Sports Medicine

, Volume 19, Issue 1, pp 9–31 | Cite as

Exercise, Training and Red Blood Cell Turnover

  • John A. Smith
Review Article

Summary

Endurance training can lead to what has been termed ‘sports anaemia’. Although under normal conditions, red blood cells (RBCs) have a lifespan of about 120 days, the rate of aging may increase during intensive training. However, RBC deficiency is rare in athletes, and sports anaemia is probably due to an expanded plasma volume. Cycling, running and swimming have been shown to cause RBC damage.

While most investigators measure indices of haemolysis (for example, plasma haemoglobin or haptoglobin), RBC removal is normally an extravascular process that does not involve haemolysis. Attention is now turning to cellular indices (such as antioxidant depletion, or protein or lipid damage) that may be more indicative of exercise-induced damage.

RBCs are vulnerable to oxidative damage because of their continuous exposure to oxygen and their high concentrations of polyunsaturated fatty acids and haem iron. As oxidative stress may be proportional to oxygen uptake, it is not surprising that antioxidants in muscle, liver and RBCs can be depleted during exercise. Oxidative damage to RBCs can also perturb ionic homeostasis and facilitate cellular dehydration. These changes impair RBC deformability which can, in turn, impede the passage of RBCs through the microcirculation. This may lead to hypoxia in working muscle during single episodes of exercise and possibly an increased rate of RBC destruction with long term exercise. Providing RBC destruction does not exceed the rate of RBC production, no detrimental effect to athletic performance should occur. An increased rate of RBC turnover may be advantageous because young cells are more efficient in transporting oxygen.

Because most techniques examine the RBC population as a whole, more sophisticated methods which analyse cells individually are required to determine the mechanisms involved in exercise-induced damage of RBCs.

