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A Life History Perspective on Athletes with Low Energy Availability

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Abstract

The energy costs of athletic training can be substantial, and deficits arising from costs unmet by adequate energy intake, leading to a state of low energy availability, may adversely impact athlete health and performance. Life history theory is a branch of evolutionary theory that recognizes that the way the body uses energy—and responds to low energy availability—is an evolved trait. Energy is a finite resource that must be distributed throughout the body to simultaneously fuel all biological processes. When energy availability is low, insufficient energy may be available to equally support all processes. As energy used for one function cannot be used for others, energetic “trade-offs” will arise. Biological processes offering the greatest immediate survival value will be protected, even if this results in energy being diverted away from others, potentially leading to their downregulation. Athletes with low energy availability provide a useful model for anthropologists investigating the biological trade-offs that occur when energy is scarce, while the broader conceptual framework provided by life history theory may be useful to sport and exercise researchers who investigate the influence of low energy availability on athlete health and performance. The goals of this review are: (1) to describe the core tenets of life history theory; (2) consider trade-offs that might occur in athletes with low energy availability in the context of four broad biological areas: reproduction, somatic maintenance, growth, and immunity; and (3) use this evolutionary perspective to consider potential directions for future research.

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References

  1. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29:37–41.

    Article  Google Scholar 

  2. Loucks A. Exercise training in the normal female: effects of low energy availability on reproductive function. In: Hackney A, Constantini N, editors. Endocrinology of physical activity and sport. 3rd ed. Springer Nature: Berlin; 2020. p. 171–91.

    Chapter  Google Scholar 

  3. Gibson M, Lawson D. Applying evolutionary anthropology. Evol Anthropol. 2015;24:3–14.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Stearns SC. Trade-offs in life-history evolution. Funct Ecol. 1989;3:259.

    Article  Google Scholar 

  5. Gadgil M, Bossert WH, The S, Naturalist A, Feb NJ, Gadgil M, et al. Life historical consequences of natural selection. Am Nat. 1970;104:1–24.

    Article  Google Scholar 

  6. Otis C, Drinkwater B, Johnson M, Loucks A, Wilmore J. American College of Sports Medicine Position Stand. The female athlete triad. Med Sci Sport Exerc. 1997;29:1–9.

    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;48:491–7.

    Article  PubMed  Google Scholar 

  8. Areta J, Taylor H, 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;121:1–21.

    Article  PubMed  Google Scholar 

  9. Hackney A. Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment? Front Endocrinol (Lausanne). 2020;11:11.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  11. Mountjoy M, Burke L, Ackerman KE, Blauwet C, Lebrun C, Melin A, et al. International Olympic Committee (IOC) consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Int J Sport Nutr Exerc Metab. 2018;28:316–31.

    Article  PubMed  Google Scholar 

  12. Reznick D, Nunney L, Tessier A. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol. 2000;15:421–5.

    Article  CAS  PubMed  Google Scholar 

  13. Zera A, Harshman L. The physiology of life history trade- offs in animals. Ecology. 2001;32:95–126.

    Google Scholar 

  14. Bronson F. Mammalian reproduction: an ecological perspective. Biol Reprod. 1985;32:1–26.

    Article  CAS  PubMed  Google Scholar 

  15. Cody M. A general theory of clutch size. Evolution (New York). 1996;20:174–84.

    Google Scholar 

  16. Thurber C, Dugas L, Ocobock C, Carlson B, Speakman J, Pontzer H. Extreme events reveal an alimentary limit on sustained maximal human energy expenditure. Sci Adv. 2019;5:eaaw0341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc. 2013;45:985–96.

    Article  PubMed  Google Scholar 

  18. Lieberman D. Exercised: the science of physical activity, rest and health. London: Penguin; 2021.

    Google Scholar 

  19. Lieberman DE, Bramble DM. Endurance running and the evolution of homo. Nature. 2004;432:345–52.

    Article  PubMed  CAS  Google Scholar 

  20. Steudel-Numbers KL, Weaver TD, Wall-Scheffler CM. The evolution of human running: effects of changes in lower-limb length on locomotor economy. J Hum Evol. 2007;53:191–6.

