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European Journal of Applied Physiology

, Volume 119, Issue 7, pp 1463–1478 | Cite as

Iron considerations for the athlete: a narrative review

  • Marc Sim
  • Laura A. Garvican-Lewis
  • Gregory R. Cox
  • Andrew Govus
  • Alannah K. A. McKay
  • Trent Stellingwerff
  • Peter PeelingEmail author
Invited Review

Abstract

Iron plays a significant role in the body, and is specifically important to athletes, since it is a dominant feature in processes such as oxygen transport and energy metabolism. Despite its importance, athlete populations, especially females and endurance athletes, are commonly diagnosed with iron deficiency, suggesting an association between sport performance and iron regulation. Although iron deficiency is most common in female athletes (~ 15–35% athlete cohorts deficient), approximately 5–11% of male athlete cohorts also present with this issue. Furthermore, interest has grown in the mechanisms that influence iron absorption in athletes over the last decade, with the link between iron regulation and exercise becoming a research focus. Specifically, exercise-induced increases in the master iron regulatory hormone, hepcidin, has been highlighted as a contributing factor towards altered iron metabolism in athletes. To date, a plethora of research has been conducted, including investigation into the impact that sex hormones, diet (e.g. macronutrient manipulation), training and environmental stress (e.g. hypoxia due to altitude training) have on an athlete’s iron status, with numerous recommendations proposed for consideration. This review summarises the current state of research with respect to the aforementioned factors, drawing conclusions and recommendations for future work.

Keywords

Iron deficiency Anaemia Hepcidin Exercise 

Abbreviations

ΔHbmass

Change in haemoglobin mass

DMT-1

Divalent metal transporter 1

DCytB

Duodenal cytochrome b

ERFE

Erythroferrone

EPO

Erythropoietin

FSH

Follicle stimulating hormone

GI

Gastro-intestinal

Hb

Haemoglobin

Hbmass

Haemoglobin mass

HIF

Hypoxia-inducible factor

IL-6

Interleukin-6

IV

Intravenous

Fe

Iron

ID

Iron deficiency

IDA

Iron deficiency anaemia

IDNA

Iron deficient non-anaemia

LHTL

Live high, train low

LCHF

Low carbohydrate, high fat

LEA

Low energy availability

LH

Luteinising hormone

VO2max

Maximal oxygen uptake

mRNA

Messenger ribonucleic acid

OCC

Oral contraceptive cycle

OCP

Oral contraceptive pill

RDI

Recommended dietary intake

RED-S

Relative energy deficiency in sport

sTfR

Soluble transferrin receptor

TfR

Transferrin receptor

TfR-2

Transferrin receptor-2

vVO2peak

Velocity at peak oxygen uptake

Notes

Author contributions

All authors on this review contributed to each section equitably. The literature search, idea development, writing, reviewing and editing for each section were completed as a collective. Furthermore, all authors have provided specific insight on key aspects relevant to each sub-heading.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to disclose.

