011.560173 21506039 · DOI
  9. [12]McCormack W.P. Shoepe T.C. LaBrie J. Almstedt H.C. Bone mineral density, energy availability, and dietary restraint in collegiate cross-country runners and non-running controls Eur. J. Appl. Physiol. 2019 119 1747 1756 10.1007/s00421-019-04164-z 31102062 PMC10496742 · DOI
  10. [13]Viner R.T. Harris M. Berning J.R. Meyer N.L. 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. 2015 25 594 602 10.1123/ijsnem.2015-0073 26131616 · DOI · Paper page
  11. [14]Koehler K. Hoerner N.R. Gibbs J.C. Zinner C. Braun H. De Souza M.J. Schaenzer W. Low energy availability in exercising men is associated with reduced leptin and insulin but not with changes in other metabolic hormones J. Sports Sci. 2016 34 1921 1929 10.1080/02640414.2016.1142109 26852783 · DOI · Paper page
  12. [15]McKay A.K.A. Peeling P. Pyne D.B. Tee N. Whitfield J. Sharma A.P. Heikura I.A. Burke L.M. Six days of low carbohydrate, not energy availability, alters the iron and immune response to exercise in elite athletes Med. Sci. Sports Exerc. 2022 54 377 387 10.1249/MSS.0000000000002819 34690285 · DOI · Paper page
  13. [16]Papageorgiou M. Elliott-Sale K.J. Parsons A. Tang J.C.Y. Greeves J.P. Fraser W.D. Sale C. Effects of reduced energy availability on bone metabolism in women and men Bone 2017 105 191 199 10.1016/j.bone.2017.08.019 28847532 · DOI · Paper page
  14. [17]Murphy C. Bilek L.D.D. Koehler K. Low energy availability with and without a high-protein diet suppresses bone formation and increases bone resorption in men: A randomized controlled pilot study Nutrients 2021 13 802 10.3390/nu13030802 33671093 PMC8000240 · DOI
  15. [19]Hackney A.C. Endurance training and testosterone levels Sports Med. 1989 8 117 127 10.2165/00007256-198908020-00004 2675257 · DOI
  16. [20]Hackney A.C. Hypogonadism in Exercising Males: Dysfunction or Adaptive-Regulatory Adjustment? Front. Endocrinol. 2020 11 11 10.3389/fendo.2020.00011 PMC7005256 32082255 · DOI
  17. [21]Filaire E. Rouveix M. Pannafieux C. Ferrand C. Eating attitudes, perfectionism and body-esteem of elite male judoists and cyclists J. Sports Sci. Med. 2007 6 50 57 24149224 PMC3778699
  18. [22]Goltz F.R. Stenzel L.M. Schneider C.D. Disordered eating behaviors and body image in male athletes Braz. J. Psychiatry 2013 35 237 242 10.1590/1516-4446-2012-0840 24142083 · DOI
  19. [23]Bratland-Sanda S. Sundgot-Borgen J. Eating disorders in athletes: Overview of prevalence, risk factors and recommendations for prevention and treatment Eur. J. Sport Sci. 2013 13 499 508 10.1080/17461391.2012.740504 24050467 · DOI · Paper page
  20. [24]Torstveit M.K. Fahrenholtz I.L. Lichtenstein M.B. Stenqvist T.B. Melin A.K. Exercise dependence, eating disorder symptoms and biomarkers of Relative Energy Deficiency in Sports (RED-S) among male endurance athletes BMJ Open Sport Exerc. Med. 2019 5 e000439 10.1136/bmjsem-2018-000439 PMC6350749 30792881 · DOI
  21. [25]Kraus E. Tenforde A.S. Nattiv A. Sainani K.L. Kussman A. Deakins-Roche M. Singh S. Kim B.Y. Barrack M.T. Fredericson M. 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. 2019 53 237 242 10.1136/bjsports-2018-099861 30580252 · DOI
  22. [26]Keay N. Overseas A. Francis G. Indicators and correlates of low energy availability in male and female dancers BMJ Open Sport Exerc. Med. 2020 6 e000906 10.1136/bmjsem-2020-000906 PMC7692996 33304605 · DOI