    Article  PubMed  Google Scholar 

  21. Pontzer H, Raichlen DA, Sockol MD. The metabolic cost of walking in humans, chimpanzees, and early hominins. J Hum Evol Elsevier Ltd. 2009;56:43–54.

    Article  Google Scholar 

  22. Longman DP, Wells JCK, Stock JT. Human athletic paleobiology; using sport as a model to investigate human evolutionary adaptation. Am J Phys Anthropol. 2020;1–18. https://doi.org/10.1002/ajpa.23992.

  23. Darwin C. On the origin of species by means of natural selection, or preservation of favoured races in the struggle for life. London: John Murray; 1859.

    Book  Google Scholar 

  24. Darwin C, Wallace A. On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. J Proc Linn Soc Lond. 1858;3:45–62.

    Google Scholar 

  25. Hill K. Life history theory and evolutionary anthropology. Evol Anthropol Issues News Rev. 1993;2:78–88.

    Article  CAS  Google Scholar 

  26. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996;11:317–21.

    Article  CAS  PubMed  Google Scholar 

  27. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos. 2000;88:87–98.

    Article  Google Scholar 

  28. McDade TW. Life history theory and the immune system: steps toward a human ecological immunology. Am J Phys Anthropol. 2003;122:100–25.

    Article  Google Scholar 

  29. Wells JCK. Evolutionary public health: How interventions may benefit from insights generated by life history theory. In: Schulkin J, Power M, editors. Integrating evolutionary biology into medical education: for maternal and child healthcare students, clinicians, and scientists. Oxford: Oxford Scholarship Online; 2020.

    Google Scholar 

  30. Stearns S. The evolution of life histories. Oxford: Oxford University Press; 1992.

    Google Scholar 

  31. Wells JCK, Nesse RM, Sear R, Johnstone RA, Stearns SC. Evolutionary public health: introducing the concept. Lancet. 2017;390:500–9.

    Article  PubMed  Google Scholar 

  32. Bronson F. Mammalian reproductive biology. Chicago: University of Chicago Press; 1991.

    Google Scholar 

  33. Wells J, Stock J. The biology of the colonizing ape. Am J Phys Anthropol. 2007;45:191–222.

    Article  PubMed  Google Scholar 

  34. Flatt T, Heyland A. Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. In: Flatt T, Heyland A, editors. New York: Oxford University Press; 2011. https://doi.org/10.1093/acprof:oso/9780199568765.001.0001.

  35. Ellison P. Endocrinology, energetics, and human life history: a synthetic model. Horm Behav. 2017;91:97–106.

    Article  PubMed  Google Scholar 

  36. West-Eberhard M. Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst. 1989;20:249–78.

    Article  Google Scholar 

  37. Pigliucci M, Murren C, Schlichting C. Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol. 2006;209:2362–7.

    Article  PubMed  Google Scholar 

  38. Wells J. The metabolic ghetto: an evolutionary perspective on nutrition, power relations, and chronic disease. Cambridge: Cambridge University Press; 2016.

    Book  Google Scholar 

  39. Ellison PT. Energetics and reproductive effort. Am J Hum Biol. 2003;15:342–51.

    Article  PubMed  Google Scholar 

  40. Lahdenpera M, Lummaa V, Helle S, Tremblay M, Russell A. Fitness benefits of prolonged post-reproductive lifespan in women. Nature. 2004;428:178–81.

