Skip to main content

Advertisement

Log in

Markers of Low Energy Availability in Overreached Athletes: A Systematic Review and Meta-analysis

  • Systematic Review
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

Background

Overreaching is the transient reduction in performance that occurs following training overload and is driven by an imbalance between stress and recovery. Low energy availability (LEA) may drive underperformance by compounding training stress; however, this has yet to be investigated systematically.

Objective

The aim of this study was to quantify changes in markers of LEA in athletes who demonstrated underperformance, and exercise performance in athletes with markers of LEA.

Methods

Studies using a ≥ 2-week training block with maintained or increased training loads that measured exercise performance and markers of LEA were identified using a systematic search following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Changes from pre- to post-training were analyzed for (1) markers of LEA in underperforming athletes and (2) performance in athletes with ≥ 2 markers of LEA.

Results

From 56 identified studies, 14 separate groups of athletes demonstrated underperformance, with 50% also displaying ≥ 2 markers of LEA post-training. Eleven groups demonstrated ≥ 2 markers of LEA independent of underperformance and 37 had no performance reduction or ≥ 2 markers of LEA. In underperforming athletes, fat mass (d =  − 0.29, 95% confidence interval [CI] − 0.54 to − 0.04; p = 0.02), resting metabolic rate (d =  − 0.63, 95% CI − 1.22 to − 0.05; p = 0.03), and leptin (d =  − 0.72, 95% CI − 1.08 to − 0.35; p < 0.0001) were decreased, whereas body mass (d =  − 0.04, 95% CI − 0.21 to 0.14; p = 0.70), cortisol (d =  − 0.06, 95% CI − 0.35 to 0.23; p = 0.68), insulin (d =  − 0.12, 95% CI − 0.43 to 0.19; p = 0.46), and testosterone (d =  − 0.31, 95% CI − 0.69 to 0.08; p = 0.12) were unaltered. In athletes with ≥ 2 LEA markers, performance was unaffected (d = 0.09, 95% CI − 0.30 to 0.49; p = 0.6), and the high heterogeneity in performance outcomes (I2 = 84.86%) could not be explained by the performance tests used or the length of the training block.

Conclusion

Underperforming athletes may present with markers of LEA, but overreaching is also observed in the absence of LEA. The lack of a specific effect and high variability of outcomes with LEA on performance suggests that LEA is not obligatory for underperformance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Meeusen R, Duclos M, Foster C, Fry A, Gleeson M, Nieman D, et al. Prevention, diagnosis, and treatment of the overtraining syndrome: Joint consensus statement of the European college of sport science and the American College of Sports Medicine. Med Sci Sports Exerc. 2013;45(1):186–205.

    PubMed  Google Scholar 

  2. Bellinger P. Functional overreaching in endurance athletes: a necessity or cause for concern? Sport Med. 2020;50(6):1059–73.

    Google Scholar 

  3. King NA, Lluch A, Stubbs RJ, Blundell JE. High dose exercise does not increase hunger or energy intake in free living males. Eur J Clin Nutr. 1997;51(7):478–83.

    CAS  PubMed  Google Scholar 

  4. Drenowatz C, Eisenmann JC, Carlson JJ, Pfeiffer KA, Pivarnik JM. Energy expenditure and dietary intake during high-volume and low-volume training periods among male endurance athletes. Appl Physiol Nutr Metab. 2012;37(2):199–205.

    CAS  PubMed  Google Scholar 

  5. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29(Suppl. 1):S7-15.

    PubMed  Google Scholar 

  6. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–82.

    PubMed  Google Scholar 

  7. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the female athlete triad-relative energy deficiency in sport (RED-S). Br J Sports Med. 2014;48(7):491–7.

    PubMed  Google Scholar 

  8. Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman KE. Endocrine effects of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab. 2018;28(4):335–49.

    CAS  PubMed  Google Scholar 

  9. McCall LM, Ackerman KE. Endocrine and metabolic repercussions of relative energy deficiency in sport. Curr Opin Endocr Metab Res. 2019;9:56–65.