References

  1. Ackerman KE, Holtzman B, Cooper KM, Flynn EF, Bruinvels G, Tenforde AS, Popp KL, Simpkin AJ, Parziale AL (2018) Low energy availability surrogates correlate with health and performance consequences of relative energy deficiency in sport. Br J Sports Med 53:628–633Google Scholar
  2. Andrade AT, Souza JP, Shaw ST Jr, Belsey EM, Rowe PJ (1991) Menstrual blood loss and body iron stores in Brazilian women. Contraception 43:241–249Google Scholar
  3. Angstwurm MWA, Gärtner R, Ziegler-Heitbrock HWL (1997) Cyclic plasma IL-6 levels during normal menstrual cycle. Cytokine 9(5):370–374Google Scholar
  4. Armstrong LE, Pumerantz AC, Fiala KA, Roti MW, Kavouras SA, Casa DJ, Maresh CM (2010) Human hydration indices: acute and longitudinal reference values. IInt J Sport Nutr Exer Metab 20(2):145–153Google Scholar
  5. Bachman E, Feng R, Travison T, Li M, Olbina G, Ostland V, Ulloor J, Zhang A, Basaria S, Ganz T (2010) Testosterone suppresses hepcidin in men: a potential mechanism for testosterone-induced erythrocytosis. J Clin Endocrinol Metab 95(10):4743–4747Google Scholar
  6. Bachman E, Travison TG, Basaria S, Davda MN, Guo W, Li M, Connor Westfall J, Bae H, Gordeuk V, Bhasin S (2013) Testosterone induces erythrocytosis via increased erythropoietin and suppressed hepcidin: evidence for a new erythropoietin/hemoglobin set point. J Gerontol Ser A Biomed Sci Med Sci 69(6):725–735Google Scholar
  7. Badenhorst C, Dawson B, Cox G, Laarakkers C, Swinkels D, Peeling P (2015) Acute dietary carbohydrate manipulation and the subsequent inflammatory and hepcidin responses to exercise. Eur J App Physiol 115(12):2521–2530Google Scholar
  8. Badenhorst CE, Dawson B, Cox GR, Sim M, Laarakkers CM, Swinkels DW, Peeling P (2016) Seven days of high carbohydrate ingestion does not attenuate post-exercise IL-6 and hepcidin levels. Eur J Appl Physiol 116(9):1715–1724Google Scholar
  9. Bartsch P, Mairbaurl H, Friedmann B (1998) Pseudo-anemia caused by sports. Ther Umsch 55(4):251–255Google Scholar
  10. Bartsch P, Saltin B, Dvorak J (2008) Consensus statement on playing football at different altitude. Scand J Med Sci Sports 18:96–99Google Scholar
  11. Beard JL (2001) Iron biology in immune function, muscle metabolism and neuronal functioning. J Nutr 131(2):568S–579SGoogle Scholar
  12. Beard J, Tobin B (2000) Iron status and exercise. Am J Clin Nutr 72(2):594S–597SGoogle Scholar
  13. Bhasin S, Woodhouse L, Casaburi R, Singh AB, Bhasin D, Berman N, Chen X, Yarasheski KE, Magliano L, Dzekov C (2001) Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab 281(6):E1172–E1181Google Scholar
  14. Brittenham GM (2018) Disorders of iron homeostasis: iron deficiency and overload. In Hoffman R, Benz EJ, Silberstein LE, Heslop HE, Weitz JI, Anastasi J, Salama ME, Abutalib SA (eds) Hematology: Basic principles and practice, 7th edn. Elsevier, Philadelphia, PA, p. 478–490.  https://doi.org/10.1016/B978-0-323-35762-3.00036-6 Google Scholar
  15. Burden RJ, Morton K, Richards T, Whyte GP, Pedlar CR (2015) Is iron treatment beneficial in, iron-deficient but non-anaemic (IDNA) endurance athletes? A systematic review and meta-analysis. Br J Sports Med 49(21):1389–1397Google Scholar
  16. Burden RJ, Pollock N, Whyte GP, Richards T, Moore B, Busbridge M, Srai SK, Otto J, Pedlar CR (2015) Effect of intravenous iron on aerobic capacity and iron metabolism in elite athletes. Med Sci Sports Exerc 47(7):1399–1407Google Scholar
  17. Burke LM, Hawley JA, Jeukendrup A, Morton JP, Stellingwerff T, Maughan RJ (2018) Toward a common understanding of diet-exercise strategies to manipulate fuel availability for training and competition preparation in endurance sport. Int J Sport Nutr Exer Metab 28(5):451–463Google Scholar
  18. Canali S, Vecchi C, Garuti C, Montosi G, Babitt JL, Pietrangelo A (2016) The SMAD pathway is required for hepcidin response during endoplasmic reticulum stress. Endocrinology 157(10):3935–3945Google Scholar
  19. Castell LM, Nieman DC, Bermon S, Peeling P (2019) Exercise-induced illness and inflammation: can immunonutrition and iron help? Int J sport Nutr Exer Metab 29(2):181–188Google Scholar
