Sickle red cell microrheology and sickle blood rheology

Microcirculation

Volumn 11, Issue 2, 2004, Pages 209-225

  Ballas, Samir K ^a   Mohandas, Narla ^b  

^a THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

^b NEW YORK BLOOD CENTER   (United States)

Author keywords

Cell deformability; Membrane mechanical properties; Rheology; Sickle cell anemia; Sickle cell disease

Indexed keywords

ARGININE; CLOTRIMAZOLE; DEOXYHEMOGLOBIN; ERYTHROPOIETIN; HEMOGLOBIN F; HEMOGLOBIN S; HYDROXYUREA; ISOBUTYRIC ACID; MAGNESIUM; NITRIC OXIDE; PHENYLACETIC ACID; VALPROIC ACID;

BLOOD RHEOLOGY; BLOOD VESSEL OCCLUSION; BLOOD VESSEL TONE; BLOOD VISCOSITY; CELL DAMAGE; CELLULAR DISTRIBUTION; CLINICAL FEATURE; CYTOMETRY; DISEASE SEVERITY; ENVIRONMENTAL FACTOR; ERYTHROCYTE; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE FRAGILITY; ERYTHROCYTE LIFESPAN; ERYTHROCYTE VOLUME; GENETIC EPISTASIS; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HEMATOCRIT; HEMOLYTIC ANEMIA; HUMAN; INFLAMMATION; MULTIPLE ORGAN FAILURE; PATHOGENESIS; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; REVIEW; SICKLE CELL ANEMIA; TISSUE INJURY; TREATMENT OUTCOME; VASCULAR ENDOTHELIUM; VASODILATATION;

ANEMIA, SICKLE CELL; ANIMALS; ENDOTHELIUM, VASCULAR; ERYTHROCYTES, ABNORMAL; HEMOGLOBIN, SICKLE; HUMANS; INFLAMMATION; RHEOLOGY; VASCULAR DISEASES;

EID: 10244242639     PISSN: 10739688     EISSN: None     Source Type: Journal    
DOI: 10.1080/10739680490279410     Document Type: Review

References (142)