    Google Scholar 

  10. Dipla K, Kraemer RR, Constantini WW, Hackney AC. Relative energy deficiency in sports (RED-S): elucidation of endocrine changes affecting the health of males and females. Hormones (Athens). 2021;20(1):35–47.

    PubMed  Google Scholar 

  11. Schaal K, VanLoan MD, Hausswirth C, Casazza GA. Decreased energy availability during training overload is associated with non-functional overreaching and suppressed ovarian function in female runners. Appl Physiol Nutr Metab. 2021;46(10):1179–88.

    CAS  PubMed  Google Scholar 

  12. Schaal K, Tiollier E, Le Meur Y, Casazza G, Hausswirth C. Elite synchronized swimmers display decreased energy availability during intensified training. Scand J Med Sci Sport. 2017;27(9):925–34.

    CAS  Google Scholar 

  13. Costill DL, Flynn MG, Kirwan JP, Houmard JA, Mitchell JB, Thomas R, et al. Effects of repeated days of intensified training on muscle glycogen and swimming performance. Med Sci Sports Exerc. 1988;20(3):249–54.

    CAS  PubMed  Google Scholar 

  14. Vanheest JL, Rodgers CD, Mahoney CE, De Souza MJ. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46(1):156–66.

    PubMed  Google Scholar 

  15. Stellingwerff T, Heikura IA, Meeusen R, Bermon S, Seiler S, Mountjoy ML, et al. Overtraining Syndrome (OTS) and Relative Energy Deficiency in Sport (RED-S): shared pathways, symptoms and complexities. Sport Med. 2021;51(11):2251–80.

    Google Scholar 

  16. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.

    PubMed  PubMed Central  Google Scholar 

  17. Bell L, Ruddock A, Maden-Wilkinson T, Rogerson D. Overreaching and overtraining in strength sports and resistance training: a scoping review. J Sports Sci. 2020;38(16):1897–912.

    PubMed  Google Scholar 

  18. De Pauw K, Roelands B, Cheung SS, de Geus B, Rietjens G, Meeusen R. Guidelines to classify subject groups in sport-science research. Int J Sports Physiol Perform. 2013;8(2):111–22.

    PubMed  Google Scholar 

  19. Decroix L, De Pauw K, Foster C, Meeusen R. Guidelines to classify female subject groups in sport-science research. Int J Sports Physiol Perform. 2016;11(2):204–13.

    PubMed  Google Scholar 

  20. Gordon CM, Ackerman KE, Berga SL, Kaplan JR, Mastorakos G, Misra M, et al. Functional hypothalamic amenorrhea: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2017;102(5):1413–39.

    PubMed  Google Scholar 

  21. Melin AK, Heikura IA, Tenforde A, Mountjoy M. Energy availability in athletics: health, performance, and physique. Int J Sport Nutr Exerc Metab. 2019;29(2):152–64.

    PubMed  Google Scholar 

  22. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. Relative energy deficiency in sport (RED-S) clinical assessment tool (CAT). Br J Sports Med. 2015;49(7):421–3.

    PubMed  Google Scholar 

  23. Melin A, Tornberg ÅB, Skouby S, Faber J, Ritz C, Sjödin A, et al. 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(7):540–5.

    PubMed  Google Scholar 

  24. Areta JL, Taylor HL, Koehler K. 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. 2021;121(1):1–21.

    PubMed  Google Scholar 

  25. Strock NCA, Koltun KJ, Southmayd EA, Williams NI, De Souza MJ. Indices of resting metabolic rate accurately reflect energy deficiency in exercising women. Int J Sport Nutr Exerc Metab. 2020;30(1):14–24.

    CAS  PubMed  Google Scholar 

  26. Torstveit MK, Fahrenholtz IL, Stenqvist TB, Sylta O, Melin A. Within-day energy deficiency and metabolic perturbation in male endurance athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):419–27.

    CAS  PubMed  Google Scholar 

  27. Trexler ET, Smith-Ryan AE, Norton LE. Metabolic adaptation to weight loss: implications for the athlete. J Int Soc Sports Nutr. 2014;11(1):1–7.

