Cited by 45Sports Performance and TrainingEating Disorders and BehaviorsMuscle metabolism and nutrition

Prevalence of low energy availability in competitively trained male endurance athletes

Open access
Lane, Amy R., Hackney, Anthony C., Smith-Ryan, Abbie, Kucera, Kristen, Registar-Mihalik, Johna, Ondrak, Kristin·2019·Medicina

Abstract

Background and Objectives: Relative energy deficiency in sport (RED-S) has been introduced as a broad-spectrum syndrome leading to possible dysfunction in numerous physiological systems, driven primarily by low energy availability (EA). Research in females has identified specific EA cut-points indicative of risk level for developing physiological and performance disturbances. Cut-points in males have yet to be evaluated. This study examined the prevalence of low EA in competitive (non-elite), recreationally trained (CRT) male endurance athletes. Materials and Methods: Subjects were 108 CRT (38.6 ± 13.8 y; 12.2 ± 5.4 h/wk training) male endurance athletes (runners, cyclists, triathletes) who completed a descriptive survey online via Qualtrics® and returned 3 day diet and exercise training records. EA was calculated from returned surveys and training records. Resting metabolic rate (RMR) and lean body mass (LBM) were estimated from self-reported survey data. Prevalence of risk group was categorized based on the female cut-points: At risk (AR) ≤30 kcal/kg LBM, moderate risk (MR) = 30–45 kcal/kg LBM, or no risk (NR) ≥45 kcal/kg LBM. Results: In this sample, 47.2% (n = 51) were classified as AR, 33.3% (n = 36) as MR, and 19.4% (n = 21) as NR for low EA. Cyclists had lower EA (26.9 ± 17.4 kcal/kg LBM, n = 45) than runners (34.6 ± 13.3 kcal/kg LBM, n = 55, p = 0.016) and all other sport categories (39.5 ± 19.1 kcal/kg LBM, n = 8, p = 0.037). Conclusions: The findings indicate this sample had a high prevalence of risk for low EA, at 47.2%. Only 19.4% of participants were at no risk, meaning ~80% of participants were at some degree of risk of experiencing low EA. Cyclists were at greater risk in this cohort of low EA, although why this occurred was unclear and is in need of further investigation. Future research should address whether the current female cut-points for low EA are appropriate for use in male populations.

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/medicina55100665

Cites

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?

  • While a universal cut-off of 30 kcal/kg FFM/day as a threshold of LEA leading to some REDs outcomes in females is debated, such a cut-off or range at which males experience REDs-related symptoms is even less understood, but appears to be lower (eg, ~9 to 25 kcal/kg FFM/day).

    “While a universal cut-off of 30 kcal/kg FFM/day as a threshold of LEA leading to some REDs outcomes in females is debated, 88 such a cut-off or range at which males experience REDs-related symptoms is even less understood, 89 but appears to be lower (eg, ~9 to 25 kcal/kg FFM/day).17 46 72 90 91”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [17]

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured
  • There is evidence that most males can sustain a lower EA before physiological and psychological disturbances manifest.

    “Indeed, there is evidence that most males can sustain a lower EA before physiological and psychological disturbances manifest.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [17]

    Section 4.2 suggests that men may require a greater reduction in energy availability before dysfunction occurs, but says the appropriate male thresholds remain unknown. It does not establish that most males can sustain a lower level, or assess when psychological disturbances manifest. (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.