  23. [27]Wilson G. Hill J. Sale C. Morton J.P. Close G.L. Elite male Flat jockeys display lower bone density and lower resting metabolic rate than their female counterparts: Implications for athlete welfare Appl. Physiol. Nutr. Metab. 2015 40 1318 1320 10.1139/apnm-2015-0354 26566241 · DOI
  24. [28]Tornberg A.B. Melin A. Manderson Koivula F. Johansson A. Skouby S. Faber J. Sjodin A. Reduced neuromuscular performance in amenorrheic elite endurance athletes Med. Sci. Sports Exerc. 2017 49 2478 2485 10.1249/MSS.0000000000001383 28723842 · DOI
  25. [30]Woods A.L. Garvican-Lewis L.A. Lundy B. Rice A.J. Thompson K.G. New approaches to determine fatigue in elite athletes during intensified training: Resting metabolic rate and pacing profile PLoS ONE 2017 12 e0173807 10.1371/journal.pone.0173807 28296943 PMC5351856 · DOI
  26. [31]McColl E.M. Wheeler G.D. Gomes P. Bhambhani Y. Cumming D.C. The effects of acute exercise on pulsatile LH release in high-mileage male runners Clin. Endocrinol. 1989 31 617 621 10.1111/j.1365-2265.1989.tb01286.x 2627755 · DOI · Paper page
  27. [32]Hackney A.C. Sinning W.E. Bruot B.C. Reproductive hormonal profiles of endurance-trained and untrained males Med. Sci. Sports Exerc. 1988 20 60 65 10.1249/00005768-198802000-00009 3343919 · DOI · Paper page
  28. [33]Roberts A.C. McClure R.D. Weiner R.I. Brooks G.A. Overtraining affects male reproductive status Fertil. Steril. 1993 60 686 692 10.1016/S0015-0282(16)56223-2 8405526 · DOI · Paper page
  29. [34]Stenqvist T.B. Torstveit M.K. Faber J. Melin A.K. Impact of a 4-Week intensified endurance training intervention on markers of Relative Energy Deficiency in Sport (RED-S) and performance among well-trained male cyclists Front. Endocrinol. 2020 11 512365 10.3389/fendo.2020.512365 PMC7545350 33101190 · DOI
  30. [38]Degoutte F. Jouanel P. Begue R.J. Colombier M. Lac G. Pequignot J.M. Filaire E. Food restriction, performance, biochemical, psychological, and endocrine changes in judo athletes Int. J. Sports Med. 2006 27 9 18 10.1055/s-2005-837505 16388436 · DOI
  31. [39]Hagmar M. Berglund B. Brismar K. Hirschberg A.L. Body composition and endocrine profile of male Olympic athletes striving for leanness Clin. J. Sport Med. 2013 23 197 201 10.1097/JSM.0b013e31827a8809 23275346 · DOI
  32. [40]Fudge B.W. Wilson J. Easton C. Irwin L. Clark J. Haddow O. Kayser B. Pitsiladis Y.P. Estimation of oxygen uptake during fast running using accelerometry and heart rate Med. Sci. Sports Exerc. 2007 39 192 198 10.1249/01.mss.0000235884.71487.21 17218902 · DOI
  33. [41]Vogt S. Heinrich L. Schumacher Y.O. Grosshauser M. Blum A. Konig D. Berg A. Schmid A. Energy intake and energy expenditure of elite cyclists during preseason training Int. J. Sports Med. 2005 26 701 706 10.1055/s-2004-830438 16158378 · DOI
  34. [42]Abedelmalek S. Chtourou H. Souissi N. Tabka Z. Caloric Restriction Effect on Proinflammatory Cytokines, Growth Hormone, and Steroid Hormone Concentrations during Exercise in Judokas Oxid. Med. Cell Longev. 2015 2015 809492 10.1155/2015/809492 26075039 PMC4446567 · DOI
  35. [43]Dolan E. McGoldrick A. Davenport C. Kelleher G. Byrne B. Tormey W. Smith D. Warrington G.D. An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys J. Bone Min. Metab. 2012 30 534 542 10.1007/s00774-012-0354-4 22491874 · DOI