    Google Scholar 

  28. Papageorgiou M, Elliott-Sale KJ, Parsons A, Tang JCY, Greeves JP, Fraser WD, et al. Effects of reduced energy availability on bone metabolism in women and men. Bone. 2017;105:191–9.

    CAS  PubMed  Google Scholar 

  29. Koehler K, Hoerner NR, Gibbs JC, Zinner C, Braun H. 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(20):1921–9.

    PubMed  Google Scholar 

  30. Kojima C, Ishibashi A, Tanabe Y, Iwayama K, Kamei A, Takahashi H, et al. Muscle glycogen content during endurance training under low energy availability. Med Sci Sports Exerc. 2020;52(1):187–95.

    CAS  PubMed  Google Scholar 

  31. Ishibashi A, Kojima C, Tanabe Y, Iwayama K, Hiroyama T, Tsuji T, et al. Effect of low energy availability during three consecutive days of endurance training on iron metabolism in male long distance runners. Physiol Rep. 2020;8(12):1–9.

    Google Scholar 

  32. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003;88(1):297–311.

    CAS  PubMed  Google Scholar 

  33. Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol. 2000;83(4–5):434–40.

    CAS  PubMed  Google Scholar 

  34. Ishibashi A, Kojima C, Kamei A, Iwayama K, Tanabe Y, Kazushige G, et al. Effect of low energy availability during three consecutive days of endurance training on iron metabolism in male long distance runners. Med Sci Sport Exerc. 2018;50(5S):461.

    Google Scholar 

  35. Badenhorst CE, Black KE, O’Brien WJ. Hepcidin as a prospective individualized biomarker for individuals at risk of low energy availability. Int J Sport Nutr Exerc Metab. 2019;29(6):671–81.

    CAS  PubMed  Google Scholar 

  36. Tornberg ÅB, Melin A, Koivula FM, Johansson A, Skouby S, Faber J, et al. Reduced neuromuscular performance in amenorrheic elite endurance athletes. Med Sci Sports Exerc. 2017;49(12):2478–85.

    PubMed  Google Scholar 

  37. Ding J-H, Sheckter CB, Drinkwater BL, Soules MR, Bremner WJ, Seattle W. High serum cortisol levels in exercise-associated amenorrhea. Ann Intern Med. 1988;108:530–4.

    CAS  PubMed  Google Scholar 

  38. Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000;278(1):43–9.

    Google Scholar 

  39. Dubuc GR, Phinney SD, Stern JS, Havel PJ. Changes of serum leptin and endocrine and metabolic parameters after 7 days of energy restriction in men and women. Metabolism. 1998;47(4):429–34.

    CAS  PubMed  Google Scholar 

  40. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol. 1994;266(3):817–23.

    Google Scholar 

  41. Wong HK, Hoermann R, Grossmann M. Reversible male hypogonadotropic hypogonadism due to energy deficit. Clin Endocrinol (Oxf). 2019;91(1):3–9.

    CAS  PubMed  Google Scholar 

  42. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19(8):1231–40.

    PubMed  Google Scholar 

  43. Johnstone AM, Murison SD, Duncan JS, Rance KA, Speakman JR. Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr. 2005;82(5):941–8.

    CAS  PubMed  Google Scholar 

  44. Lippi G, De Vita F, Salvagno GL, Gelati M, Montagnana M, Guidi GC. Measurement of morning saliva cortisol in athletes. Clin Biochem. 2009;42(9):904–6.

    CAS  PubMed  Google Scholar 

  45. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52(6):377–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Sterne JA, Egger M, Moher D. Addressing reporting biases. In: Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions. Cochrane B Ser. Chichester: Wiley; 2008. p. 298–333.

    Google Scholar 

  47. Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, editors. Cochrane Handbook for Systematic Reviews of Interventions version 6.2. Cochrane; 2021.

  48. Von Hippel PT. The heterogeneity statistic I2 can be biased in small meta-analyses. BMC Med Res Methodol. 2015;15(1):1–8.