1. Adams RJ, Kutlar A, McKic V, et al. (1993). Alpha thalassemia and stroke risk in sickle cell anemia. Am J Hematol 45:279-282.
2. Adekile AD, Kutlar F, Haider MZ, Kutlar A. (2001). Frequency of the 677C → T mutation of the methylenctetrahydrofolate reductase gene among Kuwati sickle cell patients. Am J Hematol 66:263-266.
3. Akinola NO, Steven SME, Franklin IM, et al. (1992). Rheological changes in the prodromal and established phases of sickle vasoocclusive crisis. Br J Haematol 81:598-602.
4. Al-Khatti A, Veith RW, Papayannopoulou T, et al. (1987). Stimulation of hemoglobin synthesis by erythropoietin in baboons. N Engl J Med 317:415-420.
5. Ballas SK, Dover GJ, Charache S. (1989). The effect of hydroxyurea on the rheological properties of sickle erythrocytes in vivo. Am J Hematol 32:104-111.
6. s; -α/-α)? Hemoglobin 21:405-420.
7. Ballas SK, Larner J, Smith ED, et al. (1998). Rheologic predictors of the severity of the painful sickle cell crisis. Blood 72:1216-1223.
8. Ballas SK, Marcolina MJ, Dover GJ, Barton FB. (1999). Erythropoietic activity in patients with sickle cell anemia before and after treatment with Hydroxyurea. Br J Haematol 105:491-496.
9. Ballas SK, Smith ED. (1992). Red cell changes during the evolution of the sickle cell painful crisis. Blood 79:2154-2163.
10. Ballas SK, Talacki CA, Rao VM, Steiner RM. (1989). The prevalence of avascular necrosis in sickle cell anemia: correlation with α-thalassemia. Hemoglobin 13:649-655. 1
11. Ballas SK. (2000). Hydration of sickle erythrocytes using a herbal extract (Pfaffia paniculata) in-vitro. Br J Haematol 111:359-362.
12. Ballas, SK. (1991). Sickle cell anemia with few painful crises is characterized by decreased red cell deformability and increased number of dense cells, Am J Hematol 36:122-130.
13. Baruchel S, Rees J, Bernstein ML, Goodyer P. (A 993). Relief of sickle cell priapism by hydralazine. Am J Pediatr Hematol/Oncol 15:115-116.
14. Baum K, Dun DT, Maude GH, Serjeant GR. (1987). The painful crisis of homozygous sickle cell disease: a study of risk factors. Arch Intern Med 147:1231-1234.
15. Bertles JF, Milner PFA. (1968). Irreversibly sickled erythrocytes: a consequence of the heterogeneous distribution of hemoglobin types in sickle-cell anemia. J Clin Invest 47:1731-1740.
16. Bessis M, Mohandas N. (1975). A diffractometric method for the measurement of cellular deformability. Blood Cells 1:307-313.
17. Bessis M, Mohandas N. (1977). Laser diffraction pattern of sickle cells in shear fields. Blood Cells 3:229-239.
18. Billett HH, Fabry ME, Nagel RL. (1988). Hemoglobin distribution width: a rapid assessment of dense red cells in the steady state and during painful crisis in sickle cell anemia. J Lab Clin Med 112:339.
19. Blau CA, Constantoulakis P, Shaw CM, et al. (1993). Fetal hemoglobin induction with butyric acid: efficacy and toxicity. Blood 81:529-537.
20. Boros L, Weiner WJ. (1978). Sickle cell anemia and other hemoglobinopathies. In: Handbook of Clinical Neurology, vol 38 (PJ Vinken and GW Bruyn, Eds.) Amsterdam: Elsevier. 33-51.
21. Bridgers WH. (1939). Cerebral vascular disease accompanying sickle cell anemia. Am J Pathol 15:353-561.
22. Briehl RW, Ewert S. (1973). Effects of pH, 2,3-diphosphoglycerate and salts on gelation of sickle cell deoxyhemoglobin. J Mol Biol 80:445-458.
23. Briehl RW. (1978). Gelation of sickle cell hemoglobin IV. Phase transitions in hemoglobin S gels: separate measures of aggregation and solution-gel equilibrium. J Mol Biol 123:521-538.
24. Brugnara C, Bunn HF, Tosteson DC. (1986). Regulation of erythrocytes cation and water content in sickle cell anemia. Science 232:388-390.