    Article  PubMed  CAS  Google Scholar 

  41. Kaplan H, Hill K, Lancaster J, Hurtado A. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol. 2000;9(4):156–85.

    Article  Google Scholar 

  42. Polak M, Starmer WT. Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proc R Soc B Biol Sci. 1998;265:2197–201.

    Article  CAS  Google Scholar 

  43. De Souza M, Koltun K, Williams N. 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. Sport Med. 2019;49:125–37.

    Article  Google Scholar 

  44. Koltun K, De Souza M, Scheid J, Williams N. Energy availability is associated with luteinizing hormone pulse frequency and induction of luteal phase defects. J Clin Endocrinol Metab. 2020;105:185–93.

    Article  Google Scholar 

  45. Loucks A. Energy availability, not body fatness, regulates reproductive function in women. Exerc Sport Sci Rev. 2003;31:144–8.

    Article  PubMed  Google Scholar 

  46. Tudor-Locke C, McColl R. Factors related to variation in premenopausal bone mineral status: a health promotion approach. Osteoporos Int. 2000;11:1–24.

    Article  CAS  PubMed  Google Scholar 

  47. O’Donnell E, Goodman J, Harvey P. Cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women. J Clin Endocrinol Metab. 2011;96:3638–48.

    Article  PubMed  CAS  Google Scholar 

  48. Wade G, Schneider J, Li H. Control of fertility by metabolic cues. Am J Physiol. 1996;1:1–19.

    Google Scholar 

  49. Jasienska G. The fragile wisdom: an evolutionary view on women’s biology and health. Cambridge: Harvard University Press; 2013.

    Book  Google Scholar 

  50. Butte N, King J. Energy requirements during pregnancy and lactation. Public Health Nutr. 2005;8:1010–27.

    Article  PubMed  Google Scholar 

  51. Most J, Dervis S, Haman F, Adamo K, Redman L. Energy intake requirements in pregnancy. Nutrients. 2019;11:1812.

    Article  CAS  PubMed Central  Google Scholar 

  52. Jasienska G. Costs of reproduction and ageing in the human female. Philos Trans R Soc Lond Ser B Biol Sci. 2020;375:21090615.

    Article  Google Scholar 

  53. Areta J. Case study: resumption of eumenorrhea in parallel with high training load after 4 years of menstrual dysfunction: a 5-year follow-up of an elite female cyclist. Int J Sport Nutr Exerc Metab. 2020;1–6. https://doi.org/10.1123/ijsnem.2019-0284.

  54. Cialdella-Kam L, Guebels C, Maddalozzo G, Manore M. Dietary intervention restored menses in female athletes with exercise-associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients. 2014;6:3018–39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Williams N, Mallinson R, De Souza M. Rationale and study design of an intervention of increased energy intake in women with exercise-associated menstrual disturbances to improve menstrual function and bone health: the REFUEL study. Contemp Clin Trials Commun. 2019;14:100325.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Panter-brick C, Lotstein DS, Ellison PT. Seasonality of reproductive function and weight loss in rural Nepali women. Hum Reprod. 1993;8:684–90.

    Article  CAS  PubMed  Google Scholar 

  57. Jasienska G, Bribiescas R, Furberg A, Helle S, Nunez de la Mora A. Human reproduction and health: an evolutionary perspective. Lancet. 2017;390:510–20.

    Article  PubMed  Google Scholar 

  58. Jasienska G, Ellison P. Energetic factors and seasonal changes in ovarian function in women from rural Poland. Am J Hum Biol. 2004;16:563–80.

    Article  PubMed  Google Scholar 

  59. Tenforde A, Barrack M, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sport Med. 2016;46:171–82.

    Article  Google Scholar 

  60. McGuire A, Warrington G, Doyle L. Low energy availability in male athletes: a systematic review of incidence, associations and effects. Transl Sport Med. 2020;3:173–87.

    Article  Google Scholar 

  61. Lane A, Hackney A. Reproductive dysfunction from the stress of exercise training is not gender specific: the “exercise-hypogonadal male condition.” J Endocrinol Diabetes. 2014;1:4.

    PubMed  PubMed Central  Google Scholar 

  62. Koehler K, Hoerner N, Gibbs J, Zinner C, Braun H, De Souza M, et al. 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;34:1–9.

