Interaction of antioxidants and their implication in genetic anemia

Proceedings of the Society for Experimental Biology and Medicine

Volumn 222, Issue 3, 1999, Pages 274-282

  Chan, Alvin C ^a   Chow, Ching K ^b   Chiu, Daniel ^c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF KENTUCKY   (United States)

^c CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; CAROTENOID; CATALASE; COPPER; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IRON; REACTIVE OXYGEN METABOLITE; RIBOFLAVIN; SELENIUM; SUPEROXIDE DISMUTASE; THIOCTIC ACID; UBIQUINONE DERIVATIVE; URIC ACID; ZINC;

ANEMIA; ANTIOXIDANT ACTIVITY; CELL DAMAGE; CELL RESPIRATION; CONFERENCE PAPER; GENETIC SUSCEPTIBILITY; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HEMOLYSIS; HUMAN; IRON OVERLOAD; OXIDATIVE STRESS; SICKLE CELL ANEMIA; THALASSEMIA;

EID: 0032726828     PISSN: 00379727     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1525-1373.1999.d01-144.x     Document Type: Conference Paper

References (121)

1. Gutteridge JM, Halliwell B. Antioxidants in Nutrition, Health, and Disease. New York: Oxford University Press, pp111-123, 1994.
2. Anonymous. Genetic disorders of glutathione and sulfur amino-acid metabolism: New biochemical insights and therapeutic approaches. Ann Int Med 93:330-346, 1980.
3. Meister A, Tate SS. Gultathione and related γ-glutamyl compounds. Ann Rev Biochem 45:559-604, 1979.
4. Folkers K. Relationship between coenzyme Q and vitamin E. Am J Clin Nutr 27:1026-1034, 1974.
5. Nohl H, Gille L, Staniek K. The biochemical, pathophysiological, and medical aspects of ubiquinone function. Ann N Y Acad Sci 854:394-409, 1998.
6. Stotanovsky DA, Osipov AN, Quinn PJ, Kagan VE. Ubiquinone-dependent recycling of vitamin E radicals by superoxide. Arch Biochem Biophys 323:343-351, 1995.
7. Kagan VE, Tyurina YY. Recycling and redox cycling of phenolic antioxidants. Ann N Y Acad Sci 854:425-134, 1998.
8. Chow CK. Nutritional influence on cellular antioxidant defense systems. Am J Clin Nutr 32:1066-1081, 1979.
9. Buttner GR. The pecking order of free radicals and antioxidants: Lipid peroxidation, α-tocopherol and ascorbate. Arch Biochem Biophys 300:535-543, 1993.
10. Tappel AL. Will antioxidant nutrients slow aging processes. Geriatrics 23:97-105, 1968.
11. Packer JE, Slater TF, Wilson RL. Direct observation of a free radical interaction between vitamin E and vitamin C. Nature 278:737-738, 1979.
12. Barclay LR, Locke SJ, MacNeil JM. The auto-oxidation of unsaturated lipids in micelles: Synergism of inhibitors vitamins C and E. Can J Chem 61:1288-1291, 1983.
13. Maguire JJ, Wilson DS, Packer L. Mitochondrial electron transport-linked tocopheroxyl radical reduction. J Biol Chem 264:21462-21465, 1989.
14. May JM, Qu ZC, Mendiratta S. Protection and recycling of α-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349:281-289, 1998.
15. McCay P. Vitamin E: Interaction with free radicals and ascorbate. Ann Rev Nutr 5:323-340, 1985.
16. Mehlhorn RJ, Sumida S, Packer. L. Tocopherol radical persistence and tocopherol consumption in liposomes and in vitamin E-enriched rat liver mitochondria and microsomes. J Biol Chem 264:13448-13452, 1989.
17. Niki E, Saito T, Kawakami A, Kamiya Y. Inhibition of oxidation of methyl linoleate in solution by vitamin E and vitamin C. J Biol Chem 259:4177-4182, 1984.
18. Scarpa M, Rigo A, Maiorino M, Ursini F, Gregolin C. Formation of α-tocopherol radical and recycling of α-tocopherol by ascorbate during peroxidation of phosphatidylcholine. Biochim Biophys Acta 801:215-219, 1984.
19. Stoyanovsky DA, Goldman R, Darrow RM, Organisciak DT, Kagan VE. Endogenous ascorbate regenerates vitamin E in the retina directly and in combination with exogenous dihydrolipoic acid. Curr Eye Res 14:181-189, 1995.
