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Hungry runners – low energy availability in male endurance athletes and its impact on performance and testosterone: mini-review

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Cupka, Martin, Sedliak, Milan·2023·European Journal of Translational Myology
DOI 10.4081/ejtm.2023.11104PMC PMC10388605
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Abstract

Low Energy Availability (LEA) arises from the inability to cover energy needs and requirements of training or normal physiological functions. This value differs from the energy balance, which takes into account the total daily energy intake compared to all the energy expended, regardless of the amount of fat-free mass. Insufficient energy consumption affects recovery, adaptation processes, increases the risk of injury or illness, so all of this can negatively affect performance. This mini-review is written on research articles in Pubmed database related to LEA in endurance-trained men and its impact on performance and testosterone. This article also clarifies the prevalence of LEA in male endurance athletes and its correlation to Relative Energy Deficiency in Sports (RED-S). LEA occurs in male endurance athletes and correlates with decreased testosterone levels, decreased bone density and also Resting Metabolic Rate. In endurance-trained men, there is great potential for the negative consequences of low energy availability. It can also be said that there are possibilities for primary screening, so we recommend regular check-ups of blood markers, body structure and keeping not only training but also dietary records, which can increase awareness of an adequate energy balance.

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  • Low energy availability can be detrimental to athletes, as insufficient caloric intake leads to decreased aerobic and anaerobic performance, poor muscle regeneration, and higher injury incidence leading to missed training.

    “Low energy availability can be detrimental to athletes, as insufficient caloric intake leads to decreased aerobic and anaerobic performance, poor muscle regeneration, and higher injury incidence leading to missed training [89].”

    From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [89]

    The “Energy availability and endurance performance in males” section (page unavailable) reports decreased aerobic and anaerobic performance in cyclists, worsened regeneration in rowers, and increased injury risk with low energy availability. It also reports more missed training among athletes at risk of low energy availability, but describes that training loss as disease-related, not injury-related. The cited passage does not specifically establish poor muscle regeneration. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • An immediate boost in performance with decreased body weight is far from guaranteed, and athletes may experience performance stagnation, fatigue-related injuries, or gastrointestinal problems with even short-term LEA.

    “However, an immediate boost in performance with decreased body weight is far from guaranteed, and athletes may experience performance stagnation, fatigue-related injuries, or gastrointestinal problems with even short-term LEA [89].”

    From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [89]

    The Final considerations section (page unavailable) describes a trade-off between lower body weight and LEA and lists performance stagnation, fatigue fractures, and digestive problems as possible manifestations. The Energy availability and endurance performance in males section reports worsened performance after four weeks of reduced energy supply. The copy does not establish that fatigue fractures or digestive problems can occur with even short-term LEA. (LLM, conf=0.86)

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Research works printed but not linked: 50

