Advertisement

Toxicological Reviews

, Volume 23, Issue 3, pp 169–188 | Cite as

Oxidant Stress and Haemolysis of the Human Erythrocyte

  • Marco L. A. Sivilotti
Review Article

Abstract

The erythrocyte is a highly specialised cell with a limited metabolic repertoire. As an oxygen shuttle, it must continue to perform this essential task while exposed to a wide range of environments on each vascular circuit, and to a variety of xenobiotics across its lifetime. During this time, it must continuously ward off oxidant stress on the haeme iron, the globin chain and on other essential cellular molecules. Haemolysis, the acceleration of the normal turnover of senescent erythrocytes, follows severe and irreversible oxidant injury. A detailed understanding of the molecular mechanisms underlying oxidant injury and its reversal, and of the clinical and laboratory features of haemolysis is important to the medical toxicologist. This review will also briefly review glucose-6-phosphate deficiency, a common but heterogeneous range of enzyme-deficient states, which impairs the ability of the erythrocyte to respond to oxidant injury.

Keywords

Haemolytic Anaemia Primaquine Hereditary Spherocytosis Methaemoglobin Intravascular Haemolysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The author is grateful to Ms Mary Lee for artwork and Dr John H. Matthews for the peripheral blood smears. No sources of funding were used to assist in the preparation of this review. The author has no conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Dreyfus C. Chronic hemolytic jaundice: a historical study. Bull New Engl Med Cent 1942; 4: 122–8Google Scholar
  2. 2.
    Packman CH. The spherocytic haemolytic anaemias. Br J Haematol 2001; 112(4): 888–99PubMedCrossRefGoogle Scholar
  3. 3.
    Hunter W. Is pernicious anaemia a special disease? Practitioner 1888; 41: 81–103Google Scholar
  4. 4.
    Vanlair CF, Masius JB. De la microcythemie. Bull R Acad Med Belg 1871; 5: 515–613Google Scholar
  5. 5.
    Hayem G. Sur une variete particuliere d’ictere chronique. La Presse Medicale 1898; 6: 121–2Google Scholar
  6. 6.
    Widal F, Abrami P, Brule M. Pluralite d’origine des icteres hemolytiques (recherches cliniques et experimentales). Societe Medicale Des Hospitaux de Paris 1907; 24: 1354–67Google Scholar
  7. 7.
    Third, Fourth and Fifth reports of the committee for classification of the nomenclature of cells and diseases of the blood and bloodforming organs. Am J Clin Pathol 1950; 20: 562–79Google Scholar
  8. 8.
    Alving AS, Carson PE, Flanagan CL, et al. Enzymatic deficiency in primaquine-sensitive erythrocytes. Science 1956; 124(3220): 484–5PubMedGoogle Scholar
  9. 9.
    Piccinini G, Minetti G, Balduini C, et al. Oxidation state of glutathione and membrane proteins in human red cells of different age. Mech Ageing Dev 1995; 78(1): 15–26PubMedCrossRefGoogle Scholar
  10. 10.
    Marschner JP, Seidlitz T, Rietbrock N. Effect of 2,3-diphosphoglycerate on O2-dissociation kinetics of hemoglobin and glycosylated hemoglobin using the stopped flow technique and an improved in vitro method for hemoglobin glycosylation. Int J Clin Pharmacol Ther 1994; 32(3): 116–21PubMedGoogle Scholar
  11. 11.
    Palek J. Introduction: red blood cell membrane proteins, their genes and mutations. Semin Hematol 1993; 30(1): 1–3PubMedGoogle Scholar
  12. 12.
    Seppi C, Castellana MA, Minetti G, et al. Evidence for membrane protein oxidation during in vivo aging of human erythrocytes. Mech Ageing Dev 1991; 57(3): 247–58PubMedCrossRefGoogle Scholar
  13. 13.
    Schluter K, Drenckhahn D. Co-clustering of denatured hemoglobin with band 3: its role in binding of autoantibodies against band 3 to abnormal and aged erythrocytes. Proc Natl Acad Sci USA 1986; 83(16): 6137–41PubMedCrossRefGoogle Scholar
  14. 14.
    Gow AJ, Luchsinger BP, Pawloski JR, et al. The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci USA 1999; 96(16): 9027–32PubMedCrossRefGoogle Scholar
  15. 15.
    McMahon TJ, Moon RE, Luschinger BP, et al. Nitric oxide in the human respiratory cycle. Nat Med 2002; 8(7): 711–7PubMedGoogle Scholar
  16. 16.