25. Brugnara C, DCT. (1987). Inhibition of K transport by divaleut cations in sickle erythrocytes. Blood 70:1810-1805.
26. + transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 92:520-552.
27. Brugnara C, Gee B, Armsby CC, et al. (1996). Therapy with oral clotrimazole induces inhibition of the Gardos channel and reduction of erythrocyte dehydration in patients with sickle cell disease. J Clin Invest 97:1227-1234.
28. Brugnara C, Kopin AS, Bunn HF, Tosteson DC. (1985). Regulation of cation content and cell volume in hemoglobin erythrocytes from patients with homozygous hemoglobin C disease. J Clin Invest 75:1608-1617.
29. Charache S, Dover GJ, Moore RD, Eckert S, Ballas SK, Koshy M, Milner PFA, Orringer EP, Phillips G Jr, Platt OS, Thomas GH. (1992). Hydroxyurea: effects on hemoglobin F production in patients with sickle cell anemia. Blood 79:2555-2565.
30. Charache S, Terrin ML, Moore RD, et al, and the Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. (1995). Effect of hydroxyurea on the frequency, of painful crises in sickle cell anemia. N Engl J Med 332:1317-1322.
31. Chien S, King RG, Kaperonis AA, Usami S. (1982). Viscoclastic properties of sickle cells and hemoglobin. Blood Cells 8:53-64.
32. Chien S, Usami S, Bertles JF. (1970). Abnormal rheology of oxygenated blood in sickle cell anemia. J Clin Invest 49:623-634.
33. + and water contents. Biochim Biophys Acta 646:422-432.
34. Clark MR, Mohandas N, Embury SH, Lubin BH. (1982). A simple laboratory alternative to irreversibly sickle cell (ISC) counts. Blood 60:659.
35. Clark MR, Mohandas N, Shohet SB. (1983). Deformability of oxygenated irreversibly sickled cells. J Clin Invest 65:189-196.
36. Clark MR, Mohandas N, Shohet SB. (1983). Osmotic gradient ektacytometry: comprehensive characteristics of red cell volume and surface maintenance. Blood 61:899-910.
37. Clark MR, Morrison CE, Shohet SB. (1978). Monovalent cation transport in irreversibly sickled cells. J Clin Invest 61:329-337.
38. Collins AF, Dover GJ, Luban NLC. (1994). Increased fetal hemoglobin production in patients receiving valproic acid for epilepsy. Blood 84:1690-1691.
39. Corash LM, Piomelli S, Chen HC, Seaman C, Gross E. (1974). Separation of erythrocytes according to age on a simplified density gradient. J Lab Clin Med 84:147-151.
40. Danish EH, Harris JW. (1983). Viscosity studies of deoxyhemoglobin S: evidence for formation of microaggregates during the lag phase. J Lab Clin Med 101:515-526.
41. de Franceschi L, Bachir D, Galacteros F, et al. (1997). Oral magnesium supplements reduce erythrocyte dehydration in patients with sickle cell disease. J Clin Invest 100:1847-1852.
42. de Jong K, Emerson RK, Butler J, et al. (2001). Short Survival of phosphatidylserine exposing red blood cells in murine sickle cell anemia. Blood 98:1577-1584.
43. Dover GJ, Brusilow S, Samid D. (1992). Increased fetal hemoglobin in patients receiving sodium 4-phenylbutyrate. N Engl J Med 327:569-570.
44. Eaton WA, Hofrichter J. (1987). Hemoglobin S gelation and sickle cell disease. Blood 70:1245-1266.
45. Edelstein SJ. (1981). Molecular topology in crystals and fibers of hemoglobin S. J Mol Biol 50:557-575.
46. Embury SH, Backer K, Clader BE. (1985). Monovalent cation changes in sickle erythrocytes: a direct reflection of α-globin gene number. J Lab Clin Med 106:75-79.
47. Embury SH, Clark MR, Monroy GM, Mohandas N. (1984). Concurrent sickle cell anemia and α thalassemia: effect on pathological properties of sickle red cells. J Clin Invest 73:116-123.
48. Erslev AJ. (1983). Erythrokinetics. In: Hematology, 3rd ed. (WJ Williams, E Beutler, AJ Ersley, and MA Lichtman, Eds.) New York: McGraw-Hill. 1638-1643.
