Semin Thromb Hemost 2012; 38(08): 854-864
DOI: 10.1055/s-0032-1325616
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Iatrogenic Hyperviscosity and Thrombosis

Oguz K. Baskurt
1   Koc University School of Medicine, Sariyer, Istanbul, Turkey
,
Herbert J. Meiselman
2   Department of Physiology and Biophysics, Keck School of Medicine, University of Southern California, Los Angeles, California
› Author Affiliations
Further Information

Publication History

Publication Date:
22 August 2012 (online)

Abstract

It is well known that hemostatic–thrombotic mechanisms are influenced by hemodynamic factors, such as shear forces affecting platelets or red blood cell aggregation, in turn affecting flow in stenotic regions. Endothelial cell function is also significantly influenced by shear forces acting on the vessel wall. Further, the distribution of shear forces in the vasculature is complex and closely associated with factors determining the flow properties of blood. Therefore, there is a link among alterations in the rheological properties of blood and its elements and the risk for thrombosis, with this linkage confirmed by numerous clinical studies. After discussing relevant rheological and hemodynamic concepts, this review focuses on selected drug-induced conditions that are known to be associated with both hyperviscosity conditions and increased thrombotic risk: oral contraceptives, diuretics, intravenous immunoglobulin, erythropoiesis-stimulating agents, chemotherapy, and radio-contrast media. Alterations of relationships between blood rheology and thrombotic risk related to artificial circulatory environments and physical exercise are also briefly discussed.

 
  • References

  • 1 Cokelet GR. Hemorheology and Hemodynamics. San Francisco, CA: Morgan & Claypool Life Sciences; 2011
  • 2 Cokelet GR, Meiselman HJ. Macro- and micro-rheological properties of blood. In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds. Handbook of Hemorheology and Hemodynamics. Amsterdam, Netherlands: IOS Press; 2007: 45-71
  • 3 Baskurt OK, Meiselman HJ. Blood rheology and hemodynamics. Semin Thromb Hemost 2003; 29 (5) 435-450
  • 4 Mohandas N, Chasis JA. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol 1993; 30 (3) 171-192
  • 5 Takakuwa Y, Ishibashi T, Mohandas N. Regulation of red cell membrane deformability and stability by skeletal protein network. Biorheology 1990; 27 (3–4) 357-365
  • 6 Chien S. Red cell deformability and its relevance to blood flow. Annu Rev Physiol 1987; 49: 177-192
  • 7 Alexy T, Sangkatumvong S, Connes P , et al. Sickle cell disease: selected aspects of pathophysiology. Clin Hemorheol Microcirc 2010; 44 (3) 155-166
  • 8 Vayá A, Iborra J, Falcó C , et al. Rheological behaviour of red blood cells in beta and deltabeta thalassemia trait. Clin Hemorheol Microcirc 2003; 28 (2) 71-78
  • 9 Baskurt OK. Mechanisms of blood rheology alterations. In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds. Handbook of Hemorheology and Hemodynamics. Amsterdam, Netherlands: IOS Press; 2007: 170-190
  • 10 Baskurt OK, Temiz A, Meiselman HJ. Effect of superoxide anions on red blood cell rheologic properties. Free Radic Biol Med 1998; 24 (1) 102-110
  • 11 Hebbel RP, Leung A, Mohandas N. Oxidation-induced changes in microrheologic properties of the red blood cell membrane. Blood 1990; 76 (5) 1015-1020