    Article  Google Scholar 

  63. 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.

    Article  CAS  PubMed  Google Scholar 

  64. Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43:110–6.

    Article  PubMed  Google Scholar 

  65. Pontzer H. Energy constraint as a novel mechanism linking exercise and health. Physiology. 2018;33:384–93.

    Article  CAS  PubMed  Google Scholar 

  66. Sundgot-Borgen J, Sundgot-Borgen C, Myklebust G, Solvberg N, Torstveit M. Elite athletes get pregnant, have healthy babies and return to sport early postpartum. BMJ Open Sport Exerc Med. 2019;21:e000652.

    Article  Google Scholar 

  67. Wade G, Jones J. Neuroendrocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1277-1296.

    Article  CAS  PubMed  Google Scholar 

  68. Papageorgiou M, Dolan E, Elliott KJ, Craig S. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2018;57:847–59.

    Article  PubMed  Google Scholar 

  69. Hutson M, O’Donnell E, Brooke-Wavell K, Sale C, Blagrove R. Effects of low energy availability on bone health in endurance athletes and high-impact exercise as a potential countermeasure: a narrative review. Sport Med. 2020;51:391–403.

    Article  Google Scholar 

  70. Dolan E, Varley I, Ackerman K, Pereira R, Elliott-Sale K, Sale C. The bone metabolic response to exercise and nutrition. Exerc Sport Sci Rev. 2020;48:49–58.

    Article  PubMed  Google Scholar 

  71. Ackerman K, Nazem T, Chapko D, Russell M, Mendes N, Taylor A, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab. 2011;96:3123–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Zanker CL, Swaine IL. Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med. 1998;32:167–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dolan E, McGoldrick A, Davenport C, Kelleher G, Byrne B, Tormey W, et al. An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys. J Bone Miner Metab. 2012;30:534–42.

    Article  CAS  PubMed  Google Scholar 

  74. De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone. 2008;43:140–8.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  76. Heikura I, Uusitalo A, Stellingwerff T, Bergland D, Mero A, Burke L. 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;28:403–11.

    Article  CAS  PubMed  Google Scholar 

  77. Tenforde A, DeLuca S, Wu A, Ackerman K, Lewis M, Rauh M, et al. Prevalence and factors associated with bone stress injury in middle school runners. PM&R J Inj Funct Rehabil. 2021;12673. https://doi.org/10.1002/pmrj.12673.

  78. Barrack M, Gibbs J, De Souza M, Williams N, Nichols J, Rauh M, et al. Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med. 2014;42:949–58.

    Article  PubMed  Google Scholar 

  79. Kirkwood T, Rose M. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond Ser B Biol Sci. 1991;332:15–24.

    Article  CAS  Google Scholar 

  80. Madimenos F. An evolutionary and life-history perspective on osteoporosis. Annu Rev Anthropol. 2015;44:189–206.

    Article  Google Scholar 

  81. Hutson M, O’Donnell E, Petherick E, Brooke-Wavell K, Blagrove R. Incidence of bone stress injury is greater in competitive female distance runners with menstrual disturbances independent of participation in plyometric training. J Sports Sci. 2021;39:2558–66.

    Article  PubMed  Google Scholar 

  82. Wolfe R. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84:475–82.

    Article  CAS  PubMed  Google Scholar 

  83. Elia M. Organ and tissue contribution to metabolic rate. In: Kinney J, Tucker H, editors. Energy metabolism: tissue determinants and cellular corollaries. New York: Raven Press; 1992. p. 61–80.

    Google Scholar 

  84. Cunningham J. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am J Clin Nutr. 1980;33:2372–4.

    Article  CAS  PubMed  Google Scholar 

  85. Muchlinksi M, Hemingway H, Pastor J, Omstead K, Burrows A. How the brain may have shaped muscle anatomy and physiology: a preliminary study. Anat Rec. 2018;301:528–37.