49. Evans E, Mohandas N, Leung A. (1984). Static and dynamic rigidities of normal and sickle erythrocytes: major influence of cell hemoglobin coucentration. J Clin Invest 73:477-488.
50. Farbry ME, Mears JG. Patel P, Schaefer-Rego K, Carmichael LD, Martinez G, Nagel RL. (1984). Dense cells in sickle cell anemia: the effects of gene interaction. Blood 64:1042-1046.
51. Felice AE, McKie KM, Cleek MP. et al. (1987). Effect of α-thalassemia on the developmental changes of hematological values in children with sickle cell disease from Georgia. Am J Hematol 25:389-400.
52. Ferrone FA, Hofrichter J, Eaton WA. (1985). Kinetics of sickle hemoglobin Polymerization, II: a double nucleation mechanism. J Vol Biol 183:611-631.
53. Fortier N, Snyder LM, Garver F, et al. (1988). The relationship between in vivo generated hemoglobin skeletal protein complex and increased red cell membrane rigidity. Blood 71:1427-1431.
54. Fox PD, Higg DR, Serjeant GR. (1993). Influence of α-thalassemia on the retinopathy of homozygous sickle cell disease. Br J Ophthalmol 77:89-90.
55. Gill SJ, Spokane R, Benedict RC, et al. (1980). Ligand-linked phase equilibria of sickle cell hemoglobin. J Mol Biol 140:299-312.
56. Girgis RE, Qureshi MA, Abrams J, Swerdlow P. (2003). Decreased exhaled nitric oxide in sickle cell disease: relationship with chronic lung involvement. Am J Hematol 72:177-184. PMID: 12605389 [PubMed - indexed for MEDLINE]
57. Goldberg MA, Brugnara C, Dover GJ, Schapira L, Charache S, Bunn HF. (1990). Treatment of sickle cell anemia with hydroxyurea and erythropoietin. N Engl J Med 323:366-372.
58. Goldberg MA, Husson MA, Bunn HF. (1977). The participation of hemoglobins A and F in the polymerization of sickle hemoglobin. J Biol Chem 252:3414-3421.
59. Groner W, Mohandas N, Bessis M (1980). New optical technique for Measuring erythrocyte deformability with the ektacytomeler. Clin. Chem. 26:14315-1442.
60. Hasen HB, Raines SL. (1962). Priapism associated with sickle cell disease. J Urol 88:71-76.
61. Havel TC, Hillman D, Lessin LS. (1978). Deformability characteristics of sickle cells by microelastimetry. Am J Hematol 4:9-17.
62. Hawker H, Neilson R, Hayes RJ, Serjeant GR. (1982). Haematological factors associated with avascular necrosis of the femoral head in homozygous sickle cell disease. Br J Haematol 50:29-39.
63. Hayes RJ, Condon PI, Serjeant GR. (1981). Haematologic factors associated with proliferative retinopathy in homozygous sickle cell disease. Br J Ophthalmol 65:29-35.
64. Hebbel RP, Mohandas N. (1994). Sickle cell adherence. In: Sickle Cell Disease: Basic Principles and Clinical Practice (SH Embury. RP Hebbel, N Mohandas, and MH Steinberg, Eds.) New York: Raven. 217-230.
65. Hofrichter J, Ross PD, Eaton WA. (1976). A physical description of bemoglobin S gelation. In: Proceedings of the Symposium on Molecular and Cellular Aspects of Sickle Cell Disease (JI Hercules, GL Cottan, MR Waterman, and AN Schechter, Eds.) Bethesda, MD: DHEW Publ No. (NIH) 76-1007. 185.
66. International Committee for Standardization in Hematology. (1980). Recommended method for radiosotope red-cell survival studies. Br J Haematol 45:659-666.
67. 2 and temperature control. Blood 79:2141-2147.
68. Jan K, Usami S, Smith JA. (1982). Effects of transfusion on rheological properties of blood in sickle cell anemia. Tranfusion 22:17-20.
69. Joiner CH. (1993). Cation transport and volume regulation in sickle red blood cells. Am J Physiol 264 (Cell Physiol 33):C251-C270.
70. 1 and glycoprotein IV (CD 36) are expressed on circulating reticulocytes in sickle cell anemia. Blood 82:3548-3555.
71. Kaufman R. (1992). Hydroxyurea: specific theraphy for sickle cell anemia? Blood 79:2503-2506.