  • 12 Baskurt OK, Neu B, Meiselman HJ. Red Blood Cell Aggregation. Boca Raton, Florida: CRC Press; 2011
  • 13 Rampling MW, Meiselman HJ, Neu B, Baskurt OK. Influence of cell-specific factors on red blood cell aggregation. Biorheology 2004; 41 (2) 91-112
  • 14 Alt E, Amann-Vesti BR, Madl C, Funk G, Koppensteiner R. Platelet aggregation and blood rheology in severe sepsis/septic shock: relation to the Sepsis-related Organ Failure Assessment (SOFA) score. Clin Hemorheol Microcirc 2004; 30 (2) 107-115
  • 15 Baskurt OK, Temiz A, Meiselman HJ. Red blood cell aggregation in experimental sepsis. J Lab Clin Med 1997; 130 (2) 183-190
  • 16 Berliner AS, Shapira I, Rogowski O , et al. Combined leukocyte and erythrocyte aggregation in the peripheral venous blood during sepsis. An indication of commonly shared adhesive protein(s). Int J Clin Lab Res 2000; 30 (1) 27-31
  • 17 Chong-Martinez B, Buchanan TA, Wenby RB, Meiselman HJ. Decreased red blood cell aggregation subsequent to improved glycaemic control in Type 2 diabetes mellitus. Diabet Med 2003; 20 (4) 301-306
  • 18 Zilberman-Kravits D, Harman-Boehm I, Shuster T, Meyerstein N. Increased red cell aggregation is correlated with HbA1C and lipid levels in type 1 but not type 2 diabetes. Clin Hemorheol Microcirc 2006; 35 (4) 463-471
  • 19 Cicco G, Pirrelli A. Red blood cell (RBC) deformability, RBC aggregability and tissue oxygenation in hypertension. Clin Hemorheol Microcirc 1999; 21 (3–4) 169-177
  • 20 Lebensohn N, Re A, Carrera L, Barberena L, D'Arrigo M, Foresto P. [Serum sialic acid, cellular anionic charge and erythrocyte aggregation in diabetic and hypertensive patients]. Medicina (B Aires) 2009; 69 (3) 331-334
  • 21 Reneman RS, Arts T, Hoeks APG. Wall shear stress—an important determinant of endothelial cell function and structure—in the arterial system in vivo. Discrepancies with theory. J Vasc Res 2006; 43 (3) 251-269
  • 22 Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V. Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Dis 2007; 49 (5) 307-329
  • 23 Bishop JJ, Popel AS, Intaglietta M, Johnson PC. Effects of erythrocyte aggregation and venous network geometry on red blood cell axial migration. Am J Physiol Heart Circ Physiol 2001; 281 (2) H939-H950
  • 24 Bishop JJ, Popel AS, Intaglietta M, Johnson PC. Effect of aggregation and shear rate on the dispersion of red blood cells flowing in venules. Am J Physiol Heart Circ Physiol 2002; 283 (5) H1985-H1996
  • 25 Gaehtgens P, Meiselman HJ, Wayland H. Velocity profiles of human blood at normal and reduced hematocrit in glass tubes up to 130 diameter. Microvasc Res 1970; 2 (1) 13-23
  • 26 Goldsmith HL, Cokelet GR, Gaehtgens P. Robin Fåhraeus: evolution of his concepts in cardiovascular physiology. Am J Physiol 1989; 257 (3 pt 2) H1005-H1015
  • 27 Ong PK, Jain S, Kim S. Temporal variations of the cell-free layer width may enhance NO bioavailability in small arterioles: effects of erythrocyte aggregation. Microvasc Res 2011; 81 (3) 303-312
  • 28 Goldsmith HL, Bell DN, Spain S, McIntosh FA. Effect of red blood cells and their aggregates on platelets and white cells in flowing blood. Biorheology 1999; 36 (5–6) 461-468
  • 29 Nash GB, Watts T, Thornton C, Barigou M. Red cell aggregation as a factor influencing margination and adhesion of leukocytes and platelets. Clin Hemorheol Microcirc 2008; 39 (1–4) 303-310