  36. [44]Guillaume G. Chappard D. Audran M. Evaluation of the bone status in high-level cyclists J. Clin. Densitom. 2012 15 103 107 10.1016/j.jocd.2011.08.001 22071023 · DOI
  37. [45]Olmedillas H. Gonzalez-Aguero A. Moreno L.A. Casajus J.A. Vicente-Rodriguez G. Bone related health status in adolescent cyclists PLoS ONE 2011 6 e24841 10.1371/journal.pone.0024841 21980360 PMC3184100 · DOI
  38. [46]Cumming D.C. Wheeler G.D. McColl E.M. The effects of exercise on reproductive function in men Sports Med. 1989 7 1 17 10.2165/00007256-198907010-00001 2652242 · DOI · Paper page
  39. [47]Murphy C. Koehler K. Energy deficiency impairs resistance training gains in lean mass but not strength: A meta-analysis and meta-regression Scand. J. Med. Sci. Sports 2022 32 125 137 10.1111/sms.14075 34623696 · DOI
  40. [48]Burke L.M. Lundy B. Fahrenholtz I.L. Melin A.K. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes Int. J. Sport Nutr. Exerc. Metab. 2018 28 350 363 10.1123/ijsnem.2018-0142 30029584 · DOI · Paper page
  41. [49]Ackerman K.E. Holtzman B. Cooper K.M. Flynn E.F. Bruinvels G. Tenforde A.S. Popp K.L. Simpkin A.J. Parziale A.L. Low energy availability surrogates correlate with health and performance consequences of Relative Energy Deficiency in Sport Br. J. Sports Med. 2019 53 628 633 10.1136/bjsports-2017-098958 29860237 · DOI · Paper page
  42. [50]Melin A. Tornberg A.B. Skouby S. Moller S.S. Sundgot-Borgen J. Faber J. Sidelmann J.J. Aziz M. Sjodin A. Energy availability and the female athlete triad in elite endurance athletes Scand. J. Med. Sci. Sports 2015 25 610 622 10.1111/sms.12261 24888644 · DOI
  43. [51]Kaufman B.A. Warren M.P. Dominguez J.E. Wang J. Heymsfield S.B. Pierson R.N. Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels J. Clin. Endocrinol. Metab. 2002 87 2777 2783 10.1210/jcem.87.6.8565 12050250 · DOI
  44. [52]Grande F. Anderson J.T. Keys A. Changes of basal metabolic rate in man in semistarvation and refeeding J. Appl. Physiol. 1958 12 230 238 10.1152/jappl.1958.12.2.230 13525268 · DOI · Paper page
  45. [53]Papageorgiou M. Dolan E. Elliott-Sale K.J. Sale C. Reduced energy availability: Implications for bone health in physically active populations Eur. J. Nutr. 2018 57 847 859 10.1007/s00394-017-1498-8 28721562 PMC5861178 · DOI
  46. [54]Gomez-Merino D. Chennaoui M. Drogou C. Bonneau D. Guezennec C.Y. Decrease in serum leptin after prolonged physical activity in men Med. Sci. Sports Exerc. 2002 34 1594 1599 10.1097/00005768-200210000-00010 12370560 · DOI
  47. [55]Wheeler G.D. Singh M. Pierce W.D. Epling W.F. Cumming D.C. Endurance training decreases serum testosterone levels in men without change in luteinizing hormone pulsatile release J. Clin. Endocrinol. Metab. 1991 72 422 425 10.1210/jcem-72-2-422 1899423 · DOI
  48. [56]Bennell K.L. Brukner P.D. Malcolm S.A. Effect of altered reproductive function and lowered testosterone levels on bone density in male endurance athletes Br. J. Sports Med. 1996 30 205 208 10.1136/bjsm.30.3.205 8889111 PMC1332330 · DOI
  49. [57]Kyrolainen H. Karinkanta J. Santtila M. Koski H. Mantysaari M. Pullinen T. Hormonal responses during a prolonged military field exercise with variable exercise intensity Eur. J. Appl. Physiol. 2008 102 539 546 10.1007/s00421-007-0619-0 18040709 · DOI