20. Waters RE, White LL, May JM. Liposomes containing α-tocopherol and ascorbate are protected from an external oxidant stress. Free Radic Res 26:373-379, 1997.
21. Chan AC, Tran K, Raynor C, Ganz PR, Chow CK. Regeneration of vitamin E in human platelets. J Biol Chem 266:17290-17295, 1991.
22. Bendich A, D'Apolito P, Gabriel E, Machlin LT. Interaction of dietary vitamin C and vitamin E on guinea pig immune responses to mitogens. J Nutr 114:1588-1593, 1984.
23. Igarachi O, Yonekawa K, Fujiyama-Fujihara Y. Synergistic action of vitamin E and vitamin C in vivo using a new mutant of Wister-strain rats, ODS, unable to synthesize vitamin C. J Nutr Sci Vitaminol 37:359-369, 1991.
24. Tanaka K, Hashimoto T, Tokumaru S, Iguchi H, Kojo S. Interactions between vitamin C and vitamin E are observed in tissues of inherently scorbutic rats. J Nutr 127:2060-2064, 1997.
25. Harme L, Waagbo R, Berge RK, Lie O. Vitamin C and E interact in juvenile Atlantic salmon. Free Radic Biol Med 22:137-149, 1997.
26. Jacob RA, Kutnink MA, Csallany AS, Daroszewska M, Burton GW. Vitamin C nutriture has little short-term effect on vitamin E concentrations in healthy women. J Nutr 126:2268-2277, 1996.
27. Podda M, Trischler HJ, Ulrich H, Packer L. α-Lipoic acid supplementation prevents symptoms of vitamin E deficiency. Biochem Biophys Res Commun 204:98-104, 1994.
28. Navarro F, Burgess NJ, Bello RI, De Cabo R, Arroyo A, Villalba JM. Vitamin E and selenium deficiency induces expression of the ubiquinone-dependent antioxidant system at the plasma membrane. FASEB J 12:1665-1673, 1998.
29. Diliberto EI, Dean G, Carter C, Allen PL. Tissue, subcellular and submitochondrial distribution of semidehydroascorbate reductase: Possible role of semidehydroascorbate reductase in cofactor regeneration. J Neurochem 39:563-568, 1982.
30. Green RC, O'Brien PJ. The involvement of semidehydroascorbate reductase in the oxidation of NADH by lipid peroxide in mitochondria and microsomes. Biochim Biophys Acta 293:334-342, 1973.
31. Schneider W, Staudinger HJ. Reduced nicotinamide adenine dinucleotide-dependent reduction of semidehydroascorbaic acid. Biochim Biophys Acta 96:157-159, 1965.
32. Washko PW, Rotrosen D, Levine M. Ascorbic acid transport and accumulation in human neutrophils. J Biol Chem 264:18996-19002, 1989.
33. Washko PW, Wang Y, Levine M. Ascorbic acid recycling in human neutrophils. J Biol Chem 268:15531-15535, 1993.
34. Rumsey SC, Kwon O, Xu GW, Burant CF, Simpson I, Levine M. Glucose transporter isoforms GLU1 and GLU3 transport dehydroascorbic acid. J Biol Chem 272:18982-18989, 1997.
35. Park JB, Levine M. Purification, cloning, and expression of dehydroascorbic acid reduction activity from human neutrophils: Identification as glutaredoxin. Biochem J 315:931-938, 1996.
36. Rumsey SC, Levine M. Absorption, transport, and disposition of ascorbic acid in humans. Nutr Biochem 9:116-130, 1998.
37. Misra HP. Generation of superoxide radical during the autoxidation of thiols. J Biol Chem 249:2151-2155, 1974.
38. Brownlee BR, Huttner JJ, Panganamala RV, Cornwell DG. Role of vitamin E in glutathione-induced oxidant stress: Methemoglobin, lipid peroxidation, and hemolysis. J Lipid Res 18:635-644, 1977.
39. Thomas SR, Neuzil J, Stocker R. Cosupplementation with coenyzme Q prevents the pro-oxidant effect of α-tocopherol and increases the resistance of LDL to transition metal-dependent oxidation initiation. Arterioscler Thromb Vasc Biol 16:687-696, 1996.
