CoChat
Sign Up
Cited by 57Sports Performance and TrainingEating Disorders and BehaviorsEvolutionary Psychology and Human Behavior

A Life History Perspective on Athletes with Low Energy Availability

Open access
Shirley, Meghan K., Longman, Daniel P., Elliott-Sale, Kirsty J., Hackney, Anthony C., Sale, Craig, Dolan, Eimear·2022·Sports Medicine
DOI 10.1007/s40279-022-01643-w
Open this paper in CoChat — free account

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s40279-022-01643-w

Cites

11 of 11 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Inadequate energy intake or an increased energy commitment to one biological process favours trade-offs that allocate energy away from other processes, especially growth, reproduction or maintenance.

    “Inadequate EI or an increased energy commitment to one biological process favours trade-offs that allocate energy away from other processes, especially growth, reproduction or maintenance.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [32]

  • Life History Theory proposes that various biological processes related to growth, health, activity and reproduction compete for finite energy resources, with different priorities depending on the phase in the life cycle and other circumstances.

    “Life History Theory proposes that various biological processes related to growth, health, activity and reproduction compete for finite energy resources, with different priorities depending on the phase in the life cycle and other circumstances.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [32]

  • Humans, like other animals, are adapted to cope with periods of LEA by downregulating biological processes that are temporarily unnecessary or reducible.

    “Therefore, humans, like other animals, are adapted to cope with periods of LEA by downregulating biological processes that are temporarily unnecessary or reducible.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [32]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 105