    Reiter CD, Wang X, Tanus-Santos JE, et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med 2002; 8(12): 1383–9PubMedCrossRefGoogle Scholar
  17. 17.
    Mayhew TM, Mwamengele GL, Self TJ, et al. Stereological studies on red corpuscle size produce values different from those obtained using haematocritand model-based methods. Br J Haematol 1994; 86(2): 355–60PubMedCrossRefGoogle Scholar
  18. 18.
    Lenard JG. A note on the shape of the erythrocyte. Bull Math Biol 1974; 36(1): 55–8PubMedCrossRefGoogle Scholar
  19. 19.
    Bennett V. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. [published erratum appears in Physiol Rev 1991 Jan; 71 (1)]. Physiol Rev 1990; 70(4): 1029–65PubMedGoogle Scholar
  20. 20.
    Murphy JR. Erythrocyte metabolism: II. Glucose metabolism and pathways. J Lab Clin Med 1960; 55: 286–302PubMedGoogle Scholar
  21. 21.
    Bloom GE, Zarkowsky HS. Heterogeneity of the enzymatic defect in congenital methemoglobinemia. N Engl J Med 1969; 281(17): 919–22PubMedCrossRefGoogle Scholar
  22. 22.
    Canepa L, Ferraris AM, Miglino M, et al. Bound and unbound pyridine dinucleotides in normal and glucose-6-phosphate dehydrogenase-deficient erythrocytes. Biochim Biophys Acta 1991; 1074(1): 101–4PubMedCrossRefGoogle Scholar
  23. 23.
    Micheli V, Simmonds HA, Bari M, et al. HPLC determination of oxidized and reduced pyridine coenzymes in human erythrocytes. Clin Chim Acta 1993; 220(1): 1–17PubMedCrossRefGoogle Scholar
  24. 24.
    Kondo T, Dale GL, Beutler E. Studies on glutathione transport utilizing inside-out vesicles prepared from human erythrocytes. Biochim Biophys Acta 1981; 645(1): 132–6PubMedCrossRefGoogle Scholar
  25. 25.
    Srivastava SK, Beutler E. Oxidized glutathione levels in erythrocytes of glucose-6-phosphate-dehydrogenase-deficient subjects. Lancet 1968; II(7558): 23–4CrossRefGoogle Scholar
  26. 26.
    Schuster R, Holzhutter HG, Jacobasch G. Interrelations between glycolysis and the hexose monophosphate shunt in erythrocytes as studied on the basis of a mathematical model. Biosystems 1988; 22(1): 19–36PubMedCrossRefGoogle Scholar
  27. 27.
    Minnich V, Smith MB, Brauner MJ, et al. Glutathione biosynthesis in human erythrocytes: I. identification of the enzymes of glutathione synthesis in hemolysates. J Clin Invest 1971; 50(3): 507–13PubMedCrossRefGoogle Scholar
  28. 28.
    Srivastava SK, Beutler E. The transport of oxidized glutathione from human erythrocytes. J Biol Chem 1969; 244(1): 9–16PubMedGoogle Scholar
  29. 29.
    Telen MJ. Erythrocyte blood group antigens: polymorphisms of functionally important molecules. Semin Hematol 1996; 33(4): 302–14PubMedGoogle Scholar
  30. 30.
    Skandalakis PN, Colborn GL, Skandalakis LJ, et al. The surgical anatomy of the spleen. Surg Clin North Am 1993; 73(4): 747–68PubMedGoogle Scholar
  31. 31.
    Sass MD, Caruso CJ, Farhangi M. TPNH-methemoglobin reductase deficiency: a new red-cell enzyme defect. J Lab Clin Med 1967; 70(5): 760–7PubMedGoogle Scholar
  32. 32.
    Mansouri A. Methemoglobin reduction under near physiological conditions. Biochem Med Metab Biol 1989; 42(1): 43–51PubMedCrossRefGoogle Scholar
  33. 33.
    Coleman MD, Coleman NA. Drug-induced methaemoglobinaemia: treatment issues. Drug Saf 1996; 14(6): 394–405PubMedCrossRefGoogle Scholar
  34. 34.
    Bradberry SM. Occupational methaemoglobinaemia: mechanisms of production, features, diagnosis and management including the use of methylene blue. Toxicol Rev 2003; 22(1): 13–27PubMedCrossRefGoogle Scholar
  35. 35.