  • 30 Bishop JJ, Popel AS, Intaglietta M, Johnson PC. Rheological effects of red blood cell aggregation in the venous network: a review of recent studies. Biorheology 2001; 38 (2–3) 263-274
  • 31 Bishop JJ, Nance PR, Popel AS, Intaglietta M, Johnson PC. Effect of erythrocyte aggregation on velocity profiles in venules. Am J Physiol Heart Circ Physiol 2001; 280 (1) H222-H236
  • 32 Rampling MW. Hyperviscosity as a complication in a variety of disorders. Semin Thromb Hemost 2003; 29 (5) 459-465
  • 33 Isbister JP. Hyperviscosity: clinical disorders. In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds. Handbook of Hemorheology and Hemodynamics. Amsterdam, Netherlands: IOS Press; 2007: 371-391
  • 34 Kwaan HC, Wang J. Hyperviscosity in polycythemia vera and other red cell abnormalities. Semin Thromb Hemost 2003; 29 (5) 451-458
  • 35 Kwaan HC, Bongu A. The hyperviscosity syndromes. Semin Thromb Hemost 1999; 25 (2) 199-208
  • 36 Kwaan HC. Role of plasma proteins in whole blood viscosity: a brief clinical review. Clin Hemorheol Microcirc 2010; 44 (3) 167-176
  • 37 Tsai HM. Shear stress and von Willebrand factor in health and disease. Semin Thromb Hemost 2003; 29 (5) 479-488
  • 38 Di Stasio E, De Cristofaro R. The effect of shear stress on protein conformation: physical forces operating on biochemical systems: the case of von Willebrand factor. Biophys Chem 2010; 153 (1) 1-8
  • 39 Anderson GH, Hellums JD, Moake J, Alfrey Jr CP. Platelet response to shear stress: changes in serotonin uptake, serotonin release, and ADP induced aggregation. Thromb Res 1978; 13 (6) 1039-1047
  • 40 Colantuoni G, Hellums JD, Moake JL, Alfrey Jr CP. The response of human platelets to shear stress at short exposure times. Trans Am Soc Artif Intern Organs 1977; 23: 626-631
  • 41 Jesty J, Yin W, Perrotta P, Bluestein D. Platelet activation in a circulating flow loop: combined effects of shear stress and exposure time. Platelets 2003; 14 (3) 143-149
  • 42 Nobili M, Sheriff J, Morbiducci U, Redaelli A, Bluestein D. Platelet activation due to hemodynamic shear stresses: damage accumulation model and comparison to in vitro measurements. ASAIO J 2008; 54 (1) 64-72
  • 43 Rubenstein DA, Yin W. Quantifying the effects of shear stress and shear exposure duration regulation on flow induced platelet activation and aggregation. J Thromb Thrombolysis 2010; 30 (1) 36-45
  • 44 Hellums JD. 1993 Whitaker Lecture: biorheology in thrombosis research. Ann Biomed Eng 1994; 22 (5) 445-455
  • 45 Nesbitt WS, Mangin P, Salem HH, Jackson SP. The impact of blood rheology on the molecular and cellular events underlying arterial thrombosis. J Mol Med (Berl) 2006; 84 (12) 989-995
  • 46 Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood 1996; 88 (5) 1525-1541
  • 47 Nesbitt WS, Kulkarni S, Giuliano S , et al. Distinct glycoprotein Ib/V/IX and integrin alpha IIbbeta 3-dependent calcium signals cooperatively regulate platelet adhesion under flow. J Biol Chem 2002; 277 (4) 2965-2972
  • 48 Sheriff J, Bluestein D, Girdhar G, Jesty J. High-shear stress sensitizes platelets to subsequent low-shear conditions. Ann Biomed Eng 2010; 38 (4) 1442-1450
  • 49 Michiels C. Endothelial cell functions. J Cell Physiol 2003; 196 (3) 430-443
  • 50 Toborek M, Kaiser S. Endothelial cell functions. Relationship to atherogenesis. Basic Res Cardiol 1999; 94 (5) 295-314