  20. Chepelev NL, Willmore WG (2011) Regulation of iron pathways in response to hypoxia. Free Radic Biol Med 50(6):645–666Google Scholar
  21. Clenin G, Cordes M, Huber A, Schumacher YO, Noack P, Scales J, Kriemler S (2015) Iron deficiency in sports-definition, influence on performance and therapy. Swiss Med Wkly 145:w14196Google Scholar
  22. Constantini K, Wilhite DP, Chapman RF (2017) A clinician guide to altitude training for optimal endurance exercise performance at sea level. High Alt Med Biol 18(2):93–101Google Scholar
  23. Dahlquist DT, Stellingwerff T, Dieter BP, McKenzie DC, Koehle MS (2017) Effects of macro-and micronutrients on exercise-induced hepcidin response in highly trained endurance athletes. App Physiol Nutr Metab 42(10):1036–1043Google Scholar
  24. Dasharathy SS, Mumford SL, Pollack AZ, Perkins NJ, Mattison DR, Wactawski-Wende J, Schisterman EF (2012) Menstrual bleeding patterns among regularly menstruating women. Am J Epidemiol 175(6):536–545Google Scholar
  25. Dawson B, Goodman C, Blee T, Claydon G, Peeling P, Beilby J, Prins A (2006) Iron supplementation: oral tablets versus intramuscular injection. Int J Sport Nutr Exerc Metab 16(2):180–186Google Scholar
  26. De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL (1998) High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab 83(12):4220–4232Google Scholar
  27. DellaValle DM, Haas JD (2011) Impact of iron depletion without anemia on performance in trained endurance athletes at the beginning of a training season: a study of female collegiate rowers. Int J Sport Nutr Exerc Metab 21(6):501–506Google Scholar
  28. Dellavalle DM, Haas JD (2014) Iron supplementation improves energetic efficiency in iron-depleted female rowers. Med Sci Sports Exerc 46(6):1204–1215Google Scholar
  29. Dubnov G, Constantini NW (2004) Prevalence of iron depletion and anemia in top-level basketball players. Int J Sport Nutr Exerc Metab 14(1):30–37Google Scholar
  30. Fallon KE (2004) Utility of hematological and iron-related screening in elite athletes. Clin J Sport Med 14(3):145–152Google Scholar
  31. Fallon KE (2008) Screening for haematological and iron-related abnormalities in elite athletes-analysis of 576 cases. J Sci Med Sport 11(3):329–336Google Scholar
  32. Ferrucci L, Maggio M, Bandinelli S, Basaria S, Lauretani F, Ble A, Valenti G, Ershler WB, Guralnik JM, Longo DL (2006) Low testosterone levels and the risk of anemia in older men and women. Arch Int Med 166(13):1380–1388Google Scholar
  33. Frassinelli-Gunderson EP, Margen S, Brown JR (1985) Iron stores in users of oral contraceptive agents. Am J Clin Nutr 41(4):703–712Google Scholar
  34. Gardner GW, Edgerton VR, Senewiratne B, Barnard RJ, Ohira Y (1977) Physical work capacity and metabolic stress in subjects with iron deficiency anemia. Am J Clin Nutr 30(6):910–917Google Scholar
  35. Garvican LA, Lobigs L, Telford R, Fallon K, Gore CJ (2011) Haemoglobin mass in an anaemic female endurance runner before and after iron supplementation. Int J Sports Physiol Perform 6(1):137–140Google Scholar
  36. Garvican LA, Martin D, Quod M, Stephens B, Sassi A, Gore C (2012) Time course of the hemoglobin mass response to natural altitude training in elite endurance cyclists. Scand J Med Sci Sports 22(1):95–103Google Scholar
  37. Garvican LA, Saunders PU, Cardoso T, Macdougall IC, Lobigs LM, Fazakerley R, Fallon KE, Anderson B, Anson JM, Thompson KG (2014a) Intravenous iron supplementation in distance runners with low or suboptimal ferritin. Med Sci Sports Exerc 46(2):376–385Google Scholar
  38. Garvican LA, Saunders PU, Cardoso T, Macdougall IC, Lobigs LM, Fazakerley R, Fallon KE, Anderson B, Anson JM, Thompson KG, Gore CJ (2014b) Intravenous iron supplementation in distance runners with low or suboptimal ferritin. Med Sci Sports Exerc 46(2):376–385Google Scholar
  39. Garvican-Lewis LA, Govus AD, Peeling P, Abbiss CR, Gore CJ (2016) Iron supplementation and altitude: decision making using a regression tree. J Sports Sci Med 15(1):204–205Google Scholar
  40. Garvican-Lewis LA, Sharpe K, Gore CJ (2016) Time for a new metric for hypoxic dose? Am J Physiol Heart Circ Physiol 121(1):352–355Google Scholar
