Hydroxyurea and Sickle Cell Anemia: Clinical Utility of a Myelosuppressive "Switching" Agent

Medicine

Volumn 75, Issue 6, 1996, Pages 300-326

  Charache, Samuel ^a,g   Barton, Franca B ^b   Moore, Richard D ^a   Terrin, Michael L ^b   Steinberg, Martin H ^c   Dover, George J ^a   Ballas, Samir K ^d   Mcmahon, Robert P ^b   Castro, Oswaldo ^e   Orringer, Eugene P ^f  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MARYLAND MEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF NORTH CAROLINA   (United States)

^g NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN S; HYDROXYUREA;

ARTICLE; BLOOD VESSEL OCCLUSION; CELL ADHESION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; ERYTHROCYTE MEMBRANE; HEMOLYSIS; HEMOLYTIC ANEMIA; HUMAN; PATHOPHYSIOLOGY; POLYMERIZATION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SICKLE CELL ANEMIA; TISSUE INJURY;

ADOLESCENT; ADULT; ANEMIA, SICKLE CELL; ANTISICKLING AGENTS; BLOOD CELL COUNT; DOUBLE-BLIND METHOD; ERYTHROCYTE INDICES; FEMALE; FETAL HEMOGLOBIN; GLOBINS; HUMANS; HYDROXYUREA; MALE; MIDDLE AGED;

EID: 0030464953     PISSN: 00257974     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005792-199611000-00002     Document Type: Review

References (120)

1. Adams RJ, Nichols FT, McKie VC, McKie KM, Milner PF, Gammall TE. Cerebral infarction in sickle cell anemia: mechanism based on CT and MRI. Neurology 38: 1012-17, 1988.
2. Adragna NC, Fonseca P, Lauf PK. Hydroxyurea affects cell morphology, cation transport, and red cell adhesion in cultured vascular endothelial cells. Blood 83: 553-60, 1994.
3. Akinola NO, Stevens SME, Franklin FM, Nash GB, Stuart J. Rheological changes in the prodromal and established phases of sickle cell vasoocclusive crisis. Br J Haematol 81: 598-602, 1992.
4. Aluoch JR. The treatment of sickle cell disease: a historical and chronological literature review of the therapies applied since 1910. Trop Geog Med 36 (Suppl): S1-S26, 1984.
5. Asakura T, Mayberry J. Relationship between the morphology of sickle cells and the method of deoxygenation. J Lab Clin Med 104: 987, 1984.
6. Ballas SK, Larner J, Smith ED, Surrey S, Schwartz E, Rappaport EF. The xerocytosis of Hb SC disease. Blood 69: 124-30, 1987.
7. Ballas SK, Lamer J, Smith ED, Surrey S, Schwartz E, Rappaport EF. Rheologic predictors of the severity of the painful sickle cell crisis. Blood 72: 1216-23, 1988.
8. Barabino GA, Mclntire LV, Eskin SG, Sears DA, Udden M. Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow. Blood 70: 152-7, 1987.
9. Bauer C, Ludwig I, Ludwig M. Different effects of 2,3-diphosphoglycerate and adenosine triphosphate on the oxygen affinity of adult and foetal haemoglobin. Life Sci 7: 1339, 1968.
10. Benesch RE, Edalji R, Kwong S, Benesch R. Oxygen affinity as an index of hemoglobin S polymerization: a new micromethod. Anal Biochem 89: 162-73, 1978.
11. Berk PD, Wasserman LR, Fruchtman SM, Goldberg JD. Treatment of polycythemia vera: a summary of clinical trials conducted by the polycythemia vera study group. In: Wasserman LR, Berk PD, Berlin NI, eds. Polycythemia Vera and the Myeloproliferative Disorders. Philadelphia: W. B. Saunders, p. 166, 1995.
12. Bookchin RM, Ortiz OE, Lew VL. Activation of calcium-dependent potassium channels in deoxygenated sickle cells. Prog Clin Biol Res 240: 193-200, 1987.
13. Briehl RW, Guzman AE. Fragility and structure of hemoglobin S fibers and gels and their consequences for gelation kinetics and rheology. Blood 83: 573-9, 1994.
14. Briehl RW, Nikolopoulou P. Kinetics of hemoglobin S polymerization and gelation under shear. I. Shape of the viscosity progress curve and dependence of delay time and reaction rate on shear rate and temperature. Blood 81: 2420-8, 1993.