  1. [1]Sundgot-Borgen J Torstveit MK. Aspects of disordered eating continuum in elite high-intensity sports. Scand J Med Sci Sports. 2010 Oct;20 Suppl 2: 112- 21. doi: 10.1111/j.1600-0838.2010.01190.x. PMID: 20840569. 20840569 · DOI
  2. [2]Slater J Brown R McLay-Cooke R Black K. Low Energy Availability in Exercising Women: Historical Perspectives and Future Directions. Sports Med. 2017 Feb; 47(2): 207- 220. doi: 10.1007/s40279-016-0583-0. PMID: 27430502. 27430502 · DOI · Paper page
  3. [3]Mountjoy M Sundgot-Borgen JK Burke LM Ackerman KE Blauwet C Constantini N Lebrun C Lundy B Melin AK Meyer NL Sherman RT Tenforde AS Klungland Torstveit M Budgett R. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018 Jun; 52(11): 687- 697. doi: 10.1136/bjsports-2018-099193. PMID: 29773536. 29773536 · DOI · Paper page
  4. [4]De Souza MJ Koltun KJ. Williams NI. What is the evidence for a Triad-like syndrome in exercising men? Current Opinion in Physiology. 2019 Apr; 10. doi:10.1016/j.cophys.2019.04.002 · DOI
  5. [5]Nattiv A De Souza MJ Koltun KJ Misra M Kussman A Williams NI Barrack MT 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 Jul 1; 31(4): 345- 353. doi 10.1097/JSM.0000000000000946. PMID: 34091537. 34091537 · DOI
  6. [6]Loucks AB Kiens B Wright HH. Energy availability in athletes. J Sports Sci. 2011; 29 Suppl 1: S7- 15. doi: 10.1080/02640414.2011.588958. Epub 2011 Jul 28. PMID: 21793767. 21793767 · DOI · Paper page
  7. [8]Loucks AB Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003 Jan; 88(1): 297- 311. doi: 10.1210/jc.2002-020369. PMID: 12519869. 12519869 · DOI · Paper page
  8. [10]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 Jul; 38(7): 725- 33. doi: 10.1139/apnm-2012-0373. Epub 2013 Jan 30. PMID: 23980730. 23980730 · DOI
  9. [11]van Erp-Baart AM Saris WH Binkhorst RA Vos JA Elvers JW. Nationwide survey on nutritional habits in elite athletes. Part I. Energy, carbohydrate, protein, and fat intake. Int J Sports Med. 1989 May;10 Suppl 1: S3- 10. doi: 10.1055/s-2007-1024947. PMID: 2744927. 2744927 · DOI
  10. [12]Heikura IA Burke LM Bergland D Uusitalo ALT Mero AA 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 Sep 1; 13(8): 1090- 1096. doi: 10.1123/ijspp.2017-0547. Epub 2018 Sep 13. PMID: 29431548. 29431548 · DOI · Paper page
  11. [13]Stubbs RJ O'Reilly LM Whybrow S Fuller Z Johnstone AM Livingstone MB Ritz P Horgan GW. Measuring the difference between actual and reported food intakes in the context of energy balance under laboratory conditions. Br J Nutr. 2014 Jun 14; 111(11): 2032- 43. doi: 10.1017/S0007114514000154. Epub 2014 Mar 17. PMID: 24635904. 24635904 · DOI
  12. [14]Shephard RJ Aoyagi Y. Measurement of human energy expenditure, with particular reference to field studies: an historical perspective. Eur J Appl Physiol. 2012 Aug; 112(8): 2785- 815. doi: 10.1007/s00421-011-2268-6. Epub 2011 Dec 11. PMID: 22160180. 22160180 · DOI
  13. [15]Murakami H Kawakami R Nakae S Nakata Y Ishikawa-Takata K Tanaka S Miyachi M. Accuracy of Wearable Devices for Estimating Total Energy Expenditure: Comparison With Metabolic Chamber and Doubly Labeled Water Method. JAMA Intern Med. 2016 May 1; 176(5): 702- 3. doi: 10.1001/jamainternmed.2016.0152. PMID: 26999758. 26999758 · DOI · Paper page
  14. [16]Heaney S O’Connor H Naughton G Gifford J. Towards an understanding of the barriers to good nutrition for elite athletes. International Journal of Sports Science&Coaching. 2008 Sep; 3(3), 391– 401. 10.1260/174795408786238542 · DOI
