https://doi.org/10.4081/ejtm.2023.11104
Hungry runners – low energy availability in male endurance athletes and its impact on performance and testosterone: mini-review
Submitted: 19 December 2022
Accepted: 17 March 2023
Published: 11 April 2023
Accepted: 17 March 2023
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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.
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. PMID: 20840569.
DOI: https://doi.org/10.1111/j.1600-0838.2010.01190.x
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. PMID: 27430502.
DOI: https://doi.org/10.1007/s40279-016-0583-0
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. PMID: 29773536.
DOI: https://doi.org/10.1136/bjsports-2018-099193
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: https://doi.org/10.1016/j.cophys.2019.04.002
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. PMID: 34091537.
DOI: https://doi.org/10.1097/JSM.0000000000000948
Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29 Suppl 1:S7-15. Epub 2011 Jul 28. PMID: 21793767.
DOI: https://doi.org/10.1080/02640414.2011.588958
Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007 Oct;39(10):1867-82. PMID: 17909417.
DOI: https://doi.org/10.1249/mss.0b013e318149f111
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. PMID: 12519869.
DOI: https://doi.org/10.1210/jc.2002-020369
Loucks AB. Energy balance and body composition in sports and exercise. J Sports Sci. 2004 Jan;22(1):1-14. PMID: 14974441.
DOI: https://doi.org/10.1080/0264041031000140518
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. Epub 2013 Jan 30. PMID: 23980730.
DOI: https://doi.org/10.1139/apnm-2012-0373
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. PMID: 2744927.
DOI: https://doi.org/10.1055/s-2007-1024947
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. Epub 2018 Sep 13. PMID: 29431548.
DOI: https://doi.org/10.1123/ijspp.2017-0547
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. Epub 2014 Mar 17. PMID: 24635904.
DOI: https://doi.org/10.1017/S0007114514000154
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. Epub 2011 Dec 11. PMID: 22160180.
DOI: https://doi.org/10.1007/s00421-011-2268-6
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. PMID: 26999758.
DOI: https://doi.org/10.1001/jamainternmed.2016.0152
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.
DOI: https://doi.org/10.1260/174795408786238542
Melin AK, Heikura IA, Tenforde A, Mountjoy M. Energy Availability in Athletics: Health, Performance, and Physique. Int J Sport Nutr Exerc Metab. 2019 Mar 1;29(2):152-164. Epub 2019 Feb 26. PMID: 30632422.
DOI: https://doi.org/10.1123/ijsnem.2018-0201
Eichstadt M, Luzier J, Cho D, Weisenmuller C. Eating Disorders in Male Athletes. Sports Health. 2020 Jul/Aug;12(4):327-333. Epub 2020 Jun 11. PMID: 32525767; PMCID: PMC7787561.
DOI: https://doi.org/10.1177/1941738120928991
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: https://doi.org/10.2466/pms.99.3.959-967
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.
Pfeiffer B, Stellingwerff T, Hodgson AB, Randell R, Pöttgen K, Res P, Jeukendrup AE. Nutritional intake and gastrointestinal problems during competitive endurance events. Med Sci Sports Exerc. 2012 Feb;44(2):344-51. PMID: 21775906.
DOI: https://doi.org/10.1249/MSS.0b013e31822dc809
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. PMID: 12480801.
DOI: https://doi.org/10.1080/07315724.2002.10719254
Eden BD, Abernethy PJ. Nutritional intake during an ultraendurance running race. Int J Sport Nutr. 1994 Jun;4(2):166-74. PMID: 8054961.
DOI: https://doi.org/10.1123/ijsn.4.2.166
Petrie HJ, Stover EA, Horswill CA. Nutritional concerns for the child and adolescent competitor. Nutrition. 2004 Jul-Aug;20(7-8):620-31. PMID: 15212744.
DOI: https://doi.org/10.1016/j.nut.2004.04.002
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. PMID: 9738133.
DOI: https://doi.org/10.1123/ijsn.8.3.230
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. 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.
DOI: https://doi.org/10.1210/jc.2005-2847
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. PMID: 17285782.
DOI: https://doi.org/10.4065/82.1.20
Kumar P, Kumar N, Thakur DS, Patidar A. Male hypogonadism: Symptoms and treatment. J Adv Pharm Technol Res. 2010 Jul;1(3):297-301. PMID: 22247861; PMCID: PMC3255409.