    Riccio A, Vitagliano L, di Prisco G, et al. The crystal structure of a tetrameric hemoglobin in a partial hemichrome state. Proc Natl Acad Sci USA 2002; 99(15): 9801–6PubMedCrossRefGoogle Scholar
  36. 36.
    Rifkind JM, Abugo O, Levy A, et al. Detection, formation, and relevance of hemichromes and hemochromes. Methods Enzymol 1994; 231: 449–80PubMedCrossRefGoogle Scholar
  37. 37.
    Rachmilewitz EA. Denaturation of the normal and abnormal hemoglobin molecule. Semin Hematol 1974; 11(4): 441–62PubMedGoogle Scholar
  38. 38.
    Berzofsky JA, Peisach J, Blumberg WE. Sulfheme proteins: I. Optical and magnetic properties of sulfmyoglobin and its derivatives. J Biol Chem 1971; 246(10): 3367–77PubMedGoogle Scholar
  39. 39.
    Berzofsky JA, Peisach J, Horecker BL. Sulfheme proteins: IV. The stoichiometry of sulfur incorporation and the isolation of sulfhemin, the prosthetic group of sulfmyoglobin. J Biol Chem 1972; 247(12): 3783–91PubMedGoogle Scholar
  40. 40.
    Morell DB, Chang Y. The structure of the chromophore of sulphmyoglobin. Biochim Biophys Acta 1967; 136(1): 121–30PubMedCrossRefGoogle Scholar
  41. 41.
    Chiu D, Lubin B. Oxidative hemoglobin denaturation and RBC destruction: the effect of heme on red cell membranes. Semin Hematol 1989; 26(2): 128–35PubMedGoogle Scholar
  42. 42.
    Cappellini MD, Tavazzi D, Duca L, et al. Metabolic indicators of oxidative stress correlate with haemichrome attachment to membrane, band 3 aggregation and erythrophagocytosis in beta-thalassaemia intermedia. Br J Haematol 1999; 104(3): 504–12PubMedCrossRefGoogle Scholar
  43. 43.
    Ideguchi H. Effects of abnormal Hb on red cell membranes [in Japanese]. Rinsho Byori 1999; 47(3): 232–7PubMedGoogle Scholar
  44. 44.
    Hebbel RP, Eaton JW. Pathobiology of heme interaction with the erythrocyte membrane. Semin Hematol 1989; 26(2): 136–49PubMedGoogle Scholar
  45. 45.
    McCormick DJ, Atassi MZ. Hemoglobin binding with haptoglobin: delineation of the haptoglobin binding site on the alpha-chain of human hemoglobin. J Protein Chem 1990; 9(6): 735–42PubMedCrossRefGoogle Scholar
  46. 46.
    Morgan WT, Muster P, Tatum F, et al. Identification of the histidine residues of hemopexin that coordinate with heme-iron and of a receptor-binding region. J Biol Chem 1993; 268(9): 6256–62PubMedGoogle Scholar
  47. 47.
    Smith A, Hunt RC. Hemopexin joins transferrin as representative members of a distinct class of receptor-mediated endocytic transport systems. Eur J Cell Biol 1990; 53(2): 234–45PubMedGoogle Scholar
  48. 48.
    Coburn RF, Williams WJ, Kahn SB. Endogenous carbon monoxide production in patients with hemolytic anemia. J Clin Invest 1966; 45(4): 460–8PubMedCrossRefGoogle Scholar
  49. 49.
    International Committee for Standardization in Haematology, Expert Panel on Haemoglobinometry. Recommendations for reference method for haemoglobinometry in human blood (ICSH standard 1986) and specifications for international haemiglobincyanide reference preparation. 3rd ed. Clin Lab Haematol 1987; 9(1): 73–9Google Scholar
  50. 50.
    National Committee for Clinical Laboratory Standards. Reference and selected procedures for the quantitative determination of hemoglobin in blood. 2nd ed. NCCLS H15-A2. Villanova (PA): NCCLS, 1994Google Scholar
  51. 51.
    Wilkinson SP, McHugh P, Horsley S, et al. Arsine toxicity aboard the Asiafreighter. BMJ 1975; 3(5983): 559–63PubMedCrossRefGoogle Scholar
  52. 52.
    McArthur JR, Hillman RS. Normal and abnormal peripheral blood cells. ASH slide bank. 3rd ed. Washington, DC: American Society of Hematology, 1990Google Scholar
  53. 53.
    Stevenson DK, Vreman HJ. Carbon monoxide and bilirubin production in neonates. Pediatrics 1997; 100 (2: Pt 1): 252–4PubMedCrossRefGoogle Scholar
  54. 54.