    Article  CAS  Google Scholar 

  86. Carbone JW, McClung JP, Pasiakos SM. Recent advances in the characterization of skeletal muscle and whole-body protein responses to dietary protein and exercise during negative energy balance. Adv Nutr. 2019;10:70–9.

    Article  PubMed  Google Scholar 

  87. Oliveira-Junior G, Pinto R, Shirley M, Longman D, Koehler K, Saunders B, et al. The skeletal muscle response to energy deficiency: a life history perspective. Adapt Hum Behav Physiol. 2021. https://doi.org/10.1007/s40750-021-00182-4.

  88. Henry C. The biology of human starvation: Some new insights. Nutr Bull. 2008;26:205–11.

    Article  Google Scholar 

  89. Widdowson E. The response of the sexes to nutritional stress. Proc Nutr Soc. 1976;35:175–80.

    Article  CAS  PubMed  Google Scholar 

  90. PrayGod G, Range N, Faurholt-Jepsen D, Jeremiah K, Faurholt-Jepsen M, Aabye M, et al. Predictors of body composition changes during tuberculosis treatment in Mwanza, Tanzania. Eur J Nutr. 2015;69:1125–32.

    Article  CAS  Google Scholar 

  91. Forbes G. Body fat content influences the body composition response to nutrition and exercise. Ann N Y Acad Sci. 2000;904:359–65.

    Article  CAS  PubMed  Google Scholar 

  92. Ocobock C. Body fat attenuates muscle mass catabolism among physically active humans in temperate and cold high altitude environments. Am J Hum Biol. 2017;29:23013.

    Article  Google Scholar 

  93. Areta JL, Burke LM, Camera DM, West DWD, Crawshay S, Moore DR, et al. Reduced resting skeletal muscle protein synthesis is rescued by resistance exercise and protein ingestion following short-term energy deficit. Am J Physiol Endocrinol Metab. 2014;306:989–97.

    Article  CAS  Google Scholar 

  94. Hector AJ, McGlory C, Damas F, Mazara N, Baker SK, Phillips SM. Pronounced energy restriction with elevated protein intake results in no change in proteolysis and reductions in skeletal muscle protein synthesis that are mitigated by resistance exercise. FASEB J. 2018;32:265–75.

    Article  CAS  PubMed  Google Scholar 

  95. Murphy C, Churchward-Venne T, Mitchell C, Kolar N, Kassis A, Karagounis L, et al. Hypoenergetic dietinduced reductions in myofibrillar protein synthesis are restored with resistance training and balanced daily protein ingestion in older men. Am J Physiol Endocrinol Metab. 2015;308:734–43.

    Article  CAS  Google Scholar 

  96. Pasiakos S, Vislocky L, Carbone J, Altieri N, Konopelski K, Freake H, et al. Acute energy deprivation affects skeletal muscle protein synthesis and associated intracellular signaling proteins in physically active adults. J Nutr. 2010;140:745–51.

    Article  CAS  PubMed  Google Scholar 

  97. Wilkinson D, Hossain T, Hill D, Phillips B, Crossland H, Williams J, et al. Effects of leucine and its metabolite β-hydroxy-β-methylbutyrate on human skeletal muscle protein metabolism. J Physiol. 2013;591:2911–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Longland T, Oikawa S, Mitchell C, Devries M, Phillips S. Higher compared with lower dietary protein during an energy deficit combined with intense exercise promotes greater lean mass gain and fat mass loss: a randomized trial. Am J Clin Nutr. 2016;103:738–46.

    Article  CAS  PubMed  Google Scholar 

  99. Ghoch M, Soave F, Calugi S, Dalle GR. Eating disorders, physical fitness and sport performance: a systematic review. Nutrients. 2013;5:140–60.

    Article  Google Scholar 

  100. Hackney A, Walz E. Hormonal adaptation and the stress of exercise training: the role of glucocorticoids. Trends Sport Sci. 2013;4:165–71.