DOI: https://doi.org/10.4103/0110-5558.72420
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. Epub 2013 Dec 11. PMID: 24423293.
DOI: https://doi.org/10.1210/jc.2013-3046
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. PMID: 33105389.
DOI: https://doi.org/10.1249/MSS.0000000000002519
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. PMID: 31967017; PMCID: PMC6873856.
DOI: https://doi.org/10.4158/ACCR-2018-0345
Hackney AC. Hypogonadism in Exercising Males: Dysfunction or Adaptive-Regulatory Adjustment? Front Endocrinol (Lausanne). 2020 Jan 31;11:11. PMID: 32082255; PMCID: PMC7005256.
DOI: https://doi.org/10.3389/fendo.2020.00011
Blank JL, Desjardins C. Spermatogenesis is modified by food intake in mice. Biol Reprod. 1984 Mar;30(2):410-5. PMID: 6704472.
DOI: https://doi.org/10.1095/biolreprod30.2.410
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. PMID: 1999171.
DOI: https://doi.org/10.1210/endo-128-3-1532
Cormie P, Newton RU, Taaffe DR, Spry N, Joseph D, Akhlil Hamid M, Galvão DA. Exercise maintains sexual activity in men undergoing androgen suppression for prostate cancer: a randomized controlled trial. Prostate Cancer Prostatic Dis. 2013 Jun;16(2):170-5. Epub 2013 Jan 15. PMID: 23318529.
DOI: https://doi.org/10.1038/pcan.2012.52
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. Epub 2004 Nov 20. PMID: 15618989.
DOI: https://doi.org/10.1007/s00421-004-1223-1
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. Epub 2003 Feb 28. PMID: 12665985.
DOI: https://doi.org/10.1007/s00421-003-0794-6
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. PMID: 8889111; PMCID: PMC1332330.
DOI: https://doi.org/10.1136/bjsm.30.3.205
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.
DOI: https://doi.org/10.1001/jama.252.4.514
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. Epub 2018 Apr 27. PMID: 29858867.
DOI: https://doi.org/10.1007/s42000-018-0010-z
Roberts AC, McClure RD, Weiner RI, Brooks GA. Overtraining affects male reproductive status. Fertil Steril. 1993 Oct;60(4):686-92. PMID: 8405526.
DOI: https://doi.org/10.1016/S0015-0282(16)56223-2
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.
DOI: https://doi.org/10.1016/S0015-0282(16)55684-2
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. PMID: 1899423.
DOI: https://doi.org/10.1210/jcem-72-2-422
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.
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. Epub 2017 May 3. PMID: 28470410.
DOI: https://doi.org/10.1007/s00421-017-3623-z
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. PMID: 31191973; PMCID: PMC6539156.
DOI: https://doi.org/10.1136/bmjsem-2019-000523
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. Epub 2018 Jun 26. PMID: 29405793.
DOI: https://doi.org/10.1123/ijsnem.2017-0337
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. Epub 2014 Jun 13. PMID: 24931590.
DOI: https://doi.org/10.1016/j.wem.2014.03.013
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. PMID: 29444097; PMCID: PMC5812577.
DOI: https://doi.org/10.1371/journal.pone.0191644
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. PMID: 30364549; PMCID: PMC6196965.
DOI: https://doi.org/10.1136/bmjsem-2018-000424
Sheffield-Moore M, Urban RJ. An overview of the endocrinology of skeletal muscle. Trends Endocrinol Metab. 2004 Apr;15(3):110-5. PMID: 15046739.
DOI: https://doi.org/10.1016/j.tem.2004.02.009
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. PMID: 36269123; PMCID: PMC9830406.
DOI: https://doi.org/10.4081/ejtm.2022.10876
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. Epub 2018 Oct 10. PMID: 30303470.
DOI: https://doi.org/10.1080/17461391.2018.1526973
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. PMID: 16268050.
DOI: https://doi.org/10.1556/APhysiol.92.2005.2.3
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. PMID: 35330561; PMCID: PMC8992664.
DOI: https://doi.org/10.4081/ejtm.2022.10378
How to Cite
Cupka, M., & Sedliak, M. (2023). Hungry runners – low energy availability in male endurance athletes and its impact on performance and testosterone: mini-review. European Journal of Translational Myology, 33(2). https://doi.org/10.4081/ejtm.2023.11104
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