    Petz LD. Drug-induced autoimmune hemolytic anemia. Transfus Med Rev 1993; 7(4): 242–54PubMedCrossRefGoogle Scholar
  55. 55.
    Myint H, Copplestone JA, Orchard J, et al. Fludarabine-related autoimmune haemolytic anaemia in patients with chronic lymphocytic leukaemia. Br J Haematol 1995; 91(2): 341–4PubMedCrossRefGoogle Scholar
  56. 56.
    Robak T, Blasinska-Morawiec M, Krykowski E, et al. Autoimmune haemolytic anaemia in patients with chronic lymphocytic leukaemia treated with 2-chlorodeoxyadenosine (cladribine). Eur J Haematol 1997; 58(2): 109–13PubMedCrossRefGoogle Scholar
  57. 57.
    Bennett CL, Weinberg PD, Rozenberg-Ben-Dror K, et al. Thrombotic thrombocytopenic purpura associated with ticlopidine: a review of 60 cases. Ann Intern Med 1998; 128(7): 541–4PubMedGoogle Scholar
  58. 58.
    Tsai HM, Rice L, Sarode R, et al. Antibody inhibitors to von Willebrand factor metalloproteinase and increased binding of von Willebrand factor to platelets in ticlopidine-associated thrombotic thrombocytopenic purpura. Ann Intern Med 2000; 132(10): 794–9PubMedGoogle Scholar
  59. 59.
    Bennett CL, Connors JM, Carwile JM, et al. Thrombotic thrombocytopenic purpura associated with clopidogrel. N Engl J Med 2000; 342(24): 1773–7PubMedCrossRefGoogle Scholar
  60. 60.
    Atkinson K, Biggs JC, Hayes J, et al. Cyclosporin A associated nephrotoxicity in the first 100 days after allogeneic bone marrow transplantation: three distinct syndromes. Br J Haematol 1983; 54(1): 59–67PubMedCrossRefGoogle Scholar
  61. 61.
    Dzik WH, Georgi BA, Khettry U, et al. Cyclosporine-associated thrombotic thrombocytopenic purpura following liver transplantation: successful treatment with plasma exchange. Transplantation 1987; 44(4): 570–2PubMedCrossRefGoogle Scholar
  62. 62.
    Shitrit D, Starobin D, Aravot D, et al. Tacrolimus-induced hemolytic uremic syndrome case presentation in a lung transplant recipient. Transplant Proc 2003; 35(2): 627–8PubMedCrossRefGoogle Scholar
  63. 63.
    Mach-Pascual S, Samii K, Beris P. Microangiopathic hemolytic anemia complicating FK506 (tacrolimus) therapy. Am J Hematol 1996; 52(4): 310–2PubMedCrossRefGoogle Scholar
  64. 64.
    Holman MJ, Gonwa TA, Cooper B, et al. FK506-associated thrombotic thrombocytopenic purpura. Transplantation 1993; 55(1): 205–6PubMedCrossRefGoogle Scholar
  65. 65.
    Canpolat C, Pearson P, Jaffe N. Cisplatin-associated hemolytic uremic syndrome. Cancer 1994; 74(11): 3059–62PubMedCrossRefGoogle Scholar
  66. 66.
    Gardner G, Mesler D, Gitelman HJ. Hemolytic uremic syndrome following cisplatin, bleomycin, and vincristine chemotherapy: a report of a case and a review of the literature. Ren Fail 1989; 11(2-3): 133–7PubMedCrossRefGoogle Scholar
  67. 67.
    Murgo AJ. Thrombotic microangiopathy in the cancer patient including those induced by chemotherapeutic agents. Semin Hematol 1987; 24(3): 161–77PubMedGoogle Scholar
  68. 68.
    Necheles TF, Steinberg MH, Cameron D. Erythrocyte glutathione-peroxidase deficiency. Br J Haematol 1970; 19(5): 605–12PubMedCrossRefGoogle Scholar
  69. 69.
    Yoo D, Lessin LS. Drug-associated ‘bite cell’ hemolytic anemia. Am J Med 1992; 92(3): 243–8PubMedCrossRefGoogle Scholar
  70. 70.
    Lee E, Boorse R, Marcinczyk M. Methemoglobinemia secondary to benzocaine topical anesthetic. Surg Laparosc Endosc 1996; 6(6): 492–3PubMedCrossRefGoogle Scholar
  71. 71.