    Google Scholar 

  101. Stellingwerff T, Morton J, Burke L. A framework for periodized nutrition for athletes. Int J Sport Nutr Exerc Metab. 2019;29:141–51.

    Article  CAS  PubMed  Google Scholar 

  102. Oliver S, Laing S, Wilson S, Bilzon J, Walsh N. Endurance running performance after 48 hours of restricted fluid and/or energy intake. Med Sci Sport Exerc. 2007;39:316–22.

    Article  Google Scholar 

  103. Kojima C, Ashibashi A, Tanabe Y, Iwayama K, Kamei A, Takahashi H, et al. Muscle glycogen content during endurance training under low energy availability. Med Sci Sport Exerc. 2020;52:187–95.

    Article  CAS  Google Scholar 

  104. Fogelholm G, Koskinen R, Laakso J, Rankinen T, Ruokonen I. Gradual and rapid weight loss: effects on nutrition and performance in male athletes. Med Sci Sport Exerc. 1993;25:371–7.

    Article  CAS  Google Scholar 

  105. Pons V, Riera J, Capo X, Martorell M, Sureda A, Tur J, et al. Calorie restriction regime enhances physical performance of trained athlete. J Int Soc Sports Nutr. 2018;15:12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Tornberg A, Melin A, Manderson Koivula F, Johansson A, Skouby S, Faber J, et al. Reduced neuromuscular performance in amenorrheic elite endurance athletes. Med Sci Sport Exerc. 2017;49:2478–85.

    Article  Google Scholar 

  107. Vanheest J, Rodgers C, Majoney C, De Souza M. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sport Exerc. 2014;46:156–66.

    Article  Google Scholar 

  108. Ihalainen J, Kettunen O, McGawley K, Solli G, Hackney A, Mero A, et al. Body composition, energy availability, training, and menstrual status in female runners. Int J Sports Physiol Perform. 2021;16:1043–8.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  110. da Silva K, Silva C, Costa R, De Moraes S. How does protein malnutrition or food deprivation interfere with the growth of the epiphyseal plate in animals? Int J Morphol. 2013;31:584–9.

    Article  Google Scholar 

  111. Caine D, Lewis R, O’Connor P, Howe W, Bass S. Does gymnastics training inhibit growth of females. Clin J Sport Med. 2001;11:260–70.

    Article  CAS  PubMed  Google Scholar 

  112. Baxter-Jones A, Maffuli N, Mirwald R. Does elite competition inhibit growth and delay maturation in some gymnasts? Probably not. Pediatr Exerc Sci. 2003;15:373–82.

    Article  Google Scholar 

  113. Urlacher S, Snodgrass J, Dugas L, Sugiyama L, Liebert M, Joyce C, et al. Constraint and trade-offs regulate energy expenditure during childhood. Sci Adv. 2019;5:eaax1065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Urlacher S, Ellison P, Sugiyama L, Pontzer H, Eick G, Liebert M, et al. Tradeoffs between immune function and childhood growth among Amazonian forager-horticulturalists. Proc Natl Acad Sci USA. 2018;115:E3914–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Campbell JP, Turner JE. Debunking the myth of exercise-induced immune suppression: redefining the impact of exercise on immunological health across the lifespan. Front Immunol. 2018;9:648.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Walsh NP. Nutrition and athlete immune health: new perspectives on an old paradigm. Sport Med. 2019;49:153–68.

    Article  Google Scholar 

  117. Simpson R, Campbell J, Gleeson M, Kruger L, Nieman D, Pyne D, et al. Can exercise affect immune function to increase susceptibility to infection? Exerc Immunol Rev. 2020;26:8–22.

    PubMed  Google Scholar 

  118. Shimizu K, Suzuki N, Nakamura M, Aizawa K, Imai T, Suzuke S, et al. Mucosal immune function comparison between amenorrheic and eumenorrheic distance runners. J Strength Cond Res. 2012;26:1402–6.