  41. Garvican-Lewis LA, Vuong VL, Govus AD, Peeling P, Jung G, Nemeth E, Hughes D, Lovell G, Eichner D, Gore CJ (2018) Intravenous iron does not augment the hemoglobin mass response to simulated hypoxia. Med Sci Sports Exerc 50(8):1669–1678Google Scholar
  42. Gill S (2017) British Dietetics Association food fact sheet for iron. https://www.bda.uk.com/foodfacts/iron_food_fact_sheet.pdf. Accessed 30 Apr 2019
  43. Ginsburg GS, O’Toole M, Rimm E, Douglas PS, Rifai N (2001) Gender differences in exercise-induced changes in sex hormone levels and lipid peroxidation in athletes participating in the Hawaii Ironman triathlon: Ginsburg-gender and exercise-induced lipid peroxidation. Clin Chim Acta 305(1–2):131–139Google Scholar
  44. Girelli D, Ugolini S, Busti F, Marchi G, Castagna A (2018) Modern iron replacement therapy: clinical and pathophysiological insights. Int J Hematol 107(1):16–30Google Scholar
  45. Goetze O, Schmitt J, Spliethoff K, Theurl I, Weiss G, Swinkels DW, Tjalsma H, Maggiorini M, Krayenbuhl P, Rau M (2013) Adaptation of iron transport and metabolism to acute high altitude hypoxia in mountaineers. Hepatology 58(6):2153–2162Google Scholar
  46. Govus AD, Garvican-Lewis LA, Abbiss CR, Peeling P, Gore CJ (2015) Pre-altitude serum ferritin levels and daily oral iron supplement dose mediate iron parameter and hemoglobin mass responses to altitude exposure. PLoS ONE 10(8):e0135120Google Scholar
  47. Guo W, Bachman E, Li M, Roy CN, Blusztajn J, Wong S, Chan SY, Serra C, Jasuja R, Travison TG (2013) Testosterone administration inhibits hepcidin transcription and is associated with increased iron incorporation into red blood cells. Aging Cell 12(2):280–291Google Scholar
  48. Haas JD, Brownlie T (2001) Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr 131(2):676S–690SGoogle Scholar
  49. Hackney AC (1996) The male reproductive system and endurance exercise. Med Sci Sports Exerc 28(2):180–189Google Scholar
  50. Hackney AC (2001) Endurance exercise training and reproductive endocrine dysfunction in men alterations in the hypothalamic–pituitary–testicular axis. Curr Pharmaceu Des 7(4):261–273Google Scholar
  51. Hackney A, Szczepanowska E, Viru A (2003) Basal testicular testosterone production in endurance-trained men is suppressed. Eur J Appl Physiol 89(2):198–201Google Scholar
  52. Hahn AG, Gore CJ (2001) The effect of altitude on cycling performance: a challenge to traditional concepts. Sports Med 31(7):533–557Google Scholar
  53. Hall R, Peeling P, Nemeth E, Bergland D, McCluskey WT, Stellingwerff T (2019) Single versus split dose of iron optimizes haemoglobin mass gains at 2106 m altitude. Med Sci Sports Exerc 51(4):751–759Google Scholar
  54. Hauser A, Troesch S, Steiner T, Brocherie F, Girard O, Saugy JJ, Schmitt L, Millet GP, Wehrlin JP (2018) Do male athletes with already high initial haemoglobin mass benefit from ‘live high-train low’altitude training? Exp Physiol 103(1):68–76Google Scholar
  55. Heikura IA, Uusitalo AL, Stellingwerff T, Bergland D, Mero AA, Burke LM (2018) Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. J Sport Nutr Exer Metab 28(4):403–411Google Scholar
  56. Hennigar SR, McClung JP, Pasiakos SM (2017) Nutritional interventions and the IL-6 response to exercise. FASEB J 31(9):3719–3728Google Scholar
  57. Hou Y, Zhang S, Wang L, Li J, Qu G, He J, Rong H, Ji H, Liu S (2012) Estrogen regulates iron homeostasis through governing hepatic hepcidin expression via an estrogen response element. Gene 511(2):398–403Google Scholar
  58. Houston BL, Hurrie D, Graham J, Perija B, Rimmer E, Rabbani R, Bernstein CN, Turgeon AF, Fergusson DA, Houston DS (2018) Efficacy of iron supplementation on fatigue and physical capacity in non-anaemic iron-deficient adults: a systematic review of randomised controlled trials. BMJ Open 8:e019240Google Scholar
  59. Impey SG, Hearris MA, Hammond KM, Bartlett JD, Louis J, Close GL, Morton JP (2018) Fuel for the work required: a theoretical framework for carbohydrate periodization and the glycogen threshold hypothesis. Sports Med 48(5):1031–1048Google Scholar
  60. Jacob A, Butler E, Blanche M (1965) Menstrual blood loss in iron deficiency anemia. Lancet 407:1102–1107Google Scholar