    Google Scholar 

  49. Flynn MG, Pizza FX, Boone JB, Andres FF, Michaud TA, Rodriguez-Zayas JR. Indices of training stress during competitive running and swimming seasons. Int J Sports Med. 1994;15(1):21–6.

    CAS  PubMed  Google Scholar 

  50. Flynn MG, Carroll KK, Hall HL, Bushman BA, Gunnar Brolinson P, Weideman CA. Cross training: indices of training stress and performance. Med Sci Sports Exerc. 1998;30(2):294–300.

    CAS  PubMed  Google Scholar 

  51. Franchini E, Julio UF, Panissa VLG, Lira FS, Gerosa-Neto J, Branco BHM. High-intensity intermittent training positively affects aerobic and anaerobic performance in judo athletes independently of exercise mode. Front Physiol. 2016;7:268.

    PubMed  PubMed Central  Google Scholar 

  52. Gastmann U, Petersen KG, Bocker J, Lehmann M. Monitoring intensive endurance training at moderate energetic demands using resting laboratory markers failed to recognize an early overtraining stage. J Sports Med Phys Fit. 1998;38(3):188–93.

    CAS  Google Scholar 

  53. Hackney AC, Hooper DR. Low testosterone: Androgen deficiency, endurance exercise training, and competitive performance. Physiol Int. 2019;106(4):379–89.

    CAS  PubMed  Google Scholar 

  54. Häkkinen K, Keskinen KL, Alén M, Komi PV, Kauhanen H. Serum hormone concentrations during prolonged training in elite endurance-trained and strength-trained athletes. Eur J Appl Physiol Occup Physiol. 1989;59(3):233–8.

    PubMed  Google Scholar 

  55. Hoogeveen AR, Zonderland ML. Relationships between testosterone, cortisol and performance in professional cyclists. Int J Sports Med. 1996;17(6):423–8.

    CAS  PubMed  Google Scholar 

  56. Iguchi J, Kuzuhara K, Katai K, Hojo T, Fujisawa Y, Kimura M, et al. Seasonal changes in anthropometric, physiological, nutritional and performance factors in collegiate rowers. J Strength Cond Res. 2020;34(11):3225–31.

    PubMed  Google Scholar 

  57. Jürimäe J, Mäestu J, Jürimäe T. Leptin as a marker of training stress in highly trained male rowers? Eur J Appl Physiol. 2003;90(5–6):533–8.

    PubMed  Google Scholar 

  58. Jürimäe J, Purge P, Jürimäe T. Adiponectin and stress hormone responses to maximal sculling after volume-extended training season in elite rowers. Metabolism. 2006;55(1):13–9.

    PubMed  Google Scholar 

  59. Bachero-Mena B, Pareja-Blanco F, González-Badillo JJ. Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800 m high-level athletes. Front Physiol. 2017;8:637.

    PubMed  PubMed Central  Google Scholar 

  60. Koundourakis NE, Androulakis N, Spyridaki EC, Castanas E, Malliaraki N, Tsatsanis C, et al. Effect of different seasonal strength training protocols on circulating androgen levels and performance parameters in professional soccer players. Hormones (Athens). 2014;13(1):104–18.

    PubMed  Google Scholar 

  61. Lakhdar N, Ben Saad H, Denguezli M, Zaouali M, Zbidi A, Tabka Z, et al. Effects of intense cycling training on plasma leptin and adiponectin and its relation to insulin resistance. Neuro Endocrinol Lett. 2013;34(3):229–35.

    CAS  PubMed  Google Scholar 

  62. Lee C-L, Hsu W-C, Cheng C-F. Physiological adaptations to sprint interval training with matched exercise volume. Med Sci Sports Exerc. 2017;49(1):86–95.