40. Nruzil J, Thomas SR, Stocker R. Requirement for promotion or inhibition by α-tocopherol of radical-induced initiation of plasma lipoprotein lipid peroxidation. Free Radic Biol Med 22:57-71, 1997.
41. Witting PK, Upston JM, Stocker R. Role of α-tocopheroxyl radical in the initiation of lipid peroxidation in human LDL exposed to horse radish peroxidase. Biochemistry 36:1251-1258, 1997.
42. Lovstad RA. Ascorbate and dehydroascorbate stimulation of copper-induced hemolysis: Protective action of ceruloplasmin, albumin, and apotransferrin. Int J Biochem 16:155-159, 1984.
43. Wang HP, Huang CJ, Chow CK. Red cell vitamin E and oxidative damage: A dual role of reducing agents. Free Radic Biol Med 24:291-298, 1994.
44. Weatherall DJ. Genetic disorders of haemoglobin. In: Hoffbrand AV, Lewis SM, Tuddenham, EGD, Eds. Postgraduate Haematology. Oxford, Boston: Butterworth and Heinemann, pp91-119, 1999.
45. Misra HP, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 247:6960-6962, 1972.
46. Carrell RW, Winterbourn CC, Rachmilewitz EA. Annotation: Activated oxygen and haemolysis. Br J Haematol 30:259-264, 1975.
47. Winterbourn CC, McGrath BM, Carrell RW. Reaction involving superoxide and normal and unstable haemoglobin. Biochem J 155:493-502, 1976.
48. MacDonald VW, Sharaches S. Differences in the reaction sequence associated with drug-induced oxidation of hemoglobin E, S, A, and F. J Lab Clin Med 102:762-772, 1982.
49. Hebbel RP, Morgan WT, Eaton JW, Hedlund BE. Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proc Natl Acad Sci U S A 85:237-241, 1988.
50. Chiu DTY, Van Den Berg J, Kuypers FA, Hung IJ, Wei JS, Liu TZ. Correction of membrane lipid peroxidation with oxidation of hemoglobin variants: Possibly related to the rates of heme release. Free Radic Biol Med 21:89-95, 1996.
51. Sheng K, Shariff M, Hebbel RP. Comparative oxidation of hemoglobin A and S. Blood 91:3467-3470, 1998.
52. Chiu D, Lubin B, Shohet SB. Erythrocyte membrane lipid organization during the sickling process. Br J Haematol 41:223-234, 1979.
53. Hebble RP, Eaton JW, Balasingam M, Steinberg MH. Spontaneous oxygen radical generation by sickle erythrocytes. J Clin Invest 70:1253-1261, 1982.
54. Schrier SL, Mohandas N. Globin-chain specificity of oxidation-induced changes in red blood cell membrane properties. Blood 79:1586-1592, 1992.
55. Shinar E, Rachmilewitz EA. Oxidation denaturation of red blood cells in thalassemia. Semin Hematol 27:70-91, 1990.
56. Hebbel RP, Leung A, Mohandas N. Oxidation-induced changes in microheological properties of the red cell membrane. Blood 76:1015-1022, 1990.
57. Yuan J, Bunyaratvej A, Fucharoen S, Fung C, Shinar E, Schrier SL. The instability of the membrane skeleton in thalassemic red blood cells. Blood 86:3945-3950, 1995.
58. Grinberg LN, Rachmilewitz EA, Kitrossky N, Chevion M. Hydroxyl radical generation in β-thalassemia red blood cells. Free Radic Biol Med 18:611-615, 1995.
59. Arese P, Deflora A. Pathophysiology of hemolysis in glucose-6-phosphate dehydrogenase deficiency. Semin Hematol 27:1-40, 1990.
60. Liu TZ, Lin TF, Hung IJ, Wei JS, Chiu DTY. Enhanced susceptibility of erythrocytes deficient in glucose-6-phosphate dehydrogenase to alloxan-, GSH-induced decrease in red cell deformability. Life Sci 55:PL55-60, 1994.
61. Pandolfi PP, Sonati F, Rivi R, Mason P, Grosveld F, Luzzatto L. Targeted disruption of the housekeeping gene encoding glucose-6-phosphate dehydrogenase: G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J 14:5209-5215, 1995.
62. Heyman MB, Vichinsky E, Katz R, Gaffield B, Hurst D, Castillo R, Chiu D, Kleman K, Ammann AJ, Thaler MM, Lubin B. Growth retardation in sickle-cell disease treated by nutritional support. Lancet 1:903-906, 1985.