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References

  1. 1.
    Szygula Z. Erythrocytic system under the influence of physical exercise and training. Sports Med 1990; 10: 181–97PubMedCrossRefGoogle Scholar
  2. 2.
    Weight LM. Sports anaemia: does it exist? Sports Med 1993; 16: 1–4PubMedCrossRefGoogle Scholar
  3. 3.
    Magnusson B, Hallberg L, Rossander L, et al. Iron metabolism and sports anaemia. Acta Med Scand 1984; 216: 157–64PubMedCrossRefGoogle Scholar
  4. 4.
    Hebbel RP, Eaton JW. Pathobiology of heme interaction with the erythrocyte membrane. Sem Hematol 1989; 26: 136–49Google Scholar
  5. 5.
    Mairbaurl H. Red blood cell function in hypoxia at altitude and exercise. Int J Sports Med 1994; 15: 51–63PubMedCrossRefGoogle Scholar
  6. 6.
    Besa EC. Hematologic effects of androgens revisited: an alternative therapy in various hematologic conditions. Sem Hematol 1994; 31: 134–45Google Scholar
  7. 7.
    Telford RD, Cunningham RB. Sex, sport, and body-size dependency of hematology in highly-trained athletes. Med Sci Sports Exerc 1991;23:788–94PubMedGoogle Scholar
  8. 8.
    Elgsaeter A, Mikkelsen A. Shapes and shape changes in vitro in normal red blood cells. Biochim Biophys Acta 1991; 1071: 273–90PubMedCrossRefGoogle Scholar
  9. 9.
    Waugh RE, Mohandas N, Jackson CW, et al. Rheologie properties of senescent erythrocytes: loss of surface area and volume with age. Blood 1992; 79: 1351–8PubMedGoogle Scholar
  10. 10.
    Aminoff D. The role of sialoglycoconjugates in the aging and sequestration of red cells from circulation. Blood Cells 1988; 14: 229–47PubMedGoogle Scholar
  11. 11.
    Piomelli S. Commentary to: the relationship of red cell enzymes to red cell life-span by E. Beutler. Blood Cells 1988; 14: 81–6Google Scholar
  12. 12.
    Mohandas N, Phillips WM, Bessis M. Red blood cell deformability and haemolytic anemias. Sem Hematol 1979; 16: 95–114Google Scholar
  13. 13.
    Clark MR. Senescence of red blood cells: problems and progress. Physiol Rev 1988; 68: 503–53PubMedGoogle Scholar
  14. 14.
    Kosower NS. Altered properties of erythrocytes in the aged. Am J Hematol 1993; 42: 241–7PubMedCrossRefGoogle Scholar
  15. 15.
    Beutler E. Isolation of the aged. Blood Cells 1988; 14: 1–5PubMedGoogle Scholar
  16. 16.
    Beutler E. The relationship of red cell enzymes to red cell life-span. Blood Cells 1988; 14: 69–75PubMedGoogle Scholar
  17. 17.
    Dale GL, Norenberg SL. Density fractionation of erythrocytes by percol/hypaque results in only a slight enrichment for aged cells. Biochim Biophys Acta 1990; 1036: 183–7PubMedCrossRefGoogle Scholar
  18. 18.
    Mueller TJ, Jackson CW, Dockter ME, et al. Membrane skeletal alterations during in vivo mouse red cell aging: increase in the band 4.1a: 4.1b ratio. J Clin Invest 1987; 79: 492–9PubMedCrossRefGoogle Scholar
  19. 19.
    Fortier N, Snyder LM, Garver F, et al. The relationship between in vivo generated hemoglobin skeleton protein complex and increased red cell membrane rigidity. Blood 1988; 71: 1427–31PubMedGoogle Scholar
  20. 20.
    Shiga T, Sekiy M, Maeda N, et al. Cell age-dependent changes in deformability and calcium accumulation of human erythrocytes. Biochim Biophys Acta 1985; 814: 289–99PubMedCrossRefGoogle Scholar
  21. 21.
    Beppu M, Mizukami A, Nagoya M, et al. Binding of anti-band 3 autoantibody to oxidatively-damaged erythrocytes. J Biol Chem 1990; 265:3226–33PubMedGoogle Scholar
  22. 22.
    Kay MMB, Bosman GJCGM, Johnson GJ, et al. Band-3 polymers and aggregates, and hemoglobin precipitates in red cell aging. Blood Cells 1988; 14: 275–89PubMedGoogle Scholar
  23. 23.
    Corbett JD, Golan DE. Band 3 and glycophorin are progressively aggregated in density-fractionated sickle and normal red blood cells. J Clin Invest 1993; 91: 208–17PubMedCrossRefGoogle Scholar
  24. 24.
    Fishelson Z, Marikovsky Y. Reduced CRl expression on aged erythrocytes: immunoelectron microscopic and functional analysis. Mech Ageing Dev 1993; 72: 25–35PubMedCrossRefGoogle Scholar
  25. 25.
    Lutz HU, Fasler S, Stammler P, et al. Naturally occurring anti-band 3 autoantibodies and complement in phagocytosis of oxidatively-stressed and in clearance of senescent red cells. Blood Cells 1988; 14: 175–95PubMedGoogle Scholar
  26. 26.
    Vlassara H, Valinsky J, Brownlea M, et al. Advanced glycosylation endproducts on erythrocyte cell surface induce receptor-mediated phagocytosis by macrophages: a model for turnover of aging cells. J Exp Med 1987; 166: 539–49PubMedCrossRefGoogle Scholar
  27. 27.
    Chiu D, Lubin B. Oxidative hemoglobin denaturation and RBC destruction: the effect of heme on red cell membranes. Sem Hematol 1989; 26: 128–35Google Scholar
  28. 28.
    Danon D, Marikovsky Y. The aging of the red blood cell: a multifactor process. Blood Cells 1988; 14: 7–15PubMedGoogle Scholar
  29. 29.
    Nobes PR, Carter AB. Reticulocyte counting using flow cytometry. J Clin Pathol 1990; 43: 675–8PubMedCrossRefGoogle Scholar
  30. 30.