    PubMed  Google Scholar 

  63. Lehmann M, Gastmann U, Petersen KG, Bachl N, Seidel A, Khalaf AN, et al. Training-overtraining: performance, and hormone levels, after a defined increase in training volume versus intensity in experienced middle- and long-distance runners. Br J Sports Med. 1992;26(4):233–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Lehmann M, Knizia K, Gastmann U, Petersen KG, Khalaf AN, Bauer S, et al. Influence of 6-week, 6 days per week, training on pituitary function in recreational athletes. Br J Sports Med. 1993;27(3):186–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Lopez Calbet JA, Navarro MA, Barbany JR, Garcia Manso J, Bonnin MR, Valero J. Salivary steroid changes and physical performance in highly trained cyclists. Int J Sports Med. 1993;14(3):111–7.

    CAS  PubMed  Google Scholar 

  66. Mackinnon LT, Hooper SL, Jones S, Gordon RD, Bachmann AW. Hormonal, immunological, and hematological responses to intensified training in elite swimmers. Med Sci Sport Exerc. 1997;29(12):1637–45.

    CAS  Google Scholar 

  67. Mäestu J, Jürimäe J, Jürimäe T. Hormonal reactions during heavy training stress and following tapering in highly trained male rowers. Horm Metab Res. 2003;35(2):109–13.

    PubMed  Google Scholar 

  68. Mäestu J, Jürimäe J, Jürimäe T. Hormonal response to maximal rowing before and after heavy increase in training volume in highly trained male rowers. J Sports Med Phys Fit. 2005;45(1):121–6.

    Google Scholar 

  69. Maresh CM, Armstrong LE, Bergeron MF, Gabaree CL, Hoffman JR, Hannon DR, et al. Plasma cortisol and testosterone responses during a collegiate swim season. J Strength Cond Res. 1994;8(1):1–4.

    Google Scholar 

  70. Bellinger P, Desbrow B, Derave W, Lievens E, Irwin C, Sabapathy S, et al. Muscle fiber typology is associated with the incidence of overreaching in response to overload training. J Appl Physiol. 2020;129(4):823–36.

    CAS  PubMed  Google Scholar 

  71. Miloski B, De Freitas VH, Nakamura FY, De Nogueira FCA, Bara-Filho MG. Seasonal training load distribution of professional futsal players: effects on physical fitness, muscle damage and hormonal status. J Strength Cond Res. 2016;30(6):1525–33.

    PubMed  Google Scholar 

  72. Mujika I, Chatard JC, Padilla S, Guezennec CY, Geyssant A. Hormonal responses to training and its tapering off in competitive swimmers: relationships with performance. Eur J Appl Physiol Occup Physiol. 1996;74(4):361–6.

    CAS  PubMed  Google Scholar 

  73. Muscella A, Vetrugno C, Spedicato M, Stefàno E, Marsigliante S. The effects of training on hormonal concentrations in young soccer players. J Cell Physiol. 2019;234(11):20685–93.

    CAS  PubMed  Google Scholar 

  74. Ndon JA, Snyder AC, Foster C, Wehrenberg WB. Effects of chronic intense exercise training on the leukocyte response to acute exercise. Int J Sports Med. 1992;13(2):176–82.

    CAS  PubMed  Google Scholar 

  75. Nuuttila O-P, Nikander A, Polomoshnov D, Laukkanen JA, Hakkinen K. Effects of HRV-guided vs. predetermined block training on performance, HRV and serum hormones. Int J Sports Med. 2017;38(12):909–20.

    PubMed  Google Scholar 

  76. Papacosta E, Gleeson M, Nassis GP. Salivary hormones, IGA, and performance during intense training and tapering in judo athletes. J Strength Cond Res. 2013;27(9):2569–80.

    PubMed  Google Scholar 

  77. Passelergue PA, Lac G. Salivary hormonal responses and performance changes during 15 weeks of mixed aerobic and weight training in elite junior wrestlers. J Strength Cond Res. 2012;26(11):3049–58.

    PubMed  Google Scholar 

  78. Petibois C, Déléris G. Alterations of lipid profile in endurance over-trained subjects. Arch Med Res. 2004;35(6):532–9.