  15. [18]Eichstadt M Luzier J Cho D Weisenmuller C. Eating Disorders in Male Athletes. Sports Health. 2020 Jul/Aug; 12(4): 327- 333. doi: 10.1177/1941738120928991. Epub 2020 Jun 11. PMID: 32525767; PMCID: PMC7787561. 32525767 PMC7787561 · DOI
  16. [19]Ferrand C Brunet E. Perfectionism and risk for disordered eating among young French male cyclists of high performance. Percept Mot Skills. 2004 Dec;99(3 Pt 1): 959- 67. doi: 10.2466/pms.99.3.959-967. PMID: 15648494. 15648494 · DOI
  17. [20]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 Mar 1; 6(1): 50- 7. PMID: 24149224; PMCID: PMC3778699. 24149224 PMC3778699
  18. [22]Glace BW Murphy CA McHugh MP. Food intake and electrolyte status of ultramarathoners competing in extreme heat. J Am Coll Nutr. 2002 Dec; 21(6): 553- 9. doi: 10.1080/07315724.2002.10719254. PMID: 12480801. 12480801 · DOI · Paper page
  19. [23]Eden BD Abernethy PJ. Nutritional intake during an ultraendurance running race. Int J Sport Nutr. 1994 Jun; 4(2): 166- 74. doi: 10.1123/ijsn.4.2.166. PMID: 8054961. 8054961 · DOI · Paper page
  20. [24]Petrie HJ Stover EA Horswill CA. Nutritional concerns for the child and adolescent competitor. Nutrition. 2004 Jul-Aug; 20(7-8): 620- 31. doi: 10.1016/j.nut.2004.04.002. PMID: 15212744. 15212744 · DOI
  21. [25]Rico-Sanz J Frontera WR Molé PA Rivera MA Rivera-Brown A Meredith CN. Dietary and performance assessment of elite soccer players during a period of intense training. Int J Sport Nutr. 1998 Sep; 8(3): 230- 40. doi: 10.1123/ijsn.8.3.230. PMID: 9738133. 9738133 · DOI
  22. [26]Bhasin S Cunningham GR Hayes FJ Matsumoto AM Snyder PJ Swerdloff RS Montori VM. Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2006 Jun; 91(6): 1995- 2010. doi: 10.1210/jc.2005-2847. Epub 2006 May 23. Erratum in: J Clin Endocrinol Metab. 2006 Jul; 91(7): 2688. Erratum in: J Clin Endocrinol Metab. 2021 Jun 16; 106(7): e2843. PMID: 16720669. 16720669 · DOI · Paper page
  23. [27]Boloña ER Uraga MV Haddad RM Tracz MJ Sideras K Kennedy CC Caples SM Erwin PJ Montori VM. Testosterone use in men with sexual dysfunction: a systematic review and meta-analysis of randomized placebo-controlled trials. Mayo Clin Proc. 2007 Jan; 82(1): 20- 8. doi: 10.4065/82.1.20. PMID: 17285782. 17285782 · DOI · Paper page
  24. [28]Kumar P Kumar N Thakur DS Patidar A. Male hypogonadism: Symptoms and treatment. J Adv Pharm Technol Res. 2010 Jul; 1(3): 297- 301. doi: 10.4103/0110-5558.72420. PMID: 22247861; PMCID: PMC3255409. 22247861 PMC3255409 · DOI · Paper page
  25. [29]Henning PC Scofield DE Spiering BA Staab JS Matheny RW Jr Smith MA Bhasin S Nindl BC. Recovery of endocrine and inflammatory mediators following an extended energy deficit. J Clin Endocrinol Metab. 2014 Mar; 99(3): 956- 64. doi: 10.1210/jc.2013-3046. Epub 2013 Dec 11. PMID: 24423293. 24423293 · DOI
  26. [30]Langan-Evans C Germaine M Artukovic M Oxborough DL Areta JL Close GL Morton JP. The Psychological and Physiological Consequences of Low Energy Availability in a Male Combat Sport Athlete. Med Sci Sports Exerc. 2021 Apr 1; 53(4): 673- 683. doi: 10.1249/MSS.0000000000002519. PMID: 33105389. 33105389 · DOI · Paper page
  27. [31]Narla A Kaiser K Tannock LR. EXTREMELY LOW TESTOSTERONE DUE TO RELATIVE ENERGY DEFICIENCY IN SPORT: A CASE REPORT. AACE Clin Case Rep. 2018 Nov 1; 5(2): e129- e131. doi: 10.4158/ACCR-2018-0345. PMID: 31967017; PMCID: PMC6873856. 31967017 PMC6873856 · DOI