15. Brugnara C, Bunn HF, Tosteson DC. Regulation of erythrocyte cation and water content in sickle cell anemia. Science 232: 388, 1986.
16. Brugnara C, De Franceschi L, Alper S. Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 92: 520-6, 1993.
17. Castro O, Brambilla DJ, Thorington B, Reindorf CA, Scott RB, Gillette P, Vera JC, Levy PS, the Cooperative Study of Sickle Cell Disease. The acute chest syndrome in sickle cell disease: incidence and risk factors. Blood 84: 643-9, 1994.
18. Chang YC, Smith KD, Moore RD, Serjeant GR, Dover GJ. An analysis of fetal hemoglobin variation in sickle cell disease: the relative contributions of the X-linked factor, beta-globin haplotypes, alpha-globin gene number, gender, and age. Blood 85: 1111-7, 1995.
19. Charache S. Fetal hemoglobin, sickling, and sickle cell disease. Adv Pediatr 37: 1-31, 1990.
20. Charache S, Conley CL. Factors leading to vascular occlusion in sickle cell anemia. Prog Clin Biol Res 1: 343-74, 1975.
21. Charache S, Dover GJ, Moore RD, Eckert S, Ballas SK, Koshy M, Milner PF, Orringer EP, Phillips G Jr, Platt OS, Thomas GH. Hydroxyurea: effects on hemoglobin F production in patients with sickle cell anemia. Blood 79: 2555-65, 1992.
22. Charache S, Dover GJ, Moyer MA, Moore JW. Hydroxyurea-induced augmentation of fetal hemoglobin production in patients with sickle cell anemia. Blood 69: 109-16, 1987.
23. Charache S, Terrin ML, Moore RD, Dover GJ, Barton FB, Eckert SV, McMahon RP, Bonds DR, Investigators of the Multicenter Study of Hydroxyurea Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. N Engl J Med 332: 1317-22, 1995.
24. Charache S, Terrin ML, Moore RD, Dover GJ, McMahon RP, Barton F, Waclawiw M, Eckert S, Investigators of the Multicenter Study of Hydroxyurea. Design of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. Cont Clin Trials 16: 432-46, 1995.
25. Chiu D, Lubin B, Shohet SB. Erythrocyte membrane lipid reorganization during the sickling process. Br J Haematol 41: 223-34, 1979.
26. Conover WJ. Practical Nonparametric Statistics. 2nd ed. New York: John Wiley and Sons, 1980.
27. Cox DR. Regression models and life tables (with discussion). J Royal Stat Soc B 34: 187-220, 1972.
28. De Franceschi L, Rouyer-Fessard P, Alper SL, Jouault H, Brugnara C, Beuzard Y. Combination therapy of erythropoietin, hydroxyurea, and clotrimazole in a beta thalassemic mouse: a model for human therapy. Blood 87: 1188-95, 1996.
29. DeSimone J, Heller P, Hall L, Zwiers D. 5-Azacytidine stimulates fetal hemoglobin synthesis in anemic baboons. Proc Nat Acad Sci USA 79: 4428-31, 1982.
30. DeSimone J, Schimenti JC, Duncan CH, Heller P, Lavelle D. DNA methylation and expression of baboon globin genes. In: The Red Cell: Sixth Ann Arbor Conference. New York: Alan R. Liss, p. 59, 1983.
31. Dover GJ, Charache S, Nora R, Boyer SH. Progress toward increasing fetal hemoglobin production in man: Experience with 5-azacytidine and hydroxyurea. Ann NY Acad Sci 45: 218-24, 1986.
32. Dover GJ, Humphries RK, Moore JG, Ley TJ, Young NS, Charache S, Nienhuis AW. Hydroxyurea induction of hemoglobin F production in sickle cell disease: Relationship between cytotoxicity and F cell production. Blood 67: 735-8, 1986.
33. Dover GJ, Smith KD, Chang YC, Purvis S, Mays A, Meyers DA, Shells C, Serjeant GR. Fetal hemoglobin levels in sickle cell disease and normal individuals are partially controlled by an X-linked gene located at Xp22.2. Blood 80: 816-24, 1992.
34. Drupt F, Rousseaux J, Demouveau G, Allard C, De Boisfleury A, Maigne J. Hemoglobine setif. Formation de drepanocytes in vitro. Nouv Presse Med 6: 123-4, 1977.