    Jennings LK, Brown LK, Dockter ME. Quantitation of protein 3 content of circulating erythrocytes at the single cell level. Blood 1985; 65: 1256–62PubMedGoogle Scholar
  31. 31.
    Rolfes-Curl A, Ogden LL, Omann GM, et al. Flow cytometric analysis of human erythrocytes, II: possible identification of senescent RBC with fluorescently labelled wheat-germ agglutinin. Exp Gerontol 1991; 26: 327–45PubMedCrossRefGoogle Scholar
  32. 32.
    Newhouse IJ, Clement DB. Iron status in athletes: an update. Sports Med 1988; 5: 337–52PubMedCrossRefGoogle Scholar
  33. 33.
    Selby GB, Eichner ER. Hematocrit and performance: the effect of endurance training on blood volume. Sem Hematol 1994; 31: 122–7Google Scholar
  34. 34.
    Cook JD. The effect of endurance training on iron metabolism. Sem Hematol 1994; 31: 146–54Google Scholar
  35. 35.
    O’Toole ML, Hiller WDB, Roalstad MS, et al. Hemolysis during triathlon races: its relation to race distance. Med Sci Sports Exerc 1988; 20: 272–5PubMedCrossRefGoogle Scholar
  36. 36.
    Green HJ, Sutton JR, Coates G, et al. Response of red cell and plasma volume to prolonged training in humans. J Appl Physiol 1991; 70: 1810–5PubMedGoogle Scholar
  37. 37.
    Schmidt W, Maassen N, Trost F, et al. Training-induced effects on blood volume, erythrocyte turnover, and haemoglobin oxygen-binding properties. Eur J Appl Physiol 1988; 57: 490–8CrossRefGoogle Scholar
  38. 38.
    Smith EM, Hill RL, Lehman IR, et al. Principles of biochemistry: mammalian biochemistry. 7th ed. Auckland: McGraw-Hill, 1983Google Scholar
  39. 39.
    Huebers HA, Finch CA. The physiology of transferrin and transferrin receptors. Physiol Rev 1987; 67: 520–82PubMedGoogle Scholar
  40. 40.
    Dallman PR. Biochemical basis for the manifestations of iron deficiency. Annu Rev Nutr 1993; 6: 13–40CrossRefGoogle Scholar
  41. 41.
    Schacter B. Heme catabolism by heme oxygenase: physiology, regulation and mechanism of action. Seinm Hematol 1989; 25: 349–69Google Scholar
  42. 42.
    Diess A. Iron metabolism in reticuloendothelial cells. Semin Hematol 1983; 20: 81–90Google Scholar
  43. 43.
    Miller BJ, Pate RR, Burgess W. Foot impact force and intravascular hemolysis during distance running. Int J Sports Med 1988; 9: 56–60PubMedCrossRefGoogle Scholar
  44. 44.
    Casoni I, Borsetto C, Cavicchi A, et al. Reduced hemoglobin concentration and red cell hemoglobinization in Italian marathon and ultramarathon runners. Int J Sports Med 1985; 6: 176–9PubMedCrossRefGoogle Scholar
  45. 45.
    Lijnen P, Hespel P, Fagard R, et al. Indicators of cell breakdown in plasma during and after a marathon race. Int J Sports Med 1988; 9: 108–13PubMedCrossRefGoogle Scholar
  46. 46.
    Wolf PL, Lott JA, Nitti GJ, et al. Changes in serum enzymes, lactate, and haptoglobin following acute physical stress in international-class athletes. Clin Biochem 1987; 20: 73–7PubMedCrossRefGoogle Scholar
  47. 47.
    Witte DL. Can serum ferritin be effectively interpreted in the presence of the acute-phase response? Clin Chem 1991; 37: 484–5PubMedGoogle Scholar
  48. 48.
    Seiler D, Nagel D, Franz H, et al. Effects of long-distance running on iron metabolism and hematological parameters. Int J Sports Med 1989; 10: 357–62PubMedCrossRefGoogle Scholar
  49. 49.
    Kanaley JA, Ji LL. Antioxidant enzyme activity during prolonged exercise in amenorrheic and eumenorrheic athletes. Metabolism 1991; 40: 88–92PubMedCrossRefGoogle Scholar
  50. 50.
    Cook JD, Skikne BS, Baynes RD. Serum tranferrin receptor. Annu Rev Med 1993; 44: 63–74PubMedCrossRefGoogle Scholar
  51. 51.
    Selby GB, Eichner ER. Endurance swimming, intravascular hemolysis, anemia, and iron depletion: new perspective on athletes anemia. Am J Med 1986; 81: 791–4PubMedCrossRefGoogle Scholar
  52. 52.
    Schobersberger W, Tschann M, Hasibeder W, et al. Consequences of 6 weeks strength training on red cell O2 transport and iron status. Eur J Appl Physiol 1990; 60: 163–8CrossRefGoogle Scholar
  53. 53.
    Dufaux B, Hoederath A, Streitberger I, et al. Serum ferritin, transferrin, haptoglobin, and iron in middle- and long-distance runners, elite rowers, and professional racing cyclists. Int J Sports Med 1981; 2: 43–6PubMedCrossRefGoogle Scholar
  54. 54.
    Pelliccia A, Di Nucci GB. Anemia in swimmers: fact or fiction? Study of hematologic and iron status in male and female top-level swimmers. Int J Sports Med 1987; 8: 227–30PubMedCrossRefGoogle Scholar
  55. 55.
    Berglund B, Birgegard G, Hemmingsson P. Serum erythropoietin in cross-country skiers. Med Sci Sports Exerc 1988; 20: 208–9PubMedCrossRefGoogle Scholar
  56. 56.
    Klausen T, Dela F, Hippe E, et al. Diurnal variations of serum erythropoietin in trained and untrained subjects. Eur J Appl Physiol 1993; 67: 545–8CrossRefGoogle Scholar
  57. 57.
    Klausen T, Mohr T, Ghisler U, et al. Maximal oxygen uptake and erythropoietic responses after training at moderate altitude. Eur J Appl Physiol 1991; 62: 376–9CrossRefGoogle Scholar
  58. 58.
    Weight LM, Byrne MJ, Jacobs P. Haemolytic effects of exercise. Clin Sci 1991; 81: 147–52PubMedGoogle Scholar