  50. [58]Torstveit M.K. Fahrenholtz I. Stenqvist T.B. Sylta O. Melin A. Within-day energy deficiency and metabolic perturbation in male endurance athletes Int. J. Sport Nutr. Exerc. Metab. 2018 28 419 427 10.1123/ijsnem.2017-0337 29405793 · DOI
  51. [59]Melin A. Tornberg A.B. Skouby S. Faber J. Ritz C. Sjodin A. Sundgot-Borgen J. The LEAF questionnaire: A screening tool for the identification of female athletes at risk for the female athlete triad Br. J. Sports Med. 2014 48 540 545 10.1136/bjsports-2013-093240 24563388 · DOI · Paper page
  52. [60]Magee M.K. Lockard B.L. Zabriskie H.A. Schaefer A.Q. Luedke J.A. Erickson J.L. Jones M.T. Jagim A.R. Prevalence of low energy availability in collegiate women soccer athletes J. Funct. Morphol. Kinesiol. 2020 5 96 10.3390/jfmk5040096 PMC7804888 33467311 · DOI
  53. [61]Meng K. Qiu J. Benardot D. Carr A. Yi L. Wang J. Liang Y. The risk of low energy availability in Chinese elite and recreational female aesthetic sports athletes J. Int. Soc. Sports Nutr. 2020 17 13 10.1186/s12970-020-00344-x 32131846 PMC7055083 · DOI
  54. [62]Folscher L.L. Grant C.C. Fletcher L. Janse van Rensberg D.C. Ultra-marathon athletes at risk for the Female Athlete Triad Sports Med. Open 2015 1 29 10.1186/s40798-015-0027-7 26380807 PMC4564455 · DOI
  55. [63]Rogers M.A. Appaneal R.N. Hughes D. Vlahovich N. Waddington G. Burke L.M. Drew M. 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 10.1136/bjsports-2019-101517 33199358 · DOI · Paper page
  56. [64]Drew M.K. Vlahovich N. Hughes D. Appaneal R. Peterson K. Burke L. Lundy B. Toomey M. Watts D. Lovell G. A multifactorial evaluation of illness risk factors in athletes preparing for the Summer Olympic Games J. Sci. Med. Sport 2017 20 745 750 10.1016/j.jsams.2017.02.010 28385561 · DOI
  57. [65]Black K. Slater J. Brown R.C. Cooke R. Low energy availability, plasma lipids, and hormonal profiles of recreational athletes J. Strength Cond. Res. 2018 32 2816 2824 10.1519/JSC.0000000000002540 29624522 · DOI · Paper page
  58. [67]Slater J. Low Energy availability in New Zealand recreational athletes Master’s Thesis University of Otago Dunedin, New Zealand 2015
  59. [68]Hackney A.C. Lane A.R. Register-Mihalik J. O’Leary C.B. Endurance Exercise Training and Male Sexual Libido Med. Sci. Sports Exerc. 2017 49 1383 1388 10.1249/MSS.0000000000001235 28195945 · DOI · Paper page
  60. [70]Logue D.M. Madigan S.M. Melin A. McDonnell S.J. Delahunt E. Heinen M. Corish C.A. Self-reported reproductive health of athletic and recreationally active males in Ireland: Potential health effects interfering with performance Eur. J. Sport Sci. 2021 21 275 284 10.1080/17461391.2020.1748116 32212923 · DOI
  61. [71]Foley Davelaar C.M. Ostrom M. Schulz J. Trane K. Wolkin A. Granger J. Validation of an age-appropriate screening tool for Female Athlete Triad and Relative Energy Deficiency in Sport in young athletes Cureus 2020 12 e8579 10.7759/cureus.8579 32670715 PMC7358951 · DOI
  62. [72]Parmigiano T.R. Zucchi E.V. Araujo M.P. Guindalini C.S. Castro Rde A. Di Bella Z.I. Girao M.J. Cohen M. Sartori M.G. Pre-participation gynecological evaluation of female athletes: A new proposal Einstein 2014 12 459 466 10.1590/S1679-45082014AO3205 25628197 PMC4879912 · DOI