    CAS  PubMed  Google Scholar 

  79. Rämson R, Jürimäe J, Jürimäe T, Mäestu J. Behavior of testosterone and cortisol during an intensity-controlled high-volume training period measured by a training tast-specific test in men rowers. J Strength Cond Res. 2009;23(2):645–51.

    PubMed  Google Scholar 

  80. Rämson R, Jürimäe J, Jürimäe T, Mäestu J. The effect of 4-week training period on plasma neuropeptide Y, leptin and ghrelin responses in male rowers. Eur J Appl Physiol. 2012;112(5):1873–80.

    PubMed  Google Scholar 

  81. Chicharrio J, Lopez-Mojares LM, Lucia A, Perez M, Alvarez J, Labanda P, et al. Overtraining parameters in special military units. Aviat Space Environ Med. 1998;69(6):562–8.

    Google Scholar 

  82. Saidi K, Ben Abderrahman A, Boullosa D, Dupont G, Hackney AC, Bideau B, et al. The interplay between plasma hormonal concentrations, physical fitness, workload and mood state changes to periods of congested match play in professional soccer players. Front Physiol. 2020;11:835.

    PubMed  PubMed Central  Google Scholar 

  83. Schumann M, Mykkanen O, Doma K, Mazzolari R, Nyman K, Hakkinen K. Effects of endurance training only versus same-session combined endurance and strength training on physical performance and serum hormone concentrations in recreational endurance runners. Appl Physiol Nutr Metab. 2015;40(1):28–36.

    CAS  PubMed  Google Scholar 

  84. Smith C, Myburgh KH. Are the relationships between early activation of lymphocytes and cortisol or testosterone influenced by intensified cycling training in men? Appl Physiol Nutr Metab. 2006;31(3):226–34.

    CAS  PubMed  Google Scholar 

  85. Stenqvist TB, Torstveit MK, Faber J, Melin AK. 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 (Lausanne). 2020;11: 512365.

    PubMed  Google Scholar 

  86. Sylta O, Tonnessen E, Sandbakk O, Hammarstrom D, Danielsen J, Skovereng K, et al. Effects of high-intensity training on physiological and hormonal adaptions in well-trained cyclists. Med Sci Sports Exerc. 2017;49(6):1137–46.

    PubMed  Google Scholar 

  87. Taipale RS, Mikkola J, Nummela A, Vesterinen V, Capostagno B, Walker S, et al. Strength training in endurance runners. Int J Sports Med. 2010;31(7):468–76.

    CAS  PubMed  Google Scholar 

  88. Tanaka H, West KA, Duncan GE, Bassett DR. Changes in plasma tryptophan/branched chain amino acid ratio in responses to training volume variation. Int J Sports Med. 1997;18(4):270–5.

    CAS  PubMed  Google Scholar 

  89. Taipale RS, Mikkola J, Salo T, Hokka L, Vesterinen V, Karemer WJ, et al. Mixed maximal and explosive strength training in recreational endurance runners. J Strength Cond Res. 2014;28(3):689–99.

    PubMed  Google Scholar 

  90. Urhausen A, Gabriel HHW, Kindermann W. Impaired pituitary hormonal response to exhaustive exercise in overtrained endurance athletes. Med Sci Sport Exerc. 1998;30(3):407–14.

    CAS  Google Scholar 

  91. Vervoorn C, Quist AM, Vermulst LJM, Erich WBM, De Vries WR, Thijssen JHH. The behaviour of the plasma free testosterone/cortisol ratio during a season of elite rowing training. Int J Sports Med. 1991;12(3):257–63.

    CAS  PubMed  Google Scholar 

  92. Coutts AJ, Wallace LK, Slattery KM. Monitoring changes in performance, physiology, biochemistry, and psychology during overreaching and recovery in triathletes. Int J Sports Med. 2007;28(2):125–34.

    CAS  PubMed  Google Scholar 

  93. Woods AL, Garvican-Lewis LA, Lundy B, Rice AJ, Thompson KG. New approaches to determine fatigue in elite athletes during intensified training: resting metabolic rate and pacing profile. PLoS One. 2017;12(3):1–18.