  1. [1]1. Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29:37-41. 434
  2. [3]3. In: Hackney A, Constantini N, editors. Endocrinol Phys Act Sport. 3rd ed. Springer Nature; 2020. p. 171-91. 436 3. Gibson M, Lawson D. Applying evolutionary anthropology. Evol Anthropol. 2015;24:3-14. 437
  3. [4]4. Stearns SC. Trade-offs in life-history evolution. Funct Ecol. 1989;3:259. 438
  4. [7]7. selection. Am Nat. 1970;104:1-24. 440 8. 441 9. 442
  5. [8]8. Areta J, Taylor H, Koehler K. Low energy availability: history, definition and evidence of its endocrine, 447 - metabolic and physiological effects in prospective studies in females and males. Eur J Appl Physiol. - 2021;121:1-21. 448
  6. [9]9. Hackney A. Hypogonadism in exercising males: Dysfunction or adaptive-regulatory adjustment? Front 449 - Endocrinol (Lausanne). 2020;11:11. 450
  7. [11]11. Mountjoy M, Burke L, Ackerman KE, Blauwet C, Lebrun C, Melin A, et al. International Olympic 453 - Committee (IOC) consensus statement on relative energy deficiency in sport (RED-S): 2018 Update. Int J Sport 454 - Nutr Exerc Metab. 2018;28:316-31. 455 456
  8. [12]12. Reznick D, Nunney L, Tessier A. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol - Evol. 2000;15:421-5. 457
  9. [13]13. Zera A, Harshman L. The physiology of life history trade- offs in animals. Ecology. 2001;32:95-126. 458
  10. [14]14. Bronson F. Mammalian reproduction: an ecological perspective. Biol Reprod. 1985;32:1-26. 459
  11. [15]15. Cody M. A General Theory of Clutch Size. Evolution (N Y). 1996;20:174-84. 460
  12. [17]17. Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female 463 - athlete triad. Med Sci Sports Exerc. 2013;45:985-96. 464
  13. [18]18. Lieberman D. Exercised: The science of physical activity, rest and health. Penguin; 2021. 465
  14. [19]19. Lieberman DE, Bramble DM. Endurance running and the evolution of Homo. Nature. 2004;432:345-52. 466
  15. [20]20. Steudel-Numbers KL, Weaver TD, Wall-Scheffler CM. The evolution of human running: Effects of changes 467 in lower-limb length on locomotor economy. J Hum Evol. 2007;53:191-6. 468 469 470
  16. [21]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. 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496
  17. [24]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 London. 1858;3:45-62.
  18. [25]25. Hill K. Life history theory and evolutionary anthropology. Evol Anthropol Issues, News, Rev. 1993;2:7888.
  19. [26]26. Sheldon BC, Verhulst S. Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996;11:317-21.
  20. [27]27. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: Just what is the cost of immunity? Oikos. 2000;88:87-98.
  21. [28]28. McDade TW. Life history theory and the immune system: Steps toward a human ecological immunology. Am J Phys Anthropol. 2003;122:100-25.
  22. [29]29. Wells JCK. Evolutionary public health: How interventions may benefit from insights generated by life history theory. In: Schulkin J, Power M, editors. Integr Evol Biol into Med Educ - Matern child Healthc students, Clin Sci. Oxford: Oxford Scholarship Online; 2020.
  23. [30]30. Stearns S. The evolution of life histories. Oxford: Oxford University Press; 1992.
  24. [31]31. Wells JCK, Nesse RM, Sear R, Johnstone RA, Stearns SC. Evolutionary public health: introducing the concept. Lancet. Elsevier Ltd; 2017;390:500-9.
  25. [32]32. Bronson F. Mammalian reproductive biology. Chicago: University of Chicago Press; 1991.
  26. [33]33. Wells J, Stock J. The biology of the colonizing ape. Am J Phys Anthropol. 2007;45:191-222.
  27. [34]34. Flatt T, Heyland A. Mechanisms of life history evolution: The genetics and physiology of life history traits and trade-offs. Flatt T, Heyland A, editors. New York: Oxford University Press; 2011.
  28. [35]35. Ellison P. Endocrinology, energetics, and human life history: A synthetic model. Horm Behav. 2017;91:97106.
  29. [36]36. West-Eberhard M. Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst. 1989;20:249-78. 497
  30. [37]37. Pigliucci M, Murren C, Schlichting C. Phenotypic plasticity and evolution by genetic assimilation. J Exp 498 Biol. 2006;209:2362-7. 499 500 501
  31. [38]38. Wells J. The metabolic ghetto: An evolutionary perspective on nutrition, power relations, and chronic disease. Cambridge: Cambridge University Press; 2016. 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528
  32. [39]39. Ellison PT. Energetics and reproductive effort. Am J Hum Biol. 2003;15:342-51.
  33. [40]40. Lahdenpera M, Lummaa V, Helle S, Tremblay M, Russell A. Fitness benefits of prolonged postreproductive lifespan in women. Nature. 2004;428:178-81.
  34. [42]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.
  35. [43]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.
  36. [44]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.
  37. [46]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.
  38. [47]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.
  39. [48]48. Wade G, Schneider J, Li H. Control of fertility by metabolic cues. Am J Physiol. 1996;1:1-19.
  40. [49]49. Jasienska G. The fragile wisdom: An evolutionary view on women's biology and health. Cambridge, Massachusetts: Harvard University Press; 2013.
  41. [50]50. Butte N, King J. Energy requirements during pregnancy and lactation. Public Health Nutr. 2005;8:1010-27.
  42. [51]51. Most J, Dervis S, Haman F, Adamo K, Redman L. Energy intake requirements in pregnancy. Nutrients. 2019;11:1812.
  43. [52]52. Jasienska G. Costs of reproduction and ageing in the human female. Philos Trans R Soc London Ser B Biol Sci. 2020;375:21090615.
  44. [54]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.
  45. [55]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.
  46. [56]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.
  47. [57]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.
  48. [58]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.
  49. [59]59. Tenforde A, Barrack M, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sport Med. 2016;46:171-82.
  50. [60]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.
  51. [61]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.
  52. [62]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.
  53. [63]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.
  54. [64]64. Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43:110-6.
  55. [65]65. Pontzer H. Energy constraint as a novel mechanism linking exercise and health. Physiol. 2018;33:384-93.
  56. [66]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.
  57. [67]67. Wade G, Jones J. Neuroendrocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1277-1296.
  58. [68]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. 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595
  59. [69]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.
  60. [70]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.
  61. [71]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.
  62. [72]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.
  63. [73]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.
  64. [74]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.
  65. [75]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.
  66. [76]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.
  67. [78]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.
  68. [79]79. Kirkwood T, Rose M. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc London Ser B Biol Sci. 1991;332:15-24.
  69. [80]80. Madimenos F. An evolutionary and life-history perspective on osteoporosis. Annu Rev Anthropol. 2015;44:189-206.
  70. [81]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.
  71. [82]82. Wolfe R. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84:475-82. 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629
  72. [83]83. Elia M. Organ and tissue contribution to metabolic rate. In: Kinney J, Tucker H, editors. Energy Metab Tissue Determ Cell Corollaries. New York: Raven Press; 1992. p. 61-80.
  73. [84]84. Cunningham J. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am J Clin Nutr. 1980;33:2372-4.
  74. [85]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.
  75. [87]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;in press.
  76. [88]88. Henry C. The biology of human starvation: Some new insights. Nutr Bull. 2008;26:205-11.
  77. [90]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.
  78. [91]91. Forbes G. Body fat content influences the body composition response to nutrition and exercise. Ann N Y Acad Sci. 2000;904:359-65.
  79. [92]92. Ocobock C. Body fat attenuates muscle mass catabolism among physically active humans in temperate and cold high altitude environmentsass catabolism among physically active humans in temperate and cold high altitude environments. Am J Hum Biol. 2017;29:23013.
  80. [95]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.
  81. [97]97. Wilkinson D, Hossain T, Hill D, Phillips B, Crossland H, Williams J, et al. Effects of leucine and its 2. metabolite β-hydroxy-β-methylbutyrate on human skeletal muscle protein metabolism. J Physiol. - 2013;591:2911-23. 630 631
  82. [99]99. Ghoch M, Soave F, Calugi S, Dalle Grave R. Eating disorders, physical fitness and sport performance: A systematic review. Nutrients. 2013;5:140-60.
  83. [100]100. Hackney A, Walz E. Hormonal adaptation and the stress of exercise training: the role of glucocorticoids. Trends Sport Sci. 2013;4:165-71.
  84. [101]101. Stellingwerff T, Morton J, Burke L. A framework for periodized nutrition for athletes. Int J Sport Nutr Exerc Metab. 2019;29:141-51.
  85. [102]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.
  86. [104]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.
  87. [105]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.
  88. [106]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.
  89. [108]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.
  90. [109]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.
  91. [110]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.
  92. [111]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.
  93. [112]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. 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695
  94. [114]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 U S A. 2018;115:E3914-24.
  95. [116]116. Walsh NP. Nutrition and athlete immune health: New perspectives on an old paradigm. Sport Med. Springer International Publishing; 2019;49:153-68.
  96. [117]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.
  97. [118]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.
  98. [119]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. Sports Medicine Australia; 2017;20:745-50.
  99. [120]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.
  100. [122]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.
  101. [123]123. Slotwinska S, Slowwinski R. Immune disorders in anorexia. Cent Eur J Immunol. 2017;42:294-300.
  102. [124]124. Marcos A. Eating disorder: A situation of malnutrition with peculiar chenges in the immune system. Eur J Clin Nutr. 2000;54:61-4.
  103. [125]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.
  104. [126]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. 18AD;28:1139-46.
  105. [127]127. Speakman J. Why does caloric restriction increase life and healthspan? The 'clean cupboards' hypothesis. Natl Sci Rev. 2020;7:1153-6.