  63. [73]Mountjoy M. Sundgot-Borgen J. Burke L. Carter S. Constantini N. Lebrun C. Meyer N. Sherman R. Steffen K. Budgett R. RED-S CAT. Relative Energy Deficiency in Sport (RED-S) Clinical Assessment Tool (CAT) Br. J. Sports Med. 2015 49 421 423 10.1136/bjsports-2015-094873 25896450 · DOI · Paper page
  64. [74]Mohamed O. Freundlich R.E. Dakik H.K. Grober E.D. Najari B. Lipshultz L.I. Khera M. The quantitative ADAM questionnaire: A new tool in quantifying the severity of hypogonadism Int. J. Impot. Res. 2010 22 20 24 10.1038/ijir.2009.35 19657348 PMC2834355 · DOI
  65. [75]Kallus W. Kellmann M. The Recovery-Stress Questionnaires: User Manual Pearson Assessment & Information GmbH Franfurt, Germany 2016
  66. [76]Nana A. Slater G.J. Hopkins W.G. Halson S.L. Martin D.T. West N.P. Burke L.M. Importance of standardized DXA protocol for assessing physique changes in athletes Int. J. Sport Nutr. Exerc. Metab. 2016 26 259 267 10.1123/ijsnem.2013-0111 24458265 · DOI
  67. [77]Nana A. Slater G.J. Stewart A.D. Burke L.M. Methodology review: Using dual-energy X-ray absorptiometry (DXA) for the assessment of body composition in athletes and active people Int. J. Sport Nutr. Exerc. Metab. 2015 25 198 215 10.1123/ijsnem.2013-0228 25029265 · DOI · Paper page
  68. [78]Haugen H.A. Chan L.N. Li F. Indirect calorimetry: A practical guide for clinicians Nutr. Clin. Pr. 2007 22 377 388 10.1177/0115426507022004377 17644692 · DOI
  69. [79]Weir J.B. New methods for calculating metabolic rate with special reference to protein metabolism J. Physiol. 1949 109 1 9 10.1113/jphysiol.1949.sp004363 15394301 PMC1392602 · DOI
  70. [81]Bone J.L. Burke L.M. No difference in young adult athletes’ resting energy expenditure when measured under inpatient or outpatient conditions Int. J. Sport Nutr. Exerc. Metab. 2018 28 464 467 10.1123/ijsnem.2016-0315 29140154 · DOI
  71. [82]Cunningham J.J. A reanalysis of the factors influencing basal metabolic rate in normal adults Am. J. Clin. Nutr. 1980 33 2372 2374 10.1093/ajcn/33.11.2372 7435418 · DOI · Paper page
  72. [83]Hackney A.C. Viru A. Research methodology: Endocrinologic measurements in exercise science and sports medicine J. Athl. Train. 2008 43 631 639 10.4085/1062-6050-43.6.631 19030142 PMC2582556 · DOI
  73. [85]Hackney A.C. Lane A.R. Increased prevalence of androgen deficiency in endurance-trained male runners across the life span Aging Male 2020 23 168 10.1080/13685538.2018.1523888 30457033 · DOI
  74. [86]Fawcett T. An introduction to ROC analysis Pattern Recognit. Lett. 2006 27 861 874 10.1016/j.patrec.2005.10.010 · DOI · Paper page
  75. [87]Fluss R. Faraggi D. Reiser B. Estimation of the Youden Index and its associated cutoff point Biom. J. J. Math. Methods Biosci. 2005 47 458 472 10.1002/bimj.200410135 16161804 · DOI
  76. [90]Nindl B.C. Alemany J.A. Kellogg M.D. Rood J. Allison S.A. Young A.J. Montain S.J. 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. 2007 103 340 346 10.1152/japplphysiol.01321.2006 17412783 · DOI
  77. [91]De Souza M.J. Nattiv A. Joy E. Misra M. Williams N.I. Mallinson R.J. Gibbs J.C. Olmsted M. Goolsby M. Matheson G. 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 24463911
  78. [92]Friedl K.E. Moore R.J. Martinez-Lopez L.E. Vogel J.A. Askew E.W. Marchitelli L.J. Hoyt R.W. Gordon C.C. Lower limit of body fat in healthy active men J. Appl. Physiol. 1994 77 933 940 10.1152/jappl.1994.77.2.933 8002550 · DOI