    Ferraro-Borgida MJ, Mulhern SA, DeMeo MO, et al. Methemoglobinemia from perineal application of an anesthetic cream. Ann Emerg Med 1996; 27(6): 785–8PubMedCrossRefGoogle Scholar
  72. 72.
    Cote MA, Lyonnais J, Leblond PF. Acute Heinz-body anemia due to severe cresol poisoning: successful treatment with erythrocytapheresis. CMAJ 1984; 130(10): 1319–22Google Scholar
  73. 73.
    Jollow DJ, Bradshaw TP, McMillan DC. Dapsone-induced hemolytic anemia. Drug Metab Rev 1995; 27(1–2): 107–24PubMedCrossRefGoogle Scholar
  74. 74.
    Spooren AA, Evelo CT. Hydroxylamine treatment increases glutathione-protein and protein-protein binding in human erythrocytes. Blood Cells Mol Dis 1997; 23(3): 323–36PubMedCrossRefGoogle Scholar
  75. 75.
    Sills MR, Zinkham WH. Methylene blue-induced Heinz body hemolytic anemia. Arch Pediatr Adolesc Med 1994; 148(3): 306–10PubMedCrossRefGoogle Scholar
  76. 76.
    Brandes JC, Bufill JA, Pisciotta AV. Amyl nitrite-induced hemolytic anemia. Am J Med 1989; 86(2): 252–4PubMedCrossRefGoogle Scholar
  77. 77.
    Bogart L, Bonsignore J, Carvalho A. Massive hemolysis following inhalation of volatile nitrites. Am J Hematol 1986; 22(3): 327–9PubMedCrossRefGoogle Scholar
  78. 78.
    Romeril KR, Concannon AJ. Heinz body haemolytic anaemia after sniffing volatile nitrites. Med J Aust 1981; 1(6): 302–3PubMedGoogle Scholar
  79. 79.
    Beaupre SR, Schiffman FJ. Rush hemolysis: a ‘bite-cell’ hemolytic anemia associated with volatile liquid nitrite use. Arch Fam Med 1994; 3(6): 545–8PubMedCrossRefGoogle Scholar
  80. 80.
    Todisco V, Lamour J, Finberg L. Hemolysis from exposure to naphthalene mothballs. N Engl J Med 1991; 325(23): 1660–1PubMedCrossRefGoogle Scholar
  81. 81.
    Larkin EC, Williams WT, Ulvedal F. Human hematologic reesponses to 4 hr of isobaric hyperoxic exposure (100 per cent oxygen at 760mm Hg). J Appl Physiol 1973; 34(4): 417–21PubMedGoogle Scholar
  82. 82.
    Mengel CE, Kann Jr HE, Heyman A, et al. Effects of in vivo hyperoxia on erythrocytes: II. Hemolysis in a human after exposure to oxygen under high pressure. Blood 1965; 25: 822–9PubMedGoogle Scholar
  83. 83.
    Millar J, Peloquin R, De Leeuw NK. Phenacetin-induced hemolytic anemia. CMAJ 1972; 106(7): 770–5Google Scholar
  84. 84.
    Nathan DM, Siegel AJ, Bunn HF. Acute methemoglobinemia and hemolytic anemia with phenazopyridine: possible relation to acute renal failure. Arch Intern Med 1977; 137(11): 1636–8PubMedCrossRefGoogle Scholar
  85. 85.
    Fincher ME, Campbell HT. Methemoglobinemia and hemolytic anemia after phenazopyridine hydrochloride (pyridium) administration in end-stage renal disease. South Med J 1989; 82(3): 372–4PubMedCrossRefGoogle Scholar
  86. 86.
    Maloisel F, Kurtz JE, Andres E, et al. Platin salts-induced hemolytic anemia: cisplatin- and the first case of carboplatin-induced hemolysis. Anticancer Drugs 1995; 6(2): 324–6PubMedCrossRefGoogle Scholar
  87. 87.
    Ward PC, Schwartz BS, White JG. Heinz-body anemia: ‘bite cell’ variant a light and electron microscopic study. Am J Hematol 1983; 15(2): 135–46PubMedCrossRefGoogle Scholar
  88. 88.
    Klimecki WT, Carter DE. Arsine toxicity: chemical and mechanistic implications. J Toxicol Environ Health 1995; 46(4): 399–409PubMedCrossRefGoogle Scholar
  89. 89.
    Kleinfeld MJ. Arsine poisoning. J Occup Med 1980; 22(12): 820–1PubMedCrossRefGoogle Scholar
  90. 90.