  • 51 Chien S. Molecular basis of rheological modulation of endothelial functions: importance of stress direction. Biorheology 2006; 43 (2) 95-116
  • 52 Chiu JJ, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 2011; 91 (1) 327-387
  • 53 Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999; 282 (21) 2035-2042
  • 54 Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 1998; 18 (5) 677-685
  • 55 Varin R, Mulder P, Richard V , et al. Exercise improves flow-mediated vasodilatation of skeletal muscle arteries in rats with chronic heart failure. Role of nitric oxide, prostanoids, and oxidant stress. Circulation 1999; 99 (22) 2951-2957
  • 56 Tsai AG, Friesenecker B, McCarthy M, Sakai H, Intaglietta M. Plasma viscosity regulates capillary perfusion during extreme hemodilution in hamster skinfold model. Am J Physiol 1998; 275 (6 pt 2) H2170-H2180
  • 57 Tsai AG, Acero C, Nance PR , et al. Elevated plasma viscosity in extreme hemodilution increases perivascular nitric oxide concentration and microvascular perfusion. Am J Physiol Heart Circ Physiol 2005; 288 (4) H1730-H1739
  • 58 Baskurt OK, Yalcin O, Ozdem S, Armstrong JK, Meiselman HJ. Modulation of endothelial nitric oxide synthase expression by red blood cell aggregation. Am J Physiol Heart Circ Physiol 2004; 286 (1) H222-H229
  • 59 Yalcin O, Ulker P, Yavuzer U, Meiselman HJ, Baskurt OK. Nitric oxide generation by endothelial cells exposed to shear stress in glass tubes perfused with red blood cell suspensions: role of aggregation. Am J Physiol Heart Circ Physiol 2008; 294 (5) H2098-H2105
  • 60 von Tempelhoff GF, Nieman F, Heilmann L, Hommel G. Association between blood rheology, thrombosis and cancer survival in patients with gynecologic malignancy. Clin Hemorheol Microcirc 2000; 22 (2) 107-130
  • 61 von Tempelhoff GF, Heilmann L, Hommel G, Pollow K. Impact of rheological variables in cancer. Semin Thromb Hemost 2003; 29 (5) 499-513
  • 62 Cao M, Olsen RJ, Zu Y. Polycythemia vera: new clinicopathologic perspectives. Arch Pathol Lab Med 2006; 130 (8) 1126-1132
  • 63 Tefferi A, Spivak JL. Polycythemia vera: scientific advances and current practice. Semin Hematol 2005; 42 (4) 206-220
  • 64 Landolfi R, Nicolazzi MA, Porfidia A, Di Gennaro L. Polycythemia vera. Intern Emerg Med 2010; 5 (5) 375-384
  • 65 Barbui T, Finazzi G. Evidence-based management of polycythemia vera. Best Pract Res Clin Haematol 2006; 19 (3) 483-493
  • 66 Fahraeus R. The influence of the rouleau formation of the erythrocytes on the rheology of the blood. Acta Med Scand 1958; 161 (2) 151-165
  • 67 Loscalzo J. Nitric oxide insufficiency, platelet activation, and arterial thrombosis. Circ Res 2001; 88 (8) 756-762
  • 68 Landolfi R, Cipriani MC, Novarese L. Thrombosis and bleeding in polycythemia vera and essential thrombocythemia: pathogenetic mechanisms and prevention. Best Pract Res Clin Haematol 2006; 19 (3) 617-633
  • 69 Garcia D, Quintana D. Thrombosis and malignancy: a case-based review. Semin Hematol 2011; 48 (4) 259-263
  • 70 Zahra S, Anderson JAM, Stirling D, Ludlam CA. Microparticles, malignancy and thrombosis. Br J Haematol 2011; 152 (6) 688-700
  • 71 Contrino J, Hair G, Kreutzer DL, Rickles FR. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996; 2 (2) 209-215
  • 72 Zacharski LR, Memoli VA, Ornstein DL, Rousseau SM, Kisiel W, Kudryk BJ. Tumor cell procoagulant and urokinase expression in carcinoma of the ovary. J Natl Cancer Inst 1993; 85 (15) 1225-1230