  61. Kapitsinou PP, Liu Q, Unger TL, Rha J, Davidoff O, Keith B, Epstein JA, Moores SL, Erickson-Miller CL, Haase VH (2010) Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood 116(16):3039–3048Google Scholar
  62. Kautz L, Jung G, Valore EV, Rivella S, Nemeth E, Ganz T (2014) Identification of erythroferrone as an erythroid regulator of iron metabolism. Nat Genet 46(7):678–687Google Scholar
  63. Koehler K, Braun H, Achtzehn S, Hildebrand U, Predel H-G, Mester J, Schänzer W (2012) Iron status in elite young athletes: gender-dependent influences of diet and exercise. Eur J Appl Physiol 112(2):513–523Google Scholar
  64. Koulaouzidis A, Said E, Cottier R, Saeed AA (2009) Soluble transferrin receptors and iron deficiency, a step beyond ferritin. A systematic review. J Gastrointestin Liver Dis 18(3):345–352Google Scholar
  65. Landahl G, Adolfsson P, Börjesson M, Mannheimer C, Rödjer S (2005) Iron deficiency and anemia: a common problem in female elite soccer players. Int J Sport Nutr Exerc Metab 15(6):689–694Google Scholar
  66. Larsson G, Milsom L, Lindstedt G, Rybo G (1992) The influence of a low-dose combined oral contraceptive on menstrual blood loss and iron status. Contraception 46(4):327–334Google Scholar
  67. Latour C, Kautz L, Besson-Fournier C, Island ML, Canonne-Hergaux F, Loréal O, Ganz T, Coppin H, Roth MP (2014) Testosterone perturbs systemic iron balance through activation of epidermal growth factor receptor signaling in the liver and repression of hepcidin. Hepatology 59(2):683–694Google Scholar
  68. Lehtihet M, Bonde Y, Beckman L, Berinder K, Hoybye C, Rudling M, Sloan JH, Konrad RJ, Angelin B (2016) Circulating hepcidin-25 is reduced by endogenous estrogen in humans. PLoS ONE 11(2):e0148802Google Scholar
  69. Leimberg MJ, Prus E, Konijn AM, Fibach E (2008) Macrophages function as a ferritin iron source for cultured human erythroid precursors. J Cell Biochem 103(4):1211–1218Google Scholar
  70. Li X, Rhee DK, Malhotra R, Mayeur C, Hurst LA, Ager E, Shelton G, Kramer Y, McCulloh D, Keefe D (2016) Progesterone receptor membrane component-1 regulates hepcidin biosynthesis. J Clin Investig 126(1):389–401Google Scholar
  71. Looker AC, Dallman PR, Carroll MD, Gunter EW, Johnson CL (1997) Prevalence of iron deficiency in the United States. JAMA 277(12):973–976Google Scholar
  72. Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Science 29(1):S7–S15Google Scholar
  73. Macdougall IC (2009) Evolution of iv iron compounds over the last century. J Renal Care 35:8–13Google Scholar
  74. Malczewska J, Szczepańska B, Stupnicki R, Sendecki W (2001) The assessment of frequency of iron deficiency in athletes from the transferrin receptor-ferritin index. Int J Sports Nutr Exer Metab 11(1):42–52Google Scholar
  75. McClung JP (2012) Iron status and the female athlete. J Trace Elem Med Biol 26(2–3):124–126Google Scholar
  76. McCormick R, Moretti D, McKay AKA, Laarakkers CM, van Swelm R, Trinder D, Cox GR, Zimmerman MB, Sim M, Goodman C, Dawson B, Peeling P (2019) The impact of morning versus afternoon exercise on iron absorption in athletes. Med Science Sport Exerc (Accepted and In-press) Google Scholar
  77. McKay AKA, Peeling P, Pyne DB, Welvaert M, Tee N, Leckey JJ, Sharma AP, Ross ML, Garvican-Lewis LA, Swinkels DW (2019a) Chronic adherence to a ketogenic diet modifies iron metabolism in elite athletes. Med Science Sports Exerc 51(3):548–555Google Scholar
  78. McKay AKA, Peeling P, Pyne DB, Welvaert M, Tee N, Leckey JJ, Sharma AP, Ross ML, Garvican-Lewis LA, van Swelm RP (2019b) Acute carbohydrate ingestion does not influence the post-exercise iron-regulatory response in elite keto-adapted race walkers. J Sci Med Sport.  https://doi.org/10.1016/j.jsams.2018.12.015 Google Scholar
  79. Moriyama Y, Fisher JW (1975) Effects of testosterone and erythropoietin on erythroid colony formation in human bone marrow cultures. Blood 45(5):665–670Google Scholar
  80. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R (2014) The IOC consensus statement: beyond the female athlete triad—relative energy deficiency in sport (RED-S). Br J Sports Med 48(7):491–497Google Scholar