    Fowler BA, Weissberg JB. Arsine poisoning. N Engl J Med 1974; 291(22): 1171–4PubMedCrossRefGoogle Scholar
  91. 91.
    Jenkins GC, Ind JE, Kazantzis G, et al. Arsine poisoning: massive haemolysis with minimal impairment of renal function. BMJ 1965; 5453: 78–80CrossRefGoogle Scholar
  92. 92.
    Hatlelid KM, Brailsford C, Carter DE. Reactions of arsine with hemoglobin. J Toxicol Environ Health 1996; 47(2): 145–57PubMedCrossRefGoogle Scholar
  93. 93.
    Rael LT, Ayala-Fierro F, Carter DE. The effects of sulfur, thiol, and thiol inhibitor compounds on arsine-induced toxicity in the human erythrocyte membrane. Toxicol Sci 2000; 55(2): 468–77PubMedCrossRefGoogle Scholar
  94. 94.
    Chuttani HK, Gupta PS, Gulati S, et al. Acute copper sulfate poisoning. Am J Med 1965; 39(5): 849–54PubMedCrossRefGoogle Scholar
  95. 95.
    Fairbanks VF. Copper sulfate-induced hemolytic anemia: inhibition of glucose-6-phosphate dehydrogenase and other possible etiologic mechanisms. Arch Intern Med 1967; 120(4): 428–32PubMedCrossRefGoogle Scholar
  96. 96.
    Sontz E, Schwieger J. The ‘green water’ syndrome: copper-induced hemolysis and subsequent acute renal failure as consequence of a religious ritual. Am J Med 1995; 98(3): 311–5PubMedCrossRefGoogle Scholar
  97. 97.
    Dabrowska E, Jablonska-Kaszewska I, Ozieblowski A, et al. Acute haemolytic syndrome and liver failure as the first manifestations of Wilson’s disease. Med Sci Monit 2001; 7Suppl. 1: 246–51PubMedGoogle Scholar
  98. 98.
    Buchanan GR. Acute hemolytic anemia as a presenting manifestation of Wilson disease. J Pediatr 1975; 86(2): 245–7PubMedCrossRefGoogle Scholar
  99. 99.
    Matsumura A, Hiraishi H, Terano A. Plasma exchange for hemolytic crisis in Wilson disease [letter]. Ann Intern Med 1999; 131(11): 866PubMedGoogle Scholar
  100. 100.
    Paglia DE, Valentine WN, Dahlgren JG. Effects of low-level lead exposure on pyrimidine 5′-nucleotidase and other erythrocyte enzymes: possible role of pyrimidine 5′-nucleotidase in the pathogenesis of lead-induced anemia. J Clin Invest 1975; 56(5): 1164–9PubMedCrossRefGoogle Scholar
  101. 101.
    Hulten JO, Tran VT, Pettersson G. The control of haemolysis during transurethral resection of the prostate when water is used for irrigation: monitoring absorption by the ethanol method. BJU Int 2000; 86(9): 989–92PubMedCrossRefGoogle Scholar
  102. 102.
    Knutsen OH, Jansson U. Hemolysis and pulmonary edema after a near-drowning accident in chlorated water [in Swedish]. Lakartidningen 1988; 85(52): 4646–7PubMedGoogle Scholar
  103. 103.
    Hubl W, Mostbeck B, Hartleb H, et al. Investigation of the pathogenesis of massive hemolysis in a case of Clostridium perfringens septicemia. Ann Hematol 1993; 67(3): 145–7PubMedCrossRefGoogle Scholar
  104. 104.
    Sezerino UM, Zannin M, Coelho LK, et al. A clinical and epidemiological study of Loxosceles spider envenoming in Santa Catarina, Brazil. Trans R Soc Trop Med Hyg 1998; 92(5): 546–8PubMedCrossRefGoogle Scholar
  105. 105.
    Murray LM, Seger DL. Hemolytic anemia following a presumptive brown recluse spider bite. J Toxicol Clin Toxicol 1994; 32(4): 451–6PubMedCrossRefGoogle Scholar
  106. 106.
    Bey TA, Walter FG, Lober W, et al. Loxosceles arizonica bite associated with shock. Ann Emerg Med 1997; 30(5): 701–3PubMedCrossRefGoogle Scholar
  107. 107.
    Leung LK, Davis R. Life-threatening hemolysis following a brown recluse spider bite. J Tenn Med Assoc 1995; 88(10): 396–7PubMedGoogle Scholar
  108. 108.