  • 73 Caplan LR, Hennerici M. Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol 1998; 55 (11) 1475-1482
  • 74 Sedlaczek O, Caplan L, Hennerici M. Impaired washout—embolism and ischemic stroke: further examples and proof of concept. Cerebrovasc Dis 2005; 19 (6) 396-401
  • 75 Döring A, Fröhlich M, Löwel H, Koenig W. Third generation oral contraceptive use and cardiovascular risk factors. Atherosclerosis 2004; 172 (2) 281-286
  • 76 Basaria S, Nguyen T, Rosenson RS, Dobs AS. Effect of methyl testosterone administration on plasma viscosity in postmenopausal women. Clin Endocrinol (Oxf) 2002; 57 (2) 209-214
  • 77 El Bouhmadi A, Laffargue F, Raspal N, Brun JF. 100 mg acetylsalicylic acid acutely decreases red cell aggregation in women taking oral contraceptives. Clin Hemorheol Microcirc 2000; 22 (2) 99-106
  • 78 Ernst E, Schmölzl C, Matrai A, Schramm W. Hemorheological effects of oral contraceptives. Contraception 1989; 40 (5) 571-580
  • 79 Solerte SB, Fioravanti M, Spinillo A, Ferrari E, Guaschino S. Influence of triphasic oral contraceptives on blood rheology and hemostatic and metabolic patterns in young women. Results of a three-year study. J Reprod Med 1992; 37 (8) 725-732
  • 80 Coata G, Ventura F, Lombardini R, Ciuffetti G, Cosmi EV, Di Renzo GC. Effect of low-dose oral triphasic contraceptives on blood viscosity, coagulation and lipid metabolism. Contraception 1995; 52 (3) 151-157
  • 81 Ishak R, Khim LC. Effect of combined low-dose oral contraceptives on blood viscosity and haematocrit. Malays J Reprod Health 1991; 9 (1) 5-8
  • 82 Lowe GDO, Drummond MM, Forbes CD, Barbenel JC. Increased blood viscosity in young women using oral contraceptives. Am J Obstet Gynecol 1980; 137 (7) 840-842
  • 83 Buchan PC, Macdonald HN. Altered haemorheology in oral-contraceptive users. BMJ 1980; 280 (6219) 978-979
  • 84 Durocher JR, Weir MS, Lundblad EG, Patow WE, Conrad ME. Effect of oral contraceptives and pregnancy on erythrocyte deformability and surface charge. Proc Soc Exp Biol Med 1975; 150 (2) 368-370
  • 85 Reiner JS. Contrast media and clotting: what is the evidence?. Catheter Cardiovasc Interv 2010; 75 (Suppl. 01) S35-S38
  • 86 Hardeman MR, Goedhart P, Koen IY. The effect of low-osmolar ionic and nonionic contrast media on human blood viscosity, erythrocyte morphology, and aggregation behavior. Invest Radiol 1991; 26 (9) 810-819
  • 87 Laurent A, Durussel JJ, Dufaux J , et al. Effects of contrast media on blood rheology: comparison in humans, pigs, and sheep. Cardiovasc Intervent Radiol 1999; 22 (1) 62-66
  • 88 Reinhart WH, Pleisch B, Harris LG, Lütolf M. Influence of contrast media (iopromide, ioxaglate, gadolinium-DOTA) on blood viscosity, erythrocyte morphology and platelet function. Clin Hemorheol Microcirc 2005; 32 (3) 227-239
  • 89 Smedby O. Viscosity of some contemporary contrast media before and after mixing with whole blood. Acta Radiol 1992; 33 (6) 600-605
  • 90 Scheller B, Hennen B, Thünenkötter T , et al. Effect of X-ray contrast media on blood flow properties after coronary angiography. Thromb Res 1999; 96 (4) 253-260
  • 91 Spitzer S, Münster W, Sternitzky R, Bach R, Jung F. Influence of Iodixanol-270 and Iopentol-150 on the microcirculation in man: influence of viscosity on capillary perfusion. Clin Hemorheol Microcirc 1999; 20 (1) 49-55