72. Kaul DK, Fabry ME, Nagel RL. (1989). Microvascular sites and characteristics of sickle cell adhesion to vascular endothelium in shear flow conditions: pathophysiological implications. Proc Natl Acad Sci USA 86:3356-3360.
73. Keidan AJ, Noguchi CT, Player M, et al. (1989). Erthrocyte heterogeneity in sickle cell disease: effect of deoxygenation on intracellular polymer formation and rheology of subpopulations. Br J Haematol 72:254-261.
74. Kennedy AP, Williams B, Meydrech EF, Steinberg MH. (1988). Regional and temporal variation in oscillatory blood flow in sickle cell disease. Am J Hematol 28:02-94.
75. Khademi M, Marquis JR. (1973). Renal angiography in sickle-cell disease. Radiology 107:41-46.
76. Klug PP, Kaye N, Jensen WN. (1982). Endothelial cell and vascular damage in the sickle cell disorders. Blood Cells 8:175-184.
77. Koshy M, Entsuah R, Koranda A, et al. (1989). Leg ulcers in patients with sickle cell disease. Blood 75:1403-1408.
78. Kurantsin-Mills J, Klug PP, Lessin LS. (1988). Vasoocclusion in sickle cell disease: pathophysiology of the microvascular circulation. Am J Pediatr Hematol Oncol 10:357-372.
79. Lande WM, Andrews DL, Clark MR, et al. (1988). The incidence of painful crisis in homozygous sickle cell disease: correlation with red cell deformability. Blood 72:2056-2059.
80. 1 and ion content regulation in reticulocytes: application to the pathophysiology of sickle cell dehydration. J Clin Invest 87:100-112.
81. Lew VL, Hockaday A, Sepulveda MI, et al. (1985). Compartmentation of sickle cell calcium in endocytic inside-out vesicles. Nature 315:586-588.
82. Lipowsky NH, Sheikh NU, Katz DM. (1987). Intravital microscopy of capillary hemodynamics in sickle cell disease. J Clin Invest 80:117-127.
83. Longnecker G, Culberson D, Beyers B, et al. (1991). Plasma endothelin (ET) levels are elevated in sickle cell disease (SCD). Blood 79 (suppl 1): 202a.
84. Lopez BL, Barnett J, Ballas SK, Christopher TA, Davis-Moon L, Ma X. (1996). Nitric oxide metabolite levels in acute vasoocclusive sickle-cell crisis. Acad Emerg Med 3:1098-103.
85. Lopez BL, Kreshak AA, Morris CR, Davis-Moon L, Ballas SK, Ma XL. (2003). L-Arginine levels are diminished in adult acute vasoocclusive sickle cell crisis in the emergency department. Br J Haematol 120:532-534. PMID: 12580975 [PubMed - indexed for MEDLINE].
86. Mackie LH, Hochmuth RM. (1990). The influence of oxygen tension, temperature, and hemoglobin concentration on the rheological properties of sickle erythrocytes. Blood 76:1256-1261.
87. Magdoff-Fairchild B, Poillon WN, Li TI, Bertles JF. (1976). Thermodynamic studies of polymerization of deoxygenated sickle cell hemoglobin. Proc Natl Acad Sci USA 73:990-994.
88. Merkel KHH, Ginsberg PL, Parker JC, Post MJD. (1978). Cerebrovascular disease in sickle cell anemia: a clinical, pathological and radiological correlation. Stroke 9:45-52.
89. Messmann R, Gannon S, Sarnaik S, Johnson RM. (1990). Mechanical properties of sickle cell membranes. Blood 75:1711-1717.
90. Milner PF, Kraus AP, Sebes JI, et al. (1993). Osteonecrosis of the humeral head in sickle cell disease. Clin Orthop 289:136-143.
91. Milner PF, Kraus AP, Sebes JL, et al. (1991). Sickle cell disease as a cause of osteonecrosis of the femoral head. N Engl J Med 325:1476-1481.
92. Mohandas N, Ballas SK. (1994). Erythrocyte density and heterogeneity. In: Sickle Cell Disease: Basic Principles and Clinical Practice (SH Embury, RP Habbel, N Mohandas, and MH Steinberg Eds.) New York: Raven. 195-203.
93. Mohandas N, Chasis JA, Shohet SB. (1983). The influence of membrane skeleton on red cell deformability, membrane material properties, and shape. Semin Hematol 20:225-242.