35. Eaton WA, Hofrichter J. Hemoglobin S gelation and sickle cell disease. Blood 70: 1245-66, 1987.
36. Edelstein SJ. Molecular topology in crystals and fibers of hemoglobin S. J Mol Biol 150: 557-75, 1981.
37. Embury SH, Hebbel RP, Mohandas N, Steinberg MH, eds. Sickle Cell Disease: Basic Principles and Clinical Practice. New York: Raven Press, 1994.
38. Fabry ME, Kaul DK. Sickle cell vaso-occlusion. Hematol Oncol Clin North Am 5: 375-98, 1991.
39. Farber MD, Koshy M, Kinney TR, Cooperative Study of Sickle Cell Disease. Cooperative study of sickle cell disease: demographic and socioeconomic characteristics of patients and families with sickle cell disease. J Chronic Dis 38: 495-505, 1985.
40. Fauci AS, Dale DC, Balow JE. Glucocorticosteroid therapy: mechanisms of action and clinical considerations. Ann Intern Med 84: 304-15, 1976.
41. Feinberg SE. The Analysis of Cross-Classified Categorical Data Cambridge, Mass.: MTT Press, 1980.
42. Franck PFH, Bevers EM, Lubin BH, et al. Uncoupling of the membrane skeleton from the lipid bilayer. J Clin Invest 75: 183-90, 1985.
43. Gilman JG, Huisman THJ. DNA sequence variation associated with elevated G gamma globin production. Blood 66: 783-7, 1985.
44. Goldstein RA, Bowen DL, Fauci AS. Adrenal corticosteroids. In: Gallin JI, Goldstein IM, Snyderman R, eds. Inflammation: Basic Principles and Clinical Correlates. New York: Raven Press, p. 1061, 1992.
45. Green GA, Kaira VK. Sickling-induced binding of immunoglobulin to sickle erythrocytes. Blood 71: 636-9, 1988.
46. Hattori Y, Kutlar F, Kutlar A, McKie VC, Huisman THJ. Haplotypes of beta-S chromosomes among patients with sickle cell anemia from Georgia. Hemoglobin 10: 623-42, 1986.
47. Hebbel RP, Leung A, Mohandas N. Oxidation-induced changes in microrheologic properties of the red blood cell membrane Blood 76: 1015-20, 1990.
48. Hebbel RP, Miller WJ. Phagocytosis of sickle erythrocytes: immunologic and oxidative determinants of hemolytic anemia. Blood 64: 733-41, 1984.
49. Hebbel RP, Morgan WT, Eaton JW, Hedlund BE. Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proc Natl Acad Sci USA 85: 237-41, 1988.
50. Hebbel RP, Visser MR, Goodman JL, Jacob HS, Vercellotti GM. Potentiated adherence of sickle erythrocytes to endothelium infected by virus. J Clin Invest 80: 1503-6, 1987.
51. Hebbel RP, Yamada O, Moldow CF, Jacob HS, White JG, Eaton JW. Abnormal adherence of sickle erythrocytes to cultured vascular endothelium. J Clin Invest 65: 154-60, 1980.
52. Hernandez LA, Grisham MB, Twohig B, Arfors KE, Harlan JM, Granger DN. Role of neutrophils in ischemia-reperfusion-induced microvascular injury. Am J Physiol (Heart Circ Physiol) 253: H699-H703, 1987.
53. Hofrichter J, Ross PD, Eaton WA. Kinetic and mechanism of deoxyhemoglobin S gelation: a new approach to understanding sickle cell disease. Proc Natl Acad Sci USA 71: 4864-8, 1974.
54. Hofstra TC, Kalra VK, Meiselman HJ, Coates TD. Sickle erythrocytes adhere to polymorphonuclear neutrophils and activate the neutrophil respiratory burst. Blood 87: 4440-7, 1996.
55. Hoover R, Rubin R, Wise G, Warren R. Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures. Blood 54: 872-6, 1979.
56. Joiner CH, Franco RS, Jiang M, Franco MS, Barker JE, Lux SE. Increased cation permeability in mutant mouse red blood cells with defective membrane skeletons. Blood 86: 4307-14, 1995.
57. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 53: 457-81, 1958.
58. Kasschau MR, Barabino GA, Bridges KR, Golan DE. Adhesion of sickle neutrophils and erythrocytes to fibronectin. Blood 87: 771-80, 1996.