63. Reed JD, Redding-Lallinger R, Orringer EP. Nutrition and sickle cell disease. Am J Hematol 24:441-155, 1987.
64. Williams R, George EO, Wang W. Nutrition assessment in children with sickle cell disease. J Assoc Acad Minor Phys 8:44-48, 1997.
65. Salman EK, Haymond MW, Bayne E, Sager BK, Wiisanen A, Pitel P, Darmaun D. Protein and energy metabolism in prepubertal children with sickle cell anemia. Pediatr Res 40:34-40, 1996.
66. Kopp-Hoolihan LE, van Loan MD, Menrzer WC, Heyman MB. Elevated resting energy expenditure in adolescents with sickle cell anemia. J Am Diet Assoc 99:195-199, 1999.
67. Moore C, Ehlayel M, Inostroza J, Leiva LE, Kuvibidila S, Yu L, Gardner R, Ode DL, Warrier R, Sorensen RU. Increased circulating levels of soluble HLA class-I heterodimers in patients with sickle cell anemia. J Natl Med Assoc 90:157-163, 1998.
68. Rachmilewitz EA, Shifter A, Kahane I. Vitamin E deficiency in β-thalassemia major: Changes in hematological and biochemical parameters after a therapeutic trial with α-tocopherol. Am J Clin Nutr 32:1850-1858, 1979.
69. Phillips G, Tangney CC. Relationship of plasma α-tocopherol to index of clinical severity in individuals with sickle cell anemia. Am J Hematol 41:227-231, 1992.
70. Bowie LJ, Carreathers SA, Wright AG. Lipid peroxidation, vitamin E, and the generation of irreversibly sickled cells in sickle cell anemia. Clin Chem 25:1076-1084, 1979.
71. Chiu D, Vichinsky E, Yee M, Kleman K, Lubin BH. Peroxidation, vitamin E, and sickle cell anemia. Ann N Y Acad Sci 82:323-335, 1982.
72. Leonard PJ, Losowsky MS. Effect of α-tocopherol administration on red cell survival in vitamin E-deficient subjects. Am J Clin Nutr 24:388-393, 1971.
73. Natta C, Machlin L, Brin M. A decrease in irreversibly sickled erythrocytes in sickle cell anemia patients given vitamin E. Am J Clin Nutr 33:968-971, 1980.
74. Hafez M, Amar ES, Zedan M, Hammad H, Sorour AH, el-Desouky ES, Gamil N. Improved erythrocyte survival with combined vitamin E and selenium therapy in children with glucose-6-phosphate dehydrogenase deficiency and mild chronic hemolysis. J Pediatr 108:558-561, 1986.
75. Corash L, Spielberg S, Bartsocas C, Boxer L, Steinherz R, Sheetz M, Egan M, Schlessleman J, Schulman JD. Reduced chronic hemolysis during high-dose vitamin E administration in Mediterranean-type glucose-6-phosphate dehydrogenase deficiency. New Engl J Med 303:416-420, 1980.
76. Horwitt MK, Harvey CC, Duncan GD, Wilson WC. Effects of limited tocopherol intake in man with relationships to erythrocyte hemolysis and lipid oxidations. Am J Clin Nutr 4:408-419, 1956.
77. Horwitt MK. Vitamin E and lipid metabolism in man. Am J Clin Nutr 8:451-461, 1960.
78. Farrell PM, Bieri JG, Fratantoni JF, Wood RE, di Sant'Agnese PA. The occurrence and effects of human vitamin E deficiency: A study in patients with cystic fibrosis. J Clin Invest 60:233-241, 1977.
79. Livrea MA, Tesoriere L, Pintaudi AM, Calabrese A, Maggio A, Freisleben HJ, D'Arpa D, D'Anna R, Bongiorno A. Oxidative stress and antioxidant status in β-thalassemia major: Iron overload and depletion of lipid-soluble antioxidants. Blood 88:3608-3614, 1996.
80. Lachant NA, Davidson WD, Tanaka KR. Impaired pentose phosphate shunt function in sickle cell disease: A potential mechanism for increased Heinz body formation and membrane lipid peroxidation. Am J Hematol 15:1-13, 1983.