  79. [93]Silla J.K.E. Brigham S.K. Goldstein M. Misra M. Singhal V. Clinical, biochemical, and hematological characteristics of community-dwelling adolescent and young adult males with anorexia nervosa Int. J. Eat. Disord. 2021 54 2213 2217 10.1002/eat.23622 34617624 · DOI
  80. [94]Rogers M.A. Drew M.K. Appaneal R. Lovell G. Lundy B. Hughes D. Vlahovich N. Waddington G. Burke L.M. The utility of the Low Energy Availability in Females Questionnaire to detect markers consistent with low energy availability-related conditions in a mixed-sport cohort Int. J. Sport Nutr. Exerc. Metab. 2021 31 427 437 10.1123/ijsnem.2020-0233 34284349 · DOI
  81. [95]Rauh M.J. Barrack M. Nichols J.F. Associations between the female athlete triad and injury among high school runners Int. J. Sports Phys. 2014 9 948 958 PMC4275199 25540710
  82. [96]Heikura I.A. Uusitalo A.L.T. Stellingwerff T. Bergland D. Mero A.A. Burke L.M. Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes Int. J. Sport Nutr. Exerc. Metab. 2018 28 403 411 10.1123/ijsnem.2017-0313 29252050 · DOI · Paper page
  83. [97]Stenqvist T.B. Melin A.K. Garthe I. Slater G. Paulsen G. Iraki J. Areta J. Torstveit M.K. Prevalence of surrogate markers of Relative Energy Deficiency in male Norwegian Olympic-level athletes Int. J. Sport Nutr. Exerc. Metab. 2021 31 497 506 10.1123/ijsnem.2020-0368 34489365 · DOI · Paper page
  84. [98]Hooper D.R. Kraemer W.J. Saenz C. Schill K.E. Focht B.C. Volek J.S. Maresh C.M. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition Eur. J. Appl. Physiol. 2017 117 1349 1357 10.1007/s00421-017-3623-z 28470410 · DOI · Paper page
  85. [99]Shimizu K. Suzuki N. Nakamura M. Aizawa K. Imai T. Suzuki S. Eda N. Hanaoka Y. Nakao K. Suzuki N. Mucosal immune function comparison between amenorrheic and eumenorrheic distance runners J. Strength Cond. Res. 2012 26 1402 1406 10.1519/JSC.0b013e31822e7a6c 22516912 · DOI
  86. [100]Walsh N.P. Nutrition and Athlete Immune Health: New Perspectives on an Old Paradigm Sports Med. 2019 49 153 168 10.1007/s40279-019-01160-3 31691927 PMC6901425 · DOI
  87. [101]Hanstock H.G. Govus A.D. Stenqvist T.B. Melin A.K. Sylta O. Torstveit M.K. Influence of Immune and Nutritional Biomarkers on Illness Risk During Interval Training Int. J. Sports Physiol. Perform. 2019 15 60 67 10.1123/ijspp.2018-0527 31034260 · DOI
  88. [102]Deutz R.C. Benardot D. Martin D.E. Cody M.M. Relationship between energy deficits and body composition in elite female gymnasts and runners Med. Sci. Sports Exerc. 2000 32 659 668 10.1097/00005768-200003000-00017 10731010 · DOI
  89. [103]Stone N.J. Secondary causes of hyperlipidemia Med. Clin. North Am. 1994 78 117 141 10.1016/S0025-7125(16)30179-1 8283927 · DOI · Paper page
  90. [104]Hildebrandt T. Walker D.C. Alfano L. Delinsky S. Bannon K. Development and validation of a male specific body checking questionnaire Int. J. Eat. Disord. 2010 43 77 87 10.1002/eat.20669 19247988 PMC2892168 · DOI
  91. [105]Schaefer L.M. Smith K.E. Leonard R. Wetterneck C. Smith B. Farrell N. Riemann B.C. Frederick D.A. Schaumberg K. Klump K.L. Identifying a male clinical cutoff on the Eating Disorder Examination-Questionnaire (EDE-Q) Int. J. Eat. Disord. 2018 51 1357 1360 10.1002/eat.22972 30480321 PMC6310481 · DOI