59. Kay MMB. Mechanism of removal of senescent cells by human macrophages in situ. Proc Natl Acad Sci USA 72: 3521-5, 1975.
60. Koshy M, Entsuah R, Koranda A, Kraus AP, Johnson R, Bellvue R, Flournoy-Gill Z, Levy P. Leg ulcers in patients with sickle cell disease. Blood 74: 1403-8, 1989.
61. Lande WM, Andrews DL, Clark MR, Braham NV, Black DM, Embury SH, Mentzer WC. The incidence of painful crisis in homozygous sickle cell disease: correlation with red cell deformability. Blood 72: 2056-9, 1988.
62. Lane PA, O'Connell JL, Kinney TR, Rupp EO, Labotka RJ, Wang WC. Hydroxyurea increases red cell pit counts in children and adolescents with sickle cell anemia: implications for assessment of splenic function. Blood 86 (Suppl 1): 140a, 1995.
63. Liakopoulo E, Blau CA, Li Q, et al. Stimulation of fetal hemoglobin production by short chain fatty acids. Blood 86: 3227-36, 1995.
64. Liang KY, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrika 73: 13-22, 1986.
65. Lipowsky HH, Chien S. Role of leukocyte-endothelium adhesion in affecting recovery from ischemic episodes. Ann NY Acad Sci 565: 308-15, 1989.
66. Lu Z-H, Steinberg MH, Multicenter Study of Hydroxyurea. Fetal hemoglobin concentration in sickle cell anemia: relation to regulatory regions cis to the beta-globin gene. Blood 87: 1604-11, 1996.
67. Lux SE, John KM, Kamovsky MJ. Irreversible deformation of the spectrin-actin lattice in irreversibly sickled cells. J Clin Invest 58: 955-60, 1976.
68. MacDonald VM, Charache S. Differences in the reaction sequences associated with drug-induced oxidation of hemoglobins E, S, A, and F. J Lab Clin Med 102: 762-72, 1983.
69. McCurdy PR, Sherman AS. Irreversibly sickled cells and red cell survival in sickle cell anemia. Am J Med 64: 253-8, 1978.
70. Messer MJ, Harris JW. Filtration characteristics of sickle cells: rates of alteration of filterability after deoxygenation and reoxygenation, and correlations with sickling and unsickling. J Lab Clin Med 76: 537-47, 1970.
71. Milner PF, Kraus AP, Sebes JI, Sleeper LA, Dukes KA, Embury SH, Bellevue R, Koshy M, Moohr JW, Smith J. Sickle cell disease as a cause of osteonecrosis of the femoral head. N Engl J Med 325: 1476-81, 1991.
72. Milner PF, Kraus AP, Sebes JI, Sleeper LA, Dukes KA, Embury SH, Bellevue R, Koshy M, Moohr JW, Smith J. Osteonecrosis of the humeral head in sickle cell disease. Clin Orthop Rel Res 289: 136-43, 1993.
73. Milner PF, Miller C, Grey R, Seakins M, DeJong WW, Went LN. Hemoglobin O-Arab in four Negro families and its interaction with hemoglobin S and hemoglobin C. N Engl J Med 283: 1417-1425, 1970
74. Miyoshi M, Kaneto Y, Kawai H, Ohchi H, Niki S, Hasegawa K, Shirakami A, Yamano T. X-linked dominant control of F-cells in normal adult life: characterization of the Swiss type as hereditary persistence of fetal hemoglobin regulated dominantly by gene(s) on X-chromosome. Blood 72: 1854-60, 1988.
75. Morris CL, Rucknagel DL, Joiner CH. Deoxygenation-induced changes in sickle cell-sickle cell adhesion. Blood 81: 3138-45, 1993.
76. Nagel RL, Fabry ME, Pagnier J, Zohoun I, Wajcman H, Baudin V, Labie D. Hematologically and genetically distinct forms of sickle cell anemia in Africa. N Engl J Med 312: 880-4, 1985.
77. Nand S, Stock W, Godwin J, Fisher SG. Leukemogenic risk of hydroxyurea therapy in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Am J Hematol 52: 42-6, 1996.
78. Ney PA, Christopher MM, Hebbel RP. Synergistic effects of oxidation and deformation on erythrocyte monovalent cation leak. Blood 75: 1192-8, 1990.
79. Noguchi CT, Schlechter AN. The intracellular polymerization of sickle hemoglobin and its relevance to sickle cell disease. Blood 58: 1057-68, 1981.