81. Bozzi A, Parisi M, Strom R. Erythrocyte glutathione determination in the diagnosis of glucose-6-phosphate-dehydrogenase deficiency. Biochem Mol Biol Int 40:561-569, 1996.
82. + and NADPH in glucose-6-phosphate dehydrogenase-deficient erythrocytes under oxidative stimulation. Biochim Biophys Acta 430:395-398, 1976.
83. Jain SK. Glutathione and glucose-6-phosphate-dehydrogenase deficiency can increase protein glycation. Free Radic Biol Med 24:197-201, 1998.
84. Wetterstoem N, Brewer GJ, Warth JA, Mitchinson A, Near K. Relationship of glutathione levels and Heinz body formation to irreversibly sickle cells in sickle cell anemia. J Lab Clin Med 103:589-596, 1984.
85. Steinberg D. Low-density lipoprotein oxidation and its pathobiological significance. J Biol Chem 272:20963-20966, 1977.
86. Chan AC. Vitamin E and atherosclerosis. J Nutr 1128:1593-1596, 1998.
87. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D. Modification of LDL by endothelial cells involves lipid peroxidation and degradation of LDL phospholipids. Proc Natl Acad Sci U S A 81:3883-3887, 1984.
88. Dieber-Rotheneder M, Puhl H, Waeg G, Striegl G, Esterbauer H. Effect of oral supplementation with d-α-tocopherol on the vitamin E content of human LDL and resistance to oxidation. J Lipid Res 32:1325-1332, 1991.
89. Reaven PD, Khouw A, Beltz WF, Parthasarathy S, Witztum JL. Effect of dietary antioxidant combination in humans: Protection of LDL by vitamin E but not with β-carotene. Arterioscler Thromb Vasc Biol 13:590-600, 1993.
90. Jialal I, Fuller CJ, Huet BA. The effects of α-tocopherol supplementation on LDL oxidation: A dose-response study. Arterioscler Thromb Vasc Biol 15:190-198, 1995.
91. Hirano R, Kondo K, Iwamoto T, Igarashi O, Itakura H. Effects of antioxidants on the oxidative susceptibility of LDL. J Nutr Sci Vitaminol 43:435-444, 1997.
92. Martin A, Frei B. Both intracellular and extracellular vitamin C inhibit atherogenic modification of LDL by human vascular endothelial cells. Arterioscler Thromb Vasc Biol 17:1583-1590, 1997.
93. Retsky KL, Chen K, Zeind J, Frei B. Inhibition of copper-induced LDL oxidation by vitamin C is associated with decreased copper binding to LDL and 2-oxo-histidine formation. Free Radic Biol Med 26:90-98, 1999.
94. Tesoriere L, D'Arpa D, Maggio A, Giaccone E, Livrea MA. Oxidative resistance of LDL is correlated with vitamin E status in Italy. Atherosclerosis 137:429-435, 1998.
95. Livrea MA, Tesoriere L, Maggio A, D'Arpa D, Pintaudi AM, Pedone E. Oxidative modification of LDL and atherogenic risk in β-thalassemia. Blood 92:3936-3942, 1998.
96. Tangney CC, Philips G, Bell RA, Femandes P, Hopkin R, Wu SM. Selected indices of micronutrient status in adult patients with sickle cell anemia. Am J Hematol 32:161-166, 1989.
97. Natta C, Machlin L. Plasma levels of tocopherol in sickle cell anemia subjects. Am J Clin Nutr 32:1359-1362, 1979.
98. Chiu D, Lubin B. Abnormal vitamin E and glutathione peroxidase levels in sickle cell anemia: Evidence for increased susceptibility to lipid peroxidation in vivo. J Lab Clin Med 94:542-548, 1979.
99. Chiu DT-Y, Chang M-L. Blood vitamin C in human glucose-6-phosphate dehydrogenase deficiency. In: Packer L, Fuchs J, Eds. Vitamin C in Health and Disease. New York: Marcel Dekker Inc., pp323-331, 1997.
100. Rachmilewitz EA, Shohet SB, Rubin BH. Lipid membrane peroxidation in β-thalassemia major. Blood 47:495-505, 1976.
101. Rachmilewitz EA, Komberg A, Acker M. Vitamin E deficiency due to increased consumption in β-thalassemia and in Gaucher's disease. Ann N Y Acad Sci 393:336-347, 1982.