    Google Scholar 

  94. Woods AL, Rice AJ, Garvican-Lewis LA, Wallett AM, Lundy B, Rogers MA, et al. The effects of intensified training on resting metabolic rate (RMR), body composition and performance in trained cyclists. PLoS One. 2018;13(2):e0191644.

    PubMed  PubMed Central  Google Scholar 

  95. Young KC, Kendall KL, Patterson KM, Pandya PD, Fairman CM, Smith SW. Rowing performance, body composition, and bone mineral density outcomes in college-level rowers after a season of concurrent training. Int J Sports Physiol Perform. 2014;9(6):966–72.

    PubMed  Google Scholar 

  96. Zaccaria M, Varnier M, Piazza P, Noventa D, Ermolao A. Blunted growth hormone response to maximal exercise in middle-aged versus young subjects and no effect of endurance training. J Clin Endocrinol Metab. 1999;84(7):2303–7.

    CAS  PubMed  Google Scholar 

  97. Muscella A, Stefàno E, Marsigliante S. The effects of training on hormonal concentrations and physical performance of football referees. Physiol Rep. 2021;9(8):1–11.

    Google Scholar 

  98. Domaszewska K, Kryściak J, Podgórski T, Nowak A, Ogurkowska MB. The impulse of force as an effective indicator of exercise capacity in competitive rowers and canoeists. J Hum Kinet. 2021;79(1):87–99.

    PubMed  PubMed Central  Google Scholar 

  99. Coutts AJ, Reaburn P, Piva TJ, Rowsell GJ. Monitoring for overreaching in rugby league players. Eur J Appl Physiol. 2007;99(3):313–24.

    PubMed  Google Scholar 

  100. Coutts A, Reaburn P, Piva TJ, Murphy A. Changes in selected biochemical, muscular strength, power, and endurance measures during deliberate overreaching and tapering in rugby league players. Int J Sports Med. 2006;28(2):116–24.

    PubMed  Google Scholar 

  101. Dressendorfer RH, Petersen SR, Moss Lovshin SE, Hannon JL, Lee SF, Bell GJ. Performance enhancement with maintenance of resting immune status after intensified cycle training. Clin J Sport Med. 2002;12(5):301–7.

    PubMed  Google Scholar 

  102. Farzad B, Gharakhanlou R, Agha-Alinejad H, Curby DG, Bayati M, Bahraminejad M, et al. Physiological and performance changes from the addition of a sprint interval program to wrestling training. J Strength Cond Res. 2011;25(9):2392–9.

    PubMed  Google Scholar 

  103. McCarth SF, Islam H, Hazell TJ. The emerging role of lactate as a mediator of exercise-induced appetite suppression. Am J Physiol Metab. 2020;319(4):E814–9.

    Google Scholar 

  104. Douglas JA, King JA, Clayton DJ, Jackson AP, Sargeant JA, Thackray AE, et al. Acute effects of exercise on appetite, ad libitum energy intake and appetite-regulatory hormones in lean and overweight/obese men and women. Int J Obes. 2017;41(12):1737–44.

    CAS  Google Scholar 

  105. Considine RV. Human leptin: an adipocyte hormone with weight-regulatory and endocrine functions. Semin Vasc Med. 2005;5(1):15–24.

    PubMed  Google Scholar 

  106. Staal S, Sjödin A, Fahrenholtz I, Bonnesen K, Melin AK. Low RMRratio as a surrogate marker for energy deficiency, the choice of predictive equation vital for correctly identifying male and female ballet dancers at risk. Int J Sport Nutr Exerc Metab. 2018;28(4):412–8.

    PubMed  Google Scholar 

  107. Koehler K, Williams NI, Mallinson RJ, Southmayd EA, Allaway HCM, De Souza MJ. Low resting metabolic rate in exercise-associated amenorrhea is not due to a reduced proportion of highly active metabolic tissue compartments. Am J Physiol Endocrinol Metab. 2016;311(2):E480–7.