80. Ohene-Frempong K, Horiuchi K, Stoeckert C Jr, et al. Sustained effect of hydroxyurea on Hb F production in children with sickle cell disease [Abstract]. Proceedings of the 20th Annual Meeting of the National Sickle Cell Disease Program, 1995.
81. Ohnishi ST, Horiuchi KY, Horiuchi K. The mechanism of in vitro formation of irreversibly sickled cells and modes of action of its inhibitors. Biochim Biophys Acta 886: 119-29, 1986.
82. Papayannopoulou T, Bunn HF, Stamatoyannopoulos G. Cellular distribution of hemoglobin F in clonal hematopoietic stem cell disorders N Engl J Med 298: 72-6, 1978.
83. Perutz MF. Structure and mechanism of haemoglobin. Br Med Bull 32: 195-208, 1976.
84. Platt OS, Brambilla DJ, Rosse WF, MUner PF, Castro O, Steinberg MH, Klug P. Mortality in sickle cell disease: life expectancy and risk factors for early death. N Engl J Med 330: 1639, 1994.
85. Platt OS, Falcone JF. Membrane protein interactions in sickle red blood cells: evidence of abnormal protein 3 function. Blood 86: 1992-8, 1985.
86. Platt OS, Orkin SH, Dover G, Beardsley GP, Miller B, Nathan DG. Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia. J Clin Invest 74: 652-56, 1984.
87. Platt OS, Thorington BD, Brambilla DJ, Milner PF, Rosse WF, Vichinsky E, Kinney TR. Pain in sickle cell disease: rates and risk factors. N Engl J Med 325: 11-16, 1991.
88. Repka T, Hebbel RP. Hydroxyl radical formation by sickle erythrocyte membranes: role of pathologic iron deposits and cytoplasmic reducing agents. Blood 78: 2753-8, 1991.
89. Resar LMS, Oski FA. Cold water exposure and vaso-occlusive crises in sickle cell anemia. J Pediatr 118: 407-9, 1991.
90. Richardson DR, Tran EH, Ponka P. The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents. Blood 86: 4295-4306, 1995.
91. Rodgers GP, Dover GJ, Noguchi CT, Schechter AN, Nienhuis AW. Hematologic responses of patients with sickle cell disease to treatment with hydroxyurea. N Engl J Med 322: 1037-45, 1990.
92. Rogers ZR, Dale JC, Bernini JC, Reisch JS, Primm PA, Buchanan GR. Dexamethasone shortens the duration of painful events requiring hospitalization in children with sickle cell disease: results of a randomized, double-blind, placebo-controlled trial. Blood 86 (Suppl 1): 250a, 1995.
93. Russell MO, Goldberg HI, Hodson A, Kim HC, Halus J, Reivich M, Schwartz E. Effect of transfusion therapy on arteriographic abnormalities and on recurrence of stroke in sickle cell disease. Blood 63: 162-9, 1984.
94. Schmalzer EA, Lee JO, Brown AK, Usami S, Chien S. Viscosity of mixtures of sickle and normal red cells at varying hematocrit levels: implications for transfusion. Transfusion 27: 228-33, 1987.
95. Schmid-Schonbein GW. Capillary plugging by granulocytes and the no-reflow phenomenon in the microcirculation. Federation Proc 46: 2397-2401, 1987.
96. Schroeder WA, Powars DR, Kay LM, Chan LS, Huynh V, Shelton JB, Shelton JR. Beta-cluster haplotypes, alpha gene status, and hematological data from SS, SC, and S-beta-thalassemia patients from Southern California. Hemoglobin 13: 325-53, 1989.
97. Schwartz RB, Tanaka Y, Fidler LI, Chiu DT-Y, Lubin B, Schroit AJ. Increased adherence of sickled and phosphatidylserine-enriched human erythrocytes to cultured human peripheral blood monocytes. J Clin Invest 75: 1965-72, 1985.
98. Serjeant GR. Sickle Cell Disease. 2nd ed. New York: Oxford University Press, 1992.
99. Serjeant GR, Serjeant BE, Milner PF. The irreversibly sickled cell: a determinant of haemolysis in sickle cell anaemia. Br J Haematol 17: 527-33, 1969.
100. Shelley WM, Curtis EM. Bone marrow and fat embolism in sickle cell anemia and sickle cell-hemoglobin C disease. Bull Johns Hopkins Hosp 103: 8-25, 1958.