    Article  PubMed  Google Scholar 

  119. Drew MK, Vlahovich N, Hughes D, Appaneal R, Peterson K, Burke L, et al. A multifactorial evaluation of illness risk factors in athletes preparing for the Summer Olympic Games. J Sci Med Sport. 2017;20:745–50.

    Article  PubMed  Google Scholar 

  120. Hagmar M, Hirschberg AL, Berglund L, Berglund B. Special attention to the weight-control strategies employed by olympic athletes striving for leanness is required. Clin J Sport Med. 2008;18:5–9.

    Article  PubMed  Google Scholar 

  121. Sarin HV, Gudelj I, Honkanen J, Ihalainen JK, Vuorela A, Lee JH, et al. Molecular pathways mediating immunosuppression in response to prolonged intensive physical training, low-energy availability, and intensive weight loss. Front Immunol. 2019;10:907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Longman DP, Prall SP, Shattuck EC, Stephen ID, Stock JT, Wells JCK, et al. Short-term resource allocation during extensive athletic competition. Am J Hum Biol. 2018;30:1–11.

    Article  Google Scholar 

  123. Slotwinska S, Slowwinski R. Immune disorders in anorexia. Cent Eur J Immunol. 2017;42:294–300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Marcos A. Eating disorder: a situation of malnutrition with peculiar changes in the immune system. Eur J Clin Nutr. 2000;54:61–4.

    Article  Google Scholar 

  125. Burke L, Lundy B, Fahrenholtz I, Melin A. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. Int J Sport Nutr Exerc Metab. 2018;28:350–63.

    Article  PubMed  Google Scholar 

  126. Fahrenholtz I, Sjodin A, Benardot D, Tornberg A, Skouby S, Faber J, et al. Within-day energy deficiency and reproductive function in female endurance athletes. Scand J Med Sci Sport. 2018;28:1139–46.

    Article  CAS  Google Scholar 

  127. Speakman J. Why does caloric restriction increase life and healthspan? The “clean cupboards” hypothesis. Natl Sci Rev. 2020;7:1153–6.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank Rafaela Silvério Pinto for her assistance with the development of Fig. 1.

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Authors and Affiliations

  1. Division of GI, Hepatology and Nutrition, The Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Meghan K. Shirley

  2. School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, UK

    Daniel P. Longman

  3. Musculoskeletal Physiology Research Group, Sport Health and Performance Enhancement Research Centre, School of Science and Technology, Nottingham Trent University, Nottingham, UK

    Kirsty J. Elliott-Sale & Craig Sale

  4. Department of Exercise and Sport Science, Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Anthony C. Hackney

  5. Applied Physiology and Nutrition Research Group, School of Physical Education and Sport, Rheumatology Division, Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao Paulo, SP, Brazil

    Eimear Dolan

Authors
  1. Meghan K. Shirley
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  2. Daniel P. Longman
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  3. Kirsty J. Elliott-Sale
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  4. Anthony C. Hackney
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  5. Craig Sale
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  6. Eimear Dolan
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Correspondence to Eimear Dolan.

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Funding

Eimear Dolan is financially supported by the Fundação de Ampara a Pesquisa do Estado do São Paulo (FAPESP: 2019/05616-6 and 2019/26899-6). No other sources of funding were used to assist in the preparation of this article.

Conflicts of interest

Meghan Shirley, Daniel Longman, Kirsty Elliott-Sale, Anthony Hackney, Craig Sale, and Eimear Dolan declare that they have no conflicts of interest relevant to the content of this review.

Author contributions

MKS and ED conceived the original idea and developed the initial draft of this article, with ongoing critical input from DPL, ACH, KES, and CS. All authors read and approved the final version.

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Shirley, M.K., Longman, D.P., Elliott-Sale, K.J. et al. A Life History Perspective on Athletes with Low Energy Availability. Sports Med 52, 1223–1234 (2022). https://doi.org/10.1007/s40279-022-01643-w

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