  81. Mountjoy M, Sundgot-Borgen J, Burke L, Ackerman KE, Blauwet C, Constantini N, Lebrun C, Lundy B, Melin A, Meyer N (2018) International Olympic Committee (IOC) consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Int J sport Nutr Exerc Metab 28(4):316–331Google Scholar
  82. Myhre KE, Webber BJ, Cropper TL, Tchandja JN, Ahrendt DM, Dillon CA, Haas RW, Guy SL, Pawlak MT, Federinko SP (2016) Prevalence and impact of anemia on basic trainees in the US air force. Sports Med Open 2(1):23Google Scholar
  83. Newlin MK, Williams S, McNamara T, Tjalsma H, Swinkels DW, Haymes EM (2012) The effects of acute exercise bouts on hepcidin in women. Int J sport Nutr Exerc Metab 22(2):79–88Google Scholar
  84. Nielsen P, Nachtigall D (1998) Iron supplementation in athletes. Sports Med 26(4):207–216Google Scholar
  85. Parks RB, Hetzel SJ, Brooks MA (2017) Iron Deficiency and anemia among collegiate athletes: a retrospective chart review. Med Sci Sports Exerc 49(8) 1711–1715Google Scholar
  86. Pasricha SR, Flecknoe-Brown SC, Allen KJ, Gibson PR, McMahon LP, Olynyk JK, Roger SD, Savoia HF, Tampi R, Thomson AR, Wood EM, Robinson KL (2010) Diagnosis and management of iron deficiency anaemia: a clinical update. Med J Aust 193(9):525–532Google Scholar
  87. Patterson AJ, Brown WJ, Roberts DC (2001) Dietary and supplement treatment of iron deficiency results in improvements in general health and fatigue in Australian women of childbearing age. J Am Coll Nutr 20(4):337–342Google Scholar
  88. Peake J, Nosaka KK, Suzuki K (2005) Characterization of inflammatory responses to eccentric exercise in humans. Exer Immunol Rev 11:64–85Google Scholar
  89. Pedlar CR, Brugnara C, Bruinvels G, Burden R (2018) Iron balance and iron supplementation for the female athlete: a practical approach. Eur J Sport Sci 18(2):295–305Google Scholar
  90. Peeling P, Blee T, Goodman C, Dawson B, Claydon G, Beilby J, Prins A (2007) Effect of iron injections on aerobic-exercise performance of iron-depleted female athletes. Int J Sport Nutr Exerc Metab 17(3):221–231Google Scholar
  91. Peeling P, Dawson B, Goodman C, Landers G, Trinder D (2008) Athletic induced iron deficiency: new insights into the role of inflammation, cytokines and hormones. Eur J Appl Physiol 103(4):381Google Scholar
  92. Peeling P, Sim M, Badenhorst CE, Dawson B, Govus AD, Abbiss CR, Swinkels DW, Trinder D (2014) Iron status and the acute post-exercise hepcidin response in athletes. PLoS ONE 9(3):e93002Google Scholar
  93. Peeling P, McKay AK, Pyne DB, Guelfi KJ, McCormick RH, Laarakkers CM, Swinkels DW, Garvican-Lewis LA, Ross ML, Sharma AP (2017) Factors influencing the post-exercise hepcidin-25 response in elite athletes. Eur J Appl Physiol 117(6):1233–1239Google Scholar
  94. Petkus DL, Murray-Kolb LE, De Souza MJ (2017) The unexplored crossroads of the female athlete triad and iron deficiency: a narrative review. Sports Med 47(9):1721–1737Google Scholar
  95. Piperno A, Galimberti S, Mariani R, Pelucchi S, Ravasi G, Lombardi C, Bilo G, Revera M, Giuliano A, Faini A, Mainini V, Westerman M, Ganz T, Valsecchi MG, Mancia G, Parati G (2010) Modulation of hepcidin production during hypoxia-induced erythropoiesis in humans in vivo: data from the HIGHCARE project. Blood 117(10):2953–2959Google Scholar
  96. Powell PD, Tucker A (1991) Iron supplementation and running performance in female cross-country runners. Int J Sports Med 12(05):462–467Google Scholar
  97. Rampton D, Folkersen J, Fishbane S, Hedenus M, Howaldt S, Locatelli F, Patni S, Szebeni J, Weiss G (2014) Hypersensitivity reactions to intravenous iron: guidance for risk minimization and management. Haematologica 99(11):1671–1676Google Scholar
  98. Ravasi G, Pelucchi S, Buoli Comani G, Greni F, Mariani R, Pelloni I, Bombelli S, Perego R, Barisani D, Piperno A (2018) Hepcidin regulation in a mouse model of acute hypoxia. Eur J Haematol 100(6):636–643Google Scholar
  99. Reynafarje C, Lozano R, Valdivieso J (1959) The polycythemia of high altitudes: iron metabolism and related aspects. Blood 14(4):433–455Google Scholar
  100. Robson-Ansley P, Walshe I, Ward D (2011) The effect of carbohydrate ingestion on plasma interleukin-6, hepcidin and iron concentrations following prolonged exercise. Cytokine 53(2):196–200Google Scholar