101. Singer K, Chernoff AI. Studies on abnormal hemoglobins. III. The interrelationship of type S (sickle cell) hemoglobin and type F (alkali resistant) hemoglobin in sickle cell anemia Blood 7: 47-52, 1952.
102. Smith CM II, Hebbel RP, Tukey DP, Clawson CC, White JG, Vercellotti GM. Pluronic F-68 reduces the endothelial adherence and improves the rheology of liganded sickle erythrocytes. Blood 69: 1631-6, 1987.
103. Smith EW, Conley CL. Sickle cell hemoglobin D disease. Ann Intern Med 50: 94-105, 1959.
104. Stamatoyannopoulos G, Veith R, Al-Khata A, Fritsch EF, Goldwasser E, Papayannopoulou T. On the induction of fetal hemoglobin in the adult: stress erythropoiesis, cell cycle-specific drugs, and recombinant erythropoietin. In: Stamatoyannopoulos G, Nienhuis AW, eds. Developmental Control of Globin Gene Expression. New York: Alan R. Liss, p. 443, 1987.
105. Steel RGD, Torrie JH. Principles and Procedures of Statistics. New York: McGraw-Hill, 1960.
106. Steinberg MH, Hsu H, Nagel RL, Milner PF, Adams JG, Benjamin L, Fryd S, Gillette P, Gilman J, Josifovska O, Hellman-Erlingsson S, Safaya S, Huey L, Rieder RF. Gender and haplotype effects upon hematological manifestations of adult sickle cell anemia. Am J Hematol 48: 175-81, 1995.
107. Steinberg MH, Lu Z-H, Barton FB, Terrin ML, Charache S, Dover GJ. Fetal hemoglobin in sickle cell anemia: determinants of response to hydroxyurea. Blood (in press).
108. Steinberg MH, Nagel RL, Brugnara C. Hydroxyurea-independent of Hb F - alters the erythrocytes of Hb SC disease J Invest Med 44: 233A, 1996.
109. Steinberg MH, Rosenstock W, Coleman MB, Adams JG, Platica O, Cedeno M, Rieder RF, Wilson JT, Milner P, West S, The Cooperative Study of Sickle Cell Disease. Effects of thalassemia and microcytosis on the hematologic and vasoocclusive severity of sickle cell anemia. Blood 63: 1353-60, 1984.
110. Styles L, Kuypers E, Lubin B, et al. The modulation of adhesion receptors in sickle cell disease patients treated with hydroxyurea. Blood 86 (Suppl 1): 140a, 1995.
111. 2 levels in acute chest syndrome of sickle cell disease. Blood 87: 2573-8 1996.
112. Ward PCJ, Smith CM, White JG. Erythrocytic ecdysis. An unusual morphologic finding in a case of sickle cell anemia with intercurrent cold-agglutinin syndrome. Am J Clin Pathol 72: 479-85, 1979.
113. Warren JS, Ward PA, Johnson KJ. The inflammatory response. In: Williams WJ, Beutler E, Erslev AJ, Lichtman MA, eds. Hematology. New York: McGraw-Hill, p. 63, 1990.
114. Wautier JL, Pintigny D, Wautier MP, et al. Fibrinogen, a modulator of erythrocyte adhesion to vascular endothelium. J Lab Clin Med 101: 911-20, 1983.
115. Weissmann G, Zurier RB, Hoffstein S. Leukocytes as secretory organs of inflammation. Agents Actions 3: 270, 1973.
116. West MS, Wethers D, Smith J, Steinberg M, The Cooperative Study of Sickle Cell Disease. Laboratory profile of sickle cell disease: a cross-sectional analysis. J Clin Epidemiol 45: 893-909, 1992.
117. Westerman MP, Cole ER, Wu K. The effect of spicules obtained from sickle red cells on clotting activity. Br J Haematol 56: 557-62, 1984.
118. Wick TM, Eckman JR. Molecular basis of sickle cell-endothelial cell interactions. Curr Opin Hematol 3: 118-24, 1996.
119. Wishner BC, Ward KB, Lattman EE, Love WE. Crystal structure of sickle-cell deoxyhemoglobin at 5 A resolution. J Mol Biol 98: 179-94, 1975.
120. Zimmerman GA, Prescott SM, McIntyre TM. Endothelial cell interactions with granulocytes: tethering and signaling molecules. Immunol Today 13: 93-100, 1992.