  28. [32]Hackney AC. Hypogonadism in Exercising Males: Dysfunction or Adaptive-Regulatory Adjustment? Front Endocrinol (Lausanne). 2020 Jan 31; 11: 11. doi: 10.3389/fendo.2020.00011. PMID: 32082255; PMCID: PMC7005256. 32082255 PMC7005256 · DOI
  29. [33]Blank JL Desjardins C. Spermatogenesis is modified by food intake in mice. Biol Reprod. 1984 Mar; 30(2): 410- 5. doi: 10.1095/biolreprod30.2.410. PMID: 6704472. 6704472 · DOI
  30. [34]Cameron JL Nosbisch C. Suppression of pulsatile luteinizing hormone and testosterone secretion during short term food restriction in the adult male rhesus monkey (Macaca mulatta). Endocrinology. 1991 Mar; 128(3): 1532- 40. doi: 10.1210/endo-128-3-1532. PMID: 1999171. 1999171 · DOI
  31. [36]Daly W Seegers CA Rubin DA Dobridge JD Hackney AC. Relationship between stress hormones and testosterone with prolonged endurance exercise. Eur J Appl Physiol. 2005 Jan; 93(4): 375- 80. doi: 10.1007/s00421-004-1223-1. Epub 2004 Nov 20. PMID: 15618989. 15618989 · DOI
  32. [37]Hackney AC Szczepanowska E Viru AM. Basal testicular testosterone production in endurance-trained men is suppressed. Eur J Appl Physiol. 2003 Apr; 89(2): 198- 201. doi: 10.1007/s00421-003-0794-6. Epub 2003 Feb 28. PMID: 12665985. 12665985 · DOI
  33. [38]Bennell KL Brukner PD Malcolm SA. Effect of altered reproductive function and lowered testosterone levels on bone density in male endurance athletes. Br J Sports Med. 1996 Sep; 30(3): 205- 8. doi: 10.1136/bjsm.30.3.205. PMID: 8889111; PMCID: PMC1332330. 8889111 PMC1332330 · DOI
  34. [39]Wheeler GD Wall SR Belcastro AN Cumming DC. Reduced serum testosterone and prolactin levels in male distance runners. JAMA. 1984 Jul 27; 252(4): 514- 6. PMID: 6429357. 6429357
  35. [40]Hackney AC Lane AR. Low testosterone in male endurance-trained distance runners: impact of years in training. Hormones (Athens). 2018 Mar; 17(1): 137- 139. doi: 10.1007/s42000-018-0010-z. Epub 2018 Apr 27. PMID: 29858867. 29858867 · DOI
  36. [41]Roberts AC McClure RD Weiner RI Brooks GA. Overtraining affects male reproductive status. Fertil Steril. 1993 Oct; 60(4): 686- 92. doi: 10.1016/s0015-0282(16)56223-2. PMID: 8405526. 8405526 · DOI · Paper page
  37. [42]Arce JC De Souza MJ Pescatello LS Luciano AA. Subclinical alterations in hormone and semen profile in athletes. Fertil Steril. 1993 Feb; 59(2): 398- 404. PMID: 8425638. 8425638
  38. [43]Wheeler GD Singh M Pierce WD Epling WF Cumming DC. Endurance training decreases serum testosterone levels in men without change in luteinizing hormone pulsatile release. J Clin Endocrinol Metab. 1991 Feb; 72(2): 422- 5. doi: 10.1210/jcem-72-2-422. PMID: 1899423. 1899423 · DOI
  39. [44]Hackney AC Fahrner CL Gulledge TP. Basal reproductive hormonal profiles are altered in endurance trained men. J Sports Med Phys Fitness. 1998 Jun; 38(2): 138- 41. PMID: 9763799. 9763799
  40. [45]Hooper DR Kraemer WJ Saenz C Schill KE Focht BC Volek JS Maresh CM. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J Appl Physiol. 2017 Jul; 117(7): 1349- 1357. doi: 10.1007/s00421-017-3623-z. Epub 2017 May 3. PMID: 28470410. 28470410 · DOI · Paper page
  41. [46]Keay N Francis G Entwistle I Hind K. Clinical evaluation of education relating to nutrition and skeletal loading in competitive male road cyclists at risk of relative energy deficiency in sports (RED-S): 6-month randomised controlled trial. BMJ Open Sport Exerc Med. 2019 Mar 29; 5(1): e000523. doi: 10.1136/bmjsem-2019-000523. PMID: 31191973; PMCID: PMC6539156. PMC6539156 31191973 · DOI