  59. 59.
    Landaw SA. Factors that accelerate or retard red blood cell senescence. Blood Cells 1988; 14: 47–67PubMedGoogle Scholar
  60. 60.
    Dacie JV, Lewis SM. Practical haematology. Edinburgh: Churchill-Livingstone, 1984Google Scholar
  61. 61.
    Labbe RF, Rettmer RL. Zinc protoporphyrin: a product of iron-deficient erythropoiesis. Sem Hematol 1989; 26: 40–6Google Scholar
  62. 62.
    Buysse AM, Delanghe JR, De Buyzere ML, et al. Enzymatic erythrocyte creatine determinations as an index for cell age. Clin Chim Acta 1990; 187: 155–62PubMedCrossRefGoogle Scholar
  63. 63.
    Schmidt W, Maassen N, Tegtbur U, et al. Changes in plasma volume and red cell formation after a marathon competition. Eur J Appl Physiol 1989; 58: 453–8CrossRefGoogle Scholar
  64. 64.
    Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev 1994; 74: 139–62PubMedGoogle Scholar
  65. 65.
    Demopoulos HB, Santomier JP, Seligman ML, et al. Free radical pathology: rationale and toxicology of antioxidants and other supplements in sports medicine and exercise science. In: Katch FI, editor. Sport, health and nutrition, 1984 Olympic Scientific Congress Proceedings, vol 2. Champaign, Ill.: Human Kinetics, 1986: 139–89Google Scholar
  66. 66.
    Halliwell B, Gutteridge JMC, Cross CE. Free radicals, antioxidants, and human disease: where are we now ? J Lab Clin Med 1992; 119: 598–620PubMedGoogle Scholar
  67. 67.
    Maiorino M, Coassin M, Roveri A, et al. Microsomal lipid peroxidation: effect of vitamin-E and its functional interaction with phospholipid hydroperoxide glutathione peroxidase. Lipids 1989; 24: 721–6PubMedCrossRefGoogle Scholar
  68. 68.
    Halliwell B, Gutteridge JMC. Role of free radicals and catalytic metal ions in human disease. In: Packer L, Glazer AN, editors. Oxygen radicals in biological systems, part B. Methods Enzymol 1990; 186: 1–85PubMedCrossRefGoogle Scholar
  69. 69.
    Gutteridge JMC, Halliwell B. The measurement and mechanism of lipid peroxidation in biologic systems. Trends Biochem Sci 1990; 15: 129–35PubMedCrossRefGoogle Scholar
  70. 70.
    Davies KJA, Goldberg AL. Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms. J Biol Chem 1987; 262: 8220–6PubMedGoogle Scholar
  71. 71.
    Shechter Y, Burstein Y, Patchornik A. Selective oxidation of methionine residues in proteins. Biochemistry 1975; 14: 4497–503PubMedCrossRefGoogle Scholar
  72. 72.
    Baysal E, Sullivan SG, Stern A. Prooxidant and antioxidant effects of ascorbate on tBuOOH-induced erythrocyte membrane damage. Int J Biochem 1989; 21: 1109–13PubMedCrossRefGoogle Scholar
  73. 73.
    Dean RT, Gebicki J, Gieseg S, et al. Hypothesis: a damaging role in aging for reactive protein oxidation products. Mutat Res 1992; 275: 387–93PubMedCrossRefGoogle Scholar
  74. 74.
    Oliver CN, Ahn B, Moerman EJ, et al. Age-related changes in oxidized proteins. J Biol Chem 1987; 262: 5488–91PubMedGoogle Scholar
  75. 75.
    Gebicki S, Gebicki JM. Formation of peroxides in amino acids and proteins exposed to oxygen free radicals. Biochem J 1993; 289: 743–9PubMedGoogle Scholar
  76. 76.
    Krinsky NI. Mechanism of action of biological antioxidants. Proc Soc Exp Biol Med 1992; 200: 248–54PubMedGoogle Scholar
  77. 77.
    Frei B, Kim MC, Ames B. Ubiquinol-10 is an effective lipid-soluble antioxidant at physiological concentrations. Proc Natl Acad Sci USA 1990; 87: 4879–83PubMedCrossRefGoogle Scholar
  78. 78.
    Constantinescu A, Han D, Packer L. Vitamin E recycling in human erythrocyte membranes. J Biol Chem 1993; 268: 10906–13PubMedGoogle Scholar
  79. 79.
    Hebbel RP. Erythrocyte antioxidants and membrane vulnerability. J Lab Clin Med 1986; 107: 401–4PubMedGoogle Scholar
  80. 80.
    Packer L. Protective role of vitamin E in biological systems. Am J Clin Nutr 1991; 53: 1050S–5SPubMedGoogle Scholar
  81. 81.
    Goldfarb AH. Antioxidants: role of supplementation to prevent exercise-induced oxidative stress. Med Sci Sports Exerc 1993; 25: 232–6PubMedGoogle Scholar
  82. 82.
    Traber MG. Determinants of plasma vitamin E concentrations. Free Rad Biol Med 1994; 16: 229–39PubMedCrossRefGoogle Scholar
  83. 83.
    Meister A. Glutathione-ascorbic acid antioxidant systems in animals. J Biol Chem 1994; 269: 9397–400PubMedGoogle Scholar
  84. 84.
    Miester A. On the antioxidant effects of ascorbic acid and glutathione. Biochem Pharmacol 1992; 44: 1905–15CrossRefGoogle Scholar
  85. 85.
    Burton GW, Wronska U, Stone L, et al. Biokinetics of dietary RRR-α-tocopherol in the male guinea pig at three dietary levels of vitamin C and two levels of vitamin E. Evidence that vitamin C does not spare vitamin E in vivo. Lipids 1990; 25: 199–210PubMedCrossRefGoogle Scholar
  86. 86.
    Kretzschmar M, Müller D. Aging, training and exercise: a review of effects on plasma glutathione and lipid peroxides. Sports Med 1993; 15: 196–209PubMedCrossRefGoogle Scholar
  87. 87.
    Lu SC, Garcia-Ruiz C, Kuhlenkamp J, et al. Hormonal regulation of glutathione efflux. J Biol Chem 1990; 265: 16088–95PubMedGoogle Scholar