94. Mohandas N, Chasis JA. (1993). Red cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol 30:171-192.
95. Mohandas N, Clark MR, Jacobs MS, Shohet SB. (1980). Analysis of factors regulating erythrocyte deformability. J. Clin. Invest. 66:563-573.
96. Mohandas N, Hebbel RP. (1994). Erythrocyte deformability, fragility, and rheology, In: Sickle Cell Disease: Basic Principles and Clinical Practice (SH Embury, RP Hebbel, N Mohandas, and MH Steinberg, Eds.) New York: Raven. 205-215.
97. Morris CR, Morris SM, Hagar W, Van Warmerdam J, Claster S, Kepka-Lenhart D, Machado L, Kuypers FA, Vichinsky EP. (2003). Arginine therapy: a new treatment for pullmonary hypertension in sickle cell disease? Am J Respir Crit Care Med [epub ahead of print] PMID: 12626350 [PubMed - as supplied by publisher]
98. Mueller BU, Brugnara C. (2001). Prevention of red cell dehydration: a possible new treatment for sickle cell disease. Pediatr Pathol Mol Med 20:15-25.
99. 2 on the polymerization of Hb S. Proc Natl Acad Sci USA 76:670-674.
100. Nagel RL, Erlingsson S, Fabry ME, et al. (1991). The Senegal DNA haplotype is associated with the amelioration of anemia in African-American sickle cell anemia patients. Blood 77:1371-1375.
101. Nash GB, Johnson CS, Meiselman H. (1986). Influence of oxygen tension on the viscoelastic behavior of red blood cells in sickle cell disease. Blood 67:110-118.
102. Nash GB, Johnson CS, Meiselman HJ. (1984). Mechanical properties of oxygenated red blood cells in sickle cell (HbSS) disease. Blood 63:73-80.
103. S) hybrid hemoglobin on Hb S nucleation and aggregation. Biochim Biophys Acta 829:97-102.
104. Nogachi CT, Dover GJ, Rodgers GP, Serjeant GR, Antonarakia SE, Anagnou NP, Higgs DR, Weatherall DJ, Schecter AN. (1985). α-Thalassemia changes erythrocyte heterogeneity in sickle cell disease. J clin Invest 75:1632-1637.
105. Noguchi CT, Schechter AN. (1981). The intracellular polymerization of sickle hemoglobin at its relevance to sickle cell disease. Blood 58:1057-1068.
106. Pagnier J, Mears JG, Dunda-Belkodja O, et al. (1984). Evidence for the multicentric origin of the hemoglobin S gene in Africa. Proc Nat Acad Sci USA 81:1771-1773.
107. Perrine SP, Ginder GD, Faller DV, et al. (1993). A short-term trial of burtyate to stimulate fetal-globingene expression in the b-globin disorders. N Engl J Med 328:81-86.
108. Perutz MF. (1976). Structure and Mechanism of haemoglobin. Br Med Bull 32:195-208.
109. Platt OS, Brambilla DJ, Rosse WF, et al. (1994). Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 330:1639-1644.
110. Platt OS, Thornington BD, Brambilla DJ, et al. (1991). Pain in sickle cell disease: rates and risk factors. N Engl J Med 325:11-16.
111. Poillon WN, Bertles JF. (1979). Deoxygenated sickle hemoglobin: effects of lyotropic salts on its solubility. J Biol Chem 254:3462-3467.
112. S-gene-cluster haplotypes as prognostic indicators of vital organ failure. Semin Hematol 28:202-208.
113. 2+ in sickle cells. Cell Calcium 6:397-411.
114. Rodgers GP, Dover GJ, Noguchi CT, Schechter AN, Nienhuis AW. (1990). Hematologic responses of patients with sickle cell disease to treatment with hydroxyurea. N Engl J Med 322: 366-372.
115. Rodgers GP, Dover GJ, Uyesaka N, et al. (1993). Augmentation by erythropoietin of the fetalhemoglobin response to hrydroxyurea in sickle cell disease. N Engl J Med 328:73-80.
116. Rodgers GP, Schechter AN, Nogoachi CT, et al. (1984). Periodic microcirculatory flow in patients with sickle eel] disease. N Engl J Med 311:1534-1538.
117. Ross PD, Hofrichter J, Eaton WA. (1975). Calorimetric and optical characterization of sickle cell hemoglobin gelation. J Mol Biol 96:239-256.