  • 92 Spencer CG, Felmeden DC, Blann AD, Lip GY. Effects of “newer” and “older” antihypertensive drugs on hemorrheological, platelet, and endothelial factors. A substudy of the Anglo-Scandinavian Cardiac Outcomes Trial. Am J Hypertens 2007; 20 (6) 699-704
  • 93 Muravyov AV, Yakusevich VV, Kabanov AV, Petrochenko AS. The effect of diuretics on red blood cell microrheological parameters in female hypertensive patients. Clin Hemorheol Microcirc 2005; 33 (2) 121-126
  • 94 Khder Y, Bray des Boscs L, el Ghawi R , et al. Calcium antagonists and thiazide diuretics have opposite effects on blood rheology and radial artery compliance in arterial hypertension: a randomized double-blind study. Fundam Clin Pharmacol 1998; 12 (4) 457-462
  • 95 Zannad F, Bray-Desboscs L, el Ghawi R, Donner M, Thibout E, Stoltz JF. Effects of lisinopril and hydrochlorothiazide on platelet function and blood rheology in essential hypertension: a randomly allocated double-blind study. J Hypertens 1993; 11 (5) 559-564
  • 96 Koenig W, Sund M, Ernst E , et al. Effects of felodipine ER and hydrochlorothiazide on blood rheology in essential hypertension—a randomized, double-blind, crossover study. J Intern Med 1991; 229 (6) 533-538
  • 97 Andrews RJ, Bringas JR, Muto RP. Effects of mannitol on cerebral blood flow, blood pressure, blood viscosity, hematocrit, sodium, and potassium. Surg Neurol 1993; 39 (3) 218-222
  • 98 Muravyov AV, Meiselman HJ, Yakusevich VV, Zamishlayev AV. Effects of antihypertensive therapy on hemorheological profiles in female hypertensive patients with initially low or high whole blood viscosity. Clin Hemorheol Microcirc 2002; 26 (2) 125-135
  • 99 Bird J, Carmona C. Probable interaction between warfarin and torsemide. Ann Pharmacother 2008; 42 (12) 1893-1898
  • 100 Laizure SC, Madlock L, Cyr M, Self T. Decreased hypoprothrombinemic effect of warfarin associated with furosemide. Ther Drug Monit 1997; 19 (3) 361-363
  • 101 Kaşifoğlu T, Yalçin AU. The effects of thiazide and thiazide-potassium sparing diuretics on fibrinolytic system parameters. Anadolu Kardiyol Derg 2006; 6 (2) 143-147
  • 102 Lottermoser K, Hertfelder HJ, Vetter H, Düsing R. Fibrinolytic function in diuretic-induced volume depletion. Am J Hypertens 2000; 13 (4 Pt 1) 359-363
  • 103 Bentley P, Rosso M, Sadnicka A, Israeli-Korn S, Laffan M, Sharma P. Intravenous immunoglobulin increases plasma viscosity without parallel rise in blood pressure. J Clin Pharm Ther 2012; 37 (3) 286-290
  • 104 Dalakas MC. High-dose intravenous immunoglobulin and serum viscosity: risk of precipitating thromboembolic events. Neurology 1994; 44 (2) 223-226
  • 105 Kowal P, Zmyślony A. Hemorheological changes after intravenous gammaglobulin administration in patients with neurological disorders. Clin Hemorheol Microcirc 2008; 40 (3) 229-234
  • 106 Baba R, Shibata A, Tsurusawa M. Single high-dose intravenous immunoglobulin therapy for kawasaki disease increases plasma viscosity. Circ J 2005; 69 (8) 962-964
  • 107 Ben-Ami R, Barshtein G, Mardi T , et al. A synergistic effect of albumin and fibrinogen on immunoglobulin-induced red blood cell aggregation. Am J Physiol Heart Circ Physiol 2003; 285 (6) H2663-H2669
  • 108 Game L, Voegel JC, Schaaf P, Stoltz JF. Do physiological concentrations of IgG induce a direct aggregation of red blood cells: comparison with fibrinogen. Biochim Biophys Acta 1996; 1291 (2) 138-142