  101. Rodriguez FA, Ventura JL, Casas M, Casas H, Pages T, Rama R, Ricart A, Palacios L, Viscor G (2000) Erythropoietin acute reaction and haematological adaptations to short, intermittent hypobaric hypoxia. Eur J Appl Physiol 82(3):170–177Google Scholar
  102. Roecker L, Meier-Buttermilch R, Brechtel L, Nemeth E, Ganz T (2005) Iron-regulatory protein hepcidin is increased in female athletes after a marathon. Eur J Appl Physiol 95(5–6):569–571Google Scholar
  103. Rowland T (2012) Iron deficiency in athletes: an update. Am J Lifestyle Med 6(4):319–327Google Scholar
  104. Rubeor A, Goojha C, Manning J, White J (2018) Does iron supplementation improve performance in iron-deficient nonanemic athletes? Sports Health 10(5):400–405Google Scholar
  105. Rushton DH, Dover R, Sainsbury AW, Norris MJ, Gilkes JJ, Ramsay ID (2001) Why should women have lower reference limits for haemoglobin and ferritin concentrations than men? BMJ 322(7298):1355–1357Google Scholar
  106. Ryan BJ, Wachsmuth NB, Schmidt W, Byrnes WC, Julian CG, Lovering AT, Subudhi AW, Roach RC (2014) AltitudeOmics: rapid hemoglobin mass alterations with early acclimatization to and de-acclimatization from 5260 m in healthy humans. PLoS ONE 9(10):e108788Google Scholar
  107. Santiago P (2012) Ferrous versus ferric oral iron formulations for the treatment of iron deficiency: a clinical overview. Sci World J 2012:846824Google Scholar
  108. Saunders AV, Craig WJ, Baines SK, Posen JS (2013) Iron and vegetarian diets. Med J Aust 199(4):11–16Google Scholar
  109. Schaap CC, Hendriks JC, Kortman GA, Klaver SM, Kroot JJ, Laarakkers CM, Wiegerinck ET, Tjalsma H, Janssen MC, Swinkels DW (2013) Diurnal rhythm rather than dietary iron mediates daily hepcidin variations. Clin Chem 59(3):527–535Google Scholar
  110. Schmidt W, Prommer N (2005) The optimised CO-rebreathing method: a new tool to determine total haemoglobin mass routinely. Eur J Appl Physiol 95(5–6):486–495Google Scholar
  111. Siebenmann C, Cathomen A, Hug M, Keiser S, Lundby AK, Hilty MP, Goetze JP, Rasmussen P, Lundby C (2015) Hemoglobin mass and intravascular volume kinetics during and after exposure to 3,454-m altitude. J Appl Physiol 119(10):1194–1201Google Scholar
  112. Sim M, Dawson B, Landers G, Wiegerinck ET, Swinkels DW, Townsend M-A, Trinder D, Peeling P (2012) The effects of carbohydrate ingestion during endurance running on post-exercise inflammation and hepcidin levels. Eur J Appl Physiol 112(5):1889–1898Google Scholar
  113. Sim M, Dawson B, Peeling P, Trinder D (2013) Encyclopedia of exercise medicine in health and disease. In: Mooren FC (ed) Sports anemia, 1st edn. Springer, New York.Google Scholar
  114. Sim M, Dawson B, Landers G, Trinder D, Peeling P (2014) Iron regulation in athletes: exploring the menstrual cycle and effects of different exercise modalities on hepcidin production. Int J Sport Nutr Exerc Metab 24(2):177–187Google Scholar
  115. Sim M, Dawson B, Landers G, Swinkels DW, Tjalsma H, Yeap BB, Trinder D, Peeling P (2015) Oral contraception does not alter typical post-exercise interleukin-6 and hepcidin levels in females. J Sci Med Sport 18(1):8–12Google Scholar
  116. Sim M, Dawson B, Landers G, Swinkels DW, Wiegerinck E, Yeap BB, Trinder D, Peeling P (2017) Interleukin-6 and hepcidin levels during hormone-deplete and hormone-replete phases of an oral contraceptive cycle: a pilot study. Ann Nutr Metab 70(2):100–105Google Scholar
  117. Sims ST, Heather AK (2018) Myths and methodologies: reducing scientific design ambiguity in studies comparing sexes and/or menstrual cycle phases. Exp Physiol 103(10):1309–1317Google Scholar
  118. Sinclair LM, Hinton PS (2005) Prevalence of iron deficiency with and without anemia in recreationally active men and women. J Am Diet Assoc 105(6):975–978Google Scholar
  119. Stirone C, Duckles SP, Krause DN, Procaccio V (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68(4):959–965Google Scholar
  120. Stoffel NU, Cercamondi CI, Brittenham G, Zeder C, Geurts-Moespot AJ, Swinkels DW, Moretti D, Zimmermann MB (2017) Iron absorption from oral iron supplements given on consecutive versus alternate days and as single morning doses versus twice-daily split dosing in iron-depleted women: two open-label, randomised controlled trials. Lancet Haematol 4(11):e524–e533Google Scholar