  42. [47]Torstveit MK Fahrenholtz I Stenqvist TB Sylta Ø Melin A. Within-Day Energy Deficiency and Metabolic Perturbation in Male Endurance Athletes. Int J Sport Nutr Exerc Metab. 2018 Jul 1; 28(4): 419- 427. doi: 10.1123/ijsnem.2017-0337. Epub 2018 Jun 26. PMID: 29405793. 29405793 · DOI
  43. [48]Kupchak BR Kraemer WJ Hoffman MD Phinney SD Volek JS. The impact of an ultramarathon on hormonal and biochemical parameters in men. Wilderness Environ Med. 2014 Sep; 25(3): 278- 88. doi: 10.1016/j.wem.2014.03.013. Epub 2014 Jun 13. PMID: 24931590. 24931590 · DOI
  44. [49]Woods AL Rice AJ Garvican-Lewis LA Wallett AM Lundy B Rogers MA Welvaert M Halson S McKune A Thompson KG. The effects of intensified training on resting metabolic rate (RMR), body composition and performance in trained cyclists. PLoS One. 2018 Feb 14; 13(2): e0191644. doi: 10.1371/journal.pone.0191644. PMID: 29444097; PMCID: PMC5812577. 29444097 PMC5812577 · DOI
  45. [50]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 Oct 4; 4(1): e000424. doi: 10.1136/bmjsem-2018-000424. PMID: 30364549; PMCID: PMC6196965. PMC6196965 30364549 · DOI
  46. [51]Sheffield-Moore M Urban RJ. An overview of the endocrinology of skeletal muscle. Trends Endocrinol Metab. 2004 Apr; 15(3): 110- 5. doi: 10.1016/j.tem.2004.02.009. PMID: 15046739. 15046739 · DOI
  47. [52]Križaj L Kozinc Ž Löfler S Šarabon N. The chronic effects of eccentric exercise interventions in different populations: an umbrella review. Eur J Transl Myol. 2022 Oct 21; 32(4): 10876. doi: 10.4081/ejtm.2022.10876. PMID: 36269123; PMCID: PMC9830406. 36269123 PMC9830406 · DOI
  48. [53]Logue DM Madigan SM Heinen M McDonnell SJ Delahunt E Corish CA. Screening for risk of low energy availability in athletic and recreationally active females in Ireland. Eur J Sport Sci. 2019 Feb; 19(1): 112- 122. doi: 10.1080/17461391.2018.1526973. Epub 2018 Oct 10. PMID: 30303470. 30303470 · DOI · Paper page
  49. [54]Hackney AC Moore AW Brownlee KK. Testosterone and endurance exercise: development of the "exercise-hypogonadal male condition". Acta Physiol Hung. 2005; 92(2): 121- 37. doi: 10.1556/APhysiol.92.2005.2.3. PMID: 16268050. 16268050 · DOI
  50. [55]Cesanelli L Eimantas N Iovane A Messina G Satkunskiene D. The role of age on neuromuscular performance decay induced by a maximal intensity sprint session in a group of competitive endurance athletes. Eur J Transl Myol. 2022 Mar 10; 32(1): 10378. doi: 10.4081/ejtm.2022.10378. PMID: 35330561; PMCID: PMC8992664. 35330561 PMC8992664 · DOI

Cited by

Sorted by citations

Authors
Cupka, M., & Sedliak, M.
Affiliations
Comenius University Bratislava (SK)
Corresponding author
Sedliak, Milan
ORCID
Sedliak, Milan
Venue
European Journal of Translational Myology
Publisher
PAGEPress Publications
Published
2023-04-11
Volume
33
Issue
2
ISSN
  • 2037-7452 (ISSN-L)
  • 2037-7460
DOI
10.4081/ejtm.2023.11104
PMC
PMC10388605
OpenAlex
W4364382291
Cited by
46
References
5
Citations by year
2026: 16 · 2025: 12 · 2024: 15 · 2023: 3
FWCI
2.52
Type
journal article
Language
en
Open access
Licence
Locations
  • European Journal of Translational Myology (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • 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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
Keywords
low energy availability, endurance athletes, male athletes, testosterone, relative energy deficiency in sport, athletic performance, bone mineral density, resting metabolic rate, energy balance, energy intake, injury risk, screening

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