The citation lists haven’t been fetched yet

References 35 · Cited by 45

Research works printed but not linked: 27

  1. [3]Loucks A.B. Mortola J.F. Girton L. Yen S.S.C. Alterations in the hypothalamic-pituitary-ovarian and the hypothalamic-pituitary-adrenal axes in athletic women J. Clin. Endocrinol. Metab. 1989 68 402 411 10.1210/jcem-68-2-402 2537332 · DOI
  2. [4]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 Br. J. Sports Med. 2014 48 289 10.1136/bjsports-2013-093218 25014387 · DOI · Paper page
  3. [6]Loucks A.B. Low energy availability in the marathon and other endurance sports Sports Med. 2007 37 348 352 10.2165/00007256-200737040-00019 17465605 · DOI
  4. [7]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. 2015 25 594 602 10.1123/ijsnem.2015-0073 26131616 · DOI · Paper page
  5. [8]Koehler K. Achtzehn S. Braun H. Mester J. Schnaezer 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
  6. [9]Heikura I.A. Uusitalo A.L. Stellingwerff T. Bergland D. Antti A.M. 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
  7. [10]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
  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. [15]Stewart A.L. Mills K.M. King A.C. Haskell W.L. Gillis D. Ritter P.L. CHAMPS physical activity questionnaire for older adults: Outcomes for interventions Med. Sci. Sports Exerc. 2001 33 1126 1141 10.1097/00005768-200107000-00010 11445760 · DOI
  10. [16]Ainsworth B.E. Haskell W.L. Herrmann S.D. Meckes N. Bassett D.R. Jr. Tudor-Locke C. Greer J.L. Vezina J. Whitt-Glover M.C. Leon A.S. 2011 Compendium of Physical Activities: A second update of codes and MET values Med. Sci. Sports Exerc. 2011 43 1575 1581 10.1249/MSS.0b013e31821ece12 21681120 · DOI · Paper page
  11. [17]Boer P. Estimated lean body mass as an index for normalization of body fluid volumes in man Am. J. Physiol. 1984 247 F632 F635 6496691
  12. [19]Neilson H.K. Robson P.J. Friedenreich C.M. Csizmadi I. Estimating activity energy expenditure: How valid are physical activity questionnaires? Am. J. Clin. Nutr. 2008 87 279 291 10.1093/ajcn/87.2.279 18258615 · DOI
  13. [20]Thompson J. Manore M.M. Predicted and measured resting metabolic rate of male and female endurance athletes J. Am. Diet Assoc. 1996 96 30 34 10.1016/S0002-8223(96)00010-7 8537566 · DOI
  14. [24]Whaley M.H. Brubaker P.H. Otto R.M. ACSM’s Guidelines for Exercise Testing and Prescription 7th ed. Lippincott Williams &Wilkins Philadelphia, PA, USA 2006
  15. [25]Melin A. Tornberg A.B. Scouby 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 Brit. J. Sport Med. 2014 48 540 545 10.1136/bjsports-2013-093240 24563388 · DOI · Paper page
  16. [26]Melin A. Tornberg A.B. Skouby S. Moller S.S. Sundgot-Borgen J. Faber J. 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
  17. [27]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 1 7 10.1136/bmjsem-2018-000424 30364549 PMC6196965 · DOI
  18. [28]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
  19. [29]Schaal K. Van Loan M.D. Casazza G.A. Reduced catecholamine response to exercise in amenorrheic athletes Med. Sci. Sports Exerc. 2011 43 34 43 10.1249/MSS.0b013e3181e91ece 20508538 · DOI
  20. [30]Hoch A.Z. Pajewski N.M. Moraski L. Carrera G.F. Wilson C.R. Hoffmann R.G. Gutterman D.D. Prevalence of the female athlete triad in high school athletes and sedentary students Clin. J. Sport Med. 2009 19 421 428 10.1097/JSM.0b013e3181b8c136 19741317 PMC2848387 · DOI
  21. [31]Bronson F.H. Mammalian reproduction: An ecological perspective Biol. Reprod. 1985 32 1 26 10.1095/biolreprod32.1.1 3882162 · DOI
  22. [32]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
  23. [33]Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: A review Int. J. Sport Nutr. Exerc. Metab. 2018 28 385 402 10.1123/ijsnem.2016-0332 28530498 · DOI
  24. [34]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
  25. [35]Capling L. Beck K.L. Gifford J.A. Slater G. Flood V.M. O’Connor H. Validity of dietary assessments in athletes: A systematic review Nutrients 2017 9 1313 10.3390/nu9121313 29207495 PMC5748763 · DOI
  26. [36]Yang Y.J. Kim M.K. Hwang S.H. Ahn Y. Shim J.E. Kim D.H. Relative validities of 3-day food records and the food frequency questionnaire Nutr. Res. Pract. 2010 4 142 148 10.4162/nrp.2010.4.2.142 20461203 PMC2867225 · DOI
  27. [37]El-Kateb S.I. Sridharan S. Farrington K. Davenport D. Comparison of resting and total energy expenditure in peritoneal dialysis patients and body composition measured by dual-energy X-ray absorptiometry Eur. J. Clin. Nutr. 2016 70 1337 1339 10.1038/ejcn.2016.120 27380882 · DOI

Authors
Lane, A. R., Hackney, A. C., Smith-Ryan, A., Kucera, K., Registar-Mihalik, J., & Ondrak, K.
Affiliations
  • University of North Carolina at Chapel Hill (US)
  • Curriculum of Human Movement Science, University of North Carolina at Chapel Hill, Chapel Hill, NC 27516, USA
Corresponding author
Hackney, Anthony C.
Venue
Medicina
Publisher
MDPI AG
Published
2019-10-01
Volume
55
Issue
10
Pages
665
ISSN
  • 1010-660X (ISSN-L)
  • 1648-9144
OpenAlex
W2438393107
Cited by
45
References
35
Citations by year
2026: 3 · 2025: 5 · 2024: 9 · 2023: 9 · 2022: 6 · 2021: 8 · 2020: 5
FWCI
5.05
Type
journal article
Language
en
Open access
Locations
  • Medicina (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
  • Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords
low energy availability, relative energy deficiency in sport, recreational athletes, prevalence, cyclists, runners, triathletes, resting metabolic rate, lean body mass, sex differences
MeSH terms
Adult, Cross-Sectional Studies, Humans, Male, North Carolina, Nutritional Requirements, Surveys and Questionnaires, Running, Exercise, Prevalence, Malnutrition, Young Adult, 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