  88. 88.
    Sen CK, Rankinen T, Vaisanen S, Rauramaa R. Oxidative stress after human exercise: effect of N-acetylcysteine supplementation. J Appl Physiol 1994; 76: 2570–7PubMedGoogle Scholar
  89. 89.
    Mansouri A, Lurie AA. Methemoglobinemia. Am J Hematol 1993; 42: 7–12PubMedCrossRefGoogle Scholar
  90. 90.
    Winterbourn CC, Stern A. Human red cells scavenge extracellular hydrogen peroxide and inhibit formation of hypochlorous acid and hydroxyl radical. J Clin Invest 1987; 80: 1486–91PubMedCrossRefGoogle Scholar
  91. 91.
    Emlen W, Carl V, Burdick G. Mechanism of transfer of immune complexes from red blood cell CR 1 to monocytes. Clin Exp Immunol 1992; 89: 8–17PubMedCrossRefGoogle Scholar
  92. 92.
    Seppi C, Addolorata M, Minetti G, et al. Evidence for membrane oxidation during in vivo aging of human erythrocytes. Mech Ageing Dev 1991; 57: 247–58PubMedCrossRefGoogle Scholar
  93. 93.
    Moore RB, Hulgan TM, Green JW, et al. Increased susceptibility of the sickle cell membrane Ca2+ + Mg2+-ATPase to t-butylhydroperoxide. Protective effects of ascorbate and desferal. Blood 79: 1992; 1334–41PubMedGoogle Scholar
  94. 94.
    Pigeolet E, Remade J. Susceptibility of glutathione peroxidase to proteolysis after oxidative alteration by peroxides and hydroxyl radicals. Free Rad Biol Med 1991; 11: 191–5PubMedCrossRefGoogle Scholar
  95. 95.
    Jain SK. Hyperglycemia can cause membrane lipid peroxidation and osmotic fragility in human red blood cells. J Biol Chem 1989; 264: 21340–5PubMedGoogle Scholar
  96. 96.
    Birlouez-Aragon I. Scalbert-Menanteau P, Morawiec M, et al. Evidence for a relationship between protein glycation and red blood cell membrane fluidity. Biochem Biophys Res Commun 1990; 170: 1107–13PubMedCrossRefGoogle Scholar
  97. 97.
    Hebbel RP. Beyond hemoglobin polymerization: the red blood cell membrane and sickle disease pathophysiology. Blood 1991; 77: 214–37PubMedGoogle Scholar
  98. 98.
    Hebbel RP. Autoxidation and the sickle erythrocyte membrane: a possible model of iron decompartmentalization. In: Johnson JE, Walford R, Harmon D, et al., editors. Free radicals, aging and degenerative diseases. New York: Alan R. Liss, 1986: 395–424Google Scholar
  99. 99.
    Kuross SA, Rank BH, Hebbel RR Excess heme in sickle erythrocyte inside-out membranes: possible role of thiol oxidation. Blood 1988; 71: 876–82PubMedGoogle Scholar
  100. 100.
    Kuross SA, Hebbel RP. Nonheme iron in sickle erythrocyte membranes: association with phospholipids and potential role in lipid peroxidation. Blood 1988; 72: 1278–85PubMedGoogle Scholar
  101. 101.
    Kannon R, Labotka R, Low PS. Isolation and characterization of the hemichrome-stabilized membrane protein aggregates from sickle erythrocytes. J Biol Chem. 1988; 263: 13766–73Google Scholar
  102. 102.
    Lang CA, Naryshkin S, Schneider DL, et al. Low blood glutathione levels in healthy aging adults. J Lab Clin Med 1992; 120: 720–5PubMedGoogle Scholar
  103. 103.
    Johnson RM, Ravindranath Y, El-Alfy M, et al. Oxidant damage to erythrocyte membrane in glucose-6-phosphate dehydrogenase deficiency: correlation with in vivo reduced glutathione concentration and membrane protein oxidation. Blood 1994; 83: 1117–23PubMedGoogle Scholar
  104. 104.
    Chiu D, Lubin B, Shohet SB. Peroxidative reactions in red cell biology. Free Rad Biol 1982; 5; 115–60Google Scholar
  105. 105.
    Chiu D, Kuypers F, Lubin B. Lipid peroxidation in human red cells. Sem Hematol 1989; 26: 257–76Google Scholar
  106. 106.
    Johnston CS, Meyer CG, Srilakshmi JC. Vitamin C elevates red blood cell glutathione in healthy adults. Am J Clin Nutr 1993; 58: 103–5PubMedGoogle Scholar
  107. 107.
    Sacchetta P, Battista P, Santarone S, et al. Purification of human erythrocyte proteolytic enzyme responsible for degradation of oxidant-damaged hemoglobin: evidence for identifying as a member of the multicatalytic proteinase family. Biochim Biophys Acta 1990; 107: 337–43CrossRefGoogle Scholar
  108. 108.
    Davies KJA. Protein modification by oxidants and the role of proteolytic enzymes. Biochem Soc Trans 1993; 21: 346–53PubMedGoogle Scholar
  109. 109.
    Davies KJA, Goldberg AL. Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells. J Biol Chem 1987; 262: 8227–34PubMedGoogle Scholar
  110. 110.
    Joshi W, Leb L, Piotrowski J, et al. Increased sensitivity of isolated alpha subunits of normal human hemoglobin to oxidative damage and crosslinking with spectrin. J Lab Clin Med 1983; 102: 46–52PubMedGoogle Scholar
  111. 111.
    Jain SK. The neonatal erythrocyte and its oxidative susceptibility. Sem Hematol 1989; 26: 286–300Google Scholar
  112. 112.
    Witt E, Reznick A, Viguie CA, et al. Exercise, oxidative damage, and effects of antioxidant manipulation. J Nutr 1992; 122Suppl. 3: 766–73PubMedGoogle Scholar
  113. 113.
    Gohil K, Viguie C, Stanley WC, et al. Blood glutathione oxidation during human exercise. J Appl Physiol 1988; 64: 115–9PubMedGoogle Scholar