  92. [106]Mond J. Hall A. Bentley C. Harrison C. Gratwick-Sarll K. Lewis V. Eating-disordered behavior in adolescent boys: Eating disorder examination questionnaire norms Int. J. Eat. Disord. 2014 47 335 341 10.1002/eat.22237 24338639 · DOI
  93. [107]Cartagena-Ramos D. Fuentealba-Torres M. Rebustini F. Leite A. Alvarenga W.A. Arcencio R.A. Dantas R.A.S. Nascimento L.C. Systematic review of the psychometric properties of instruments to measure sexual desire BMC Med. Res. Methodol. 2018 18 109 10.1186/s12874-018-0570-2 30340533 PMC6194697 · DOI
  94. [108]Dipla K. Kraemer R.R. Constantini N.W. Hackney A.C. Relative energy deficiency in sports (RED-S): Elucidation of endocrine changes affecting the health of males and females Hormones 2021 20 35 47 10.1007/s42000-020-00214-w 32557402 · DOI
  95. [109]Piontek A. Szeja J. Blachut M. Badura-Brzoza K. Sexual problems in the patients with psychiatric disorders Wiadomosci Lekarskie 2019 72 1984 1988 10.36740/WLek201910125 31982027 · DOI
  96. [110]Lane A.R. Hackney A.C. Smith-Ryan A.E. Kucera K. Register-Mihalik J.K. Ondrak K. Energy availability and RED-S risk factors in competitive, non-elite male endurance athletes Transl. Med. Exerc. Prescr. 2021 1 25 32 10.53941/tmep.v1i1.29 34296227 PMC8294781 · DOI
  97. [111]Logue D. Madigan S.M. Delahunt E. Heinen M. Mc Donnell S.J. Corish C.A. Low Energy Availability in Athletes: A Review of Prevalence, Dietary Patterns, Physiological Health, and Sports Performance Sports Med. 2018 48 73 96 10.1007/s40279-017-0790-3 28983802 · DOI · Paper page
  98. [113]Koehler K. Achtzehn S. Braun H. Mester J. Schaenzer W. 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 10.1139/apnm-2012-0373 23980730 · DOI

Cited by

Sorted by citations

Authors
Lundy, B., Torstveit, M. K., Stenqvist, T. B., Burke, L. M., Garthe, I., Slater, G. J., Ritz, C., & Melin, A. K.
Affiliations
  • Australian Catholic University (AU)
  • University of Agder (NO)
  • Norwegian Olympic Sports Centre, Department of Sports Nutrition, 0806 Oslo, Norway
  • University of the Sunshine Coast (AU)
  • Danish National Institute of Public Health (DK)
  • Linnaeus University (SE)
Corresponding author
Burke, Louise M.
Venue
Nutrients
Publisher
MDPI AG
Published
2022-04-29
Volume
14
Issue
9
Pages
1873
ISSN
2072-6643 (ISSN-L)
OpenAlex
W4225264738
Cited by
70
References
14
Citations by year
2026: 27 · 2025: 11 · 2024: 12 · 2023: 14 · 2022: 3 · 2020: 2 · 2019: 1
FWCI
9.13
Type
journal article
Language
en
Open access
Locations
  • Nutrients (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Diva portal (Dalarna University Library) (submittedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
  • University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, cc-by)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
Topics
  • Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
  • Health Sciences › Nursing › Nutrition and Dietetics › Nutrition, Health and Food Behavior
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
low energy availability, male athletes, screening questionnaire, questionnaire validation, sexual desire, dizziness, fatigue, illness, thermoregulation, gastrointestinal symptoms, injuries, recovery, sleep, endurance sports
MeSH terms
Dizziness, Female, Humans, Male, Surveys and Questionnaires, Reproducibility of Results, Biomarkers, Athletes, Sports Nutritional Physiological Phenomena

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