118. Ross PD, Hofrichter J, Eaton WA. (1977). Thermodynanics of gelation of sickle deoxyhemoglobin. J Mol Biol 115:111-134.
119. Rothman SM, Fulling KH, Nelson JS. (1986). Sickle cell anemia and central nervous system infarction: a neuropathological study. Ann Neurol 20:684-690.
120. 2+ levels. J Cell Physiol 126:53-59.
121. Rybicki AC, Musto S, Swinson GI, et al. (1991). Increased levels of endothelin-1 in plasma of sickle cell anemia patients. Blood 78(Suppl 1):202a.
122. Saleh AW, van Goethem A, Jansen R, et al. (1995). Isobutyramide therapy in patients with sickle cell anemia. Am J Hematol 49:244-246.
123. Samuel RE, Salmon ED, Briehl RW. (1990). Nucleation and growth of fibers and gel formation in sickle cell haemoglobin. Nature 345:833-835.
124. Sarnaik S, Ballas SK. (2001). Molecular characteristics of pediatric patients with sickle cell anemia and stroke. Am J Hematol 67:179-182.
125. Schmalzer E, Chien S, Brown AK. (1982). Transfusion therapy in sickle cell disease. Am J Pediatr Hematol Oncol 4:395-406.
126. Schmalzer EA, Lee JO, Brown AK, et al. (1987). Viscosity of mixtures of sickle and normal red cells at varying hematocrit levels: Implications for transfusion. Transfusion 27:228-233.
127. Schmalzer EZ, Manning RS, Chien S. (1989). Filtration of sickle cells: recruitment into a rigid fraction as a function of density and oxygen tension. J Lab Clin Med 113:727-734.
128. Serjeant BE, Mason KP, Kenny KW, Stuart J, Higgs DR, Weatheral DJ, Hayes RJ, Serjeant GR. (1983). Effect of alpha thalassemia on the rheology of homozygous sickle cell disease. Br J Haematol 55:479-486
129. Serjeant GR, Serjeant BE. (2001). Sickle Cell Disease, 3rd ed. New York: Oxford University Press.
130. Setty BN, Kulkarni S, Dampier CD, et al. (2001). Fetal hemoglobin in sickle cell anemia: relationship to erythrocyte adhesion markers and adhesion. Blood 97:2568-2573.
131. Setty BN, Kulkarni S, Rao AK, et al. (2000). Fetal hemoglobin in sickle cell disease: Relationship to erythrocyte phosphatidylserine exposure and coagulation activation. Blood 96:1119-1124.
132. Smith CM, Kuettner JF, Takey DP, et al. (1981). Variable deformability of irreversibly sickled erythrocytes. Blood 58:71-76).
133. Sorette MP, Lavenant MG, Clark MR. (1987). Ektacytometric measurement of sickle cell deformability as a continuous function of oxygen tension. Blood 69:316-322.
134. Steinberg MH, Embury SH. (1986). Thalassemia in blacks: Genetic and clinical aspects and interactions with the sickle hemoglobin gene. Blood 68:985-990.
135. Steinberg MH, Hsu H, Nagel RL, et al. (1995). Gender and haplotype effects upon hematological manifestations of adult sickle cell anemia. Am J Hematol 48:175-181.
136. Stockman JA, Nigro MA, Mishkin MM, Oski FA. (1972). Occlusion of large cerebral vessels in sicklecell anemia. N Engl J Med 287:846-850.
137. Styles LA, Hoppe C, Klitz W, Vichinsky E, Lubin B, Trachtenberg E. (2000). Evidence for HLA-related susceptibility for stroke in children with sickle cell disease. Blood 95:3562-3567.
138. Sunshine HR, Hofrichter J, Ferrone FA. (1981). Oxygen binding by sickle cell hemoglobin polymers. J Mol Biol 158:251-273.
139. 1-integrin expression on sickle reticulocytes: vascular cell adhesion molecule-1-dependent binding to endothelium. Blood 82:1891-1899.
140. Talbot JF, Bird AC, Maude GH, et al. (1988). Sickle cell retinopathy in Jamaican children: further observations from a cohort study. Br J Ophthamol 72:727-732.
141. Usami S, Chien S, Bertles JF. (1975). Deformability of sickle cells as studied by microseiving. J Lab Clin Med 86:274-279.
142. Zwaal RFA, Schroit AJ. (1997). Pathophysiologic implications of membrane phospholipid asymmetry in blood cells: a review. Blood 89:1121-1132.