  114. 114.
    Viguie C, Frei B, Shigenaga MK, et al. Antioxidant status and indexes of oxidative stress during consecutive days of exercise. J Appl Physiol 1993; 75: 566–72PubMedGoogle Scholar
  115. 115.
    Duthie GG, Robertson JD, Maughan RJ, et al. Blood antioxidant status and erythrocyte lipid peroxidation following distance running. Arch Biochem Biophys 1990; 282: 78–83PubMedCrossRefGoogle Scholar
  116. 116.
    Kretzschmar M, Müller D, Hubscher J, et al. Influence of aging, training and acute physical exercise on plasma glutathione and lipid peroxides in man. Int J Sports Med 1991; 12: 218–22PubMedCrossRefGoogle Scholar
  117. 117.
    Ohno H, Sato Y, Yamashita K, et al. The effect of brief physical exercise on free radical scavenging enzyme systems in human red blood cells. Can J Physiol Pharmacol 1986; 64: 1263–5PubMedCrossRefGoogle Scholar
  118. 118.
    Ji LL, Katz A, Fu R, et al. Blood glutathione status during exercise: effect of carbohydrate supplementation. J Appl Physiol 1993; 74: 788–92PubMedGoogle Scholar
  119. 119.
    Schofield D, Mei G. Braganza JM. Some pitfalls in the measurement of blood glutathione. Clin Sci 1993; 85: 213–8PubMedGoogle Scholar
  120. 120.
    Garner M, Reglinski J, Smith WE, et al. Oxidation state of glutathione in the erythrocyte. Clin Sci 1992; 83: 637PubMedGoogle Scholar
  121. 121.
    Smith JA, Kolbuch-Braddon M, Gillam I, et al. Effect of oxidative and osmotic stress on red blood cells following submaximal exercise. Eur J Appl Physiol. In pressGoogle Scholar
  122. 122.
    Pincemail J, Deby C, Gamus G, et al. Tocopherol mobilization during intensive exercise. Eur J Appl Physiol 1988; 57: 189–91CrossRefGoogle Scholar
  123. 123.
    Sumikawa K, Mu Z, Inoue T, et al. Changes in erythrocyte membrane phospholipid composition induced by physical training and physical exercise. Eur J Appl Physiol 1993; 67: 132–7CrossRefGoogle Scholar
  124. 124.
    Gleeson M, Robertson JD, Maughan RJ. Influence of exercise on ascorbic acid status in man. Clin Sci 1987; 73: 501–5PubMedGoogle Scholar
  125. 125.
    Ohno H, Yahata Y, Sato Y, et al. Physical training and fasting erythrocyte activities of free radical scavenging enzyme activities in sedentary men. Eur J Appl Physiol 1988; 57: 173–6CrossRefGoogle Scholar
  126. 126.
    Evelo CTA, Palmen NGM, Artur Y, et al. Changes in blood glutathione concentrations, and in erythrocyte glutathione reductase and glutathione-S-transferase activity after running training and after participation in contests. Eur J Appl Physiol 1992; 64: 354–8CrossRefGoogle Scholar
  127. 127.
    Robertson JD, Maughan RJ, Duthie GG, et al. Increased blood antioxidant systems of runners in response to training load. Clin Sci 1991; 80: 611–8PubMedGoogle Scholar
  128. 128.
    Mena P, Maynar M, Gutierrez JM, et al. Erythrocyte free radical scavenger enzymes in bicycle professional racers: adaptation to training. Int J Sports Med 1991; 12: 563–6PubMedCrossRefGoogle Scholar
  129. 129.
    Gerli GC, Mongiat R, Sandri MT, et al. Antioxidant system and serum trace elements in α-thalassemia and haemoglobin lepore trait. Eur J Haematol 1987; 39: 23–7PubMedCrossRefGoogle Scholar
  130. 130.
    Novelli GP, Bracciotti G, Falsini S. Spin-trappers and vitamin-E prolong endurance to muscle fatigue in mice. Free Rad Biol Med 1990; 8: 9–13PubMedCrossRefGoogle Scholar
  131. 131.
    Novelli GP, Falsini S, Bracciotti G. Exogenous glutathione increases endurance to muscle effort in mice. Pharm Res 1991; 23: 149–55CrossRefGoogle Scholar
  132. 132.
    Simon-Schnass I, Korniszewski L.. The influence of vitamin-E on rheological parameters in high altitude mountaineers. Int J Vitam Nutr Res 1990; 60: 26–34PubMedGoogle Scholar
  133. 133.
    Glass GA, Gershon D. Decreased enzymic protection and increased sensitivity to oxidative damage in erythrocytes as a function of cell and donar aging. Biochem J 1984; 218: 531–7PubMedGoogle Scholar
  134. 134.
    Kark JA, Posey DM, Schumacher H, et al. Sickle-cell trait as a risk factor for sudden death in physical training. N Engl J Med 1987; 317: 781–7PubMedCrossRefGoogle Scholar
  135. 135.
    Gozal D, Thiriet P, Mbala E, et al. Effect of different modalities of exercise and recovery on exercise performance in subjects with sickle cell trait. Med Sci Sports Exerc 1992; 24: 1325–31PubMedGoogle Scholar
  136. 136.
    Konotey-Ahulu FID. The sickle cell diseases. Arch Intern Med 1974; 133: 611–9PubMedCrossRefGoogle Scholar
  137. 137.
    Das SK, Hinds JE, Hardy RE, et al. Effects of physical stress on peroxide scavengers and sickle cell trait erythrocytes. Free Rad Biol Med 1993; 14: 139–47PubMedCrossRefGoogle Scholar
  138. 138.
    Boucher JH, Lessin LS, McKeekin RR. Echinocytosis the cause of equine exertional diseases — a hypothesis. In: Boese A, editor. Dynamics of equine athletic performance. Lawrenceville, NJ: Veterinary Learning Systems, 1985: 97–112Google Scholar
  139. 139.
    Chien S. Red cell deformability and its relevance to blood flow. Annu Rev Physiol 1987; 49: 177–92PubMedCrossRefGoogle Scholar