    PubMed  Google Scholar 

  108. Melin A, Tornberg B, Skouby S, Møller SS, Sundgot-Borgen J, Faber J, et al. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sport. 2015;25(5):610–22.

    CAS  Google Scholar 

  109. Müller MJ, Bosy-Westphal A. Adaptive thermogenesis with weight loss in humans. Obesity. 2013;21(2):218–28.

    PubMed  Google Scholar 

  110. Cunningham J. Body composition as a determinant of energy expenditure: a synthetic review and a proposed general prediction equation. Am J Clin Nutr. 1991;54(6):963–9.

    CAS  PubMed  Google Scholar 

  111. Le Meur Y, Pichon A, Schaal K, Schmitt L, Louis J, Gueneron J, et al. Evidence of parasympathetic hyperactivity in functionally overreached athletes. Med Sci Sports Exerc. 2013;45(11):2061–71.

    PubMed  Google Scholar 

  112. Flatt AA, Hornikel B, Esco MR. Heart rate variability and psychometric responses to overload and tapering in collegiate sprint-swimmers. J Sci Med Sport Sports Med. 2017;20(6):606–10.

    Google Scholar 

  113. Coates AM, Incognito AV, Seed JD, Doherty CJ, Millar PJ, Burr JF. Three weeks of overload training increases resting muscle sympathetic activity. Med Sci Sports Exerc. 2018;50(5):928–37.

    PubMed  Google Scholar 

  114. Greenham G, Buckley JD, Garrett J, Eston R, Norton K. Biomarkers of physiological responses to periods of intensified, non-resistance-based exercise training in well-trained male athletes: a systematic review and meta-analysis. Sport Med. 2018;48(11):2517–48.

    Google Scholar 

  115. Hackney A. Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment. Front Endocrinol (Lausanne). 2020;11:1–16.

    Google Scholar 

  116. Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM. 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(4):403–11.

    CAS  PubMed  Google Scholar 

  117. Drew M, Vlahovich N, Hughes D, Appaneal R, Burke LM, Lundy B, et al. Prevalence of illness, poor mental health and sleep quality and low energy availability prior to the 2016 summer Olympic games. Br J Sports Med. 2018;52(1):47–53.

    PubMed  Google Scholar 

  118. Ihalainen JK, Kettunen OK, McGawley K, Solli G, Mero AA, Kyröläinen H. Body composition, energy availability, training, and menstrual status in female runners. Int J Sports Physiol Perform. 2021;16(7):1043–8.

    PubMed  Google Scholar 

  119. O’Connor H, Olds T, Maughan RJ. Physique and performance for track and field events. J Sports Sci. 2007;25(Suppl 1):49–60.

    Google Scholar 

  120. Stellingwerff T. Case study: body composition periodization in an olympic-level female middle-distance runner over a 9-year career. Int J Sport Nutr Exerc Metab. 2018;28(4):428–33.

    PubMed  Google Scholar 

  121. Bruinvels G, Burden RJ, McGregor AJ, Ackerman KE, Dooley M, Richards T, et al. Sport, exercise and the menstrual cycle: where is the research? Br J Sports Med. 2017;51(6):3–5.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jamie F. Burr.

Ethics declarations

Author contributions

All authors contributed to the production of this review and have read and approved the final manuscript. MK was involved in screening, data extraction and data analysis, and led the writing of this review. AC was involved in screening and contributed to the writing of this review. JB resolved any conflicts in screening and contributed to the writing of this review.

Funding

No sources of funding were used to assist in the preparation of this article.

Registration

This review was not registered.

Conflict of interest

Megan Kuikman, Alexandra Coates, and Jamie Burr declare that they have no conflicts of interest relevant to the contents of this review.

Availability of data and material

Please contact the corresponding author for data requests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 40 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuikman, M.A., Coates, A.M. & Burr, J.F. Markers of Low Energy Availability in Overreached Athletes: A Systematic Review and Meta-analysis. Sports Med 52, 2925–2941 (2022). https://doi.org/10.1007/s40279-022-01723-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40279-022-01723-x

Navigation