  • 109 Macdougall IC, Davies ME, Hutton RD, Coles GA, Williams JD. Rheological studies during treatment of renal anaemia with recombinant human erythropoietin. Br J Haematol 1991; 77 (4) 550-558
  • 110 Nowicki M. Erythropoietin and hypertension. J Hum Hypertens 1995; 9 (2) 81-88
  • 111 Crowley JP, Chazan JA, Metzger JB, Pono L, Valeri CR. Blood rheology and 2,3-diphosphoglycerate levels after erythropoietin treatment. Ann Clin Lab Sci 1993; 23 (1) 24-32
  • 112 Delamaire M, Durand F, Hamel D, Joyeux V, Lepogamp P, Genetet B. [Improvement of hemorheologic parameters in hemodialyzed patients treated with human recombinant erythropoietin]. J Mal Vasc 1991; 16 (3) 289-294
  • 113 Hassan K, Roguin N, Kaganov Y, Hasan S, Kristal B. Effect of erythropoietin therapy on red cells filterability and left ventricular mass in predialysis patients. Ren Fail 2005; 27 (2) 177-182
  • 114 Singh A, Eckardt KU, Zimmermann A , et al. Increased plasma viscosity as a reason for inappropriate erythropoietin formation. J Clin Invest 1993; 91 (1) 251-256
  • 115 Bor-Kucukatay M, Yalcin O, Meiselman HJ, Baskurt OK. Erythropoietin-induced rheological changes of rat erythrocytes. Br J Haematol 2000; 110 (1) 82-88
  • 116 Vaziri ND, Ritchie C, Brown P , et al. Effect of erythropoietin administration on blood and plasma viscosity in hemodialysis patients. ASAIO Trans 1989; 35 (3) 505-508
  • 117 Shinaberger JH, Miller JH, Gardner PW. Erythropoietin alert: risks of high hematocrit hemodialysis. ASAIO Trans 1988; 34 (3) 179-184
  • 118 Lippi G, Franchini M, Favaloro EJ. Thrombotic complications of erythropoiesis-stimulating agents. Semin Thromb Hemost 2010; 36 (5) 537-549
  • 119 von Tempelhoff GF, Niemann F, Schneider DM, Kirkpatrick CJ, Hommel G, Heilmann L. Blood rheology during chemotherapy in patients with ovarian cancer. Thromb Res 1998; 90 (2) 73-82
  • 120 von Tempelhoff GF, Heilmann L, Pollow K, Hommel G. Monitoring of rheologic variables during postoperative high-dose brachytherapy for uterine cancer. Clin Appl Thromb Hemost 2004; 10 (3) 239-248
  • 121 Kameneva MV, Antaki JF. Mechanical trauma to blood. In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds. Handbook of Hemorheology and Hemodynamics. Amsterdam, Netherlands: IOS Press; 2007: 206-227
  • 122 Hirayama T, Roberts D, William-Olsson G. Mechanical trauma to red blood cells caused by Björk-Shiley and Carpentier-Edwards heart valves. Scand J Thorac Cardiovasc Surg 1985; 19 (3) 253-256
  • 123 Hirayama T, Yamaguchi H, Allers M, Roberts D, William-Olsson G. Changes in red cell deformability associated with anaesthesia and cardiopulmonary bypass in open-heart surgery. Scand J Thorac Cardiovasc Surg 1985; 19 (3) 257-262
  • 124 Vaisman S, Kensey K, Cho YI. Effect of hemodialysis on whole blood viscosity. Int J Artif Organs 2009; 32 (6) 329-335
  • 125 Martínez M, Vayá A, Alvariño J , et al. Hemorheological alterations in patients with chronic renal failure. Effect of hemodialysis. Clin Hemorheol Microcirc 1999; 21 (1) 1-6
  • 126 Dhar P, Eadon M, Hallak P, Munoz RA, Hammes M. Whole blood viscosity: effect of hemodialysis treatment and implications for access patency and vascular disease. Clin Hemorheol Microcirc 2012; . In press