  140. 140.
    Stuart J, Ellory JC. Rheological consequences of erythrocyte dehydration. Br J Haematol 1988; 69: 1–4PubMedCrossRefGoogle Scholar
  141. 141.
    Canham PB, Parkinson DR. The area and volume of single human erythrocytes during gradual osmotic swelling to hemolysis. Can J Physiol Pharmacol 1970; 48: 369–76PubMedCrossRefGoogle Scholar
  142. 142.
    Buono MJ, Faucher PE. Intraerythrocyte and plasma osmolality during graded exercise inn humans. J Appl Physiol 1985; 58: 1069–72PubMedGoogle Scholar
  143. 143.
    Van Beaumont W, Underkofler S, Van Beaumont S. Erythrocyte volume, plasma volume, and acid-base changes in exercise and heat dehydration. J Appl Physiol 1981; 50: 1255–62PubMedGoogle Scholar
  144. 144.
    Staubli M, Roessler B. The mean red cell volume in long distance runners. Eur J Appl Physiol 1986; 55: 49–53CrossRefGoogle Scholar
  145. 145.
    Van Beaumont W, Rochelle, RH. Erythrocyte volume stability with plasma osmolarity changes in exercising man. Proc Soc Exp Biol Med 1974; 145: 240–3PubMedGoogle Scholar
  146. 146.
    Bodemann HH, Irmer M, Schluter KJ, et al. Activation of sodium transport in human erythrocytes by β-adrenoceptor stimulation in vivo. Eur J Appl Physiol 1987; 56: 375–80CrossRefGoogle Scholar
  147. 147.
    Rasmussen H, Lake W, Allen JE. The effect of catecholamines and prostaglandins uponhuman and rat erythrocytes. Biochim Biophys Acta 1975; 411: 63–73PubMedCrossRefGoogle Scholar
  148. 148.
    Poole RC, Halestrap AP. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol 1993; 264: C761–C782PubMedGoogle Scholar
  149. 149.
    Usami S, Chien S, Gregersen MI. Viscometric behavior of young and aged erythrocytes. In: Hartlet HH, Copley AL, editors. Theoretical and clinical hemorheology. Berlin: Springer-Verlag, 1971: 266–70CrossRefGoogle Scholar
  150. 150.
    Brugnara C, Van Ha T, Tosteson DC. Acid pH induces formation of dense cells in sickle erythrocytes. Blood 1989; 74: 487–95PubMedGoogle Scholar
  151. 151.
    Fabry ME, Romero JR, Buchanan ID, et al. Rapid increase in red blood cell density driven by K:C1 cotransport in a subset of sickle cell anemia reticulocytes and discocytes. Blood 1991; 78: 217–25PubMedGoogle Scholar
  152. 152.
    Piatt OS, Lux SE, Nathan DC. Exercise-induced hemolysis in xerocytosis. J Clin Invest 1981; 68: 631–8CrossRefGoogle Scholar
  153. 153.
    Fischer TM, Meloni T, Pescarmona T, et al. Membrane cross bonding in red cells in favic crisis: a missing link in the mechanism of extravascular haemolysis. Br J Haematol 1985; 59: 159–69PubMedCrossRefGoogle Scholar
  154. 154.
    Snyder LM, Sauberman N, Condara H, et al. Red cell membrane response to hydrogen peroxide-sensitivity in hereditary xerocytosis and in other abnormal red cells. Br J Haematol 1981; 48: 435–44PubMedCrossRefGoogle Scholar
  155. 155.
    Jain SK, Ross JD, Levy GJ, et al. The accumulation of malonyldialdehyde, an end product of membrane lipid peroxidation, can cause potassium leak in normal and sickle red blood cells. Biochem Med Metabol Biol 1989; 42: 60–5CrossRefGoogle Scholar
  156. 156.
    Wilkerson JE, Gutin B, Horvath SM. Exercise-induced changes in blood, red cell, and plasma volumes in man. Med Sci Sports 1977; 9: 155–8PubMedCrossRefGoogle Scholar
  157. 157.
    Wade CE. Response, regulation, and actions of vasopressin during exercise: a review. Med Sci Sports Exerc 1984; 16: 506–11PubMedCrossRefGoogle Scholar
  158. 158.
    Hespel P, Lijnen P, Fiocchi R, et al. Cationic concentrations and transmembrane fluxes in erythrocytes of humans during exercise. J Appl Physiol 1986; 61: 37–43PubMedGoogle Scholar
  159. 159.
    Evans E, Mohandas N, Leung A. Static and dynamic rigidities of normal and sickle erythrocytes: major influence of cell hemoglobin concentration. J Clin Invest 1984; 73: 477–88PubMedCrossRefGoogle Scholar
  160. 160.
    Mairbaurl H, Humpeler E, Schwaberger G, et al. Training-dependent changes of red blood cell density and erythrocytic oxygen transport. J Appl Physiol 1983; 55: 1403–7PubMedGoogle Scholar
  161. 161.
    Robertson JD, Maughan RJ, Davidson RJL. Changes in red cell density and related indices in response to distance running. Eur J Appl Physiol 1988; 57: 264–9CrossRefGoogle Scholar
  162. 162.
    Nicak A, Bohus B. Influence of long-distance running on red blood cell stability. Sports Med Training Rehab 1993; 4: 249–56CrossRefGoogle Scholar
  163. 163.
    Beutler E, Kuhl W, West C. The osmotic fragility of erythrocytes after prolonged liquid storage and after reinfusion. Blood 1982; 59: 1141–7PubMedGoogle Scholar
  164. 164.
    Telford RD, Kolbuch-Braddon M, Weidemann MJ, et al. Red blood cell uptake of lactate during exercise alters their physical properties independently of pH [abstract]. Med Sci Sports Med 1994; 26Suppl. 1: A191Google Scholar
  165. 165.
    Shand BI. Changes in blood rheology induced by lactic acid. Proc Univ Otago Med Sch 1986; 64: 71–2Google Scholar
  166. 166.