Cited by

Sorted by citations

Authors
Shirley, M. K., Longman, D. P., Elliott-Sale, K. J., Hackney, A. C., Sale, C., & Dolan, E.
Affiliations
  • Children's Hospital of Philadelphia (US)
  • Loughborough University (GB)
  • Nottingham Trent University (GB)
  • University of North Carolina at Chapel Hill (US)
  • Universidade de São Paulo (BR)
Corresponding author
Dolan, Eimear
ORCID
Venue
Sports Medicine
Publisher
Springer Science and Business Media LLC
Published
2022-02-03
Volume
52
Issue
6
Pages
1223-1234
ISSN
  • 0112-1642 (ISSN-L)
  • 1179-2035
DOI
10.1007/s40279-022-01643-w
OpenAlex
W4210301852
Cited by
57
References
11
Citations by year
2026: 14 · 2025: 5 · 2024: 13 · 2023: 16 · 2022: 6 · 2020: 2 · 2019: 1
FWCI
2.19
Type
journal article
Language
en
Open access
Licence
Locations
  • Sports Medicine (publishedVersion)
  • PubMed (publishedVersion)
  • Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
  • e-space (Manchester Metropolitan University) (acceptedVersion)
  • Loughborough University Research Repository (Loughborough University) (submittedVersion, cc-by)
Funders
Fundação de Amparo à Pesquisa do Estado de São Paulo (2019/05616-6, 2019/26899-6)
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
  • Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
Keywords
low energy availability, life history theory, athletes, energy trade-offs, negative energy balance, energy intake, athlete health, athletic performance, reproduction, somatic maintenance, growth, immunity, evolutionary biology
MeSH terms
Energy Intake, Energy Metabolism, Humans, Reproduction, Sports, Athletes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review