  121. Stray-Gundersen J, Alexander C, Hochstein A, deLemos D, Levine BD (1992) Failure of red cell volume to increase to altitude exposure in iron deficient runners. Med Sci Sports Exer 24(5):S90Google Scholar
  122. Tan D, Dawson B, Peeling P (2012) Hemolytic effects of a football-specific training session in elite female players. Int J Sports Physiol Perform 7(3):271–276Google Scholar
  123. Taylor NA (2011) Human heat adaptation. Compr Physiol 4(1):325–365Google Scholar
  124. Telford RD, Sly GJ, Hahn AG, Cunningham RB, Bryant C, Smith JA (2003) Footstrike is the major cause of hemolysis during running. J Appl Physiol 94(1):38–42Google Scholar
  125. Theodorou AA, Nikolaidis MG, Paschalis V, Sakellariou GK, Fatouros IG, Koutedakis Y, Jamurtas AZ (2010) Comparison between glucose-6-phosphate dehydrogenase-deficient and normal individuals after eccentric exercise. Med Sci Sport Exerc 42(6):1113–1121Google Scholar
  126. Thomas DT, Erdman KA, Burke LM (2016) Position of the academy of nutrition and dietetics, dietitians of canada, and the american college of sports medicine: nutrition and athletic performance. J Acad Nutr Diet 116(3):501–528Google Scholar
  127. Tolkien Z, Stecher L, Mander AP, Pereira DI, Powell JJ (2015) Ferrous sulfate supplementation causes significant gastrointestinal side-effects in adults: a systematic review and meta-analysis. PLoS ONE 10(2):e0117383Google Scholar
  128. Trumbo P, Yates AA, Schlicker S, Poos M (2001) Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J Am Diet Assoc 101(3):294–301Google Scholar
  129. Tsalis G, Nikolaidis MG, Mougios V (2004) Effects of iron intake through food or supplement on iron status and performance of healthy adolescent swimmers during a training season. Int J Sports Med 25(04):306–313Google Scholar
  130. United States Department of Agriculture. Agricultural Research Service. USDA Food Composition Databases. https://ndb.nal.usda.gov/ndb/nutrients/index. Accessed 30 Apr 2019
  131. Venderley AM, Campbell WW (2006) Vegetarian diets. Sports Med 36(4):293–305Google Scholar
  132. Voss S, Alsayrafi M, Bourdon P, Klodt F, Nonis D, Hopkins W, Schumacher Y (2014) Variability of serum markers of erythropoiesis during 6 days of racing in highly trained cyclists. Int J sports Med 35(02):89–94Google Scholar
  133. Warren MP, Perlroth NE (2001) The effects of intense exercise on the female reproductive system. J Endocrinol 170(1):3–11Google Scholar
  134. Woods A, Garvican-Lewis LA, Saunders PU, Lovell G, Hughes D, Fazakerley R, Anderson B, Gore CJ, Thompson KG (2014) Four weeks of IV iron supplementation reduces perceived fatigue and mood disturbance in distance runners. PLoS ONE 9(9):e108042Google Scholar
  135. Woodson RD, Wills RE, Lenfant C (1978) Effect of acute and established anemia on O2 transport at rest, submaximal and maximal work. J Appl Physiol Respir Environ Exerc Physiol 44(1):36–43Google Scholar
  136. Yang Q, Jian J, Katz S, Abramson SB, Huang X (2012) 17β-Estradiol inhibits iron hormone hepcidin through an estrogen responsive element half-site. Endocrinology 153(7):3170–3178Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Medical and Health SciencesEdith Cowan UniversityJoondalupAustralia
  2. 2.Medical School, Royal Perth Hospital UnitThe University Western AustraliaPerthAustralia
  3. 3.Australian Institute of SportCanberraAustralia
  4. 4.Mary MacKillop Institute for Health ResearchAustralian Catholic UniversityMelbourneAustralia
  5. 5.Faculty of Health Sciences and MedicineBond UniversityGold CoastAustralia
  6. 6.Department of Rehabilitation, Nutrition and Sport, School of Allied HealthLa Trobe UniversityMelbourneAustralia
  7. 7.School of Human Sciences (Exercise and Sport Science)The University of Western AustraliaCrawleyAustralia
  8. 8.The Western Australian Institute of SportMt ClaremontAustralia
  9. 9.Canadian Sport Institute-PacificVictoriaCanada
  10. 10.Department of Exercise Science, Physical and Health EducationUniversity of VictoriaVictoriaCanada

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