102. Zannos-Mariolea L, Yzortzatou F, Dendaki-Svolaki K, Katerellos C, Kavaliari M, Matsaniotis M. Serum vitamin E levels with β-thalassemia major: Preliminary report. Br J Haematol 26:193-199, 1974.
103. Zannos-Mariolea L, Papagregoriou-Theodoridou M, Costantzas N, Matsaniotis N. Relationship between tocopherols and serum lipid levels in children with β-thalassemia major. Am J Clin Nutr 31:259-262, 1978.
104. Giardini O, Cantani A, Donfrancesco A. Vitamin E therapy in homozygous β-thalassemia. New Engl J Med 305:644, 1981.
105. Giardini O, Cantani A, Donfrancesco A, Martino F, Mannarino O, D'Eufemia P, Miano C, Ruberto U, Lubrano R. Biochemical and clinical effects of vitamin E administration in homozygous β-thalassemia. Acta Vitaminol Enzymol 7:55-60, 1985.
106. Chantharaksri U, Tonsuwonnont W, Fucharoen S, Wasi P. Pathogenesis of hypoxemia. Southeast Asian J Trop Med Public Health 23(Suppl 2):32-35, 1992.
107. Suthutvoravut U, Hathirat P, Sirichakwal W, Tassaneeyakul A, Feungpean B. Vitamin E status, glutathione peroxidase activity, and the effect of vitamin E supplementation in children with thalassemia. J Med Asso Thailand 76(Suppl 2):146-152, 1993.
108. Kahane I, Rachmilewitz EA. Alterations in the red blood cell membrane and the effect of vitamin E on osmotic fragility in β-thalassemia major. Israel J Med Sci 12:11-15, 1976.
109. Miniero R, Canducci E, Ghigo D, Saracco P, Vullo C. Vitamin E in β-thalassemia. Acta Vitamin Enzymol 4:21-25, 1982.
110. Natta C, Chen LC, Chow CK. Selenium and glutathione peroxidase levels in sickle cell anemia. Acta Haematol 83:130-132, 1990.
111. Zimmerman CP, Natta C. Glutathione peroxidase activity in whole blood of patients with sickle cell amenia. Scand J Haematol 26:177-181, 1981.
112. Beutler E, Matsumoto F, Powars D, Warner J. Increased glutathione peroxidase activity in α-thalassemia. Blood 50:647-655, 1997.
113. Gerli GC, Beretta L, Bianchi M, Agostoni A, Gualadri V, Orsini GB. Erythrocyte superoxide dismutase, catalase, and glutathione peroxidase in glucose-6-phosphate-dehydrogenase deficiency. Scand J Haematol 29:135-140, 1982.
114. Jain SK, Willaims DW. Reduced levels of plasma ascorbate in sickle cell patients: Its possible role in oxidative damage to sickle cells in vivo. Clin Chim Acta 149:257-264, 1985.
115. Chiu D, Vichinsky E, Ho SL, Liu T, Lubin BH. Vitamin C deficiency in patients with sickle cell anemia. Am J Pediatr Hematol-Oncol 12:262-267, 1990.
116. Michelson J, Cohen A. Incidence and treatment of fractures in thalassemia. J Orthop Trauma 2:29-32, 1988.
117. Natta C, Stacewiecz-Sapuntakis M, Bhagavan H, Bowen P. Low serum levels of carotenoids in sickle cell anemia. Eur J Haematol 41:131-135, 1988.
118. Magnani M, Stocchi V, Canestrari F, Cucchiarini L, Stocchi O, Coppa GV, Felici L, Giorgi PL, Fornaini G. Redox and energetic state of red blood cells in G6PD deficiency, heterozygous β-thalassemia and the combination of both. Acta Haematol 75:211-214, 1986.
119. Johnson RM, Ravindranath Y, el-Alfy M, Goyette G. Oxidative damage to erythrocyte membrane in glucose-6-phosphate-dehydrogenase deficiency: Correlation with in vivo reduced glutathione concentration and membrane protein oxidation. Blood 83:1117-1123, 1994.
120. Kajanachumpol S, Tatu T, Sasanakul W, Chuansumrit A, Hathirat P. Zinc and copper status of thalassemic children. Southeast Asian J Trop Med Public Health 28:877-880, 1997.
121. Chan AC. Partners in defense: Vitamin C and vitamin E. Can J Physiol Pharmacol 71:725-731, 1993.