  • 127 Ibrahim FF, Ghannam MM, Ali FM. Effect of dialysis on erythrocyte membrane of chronically hemodialyzed patients. Ren Fail 2002; 24 (6) 779-790
  • 128 Kameneva MV, Marad PF, Brugger JM , et al. In vitro evaluation of hemolysis and sublethal blood trauma in a novel subcutaneous vascular access system for hemodialysis. ASAIO J 2002; 48 (1) 34-38
  • 129 Ocak G, Vossen CY, Rotmans JI , et al. Venous and arterial thrombosis in dialysis patients. Thromb Haemost 2011; 106 (6) 1046-1052
  • 130 Minneci PC, Deans KJ, Zhi H , et al. Hemolysis-associated endothelial dysfunction mediated by accelerated NO inactivation by decompartmentalized oxyhemoglobin. J Clin Invest 2005; 115 (12) 3409-3417
  • 131 Connes P, Brun JF, Baskurt OK. Blood rheology and exercise. In: Connes P, Hue O, Perrey S, eds. Exercise Physiology: From a Cellular to an Integrative Approach. Amsterdam, Netherlands: IOS Press; 2010: 213-229
  • 132 Vandewalle H, Lacombe C, Lelièvre JC, Poirot C. Blood viscosity after a 1-h submaximal exercise with and without drinking. Int J Sports Med 1988; 9 (2) 104-107
  • 133 Yalcin O, Erman A, Muratli S, Bor-Kucukatay M, Baskurt OK. Time course of hemorheological alterations after heavy anaerobic exercise in untrained human subjects. J Appl Physiol 2003; 94 (3) 997-1002
  • 134 Ernst E, Daburger L, Saradeth T. The kinetics of blood rheology during and after prolonged standardized exercise. Clin Hemorheol 1991; 11: 429-439
  • 135 Brun JF, Belhabas H, Granat MCh , et al. Postexercise red cell aggregation is negatively correlated with blood lactate rate of disappearance. Clin Hemorheol Microcirc 2002; 26 (4) 231-239
  • 136 Gaudard A, Varlet-Marie E, Monnier JF , et al. Exercise-induced central retinal vein thrombosis: possible involvement of hemorheological disturbances. A case report. Clin Hemorheol Microcirc 2002; 27 (2) 115-122
  • 137 Connes P, Tripette J, Chalabi T , et al. Effects of strenuous exercise on blood coagulation activity in sickle cell trait carriers. Clin Hemorheol Microcirc 2008; 38 (1) 13-21
  • 138 El-Sayed MS, Nagia A. Blood hemostasis in exercise and training. In: Connes P, Hue O, Perrey S, eds. Exercise Physiology: From a Cellular to an Integrative Approach. Amsterdam, Netherlands: IOS Press; 2010: 259-281
  • 139 Lippi G, Maffulli N. Biological influence of physical exercise on hemostasis. Semin Thromb Hemost 2009; 35 (3) 269-276
  • 140 Ikarugi H, Shibata M, Shibata S, Ishii H, Taka T, Yamamoto J. High intensity exercise enhances platelet reactivity to shear stress and coagulation during and after exercise. Pathophysiol Haemost Thromb 2003; 33 (3) 127-133
  • 141 Connes P, Machado R, Hue O, Reid H. Exercise limitation, exercise testing and exercise recommendations in sickle cell anemia. Clin Hemorheol Microcirc 2011; 49 (1–4) 151-163
  • 142 Tripette J, Loko G, Samb A , et al. Effects of hydration and dehydration on blood rheology in sickle cell trait carriers during exercise. Am J Physiol Heart Circ Physiol 2010; 299 (3) H908-H914
  • 143 Lippi G, Banfi G. Doping and thrombosis in sports. Semin Thromb Hemost 2011; 37 (8) 918-928
  • 144 Leigh-Smith S. Blood boosting. Br J Sports Med 2004; 38 (1) 99-101
  • 145 Segura J, Ventura R, Pascual JA. Current strategic approaches for the detection of blood doping practices. Forensic Sci Int 2011; 213 (1–3) 42-48
  • 146 Gauthier J. [Blood doping and cardiovascular consequences]. Presse Med 2002; 31 (40) 1904-1908