    Tambourgi DV, Morgan BP, de Andrade RM, et al. Loxosceles intermedia spider envenomation induces activation of an endogenous metalloproteinase, resulting in cleavage of glycophorins from the erythrocyte surface and facilitating complement-mediated lysis. Blood 2000; 95(2): 683–91PubMedGoogle Scholar
  109. 109.
    van Den Berg CW, de Andrade RM, Magnoli FC, et al. Loxosceles spider venom induces metalloproteinase mediated cleavage of MCP/CD46 and MHCI and induces protection against C-mediated lysis. Immunology 2002; 107(1): 102–10CrossRefGoogle Scholar
  110. 110.
    Patel KD, Modur V, Zimmerman GA, et al. The necrotic venom of the brown recluse spider induces dysregulated endothelial cell-dependent neutrophil activation: differential induction of GM-CSF, IL-8, and E-selectin expression. J Clin Invest 1994; 94(2): 631–42PubMedCrossRefGoogle Scholar
  111. 111.
    Campbell CH. Myotoxic paralysis and hemolytic anemia due to king brown snake bite. Aust N Z J Med 1984; 14(2): 169PubMedCrossRefGoogle Scholar
  112. 112.
    Hung DZ, Wu ML, Deng JF, et al. Russell’s viper snakebite in Taiwan: differences from other Asian countries. Toxicon 2002; 40(9): 1291–8PubMedCrossRefGoogle Scholar
  113. 113.
    Mukherje AK, Ghosal SK, Maity CR. Some biochemical properties of Russell’s viper (Daboia russelli) venom from Eastern India: correlation with clinico-pathological manifestation in Russell’s viper bite. Toxicon 2000; 38(2): 163–75PubMedCrossRefGoogle Scholar
  114. 114.
    Phillips RE, Theakston RD, Warrell DA, et al. Paralysis, rhabdomyolysis and haemolysis caused by bites of Russell’s viper (Vipera russelli pulchella) in Sri Lanka: failure of Indian (Haffkine) antivenom. Q J Med 1988; 68(257): 691–715PubMedGoogle Scholar
  115. 115.
    Gillissen A, Theakston RD, Barth J, et al. Neurotoxicity, haemostatic disturbances and haemolytic anaemia after a bite by a Tunisian saw-scaled or carpet viper (Echis ‘pyramidum’-complex): failure of antivenom treatment. Toxicon 1994; 32(8): 937–44PubMedCrossRefGoogle Scholar
  116. 116.
    Gibly RL, Walter FG, Nowlin SW, et al. Intravascular hemolysis associated with North American crotalid envenomation. J Toxicol Clin Toxicol 1998; 36(4): 337–43PubMedCrossRefGoogle Scholar
  117. 117.
    Vetter RS, Visscher PK, Camazine S. Mass envenomations by honey bees and wasps. West J Med 1999; 170(4): 223–7PubMedGoogle Scholar
  118. 118.
    Munoz-Arizpe R, Valencia-Espinoza L, Velasquez-Jones L, et al. Africanized bee stings and pathogenesis of acute renal failure [letter]. Nephron 1992; 61(4): 478PubMedCrossRefGoogle Scholar
  119. 119.
    Melvin JD, Watts RG. Severe hypophosphatemia: a rare cause of intravascular hemolysis. Am J Hematol 2002; 69(3): 223–4PubMedCrossRefGoogle Scholar
  120. 120.
    Altuntas Y, Innice M, Basturk T, et al. Rhabdomyolysis and severe haemolytic anaemia, hepatic dysfunction and intestinal osteopathy due to hypophosphataemia in a patient after Billroth II gastrectomy. Eur J Gastroenterol Hepatol 2002; 14(5): 555–7PubMedCrossRefGoogle Scholar
  121. 121.
    Kaiser U, Barth N. Haemolytic anaemia in a patient with anorexia nervosa. Acta Haematol 2001; 106(3): 133–5PubMedCrossRefGoogle Scholar
  122. 122.
    Beutler E, Dern RJ, Alving AS. The hemolytic effect of primaquine: IV. The relationship of cell age to hemolysis. J Lab Clin Med 1954; 44(3): 439–42PubMedGoogle Scholar
  123. 123.
    Mason PJ. New insights into G6PD deficiency. Br J Haematol 1996; 94(4): 585–91PubMedGoogle Scholar
  124. 124.
    Beutler E. G6PD deficiency. Blood 1994; 84(11): 3613–36PubMedGoogle Scholar
  125. 125.