    Brun JF, Fons C, Raynaud E., et al. Influence of circulating lactate on blood rheology during exercise in professional football players. Rev Port Haemorheol 1991; 5: 219–29Google Scholar
  167. 167.
    Van Beaumont W. Red cell volume with changes in plasma osmolarity during maximal exercise. J Appl Physiol 1973; 35: 47–50PubMedGoogle Scholar
  168. 168.
    Klug BP, Lessin LS, Radice P Rheological aspects of sickle cell disease. Arch Intern Med 1974; 133: 577–90PubMedCrossRefGoogle Scholar
  169. 169.
    Vallance P, Collier J, Moncada S. Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet 1989; 2: 997–1000PubMedCrossRefGoogle Scholar
  170. 170.
    Borch FH, Werre JM, Schipper L, et al. Determinants of red blood cell deformability in relation to cell age. Eur J Haematol 1994; 52: 35–41Google Scholar
  171. 171.
    Sutera SP, Gardner RA, Boylan CW, et al. Age-related changes in deformability of human erythrocytes. Blood 1985; 65: 275–82PubMedGoogle Scholar
  172. 172.
    Kamada T, Tokuda S, Aozaki S-I, et al. High levels of erythrocyte fluidity in sprinters and long-distance runners. J Appl Physiol 1993; 74: 354–8PubMedGoogle Scholar
  173. 173.
    Morse PD, Warth JA. Direct measurement of the internal viscosity of sickle erythrocytes as a function of cell density. Biochim Biophys Acta 1990; 1053: 49–55PubMedCrossRefGoogle Scholar
  174. 174.
    Nash GB, Meiselman HJ. Red cell and ghost viscoelasticity: effects of hemoglobin concentration and in vivo aging. Biophys J 1983; 43: 63–73PubMedCrossRefGoogle Scholar
  175. 175.
    Chassis JA, Schrier SL. Membrane deformability and the capacity for shape change in the erythrocyte. Blood 1989; 74: 2562–8Google Scholar
  176. 176.
    Jain SK, Ross JD, Levy GJ, et al. The effect of malo-nyldialdehyde on viscosity of normal and sickle red blood cells. Biochem Med Metabol Biol 1990; 44: 37–41CrossRefGoogle Scholar
  177. 177.
    Kon K, Maeda N, Suda T, et al. Protective effect of α-tocopherol on the morphological and rheological changes of rat red cells. Acta Haematol 1983; 69: 111–6PubMedCrossRefGoogle Scholar
  178. 178.
    Charm SE, Paz H, Kurland GE. Reduced plasma viscosity among joggers compared with non-joggers. Biorheology 1979; 16: 185–9PubMedGoogle Scholar
  179. 179.
    Ernst E, Schmid M, Matrai A. Intraindividual changes of hemorheological and other variables by regular exercise. J Sports Cardiol 1985; 2: 50–4Google Scholar
  180. 180.
    Silva JM. Blood rheological adaptation to physical exercise. Rev Port Haemorheol 1988; 2: 63–7Google Scholar
  181. 181.
    Telford RD, Kovacic JC, Skinner, SL, et al. Resting whole blood viscosity of elite rowers is related to performance. Eur J Appl Physiol 1994; 68: 470–6CrossRefGoogle Scholar
  182. 182.
    Weed RI. The importance of erythrocyte deformability. Am J Med 1970; 49: 147–50PubMedCrossRefGoogle Scholar
  183. 183.
    Reinhart WH, Chien S. Stomatocytic transformation of red blood cells after marathon running. Am J Hematol 1985; 19: 201–4PubMedCrossRefGoogle Scholar
  184. 184.
    Reinhart WH, Staubli, M, Straub PW. Impaired red cell filter-ability with preferential elimination of old red blood cells during a 100 km race. J Appl Physiol 1983; 54: 827–33PubMedGoogle Scholar
  185. 185.
    Costill DL, Fink WJ. Plasma volume changes following exercise and thermal dehydration. J Appl Physiol 1974; 37: 521–5PubMedGoogle Scholar
  186. 186.
    Vandewalle H, Lacombe C, Lelievre JC, et al. Blood viscosity after a 1-h submaximal exercise with and without drinking. Int J Sports Med 1988; 9: 104–7PubMedCrossRefGoogle Scholar
  187. 187.
    Guezennec CY, Nadaud JF, Satabin P, et al. Influence of polyunsaturated fatty acid diet on the hemorrheological response to physical exercise in hypoxia. Int J Sports Med 1989; 10: 286–91PubMedCrossRefGoogle Scholar
  188. 188.
    Ernst E, Saradeth T, Achhammer G. Blood cell rheology influence of exercise and omego-3 fatty acids. Clin Hemorheol 1990; 10: 157–63Google Scholar
  189. 189.
    Freund BJ, Shizuru EV, Hashiro GM, et al. Hormonal, electrolyte, and renal responses to exercise are intensity dependent. J Appl Physiol 1991; 70: 900–6PubMedGoogle Scholar
  190. 190.
    Zamir N, Tuvia S, Riven-Kreitman R, et al. Atrial natriuretic peptide: direct effects on human red blood cell dynamics. Biochem Biophys Res Commun 1992; 188: 1003–9PubMedCrossRefGoogle Scholar
  191. 191.
    Follenius M, Candas V, Bothorel B, et al. Effect of rehydration on atrial natriuretic peptide release during exercise in the heat. J Appl Physiol 1989; 66: 2516–21PubMedGoogle Scholar
  192. 192.
    Valensi P, Gaudey F, Parries J, et al. Glucagon and noradrenaline reduce erythrocyte deformability. Metabolism 1993; 42: 1169–72PubMedCrossRefGoogle Scholar

Copyright information

© Adis International Limited 1995

Authors and Affiliations

  • John A. Smith
    • 1
  1. 1.National Quality of Life Foundation, c/- Department of Physiology and Applied NutritionAustralian Institute of SportBelconnenAustralia

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