    Bulliamy T, Luzzatto L, Hirono A, et al. Hematologically important mutations: glucose-6-phosphate dehydrogenase. Blood Cells Mol Dis 1997; 23(2): 302–13PubMedCrossRefGoogle Scholar
  126. 126.
    Nagel RL, Roth Jr EF. Malaria and red cell genetic defects. Blood 1989; 74(4): 1213–21PubMedGoogle Scholar
  127. 127.
    Luzzatto L, Usanga FA, Reddy S. Glucose-6-phosphate dehydrogenase deficient red cells: resistance to infection by malarial parasites. Science 1969; 164(881): 839–42PubMedCrossRefGoogle Scholar
  128. 128.
    Steinberg MH, West MS, Gallagher D, et al. Effects of glucose-6-phosphate dehydrogenase deficiency upon sickle cell anemia. Blood 1988; 71(3): 748–52PubMedGoogle Scholar
  129. 129.
    Takizawa T, Huang IY, Ikuta T, et al. Human glucose-6-phosphate dehydrogenase: primary structure and cDNA cloning. Proc Natl Acad Sci USA 1986; 83(12): 4157–61PubMedCrossRefGoogle Scholar
  130. 130.
    Beutler E, Vulliamy T, Luzzatto L. Hematologically important mutations: glucose-6-phosphate dehydrogenase. Blood Cells Mol Dis 1996; 22(1): 49–56PubMedCrossRefGoogle Scholar
  131. 131.
    Beutler E, Vulliamy TJ. Hematologically important mutations: glucose-6-phosphate dehydrogenase. Blood Cells Mol Dis 2002; 28(2): 93–103PubMedCrossRefGoogle Scholar
  132. 132.
    Kaplan M, Algur N, Hammerman C. Onset of jaundice in glucose-6-phosphate dehydrogenase-deficient neonates. Pediatrics 2001; 108(4): 956–9PubMedCrossRefGoogle Scholar
  133. 133.
    Huang CS, Hung KL, Huang MJ, et al. Neonatal jaundice and molecular mutations in glucose-6-phosphate dehydrogenase deficient newborn infants. Am J Hematol 1996; 51(1): 19–25PubMedCrossRefGoogle Scholar
  134. 134.
    Valaes T. Pathophysiology of spontaneous neonatal bilirubinemia associated with glucose-6-phosphate dehydrogenase deficiency. J Pediatr 1996; 128(6): 863–4PubMedCrossRefGoogle Scholar
  135. 135.
    MacDonald MG. Hidden risks: early discharge and bilirubin toxicity due to glucose 6-phosphate dehydrogenase deficiency. Pediatrics 1995; 96 (4 Pt 1): 734–8PubMedGoogle Scholar
  136. 136.
    Fiorelli G, Martinez DM, Cappellini MD. Chronic non-spherocytic haemolytic disorders associated with glucose-6-phosphate dehydrogenase variants. Baillieres Best Pract Clin Haematol 2000; 13(1): 39–55CrossRefGoogle Scholar
  137. 137.
    Chevion M, Navok T, Glaser G, et al. The chemistry of favism-inducing compounds: the properties of isouramil and divicine and their reaction with glutathione. Eur J Biochem 1982; 127(2): 405–9PubMedCrossRefGoogle Scholar
  138. 138.
    Beutler E. Glucose-6-phosphate dehydrogenase deficiency. N Engl J Med 1991; 324(3): 169–74PubMedCrossRefGoogle Scholar
  139. 139.
    Sklar GE. Hemolysis as a potential complication of acetaminophen overdose in a patient with glucose-6-phosphate dehydrogenase deficiency. Pharmacotherapy 2002; 22(5): 656–8PubMedCrossRefGoogle Scholar
  140. 140.
    Wright RO, Perry HE, Woolf AD, et al. Hemolysis after acetaminophen overdose in a patient with glucose-6-phosphate dehydrogenase deficiency. J Toxicol Clin Toxicol 1996; 34(6): 731–4PubMedCrossRefGoogle Scholar
  141. 141.
    Glucose-6-phosphate dehydrogenase deficiency. WHO Working Group. Bull World Health Organ 1989; 67(6): 601–11Google Scholar

Copyright information

© Adis Data Information BV 2004

Authors and Affiliations

  1. 1.Departments of Emergency Medicine, and of Pharmacology and ToxicologyQueen’s UniversityKingstonCanada
  2. 2.Ontario Regional Poison Information CentreTorontoCanada

Personalised recommendations